Squirrel v. rattlesnake

This article is part of a series highlighting new research in snake biology presented by herpetologists at the World Congress of Herpetology VII in Vancouver, British Columbia. If you want to learn more about the WCH, check out the June 2012 issue of Herpetological Review, or follow the Twitter hashtag #wch2012, with which I will tag all posts in this series.

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It might seem like a lopsided contest, but in the majority of interactions between Northern Pacific Rattlesnakes (Crotalus oreganus) and California ground squirrels (Spermophilus beecheyi), the squirrels walk away with their lives. This surprising result come from Rulon Clark, who in his talk during the venomous snake evolution session of the WCH7 last week filled us in on the latest work from his behavioral ecology lab at San Diego State University. Building on the work done by mammalogists Richard Coss and Don Owings at UC Davis, the Clark lab studies what ground squirrels are trying to say to their rattlesnake predators. You see, when a ground squirrel encounters a rattlesnake, it performs a behavior known as 'tail-flagging'. You can see an example of this behavior in the first half of this video:

and the potential consequence of not exhibiting it in the second half! It's been apparent for almost 35 years now that tail-flagging adult squirrels are safer from rattlesnakes than squirrels that don't perform this behavior, but why?

Dr. Clark enumerated several hypotheses that his lab has tested and falsified:

• tail-flagging does not appear to be a form of quality advertisement, like stotting in ungulates, because its use is not correlated with the health or vigor of the squirrel
• tail-flagging does not appear to result in predator confusion or misdirection, because the rattlesnakes that strike at tail-flagging squirrels are equally accurate in their strike direction as those that strike at squirrels that aren't tail-flagging
• tail-flagging does not appear to be a form of harassment, like mobbing in birds & other animals, because the squirrels never attack rattlesnakes if the snakes are free-ranging (although they will if the snakes are caged, as they were in early experiments) and eventually leave the snakes alone after tail-flagging at them for a while.

Additionally, the tail-flag display is frequently given in the absence of a rattlesnake, as if to probe for potential predators nearby. So how is tail-flagging helpful? By videotaping countless hours of snake-squirrel interactions using stationary cameras - fortunately, rattlesnakes are fairly stationary themselves - Clark's group thinks they have the answer.

Crotalus oreganus from Utah

First, the squirrels are probably advertising their perception of the snakes, both to the snakes themselves and to each other. This is likely because tail-flagging by one squirrel increases the vigilance of other squirrels in the area. Furthermore, rattlesnakes that have been tail-flagged are actually more likely to abandon their ambush sites. Both these things only happen, however, when the tail-flagging squirrel is an adult. Similarly, we respond more seriously to cries of a fire by an adult than by a child. Juvenile squirrels also tail-flag, but presumably they are just practicing, so adults apparently do not take them seriously.

Second, the adult squirrels are probably also advertising their vigilance to the snakes. This is likely for two reasons: 1) the snakes are less likely to strike an adult tail-flagging squirrel than a non-tail-flagging one, and 2) if they do, squirrels that tail-flagged are more likely to successfully dodge the rattlesnake's strike. That's right - these ground squirrels can actually evade the snake's strikes. Don't believe it?

I hardly can either, but wow, that squirrel pulled a 180 and totally avoided what should have been a lethal strike. Although the squirrel in that video wasn't tail-flagging, Clark's group has shown that within about one foot of a rattlesnake, tail-flagging squirrels are more likely to dodge strikes successfully. As a result, rattlesnakes are less likely to strike at a tail-flagging squirrel - not because the energy cost is too high, but because a strike will surely cause the squirrel to run off, while waiting might result in the squirrel making a mistake by getting too close. After all, once a snake has been tail-flagged, it might as well move ambush sites, because the local squirrels are now aware of its presence.

In addition to employing highly effective perception and vigilance advertisement behaviors, those darn squirrels have also evolved to anoint their fur with rattlesnake scent! They get this odor from chewing up shed rattlesnake skins. Barbara Clucas showed that the snake scent application did not deter other squirrels or help reduce ectoparasites, bolstering the case that it is a form of olfactory camouflage that serves to reduce squirrel detectability to snake predators or to repel other rattlesnakes motivated to avoid hunting in the same area as a conspecific.

Figure from Clucas et al. 2008

By now, I imagine the snake biologists in the audience are itching to see a snake actually get one for once. Here you go:

If you want to see more videos and stay current on the Clark lab's research, subscribe to their Youtube channel or to Strike, Rattle, & Roll, a rattlesnake behavior blog published by Clark lab PhD student Bree Putman.

ACKNOWLEDGMENTS

Thanks to Rulon Clark for his helpful review of this article.

