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Genus Stumpffia) from Madagascar 67 (3): 271– 398 © Senckenberg Gesellschaft für Naturforschung, 2017. 28.11.2017 Describing the smaller majority: integrative taxonomy reveals twenty-six new species of tiny microhylid frogs (genus Stumpffia) from Madagascar Andolalao Rakotoarison 1, 2, Mark D. Scherz 1, 3, Frank Glaw 3, Jörn Köhler 4, Franco Andreone 5, Michael Franzen 3, Julian Glos 6, Oliver Hawlitschek 3, 7, Teppei Jono 8, 9, Akira Mori 8, Serge H. Ndriantsoa 2, Noromalala Rasoamam- pionona Raminosoa 2, Jana C. Riemann 6, Mark-Oliver Rödel 10, Gonçalo M. Rosa 11, 12, 13, David R. Vieites 14, Angelica Crottini 15, Miguel Vences 1, * 1 Division of Evolutionary Biology, Zoological Institute, Braunschweig University of Technology, Mendelssohnstr. 4, 38106 Braunschweig, Germany — 2 Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo, Antananarivo 101, Madagascar — 3 Zoologische Staatssammlung München (ZSM-SNSB), Münchhausenstr. 21, 81247 München, Germany — 4 Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany — 5 Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, I-10123 Torino, Italy — 6 Zoological Institute, University of Hamburg, Martin-Luther-King Platz 3, 20146 Hamburg, Germany — 7 Institut de Biologia Evolutiva (CSIC- UPF), Passeig Marítim de la Barceloneta 37, 08003 Barcelona, Spain — 8 Department of Zoology, Graduate School of Science, Kyoto Univer- sity, Sakyo, Kyoto 606-8502, Japan — 9 Tropical Biosphere Research Center, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 901- 0213, Japan — 10 Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstr. 43, 10115 Berlin, Germany — 11 Department of Biology, University of Nevada, Reno, NV 89557, USA — 12 Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK — 13 Centre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências Universidade de Lisboa, 1749-016 Lisboa, Portugal — 14 National Natural History Museum, Spanish Scientific Research Council (CSIC), C/José Gutierrez Abascal 2, 828006, Madrid, Spain — 15 CIBIO, Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, Nº 7, 4485-661 Vairão, Portugal — * Corresponding author; [email protected] Accepted 4.x.2017. Published online at www.senckenberg.de/vertebrate-zoology on 13.xi.2017. Abstract The genus Stumpffia BOETTGER, 1881 currently contains 15 named, small to miniaturized frog species, classified in the endemic Malagasy subfamily Cophylinae of the family Microhylidae. Stumpffia are terrestrial frogs with a largely unknown biology, probably due to their small size and secretive habits. Previous studies have suggested a large proportion of undescribed diversity in the genus. We revise the genus on the basis of a combination of molecular, bioacoustic, and morphological data and describe 26 new species that are all genetically divergent, almost all of them with high pairwise genetic divergences > 4% p-distance in a segment of the mitochondrial 16S rRNA gene and concord- ant differentiation in a segment of the nuclear Rag-1 gene. The majority of the new species can also be distinguished by the structure of their advertisement calls (where bioacoustic data are available), and in most comparisons the species can also be distinguished morphologically. Furthermore, a molecular phylogeny reconstructed from DNA sequences of one nuclear and four mitochondrial gene segments revealed that in many cases, morphologically similar species are not each other’s closest relatives, thus confirming their identity as independent evo- lutionary lineages and revealing repeated phenotypic divergence and convergence among and within clades. The phylogeny distinguishes four main clades in the genus: Clade A containing 17 species (Stumpffia be, S. hara, S. megsoni, S. staffordi, S. psologlossa, S. analamaina, S. gimmeli, S. madagascariensis, S. pygmaea, S. angeluci sp. nov., S. huwei sp. nov., S. iharana sp. nov., S. larinki sp. nov., S. maledicta sp. nov., S. mamitika sp. nov., S. sorata sp. nov., and S. yanniki sp. nov.) mostly from northern and northwestern Madagascar, generally characterized by limited digital reduction and divided in subclades of comparatively large, small, and miniaturized body size, respectively; Clade B with four species (S. miery, S. meikeae sp. nov., S. obscoena sp. nov., and S. davidattenboroughi sp. nov.) morphologically ranging from miniaturized with strong digital reduction to comparatively large-sized; Clade C with 18 species (S. grandis, S. kibomena, S. roseif- emoralis, S. tetradactyla, S. nigrorubra sp. nov., S. achillei sp. nov., S. diutissima sp. nov., S. pardus sp. nov., S. edmondsi sp. nov., S. fusca sp. nov., S. jeannoeli sp. nov., S. spandei sp. nov., S. garraffoi sp. nov., S. analanjirofo sp. nov., S. miovaova sp. nov., S. makira