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Home , Boophis, Frank Glaw, Laliostoma, Laliostominae, Madecassophryne, Miguel Vences

Species Review of Extinction Risks in : Conclusions from the Global Amphibian Assessment

FRANCO ANDREONE,∗ JOHN E. CADLE,† NEIL COX,‡ ,§ RONALD A. NUSSBAUM,∗∗ CHRISTOPHER J. RAXWORTHY,†† SIMON N. STUART,‡ DENIS VALLAN,‡‡ AND §§ ∗Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, I-10123 Torino, Italy, email [email protected] †Department of , Chicago Zoological Society, 3300 Golf Road, Brookfield, IL 60513, U.S.A. ‡IUCN/SSC-CI/CABS Assessment Initiative, c/o Center for Applied Biodiversity Science, Conservation International, 1919 M Street NW, Suite 600, Washington, D.C. 20036, U.S.A. §Zoologische Staatssammlung, M¨unchhausenstrasse 21, D-81247 M¨unchen, ∗∗Division of and , Museum of Zoology, University of Michigan, Ann Arbor, MI 48109-1079, U.S.A. ††Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192, U.S.A. ‡‡Universit¨at Bern, Zoologisches Institut, Baltzerstrasse 6, CH-3012 Bern, and Natur-Museum Luzern, Kasernenplatz 6, CH-6003 Luzern, Switzerland §§Institute of Biodiversity and Ecosystem Dynamics, Zoological Museum, Mauritskade 61, 1092 AD Amsterdam, The Netherlands

Abstract: We assessed the extinction risks of Malagasy amphibians by evaluating their distribution, occur- rence in protected areas, population trends, quality, and prevalence in commercial trade. We estimated and mapped the distribution of each of the 220 described Malagasy and applied, for the first time, the IUCN Red List categories and criteria to all species described at the time of the assessment. Nine species were categorized as , 21 as endangered, and 25 as vulnerable. The most threatened species occur on the High Plateau and/or have been subjected to overcollection for the pet trade, but restricted ex- tent of occurrence and ongoing were identified as the most important factors influencing extinction threats. The two areas with the majority of threatened species were the northern Tsaratanana- Marojejy-Masoala highlands and the southeastern Anosy Mountains. The current system of protected areas includes 82% of the threatened amphibian species. Of the critically , 6 did not occur in any protected area. For conservation of these species we recommend the creation of a reserve for the species of the Mantella aurantiaca group, the inclusion of two species in the Convention on the International Trade in Endangered Species Appendix II, and the suspension of commercial collecting for Mantella cowani. Field surveys during the last 15 years reveal no pervasive extinction of Malagasy amphibians resulting from disease or other agents, as has been reported in some other areas of the world.

Key Words: IUCN, species risk categorization, species status assessment

Revisi´on del Riesgo de Extinci´on de Anfibios en Madagascar: Conclusiones de Evaluaci´on Global de Anfibios Resumen: Evaluamos los riesgos de extincion´ de anfibios malgaches mediante el analisis´ de su distribucion,´ ocurrencia en areas´ protegidas, tendencias poblacionales, calidad del habitat´ y prevalencia en el comercio. Estimamos y mapeamos la distribucion´ de cada una de las 220 especies descritas para Madagascar y aplicamos, por primera vez, las categor´ıas y criterios de la Lista Roja de IUCN a todas las especies descritas al momento

Paper received July 19, 2004; revised manuscript accepted January 20, 2005. 1790 Conservation 1790–1802 C 2005 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2005.00249.x Andreone et al. Conservation of Malagasy Amphibians 1791 de la evaluacion.´ Nueve especies fueron clasificadas en peligro cr´ıtico, 21 como amenazadas y 25 como vulnerables. Las especies mas´ amenazadas ocurren en High Plateau y/o han sido sujetas a sobreexplotacion´ para el comercio de mascotas, pero identificamos a la extension´ restringida de ocurrencia y a la destruccion´ del habitat´ como los factores que mas´ influyen sobre las amenazas de extincion.´ Las mesetas de Tsaratanana- Marojejy-Masoala en el norte y las Montanas˜ Anosy en el sureste fueron las dos areas´ con la mayor´ıa de especies amenazadas. El actual sistema de areas´ protegidas incluye a 82% de las especies de anfibios amenazadas. De las especies en peligro cr´ıtico, 6 no ocurrieron en ninguna area´ protegida. Para la conservacion´ de estas especies recomendamos la creacion´ de una reserva para especies del grupo de Mantella aurantiaca,lainclusion´ de dos especies de Scaphiophryne en el Ap´endice II de la Convencion´ Internacional para el Comercio de Especies en Peligro y la suspension´ de la colecta comercial de Mantella cowani. Los estudios de campo llevados a cabo en los ultimos´ 15 anos˜ no muestran la extincion´ generalizada de anfibios malgaches debido a enfermedades u otros agentes, como se ha registrado en algunas otras partes del mundo.

