Abstract
We describe ten new species of treefrogs assigned to the genus Boophis (Anura: Mantellidae) and resurrect two species from synonymy, based on materials collected during fieldwork in Madagascar, carried out mainly between 2000 and 2007. Our comparative database assembled over the past years comprises fresh material for molecular analysis from all 58 nominal Boophis species, and advertisement call recordings from all except three species. We follow an integrative approach and combine molecular, bioacoustic and morphological evidence to diagnose the new species. In most cases, the new species have uncorrected molecular divergences of over 4–5% in the mitochondrial 16S rRNA gene to their closest relatives. In some cases the divergences are lower (2–2.5%) but are then accompanied by distinct differences in advertisement calls or morphology. Boophis piperatus sp. nov. from Ranomafana National Park is a small brown species assigned to the B. majori group that is similar to B. miniatus but differs in morphology and advertisement calls. Boophis arcanus sp. nov. is assigned to the B. majori group as well and is known from only two female specimens from a site close to Ranomafana; it is described mainly based on its strong genetic differentiation (> 7.2% to all other species). Boophis entingae sp. nov. is a species of the Boophis goudoti group occurring in northern Madagascar, similar to and sympatric with B. brachychir, but with a strongly different advertisement call. Boophis roseipalmatus sp. nov. belongs to the B. goudoti group, is similar to B. madagascariensis, and appears to replace this species in most of northern Madagascar, with possible areas of sympatry in the north east. Boophis spinophis sp. nov. is an enigmatic, morphologically highly divergent species from Ranomafana National Park that belongs into the B. goudoti group but differs from all other spe-4 · Zootaxa 2383 © 2010 Magnolia Presscies in the group by having distinct dermal tubercles along the lateral parts of the shank and around the elbow. Boophis praedictus sp. nov. is a sibling species of B. albilabris in the B. albilabris group, diagnosable by its red iris periphery and distributed in rainforest along the east coast. Boophis sandrae sp. nov. belongs to the B. luteus group and is superficially similar to the sympatric B. elenae, but has a faster call and smaller body size. Boophis miadana sp. nov. and B. haingana sp. nov., both in the B. albipunctatus group and syntopically occurring at Andohahela National Park, are related to B. ankaratra and B. schuboeae and differ mainly by their advertisement calls. Boophis luciae sp. nov., also in the B. albipunctatus group, differs from the sympatric B. albipunctatus and B. sibilans by having slightly smaller body size and different advertisement calls. We furthermore resurrect Rhacophorus obscurus Boettger, 1913 (as Boophis obscurus in the B. goudoti group) from the synonymy of Boophis goudoti as well as Rhacophorus andrangoloaka Ahl, 1928 (as Boophis andrangoloaka in the B. microtympanum group) from the synonymy of Boophis rhodoscelis, and propose to consider Rhacophorus brevirostris Ahl, 1928 as junior synonym of Boophis andrangoloaka. We discuss our integrative methodological approach and the different lines of evidence used to delimitate the species described or resurrected herein. By applying IUCN Redlist criteria, we evaluate the threat status of the species considered: six species are classified Data Deficient (B. arcanus, B. haingana, B. miadana, B. piperatus, B. praedictus, B. spinophis), four Vulnerable (B. andrangoloaka, B. entingae, B. roseipalmatus, B. sandrae), and two Least Concern (B. luciae, B. obscurus).References
Ahl, E. (1928) Neue Frösche der Gattung Rhacophorus aus Madagaskar. Zoologischer Anzeiger, 75 (11/12), 311–318.
Andreone, F. (1993) Two new treefrogs of the genus Boophis (Anura: Rhacophoridae) from central-eastern Madagascar. Bollettino del Museo Regionale di Scienze Naturali di Torino, 11, 289–313.
Andreone, F. (1994) The amphibians of Ranomafana rain forest, Madagascar - preliminary community analysis and conservation considerations. Oryx, 28, 207–214.
Andreone, F. (1996) Another new green treefrog, Boophis anjanaharibeensis n. sp. (Ranidae: Rhacophorinae), from northeastern Madagascar. Aqua, 2, 25–32.
