Leptodactylus guianensis is reported for the first time for Colombia along with a distributional map of the species. The species is the fifth species of the L. latransspecies group documented in the country. Males possess a single, conical and slightly chisel-shaped thumb spine; only three species in the group have a single thumb spine. In collections, specimens of L. guianensis are misidentified as L. macrosternum, L. latrans or L. bolivianus. We provide morphological, colouration and habitat descriptions for where the species occurs in Colombia

de Sá, Rafael O.

Gutiérrez-Lamus, Doris L.

Muñoz, Mariela Osorno

English

University of Richmond

University of Richmond UR Scholarship Repository Biology Faculty Publications Biology 4-26-2019 Presence and distribution of Leptodactylus guianensis Heyer and de Sá, 2011 in Colombia: comparisons with other species in the L. latrans group Mariela Osorno Muñoz Doris L. Gutiérrez-Lamus Rafael O. de Sá University of Richmond, rdesa@richmond.edu Follow this and additional works at: https://scholarship.richmond.edu/biology-faculty-publications  Part of the Agricultural and Resource Economics Commons, Biology Commons, Population Biology Commons, Research Methods in Life Sciences Commons, and the Terrestrial and Aquatic Ecology Commons Recommended Citation Osorno, M., Gutierrez, D.L., and de Sá, R.O. 2019. Presence and distribution of Leptodactylus guianensis Heyer and de Sá, 2011 in Colombia: comparisons with other species in the L. latrans group. Journal of Natural History 53(9-10):577-584. https://doi.org/10.1080/00222933.2019.1600755. This Article is brought to you for free and open access by the Biology at UR Scholarship Repository. It has been accepted for inclusion in Biology Faculty Publications by an authorized administrator of UR Scholarship Repository. For more information, please contact scholarshiprepository@richmond.edu. ARTICLEPresence and distribution of Leptodactylus guianensis Heyerand de Sá, 2011 in Colombia: comparisons with other speciesin the L. latrans groupMariela Osorno Muñoza, Doris L. Gutiérrez-Lamusa and Rafael O. de SábaInstituto Amazónico de Investigaciones Científicas SINCHI, Bogotá, Colombia; bDepartment of Biology,University of Richmond, Richmond, VA, USAABSTRACTLeptodactylus guianensis is reported for the first time for Colombiaalong with a distributional map of the species. The species is thefifth species of the L. latrans species group documented in thecountry. Males possess a single, conical and slightly chisel-shapedthumb spine; only three species in the group have a single thumbspine. In collections, specimens of L. guianensis are misidentified asL. macrosternum, L. latrans or L. bolivianus. We provide morpholo-gical, colouration and habitat descriptions for where the speciesoccurs in Colombia.ARTICLE HISTORYReceived 6 July 2018Accepted 24 March 2019KEYWORDSMorphology; ecology;habitat; male nuptial spines;distributionIntroductionThe Neotropical genus Leptodactylus Fitzinger, 1826 currently consists of 75 species thatare clustered into four species groups (Heyer 1969; Larson and de Sá 1998; de Sá et al.2014). The L. latrans species group contains eight recognised taxa: L. bolivianusBoulenger, 1898, L. chaquensis Cei, 1950, L. guianensis Heyer and de Sá, 2011,L. insularum Barbour, 1906, L. latrans (Steffen 1815), L. macrosternum Miranda-Ribeiro,1926, L. silvanimbus McCranie et al., 1980 and L. viridis Jim and Spirandeli-Cruz, 1973.One species, L. silvanimbus, is endemic to Honduras, and the remaining species arewidely distributed in South America with L. insularum entering Mesoamerica and reach-ing Costa Rica. The latrans species group is recognised by five osteological cranialsynapomorphies (de Sá et al. 2014). Four species of the latrans species group havebeen reported to occur in Colombia: L. bolivianus, L. insularum, L. latrans andL. macrosternum. The description of Leptodactylus guianensis suggested the species ismost closely related to L. bolivianus based on the presence of a single keratinised thumbspine in both species (Heyer and de Sá 2011). In addition, it reported the species inhabitslowland environments