APRIL 1995

Burt Jones/Maurine Shim lock

OceanReabnINTERNATIONAL MAGAZINE OF THE SEA

FEATURES

Tragety In The Gulfby Laura Brown and Chrisjaffe 34

Above Caymanby Harvey Lloyd 41

Sea Snakes

by Robin Milton Love 48

Commuting On The Tropical Tides:The Life Of The Yellow-Lipped Sea Krait 42

by Harold K. and Helen H. Voris 57

Heat Run

by Phillip Colla 62

Portfolio

by Ron and Valerie Taylor 71

DEPARTMENTS

Marine Watch 7

Sea Salt 17

Marine Life 19

Essay 23Freeze Frame 28

Photo Realm 86

Soundings 91

Updates 94

Parting Shot 96

COVERPhotograph by Ron &Valerie Taylor

Territorial dispute between tWo harlequin tuskfish, LienardellafasciatusGreat Barrier Reef, Australia

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"

hree to six feet long with a striking pattern ofblack and white banding, a yellow-lipped seakrait slips out of the warm, tropical waters ofthe South China Sea and makes itsway acrossa jumble of boulders and through the thick

layer of coral debris on its tiny island home in MalaysianBorneo-Pulau Kalampunian Damit. Although related tothe forty-five species of true sea snakes which are fullyaquatic, the five species of sea kraits are amphibious,commuting between land and sea. True sea snakes haveleft behind all traces of their life on land except for theirneed to return to the surface to breathe air. The sea kraits,on the other hand, have partitioned their major lifefunctions between the two environments and havecertain adaptations to each.

Over a three-year period starting in 1986,University ofMalaysiaProfessor Rob Stuebing, graduate studentEngkamat Ak.Lading,and I (HKV)investigated how theyellow-lipped sea krait,Laticauda colubrina, divides itslifebetween aquatic and terrestrial worlds. Our tropical is-land roughly in the center of the species' range seemed anexcellent place to look at sea krait life in the year-roundheat of the equator and compare itwith what was knownof the species in more seasonal regions. We also wantedto see ifwhat we learned about the sea krait's way oflifecould help us understand the advantages, disadvantages,and trade-offs of itscommuter lifestyle. Much remains amystery, but our fieldwork as well as ecological studies byH. SaintGirons in New Caledonia, and byJ. c. Pernettaand M.1.Guinea in Fiji,provide tantalizing clues to under-standing what we have observed.

Sea snakes and the biological problems they presenthave interested us for nearly thirty years. In 1975we livedfor ten months in a small Malayvillage located at themouth of the Muar Riverwhere it empties into the StraitsofMalacca between the MalayPeninsula and Sumatra.There we studied a number of species of true sea snakesand devised marking techniques for studying their popu-lation size. Unexpectedly, we came upon an annualbreeding cycle which allowed us to study hundreds ofjuvenile sea snakes for the first time and to observe theirfeeding behavior and dietary preferences. At that timewe also came upon our first colony of yellow-lipped seakraits. That preliminary work led to the present studywhich we began by following leads from local fishermen.They told us about a place they called "Snake Island."Kalampunian Damit is a small rocky island about the sizeof a football field, lying about fiftykilometers southwestof Kota Kinabalu, capital of the Malaysian state of Sabah(formerly called North Borneo). The island is locatedwithin Pulau Tiga Park of the Sabah park system, and wearranged with park rangers to visit it.

As our open Boston whaler sped across the two-milestretch of sea between the ranger station on Pulau Tigaand our island, we were grateful for the cooling breeze

which provided temporary relief from the burningequatorial sun overhead. Upon reaching the leewardside of the island we threw out the anchor about twentymeters offshore in thick coral rubble and continuedtoward the island with the motor running. Although thiswas the island's better side for landing, itwas not for ama-teurs. About ten meters offshore, one of the rangersjumped into the water and swam to the rocky shore witha tow rope, which he tied to a tree. Thus tetheredbetween two points, the boat was prevented fromcrashing into the boulders along the edge of the island.With our gear in plastic bags carried over our heads, wetoo jumped in the water, waded ashore, and scrambledover the slippery, algae-covered, jagged boulders to findour way about. Itwas a process we repeated many timeson subsequent visits to the island. Leaving behind thecool breeze of the moving boat, we instantly felt theintense heat of the tropical sun bearing down on us.Later measurements told us that in exposed areas thetemperature reaches a sizzling 115degrees Fahrenheit.

Five to fifteen meters beyond the rocky shoreline, astand of deciduous trees covered the island with a thick,dark canopy up to twenty meters high. During theannual dry season, late January to April, theysynchronously shed their leaves. The absence of any leafcover makes this the hottest period of all. The resultantleaf litter which accumulates here and there in rockydepressions creates small oases of relative coolness inwhich we sometimes found a few sea kraits resting.

