The dangerously venomous snakes of the Philippine Archipelago with identification keys and ...

58 Pages·2014·8.9 MB·English

Reprintedfrom:Williams,GaryC.,andTerrenceM.Gosliner,eds.2014. :
CaliforniaAcademyofSciences,SanFrancisco,California94118,USA.Published15April14.
The Dangerously Venomous Snakes
of the PhilippineArchipelago
withIdentificationKeys andSpeciesAccounts
AlanE.Leviton1,RafeM.Brown2,CameronD.Siler3
1
2 3
1 2 3
PhotographsbyRafeM.Brown,ArvinC.Diesmos,DongLin,AaronLobo,
CameronD.Siler,JohnTashjian,MarkusOulehla,andHaroldVoris
IllustrationsbyEmilyEngandMichaelGarfield
Table of Contents
INTRODUCTION ...............................................................475
ACKNOWLEDGMENTS...........................................................477
IDENTIFICATIONKEYSTOTHEDANGEROUSLYVENOMOUSSNAKESOFTHEPHILIPPINEARCHIPELAGO479
TABLEOFTAXONOMICEQUIVALENTS...............................................491
SPECIESACCOUNTSFORTHEDANGEROUSLYVENOMOUSSNAKESOFTHEPHILIPPINEARCHIPELAGO493
Elapidae:Elapinae(cobras,coralsnakes,andkraits)...............................493
Calliophis ..............................................................493
Hemibungarus...........................................................494
Naja...................................................................496
Ophiophagus............................................................497
Elapidae:Hydrophiinae(seasnakes) ...........................................499
Aipysurus...............................................................500
Emydocephalus ..........................................................501
Hydrophis(includingAcalyptophis,Astrotia,Disteira,Enhydrina,Kerilia,Kolpophis,
Lapemis,Leioselasma,Pelamis,Praescutata,Thalassophis) ....................501
Elapidae:Laticaudinae(seakraits).............................................513
Laticauda...............................................................513
Viperidae:Crotalinae(pitvipers)...............................................515
Trimeresurus(Parias).....................................................515
Tropidolaemus...........................................................518
BIBLIOGRAPHY ...............................................................521
APPENDIXA:GLOSSARYOFTECHNICALTERMS.......................................526
APPENDIXB:INDEXTOSCIENTIFICNAMES ..........................................528
APPENDIXC:INDEXTOSTANDARDENGLISHNAMES...................................530
473
474 THECORALTRIANGLE:HEARSTBIODIVERSITYEXPEDITION
FIGURE2.
PhotobyCameronD.Siler
LEVITON,BROWN,&SILER:PHILIPPINEVENOMOUSSNAKES 475
The Dangerously Venomous Snakes of the PhilippineArchipelago
INTRODUCTION
No fewer than 33 species of dangerously venomous snakes inhabit the PhilippineIslands
andthesurroundingcoastalwaters(41,ifoneincludes eightseasnakes thathaveyetto
befoundinPhilippinecoastalwatersbutarelikelytooccurthere).Ofthepossible41species,26
areseasnakesandexceptfortwo,LaticaudacolubrinaandL.laticaudata,nonevoluntarilycome
ontoland(althoughsomeseasnakesmaywashashoreduringsevereweather).Theremaining15
species are terrestrial living in various habitats on land and in freshwater. Several terrestrial
species, such as Tropidolaemus [formerly Trimeresurus] subannulatus [formerly wagleri], favor
arborealhabitatsandseldomdescendtotheground.Allterrestrialspeciescanswim,andsomereg-
ularly occur near human habitations, in agricultural areas, and typically around sources of water
suchasfloodedricefields,rivers,andstreams.
