Redescription of Adenomera diptyx (Boettger, 1885) (Anura, Leptodactylidae) and description of a closely related new species
Abstract
Adenomera is a genus of Neotropical leaf-litter frogs widely distributed in South America and regarded taxonomic-wise challenging. One of these is the open-habitat Adenomera diptyx from Paraguay, which may correspond to a species complex. An integrative analysis of morphological variation, in combination with acoustic and molecular data of several populations from Argentina, Paraguay, and Brazil resulted in the recharacterization of nominal A. diptyx and the description of a new, closely related species. Adenomera diptyx is recognized by its advertisement call given at a high repetition rate (176–299 per minute), and the dorsal color pattern consisting of a light mid-dorsal line and a dark brown interorbital bar with irregular black edges. In comparison with A. diptyx, the new species, Adenomera guarani sp. nov., produces its advertisement call at a lower repetition rate (73–147 per minute), and the dorsal color pattern consists of a light, broad, mid-dorsal stripe and a mask-like patch in the interorbital region. The redefinition of A. diptyx will contribute to future studies focusing on the taxonomic status of other genetic lineages tentatively assigned to this species complex, which could represent additional unnamed species in the open-habitat Adenomera clade.
References
Airaldi Wood K., Lavilla E.O. & Garcete-Barrett B.R. 2013. Anuros de la Reserva de Recursos Manejados Ybyturuzú. Un enfoque sobre su estado de conservación. Reportes Científicos de la FACEN 4: 21–33.
Aljanabi S.M. & Martinez I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR based techniques. Nucleic Acids Research 25: 4692–4693. https://doi.org/10.1093/nar/25.22.4692
Almeida A.P. & Angulo A. 2006. A new species of Leptodactylus (Anura: Leptodactylidae) from the state of Espírito Santo, Brazil, with remarks on the systematics of associated populations. Zootaxa 1334 (1): 1–25. https://doi.org/10.11646/zootaxa.1334.1.1
Angulo A. & Icochea J. 2010. Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura, Leptodactylidae). Systematics and Biodiversity 8 (3): 357–370. https://doi.org/10.1080/14772000.2010.507264
Angulo A. & Reichle S. 2008. Acoustic signal, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society 152 (1): 59–77. https://doi.org/10.1111/j.1096-3642.2007.00338.x
Angulo A., Cocroft R.B. & Reichle S. 2003. Species identity in the genus Adenomera (Anura: Leptodactylidae) in Southeastern Peru. Herpetologica 59 (4): 490–504. https://doi.org/10.1655/20-104
Audacity Team. 2017. Audacity(R): Free Audio Editor and Recorder. Ver. 2.1.1. Available from https://audacityteam.org [accessed 5 May 2018].
Berneck B.V.M., Costa C.O.R. & Garcia P.C.A. 2008. A new species of Leptodactylus (Anura: Leptodactylidae) from the Atlantic Forest of São Paulo State, Brazil. Zootaxa 1795 (1): 46–56. https://doi.org/10.11646/zootaxa.1795.1.3
Boettger O. 1885. Liste von Reptilien und Batrachiern aus Paraguay. Zeitschrift für Naturwissenschaften 58: 213–248. Available from https://www.biodiversitylibrary.org/page/31401231 [accessed 31 May. 2023].
Boettger O. 1892. Kriechthiere der Kaukasusländer, gesammelt durch die Radde-Valentin’sche Expedition nach dem Karabagh und durch die Herren Dr. J. Valentin un P. Reibisch. Bericht über die Senckenbergische Naturforschende Gesellschaft 1892: 131–150.
Boistel R., Massary J.C. & Angulo A. 2006. Description of a new species of the genus Adenomera (Amphibia, Anura, Leptodactylidae) from French Guiana. Acta Herpetologica 1 (1): 1–14. https://doi.org/10.13128/Acta_Herpetol-1249
Brusquetti F. & Lavilla E. 2006. Lista comentada de los anfibios de Paraguay. Cuadernos de Herpetología 20 (2): 3–79.