Palabras Clave: clasificaci´on del riesgo de especies, evaluaci´on del estatus de especies, IUCN

Introduction only Malagasy hyperoliids are in the endemic Heter- ixalus (11 species), which inhabits and The diversity and endemism of Malagasy amphibians have edges (Vences et al. 2003). been highlighted in recent decades (Blommers-Schl¨osser The different life-history traits of these amphibians are & Blanc 1991; Stuart et al. 2004), illustrating the impor- mirrored by their differential ecological sensitivity and tance of this group to understanding - conservation needs (Andreone & Luiselli 2003). Most ary processes and in identifying conservation priorities. of the Malagasy inhabit the eastern rainforest, an High rates of deforestation and general habitat degrada- ecosystem that allowed the rapid diversification of some tion are among the most immediate threats to Madagas- groups such as (Vences et al. 2002b), Man- car’s biota and landscapes, and it is important to review tidactylus (Andreone 2003), and cophyline microhylids the current of endemic species and (Andreone et al. 2005). The original eastern rainforest speciose groups such as amphibians, which are sensitive block is now severely fragmented because of deforesta- to environmental change (Vallan 2002, 2003). tion in recent times (Green & Sussman 1990), and it con- There are four families of frogs in Madagascar: Man- tinues to be subject to heavy anthropogenic pressure tellidae, , Ranidae, and Hyperoliidae (Glaw (Vallan 2000b). As a rule, forest fragmentation has led &Vences 2003). is the most speciose group to an impoverishment of the native amphibian fauna, al- and is endemic to Madagascar and the Comoro Islands. though in some cases this loss of amphibian species rich- It includes the genera (90 species), Man- ness is not immediately evident (Vallan et al. 2004) be- tella (15 species), Boophis (50 species), Aglyptodacty- cause species have differing sensitivities to habitat alter- lus (3 species), and (1 species). Mantidacty- ations (Andreone 1994). Overharvesting for the pet trade lus and Mantella show peculiar features related to repro- is an additional threat to the long-term survival of a num- duction, such as essential absence of amplexus (mating ber of Malagasy amphibians. Thousands of colorful frogs embrace) and nuptial pads, eggs laid outside water, and (e.g., Mantella, Scaphiophryne, Dyscophus species) are presence (in most species) of femoral glands. Species of exported each year to Europe, North America, or Japan, Mantella (Vences et al. 1999) are brightly colored and where they can fetch high prices (Behra & Raxworthy show accumulation of alkaloids in the skin (Daly et al. 1991). The effects of trade on natural populations are still 1996). Boophis species are arboreal frogs that lay eggs in poorly studied, and we did not consider the effects of water (Blommers-Schl¨osser 1979). and collecting on the long-term survival of these populations Laliostoma are terrestrial and breed in temporary ponds (Raxworthy & Nussbaum 2000; Andreone & Luiselli 2003; (Vences & Glaw 2001). Ranids include the opportunis- Rabemanjara et al. 2005). tic and widely distributed Ptychadena mascareniensis, Current conservation strategies in Madagascar include present also in the Mascarene Islands and Seychelles, identifying priority areas for threatened species or over- and Hoplobatrachus tigerinus, introduced to Madagascar all species diversity and including these areas in nature from southern Asia (Kosuch et al. 2001). Microhylids are reserves (Ganzhorn et al. 1997; ANGAP 2001). The pres- represented by 10 genera (and approximately 50 species) ence of a rich amphibian fauna or of threatened amphib- with diverse life histories (Blommers-Schl¨osser & Blanc ian species was only rarely considered in the establish- 1991): Dyscophus, Paradoxophyla, Scaphiophryne, Co- ment of new protected areas because other, more “vis- phyla, Platypelis, Anodonthyla, Plethodontohyla, Made- ible” taxa (e.g., lemurs, birds) were often considered a cassophryne, Rhombophryne, and .Finally,the priority. Most Malagasy amphibian species occur in one

Conservation Biology Volume 19, No. 6, December 2005 1792 Conservation of Malagasy Amphibians Andreone et al. or more protected areas. Some species, however, known gasy species. This shapefile was then dissolved against as “gap species,” do not occur in protected areas and are the species name record included in the associated at- of particular concern (Rodrigues et al. 2004). tribute table, creating a single distribution polygon for As part of the Global Amphibian Assessment (GAA, Stu- each species. We then used a script to create a grid (with art et al. 2004), we evaluated the conservation status of cell size of 0.1◦)from each polygon. We overlaid these all described amphibians from Madagascar, based on the grids and calculated the value for the number of species IUCN Red List Categories and Criteria (IUCN 2001). We present within each cell. We then created two species- summarize the results of the GAA workshop, provide up- richness maps for all species, and a combined map of dated information on species distributions, and discuss species density for the three (CR + EN + VU) highest how life-history traits and other factors influence con- IUCN threat categories. servation assessment of amphibians. We also provide up- dated or new red listings for all amphibian species and highlight general patterns gleaned from our assessment. Results

