DOCSLIB.ORG

Vast Underestimation of Madagascar's Biodiversity Evidenced By

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Vast Underestimation of Madagascar's Biodiversity Evidenced By Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory David R. Vieitesa,1, Katharina C. Wollenbergb, Franco Andreonec,Jo¨ rn Ko¨ hlerd, Frank Glawe, and Miguel Vencesb aMuseo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, c/ Jose´Gutierrez Abascal 2, 28006 Madrid, Spain; bZoological Institute, Technical University of Braunschweig, Spielmannstrasse 8, 38106 Braunschweig, Germany; cMuseo Regionale di Scienze Naturali, Via Giolitti 36, 10123 Turin, Italy; dHessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany; and eZoologische Staatssammlung Mu¨nchen, Mu¨nchhausenstrasse 21, 81247 Munich, Germany Edited by David B. Wake, University of California, Berkeley, CA, and approved March 27, 2009 (received for review October 26, 2008) Amphibians are in decline worldwide. However, their patterns of Among terrestrial vertebrates, amphibians are characterized by a diversity, especially in the tropics, are not well understood, mainly rapid rate of species discovery (8, 9), with an overall increase in the because of incomplete information on taxonomy and distribution. number of amphibian species globally of 19.4% during the last We assess morphological, bioacoustic, and genetic variation of decade, reaching 6,449 currently recognized species (10). An im- Madagascar’s amphibians, one of the first near-complete taxon portant acceleration in the rate of new discoveries, mainly from samplings from a biodiversity hotspot. Based on DNA sequences of tropical areas, is obvious from many recent studies (11–16). These 2,850 specimens sampled from over 170 localities, our analyses discoveries are not the result of taxonomic inflation (9, 14, 17), but reveal an extreme proportion of amphibian diversity, projecting an correspond to real divergent species (18, 19). Although high almost 2-fold increase in species numbers from the currently numbers of undescribed amphibians have been estimated to exist in described 244 species to a minimum of 373 and up to 465. This poorly studied tropical regions (11, 15), these results remain un- diversity is widespread geographically and across most major verified for complete, highly diverse amphibian faunas. In parallel, phylogenetic lineages except in a few previously well-studied an increase of threatened amphibian species has been reported genera, and is not restricted to morphologically cryptic clades. We worldwide (8, 20, 21). Amphibians are of high conservation con- classify the genealogical lineages in confirmed and unconfirmed cern, with 43% of species being globally threatened (20), most of EVOLUTION candidate species or deeply divergent conspecific lineages based them in tropical regions with high amphibian diversity. on concordance of genetic divergences with other characters. This Madagascar is one of the top priority global hotspots for integrative approach may be widely applicable to improve esti- biodiversity conservation (1), affected by a high rate of habitat mates of organismal diversity. Our results suggest that in Mada- destruction (22). Its fauna and flora evolved largely in isolation gascar the spatial pattern of amphibian richness and endemism (23), and many taxa are characterized by a high degree of must be revisited, and current habitat destruction may be affecting microendemism within Madagascar (24–27). The native amphib- more species than previously thought, in amphibians as well as in ian fauna is constituted by 5 endemic evolutionary lineages of other animal groups. This case study suggests that worldwide frogs with 100% species-level endemism, 2 of which (the man- tropical amphibian diversity is probably underestimated at an tellids and the cophyline and scaphiophrynine microhylids) are unprecedented level and stresses the need for integrated taxo- very species-rich. Large-scale taxonomic inventories conducted nomic surveys as a basis for prioritizing conservation efforts within since 1991 have led to an increase from 133 to 244 described biodiversity hotspots. species, largely due to the exploration of new areas and the application of more efficient techniques. About 46 species were identified during the 1990s mainly based on bioacoustics; the biodiversity estimates ͉ new candidate species ͉ phylogeny ͉ application of combined methods, including molecular genetics, DNA barcoding was crucial in the discovery of 51 new species since 2000 as well as in the resurrection of species formerly considered to represent he current biodiversity crisis demands the study of broad- synonyms. Tscale spatial variation in species richness and endemism to Undescribed diversity may have an important impact on under- identify areas that merit special conservation attention. Global standing the spatial patterns of endemic radiations on the island, efforts to minimize biodiversity loss have led to prioritizing but objective estimates of species numbers are not available so far. biodiversity hotspots (1) which are defined as areas with high We report a comprehensive assessment of morphological, bio- concentrations of endemic species and that are undergoing acoustic, and genetic variation of the anuran fauna of Madagascar. exceptional habitat loss (2–4). A second step is the efficient Our goals are (i) to provide a reliable estimate of the proportion of implementation of conservation measures at a local scale which yet-undescribed amphibian species from Madagascar and their requires an understanding of spatial patterns of richness and phylogenetic and geographic distribution, (ii) to discuss the impact endemism within these hotspots (5). Assessments of such re- of our findings for global estimates of amphibian diversity, and (iii) gional priority areas are often hampered by incomplete distri- to propose a novel terminology to be better able to assess the butional and taxonomic information. The operational units used increasing number of identified but taxonomically undescribed to assess conservation priority areas are described species, candidate species of animals. whereas estimates of undiscovered and undescribed species are usually ignored. Recently, many potential new species have been Author contributions: D.R.V. and M.V. designed research; D.R.V., K.C.W., F.A., J.K., F.G., and identified by DNA barcoding, but a taxonomic validation of M.V. performed research; D.R.V., K.C.W., J.K., and M.V. analyzed data; and D.R.V. and M.V. these species will outdate the short time span left for efficient wrote the paper. biodiversity conservation prioritization, and so far it is not clear The authors declare no conflict of interest. how this undescribed diversity can nonetheless be considered. This article is a PNAS Direct Submission. This undescribed diversity also bears relevance for understand- Data deposition: The sequences reported in this paper have been deposited in the Genbank ing the tree of life: The completeness of taxon sampling is one database (accession nos. FJ559069–FJ559372 and FJ217329–FJ217345) of the major prerequisites for reliable phylogenetic analysis, 1To whom correspondence should be addressed. E-mail: [email protected]. reconstruction of character evolution, and inference of macro- This article contains supporting information online at www.pnas.org/cgi/content/full/ evolutionary processes (6, 7). 0810821106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810821106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 30, 2021 Fig. 1. Phylogenetic, geographic, and historical pat- terns of undescribed amphibian diversity in Madagas- car. (A) Bayesian phylogenetic tree of 236 (out of 244) described species and 258 deeply divergent genealog- ical lineages of Malagasy frogs (among them 129 CCS and 92 UCS and 37 DCL with Ͼ3% genetic divergence to nearest described neighbor) based on a fragment of the mitochondrial 16S rRNA gene. Circles represent CCS (brown), UCS (orange), and DCL (light orange). Inset photos show some of these forms (see SI Appen- dix). He, Heterixalus (Hyperoliidae); Dy, Dyscophus; Sc, Scaphiophryninae; Co, Cophylinae (Microhylidae); Sp, Spinomantis; Md, Mantidactylus; Mt, Mantella; Gu, Guibemantis; Ge, Gephyromantis; Bo, Boophis; Bl, Blommersia; Ag, Aglyptodactylus (Mantellidae). (B and C) Maps of collecting localities of described species (B) and of CCS and UCS (C) of Malagasy frogs, and remain- ing primary vegetation (evergreen forests, blue; non- evergreen forests, gray). Current protected area net- work is shown in red. (D) Cumulative number of species currently considered as valid per 10-year intervals (2001–2008 for the current decade), and the CCS, UCS, and DCL identified in the present paper. (E) Total num- bers of described