Carvalho T.R. & Giaretta A.A. 2013a. Taxonomic circumscription of Adenomera martinezi (Bokermann, 1956) (Anura: Leptodactylidae: Leptodactylinae) with the recognition of a new cryptic taxon through a bioacoustic approach. Zootaxa 3701 (2): 207–237. https://doi.org/10.11646/zootaxa.3701.2.5
Carvalho T.R. & Giaretta A.A. 2013b. Bioacoustics reveals two new syntopic species of Adenomera Steindachner (Anura: Leptodactylidae: Leptodactylinae) in the Cerrado of central Brazil. Zootaxa 3731 (3): 533–551. https://doi.org/10.11646/zootaxa.3731.4.6
Carvalho T.R., Giaretta A.A., Maciel N.M., Barrera D.A., Aguilar-Puntriano C., Haddad C.F.B., Kokubum M.N.C., Menin M. & Angulo A. 2019a. On the uncertain taxonomic identity of Adenomera hylaedactyla (Cope, 1868) and the composite type series of A. andreae (Müller, 1923) (Anura, Leptodactylidae). Copeia 107 (4): 708–723. https://doi.org/10.1643/CH-19-237
Carvalho T.R., Angulo A., Kokubum M.N.C., Barrera D.A., Souza M.B., Haddad C.F.B. & Giaretta A.A. 2019b. A new cryptic species of the Adenomera andreae clade from southwestern Amazonia (Anura, Leptodactylidae). Herpetologica 75 (3): 233–246. https://doi.org/10.1655/D-18-00049
Carvalho T.R., Giaretta A.A., Angulo A., Haddad C.F.B. & Peloso P.L.V. 2019c. A new Amazonian species of Adenomera (Anura: Leptodactylidae) from the Brazilian state of Para: a tody-tyrant voice in a frog. American Museum Novitates 3919:1–21 https://doi.org/10.1206/3919.1
Carvalho T.R., Cassini C.S., Taucce P.P.G. & Haddad C.F.B. 2019d. A new, morphologically cryptic species of Adenomera closely related to A. araucaria from the Atlantic Forest of southern Brazil (Anura, Leptodactylidae). Journal of Herpetology 53 (2): 131–143. https://doi.org/10.1670/18-172
Carvalho T.R., Angulo A., Barrera D.A., Aguilar-Puntriano C. & Haddad C.F.B. 2020a. Hiding in plain sight: a fourth new cryptic species of the Adenomera andreae clade (Anura: Leptodactylidae) from southwestern Amazonia. Herpetologica 76 (3): 304–314. https://doi.org/10.1655/HERPETOLOGICA-D-19-00068.1
Carvalho T.R., Moraes L.J.C.L., Angulo A., Werneck F.P., Icochea J. & Lima A.P. 2020b. New acoustic and molecular data shed light on the poorly known Amazonian frog Adenomera simonstuarti (Leptodactylidae): implications for distribution and conservation. European Journal of Taxonomy 682: 1–18. https://doi.org/10.5852/ejt.2020.682
Carvalho T.R., Simões P.I., Gagliardi-Urrutia G., Rojas-Runjaic F.J.M., Haddad C.F.B. & Castroviejo-Fisher S. 2020c. A new forest-dwelling frog species of the genus Adenomera (Leptodactylidae) from Northwestern Brazilian Amazonia. Copeia 108 (4): 924–937. https://doi.org/10.1643/CH-19-329
Carvalho T.R., Moraes Leandro J.C.L, Lima A.P., Fouquet A., Peloso P.L.V., Pavan D., Drummond L.O., Rodrigues M.T., Giaretta A.A., Gordo M., Neckel-Oliveira S. & Haddad C.F.B. 2021. Systematics and historical biogeography of Neotropical foam-nesting frogs of the Adenomera heyeri clade (Leptodactylidae), with the description of six new Amazonian species. Zoological Journal of the Linnean Society 191 (2): 395-433. https://doi.org/10.1093/zoolinnean/zlaa051
Cassini C.S., Taucce P.P.G., Carvalho T.R., Fouquet A., Solé M., Haddad C.F.B. & Garcia P.C.A. 2020. One step beyond a broad molecular phylogenetic analysis: species delimitation of Adenomera marmorata Steindachner, 1867 (Anura: Leptodactylidae). PLoS ONE 15 (2): e0229324 https://doi.org/10.1371/journal.pone.0229324
Cei J.M. 1956. Nueva lista sistemática de los batracios de Argentina y breves notas sobre su biología y ecología. Investigaciones Zoológicas Chilenas 3: 35–68.
