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D — .MCZ The University ofKansas . NaturalHistory Museum HARVAR MiscellaneousPublicationNo. 87 13 September 1995 Ecuadorian Frogs of the Genus Colostethus (Anura: Dendrobatidae) Luis A. Coloma Division ofHerpetology NaturalHistoryMuseum , DepartmentofSystematicsandEcology The UniversityofKansas Lawrence, Kansas66045-2454, USA. Present address: Museo de Zoologia, Departamento de Ciencias Biologicas, Pontificia Universidad Catolica del Ecuador, Av. 12 de Octubre,Apdo. 17-01-2184, Quito, Ecuador. Natural History Museum The UniversityofKansas Lawrence, Kansas MISCELLANEOUS PUBLICATIONS Editor: Linda Trueb Managing Editor: Joseph T. Collins Miscellaneous Publication No. 87 Pp. 1—72; 16 figures; 3 tables; 3 color plates; 1 appendix Published 13 September 1995 ISBN: 0-89338-052-0 © 1995 by Natural History Museum Dyche Hall TheUniversity ofKansas Lawrence, Kansas 66045-2454 USA Printedby UniversityofKansasPrintingService Lawrence,Kansas — ABSTRACT The present knowledge ofdendrobatid frogs ofthe genus Colostethus in Ecuador is summarized.Thetaxonomichistoryofthegenusisdiscussedandtaxonomicallyusefulcharacters(e.g., external morphology, gonads, tadpoles, and calls) are described. Thirty-one species are recognized, including fivenew speciesdescribedherein. Eightnominalspeciesareassignedtoitssynonymy; they are viz., Colostethus citreicola (C. nexipus), C.festae (Epipedobatesparvulus), C. intermedins (C. kingsburyi), C. maculosus (C. bocagei), C. parens (C. exasperatus), C. taeniatus (C. pulchellus), C. tergogranulans (C. pulchellus), and C. torrenticola (C. jacobuspetersi). Lectotype designations are made forC. bocageiandC. infraguttatus,andaneotype isproposedforC.pulchellus. Several species areredescribed,andtaxonomicaccountswithdataonvariationaregivenforeachspecies.Newlocality records and distribution maps are provided. The ranges of species previously known from other countries (C.breviquartus, C. lehmanni,andC. talamancae) areextendedtoEcuador. New ecological dataarepresented, and descriptions oftadpoles ofeight species andcalls ofsix species are provided. A dichotomouskey is included to assist in the identificationofspecimens. Systematic, distributional, natural history, and extinction trends summaries are presented. Key words: Dendrobatidae; Colostethus; Ecuador; Systematics; Ecology; Distribution; Natural history; Extinction. INTRODUCTION The cryptically colored and nonpoisonous analyses were hampered by the lack of detailed dendrobatid frogs ofthe genus Colostethus (sensu informationonColostethusinregionssuchasEcua- lato) are highly diversified in the neotropics; 92 dor.Detailedinformationthatispivotaltoacompre- speciescurrentlyarerecognized.Colostethusranges hensive systematic analysis of the genus is pre- from Costa Rica and the LesserAntilles to Bolivia sented herein. andBrazil;theelevationaldistributionextendsfrom In the last three decades, increased collecting sealevel toabout4000m. The frogs are associated efforts in the Andes and adjacent lowlands have withvegetationaltypesvaryingfromdryandhumid revealed the existence of many species, some of tropical forests to montane forest and paramo. which have been described only recently (Rivero, Edwards (1974a) performed aphenetic analysis 1984, 1991a,b;LaMarca, 1985, 1989;Pefaur, 1984, to clarify the systematics ofColostethus. Attempts 1985;LynchandRufz-Carranza, 1985;Riveroetal., to recognize natural species groups and the evolu- 1986; Rivero and Serna, 1986, 1991; Frost, 1986; tionary history of its members also were made by DuellmanandSimmons, 1988;DuellmanandLynch, Rivero(1989),RiveroandSerna("1988"),Myerset 1988; Rivero and Granados-Diaz 1989: Morales al. (1991), and La Marca (1992). However, these andSchulte, 1993). HISTORICALRESUME ThefirstdescriptionsofColostethusfromEcua- By the endofthe 19th Century and the first half dor {Hyloxalusfuliginosus, and H. bocagei) were ofthe 20th