What the Provincial Snakes of Canada Should Be

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In case, like many Americans, you need a map

Happy Canada Day! And indeed there is a lot to celebrate, in particular Canada's new liberal government and the positive effects it has had on science and the environment. Three summers ago, I wrote in two parts (I and II) about what the symbolic snakes of each of the US states should be, inspired by the witty and spot-on post 'The State Birds: What They SHOULD Be' from thebirdist.com. In response to a tweet from Canadian Field Naturalist, a journal that publishes ecology, behaviour, taxonomy, conservation, and other topics relevant to Canadian natural history, and because Canadian provinces also have various representative symbols (none reptilian, except for the feathered kind, which I might add are somewhat better chosen than those of the US states), this summer I decided to cover the US's northern neighbor as well. Does Canada even have any snakes, you might ask? In fact, Canada is home to 27 species of snake, which might surprise those of us who have grown up in regions farther south. That's enough for every province and territory to have two provincial snakes, with one left over, although the uneven geographic distribution of species precludes that, as we'll see. I followed the same "no duplication" rule as I did for the State Snakes, but I allowed snakes that had been used as U.S. State Snakes to be used again, because almost all of the species found in Canada had also been used for a U.S. state. Feel free to chime in with your opinion about what your favorite province's snake should be, if it differs from my choice.

1. Alberta. Prairie Rattlesnake (Crotalus viridis)

Prairie Rattlesnake (Crotalus viridis)

Alberta, well-known for its dinosaurs, also harbors a fairly substantial diversity of modern reptiles for a place with such long winters. Seven species of snake can be found in the province, but perhaps the most quintessential are Prairie Rattlesnakes. Prairie Rattlesnakes in Alberta occur in shortgrass prairies, dry grasslands, and sagebrush in the southeastern part of the province. At the northwestern edge of their range, Prairie Rattlesnakes in Alberta take 5-8 years to reach sexual maturity, and give birth to 4-12 live young, which are quite large (~11" long; compared to ~9" in the more southerly parts of their range). Females may remain with their young for up to 10 days after giving birth. Historically, Prairie Rattlesnakes were found as far west as Calgary and almost as far north as Red Deer, but the species has declined in many areas due to persecution and habitat loss. Venomous snakes are rarely very popular, but provincial symbol-hood might help establish rattlesnakes as wildlife to be valued rather than pests to be exterminated (and Alberta is already quite progressive about protecting its snakes).

2. British Columbia. Sharp-tailed Snake (Contia tenuis)

Sharp-tailed Snake (Contia tenuis)

BC might be my favorite province, principally because of the Nanaimo Bar, a three-layer no-bake dessert created in the eponymous coastal city of Nanaimo. I chose the Sharp-tailed Snake to represent BC because in some ways it resembles a reversed Nanaimo Bar—the dorsal coloration is similar to the graham-cracker-and-almond base, the color of the sides to the vanilla custard center (sort of), and the belly to the delectable chocolate-and-coconut topping. These snakes are found on Vancouver Island, the nearby Gulf Islands, and possibly on the adjacent mainland. These cute little snakes eat slugs, including the infamous banana slugs, which I bet don't taste anywhere near as good as Nanaimo Bars. Descriptions of Sharp-tailed Snakes were first published in 1852 (by herpetologists Spencer Fullerton Baird & Charles Frédéric Girard, who received collections made the decade before in the Puget Sound area), exactly 100 years before the first printed recipes featuring Nanaimo bar ingredients were published in the Women's Auxiliary to the Nanaimo Hospital Cookbook (although I'll admit that's a pretty tenuis connection).

3. Manitoba. Western Hog-nosed Snake (Heterodon nasicus)

Western Hog-nosed Snake (Heterodon nasicus)

Even though Manitoba is very well-known for its Narcisse Gartersnake Dens, it has greater snake diversity than several of the other provinces, for which the gartersnake must be reserved. Some of Manitoba's most interesting snakes are Western Hog-nosed Snakes, which are found in sandy areas in the southwestern part of the province. As with other snakes at the northern limits of their range, they have a short activity season—they mate in May and lay 5-12 eggs in late June or early July, which then hatch by August. A study of Western Hog-nosed Snakes in Spruce Woods Provincial Heritage Park, Manitoba, found that they emerge from their burrows on any day when they could achieve a body temperature of at least 29°C (84°F). Like gartersnakes (though not quite to the same extent), these snakes can achieve fairly high densities in certain areas, so I think they could be good candidates for expanding our knowledge of snake ecology and behavior in the wild into phylogenetically-uncharted territory, challenging the statement made by Rick Shine in 1987 that "It's a good thing you Yanks have garter snakes, or you wouldn't have anything to study."