By eight in the morning the intense heat had forcedvirtually all snakes to seek shelter. Exploring rock byrock and tree by tree, we confirmed what the fishermenhad said: In a matter of a few hours we found over ahundred sea kraits distributed in a ring around the islandunder or between rocks, generally above the high tidemark. We also found some under logs or roots, and evena few up in trees or in nest holes excavated in large treeson the island hilltop by the common kingfisher.

As snakes

go, these kraits are not huge. The largest females growup to six feet in length and weigh two or three pounds,about the size and thickness of a broomhandle. We wereable to distinguish males and females quite easily sincemales are as much as a third shorter and half the mass ofthe females; also, the paddle tails of the males are swollenat the base where the sex organs are located. Althoughwe knew from previous work that we could distinguishjuvenile sea kraits from adults on the basis of their size,we found no juvenile sea kraits on Kalampunian Damit.

We were excited by the abundance of sea kraits on theisland and the feasibility of studying them. First wewanted to find out the size of the sea krait populationusing the island, using the mark and recapture method

58 Ocean Realm

,

in which as many individuals as possible are caught,marked, and then released back into the generalpopulation. To mark the sea kraits we used a small T-shaped plastic anchor tag, identical to those used in the re-tail clothing business, except that our snake tags were indi-vidually numbered. We inserted the anchor of each tag justunder the skin on the flank of the sea krait, using theneedle point of a tagging gun. One person held the snake'shead, another the tail,and a third attached the tag.We alsomeasured each snake, took its cloacal temperature, andpalpitated itsstomach to determine if ithad eaten recently.

Eventually we tagged forty-fivesnakes on our islandover five months, and we estimated the total populationsize to be 600 to 800 snakes. SaintGirons, working in NewCaledonia, marked about 100sea kraits and obtainedroughly similar population estimates. We surveyednumerous other islands within fiftykilometers along thecoast of the mainland and determined that six also hostedthe yellow-lipped sea krait, yet never did we turn up one ofour marked snakes on those islands. These observationssuggest to us that localized populations exhibit some hom-ing behavior with respect to individual islands.

The motivation for entering the sea is food. Once inthe water, sea kraits swim along the bottom, following it todeeper sandy areas where they continue to cruise aroundcoral reefs, poking their heads into nooks, crannies, andburrows in search of eels. Foraging trips last a few days toa few weeks, perhaps as long as a month and a half. Seakraits surface to breathe as frequently as every fewminutes, but may stay submerged as long as an hour ormore. When they need air, they swim almost straightupward; they stay at the surface only a few seconds andthen immediately dive straight back down.

Yellow-lipped sea kraits feed almost exclusively oneels, which are ideal prey since they are packaged in aform which neatly matches that of the snakes. Asingle eelcan filla sea krait to capacity. While we found one seakrait that had eaten an eel over half its own body weight,most sea kraits take eels that are between 20 and 40percent of their own length.

When a sea krait detects an eel in a crevice or burrow, itdelivers a bite, shooting a highly neurotoxic venomthrough its anterior fixed fangs (similar to cobras, whichhas been the basis of the theory that sea kraits and cobrasshare common ancestry). The venom shuts off the eel'srespiratory muscles, paralyzing it in three to ten minutes.Subsequently, the snakes swallow their dead orimmobilized prey head first.

We saw related feeding behaviors in our 1975study ofthe beaked sea snake which eats catfishand puff fish. Thesnakes would wait until the venom took effect-an averageof about fiveminutes for catfish and eleven minutes forpuffers-before attempting to swallow their prey. Puffersusually inflated themselves before the venom had a chanceto act, so the snake looked like a small tether attached to aping pong ball, and it seemed impossible that the snakewould ever be able to swallow the puffer. Yetgradually itwould position the fishhead first,and then amazingly beginto creep its jaws bit by bit over the puffer's body. From thetime the fish's head entered the snake's mouth until itstaildisappeared took anywhere from fifteen seconds to threeminutes for a catfish,and thirtyseconds to seven minutes forpuffers. Immediately afterwards, the snakes would alternatebursts of rapid swimming and knotting about themselvesto move the prey down their bodies into their stomachs.

While both male and female yellow-lipped sea kraitsspecialize in eating eels, they tend to dine on differentspecies. In Fiji,Pernetta found that males ate smallerspecies of eels which were found on inshore reef flats,while females took larger eel species found in deeperwaters adjacent to reefs. Females seem to forage bothfarther (to the outer ranges of reefs rather than inshoreareas) and longer (not spending as much time on land asthe males do), taking larger species of eels to support theirlarger size and reproduction needs. The net effect ofthese differences is that males and females effectivelydivvy up the available resources-eating different speciesof eels from different habitats-rather than competing forthe same ones. At the same time, this strategy increasesthe resources available to the species as a whole.

