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Predation by a Yellow‐lipped Sea Krait, Laticauda colubrina (Schneider 1799), on a Moray Eel (Gymnothorax sp.) at Balayan Bay, Philippines

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Sevilla, A., Zdunek, P. 2023. Predation by a Yellow‐lipped Sea Krait, Laticauda colubrina (Schneider 1799), on a Moray Eel (Gymnothorax sp.) at Balayan Bay, Philippines. Southeast Asia Vertebrate Records 2023: 013‐014.
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13
SEAVR2023:013014
ISSN:24248525
Dateofpublication:03May2023
Hostedonlinebyecologyasia.com
PredationbyaYellowlippedSeaKrait,Laticaudacolubrina(Schneider1799),
onaMorayEel(Gymnothoraxsp.)atBalayanBay,Philippines
ArnelSEVILLA&PrzemysławZDUNEK
arnel@portulano.com(Sevilla),zdunek.komodo@gmail.com(Zdunek)
Observer:ArnelSevilla.
Photographsby:ArnelSevilla.
Subjectsidentifiedby:PrzemysławZdunek.
Location:BalayanBay,Batangas,LuzonIsland,Philippines(13.82017°N,120.90144°E;WGS84).
Elevation:Approx.15metresbelowsealevel.
Habitat:Dominatedbysoftandfancorals.
Dateandtime:08January2023,aroundnoon.
Identityofsubjects:
(i)YellowlippedSeaKrait,Laticaudacolubrina(Reptilia:Squamata:Elapidae)
(ii)MorayEel,Gymnothoraxsp.(Actinopterygii:Anguilliformes:Muraenidae).
Fig.1.Gymnothora
x
sp.spottedandbeingengulfedbyanadultLaticaudacolubrina. ©ArnelSevilla
14
Descriptionofrecord:
DuringadivetouratThePinnacledivesite,BalayanBay,anadult(estimatedtotallength~120cm)Yellowlipped
SeaKrait(Laticaudacolubrina)wasobservedforagingincrevicesatadepthofabout15meters.Thewater
temperaturewas26°Cwithastrongcurrent.Afterawhile,thesnakenoticedaneel’shead(Gymnothoraxsp.)
protrudingfromacrevice.Thesnakebititsprey,holdingitbyitsheaduntilitstoppedstruggling(Fig.1).Duetothe
strongcurrent,theactofswallowingthepreywasnotphotographed.
Remarks:
Thebandedpatterning,anddistinctiveyellowupperlipandsnoutclearlyidentifythissnakeastheYellowlipped
SeaKrait(Laticaudacolubrina,Schneider1799)(Das2021).Theeelisidentifiedasamorayeelofthegenus
Gymnothoraxbasedonlocation,jawshape,eyecolor,andgeneralcoloration(Allenetal.2015).
Laticaudacolubrinaisawidelydistributed,semiaquaticvenomoussnake(Das2021).Ithasaneelspecialistdiet,
althoughtheyareknowntoalsopreyuponothersmallfishspecies(Tanetal.2017).Observationsofthistypeare
knownfromotherareasofoccurrenceofthisspecies(Heatwoleetal.2005;Bonnetetal.2010)byexaminingthe
contentsofthestomach(Herre1942).ShettyandShine(2002)documentedsomesexualdivergenceintermsof
dietaryhabitswithfemales,whicharelarger,primarilypreyinguponcongereels(Congerspp.),andmales,which
aresmaller,onmorayeels(Gymnothoraxspp.).
Tothebestofourknowledge,oursisthefirstdocumenteddirectobservationofpredationbyL.colubrinaon
Gymnothoraxsp.atBalayanBay,Philippines(HerreandRabor,1949).Evenasasingleevent,thisrecordbroadens
thescopeofinformationaboutthenaturalhistoryandecologyofseakraitsandtheirprey.
References:
Allen,G.,Steene,R.,Humann,P.,DeLoach,N.(2015).Reeffishidentification:TropicalPacific.2ndedition.New
WorldPublications,Jacksonville,Florida,USA.502pp.
