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Tuesday, July 7, 2015

Snakes that decapitate their food

Crab-eating Snake (Fordonia leucobalia) eating a crab
A few years ago I wrote an article about southeast Asian crab-eating snakes, the only snakes (at the time) known to break apart their food instead of swallowing it whole. Although I ended that article by wondering how many more strange snake dietary adaptations we might discover, I didn't actually anticipate writing a sequel to that article—it was so unique that the BBC filmed it for their series Life in Cold Blood, and I doubted that anyone would discover another snake that tore apart its prey. You can imagine my surprise when recently I was asked to review a paper about another snake that breaks its food apart! I was also delighted that this snake was a scolecophidian, because I feel that they are underrepresented both on this blog and in snake biology in general. It is a bit unsatisfying that it is the Brahminy Blindsnake (Indotyphlops braminus, formerly known as Ramphotyphlops braminus), the best studied scolecophidian by far by virtue of its enormous range and unusual breeding habits, but I think this exciting discovery could become extended to some or most of the other >400 species of blindsnakes.

A blindsnake with decapitated termite heads
stuck to the back of its head
Late last year, herpetologist Yosuke Kojima, a postdoctoral researcher at Kyoto University, and entomologist Takafumi Mizuno, a graduate student at Kyoto Institute of Technology, made a chance finding. They had been close friends since elementary school and shared an interest in behavioral and chemical ecology. Together, they planned some experiments to learn more about interactions between blindsnakes and their primary prey, ants. Mizuno's lab also kept colonies of termites (in this case, Reticulitermes speratus), which are also eaten by blindsnakes. Blindsnakes are unusual in that they eat many small prey at a time rather than a few large prey infrequently. Blindsnakes often eat 20 or more prey items at a time, and the maximum number of prey items ingested by a single individual is 1,431 for Anilios (Ramphotyphlops) nigrescens from Australia. Because blindsnakes often gorge themselves when feeding in an ant or termite nest, they often eat very quickly, using a raking technique of the mandibles (in leptotyphlopids) or of the maxillae (in typhlopids). Nate Kley's lab at Stony Brook University has taken some fantastic videos of blindsnake feeding techniques.

Time-sequence of a blindsnake ingesting and decapitating
a termite worker. From Mizuno & Kojima 2015
Supplementary video here
As Mizuno fed termites to the blindsnakes, he observed something very unusual. The blindsnakes typically grabbed and swallowed the termites backwards. Most snakes usually swallow their prey head-first, so this was weird enough. But, it gets weirder. Often, when the snake had maneuvered a termite so that only its head stuck out of the snake's mouth, it would rub its face on the bottom of the tank, decapitating the termite. All of the termite soldiers and about half of the termite workers offered to the blindsnakes were decapitated. Occasionally, a snake would regurgitate a termite that it had consumed whole, decapitate it, and re-consume the body. Decapitated termite heads became attached to the back of the snake’s head or were scattered around the bottom of the cage. The snakes never ate the decapitated heads. There did not appear to be a cost to decapitation—whether a snake decapitated a termite or not, the time required to completely ingest it was about 3 seconds. However, twice blindsnakes were observed swallowing termites head-first, which took only about 1-1.5 seconds. This may not seem like a big difference, but when you're eating hundreds or thousands of prey items in one sitting, it can add up!

Intact termite heads in the feces of a blindsnake
From Mizuno & Kojima 2015
Why do blindsnakes remove the heads of their prey? One reason might be that termite heads contain glands full of toxic chemicals called terpenes. But, unlike predators that remove the skin of various amphibians to avoid the toxins in their skin glands, blindsnakes don't always remove the heads of their prey, suggesting that they aren't that susceptible to terpene poisoning. It's even been suggested that some blindsnakes might be sequestering defensive chemicals from the ants and termites that they eat, just as gartersnakes sequester tetrodotoxin from newts, in which case they might actually prefer the part of the termite with more chemicals. A more likely hypothesis is that the heads are less digestible than the termites' bodies. Between 26 and 100% of the termite heads consumed by blindsnakes in Mizuno & Kojima's experiment remained undigested in the snakes' feces. Additionally, the snakes preferred to eat the worker termites rather than the more heavily-armored soldier termites, and the few soldier termites they did eat were newly-molted. Removing the termites' scleritized heads might allow blindsnakes to pack more soft, squishy bodies into their stomachs, maximizing the nutrition they get out of their meals. It's a bit like you or me peeling a banana or an orange, or removing the husk from a coconut. Since soldier termites have pinching mandibles, removing their heads might also prevent the blindsnakes from being bitten from the inside, which is a bit like you or me...removing the horns of a cow before eating it, if we ate cows alive and whole, I guess?

