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Friday, March 31, 2017

Snakebite, antivenom research, and basic science

Soon available in Spanish
Pronto disponibile 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, birdstoads, 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 EuropeScandinavia 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.


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.


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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>

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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>

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Creative Commons License

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

Tuesday, February 28, 2017

Shield-tailed snakes (Uropeltidae)

Large-scaled Earth Snake (Uropeltis macrolepis)
Shield-tailed snakes (family Uropeltidae) are poorly studied, fossorial snakes endemic to montane regions of peninsular India & Sri Lanka. Together with the families Cylindrophiidae (14 species) and Anomochilidae (3 species) they make up the superfamily Uropeltoidea, which is named for them because they are the most diverse subgroup, with 55 species in 8 genera (9 until recently, more below). Most phylogenetic studies suggest that Uropeltoidea is the sister group to Pythonoidea, although these two lineages share only a few obvious features and likely diverged at least 60 and possibly up to 85 million years ago. If it's true, this relationship is pretty interesting because it means that the familiar giant pythons are more closely related to the ~18" long burrowing uropeltoids than they are to their most obvious ecological analogues, the giant Neotropical boas. However, this kind of relationship is not unprecedented: the emerging picture of henophidian taxonomy is that constriction and large gape size have evolved at least three or four times within snakes, a good example being the sister relationship now widely accepted between the "pipesnake" family Aniliidae and the "dwarf boa" family Tropidophiidae (the "Amerophidia"), both of which were formerly considered members of the Uropeltoidea. Even some species of Cylindrophis (and, possibly, Anilius) immobilize their prey with their coils, although they have small gapes.

The southern Western Ghats
Uropeltids are the Darwin's Finches of snakes. They have radiated spectacularly across an archipelago of "sky islands", reaching their highest diversity and endemism in the mountain ranges of India's southern tip. These volcanic mountains run parallel to the coast, creating a rain shadow of dry plains to the east and generating torrential rainfall within their hills as trade winds blow monsoonally wet air northeast from the Arabian Sea. Known as the Great Escarpment of India, these mountains are an ancient coastline, formed during the break-up of the supercontinent Gondwana some 150 million years ago. Uropeltids are especially diverse in the high, wet 'shola' forests of the Anai Malai Hills (also known as the Elephant Hills), but are also highly diverse in the the Pothigai (Agasthyar Malai), Nilgiri, and Cardamom Hills, as well as the northern and central Western Ghats, the Eastern Ghats, and on Sri Lanka. Many of these mountain ranges are part of the UNESCO World Network of Heritage Sites and are among the "hottest hot-spots" of biological diversity in the world. They're home to the world's largest wild population of Indian Elephants, the second largest wild tiger population, and even more critically-endangered, endemic mammals such as Nilgiri tahr and Malabar large-spotted civets. Sixty-five percent of reptile species in this area are found nowhere else. In addition to uropeltids, the Ghats are home to diverse radiations of endemic freshwater crabs and shrimps, minnows and carps, tree frogs, and caecilians. Other endemic reptiles include the cane turtle (Vijayachelys silvatica) and travancore tortoise (Indotestudo travancorica), two genera of skinks (Ristella and Kaestlea), spiny tree lizards (genus Salea), and wood snakes (genus Xylophis, also named by Beddome, which were thought to be xenodermids but from which we have just recently obtained the first DNA sequences, placing at least one species with pareids and another with natricines). Besides Xylophis and uropeltids, there are at least 29 other species of endemic snakes, ranging from blindsnakes to sand boas, vine snakes, coral snakes, and vipers.