4. Newfoundland & Labrador. Maritime Gartersnake (Thamnophis sirtalis pallidulus)

Maritime Gartersnake (Thamnophis sirtalis pallidulus)

Newfoundland and Labrador is the only Canadian province without any native snakes. However, in recent years southwestern Newfoundland in the vicinity of St. David's has apparently been colonized by Maritime Gartersnakes, a beautiful subspecies of Common Gartersnake. Although no genetic analyses have been performed, it's likely that this population was founded by individuals shipped across the Gulf of St. Lawrence in hay bales or other cargo from Québec, New Brunswick, Nova Scotia, or Prince Edward Island. A poll by the CBC revealed that 12% of respondents thought that the recent colonization was "actually kind of cool", whereas a discouraging 49% of respondents were "not happy about it at all". It's rumored that gartersnakes were purposefully but unsuccessfully released in the St. John's area in eastern Newfoundland decades ago, either by farmers hoping to control rat populations or by someone who brought them back from the mainland hoping to sell them as pets (though both scenarios are likely more urban legend than fact). A string of recent mild winters may have allowed the gartersnakes in western Newfoundland to persist, but the extent to which climate change will enable a Florida-pythons scenario writ-small in Newfoundland remains to be seen. At the very least, this could be a golden opportunity for snake biologists to study what happens when snakes enter an ecosystem from which they have been absent for thousands of years, a rare event even in an age of snake invasions.

5. New Brunswick. Smooth Greensnake (Opheodrys vernalis)

Smooth Greensnake (Opheodrys vernalis)

Soctsman Andrew Leith Adams was an army physician who served in India, Egypt, and Canada during the 1800s. He spent his spare time studying the natural history of these countries, about which he later wrote several books, including his 1873 Field and forest rambles, with notes and observations on the natural history of eastern Canada. In it, he wrote "The Reptiles of New Brunswick are neither numerous nor formidable.", which, compared with the snake fauna he doubtless experienced in Egypt and India, was certainly true. He mentioned several snake species, in particular noting that "One of our most common fangless snakes is the active little green species (C. vernalis)", using the C. to abbreviate the genus Coluber, which Linnaeus had used for practically all snakes except boas and rattlesnakes. This handsome species has also frequently gone by the binomial Liochlorophis vernalis, among a half-dozen other genera into which it has been placed over the years.

6. Northwest Territories. Red-sided Gartersnake (Thamnophis sirtalis parietalis)

Mating ball of Thamnophis sirtalis parietalis

Red-sided Gartersnakes are the only snakes found in the Northwest Territories, where they achieve high densities near Fort Smith between the southern shore of the Great Slave Lake and Wood Buffalo National Park. Because there are few suitable hibernacula, thousands of individuals share the same den. Long winters and short, cool summers have resulted in a mating system that is unusual among snakes, although it is also possibly the most well-known because it is easily studied. Upon emergence from the in mid-April, snakes spend 2-3 weeks hanging around the entrance, during which time males compete fiercely to mate with females, forming colossal "mating balls". They then migrate over 2.3 miles (3.75 km) to their summer marshland habitat, where they remain until late August, giving birth to litters of young that are relatively small in number (~12 vs. ~19 in Manitboa) and large in body size (191 mm SVL vs. 154 mm in Manitoba). Females in the NWT rarely give birth in two successive years, instead saving up energy from one year in order to reproduce the next. They also mature at larger body sizes (570 mm SVL vs. 527 mm in Manitboa) than snakes further south. I bent the rules a little here since both Newfoundland and the NWT have only T. sirtalis (they have different subspecies, and this species might be split up fairly soon). 

