{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T23:25:49Z","timestamp":1777505149732,"version":"3.51.4"},"reference-count":63,"publisher":"Proceedings of the National Academy of Sciences","issue":"20","content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2009,5,19]]},"abstract":"<jats:p>Amphibians are in decline worldwide. However, their patterns of diversity, especially in the tropics, are not well understood, mainly because of incomplete information on taxonomy and distribution. We assess morphological, bioacoustic, and genetic variation of Madagascar's amphibians, one of the first near-complete taxon samplings from a biodiversity hotspot. Based on DNA sequences of 2,850 specimens sampled from over 170 localities, our analyses reveal an extreme proportion of amphibian diversity, projecting an almost 2-fold increase in species numbers from the currently described 244 species to a minimum of 373 and up to 465. This diversity is widespread geographically and across most major phylogenetic lineages except in a few previously well-studied genera, and is not restricted to morphologically cryptic clades. We classify the genealogical lineages in confirmed and unconfirmed candidate species or deeply divergent conspecific lineages based on concordance of genetic divergences with other characters. This integrative approach may be widely applicable to improve estimates of organismal diversity. Our results suggest that in Madagascar the spatial pattern of amphibian richness and endemism must be revisited, and current habitat destruction may be affecting more species than previously thought, in amphibians as well as in other animal groups. This case study suggests that worldwide tropical amphibian diversity is probably underestimated at an unprecedented level and stresses the need for integrated taxonomic surveys as a basis for prioritizing conservation efforts within biodiversity hotspots.<\/jats:p>","DOI":"10.1073\/pnas.0810821106","type":"journal-article","created":{"date-parts":[[2009,5,4]],"date-time":"2009-05-04T21:54:30Z","timestamp":1241474070000},"page":"8267-8272","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":500,"title":["Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory"],"prefix":"10.1073","volume":"106","author":[{"given":"David R.","family":"Vieites","sequence":"first","affiliation":[{"name":"Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cient\u00edficas, c\/ Jos\u00e9 Gutierrez Abascal 2, 28006 Madrid, Spain;"}]},{"given":"Katharina C.","family":"Wollenberg","sequence":"additional","affiliation":[{"name":"Zoological Institute, Technical University of Braunschweig, Spielmannstrasse 8, 38106 Braunschweig, Germany;"}]},{"given":"Franco","family":"Andreone","sequence":"additional","affiliation":[{"name":"Museo Regionale di Scienze Naturali, Via Giolitti 36, 10123 Turin, Italy;"}]},{"given":"J\u00f6rn","family":"K\u00f6hler","sequence":"additional","affiliation":[{"name":"Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany; and"}]},{"given":"Frank","family":"Glaw","sequence":"additional","affiliation":[{"name":"Zoologische Staatssammlung M\u00fcnchen, M\u00fcnchhausenstrasse 21, 81247 Munich, Germany"}]},{"given":"Miguel","family":"Vences","sequence":"additional","affiliation":[{"name":"Zoological Institute, Technical University of Braunschweig, Spielmannstrasse 8, 38106 Braunschweig, Germany;"}]}],"member":"341","published-online":{"date-parts":[[2009,5,19]]},"reference":[{"key":"e_1_3_3_1_2","volume-title":"Hotspots Revisited: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions","author":"Mittermeier RA","year":"2005","unstructured":"RA Mittermeier, et al. Hotspots Revisited: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions (Conservation International, Arlington, VA, 2005)."},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1038\/35002501"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature03850"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1127609"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-3207(02)00425-1"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1080\/10635150290102339"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1080\/10635150701884640"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(98)01534-1"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1641\/0006-3568(2005)055[0693:NAAGCA]2.0.CO;2"},{"key":"e_1_3_3_10_2","unstructured":"Information on amphibian biology and conservation. Available at www.amphibiaweb.org. (2008)."},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.298.5592.379"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1206\/0003-0090(2005)294[0001:SROTFF]2.0.CO;2"},{"key":"e_1_3_3_13_2","first-page":"163","article-title":"The Sri Lankan shrub-frogs of the genus Philautus Gistel, 1848 (Ranidae:Rhacophorinae), with description of 27 new species","volume":"12","author":"Manamendra-Arachchi K","year":"2005","unstructured":"K Manamendra-Arachchi, R Pethiyagoda, The Sri Lankan shrub-frogs of the genus Philautus Gistel, 1848 (Ranidae:Rhacophorinae), with description of 27 new species. Raffles Bull Zool Suppl 12, 163\u2013303 (2005).","journal-title":"Raffles Bull Zool Suppl"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2006.0505"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0001109"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1655\/07-011.1"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1080\/1063515060081588"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature02019"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature03474"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1103538"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0801921105"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0376892907004262"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.37.091305.110239"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2007.05.028"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1122806"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0502092102"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1007\/0-387-31710-4_9"},{"key":"e_1_3_3_28_2","first-page":"1","article-title":"Amphibiens (premi\u00e8re partie)","volume":"75","author":"Blommers-Schl\u00f6sser RMA","year":"1991","unstructured":"RMA Blommers-Schl\u00f6sser, CP Blanc, Amphibiens (premi\u00e8re partie). Faune de Madagascar 75, 1\u2013379 (1991).","journal-title":"Faune de Madagascar"},{"key":"e_1_3_3_29_2","volume-title":"A Field Guide to the Amphibians and Reptiles of Madagascar","author":"Glaw F","year":"2007","unstructured":"F Glaw, M Vences A Field Guide to the Amphibians and Reptiles of Madagascar (K\u00f6ln, Vences & Glaw, 3rd ed, K\u00f6ln, Germany, 2007).","edition":"3"},{"key":"e_1_3_3_30_2","volume-title":"Conservation International Tropical Field Guide","author":"Mittermeier RA","year":"2006","unstructured":"RA Mittermeier, et al., Lemurs of Madagascar. Conservation International Tropical Field Guide (Conservation International, Arlington, VA, 2006)."