Col. Richard H. Beddome
Perhaps it isn't surprising that most species of uropeltids "were described in a burst of activity in the 19th century", because British colonials cleared large swaths of mountain forest for timber and tea, coffee, and teak plantations between 1860 and 1950. Forty percent (22) of the known species were discovered and described by Colonel Richard Henry Beddome, a naturalist who "…exploited the South Indian Hills, including the Palni Hills, to such purpose in the seventies and eighties of the last century, that he has hardly left a snake for any later enthusiast to discover" wrote distinguished herpetologist Frank Wall in 1922.1 Perhaps somewhat ironically, Beddome's 1911 obituary states that his career as a naturalist and forester coincided with "the first systematic steps to save the forests of Southern India from the denudation at the hands of the rural population to which they had long been exposed". However, Beddome used his tours in the montane forests to carefully document, describe, and make exhaustive and useful collections of plants, land snails, amphibians, and reptiles. In his lifetime Beddome described over a thousand species of animals and plants, and many others have been named for him.2

Heads and tails of uropeltids. 
The blade-like, "boomerang rostral" and polygonal eye shield
of Rhinophis punctatus (top left [top] and top right [side]).
Shield-like tail of Uropeltis rubromaculata (bottom left)
 Rhinophis philippinus (bottom right). From Pyron et al. 2016
Uropeltids are supremely adapted for burrowing, perhaps more so than any other snake. They construct a network of burrows during the rainy season, when the soil is soft, and wander through them after they harden. They can dig as deep as two meters and for extended periods of time. They have stout, relatively lizard-like skulls with few teeth, and conical, slender heads that are much narrower than their thick bodies. The eyes of some species are protected by polygonal scalesRhinophis and some Uropeltis have keeled, blade-like rostral scales that give the head a distinct pointed appearance. Uropeltids have narrow ventral scales similar to their dorsal scales, and short, blunt, often shield-like tails, from which they get their common name. Uropeltid tail morphology ranges from relatively normal (in Brachyophidium, Platyplectrurus, and Teretrurus) or somewhat compressed with a multi-pointed scute on the end (in Melanophidium, Plectrurus, and Pseudoplectrurus), through decidedly unusual, including tails terminating in a projecting, rugose, keratinous disc (in Rhinophis and Pseudotyphlops), to the classic, highly modified “shield” tail of some Uropeltis, in which the body appears to have been sliced off at a ~45° angle, leaving a flattened disc covered with rugose scales. However, the real specializations for burrowing are hidden within.

Diagram of  a dissected Rhinophis drummondhayi
showing the extent of red and white muscle along the body
and in 
two cross-sections. From Gans et al. 1978
Firstly, the heads of uropeltids are battering rams that are used against the soil. They are the only amniotes whose skulls are supported at the base by two vertebrae: that is, both the first and second vertebra (the human atlas and axis) articulate directly with the occipital condyle at the base of the skull. Furthermore, their braincases are reinforced and many other skull bones are strong and stout, especially for a snake. The anatomy and physiology of the anterior third of a uropeltid's body is adapted for driving this strong head forward into the soil. The muscles along the anterior portion of the trunk are large, thick, deep red, and rich in myoglobin, catalytic enzymes, and mitochondria, all biochemical or cellular adaptations that permit sustained activityThese muscles are loosely attached to the rest of the body, so they can simultaneously push the sides of the body against the tunnel walls and move the head forward, without pushing the rest of their bodies backwards. To accomplish this, muscles in the posterior body squeeze the anterior vertebral column into a sequence of hairpin turns, not unlike those formed in the vertebrae of large, elongate prey when they are eaten by snakes.3 Because the tip of the nose creates a narrow burrow that is later widened by the flexing of the body, uropeltids can burrow effectively among rocks and roots.4 Like a freight train, the anterior fifth of the body is like a locomotive in that it contains almost all of the propulsive machinery, and pulls along behind it the mostly-inert posterior trunk like the other train cars, containing viscera, embryos, food, etc., all protected on the end by a caboose-like caudal shield.  You can get some idea of how it works in this video (compare the forceful muscle contractions here with how the rest of the body is simply dragged underground here).