Andreone, F., Cadle, J.E., Cox, N., Glaw, F., Nussbaum, R.A., Raxworthy, C.J., Stuart, S.N., Vallan, D. & Vences, M. (2005) Species review of amphibian extinction risks in Madagascar: conclusions from the Global Amphibian Assessment. Conservation Biology, 19, 1790–1802.
Andreone, F., Carpenter, A. I., Cox, N., du Preez, L., Freeman, K., Furrer, S., García, G., Glaw, F., Glos, J., Knox, D., Köhler, J., Mendelson III, J.R., Mercurio, V., Mittermeier, R.A., Moore, R.D., Rabibisoa, N.H.C., Randriamahazo, H., Randrianasolo, H., Rasomampionona Raminosoa, N., Ravoahangimalala Ramilijaona, O., Raxworthy, C.J., Vallan, D., Vences, M., Vieites, D.R. & Weldon, C. (2008a) The challenge of conserving amphibian megadiversity in Madagascar. PLoS Biology, 6: e118.
Andreone, F., Cox, N., Glaw, F., Köhler, J., Rabibisoa, N.H.C., Randriamahazo, H., Randrianasolo, H., Raxworthy, C.J., Stuart, S.N., Vallan, D. & Vences, M. (2008b) Update of the Global Amphibian Assessment for Madagascar in light of new species discoveries, nomenclature changes, and new field information. Monografie del Museo Regionale di Scienze Naturali di Torino, 45, 419–438.
Andreone, F., Glaw, F., Nussbaum, R.A., Raxworthy, C.J., Vences, M. & Randrianirina, J.E. (2003) The amphibians and reptiles of Nosy Be (NW Madagascar) and nearby islands: a case study of diversity and conservation of an insular fauna. Journal of Natural History, 37, 2119–2149.
Andreone, F., Vences, M., Guarino, F.M., Glaw, F. & Randrianirina, J.E. (2002) Natural history and larval morphology of Boophis occidentalis (Anura: Mantellidae: Boophinae) provide new insights into the phylogeny and adaptive radiation of endemic Malagasy frogs. Journal of Zoology, London, 257, 425–438.
Andreone, F., Nincheri, R. & Piazza, R. (1995) Un nouveau Boophis vert (Ranidae: Rhacophorinae) des forêts pluviales du Sud de Madagascar. Revue francaise de Aquariologie et Herpetologie, 21, 121–127.
Aprea, G., Andreone, F., Capriglione, T., Odierna G. & Vences M. (2004) Evidence for a remarkable stasis of chromosome evolution in Malagasy treefrogs (Boophis: Mantellidae). Italian Journal of Zoology, Supplement, 2, 237–243.
Bauer, A. M., Günther, R. & Klipfel, M. (1995) The herpetological contributions of Wilhelm C. H. Peters (1815–1883). SSAR Facsimile Reprints in Herpetology, 714 pp.
Blommers-Schlösser, R.M.A. (1979) Biosystematics of the Malagasy frogs. II. The genus Boophis (Rhacophoridae). Bijdragen tot de Dierkunde, 49, 261–312.
Blommers-Schlösser, R.M.A. & Blanc, C.P. (1991) Amphibiens (première partie). Faune de Madagascar, 75 (1), 1–379.
Blommers-Schlösser, R.M.A. & Blanc, C.P. (1993) Amphibiens (deuxième partie). Faune de Madagascar, 75 (2), 384–530, planches 13–20.
Boettger, O. (1913) Reptilien und Amphibien von Madagascar, den Inseln und dem Festland Ostafrikas, pp. 269–375, Tafeln 23–30, in Voeltzkow, A.: Reise in Ostafrika in den Jahren 1903–1905, Wissenschaftliche Ergebnisse, dritter Band, systematische Arbeiten, Schweizerbartsche Verlagsbuchhandlung, Stuttgart.
Boulenger, G..A. (1888) Descriptions of new reptiles and batrachians from Madagascar. Annals and Magazine of Natural History, ser. 6, 1, 101–107.
