Snakebite, antivenom research, and basic science

Click here to read in Spanish
Haga clic aquí para leer en español

In the past few weeks, a peculiar congruence of several seemingly-unrelated events took place. (At least) two new scientific papers about snake biology were published, a new video series was announced, some scientists entered contests, and the U.S. executive branch announced a budget proposal with deep cuts to science funding. However, these events aren't as unrelated at they might seem at first glance, and they have something to tell us about where snake biology, and science in general, are going in the future.

The science: part I (puff adders)

A puff adder (Bitis arietans)

Puff Adders (Bitis arietans) are among Africa's most widespread vipers. They are heavy-bodied snakes that are found in savannas and open woodlands. Like most vipers, they eat mostly rodents as adults, which they ambush from carefully-selected sites, which they sometimes occupy for weeks at a time. Recently, Xavier Glaudas and Graham Alexander published a new study showing that, even though Puff Adder strikes last less than two seconds, they can choose to either hold onto or let go of the prey depending on its size. Specifically, they hold onto small mice, shrews, birds, toads, and lizards, but strike & release larger rodents and rabbits, because retaliatory rat bites are dangerous to them. After they let go of these larger prey, which usually run off a short distance before the venom kills them, they track them down again using stereotypic strike-induced chemosensory searching behavior to locate the scent of non-toxic components of their own venom. This is really similar to findings by Bree Putman and Rulon Clark that Southern Pacific Rattlesnakes (Crotalus oreganus) were more likely to hold onto smaller rodents than to larger ground squirrels. You can watch 26 awesome videos selected from an archive of thousands of hours of video taken in the wild over more than two years.¹

This research matters because venomous snakes and their prey are in constant evolutionary arms races, leading to:

1. a mosaic of new biochemical compounds that are often useful in treating disease
2. a mosaic of new biochemical compounds that can make venomous snakebite really hard to treat

We'll come back to the second one in a minute. The obvious importance of human medicine and venomous snakebite treatment overshadow a third important reason to study snakes and what they eat. Although the beneficial role of snakes in rodent control is taken as gospel by many advocates of snake conservation, the amount of data that we actually have on what snakes eat in the wild is surprisingly small. For many species, we don't even have a general idea of what kinds of prey they like to eat. Given recent estimates that spiders eat about as much meat as people do worldwide, and the potential for snakes to reach very high population densities in certain habitats, it's likely that the top-down effects of snakes as predators are significant ecosystem services that most humans aren't aware of and thus undervalue. Indirect effects on other aspects of the ecology of snake prey species, such as predation release and disease transmission, link snake predation even more strongly to human health. This is particularly timely in light of recent predictions that 2017 will be a big year for white-footed mice and thus for Lyme disease in the northeastern USA, controversy over the reintroduction of Timber Rattlesnakes, one of the white-footed mouse's top predators, to Quabbin Island in Massachusetts², and the continuation of both the infamous Sweetwater Rattlesnake Roundup³ and the reformed Claxton Wildlife Festival and Lone Star Rattlesnake Days earlier this month.

The science: part II (how cobras got their flesh-eating venoms)

A Mozambique spitting cobra (Naja mossambica) spitting its venom

Spitting cobras are even more well-known than puff adders because of their defensive venom spitting abilities, showcased on the BBC's Life in Cold Blood. They are found in Africa and Asia and are thought to have evolved two or three times from non-spitting cobras. A new paper from the lab of Bryan Fry at the University of Queensland sheds some light on when and why venom spitting evolved. Elapid snakes, including cobras, have venoms rich in neurotoxins, which are highly potent toxins that are very effective at paralyzing their prey. Cobras also have less potent cytotoxins that kill cells directly, which is a bit weird. What is the function of these toxins?

Toxicity of snake venom to human cells grown in culture.
Warm colors indicate higher toxicity.
From Panagides et al. 2017

The hypothesis put forth here is that the first step towards venom spitting was the evolution of hooding behavior and morphology, which happened twice in elapids: once in "regular" cobras and once in King Cobras, which are more closely related to mambas. Only once a conspicuous visual display was present was there selective pressure for cytotoxic venom components delivered to the eyes of potential predators via spitting. Although the venom of both groups is cytotoxic, Hemachatus (rinkhals) and Naja cobras use three-finger toxins, whereas King Cobras use L-amino acid oxidase enzymes, consistent with the undirected, opportunistic nature of our current model of venom evolution by gene duplication and mutation. The authors suggest that further elevations in cytotoxicity are linked to bright bands and other aposematic colors or hood markings, although their paper did not attempt to quantify these attributes of cobra displays, which can be quite diverse even within species. Further evidence in support of the hypothesis is that Naja naja and Naja oxiana seem, based on their nested position, to have lost spitting but to have retained cytotoxicity, and their close relatives Naja atra and Naja kaouthia might represent steps down this evolutionary path, being capable of spitting only in some populations and with less accuracy than the African and southeast Asian clades of true spitting cobras.