TwofamiliesofdangerouslyvenomoussnakesarerepresentedinthePhilippineherpetofauna,
Elapidae (including sea snakes [subfamilies Hydrophiinae and Laticaudinae]), and Viperidae. A
numberofmildlyvenomoussnakesoccurinthearchipelagoaswell,andmostaremembersofthe
highlydiversesnakefamilyColubridae;theseincludetherear-fangedAsianvine-snakes(Ahaetul-
la), cat-eyed snakes (Boiga), mock viper (Psammodynastes), and two aquatic and semi-aquatic
snakes(Enhydris,Cerberus).Howdangerousanyofthesearetohumansisstillanopenmatterfor
research.Severalofthesupposedlynon-venomousAsiancolubridshavebeenshowntohavetoxic
salivas, and some can be considered mildly, if not dangerously, venomous. Some non-Philippine
watersnakes(selectedspeciesofTropidonophisandRhabdophis)havebeenshowntobelifethreat-
ening to humans butto date,inthePhilippines noneof thesegenera havebeenshowntobedan-
gerous.Whatwedoknowisthatweoftenunderestimatetheseverityofmanysnakebitesofboth
juvenile dangerously venomous and supposedly non-dangerously venomous snakes.Yet, bites of
just such animals have been implicated in the deaths of several knowledgeable professional her-
petologists,notablyKarlPattersonSchmidtwho,in1957attheageof67,wasbittenbyajuvenile
boomslang(Dispholidustypus), anAfricanrear-fangedsnake,anddiedadaylater;in1965,Fred
Shannon,M.D.,wasbittenbyCrotalusscutellatus,andafewyearslater,in1975,RobertMertens,
wasbittenbyanotherAfricanrear-fangedsnake,Thelotorniscapensis,andbothdiedasaresultof
the bites.And, most recently,in 2001, Joseph Slowinski,attheage of38, was bitten by a30cm
long juvenile krait, Bungarus wanghaotingi, and
diedwithin48hours.
At this point we emphasize that extreme care
shouldbeexercisedwhenhandlinganysnake,even
those that are supposedly non-venomous. It is not
alwayspossibletotellthedifferencebetweenven-
omous and non-venomous species without careful
inspection.InthePhilippines,forinstance,several
snakesareblackwithwhitebandings;amongthese
are Lycodon subcinctus, Calamaria lumbricoidea,
juveniles of several species of Oxyrhabdion,
Oligodon, and Chrysopelea, as well as the six FIGURE1.Lookscanbedeceiving.Afieldcolleague
recently picked up and photographed this innocent-
speciesofvenomoussnakesthatarereferredtothe
looking snake in the belief it was a non-venomous
genera Hemibungarus and Calliophis. The snakes speciesof .Itis,infact,acoralsnake,ofthe
ofthefirstgrouparenon-venomous,thelattertwo, genus .PhotobyN.Antoque.
476 THECORALTRIANGLE:HEARSTBIODIVERSITYEXPEDITION
Hemibungarus and Calliophis,dangerouslyvenomous.Theonly definitivewaytoknow whether
adark and lightbanded snake is avenomous or non-venomous species is to examinetheside of
theheadjustinfrontoftheeyetoseeifalorealscale(seefig.onp.480)ispresent.Ifitisabsent,
thesnakemaywellbeavenomousspecies.Intheillustratedkeysthatfollow,theseandotherdefin-
ingcharactersareclearlynoted.
Withrespecttothetreatmentofsnake-bites,againitcannotbeoverstatedthatallbitesshould
betakenseriously.Itistruethatalargepercentageofbites,evenbydangerouslyvenomoussnakes,
are“drybites,”thatisbitesinwhichnoenvenomationoccurs.Becauseitisnotalwayspossibleto
knowimmediatelyfollowingabitewhetherornotenvenomationhasoccurred,itisimperativeto
seek appropriatemedicaltreatmentas soon as possible.Morecomplete instructions areavailable
inotherpublications,severalofwhicharegiveninthebibliography(seeinparticularWHO1999
andLewin[thisvolume]).