of the Guiana Shield, occurring in Guyana, Suriname, Venezuelaand Brazil. A more extensive distribution was suggested with question marks, pendingconfirmation, since those specimens did not include males with sexual secondarycharacters (i.e. only juveniles and females; Heyer and de Sá 2011). Although the specieshas been reported to occur in Colombia (e.g. Frost 2011; Cole et al. 2013), this has notCONTACT Mariela Osorno Muñoz mosorno@sinchi.org.co; Rafael O. de Sá rdesa@richmond.eduJOURNAL OF NATURAL HISTORY2019, VOL. 53, NOS. 9–10, 577–584https://doi.org/10.1080/00222933.2019.1600755© 2019 Informa UK Limited, trading as Taylor & Francis Groupbeen verified from specimens collected in Colombia. We report the presence ofLeptodactylus guianensis in Colombia and discuss the characteristics that differentiateit from breeding adult males of L. bolivianus. We also provide information on the habitatoccupied by L. guianensis in Colombia.Material and methodsSpecimens herein identified as L. guianensis are deposited in the amphibian collectionsof the Instituto Amazónico de Investigaciones Científicas (SINCHI; Bogotá, Colombia)under the numbers SINCHI-A 3318–23, 5200, 5225 and 2453; and the Instituto deCiencias Naturales, Universidad Nacional de Colombia, with number ICN 46855; speci-mens SINCHI-A 3320–21 and 2453, and ICN 46855, are adult males with distinct second-ary sexual breeding traits. Measurements were taken with digital Mitutoyo callipers tothe nearest 0.1 mm; morphological terminology follows Heyer and de Sá (2011) and deSá et al. (2014).ResultsDescription of specimensAdult specimens of Leptodactylus guianensis from Colombia (Figure 1) have a snout-ventlength (SVL) in females of 73.25–90.70 mm, x = 82.97 mm, n = 5, and in males of78.70–104 mm, x = 90.36 mm, n = 4; and the SVL of the one juvenile was 69.65 mm. Twoof the specimens examined correspond to adult males, one with hypertrophied armsFigure 1. Adult female (SINCHI-A 3318) of Leptodactylus guianensis.578 M. OSORNO MUÑOZ ET AL.and distinct (fully developed) thumb spines (SINCHI-A 3320) and the second one(SINCHI-A 3321) with non-hypertrophied arms and thumb spines that are not fullykeratinised. Vomerine teeth are arranged in two arches found posteriorly and slightlymedially to the choanae. Tympana are distinct; in adult males, the rim of the tympanum(edge of underlying tympanic ring) bears small tubercles (during the breeding seasonthey may be keratinised); small tubercles are also found on the area between thetympanum and the eye and may be present on the supratympanic fold (Figure 2(d)).Finger lengths in increasing order are V < III < II < IV; all fingers have lateral fleshy ridgeswhich are less defined on finger V; ridges of fingers III and IV have abundant andkeratinised spines (the spines are less abundant and not keratinised in females); smallkeratinised spines are also found on the laterodorsal surfaces of fingers II, III, and IV, butare scarce on finger II; no spines were found on the laterodorsal surface of fingers onfemales. Subarticular tubercles large, rounded and distinct; thenar tubercle large, slightlyFigure 2. Adult males of (a,b) Leptodactylus bolivianus SINCHI-A 2335: (a) non-conical, square, andchisel-shaped thumb spine; (b) tympanum without tubercles; and (c,d) Leptodactylus guianensisSINCHI-A 2453: (c) conical, slightly chisel-shaped thumb spine, (d) tympanum and tympanic regionwith tubercles.JOURNAL OF NATURAL HISTORY 579triangular with apex towards the wrist and narrowly separated from the palmar tubercle;palmar tubercle large and rounded with outer margin slightly bifid.Breeding males with keratinised thumb spines that are overall conical and slightlychisel shaped distally (Figure 2(c)), usually ending in two or three very small cusps. Onemale (SINCHI-A 3320) shows a central patch of keratinised spines on chest. Toe lengthsin increasing order are I < II < V < III < IV; toes with distinct lateral fleshy ridges thatbasally form the interdigital membrane; ulnar ridge distinct, extending almost the entirelength of the tarsus and reaching the base of an elongated inner metatarsal tubercle,outer metatarsal tubercle