Century, several other species and new published in 1871 by the Spanish naturalist and locality records were added through the efforts of explorer Marcos Jimenez de la Espada, who tra- several naturalists and professional collectors who versed Ecuador and much of Latin America. The sent specimens to European museums. George A. type material ofthese species was deposited in the Boulenger described Prostherapis whymperi, Museo Nacional de Ciencias Naturales in Madrid, Phyllobatesinfraguttatus.Phyllodromusvertebralis, Spain. Jimenez de la Espada (1875:pl. 3) provided mdPhyllobateskingsburyi(1882, 1898, 1899, 1918, illustrations of both Hyloxalus fuliginosus and respectively) based on collections deposited in the Hyloxalus bocagei, and an illustration (but no de- British Museum ofNatural History that weremade scription) of a third species, Phyllodromus by naturalists and explorers such as Edward pulchellum. Whymper,W. F. H. Rosenberg, R O. Simmons,and ) UNIV. KANSAS NAT. HIST. MUS. MISC. PUBL. NO. 87 M. G. Palmer. Peracca (1904) added new locality Duellmanetal. (1989a,b) describedthree speciesof records for several Ecuadorian Colostethus based ColostethusfromtheeasternsideoftheAndes.Myers on collections made by an Italian naturalist. Dr. (1991) recorded C. chocoensis from Ecuador. Enrico Festa. Rivero("1988")andRiveroand Serna("1988") Betweenthetimeofthesignificantcontributions recognized several putative monophyletic groups ofBoulenger until 1945, there were no remarkable withinColostethus;fiveofthesegroups(C.brunneus, additionstoourknowledgeofColostethusin Ecua- C.fuliginosus, C. inguinalis, C. subpunctatus, and dor.Andersson(1945),describedseveralnewEcua- C. vertebralis groups) include Ecuadorian species. dorianfrogsbasedoncollectionsmadebyanAmeri- Coloma (1991) listed 18 species of Ecuadorian can collector W. Clarke-Maclntyre and a Swedish Colostethusinageographicalchecklist.Rivero(1991a, travelerRolfBlomberg.Andersson describedthree b)described 12speciesbasedonmaterialcollectedby Colostethus (Phyllobates taeniatus, P. intermedins, several persons (e.g., members ofthe Olalla family and P. riocosangae); the types are deposited in the andJamesA. Peters) anddepositedinthecollections Swedish Museum ofNatural History. of the Smithsonian Institution and the Museum of After 1945, about 25 years elapsed before the ComparativeZoology.RiveroandAlmendariz(1991 advent of a new period of systematic work on andAlmendariz ("1991") summarized the systemat- EcuadorianColostethus.Edwards(1971)described ics and distribution of 30 nominal species plus 10 C. elachyhistus and C. anthracinus, and provided a unnamed Ecuadorian Colostethus. Finally, Morales redescription of C. vertebralis. Edwards (1974b) and Schulte (1993) described C.fugax. redescribed C. taeniatus, C. marchesianus, and C. Theprevious studiesprovidedabaselineformy intermedins,anddescribedC.sauli.Edwards(1974a) work on Ecuadorian Colostethus, the objectives of recognized 22 nominal species from Ecuador (in- which are to (1) describe five new taxa, (2) re- cluding several new species). Most of Edwards' describepoorlyknownspecies,and(3)addnewdata contributions are based primarily on material col- on the morphology, biology, ecology, and distribu- lected by field parties led by William E. Duellman tionofall species. Ultimately,itisexpectedthatthe andJohnD. Lynchanddepositedinthe Museumof data presented herein will help to provide a better Natural History atThe University ofKansas. Subse- understanding of the evolution of this important quently,Frost(1985) listed 14speciesofColostethus componentoftheneotropical herpetofauna,aswell fromEcuadorwithtaxonomicandgeographicalrefer- asabasisforfurtherecological studies andconser- ences, and described C. nexipus (Frost, 1986). vation efforts. ACKNOWLEDGMENTS For the loan of specimens and/or provision of FieldworkinEcuadorwassupportedbygrantsfrom working space in their institutions I thank Ana the Panorama