Cei J. M. 1980. Amphibians of Argentina. Monitore Zoologico Italiano (NS), Monografia 2.
Cei, J.M. 1987. Additional notes to “Amphibians of Argentina”: an update, 1980-1986. Monitore Zoologico Italiano (NS) 21: 209–272.
Cochran D.M. 1955. Frogs of southeastern Brazil. Bulletin of the United States National Museum 206: 1–423. https://doi.org/10.5479/si.03629236.206.1
Cope E.D. 1868. An examination of the Reptilia and Batrachia obtained by the Orton Expedition to Equador and the Upper Amazon, with notes on other species. Proceedings of the Academy of Natural Sciences of Philadelphia 1868: 96–140. Available from https://www.biodiversitylibrary.org/page/9768245 [accessed 31 May 2023].
De la Riva I. 1995. A new reproductive mode for the genus Adenomera (Amphibia: Anura: Leptodactylidae): Taxonomic implications for certain Bolivian and Paraguayan populations. Studies on Neotropical Fauna and Environment 30 (1): 15–29. https://doi.org/10.1080/01650529509360937
De la Riva I. 1996. The specific name of Adenomera (Anura: Leptodactylidae) in the Paraguay River basin. Journal of Herpetology 30 (4): 556–558. https://doi.org/10.2307/1565706
Dinerstein, E., Olson, D., Joshi A., Vynne C., Burgess N.D., Wikramanayake E., Hahn N., Palminteri S., Hedao P., Noss R., Hansen M., Locke H., Ellis E.C, Jones B., Barber C.V., Hayes R., Kormos C., Martin V., Crist E., Sechrest W., Price L., Baillie J.E.M., Weeden D., Suckling K., Davis C., Sizer N., Moore R., Thau D., Birch T., Potapov P., Turubanova S., Tyukavina A., De Souza N., Pintea L., Brito J.C., Llewellyn O.A., Miller A.G., Patzelt A., Ghazanfar S.A., Timberlake J., Klöser H., Shennan-Farpón Y., Kindt R., Barnekow Lillesø J.-P., Van Breugel P., Graudal L., Voge M., Al-Shammari K.F. & Saleem M. 2017. An ecoregion-based approach to protecting half the terrestrial realm. BioScience 67 (6): 534–545. https://doi.org/10.1093/biosci/bix014
Duellman W.E. & Trueb L. 1994. Biology of Amphibians. The John Hopkins University Press, Baltimore, Maryland.
Faivovich J., Haddad C.F.B., Garcia P.C.A., Frost D.R., Campbell J.A. & Wheeler W.C. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletin American Museum Natural History 294: 1–240. https://doi.org/10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2
Fouquet A., Cassini C.S., Haddad C.F.B., Pech N. & Trefaut Rodrigues M. 2014. Species delimitation, patterns of diversification and historical biogeography of the Neotropical frog genus Adenomera (Anura, Leptodactylidae). Journal of Biogeography 41 (5): 855–870. https://doi.org/10.1111/jbi.12250
Freiberg M.A. 1942. Enumeración sistemática y distribución geográfica de los batracios argentinos. Physis 19 (52): 219–240.
Gallardo J.M. 1966. Zoogeografía de los anfibios chaqueños. Physis 26 (71): 67–81.
Gallardo J.M. 1986. La diversidad de la herpetofauna en la selva subtropical misionera. Actas X Congreso Latinoamericano de Zoología. Anales del Museo de Historia Natural de Valparaíso 17: 153–159.
Gallardo J.M. 1987a. Anfibios Argentinos. Guía para su Identificación. Biblioteca Mosaico, Buenos Aires.
Gallardo J.M. 1987b. Anfibios argentinos. Parte 1. Amphibia & Reptilia (Conservación) 1 (3): 60–66.
Gallardo J.M. & Varela de Olmedo E. 1992. Anfibios de la República Argentina: Ecología y Comportamiento. Fauna de agua dulce de la República Argentina 41 (1): 1–116.
Gavetti E. & Andreone F. 1993. Revised Catalogue of the Herpetological Collection in Turin University. I. Amphibia. Museo Regionale di Scienze Naturali, Cataloghi X, Torino.