Evidently the raking maxillae of typhlopids
are sufficiently dexterous to manipulate
prey inside the mouth to position them
for decapitation.
From Kley 2001
Since snakes don't have hands, they've got to remove any indigestible parts using the only maneuverable part they do have—their jaws. Unlike other blindsnakes (which use bilaterally synchronous jaw movements similar to those of all other vertebrates) but like alethinophidians, typhlopid blindsnakes can move the left and right sides of their highly mobile upper jaws independently and asynchronously. Despite its sophistication, the ratcheting movements of their maxillary raking mechanism are insufficient, by themselves, to allow them to decapitate their prey. We must await further functional-morphological studies to assess the role of the toothless lower jaw, which could act as a wedge or blade, in this process. Since snakes cannot really "bite", arthropods, with their jointed limbs and bodies, might be the only type of prey that a snake could pull apart. There are a fair number of snakes that eat arthropods, but most of them are relatively obscure. Besides the crab-eating snakes, one might look for prey-dismembering behavior in sonorines, a tribe of desert-dwelling snakes from southwestern North America, other North American snakes such as the colubrines Tantilla and Opheodrys and the natricine Regina, the dwarf racers of Africa and the Middle East (genus Eirenis), the centipede-snakes of Africa (genus Aparallactus), or certain kukrisnakes (genus Oligodon). In addition to the typhlopid blindsnake in this study, two short notes from the 1950s and 60s document similar decapitation behaviors in two different species of leptotyphlopids (Epictia goudotii [formerly Leptotyphlops phenops] from Central America and Rena dulcis [formerly L. dulcis] from Texas), despite their radically different jaw morphology. I won't be surprised if it turns up in other scolecophidian families as well, since this most-basal group of living snakes probably co-evolved with the early radiation of ants and termites, their favorite prey.

ACKNOWLEDGMENTS

Thanks to Brendan Schembri for the use of his photo, and to Takafumi Mizuno and Yosuke Kojima for giving me the opportunity to write about their discovery in advance of its publication and for translating it into Japanese.

REFERENCES

Kley, N.J. 2001. Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. American Zoologist 41:1321-1337 <link>

Mizuno, T. and Y. Kojima. In press. A blindsnake that decapitates its termite prey. Journal of Zoology 10.1111/jzo.12268 <link>

Prestwich, G.D., B. Bierl, E. Devilbiss, and M. Chaudhury. 1977. Soldier frontal glands of the termite Macrotermes subhyalinus: Morphology, chemical composition, and use in defense. Journal of Chemical Ecology 3:579-590 <link>

Reid, J.R. and T.E. Lott. 1963. Feeding of Leptotyphlops dulcis dulcis (Baird and Girard). Herpetologica 19:141-142  <link>

Savitzky, A.H., A. Mori, D.A. Hutchinson, R.A. Saporito, G.M. Burghardt, H.B. Lillywhite, and J. Meinwald. 2012. Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22:141-158 <link>

Shine, R. and J.K. Webb. 1990. Natural history of Australian typhlopid snakes. Journal of Herpetology 24:357-363 <link>

Smith, H.M. 1957. Curious feeding habit of a blind snake, Leptotyphlops. Herpetologica 13:102 <link>

Stokes, A.N., A.M. Ray, M.W. Buktenica, B.G. Gall, E. Paulson, D. Paulson, S.S. French, E.D.B. III, and J. E.D. Brodie. 2015. Otter predation on Taricha granulosa and variation in tetrodotoxin levels with elevation. Northwestern Naturalist 96:13-21 <link>

Vidal, N., J. Marin, M. Morini, S. Donnellan, W.R. Branch, R. Thomas, M. Vences, A. Wynn, C. Cruaud, and S.B. Hedges. 2010. Blindsnake evolutionary tree reveals long history on Gondwana. Biology Letters 6:558-561 <link>

Creative Commons License

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

11 comments:

Hari said...

