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Showing posts with label Crotalus. Show all posts
Showing posts with label Crotalus. Show all posts

Sunday, September 9, 2018

Venom resistance in kingsnakes

A kingsnake eating a rattlesnake
Kingsnakes get their name because they eat other snakes, including venomous snakes like copperheads, cottonmouths, and rattlesnakes. They also eat lots of other kinds of prey, including non-venomous snakes, lizards, turtle eggs, and small mammals.

You often hear people say that kingsnakes are resistant or immune to the venom of copperheads, cottonmouths, and rattlesnakes. There is a subtle difference between the meaning of these two words.

Resistance is any physiological ability to tolerate or counteract the effects of a toxin or disease. Like many things in biology, resistance is not an all-or-nothing status, but a gradient. High enough resistance can result in immunity, where the toxin or disease has negligible or no effects.

A kingsnake eating a cottonmouth
Individuals can acquire resistance through repeated exposure to low doses of a toxin. The immune system recognizes the toxin as foreign and attacks it. It forms a memory of each attack and stores the pattern for later, which makes later responses to the same toxin quicker and more effective. If the toxin dose is later increased, the memory is reinforced & may become stronger. This is how antivenom is made, how people become resistant to snake venom, and also how vaccines against infectious diseases work.1

It is not how kingsnake resistance to viper venom works. Kingsnake resistance is evolved rather than acquired. This means that kingsnakes are born resistant to venom. As far as we know, their resistance levels are fixed for life & don’t change with age or exposure. This has happened over a long time through natural selection, over many generations of kingsnakes. We don't actually have a very exact  understanding of the physiological and molecular mechanisms behind how kingsnakes resist the toxic effects of viper venom. At least some of their resistance comes from antibodies—chemicals in their blood that interfere with the venom—because mice injected with kingsnake blood survive viper venom better than those that aren't, and the chemical composition of kingsnake blood changes after exposure to viper venom.

A kingsnake eating a western hognose snake
Any time a weapon appears, there is potential for counter-weapons (i.e. resistance and immunity) to appear in response. This happens through a process called a co-evolutionary arms race2. Just as the United States and the Soviet Union were involved in an arms race centered around nuclear weapons during the Cold War, so are venomous snakes and their prey & predators involved in arms races centered around their primary weapon—venom.

A major difference is that, unlike nations or humans, animals cannot plan for the future and decide to invest more energy in research & development of novel or better weapons technology for future generations. Instead, co-evolutionary arms races happen through natural selection. What start out as tiny variations in toxin resistance can be magnified over many generations. 

A kingsnake and a copperhead biting one another
When vipers were first evolving their front fangs, defensive bites became a new option for them. At first, their predators were probably not very good at resisting the effects of the venom, especially if the predator’s physiology was similar to that of their prey, and venom would have made a very good defense mechanism. Vipers would sometimes be killed and eaten, but many predators later died from their bites. Kingsnake predators that were slightly better able to tolerate the effects of the venom were more likely to survive. Eventually, all the kingsnakes without these venom resistance traits had been killed by vipers that they tried to eat, and only the resistant ones remained. On the other side, vipers that had venom with toxins that were, for example, slightly more painful or fast-acting, might have been more likely to survive a predatory attack. Thus, the arms race escalates. Vipers also exhibit flipping, jerking, “body bridging” and other escape behaviors as a defense against kingsnakes—suggesting, since they do not try to bite kingsnakes in defense, that their venom is essentially useless as an anti-kingsnake defense mechanism by now and that kingsnakes have “won” this arms race.

A mongoose eating a boomslang
This is why kingsnakes are immune to the venom of copperheads, cottonmouths, and North American rattlesnakes, but not to the venom of, for example, king cobras or black mambas. Because they live on different continents, there has never been an opportunity for kingsnakes and black mambas to enter into a co-evolutionary arms race (although both prey and predators of black mambas in Africa, such as honey badgers, and of king cobras in India, such as mongeese, have probably accomplished much the same thing).