species and CCS, UCS, and DCL in major clades of Malagasy frogs. Results frogs, indicating that they are not the result of taxonomic inflation From our integrative analyses of morphological, bioacoustic, and (e.g., elevating subspecies to specific status). genetic data, we identified many more species of Malagasy frogs New discoveries are also geographically ubiquitous. They occur than there are names available. The number of described species throughout Madagascar, both in poorly explored and in better- of Malagasy frogs has slowly increased during the 20th century, studied areas. Described species are known from 451 sites and reaching 100 described species around 1940, and 133 at the time 87.3% are found in protected areas, whereas CCS and UCS are of the last monographic account in 1991 (28) (Fig. 1). The known from 168 sites and only 66.4% are
Load more

Recommended publications
  • Blumgart Et Al 2017- Herpetological Survey Nosy Komba
    Journal of Natural History ISSN: 0022-2933 (Print) 1464-5262 (Online) Journal homepage: http://www.tandfonline.com/loi/tnah20 Herpetological diversity across intact and modified habitats of Nosy Komba Island, Madagascar Dan Blumgart, Julia Dolhem & Christopher J. Raxworthy To cite this article: Dan Blumgart, Julia Dolhem & Christopher J. Raxworthy (2017): Herpetological diversity across intact and modified habitats of Nosy Komba Island, Madagascar, Journal of Natural History, DOI: 10.1080/00222933.2017.1287312 To link to this article: http://dx.doi.org/10.1080/00222933.2017.1287312 Published online: 28 Feb 2017. Submit your article to this journal Article views: 23 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tnah20 Download by: [BBSRC] Date: 21 March 2017, At: 02:56 JOURNAL OF NATURAL HISTORY, 2017 http://dx.doi.org/10.1080/00222933.2017.1287312 Herpetological diversity across intact and modified habitats of Nosy Komba Island, Madagascar Dan Blumgart a, Julia Dolhema and Christopher J. Raxworthyb aMadagascar Research and Conservation Institute, BP 270, Hellville, Nosy Be, Madagascar; bDivision of Vertebrate Zoology, American, Museum of Natural History, New York, NY, USA ABSTRACT ARTICLE HISTORY A six month herpetological survey was undertaken between March Received 16 August 2016 and September 2015 on Nosy Komba, an island off of the north- Accepted 17 January 2017 west coast of mainland Madagascar which has undergone con- KEYWORDS fi siderable anthropogenic modi cation. A total of 14 species were Herpetofauna; conservation; found that have not been previously recorded on Nosy Komba, Madagascar; Nosy Komba; bringing the total island diversity to 52 (41 reptiles and 11 frogs).
    [Show full text]
  • Blanchard's Cricket Frog
    NOTES 129 BLANCHARD’S CRICKET FROG IN NEBRASKA AND SOUTH DAKOTA -- Blanchard’s cricket frog (Acris crepitans blanchardi) is a small warty anuran known for its exceptional leaping ability and is common along stream banks and ponds throughout much of the eastern two-thirds of North America. Its color pattern is highly variable being comprised of greens, reds, browns, and grays, culminating frequently in a stripe or series of splotches arranged along the cranial- caudal dorsal midline. The Blanchard’s cricket frog can often be identified by a small triangle pointing caudally, whose base extends between each eye (Harper 1947). Other stripes and lines are not uncommon. In South Dakota the range of Blanchard’s cricket frog is limited to the extreme south-central and southeastern counties; in Nebraska, the species is known statewide. Despite the lack of natural history information on Blanchard’s cricket frog in Nebraska and South Dakota, several studies from other states have provided a substantial amount of life history data for this species (Johnson and Christiansen 1976; Gray 1983, 1984; Burkett 1984). Harper (1947) described Blanchard’s cricket frog with mean snout-vent lengths (SVL) of 24.1 mm for adult males and 29.2 for adult females. Average body mass was determined to be 1.3 g for adult males and 2.2 g for adult females. In Iowa, Blanchard’s cricket frog attains its maximum body size between June and July (Johnson and Christiansen 1976), whereas maximum body size is attained as early as May in Kansas (Burkett 1984). These frogs appear to be active from April through October in Iowa (Johnson and Christiansen 1976) and from March through December in Kansas (Burkett 1984).