This is an extremely cool and popular topic. It was covered by IFLS, The Wire, Gizmodo, and the Washington Post. It goes to show that people worldwide are fascinated by venomous snakes, and the Fry lab has done a great job capitalizing on that interest (among other accolades, Fry's graduate student Jordan Debono recently won the Queensland Women in Science Peoples' Choice Award [a contest that was decided by an online popular vote; more on this later] for her research on global snakebite treatments). One reason for this fascination has to do with the question of who, exactly, these cobras are defending themselves from? The most reasonable hypothesis, given the timing and geography of the diversification of spitting cobras and the precision with which they can target forward-facing eyes and hominoid faces, is primates. Us, and our ancestors, who have eaten and been eaten by snakes for millions of years. Studying spitting cobras is a window into our own evolutionary past, a way for us to learn about ourselves. But, let us not be misled into thinking that interactions between humans and cobras are a thing of the past.

The upshot: the truth about snakebite

You can follow the ASV @Venimologie

If you haven't read the blog by medical toxinologist Leslie Boyer, you really should. Earlier this month she wrote about the vicious circle of antivenom shortage in sub-Saharan Africa, where millions of people are bitten by venomous snakes every year, many of which die or suffer awful injuries because they lack access to good antivenom. This crisis has prompted the creation of the African Society of Venimology and a new series of snakebite training videos in English, French, and Spanish. The politics and economics of antivenom are complicated and reflect larger issues in medicine, education, quality control, supply and demand, and how global economics and corporations have failed to respond to the needs of local communities and consumers. In a nutshell, the issue is that antivenom manufacturers don't make enough good antivenom, because not enough people buy it. People don't buy it because it's expensive, and it's expensive because not that much is made. This is despite a huge need for it—but not everybody with a snakebite goes to a hospital and gets antivenom in Africa, partially because it's not certain there will be any and partially because a lot of patients and doctors don't know about antivenom, because it's not in widespread use (which is mostly because of the reasons above). Other exacerbating problems include that it's often not certified, fake products can price the real antivenom out of the market, and the infrastructure for distributing antivenom and information in Africa is sub-optimal (but improving). Fixing any one or even most of these problems won't fix the whole system—if any one of them break down, supply and demand will be out of balance and people won't get the care they need.

A lot of the same issues used to be present in Mexico, but product improvements, government outreach, and massive education efforts in the 1980s and 1990s dramatically reduced mortality from venomous snakebite and led Mexico to become a major producer and consumer of high-quality, affordable antivenom, so much so that the USA now imports some of these drugs from Mexico. The Mexican government enabled the Mexican antivenom industry to be competitive and reach its market, which is much larger than the domestic market for American antivenom manufacturers—medically-serious venomous snakebites (and scorpion stings) in the USA are mostly confined to the southwest, and the per-capita risk of snakebite is the lowest in the world. This creates its own unique problems. You may have heard about the controversy surrounding the discontinued coralsnake antivenom made by Wyeth, and there are compelling arguments that the Mexican polyvalent antivenoms Anavip (made by Bioclon for humans) and ViperSTAT (made by Veteria Labs for cats and dogs) are more effective and much less expensive (although this is due almost exclusively to the idiosyncrasies of the US healthcare finance system) than the only FDA-approved viper antivenom, CroFab (although BTG, the maker of CroFab, filed a complaint asserting that these Mexican products infringe on its patent).

Finally, the global importance of the availability of high-quality, affordable antivenom for Latin American, African, and other exotic snakes is only going to increase as venomous snakes become more popular as pets and in zoos. This is particularly true in parts of the world completely lacking venomous snakes or with only very benign, non-life-threatening species, such as northern Europe, Scandinavia and northern North America, where doctors may be totally unprepared for a snakebite emergency and may not have appropriate antivenom on hand. This is exactly the kind of situation where government funding, in the form of orphan disease R&D grants, could play a role in making it affordable for researchers and doctors to save lives.

For a great introduction to and more in-depth coverage of these issues, you should watch The Venom Interviews or read their coverage of the recent video series.

The future: sequence the Temple Pitviper genome

Temple or Wagler's Pitvipers (Tropidolaemus wagleri)
at the famous Temple of the Azure Cloud in Penang, Malaysia
You can vote to sequence their genome here!

