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

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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

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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.

Snakes that chew their food

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I have to admit right up front that the title of this article is not really accurate. No snakes chew their food the way we do. Almost all snakes must swallow their food whole, which limits their (often considerable) gape to items they can jaw-walk their kinetic skulls over. Taken as a whole, there are few animals on Earth that snakes do not eat -- whales and dolphins, elephants, animals endemic to the polar regions, some very toxic millipedes. There are snakes that swallow leopards whole, snakes that eat porcupines without removing the quills, snakes that tolerate stabs from catfish spines, snakes that eat other snakes longer than they are. Here's a video of a Tantilla eating a giant centipede. As a group, they can eat nearly anything. They all swallow their prey whole. Almost.

Except for this one

Its genus name is Fordonia, which is probably meaningless, seeing as it was biologist J.E. Gray of the British Museum of Natural History,"well known for inventing many apparently meaningless scientific names", who came up with it (he also named the North American Farancia). Commonly known as the Crab-eating Water Snake or White-bellied Mangrove Snake (after the specific epithet), Fordonia leucobalia is native to the mangrove swamps and tidal mud flats of southeast Asia and northern Australia. It lives in mud lobster and fiddler crab burrows, and moves by jumping across the soft mud, into which it would sink if it tried to slither.

Part of a small but interesting group of live-bearing snakes known as homalopsids, Fordonia is southeast Asia's answer to the North American natricine Nerodia, for many the archetypical semi-aquatic snake. What sets Fordonia apart from other homalopsid snakes, which feed mostly on fishes, is that it eats crabs, an observation first made by Cantor in 1847. (This may be highly cathartic for the snakes, whose primary predators as juveniles include large crabs.)

Those are hard-shelled decapod crustaceans, for you biologists out there 

Like many other arthropods, crabs have an anti-predator adaptation called leg autotomy, similar to tail autotomy in lizards, salamanders, and some snakes. This means that their legs can break off when grabbed and will later regrow - better to lose a limb and escape than to be eaten whole. But Fordonia has evolved behaviors that exploit the crabs' ability to autotomize their legs - it pins the crab's body to the mud and pulls off its legs, eating them one at a time! Sometimes they also consume the crab's body, but often they just leave it behind. This makes Fordonia the only snake that breaks its prey apart prior to eating it, although we must admit that it is somewhat helped along by the crab's autotomy. This discovery was sufficiently exciting to be published in the prestigious journal Nature.

The five crab legs at the top, eaten by this snake, came from a crab about the size of the one on the bottom. The white circle represents the maximum-sized prey item the snake could have eaten whole. Figure from Jayne et al. 2002

The adaptations of Fordonia to cancrivory don't end there. As anyone who has eaten crab legs knows, a crab's exoskeleton is very tough - we humans must use tools to break into it. In order not to be internally lacerated by their prey, Fordonia have evolved extra tough, muscular stomach lining. Other crustacean-eating snakes, such as the North American crayfish snakes (genus Regina), as well as the arthropod-eating False Hook-nosed Snake (Pseudoficimia frontalis, a sonorine snake from western Mexican dry forests), also have thickened muscles surrounding their stomachs, to prevent internal damage from they prey's sharp exoskeletons.

Digestion in snakes is an intense process: their digestive enzymes are very strong, capable of breaking down  even bone. Still, a little mastication can help the digestive process along considerably. For most snakes this isn't an option, because their needle-like teeth and highly mobile skull bones are ill-suited to both cutting and generating bite forces. However, snake biologist Alan Savitzky reported that recently ingested crab legs extracted from Fordonia stomachs were crushed. How is this possible? In fact, Fordonia possess remarkably robust and compact teeth for a snake, almost like molars! Although this is an extreme morphological modification, Savitzky remarked that it is almost surprising that the teeth and skulls of Fordonia aren't more abnormal, considering their unusual diet. Finally, Fordonia has evolved a large salt gland to help maintain osmotic balance on a high-salt diet (crabs are isosmotic to their environment, meaning that they have the same salt content as sea water).