Society Fund, Natural History Museum, Almendariz(EPN), FrancoAndreone (MZU),John The UniversityofKansas, by agrantfromthe National E. Cadle (ANSP), Barry Clarke (BM), Tjitte De Science Foundation (BSR 8805920 to William E. Vries (QCAZ), Jose Enrique Gonzalez Fernandez Duellman),andbytheGraduateStudentResearchFund (MNCN), W. Ronald Heyer (USNM), Marinus S. ofthe Department ofSystematics and Ecology ofThe Hoogmoed (RMNH), Sven O. Kullander (NRM), University of Kansas. William Duellman, Philip S. Alan E. Leviton (CAS). Juan Carlos Matheus Humphrey, and Hans-Peter Schultze were especially (MECN), Charles W. Myers (AMNH), Ronald A. helpful in gathering the financial support. Collecting Nussbaum(UMMZ),JoseRosado(MCZ),Elisabeth permits(002IC,031,060DNF-ANRS) wereissuedby Samec (NMW), Beat Schatti (MHNG), and John SergioFigueroaoftheDirectionNacionalForestalofthe AMNH Wright(LACM). Studyofspecimensinthe MinisteriodeAgriculturay Ganaderiaofthe Repiiblica was made possible by grants from the Collection del Ecuador. Study Grant Program (AMNH), and the Panorama Many people extended valuable assistance and/ Society Fund, Natural History Museum, The Uni- or logistic support during field trips in Ecuador. I versity ofKansas. thankthemalland,inparticular.LauraArcosTeran, ECUADORIAN FROGSOFTHEGENUSCOLOSTETHUS Tjitte DeVries,GiovanniOnore,andHugoRoman. ously shared data with me that contributed signifi- I ext—end my deepest thanks to many field compan- cantly to the completion ofthis project. ions Felipe Campos Y, Oscar Delgado, Andrew I thank William Duellman, Linda Trueb, and Gluesenkamp, David A. Kizirian, Diego F. RobertM.Timm,membersofmygraduatecommit- Lombeida, Luis Eduardo Lopez, Jenny Naranjo, tee, for their encouragement and their criticism of Giovanni Onore, Patricio Ponce, Ricardo Schmal- the present work. Thanks go toWilliam Duellman. bach, Stellade laTorre, DiegoTirira, MarioTapia, Linda S. Ford, David Kizirian, John D. Lynch, Sebastian Valdivieso, John J. Wiens, and Vlastimil Adrian Nieto, Robert M. Timm, Linda Trueb, and Zak. I am particularly indebtedtoAnaAlmendariz, John Wiens, who read parts orthe entire versionof William Duellman. Stephen R. Edwards, John D. this manuscript and generously provided sugges- Lynch,andGiovanni Onore, who ledmanycollect- tionsforitsimprovement.WilliamDuellmantaught ing trips, and whose collecting efforts have been methe useofthe Vibralizer; MarcusV. Vieiradrew pivotal for the development of the present work; Figure4,andErikR.Wilddrew Figure5.Giovanni alsothey generously allowed me to use field notes, Onore translated a species description; John E. recordings and photographic material. Stephen Simmonshelpedwithphotography,andJohnWiens EdwardsallowedmetousehisPh.D.dissertationas aidedwithosteologicalpreparations.Finally.Ihave a reference for the Ecuadorian Colostethus depos- an unpayabledebttoJohnSimmons,LigiaGalarza, ited atthe Natural History MuseumofThe Univer- Sofia Ana Simmons, and my family all of whom sity of Kansas. I also thank Charles W. Myers, have been an enduring source of moral support Enrique La Marca, and JuanA. Rivero who gener- through my studies in Kansas. MATERIALSAND METHODS Specimensexaminedinthecourseofthisstudyare MHNG Museum d'Histoire Naturelle, Geneva, listed in theAppendix. Throughout the text andAp- Switzerland. pendix, specimens are listed with theircatalog num- MNCN Museo Nacional de Ciencias Naturales, bers. Museum abbreviations are taken from Frost Madrid. Spain. (1985) andDuellman (1993); they are, as follow: MZU Museo Regionale di Scienze Naturali, Torino, Italy. AMNH American Museum of Natural History, NHMG Naturhistoriska Museet, Goteborg, Swe- New York. den. ANSP Academy of Natural Sciences, Philadel- NMW NaturhistorischesMuseumWien,Vienna. phia. Austria. BM BritishMuseum(NaturalHistory),United NRM Swedish Museum of Natural History, Kingdom. Stockholm, Sweden. CAS California Academy of Sciences, San QCAZ Museo de