Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 3620 No. 3: 7 Mar. 2013
Type: Articles
Published: 2013-03-07
DOI: 10.11646/zootaxa.3620.3.1
Page range: 301–350
Abstract views: 27
PDF downloaded: 1

Taxonomy of the super-cryptic Hyperolius nasutus group of long reed frogs of Africa (Anura: Hyperoliidae), with descriptions of six new species

Biodiversity and Conservation Biology Department, University of the Western Cape, Private Bag X17, Bellville, 7535, South Africa
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Herpetology, Invalidenstr. 43, 10115 Berlin, Germany Across the River – a Transboundary Peace Park for Sierra Leone and Liberia, The Royal Society for the Protection of Birds, 164 Dama Road, Kenema, Sierra Leone
Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Herpetology, Invalidenstr. 43, 10115 Berlin, Germany
Trier University, Biogeography Department, Universitätsring 15, 54295 Trier, Germany
Port Elizabeth Museum (Bayworld), P.O. Box 13147, Humewood, Port Elizabeth 6013, South Africa
Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Herpetology, Invalidenstr. 43, 10115 Berlin, Germany
Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085, USA
Institut für Integrierte Naturwissenschaften, Abteilung Biologie, Universität Koblenz-Landau, Universitätsstraße 1, 56070 Koblenz, Germany
School of Environmental; Sciences and Development, North-West University, Private Bag X6001, Potchefstroom 2531, South Africa
Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark
Biodiversity and Conservation Biology Department, University of the Western Cape, Private Bag X17, Bellville, 7535, South Africa
Amphibia Hyperolius nasutus group new species phylogeny taxonomy advertisement calls biogeography molecular genetics morphology species distribution model

Abstract

Specimens from across the range of the Hyperolius nasutus species group were sequenced for two mitochondrial genes and one nuclear gene. Advertisement calls were recorded from the same specimens where possible, and morphological characters were compared. Bayesian inference and maximum likelihood produced a tree indicating 16 clades. The clades show little or no overlap in combinations of 16S sequence difference, shared tyr haplotypes, advertisement call parameters, snout profiles and webbing. On the basis of these data we recognise H. acuticeps, H. adspersus, H. benguellensis, H. dartevellei, H. igbettensis, H. nasutus, H. nasicus, H. poweri, H. viridis and describe six new species: Hyperolius friedemanni sp. nov. Mercurio & Rödel, Hyperolius howelli sp. nov. Du Preez & Channing, Hyperolius inyangae sp. nov. Channing, Hyperolious jacobseni sp. nov. Channing, Hyperolius rwandae sp. nov. Dehling, Sinsch, Rödel & Channing, and Hyperolius lupiroensis sp. nov. Channing. Hyperolius lamottei is confirmed to be outside the H. nasutus group clade. Hyperolius granulatus, H. oxyrhynchus, H. punctulatus and H. sagitta are assigned as junior synonyms. As our results are based on a small number of specimens, these hypotheses await testing with larger sample sizes and more characters. A species distribution model suggests where outlier populations might be found.

References

  1. Adeba, P.J., Kouassi, P. & Rödel, M.-O. (2010) Anuran amphibians in a rapidly changing environment – revisiting Lamto, Côte d’Ivoire, 40 years after the first herpetofaunal investigations. African Journal of Herpetology, 59, 1–16. http://dx.doi.org/10.1080/04416651003595337

    Amiet, J.-L. (2005) Les Hyperolius camerounais du groupe d' H. nasutus (Amphibia, Anura, Hyperoliidae). Revue Suisse de Zoologie, 112, 271–310.

    Amiet, J.-L. (2006a) Hyperolius igbettensis, In: IUCN 2008. IUCN Red List of Threatened Species. Version 2008. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Amiet, J.-L. (2006b) Hyperolius adspersus, In IUCN 2008. IUCN Red List of Threatened Species. Version 2008. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Benson, D.A., Karsch-Mizrachi, I, Clark, K., Lipman, D.J., Ostell, J. & Sayers, E.W. (2012) GenBank. Nucleic Acids Research 40 (Database issue), D48–53. http://dx.doi.org/10.1093/nar/gkr1202

    Biju, S.D., Van Bocxlaer, I., Mahoney, S., Dinesh, K.P., Radhakrishnan, C., Zachariah, A., Giri, V. & Bossuyt, F. (2011) A taxonomic review of the Night Frog genus Nyctibatrachus Boulenger, 1882 in the Western Ghats, India (Anura: Nyctibatrachidae) with description of twelve new species. Zootaxa, 3029, 1–96.

    Bossuyt, F. & Milinkovitch, M.C. (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences, USA, 97, 6585–6590. http://dx.doi.org/10.1073/pnas.97.12.6585

    Channing, A., Moyer, D. & Burger, M. (2002) Cryptic species of sharp-nosed reed frogs in the Hyperolius nasutus complex: advertisement call differences. African Zoology, 37, 91–99.

    Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660. http://dx.doi.org/10.1046/j.1365-294x.2000.01020.x

    Dehling, J.M. (2012) An African glass frog: a new Hyperolius species (Anura: Hyperoliidae) from Nyungwe National Park, southern Rwanda. Zootaxa, 3391, 52–64.

    Flot, J.-F. (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Molecular Ecology Resources, 10, 162–166. http://dx.doi.org/10.1111/j.1755-0998.2009.02732.x

    Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M. & Gemmell, N.J. (2007) Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE, 2:e1109. http://dx.doi.org/10.1371/journal.pone.0001109

    Frost, D.R. (2011) Amphibian Species of the World: an Online Reference, Version 5.5 (31 January, 2011) Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/
    American Museum of Natural History, New York, USA. http://dx.doi.org/10.1126/science.os-1.19.223

    Goebel, A.M., Donnelly, J.M. & Atz, M.E. (1999) PCR primers and amplification methods for 12S ribosomal DNA, the control region, cytochrome oxidase I, and cytochrome b in bufonids and other frogs, and an overview of PCR primers which have amplified DNA in amphibians sucessfully. Molecular Phylogenetics & Evolution, 11, 163–199. http://dx.doi.org/10.1006/mpev.1998.0538

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978. http://dx.doi.org/10.1002/joc.1276

    Hijmans, R.J., Phillips, S.,Leathwick, J. & Elith, J. (2012) Dismo: Species distribution modelling. R package version 0.7-17. http://CRAN.R- project.org/package=dismo.

    Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K. & Zimmer, E.A. (1996) Nucleic acids IV: Sequencing and cloning, In Hillis, D.M., Moritz, C. &. Mable, B.K (eds) Molecular Systematics 2nd ed. Sinauer Associates, Sunderland, Massachusetts, USA.

    IUCN (2011) IUCN Red List of Threatened Species. Version 2011.2 <www.iucnredlist.org>. Downloaded on 06 April 2012.

    Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA, 86, 6196–6200. http://dx.doi.org/10.1073/pnas.86.16.6196

    Köhler, J., Scheelke, K., Schick, S., Veith, M. & Lötters, S. (2005a) Contribution to the taxonomy of hyperoliid frogs (Amphibia: Anura: Hyperoliidae): advertisement calls of twelve species from East and Central Africa. African Zoology, 40, 127–142.

    Köhler, J., Vietes, D.R., Bonett, R.M., Hita Garcia, F., Glaw, F., Steinke, D. & Vences, M. (2005b) New amphibians and global conservation: a boost in species discoveries in a highly endangered vertebrate group. BioScience, 55, 693–696.
    h    ttp://dx.doi.org/10.1641/0006-3568(2005)055[0693:NAAGCA]2.0.CO;2

    Lötters, A., Schick, S., Scheelke, K., Teege, P., Kosuch, J. Rotich, D. & Veith, M. (2004) Bio-sketches and partitioning of sympatric reed frogs, genus Hyperolius (Amphibia; Hyperoliidae), in two humid tropical African forest regions. Journal of Natural History, 38, 1969–1997. http://dx.doi.org/10.1080/00222930310001613584

    Mercurio, V. (2011) Amphibians of Malawi. Edition Chimaira, Frankfurt am Main. http://dx.doi.org/10.1086/659940

    Moritz, C. & Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology 2(10), e354. http://dx.doi.org/10.1371/journal.pbio.0020354

    Myers, C.W. & Duellman, W.E. (1982) A new species of Hyla from Cerro Colorado, and other treefrog records and geographical notes from western Panama. American Museum Novitates, 2752, 1–32.

    Nix, H. (1986) A biogeographic analysis of Australian elapid snakes. In Atlas of elapid snakes of Australia, ed Longmore, R. Bureau of Flora and Fauna, Canberra, pp 4–15.

    Noonan, B.P. & Gaucher, P. (2005) Phylogeography and demography of Guianan harlequin toads (Atelopus): diversification within a refuge. Molecular Ecology, 14, 3017–3031. http://dx.doi.org/10.1111/j.1365-294X.2005.02624.x

    Padial, J.M., Miralles, A., de la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, article 16. http://dx.doi.org/10.1186/1742-9994-7-16

    Perret, J.-L. (1976) Revision des amphibiens Africaines et principalement des types conservés au Musée Bocage de Lisbonne. Arqivos do Museu Bocage ser 2, 6, 15–34.

    Poynton, J.C. (1964) The amphibians of southern Africa: a faunal study. Annals of the Natal Museum, 17, 1–334.

    Poynton, J.C. & Broadley, D.G. (1987) Amphibia Zambesiaca 3. Rhacophoridae and Hyperoliidae. Annals of the Natal Museum, 28, 161–229.

    Rödel, M.-O. (2000) Herpetofauna of West Africa, Vol. I: Amphibians of the West African savanna. Edition Chimaira, Frankfurt am Main.

    Rödel, M.-O. & Agyei, A.C. (2003) Amphibians of the Togo-Volta highlands, eastern Ghana. Salamandra, 39, 207–234.