Species Summary Methods There were 55 species in threatened categories, corre- sponding to 25% of the Malagasy amphibians (Tables 1 Conservation Priorities Investigation & 2). Of these, 13 species are collected and exported in During the GAA workshop of 2003 we evaluated 220 am- pet trade and 11 are listed in CITES (Convention on In- phibian species (described or in press as of December ternational Trade in Endangered Species of Wild Fauna 2003) based on published data and our own unpublished and Flora) Appendix II (www..org/eng/appendices. information on species distributions and systematics (Ta- shtml). Two species classified as threatened and involved bles 1 & 2). We followed IUCN categorization rules (re- in trade but not listed in CITES are Scaphiophryne bori- ported in IUCN [2001]) in which species are classified as bory and S. marmorata. The remaining species were critically endangered (CR), endangered (EN), vulnerable not categorized in the three highest threat categories, al- (VU), near threatened (NT), data deficient (DD), or least though some of them were classified as NT. These include concern (LC). two species that are sometimes in trade (Mantella lae- To establish the threat category for each species, one vigata and Scaphiophryne madagascariensis) and one of us (R.A.N.) conducted a preliminary screening of species that is the only Malagasy amphibian currently the available information regarding the distribution and listed in CITES Appendix I, the tomato frog (Dyscophus threats of each species. Based on his findings, he drew antongili). Species assigned to the DD category included a distribution map for the species and entered data poorly known species. on the distribution, abundance, population trends, ecol- ogy, habitat preferences, threats, utilization, conserva- Critically Endangered Species tion measures, and red-list status into the GAA database, following data standards outlined in IUCN (2001). The We categorized nine species as CR: Boophis williamsi, rest of us reviewed the data sheets compiled by R.A.N., Mantella aurantiaca, M. cowani, M. expectata, M. and then at the GAA Madagascar workshop added fur- milotympanum, M. viridis, Mantidactylus pauliani, ther information and data. At the workshop we reached , and Stumpffia helenae (Fig. 2). agreement on the data associated with each species. We listed Boophis williamsi as CR based on its extent < 2 (The GAA data for Madagascar are publicly available from of occurrence (EOO) of 100 km and its area of occu- < 2 www.globalamphibian.org.) We then determined the ap- pancy (AOO) of 10 km . Since its description in 1974 propriate IUCN category for each species based on these the only known population of this species is a single un- data, not on expert opinion. Localities mentioned in the protected site in the Ankaratra Massif at 2100 m of ele- text are shown in Fig. 1. vation (Vences et al. 2002b). The extent and quality of habitat in this area continue to decline. B. williamsi may have lived originally in montane rainforest, but it is now Statistical Procedures and Graphical Analysis restricted to high-elevation grasslands with relict mon- Spatial analyses of the species’ distribution maps were tane forest. It breeds in fast-flowing mountain streams performed with ESRI ArcView 3.2a Spatial Analyst ex- and inhabits nearby degraded areas. This habitat is an- tension (ESRI 2000) to determine the areas with the nually burned and is subject to extensive overgrazing and highest diversities of amphibian species and those areas cultivation (potato fields). The species appears to be very with a high diversity of species in IUCN threatened cat- rare and was only occasionally encountered. egories. The individual digitized, multipolygon-based dis- Mantella aurantiaca was categorized CR based on its tribution maps were assembled to create a single shapefile AOO of < 10 km2. Its distribution is now severely frag- that contained the distribution information for all Mala- mented. Although localized, the population density of M.

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Table 1. Statusa of globally threatened Madagascan amphibians.

Occurrence in Occurrence in Species Family Red-list criteriumb pet trade CITES appendixc protected areas

Critically endangered (CR) Boophis williamsi Mantellidae B1ab(iii)+2ab(iii) Mantella aurantiaca Mantellidae B2ab(iii, v) + II Mantella cowani Mantellidae A2acd + B2ab(iii) + II Mantella expectata Mantellidae B2ab(iii, v) + II + Mantella milotympanum Mantellidae B2ab(iii) + II Mantella viridis Mantellidae B2ab(iii) + II Mantidactylus pauliani Mantellidae B2ab(iii) Scaphiophryne gottlebei Microhylidae B2ab(iii, v) + II + Stumpffia helenae Microhylidae B2ab(iii) + Endangered (EN) Aglyptodactylus laticeps Mantellidae B1ab(iii) + Mantella bernhardi Mantellidae B2ab(iii, v) + II + Mantella crocea Mantellidae B1ab(iii, v) + 2ab(iii, v) + II + Mantidactylus brunae Mantellidae B1ab(iii) + Mantidactylus corvus Mantellidae B2ab(iii) + Mantidactylus guibei Mantellidae B1ab(iii) + Mantidactylus horridus Mantellidae B1ab(iii) + Mantidactylus madecassus Mantellidae B1ab(iii) + 2ab(iii) + Mantidactylus microtis Mantellidae B1ab(iii) + Mantidactylus microtympanum Mantellidae B2ab(iii) + Mantidactylus silvanus Mantellidae B1ab(iii) + 2ab(iii) + Mantidactylus webbi Mantellidae B1ab(iii) + 2ab(iii) + Anodonthyla rouxae Microhylidae B1ab(iii) Madecassophryne truebae Microhylidae B1ab(iii) + Platypelis alticola Microhylidae B1ab(iii) + Platypelis mavomavo Microhylidae B1ab(iii) + Platypelis milloti Microhylidae B1ab(iii) + Platypelis tetra Microhylidae B1ab(iii) + Plethodontohyla brevipes Microhylidae B1ab(iii) + Plethodontohyla guentherpetersi Microhylidae B1ab(iii) + Microhylidae B1ab(iii, v) + Vulnerable (VU) Boophis andreonei Mantellidae B1ab(iii) + Boophis blommersae Mantellidae B1ab(iii) + Boophis haematopus Mantellidae B1ab(iii) + Boophis jaegeri Mantellidae B1ab(iii) + Mantella haraldmeieri Mantellidae B1ab(iii) + II + Mantella madagascariensis Mantellidae B1ab(iii) + II + Mantella pulchra Mantellidae B1ab(iii) + II + Mantidactylus ambohitra Mantellidae B1ab(iii) + Mantidactylus elegans Mantellidae B1ab(iii) + 2ab(iii) + Mantidactylus klemmeri Mantellidae B1ab(iii) + Mantidactylus massorum Mantellidae B1ab(iii) + 2ab(iii) + Mantidactylus rivicola Mantellidae B1ab(iii) + Mantidactylus salegy Mantellidae B1ab(iii) + Mantidactylus schilfi Mantellidae D2 + Mantidactylus striatus Mantellidae B1ab(iii) + Mantidactylus tandroka Mantellidae B1ab(iii) + Anodonthyla montana Microhylidae D2 + Platypelis tsaratananaensis Microhylidae B1ab(iii) + Plethodontohyla coronata Microhylidae B2ab(iii) Plethodontohyla coudreaui Microhylidae B1ab(iii) + Plethodontohyla serratopalpebrosa Microhylidae B1ab(iii) + Plethodontohyla tuberata Microhylidae B1ab(iii) + Rhombophryne testudo Microhylidae D2 + Microhylidae B1ab(iii) ++ Stumpffia pygmaea Microhylidae D2 + aStatus based on IUCN (2001) criteria. bCriteria coding defined in IUCN (2001) (also available from http://www.redlist.org/info/categories criteria2001.html#critical). cCITES, Convention of International Trade of Endangered Species of Wild Fauna and Flora.