7. Nova Scotia. Ring-necked Snake (Diadophis punctatus)

Brown-morph and normal Diadophis punctatus from Nova Scotia
From Gilhen 2011

Ring-necked Snakes are cute little snakes that mostly eat invertebrates, although they have been known to snack on the occasional salamander. In Nova Scotia, they can be found almost throughout the province, and an unusual brown morph occurs, particularly on Big Tancook Island in Mahone Bay along the east coast. According to the notebooks of Harry Piers, an early 20th century naturalist, museum curator, and historian, ringnecks were known to the native Mi'kmaq People as “the worst snake, Um-taa-kum (k)”, although it's not clear why. One communal nest found under a boulder near McCabe Lake in Halifax County contained 117 eggs, which must have been laid by at last 15, and probably many more, females (clutch size ranges from one to eight).

8. Nunavut. Ellesmere Island erycine (Eocene boa)

Drawing of Ellesmere Island erycine vertebra
Dotted lines show best-guesses at broken-off parts
A. Dorsal and B. right lateral view
From Estes & Hutchison 1980

Unfortunately, there are no living wild snakes in Nunavut. Initially I was going to get around this by writing only about the true provinces, but then I found evidence that a 50-million-year-old fossil snake vertebrae was found on Ellesmere Island, above the Arctic Circle at about 78.5° north (find it here at the awesome new Paleobiology Database Navigator). This vertebra belonged to an undescribed species of boid snake probably related to rubber boas, and it was found in an Eocene fossil deposit that used to be a lush river delta and floodplain, with abundant swamps, alongside pike, bowfin, and gar, mud & softshell turtles, alligators, monitor lizards, giant salamanders, and even primates. The single bone is part of the collection of the Canadian Museum of Nature (specimen number 32403) and hasn't been assigned to a species or even a genus because it's broken. Paleontologists are fairly confident that it is an erycine boid based on comparisons made with a half-dozen other extinct genera that probably belong in this group. Recent phylogenies of booids elevate Erycinae to a family, but do not include extinct taxa, so it's difficult to say for sure how these snakes were related to each other and to living species.

9. Ontario. Eastern Foxsnake (Pantherophis vulpinus)

Eastern Foxsnake (Pantherophis vulpinus)

Ontario has more snake species to choose from than any other province, including seven that are found nowhere else in Canada. At the JMIH meeting in Reno last summer, I posed the question of which one best represented Ontario to herpetologist Jacqueline Litzgus, a native of Ontario and a professor at Laurentian University. She was unhesitant in recommending the Eastern Foxsnake, the only species of snake whose range is mostly in Canada (which perhaps makes it sort of a national snake as well, although the common gartersnake is found in more provinces). Foxsnakes are large constrictors that are closely related to cornsnakes and (slightly less closely) to ratsnakes. They probably recolonized northern North America more quickly after the retreat of the glaciers than most snakes because of their mobility and the flat terrain left behind in the midwest. We once thought that the two species had a disjunct range, with the western foxsnake (formerly P. vulpinus) being found in the USA between the Missouri River and Lake Michigan, separated by a foxsnake-less area in northeastern Indiana and the lower peninsula of Michigan from the eastern foxsnake (formerly P. gloydi), which was found south and east of Lake Huron in Ontario, Michigan, and Ohio. However, a 2011 study used evidence from a single mitochondrial gene to suggest that the Mississippi River seemed to be a more significant genetic barrier and that western foxsnakes east of the Big Muddy in Wisconsin and Illinois were more closely related to eastern foxsnakes than they were to western foxsnakes in Iowa and Minnesota. Because the type specimens for both former foxsnake species were within the eastern lineage, this species became P. vulpinus (the older name), P. gloydi disappeared, and the "new" western foxsnake was named P. ramspotti. Runner up: Massasauga (Sistrurus catenatus), because of the town of Missisauga, Ontario.

10. Prince Edward Island. Red-bellied Snake (Storeria occipitomaculata)

Red-bellied Snake (Storeria occipitomaculata)

Located in the Gulf of St. Lawrence, Prince Edward Island was formed as a sandstone peninsula 250-300 million years ago. The end of the ice age 15,000 years ago and the retreat of the glaciers laid down glacial till and increased the sea level, disconnecting PEI from the mainland. PEI only has three species of snakes, all of which colonized the island within the last 15,000 years. Despite the fact that no lizards or turtles have been able to make the same crossing, PEI is still way ahead of Québec's similarly-sized Île d'Anticosti, which lies ~190 miles (~300 km) to the north and has no native species of amphibians or reptiles. Of the tiny red-bellied snake, PEI naturalist John Mellish wrote in the 1870s "This variety is numerous, is smaller in size, and seems to be less courageous than some of the other species". Although Mellish got this much right, he was as prone to exaggeration as many modern observers, interspersing his species accounts with tales of snakes charming their prey, swallowing their young, and attacking people. In reality, red-bellied snakes mostly attack slugs, and their peculiar lip-curling display is hardly threatening to a human.

