A new cryptic species of Pithecopus (Anura, Phyllomedusidae) in north-eastern Brazil
Abstract
The genus of Neotropical frogs Pithecopus includes 11 species occurring east of the Andes from southern Venezuela to northern Argentina. Recent genetic approaches pointed out an unusual genetic diversity among populations from localities in north-eastern Brazil recognized as P. nordestinus. In fact, one of these studies confirmed the hypothesis that the São Francisco River acted as an effective geographical barrier during vicariant events in the evolutionary history of P. nordestinus, resulting in two principal, highly divergent clades. Herein we formally describe this divergent clade as a new cryptic species of Pithecopus from north-eastern Brazil, the sister clade of P. nordestinus. It differs from other species of Pithecopus, except for P. azureus and P. nordestinus, by its small body size, lack of the reticulate pattern on flanks, smaller head width, and advertisement calls generally composed of a three-pulsed core.
References
Antoniazzi M.M., Neves P.R., Mailho-Fontana P.L., Rodrigues M.T. & Jared C. 2013. Morphology of the parotoid macroglands in Phyllomedusa leaf frogs. Journal of Zoology 291 (1): 42–50. https://doi.org/10.1111/jzo.12044
Bickford D., Lohman D.J., Sodhi N.S., Ng P.K.L., Meier R., Winker K., Ingram K.K. & Das I. 2007. Cryptic species as a window on diversity and conservation. TRENDS in Ecology and Evolution 22 (3): 148–155. https://doi.org/10.1016/j.tree.2006.11.004
Bioacoustics Research Program. 2014. Raven Pro: Interactive Sound Analysis Software, version 1.5. The Cornell Lab of Ornithology, Ithaca, New York. Available from http://www.birds.cornell.edu/raven [accessed 5 Feb. 2015].
Bokermann W.C.A. 1965. Três novos batráquios da região central de Mato Grosso. Brazilian Journal of Biology 25: 257–264.
Brand G.D., Santos R.C., Arake L.M., Silva V.G., Veras L.M.C., Costa V., Costa C.H.N., Kuckelhaus S.S., Alexandre J.G., Feio M.J. & Leite J.R.S.A. 2013. The skin decretion of the amphibian Phyllomedusa nordestina: a source of antimicrobial and antiprotozoal peptides. Molecules 18: 7058–7070. https://doi.org/10.3390/molecules18067058
Brandão R.A. 2002. A new species of Phyllomedusa Wagler, 1830 (Anura: Hylidae) from central Brazil. Journal of Herpetology 36 (4): 571–578. https://doi.org/10.2307/1565926
Brandão R.A. & Álvares G.F.R. 2009. Remarks on a new Phyllomedusa Wagler (Anura: Hylidae) with reticulated pattern on flanks from Southeastern Brazil. Zootaxa 2044: 61–64. https://doi.org/10.11646/zootaxa.2044.1.4
Brandão R.A., Álvares G.F.R., Crema A. & Zerbini G.J. 2009. Natural history of Phyllomedusa centralis Bokermann 1965 (Anura: Hylidae: Phyllomedusinae): tadpole and calls. South American Journal of Herpetology 4: 61–68. https://doi.org/10.2994/057.004.0108
Bruschi D.P., Busin C.S., Toledo L.F., Vasconcellos G.A., Strussmann C., Weber L.N., Lima A.P., Lima J.D. & Recco-Pimentel S.M. 2013. Evaluation of the taxonomic status of populations assigned to Phyllomedusa hypochondrialis (Anura, Hylidae, Phyllomedusinae) based on molecular, chromosomal, and morphological approach. Genetics 14 (70): 1–14. https://doi.org/10.1186/1471-2156-14-70
Bruschi D.P., Lucas E.M., Garcia P.C. & Recco-Pimentel S.M. 2014. Molecular and morphological evidence reveals a new species in the Phyllomedusa hypochondrialis group (Hylidae, Phyllomedusinae) from the Atlantic Forest of the highlands of southern Brazil. PloS ONE 9 (8): e105608. https://doi.org/10.1371/journal.pone.0105608
Bruschi D.P, Peres E.A., Lourenço L.B., Bartoleti L.F.M., Sobral-Souza T. & Recco-Pimentel S.M. 2019. Signature of the paleo-course changes in the São Francisco River as source of genetic structure in Neotropical Pithecopus nordestinus (Phyllomedusinae, Anura) treefrog. Frontiers in Genetics 10: 728. https://doi.org/10.3389/fgene.2019.00728
Caramaschi U. 2006. Redefinição do grupo de Phyllomedusa hypochondrialis, com redescrição de P. megacephala (Miranda-Ribeiro, 1926), revalidação de P. azurea Cope, 1862 e descrição de uma nova espécie (Amphibia, Anura, Hylidae). Archivos do Museu Nacional do Rio de Janeiro 64 (2): 159–179.