Left: Tooth of Cerberus rynchops; Right: Teeth of Fordonia leucobalia

While Fordonia does all this with hard-shelled crabs, another homalopsid species found in the same mangroves, the Cat-eyed Watersnake (Gerarda prevostiana), has been found to consume freshly-molted (and therefore soft-shelled) crabs in much the same way. This kind of specialization is also found among the four species of North American Crayfish Snakes (Regina) - two of which (R. rigida, R. alleni) have hinged teeth to help them consume hard-shelled crayfish, and two of which (R. grahamii, R. septemvittata) seek out freshly-molted crayfish by smelling their molting secretions. Incredibly, although Gerarda lacks the morphological adaptations for cancrivory of Fordonia, it was observed tearing apart the soft carapaces of crabs after eating their legs, which probably allows Gerarda to consume crabs that would otherwise be too large for them to swallow whole. The feeding mechanisms used by Fordonia and Gerarda differ in the modes of attack and prey restraint, the usual orientation for swallowing crabs, and how pieces were torn from prey, suggesting that they might have evolved their crab-eating habits independently and convergently, rather than inheriting them from a shared common ancestor (although they are evolutionary sisters, one another's closest relatives). Two other closely related genera of homalopsine, Myron and Cantoria, also consume some crustaceans, but are less well-known. How many snakes are out there with strange dietary adaptations that remain to be discovered? We may never know.

This snake only eats soft-shelled crabs - what a snob

ACKNOWLEDGMENTS

Thanks to A. Captain and Brendan Schembri for photographs.

REFERENCES

Alfaro ME, Karns DR, Voris HK, Brock CD, Stuart BL (2008) Phylogeny, evolutionary history, and biogeography of Oriental-Australian rear-fanged water snakes (Colubroidea: Homalopsidae) inferred from mitochondrial and nuclear DNA sequences. Molecular phylogenetics and evolution 46:576-593

Jayne BC, Voris HK, Ng PKL (2002) Snake circumvents constraints on prey size. Nature 418:143

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

Shine R, Schwaner T (1985) Prey constriction by venomous snakes: a review, and new data on Australian species. Copeia 1985:1067-1071

Voris HK, Jeffries WB (1995) Predation on marine snakes: a case for decapods supported by new observations from Thailand. Journal of Tropical Ecology 11:569-576

Voris HK, Murphy JC (2002) The prey and predators of Homalopsine snakes. Journal of Natural History 36:1621-1632

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 beetles

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So little is known about the parasites of snakes that we tend to discount them all together, but the ecological  and evolutionary interactions between hosts and their parasites can be very strong. This is a story about how two enterprising snake biologists solved a mystery that had been puzzling entomologists for decades.

Burying beetles (genus Nicrophorus) conceal small vertebrate carcasses underground and prepare them for consumption by their young by excavating a crypt up to 60 cm deep, removing fur or feathers from the carcass, and covering it in anal secretions to prevent fungal growth. The two parents slowly eat the carcass, defending it from other carrion eaters, and feed regurgitated bits of it to their altricial larvae, which hatch from eggs they lay in the walls of the crypt and beg to be fed like baby birds. Although feeding your babies poop-coated vomit sounds like the plot of a gruesome horror movie, it has been a successful evolutionary strategy for the burying beetles. Their complex social behavior, including biparental care and communal breeding, is unusual among insects. The whole process takes about two weeks.

Nicrophorus pustulatus

Of the nearly 75 species of burying beetle, distributed throughout the Northern Hemisphere, one in particular stands out for its unusual natural history. Entomologists studying the group use dead mice to bait traps, but one species, Nicrophorus pustulatus, never seemed attracted to the carrion. In addition, they are able to produce very large broods (up to 190 vs. 30-45 for most other species of burying beetle) of large offspring on carcasses in the laboratory. Usually, a large brood size comes hand-in-hand with a decrease in individual offspring size, but not in this species apparently. Why not?