11. Québec. Milksnake (Lampropeltis triangulum)

Milksnake (Lampropeltis triangulum)

Québec is best emblematized by the Milksnake, which was first described by a French herpetologist, Bernard Germain de Lacépède, in 1789. Lacépède's two-volume masterpiece, Histoire Naturelle, is a classic work in herpetology. Although Lacépède mostly used French vernacular names,  ("le triangle" for the milksnake, after the double triangles on top of its head), he used Linnaeus's Latin binomial system about 65% of the time in a 59-page table in the third section of the second volume, which covered legless amphibians and reptiles. However, because he was not consistent in his use of Latin binomials, the taxonomic community decided in 1987 that the names in volume two were not valid (volume one, which covers turtles, lizards, and amphibians, contains a 3.5' x 1.75' fold-out table that was consistently binomial, so these names remain valid). Four snake names, including Lampropeltis triangulum, were rescued because of their long history of use. The other three (Agkistrodon piscivorus, Langaha madagascarensis, and Python reticulatus) were much longer-used than L. triangulum, which probably wouldn't have made the cut if not for an earlier decision by the ICZN as part of a case involving the mistaken identity of Linnaeus's scarletsnake (Cemophora coccinea) specimen and the name he gave it, Coluber doliatus, which was mistakenly used for the milksnake for over 150 years. The 1967 case invalidated doliatus and fixed triangulum as the specific epithet of the milksnake, which prevented it from later being invalidated with the rest of Lacépède's snake names. In this way the species is somewhat rebellious (in a nomenclatural sense), which I think would please many Québécois.

12. Saskatchewan. Gophersnake (Pituophis catenifer)

Gophersnake (Pituophis catenifer)

On the first page of one of my favorite novels, Farley Mowat's Owls in the Family, the author describes growing up in Saskatoon, Saskatchewan: "When you stepped off the end of the Railroad Bridge you stepped right onto the prairie and there you were—free as the gophers. Gophers were the commonest thing on the prairie. The little mounds of yellow dirt around their burrows were so thick, sometimes, it looked as if the fields had yellow measles." Although I like owls, these days I more often have another gopher predator in mind—the eponymous gophersnake (Pituophis catenifer), also less-aptly known as the bullsnake. These harmless creatures are often mistaken for rattlesnakes, because they have a superficially similar pattern (and they do rattle their tails, although they have no specialized noise-making structure). Confusion over the common name led Edward Abbey or one of his editors to include the scientific name of the eastern indigo snake (aka the blue gophersnake), Drymarchon corais couperi, for the bullsnake in the essay 'The Serpents of Paradise' in the 1968 edition of Desert Solitaire (although it is correct in 1988 edition).

13. Yukon. ?

I hope they find a snake

The Yukon Territory has no living snakes and no snake fossils (yet). This is actually quite ironic, because most living North American snakes crossed into our continent from Asia over the Bering Land Bridge, and some of them almost certainly slithered through what is today the Yukon. It is possible that somewhere in the southern Yukon exists a population of gartersnakes, which are found in the southern NWT and also possibly in the Alaskan panhandle. Three reliable sight records and one specimen (now lost) from remote areas along Taku & Stikine Rivers in Alaska give us hope, although unfortunately neither basin enters the Yukon. Other snake sightings of snakes from Alaska include odd T. sirtalis and T. ordinoides specimens from more urban areas, which almost certainly represent translocations (genetic evidence supports this in at least one case). T. sirtalis are found just 200 miles (320 km) south of the Yukon border in BC. It isn't completely crazy to imagine snakes living at such northerly latitudes; European Adders (Vipera berus) are found above the Arctic Circle in Scandinavia. If nothing else, gartersnakes from British Columbia will probably disperse there eventually if climate change keeps up with predictions.