Zoologia, Pontificia Universi- Francisco. dad Catolica del Ecuador, Quito. CSJ Museo de Historia Natural, Colegio San RMNH Rijksmuseum van Natuurlijke Historic Jose, Medelli'n. Colombia. Leiden, The Netherlands. EPN Escuela Politecnica Nacional, Quito, E- USNM National Museum of Natural History, cuador. SmithsonianInstitution,Washington.D.C. KU University of Kansas, Natural History UMMZ University of Michigan, Museum ofZo- Museum, Lawrence. ology, Ann Arbor. LACM Natural History Museum ofLosAngeles County, Los Angeles. Measurements were obtained with Helios dial MCZ MuseumofComparativeZoology,Harvard calipers and recorded to the nearest 0.1 mm in the University, Cambridge. mannerdescribedbyDuellmanandSimmons 988 (1 ). MECN MuseoEcuatorianodeCienciasNaturales, Throughout the text SVL = snout-vent length. Sex Quito, Ecuador. was determined by dissection and the presence of UNIV. KANSAS NAT. HIST. MUS. MISC. PUBL. NO. 87 sexually dimorphic characters. Sexual maturity of numbers and depository of primary types and the females was determinedby the presence ofeggs or typelocality.Diagnosesfollowcloselytheformatof convoluted oviducts. DuellmanandSimmons(1988)withtheadditionof Webbingformulaearedescribedinthemannerof other character, which is the color of the testes in Duellman and Simmons (1988). The webbing males. Data of the diagnoses are taken from the formula II—VAIII—VAJEl—2IV2—IV is illus- specimens examined, unless otherwise indicated. trated in Figure 1. In some cases, the webbing MeasurementsofColostethuspumilusandC.fallax formulae are subjective because the distinction be- were taken from the original descriptions. tweenthe webbing and lateral fringe isambiguous. ColostethusfugaxandC.peculiariswerenotexam- Drawings ofspecimens immersed in alcohol were inedandalldataaretakenfromtheoriginaldescrip- madeusingaWildM-8stereomicroscopeequipped tions.Becauseitisdifficulttodistinguishadultsand with acamera lucida. juveniles males, I do not report a mean SVL for Because Colostethus hasnotbeen diagnosed by adults; rather, I present the range of SVL for all uniquely derived characters, species placement in malesofeachspecies(excludingrecentlymetamor- the genus is a matter of convenience based on a phosed juveniles); mean SVL for females is re- taxon's lack of the apomorphies that characterize ported for adults. Each species is compared with, monophyleticgroupswithintheDendrobatidae.The anddistinguishedfrom, similarEcuadorian species recentlydescribedgenusMannophryne(LaMarca, tofacilitateidentification.Descriptionsofholotypes 1992)accommodatesseveralEcuadorianColostethus areprovidedforthenewtaxaandforpoorlydescribed that have either one or several of the putative taxa. Dataon intraspecificvariationarepresentedfor synapomorphies of the new genus (e.g., bandlike most species. Coloration in life, larvae morphology, marks on throat; complex, aggressive and mating vocalization,etymology,distribution,andecologyare behavior; yellow throats); however, I think that the provided for each species. A dichotomous key is unique characters that defineMannophryne should included to aid in identification ofspecimens. be studied inmore detail andcorroborated within a I chose to describe and compare back-riding phylogenetic analysis of all Colostethus and tadpolesinStages24and25 (Gosner, 1960)(except Colostethus-Yike forms. Thus, I place within thetadpolesofColostethusanthracinusandC.awa, Colostethus several species that possess one or whichwererearedincaptivity)becausetheycanbe several ofthe characters that define Mannophryne identified with confidence. The occurrence ofsev- pending phylogenetic analyses. eral species of Dendrobatidae in sympatry causes In delimiting species, I relied on characters cur- uncertainty inassigningfree-swimmingtadpolesto rentlyusedindendrobatidtaxonomyandadditional a particular species in the absence of complete onesthatIfoundtobeconstantwithin populations. developmental series. In agreement