Theories ranged from that N. pustulatus used larger carcasses, such as rabbits, without burying them, to that  it was an interspecific brood parasite, like a brown-headed cowbird, laying its eggs in the nests of other burying beetles. But in 2000, a paper in the journal Ecoscience by two snake biologists, Gabriel Blouin-Demers and Patrick Weatherhead, then of Carleton University in Ontario, revealed a surprising discovery. They were studying the nesting ecology of black ratsnakes (Pantherophis obsoletus, formerly Elaphe obsoleta) in Canada by radio-tracking adult female ratsnakes to their oviposition sites. Their purpose was to document the use of communal nests by these snakes and to collect information on clutch size and juvenile survival. When they examined the ratsnake nests they found, they discovered that many of them contained adult and larval  N. pustulatus.

Ratsnake eggs parasitized by carrion beetles

Blouin-Demers and Weatherhead found evidence of beetles in six of the seven nests they looked at. In some nests, only old eggshells with small holes evidenced the beetles' presence, but in others 100% of the eggs were destroyed by the beetles and their larvae. Because black ratsnakes nest communally in this part of the world, up to 111 eggs can constitute a nest, even though the average clutch size is only 11-15 eggs per female. The ratsnakes use the same communal nesting sites year after year, which can be highly beneficial because of increased nest temperature and shorter development time. At such northern latitudes, female ratsnakes do not lay eggs until June or July, and the babies must hatch by late August in order to avoid being killed by an early frost. A mother ratsnake's only parental care is her nest site choice, and research has shown that eggs laid in communal nests hatch earlier, grow larger in their first year, and can even swim faster than those incubated with just their clutchmates. However, the probability of a beetle infection probably increases with increasing nest size, because it only takes one infected egg to spread the beetles to the whole nest. This is why N. pustulatus is so fecund compared to other carrion beetles - because it can raise enormous numbers of larvae on large snake nests, full of nutritious eggs and already hidden away in sites with ideal thermal and humidity.

Black Ratsnake (Pantherophis obsoletus)

Based on their findings, Blouin-Demers and Weatherhead characterized N. pustulatus as a parasitoid of snakes. A parasitoid is different from a parasite because they are parasitic only as larvae (although in this case, with a little help from their parents), and they always kill their host. However, they are also different from predators, because each parasitoid larva only kills a single host individual instead of many. Blouin-Demers and Weatherhead suggested that theirs was the first example of a vertebrate being host to an arthropod parasitoid, and so far they are correct.

The full mystery is far from solved, though. Did N. pustulatus evolve this behavior by first exploiting snake eggs that failed to hatch? How do the beetles find reptile eggs? Are communal nests easier for the beetles to find, or do they simply prefer them because of their higher concentration of resources? How has parasitism by this beetle influenced ratsnake evolution? Do any other species of Nircophorus also parasitize reptile eggs? Does N. pustulatus beetles also parasitize the eggs of other species of snake? Observations of fox snake (Pantherophis vulpinus) nests in Illinois have also yielded beetle larvae. The range of N. pustulatus extends farther north than that of any oviparous snake species (snakes at high latitudes tend to be viviparous, because the females can more precisely control the temperature of their developing offspring if they carry them around). What do they use for rearing their young up there? Could it be turtle eggs, or do they use small animal carcasses like their ancestors?

Nicrophorus pustulatus with phoretic mites

From the beetle's perspective, it has arrived at a very successful reproductive strategy by shifting hosts. By moving away from nesting in carcasses, for which they must compete with flies, ants, fungi, bacteria, and scavenging vertebrates such as skunks and raccoons, it has secured an apparently unique niche. As a defense against carcass competitors, some Nicrophorus species carry phoretic mites that eat fly eggs, but lab experiments have shown that the mites sometimes eat the beetles' eggs too, so the benefit is not without risk. Additionally, not having to move or bury snake eggs saves the parent beetles a lot of energy prior to laying their eggs. Experiments have shown that N. pustulatus females oviposit rapidly in house snake (Lamprophis) eggs, and that male beetles elevate their sex pheromone emission in response to snake eggs. Other beetles in the genus Nicrophorus did not show the same response. While N. pustulatus will use mouse carcasses to rear their young in the lab, no one has ever found them doing so in the field. The entomologists who performed these lab tests also found that N. pustulatus adjusted its fecundity to the available mass of snake eggs.