Gelman A. & Rubin D.B. 1992. Inference from iterative simulation using multiple sequences. Statistical Sciences 7: 457–472.
Gorham S.W. 1966. Liste der rezenten Amphibien and Reptilien. Das Tierreich 85: 1–222.
Gorham S.W. 1974. Check-list of World Amphibians up to January 1, 1970. The New Brunswick Museum, St. John, Canadá.
Heyer W.R. 1973. Systematics of the marmoratus group of the frog genus Leptodactylus (Amphibia, Leptodactylidae). Contributions in Science, Los Angeles County Natural History Museum 251: 1–50. https://doi.org/10.5962/p.241234
Heyer W.R. 1975. Adenomera lutzi (Amphibia: Leptodactylidae), a new species of frog from Guyana. Proceedings of the Biological Society of Washington 88: 315–318. Available from https://www.biodiversitylibrary.org/page/34561319 [accessed 31 May 2023].
Heyer W.R & Silverstone P.A. 1969. The larva of the frog Leptodactylus hylaedactylus (Leptodactrylidae). Fieldiana Zoology 51 (11): 141–145. https://doi.org/10.5962/bhl.title.3047
Heyer W.R., Rand A.S., Cruz C.A.G., Peixoto O.L. & Nelson C.E. 1990. Frogs of Boracéia. Arquivos de Zoologia 31: 231–410.
Howell W.M. & Black D.A. 1980. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1- step method. Experientia 36: 1014–1015. https://doi.org/10.1007/BF01953855
Hurvich C. & Tsai C. 1989. Regression and time series model selection in small samples. Biometrika 76 (2): 297–307. https://doi.org/10.1093/biomet/76.2.297
Kok P.J.R., Kokubum M.N.C., MacCulloch R.D. & Lathrop A. 2007. Morphological variation in Leptodactylus lutzi (Anura, Leptodactylidae) with description of its advertisement call and notes on its courtship behavior. Phyllomedusa 6 (1): 45–60. https://doi.org/10.11606/issn.2316-9079.v6i1p45-60
Kokubum M.N.C. & Sousa M.B. 2008. Reproductive ecology of Leptodactylus aff. hylaedactylus (Anura, Leptodactylidae) from an open area in Northern Brazil. South American Journal of Herpetology 3: 15–21. https://doi.org/10.2994/1808-9798(2008)3[15:REOLAH]2.0.CO;2
Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093%2Fmolbev%2Fmsy096
Kwet A. 2007. Bioacoustic variation in the genus Adenomera in southern Brazil, with revalidation of Leptodactylus nanus Müller, 1922 (Anura: Leptodactylidae). Zoologische Reihe 83: 56–68. https://doi.org/10.1002/mmnz.200600027
Kwet A. & Angulo A. 2002. A new species of Adenomera (Anura, Leptodactylidae) from the Araucaria forest of Rio Grande do Sul (Brazil), with comments on the systematic status of southern populations of the genus. Alytes 20 (1–2): 28–43.
Kwet A., Steiner J. & Zillikens A. 2009. A new species of Adenomera (Amphibia: Anura: Leptodactylidae) from the Atlantic rain forest in Santa Catarina, southern Brazil. Studies on Neotropical Fauna and Environment 44 (2): 93–107. https://doi.org/10.1080/01650520902901659
Lanfear, R., Calcott, B., Ho, S. Y. & Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29 (6): 1695–1701. https://doi.org/10.1093/molbev/mss020
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34 (3): 772–773. https://doi.org/10.1093/molbev/msw260
Lavilla E.O. 1992. Tipos portadores de nombre y localidades tipo de anfibios de Argentina. Acta Zoológica Lilloana 42 (1): 61–100.
Lavilla E.O. & Cei J. M. 2001. Amphibians of Argentina, a Second Update, 1987-2000. Monitore Zoologico Italiano (NS) Monografie 28, Torino, Italia.
Ligges U., Krey S., Mersmann O. & Schnackenberg S. 2017. tuneR: Analysis of music and speech. Available from https://CRAN.R-project.org/package=tuneR [accessed 11 Jan. 2019].