Genomics of snakes is taking off in a big way, and we stand to learn a lot more about the evolution and function of snake venoms and the treatment of their effects. But, funding for basic science isn't a priority for many people, and more and more scientists are turning to crowd-funding their research or relying on limited funding from private foundations, which often decide which projects to fund through a crowd-sourced voting process. This isn't necessarily a bad thing; in fact, I think it's a great thing in many cases. But, it's important to realize that government funding for science is different from private funding in two crucial ways: 1) there is a lot more of it (at least for now), and 2) it's not driven by specific, private interests. A great example is the Orianne Society, a non-profit reptile conservation organization whose founding purpose was preventing the extinction of Eastern Indigo Snakes (Drymarchon couperi). Thanks to generous donations from private funding sources, the Society succeeded in purchasing large areas of critical habitat for this endangered snake and protecting them in perpetuity, probably the most effective and laudable conservation goal in existence. Another good example is the work of the Durrell Wildlife Conservation Trust, who have essentially saved a globally-rare snake, Casarea dussumieri, from extinction in the wild. I wish the quality conservation work that these organizations have become well-known for were more common, but to date their donors are some of the only large private backers of reptile research and conservation in the world.

Snakes are part of human economics, albeit to a lesser extent than many insects, fishes, birds, and mammals—they are hunted for food (although there are many issues surrounding better management of unsustainable harvests), kept as pets, their skins made into leather, and their venom harvested to make antivenom and other drugs. But, in their current form, these industries place very little emphasis on finding out more about snake biology in the wild; it just isn't necessary for them to make a profit, even though the information is important for what they do. Antivenom manufacturers are accountable to their shareholders, but trying to block FDA approval of Mexican antivenom is certainly not going to result in better treatment for snakebite victims in the USA, and American companies aren't investing in any research to create new, better products themselves, since drug development is expensive and risky, and they already have a monopoly on antivenom in the USA.

It's no secret that snakes and snake research have a PR problem: even scientific journals are less likely to publish research articles about snakes than about mammals and birds (although the bias is likely subliminal). Many people prefer cute fuzzy animals that are similar to humans, but research into the biology of un-fuzzy animals is equally important. There's a parallel to the divide between funding for basic and applied science. Basic science isn't usually as sexy as the exciting, fun applications that come later, like saving lives, curing diseases, or discovering new complex biological phenomena. However, important applied science like antivenom creation cannot happen without basic science, in particular basic science on snakes. Private companies can't afford to invest in basic science the way they once did. Which leaves government funding and that from a limited number of interested, private backers.

We should support public funding for science and elect politicians who will do the same; better treatment for snakebite should be the least partisan and most universally-agreed-upon goal in the world. I think the path between basic (snake ecology, venomics, and genomics) and applied (antivenom manufacturing and public health) science is shorter and clearer in this context than in many, but the same principles apply—you cannot have medicine, conservation, and the other good parts of civilization without science.

You can vote now through April 5th 2017 for a project sequencing the entire genome of the Temple Pitviper (Tropidolaemus wagleri) co-led by Ryan McCleary.

Stay tuned for more about the role of snake venom proteins in treating human diseases, and the role of snakes as predators in ecosystems.

---

1 Naturally, I wanted to link to the full-text of the paper so that anyone interested in learning more could read it, but the publisher (Wiley) has a 12-month embargo on posting the PDF anywhere online. They actually expect you to pay between $6 and $38 to read the article. Now, I think it's great research, and it probably cost Glaudas, Alexander, and their university thousands of dollars and thousands of hours to do it. But, if you pay Wiley to read their paper, none of that money will go to them, nor to the scientists who peer-reviewed their work for free. It will go to Wiley, who Xav paid (maybe) to publish. They could have paid $3,000 to make it open access, but you can understand why they didn't. No wonder most most science is read by fewer than 10 people. It's an outdated model that can't go away fast enough. In contrast, the spitting cobra paper is open access, which cost its authors over $1,500. This is typical; academic authors almost always lose money on a publication.^↩

---

2 Recent update here; you can write the governor of Massachusetts here.^↩

---

3 Reports suggest that this year, like last year, a much larger number of live rattlesnakes were collected than markets could support, and at least one person died from a snakebite sustained while trying to capture a rattlesnake for a roundup.^↩

ACKNOWLEDGMENTS

Thanks to Bryan Fry for alerting me in advance of his publication, and to Colin Donahue, Markus Oulehla, and Ian Glover for the use of their photos.