Boumans, L., Vieites, D.R., Glaw, F. & Vences, M. (2007) Geographical patterns of deep mitochondrial differentiation in widespread Malagasy reptiles. Molecular Phylogenetics and Evolution, 45, 822–839.
Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Single-locus and multilocus DNA fingerprint. In: Molecular Genetic Analysis of Populations: A Practical Approach (Ed. Hoelzel, A.R.), IRL Press, Oxford , 225–270.
Cadle, J. (1995) A new species of Boophis (Anura: Rhacophoridae) with unusual skin glands from Madagascar, and a discussion of variation and sexual dimorphism in Boophis albilabris (Boulenger). Zoological Journal of the Linnean Society, 115, 313–345.
Cadle J.E. (2003) Boophis. In: Goodman, S.M. & Benstead, J.P., editors. The natural history of Madagascar. Chicago: University of Chicago Press. Pp. 916–919.
Cardoso, A., Serrano, A. & Vogler, A.P. (2009) Morphological and molecular variation in tiger beetles of the Cicindela hybrida complex: is an 'integrative taxonomy' possible? Molecular Ecology, 18, 648–664.
Chiari, Y., Vences, M., Vieites, D.R., Rabemananjara, F., Bora, P., Ramilijaona Ravoahangimalala, O. & Meyer, A. (2004) New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella). Molecular Ecology, 13, 3763–3774.
Dayrat, B. (2005) Toward integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415
D'Cruze, N., Köhler, J., Franzen, M. & Glaw, F. (2008) A conservation assessment of the amphibians and reptiles of the Forêt d'Ambre Special Reserve, north Madagascar. Madagascar Conservation & Development, 3, 44–54.
De Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations, 57–75 in: Howard, D. J. and Berlocher, S. H. (eds.): Endless forms: Species and speciation. New York, Oxford University Press.
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
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(10): e1109.
Glaw, F., Hoegg, S. & Vences, M. (2006) Discovery of a new basal relict lineage of Madagascan frogs and its implications for mantellid evolution. Zootaxa, 1334, 27–43
Glaw, F. & Thiesmeier, B. (1993) Bioakustische Differenzierung in der Boophis luteus-Gruppe (Anura: Rhacophoridae), mit Beschreibung einer neuen Art und einer neuen Unterart. Salamandra, 28, 258–269.
Glaw, F. & Vences, M. (1992) A fieldguide to the amphibians and reptiles of Madagascar. Cologne, Vences & Glaw Verlag, 331 pp.
Glaw, F. & Vences, M. (1994) A fieldguide to the amphibians and reptiles of Madagascar. 2nd edition. Cologne, Vences & Glaw Verlag, 480 pp.
Glaw, F. & Vences, M. (1997a) Anuran eye colouration: definitions, variation, taxonomic implications and possible functions, pp. 125–138. In: Böhme, W., Bischoff, W. and Ziegler, T., Eds. Herpetologia Bonnensis. SEH Proceedings, Bonn.
Glaw, F. & Vences, M. (1997b) Neue Ergebnisse zur Boophis goudoti-Gruppe aus Madagaskar: Bioakustik, Fortpflanzungsstrategien und Beschreibung von Boophis rufioculis sp. nov. Salamandra, 32, 225–242.
Glaw, F. & Vences, M. (1997c) New species of the Boophis tephraeomystax group (Anura: Ranidae: Rhacophorinae) from arid western Madagascar. Copeia, 1997, 572–578.
Glaw, F. & Vences, M. (2002) A new cryptic treefrog species of the Boophis luteus group from Madagascar: bioacoustic and genetic evidence (Amphibia, Anura, Mantellidae). Spixiana, 25, 173–181.
Glaw, F. & Vences, M. (2006) Phylogeny and genus-level classification of mantellid frogs. Organisms Diversity & Evolution, 6, 236–253.
Glaw, F. & Vences, M. (2007) A field guide to the amphibians and reptiles of Madagascar. Third edition. Cologne, Vences & Glaw Verlag, 496 pp.
