IRCFREPTILES&AMPHIBIANS•21(3):86–92•SEP2014

Natural History Observations of Amazon Treeboas (Corallus hortulanus) on Three Islands

in the Parnaíba Delta, BrazilPedro da Costa Silva1 and Robert W. Henderson2

1Núcleo de Pesquisa em Biodiversidade e Biotecnologia, BIOTEC, Universidade Federal do Piauí, CampusMinistroReisVellozo,Parnaíba,Piauí.Cep:64202-020,Brazil

2MilwaukeePublicMuseum,Milwaukee,Wisconsin53233,USA(henderson@mpm.edu)

Photographsbytheseniorauthorexceptwhereindicated.

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IRCF REPTILES & AMPHIBIANS • VOL15, NO 4 • DEC 2008 189TABLE OF CONTENTS

T A B L E O F C O N T E N T S

F E A T U R E A R T I C L E S

Chasing Bullsnakes (Pituophis catenifer sayi) in Wisconsin: On the Road to Understanding the Ecology and Conservation of the Midwest’s Giant Serpent ...................... Joshua M. Kapfer 190

The Shared History of Treeboas (Corallus grenadensis) and Humans on Grenada: A Hypothetical Excursion ............................................................................................................................Robert W. Henderson 198

R E S E A R C H A R T I C L E S

The Texas Horned Lizard in Central and Western Texas ....................... Emily Henry, Jason Brewer, Krista Mougey, and Gad Perry 204 The Knight Anole (Anolis equestris) in Florida

.............................................Brian J. Camposano, Kenneth L. Krysko, Kevin M. Enge, Ellen M. Donlan, and Michael Granatosky 212

C O N S E R V A T I O N A L E R T

World’s Mammals in Crisis ............................................................................................................................................................. 220 More Than Mammals ...................................................................................................................................................................... 223 The “Dow Jones Index” of Biodiversity ........................................................................................................................................... 225

H U S B A N D R Y

Captive Care of the Central Netted Dragon ....................................................................................................... Shannon Plummer 226

P R O F I L E

Kraig Adler: A Lifetime Promoting Herpetology ................................................................................................ Michael L. Treglia 234

C O M M E N T A R Y

The Turtles Have Been Watching Me ........................................................................................................................ Eric Gangloff 238

B O O K R E V I E W

Threatened Amphibians of the World edited by S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R. Berridge, P. Ramani, and B.E. Young .............................................................................................................. Robert Powell 243

CONSERVATION RESEARCH REPORTS: Summaries of Published Conservation Research Reports ................................. 245 NATURAL HISTORY RESEARCH REPORTS: Summaries of Published Reports on Natural History ................................. 247 NEWBRIEFS ...................................................................................................................................................................................... 248 EDITORIAL INFORMATION ..................................................................................................................................................... 251 FOCUS ON CONSERVATION: A Project You Can Support ............................................................................................... 252

Front Cover. Shannon Plummer.Totat et velleseque audant mo estibus inveliquo velique rerchil erspienimus, quos accullabo. Ilibus aut dolor apicto invere pe dolum fugiatis maionsequat eumque moditia erere nonsedis ma sectiatur ma derrovitae voluptam, as quos accullabo.

Back Cover. Michael KernTotat et velleseque audant mo

estibus inveliquo velique rerchil erspienimus, quos accullabo. Ilibus

aut dolor apicto invere pe dolum fugiatis maionsequat eumque

moditia erere nonsedis ma sectia-tur ma derrovitae voluptam, as

IRC

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REPTILES & AMPHIBIANSC O N S E R V AT I O N A N D N AT U R A L H I S T O R Y

Copyright©2014.PedrodaCostaSilva.Allrightsreserved.

WWW.IRCF.ORG/REPTILESANDAMPHIBIANSJOURNAL

InJuneof2010,theseniorauthorinitiatedsurveysofAmazonTreeboas(Corallus hortulanus;Fig.1)alongwaterwaysoftheParnaíbaDelta.Sincethen,hehaslogged1,440surveyhoursthatresultedin1,320encounterswithC. hortulanus.

Study AreaTheParnaíbaDeltaisanareaof2,700km2, comprised of more than70islandsandisletsdividedbetweentheBrazilianstatesofPiauíandMaranhão.Surveyswereconductedinthreeareas

Fig. 1.AnAmazonTreeboa(Corallus hortulanus)inadaytimeretreatonBatatasIslandintheParnaíbaDelta,Brazil.