with Frostand Hillis (1990), binomi- Ecologicaldistributionsofeachspeciesaregiven als areexpectedtoreflectlineages,thecomponents in the Ecuadorian life zones defined by Canadas- ofwhicharenotincontrovertiblyindifferentphylo- Cruz (1983). Unless otherwise indicated, climato- genetictrajectories.However,becauseofthelackof logicaldataforthelifezonesaretakenfromCanadas- adequate information for some species, errors of Cruz(1983).Distributionmapswithlocalityrecords eitherunderestimationoroverestimationofthereal are based on specimens examined and reliable lit- historical species are plausible. erature records. The ranges ofmost species do not Toaidreaders withtheapplicationsofnamesby necessarily reflect theiractual distribution (see Ex- authors dealing with Dendrobatidae, I present in tinction Trends for more detail). Illustrations of Table 1 a list of the trivial and present names of relevant characters and color photographs are pro- Colostethus and Epipedobates reported from the vided formost ofthe species. Ecuadorian fauna. Colostethus brunneus and C. Callsofsixspecieswererecorded.Recordingsof sylvaticus, that were included in the Ecuadorian all species except Colostethusjacobuspetersi were fauna by Almendariz ("1991"), are excluded from obtainedwithaMarantzstereocassetterecorderand this report, because no records were provided. a Sennheizer K3U microphone. Two recordings of In the species accounts, synonymies include the C.jacobuspetersi were obtained with a Sony cas- ECUADORIAN FROGSOFTHEGENUSCOLOSTETHUS sette recorderandaUher(Model4000-S)recorder. ofcallsperminute)weremeasuredwithastopwatch Periodsduringwhichthefrogappearedtobeundis- directly from the tapes. Notes percall, call length, turbedbytheinvestigatorwerechosenforanalysis. noteduration,andphase (timebetweennotes)were AudiospectrogramsweremadeonaVibralizer(Kay measuredfromwaveformsgeneratedbySoundEdit ElectricCompany)usingthenarrowbandfrequency of the Farallon MacRecorder Sound System soft- (45 Hz). Frequencymeasurementsofthecalls were ware. Original tapes are on hie in the tape archive, obtainedbyusingagridmarkedonaplasticoverlay DivisionofHerpetology,Natural History Museum, ontopoftheaudiospectrograms.Callrates(number The University ofKansas. Table 1. Alphabetical synonymy ofEcuadorian Colostetluts and Epipedobates. Trivial name Original generic name, author, and date Present name anthonyi Phyllobates Noble 1921 Epipedobates tricolor citreicola Colostetluts Rivero 1991b Colostetlutsnexipus festae Prostherapis Peracca 1904 Epipedobates parvulus intermedins Phyllobates Andersson 1945 Colostetlutskingsburyi maculosus Colostetluts Rivero 1991a Colostetluts bocagei paradoxus Colostetluts Rivero 1991a Epipedobates tricolor parens Colostetluts Rivero 1991b Colostetluts exasperatus rioeosangae Phyllobates Andersson 1945 Colostetlutspulehellus taeniatus Phyllobates Andersson 1945 Colostetlutspulehellus tergogranularis Colostetluts Rivero 1991b Colostetlutspulehellus torrenticola Colostetluts Rivero 1991b Colostetluts jaeobuspetersi CHARACTERS Followingisasummaryofthecharactersused,or vertebralis, have discs about equal in width to the that are potentially useful, in the diagnoses ofthe digits. Species at lower elevations usually have species. expanded discs. A similar elevational trend occurs — Size. ThespeciesofColostetlutsfromEcuador among populations assigned to C. elachyhistus. In generally are small-to-medium-sized (Table 2), thediagnoses,discsofthethirdfingerandfourthtoe compared to other dendrobatid frogs, such as were used to assess disc size. — Aromobates,whichreaches64mmSVL.Thesmall- Relativelengthsoffirstandsecondfinger. hi est species is C. machalilla, attaining a maximum most Ecuadorian Colostetluts, the first finger is SVLof17.6mm.Thelargestspecies,C.fuliginosus, about equal in length to the second finger (I = II), has a maximum SVL of 32.5 mm. The smallest whenthefingersareadpressed.InC.chocoensis,C. recently metamorphosedjuvenile