    [Show full text]
  • Which Frogs Are out There? a Preliminary Evaluation of Survey Techniques and Identification Reliability of Malagasy Amphibians
    A Conservation Strategy for the Monografie del Museo Regionale di Scienze Naturali Amphibians of Madagascar di Torino, XLV (2008): pp. 233-252 Miguel VENCES1, Ylenia CHIARI2, Meike TESCHKE3, Roger-Daniel RANDRIANIAINA1, Liliane RAHARIVOLOLONIAINA4, Parfait BORA4, David R. VIEITES5, Frank GLAW6 Which frogs are out there? A preliminary evaluation of survey techniques and identification reliability of Malagasy amphibians ABSTRACT We provide an estimate of identification reliability of Malagasy frog species based on different methods. According to our estimate, for 168 out of 358 species, a reliable identification based on morphology alone is not possible for reasonably trained researchers. By also considering colouration in life, this number went down to 116 species. Of 252 species for which calls are known, a reliable identification based exclusively on bioacoustics is not possible for 59 species. DNA barcoding performs distinctly better; problems with molecular identification are only known for 61 out of 347 species for which genetic data are available. In a second approach we also present preliminary data on a comparative study of performance of various inventory techniques applied to three frog communities along eastern rainforest streams. At these streams tadpole collection and their subsequent identification via DNA barcoding allowed for an average detection success of 45% of all species per site, while standardized call surveys detected 28% and visual encounter surveys 29% of the species. However, these results varied widely among rough ecological guilds of frogs, with forest frogs that breed independently from open water, obviously, being undetectable in the tadpole surveys, arboreal frogs being poorly detectable in visual encounter surveys, and stream edge frogs being very poorly detectable in bioacoustic surveys.
    [Show full text]
  • Analyses of Proposals to Amend
    CoP17 Prop. 38 Inclusion of False Tomato Frog Dyscophus guineti and Antsouhy Tomato Frog D. insularis in Appendix II Proponent: Madagascar Summary: The False Tomato Frog Dyscophus guineti and the Antsouhy Tomato Frog D. insularis comprise two of three species in the genus Dyscophus, all of which are endemic to Madagascar. The third species, D. antongilii was included in Appendix I in 1987. It is subject to a separate proposal to be transferred from Appendix I to Appendix II (Proposal 37). All three are attractive red-orange coloured frogs. Dyscophus are known to breed explosively with the availability of water during the rainy season (typically January-March) and during that time they can be found in abundance at breeding sites. Hundreds of eggs are laid in water following mating. Dyscophus guineti The known distribution of D. guineti includes a number of patches in the remnant central eastern rainforest of Madagascar. The species is secretive and believed likely to be more widespread than records indicate1. Overall population is unknown; locally the species can vary from extremely common to very rare1. Sexual maturity is attained between two and four years, comparatively earlier in males than in females2. The habitat of the species is affected by conversion of forest to agriculture, timber extraction, charcoal production and potentially small-scale mining activities. The species reportedly does not tolerate severe degredation1. There is not known to be local use of the species. As a consequence of the Appendix-I listing in 1987 of the similar Dyscophus antongilii, collectors interested in "red Dyscophus" have shifted their attention to D.