This is amazing! In my teens, I used to keep a colony of these snakes, among others. Fed them on termites but never really noticed this. It was hard to watch them feed as they would burrow down into the soil as soon as I switched on the lights.

Andrew Durso said...

Thanks Hari, I agree! What we don't know about blindsnakes could fill a bookshelf.

Eric Vanderduys said...

Hi Andrew,
Thanks for writing about this feeding behaviour. I was unaware of it despite having kept I. braminus for a number of years, and watching them feed very closely on numerous occasions. I never fed mine termites though, only the eggs and pupae of a couple of species of ants, mostly the introduced Paratrechina longicornis, and another species whose name escapes me. Availability dictated this food choice. I remember trying them on termites, but they never seemed interested (though they may have consumed them when I wasn't looking). The snakes are introduced here, and after reading this I think I will give our Australian termites a go again. Similarly, if I can get the right permits, I might try with a native blind snake or two.
All the best, Eric

Andrew Durso said...

Thanks Eric. I suspect they wouldn't do this behavior when feeding on eggs and pupae. Let me know what you observe!

Timothy Gould said...

Hello Andrew,

You may find two things interesting from my personal experience:

1) My first snake ever, an 0.0.1 Opheodrys aestivus acquired on 21 November 1991, only ate one (1) cricket in my care - a freshly shed, thus powder white, large cricket. Wouldn't take caterpillars, ants, spiders, moths, fireflies, et cetera...one meal, and it died in maybe January or February.

2) The more interesting bit, is about an 0.0.1 Chionactis occipitalis occipitalis I had in 1992-93. Not even able to see its nose, it would lunge out from the sand unsuspectingly to grab its crickets, and ate everything BUT the heads! Even more interesting is the contrast to my 0.0.1 C. o. occipitalis in 2014-15 (<2 years ago), which came out of the sand to chase crickets, and it ate everything including the head.

Aside from Opheodrys spp. and Chionactis o. occipitalis, other insectivores I've kept are Tantilla nigriceps, Gyalopion canum, and Sonora semiannulata - all of which I fed Texas Gold Scorpions (Vaejovis sp.) and spiders to (I bought the Vaejovis in bulk at $1.25/ea from Regal Reptiles over 10 ten years ago, who were arachnid specialists), and everything was consumed whole. Interestingly, all of those species would do great for a few months, then suddenly cease feeding and shortly die thereafter...?! Nothing changed in the terrariums nor the snake room. Some species just don't live long-term, I guess, like many saltwater fish such as Powder Blue Tangs: they do great for maybe nine (9) months, then keel over.

Anyway; great article! I may have to add these guys to my 'wish list', right along Fordonia leucobalia and Gerarda prevostiana from three (3) years ago! :)

Sincerely,
Timothy

Andrew Durso said...

Thanks again for the informative comment Tim! It certainly doesn't help that many of the insectivorous snakes about which we'd like to learn more don't do well in captivity. Keeping certain reptiles (and fish) in captivity is definitely a labor of love. And, re: your Chionactis observations (and those of others on I. braminus, above), I think it highlights the fact that one size does not fit all—there will always be individual and other variation within a species, the raw material of natural selection. Thanks for reading!

Timothy Gould said...

Welcome, Andrew! Indeed; it can be discouraging, but We must keep at it with discipline and dedication if We are to unlock the mysteries, and passion and love is what drives perseverance. Regarding Chionactis and Indotyphlops braminus, "one size does not fit all" just emphasizes the individuality of some specimens. :) Analogically, it's similar to a species having a general disposition/demeanor, say, more feisty, but then the occasional--even wild--specimen being relaxed, such as my adult male Naja pallida which was imported from Arusha, Tanzania, in January 2015...since acquisition on 13 September 2015, he has never spit or even hooded, eats well and is normally active (not skittish like my female which also doesn't spit or hood), and rides hooks like a champ. Welcome, I always enjoy this blog! :)

Andrew Durso said...

The "personalities" (if you will) of snakes have always intrigued me, both within a species and among species.

Timothy Gould said...

Agreed. Just like humans (hence: personalities), I love seeing the diversity on different levels.

Bk Jeong said...

I would also look at the extinct palaeophiids as possible prey dismemberers.

Andrew Durso said...

@Bk Jeong: very interesting, thank you for this tip!