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Table 2. Malagasy frog species classified as near threatened, least concern, and data deficient.

Family—subfamily Near threatened Least concern Data deficient

Hyperoliidae Heterixalus carbonei, Heterixalus alboguttatus,a H. andrakata, H. rutenbergi H. betsileo,a H. boettgeri, H. luteostriatus a H. madagascariensis,a H. punctatus, H. tricolor,a H. variabilis Mantellidae— Boophis majori, Boophis albilabris,a B. albipunctatus, Boophis andohahela, Boophinae B. occidentalis, B. ankaratra, B. boehmei, B. bottae, B. anjanaharibeensis, B. rhodoscelis, B. doulioti, B. erythrodactylus, B. brachychir, B. burgeri, B. rufioculis B. goudotii, B. guibei, B. idae, B. elenae, B. englaenderi, B. lichenoides, B. luteus, B. feonnyala, B. hillenii, B. madagascariensis, B. marojezensis, B. laurenti, B. liami, B. microtympanum,a B. miniatus, B. mandraka, B. periegetes, B. opisthodon, B. pauliani, B. picturatus, B. schuboeae, B. pyrrhus, B. rappiodes, B. reticulatus, B. septentrionalis, B. sibilans, B. tasymena, B. tephraeomystax, B. solomaso, B. xerophilus B. viridis, B. vittatus Mantellidae— Aglyptodactylus madagascariensis, A. securifer, Laliostoma labrosum Mantellidae— Mantella laevigata,a Mantella baroni,a M. betsileo,a Mantella manery, Mantidactylus Mantellinae Mantidactylus bertini, M. nigricans,a Mantidactylus albofrenatus, M. albolineatus, M. blanci, M. decaryi, aerumnalis, M. aglavei, M. alutus, M. ambohimitombi, M. leucocephalus, M. ambreensis, M. argenteus, M. asper, M. cornutus, M. eiselti, M. enki, M. leucomaculatus, M. betsileanus, M. bicalcaratus, M. kathrinae, M. madinika, M. plicifer, M. biporus, M. blommersae, M. punctatus, M. sarotra, M. spiniferus M. boulengeri, M. brevipalmatus, M. thelenae, M. tricinctus, M. charlotteae, M. curtus, M. tschenki, M. zavona, M. depressiceps, M. domerguei, M. zolitschka M. femoralis, M. fimbriatus, M. flavobrunneus, M. grandidieri, M. grandisonae, M. granulatus, M. guttulatus, M. kely, M. liber, M. lugubris, M. luteus, M. majori, M. malagasius, M. melanopleura, M. mocquardi, M. moseri, M. opiparis, M. peraccae, M. phantasticus, M. pseudoasper, M. pulcher, M. redimitus, M. sculpturatus, M. tornieri, M. ulcerosus, M. ventrimaculatus. M. wittei, M. zipperi Ranidae—Raninae Hoplobatrachus tigerinus,c Ptychadena mascareniensis Microhylidae— Dyscophus antongilib Dyscophus guineti,a D. insularisa Dyscophinae Microhylidae— Scaphiophryne Paradoxophyla palmata, Scaphiophryne madagascariensisa brevis, S. calcarata, S. spinosaa Microhylidae— Anodonthyla boulengeri, Cophyla Anodonthyla nigrigularis, phyllodactyla, Platypelis barbouri, Platypelis cowanii, P. occultans, P. grandis, P. tuberifera, Plethodontohyla P. pollicaris, Plethodontohyla alluaudi, P. bipunctata, P. inguinalis, minuta, Stumpffia grandis, P. laevipes, P. mihanika, P. notosticta, S. psologlossa, S. roseifemoralis, P. ocellata, Stumpffia gimmeli S. tetradactyla, S. tridactyla aSpecies in the pet trade. bSpecies included in CITES Appendix I. cSpecies included in CITES Appendix II and introduced from southeast Asia. aurantiaca can be high within just a few hectares. This central Madagascar centered in the Torotorofotsy area and species lives in damp swamp usually associated the Andranomena Forest (at 920–960 m) (Vences et al. with Pandanus screw pines (Vences et al. 1999). The ex- 2004). In 2001 much of the forest bordering the Toroto- tent of its forest habitat is declining, and overharvesting rofotsy areas, probably including some of the remaining fortrade may have reduced some of the existing popu- habitat suitable for Mantella,wasburned in a large for- lations. M. aurantiaca has a narrow distribution in east- est fire (Vences et al. 2004). The area did not appear to