smaller (about 50–55% the length of inner tubercle), roundedto slightly triangular (wider distally), tarsal ridge and tarsus scattered with small tuber-cles, of variable size, with keratinised tips and extending over the ventral surface ofmetatarsal element; these small tubercles are more abundant in males. Texture of theanterior 2/3 of the body is smooth; from the anterior tip of the ilium and over the dorsalsurfaces of thigh and shank, the skin is scattered with tubercles (larger on the legs thanon the posterior dorsal body). Dorsal folds absent; dorsolateral folds complete, extend-ing from posterior eye to groin; lateral fold present continuous or interrupted. Anelongated gland is found above the insertion of the arm; it is continuous with thecommissural gland, but it differs from the latter by its brownish, darker colouration. Thecolouration of the throat ranges from almost homogeneously grey to a mottled pattern(with mottling of varying sizes); the mottled pattern on the chest and ventral surface ofthe arms is continuous on the belly (mottling becomes scarce on mid- and posteriorbelly), ventral surface of thighs varies from entirely mottled to mottled only close to theedges, or non-mottled; posterior surface of thighs mottled. Colouration of dorsum (i.e.between dorsolateral folds) lighter than lateral body colouration; a large, triangularinterorbital marking extends from the eyes posteriorly on the dorsum, gradually narrow-ing and usually ending in a truncated apex (posterior width about 1/3 of the anteriormargin), immediately behind a light coloured spot that is rounded to oval; dorsalsurfaces of thighs and shanks with distinct dark brown bars; a dark band extends overthe posterior surface of the arm from the insertion of the arm-body to the elbow; snoutis rounded in dorsal and lateral views; light stripe on upper lip, extending from belowthe eye and continuous over the elongated commissural gland, which is always lightcoloured; dark band from anterior edge of eye, reaching the tip of the snout; canthusrostralis indistinct, tympanum distinct. A distinct, dark-coloured supratympanic foldextending from the posterior corner of the eye, running above the tympanum, andcurving ventrally to reach the posterior end of the commissural gland.DiscussionAmong species in the L. latrans group, breeding males of only L. bolivianus, L. guianensis,and L. viridis have a single keratinised thumb spine (two thumb spines in all otherspecies). Consequently, L. guianensis can be differentiated from all species in theL. latrans species group possessing two thumb spines in breeding males. The thumbspine of only one species in the L. latrans group has not been reported, L. macrosternum.However, previous work suggested that the taxonomic status of L. macrosternum is notclear and the distribution was restricted to the type locality (de Sá et al. 2014), whichmakes L. guianensis allopatric with L. macrosternum [Leptodactylus macrosternum580 M. OSORNO MUÑOZ ET AL.Miranda-Ribeiro, 1926, type locality: Bahia, Brazil (subsequently restricted to Salvador,Bahia, Brazil, by Bokermann 1966)]. A wide allopatric distribution is also observedbetween L. guianensis and L. viridis Jim and Spirandeli-Cruz, 1973 (1979), another specieswith a single thumb spine (type locality: Fazenda Pedra Branca, Município de Itajibá,Bahia State, Brazil). Consequently, our comparison suggests that adult specimens ofL. guianensis with fully developed secondary sexual traits collected from Colombia canonly be confused with L. bolivianus.Leptodactylus guianensis is a medium- to large-sized species within the L. latransspecies group. Although specimens from Colombia fit within the size range reportedfor L. guianensis, morphometric data are not useful to differentiate the species fromL. bolivianus (females: SVL 61.2–107.7 mm, x = 85.3 mm; males: SVL 79.0–121.5 mm, x =104.6 mm; L. guianensis: females: SVL 66.0–109.2 mm, x = 88.2 mm; males: SVL79.5–109.5 mm, x = 94.8 mm) (Heyer and de Sá 2011). Adult breeding males ofL. guianensis and L. bolivianus can be unequivocally distinguished by the presence ofa single and slightly chisel-shaped thumb spine