Kingsnakes also eat coralsnakes, but amazingly they are not immune to the venom of Eastern Coralsnakes (Micrurus fulvius)—kingsnakes injected with coralsnake venom die quickly, and kingsnake blood is 0% effective at neutralizing venom proteins from coralsnakes. Presumably they are able to catch and consume coralsnakes without getting bitten. This could be because coralsnakes often eat other snakes, so perhaps their venom is more difficult for kingsnakes to evolve resistance against. Or, perhaps coralsnakes are rare or dangerous prey for kingsnakes, and it’s possible but not worth it for them to evolve resistance.

A milksnake constricting a Dekay's brownsnake
Not every kingsnake species has been tested against every venom, but we do know that there is variation in which species are immune to which venoms. The only study to compare species in depth injected mice with mixtures of venom & snake blood and measured mouse symptoms and survival. They found that blood from Eastern Kingsnakes (Lampropeltis getula) had the widest spectrum of protection against the venoms tested and was the most effective at neutralizing many rattlesnake venoms, but the least effective against copperhead venom. Blood from kingsnakes from Florida & the Gulf Coast was the most effective at neutralizing the venom of copperheads & cottonmouths. Mole Kingsnake (Lampropeltis calligaster) blood is about 75% as effective at neutralizing Mojave Rattlesnake (Crotalus scutulatus) venom as the blood of Eastern Kingsnakes. Gray-banded Kingsnakes (L. alterna) have moderate neutralization potential against Western Diamondback (C. atrox) venom, but none against Eastern Diamondback (C. adamanteus) venom. Blood from milksnakes (formerly all called L. triangulum) from various locations had intermediate neutralization capacity, with blood from North American milksnakes being about 70% more effective against rattlesnake venom than blood from Central American milksnakes. Another study found that an eastern milksnake injected with copperhead venom died, and one injected with pigmy rattlesnake venom had "no noticeable ill effects", but a lack of replication prevents these results from being particularly meaningful. Somewhat surprisingly, blood from Long-nosed Snakes (Rhinocheilus lecontei), Cornsnakes (Pantherophis guttatus), Mussuranas (Clelia clelia), and Japanese Four-lined Ratsnakes (Elaphe quadrivirgata) was also effective at protecting mice from viper venoms, but blood from pinesnakes (Pituophis) and gartersnakes (Thamnophis) was not. Both vipers and elapids appear to have at least some level of resistance to their own venom, although detailed studies are lacking for most species.

Fight of the Mongoose and the Serpent Armies
An 1850 folio from the Mahabharata
Kingsnakes are just one of many species that have partial immunity or resistance to venom. Hedgehogs, skunks, opossums, and possibly snake-eagles also have resistance to viper venoms, and eels are resistant to sea krait venom. Unlike kingsnakes, we have actually figured out exactly which proteins in opossum blood are responsible for its snake venom neutralization capacity. We also know that mongeese have followed a different route, changing the shape of the toxin targets in their cells rather than putting molecules into their blood to combat the toxins (which means that their immunity cannot be transferred). Other predators of venomous snakes, such as indigo snakes (genus Drymarchon), appear to have gotten away with not evolving immunity, although I was unable to find any actual data on physiological responses of indigo snakes to venom, just statements saying they were not resistant, so it's possible that actual tests have not been carried out.

A mountain kingsnake constricting a skink
Opossum resistance to copperhead venom probably evolved in a similar way to kingsnake resistance, but vipers are also involved in co-evolutionary arms races with their prey. Many rodent prey of North American vipers are resistant, including wood rats, prairie voles, and ground squirrels. Think of how the U.S. during the Cold War had to balance foreign policy not just with the Soviet Union, but also with other nations. The emerging foreign policy is a compromise, just as the venom that evolves is a compromise of selection pressures from predators and prey. Resistant prey may select for venoms that are better at quickly incapacitating, whereas resistant predators may select for venoms that are less deadly and more painful; it’s difficult to predict exactly what will happen without knowing the exact mechanism of resistance. Sometimes selection from predators and prey may act in the same direction, other times in opposite directions. The details of these processes are what evolutionary biologists study on a day-to-day basis.