REFERENCES

Bonnet, X., R. Shine, and O. Lourdais. 2002. Taxonomic chauvinism. Trends in Ecology & Evolution 17:1-3 <link>

Boyer, L. V. 2016. On 1000-Fold Pharmaceutical Price Markups and Why Drugs Cost More in the United States than in Mexico. The American Journal of Medicine 128:1265-1267 <full-text>

Boyer, L. V. and A.-M. Ruha. 2016. Pitviper Envenomation Guidelines Should Address Choice Between FDA-approved Treatments for Cases at Risk of Late Coagulopathy. Wilderness and Environmental Medicine. 27:341–342 <full-text>

Boyer, L. V., P. B. Chase, J. A. Degan, G. Figge, A. Buelna-Romero, C. Luchetti, and A. Alagón. 2013. Subacute coagulopathy in a randomized, comparative trial of Fab and F (ab′) 2 antivenoms. Toxicon 74:101-108 <full-text>

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 <full-text>

Chew, M., A. Guttormsen, C. Metzsch, and J. Jahr. 2003. Exotic snake bite: a challenge for the Scandinavian anesthesiologist? Acta Anaesthesiologica Scandinavica 47:226-229 <full-text>

Chippaux, J.-P. 2012. Epidemiology of snakebites in Europe: a systematic review of the literature. Toxicon 59:86-99 <full-text>

Glaudas, X., T. C. Kearney, and G. J. Alexander. 2017. To hold or not to hold? The effects of prey type and size on the predatory strategy of a venomous snake. Journal of Zoology 10.1111/jzo.12450 <abstract>

Glaudas, X. and G. Alexander. 2017. Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake. Behavioral Ecology and Sociobiology 71:5 <link>

Margres, M. J., J. J. McGivern, M. Seavy, K. P. Wray, J. Facente, and D. R. Rokyta. 2015. Contrasting modes and tempos of venom expression evolution in two snake species. Genetics 199:165-176 <full-text>

McCleary, R. J. and R. M. Kini. 2013. Non-enzymatic proteins from snake venoms: a gold mine of pharmacological tools and drug leads. Toxicon 62:56-74 <full-text>

Natusch, D. J. D., J. A. Lyons, Mumpuni, A. Riyanto, S. Khadiejah, N. Mustapha, Badiah, and S. Ratnaningsih. 2016. Sustainable Management of the Trade in Reticulated Python Skins in Indonesia and Malaysia. IUCN, Gland, Switzerland <full-text>

Nyffeler, M. and K. Birkhofer. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. The Science of Nature 104:30 <full-text>

Panagides, N., Timothy N. Jackson, R. Pretzler, M. P. Ikonomopoulou, Kevin Arbuckle, D. C. Yang, S. A. Ali, I. Koludarov, J. Dobson, B. Sanker, A. Asselin, R. C. Santana, I. Hendrikx, Harold van der Ploeg, J. Tai-A-Pin, R. v. d. Bergh, H. M. I. Kerkkamp, F. J. Vonk, A. Naude, M. Strydom, L. Jacobsz, N. Dunstan, M. Jaeger, W. C. Hodgson, J. Miles, and Bryan G. Fry. 2017. How the cobra got its flesh-eating venom: cytotoxicity as a defensive innovation and its co-evolution with hooding and spitting. Toxins 9 <full-text>

Putman, B. J., M. A. Barbour, and R. W. Clark. 2016. The foraging behavior of free-ranging Rattlesnakes (Crotalus oreganus) in California Ground Squirrel (Otospermophilus beecheyi) colonies. Herpetologica 72:55-63 <full-text>

Stock, R. P., A. Massougbodji, A. Alagon, and J.-P. Chippaux. 2007. Bringing antivenoms to Sub-Saharan Africa. Nature Biotechnology 25:173-177 <full-text>

Wade, L. 2014. For Mexican antivenom maker, US market is a snake pit. Science 343:16-17 <full-text>

Willson, J. D. 2016. Indirect effects of invasive Burmese pythons on ecosystems in southern Florida. Journal of Applied Ecology 10.1111/1365-2664.12844 <full-text>

Willson, J. D. and C. T. Winne. 2016. Evaluating the functional importance of secretive species: A case study of aquatic snake predators in isolated wetlands. Journal of Zoology 298:266-273 <full-text>

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

The Truth About Snakebite

Click here to read this article in Spanish!
Haga clic aquí para leer este artículo en español!

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% [edit 10/23/2015: I made a mistake here. The source cites two other sources that say that rattlensakes inject venom 75-80% of the time (i.e., 20-25% dry bites), not the other way around as I originally wrote. But, Hayes goes on to say that neither of these sources appear to be based on empirical data, and then he gives some other sources that do. These list rattlesnake and other viper dry bite percentages between 7 and 43% (i.e., injecting venom 57-93% of the time). So, indeed, much higher than the 20-25% I originally listed, but still less than for predatory strikes. I apologize for the error.] 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.
Contrary to the popular myth, a recent study showed that
larger rattlesnakes cause more serious bites than smaller ones,
which makes sense because they have more venom to inject
(see also unpublished data from the Hayes lab at
Loma Linda University showing the same trend and also
that smaller bite victims have more 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 Ben Franklin, 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 4,700 (edit: some sources say up to 8,000) bites occur, putting your chances of being bitten by a venomous snake in the USA at about 1 in 100,000 (1 in 40,000 with higher bite estimate).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; for a more thoughtful discourse on snakebite in India, click here), 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.