    [Show full text]
  • Congolius, a New Genus of African Reed Frog Endemic to The
    www.nature.com/scientificreports OPEN Congolius, a new genus of African reed frog endemic to the central Congo: A potential case of convergent evolution Tadeáš Nečas1,2*, Gabriel Badjedjea3, Michal Vopálenský4 & Václav Gvoždík1,5* The reed frog genus Hyperolius (Afrobatrachia, Hyperoliidae) is a speciose genus containing over 140 species of mostly small to medium-sized frogs distributed in sub-Saharan Africa. Its high level of colour polymorphism, together with in anurans relatively rare sexual dichromatism, make systematic studies more difcult. As a result, the knowledge of the diversity and taxonomy of this genus is still limited. Hyperolius robustus known only from a handful of localities in rain forests of the central Congo Basin is one of the least known species. Here, we have used molecular methods for the frst time to study the phylogenetic position of this taxon, accompanied by an analysis of phenotype based on external (morphometric) and internal (osteological) morphological characters. Our phylogenetic results undoubtedly placed H. robustus out of Hyperolius into a common clade with sympatric Cryptothylax and West African Morerella. To prevent the uncovered paraphyly, we place H. robustus into a new genus, Congolius. The review of all available data suggests that the new genus is endemic to the central Congolian lowland rain forests. The analysis of phenotype underlined morphological similarity of the new genus to some Hyperolius species. This uniformity of body shape (including cranial shape) indicates that the two genera have either retained ancestral morphology or evolved through convergent evolution under similar ecological pressures in the African rain forests. African reed frogs, Hyperoliidae Laurent, 1943, are presently encompassing almost 230 species in 17 genera.
    [Show full text]
  • Cop17 Prop. 37
    Original language: English CoP17 Prop. 37 CONVENTION ON INTERNATIONAL TRADE IN ENDANGERED SPECIES OF WILD FAUNA AND FLORA ____________________ Seventeenth meeting of the Conference of the Parties Johannesburg (South Africa), 24 September – 5 October 2016 CONSIDERATION OF PROPOSALS FOR AMENDMENT OF APPENDICES I AND II A. Proposal Downlisting of Dyscophus antongilii from Appendix I to Appendix II B. Proponent Madagascar* C. Supporting statement 1. Taxonomy 1.1 Class: Amphibia 1.2 Order: Anura 1.3 Family: Microhylidae Gunther 1859, subfamily Dyscophinae 1.4 Genus, species: Dyscophus antongilii Grandidieri 1877 1.5 Scientific synonyms: 1.6 Common names: English: Tomato Frog French: La grenouille tomate, crapaud rouge de Madagascar Malagasy: Sahongoangoana, Sangongogna, Sahogongogno (and similar writings) 2. Overview The genus Dyscophus contains three species of large microhylids composing the subfamily Dyscophinae endemic to Madagascar. D. antongilii, D. guineti and D. insularis. Dyscophus antongilii is red-orange in coloration and commonly called the tomato frogs because of its appearance. It is well-known and iconic amphibian species. Described by Alfred Grandidier in the 1877, D. antongilii occurs in a moderate area of northeast and east of Madagascar. Dyscophus antongilii has been listed within CITES Appendix I since 1987 while the other two species currently have no CITES listing but proposed to be inserted into Appendix II for this year by a separate proposal. Some studies on the species led by F. Andreone demonstrate that this species is frequently found outside of protected area and one of the strategies to conservation purpose is the trade. The species is listed as Near Threatened on the IUCN Red List.