Sea kraits come on shore to digest their food.Whenever we returned snakes to the water after takingtheir temperatures or tagging them, those with evidenceof food in their stomachs almost invariably moved ashoreagain immediately.

They alsoreturn to land to lay leathery eggs which resemble thoseof terrestrial kraits. By contrast, the true sea snakes bearlive young at sea and have no need to return to land at all.They have evolved a flattened body shape with tiny bellyscales or a distinct ventral keel which makes locomotionvery efficient in water but almost impossible on land.However, both true sea snakes and sea kraits haveflattened paddle-like tails which increase their propulsivethrust in water.

We found that the amount of clumping amongsea kraits varies during the year, but no matter how largethe group, males almost always outnumbered the females

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at least four to one, and never were there more than threefemales per group. We have no reason to think that thesexes begin life in unequal numbers-a one-to-one ratiois typical for snakes, and on islands where we observedjuvenile yellow-lipped sea kraits, males and females werepresent in balanced numbers. Given what we knowabout the feeding habits of the two sexes, we think thatthe unequal sex ratio among the adults on our island wasmost likely due to the females foraging farther in deeperwaters and spending more time at sea.

Observing sea kraits day and night, we were able todiscover more pieces of the story. Atnight, when it wascooler, we saw numerous single males crawling amongthe rocks, draped over boulders, and lying at the water'sedge. Whenever a female emerged from the water, oneor more males immediately began tracking along afterher, tongue-flicking to detect and follow her scent. InFiji,Guinea also observed this "tactile-chase," the firstphaseof snake courtship. He commented that the males wereso intent on following the scent of females that theyignored his presence-even when he disturbed and inter-rupted them-and continued their single-minded trekover any item the female contacted.

By morning the females and their entourages of maleshad holed up under rocks, where courtship continued.Malesnakes lying adjacent to females would contract theirbodies in undulating spasms lasting a second or two. Afteran intervening pause of several seconds, another pulsewould occur in a rhythmic pattern of ten to twenty pulsesper minute. Sometimes only one male in a group woulddisplay this behavior; sometimes more. It often went onfor several hours. "Chin-rubbing," in which male snakesrub their mouths and lower jaws against a female's headand side, also takes place prior to copulation. The femalesseemed to pay as little attention to the males duringcourtship as the males did to external distractions.

When the female finished digesting and returned tothe sea during the intense heat of the daytime, the malesdid not follow. Females emerging from the sea during thedaytime usually crawled directly under rocks; no snakeparades occurred. Likeother cold-blooded reptiles, thesea kraits have no internal mechanisms for temperaturecontrol, and so they must avoid extremes of temperaturein order to maintain their ability to function. We decidedto look into this further, firstby finding out the range oftemperatures to which the sea kraits were exposed on theisland. To do so we made snake models out of copperthroughout the island: underwater in the intertidal zone,on exposed sand, on leaf litter, in a tree hole, on top of aboulder, beneath rocks, and inside a large ball of snakes.We placed a tiny thermistor inside each snake model and

connected the thermistors to a central station whichrecorded the temperature at each site every thirty minutesover a day and a night. As might be expected, the mostprotected area (under a rock) registered the coolesttemperatures (eighty-one to eighty-five degreesFahrenheit), and the exposed sand beach, the hottest(eighty-two to 115degrees Fahrenheit). No wonder wefound the snakes located under rocks during the daytimeand moving about only after dark!

To find out what was happening to the snakes' internaltemperatures during all of this, we took the cloacaltemperature of each snake we found during our snakesurvey and noted the snake's exact location. We also feda number of snakes miniature radio transmitters whichbroadcast information on their internal temperatures.

Itwas not by accident that we often noticed small portionsof the sea kraits' bodies sticking out from under rocksduring the daytime: Our data revealed that the snakeswere fine-tuning their body temperatures a few degreesupward to their preferred level by deliberately exposingjust a small section of their bodies to the heat of the sun.InNew Caledonia, which is more seasonal, the snakesmust sun themselves fully during winter days, as SaintGirons observed, in order to raise their body temperaturessufficiently to move about. There they hole up at nightwhen it is too cool for them to be active.

Although we observed courtship behavior frequentlyon our island, we did not find any eggs. In thePhilippines, close relatives of the yellow-lipped sea kraitare known to lay their eggs in communal intertidalgrottoes. Underground cavities on Kalampunian Damitwhich would offer the same protected, watery, humidconditions were unfortunately too small and inaccessiblefor us to explore, but it's possible that when we are ableto do so, our egg hunt will end right beneath our feet.

From numerous studies on preserved sea kraits (ourown as well as others), we know that females prQducefour to nineteen eggs per clutch. Sea krait egg productionseems to be seasonal in the more temperate areas of thesnake's range; however, we have found no such evidenceof seasonality among sea kraits at the equator.