The USA (bottom left) is the safest country in the world in terms of snakebite risk.
Countries without any venomous snakes not shown.
Data from Kasturiratne et al. 2008
Click for larger version

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 up to 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 [Edit 16 May 2018: although recently, more well-replicated studies have shown that this figure is actually closer to 20% to 30%. Even so, I think it's safe to say that trying to catch a snake for any reason increases the chances that it will try to bite you. Killing a snake from a distance, e.g. by shooting it, is of course not nearly as risky from a snakebite perspective, but there are other associated risks and plenty of good reasons not to do that.]. 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 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 they are 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 are terrified of snakes. One notable exception is Madagascar, where no venomous snakes occur and it is fady to kill any snake (edit: although apparently superstitions still abound). 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.

For more about snakebite research and treatment, check out Dr. Leslie Boyer's blog and Bill Hayes's snakebite research page.

---

1 Venomous snakes that are striking at their prey practically always inject venom, and some evidence suggests that they 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. Dry bites to humans may result from the snake's deliberate decision to withhold venom or from kinematic constraints that reduce the duration and coordination of fang contact when striking a large, vertical object.^↩

---

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. If you're so inclined, check out David Steen's post on why it doesn't make sense to kill venomous snakes in your yard here and Jessica Tingle's historical view of the subject here.

SELECTED REFERENCES
(click here for a longer list of references pertaining to snakebite [last updated February 2017])

Scientific illustrator Liz Nixon made this infographic

featuring facts in this post!

Click here for a larger version.

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>

Ruha, A.-M., K. C. Kleinschmidt, S. Greene, M. B. Spyres, J. Brent, P. Wax, A. Padilla-Jones, and S. Campleman. 2017. The epidemiology, clinical course, and management of snakebites in the North American Snakebite Registry. Journal of Medical Toxicology 13:309-320. <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>

Wasko, D. K. and S. G. Bullard. 2016. An Analysis of Media-Reported Venomous Snakebites in the United States, 2011-2013. Wilderness and Environmental Medicine 27:219-226. <link>

Basics of Snake Fangs

Click here to read this post in Spanish!
Haga clic aquí para leer este blog en español!

Solenoglyphous fangs of a Gaboon Viper

Snake fangs are specialized, elegantly modified teeth. Some are like hypodermic needles, others are more like water slides. But all serve essentially the same purpose: to inject venom into the snake's prey. Occasionally, the fangs are also used in defense, but studies show that snakes striking in defense are far less likely to inject venom than when they're striking at a prey item, a fact that has assuaged the fears of many an ophidiophobic. I wanted to write a brief review of snake fang types, because their anatomy is very interesting and also because of their important role in classifying snakes and understanding how different groups of snakes are related to each other.

Cross-sections of fangs:
F is an aglyphous tooth.
G is an opisthoglyphous fang.
H is a proteroglyphous fang.
I is a hollow solenoglyphous fang.
From Bauchot (2006)

Many snakes produce venom, which is essentially very strong saliva, in glands in their heads (which is where you produce your saliva, too). We call these glands venom glands if they are well-developed, complete with an interior cavity, a duct connecting to a hollow fang, and compressor muscles that generate high pressures when the jaws are rapidly closed. If they lack these features, we usually call them Duvernoy's glands instead. Because there is a lot of variation among snake species in the structure of these glands and their associated teeth, there is some debate about whether or not venom glands and Duvernoy's glands are really two forms of the same thing. Either way, three groups of snakes (atractaspidines, elapids, and viperids) have independently evolved an advanced apparatus to deliver large quantities of venom during a brief strike, and many other snakes (and a few lizards) have evolved less sophisticated, but still relatively effective, modifications to their teeth in order to deliver venom after they have grabbed their prey and are "chewing" on it. The teeth of modern snakes are classically divided into four types, three of which are typically called fangs. The four tooth types have fancy names, all of which involve the Greek word glyph, one of the meanings of which is "groove". They are as follows:

Solenoglyphous

Folding of solenoglyphous fangs.
Fang is in red, maxilla green,
prefrontal orange, pterygoid yellow,
ectopterygoid purple. Vipers lack
premaxillary and palatine teeth.
From Bauchot (2006)