Schematic diagram of a uropeltid burrowing, from Gans et al. 1978.
The dark black areas between the snake and the tunnel wall indicate
firm contact. In A) the snake's vertebral column is curved and pushing
against the sides of the tunnel. In B) the firm contact between the curved spine
and the tunnel walls acts as a base against which the head can push,
extending the tunnel forward. The widened body narrows as the spine uncurves.
In C) the snake pulls its vertebral column forward and reintroduces
the curves, which widen the body and the tunnel. The rest of the body
is pulled along without doing any work or needing to resist any force.
This division of labor is similar to that seen in some caecilians, which burrow in a similar way and thereby create tunnels that are wider than their bodies.  And, unlike scolecophidians and amphisbaenians5, they can burrow without pushing against their tails, which leads to the question of what exactly their weird, shield-like tails are for, if not being pushed against? It is thought that the function of these eponymous tails is to collect dirt as the snakes burrow, forming a "plug" that protects the snake from behind. The scale texture of the tail shield scales is deeply ridged, in sharp contrast to the texture of the body scales, which instead bear regular microstructure that inhibits wetting, sheds dirt, reduces friction, and produces iridescent colors. There is also evidence that the tail disc develops over the lifetime of some species, because juveniles do not have modified tails (although they do have large, deep red axial muscles like those of adults).

Uropeltids from Duméril, Bibron, & Duméril's
1854 Erpetologie Générale

Top left and top right: Rhinophis philippinus
Center left and center right: Rhinophis saffragamus
(formerly Pseudotyphlops philippinus)
Bottom left and bottom right: Uropeltis ceylanica
Center top and center bottom: Plectrurus perroteti
A new phylogeny, the most comprehensive yet, nevertheless includes DNA from just five of the eight genera of uropeltids. The most diverse and well-known genera are Uropeltis and Rhinophis, containing 24 and 19 species respectively. These are also the most highly specialized for burrowing. Rhinophis is so bizarre that it was originally described as a subgenus of the legless lizard genus Anguis. In contrast, the smaller and more poorly-known genera Brachyophidium (1 species), Melanophidium (4 species), Platyplectrurus (2 species), Plectrurus (4 species), and Teretrurus (1 species) have less highly modified heads, tails, and body musculature. Apparently these species are unable to tunnel in dry grassland soils, instead remaining belowground until rain softens the soil. Although the 'shola' forests have been greatly reduced, in recent years many of the remnants have been protected. In contrast, the high-altitude grasslands favored by certain species have, like grasslands all over the world, been largely ignored from a conservation standpoint. A single species in an eighth genus, Pseudoplectrurus, is known only from the original specimens collected by Beddome in 1870, from atop the 6000' Mount Kudremukh. It seems that uropeltids first evolved in India at least 37 million years ago, and crossed only once onto Sri Lanka, an island with one of the most phylogenetically diverse snake faunas in the world, but which has maintained its distinctiveness from the Indian mainland despite several extended periods of land connection during the past 500,000 years.

Uropeltis macrolepis eating an earthworm
Unfortunately, we still know precious little about the ecology of uropeltids. Most species eat 80-90% earthworms, but they may snack upon the occasional earwigs, termites, or caterpillars. They are eaten by kraits (genus Bungarus) and vinesnakes (genus Ahaetulla), as well as wild boars, mongoose, owls, and galliform birds. They mate during the rainy season and females give birth to 3-9 live young at a time. Like many fossorial snakes, some species are brightly colored on the underside, especially on the tail and neck. These colors may send warning signals to predators, including possibly mimicking the coloration of some venomous kraits or centipedes. It's likely that a high amount of diversity remains to be described. If you want to read about the current state of our knowledge of uropeltid diversity and taxonomy, including outlines of the genus-level groups that are supported by molecular and morphological phylogenies, not to mention numerous color photographs, you can do so here.

1 In the same issue, sandwiched between "Alpine Orthoptera from central Asia" and "Hand-list of the Birds of India, Part IV", appears an article with the nonchalant title "A few hints on crocodile shooting (with two Plates)", as well as a short note by a Miss Kennion called "Crocodile shooting in Nepal". Sport hunting of predators was common during the British colonial period, and evidently human babies were sometimes used as bait. It's a good thing Beddome and Wall were paying attention to uropeltids back then, because nobody else was.

2 Interestingly, a children's book written in 1947 by Vera Barclay contains a possible description of Col. Beddome. The book is called "They Met a Wizard" and the titular wizard is a zoologist living in colonial India with a special interest in snakes. Ms. Barclay was the great niece of Col. R.H. Beddome and it's likely that she knew him growing up and based her description of the zoologist in the story at least in part on her memories of him.