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knowntobeusedbyforagingtreeboas(Fig.2):CamaleõesCreekonIlhadasBatatas,BaixãoCreekonIlhaGrande,andGuirindóCreekonCanárias(Fig.3).Thethreeislandsarecharacterizedbyvegetationthatoccursonwetlandsadjacenttoriversandcreeksandcomprisedmainlybyanaquaticmac-rophyte(Montrichardia linifera), thorn-ladenMachaerium

lunatum, Pumpwoods (Cecropia sp.),OilPalm(Elaeis guine-sis),Java-plum(Syzygium cumini), Jenipapeiro(Jenipa ameri-cana),Ingadepaca (Inga vera),Monguba (Pachira aquatic), Red Mangrove (Rhizophora mangle), and Black Mangrove (Avicennia germinans).Theareaalsoisusedforagriculture,includingrice(plantedinthewetlandsadjacenttocreeks),

IRCFREPTILES&AMPHIBIANS•21(3):86–92•SEP2014DA COSTA SILVA AND HENDERSON

Fig. 2.Mapsdepictingthethreeislands,theircreeks,andtheirgeographiclocationinBrazil.

Fig. 3. Habitat along Guirindó creek.

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bananas,beans,andcanesugarontheuplandsintheinterioroftheislands.Averageannualrainfallexceeds1,200mm,fall-ingmainlyduringJanuarytoMay(IBAMA,1998).

MethodsSurveysbycanoe(Fig.4)alongeachcreekwereconductedmonthlyfromJune2010untilApril2014.Thecreeksrangefrom1–5kminlength,althoughonly1.5kmwereacces-siblebycanoe.Treeboaswereobservedandphotographed;aninfraredmonocular(Yukonnightfall),anLEDflashlight,andacamerawithnightvisioncapability(SonyCCDTRV128)wereusedtoobserveandrecordtreeboabehavior.Treeboaencountersusuallystartedatdusk(~1830h)andcontinuedto2355h.Ifnecessary,additionalsurveysweremadefrom0010hto0500h.

ResultsDorsalgroundcolors recordedon the three islandsweredarkgray(65%),darkorange(30%),andyellow(5%)onCamaleõesandBaixãocreeks,anddarkgray(50%),darkorange (40%), and yellow (10%) on Guirindó Creek.Minimumandmaximumnocturnalboaperchheightsvar-iedaccordingtohighandlowtides;someindividualswereobservedat1.2–2.5monmoonlessnights,butperchheightswere2.3–7.0mduringthefullmoon.Duringthedryseason,airtemperaturerangedbetween29ºCand26ºCbetween1759hand2350h,andfrom26ºCto24ºCduring0030hto0445h.Duringtherainyseason,airtemperatureswerebetween28 ºCand26 ºC from1759h to2359h, andbetween26ºCand22ºCduring0002hand0500h. Activity.—In 1,320 encounters withC. hortulanus, approximately30%wereadults(1,000–1,500mmSVL),50%subadults(800–1,000mmSVL),15%juveniles(500–

Fig. 4.TheseniorauthorwithaspectacularyellowAmazonTreeboa(Corallus hortulanus).PhotographbyMr.Boiteau.

Fig. 5. Corallus hortulanusbeginningtoswallowaPurpleGallinule(Prophyrio martinica).

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600mmSVL),and5%neonates(270–350mmSVL).Sevenhundredninety-fiveencountersoccurredduringmoonlessnights(newmoonandfirstquarter),andthreeboashadcap-turedprey:AGreatAni(Crotophaga major; da Costa Silva andHenderson2010), a Purple Gallinule (Prophyrio martin-ica;daCostaSilvaandHenderson2013b;Fig.5), and a Black Myotis(Myotis nigricans). Threeotherboaswereobservedstalkingtwodifferentpreyspecies,aSpinyRat(Makalata sp.; daCostaSilvaandHenderson2012)andtwo Green Iguanas (Iguana iguana), withoutsuccess.Inaddition,48adultsandtwoneonateswerecoiledinrestingpostureswithobviousbulgesintheirbodiesindicatingarecentlyingestedmeal.Mating C. hortulanuswereobservedcopulatingintheafter-noonduringSeptemberandduringthenightof27June. Threehundredencounterswererecordedduringmoon-litnights(fullmoonandlastquarter).Individualboashadcaptured a Great Kiskadee (Pitangus sulphuratus) andanIguana(Iguana iguana;daCostaSilvaetal.2012)andtwootherswereobservedhangingbytheirtailswithsmallpor-tionsoftheirheadssubmerged,possiblyforagingforfish(daCostaSilvaandHenderson2010). Otherboaswereobservedattempting(unsuccessfully)tocaptureaSpinyRat(Makalata sp.), a Black Ani (Crotophaga ani), aGreatAni(Crotophaga major), a Tropical Screech-Owl (Megascops choliba), aScaledDove(Columbina squammata),andaStriatedHeron(Butorides striata)onanestalongoneofthecreeks.