REFERENCES

Barbour, M. A. and R. W. Clark. 2012. Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes. Proceedings of the Royal Society B: Biological Sciences doi:10.1098/rspb.2012.1112. <link>

Clark, R. W., S. Tangco, and M. A. Barbour. 2012. Field video recordings reveal factors influencing predatory strike success of free-ranging rattlesnakes (Crotalus spp.). Animal Behaviour 84:183-190. <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>

Coss, R. G. and D. H. Owings. 1978. Snake-directed behavior by snake naive and experienced California Ground Squirrels in a simulated burrow. Zeitschrift für Tierpsychologie 48:421-435. <link>

Owings, D. H. and R. G. Coss. 1977. Snake mobbing by California ground squirrels: adaptive variation and ontogeny. Behaviour 62:50-69. <link>

Rundus AS, Owings DH, Joshi SS, Chinn E, Giannini N (2007) Ground squirrels use an infrared signal to deter rattlesnake predation. Proceedings of the National Academy of Sciences 104:14372-14376 <link>

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

Goo-eating snakes and the eggs that evade them

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I have just returned from attending the Seventh World Congress of Herpetology (WCH7) in Vancouver, Canada. This meeting is held once every four years, always in the same year as the Summer Olympics, from which it differs in several important ways. Although many celebrities attend each, the WCH primarily consists of scientific, rather than physical, displays of prowess. Until a gold medal is given in lizard noosing, herpetologists will continue to present their research at the WCH, as I had the opportunity to do this year. Because of the large number of excellent talks highlighting new research in snake biology, I have decided that the next several articles on LISBSOL will constitute a series inspired by the work of the many herpetologists whom I saw presenting at WCH7. If you want to learn more about the WCH, check out the June 2012 issue of Herpetological Review, or follow the Twitter hashtag #wch2012, with which I will tag all posts in this series (disappointing though it is that herpetologists should be forced to 'tweet' their research rather than 'hiss' or 'croak' it [I couldn't figure out how to spell the sound that alligators make]).

One tradition at WCH meetings is to open each day with a plenary talk, which is an hour-long presentation by a distinguished herpetologist. Of the several plenaries at WCH7, the one that impressed me the most was given on the first day by Karen Warkentin, a herpetologist at Boston University who studies environmentally-cued hatching of amphibian eggs. One of the foundations of her research is that the timing of hatching, a critical life-stage transition in the life of an amphibian (or reptile), should be flexible in order to maximize the likelihood of survival of the young animals. That is, if the egg is safe from predators and pathogens, hatching should be delayed as long as possible (typically until the embryo is as large as it can get without leaving the egg). However, if the egg is in danger, hatching should speed up, as long as the embryo is capable of living outside of the egg. This phenomenon is observed in a variety of reptiles and amphibians, including  the Agalychnis (red-eyed) treefrogs that Dr. Warkentin studies. These frogs lay their eggs on leaves overhanging pools in the Neotropical rain forests, so that when they hatch the tadpoles can drop into the water.

Agalychnis callidryas in amplexus

The primary predators of Agalychnis eggs are wasps and snakes. In the wild, snakes consume as much as 50% of all Agalychnis eggs laid, so it makes sense that there would be strong selection for eggs that could escape snake predation. If a snake or wasp attacks a clutch of eggs, the vibrations trigger the eggs to hatch almost immediately. If that sounds impossible, check out this video of a Parrotsnake (Leptophis) attacking a clutch of eggs:

Look at those little guys hatch! You can see other videos at Dr. Warkentin's website, where you can compare the feeding behavior of Leptophis with that of the Cat-eyed Snake (Leptodeira). Embryos in the last third of their development escape from snake attacks with about an 80% success rate by hatching up to 30% early, which is really remarkable. Furthermore, they can distinguish snake attacks from other sources of vibration, so that they don't hatch every time it rains. To do this, they respond to several non-redundant vibrational cues, including frequency, duration, and their interaction. These cues propagate throughout the jelly matrix of the eggs, so that eggs that have not yet been touched by the snake can escape. In two species of Agalychnis that have reduced jelly, escape success is much lower, because the signals do not propagate as well.

Vibration profile of a snake attack

According to Dr. Warkentin, the snakes do not appear to prefer younger eggs (which would be incapable of hatching early) or to forage preferentially in the rain (when their vibrations might be masked by raindrops). Along with Leptophis and Leptodeira, two other snake genera, Sibon and Dipsas, possess morphological and behavioral adaptations for feeding on frog eggs and other prey items that are essentially 'goo'. Not unlike the southeast Asian pareatids I've covered before, these Neotropical snakes have numerous, long, slender teeth on the dentary (lower jaw), and they have many skeletal and muscular modifications that allow for jaw flexibility beyond even that normally seen in snakes. Extinction of many frogs due to chytrid fungus in Central America has caused dietary shifts and changes in abundance of these snakes.

Sibon argus eating frog eggs

Environmentally-cued hatching in response to vibrations also occurs in the eggs of other treefrogs, centrolenid glass frogs, and African reed frogs. It can also occur in response to other environmental dangers, such as flooding (in salamander and some turtle eggs) and disease (in frog eggs and also in painted turtle hatchlings, which often overwinter in the nest but are more likely to emerge early when infected with sarcophagid fly larvae). This last example comes from the thesis work of Julia Riley at Laurentian University, who presented preliminary results at the WCH. She also found that turtles hatching in nests that were on steeper slopes were more likely to emerge early, possibly to avoid collapse of the nest over the winter. Whether research will one day show that snake eggs also possess environmentally-cued hatching plasticity is an open question, but I suggest that a good system to start looking would be the Nicrophorus beetle hosts. Maybe we'll be hearing about that at WCH8 in Hangzhou, China!

ACKNOWLEDGMENTS

Thanks to Otto Monge, Brad Wilson, and the Warkentin lab website for providing photos and videos.

