Life is Short but Snakes are Long is two years old this month!

Wednesday, March 19, 2014

Why do snakes have two penises?


Figure from Laszlo 1975
Recently somebody asked me "Why do snakes have two penises?" When I tried to answer, I realized that I didn't really know. I did know that they only use one at a time, and I had once heard that it was so that they could copulate with a female no matter which side she was on, but that doesn't really seem to make sense to me any more, especially considering that lizards also have two penises. Together, the two penises of squamates (snakes and lizards) are called hemipenes, and each individually is called a hemipenis. Each hemipenis is associated with a single testis, meaning that sperm produced in the right testis are ejaculated through the right hemipenis, and those produced on the left come out of the left. Hemipenes are normally stored inside out in the base of the tail, forming a pocket into which a probe can be, well, probed to check the sex of a lizard or snake. This is shown nicely in the above diagram. During mating, one hemipenis or the other is everted in a manner similar to taking off a sock. Sexual dimorphism is rare in snakes, except that male snakes almost always have longer, thicker tails than females, because they need someplace to store their hemipenes.

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

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

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

Mating Western Diamondbacks, Crotalus atrox (from Clark et al. 2014)
It's advantageous for a female snake to mate with as many males as she can, so that she has a wide variety of sperm to choose from. Female adders with more mates have higher offspring survival, probably due to less inbreeding and more genetic diversity to choose from, especially in regions of the genome where diversity is important, such as the MHC, which codes for proteins involved in recognizing pathogens and initiating an immune response. Many species, including humans, select their mates at least partly on the basis of MHC dissimilarity (which they can judge by smell), and this may also be the case in snakes. However, many male and female snakes often have pretty limited time to get together, since they're only in the same place at the same time for short periods in spring and fall when they're entering and leaving hibernation sites, which might mean that they have to make rapid decisions about who to mate with. However, a recent paper by Rulon Clark and others showed that male Western Diamondback Rattlesnakes have distinct mating strategies depending on their body size. Larger males were more likely to guard their mates throughout the active season. Curiously, this behavior did not result in their fathering more offspring, possibly due to sperm the females had stored from previous years. In one of the most extreme examples of clustered mating, Common Gartersnakes in Canada emerge in huge numbers in spring and mate immediately upon emergence. Unlike in most snakes, there is conflict between males and females over how each sex best maximizes their reproductive success. There's also some evidence that male gartersnakes are "right-handed", preferring to use their right hemipenis unless they have just used it recently (it's connected to the larger right testis in this species). There are fewer studies of the mating systems of tropical snakes, which do not hibernate at all, but I suspect there is more diversity in parts of the world where it is always warm (we just don't know about it yet). One study found that larger male Slatey-grey Snakes (Stegonotus cucullatus) from tropical Australia fathered more offspring than smaller males, which is similar to the situation in many temperate snakes, but the exact evolutionary causes of this phenomenon are complex and have yet to be explained.

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

ACKNOWLEDGMENTS

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

REFERENCES

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Thursday, February 13, 2014

Snakes that Give Virgin Birth

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



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

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

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

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

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

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

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

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

ACKNOWLEDGMENTS

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

REFERENCES

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

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

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

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

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

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

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

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

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

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

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

Tuesday, January 28, 2014

The first invasive snake

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

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

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

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

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

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

ACKNOWLEDGMENTS

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

REFERENCES

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

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

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

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

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

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

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

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

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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.

Monday, December 9, 2013

Blog Carnival: Ecology of Snake Sheds


Today I am participating in my first Blog Carnival (or blogeroclick 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 a partners in a coevolutionary relationship that goes back millions of years and has been well-studied by scientists from both the predator's and the prey's point-of-view.

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

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

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

ACKNOWLEDGMENTS

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

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

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

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

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

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

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

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

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

REFERENCES

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

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

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

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

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

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

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

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

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

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

Creative Commons License

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

Tuesday, December 3, 2013

#SnakesAtYourService Blog Carnival - 9th December!


Rough Green Snakes (Opheodrys aestivus)
mostly eat insects and spiders.
Photo by Kevin Durso
Next week, a few herpetology bloggers, including myself, are putting on a blogging carnival to celebrate the Year of the Snake! The theme is going to be ecosystem services of snakes - from the relatively well-studied relationships between snakes and their ecosystems in some parts of North America, to the basically unknown services rendered by snakes in Madagascar and elsewhere.

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

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

December 9th 2013 Participating Blogs and Authors:

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

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

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

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

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

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

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


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

Wednesday, November 27, 2013

The Truth About Snakebite


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

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

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

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

Figure from Gibbons & Dorcas (2002)
In a field test of these famous anecdotes, Whit Gibbons and Mike Dorcas molested 45 wild cottonmouths (Agkistrodon piscivorus) in South Carolina swamps and found that only 2 in 5 bit their fake hand when picked up, only 1 in 10 bit a fake foot when it stepped on them, and none bit a false leg that stood beside them. In a similar test, Xav Glaudas and colleagues picked up over 335 pigmy rattlesnakes (Sistrurus miliarius) in Florida and found that only 8% bit the thick glove they were wearing. Further evidence to support the fact that vipers are reluctant to bite potential predators comes from anecdotes from snake biologists radio-tracking snakes to study their spatial ecology, in which the biologist has accidentally stood on Timber and Eastern Diamondback Rattlesnakes and Puff Adders without provoking any responses. This makes sense because striking is a last resort for these snakes, which have a lot to lose and very little to gain by it. Although this isn't a perfect simulation of a typical snake-human interaction (these researchers weren't trying to kill the snakes in their experiments, after all), these findings are a good argument in the snakes' defense - if they bite you, they probably had a good reason.

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

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

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

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

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

Eastern Brown Snakes (Pseudonaja textilis) are one of
Australia's more dangerous snakes, but even they won't
chase, bite, or attack people without trying to escape
or bluff first. Australia's low population density
also contributes to their low prevalence of snakebite.
Data on fear of snakes in developing countries is lacking, and it is difficult to generalize, but based on the impressions of several people I know who have lived and worked there, most inhabitants of rural areas in developing countries are terrified of snakes. One notable exception is Madagascar, where no venomous snakes occur and it is fady to kill any snake. In contrast, in Australia people seem to have a relatively high level of respect for snakes and don't seem to mess with them solely out of machismo the way they do in the USA. Venomous snakebites are relatively rare, which is remarkable considering that the majority of snakes in Australia are venomous. I heard a story recently about a newly-hired Australian CEO of an American mining company. When the new boss asked about the snake policy, the employees jokingly replied that it was "a No. 2 shovel". The Australian CEO was not amused, because at his previous company Down Under routinely relocated much more dangerous snakes at their job sites. He instituted a company-wide training program to teach safe venomous snake practices. These classes are also available to the general public in some areas, especially in southern Africa.

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



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



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



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

ACKNOWLEDGMENTS

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

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

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

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

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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.