1 Creating a vaccine against snake venom is harder than creating one against an infectious disease that is caused by a virus or a bacterium. There are pit viper venom vaccines available for dogs and horses, made from the venom of Western Diamondback Rattlesnakes, but none are available for humans. Additionally, the canine vaccines must be given twice per year, immediate veterinary care is still required, & protection against other species of venomous snakes is poor, so the technology has a long way to go.



2 The most famous co-evolutionary arms race is between toxin-resistant gartersnakes & tetrodotoxin-defended newts in the Pacific Northwest of the US & Canada, although there are many others, such as that between most pathogens & the immune systems of their hosts, between brood parasites such as cuckoos & their hosts, and between bad-tasting plants and herbivores.


ACKNOWLEDGMENTS

If you want to know more, I'd suggest chapter 3 of Christie Wilcox's book Venomous, from which I drew while researching & writing this article. Thanks to Connie Wade, Pierson Hill, Alan Cressler, Joe McDonald, Elana Erasmus, and the Los Angeles County Museum of Art [public domain] via Wikimedia Commons for providing their images for this article. Thanks to Laura Connelly for reading a draft of this article.

REFERENCES

A kingsnake eating a ringneck snake
Barchan, D., S. Kachalsky, D. Neumann, Z. Vogel, M. Ovadia, E. Kochva, and S. Fuchs. 1992. How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proceedings of the National Academy of Sciences 89:7717-7721 <full-text>

Bdolah, A., E. Kochva, M. Ovadia, S. Kinamon and Z. Wollberg. 1997. Resistance of the egyptian mongoose to sarafotoxins. Toxicon 35:1251-1261 <abstract>

Bonnett, D. E. and S. I. Guttman. 1971. Inhibition of moccasin (Agkistrodon piscivoris) venom proteolytic activity by the serum of the Florida king snake (Lampropeltis getulus floridana). Toxicon 9:417-425 <abstract>

Carpenter, C. C. and J. C. Gillingham. 1975. Postural responses to kingsnakes by crotaline snakes. Herpetologica 31:293-302 <PDF>

Cates, C. C., E. V. Valore, M. A. Couto, G. W. Lawson, and J. G. McCabe. 2015. Comparison of the protective effect of a commercially available western diamondback rattlesnake toxoid vaccine for dogs against envenomation of mice with western diamondback rattlesnake (Crotalus atrox), northern Pacific rattlesnake (Crotalus oreganus oreganus), and southern Pacific rattlesnake (Crotalus oreganus helleri) venom. American Journal of Veterinary Research 76:272-279 <PDF>

Darawshi, S., U. Motro, and Y. Leshem. 2006. The ecology of the Short-toed Eagle (Circaetus gallicus) in the Judean Slopes Israel. The Rufford Foundation, RSG project, detailed final report <project>

de Wit, C. A. 1982. Resistance of the prairie vole (Microtus ochrogaster) and the woodrat (Neotoma floridana), in Kansas, to venom of the Osage copperhead (Agkistrodon contortrix phaeogaster). Toxicon 20:709-714 <abstract>

de Wit, C. A. and B. R. Weström. 1987. Venom resistance in the hedgehog, Erinaceus europaeus: purification and identification of macroglobulin inhibitors as plasma antihemorrhagic factors. Toxicon 25:315-323 <abstract>

Drabeck, D. H., A. M. Dean, and S. A. Jansa. 2015. Why the honey badger don't care: Convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites. Toxicon 99:68-72 <academia.edu>

Heatwole, H. and J. Powell. 1998. Resistance of eels (Gymnothorax) to the venom of sea kraits (Laticauda colubrina): a test of coevolution. Toxicon 36:619-625 <PDF>

Holding, M. L., D. H. Drabeck, S. A. Jansa, and H. L. Gibbs. 2016. Venom Resistance as a Model for Understanding the Molecular Basis of Complex Coevolutionary Adaptations. Integrative and Comparative Biology 10.1093/icb/icw082 <full-text>

Jansa, S. A. and R. S. Voss. 2011. Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS ONE 6:e20997 <full-text>