3 As a result, some early descriptions of uropeltids, such as Günther's The Reptiles of British India or Wall's Ophidia Taprobanica, contained erroneous claims that the neck was "swollen and knuckled" or that the head was very frequently bent to one side, as a result of the snake being preserved with the axial muscles contracted and unconstrained by tunnel walls.

4 I cannot improve upon the ingenious phrasing used by Carl Gans to describe the burrowing of uropeltids: "The burrowing method provides an ideal tunneling device for an unpredictably inhomogeneous substratum. The initial divot driven by the head is quite narrow and will be deflected by roots or rocks. When it passes close to such effectively nondeformable and nondisplacable objects, the opposite wall of the tunnel will be compressed unevenly so that the final tunnel achieves its full if meandering diameter by extra asymmetric compression of the softer zones."

5 Most amphisbaenians bite pieces out of their prey rather than swallowing it whole, so they are less likely to be impeded by a food bolus while burrowing.


Thanks to Sara Ruane, Satyen Mehta, and M for the use of their photos, and to the Rare, Endangered and Threatened Plants of Southern Western Ghats database for sharing their beautiful map.


Extremely similar head (top) and tail (bottom) of
Uropeltis macrorhynchus
Beddome, R. H. 1886. An account of the earth-snakes of the peninsula of India and Ceylon. Annals and Magazine of Natural History 17:3-33 <Biodiversity Heritage Library>

Bossuyt, F., M. Meegaskumbura, N. Beenaerts, D. J. Gower, R. Pethiyagoda, K. Roelants, A. Mannaert, M. Wilkinson, M. M. Bahir, K. Manamendra-Arachchi, K. L. N. Peter, C. J. Schneider, V. O. Oommen, and M. C. Milinkovitch. 2004. Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot. Science 306:479-481 <download>

Comeaux, R. S., J. C. Olori, and C. J. Bell. 2010. Cranial osteology and preliminary phylogenetic assessment of Plectrurus aureus Beddome, 1880 (Squamata: Serpentes: Uropeltidae). Zoological Journal of the Linnaean Society of London 160:118-138 <ResearchGate>

Gans, C. and D. Baic. 1977. Regional specialization of reptilian scale surfaces: relation of texture and biologic role. Science 195:1348-1350 <abstract>

Gans, C., H. C. Dessauer, and D. Baic. 1978. Axial differences in the musculature of uropeltid snakes: the freight-train approach to burrowing. Science 199:189-192 <abstract>

Ganesh, S. 2010. Richard Henry Beddome and south India’s herpetofauna—a tribute on his centennial death anniversary. Cobra 4:1-11 <link>

Ganesh, S. 2015. Shieldtail snakes (Reptilia: Uropeltidae)–the Darwin’s finches of south Indian snake fauna? Pages 13-24 in P. Kannan, editor. Manual on identification and preparation of keys of snakes with special reference to their venomous nature in India. Proceedings by Govt. Arts College, Udhagamandalam, Tamilnadu, India <ResearchGate>

Ganesh, S. R. and S. R. Chandramouli. 2013. Endangered and Enigmatic Reptiles of Western Ghats – An Overview. Pages 35-61 in N. Singaravelan, editor. Rare Animals of India. Bommanampalayam Bharathiyar University (Post), Tamil Nadu, India <Google book>

Gaymer, R. 1971. New method of locomotion in limbless terrestrial vertebrates. Nature 234:150-151 <abstract>

Gower, D. J. 2003. Scale microornamentation of uropeltid snakes. Journal of Morphology 258:249-268 <full-text>

Günther, A. 1864. The Reptiles of British India. Robert Hardwick, London <Biodiversity Heritage Library>

Olori, J. C. and C. J. Bell. 2012. Comparative skull morphology of uropeltid snakes (Alethinophidia: Uropeltidae) with special reference to disarticulated elements and variation. PLoS ONE 7:e32450 <full-text>

Smith, M. A. 1943. The Fauna of British India. Volume III. Serpentes. Taylor & Francis, London <full-text>

Pyron, R. A., S. R. Ganesh, A. Sayyed, V. Sharma, V. Wallach, and R. Somaweera. 2016. A catalogue and systematic overview of the shield-tailed snakes (Serpentes: Uropeltidae). Zoosystema 38:453-506 <link>

Rajendran, M. 1985. Studies in uropeltid snakes. Madurai Kamaraj University, Madurai.