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ularly subjected to fire. Ongoing field research (F.A., un- published) revealed that the surviving populations are now often composed of just a few individuals, which are difficult to detect. At a single site next to Antoetra we as- certained the existence of hybrids with M. baroni (F. A., unpublished). A moratorium on the export of M. cowani was implemented in 2003. Mantella expectata was categorized as CR based on its EOO of < 100 km2. M. expectata occurs mainly in syntopy with Scaphiophryne gottlebei, and the same threats affect both species. Recent surveys revealed that M. expectata is present in several locations around the Isalo Massif (at 700–1000 m). Records from near Toliara (Busse & B¨ohme 1992) were probably erroneous (Vences et al. 1999). Records from Morondava region and Mandena (Glaw & Vences 1994) are unreliable because no voucher spec- imens or recent field surveys document the species in these areas. At Isalo, M. expectata is sometimes abundant next to seasonal streams, and in wet canyons sometimes it is associated with narrow gallery forest. This species appears to be locally abundant and is actively sought for the pet trade, and during the rainy season up to several thousand specimens are collected. Sapphire mining activ- ities and related habitat alteration in the vicinity are also possible threats. We categorized Mantella milotympanum as CR be- cause its AOO is <10 km2, its distribution is severely frag- mented, and the extent of its forest habitat in east-central Madagascar is declining. The species is known in a few un- protected locations in east-central Madagascar near Fier- Figure 1. Map of Madagascar, with the localities cited enana (at 900–1000 m). It is locally common in gallery in the text. Square is capital city. forest around swamps and in seasonally flooded forest. Its habitat is receding because of subsistence agriculture, timber extraction, charcoal manufacture, livestock graz- be heavily affected, and 3 years later Mantella were still ing, and fires. common (M.V., personal observation). This species was Mantella viridis was categorized as CR because its kept in about 35 zoological gardens and other institutions AOO is <10 km2, its distribution is fragmented, and the and is commonly bred in captivity (Glaw et al. 2000). A size and quality of its habitat continue to decline. It oc- management plan to ensure a controlled and sustainable curs in unprotected sites at the Montagne des Fran¸cais trade through the establishment of a trade quota is being in northern Madagascar and in the Antongombato Massif developed. M. aurantiaca is locally extremely abundant, south of Antsiranana (at 50–300 m), where it is locally and the collecting of specimens for the pet trade has not abundant. M. viridis is typical of deciduous dry forest as- had a visible effect on populations. sociated with limestone landscape, usually occurring near We categorized Mantella cowani as CR based on its temporary brooks and streams. Recent observations con- AOO of < 10 km2.Adrastic population decline occurred firmed its presence in degraded with good vege- recently, as deduced from a dramatic reduction in its dis- tational cover, which provides higher humidity and shade tribution and in the number of mature adults (Andreone & than adjacent nonvegetated areas. Because forest loss fre- Randrianirina 2003). The fact that this decline followed quently leads to permanent drying of smaller streams, a period of increased exploitation for the international however, reduction of natural habitats of this species is a pet trade suggests that populations were overcollected, serious concern. The known localities are subject to fires, resulting in a population crash. Although its complete dis- selective logging, firewood collection, and livestock graz- tribution is unknown, M. cowani appears to be limited ing. to unprotected High Plateau sites of east-central Mada- Mantidactylus pauliani was categorized as CR be- gascar near Antoetra and Tsinjoarivo (at 1000–2000 m). cause its AOO is < 10 km2, and its only known popu- It is a terrestrial frog that lives along streams in highland lation is in a single unprotected site at about 2200 m in moors, in areas virtually without forest cover that are reg- the Ankaratra Massif (Vences et al. 2002a). Like Boophis

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Figure 2. The nine critically endangered frog species of Madagascar, two endangered species, and the CITES Appendix I listed Dyscophus antongili. (a) Boophis williamsi, Ankaratra Massif (CR) (photo by M. Vences); (b) Mantella aurantiaca, Andranomena (CR) (photo by M. Vences); (c) Mantella expectata, Ilakaka (CR) (photo by F. Andreone); (d) Mantella cowani, Soamazaka, Antoetra (CR) (photo by F. Andreone); (e) Mantella milotympanum, Fierenana (CR) (photo by M. Vences); ( f ) Mantella viridis, Montagne des Franc¸ais (CR) (photo by C. J. Raxworthy); (g) Mantella bernhardi,Tolongoina region (EN) (photo by F. Andreone); (h) Mantidactylus pauliani, Ankaratra Massif (CR) (photo by M. Vences); (i) Stumpffia helenae, Ambohitantely (CR) (photo by D. Vallan); ( j) Aglyptodactylus laticeps, Kirindy Forest (EN) (photo by F. Glaw); (k) Dyscophus antongili, Maroantsetra (NT) (photo by M. Vences); (l) Scaphiophryne gottlebei, Ilakaka (CR) (photo by F. Andreone). Abbreviations: CR, critically endangered; EN, endangered; NT, near threatened. williamsi, this Mantidactylus is rarely encountered, and farming. Pollution and sedimentation of the streams as a presumably lived originally in montane rainforest but result of agriculture and mining are observed in the area. is now known only along a single stream and in high- We categorized Scaphiophryne gottlebei as CR because elevation with relict forests. The main threats its EOO is <100 km2. All records for this species are from to the habitat are fire, overgrazing, and expanding potato afew areas within the Isalo Massif (at 700–1000 m). It