As a driver of evolution in oviparous snake nesting strategies, Nicrophorus pustulatus may play an important role. Could they potentially pose a threat to egg-laying snake species that are of conservation concern, such as the Eastern Indigo Snake (Drymarchon couperi)? What might happen if they were introduced to a continent whose snakes had not evolved with parasitic beetles eating their eggs? There is still so much we don't understand about snake behavior, reproduction, ecology, and evolution, especially in the wild. Thanks to the observations of a few scientists who thought they were studying something else entirely, we are one step closer.

ACKNOWLEDGMENTS

Thanks to Joyce Gross, Loren Padelford, and Gabriel Blouin-Demers for allowing me to use their photographs.

REFERENCES

Blouin-Demers G, Weatherhead PJ (2000) A novel association between a beetle and a snake: parasitism of Elaphe obsoleta by Nicrophorus pustulatus. Ecoscience 7:395-397 <link>

Blouin-Demers G, Weatherhead PJ, Row JR (2004) Phenotypic consequences of nest-site selection in black rat snakes (Elaphe obsoleta). Canadian Journal of Zoology 82:449-456 <link>

Ikeda H, Kubota K, Kagaya T, Abe T (2006) Niche differentiation of burying beetles (Coleoptera: Silphidae: Nicrophorinae) in carcass use in relation to body size: estimation from stable isotope analysis. Applied Entomology and Zoology 41:561-564 <link>

Robertson IC (1992) Relative abundance of Nicrophorus pustulatus (Coleoptera: Silphidae) in a burying beetle community, with notes on its reproductive behavior. Psyche 99:189-198 <link>

Scott MP (1998) The ecology and behavior of burying beetles. Annual Review of Entomology 43:595-618 <link>

Smith G, Trumbo S, Sikes D, Scott M, Smith R (2007) Host shift by the burying beetle, Nicrophorus pustulatus, a parasitoid of snake eggs. Journal of Evolutionary Biology 20:2389-2399 <link> 

Trumbo ST (2007) Defending young biparentally: female risk-taking with and without a male in the burying beetle, Nicrophorus pustulatus. Behavioral Ecology and Sociobiology 61:1717-1723 <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.

The snakes that eat caviar

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Banded sea krait, Laticauda colubrina

Marine snakes are fascinating. Entire articles have been written about their morphological and physiological adaptations to marine life, from their lingual salt glands, which are more efficient than kidneys at removing sodium ions from their body, to their rudimentary left lung, which serves a function for the first time in millions of years, aiding in buoyancy control in a manner analogous to the swim bladders of many fishes. There appear to have been three separate invasions of the ocean by terrestrial snakes, all from the family Elapidae, which also includes cobras, mambas, and coral snakes. Although they have spread to east Africa and the south Pacific, all of these invasions have taken place in the shallow seas around Australia and southeast Asia. This is the center of elapid species diversity, so it's no surprise that the greatest ecological diversity is also found here. Among the nearly 70 species of sea snake, however, two genera in particular stand out.

Most marine snakes eat eels and other tropical shore fishes, in accordance with their ancestors' diets of large, bulky prey items that required venom or constriction to subdue. But in 1966, Harold Voris reported that the stomachs of two species of sea snake in the genus Emydocephalus, the turtle-headed sea snakes, were found to contain only fish eggs. This was a remarkable discovery, because most snakes eat prey that are relatively large compared to themselves, and they do so infrequently. It's perhaps one of the evolutionary novelties that has allowed snakes to be so successful. But Emydocephalus eats tiny eggs, and it does so several times an hour, using a foraging mode similar to herbivorous browsing mammals, and to the lizard ancestors of snakes, than to other snakes. Turtle-headed sea snakes use chemoreception to locate the eggs, and the parent fishes are sometimes able to chase them away, despite being far smaller. The parent fishes are never eaten, and indeed they have little to fear, except for their fitness. Why?