This most sophisticated fang type evolved once, in the ancestor to all modern vipers, which lived in Asia about 40 million years ago. Fossils suggest that solenoglyphous fangs have changed little since that time, even though vipers have undergone an incredibly successful radiation into 320 extant species found on all continents except for Australia and Antarctica. Solenoglyphous fangs are long and tubular and are attached to the snake's maxillary bone. Most snakes have several tooth-bearing bones, including four (the premaxilla, maxilla, pterygoid, and palatine) in the upper jaw, and one (the dentary) in the lower. In humans, three of these bones (the premaxilla, maxilla, and dentary) also bear teeth - your premaxilla holds your top incisors, while your maxilla holds your upper canines and molars and your dentary all your lower teeth - while the others form part of the roof of the mouth. In vipers, the maxilla bears only a single tooth (the fang) and is hinged so that the fangs can be folded back parallel to the jaws when the mouth is closed, or erected perpendicular to the jaws, the position when striking. The teeth in the pterygoids and dentaries work together to manipulate food once it gets into the mouth. Solenoglyphous fangs are strikingly similar to hypodermic needles. They have a hollow core that receives venom from the venom gland at the entrance orifice near the base and injects it from a slit-like exit orifice on the front of the fang near the tip. If the opening were at the very tip of the fang, its strength would be compromised and it would lack the sharp point needed to penetrate the target. Even under normal use, vipers shed their fangs every two months.

Modified solenoglyphous fang of
African Burrowing Asp (Atractaspis engaddensis)

A similar fang type evolved a second time about 29 million years ago in a group of African snakes, currently placed in the family Lamprophiidae, subfamily Atractaspidinae. Two genera, Atractaspis (mole vipers, burrowing asps, or stiletto snakes) and Homoroselaps (African dwarf garter or harlequin snakes), possess elongate anterior fangs, although only those of the stiletto snakes are movable. Stiletto snake fangs pivot on a socket-like joint that is more flexible than those of vipers, allowing these snakes to strike beside and behind them with their mouth closed. This is an adaptation to living underground and envenomating small mammals and other reptiles in narrow subterranean burrows. The fang morphology of atractaspidines and viperids is remarkably similar, considering that these two snake lineages last shared a common ancestor over 40 million years ago.

Proteroglyphous

Proteroglyphous fangs of an Eastern Green Mamba
(Dendroaspis angusticeps). Don't try this.
From Bauchot (2006)

This fang type also evolved only once, in the ancestor to all modern elapids, which lived 25-40 mya in Asia or Africa. Proteroglyphous fangs are in the front of the mouth and are about three times shorter than solenoglyphous fangs. This is because they are not hinged. Snakes with proteroglyphous fangs typically strike their prey and hang on until the venom has taken effect, as opposed to releasing they prey and then tracking it down. Some elapids constrict their prey at the same time as envenomating it. Over 350 species of elapids exist today, including well-known groups such as cobras, mambas, death adders, taipans, coralsnakes, and sea snakes, and less-well-known species, mainly found in Australia, of which a good number are small, secretive, and not considered dangerous to humans.

Maxilla of a proteroglyphous snake showing the almost
completely closed groove along the anterior edge connecting
the two orifices, as well as the aglyphous tooth at the
rear of the maxilla. This line may be obscured in longer fangs.
From Shea et al. 1993

Unlike solenoglyphs, some proteroglyphs have other teeth on the maxilla behind the fang. However, the fang is always separated from the other teeth by a gap, called a diastema. Some elapids have more than one functional fang on each side. In both vipers and elapids, there are usually at least two fangs on each maxilla at any one time, one that is in use and one that is a reserve fang. Both fangs are draped in a layer of connective tissue and skin called the fang sheath. Some proteroglyphs have partially movable fangs, including many of the most dangerous species such as mambas, taipans, and death adders. A few, such as spitting cobras, have modified exit orifices to their fangs that are smaller and rounder than in other cobras, a modification that increases the velocity with which venom is ejected. Modifications to the muscles and the fang sheath also facilitate spitting in these cobras. A few elapids, such as sea snakes that eat only fish eggs, have lost their fangs and their venom glands, which suggests that the primary role of venom, at least among elapids, is in feeding rather than in defense.

Opisthoglyphous

Opisthoglyphous fang of Eastern Hog-nosed Snake

These are commonly known as "rear-fanged" snakes. Opisthoglyphous fangs are grooved rather than hollow and are found near the back of the maxilla, behind the normal teeth. Typically, snakes with rear fangs must chew on their prey to bring their fangs into a biting position. There is considerable variation in the size, shape, and number of opisthoglyphous fangs from species to species, and sometimes even within a species. Most opisthoglyphous fangs are connected to Duvernoy's glands, which differ from true venom glands in several important ways, most notably in that they lack associated muscles to generate the pressure needed to evacuate venom, as in solenoglyphous and proteroglyphous snakes. The pressure on the venom glands of biting solenoglyphs and proteroglyphs can exceed 30 psi, the pressure of a car tire, whereas the pressure inside the Duvernoy's glands of opisthoglyphs is generally less than 5 psi. Because Duvernoy's glands also lack a chamber for storing venom, the idea is emerging that opisthoglyphous snakes probably secrete their venom only during chewing, which explains why prolonged bites by opisthoglyphs generally have more severe effects.