    [Show full text]
  • Correlates of Eye Colour and Pattern in Mantellid Frogs
    SALAMANDRA 49(1) 7–17 30Correlates April 2013 of eyeISSN colour 0036–3375 and pattern in mantellid frogs Correlates of eye colour and pattern in mantellid frogs Felix Amat 1, Katharina C. Wollenberg 2,3 & Miguel Vences 4 1) Àrea d‘Herpetologia, Museu de Granollers-Ciències Naturals, Francesc Macià 51, 08400 Granollers, Catalonia, Spain 2) Department of Biology, School of Science, Engineering and Mathematics, Bethune-Cookman University, 640 Dr. Mary McLeod Bethune Blvd., Daytona Beach, FL 32114, USA 3) Department of Biogeography, Trier University, Universitätsring 15, 54286 Trier, Germany 4) Zoological Institute, Division of Evolutionary Biology, Technical University of Braunschweig, Spielmannstr. 8, 38106 Braunschweig, Germany Corresponding author: Miguel Vences, e-mail: [email protected] Manuscript received: 18 March 2013 Abstract. With more than 250 species, the Mantellidae is the most species-rich family of frogs in Madagascar. These frogs are highly diversified in morphology, ecology and natural history. Based on a molecular phylogeny of 248 mantellids, we here examine the distribution of three characters reflecting the diversity of eye colouration and two characters of head colouration along the mantellid tree, and their correlation with the general ecology and habitat use of these frogs. We use Bayesian stochastic character mapping, character association tests and concentrated changes tests of correlated evolu- tion of these variables. We confirm previously formulated hypotheses of eye colour pattern being significantly correlated with ecology and habits, with three main character associations: many tree frogs of the genus Boophis have a bright col- oured iris, often with annular elements and a blue-coloured iris periphery (sclera); terrestrial leaf-litter dwellers have an iris horizontally divided into an upper light and lower dark part; and diurnal, terrestrial and aposematic Mantella frogs have a uniformly black iris.
    [Show full text]
  • New Sahonagasy Action Plan 2016-2020
    New Sahonagasy Action Plan 2016-2020 1 New Sahonagasy Action Plan 2016 – 2020 Nouveau plan d’Action Sahonagasy 2016 – 2020 Edited by: Franco Andreone, IUCN SSC Amphibian Specialist Group - Madagascar Jeff S. Dawson, Durrell Wildlife Conservation Trust Falitiana C. E. Rabemananjara, IUCN SSC Amphibian Specialist Group - Madagascar Nirhy H.C. Rabibisoa, IUCN SSC Amphibian Specialist Group - Madagascar Tsanta F. Rakotonanahary, Durrell Wildlife Conservation Trust With assistance from: Candace M. Hansen-Hendrikx, Amphibian Survival Alliance James P. Lewis, Amphibian Survival Alliance/Rainforest Trust Published by: Museo Regionale di Scienze Naturali (Turin, Italy) and Amphibian Survival Alliance (Warrenton, VA) Publication date: June 2016 Recommended citation: Andreone, F., Dawson, J.S., Rabemananjara, F.C.E., Rabibisoa, N.H.C. & Rakotonanahary, T.F. (eds). 2016. New Sahonagasy Action Plan 2016–2020 / Nouveau Plan d'Action Sahonagasy 2016–2020. Museo Regionale di Scienze Naturali and Amphibian Survival Alliance, Turin. ISBN: 978-88-97189-26-8 Layout by: Candace M. Hansen-Hendrikx, Amphibian Survival Alliance Translation into French: Mathilde Malas, Speech Bubbles, www.speechbubbles.eu Printed by: Centro Stampa Regione Piemonte, Turin Front cover: Spinomantis aglavei, Gonçalo M. Rosa Back cover: Mantella expectata, Gonçalo M. Rosa IUCN - International Union for Conservation of Nature Founded in 1948, The International Union for Conservation of Nature brings together States, government agencies and a diverse range of nongovernmental organizations in a unique world partnership: over 1,000 members in all spread across some 140 countries. As a Union, IUCN seeks to influence, encourage and assist societies throughout the world to conserve the integrity and diversity of nature and to ensure that any use of natural resources is equitable and ecologically sustainable.