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Figure 3. Amphibian species diversity in Madagascar: (a) distribution based on overlaying the estimated distributions of all species described or in press up to December 2003; (b) distribution of total diversity with an emphasis on the species richness in the less diverse western regions (grid cells with > 18 species shaded alike to emphasize and permit greater discrimination among areas with fewer species); (c) distribution of species assigned IUCN categories of threat during the Global Amphibian Assessment workshop (critically endangered, endangered, or vulnerable). appears to be a localized frog, although it is abundant Areas of Diversity and Distribution of Threatened in the humid canyons where it usually lives. The extent Species and quality of its habitat continue to decline, and it is subject to overcollecting for the pet trade. Other threats The highest-diversity areas for the amphibian fauna were are similar to those affecting Mantella expectata, with in eastern and northeastern Madagascar (Fig. 3a). These which it is syntopic. regions had 64–82 species per grid cell. The arid west- Stumpffia helenae was categorized as CR because it is ern and southern areas associated with deciduous dry or known only from two forest fragments at 1500 m within spiny forests had still fewer frog species. the R´eserve Sp´eciale d’Ambohitantely in central Madagas- Because the species diversity in the eastern forests is car (Vallan 2000a). Its AOO is < 10 km2, and the extent much greater than in other regions, we successively eval- of its habitat is declining because of fire, wood cutting, uated the frog species with more coarse-grained species and overgrazing. The size of the Ambohitantely forest has richness categories and combined all areas with more been shrinking since the nineteenth century (Langrand than 18 species into a single category (Fig. 3b). This &Wilm´e 1997), and between 1995 and 1997 this degra- approach permitted a finer discrimination among areas dation increased. Since 2002 the situation has worsened: in western Madagascar with generally low species diver- fires have encroached on the edges of the remaining frag- sity, thus permitting identification of areas of dry forests ments, and recently 30 ha of a parcel burned (D.V., un- worthy of special attention. The northwestern sector ap- published). peared more diversified than the other western areas. The

Conservation Biology Volume 19, No. 6, December 2005 1798 Conservation of Malagasy Amphibians Andreone et al. areas of highest diversity in the west coincided with some tion of (unknown) locally endemic species (Raxworthy protected forest fragments (e.g., Ampijoroa, Bemaraha, & Nussbaum, 1996; Raxworthy 2003). Kirindy, and Isalo). Patterns of species richness on the central High Plateau paralleled the general trend toward greater richness in the east and lower richness in the west Protected Areas and Endangered Species (Fig. 3a, b). In fact, the eastern portion of the High Plateau Forty-five threatened species of frogs were found in pro- wasmuch richer in species than its remaining portion. tected areas. Of the nine CR species, only three (Stumpf- The flora and fauna of the eastern area of the plateau are fia helenae, Scaphiophryne gottlebei, and Mantella ex- characterized by a species composition that is more sim- pectata) currently occur within a protected area (R´eserve ilar to the eastern rainforests than regions farther west. Sp´ecial d’Ambohitantely and Parc National de l’Isalo), and The overlay of the distributions of highly threatened therefore benefit from legal protection. M. aurantiaca species showed that many of them fall primarily in occurs at a site (Torotorofotsy Marsh) that soon will be- the northern and northeastern highlands (Fig. 3c), in- come legally protected as a Ramsar site (ANGAP 2001). Of cluding the protected areas of Masoala and Marojejy- the threatened species in other categories (EN, VU; Table Anjanaharibe, Tsaratanana, Manongarivo, Lokobe (Nosy 1), three are not known from protected areas: Anodon- Be), and Montagne d’Ambre. A second concentration thyla rouxae, Plethodontohyla coronata, and Scaphio- point of threatened species occurred in the extreme phryne boribory. Their threatened status is thus worthy southeast, in humid forests of the Anosy and Vohimena of special attention in defining new protected areas. mountains. A third group of threatened species occurred The CR species most at risk of extinction (Mantella on the central massifs of Ankaratra and Andringitra. cowani, Boophis williamsi, Mantidactylus pauliani, Other areas with important concentrations of threatened and Stumpffia helenae) live on the High Plateau, where species are in the vicinity of Moramanga (for many species much of the original habitat has been lost because of Mantella) and at Isalo Massif (for Mantella expectata of extensive slash-and-burn agricultural practices and and Scaphiophryne gottlebei). erosion. These species survive in only a few isolated sites surrounded by landscapes hostile to amphibians Discussion (e.g., secondary savannahs and spoiled soils) that rep- resent dispersal barriers between populations. Degrada- Present Extinction Status of Amphibian Fauna tion of montane habitats in the High Plateau may also af- fect other species classified as endangered: Mantidacty- An interesting result of our evaluation is that, with the ex- lus guibei, M. madecassus, M. microtis, Anodonthyla ception of two species (Anodonthyla rouxae and Man- rouxae, Platypelis alticola, and Plethodontohyla guen- tidactylus ambohimitombi), the existence of all species therpetersi. of Malagasy frogs described since the nineteenth century The remaining threatened species (mostly in EN and VU was confirmed during the last 15 years in our own field- categories) occur in the eastern and northwestern rain- work. This suggests that Madagascar has so far escaped forest belt at low- to mid-elevation areas (≤1000 m): Man- large-scale, recent amphibian extinctions such as those tella bernhardi, Mantidactylus brunae, M. horridus, reported in many other areas of the world (e.g., Central M. microtympanum, M. silvanus, M. webbi, Madecas- America, Australia, and the United States) (Heyer et al. sophryne truebae, Platypelis milloti, Plethodontohyla 1988; Alexander & Eischeid 2001; Young et al. 2001). brevipes, and Scaphiophryne boribory. They all have re- We currently suspect our failure to confirm Anodonthyla stricted ranges and some are rare or localized, although rouxae (in the Anosy Mountain chain in southeastern sometimes locally abundant. Madagascar) and Mantidactylus ambohimitombi (in the High Plateau) is a consequence of insufficient field re- search in these regions. Data-Deficient Species and Undersampled Areas Species rarefaction of Malagasy amphibians is due mainly to habitat loss. Extensive habitat degradation and Forty-six species (20.6% of the known amphibians) were forest destruction, however, have not yet caused perceiv- categorized as data deficient (DD). For these species it able extinctions of amphibian species. We believe the rea- was difficult to provide reliable conservation recommen- son for this is that amphibian species are able to survive in dations, except based on ecological parameters (e.g., An- small forest areas within comparatively small populations. dreone & Luiselli 2003). The DD list includes mostly re- Nonetheless, habitat alteration can quantitatively affect cently described species, for which geographic distribu- the species composition of communities over brief time tions are still poorly known, that in many cases are still scales (Andreone 1994; Vallan 2000b, 2002). Although restricted to a single forest site (e.g., Boophis feonnyala, we are not aware of documented species extinctions, we B. liami, and B. solomaso) (Glaw et al. 2001; Vallan et al. cannot exclude the possibility that the extensive clearing 2003). Field research is therefore badly needed to update of the High Plateau may have already caused the extinc- and clarify their status in the wild.