Rieppel, O. and H. Zaher. 2002. The skull of the Uropeltinae (Reptilia, Serpentes), with special reference to the otico-occipital region. Bulletin of the Natural History Museum: Zoology 68:123 <download>

Shanker, K. 1996. Nature watch: secrets of the shieldtails. Resonance 1:64-70 <full-text>

Wall, F. 1921. A new snake of the family Uropeltidae. Journal of the Bombay Natural History Society 28:41-42 <Biodiversity Heritage Library>

Wall, F. 1921. Ophidia Taprobanica, or the Snakes of Ceylon. H. R. Cottle, Govt. Printer, Colombo <Biodiversity Heritage Library>

Wall, F. 1922. Acquisition of four more specimens of the snake Brachyophidium rhodogaster Wall. Journal of the Bombay Natural History Society 28:556-557 <Biodiversity Heritage Library>

Williams, E. E. 1959. The occipito-vertebral joint in the burrowing snakes of the family Uropeltidae. Breviora 106:1-10 <Biodiversity Heritage Library>

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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.

Tuesday, January 31, 2017

Do snakes have a third eye?

This post will soon be available in Spanish

Limerick written by Annie Simminger about her nephew,
Richard Marshall Eakin, and published in his 1983 book The Third Eye.
Eakin and Robert C. Stebbins performed and published many
experiments on the structure and function of the third eyes of lizards
Many lizards have a parietal eye, also known as a third eye or pineal eye. This "eye" is a photosensory organ located on the top of the skull, in the center. It has a well-defined lens, cornea, and retina, and is lined on the inside with photosensitive cells that resemble the cones of the lateral eyes and contain the light-sensitive pigment vitamin A1. These cells are connected by the parietal nerve to the pineal organ in the brain, which produces melatonin2, the hormone that controls sleep patterns, circadian rhythms, and seasonal cycles such as mating, migration, and hibernation. The parietal eye can see light and is primarily used to sense changes in day length. Many lizards have a parietal eye, although it is most well-developed in tuataras, even serving as the inspiration for a New Zealand brewery.

Parietal eye (black outline) and parietal scale (white outline)
of Liolaemus bisignatus (Philippi's Tree Iguana).
From Labra et al. 2010
Recently, a Twitter conversation led me to evaluate the evidence for a parietal eye in snakes. As with many things, you would assume that if lizards have parietal eyes, then snakes have them too, since snakes are just one group of legless lizards. And, as with many things, you'd be wrong (probably; read on). It turns out that studies on the parietal eyes of snakes are almost non-existent. Maybe this isn't surprising, considering how little we know about other basics of snake physiology, like how well they can hear or whether or not they sleep. The evidence for the existence of  a parietal eye in snakes is scant at best, and despite evidence for its absence, "amazingly few species have been studied", just seven as of 1979, and barely any others since then. Detailed studies have been made on the pineal organ of just one species, Natrix natrix, the European Grass Snake, in contrast to a large body of work on the pineal complex of lizards and tuataras. The tale of the evolution of the parietal eye is helpful in understand the assumptions made about snake parietal eyes, in the absence of much direct research on them.