Glaw, F., Vences, M., Andreone, F. & Vallan, D. (2001) Revision of the Boophis majori group (Amphibia: Mantellidae) from Madagascar, with descriptions of five new species. Zoological Journal of the Linnean Society, 133, 495–529.
Guibé, J. (1947) Description d'un batracien nouveau de Madagascar (Boophis laurenti n. sp.) et synonymie de plusieurs espèces du genre Boophis. Bulletin du Muséum national d'Histoire Naturelle, Paris (ser. 2), 19, 438–439.
Guibé, J. (1978) Les batraciens de Madagascar. Bonner zoologische Monographien, 11, 1–140.
Hall, T.A. (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Ser., 41, 95–98.
Isaac, N.J.B., Mallet, J. & Mace, G.M. (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology and Evolution, 19, 464–469.
Köhler, J. (2000) Amphibian diversity in Bolivia: a study with special reference to montane forest regions. Bonner zoologische Monographien, 48, 1–243.
Köhler, J., Glaw, F. & Vences, M. (2007) A new green treefrog, genus Boophis Tschudi 1838 (Anura Mantellidae), from arid western Madagascar: phylogenetic relationships and biogeographic implications. Tropical Zoology, 20, 215–227.
Köhler, J., Glaw, F. & Vences, M. (2008) Two additional treefrogs of the Boophis ulftunni species group (Anura: Mantellidae) discovered in rainforests of northern and south-eastern Madagascar. Zootaxa, 1814, 37–48.
Köhler, J., Vieites, D.R., Bonett, R.M., Hita García, F., Glaw, F., Steinke, D. & Vences, M. (2005) Boost in species discoveries in a highly endangered vertebrate group: new amphibians and global conservation. BioScience, 55, 693–696.
Kremen, C., Cameron, A., Moilanen, A., Phillips, S.J., Thomas, C.D., Beentje, H., Dransfield, J., Fisher, B.L., Glaw, F., Good, T.C., Harper, G.J., Hijmans, R.J., Lees, D.C., Louis Jr., E., Nussbaum, R.A., Raxworthy, C.J., Razafimpahanana, A., Schatz, G.E., Vences, M., Vieites, D.R. & Zjhra, M.L. (2008) Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science, 320, 222–226.
Narins, P.M., Lewis, E.R. & McClelland, B.E. (2000) Hyperextended call note repertoire of the endemic Madagascar treefrog Boophis madagascariensis (Rhacophoridae). Journal of Zoology, London, 250, 283–298.
Nylander, J.A. (2004) MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala University.
Padial, J.M., Castroviejo-Fisher, S., Köhler, J., Vilà, C., Chaparro, J.C. & De la Riva, I. (2009) Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoologica Scripta, 38, 431–447.
Padial, J.M. & De la Riva, I. (2006) Taxonomic inflation and the stability of species lists: the perils of ostrich’s behavior. Systematic Biology, 55, 859–867.
Padial, J.M. & De la Riva, I. (2007) Integrative taxonomists should use and produce DNA barcodes. Zootaxa, 1586, 67–68.
Padial, J.M. & De la Riva, I. (2009) Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura). Zoological Journal of the Linnean Society, 155, 97–122.
Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The Simple Fool's Guide to PCR, Version 2.0., Privately published, University of Hawaii.
Peters, W.C.H. (1874) Ueber neue Amphibien. – Gesammtsitzung (15. Oktober 1874), Monatsb. Akad. Wiss. Berlin, 616–624.
Randrianiaina, R.-D., Raharivololoniaina, L., Preuss, C., Strauß, A., Glaw, F., Teschke, M., Glos, J., Raminosoa, N. & Vences, M. (2009) Descriptions of the tadpoles of seven species of Malagasy treefrogs, genus Boophis. Zootaxa, 2021, 23–41.
Rabemananjara, F.C.E., Chiari, Y., Ravoahangimalala Ramilijaona, O. & Vences, M. (2007) Evidence for recent gene flow between north-eastern and south-eastern Madagascar from a phylogeography of the Mantella cowani group. Frontiers in Zoology, 4, article 1.