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The DD list also includes species whose and cies. Not all species of these genera are highly sought after identifications are provisional. Many of these are, in real- by the pet trade. For example, some less attractive species ity, assemblages of closely related taxa, and their system- of Mantella (e.g., M. betsileo, M. bernhardi, and M. har- atic revision will result in the descriptions of new species. aldmeieri)are only occasionally collected for commercial The IUCN listing will therefore need to be updated once purposes and are mainly threatened by habitat modifica- their systematic status is resolved. Many of the DD frogs tions (Rabemanjara et al. 2005). Other species (e.g., M. are cophyline microhylids, for which the taxonomy and nigricans, M. baroni, and M. pulchra)are more regularly even the specific attribution are often dubious (Andreone seen in commercial markets but are not especially threat- et al. 2005). For example, within this group we lack suffi- ened at present because they have wide distributions. cient systematic resolution of Platypelis cowani, P. polli- Ageneral problem concerning traded species is the caris, Plethodontohyla minuta, Stumpffia psologlossa, lack of information about the effect of commercial col- and S. tetradactyla to provide a reliable conservation as- lecting on the integrity of populations. Nonetheless, it sessment. Similar problems pertain to species of Boophis is our conviction that when ecological requirements and and Mantidactylus (e.g., B. brachychir and M. puncta- sensitivity to habitat alteration are combined with inten- tus). sive capture, the species in question become more en- Most of the research activity in Madagascar has been dangered. This is the case for Mantella cowani, whose carried out in areas that are already known for high small distribution, concurrent habitat alteration, and col- species diversity (e.g., Andasibe) or have good vegeta- lection combine to make this one of the most threatened tional cover (e.g., Masoala, Marojejy). There are other ar- frog species of Madagascar (Andreone & Randrianirina eas that are undersampled, such as large portions of south- 2003). In other cases, such as for Mantella aurantiaca eastern Madagascar, especially between the Andringitra and Scaphiophryne gottlebei, populations are still large Massif and the Anosy Mountains. Especially little is known enough to sustain some well-regulated commercial col- of areas that are not yet legally protected. In these areas lecting. the abundance and diversity of amphibians can be rapidly The tomato frog, Dyscophus antongili,isthe only assessed; therefore, amphibians here are well suited for species of Malagasy amphibian currently listed in CITES, biological assessment surveys (Andreone & Randrianirina Appendix I (since 1987). Its inclusion implies a complete 2000). Indeed, the analysis of amphibian diversity in some ban on trade because large quantities of this attractive unprotected areas was the basis for their upgrading and species were formerly exported. Our observations in the for integrations of protected networks, such at Betaolana coastal town of Maroantsetra indicate the tomato frog between Anjanaharibe-Sud and Marojejy (Andreone et al. is moderately common, living partly burrowed in sandy 2000). soil and reproducing in sewage ditches (Glaw & Vences Another area where the pattern of amphibian diversity 1994), and that trade does not constitute a current threat. is almost unknown is the central High Plateau. We believe Habitat alteration and the uncertainty of its occurrence in this area was originally less rich in species than the eastern protected areas (e.g., no reliable records within the Ma- rainforest escarpment. Now heavy anthropogenic pres- soala National Park), however, pose some problems for sure has resulted in an almost total deforestation of the survivorship of the largest populations. Surprisingly, ex- area and caused further impoverishment, with presence cept for a few notes (e.g., Pintak 1987), little is known of savannah-like grasslands and eroded lands. The resid- about this species. The tomato frog was previously cate- ual small forest fragments and small vegetation belts along gorized as vulnerable by IUCN (Raxworthy & Nussbaum the streams and rivers and a few high-elevation moors are 2000), whereas we classified it as near threatened. The the only surviving natural habitats. These forest islands tomato frog is regularly bred in captivity (De Vosjoli & may harbor undescribed species. Mailloux 1990), and this may constitute an advantage with Other undersampled areas for amphibians include the respect to other species because the trade could be sup- western deciduous forests, which are heavily logged; the plied with captive-bred rather than wild individuals. In- dry area between Montagne d’Ambre and the Marojejy- stead, attention should be paid to the situation regarding Masoala complex in northeastern Madagascar; and the D. guineti, which has become more subject to capture lowlands of the east coast south of Toamasina, which is as a consequence of the inclusion of D. antongili in Ap- largely deforested. A program of survey work in these pendix I. areas is therefore urgent. Proposals for Amphibian Conservation International Trade Impacts and CITES Listings The CR frog species could be used to catalyze amphib- Several CR and EN species are in demand for interna- ian conservation action in Madagascar, where a “flagship tional trade. The genus with the highest number of threat- approach” may be useful. In particular, the establishment ened species is Mantella, with 10 out of the 15 described of Mantella sanctuaries would afford protection for Man- species, followed by Scaphiophryne, with 3 out of 7 spe- tella and other amphibian species. We suggest that at least