The "chimney-like" pineal foramen of
the extinct 3-foot-long 250 million year old
South African fossil therapsid Hipposaurus.
From Haughton 1929
Tuataras and many lizards have relatively well-developed parietal eyes. These organs face upwards between the parietal bones of the skull, and were it not for their covering of skin they would effectively connect the outside world with the brain (more or less as our "normal" [lateral] eyes do). There are no eyelids, or rather, like the lateral eyes of snakes, there is a fused, clear eyelid. In young lizards, the opening in the skull is large and T-shaped, like the familiar soft fontanelle of an infant human's skull, whereas in adult lizards the opening becomes ossified and may close completely late in life. Some extinct reptiles had bony protuberances around the margins of their parietal eyes: one, Hipposaurus, had a "chimney-like structure". For a long time paleontologists debated whether holes in the parietal bones of fossil skulls were necessarily evidence of ancient parietal eyes. The German-American paleoneurologist and "fossil brain" expert Tilly Edinger3 snarkily wrote that "if one doubts that this association existed also in extinct vertebrates, one may as well doubt that the orbits of fossil skulls contained eyes", because other than lizards and tuatara, no other living animals possess such holes. Many extinct tuatara relatives had even larger and more well-developed parietal eyes than do living tuataras—in some extinct pliosaurs, the opening was as large as 50 mm (2") by 20 mm (almost 1"), whereas in living tuataras it rarely exceeds 3 mm and modern lizards 1 mm. A more useful comparison may be the size of the parietal eye relative to that of the braincase: in living tuataras, this is about 1:7, whereas in living lizards it varies from 1:21 to 1:36 or less. The absence of any traces of musculature in fossil skulls or signs of more a complex past during embryonic development suggests that parietal eyes have never been any more elaborate in structure than they are in modern lizards and tuatara, although the larger parietal eyes of extinct reptiles were probably better at seeing than the tiny ones of living species.

Endocast of the brain of the dog-sized 250-million-year-old
dicynodont Lystrosaurus, the "humble badass of the Triassic",
showing the large parietal eye (dark structure at the top).
From Edinger 1955
Iguanids, agamids, varanids, cordylids, lacertids, and shinisaurids are diurnal, surface-active lizards that have well-developed parietal eyes. Several families of lizards that are mostly nocturnal and/or spend a great deal of time underneath cover or beneath the ground also have parietal eyes, including scincids, anguids, anniellids, xantusiids, amphisbaenids, and xenosaurids. Chameleons have a degenerated parietal eye that lies above the foramen; presumably it is redundant with the lateral eyes of chameleons, which can move independently and cover 180° horizontally and 90° vertically. Some surface-active (teiids). burrowing (dibamids), and intermediate nocturnal (geckos) and diurnal (helodermatids and lanthanotids) lineages lack parietal eyes. Many of the lizard genera lacking a parietal eye have more equatorial geographic distributions. It has been suggested that a long evolutionary history in the tropics could lead to the loss of the parietal eye, because changes in day length are so minor close to the Equator. Even though there are seasons in the tropics (normally wet and dry), they are not associated with day length or light level cues that animals could use to know when the switch between the two is going to happen (and alter their lifestyles accordingly). There are no truly polar reptiles or amphibians, but some polar mammals (e.g., walruses, Weddell seals) have unusually large pineal organs, whereas some tropical mammals (e.g., sloths, pangolins) have lost their pineal organs, suggesting that the function of the pineal complex is more important where day length is more variable.

Paired parietal foramina in the parietal (ptl)
bone of a Banded Krait (Bungarus fasciatus)
skull. From Scanlon & Lee 2004
It's thought that the parietal eye is retained in many burrowing lizards because these animals are occasionally exposed to light, and perhaps the parietal eye is a more suitable photoreceptor for a burrower than are lateral eyes, because it is already oriented upwards. If snakes evolved underground, as the leading hypothesis suggests, then it would make sense that they lost their parietal eye. Their normal eyes appear to have lost some muscles and modern surface-dwelling snakes have lost at least two of the five visual pigment (opsin) genes found in other vertebrates. Fossil and modern osteological evidence shows that a median parietal foramen like that of lizards was lost in an ancestor of all snakes (about 125 million years ago) and is not present in any living or fossil snakes. About 60 million years ago, small, laterally paired foramina evolved in early colubroids, and are present in many, but not all, living elapids, viperids and other colubroid groups. As in lizards, these may be present only in juveniles, becoming obliterated externally by bone growth later in life. Snake osteology expert John Scanlon told me that "Nobody, as far as I'm aware, has investigated whether the paired foramina [of snakes] are homologous or functionally similar to the median foramen of basal lepidosaurs [lizards]." The loss of parietal eyes is also supported by developmental formation and then fusion with the pineal gland in embryonic snakes, birds, and mammals4.