Mostindividualswereforaging(moving)intheshad-owsoftreesandusuallyabout3mabovetheground.ThehighnumberofC. hortulanus restrictingtheiractivitiestomoonlessnightsislikelyattributabletotheriskofbecomingprey(althoughtheymayremainvisibletopredatorssuchasBarn Owls, Tyto alba;daCostaSilvaandHenderson2013a). Duringtherainyseason,boaencountersdecreased,although53observationsweremadeduringrainlessintervals.Whenraining, C. hortulanuswasfrequentlycoiledundershelterpro-videdbytheleavesofthemacrophyteMontrichardia linifera. On26April2014,at1830hafter35minutesofheavyrain,twoboaswereobserved;at1901hoursearchwasinterruptedbyheavyrainandlightning.At1930h,therainhadstopped,thesurveyresumed,andanother13treeboaswereobservedby2030h(foratotaloftenadults~1.30–1.50mandfivejuvenilesto500mm);allwereactive. Aneffortwasmadetodeterminehowtheboasspenddaylighthours.Basedon225encounters,boas remainedcoiledundershelterprovidedbyvegetationalongthecreek.Onlyamatingcouplewasrecordedasactiveduringtheday(daCostaSilvaandHenderson2014).Thirty-oneboaswereobservedwithnoticeablebulgesintheirbodies,indicatingthattheyhadrecentlyingestedameal.Boasthathadrecentlyfedmayspenduptotendays(dependingonpreysize)inasecludedsitewhiledigestingthemeal,showingneitherovertmovementsnoranecessitytodrink.Fifty-fivepercentof

Fig. 6. Corallus hortulanusabouttocaptureabat(Myotis nigricans).

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subadult C. hortulanuswerefullyactive,havingcapturedorattemptedtocaptureprey,comparedtoonly25%foradults,15%forjuveniles,and5%forlikelyneonatesonthethreecreeks. Thesurveysalsoindicatedthatotherspeciesweremoreactiveorconspicuousalongthethreecreeksduringmoon-lessnights.Fiftyto80birds,representedby8–13species,wereobservedduringeachofthosesurveys,includingspe-cies thatareknownpreyofC. hortulanus.Themost fre-quently seenwere:GreatAni (Crotophaga major),BlackAni (Crotophaga ani), GreatKingfisher (Ceryle torquata), GreatKiskadee(Pitangus sulphuratus), WoodRail(Aramides mangle),GreenKingfisher (Chloroceryle americana), Purple Gallinule (Porphryrio martinica), Scaled Dove (Columbina squammata), SouthernHouseWren (Troglodytes musculus), Limpkin (Aramus guarauna), Barn Swallow (Hirundo rus-tica), Guira Cuckoo (Guira guira), TropicalScreech-Owl(Megascops choliba), and Striated Heron (Butorides striata).Additionally,between 90and150adultandhatchlingGreenIguanas(Iguana iguana)andtenrodents,mainlySpinyRats(Makalata sp.), twoFour-eyedOpossums(Philander sp.), and atleast25batswereobservedalongthecreeks.Duringmoon-litnights,however,birdswerenotobserved,exceptin“totalalert”indeepforestshadows;thisbehaviorcontinueduntilthemoonwastotallydown. Foraging and predation.—DuringanApril2013surveyatCamaleõescreek,tenC. hortulanusofvaryingsizeswereobservedperchedupto7.0monbranchesofPumpwoodTrees(Cecropia sp.)Theboasremainedrelativelyclosetoflowersandfruitsbeingvisitedbybats.Onthenightof20April2014at1942halongLaranjeiracreek(3–5mwideand~1.0kminlength),wespottedtheeyereflectionofanadult C. hortulanus (~1.5m)abouttocaptureanadultbat(Myotis nigricans) withabodylength ofabout7cm(Fig.6). Theboawas perchedabout2.5mabovewaterlevelonaliana,andthebatwaswrappedintwoofthesnake’scoils.Itremainedinthatpositionforfiveminutesandthebatwasstillalive.Theboahadbittenthebat’sbackandat1951hitappearedtobedead.At1952,theboabegansearchingforthebat’shead,butat1953hthebatwasreleased.At1954h,theboabitthebat’sheadasecondtimeand,withthebatinitsmouth,ascendedtowardthetopofthebush.At1956h,thebat was dropped and fell on dried leaves of M. linifera; it was immediatelyrecoveredandswallowingbeganat1957h(Fig.7).Theboaagainascendedtowardthetopofthecanopy,whereitremainedpartiallycoveredandby1959honlyasmallportionoftheventercouldbeseen,butitwasappar-entthatdeglutitionwasnearlycomplete.At2003h,theboadescendedabout15cmandcoiledinatypicalrestingpos-ture.Bymorningithadmovedtoanothersite. Vegetationknownas“restinga”orcoastalforestoccursonthenorthernportionofIlhaGrande(Fig.8).Muchofthis