Lyra M.L., Haddad C.F.B. & Azeredo-Espin A.M.L. 2017. Meeting the challenge of DNA barcoding Neotropical amphibians: Polymerase chain reaction optimization and new COI primers. Molecular Ecology Resources 17: 966–980. https://doi.org/10.1111/1755-0998.12648
Lutz A. 1930. Segunda memoria sobre especies brasileiras do genero Leptodactylus, incluindo outras alliadas. Memórias do Instituto Oswaldo Cruz 23 (1): 1–34. https://doi.org/10.1590/S0074-02761930000100001
Mcdiarmid R.W. & Foster M.S. 1987. Additions to the reptile fauna of Paraguay with notes on a small herpetological collection from Amambay. Studies on Neotropical Fauna and Environment 22 (1): 1–9. https://doi.org/10.1080/01650528709360714
Márquez R., De la Riva I. & Bosch J. 1995. Advertisement calls of Bolivian Leptodactylidae (Amphibia, Anura). Journal of Zoology 237: 313–336. https://doi.org/10.1111/j.1469-7998.1995.tb02765.x
Mercolli C., Yanosky A.A. & Dixon J.R. 1995. Natural history of Adenomera hylaedactyla (Anura: Leptodactylinae) in the eastern Chaco of Argentina. Bulletin of the Maryland Herpetological Society 31: 117–129.
Miller M.A., Pfeiffer W. & Schwartz T. 2011. The CIPRES science gateway: a community resource for phylogenetic analyses. Proceedings of the 2011 TeraGrid Conference: extreme digital discovery 41: 1–8. https://doi.org/10.1145/2016741.2016785
Milto K.D. 2010. On the identity of Bufo levicristatus Boettger, 1885. Russian Journal of Herpetology 17 (4): 257–258.
Moritz C., Schneider C.J. & Wake D.B. 1992. Evolutionary relationships within the Ensatina eschscholtzii complex confirm the ring species interpretation. Systematic Biology 41: 273–291. https://doi.org/10.1093/sysbio/41.3.273
Nieden F. 1923. Anura I Subordo Aglossa und Phaneroglossa. Sectio 1. Arcifera. Das Tierreich 46: i–xxxii + 1–584.
R Core Team 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/ [accessed 11 Jan. 2019].
Ronquist F., Teslenko M., Van Der Mark P., Ayres D. L., Darling A., Höhna, S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Schmid M. 1978. Chromosome banding in Amphibia I. Constitutive heterochromatin and nucleolus organizer regions in Bufo and Hyla. Chromosoma 66: 361–388. https://doi.org/10.1007/BF00328536
Sueur J., Aubin T. & Simonis C. 2008. Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18: 213–226. https://doi.org/10.1080/09524622.2008.9753600
Vaidya G., Lohman D.J. & Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27 (2): 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Yanosky A.A., Dixon J.R & Mercolli C. 1993. The herpetofauna of El Bagual Ecological Reserve (Formosa, Argentina) with comments on its herpetological collection. Bulletin of the Maryland Herpetological Society 29 (4): 160–171.
Zaracho V.H. & Hernando A.B. 2011. The karyotype of Adenomera diptyx (Boettger 1885) (Anura, Leptodactylidae) from northeastern Argentina. Genetics and Molecular Biology: 34 (1): 84–87. https://doi.org/10.1590/S1415-47572010005000116
Zaracho V.H. & Kokubum M.N.C. 2017. Reproduction and larval morphology of Adenomera diptyx (Anura: Leptodactylidae) from the Argentinean humid Chaco and Brazilian pantanal. Salamandra 53: 1–9.
Zaracho V.H. & Lamas M.F. 2008. Leptodactylus diptyx. Endoparasites. Natural History Notes. Herpetological Review 39 (3): 337.
Zaracho V.H., Acosta J.L. & Lamas M.F. 2012a. Dieta y parasitismo de Leptodactylus diptyx (Anura: Leptodactylidae) del nordeste argentino. Revista Mexicana de Biodiversidad 83: 1180–1186. https://doi.org/10.22201/ib.20078706e.2012.4.1016
Zaracho V.H., Schaefer E. & Duré M. 2012b. Leptodactylus diptyx (Boettger, 1885). In: Categorización del Estado de Conservación de la Herpetofauna de la República Argentina. Ficha de los Taxones. Anfibios. Cuadernos de Herpetología 26 (S1): 204.
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