ThesnakefaunaofthePhilippines is reasonably wellknown,althoughthereareareasofthe
country that have not been thoroughy investigated, especially parts of Luzon, Mindanao, and
Palawan.Itshould beemphasizedthat preciseknowledgeofthekinds ofvenomous snakes pres-
entisimperativeifoneisgoingtoreceiveeffectivemedicaltreatmentforasnakebite.Forinstance,
in thePhilippines,heretofore,onlyonespecieswiththreesubspeciesofthePhilippinecobrawas
recognized, Naja naja, but extensive work by investigators demonstrated that in reality the three
subspeciesarequitedistinctandarenow recognizedas fullspecies.However,inthePhilippines,
onlyoneantiveninismanufacturedandreadilyavailable,forNajaphilippinensis.Theimportance
ofthiscanbeappreciatedwhenoneconsidersthattotreatasnakebiteonemustoftenusespecies-
specificantivenominasmuchastheantivenomusedtotreatonekindofsnakebitemaynotwork
forthebitesofotherspecies.Whetherthespecies-specificantivenomforthePhilippinecobra,Naja
philippinensis,worksforothercobrasnakebitesisnotknown.
The Philippines has a highly diverse fauna.And as aresult of recentsurveys,starting in the
1950s by the late Walter C. Brown of Menlo College, California, and and his colleague Angel
Alcala, then at Silliman University, Dumaguete, and thanks to recent field work throughout the
archipelago,knowledgeofthefaunaldiversityhasimprovedgreatly.Itishopedthatthiscontribu-
tionwillenablethoseengagedinthestudyofthefaunainthefieldandthelaboratorytorecognize
morereadilythemostdangerouscomponentsofthatfauna.
Thepresentworkrepresentsaneffortwithasinglepurpose,toaidintheidentificationofven-
omoussnakesofthePhilippines.Thus,wehavemadenoattempttoprovideinclusivesynonymies,
which are available in several of the works we cite, namely, Taylor (1922a), Leviton (1964a,
1964b),Golayetal.(1993),McDiarmid,CampbellandTouré(1999),andDavidandIneich(1999).
Wherenecessary,weprovideadditionalreferences.DESCRIPTIONSof individualspecies areinten-
tionallybrief,buttheyincludethedatanecessaryforconfirmationofidentifications.Thedatafor
SIZE refer to known maximum lengths recorded for the species; when available, total and tail
lengthsformalesandfemalesaregivenseparately.InthestatementsonDISTRIBUTION,welistonly
the country for non-Philippine localities and, where known, to Island and/or Province within the
Philippines(seemap,p.492).
WeacceptnamesforallofthedangerouslyvenomoussnakespeciesinthePhilippinesthatrep-
resentthemostcurrenttaxonomicarrangements,althoughwithrespecttoseasnakeswehavefol-
lowedSandersetal.(2013)(seealsoPyronetal.2013)intheuseofgenericassignmentsofspecies
andRasmussenetal.(2011)forsubfamilyassignments.Weprovideabrieftableofequivalencies
(p. 487) so that those familiar with older names can quickly locate the species of interest. For
instance,inthePhilippines,snakesformerlyreferredtocollectivelyasTrimeresuruswagleri,have
been assigned to two different species under the genus name Tropidolaemus (i.e., T. philippensis
LEVITON,BROWN,&SILER:PHILIPPINEVENOMOUSSNAKES 477
andT.subannulatus);theannulatedorbarredcoralsnake,Calliophiscalligaster,isnowplacedin
thegenus Hemibungarus,whereas thebandedcoralsnake, Maticora intestinalis,is referred to as
Calliophis intestinalis. In addition, in recent years, the pit vipers usually referred to the genus
Trimeresurushavebeensubjectedtointensescrutinyandattimeshavebeenreassignedtoseveral
genera,Trimeresurus, Parias,and,as alreadynoted, Tropidolaemus.Atthetimeof thewriting of
this report, the species of pit vipers assigned to the nominal genus Parias, havebeen returned to
the genus Trimeresurus (e.g., T. flavomaculatus, T. mcgregori, and T. schultzei); however, some
researchersrecognizePariasasasubgenusofTrimeresurus,andwehaveadoptedthatassignment
here, whereas Tropidolaemus is still valid as a distinct genus. These changes, though frequently
confusing to the non-specialist, often represent significant advances to our understanding of the
relationshipsandareimportantinleadingtomoreeffectivetreatmentofsnakebitesbyallowingfor
theselectionandadministrationofappropriatespecies-specificantivenoms.