REFERENCES

Caldwell MS, McDaniel JG, Warkentin KM, 2009. Frequency information in the vibration-cued escape hatching of red-eyed treefrogs. J Exp Biol 212:566-575. <link>

Caldwell, M. S., J. G. McDaniel, and K. M. Warkentin. 2010. Is it safe? Red-eyed treefrog embryos assessing predation risk use two features of rain vibrations to avoid false alarms. Animal Behaviour 79:255-260 <link>

Gomez-Mestre I, Warkentin KM, 2007. To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs. Oecologia 153:197-206. <link>

Gomez-Mestre I, Wiens JJ, Warkentin KM, 2008. Evolution of adaptive plasticity: risk-sensitive hatching in neotropical leaf-breeding treefrogs. Ecol Monogr 78:205-224. <link>

Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP, 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci USA 103:3165-3170. <link>

Ray JM, Montgomery CE, Mahon HK, Savitzky AH, Lips KR, 2012. Goo-eaters: Diets of the Neotropical snakes Dipsas and Sibon in central Panama. Copeia 2:197-202. <link>

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

Warkentin, KM, 2005. How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Animal Behaviour 70:59-71. <link>

Warkentin KM, Caldwell MS, McDaniel JG, 2006. Temporal pattern cues in vibrational risk assessment by embryos of the red-eyed treefrog, Agalychnis callidryas. J Exp Biol 209:1376-1384. <link>

Warkentin KM, Caldwell MS, Siok TD, D'Amato AT, McDaniel JG, 2007. Flexible information sampling in vibrational assessment of predation risk by red-eyed treefrog embryos. J Exp Biol 210:614-619. <link>

Warkentin KM, Currie CR, Rehner SA, 2001. Egg-killing fungus induces early hatching of red-eyed treefrog eggs. Ecology 82:2860-2869. <link>

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

Scientific American Guest Blog

Also now available in Spanish!

Ahora también disponible en español!

Check out the piece on toxin-sequestering snakes I was invited to write for the Scientific American Guest Blog!!

http://blogs.scientificamerican.com/guest-blog/2012/08/21/poisonous-snakes-cant-resist-toxic-toad-tucker-or-can-they/

Heterodon platirhinos eating Acris crepitans. Photo by Nick Kiriazis

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

Stiletto snakes

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Atractaspis duerdeni

I've always thought that the atractaspids were a highly interesting group of snakes, deserving of an article or two. During the early stages of my cursory research, however, I found that palaeozoologist Darren Naish, author of the excellent blog Tetrapod Zoology, has already written an article containing what one commenter called "the most comprehensive information on Atractaspids anywhere on the web." Since I didn't think I could top that, I decided to focus on what we've learned about atractaspids since Darren's article came out in 2008. If you want to learn more about the many fascinating adaptations atractaspids have evolved for burrowing and closed-mouth fang-stabbing, including why they're known as والد من سواد ('father of blackness'), among other such macabre names, in Arabic-speaking countries in their native range, you'll want to read that article in addition to this one.

The correct placement of the atractaspids within the snake tree of life has been elusive since their initial description in 1843, when they were placed in the Elapidae alongside cobras and coralsnakes. In later classifications, they have been placed in the Viperidae, the Colubridae, the Lamprophiidae, or in their own family, to which various names have been applied, including Atractaspidae (atractaspids), Atractaspididae (atractaspidids, because why not add in an extra 'id'?), and Atractaspidinae (atractaspidines; this last name referring to a subfamily rather than a family). Once considered to include a wider diversity of snakes, the Atractaspidinae is now comprised of just two genera, the proteroglyphous Homoroselaps (2 species, known as Harlequin Snakes) and the eponymous, solenoglyphous Atractaspis (21 species). Aglyphous and opisthoglyphous snakes formerly included in this group are now assigned to a closely related subfamily, the Aparallactinae, which includes 50 species in nine genera, several of which are deserving of their own articles. This taxonomy is based on part of a larger analysis of advanced snakes undertaken by Alex Pyron and colleagues and published in 2010, and hinted at in earlier analyses such as this one by Kraus & Brown.

Part of the tree presented in Pyron et al. 2010, showing the relationships of atractaspids to other African snakes now placed in the Lamprophiidae. A surprising finding of this paper was that lamprophiids share a common ancestor with the front-fanged elapids, including cobras, sea snakes, and coral snakes, about 44 million years ago.

Morphological work on atractaspids has continued to be carried out by Dave Cundall and his students and colleagues at Lehigh University. I had the opportunity to hang out with Dave a bit recently, and he shared some of his recent findings with me. For instance, he said, the long-held idea that Atractaspis fed predominantly on litters of baby mammals might be only party true. The stomach of some atractaspids, he told me, is almost as long as the entire body, an adaptation that could be construed as functioning to accommodate multiple prey items (pups in a litter) but also large, elongate ones (such as amphisbaenians or caecilians), which also frequently occupy underground spaces where hunting by fang-stabbing is effective. Dave also mentioned that digestion in these snakes takes place, as one might expect, only in the stomach, not in the esophagus, although ingested prey may extend forward into the esophagus if they are too large to fit in the stomach. Differences in the tissue lining these two parts of the digestive system account for a pH change of up to 4 units between the esophagus and the stomach, one of the few clues that these two organs in snakes are derived from separate structures in other vertebrates (since their morphological separation in many snakes is subtle at best). Other discoveries made by Dave and his student Alex Deufel, including how atractaspids, perhaps uniquely among advanced snakes, have traded-off prey transport for maximum fang-stabbing ability, have been described in excellent detail by Darren at TetZoo.