Chen S.Y., Feng Z. & Yi X. 2017. A general introduction to adjustment for multiple comparisons. Journal of Thoracic Disease 9 (6): 1725–1729. https://doi.org/10.21037/jtd.2017.05.34
Clemente-Carvalho R.B.G., Giaretta A.A., Condez T.H., Haddad C.F.B. & Reis S.F.D. 2012. A new species of miniaturized toadlet, genus Brachycephalus (Anura: Brachycephalidae), from the Atlantic Forest of southeastern Brazil. Herpetologica 68 (3): 365–374. https://doi.org/10.1655/HERPETOLOGICA-D-11-00085.1
de Queiroz K. 1998. The general lineage concept of species, species criteria, and the process of speciation and terminological recommendations. In: Howard D.J. & Berlocher S.H. (eds) Endless Forms: Species and Speciation: 57–75. Oxford University Press, Oxford.
de Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56 (6): 879–886. https://doi.org/10.1080/10635150701701083
Dubeux M.J.M., Silva G.R.S., Nascimento F.A.C., Gonçalves U. & Mott T. 2019. Síntese histórica e avanços no conhecimento de girinos (Amphibia: Anura) no estado do Alagoas, nordeste do Brasil. Revista Nordestina de Zoologia 12: 18–52.
Dubeux M.J.M, Nascimento F.A.C., Lima L.R., Magalhães F.M., Silva I.R., Gonçalves U., Almeida J.P.F., Correia L.L., Garda A.A., Mesquita D.O., Rossa-Feres D.C. & Mott T. 2020. Morphological characterization and taxonomic key of tadpoles (Amphibia: Anura) from the northern region of the Atlantic Forest. Biota Neotropica 20 (2): e20180718. https://doi.org/10.1590/1676-0611-BN-2018-0718
Duellman W.E. 1970. The Hylid Frogs of Middle America. Vol. 1. Monograph of the Museum of Natural History 1, University of Kansas, Lawrence. https://doi.org/10.5962/bhl.title.2835
Duellman W.E., Marion A.B. & Hedges S.B. 2016. Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa 4104 (1): 001–109. https://doi.org/10.11646/zootaxa.4104.1.1
Drummond A.J., Suchard M.A. & Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29 (8): 1969–1973. https://doi.org/10.1093/molbev/mss075
Ezard T.H.G., Fujisawa T.E. & Barraclough T.G. 2014. splits: SPeciesʼ LImits by Threshold Statistics. R package version 1.0-19/r51. Available from https://R-Forge.R-project.org/projects/splits/ [assessed 21 Mar. 2020].
Faivovich J., Haddad C.F.B., Baêta D., Jungferd K.H., Alvares G.F.R., Brandão R.A., Sheil C., Barrientos L.S., Barrio-Amorós C.L., Cruz C.A.G. & Wheeler W.C. 2010. The phylogenetic relationships of the charismatic poster frogs, Phyllomedusinae (Anura, Hylidae). Cladistics 26 (3): 227–261. https://doi.org/10.1111/j.1096-0031.2009.00287.x
Fišer C., Robinson C.T. & Malard F. 2018. Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27 (3): 613–635. https://doi.org/10.1111/mec.14486
Fontaneto D., Herniou E., Boschetti C., Caprioli M., Melone G., Ricci C. & Barraclough T.G. 2007. Independently evolving species in asexual bdelloid rotifers. Plos Biology 5: e87. https://doi.org/10.1371/journal.pbio.0050087
Frost D.R. 2020. Amphibian Species of the World: an Online Reference. Ver. 6.0. American Museum of Natural History, New York. Available from http://research.amnh.org/herpetology/amphibia/index.html [accessed 3 Apr. 2020].
