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Type: Article
Published: 2024-01-08
Page range: 451-485
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Unexpected diversity and co-occurrence of phytotelmic frogs (Guibemantis) around Andasibe, one of the most intensively surveyed amphibian hotspots of Madagascar, and descriptions of three new species

Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
Hessisches Landesmuseum Darmstadt; Friedensplatz 1; 64283 Darmstadt; Germany
Mention Zoologie et Biodiversité Animale; Université d’Antananarivo; BP 906; Antananarivo; 101 Madagascar
Illinois Natural History Survey; University of Illinois Urbana-Champaign; USA
Universidad de A Coruña; Facultad de Ciencias; Campus de A Zapateira; s/n; (Grupo de Investigación en Biología Evolutiva; GIBE); E-15071 A Coruña; Spain
Zoologische Staatssammlung München (ZSM-SNSB); Münchhausenstr. 21; 81247 München; Germany
The College of Wooster; Department of Biology; 931 College Mall; Wooster; Ohio; 44691 USA
Mention Agriculture; Universite de l’Itasy; Faliarivo Ambohidanerana; 118 Soavinandriana Itasy; Madagascar; School for International Training; VN 41A Bis Ankazolava Ambohitsoa; Antananarivo; 101 Madagascar
Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
Amphibia Anura Mantellidae Pandanusicola Guibemantis rianasoa sp. nov. Guibemantis ambakoana sp. nov. Guibemantis vakoa sp. nov. Pandanus bioacoustics phytotelmic breeding microendemism sympatry phylogeny systematics taxonomy

Abstract

The area around the Malagasy village of Andasibe, which includes Analamazaotra-Mantadia National Park as well as other protected areas, is characterized by very species-rich and well-studied communities of animals and plants, but new species are still regularly discovered. Three species of phytotelmic frogs of the subgenus Pandanusicola in the genus Guibemantis are known from this area, G. flavobrunneus, G. liber, and G. pulcher. Further Pandanusicola frogs from this area have been provisionally assigned to G. bicalcaratus or G. albolineatus, pending detailed taxonomic review. During preliminary exploration of the ecology of these specialized frogs that live and reproduce in the leaf axils of Pandanus screw pines, we noticed the syntopic presence of two differently colored and differently sized Pandanusicola in Andasibe that could not be unambiguously assigned to any known species. A genetic screening revealed that these correspond to yet two further species in the area. Based on our data, seven species of Pandanusicola occur in Andasibe and nearby forests: (1) G. liber, the only non-phytotelmic species of the subgenus in the region; (2) G. flavobrunneus which is the largest species and characterized by a diagnostic yellowish brown dorsal pattern; (3) G. pulcher, characterized by translucent-green color with purplish brown spotting not observed in any other species in the area; (4) G. methueni, a brownish species usually lacking contrasted dorsolateral bands that differs from the other species in the area by emitting a characteristic trill-like advertisement call series (rather than clicks or chirps) and according to our data is widespread along Madagascar’s east coast; as well as three new species: (5) G. ambakoana sp. nov., a brownish species, typically with contrasted incomplete light dorsolateral bands and with single click-like advertisement calls; (6) G. vakoa sp. nov., a species that is equally brownish but lacks contrasted light dorsolateral bands and that has single click-like advertisement calls of very short duration; and (7) G. rianasoa sp. nov., a species that is smaller sized and has less distinct femoral glands than all the others, and emits a short series of soft chirp-like advertisement calls. All these species are genetically highly distinct, with >5% uncorrected pairwise distances in the mitochondrial 16S rRNA gene, and lack of haplotype sharing in two nuclear-encoded genes. The co-occurrence of seven Pandanusicola frogs in a relatively small geographic area is unprecedented in Madagascar and calls for in-depth studies of a possible differentiation in habitat use and life history.