ofC. chocoensis nexipus, and C. pumilus, the first finger is shorter mm is 6.7 in SVL. Males usually are smaller than than the second; in C. kingsburyi, C. machalilla, C. females (Table 2). — marchesianus, C. talamancae, and C. touchi, the Discsonfingersandtoes. SomeColostetluts first finger is longerthan the second—. have greatlyexpanded terminal discs on the digits; Fringeson fingersandtoes. Thefringeisa others have small discs about the same diameteras lateraldermalfoldonthedigits. Somespecies(e.g., thewidthofthedigits. Speciesathigherelevations, Colostetluts elachyhistus, C. exasperatus, C. such as C. anthracinus, C. jaeobuspetersi, and C. talamancae, and C. suuli) clearly have this charac- UNIV. KANSAS NAT. HIST. MUS. MISC. PUBL. NO. 87 Table2. Snout-ventlengths(mm)ofEcuadorianColostethus Range isgivenforadultfemales. Rangeformales includes adult and subadult individuals. Females Males Species Range (mean) n Range ECUADORIANFROGSOFTHEGENUSCOLOSTETHUS Fig. 1. Colostethus chocoensis. A. Right hand (MNHG (GO 47]). B—. Left f—oot (MNH—G 191—07). Notice webbing between fingers on hand. Foot illustrates awebbing formula ofII l'/illl l'/2llll 2IV2 IV. Lines equal 1 mm. — ter,whereasothers (e.g.,C. bocagei,C. chocoensis, Thirdfingerinmales. Thedistalsegmentsof C.fuliginosus,andC.nexipus)ha.vewell-developed the third finger in males is distinctly swollen in fringes on hands, but the fringes on the feet are several ColostethusandEpipedobates. Myerset. al continuouswiththeinterdigital webbing. Mostspe- (1991) indicated that this character is expressed cies lack fringes; in some, such as C. awa, C. more strongly in some species, and that in some kingsburyi, C. mystax, and C. shuar, fringes are speciesatleast,itisnotexpressedinalladultmales. poorly developed. In some cases, the intraspecihc OftheEcuadorianColostethus,onlyC.fugaxandC. variation observed may be an artifact ofpreserva- machalillci have th—is character. tion that tightens the skin to the digit. When it was Tarsal folds. Therearetwokindsoffolds.A difficult to distinguish between a real fringe and a dermal foldmayoccuralongtheouterventral edge preservation artifact, I describe the dermal modifi- of the tarsus. About half of the Ecuadorian cation as a "keel." Colostethus lacks this fold; however, it is well UNIV. KANSAS NAT. HIST. MUS. MISC. PUBL. NO. 87 Fig. 2. Dorsal color patterns of Colostethus. A. C.jacobuspetersi, QCAZ 1378. B. C. maquipucuna, KU 202882. C.C. machalilla, KU 132330. D.C. chocoensis, MNHG (GO47). E. C. infraguttatus KU 142401. F. C. anthracinus, KU 120653. Lines equal 5 mm, except in A, in which it is 2 mm. developed in C. bocagei, C. elachyhistus, C. unwebbed to almost completely webbed. Also, in- fuliginosus, C. talamancae C. sauli, and C. shuar. traspecific variation in foot webbing exists among , In otherspecies, it is weakly developed.Asigmoid populationsofC. infraguttatusandC. elachyhistus, or straight inner tarsal fold is present in most spe- and within populations ofC.—toachi. cies; itextends from the distal halfortwo thirds of Dorsalcolor patterns. SeveralColostethus the tarsus to the innermetatarsal tubercl—e. have a uniform brown dorsum; however, mostspe- Webbingbetweenfingersandtoes. Webbing cieshave dark marks ordark stripes on the dorsum is absent between the fingers in most Ecuadorian (Fig. 2). Dark marks may be in an irregular or Colostethus; however, some species, such as C. reticulatepatternasinC.maquipucuna,somespeci- chocoensis(Fig. 1)andC.peculiarispossessasmall mensofC.pulchellus,andC.jacobuspetersi. Some webbing between Fingers II and III that is continu- populations of C. elachyhistus and C. shuar have ous with a lateral fringe. The amount of webbing irregularly distributed dark spots. The most com- between the fingers in C. chocoensis varies. The monpatternisthatofatransversemarkbetweenthe extent of webbing between toes varies from eyes, followed posteriorly by a "V"-shaped mark