in L. guianensis (Heyer and de Sá 2011).Furthermore, the single spine in L. guianensis is overall conical in shape, whereas that ofL. bolivianus is square (Figure 2(a,c), also see Heyer and de Sá 2011). The presence oftubercles on the rim of the tympanum and surrounding area in in males L. guianensis,absent in L. bolivianus, also helps to differentiate the two species (Figure 2(b,d)). Othercharacters are less reliable due to variation in populations (Heyer and de Sá 2011).Leptodactylus bolivianus was reported to have a white stripe on the upper lips extendingfrom the snout to the commissural gland, whereas in L. guianensis it extends from belowthe eye to the commissural gland. The appearance of the posterior thigh of L. bolivianusranges from mostly uniform to a moderately mottled pattern, whereas in L. guianensisthe posterior thighs show a boldly mottled pattern with larger irregular spots on a darkbackground. Although the latter two characters show some variation within each of thespecies, they are useful in combination with the thumb spine and characteristics of thetympanum’s rim. One trait that needs additional observations, on adult males during thebreeding season, is the presence of patches of chest spines. Leptodactylus guianensis andL. bolivianus were reported to possess a central patch of keratinised spines and twolateral tubercles on the chest (Heyer and de Sá 2011). We found only a central patch ofkeratinised chest spines on one individual of L. guianensis (SINCHI-A 3320) which exhibitsall other traits expected of an adult male during a breeding period; the second male weexamined (SINCHI-A 3321) is an adult male that had not yet fully reached the breedingstage (e.g. conical, thumb spine is not fully keratinised and chest spines not visible). Thelargest male examined (SINCHI-A 2453) has a central and a smaller lateral patch of chestspines on either side. We also observed a central patch of chest spines in the largebreeding male of L. bolivianus we examined (SINCHI-A 2335). The development ofsecondary characters (e.g. chest spines) may be variable with the age, size, and endo-crine stage of the individual; consequently, they need to be assessed carefully whenbeing used to identify species.Larval stages and the advertisement call of Leptodactylus guianensis have not beenreported. In Colombia, Leptodactylus guianensis is reported from the geologicalformation of the Guiana Shield (Gibbs and Barron 1993; Hollowell and Reynolds2005). The species occurs in the Departments of Guainía and Vichada (Figure 3;Appendix).JOURNAL OF NATURAL HISTORY 581The specimens we collected were active at night, moving on the ground in floodedforest areas and close to the Amazonian whitewater rivers Guaviare and Orinoco.Sampling occurred during the rainy season and in partially flooded forests; specimenswere found on top of floating logs or in dry areas of riverbeds. The examined specimenof L. bolivianus was collected from the same locality as at least one individual ofL. guianensis (SINCHI-A 2453).AcknowledgementsThe authors thank the local communities (Carrizal and communities of Matavén, sector CañoFruta) for allowing and participating in the SINCHI Biological Inventories, and Leonel Naranjo andJoel Ganeden for support with fieldwork. We thank Sonia Sua, SINCHI, for assistance with thedistribution map. This research was done under the Scientific Cooperation Agreement betweenthe Instituto Amazónico de Investigaciones Científicas SINCHI and the University of Richmond.Rafael O. de Sá was supported by a Fulbright Award to Colombia. We appreciate comments fromtwo anonymous reviewers and from Dr Jeffrey Streicher.Disclosure statementNo potential conflict of interest was reported by the authors.Figure 3. Triangles denote the reported distribution of Leptodactylus guianensis in Colombia.582 M. OSORNO MUÑOZ ET AL.FundingThis work was supported by a Fulbright US–Colombia Award.ReferencesBarbour T. 1906. Vertebrata from the savanna of Panamá. Reptilia and amphibia. Bull Mus CompZool Harv Coll. 46:224–229.Bokermann WCA. 1966. Lista Anotada das Localidades Tipo de Anfíbios Brasileiros. São Paulo:Serviço de Documentação - RUSP; p. 183.Boulenger GA. 1898. A list of the reptiles and batrachians collected by the late Prof. L. Balzan inBolivia. Ann Mus Civ Storia Nat Genova ser 2. XIX:128–133.Cei JM. 1950. Leptodactylus chaquensis n. sp. y el valor sistemático real de la especie linneanaLeptodactylus ocellatus en la Argentina. Acta Zool Lill. 9:395–423+ 3 Plates.Cole CJ, Townsend CR, Reynolds RP, MacCulloch RD, Lathrop A. 2013. Amphibians and reptiles ofGuyana, South America: illustrated keys, annotated species accounts, and a biogeographicsynopsis. Proc Biol Soc Washington. 