ACKNOWLEDGMENTS

Thanks to Ben Lowe, David O'Connor, JD Willson, Todd Pierson, Andy Teucher, Michael, Gary Nafis, and Nick Scobel for the use of their photos, to Jackie Litzgus for helping me make the decision about Ontario, and to Gareth Hopkins for introducing me to Nanaimo bars.

REFERENCES

Manitoba Thamnophis on the side of a U-Haul truck

Anonymous. 1987. Opinion 1463. De Lacépède, 1788-1789, Histoire Naturelle des Serpens and later editions: rejected as a non-binominal work. Bulletin of Zoological Nomenclature 44:265-267 <link>

Baird, S.F. and C. Girard. 1852. Descriptions of new species of reptiles, collected by the U.S. exploring expedition under the command of Capt. Charles Wilkes, U.S.N. First part. - Including the species from the Western coast of America. Proceedings of the Academy of Natural Sciences of Philadelphia 6:174-177 <link>

Brongersma, L.D. 1972. On the “Histoire naturelle des Serpens” by de la Cépède, 1789 and 1790, with a request to reject this work as a whole, and with proposals to place seven names of snakes, being nomina oblita, on the Official index of rejected and invalid names in zoology, and to place three names of snakes on the Official list of specific names in zoology (Class Reptilia). Bulletin of Zoological Nomenclature 29:44-61 <link>

Crother, B.I., M.E. White, J.M. Savage, M.E. Eckstut, M.R. Graham, and D.W. Gardner. 2011. A reevaluation of the status of the Foxsnakes Pantherophis gloydi Conant and P. vulpinus Baird and Girard (Lepidosauria). ISRN Zoology 2011 <link>

Estes R, Howard Hutchison J, 1980. Eocene lower vertebrates from Ellesmere Island, Canadian Arctic Archipelago. Palaeogeography, Palaeoclimatology, Palaeoecology 30:325-347 <link>

Gilhen, J. 2011. The Brown Morph of the Northern Ringneck Snake, Diadophis punctatus edwardsii, on Big Tancook Island, Mahone Bay, Nova Scotia. The Canadian Field-Naturalist 125:69-71  <link>

Hodge, R.P. 1976. Amphibians and Reptiles in Alaska, the Yukon, and Northwest Territories. Alaska Northwest Pub. Co.

Larsen KW, Gregory PT, Antoniak R, 1993. Reproductive ecology of the Common Garter Snake Thamnophis sirtalis at the northern limit of its range. American Midland Naturalist 129:336-345 <link>

Leavesley, L.K. 1987. Natural history and thermal relations of the Western Hognose Snake (Heterodon nasicus nasicus) in southwestern Manitoba. MS thesis. University of Manitoba, Winnipeg, Manitoba.

Rossman, D.A., N.B. Ford, and R.A. Seigel. 1996. The Garter Snakes: Evolution and Ecology. University of Oklahoma Press, Norman, Oklahoma. (Shine quote opens chapter 4, page 55)

West, R.M., M.R. Dawson, and J.H. Hutchison. 1977. Fossils from the Paleogene Eureka Sound Formation, N.W.T., Canada; occurrence, climatic and paleogeographic implications. Milwaukee Public Museum Contributions in Biology and Geology 2:77-93.

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

Snake poop and the adaptive ballast hypothesis

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Alternate title suggested by David Steen: Why snakes might benefit from holding it 

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

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

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

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

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

Uromacer oxyrhynchus just can't hold it's poop

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

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

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

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

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

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

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

ACKNOWLEDGMENTS

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

REFERENCES

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

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

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

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

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

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

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

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

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

Blog Carnival: Ecology of Snake Sheds

Clic aquí para la edición española

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

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

Part I: Contributions to nutrient cycling

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

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

A food web showing snakes as top predators

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

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

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

Part II: Use by other animals

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

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

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

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

A Great-crested Flycatcher nest with several
snake sheds

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

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

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

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

ACKNOWLEDGMENTS

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

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

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

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

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

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

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

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

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

REFERENCES

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

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

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

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

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

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

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

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

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

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

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

How snakes see through closed eyes

Early American symbols depicting rattlesnakes:

(top) Rattlesnake on the $20 bill issued in 1778 by Georgia.
The Latin motto (Nemo me impune lacesset) means,
"No one will provoke me with impunity."