},{"key":"e_1_3_3_31_2","first-page":"2613","volume-title":"Amphibian Biology","author":"Vences M","year":"2007","unstructured":"M Vences, DB Wake, Speciation, species boundaries and phylogeography of amphibians. Amphibian Biology, eds HH Heatwole, M Tyler (Surrey Beatty & Sons, Chipping Norton, Australia) Vol 6, 2613\u20132669, Systematics. (2007)."},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2003.0130"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2005.1725"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-44-1-174"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-45-1-186"},{"key":"e_1_3_3_36_2","first-page":"1043","article-title":"Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology","volume":"52","author":"Stackebrandt E","year":"2002","unstructured":"E Stackebrandt, et al., Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043\u20131047 (2002).","journal-title":"Int J Syst Evol Microbiol"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(03)00184-8"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.35.112202.130128"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.34.011802.132421"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2005.1717"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8312.2004.00366.x"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.200121897"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2005.1714"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.11646\/zootaxa.1843.1.2"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2007.02.024"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8312.2005.00503.x"},{"key":"e_1_3_3_47_2","first-page":"910","article-title":"Relative rates of morphological evolution in primates, carnivores and frogs","volume":"17","author":"Cherry LM","year":"1977","unstructured":"LM Cherry, SM Case, AC Wilson, Relative rates of morphological evolution in primates, carnivores and frogs. Am Zool 17, 910 (1977).","journal-title":"Am Zool"},{"key":"e_1_3_3_48_2","first-page":"1","article-title":"Convergence and morphological constraint in frogs: Variation in postcranial morphology","volume":"43","author":"Emerson SB","year":"1986","unstructured":"SB Emerson, Convergence and morphological constraint in frogs: Variation in postcranial morphology. Fieldiana Zool 43, 1\u201319 (1986).","journal-title":"Fieldiana Zool"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1086\/285234"},{"key":"e_1_3_3_50_2","first-page":"397","article-title":"Towards understanding the spatial pattern of amphibian diversity in Madagascar","volume":"45","author":"Vieites DR","year":"2008","unstructured":"DR Vieites, S Nieto-Rom\u00e1n, M Vences, Towards understanding the spatial pattern of amphibian diversity in Madagascar. A Conservation Strategy for the Amphibians of Madagascar, ed F Andreone 45, 397\u2013340, Mon Mus Reg Sci Nat Torino. (2008).","journal-title":"A Conservation Strategy for the Amphibians of Madagascar"},{"key":"e_1_3_3_51_2","first-page":"946","volume-title":"The Natural History of Madagascar","author":"Raxworthy CJ","year":"2003","unstructured":"CJ Raxworthy, Introduction to reptiles. The Natural History of Madagascar, eds SM Goodman, JP Benstead (Chicago Univ Press, Chicago), pp. 946\u2013949 (2003)."},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1155193"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-3207(00)00041-0"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1017\/S026646740200247X"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.0060118"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2005.1729"},{"key":"e_1_3_3_57_2","volume-title":"The Calls of the Frogs of Madagascar","author":"Vences M","year":"2006","unstructured":"M Vences, F Glaw, R Marquez The Calls of the Frogs of Madagascar (Alosa, Barcelona, 3 Audio CDs (total duration 220 min) and booklet. (2006)."},{"key":"e_1_3_3_58_2","first-page":"2892","volume-title":"Amphibian Biology","author":"Schneider H","year":"2007","unstructured":"H Schneider, U Sinsch, Contributions of bioacoustics to the taxonomy of Anura. Amphibian Biology, ed H Heatwole (Surrey Beatty & Sons, Chipping Norton, Australia) Vol 7, 2892\u20132931, Phylogeny and Systematics. (2007)."},{"key":"e_1_3_3_59_2","volume-title":"Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions","author":"Gerhardt HC","year":"2002","unstructured":"HC Gerhardt, F Huber Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions (Univ Chicago Press, Chicago, 2002)."},{"key":"e_1_3_3_60_2","first-page":"2435","article-title":"Allozyme and advertisement call variation in the t\u00fangara frog, Physalaemus pustulosus","volume":"50","author":"Ryan MJ","year":"1996","unstructured":"MJ Ryan, AS Rand, LA Weigt, Allozyme and advertisement call variation in the t\u00fangara frog, Physalaemus pustulosus. Evolution 50, 2435\u20132453 (1996).","journal-title":"Evolution"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature04004"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1095-8312.1991.tb00619.x"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2006.3736"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.0810821106","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,12]],"date-time":"2022-04-12T17:38:45Z","timestamp":1649785125000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.0810821106"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,5,19]]},"references-count":63,"journal-issue":{"issue":"20","published-print":{"date-parts":[[2009,5,19]]}},"alternative-id":["10.1073\/pnas.0810821106"],"URL":"https:\/\/doi.org\/10.1073\/pnas.0810821106","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1162816.624423","asserted-by":"object"}]},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,5,19]]},"assertion":[{"value":"2008-10-26","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2009-05-19","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}