Developmental origins of the parietal ("median") eye and the lateral eye.
The cilia are cellular structures that normally function for movement
(e.g., of debris out of the nose, of water over gills, of eggs into oviducts,
of sperm cells to the egg). In the eye, they have evolved into photoreceptors.
So, snakes join most mammals, birds, turtles, and most amphibians5 in having lost their parietal eyes but retaining a photosensitive pineal organ in the brain that is not directly exposed to the outside of the skull. However, a recent review of the function of the pineal complex in reptiles states that the pineal gland of adult snakes does not contain photoreceptor-like cells. Instead, the principal cells are pineal parenchymal cells, which secrete melatonin but do not sense light. Nevertheless, experiments on gartersnakes have shown that removing the pineal organ of male gartersnakes in the fall, before hibernation, alters their melatonin cycle and reduces their courtship behavior when they emerge in the spring, so the pineal organ clearly functions to regulate melatonin and annual cycles in snakes.

Diagram of the lizard parietal eye
From Solessio & Engbretson 1993
At first glance, it doesn't seem to make sense to have a deep brain photoreceptor that isn't connected to the outside world, because it doesn't seem possible for it to be able to sense light or darkness from inside of your skull. But, don't forget that the two lateral eyes allow light to enter the brain; it is this light that the pineal organ is sensing. Humans have pineal organs too, and clearly we have no third eye (except in Greek mythology and Grimm's fairytales). Think of how sleepy you feel when you have to get up before the sun, or how awake you feel when a bright light is turned on at night. This is because your pineal organ senses the ambient light or darkness and adjusts your melatonin levels, telling you (if it's bright) to wake up or (if it's dark) to stay asleep. Melatonin is also synthesized directly by the parietal eye of lizards. Although the pineal organ can only sense light and dark, there is evidence that the the parietal eye can also detect different colors of light, including ultraviolet but not infrared light, and that it may be especially sensitive to the order of appearance of  light of different wavelengths, enabling lizards to detect dawn and dusk with great precision. Detailed anatomical studies have shown that the pineal organs of certain lizards possess either a finger-like projection that extends toward the parietal eye, or convolutions of the pineal wall, both of which result in exposing and orienting more photoreceptor cells towards the skull roof, where they can detect light. Although these are sometimes occluded by cartilage or blood sinuses, their existence suggests that the pineal organ of lizards is a more important photoreceptor than previously realized.

Comparative morphology of the pineal complex in A) lamprey,
B) frog, C) lizard, and D) human. From Edinger 1955
The parietal eye of a Western Fence Lizard (Sceloporus occidentalis)
C = cornea; CC = connective tissue; L = lumen;
LS = lens; PN = parietal nerve; R = retina
Light micrograph from Eakin 1970
Many hypotheses have been put forth to explain the exact function of the parietal eye, which in some ways is still unclear. Rejected hypotheses include that the parietal eye is used for detection or deterrence of aerial predators. Even in tuataras, the parietal eye is barely noticeable (it wasn't described until the 1870s), so predator deterrence is unlikely. It may play a minor role in predator detection, because the photoreceptive cells can respond to changes in light intensity as quickly as those of the lateral eyes, but sending sleepiness signals by initiating a melatonin cascade would be counterproductive to predator avoidance, to say the least. The most straightforward hypothesis is that it measures light intensity, functioning in regulating seasonal seasonal behaviorphysiology, and thermoregulation. Although reptiles do have thermally sensitive neurons in their brains, we now know that the pineal complex does not directly sense heat. Instead, reptiles have specially-adapted transient receptor potential ion channels (TRPs), which are proteins found throughout the body that act as internal thermometers and external temperatures sensors. Blocking the genes that make these proteins causes crocodiles to abandon their typical regime of behavioral thermoregulation and leads to significantly altered body temperature patterns. Changes in melatonin levels also affect the body temperatures selected by some reptiles, but in opposite ways in lacertids and iguanids. There is also a great deal of evidence that the parietal eye is sensitive to polarized light: blocking the parietal eye disrupts sun-compass orientation and homing ability of displaced individuals in several lizard species. This makes sense because there is no evidence that lizards can see polarized light with their lateral eyes. 

