Tuesday, May 22, 2012

The snakes that eat caviar



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 

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

3 comments:

Colin McCarthy said...

Congratulations on a masterful summary of a fascinating topic. I'm Colin McCarthy whose 1987 paper you cite above (and who you recently kindly accepted as a FB friend). Just to clarify, I don't think the feeding mechanism had been observed at the time I wrote my paper so I proposed testable theories based on morphology. Guinea's observation of the lip scales in Emydocephalus being used to scrape fish eggs had not entered my imagination although I did state that such scales would "impart greater ridgidity". Additionally, although the proposed 'suction' mechanism has not yet been observed, I suggest it remains a likely possibility. I think it might explain why large quantities of sand are sometimes ingested at the same time as the eggs and may also account for the fact Aipysurus eydouxii can feed on fish eggs without having the lip scale consolidation found in Emydocephalus.
With best regards
Colin

Andrew Durso said...

Colin,

Thanks very much for the thoughtful comment and clarification. I'm so glad you enjoyed the article! This one was one of my favorites to write - I'm actually planning several more sea snake articles, since there is so much to write about!

AMD

Colin McCarthy said...

That's great Andrew, really looking forward to them.
All the best
Colin