 

References

  1. AmphibiaWeb (2023) Information on amphibian biology and conservation. AmphibiaWeb, Berkeley, California. Available from: http://amphibiaweb.org/ (accessed 26 July 2023)
  2. Avise, J.C. & Ball, R.M. (1990) Principles of genealogical concordance in species concepts and biological taxonomy. In: Futuyma, D. & Antonovics, J. (Eds.), Oxford Surveys in Evolutionary Biology. Oxford University Press, Oxford, pp. 45–67.
  3. Bletz, M.C., Scherz, M.D., Rakotoarison, A., Lehtinen, R.M., Glaw, F. & Vences, M. (2018) Stumbling upon a new frog species of Guibemantis (Anura: Mantellidae) on the top of the Marojejy massif in northern Madagascar. Copeia, 106, 255–263. https://doi.org/10.1643/CH-17-655
  4. Blommers-Schlösser, R.M.A. (1975) A unique case of mating behaviour in a Malagasy tree frog, Gephyromantis liber (Peracca 1893), with observations on the larval development (Amphibia, Ranidae). Beaufortia, 23, 15–23.
  5. Blommers-Schlösser, R.M.A. (1979) Biosystematics of the Malagasy frogs. I. Mantellinae (Ranidae). Beaufortia, 29, 1–77.
  6. 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. https://doi.org/10.1016/j.ympev.2007.05.028
  7. Brown, J.L., Cameron, A., Yoder, A.D. & Vences, M. (2014) A necessarily complex model to explain the biogeography of the amphibians and reptiles of Madagascar. Nature Communications, 5, e5046. https://doi.org/10.1038/ncomms6046
  8. Brown, J.L., Sillero, N., Glaw, F., Bora, P., Vieites, D.R. & Vences, M. (2016) Spatial biodiversity patterns of Madagascar’s amphibians and reptiles. PloS ONE, 11, e0144076. https://doi.org/10.1371/journal.pone.0144076
  9. Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Single-locus and multilocus DNA fingerprint. In: Hoelzel, A.R. (Ed.), Molecular Genetic Analysis of Populations: A Practical Approach. IRL Press, Oxford, pp. 225–270.
  10. Callmander, M.W., Laivao, M.O. & Buerki, S. (2022) Pandanaceae, screw-pines, vakoa, hofa, frandra. In: Goodman, S.M. (Ed.), The New Natural History of Madagascar. Princeton University Press, Princeton, pp. 551–559. https://doi.org/10.2307/j.ctv2ks6tbb.67
  11. Chan, K.O., Hertwig, S.T., Neokleous, D.N., Flury, J.M. & Brown, R.M. (2022) Widely used, short 16S rRNA mitochondrial gene fragments yield poor and erratic results in phylogenetic estimation and species delimitation of amphibians. BMC Ecology and Evolution, 22, 37. https://doi.org/10.1186/s12862-022-01994-y.
  12. Colwell, R.K. & Lees, D.C. (2000) The mid-domain effect: geometric constraints on the geography of species richness. Trends in Ecology & Evolution, 15, 70–76. https://doi.org/10.1016/S0169-5347(99)01767-X
  13. Crottini, A., Madsen, O., Poux, C., Strauß, A., Vieites, D.R. & Vences, M. (2012) Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K–T boundary in Madagascar. Proceedings of the National Academy of Sciences, 109, 5358–5363. https://doi.org/10.1073/pnas.1112487109
  14. Delić, T., Trontelj, P., Rendoš, M. & Fišer, C. (2017) The importance of naming cryptic species and the conservation of endemic subterranean amphipods. Scientific Reports, 7, 3391. https://doi.org/10.1038/s41598-017-02938-z
  15. de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms. Species and Speciation. Oxford University Press, Oxford, pp. 49–89.