Haddad C.F.B. & Prado C.P. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55 (3): 207–217. https://doi.org/10.1641/0006-3568(2005)055[0207:RMIFAT]2.0.CO;2
Haddad C.F.B., Toledo L.F., Prado C.P.A., Loebmann D., Gasparini J.L. & Sazima I. 2013. Guide to the Amphibians of the Atlantic Forest: Diversity and Biology. First Edition. Anolis Books, São Paulo.
Haga I.A., Andrade F.S., Bruschi D.P., Recco-Pimentel S.M. & Giaretta A.A. 2017a. Unrevealing the leaf frogs Cerrado diversity: a new species of Pithecopus (Anura, Arboranae, Phyllomedusidae) from the Mato Grosso state, Brazil. PLoS ONE 12 (9): e0184631. https://doi.org/10.1371/journal.pone.0184631
Haga I.A., Carvalho T.R., Andrade F.S. & Giaretta A.A. 2017b. Advertisement and aggressive calls of Pithecopus azureus (Anura: Phyllomedusidae) from the border of Brazil and Paraguay. Phyllomedusa 16 (1): 47–56. https://doi.org/10.11606/issn.2316-9079.v16i1p47-56
Huelsenbeck J.P. & Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Hothorn T., Hornik K., Van de Wiel M.A. & Zeileis A. 2008. Implementing a class of permutation tests: the coin package. Journal of Statistical Software 28 (8): 1–23. https://doi.org/10.18637/jss.v028.i08
Jombart T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T. & Ahmed I. 2011. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27 (21): 3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jombart T., Devillard S. & Balloux F. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. Genetics 11: 1–15. https://doi.org/10.1186/1471-2156-11-94
Köhler J. & Lötters S. 1999. Annotated list of amphibian records from the Departamento Pando, Bolivia, with description of some advertisement calls. Bonner zoologische Beiträge 48: 259–273.
Köhler J., Jansen M., Rodríguez A., Kok P.J.R., Toledo L.F., Emmrich M., Glaw F., Haddad C.F.B., Rödel M.O. & Vences M. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251: 1–124. https://doi.org/10.11646/zootaxa.4251.1.1
Korkmaz S., Goksuluk D. & Zararsiz G. 2014. MVN: an R package for assessing multivariate normality. The R Journal 6 (2): 151–163. https://doi.org/10.32614/RJ-2014-031
Kozlov A.M., Darriba D., Flouri T., Morel B. & Stamatakis A. 2019. RAxML-NG: a fast, scalable, and user-friendly tool for maximum likelihood phylogenetics inference. Bioinformatics 35 (21): 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Kumar S., Stecher G., Li M., Knyas C. & Tamura K. 2018. MEGA X: Molecular genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547–1549. https://doi.org/10.1093/molbev/msy096
Lee J. 2009. The São Francisco River Transposition Project: friend or foe to the Brazilian people. Law and Business Review of the Americas 15: 425–434.
Liaw A. & Wiener M. 2002. Classification and regression by randomForest. R News 2 (3): 18–22.
Ligges U., Krey S., Mersmann O. & Schnackenberg S. 2018. tuneR: Analysis of Music and Speech. Available from https://CRAN.R-project.org/package=tuneR [accessed 1 Jul. 2018].
Loebmann D. & Haddad C.F.B. 2010. Amphibians and reptiles from a highly diverse area of the Caatinga domain: composition and conservation implications. Biota Neotropica 10 (3): 227–256. https://doi.org/10.1590/S1676-06032010000300026
Lutz B. 1966. Pithecopus ayeaye, a new Brazilian hylid with vertical pupils and grasping feet. Copeia 48: 236–240. https://doi.org/10.2307/1441130
Neiva M., Vargas D.C., Conceição K., Rádis-Baptita G., Assakura M.T., Jared C. & Hayashi M.A.F. 2013. Gene expression analysis by ESTs sequencing of the Brazilian frog Phyllomedusa nordestina skin glands. Toxicon 61: 139–150. https://doi.org/10.1016/j.toxicon.2012.10.016
Paradis E. & Schliep K. 2018. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528. https://doi.org/10.1093/bioinformatics/bty633
Pfennig D.W. & Pfennig K.S. 2010. Character displacement and the origins of diversity. The American Naturalist 176: S26–S44. https://doi.org/10.1086/657056
Pinto E.G., Pimenta D.C., Antoniazzi M.M., Jared C. & Tempone A.G. 2013. Antimicrobial peptides isolated from Phyllomedusa nordestina (Amphibia) alter the permeability of plasma membrane of Leishmania and Trypanosoma cruzi. Experimental Parasitology 135: 655–660. https://doi.org/10.1016/j.exppara.2013.09.016
Pohar M., Blas M. & Turk S. 2004. Comparison of logistic regression and linear discriminant analysis: a simulation study. Metodološki zvezki 1 (1): 143–161.
Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P. & Hazell S. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609. https://doi.org/10.1080/10635150600852011
R Core Team. 2017. R: a Language and Environment for Statistical Computing. Ver. 3.1.2. R Foundation for Statistical Computing, Vienna. Available from http://www.R-project.org/ [accessed 1 Jul. 2017].
Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbio/syy032
RIMA – Relatório de Impacto Ambiental. 2004. Projeto de Integração do Rio São Francisco com Bacias Hidrográficas do Nordeste Setentrional. Ministério da Integração Nacional. Available from https://antigo.mdr.gov.br/images/stories/ProjetoRioSaoFrancisco/ArquivosPDF/documentostecnicos/RIMAJULHO2004.pdf [accessed 5 Oct. 2015].
Roberto I.J. & Loebmann D. 2016. Composition, distribution patterns, and conservation priority areas for the herpetofauna of the state of Ceará, northeastern Brazil. Salamandra 52 (2): 134–152.
Röhr D.L., Guimarães F.C.A., Martinez P.A., Mobley R.S.S., Juncá F.A. & Garda A.A. 2020. Habitat-dependent advertisement call variation in the monkey frog Phyllomedusa nordestina. Ethology 126 (6): 651–659. https://doi.org/10.1111/eth.13017
Silva G.R., dos Santos C.L., Alves M.R., de Sousa S.D.V. & Annunziata B.B. 2010. Anfíbios das dunas litorâneas do extremo norte do Estado do Piauí, Brasil. Sitientibus. Série Ciências Biológicas 7 (4): 334–340.
Silva F.P., Fernandes-Ferreira H., Montes M.A. & Silva L.G. 2020. Distribution modeling applied to deficient data species assessment: a case study with Pithecopus nordestinus (Anura, Phyllomedusidae). Neotropical Biology and Conservation 15: 165–175. https://doi.org/10.3897/neotropical.15.e47426
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
Toledo L.F. & Batista R.F. 2012. Integrative study of Brazilian anurans: relationship between geographic distribution, size, environment, taxonomy, and conservation. Biotropica 44 (6): 785–792. https://doi.org/10.1111/j.1744-7429.2012.00866.x
Toledo L.F., Martins I.A., Bruschi D.P., Passos M.A., Alexandre C. & Haddad C.F.B. 2015. The anuran calling repertoire in the light of social context. Acta Ethologica 18 (2): 87–99. https://doi.org/10.1007/s10211-014-0194-4
Valencia-Aguilar A., Ruano-Fajardo G., Lambertini C., Leite D.S., Toledo L.F. & Mott T. 2015. The chytrid fungus acts as a generalist pathogen that infects species-rich amphibian families in Brazilian rainforests. Diseases of Aquatic Organisms 114 (1): 61–67. https://doi.org/10.3354/dao02845
Vilaça T., Silva J.R.S. & Solé M. 2011. Vocalization and territorial behaviour of Phyllomedusa nordestina Caramaschi, 2006 (Anura: Hylidae) from southern Bahia, Brazil. Journal of Natural History 45 (29–30): 1823–1834. https://doi.org/10.1080/00222933.2011.561018
Watters J.L., Cummings S.T., Flanagan R.L. & Siler C.D. 2016. Review of morphometric measurements used in anuran species descriptions and recommendations for a standardized approach. Zootaxa 4072 (4): 477–495. https://doi.org/10.11646/zootaxa.4072.4.6
Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876. https://doi.org/10.1093/bioinformatics/btt499
Copyright (c) 2020 Felipe Silva de Andrade, Isabelle Aquemi Haga, Johnny Sousa Ferreira, Shirlei Maria Recco-Pimentel, Luís Felipe Toledo, Daniel Pacheco Bruschi
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.