No one is quite sure why, but some Atractaspis also possess extremely elongate venom glands, such as those seen here in a dissected A. fallax.

Other recent work on atractaspids includes advances in understanding their unusual venom chemistry and in treating its effects, including the discovery and production of the first atractaspid antivenom in 2007. In a test of this antivenom conducted at the National Antivenom and Vaccine Production Center in Riyadh, Saudi Arabia, rabbits injected with a lethal dose of Atractaspis venom were saved from death by a pre-injection treatment of any one of three drugs: nitroglycerin, atractaspid antivenom, or bosentan, a drug for the treatment of pulmonary hypertension. However, when the drugs were administered after the venom, as would be the case in an actual snakebite, all rabbits treated with nitroglycerin and half the rabbits treated with atractaspid antivenom died. Only the hypertension drug bosentan protected rabbits from the venom in the realistic scenario, leading the author to conclude that bosentan might have a higher affinity to the venom receptors than either the antivenom or the venom compounds themselves.

Atractaspis engaddensis

Finally, a 2011 study by Katie Moyer and Kate Jackson of Whitman College helped initiate our understanding of how the 21 species of Atractaspis are related to one another. Remarkably, this is the first time someone has investigated this question, and because Moyer & Jackson used morphological data, there are likely to be some changes once DNA sequences for these species become available. Using characteristics of the scale arrangements, they prepared an evolutionary tree that differed from all previous hypotheses about how the species of Atractaspis are related. Although their analysis is limited by the paucity of available data, it represents a starting point for understanding the evolution of this highly unique group of snakes.

ACKNOWLEDGMENTS

Thanks to Michael & Patricia Fogden and Donald Schultz for photographs.

REFERENCES

Abd-Elsalam M, 2011. Bosentan, a selective and more potent antagonist for Atractaspis envenomation than the specific antivenom. Toxicon 57:861-870.

Bourgeois M, 1961. Atractaspis – a misfit among the Viperidae? News Bulletin of the Zoological Society of South Africa 3:29.

Deufel A, Cundall D, 2003. Feeding in Atractaspis (Serpentes: Atractaspididae): a study in conflicting functional constraints. Zoology 106:43-61.

Greene HW, 1997. Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press.

Ismail M, Al-Ahaidib M, Abdoon N, Abd-Elsalam M, 2007. Preparation of a novel antivenom against Atractaspis and Walterinnesia venoms. Toxicon 49:8-18.

Moyer K, Jackson K, 2011. Phylogenetic relationships among the Stiletto Snakes (genus Atractaspis) based on external morphology. African Journal of Herpetology 60:30-46.

Naish D, 2008. Side-stabbing stiletto snakes. Tetrapod Zoology.
<http://scienceblogs.com/tetrapodzoology/2008/05/26/sidestabbing-stiletto-snakes/>

Pyron RA, Burbrink FT, Colli GR, de Oca ANM, Vitt LJ, Kuczynski CA, Wiens JJ, 2010. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58:329-342.

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

Snakes flying without planes

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By now, all of us herpetologists have heard quite enough 'Snakes on a Plane' jokes, thank you very much (they're second only to jokes about how we probably study STDs - never heard that one before). Meanwhile, in reality, snakes have been flying - well, gliding, really - since long before Samuel L. Jackson had had it with them.

True flight, actively wing-powered and sustained for lengthy periods of time, has evolved only four times (in insects, pterosaurs, birds, and bats). In contrast, gliding flight (defined as falling at an angle more shallow than 45° from horizontal) is more energy efficient and has evolved many times, and many birds use both gliding flight and true flight depending on the circumstance. Among the vertebrates are found gliding lemurs, squirrels, fishes, frogs, lizards, ants, squids, and of course snakes. Of all the groups that have evolved gliding, snakes would seem to be the least likely candidates, because of their long, cylindrical body that seems ill-suited for flight. But evolve to glide they have. Many gliding groups live in the rainforests of Asia, especially on the island of Borneo, where the trees are very tall and widely spaced, and southeast Asia is where you will find the five species of gliding snake, genus Chrysopelea.

Chrysopelea paradisi

As with many species native to this region of the world, there are a lot of unknowns about gliding snakes. We don't know very much about how they spend their time in the wild, what they eat, or what eats them. Until recently, relatively few scientific papers had been published on Chrysopelea, including a note on their flight in 1906.¹

Jake Socha, a comparative biomechanics researcher at Virginia Tech, studies the gliding flight of Chrysopelea. For his PhD at the University of Chicago, he characterized their mechanism of takeoff, the postures they adopt while gliding, and contributed substantially to our knowledge of their morphology. Socha and colleagues used multiple synchronized video cameras to film and digitally reconstruct the trajectory, speed, and body posture of gliding Chrysopelea, which they frightened off a three-story scaffolding built with a branch sticking out of the side, to simulate a tree. The videos showed that the snakes could descend at a very shallow angle of 13°, comparable to flying squirrels and other accomplished gliding vertebrates.