(middle) Benjamin Franklin's "Join or Die" cartoon,
first published in the Pennsylvania Gazette in 1754.
Franklin advocated a rattlesnake as the national symbol
by writing: "...her eye excelled in brightness...she has no
eye-lids. She may therefore be esteemed
an emblem of vigilance."

(bottom) The Gadsden flag, used during
the American Revolution

Click here to read this post in Spanish!

Haga clic aquí para leer este blog en español!

Normally when someone asks me how to tell the difference between a snake and a legless lizard, I tell them to look at the eyes. Lizards have eyelids whereas snakes do not. Whenever I say this I am lying, although really I am just oversimplifying for the sake of clarity. Most lizards have obvious movable eyelids and so can blink like we do. Snakes, by contrast, seem not to have eyelids. They are ever-staring, ever-vigilant. Ben Franklin esteemed the rattlesnake as a symbol of vigilance because its eyes were always open.

Snakes' eyes are closed all the time. Rather than having movable eyelids, snakes have a single, fused, clear layer of skin over their eye, called a spectacle or brille (German for "glasses"), which protects the eye. A snake's skin is covered in scales, and the outer part of the spectacle is indeed a scale. The deeper layers of the spectacle are formed, during development, from the same embryonic tissue that in other animals forms the eyelid. The spectacle is not attached to the snake's eye in any way, so the eye can move freely behind it, although its movement is limited. This limited movement is because snakes are probably descended from fossorial lizard ancestors that lived underground and had degenerate eyes, much like today's amphisbaenians, although fossil evidence for this hypothesis is scant (as are snake fossils in general).

Eye of an Eastern Ribbonsnake (Thamnophis sauritus)
during the phase prior to shedding when fluid
has built up between the old and new spectacles

Unlike other animals' eyelids, snakes' spectacles are transparent, like a window in their skin, allowing them to see out through their always-closed eyelids. Just before a snake sheds its skin, a layer of fluid builds up between the new inner skin and the old outer layer, clouding the spectacle and causing the other scales to have a faded, milky appearance. This period usually lasts a few days, during which snakes have difficulty seeing and usually will not eat. People who keep snakes as pets have observed that they may become particularly ornery during this period, perhaps as a result of not being able to see clearly.

The horizontal, key-shaped pupil
of Ahaetulla prasina

Another obstacle to snake vision that has been long known but little studied is that snakes' spectacles are vascularized, meaning that they have blood vessels running through them. It is very unusual for tetrapods to have blood vessels in a place that might interrupt their field of vision. First noticed in 1852, these vessels are small but symmetrically distributed across the optically transmissive region of the eye in most species, although the arrangement is radial in basal snakes, acrochordids, and vipers but vertical in colubrids and elapids. In one visually-oriented species, the Asian vine snake (Ahaetulla nasuta), these blood vessels are less dense in the region of the field of vision known as the fovea, where the maximum sharpness is achieved. Most snakes don't have foveas, suggesting that the unusual arrangement of blood vessels in the eyes of Ahaetulla is an adaptation to minimize visual disturbance in this region of highest visual acuity.

Until recently, no one had considered whether movement of blood into and out of the spectacle blood vessels might aid snakes in being able to see. In an article published this week in The Journal of Experimental Biology, Kevin van Doorn and Jacob Sivak of the University of Waterloo in Ontario presented the first evidence that snakes are able to do this. When van Doorn was investigating the mechanisms snakes' eyes use to focus, he noticed the blood vessels in the spectacle, which led him to look more closely at their function. He found that coachwhips, another highly visual species, were able to reduce blood flow to the spectacle in the presence of a potential threat. At rest and undisturbed, newly oxygenated blood flowed into the spectacle blood vessels of the coachwhips for about a minute at a time, interspersed with approximately two minute periods during which no flow took place. When an experimenter walked into the room to perform some routine tasks, spectacle blood flow was almost completely cut off. What little flow there was during this period occurred in short spurts of around 30 seconds each, about half the length of the flow period in undisturbed coachwhips. When the experimenter left the room, the pattern of blood flow in the snakes' eyes returned to normal almost immediately.