    [Show full text]
  • Overwintering Physiology and Hibernacula Microclimates of Blanchard’S Cricket Frogs at Their Northwestern Range Boundary
    Copeia 2010, No. 2, 247–253 Overwintering Physiology and Hibernacula Microclimates of Blanchard’s Cricket Frogs at Their Northwestern Range Boundary David L. Swanson1 and Seth L. Burdick1 Blanchard’s Cricket Frogs (Acris crepitans blanchardi) in the central portion of their range show minimal capacities for freezing tolerance and survive overwinter by using terrestrial hibernacula where they avoid freezing. However, frogs may exhibit greater freeze-tolerance capacity at high latitude range limits, where winter climate is more severe. We studied freezing tolerance, glucose mobilization during freezing, and hibernacula microclimates of cricket frogs in southeastern South Dakota, at the northwestern limit of their range. Cricket frogs from South Dakota generally survived freezing exposure at 21.5 to 22.5uC for 6-h periods (80% survival), but uniformly died when exposed to these same temperatures for 24-h freezing bouts. Hepatic glucose levels and phosphorylase a activities increased significantly during freezing, but hepatic glucose levels during freezing remained low, only reaching levels approximating those prior to freezing in freeze-tolerant species. Moreover, muscle glucose and hepatic glycogen levels did not vary with freezing, suggesting little mobilization of glucose from hepatic glycogen stores during freezing, contrasting with patterns in freeze-tolerant frogs. Temperatures in soil cracks and burrows potentially used for hibernacula were variable, with some sites remaining above the freezing point of the body fluids throughout the winter, some sites dropping below the freezing point for only short periods, and some sites dropping below the freezing point for extended periods. These data suggest that cricket frogs in South Dakota, as in other portions of their range, survive overwinter by locating hibernacula that prevent freezing, although their toleration of short freezing bouts may expand the range of suitable hibernacula.
    [Show full text]
  • Widespread Presence of the Pathogenic Fungus Batrachochytrium Dendrobatidis in Wild Amphibian Communities in Madagascar
    OPEN Widespread presence of the pathogenic SUBJECT AREAS: fungus Batrachochytrium dendrobatidis CONSERVATION BIOLOGY in wild amphibian communities in MOLECULAR ECOLOGY Madagascar Received 1,2 3,4,5 6,7 8,9 10,11 7 August 2014 Molly C. Bletz *, Gonçalo M. Rosa *, Franco Andreone , Elodie A. Courtois , Dirk S. Schmeller , Nirhy H. C. Rabibisoa7,12, Falitiana C. E. Rabemananjara7,13, Liliane Raharivololoniaina13, Accepted Miguel Vences2, Che´ Weldon14, Devin Edmonds15, Christopher J. Raxworthy16, Reid N. Harris1, 12 January 2015 Matthew C. Fisher17 & Angelica Crottini18 Published 26 February 2015 1Department of Biology, James Madison University, Harrisonburg, VA 22807, USA, 2Technische Universita¨t Braunschweig, Division of Evolutionary Biology, Zoological Institute, Mendelssohnstr. 4, 38106 Braunschweig, Germany, 3Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury, Kent CT2 7NR, UK, 4Institute Correspondence and of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK, 5Centre for Ecology, Evolution and Environmental requests for materials Changes (CE3C), Faculdade de Cieˆncias da Universidade de Lisboa, Bloco 2, Piso 5, Campo Grande, 1749-016 Lisbon, Portugal, should be addressed to 6Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, I-10123, Torino, Italy, 7IUCN SSC Amphibian Specialist 8 M.C.B. (molly.bletz@ Group-Madagascar, 101 Antananarivo, Madagascar, CNRS-Guyane, USR 3456, 2 avenue Gustave Charlery, 97300 Cayenne, Guyane Française, 9Station d’e´cologie expe´rimentale du CNRS a` Moulis, USR 2936, 2 route du CNRS, 09200 Moulis, France, gmail.com); G.M.R. 10UFZ – Helmholtz Centre for Environmental Research, Department of Conservation Biology, Permoserstr. 15, 04318 Leipzig, (goncalo.m.rosa@ Germany, 11EcoLab (Laboratoire Ecologie Fonctionnelle et Environnement), CNRS/Universite´ de Toulouse; UPS, INPT; 118 route de gmail.com) or F.A.