Next, Socha and colleagues looked for relationships between measures of the snakes' flight performance, such as glide angle and horizontal speed, and morphological characteristics of the snakes. They found that smaller snakes were better able to glide long distances than larger ones, and that the wave amplitude of the snake's body was a more important predictor of flight behavior than its wave frequency, the latter of which they hypothesize helps maintain stability during flight.

Undulating behavior of gliding Chrysopelea

In order to transform their bodies from fairly non-aerodynamic cylinders into a more aerodynamic wing-like shape that generates lift, Chrysopelea can flatten their body by extending their ribs, an observation first made by Robert Shelford (also the first person to document their gliding behavior, in 1906). The flattening process proceeds from anterior to posterior, does not include the tail, and takes only 100–350 milliseconds to complete. Although the exact mechanism of rib expansion has not been examined, it is presumably similar to that used by cobras to spread their hoods. Because the rib muscles are also involved in breathing, it is likely that Chrysopelea cannot breathe when gliding, which could physiologically limit the duration of their glides.

Figure from a 1906 paper describing the change in shape of the body of Chrysopelea.

Finally, Socha and colleagues have investigated Chrysopelea's take-off behavior in great detail, using the same synchronized camera set-up they used to film the snakes in flight. I won't go into excruciating detail (you can read the whole paper here), but you can get an idea of the movements involved by looking at the beautiful images produced below.

So far, the five species of Chrysopelea are the only known gliding snakes, although anecdotal reports suggest that their close relatives, the Bronzeback Snakes in the genus Dendrelaphis, are also capable of making gliding leaps. Although Chrysopelea have been known since the time of Linneaus (who described only their color, as "green, with a yellow line on both sides"), we are still learning about them today, and will probably never know all there is to know. In addition to having a fascinating natural history, these snakes are also incredibly graceful and beautiful. I think I would like to see one in the wild more than just about any other snake, which is always a bold statement to make. One day... 

---

1 The author, Robert Shelford, was brought dead specimens of Chrysopelea in the late 1890s by Dyak villagers in inland Borneo, who told him that they were of a flying species. Skeptical, he obtained some live specimens and tested them by dropping them from heights of 15-20'; "after one or two false starts the snake was felt to glide from the experimenter's hands".

ACKNOWLEDGMENTS

Thanks to photographers Angi Nelson and Jake Socha. If you have more questions about Chrysopelea, check out Jake Socha's Chrysopelea FAQ.

REFERENCES

Shelford R (1906) A note on "flying" snakes. Proceedings of the Zoological Society of London 76:227-230

Socha JJ (2002) Kinematics: Gliding flight in the paradise tree snake. Nature 418:603-604

Socha JJ (2006) Becoming airborne without legs: the kinematics of take-off in a flying snake, Chrysopelea paradisi. Journal of Experimental Biology 209:3358-3369 <link>

Socha JJ (2011) Gliding flight in Chrysopelea: Turning a snake into a wing. Integrative and Comparative Biology 51:969-982 <link>

Socha JJ, LaBarbera M (2005) Effects of size and behavior on aerial performance of two species of flying snakes (Chrysopelea). Journal of Experimental Biology 208:1835-1847 <link>

Socha JJ, O'Dempsey T, LaBarbera M (2005) A 3-D kinematic analysis of gliding in a flying snake, Chrysopelea paradisi. Journal of Experimental Biology 208:1817-1833 <link>

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

Snake-eating snakes

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I've mentioned before how snakes can eat nearly anything, due to amazing adaptations of their head and jaws that allow them to swallow objects bigger than their heads. But surely they must be limited to eating prey that are shorter than they are in overall length, right? What about items that are just a bit longer?

There are a wide variety of snakes that eat other elongate vertebrates, including other snakes, legless lizards, lizards with relatively small legs (like skinks), amphisbaenians, caecilians, and eels (today we'll focus on snakes, but look out for future articles on some of these other specialized diets). In many ways, this kind of diet is convenient for a snake, because they are already elongate, so they don't have to deform their stomachs, bodies, and mouths to the same extent as snakes that eat bulkier prey. Many are relatively primitive snakes that retain the robust skulls of their lizard-like ancestors, but quite a few derived snakes are snake-eaters as well, including the King Cobra, Ophiophagus hannah, the world's largest venomous snake.

The genus Ophiophagus means 'snake-eating'

Other familiar snake-eaters include the North American Kingsnakes (genus Lampropeltis), which have evolved resistance to the venom of many species of viper. Eastern Indigo Snakes (Drymarchon couperi) and their Central and South American relatives are also frequent snake eaters, and many other species of North American colubrids sometimes dine on each other, including Racers (Coluber constrictor), Coachwhips (genus Masticophis, now sometimes included in the racer genus Coluber), Garter and Ribbon Snakes (genus Thamnophis), and Coral Snakes (genus Micrurus). Among their prey are many of North America's venomous snakes, including the Copperhead (Agkistrodon contortrix), Cottonmouth (or water mocassin, Agkistrodon piscivorus), and many species of rattlesnake (genera Crotalus and Sistrurus), as well as many non-venomous species of snake. Because all snakes are predatory, the existence of snake-eating snakes implies that some snakes are feeding at a very high trophic level indeed, and indeed they may represent top predators in some ecosystems.

