Monday 12 May 2014

Sea Snakes: Raining on the Parade

An interesting story has hit the newspapers in the last month or so. It is the culmination of research over several years on how sea snakes survive at sea. When Jim Linzell and I wrote our monograph on salt glands in 1975 (Salt Glands in Birds and Reptiles) the first part of the story had been completed. Between 1966 and 1971 Bill Dunson and his colleagues established that there is a salt gland in sea snakes and that the gland responsible is the posterior sublingual gland which empties into the tongue sheath. So it was clear then, as it remains clear now, that extra-renal salt excretion is, as in marine birds, used for survival at sea. However, those findings did not mean, as some have taken them to mean, that even the most pelagic sea-snakes can survive entirely without freshwater or that the latter is not either sought out for drinking or preferred to sea water when both are available. There always lurked in the back of the mind the suspicion that the glands were simply not big enough in sea-snakes to cope with a fully marine life, i.e. the ability to drink seawater and then eliminate all the excess salt through the salt glands to obtain osmotically free water.

Yellow-bellied Sea Snake
By Aloaiza
Photograph used by Wikipedia
The species thought most likely to be able to survive without fresh or brackish water was the more pelagic and widely-distributed Pelamis platurus*, the Yellow-bellied Sea Snake. However, the qualms over the truly marine nature, in physiological terms, of this species were never dispelled especially when Dunson and Robinson showed in 1976 that the skin of this species was permeable to water but not to sodium. The outward osmotic flow of water caused a loss in body-weight of 0.4% per day when fasting animals were kept in seawater. So while, the salt gland could account for any salt intake, the snakes were not in water balance; they were slowly dehydrating. Did they somehow return to where they could obtain fresh or estuarine water periodically, was the question. Or was water intake from their fish prey sufficient to balance that loss through the skin?

The question of whether the water losses through the skin could be made up by intake from prey (minus any needs for nitrogenous excretion) has been addressed recently as part of a study of three not nearly so pelagic species of the genus Laticauda that occur around Taiwan. In brief, these snakes could be found in a dehydrated condition in the wild, they would not drink sea or strongly brackish water when dehydrated; they would drink freshwater or weakly brackish water when dehydrated but not hydrated. Calculations suggested that even when feeding, these snakes would gradually be losing water; intake of osmotically free and metabolic water from their prey would be insufficient. Therefore, these snakes seemed to become dehydrated at sea and tolerate that dehydration for weeks and months. The scenario would appear to be that as water is lost osmotically through the skin, and the salt in extracellular fluid retained, they would be able to maintain salt balance by using their salt glands to remove the then excess salt. In other words, volume regulation drifts while ionic balance is maintained—the opposite to the old dogma for vertebrates.

The latest report shows that Pelamis platurus, the most pelagic of all the sea-snakes, becomes dehydrated while in seawater and spends a significant part of its life in a dehydrated state. The snakes do not drink seawater. They must, therefore, obtain freshwater from somewhere. The authors found a relation with rainfall:

Snakes that are captured following prolonged periods without rainfall have lower body water content, lower body condition and increased tendencies to drink fresh water than do snakes that are captured following seasonal periods of high rainfall…individuals may live in a dehydrated state for possibly six to seven months at a time (Lillywhite et al 2014).

The answer to the source of fresh or weakly brackish water should have been obvious earlier. It is the layer of freshwater that lies for a while on the surface of the sea after heavy rain, freshwater being less dense than seawater. Therefore, after rain, sea snakes can drink freshwater as well as breathe when they come to the surface. As far as I can recall, nobody had thought of this transient source of freshwater as a source of drinking water for marine reptiles or birds in any of the early work on salt glands. This explanation can account for the relation between the distribution of pelagic sea snakes and the rainfall pattern, and could account for the local extinction of populations as rainfall patterns change either cyclically or permanently.

While it looks likely that we shall soon have a pretty complete picture of how sea snakes live at sea from the point of view of salt and water balance, many more questions are raised as to what happens during the periods of dehydration. The condition of dehydrated sea snakes appears from the photographs to be awful. Are they still able to feed? Do the digestive organs remain functional? Is blood volume maintained? What are the electrolyte concentrations in plasma during dehydration and rehydration?

So, if sea snakes rely on rain for fresh water, the question arises of whether turtles, in the British sense, i.e. marine chelonians, also drink and need freshwater. There is a difference between drinking fresh water and needing fresh water because almost all birds with a salt gland will drink freshwater if it is available. This is not surprising. Pumping salt against a large concentration gradient needs a great deal of energy and freshwater would relieve that energy expenditure.

The thought crossed my mind a few years ago that birds we typically regard as marine may have access to temporary supplies of fresh water from the surface of the sea after a tropical shower. Twice in the South Pacific I have been in the front of a Zodiac moving slowly from the shore to ship after a heavy downpour. I could see the interface between the sea and freshwater caused by the difference in refractive index (called, I see, the halocline). So I tasted the top of the surface layer to find not a trace of saltiness. That really made me wonder whether some of the petrels that nest on islands like Ducie and Henderson that lack freshwater, for example, could be using the freshwater forming a layer after rain and if they would seek out a storm in order to do so. If that proves to be the case remember that you read it here first!

But if marine birds could have access to transient supplies of fresh water from rain, what about those in the Arctic and Antarctic where fresh water ice melts in the sea during the summer. Were the Chinstrap, Gentoo and Adélie penguins I saw breeding on the Antarctic peninsula getting freshwater from melting glaciers and sea-ice?

Plenty more research to do then, physiological, ecological and at the interface between the two. Knut Schmidt-Nielsen would have been pleased.

Key References

Lillywhite, H.B., Sheehy, C.M., Brischoux, F., Grech, A. 2014. Pelagic sea snakes dehydrate at sea. Proceedings of the Royal Society B 281 20140119.

Lillywhite, H.B., Babonis, L.S., Sheehy, C.M., Tu, M.-C. 2008. Sea snakes (Laticauda spp.) require fresh drinking water: implication for the distribution and persistence of populations. Physiological and Biochemical Zoology 81, 785-796.

Dunson, W.A., Robinson, G.D. 1976. Sea snake skin: Permeable to water but not to sodium. Journal of Comparative Physiology 108, 303-311.

*Somebody noticed that the Pelamis platurus was incorrect in terms of the rules and latin grammar; platur should have had the feminine ending a and not the masculine ending us. So they changed the name to P platura and some authorities have foolishly followed this change. By all means get it right in the beginning but to change a name afterwards by such nitpicking can only lead to confusion and pull taxonomists and taxonomy even lower in the scientific pecking order.