sp. nov., S. betampona sp. nov., and S. dolchi sp. nov.) mostly distributed in eastern and northeastern Madagascar, containing species of compara- ISSN 1864-5755 271 Rakotoarison, A. et al.: Integrative taxonomy of Stumpffia frogs tively large size as well as small-sized species, many of which are characterized by a moderate degree of digital reduction; and Clade D with two miniaturized species (S. tridactyla and S. contumelia sp. nov.) with strong digital reduction, which form the sister group of all other Stumpffia. Two of the newly described species (S. angeluci and S. maledicta) are not separated by the 4% threshold in the 16S gene but occur in sympatry and do not share Rag-1 haplotypes. To achieve a comprehensive review of this species-rich genus, we provide simplified dif- ferential diagnoses and descriptions and abbreviated descriptions of morphological variation. Despite the large number of Stumpffia species newly described herein, we identify several additional candidate species with currently insufficient data to warrant formal description, and highlight that some species such as S. analanjirofo, S. gimmeli, S. kibomena, S. madagascariensis, S. roseifemoralis and S. obscoena are composed of two or more deep mitochondrial lineages that might also turn out to be distinct taxa after in-depth study. We confirmStumpffia as a genus of highly microendemic frogs with many species apparently restricted to very small ranges, and provide evidence that two of the new species (S. achillei and S. davidattenboroughi) do not construct foam nests but lay their eggs in wet places in the leaf litter, or in cavi- ties such as empty snail shells. We propose a conservation status for all the described species according to IUCN Red List Criteria, but also discuss several problems applying these criteria to such microendemic and poorly known frogs. Key words Amphibia; Anura; Microhylidae; diversity; systematics; bioacoustics; molecular genetics; morphology; microendemism. Table of content Abstract ..................................................................................................................................................................... 271 Introduction ............................................................................................................................................................... 274 Materials and Methods .............................................................................................................................................. 275 Results ....................................................................................................................................................................... 279 Molecular species delimitation ................................................................................................................................. 279 Molecular phylogeny ................................................................................................................................................ 285 Morphological and bioacoustic comparisons ............................................................................................................ 286 Taxonomic accounts .................................................................................................................................................. 293 1. Small-sized or miniaturized species of clade A ............................................................................................. 294 Stumpffia psologlossa BOETTGER, 1881 (type species of the genus Stumpffia) ........................................ 295 Stumpffia analamaina KLAGES, GLAW, KÖHLER, MÜLLER, HIPSLEY & VENCES, 2013 ................................ 304 Stumpffia gimmeli GLAW & VENCES, 1992 ................................................................................................ 306 Stumpffia madagascariensis MOCQUARD, 1895 ........................................................................................ 307 Stumpffia pygmaeaV ENCES & GLAW, 1991 .............................................................................................. 310 Stumpffia angeluci sp. nov. ...................................................................................................................... 310 Stumpffia huwei sp. nov. .......................................................................................................................... 314 Stumpffia iharana sp. nov. ....................................................................................................................... 317 Stumpffa larinki sp. nov. .........................................................................................................................
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