Just how does a snake accomplish eating another? It is an arduous process, especially when the prey snake is as long as or longer than the predator. It's true: some snakes are able to ingest other snakes that equal or exceed their own body length. That means that these snakes must fit an object longer than their entire body into just their stomach, which (perhaps it goes without saying) is not as long as their whole body. The prey must be fit into the stomach, and cannot extend into the intestine or the esophagus, because the lining of the stomach is the only part of the digestive system that secretes digestive enzymes.

Body width is not nearly as much as a problem - snakes have highly kinetic skulls and very strong and flexible trunk muscles, so they can both expand their body cavity and compress their prey in order to accommodate very wide meals. But there is a limit to the length of their gut - it cannot extend into their tail, which is solid with muscle, nor can the prey easily be left hanging out of the mouth, where it could impede the snake's movement, interfere with sensory processes, or begin to decompose.

As determined in a paper by one of my favorite herpetologists, Kate Jackson, the author of the popular herpetological book Mean and Lowly Things, the solution hit upon by North American Kingsnakes seems to be to throw the prey into waves to decrease its length and pack it into the space available. They accomplish this by concertina-like motions of their own vertebral column, which causes the (dead) prey snake's body to conform in shape to that of its predator. The predator snake can then straighten out again while advancing its jaws, so that the standing waves were left in the body of the prey snake. As you can see from the below X-ray images, taken from Jackson's paper with  functional morphologists Nathan Kley and Elizabeth Brainerd, this allows the predator snake to pack pretty long snakes into its gut. It's the same principle as meandering your path increases the total distance you walk without affecting the straight-line distance from your starting point (in this case, the snake's mouth) to your finishing (here, the posterior end of the snake's stomach). Kingsnakes tested in Jackson et al.'s paper were able to ingest Cornsnakes (Pantherophis guttatus) up to 139% of their body length and up to 135% of their pre-feeding body mass, which would be like a 6'0", 175 lb. person eating an 8'4", 236 lb. meal - in one bite. Without using their hands.

As the prey snake is digested, a decrease in wavelength and increase in amplitude of the waves of the prey snake’s vertebral column takes place, because the prey snake's body becomes more compressible as its tissues are digested off. In Jackson's experiment, it took the Kingsnakes about 7-10 days to completely digest these huge meals (although a few of them regurgitated their prey after a couple days).

Once, I was lucky enough to observe a young racer that had just eaten a Ring-necked Snake (Diadophis punctatus) at a nature preserve in east-central Illinois:

As you can see, she was pretty much catatonic. The Ring-necked Snake she had eaten was 26.5 cm in length, and she herself measured only 28.9 cm, so her prey was >90% of her total length! You can really get an impression from this photo of the lumpy, kinked quality of the body of a snake that has recently eaten another, caused by the waves of the prey snake's body inside the gut of the predator.

An x-ray of a mudsnake (Farancia abacura) with a
three-toed amphiuma (Amphiuma tridactylum)
From Haertle et al. 2015

Edit: an observation published in 2015 showed that mudsnakes, which eat large, elongate prey such as sirens and amphiumas, also push their prey's vertebral columns into waves in order to fit them into their guts.

ACKNOWLEDGMENTS

Thanks to Belinda Wright for the photograph of the King Cobra.

REFERENCES

Durso, AM & NM Kiriazis. 2011. Coluber constrictor (North American Racer) Prey Size. Natural History Note. Herpetological Review. 42(2):285 <link>

Haertle, N. E., P. M. Hampton, P. N. Vogrinc, and J. D. Willson. 2015. Farancia abacura (Red-bellied Mudsnake). Feeding behavior. Herpetological Review 46:449-450 <link>

Jackson K, Kley NJ, Brainerd EL. 2004. How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae). Zoology 107(3):191-200. <link>

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

This blog is supposed to be about snakes, but if you can't make exceptions for family, then you're a jerk

Click here for this article in Spanish!

Haga clic aquí para ver este artículo en español!

Sphaerodactylus elegans of Cuba

Geckos are some of the most diverse and widespread squamates on Earth. They range in size from the dwarf Sphaerodacylus of the Antilles (16-18 mm) to the (probably) extinct Kawekaweau or Delcourt's Giant Gecko, Hoplodactylus delcourti, of New Zealand (as long as a tuatara and as thick as a man's wrist). Except for a few species, none have eyelids, and most have adhesive pads on their toes that allow them to climb slick surfaces. Some are parthenogenic. A few owe their success partly to humans, and it is these that we consider here today.

Several species of gecko have been introduced to the United States by humans, most accidentally, as stowaways or through the pet and greenhouse trade. One of the most ubiquitous is the Mediterranean House Gecko, Hemidactylus turcicus. Described by Linnaeus in the first edition of his Systema Naturae, it is a yellow-tan, nocturnal, insectivorous gecko about six inches long. Whereas most of our non-native lizards are limited to a few small areas in Florida, H. turcicus can be found in 17 states, from California to Maryland. It isn't continuously distributed across the southern US, but rather locally common in urban sites, due to many separate introductions, the earliest of which occurred in Key West before 1915. One such population is in a middle school in Cary, North Carolina.