Figure from van Doorn & Sivak 2013 showing blood vessels in the spectacle of a Coachwhip (Masticophis flagellum). (A) Image taken during the renewal phase of the integument when the spectacle becomes cloudy. The vessels are most apparent in the region that overlays the iris–pupil boundary because of their higher contrast with the background in this region. (B) The spectacle under retro-illumination, showing the vessels in the illuminated anterior portion of the pupil on the right side. The vessels are dorso-ventrally arranged as is typical for colubrid snakes. Debris and scratches are visible on the spectacle scale (particularly the left side), attesting to its protective role.

Shed skin of a Cornsnake (Pantherophis guttatus)
showing the shed spectacles

Furthermore, van Doorn & Sivak found that when snakes were handled they cut off blood flow to the spectacle completely, probably as part of a sympathetic nervous response. In contrast, blood flow to the eye was continuous and uninterrupted, even during handing, in shedding snakes. You can see a video of blood flow in the spectacle of a shedding corn snake here. Although no experimental evidence has been gathered that filled blood vessels in the spectacle reduce a snake's ability to see, it seems likely given that the blood vessels themselves are quite difficult to see when they are not filled with blood. Snakes actually have remarkably good color vision, better than that of rats and on par with the visual acuity of a cat. Because they move their eyes so little compared to humans, they might be less likely to notice the interruption to their visual field by these blood vessels.

Geckos and some other lizards also have spectacles. A few other species of tetrapods have blood vessels in their optical path, including manatees, armadillos, and some blind salamanders, none of which are renowned for their visual prowess. Little is known about the images these vessels might project onto the vision of these animals, but because they are part of the cornea and so move about with the eye rather than remain stationary relative to it, their area of occlusion would appear to remain stationary to the animal. This is not true for animals with nictitating membranes (diving animals such as penguins or crocodilians) or those with spectacles, both of which have the potential to interrupt the animal's vision. We don't know yet how crocodilians and geckos deal with this issue, but as with so many other features of their lives, snakes have evolved an ingenious and potentially unique solution to a vexing problem, allowing them to remain vigilant as well as keep their eyes protected. Snakes have guarded the Golden Fleece in the Greek tale of the hero Jason and his band of Argonauts, a treasure chamber beneath an ancient city in Rudyard Kipling’s The Jungle Book, and various other treasures in Hindu, Inca, and Basque mythology, all with their eyes closed.

ACKNOWLEDGMENTS

Thanks to Hans Breuer and Kwok Wai for their photographs of Ahaetulla prasina.

Correction: I originally said that the fovea work was done on Ahaetulla prasina, but it was actually Ahaetulla nasuta. Both species have horizontal pupils so it is likely that the reduction in blood vessels is found in both.

REFERENCES

Baker, RA, TJ Gawne, MS Loop, and S Pullman (2007) Visual acuity of the midland banded water snake estimated from evoked telencephalic potentials. J. Comp. Physiol. A 193, 865-870 <link>

Crump, M. Expected 2015. Eye of Newt and Toe of Frog, Adder's Fork and Lizard's Leg. University of Chicago Press, Chicago, Illinois.

Foureaux, G, MI Egami, C Jared, MM Antoniazzi, RC Gutierre, and RL Smith. (2010) Rudimentary eyes of squamate fossorial reptiles (Amphisbaenia and Serpentes). Anat. Rec. (Hoboken) 293, 351-357 <link>

Franklin, B (1775) The rattlesnake as a symbol of America. Pennsylvania Journal. <link>

Lüdicke M, 1969. Die kapillarnetze der brille, der iris, des glaskörpers und der chorioidea des auges vom baumschnüffler Ahaetulla nasuta Lacepede 1789 (Serpentes, Colubridae). Zoomorphology 64:373-390.

Mead, AW (1976) Vascularity in the reptilian spectacle. Invest. Opthalmol. Vis. Sci.15, 587-591 <link>

Neher, EM (1935) The origin of the brille in Crotalus confluentus lutosus (Great Basin rattlesnake). Trans. Am. Ophthalmol. Soc. 33, 533-545 <link>

Quekett, J. (1852). Observations on the vascularity of the capsule of the crystalline lens, especially that of certain reptilia. Trans. Microsc. Soc. Lond. 3, 9-13. doi:10.1111/j.1365-2818.1852.tb06020.x

van Doorn, K. and Sivak, J. G. (2013). Blood flow dynamics in the snake spectacle. J. Exp. Biol. 216, 4190-4195 <link>
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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.