Opisthoglyphous fangs of Boomslang (Dispholidus typus)
Don't do this either.

Most of these snakes are not harmful to humans, with a few notable exceptions. Boomslangs and Twigsnakes are arboreal, diurnal African colubrines that prey on lizards and birds. They have short heads, rear fangs situated comparatively close to the front of the mouth, and partially muscled Duvernoy's glands. They also have potent venoms and their bites have killed several people, including two prominent snake biologists, Karl Schmidt and Robert Mertens. Bites from other rear-fanged snakes are known to cause relatively mild, transient, and local symptoms, but clinical documentation of these bites and their effects is scattered, incomplete, and frequently anecdotal. Many are written by the victim themselves! The above notwithstanding, bites from opisthoglyphs are generally less medically important than those from proteroglyphs and solenoglyphs. As a result, snake venom research has not focused on them, so there is still much that we do not know about this group of snakes, some of which are becoming increasingly common in the pet trade. Based on what little we do know, the composition of opisthoglyph venom/Duvernoy's secretion is fairly similar to that of viperids, elapids and atractaspidines, which makes sense given that each of these groups is more closely related to certain opisthoglyphs than they are to one another.

A: python, B: viper, C: rear-fanged colubroid, D: cobra
The f  marks the portion of the maxilla where the fang develops.
E shows the elongation of the posterior part of the
maxilla pushing forward the developing fang of a
night adder (d.a.o. = days after oviposition)
From Vonk et al. 2008

Unlike the first two groups, opisthoglyphous fangs appear to have evolved more than once, in snakes as diverse as Quill-snouted Snakes, Neck-banded Snakes, and Boomslangs. At least, that's what we used to think. Actually, it is likely that both solenoglyphous and proteroglyphous fangs evolved from opisthoglyphous fangs, as revealed by an ingenious study that used evidence from embryology and genetics to reveal the evolutionary origins of the three types of snake fangs. In a snake embryo, tubular fangs are formed by the infolding of ridges on the front and back sides of the fang, such as those that form the groove of opisthoglyphous fangs. Furthermore, front fangs develop from the rear part of the upper jaw, and are strikingly similar in their formation to rear fangs. They are pushed into the front of the mouth by disproportionate growth of the initially small part of the maxilla that is behind them. Finally, in the anterior part of the maxilla of front-fanged snakes, expression of a gene called sonic hedgehog, which is responsible among other things for the formation of teeth, is suppressed.

Relative size of the venom gland (VG) in
A: rear-fanged colubrid (Helicops leopardinus),
B: boomslang, C: homalopsid,
D: cornsnake, E: African egg-eater
SG = supralabial salivary gland
From Fry et al. 2008

Although developmental similarity is not conclusive proof of structural homology (similarity due to inheritance rather than due to other factors), these findings are consistent with the hypothesis that solenoglyphous, proteroglyphous, and at least some opisthoglyphous fangs are homologous structures. The hypothetical evolutionary trajectory was thus: some snakes evolved grooved fangs in the rear of their mouth. In a few cases (viperids, elapids, and atractaspidines), they subsequently lost the preceding teeth as what was formerly a rear fang became a tubular front fang. Other snakes retained their anterior teeth (at least some non-front-fanged colubroids), and still others developed fangs but then lost them (aglyphs such as ratsnakes). Evidence for this surprising final part comes from the formation of the maxilla and its teeth, which takes place in a single piece in pythons, but from two pieces in all fanged snakes as well as in ratsnakes, a pattern which supports a single evolutionary origin and subsequent loss of fangs. Additionally, vestigial Duvernoy's glands have been found in ratsnakes, egg-eaters, pareatid slug-eaters, and other nonvenomous aglyphs, a discovery that has led to the misleading generalization that all snakes are venomous and much subsequent misunderstanding among the non-scientific community. Toxic saliva does not a venomous animal make, as evidenced by the fact that even human saliva injected subcutaneously will produce pain and swelling.

Aglyphous

Both boas and pythons have only
aglyphous teeth, which is about
the only thing this film got right.

This word is used to describe unmodified teeth, essentially non-fangs. All snakes, even those that possess fangs of the first three types, have aglyphous teeth which they use for gripping their prey as they manipulate it during swallowing. As I just mentioned, many advanced snakes that today have only aglyphous teeth probably evolved from fanged ancestors. Several of these snakes, such as North American kingsnakes, ratsnakes, and bullsnakes, have atrophied Duvernoy's glands that lack toxin-producing serous cells. These snakes employ other sophisticated techniques, such as constriction, which is also used by more primitive snakes like boas and pythons (which did not evolve from fanged ancestors).