Norway rats, accidentally introduced by visiting boats,now thrive on Kalampunian Damit, and we would not besurprised if they ate sea krait eggs, but as yet we have nodirect evidence of this.

We

have seen white-breasted sea eagles carrying sea kraitsand have come upon their partially devoured carcassesseveral times. InFiji,Guinea described how one

60 Ocean Realm

afternoon he came upon a crab eating a juvenile yellow-lipped sea krait. He first noticed the snake thrashing aboutin a tidal pool, then he saw the crab had the snake by its tailand had eaten some flesh along the backbone. Guineafreed the snake and set it at the side of the pool tophotograph it, but the crab came right back after it andpulled it into deeper water where it continued to eat.

Although sea kraits-particularly juveniles-may wellhave other predators, living on small islands clearlyminimizes possible exposure to them. There is a diversityof potential mammalian and reptilian predators on themainland (weasels, civets, crocodiles, and water monitors

among others), but as islands get small and further from themainland, the number of predators on them decreases.

Islands offer another advantage: In a vast sea, theyprovide natural geographic centers for sea kraits toencounter one another reliably, as they must to mate andreproduce. The seas are a medium of dispersal, particularlywhen the sexes forage over different ranges. We know thatsea kraits are very persistent about their attraction toislands: Never have we or other researchers found sea

kraits living on mainland coasts even when the coastalareas were very near islands with populations of sea kraitsand the habitats were virtually identical. But how do seakraits make sure that they are hauling out on an islandinstead of the mainland? This is a crucial distinction if theywish to reduce predation on their young.

Homing behavior obviously answers boththese questions, and indeed both we and Saint Gironshave evidence that the yellow-lipped sea kraits seemto practice homing.

A compelling reason to return to land, such as the needto reproduce, mandates that the sea kraits also retainphysical features such as broad belly scales thatenable them to locomote on land. The snakes have also

retained waxier, larger body scales, like those of their terres-trial ancestors, adapted to crawling around rough surfaces.The completely aquatic true sea snakes on the other hand,have softer, smaller scales, and well-vascularized skin whichallows them to carry on some cutaneous respiration-obtain-ing oxygen through their skin. Sea kraits, with no suchability to take in oxygen through their skins, must return tothe surface for all the air they need. Movement to and fromthe surface is a labor in each direction: Diving downwardthe snakes must work against the buoyancy of their fresWyoxygenated lungs; as oxygen is used up and carbon dioxidepassed out of their system when they are submerged, theylose their buoyancy and must work to return to the surface.Furthermore, retaining a body form and scalation that allowfor terrestrial locomotion necessarily limits the degree ofstreamlining the kraits can attain for efficient

locomotion in water. Again, in contrast, the true seasnakes are much more laterally compressed with verysmall belly scales or even a sharp ventral keel. Perhapsthis explains why sea kraits come up on land to rest anddigest, even though the equatorial seas usually measureeighty-four to eighty-six degrees, their preferred bodytemperature. It simply takes less energy to hole up undera rock than to swim up and down in the sea, no matterhow congenial the temperature.

Are the amphibious sea kraits on the way to a moreaquatic way of life? Does what we know about theiramphibious lifestyletell us anything about how the truesea snakes may have made their transition from aterrestrial to a completely aquatic existence?

Both groupsof snakes have re-entered the sea to exploit its generousproductivity as a food resource, and both groups haveevolved certain physical characteristics adapted tofunctioning in the water, notably paddle tails and dorsalnostrils which allow the snakes to obtain air at thesurface without lifting their heads out of the water.But there the similarity ends.

While the true sea snakes conduct almost all of theirlife functions in the sea, except for continuing tobreathe air at the surface (and even that they aremodifying through the evolution of cutaneousrespiration), the sea kraits conduct almost all of theirlife functions (except for foraging for food) in aterrestrial environment. A key to understanding thesedifferences may lie in the origins oftheir distinctmodes of reproduction.

Virtually all work on marine snake evolutionsuggests that the true sea snakes evolved fromAustralian elapid snakes, while the sea kraits appear tohave evolved from the kraits of southern Asia.Most

elapids bear their young alive, while all kraits lay eggson land. For the true sea snakes the ability to bear liveyoung right from the beginning eliminated the need toreturn to land to reproduce and thus a major reason forneeding to locomote on land. It paved the way for com-plete adaptation to an aquatic environment. The seakraits, however, having inherited the laying of leatheryeggs from their terrestrial ancestors, remain compelledto return to land to reproduce, and consequently theymust also retain the ability to locomote on land.

This ability is necessarily intertwined with a numberof compromises and trade-offs in morphology, function,and behavior. And these compromises allow the yellow-lipped sea krait to live in two very different ecologicalzones, and to commute between them regularly on thetropical tides. 0

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