Lastly, we emphasize that whereas we believe all snakes should be treated with care, ven-
omous or not, snakes are also highly beneficial to the ecosystem and should not be wantonly
destroyedbecauseoffear.ThevastmajorityofthePhilippines’180+speciesofsnakesarenotdan-
geroustohumans.
An early version of this publication titled “Keys to the dangerously venomous terrestrial
snakesofthePhilippines”waspublishedintheSillimanJournal(Leviton1961).Thatpublication
wasfollowedbyAngelAlcala’s1986treatmentofthevenomoussnakesofthePhilippinesinvol-
umeX, Amphibians andReptiles,intheGuidetoPhilippineFloraandFauna.Sincethesepubli-
cationsappeared,additionalnewinformationfrombothfieldandlaboratoryresearchhascometo
light.Indeed,anumberofgroupsinEuropeandtheUnitedStatesareactivelyengagedinresearch
aimed at clarifying the taxonomy of the viperid genera Trimeresurus and Tropidolaemus, as well
astheelapidsnakesinthegeneraCalliophisandHemibungarusandtheseasnakes.Asaresult,we
expectthattheclassification of thevenomous snakespresented herewillcontinueto change(see
Bibliography for references, especially for authors David, Ineich, and Vogel, Rasmussen et al.,
Thorpe,Maholtra,andWüster).
ACKNOWLEDGMENTS
TheauthorsexpresstheirprofoundappreciationtoHaroldVoris,DougLin,andJohnTashjian,
who are responsible for several of the photographs that are reproduced here. Please note that in
thosefigurelegendswherethewords“Photoby”appear,copyrightownershipoftheimagesresides
withtheindividualacknowledgedandnottheCaliforniaAcademyofSciences.
Weoweaspecial thanks toour friend and collaboratorA. C.Diesmos (NationalMuseum of
the Philippines) for his continued support, past companionship in the field, for the use of photo-
graphs reproduced here, and for the logistical assistance he has generously provided through the
years.
And,lestweforget,oneofus(AEL)wantstoexpresshisappreciationagaintothestaffofthe
NationalMuseumofNaturalHistory,specificallyGeorgeZug,AddisonWynn,andKennethTighe,
fortheirongoingassistanceinlocatingspecimensandprovidingonsiteworkspace.
Lastly,wethankDr.MicheleL.Aldrichwhoperusedanearlyversionofthemanuscriptwith
extraordinarycareandmadesubstantivesuggestionsforimprovingtheoverallpresentation.Weare
alsoindebtedtotheexternalreviewersfortheirthoughtfulcomments.Dr.GeorgeZug,inparticu-
lar, suggested a number of changes, most of which we heartily accepted. Having said this, the
authorsstillbearfullresponsibilityfortheirdecisionstoacceptorrejectspecificrecommendations
aswellasforerrorsofcommissionoromission.
478 THECORALTRIANGLE:HEARSTBIODIVERSITYEXPEDITION
Fieldwork was supported partially by a National Science Foundation Doctoral Dissertation
Improvementgrant(DEB0804115toCDS),FulbrightandFulbright-HayesFellowships(toCDS);
and an NSF BioticSurveys and Inventories grant(DEB 0743491 to RMB).We thank thePhilip-
pinegovernment's ProtectedAreas andWildlifeBureau(PAWB)of thePhilippineDepartmentof
Environmentand NaturalResources for facilitating field studies that involvednumerous encoun-
terswithvenomoussnakes.
AlanE.Leviton,RafeM.Brown,andCameronD.Siler
06January2014
LEVITON,BROWN,&SILER:PHILIPPINEVENOMOUSSNAKES 479
Identification Keys to the Species of Dangerously Venomous Snakes
of the PhilippineArchipelago
GENERALNOTEANDTAXONOMIC(NAME)CHANGES:Thiskeyhasbeenformulatedtoaccommo-
dateonly the dangerously venomous snakes known fromthe Philippine Islands. It should not be
used, even at the generic or familial group levels, to identify venomous snakes from outside the
archipelago.Colors mentionedinthekeys arebasedoncolorsinlife;inpreservative,colors may
belostorchanged,greensturnbluish,redsarelost,andotherbrightcolorsbecomedull.Inprepar-
ing this key and the species accounts that follow, we have been guided by the latest revisionary
studies, but wehavealso taken aconservativepositionbecauseofthenatureoftheanimals with
whichweareworking(seebelow).Thesectionofthekeydealingwiththeseasnakes(couplets17
et seq.) has been modified from Smith (1926 and 1943 and Rasmussen, Elmberg, Gravlund, and
Ineich2011). Furthermore,wehaveculledfromtheliteratureandadoptedthemostrecentphylo-
geneticarrangementforthegeneraofviviparousseasnakes,notablythatofSandersetal.2013,so
thatmanyheretoforefamilar genericnames,such asEnhydrina, Lapemis,and Pelamis,and their
includedspecies,havebeenreferredtothegenusHydrophis.