    Rödel, M.-O., Bangoura, M.A. & Böhme, W. (2004) The amphibians of south-eastern Republic of Guinea (Amphibia: Gymnophiona, Anura). Herpetozoa, 17, 99–118.

    Rödel, M.-O. & Ernst, R. (2003) The amphibians of Marahoué and Mont Péko National Parks, Ivory Coast. Herpetozoa, 16, 23–39.

    Rödel, M.-O., Kosuch, J., Grafe, T.U., Boistel, R., Assemian, N.E., Kouamé, N.G., Tohé, B., Gourène, G., Perret, J.-L., Henle, K., Tafforeau, P., Pollet, N. & Veith, M. (2009) A new tree-frog genus and species from Ivory Coast, West Africa (Amphibia: Anura: Hyperoliidae). Zootaxa, 2044, 23–45.

    Rödel, M.-O., Lampert, K.P. & Linsenmair, K.E. (2006) Reproductive biology of the West African savannah frog Hyperolius nasutus Günther, 1864 (Amphibia: Anura: Hyperoliidae). Herpetozoa, 19, 3–12.

    Rödel, M.-O., Sandberger, L., Penner, J., Mané, Y. & Hillers, A. (2010) The taxonomic status of Hyperolius spatzi Ahl, 1931 and Hyperolius nitidulus Peters, 1875 (Amphibia: Anura: Hyperoliidae). Bonn zoological Bulletin, 57, 177–188.

    Rödel, M.-O. & Schiøtz, A. (2004) Hyperolius lamottei, In IUCN 2009. IUCN Red List of Threatened Species. Version 2009.1. <www.iucnredlist.org>. Downloaded on 19 January 2012.

    Schick, S., Kielgast, J. Rödder, D., Muchai, V., Burger, M. & Lötters, S. (2010) New species of reed frog from the Congo Basin with discussion of paraphyly in cinnamon-belly reed frogs. Zootaxa, 2501, 23–36.

    Schiøtz, A. (1975) The treefrogs of Eastern Africa. Steenstrupia, Copenhagen.

    Schiøtz, A. (1999) Treefrogs of Africa. Edition Chimaira, Frankfurt am Main.

    Schiøtz, A. (2006a) Notes on the genus Hyperolius (Anura, Hyperoliidae) in central République Démocratique du Congo. Alytes, 24, 40–60.

    Schiøtz, A. (2006b) Reflections on the Hyperolius nasutus group. Alytes, 24, 61–71.

    Schiøtz, A. (2008) Hyperolius nasicus. In: IUCN 2009. IUCN Red List of Threatened Species. Version 2009.1. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Schiøtz, A., Channing, A., Largen, M., Howell, K., Lötters, S. (2004) Hyperolius acuticeps. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. <www.iucnredlist.org>. Downloaded on 24 September 2012.

    Schiøtz, A., Channing, A., Burger, M. & Largen, M. (2008a) Hyperolius nasutus, In: IUCN 2008. 2008 IUCN Red List of Threatened Species. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Schiøtz, A., Channing, A., Largen, M., Howell, K. & Lötters, S. (2008b) Hyperolius acuticeps. In: IUCN 2008. 2008 IUCN Red List of Threatened Species. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Schiøtz, A. & Poynton, J. (2008) Hyperolius benguellensis. In: IUCN 2008. 2008 IUCN Red List of Threatened Species. <www.iucnredlist.org>. Downloaded on 9 January 2012.

    Schiøtz, A. & van Daele, P. (2003) Notes on the treefrogs (Hyperoliidae) of North-Western Province, Zambia. Alytes, 20, 137–149.

    Stephens, M. & Donnelly, P. (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162–1169. http://dx.doi.org/10.1086/379378

    Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping aqnd DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.

    Veith, M., Kosuch, J., Rödel, M.-O., Hillers, A., Schmitz, A., Burger, M. & Lötters, S. (2009) Multiple evolution of sexual dichromatism in African reed frogs. Molecular Phylogenetics & Evolution, 51, 388–393. http://dx.doi.org/10.1016/j.ympev.2008.12.022

    Vences, M., Thomas, M., van der Meijden, A., Chiari, A. & Vieites, D.R. (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2, 5. http://dx.doi.org/10.1186/1742-9994-2-5

    Vences, M. & Wake, D.B. (2007) Speciation, species boundaries and phylogeography of amphibians. In Amphibian Biology, eds. Heatwole, H. & Tyler, M.J. pp 2613–2671, Surrey beatty & Sons, Chipping Norton.

    Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Science USA, 196, 8267–8272. http://dx.doi.org/10.1073/pnas.0810821106

    Wager, V.A. (1986) Frogs of South Africa. Delta Books, Craighall.

    Zimkus, B.M. & Schick, S. (2010) Light at the end of the tunnel: insights into the molecular systematics of East African puddle frogs (Anura: Phrynobatrachidae). Systematics and Biodiversity, 8, 39–47. http://dx.doi.org/10.1080/14772000903543004