Raharivololoniaina, L., Grosjean, S., Rasoamampionona Raminosoa, N., Glaw, F. & Vences, M. (2006) Molecular identification, description and phylogenetic implications of the tadpoles of 11 species of Malagasy treefrogs, genus Boophis. Journal of Natural History, 40, 1449–1480.
Raxworthy, C.J., Ingram, C.M., Rabibisoa, N. & Pearson, R.G. (2007) Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology, 56, 907–923.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Sites, J.W. & Marshall, J.C. (2004) Delimiting species: a renaissance issue in systematic biology. Trends in Ecology and Evolution, 18, 462–470.
Steindachner, F. (1864) Batrachologische Mittheilungen. Verhandlungen der zoologisch-botanischen Gesellschaft in Wien, 14, 239–288.
Swofford, D.L. (2002) PAUP* Phylogenetic Analysis using Parsimony (* and other methods), Version 4b10. Sinauer Associates, Sunderland, MA.
Tschudi, J.J. (1838) Classification der Batrachier, mit Berücksichtigung der fossilen Thiere dieser Abtheilung der Reptilien. [Reprint 1839 in: Mém. Soc. Neuchatel Sci. Nat. 2, 1–102].
Vallan, D. (2000) Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar. Biological Conservation, 96, 31–43.
Vallan, D., Vences, M. & Glaw, F. (2010) Forceps delivery of a new treefrog species of the genus Boophis from eastern Madagascar (Amphibia: Mantellidae). Amphibia-Reptilia 31, 1-8.
Vences, M., Andreone, F., Glaw, F., Kosuch, J., Meyer, A., Schaefer, H.-C. & Veith, M. (2002) Exploring the potential of life-history key innovation: brook breeding in the radiation of the Malagasy treefrog genus Boophis. Molecular Ecology, 11, 1453–1463.
Vences, M., Andreone, F. & Vieites, D.R. (2005a) New tree frog of the genus Boophis Tschudi 1838 from the northwestern rainforests of Madagascar. Tropical Zoology, 18, 237–249.
Vences, M., Chiari, Y., Teschke, M., Randrianiaina, R.-D., Raharivololoniaina, L., Bora, P., Vieites, D.R. & Glaw, F. (2008) Which frogs are out there? A preliminary evaluation of survey techniques and identification reliability of Malagasy amphibians. Monografie del Museo Regionale di Scienze Naturali di Torino, 45, 233–253.
Vences, M. & Glaw, F. (2001) Systematic review and molecular phylogenetic relationships of the direct developing Malagasy anurans of the Mantidactylus asper group (Amphibia, Mantellidae). Alytes, 19, 107–139.
Vences, M. & Glaw, F. (2002) Two new treefrogs of the Boophis rappiodes group from eastern Madagascar. Tropical Zoology, 15, 141–163.
Vences, M. & Glaw, F. (2004) Revision of the subgenus Chonomantis (Anura: Mantellidae: Mantidactylus) from Madagascar, with description of two new species. Journal of Natural History, 38, 77–118.
Vences, M., Glaw, F. & Márquez, R. (2006) The Calls of the Frogs of Madagascar. 3 Audio CDs and booklet, 44 pp. Alosa-Fonozoo, Barcelona.
Vences, M., Thomas, M., Bonett, R.M. & Vieites, D.R. (2005b) Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philosophical Transactions of the Royal Society London, Series B, 360, 1859–1868.
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 of the USA, 106, 8267–8272.
Wiens, J.J. (2007) Species delimitation: new approaches for discovering diversity. Systematic Biology, 56, 875–878.
Wiens, J.J. & Penkrot, T.L. (2002) Delimiting species based on DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology, 51, 69–91.
Wollenberg, K.C., Andreone, F., Glaw, F. & Vences, M. (2008) Pretty in pink: a new treefrog species of the genus Boophis from north-eastern Madagascar. Zootaxa, 1684, 58–68.