Also, we have, rather arbitrarily, chosen to accord all recognizably distinct allopatric sub-
species fullspecies status rather than getembroiled in arguments of why raise onesubspecies to
fullspeciesstatusbutretainanotheras asubspecies,thoughbothcanbereadily,thoughdifferen-
tially, diagnosed taxonomically.Arguments as to what constititues a biological “species” versus
“subspecies” are most often not fruitful and usually based on arbitrary assessments by a given
workeronjusthow“important”acharacterorcharacterstateisininferringthe“closeness”ofbio-
logicalaffinities,i.e.,thegenealogicalrelationshipsamongtheparties.
Aswehavealreadymentioned(pp.472–473),inrecentyearsthemostsignificantnomenclat-
uralchanges havebeenintheallocation ofspecies amonggeneraofvenomous snakes.Thus,we
hasten to emphasize, many of these changes are not to be taken lightly inasmuch as they reflect
importantchangesinourunderstandingoftherelationshipsamongthesevenomoussnakespecies
and are highly relevant because of the significant medical implications, vis-a-vis the production
anduseofantiveninsinthetreatmentofsnakebites.
Also,pleasenote,manyoftheimageshavebeenprovidedbycolleaguesasacourtesyforthe
expressuseofmembersoftheHearstPhilippineExpeditionparticipants;theimagesareownedand
copyrightedbythedonorsandmustnotbecopiedorotherwisedistributed.
480 THECORALTRIANGLE:HEARSTBIODIVERSITYEXPEDITION
A
B C
G
H
G.Lateralanddorsalviewsoftheheadofakingcobra,
.Noteinparticulartheabsenceofthelorealscalebetween
thepostnasalandthepreocularscales.Thisischaracteristicofall
elapinesnakes,buttheabsencemustbeusedwithcarebecausea
numberofnon-venomouscolubrinesnakesalsolacktheloreal.
D E
H.LateralanddorsalviewofatypicalPhilippineviperinesnake,
Diagramsofheadandbodyscalationinatypi- ( ) .Notethepositionofthe
calsnake. :(A)lateral,(B)dorsal, sensorypitlocatedonthesideoftheheadbetweenthe
and(C)Ventralviews. nostrilandtheeye.
andhowbesttocountscale
rows.Bodyscalesarrangedin(D)obliquerows,
and(E)parallelrows.
DiagramsmodifiedfromSmith(1943)
I J
Diagramsofskullsofelapine( )(I)andcrotalineviper( )(J)skulls.
(I)maxillaisattachedtoectopterygoidandcannotrotate;smallpost-fangmaxillaryteethusuallybehindvenom
deliveryfangs;(J)Maxillarybonesmall,rotatesagainstectopterygoid;noteethbehindvenomdeliveryfangs.
DiagramsfromBoulenger(1893,3:373and3:518)
(max=maxillarybone;ect=ectoptygeroidbone)
FIGURES3A–J.DiagramsofdiagnosticscaleanddentalcharactersofPhilippinesnakes.
