202 IRCFReptIles&AmphIbIAns•Vol18,no4•DeC2011

Corallus annulatusfromtheCañopalmabiologicalstationconsumingwhatislikelyabrazilianlong-nosedbat(Rhynchonycteris naso).

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Ecological Notes on the Annulated Treeboa (Corallus annulatus) from a Costa Rican

Lowland Tropical Wet ForesttoddR.lewis1,paulb.C.Grant2,Robertw.henderson3,AlexFigueroa4,andmikeD.Dunn5

1wareham,Dorset,bh204pJUnitedKingdom(ecolewis@gmail.com)24901Cherrytreebend,Victoria,britishColombia,V8Y1s1Canada

3milwaukeepublicmuseum,milwaukee,wisconsin53233-1478,UsA(henderson@mpm.edu)4Departmentofbiologicalsciences,Universityofneworleans,neworleans,louisiana70122,UsA

557ponderosaDrive,whitehorse,Yukonterritory,Y1A5e4Canada

theAnnulatedtreeboa(Corallus annulatus;Figs.1–4)isoneofninecurrentlyrecognizedspeciesintheboidgenusCorallus(hendersonet

al.2009).ItsdisjunctrangeextendsfromeasternGuatemalaintonorthernhonduras,southeasternnicaragua,northeasternCostaRica,andsouth-westernpanamatonorthernColombiawestoftheAndes(hendersonetal.2001,mcCranie2010).ItistheonlyspeciesofCorallusfoundontheCaribbeanversantofCostaRica,whereitoccursatelevationstoatleast650mandperhapsashighas1,000m(solórzano2004).Corallus annulatusoccursmostlyinprimaryandsecondarylowlandtropicalwetandmoistrainforest(holdridge1967)anditappearstobegenuinelyrare(hendersonetal.2001).besidesC. cropaniiandC. blombergi(thelattercloselyrelatedtoC. annulatus),itistherarestmemberofthegenus.Asidefrominforma-tiononhabitatandactivity,littleisknownregardingitsnaturalhistory. Innovember2001,aherpetologicalinvestigationatCañopalmabiologicalstation,tortuguero,innortheasternCostaRica(Figs.5&6)discoveredthepresenceofC. annulatusfromasinglepreservedspecimenheldatthebiologicalstation.Furthersurveysintheareadetectedthespe-ciesinManicaria swampforest(lewisetal.2010)thatapparentlyheldlocallycommonpopulationsofthesnake(Fig.7).FurtherinventoryandabundancesurveysoverthenexttenyearsresultedinsomepreliminarymorphometricandecologicaldataonC. annulatus.

Study Site and MethodsCañopalmabiologicalstation’sclimatehasaveragedailytemperaturesof26°C(23–32°C)and70%Rh(60–95%).theregionissubjecttothe

customarywet(september–February)anddry(march–september)seasonsoftheneotropics,butisoftenaffectedbyonshoreweatherandstormsfromtheCaribbeansea.theCañopalmaareahashighlyunpredictableannualrainfallthatcanexceed6,500mm(lewis2009).over100cmofrainoverthecourseofafewdays,resultingintemporaryfloodingofthestationanditsgrounds,isnotunusual.suchabundantandseriousrain-fallinaknownlowlandcatchmentareacreatesahabitatthatisverywet,botanicallydiverse,andunusuallydominatedbypalms(Manicaria saccifera,locallyknownas“palmareal”),resultinginalowlandtropicalwetforestonrisenterrain(myers1990,lewis2009,lewisetal.2010).

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Fig. 1.Corallus annulatusinapalm(Raphia taedigera)attheCañopalmabiologicalstation.

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Fig. 2.Corallus annulatusfromtheCañopalmabiologicalstationafterconsumingabat.

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Fig. 3.Corallus annulatusfromtheCañopalmabiologicalstation.

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Fig. 4.Corallus annulatusinapalm(Raphia taedigera)attheCañopalmabiologicalstation.