Keegan, H. L. and T. F. Andrews. 1942. Effects of crotalid venom on North American snakes. Copeia 1942:251-254 <PDF>

Keegan, H. L. 1944. Indigo snakes feeding upon poisonous snakes. Copeia 1944:59 <PDF>

Lee, C.-Y., editor. 1979. Snake Venoms. Springer-Verlag, Berlin. <full-text>

Liu, Y.-B. and K. Xu. 1990. Lack of the blocking effect of cobrotoxin from Naja naja atra venom on neuromuscular transmission in isolated nerve muscle preparations from poisonous and non-poisonous snakes. Toxicon 28:1071-1076 <abstract>

Lomonte, B., L. Cerdas, J. Gené, and J. Gutierrez. 1982. Neutralization of local effects of the terciopelo (Bothrops asper) venom by blood serum of the colubrid snake Clelia clelia. Toxicon 20:571-579 <abstract>

Moussatché, H. and J. Perales. 1989. Factors underlying the natural resistance of animals against snake venoms. Memorias do Instituto Oswaldo Cruz 84:391-394 <PDF>

Neves-Ferreira, A. G., N. Cardinale, S. L. Rocha, J. Perales, and G. B. Domont. 2000. Isolation and characterization of DM40 and DM43, two snake venom metalloproteinase inhibitors from Didelphis marsupialis serum. Biochimica et Biophysica Acta (BBA)-General Subjects 1474:309-320 <abstract>

Nichol, A. A., V. Douglas, and L. Peck. 1933. On the immunity of rattlesnakes to their venom. Copeia 1933:211-213 <PDF>

Ovadia, M. and E. Kochva. 1977. Neutralization of Viperidae and Elapidae snake venoms by sera of different animals. Toxicon 15:541-547 <abstract>

Perez, J. C., W. C. Haws, V. E. Garcia, and B. M. Jennings III. 1978. Resistance of warm-blooded animals to snake venoms. Toxicon 16:375-383 <abstract>

Perez, J. C., W. C. Haws, and C. H. Hatch. 1978. Resistance of woodrats (Neotoma micropus) to Crotalus atrox venom. Toxicon 16:198-200 <abstract>

Perez, J. C., S. Pichyangkul, and V. E. Garcia. 1979. The resistance of three species of warm-blooded animals to western diamondback rattlesnake (Crotalus atrox) venom. Toxicon 17:601-607 <abstract>

Philpot, V. 1954. Neutralization of snake venom in vitro by serum from the nonvenomous Japanese snake Elaphe quadrivirgata. Herpetologica 10:158-160 <PDF>

Philpot, V. and R. G. Smith. 1950. Neutralization of pit viper venom by king snake serum. Experimental Biology and Medicine 74:521-523 <abstract>

Philpot, V. B., E. Ezekiel, Y. Laseter, R. G. Yaeger, and R. L. Stjernholm. 1978. Neutralization of crotalid venoms by fractions from snake sera. Toxicon 16:603-609 <abstract>

Poran, N. S., R. G. Coss, and E. Benjamini. 1987. Resistance of California ground squirrels (Spermophilus beecheyi) to the venom of the northern Pacific rattlesnake (Crotalus viridis oreganus): a study of adaptive variation. Toxicon 25:767-777 <abstract>

Swanson, P. L. 1946. Effects of snake venoms on snakes. Copeia 1946:242-249 <full-text>

Voss, R. S. and S. A. Jansa. 2012. Snake-venom resistance as a mammalian trophic adaptation: lessons from didelphid marsupials. Biological Reviews 87:822-837 <PDF>

Weinstein, S. A., C. F. DeWitt, and L. A. Smith. 1992. Variability of venom-neutralizing properties of serum from snakes of the colubrid genus Lampropeltis. Journal of Herpetology 26:452-461 <PDF>

Weldon, P. J. 1982. Responses to ophiophagous snakes by snakes of the genus Thamnophis. Copeia 1982:788-794 <PDF>

Weldon, P. J. and G. M. Burghardt. 1979. The ophiophage defensive response in crotaline snakes: extension to new taxa. Journal of Chemical Ecology 5:141-151 <PDF>