  16. de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083
  17. Dufresnes, C., Brelsford, A., Jeffries, D.L., Mazepa, G., Suchan, T., Canestrelli, D., Nicieza, A., Fumagalli, L., Dubey, S., Martínez-Solano, I., Litvinchuk, S.N., Vences, M., Perrin, N. & Crochet, P.A. (2021) Mass of genes rather than master genes underlie the genomic architecture of amphibian speciation. Proceedings of the National Academy of Sciences of the USA, 118, e2103963118. https://doi.org/10.1073/pnas.2103963118
  18. Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2021) raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12, 373–377. https://doi.org/10.1111/2041-210X.13512
  19. Fedosov, A., Achaz, G., Gontchar, A. & Puillandre, N. (2022) mold, a novel software to compile accurate and reliable DNA diagnoses for taxonomic descriptions. Molecular Ecology Resources, 22, 2038–2053. https://doi.org/10.1111/1755-0998.13590.
  20. Fišer, C., Robinson, C.T. & Malard, F. (2018) Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology, 27, 613–635. https://doi.org/10.1111/mec.14486
  21. 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. https://doi.org/10.1371/journal.pone.0001109
  22. Fulgence, T.R., Martin, D.A., Kreft, H., Ratsoavina, F.M. & Andrianarimisa, A. (2020) Spider traps amphibian in northeastern Madagascar. Ecology and Evolution, 11, 682–687. https://doi.org/10.1002/ece3.7102
  23. Glaw, F., Köhler, J., Crottini, A., Gehring, P.-S., Prötzel, D., Randriamanana, L., Andreone, F. & Vences, M. (2021) An additional level of cryptic diversity: A new green-coloured Malagasy treefrog of the Boophis luteus species group. Salamandra, 57, 295–308.
  24. Glaw, F. & Vences, M. (1994) A Fieldguide to the Amphibians and Reptiles of Madagascar. 2nd Edition, including Mammals and Freshwater Fish. Vences and Glaw Verlag, Cologne.
  25. Glaw, F. & Vences, M. (2006) Phylogeny and genus-level classification of mantellid frogs. Organisms Diversity and Evolution, 6, 236–253. https://doi.org/10.1016/j.ode.2005.12.001
  26. Glaw, F. & Vences, M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar, 3rd Edition. Vences and Glaw Verlag, Cologne, 496 pp.
  27. Glaw, F., Vences, M. & Gossmann, V. (2000) A new species of Mantidactylus (subgenus Guibemantis) from Madagascar, with a comparative survey of internal femoral gland structure in the genus (Amphibia: Ranidae: Mantellinae). Journal of Natural History, 34, 1135–1154. https://doi.org/10.1080/00222930050020140
  28. Goodman, S.M. (2010) Biological research conducted in the general Andasibe region of Madagascar with emphasis on enumerating the local biotic diversity. Malagasy Nature, 3, 13–34.
  29. Guillaumet, J.L. (1973) Formes et développement des «Pandanus» malgaches. Webbia, 28 (2), 495–519. https://doi.org/10.1080/00837792.1973.10670009
  30. Heinermann, J., Rodríguez, A., Segev, O., Edmonds, D., Dolch, R. & Vences, M. (2015) Year-round activity patterns in a hyperdiverse community of rainforest amphibians in Madagascar. Journal of Natural History, 49, 2213–2231. https://doi.org/10.1080/00222933.2015.1009513
  31. Jörger, K.M. & Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10, 59. https://doi.org/10.1186/1742-9994-10-59
  32. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
  33. Köhler, J., Jansen, M., Rodríguez, A., Kok, P.J.R., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rödel, M.O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 1–124. https://doi.org/10.11646/zootaxa.4251.1.1
  34. Koppetsch, T., Pabijan, M., Hutter, C.R., Köhler, J., Gehring, P.-S., Rakotoarison, A., Ratsoavina, F.M., Scherz, M.D., Vieites, D.R., Glaw, F. & Vences, M. (2023) An initial molecular resolution of the mantellid frogs of the Guibemantis liber complex reveals three new species from northern Madagascar. Vertebrate Zoology, 73, 397–432. https://doi.org/10.3897/vz.73.e94063
  35. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  36. Lees, D.C. (1994) The Périnet effect? Diversity gradients in an adaptive radiation of butterflies in Madagascar (Satyrinae: Mycalesina) compared with other rainforest taxa. In: Lourenço W.R. (Ed.), Biogéographie de Madagascar. Editions de l'ORSTOM 1996, Paris, pp. 479–90.