Bonnet,X.,Brischoux,F.,Lang,R.(2010).Highlyvenomousseakraitsmustfighttogettheirprey.CoralReefs29:
379.
Das,I.(2021).SnakesofSoutheastAsia.3rdedition.JohnBeaufoyPublishing,Oxford.176pp.
Heatwole,H.,Busack,S.,Cogger,H.(2005).GeographicvariationinseakraitsoftheLaticaudacolubrinacomplex
(Serpentes:Elapidae:Hydrophiinae:Laticaudini).HerpetologicalMonographs19(1):1–136.
Herre,A.W.C.T.(1942).NotesonPhilippineSeaSnakes.Copeia1:79.
Herre,A.W.C.T.&Rabor,D.S.(1949).NotesonPhilippineSeaSnakesoftheGenusLaticauda.Copeia4:282284
Shetty,S.,&Shine,R.(2002).SexualdivergenceindietsandmorphologyinFijianseasnakesLaticaudacolubrina
(Laticaudinae).AustralEcology27(1):7784.
Tan,C.H.,Wong,K.Y.,Tan,K.Y.,Tan,N.H.(2017).Venomproteomeoftheyellowlippedseakrait,Laticauda
colubrinafromBali:Insightsintosubvenomicdiversity,venomantigenicityandcrossneutralizationbyantivenom.
JournalofProteomics166:48–58.
ResearchGate has not been able to resolve any citations for this publication.
Article
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The Laticauda colubrina complex previously consisted of three species, Laticauda saintgironsi from New Caledonia and the Loyalty Islands, Laticauda frontalis from Vanuatu, and Laticauda colubrina, a widespread species ranging from the Andaman and Nicobar Islands and the Myanmar-Thai-Malaysian peninsula, through the Indonesian archipelago to New Guinea, north to Palau, the Philippines, Taiwan and the Ryukyu Islands, and southeastward along the island-chain of the Solomon Islands, Vanuatu, Fiji and Tonga. Their geographic variation, based on 1515 specimens involving 33 characters of coloration and scutellation, was analyzed in two different ways: (1) an hierarchical analysis and (2) an analysis of principal components and discriminant function. Sexual dimorphism occurred in many characters and for those, females and males were analyzed separately. The results confirmed the distinctiveness of the three original species. Within L. colubrina different characters displayed slightly different geographic patterns of variation, but overall five general groupings of populations could be discerned: (1) a north-south axis from Sabah, north through the Philippines to Taiwan and the Ryukyus, (2) an east-west axis encompassing localities from the Andaman and Nicobar Islands in the west through New Guinea and the Solomon Islands in the east, (3) the eastern islands of Vanuatu, Fiji, and Tonga, (4) a partially isolated population in Palau, and finally (5) an isolate in southern Papua. Despite significant differences among these regions, different characters showed slightly different patterns of geographic variation across their boundaries; similarly, within each axis the pattern of variation among islands differed for different characters. Divergence was deemed sufficiently consistent to warrant taxonomic distinction only in the case of the population in southern Papua that was accorded recognition as a new species, Laticauda guineai. In some characters, widely peripheral populations were more similar morphologically to each other than to more central ones, and alternative hypotheses accounting for this are discussed. The observed distribution and the geographic patterns of variation are attributable to a combination of present and past ecological restrictions, directions of sea currents, and paleogeography.