Weldon, P. J. and F. M. Schell. 1984. Responses by king snakes (Lampropeltis getulus) to chemicals from colubrid and crotaline snakes. Journal of Chemical Ecology 10:1509-1520 <ResearchGate>

Werner, R. M. and J. A. Vick. 1977. Resistance of the opossum (Didelphis virginiana) to envenomation by snakes of the family Crotalidae. Toxicon 15:29-32 <PDF>

Wilcox, C. 2016. Venomous: How Earth's Deadliest Creatures Mastered Biochemistry. Scientific American. <official page>

Witsil, A. J., R. J. Wells, C. Woods, and S. Rao. 2015. 272 cases of rattlesnake envenomation in dogs: Demographics and treatment including safety of F(ab')2 antivenom use in 236 patients. Toxicon 105:19-26 <abstract>

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.

Friday, October 28, 2016

Snakes with feet, anti-goo saliva, and more recent updates

This post will soon be available in Spanish


More of the latest snake news and research (for other recent updates, see posts from March, June, and August)—and, perhaps the most exciting news of all is that I have defended my dissertation and will be returning to writing more in-depth content in the next few months!

Rattlesnake Roundups (I and II)

A Texas conservation licence plate ironically depicting
a Western Diamond-backed Rattlesnake (Crotalus atrox).
Funds from these plates support a variety of valuable
conservation projects in Texas
 under the Texas
Wildlife Action Plan
, although none are specific to snakes.
Advocates for increasing state oversight of rattlesnake roundups in Texas received disappointing news this week when the Texas Parks and Wildlife Commission decided that they would not support a proposed ban on using gasoline fumes to collect rattlesnakes. Rather than reviewing and voting on the issue at their bi-annual meeting next month, the TPW Commission decided to remove it from their agenda entirely, citing "insufficient support from legislative oversight or the potentially regulated community". This decision marks the second time reviewing the ban has been put off, and unfortunately it is likely to be the last until the effort to reform roundups is re-initiated. The announcement included the statement that "TPWD [Texas Parts and Wildlife Department] staff still believe that there are better options for collecting snakes that do not adversely impact non-target species, and we will continue to work with the snake collecting community to develop and implement best practices that reduce potential impacts to these species", although in the absence of specific details it is hard to believe that this issue will remain at the fore of wildlife management in Texas without continued pressure from advocates of scientific rattlesnake management. However, Representative Susan King of Sweetwater's 2015 house bill 763 requires that petitions to state agencies (including TPWD) that are signed by <51% Texas residents are not valid, which means that the ability of non-Texans to influence policy on this issue is now greatly diminished.

If you're not familiar with the issues surrounding the gassing ban, I encourage you to read the 2016 Snake Harvest Working Group report, the same document that was available to the TPW Commission prior to their decision this week. Among other topics, it contains data on the adverse impacts of gassing on non-target endangered species, which is the primary impetus for the ban. It hints at human health impacts of consuming meat from gassed rattlesnakes. The SHWG report also summarizes previously unavailable data on roundup economics, showing that profits are not related to the number of rattlesnakes at an event and did not decline after gassing was banned in Alabama and Oklahoma. Stakeholder survey responses and the vast majority (>90%) of public comments from Texans were in favor of the gassing ban, as are many TWPD employees.

The TPW Commission is solely responsible for this decision. You can let the TPW Commission and Texas State Representative Susan King of Sweetwater (or your own state representative, if you live in Texas) know whether you think they are acting in the best interest of the majority of the public and in accordance with game management principles at the links provided (if you no longer have a fax machine, you can send a fax over the Internet here).