  37. Lehtinen, R.M. (2002) The use of screw pines (Pandanus spp.) by amphibians and reptiles in Madagascar. Herpetological Bulletin, 82, 20–25.
  38. Lehtinen, R.M. (2003) Parental care and reproduction in two species of Mantidactylus (Anura: Mantellidae). Journal of Herpetology, 37, 766–768. https://doi.org/10.1670/87-03N
  39. Lehtinen, R.M. (2004) Tests for competition, cannibalism, and priority effects in two phytotelm-dwelling tadpoles from Madagascar. Herpetologica, 60, 1–13. https://doi.org/10.1655/02-88
  40. Lehtinen, R.M. (2005) Competitive interactions and distributional dynamics in two Malagasy frogs. Journal of Tropical Ecology, 21, 569–576. https://doi.org/10.1017/S0266467405002580
  41. Lehtinen, R.M. (2009) The natural history of two plant-breeding frogs from Madagascar, Guibemantis bicalcaratus and G. punctatus (Anura: Mantellidae). Salamandra, 45, 39–49.
  42. Lehtinen, R.M., Glaw, F., Andreone, F., Pabijan, M. & Vences, M. (2012) A new species of putatively pond breeding frog of the genus Guibemantis from Madagascar. Copeia, 2012, 648–662. https://doi.org/10.1643/CH-11-128
  43. Lehtinen, R.M., Glaw, F., Vences, M., Rakotoarison, A. & Scherz, M.D. (2018) Two new Pandanus frogs (Guibemantis: Mantellidae: Anura) from northern Madagascar. European Journal of Taxonomy, 451, 1–20. https://doi.org/10.5852/ejt.2018.451
  44. Lehtinen, R.M., Glaw, F. & Vences, M. (2011) Two new plant-breeding frog species (Anura: Mantellidae, Guibemantis) from southeastern Madagascar. Herpetological Journal, 21, 95–112.
  45. Lehtinen, R.M. & Carfagno, G.L. (2011) Habitat selection, the included niche, and coexistence in plant-specialist frogs from Madagascar. Biotropica, 43, 58–67. https://doi.org/10.1111/j.1744-7429.2010.00730.x
  46. Lehtinen, R.M., Nussbaum, R.A., Richards, C.M., Cannatella, D.C. & Vences, M. (2007) Mitochondrial genes reveal cryptic diversity in plant-breeding frogs from Madagascar (Anura, Mantellidae, Guibemantis). Molecular Phylogenetics and Evolution, 44, 1121–1129. https://doi.org/10.1016/j.ympev.2007.05.020
  47. Librado, P. & Rozas, J. (2009) DnaSP. Version 5. A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
  48. MacArthur, R. & Levins, R. (1967) The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist, 101, 377–385. https://doi.org/10.1086/282505
  49. Miralles, A., Köhler, J., Glaw, F., Wollenberg Valero, K.C., Crottini, A., Rosa, G.M., du Preez, L., Vieites, D.R., Ratsoavina, F.M. & Vences, M. (2023) An endless harvest: integrative revision of the Gephyromantis boulengeri and G. blanci complexes reveals six new species of mantellid frogs from Madagascar. Salamandra, 59, 1–41.
  50. Moat, J. & Smith, P. (2007) Atlas of the Vegetation of Madagascar. Royal Botanic Gardens, Kew, 124 pp.
  51. Pabijan, M., Wollenberg, K.C. & Vences, M. (2012) Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae). Journal of Evolutionary Biology, 25, 2310–2324. https://doi.org/10.1111/j.1420-9101.2012.02613.x
  52. Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16. https://doi.org/10.1186/1742-9994-7-16
  53. 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, Honolulu.