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nocturnalvisualencountersurveys(Ves)(heyeretal.1994)wereconductedonknowntrailsandtransectsatCañopalmabiologicalstationtolocateCorallus annulatus.wewerealertedtosomeadditionalindividu-alsbylocalresidents.Datarecordedincludedmorphometrics:weight(g),snout-ventlength(sVl),totallength(tl);aswellassex,habitat,diet,andperchheight(ph),wherepossible.surveyandmorphometricmeasure-mentswerecarriedoutunderresearchpermitsgrantedbytheministerio

delAmbienteenergíatelecomunicaciones(mInAet)underthesistemanacionaldeÁreasdeConservación(sInAC)investigationprogram.Intheinterestofconservingthespecies,anddespitealackofpreservedspecimensinknowncollectionsglobally,nospecimenswerecollected.spearmanRankcorrelationcoefficients(rs)conductedinstatistica™Ver.7(statsoft,Inc.,tulsaoklahoma)wereusedtoinvestigatemorphologicalcharacteristics.

Results and Discussionoveraspanoftenyears,wecapturedtenfemaleandtenmaleC. annulatus (table1),butobserved26intotal.basedonsizedata,17ofthesnakes

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Fig. 6.lithographshowingtheapproximatelocationofCañopalma;thelocationoftheRíolasuerteandtheCañopalacio/Cañopalmaconfluence.

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Fig. 5.CostaRica’sprovincialandnortheasternzone.

Table 1.morphometricandhabitatdetailsofCorallus annulatus atCañopalmabiologicalstation,2001–2011(sVlandtotallengthinmm,massing,perchheightincm;nR=notrecorded).

Date Sex Age Color SVL (TL)/Mass Perch Habitat Prey Height

01may2001 F Adult orange 580(654)/57 250 Pentaclethra macroloba —

16Aug2001 m Adult gray 593(800)/65 850 Bambusa vulgaris —

21Aug2001 m Adult orange 992(1,306)/172 300 Manicaria saccifera —

12oct2001 m Adult lightgray 825(1,210)/168 900 Bambusa vulgaris —

28oct2001 F Adult gray 600(720)/56 380 Citrus aurantiun —

12Jan2002 F Juvenile black 180(270)/27 240 boatdock Rhynchonycteris naso

16nov2002 m Adult gray/orange 672(990)/96 850 Bambusa vulgaris Wilsonia canadensis

29nov2002 F Adult orange 590(660)/44.5 550 Bambusa vulgaris —

07Jan2003 m Adult orange 900(1,100)/157 180 Bambusa vulgaris —

15Jul2003 m Adult orange 512(584)/36 200 Manicaria saccifera Rhynchonycteris naso

28nov2003 m Juvenile gray/orange 198(287)/38 280 Manicaria saccifera —

06Dec2004 m Adult orange 1,020(1,200)/165 30 Manicaria saccifera —

27Jan2005 m Adult orange 910(1,250)/170 500 Manicaria saccifera —

03Feb2005 F Adult orange 780(970)/237 250 Manicaria saccifera —

15Feb2010 F Juvenile gray 392(472)/nR nR pondshrub —

17Jul2010 m Adult orange 874(1,008)/nR nR Ranchobuilding Unidentifiedbat

15sep2010 F Adult orange 1,434(1,544)/448 120 Zygia latifolia —

28Dec2010 F Adult gray/orange 968(1,077)/282 120 Vochysia ferrugenia —

10Jun2011 F Adult gray/orange 850(1,013)/141 150 Mangifera indica —

15Jun2011 F Adult orange 629(738)/90 100 Heliconiasp. —

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wereadultsandthreewerejuveniles.meansVlofmaleswas749.6±81.1mm(198–1,020mm)andforfemales700.3±107.8(180–1,434mm)(Fig.8).wefoundafemaleof1,434mmsVland1,544mmtotallength,verycloseinsizetothelargestknownindividual,alsoafemale,of1,447mmsVl(1,725mmtotallength)fromGuatemala(smithandAcevedo1997).massvariedbetween27and448g.totallength,sVl,andmasswereallpositivelycorrelated(rs=0.789,0.955,0.913;p<0.05). Fifteenoftheboaswereorangetocinnamonindorsalcoloration,withbrown/orangesaddlemarkings.Fourwereaslate-graytobrownwithdarkcrossbandsandsaddlemarkings.onlyoneindividualwasblack,butwedonotthinkitwasmelanisticoranerythristicduetothefactthatitshowedpartialsaddlemarkingsandlightermarkingsontheunderside.Colordidnotcorrelatesignificantlywithmorphology(rs=-0.464;p>0.05)anddidnotrelatetogender. habitatsvariedconsiderably,butwefoundnosignificantcorrela-tionbetweenhabitattype,morphology,orcolor(rs=0.078–0.248;p>0.05).sixindividualswerefoundinprimaryManicaria swampforestandtwowerefoundinhuman-madestructureswithinthebiologicalstation.Afavoredarea(fiveindividuals)wasariparianstandofmature,introducedbamboo(Bambusasp.)locatedinthegardenareaofthebiologicalstation.herewefoundaboathathadswallowedaCanadianwilson’swarbler(Wilsonia canadensis),aknownwintermigranttotheregion.Clearly,C. annulatus isabletoutilizehabitatsinnaturalandhuman-alteredsituationsand,likeseveralotherspeciesofCorallus(C.cookii,C.grenadensis,C.hortu-lanus),doesnothesitatetoexploitman-madestructures(henderson,2002,powelletal.2007).