LEVITON,BROWN,&SILER:PHILIPPINEVENOMOUSSNAKES 481
1a.Pupilofeyeround;lorealscaleabsent(Fig.4);venomfangsshort,permanentlyerect;maxil-
lary bone elongate, usually with several small teeth behind front fangs (Family Elapidae,
includingcobras,coralsnakes,andseasnakes)(seeFig.3I).........................2
1b.Pupilofeyeverticallyelliptical(Fig.5A);lorealscaleabsent;uppersurfaceofheadeithercov-
eredbysmallscales (Fig.5B)orlarge,symmetricalscales;adeepsensorypitpresentimme-
diatelybehindthenostril(Fig.5A);venomfangsvariableinlength,fixedtoashortmoveable
maxillary bone that allows for rotation of the fangs backward when the mouth is closed; no
teethbehindfangs(FamilyViperidae)(seeFig.3J)...............................12
2a.Tailflattenedlaterally,oar-like(Fig.6A)(seasnakes)..............................16
2b.Tailrounded,tapering(Fig.6B)(terrestrialsnakes)................................3
3a. Scales in 13–15 longitudinal rows at midbody; scales on sides of body variable, in either
obliqueorparallelrows(Figs.3D,3E,8A,and8B)...............................4
3b. Scales in 17–25 longitudinal rows at midbody; scales on sides of body in oblique rows [Fig.
3D,alsoFig.8AforOphiophagus](GenusNaja).................................10
4a.Scalesonsidesofbodyinobliquerows(Figs.3D,8A);numberofscalesonposteriorthirdof
body at least two less than on anterior third (Balabac, Jolo, Luzon, Mindanao, Mindoro,
Negros,Panay,Palawan,Polillo)........................Ophiophagushannah(Fig.7A)
4b.Scalesonsidesofbodyinparallelrows(Figs.3E,8B);numberofscalesonposteriorthirdof
bodyequaltonumberonanteriorthird.........................................5
5a.Scalesin15longitudinalrowsatmidhody(GenusHemibungarus).....................6
5b.Scalesin13longitudinalrowsatmidbody(GenusCalliophis)........................8
6a. Black rings on dorsum of body not divided by narrow white annuli; temporal region heavily
pigmentedwithmelanin;whiteannuliondorsumusuallylessthan60.................7
FIGURE4.Pupilofeyeof ;lorealscaleabsent.
A B
FIGURES5A–B. :(A)Lateralviewofhead(B)Dorsalviewofhead.
A B
FIGURES6A–B.Tailsofseasnakes(A.laterallycompressed,paddle-shaped)and
terrestrialsnakes(B.notcompressed,roundedandtaperingtowardtip).
482 THECORALTRIANGLE:HEARSTBIODIVERSITYEXPEDITION
6b. Black rings on dorsum of body divided by narrow white annuli; temporal region not heavily
pigmented with melanin; white annuli on dorsum usually more than 60; ventral shields: (♂)
197–216, (♀) 218–227 (Cebu, Negros, Panay). . . . . . . . . . . . . . . . Hemibungarusgemianulis
7a. Ventral shields: (♂) 223–233; (♀) 252–259 (Luzon). . . . . . . Hemibungaruscalligaster(Fig.9)
7b. Ventral shields: (♂) 206 (two specimens) (Polillo and adjacent Aurora Prov., Luzon). . . . . . . .
.....................................................Hemibungarusmcclungi
8a.Blackcrossbarsonventerdonotcomeincontactwithblackofsides;adistinctwhitelinepres-
ent on sides occupying entire first scale row or parts of first and second rows (Balabac,
Busuanga,Culion,Palawan)...................................Calliophisbilineata
8b.Blackcrossbars onventercontactblackofsides;nodistinctwhitelinealongouterscalerows
.......................................................................9
9a.Creamcoloredcrossbarsonventerdonotextendontosideofbodyabovefirstscalerow(Jolo)
........................................................ Calliophissuluensis
9b. Creamcolored crossbars on venter extend onto side of body, often to fourth scalerow (Min-
danao,Samar).....................................Calliophisphilippina(Fig.10)
A
B
FIGURES7A–B.Juneilesof(A) .and(B)
Photos.courtesyof(A)JohnTashjianand(B)MarkusOulehla
A B
FIGURES8A–B.Scalesonsidesofbody:(A)slantingdownward[oblique]( );
(B)horizontal[parallel]( ).
FIGURE9. . FIGURE10. .
PhotobyRafeBrown. PhotobyRafeBown.