  54. Perl, R.G.B., Nagy, Z.T., Sonet, G., Glaw, F., Wollenberg, K.C. & Vences, M. (2014) DNA barcoding Madagascar’s amphibian fauna. Amphibia-Reptilia, 35, 197–206. https://doi.org/10.1163/15685381-00002942
  55. Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: Assemble Species by Automatic Partitioning. Molecular Ecology Resources, 21, 609–620. https://doi.org/10.1111/1755-0998.13281
  56. Pyron, R.A., O'Connell, K.A., Duncan, S.C., Burbrink, F.T. & Beamer, D.A. (2023) Speciation hypotheses from phylogeographic delimitation yield an integrative taxonomy for seal salamanders (Desmognathus monticola). Systematic Biology, 72, 179–197. https://doi.org/10.1093/sysbio/syac065
  57. Rosa, G.M., Márquez, R. & Andreone, F. (2011) The astonishing calls of the frogs of Betampona. Museo Regionale di Scienze Naturali di Torino & Fonoteca Madrid, Torino. [CD and booklet]
  58. Roughgarden, J. (1976) Resource partitioning among competing species—a coevolutionary approach. Theoretical Population Biology, 9, 388–424. https://doi.org/10.1016/0040-5809(76)90054-X
  59. Salzburger, W., Ewing, G.B. & Von Haeseler, A. (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology, 20, 1952–1963. https://doi.org/10.1111/j.1365-294X.2011.05066.x
  60. Scherz, M.D., Crottini, A., Hutter, C.R., Hildenbrand, A., Andreone, F., Fulgence, T.R., Köhler, G., Ndriantsoa, S.H., Ohler, A., Preick, M., Rakotoarison, A., Rancilhac, L., Raselimanana, A.P., Riemann, J.C., Rödel, M.-O., Rosa, G.M., Streicher, J.W., Vieites, D.R., Köhler, J., Hofreiter, M., Glaw, F. & Vences, M. (2022) An inordinate fondness for inconspicuous brown frogs: integration of phylogenomics, archival DNA analysis, morphology, and bioacoustics yields 24 new taxa in the subgenus Brygoomantis (genus Mantidactylus) from Madagascar. Megataxa, 7 (2), 113–311. https://doi.10.11646/megataxa.7.2.1
  61. Scherz, M.D., Glaw, F., Hutter, C.R., Bletz, M.C., Rakotoarison, A., Köhler, J. & Vences, M. (2019) Species complexes and the importance of Data Deficient classification in Red List assessments: The case of Hylobatrachus frogs. PLoS One, 14, e0219437. https://doi.org/10.1371/journal.pone.0219437
  62. Shen, X.X., Liang, D. & Zhang, P. (2012) The development of three long universal nuclear protein-coding locus markers and their application to osteichthyan phylogenetics with nested PCR. PLoS One, 7, e39256. https://doi.org/10.1371/journal.pone.0039256
  63. Speybroeck, J., Beukema, W., Dufresnes, C., Fritz, U., Jablonski, D., Lymberakis, P., Martínez-Solano, I., Razzetti, E., Vamberger, M., Vences, M., Vörös, J. & Crochet, P. (2020) Species list of the European herpetofauna – 2020 update by the Taxonomic Committee of the Societas Europaea Herpetologica. Amphibia-Reptilia, 41, 139–189. https://doi.org/10.1163/15685381-bja10010
  64. Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  65. Stephens, M., Smith, N.J. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989. https://doi.org/10.1086/319501
  66. Vacher, C., Tamaddoni-Nezhad, A., Kamenova, S., Peyrard, N., Moalic, Y., Sabbadin, R., Schwaller, L., Chiquet, J., Smith, M.A., Vallance, J., Fievet, V., Jakuschkin, B. & Bohan, D.A. (2016) Learning ecological networks from next-generation sequencing data. Advances in Ecological Research, 54, 1–39. https://doi.org/10.1016/bs.aecr.2015.10.004
  67. Vences, M., Glaw, F. & Marquez, R. (2006) The Calls of the Frogs of Madagascar. 3 Audio CD's and booklet. Alosa, Barcelona, 44 pp.