There are very few dangerous species of aglyphs, but one, Rhabdophis tigrinus, is becoming well-known as one of the only snakes capable of sequestering toxins from its prey for use in its own defense. This species has enlarged posterior maxillary teeth that lack grooves, so they are by definition aglyphous. However, it has relatively potent venom and has caused the deaths of several people. Among colubroids, the distinction between opisthoglyphs and aglyphs has never been entirely clear, but I'm distinguishing between them here because they are two of the four traditionally recognized types of snake teeth. Although the four types of snake teeth in this article are commonly discussed, a more accurate classification for snake teeth might be to divide them into tubular (the fangs of viperids, elapids, and atractaspidines), grooved (the rear fangs of non-front-fanged colubroids), and ungrooved (all other snake teeth).

Aglyphous (ungrooved) teeth and rear fangs of
Rhabdophis tigrinus
From Mittleman & Goris 1974

Happily for snake biologists like myself, the evolution of fangs opened the door for a massive evolutionary radiation of advanced snakes (>2800 species, or >80% of all living snake species). Although sophisticated venom delivery systems, of which fangs are just one of many integral parts, were clearly evolutionary advantageous, they have obviously also been costly at times, leading to their loss in ratsnakes, egg-eaters, and other lineages of advanced snakes. Also worth noting is that many lineages of basal snakes have got along just fine without venom, so there is not an inherent superiority of being venomous as the word "advanced" seems to imply. Rather, some have suggested that during periods of transition from forest to grassland, such as that which took place simultaneous to the dramatic colubroid radiation during the Miocene, snake taxa that were characterized by slow locomotion and constriction (boas & pythons) were supplanted by those characterized by rapid locomotion (many aglyphous colubrids) or passive immobilization (tubular- and grooved-fanged vipers, elapids, and atractaspidines that could use venom to catch their prey). Of course, both slow locomotion and constriction have subsequently been re-evolved among the colubroids, but there has been a lot of time since the Miocene.

ACKNOWLEDGMENTS

Thanks to Daniel Rosenberg (boomslang fang) and Nick Kiriazis (hognose fang) for use of their photographs.

REFERENCES

Bauchot R, editor. 2006. Snakes: A Natural History. New York, New York: Sterling Publishers. <link>

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

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

Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SR, Vidal N, Poelmann RE, Norman JA, 2008. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics 7:215-246 <link>

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

Jackson K, 2002. How tubular venom‐conducting fangs are formed. J Morphol 252:291-297 <link>

Kardong, K. V. & T. L. Smith, (2002) Proximate factors involved in rattlesnake predatory behavior: a review. In: Biology of the Vipers: 253-266. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <link>

Kardong KV, 1996. Snake toxins and venoms: an evolutionary perspective. Herpetologica 52:36-46 <link>

Kuch, U., J. Müller, C. Mödden & D. Mebs (2006). Snake fangs from the Lower Miocene of Germany: evolutionary stability of perfect weapons. Naturwissenschaften 93, 84-87

LaDuc, T. J., (2002) Does a quick offense equal a quick defense? Kinematic comparisons of predatory and defensive strikes in the Western Diamond-backed Rattlesnake (Crotalus atrox). In: Biology of the Vipers: 267-278. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <link>

Mittleman M, Goris R, 1974. Envenomation from the bite of the Japanese colubrid snake Rhabdophis tigrinus (Boie). Herpetologica 30:113-119 <link>

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

Savitzky AH, 1980. The role of venom delivery strategies in snake evolution. Evolution 34:1194-1204 <link>

Shea G, Shine R, Covacevich JC, 1993. Elapidae. In: Glasby C, Ross G, Beesley P, editors. Fauna of Australia. Canberra: AGPS <link>

Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MA, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, 2008. Evolutionary origin and development of snake fangs. Nature 454:630-633 <link>

Weinstein SA, Warrell DA, White J, Keyler DE, 2011. "Venomous" Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of "Colubrid" Snake Bites. Amsterdam: Elsevier <link>

Weinstein SA, White J, Keyler DE, Warrell DA, 2013. Non-front-fanged colubroid snakes: A current evidence-based analysis of medical significance. Toxicon. 69, 103-113 <link>

Weinstein S, White J, Westerström A, Warrell DA, 2013. Anecdote vs. substantiated fact: the problem of unverified reports in the toxinological and herpetological literature describing non-front-fanged colubroid (“colubrid”) snakebites. Herpetological Review 44:23-29.

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

Young BA, Dunlap K, Koenig K, Singer M, 2004. The buccal buckle: the functional morphology of venom spitting in cobras. J Exp Biol 207:3483-3494 <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.