Inadditiontothewarbler,weobservedasmall(180mmsVl)C. annulatusfeedingonabrazilianlong-nosedbat(Rhynchonycteris naso)(lewisetal.2009).In2010,oneofus(mD)observedaboaconsum-ingabatinaRancho-stylebuildingatthebiologicalstation.thisbatwasprobablyalsoaR. naso, asthisspecieswasoftenfoundintheRancho,butitsidentitywasnotconfirmed. tothebestofourknowledge,smallrodentswerepreviouslytheonlydocumentedpreyforwildC. annulatus(hendersonetal.1995).basedondataforotherspeciesofCorallus (i.e.,C. grenadensis,C. hortulanus,andC. ruschenbergerii;henderson2002andpaperscitedtherein),treeboaswithsVlsof~900mmandlongerarelargelymammalpredatorsandcharacteristicallyexhibitanambush-foragingstrategy,whereintheypositionthemselveslowinvegetationaboveatrailperceivedtobeusedbysmallmammals.theseambushsitesareusuallylowerinthevegetationwhencomparedtotheheightsatwhichsmallerboasactivelyforagefornocturnallyquiescentprey(i.e.,sleepinglizardsandbirds).thesixC. annulatusinoursamplewithsVls≥900mm(mean=1037.3±81.6mm;range=900–1,434mm)wereencounteredatameanperchheightof208.3±68.7cm(30–500cm).Incontrast,boaswithsVls<900mm(mean=584.1±61.2mm;180–874mm)hadameanperchheightof416.7±84.9cm(100–900cm),ortwiceashighaslargerindi-viduals,althoughperchheightswerenotsignificantlycorrelatedwithsVl(rs=-0.198;p>0.05),probablyattributabletooursmallsamplesizes.basedonthesedata,wesuspectthatC. annulatus,likeotherspeciesinthegenus,islargelyasmallmammalpredator. Activity in C. annulatus was usually minimal upon encounter.nineteenoftheindividualscaptured,and23ofthetotalseen,werefoundatnight,coiledonbranchesbeforemovingslowlyawayinanupwarddirectionwhenapproached.mostweredetectedbytheirlighter-coloredundersideandtelltalereflectiveorangeeye-shine.Uponcapture,manyindi-vidualsattemptedaswiftandoccasionallysuccessfulbite;otherdefensivebehaviorsincludedassumingaballed-upposture,voidingthecloaca,andtailvibration.nearlyallboasappearedtobehealthy,withonlytwopossess-ingsmallskinlesionsorharboringexternalparasitessuchasticks(Acari). DespitethesizeofC. annulatus andtheconspicuousred-orangeeye-shineinthebeamofaheadlamp,only26individualswereencounteredovera10-yearperiod,furtherattestingtotherarityofthespecies.Incontrast,onecanobserveseveralothersnakespeciesmorefrequentlyatCañopalmabiologicalstation.Forexample,29eyelashVipers(Bothriechis schlegelii),22Allen’sCoralsnakes(Micrurus alleni),13blunt-headedtreesnakes(Imantodes cenchoa),13Cloudedsnail-suckers(Sibon nebulatus),4Ringedsnail-eaters(Sibon annulatus),and4RedCoffeesnakes(Ninia sebae)wereobservedoverafour-monthspan(AF,unpublisheddata).wehopethatfurtherdatacollection,onlypossibleovermanyyearsoffieldwork,will

Fig. 8.plotofsnout-ventlength(sVl)andmassformaleandfemaleCorallus annulatus fromtheCañopalmabiologicalstation,2001–2011.