  68. Vences, M., Hauswaldt, S. & Glaw, F. (2011) The advertisement call of Guibemantis pulcher, a phytotelmic frog from Madagascar. Herpetology Notes, 4, 377–379
  69. Vences, M., Hutter, C., Glaw, F., Rakotoarison, A., Raselimanana, A. & Scherz, M. (2023) A new species of Pandanus-dwelling frog from northern Madagascar related to Guibemantis pulcher. Zootaxa, 5306 (1), 97–115. https://doi.org/10.11646/zootaxa.5306.1.4
  70. Vences, M., Köhler, J., Andreone, F., Craul, A.-K., Crottini, A., du Preez, L., Preick, M., Rancilhac, L., Rödel, M.-O., Scherz, M.D., Streicher, J.W., Hofreiter, M. & Glaw, F. (2021a): Target-enriched DNA sequencing clarifies the identity of name-bearing types of the Gephyromantis plicifer complex and reveals a new species of mantellid frog from Madagascar. Spixiana, 44, 175–202.
  71. Vences, M., Miralles, A., Brouillet, S., Ducasse, J., Fedosov, A., Kharchev, V., Kostadinov, I., Kumari, S., Patmanidis, S., Scherz, M.D., Puillandre, N. & Renner, S.S. (2021b) iTaxoTools 0.1: Kickstarting a specimen-based software toolkit for taxonomists. Megataxa, 6 (2), 77–92. https://doi.org/10.11646/megataxa.6.2.1
  72. Vences, M., Patmanidis, S., Kharchev, V. & Renner, S.S. (2022) Concatenator, a user-friendly program to concatenate DNA sequences, implementing graphical user interfaces for MAFFT and FastTree. Bioinformatics Advances, 2, vbac050. https://doi.org/10.1093/bioadv/vbac050
  73. Vences, M., Rakotoarison, A., Rakotondrazafy, A.M.A., Ratsoavina, F.M., Randrianiaina, R.D., Glaw, F., Lehtinen, R.M. & Raxworthy, C.J. (2013) Assessing the diversity of phytotelmic frogs along Madagascar’s east coast: Redefinition of Guibemantis bicalcaratus (Boettger, 1913) and revalidation of Guibemantis methueni (Angel, 1929). Vertebrate Zoology, 63, 193–205. https://doi.org/10.3897/vz.63.e31427
  74. Vences, M., Wahl-Boos, G., Hoegg, S., Glaw, F., Spinelli Oliveira, E., Meyer, A. & Perry, S. (2007) Molecular systematics of mantelline frogs from Madagascar and the evolution of their femoral glands. Biological Journal of the Linnean Society, 92, 529–539. https://doi.org/10.1111/j.1095-8312.2007.00859.x
  75. Vieilledent, G., Grinand, C., Rakotomalala, F.A., Ranaivosoa, R., Rakotoarijaona, J-R., Thomas Allnutt, T.F. & Achard, F. (2018) Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biological Conservation, 222, 189–197. https://doi.org/10.1016/j.biocon.2018.04.008.
  76. 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. https://doi.org/10.1073/pnas.0810821106
  77. Wollenberg, K.C., Jenkins, R.K.B., Randrianavelona, R., Rampilamanana, R., Ralisata, M., Ramanandraibe, A., Ramilijaona Ravoahangimalala, O. & Vences, M. (2011) On the shoulders of lemurs: pinpointing the ecotouristic potential of Madagascar’s unique herpetofauna. Journal of Ecotourism, 10, 101–117. https://doi.org/10.1080/14724049.2010.511229