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Molecular Phylogeny, Morphology and Bioacoustics Reveal Five Additional Species of Arboreal Microhylid Frogs of the Genus Anodonthyla from Madagascar

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Molecular Phylogeny, Morphology and Bioacoustics Reveal Five Additional Species of Arboreal Microhylid Frogs of the Genus Anodonthyla from Madagascar Contributions to Zoology, 79 (1) 1-32 (2010) Molecular phylogeny, morphology and bioacoustics reveal five additional species of arboreal microhylid frogs of the genus Anodonthyla from Madagascar Miguel Vences1, 5, Frank Glaw2, Jörn Köhler3, Katharina C. Wollenberg1, 4 1 Zoological Institute, Technical University of Braunschweig, Spielmannstr. 8, 38106 Braunschweig, Germany 2 Zoologische Staatssammlung München, Münchhausenstr. 21, 81247 München, Germany 3 Department of Natural History – Zoology, Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany 4 Department of Organismic and Evolutionary Biology & Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA 5 E-mail: [email protected] Key words: Amphibia, Anura, Cophylinae, integrative taxonomy, Microhylidae, new species Abstract Contents We provide a partial revision of the microhylid frogs of the ge- Introduction ......................................................................................... 1 nus Anodonthyla, endemic to Madagascar, based on compre- Material and methods ........................................................................ 2 hensive molecular, bioacoustic and morphological data sets that Results .................................................................................................. 5 include newly collected specimens from multiple localities. The Molecular diversity and phylogenetic relationships of molecular trees provide strong evidence for the polyphyly of Anodonthyla .................................................................................. 5 several nominal species as they were previously defined, espe- Bioacoustic and morphological differentiation of cially of Anodonthyla boulengeri and A. nigrigularis. As a con- Anodonthyla species .................................................................... 7 sequence, we here resurrect the nomen Mantella pollicaris Discussion ........................................................................................... 9 Boettger as Anodonthyla pollicaris from the synonymy of A. Species diversity in Anodonthyla ............................................. 9 boulengeri, and we describe four new species, all with strong Biogeography ............................................................................ 10 genetic divergences to other nominal species: Anodonthyla Evolution of calls in Anodonthyla ......................................... 11 emilei from Ranomafana National Park, a comparatively medi- Conservation and IUCN red list assessment ....................... 11 um-sized species characterized by a multi-note advertisement Acknowledgements ........................................................................ 12 call with high note repetition rate; A. theoi from Manombo Spe- References ........................................................................................ 13 cial Reserve, a small species characterized by low note repeti- Appendix .......................................................................................... 15 tion rate, long note duration and high spectral call frequency; A. vallani, a medium-sized species from Ambohitantely Special Reserve, characterized by low note repetition rate, long note du- ration and low spectral call frequency; and A. jeanbai, a small Introduction species from Andohahela National Park, characterized by a long and narrow head, presence of short dorsolateral folds, a very Frogs of the family Microhylidae Günther, 1859 are short first finger, and a yellowish ventral colour. A further candi- among the most poorly known amphibian groups. date species comprises populations previously assigned to A. boulengeri from the Ranomafana region, which we do not de- Several factors contribute to the difficulty of their scribe because the corresponding data set is too fragmentary, study: some species have a very seasonal breeding be- and we refer to it as A. sp. aff. boulengeri ‘Ranomafana’. The haviour and are thus difficult to find, other species are molecular phylogeny indicates recurrent shifts between high minute in body size and therefore often overlooked. and low note repetition rates in calls, based mainly on three The high frequency of evolutionary change in some strongly supported sister groups: A. moramora with low repeti- tion rate and A. nigrigularis with moderately low repetition rate; osteological characters, especially reductions in the A. theoi with low repetition rate and A. pollicaris with high rep- shoulder girdle, has led to the definition of a large etition rate; and A. vallani with low repetition rate