Fig. 7.typicalManicaria palmswampforest,dominatedbypalmaReal(Manicaria saccifera),atthenorthernsectionoftheCañopalmabiologicalstation’sforest.

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revealmoreoftheelusiveecologyandnaturalhistoryofC. annulatus.thatthespecieswarrantsspecialattentionbyconservationbiologistsissupple-mentaltothemoreurgentrequirementtoensurethatboththeprimaryandsecondaryforestswherethespeciesoccursare,orremain,protectedforfuturegenerationstogatherdata.

AcknowledgementswethankAnamariamonge,JavierGuevara,andCarlosCalvo(mInAet)forassistancewithlicensingandsupportfortheworkconductedinthebarradelColoradowildlifeRefugeandtortugueronationalpark,CostaRica.wethanktommason,GabrielDavid,Darylloth,Rossballard,and Josh Feltham for informative discussions pertaining to the spe-cies.theCanadianorganizationfortropicaleducationandRainforestConservationkindlypermittedthelong-terminvestigationonitsproperty.wealsothankthelatepeterstafford,who,despiteneverseeingthisstudycometofruition,eagerlysupporteditfromconception.

Literature Citedhenderson,R.w.2002.Neotropical Treeboas: Natural History of the Corallushor-

tulanusComplex. KriegerpublishingCo.,malabar,Florida.

henderson, R.w., t.w.p. micucci, G. puorto, and R.w. bourgeois. 1995.ecologicalcorrelatesandpatternsinthedistributionofneotropicalboines(serpentes:boidae):Apreliminaryassessment.Herpetological Natural History 3:15–27.

henderson,R.w.,m.hoggren,w.w.lamar,andl.porras.2001.DistributionandvariationinthetreeboaCorallus annulatus(serpentes:boidae).Studies in Neotropical Fauna and Environment36:39–47.

henderson,R.w.,p.passos,andD.Feitosa.2009.Geographicvariationintheemeraldtreeboa,Corallus caninus(squamata:boidae).Copeia2009:572–582.

heyer,w.R.,m.A.Donnelly,R.w.mcDiarmid,l.C.hayek,andm.s.Foster.1994.Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. smithsonianInstitutionpress,washington.

holdridge,l.R.1967.Lifezone Ecology.sanJosétropicalscienceCentre,CostaRica.

lewis,t.R.2009.environmentalinfluencesonthepopulationecologyofsixteenanuranamphibiansinaseasonallyfloodedneotropicalforest.Unpublishedph.D.thesis,FarnboroughCollegeoftechnology,surrey,UnitedKingdom.

lewis,t.R.,D.J.nash,andp.b.C.Grant.2009.predationbyCorallus annulatus(boidae)onRhynchonycteris naso(emballonuridae)inalowlandtropicalwetforest,CostaRica.Cuadernos de Herpetologia23:93–96.

lewis,t.R.,p.b.C.Grant,m.Garcia-Quesada,C.Ryall,andt.C.laDuke.2010.ApreliminarybotanicalstudyofCañopalmabiologicalstation,tortuguero,CostaRica.Brenesia74:73–84.

mcCranie, J.R. 2010.The Snakes of Honduras: Systematics, Distribution, and Conservation.Contributions toherpetology,volume26.society for thestudyofAmphibiansandReptiles,saltlakeCity,Utah.

myers,R.l.1990.palmswamps,pp267–278.In:A.e.lugo,m.brinson,ands.brown (eds.),Ecosystems of the World 15: Forested Wetlands.elsevier,oxford.

powell,s.D.,m.l.treglia,R.w.henderson,andR.powell.2007.treeboasinthewestIndies:ResponsesofCorallus cookiiandC. grenadensistodisturbedhabitats,pp.375–386.In:R.w.hendersonandR.powell(eds.),Biology of the Boas and Pythons.eaglemountainpublishinglC,eaglemountain,Utah.

smith,e.n.andm.e.Acevedo1997.thenorthernmostdistributionofCorallus annulatus (boidae),with commentson itsnaturalhistory.Southwestern Naturalist42:347–349.

solórzano,A.2004.Serpientes de Costa Rica/Snakesof Costa Rica.Inbio,santoDomingodeheredia,CostaRica.

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