Parietal spots of a Copperhead
(Agkistrodon contortrix)
One study of thirty species of South American Liolaemus lizards found that parietal eye size did not vary meaningfully with latitude, altitude, environmental temperature, thermal tolerance, or body size, and that there was no evidence of phylogenetic inertia and high intraspecific variation in parietal eye size, suggesting that parietal-eye size may not be under strong selection for accuracy. Another detailed study found that removal of the parietal eye and pineal organ did not prevent 8 species of lizards from four families from carrying out their normal circadian rhythms. They concluded that other photoreceptors within the brain were compensating, although the aforementioned extensions of the pineal organ may also be a factor in the occasional “failure” of parietalectomy experiments. It's actually not clear that we even have enough baseline data on seasonal changes in snake circadian rhythms to correctly interpret the results of experiments that attempted to manipulate the pineal organs of snakes.

Dorsal view of a Copperhead skull, from DigiMorph

Pigmented apical pits of a ratsnake
But could the paired parietal formaina of some snakes function as parietal eyes? The question that started me looking into this was about Copperheads (Agkistrodon contortrix), which usually have a pair of small dark spots on their parietal scales. Evidently a National Geographic documentary called them nostrils, which is totally absurd. But, the spots do seem to be in the approximate location of the parietal foramina in other snakes. The DigiMorph scan of a copperhead skull does not show any parietal foramina, although if it is of an adult specimen (not stated) then they may have closed up on top. A few other snake species also have such spots, and many snakes have pigmented sensory or apical scale pits elsewhere on their bodies. The parietal eyes of some lizards are also differentially pigmented. Do we need to open our (lateral) eyes to some new possibilities? I think it's clear that snake photoreception, although well-known in species with pit organs, is still relatively poorly understood for snakes as a whole.

1 The function of vitamin A in eyesight was the basis for a WWII propaganda campaign that eating more carrots could improve human night vision. Although it's true that carrots and vitamin A are essential for good eyesight, the extent to which eating more carrots can improve a person's eyesight was apparently greatly exaggerated in 1940 to create a cover story for the novel abilities of Allied pilots to pinpoint Axis fighter jets at night, which in reality was due to on-board Airborne Interception Radar (although there is in turn some disagreement among historians as to how purposeful the deception was and how much both sides knew about the other side's radar capabilities).

2 Melatonin is synthesized from the amino acid tryptophan, which is the origin of another common myth: that eating a ton of turkey causes you feel sleepy.

3 Tilly Edinger was among the very last scientists of Jewish ancestry to leave pre-WWII Germany. A 1938 letter to the U. S. State Department in support of her immigration application from George Gaylord Simpson read "She is a research scientist of the first rank and is favorably known as such all over the world. She is everywhere recognized as the leading specialist on the study of the brain and nervous system of extinct animals and on the evolution of the gross structure of the brain. She is so preeminent in this field that she may really be said to have created a new branch of science, that of paleo-neurology, a study of outstanding value and importance”. She was the first female president of the Society of Vertebrate Paleontology, and authored over 1200 scientific papers and books, many sprinkled with sharp-witted, humorous phrases and observations. Her pioneering work in paleoneurology is well-chronicled here.

4 During embryonic development, the parietal eye and the pineal organ form together from a pocket formed in the brain ectoderm. The ancestral state is presumed to have been a possibly paired photosensory organ, as seen in extant lampreys. The parietal eye and the pineal gland of tetrapods are probably the descendants of the left and right parts of this organ, respectively. Some Devonian fishes have two parietal foramina in their skulls, suggesting an ancestral bilaterality of parietal eyes.

5 Crocodilians and some tropical lineages of mammals (some xenarthrans [sloths], pangolins, sirenians [manatees & dugongs], some marsupials [sugar gliders]) have lost both their parietal eye and their pineal organ. All amphibians have a pineal organ, but some frogs and toads also have what is called a "frontal organ", which is essentially a parietal eye. The word "pineal" comes from the shape of the human pineal organ, which resembles a pine cone.


Thanks to Daniel, Helen Plylar, and David Steen for initiating a discussion of this topic on Twitter, to John Scanlon for providing additional details about the evolution of parietal bone anatomy in squamates, and to Sandy Durso and J. D. Willson for the use of their photos.


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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.