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A long-term recapture study in New Caledonia has shown sea kraits (Laticauda laticaudata and L. saintgironsi) have a strong predator prey relationship with anguilliform fish (Brischoux et al. 2007; Ineich et al. 2007). Considering krait versus prey body size (sometimes almost of the same size), many conger eels (e.g., Conger cinereus) and moray eels captured by the sea kraits have the potential to retaliate. We observed typical ‘‘V-shaped'' injuries on many snakes: 29.7% L. laticaudata had scars and 11.4% recent injuries (N = 2,797 individually marked snakes); 33.2% L. saintgironsi had scars and 9.5% recent injuries (N = 3,582). Deep cuts sometimes resulted in very large and deep wounds (N > 100). Because anguilliform fish are indeed capable of inflicting dangerous bites, the trophic relationships between these two predators are more complex than assumed: the benefit of maximising the amount of energy per foraging trip associated with the capture of large prey trades off against the injury risk that increases with prey size. Prey selection, searching effort, killing tactics, and venom efficiency selection can all be affected. Figure 1a (20 m depth, island of Taveuni, Fiji, November 2004) clearly illustrates the ability of moray eels to bite sea kraits (see Fig. 1b) during predation as a defence mechanism. We regularly observed sea kraits with recent deep ‘‘V-shaped'' bites coming on shore without prey in the stomach, possibly to rest and recover (Fig. 1c). Perhaps capturing fish is more difficult than previously assumed, even for the highly venomous sea kraits.
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Biological significance: Laticauda colubrina (yellow-lipped sea krait) is a widely distributed, semi-aquatic venomous snake species. The venom proteome at the level of protein family is unsophisticated and consistent with its restricted prey selection. Nonetheless, the subproteomic findings revealed geographical variability of the venom for this widely distributed species. In contrast to two previous reports, the results for the Balinese L. colubrina venom showed that LNTX Neurotoxin a and Neurotoxin b were co-existent while the PLA2 lethal subtype (PLA-II) was undetected by means of LCMS/MS and by in vivo assay. This is an observable trait of L. colubrina considered divergent from specimens previously studied for the Philippines and the Solomon Islands. The stark geographical variation might be reflective of trophic adaptation following evolutionary arms race between the snake and the prey (eels) in different localities. The preferred trait would likely propagate and remain significant within the geographical population, since the strong behaviour of site fidelity in the species would have minimized gene flow between distant populations. Meanwhile, the in vivo neutralization study verified that the efficacy of the heterologous Sea Snake Antivenom (Australian product) is attributable to the cross-neutralization of SNTX and LNTX, two principal lethal toxins that made up the bulk of L. colubrina venom proteins. The findings also implied that L. colubrina, though could be evolutionarily more related to the terrestrial elapids, has evolved a much streamlined, neurotoxin- and PLA2-predominated venom arsenal, with major antigenicity shared among the true sea snakes and the Australo-Papuan elapids. The findings enrich our current understanding of the complexity of L. colubrina venom and the neutralizing spectrum of antivenom against the principal toxins from this unique elapid lineage.
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In the Fiji Islands, female yellow-lipped sea kraits (Laticauda colubrina) grow much larger than males, and have longer and wider heads than do conspecific males of the same body length. This morphological divergence is accompanied by (and may be adaptive to) a marked sex divergence in dietary habits. Adult female sea kraits feed primarily on large conger eels, and take only a single prey item per foraging bout. In contrast, adult males feed upon smaller moray eels, and frequently take multiple prey items. Prey size increases with snake body size in both males and females, but the sexes follow different trajectories in this respect. Female sea kraits consume larger eels relative to predator head size and body length than do males. Thus, the larger relative head size of female sea kraits is interpreted as an adaptation to consuming larger prey items. Our results are similar to those of previous studies on American water snakes (natricines) and Australian file snakes (acrochordids), indicating that similar patterns of sex divergence in dietary habits and feeding structures have evolved convergently in at least three separate lineages of aquatic snakes.
Reef fish identification: Tropical Pacific
  • G Allen
  • R Steene
  • P Humann
  • N Deloach
Allen, G., Steene, R., Humann, P., DeLoach, N. (2015). Reef fish identification: Tropical Pacific. 2nd edition. New World Publications, Jacksonville, Florida, USA. 502 pp.
Snakes of Southeast Asia
  • I Das
Das, I. (2021). Snakes of Southeast Asia. 3rd edition. John Beaufoy Publishing, Oxford. 176 pp.