There's a reason there was no turtle-headed sea snake character in Finding Nemo

Voris also noticed that the dentition of these snakes was highly unusual, in that they almost completely lack teeth. Most snakes have teeth on up to five of their skull bones on each side: the maxilla, premaxilla, palatine, pterygoid, and dentary. Three of these bones (maxilla, premaxilla, and dentary) also bear teeth in humans and other mammals - the first two in your upper jaw, and the dentary (also called the mandible) in the lower. The palatine and pterygoid teeth of snakes are located on the bones that form the roof of your mouth, and they form what is essentially a second set of upper jaws inside of the first, which can move independently of the outer upper jaws and of each other. In Emydocephalus, only the pterygoid bone has any teeth, except for a single large proteroglyphous fang on each maxilla.

Partial skull of three species of sea snake, looking at the roof of the mouth from below.
Figure modified from McCarthy 1987 

It's clear that a snake that ate only soft fish eggs wouldn't need those teeth, but Voris couldn't figure out how Emydocephalus actually ate fish eggs. He did notice that their stomachs also contained a good bit of sand, and occasionally a copepod (a type of crustacean). In 1987, Colin McCarthy proposed a mechanism that is very similar to that used by most fishes: suction. Based on his observations of the throat musculature of a closely related sea snake, Aipysurus eydouxi, also known to eat fish eggs, he suggested that the two genera of egg-eating sea snakes could create suction by contraction of the geniomucosalis muscle, which originates on the lower jaw and inserts on the oral mucosa (the lining of the mouth). The same mechanism is used by blindsnakes (Scolecophidia), the taxon in which the muscle was described only eight years earlier, to create suction as they feed on ant and termite pupae and larvae.

Graph showing the number of true sea snakes that feed on a variety of prey shapes
From Voris and Voris, 1983

Other modifications of the head aid Emydocephalus and Aipysurus in finding and consuming fish eggs. Most snakes have six to eight labial scales (scales along the lip), whereas Emydocephalus has only three, giving it the appearance of a beak similar to that of a turtle (its genus name means 'turtle-headed' in Greek). McCarthy thought this helped keep the lips rigid during suction feeding. A spine at the tip of the rostral scale might aid in probing the sand for fish eggs buried there, but a secondary sexual function is also likely, because only adult male Emydocephalus have it.

Male Emydocephalus annulatus

In 1996, Michael Guinea published some of the first behavioral observations of wild Emydocephalus from northwestern Australia. While snorkeling, he watched as many as twenty individual E. annulatus interact on a circular coral mass only 25 feet in diameter. Algae grew on them, they moved so little. Mating males touched females with their spines, which might help them synchronize hourly trips to the surface for air and keep track of the female's location as the pair return to the bottom, where Guinea observed pairs mating for over an hour. He also observed E. annulatus using their enlarged labial scales to scrape damselfish eggs off coral, but did not notice any evidence of suction feeding. He suggested that the geniomucosalis muscle was  instead used in rapid exhalation at the surface, and noted that exhalations of Emydocephalus can be heard, whereas those of other sea snakes lacking a geniomucosalis cannot (unlike Emydocephalus, other sea snakes exhale on their way to the surface, leaving a trail of bubbles).

Emydocephalus annulatus courting

You might have immediately associated sea snakes with potent venom, and you're right to do so. It has been suggested that these marine snakes evolved simple, especially fast-acting venoms to immobilize their fish prey, which can escape in three dimensions rather than just two. However, Min Li and colleagues examined the venom of Aipysurus eydouxii and found a mutation that caused a 50- to 100-fold decrease in venom neurotoxicity. They also noted that A. eydouxii has greatly atrophied venom glands and relatively ineffective fangs. In their words, "It is interesting to note that a potent venom was not maintained for use in defense, thus reinforcing that the primary use of snake venom is for prey capture." This is the first case of decelerated evolution of toxins in snake venom, which is usually evolving rapidly, in an "arms race" with the immune system of the prey. Emydocephalus also have reduced fangs and venom glands, but no study of the chemical properties of their venom has been undertaken.