and A. sp. aff. number of microhylid genera containing only one or a boulengeri ‘Ranomafana’ with high repetition rate. The two spe- few species, and phylogenetic relationships among cies with the northernmost ranges, A. hutchisoni and A. bouleng- genera and among major microhylid clades have long eri, are phylogenetically nested within clades of species occur- ring further south, confirming that the center of origin of the remained enigmatic. Recently, molecular data have genus Anodonthyla was most likely in the South East of Mada- started to decipher microhylid diversity and relation- gascar. ships. Studies of multigene datasets have produced 2 Vences et al. – Five additional species of arboreal microhylid frogs, Madagascar the first comprehensive phylogenies of major micro- runs along the first finger and generally is closely hylid lineages (Van der Meijden et al., 2004, 2007; connected to the first finger over most of its length. Van Bocxlaer et al., 2006) although several basal rela- Correlated to this character, in males and females, the tionships remained unclarified. Phylogenies based on first finger is very short compared to other cophylines. dense taxon sampling of microhylids from New Guin- Anodonthyla at present comprises six species (Blom- ea (Köhler and Günther, 2008) and Madagascar (An- mers-Schlösser, 1975; Blommers-Schlösser and Blanc, dreone et al., 2005b; Wollenberg et al., 2008) provided 1991; Glaw and Vences, 2005, 2007; Fenolio et al., evidence for a high proportion of undescribed diversi- 2007), of which five are arboreal species that breed, as ty, with many candidate species exhibiting high ge- far as known, in holes of tree or bamboo trunks: Ano- netic divergence to all known species. donthyla boulengeri Müller, 1892; A. hutchisoni Feno- In Madagascar, microhylids are represented by lio, Walvoord, Stout, Randrianirina, and Andreone, three subfamilies: the Dyscophinae Boulenger, 1882 2007; A. moramora Glaw and Vences, 2005; A. nigrigu- with one genus and three species, the Scaphiophryni- laris Glaw and Vences, 1992; A. rouxae Guibé, 1974. nae Laurent, 1946 with two genera and ten species, In contrast, Anodonthyla montana Angel, 1925 ap- and the Cophylinae Cope, 1889 with seven genera and pears to be restricted to areas of the granitic Andringi- 45 species (Glaw and Vences, 2007; Fenolio et al., tra massif above the tree line and here breeds in small 2007). Molecular data indicate that scaphiophrynines rock cavities. However, preliminary data already indi- and cophylines together form a clade that is endemic cated that these species numbers are underestimations to Madagascar and has unclarified relationships to since the available molecular and bioacoustic evidence other microhylids, whereas dyscophines form a sepa- pointed to several highly divergent genealogical line- rate evolutionary lineage related to Asian microhylids ages within A. boulengeri, and to geographically high- (Van der Meijden et al., 2007). Although new species ly distant populations within A. nigrigularis that war- of scaphiophrynines have been discovered in the last ranted further taxonomic study (Vallan, 2000; Glaw years (e.g. Glos et al., 2005; Andreone et al., 2006), and Vences, 2005, 2007; Fenolio et al., 2007). Here we the bulk of undescribed microhylid diversity in Mada- present a survey of molecular variation based on mito- gascar is found in the Cophylinae (Wollenberg et al., chondrial genes, in combination with bioacoustic and 2008; Vieites et al., 2009). morphological data from new Anodonthyla collections Cophylines are characterized by a derived mode of mainly obtained through intensive fieldwork over the larval development: whereas most microhylids have past five years. Based on these data we conduct a par- a specialized filter-feeding tadpole, cophylines have tial revision of the genus that leads to the description non-feeding tadpoles that develop either in tree holes, of four new species and the resurrection of one further terrestrial foam nests, or terrestrial jelly nests (Blom- species from synonymy. mers-Schlösser, 1975; Glaw and Vences, 2007; Gros- jean et al., 2007). Most cophylines have very simple advertisement calls, consisting of single melodious Material and methods notes that are repeated after regular intervals and for long periods of time, usually lasting several minutes. Specimens were collected at night by opportunistic Correlated to the reproductive mode of the various searching and localizing calling males, using torches cophyline lineages is their arboreal versus terrestrial and head lamps. They were euthanized in a chlorobu- or fossorial ecology, and apparently, multiple evolu- tanol solution, fixed in 95% ethanol or 7% formalin, tionary shifts between arboreal and terrestrial habits and preserved in 70% ethanol. Locality information have occurred in this subfamily (Andreone et al., was recorded with GPS receivers. Specimens studied 2005b).
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