Goo-eating Snakes and the Eggs that Evade Them and Basics of Snake Fangs

Mandibular glands of Dipsas alternans
From Zaher et al. 2014
This discovery is from 2014, but it's newer than either of the past posts to which it's germane and I just found out about it. Perhaps you've seen the incredible rapid hatching behavior that treefrog eggs have evolved to escape from snake predators, including cat-eyed snakes (genus Leptodeira), blunt-headed tree snakes (genus Imantodes), and snail-sucking snakes (genera Sibon and Dipsas). These snakes also eat a variety of other gooey prey, such as earthworms, leeches, snails, slugs, adult frogs, caecilians, and, more rarely, non-gooey prey like lizards and reptile eggs. They have a number of adaptations that help them consume their sticky, viscous prey, including long, slender teeth, skull bones and muscles modified for extreme lower jaw extrusion, and a short-snouted, large-eyed look that resembles a snake embryo. Recently, a team of scientists from Brazil discovered a new one: a protein-secretion delivery system in the lower jaw.

Are the secretions venom? No. Dipsas and its relatives always extract snails using a sudden strike, followed by fast, alternating probing motions of the mandible inside the shell; this behavior could hardly depend on a chemical reaction of any kind. Instead, the gland secretions probably play a role in mucus control and prey transport rather than immobilization or killing of the prey. Although the glands in some species are associated with muscles, they are not connected to any teeth, but rather open onto the floor of the mouth, which in some species is covered with extensively loose, folded skin. Hypertrophied infralabial glands have been known from some dipsadine species since the 1960s, but the new paper describes the muscles and other soft tissues surrounding them and documents their variation among several dozen species of this very speciose group of snakes. On the other side of the world, pareatid snail-eating snakes have independently evolved a similar lifestyle, complete with upper jaw glands of perhaps similar function.

Why snakes are long and Why do snakes have two penises?

Pelvic girdles (dark blue) and hind limbs (red) of lizards,
living snakes, and extinct snakes with fully-developed limbs.
ZRS is the name of the SHH enhancer gene
that has been partially deleted in snakes.
From Leal & Cohn 2016
Many people are familiar with the tiny vestigial legs or "spurs" of boas, pythons, and other henophidian snakes. These structures are sexually dimorphic and are used by male boas and pythons in male-male combat and also to titillate females before and during matingNew data from the University of Florida describes how the spurs are formed: a weak flicker of activity by a gene called Sonic hedgehog (SHH) during the first few hours of embryonic development, in contrast to strong, sustained activity of this gene in lizard embryos throughout their development, forming legs. In snakes, unique genetic deletions from an enhancer of SHH explain its weak activity; transgenic mouse embryos with the same deletions showed similarly weak SHH activity, whereas mouse embryos grown with a lizard enhancer developed normally. Caenophidian snakes, such as vipers, gartersnakes, and cobras, had more extreme deletions and mutations, with the cobra barely retaining any of the SHH enhancer gene.

Amazingly, the researchers also found that HOXD13, the part of the limb-building gene that's responsible for building hands and feet, was unaltered in python embryos, and that python embryos develop not just a pelvic girdle and femur, which form the spur in adulthood, but cartilaginous templates of a tibia, fibula, and foot, which are reabsorbed prior to hatching. Although living snakes appear to follow a gradual pattern of limb shrinkage and loss, some extinct snakes that are thought to have been more similar to boas and pythons than they were to blindsnakes also had fully-developed, albeit small, limbs, complete with feet, as adults. This new discovery helps explain the apparent evolutionary "re-appearance" of these structures; they were never completely lost in the first place. As for the reason why not, snake HOXD genes and their regulators appear to be equally important to the development of their paired hemipenes, structures of obvious importance.

REFERENCES

Oliveira, L., A. L. Costa Prudente, and H. Zaher. 2014. Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology 275:87-99 <link>

Leal, F. & Cohn, M.J. 2016. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Current Biology DOI:10.1016/j.cub.2016.09.020 <link>

Leal, F. & Cohn, M.J. 2014. Development of hemipenes in the ball python snake Python regius. Sexual Development, 9, 6-20 <link>

Savitzky, A.H. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist, 23, 397-409 <link>

Texas Parks and Wildlife Department. 2016. Snake Harvest Working Group Final Report <link> <references> <summary>

Zaher, H., de Oliveira, L., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, M.M. & Prudente, A.L. 2014. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary Biology, 14, 1-28 <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.

Friday, July 1, 2016

What the Provincial Snakes of Canada Should Be

This post will soon be available in Spanish!

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 LoweDavid 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.

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