Hemidactylus turcicus

Legend has it that a science teacher during the early 1980s was keeping some H. turcicus in a terrarium. All was well until an absentminded student left the lid off one day. The lizards escaped, and a small population has been living in the walls of the school campus ever since. At least, that's what everyone thought. An ongoing summer of research conducted by a wildlife student at North Carolina State University, my brother Kevin Durso, in 2012, has revealed that the population is much larger than anyone thought.

Bags of geckos

On the first night, Kevin counted 82 geckos on the walls of the campus buildings. He came back with reinforcements - tall college students and volunteers armed with lizard nooses and water guns, for blasting geckos off ceilings and walls. On some nights, students at the middle school come out with their teachers and parents to see what the research is all about. Kevin & Co. are marking each gecko they capture with glow-in-the-dark elastomer, so they can be individually identified upon later capture. Once captures of new, unmarked geckos begin to decline, he can begin to estimate the total size of the population using a mathematical model. Whether this will happen sooner or later is still hard to know. Kevin is also keeping track of the exact location of each gecko sighting, so that a home range size estimate can be made. He works at night, when the geckos are most active. Perhaps this is why no one knew the true size of the gecko population until now - how often is anyone at school at night? Not if I can help it, Mom!

Super Soaking a gecko off a wall

Previous research on house geckos has revealed that they inhabit similar areas, both climatically and in terms of microhabitat, in their native and non-native range. A population on the Stephen F. Austin State University campus in Nacogdoches, Texas, ate mostly grasshoppers, moths, and isopods. Their great success in southern North America has been attributed to low predation pressure, little interspecific competition, and a life history which maximizes survival at all ages. House geckos in southern Louisiana are host to native North American parasitic worms, so there is some potential for parasites to regulate populations of these non-native lizards.

Injecting a gecko with glow-in-the-dark elastomer

What factors have allowed the Cary H. turcicus population to grow so large? What effects do these non-native geckos have on the local ecosystem, from the arthropods they eat to the birds and snakes they are eaten by? Have they been spreading around the Triangle area since the 1980s, brought home on schoolbuses in students' backpacks and coats? Only time, and further research, will tell.

ACKNOWLEDGMENTS

The College of Natural Resources and the Office of Undergraduate Research at NC State University provided support and funding for this project. Thanks to Konrad Mebert, Miguel Landastoy, Alex Morrison, Kevin Durso, and Sandy Durso for photographs.

REFERENCES

Davis WK (1974) The Mediterranean gecko, Hemidactylus turcicus in Texas. Journal of Herpetology 8:77-80

Rödder D, Lötters S (2009) Niche shift versus niche conservatism? Climatic characteristics of the native and invasive ranges of the Mediterranean house gecko (Hemidactylus turcicus). Global Ecology and Biogeography 18:674-687

Rose FL, Barbour CD (1968) Ecology and reproductive cycles of the introduced gecko, Hemidactylus turcicus, in the southern United States. American Midland Naturalist 79:159-168

Saenz D (1996) Dietary overview of Hemidactylus turcicus with possible implications of food partitioning. Journal of Herpetology 30:461-466

Selcer KW (1986) Life history of a successful colonizer: the Mediterranean gecko, Hemidactylus turcicus, in southern Texas. Copeia 1986:956-962

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

Egg-eating snakes

To view this blog post in Spanish, click here!

Para ver este blog en español, haga clic aquí!

I think we can all agree that amniotic eggs are delicious. They also happen to be one of the best sources of energy out there, and this is at least partially why we, and many other animals, enjoy eating them so much. In addition, they rarely fight back, and they almost never have physical defenses, such as spines, or chemical ones, such as deadly toxins. In fact, on the inside they're pretty much all lipids (a group of molecules including fats and cholesterol), surrounded by either a leathery (in monotremes and most reptiles) or a hard, calcified (in birds) shell. I've already written about a species of burying beetle that specializes on snake eggs, apparently with great benefit to its fecundity relative to other burying beetles that use carrion. Turns out, snakes aren't above specialized oophagy themselves.

There are a few snakes that eat anamniotic eggs, such as the turtle-headed sea snakes (about which I've written before) and the South American goo-eaters. These have many amazing adaptations to eating shell-less eggs, but I'd like to focus on the amniotic egg-eating snakes for now. To review, an amniotic egg is one with a shell and several other embryonic membranes, called the amnion, chorion, and allantois. These structures physically protect the embryo and facilitate gas and waste exchange between the embryo and its surroundings, because the shell is too thick to allow the embryo to breathe and excrete by diffusion alone. These eggs are laid by birds, many reptiles, and monotremes (egg-laying mammals such as the platypus and echidna). In placental mammals (including humans), which are also amniotes, some of these structures are part of the umbilical cord, while others are vestigial. Amniotic eggs are adapted for being laid on land, and even the most aquatic of amniotes, such as sea turtles and pelagic birds, must come to land to lay their eggs.