foresthasbeenlostlargelyduetocuttingforcharcoalproduc-tion,clearingforagriculture,andexpandingsanddunes.TheforestiscomprisedmainlyofCarnaúba(Copernicia prunifera), Cashew (Anacardium occidentale), Angelica (Guettarda angelica), ImburanadeEspinho(Commiphora leptophloeos), JenipapoBravo(Tocoyena sellowiana),WildPassionFruit(Passiflora subrotunda),Mucunã (Dioclea violacea), Café Bravo (Casearia guianensis),Mandacarú(Pilosocereus catingi-cola), Cereus jamacaru,andGuajiru(Chrysobalanus icaco) thatgrowsonsandysoils.InaTremembéIndianvillagecalledSaquim, restinga forest still survives in a preserved area. Duringthecourseofmanyyearsexploringrestingaforest,theseniorauthorfinallyencounteredhisfirsttwoC. hortula-nus between1830hand2350hduringasurveyon14June2014.Anadultfemalewithatotallengthof~1.10mwas

Fig. 7.ThesamesnakeasinFig6.withthecapturedbat.

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seenmigratingfromthemangroveswamptotherestingafor-estandanotheradultfemale(~1.3mtotallength)thathadcapturedafemaleBare-tailedWoollyOpossum(Caluromys philander). At2025h,anunusualnoise,soundinglikethedistresscallofabird,washeardcomingfrom20maway.At2033, the soundwas eventually traced to theground

wherethetreeboahadthreecoilswrappedontheC. philan-der.Apparentlytheinitialcapturewasmadeinatree,buttheensuingstruggletookthemtotheground.Theboahaddifficultykillingtheopossumasitwasstillalive,screamingandtryingtoescape,whiletheboakeptbitingthebaseoftheopossum’stail.Theopossumhadexpelledanewbornfrom

Fig. 8.RestingaforestonIlhaGrande.

Fig. 9. Corallus hortulanuswithaBare-tailedWoollyOpossum(Caluromys philander).

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itsmarsupium(pouch)at2056h.From2100hto2120h,theboa’sattemptstoswallowtheopossumwereexasperatedbyantsthatwereapparentlyattractedtotheprey;theybittheboa’slowerjawanditresortedtohittingitsheadonthegroundseveraltimesinanattempttodislodgetheants.At2121h,withsomedifficulty,theboabegantoascendintoaCashewTree.Finally,at2136h,withtheposteriorhalfofitsbodysuspendedandtheCaluromysgraspedbytwocoilsofitstail(Fig.9),theboareachedasecureperch.Theopossum’sheadwasseizedat2149h,swallowingcommenced,andwascompletedat2202h.Between2203hand2215h,theboamovedslowlyamongbranches,andat2220h,finallycoiledunder an umbrella of Carnaúba Palm fronds and leaves of WildPassionFruit.At0930honthefollowingmorning,asearchfortheboawasunsuccessful. ThedietofCorallus hortulanusisthemosttaxonomi-callybroadofanyspeciesofCorallus(Pizzattoetal.2009;HendersonandPauers2012;Henderson,inpress),includingfrogs,lizards,andawidetaxonomicrangeofbirdsandmam-mals(marsupials,rodents,bats).Thereasonforthistrophicbreadthistwofold:(1)C. hortulanusoccursinhabitatsthatsupportgreatbiodiversity,and(2)thespeciesutilizesbothambushandactiveforagingstrategies.Byusingbothstrate-gies, C. hortulanusencountersgreaterpreydiversitythanifonlyoneortheotherstrategyisused.Asanambushforager,ithasthepotentialtoencounternocturnallyactivespeciesand,asanactiveforager,ithasthepotentialtoencounterpreythatisnocturnallyquiescent(e.g.,sleepingandnestingbirds).

AcknowledgmentsThe senior authordedicates this paper toProf.AntônioAlvaresTavares.HealsothanksJoséRobertoS.A.Leite,Prof.RoyRosenstein(AmericanUniversityofParis),BabaraCox,andDeuzienedeSouzaSilvaforhelpduringfieldexpeditions.Inaddition,heisgratefultoEthielleBarrosodeAndradeforproducingthemapofthestudysites.

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