    [Show full text]
  • Larval Morphology and Development of the Malagasy Frog Mantidactylus Betsileanus
    SALAMANDRA 49(4) 186–200 30 December 2013Sarah ScheldISSN 0036–3375 et al. Larval morphology and development of the Malagasy frog Mantidactylus betsileanus Sarah Scheld 1,2,4, R. G. Bina Perl 1,2,3, Anna Rauhaus 1, Detlef Karbe 1, Karin van der Straeten 1, J. Susanne Hauswaldt 3, Roger Daniel Randrianiaina 3, Anna Gawor 1, Miguel Vences 3 & Thomas Ziegler 1,2 1) Cologne Zoo, Riehler Str. 173, 50735 Köln, Germany 2) Cologne Biocenter, University of Cologne, Zülpicher Str. 47b, 50674 Köln, Germany 3) Zoological Institute, Technical University of Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany 4) Institute of Ecology, University of Innsbruck, Technikerstr. 25, 6020 Innsbruck, Austria Corresponding author: Thomas Ziegler, e-mail: [email protected] Manuscript received: 21 September 2013 Abstract. The Mantellidae is a species-rich family of neobatrachian frogs endemic to Madagascar and Mayotte. Although tadpoles have been described from many mantellids, detailed studies of their early embryonic development are rare. We provide a documentation of the developmental stages of Mantidactylus betsileanus, a common mantellid frog of Madagas- car’s eastern rainforests, based on clutches deposited and raised in captivity. Metamorphosis was completed after 89 days on average. External gills were not recognizable in the embryos, similar to three other, previously studied mantellids, which apparently constitutes a difference to the mantellid sister group, the Rhacophoridae. We also provide updated de- scriptions of the species’ larval morphology at stage 25 and stage 36, respectively, from captive bred and wild-caught indi- viduals, and report variations in the keratodont row formula from 0/2, 1/1, 1/3 to 1:1+1/3.
    [Show full text]
  • Miocene Plio-Pleistocene Oligocene Eocene Paleocene Cretaceous
    Phrynomantis microps Hemisus sudanensis Hemisus marmoratus Balebreviceps hillmani Breviceps mossambicus Breviceps adspersus Breviceps montanus Breviceps fuscus Breviceps gibbosus Breviceps macrops Breviceps namaquensis Breviceps branchi Spelaeophryne methneri Probreviceps loveridgei Probreviceps uluguruensis Probreviceps durirostris Probreviceps sp. Nguru Probreviceps sp. Rubeho Probreviceps sp. Kigogo Probreviceps sp. Udzungwa Probreviceps rungwensis Probreviceps macrodactylus Callulina shengena Callulina laphami Callulina dawida Callulina kanga Callulina sp lowland Callulina sp Rubeho Callulina hanseni Callulina meteora Callulina stanleyi Callulina kisiwamsitu Callulina kreffti Nyctibates corrugatus Scotobleps gabonicus Astylosternus laticephalus Astylosternus occidentalis Trichobatrachus robustus Astylosternus diadematus Astylosternus schioetzi Astylosternus batesi Leptodactylodon mertensi Leptodactylodon erythrogaster Leptodactylodon perreti Leptodactylodon axillaris Leptodactylodon polyacanthus Leptodactylodon bicolor Leptodactylodon bueanus Leptodactylodon ornatus Leptodactylodon boulengeri Leptodactylodon ventrimarmoratus Leptodactylodon ovatus Leptopelis parkeri Leptopelis macrotis Leptopelis millsoni Leptopelis rufus Leptopelis argenteus Leptopelis yaldeni Leptopelis vannutellii Leptopelis susanae Leptopelis gramineus Leptopelis kivuensis Leptopelis ocellatus Leptopelis spiritusnoctis Leptopelis viridis Leptopelis aubryi Leptopelis natalensis Leptopelis palmatus Leptopelis calcaratus Leptopelis brevirostris Leptopelis notatus
    [Show full text]