Because of the resilience and self-contained nature of amniotic eggs, many organisms that lay them have done away with parental care. Choosing a nest site, usually under a rock, log, or pile of poop, or in a nest dug underground, is the extent of it. Beyond that, a female snake or turtle will most likely never see her kids hatch, let alone grow up, graduate, or become successful. This also means that their eggs are basically undefended from predators, except for being concealed and not smelling very much. Birds are slightly better parents, but they risk giving away the location of their nest to predators by flying back and forth to it many times a day. Experiments conducted by herpetologist Steve Mullin and ornithologist Bob Cooper have shown that gray ratsnakes locate bird nests over twice as quickly when parents are attending than when they aren't, a phenomenon so prevalent that it has its own name (Skutch's hypothesis) and is thought to influence the evolution of optimal clutch size in birds (because more offspring need to be fed more often, necessitating more trips to and from the nest and increasing the likelihood of detection by a predator).

Ok, enough - let's get to the pictures of snakes eating eggs!

East African Egg-eating Snake, Dasypeltis medici

How do they do that!? That snake is going to choke itself! Got to be a faked, Photoshopped image, right? Think again:

Damn, that's impressive. If you watched the video above, you saw an African Egg-eating Snake, perhaps the most specialized oophagous snake there is, swallow a bird egg whole, crack it open, and regurgitate the  shell. How does it do it? The highly kinetic, flexible skull of this snake allows it to maneuver its jaws around an egg many times bigger than its head, despite the smooth, round surface and the snake's lack of hands. It'd be like a human trying to eat a whole watermelon. Egg-eating snakes lack teeth almost entirely, not needing them for gripping their prey. In addition, the snake's skin is stretchy enough to accommodate the egg's passage - the scale rows are clearly visible, widely separated by the skin in between. Most of the time, this skin can't be seen, because the skin is relaxed so that the rows of scales are in contact with one another.

Once the egg is in the snake's esophagus, how does it get cracked open? Snakes have strong digestive juices, but waiting for them to dissolve the shell of an egg would take too long. OK, are you ready? This is the coolest part:

Vertebral hypapophyses of  African egg-eating snakes, Dasypeltis

See those spines? Those are called hypapophyses, which is a fancy term for things that stick off the bottom (ventral side) of vertebrae. You've got them too - but in egg-eating snakes, they're modified to be much larger and sharper, the better to pierce eggshells with, my dear. At least, the ones on vertebrae 17-38 are, the vertebrae that sit right above the esophagus and thus above egg once it has been swallowed. The esophagus itself is modified as well - it has loose folds, like pockets, into which each of the hypapophyses fits, so that they don't puncture the esophagus itself. See how it works in the following video, from the BBC's Life in Cold Blood:

Starting at 2:45, you can see the moving x-ray of the egg-eating snake swallowing the egg. Continuing through the end of the video, the snake cracks the shell, allows the yolk inside to drain into its stomach, and regurgitates the eggshell. Most amazing, young Dasypeltis don't appear to have these hypapophyses - they grow as the snakes get older, which raises questions about what the juveniles eat. Even though eggs are nutritious, Dasypeltis must feed relatively often for a snake - one that my advisor kept in captivity ate several quail eggs a week.

Lateral view of the skull of Dasypeltis, from Gans 1952

The adaptations of the nine species of Dasypeltis allow them to eat eggs that are very large relative to their body size, and as far as we know they eat almost nothing else. Several generalist snakes also eat eggs; adult Eastern Kingsnakes (Lampropeltis getula), Western Hog-nosed Snakes (Heterodon nasicus), and Formosa Kukrisnakes (Oligodon formosanus) frequently consume reptile eggs, and many members of the rat snake genera Pantherophis and Elaphe opportunistically feed on both eggs and nestling birds. These snakes, however, have no special morphological or behavioral adaptations to assist them in the consumption of eggs. One species, the Japanese rat snake (Elaphe climacophora), can ingest relatively large eggs, and has several vertebral hypapophyses. However, E. climacophora ingests the entire egg, including the shell. Only Dasypeltis, and possibly a poorly-known species from India called Elachistodon westermanni, specialize in ingesting large eggs, then crushing the shell and retaining solely the contents.

Defensive display by Dasypeltis scabra

ACKNOWLEDGMENTS

Thanks to David Marti, Armata, Tony Phelps, and the BBC for images and videos.

REFERENCES

Coleman K, Rothfuss LA, Ota H, Kardong KV (1993) Kinematics of egg-eating by the specialized Taiwan snake Oligodon formosanus (Colubridae). Journal of Herpetology 27:320-327

Gans C (1952) The functional morphology of the egg-eating adaptations in the snake genus Dasypeltis. Zoologica 37:209-244

Gans C, Oshima M (1952) Adaptations for egg eating in the snake Elaphe climacophora (Boie). American Museum Novitates 1571:1-16

Gartner G, Greene H (2008) Adaptation in the African egg-eating snake: a comparative approach to a classic study in evolutionary functional morphology. Journal of Zoology 275:368-374

Mullin SJ (1996) Adaptations facilitating facultative oophagy in the gray rat snake, Elaphe obsoleta spiloides. Amphibia-Reptilia 17:387-394

Mullin SJ, Cooper RJ (1998) The foraging ecology of the Gray Rat Snake (Elaphe obsoleta spiloides)—visual stimuli facilitate location of arboreal prey. The American Midland Naturalist 140:397-401

Savitzky AH (1983) Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist 23:397-409

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