Aipysurus eydouxii

Are there any freshwater snakes that have similar adaptations to  Emydocephalus and Aipysurus? There are plenty that fill similar ecological roles to other sea snakes, eating fishes and crustaceans. There are lots of fishes and amphibians that lay tasty eggs in fresh water, but no freshwater snakes are known to have anything close to the morphological adaptations for oophagy of  Emydocephalus and Aipysurus. There are some terrestrial snakes that eat eggs, such as the neotropical Leptoderia, the African Dasypeltis, and the Australian Brachyurophis, the latter two of which  have lost many of their teeth and are incapable of eating other prey.

Leptodeira annulata eating Agalychnis callidryas eggs 

For more contemporary herp blogging, check out Aaron Reedy's recent post on endangered amphibians, and Tim Mitchell's thoughts on the 25th Anniversary of turtle research in northern Illinois.

ACKNOWLEDGMENTS

Thanks to the Field Museum archive for many of these images, and to Klaus Stiefel and il_mare77.

REFERENCES

Guinea ML (1996) Functions of the cephalic scales of the sea snake Emydocephalus annulatus. Journal of Herpetology 30:126-128

Li M, Fry B, Kini RM (2005) Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). Journal of Molecular Evolution 60:81-89 <link>

Li M, Fry BG, Kini RM (2005) Putting the brakes on snake venom evolution: the unique molecular evolutionary patterns of Aipysurus eydouxii (Marbled sea snake) phospholipase A2 toxins. Molecular Biology and Evolution 22:934-941

McCarthy C (1987) Adaptations of sea snakes that eat fish eggs; with a note on the throat musculature of Aipysurus eydouxi (Gray, 1849). Journal of Natural History 21:1119-1128

Shine R, Bonnet X, Elphick M, Barrott E (2004) A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Functional Ecology 18:16-24 <link>

Voris HK (1966) Fish eggs as the apparent sole food item for a genus of sea snake, Emydocephalus (Krefft). Ecology 47:152-154 <link>

Voris HK, Voris HH (1983) Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioral and ecological relationships. American Zoologist 23:411-425

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

Identifying snake sheds, part II

For a more comprehensive guide to identifying snake sheds in the USA and Canada, see this post.

To view this post in Spanish, click here!
Para ver este blog en español, haga clic aquí!

Not long ago, I posted about some techniques I used to identify a couple of snake sheds that I found in  Florida. I didn't plan a second post, because snake sheds are rarely found intact, but this week in southern Utah I had the opportunity to identify another snake shed, this one in nearly perfect shape. I found it snaked through the grass pointing at the opening of a burrow with an opening about the size of a quarter. Surely the snake had gone down the burrow, which led underneath a rock that was too large to lift (or else I would have!).

Habitat from the area

Despite being relatively fresh, the shed had already dried out, because it was extremely windy where I found it, at the base of a dam at Quail Lake State Park. In extricating it from the grass, I tore it at the midbody, which luckily didn't impair my ability to identify it later on. Importantly, the head was in perfect shape. I cupped it in my hands during the long walk back to the car, to prevent it being torn or blown away by the strong wind. As a result, I didn't get a chance to actually look at it closely for about half an hour, during which time a slew of possibilities ran through my mind as to what it could be. I am new to the southwest, so many of the species here are still unfamiliar to me. Because of what appeared to be a blunt head, as well as the overall small size (about 10 inches in SVL and 11.5 inches in total length), I first thought of a blindsnake, something I have wanted to see for quite some time. If the shed proved to be a blindsnake, I was prepared to recruit some serious help in lifting that rock. However, a glance through my fingers revealed differentiated ventral scales, which are characteristic of advanced snakes. I ruled out Scolecophidia.