125(4):317–620. doi:10.2988/0006-324X-125.4.317de Sá RO, Grant T, Camargo A, Heyer WR, Ponssa ML, Stanley E. 2014. Systematics of theneotropical genus Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae): phylogeny, the rele-vance of non-molecular evidence, and species accounts. S Amer J of Herp. 9(s1):S1–S100.doi:10.2994/sajh-d-13-00022.1Fitzinger LJ. 1826. Neue Classification der Reptilien nach ihren Natürlichen Verwandtschaftennebst einer Verwandtschafts - Tafel und einem Verzeichnisse der Reptilien - Sammlung desK. K. Zoologischen Museum‘s zu Wien. Wien: J. G. Heubner; p. 66.Frost DR. 2011. Amphibians species of the world: an online reference. Version 5.5. New York (USA):Am Mus Nat Hist. Electronic data base accessible at http://research.amnh/herpetology/amphibinas/index.htl.Gibbs AK, Barron CN, eds. 1993. The Geology of the Guiana Shield. Oxford (UK): Oxford UniversityPress.Heyer WR. 1969. Studies on the genus Leptodactylus (Amphibia, Leptodactylidae). III. A redefinitionof the genus Leptodactylus and a description of a new genus of leptodactylid frogs. Cont Sci, LosAngeles County Mus Nat Hist. 155:1–14.Heyer WR, de Sá RO. 2011. Variation, systematics, and relationships of the Leptodactylus bolivianuscomplex (Amphibia: Anura: Leptodactylidae). Smith Cont Zool. 635:1–58.Hollowell T, Reynolds RP. 2005. Checklist of the terrestrial vertebrates of the guiana shield. BullBiolog Soc Washington. 13:1–98. doi:10.2988/0097-0298(2005)13[1:I]2.0.CO;2Jim J, Spirandeli-Cruz EF. 1973. Uma nova espécie de Leptodactylus da Bahia, Brasil (Amphibia,Anura). [Abstract]. An Jor Cient Fac Ciênc Mêd Biol Botucatu. 3:13.Jim J, Spirandeli-Cruz EF. 1979. Uma nova espécie de Leptodactylus do Estado da Bahia, Brasil(Amphibia, Anura). Rev Bras Biol. 39:707–710.Larson P, de Sá RO. 1998. Chondrocranial morphology of Leptodactylus larvae (Leptodactylidae:Leptodactylinae): its utility in phylogenetic reconstruction. J Morp. 238:287–305. doi:10.1002/(SICI)1097-4687(199812)238:3<287::AID-JMOR2>3.0.CO;2-8McCranie JR, Wilson LD, Porras L. 1980. A new species of Leptodactylus from the cloud forests ofHonduras. J Herp. 14:361–367. doi:10.2307/1563691Miranda-Ribeiro A. 1926. Notas para servirem ao estudo dos Gymnobatrachios (Anura) Brasileiros.Tomo primeiro. Arc Mus Nac. 27:1–227+ 22 plates.Steffen GA. 1815. De Ranis Nonnullis. Observationes Anatomicae. Berlin: Joannis Friderici Starckii;p. 24 pp + 1 plate.JOURNAL OF NATURAL HISTORY 583Appendix. Voucher specimens and locality dataLeptodactylus guianensis SINCHI-A 3318–23, 5200, 5225, Department of Vichada, Municipio Cumaribo(4.417°N, 68.2°W); SINCHI-A 2453,Department ofGuainía,Municipio Inírida (3.56°N, 68.07°W); ICN46855Department of Amazonas, Municipio Leticia, Lago Yaguarcaca (4.183° N, 69.95° W).Leptodactylus bolivianus SINCHI-A 2335, Department of Guainía, Municipio Inírida (3.933° N, 68.117° W).584 M. OSORNO MUÑOZ ET AL.Copyright of Journal of Natural History is the property of Taylor & Francis Ltd and itscontent may not be copied or emailed to multiple sites or posted to a listserv without thecopyright holder's express written permission. However, users may print, download, or emailarticles for individual use.

Presence and Distribution of Leptodactylus Guianensis Heyer and de Sa, 2011 in Colombia: Comparisons with Other Species in the L. Latrans Group.

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Presence and Distribution of Leptodactylus Guianensis Heyer and de Sa, 2011 in Colombia: Comparisons with Other Species in the L. Latrans Group.

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