Utah Blindsnake, Leptotyphlops humilis

There were many other possibilities, because the southwestern corner of Utah is in the Mojave desert, home to many species of reptiles that are not found in the rest of Utah. Another possibility that crossed my mind was the Southwestern Black-headed Snake, Tantilla hobartsmithi. Like the blindsnake, this species is adapted for burrowing. It is named for esteemed herpetologist Hobart Smith, who was born in 1912 and continues to conduct research and publish papers on reptiles and amphibians today, at age 99, despite having retired twice, in 1968 and 1983. Having published more than 1,600 manuscripts, Smith is the most published herpetologist of all time. He has described 102 species of reptile and amphibian, ranking 13th among all biologists in this regard.

Southwestern Black-headed Snake, Tantilla hobartsmithi

When the shed and I were safely in the car, however, I noticed that the head of my snake shed was not dark. Furthermore, the dorsal scales were boldly patterned with regularly-spaced dark blotches, twenty-eight in all (twenty-six on the body and two on the tail). The tail tip was broken, so I would guess that there were either thirty or thirty-one blotches in total. This was an important clue. The blotches were somewhat reminiscent of a kingsnake, milksnake, or long-nosed snake. However, they were restricted to the dorsal scales, rather than ringing the body as in king and milksnakes, and their edges were very clean, with no pattern in between, unlike the messier blotches of the long-nosed snake. Other options included the nightsnake and the glossy snake, but the blotches of my snake were very dark and regular, whereas these species have smaller, more irregular blotches.

Western Long-nosed Snake, Rhinocheilus lecontei

Finally, I turned to the scales for clues. As always, scale counts provide the most unambiguous evidence, although at this point I had a pretty good idea of what I thought it was. The dorsal scales were smooth and shiny, in 15 rows, and the subcaudal scales were divided, as was the anal plate. The head scales, most important, were somewhat reduced, consistent with a fossorial (burrowing) lifestyle. There were two postocular scales and only a single temporal scale in the first row, followed by two small temporals in the second row that I mistook for undifferentiated occipital scales at first. The upper labials were difficult to count, because the shed had already dried a little, and the snake had probably scraped it off using the labials as a leverage point. The same was true of the lower labials, but only a single pair of chin shields was evident.

Anterior part of the shed

Dorsal, lateral, and ventral views of the head

Rest of the body

After consulting some books to make sure I was right, I concluded that the shed belonged to a Ground Snake, Sonora semiannulata. These small snakes are highly variable in their body coloration and pattern, without consistent within-population variation. Although it is primarily restricted to the Mojave portion of Utah, records from the northeastern and central parts of the state suggest that it might be more widespread. It is found from southwestern Missouri west to southern California, north to Oregon and Idaho, and south to Mexico. Like other members of the tribi Sonorini, Ground Snakes eat mostly arthropods, including insects,  scorpions, spiders, and centipedes. Little is known about the species despite its wide range.

Ground Snake, Sonora semiannulata

It was exciting, almost forensic, to identify the shed of a species I had never seen before. Now I had a debate on my hands about whether to include it on my life list or not (a life list is a compilation of all the species of something - often birds, but in my case herps - that an individual has seen in their life). My friend Kerry Nelson and I have had lengthy discussions about what counts and what doesn't, including whether animals that others find are valid, whether dead animals are valid, and whether or not species seen in dreams (including those that exist only in dreams) are valid. What do you think? Would you count a shed, unambiguously identified, as seeing a species? I decided against it, but I'm very much looking forward to finding a live ground snake so I can add it to the list!

ACKNOWLEDGMENTS

I would like to thank Brian Eager, Matthijs Hollanders, Pierson Hill, and William Flaxington for use of their photographs.

REFERENCES

Cox DT, WW (1995) Snakes of Utah. Bean Life Science Museum, Provo, UT

Ernst CH, Ernst EM (2003) Snakes of the United States and Canada. Smithsonian Institution Press, Washington D.C.

Uetz P (2010) The original descriptions of reptiles. Zootaxa 2334:59-68 <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.