Conservation Biology Volume 19, No. 6, December 2005 1800 Conservation of Malagasy Amphibians Andreone et al. some of these areas be integrated into a protected-area bution modeling approaches in Madagascar (Raxworthy network. A possible sanctuary in central-eastern Madagas- et al. 2003). This would allow us, for example, to map car might include the Torotorofotsy wetlands and nearby the distributions of amphibian species currently excluded areas, where M. aurantiaca, M. crocea, M. baroni, and from protected areas and thus make recommendations for M. pulchra occur. At least some areas here, with a high new protected areas that maximize unprotected amphib- diversity of CR species, fall within areas of high overall ian inclusion. amphibian diversity (Fig. 3). This area and the forests sur- The inclusion of some species in CITES listings may rounding Andasibe are known for their high frog diversity present a reliable method for monitoring and thereby pro- (>100 species, F.G. and M.V., unpublished) and for high tecting species in the commercial trade. With the excep- levels of biological diversity overall. tion of the tomato frog, most of the other traded species Moreover, some other areas that host threatened are in Appendix II. The only species in trade that are not species are not yet included in the protected-area net- included on any list and are classified as EN or VU are work. These are, for example, Fierenana, which contains Scaphiophryne boribory and S. marmorata. These two typical habitat for Scaphiophryne boribory and Mantella species should be incorporated in CITES Appendix II be- milotympanum, and Montagne des Fran¸cais, which con- cause of their attractiveness and high market demand. tains typical habitat for Mantella viridis. General habitat Regulation of their exportation would allow monitoring conservation in these areas will aid in the protection of for this and other traded and threatened species. the CR species, and protection of a CR species (such as M. aurantiaca at Torotorofotsy) will help preserve a habitat that otherwise would be subject to degradation or defor- Acknowledgments estation. Because Mantella cowani is present only in relict natu- Many people helped us during our fieldwork and other ralhabitats on the High Plateau, where the overall species efforts in surveying the biodiversity of Madagascar: B. diversity is low, a special effort should be made to pre- Andriamihaja, G. Aprea, J. L. Behler, O. Behra, P. Bora, serve high-elevation moors and heaths where the species Y. Chiari, E. J. Edwards, S. M. Goodman, F. Mattioli, occurs (Raxworthy & Nussbaum 1996). This could be at S. Mahaviasy, M. Puente, F. C. E. Rabemanjara, N. Ra- some sites next to Antoetra, where the species is present bibisoa, L. Raharivololoniaina, E. Rajeriarison, D. Rako- and where the major haplotype richness has been con- tomalala, E. Rakotomavo, D. M. Rakotondramanana, D. firmed (Chiari et al. 2005). Banning trade in M. cowani Rakotondravony, J. B. Ramanamanjato, O. Ramilijaona, and investigating whether the species could be reliably O. Ramilison, H. Randriamahazo, R. D. Randrianiaina, bred in captivity to generate captive stocks should be J. E. Randrianirina, A. P. Raselimanana, R. Razafindra- associated with efforts to get more precise data on its dis- soa, A. and A. Razafimanantsoa, G. Schneider, M. O. So- tribution, population abundance, and genetic isolation. hantenaina, M. Thomas, D. R. Vieites, P. Talata, and P. This approach must be carefully managed because the C. Wright. The fieldwork was conducted under agree- species has not yet been bred successfully in captivity. ments with the Minist`ere des Eaux et Forˆets and the A major concern is the conservation of other plateau Association Nationale pour la Gestion des Aires Pro- species such as Boophis williamsi and Mantidactylus teg´ees (ANGAP), which provided the necessary autho- pauliani that occur at a few unprotected sites in areas rizations. The Global Amphibian Assessment was primar- with comparatively low species diversity. We suggest that ily funded by the Moore Family Foundation, and the Gor- further research be conducted on these species and that don and Betty Moore Foundation. The GAA workshop known distribution areas will benefit from special atten- on the amphibians of Madagascar was funded by Conser- tion. vation International (Madagascar). This study was sup- A complementary conservation approach is necessary ported by grants of the following institutions: BIOPAT to identify unprotected areas with high amphibian di- Foundation, Chicago Zoological Society, Declining Am- versity. Areas thus identified can then be proposed as phibian Population Task Force, Deutsche Gesellschaft f¨ur amphibian reserves. Some of these areas are coincident Herpetologie und Terrarienkunde, Deutsche Forschungs- with Mantadia-Analamazaotra and the Torotorofotsy wet- gemeinschaft, Deutscher Akademischer Austauschdienst, lands and Fierenana forest. Others are around Andoha- Douroucouli Foundation, Earthwatch, MacArthur Foun- hela, the more northerly Anosy-Vohimena Mountains, and dation, Madagascar Fauna Group, MAVA Foundation, the northern corridor forests that link the four reserves Nando Peretti Foundation, National Amphibian Conser- of Masoala, Anjanaharibe-Sud, Marojejy, and Tsaratanana. vation Center, National Geographic Society, National Sci- Some of these reserves already have well-established ence Foundation, Netherlands Organisation for Scien- conservation programs, and it should be possible to in- tific Research, Swiss Academy of Sciences, U.S. Depart- clude long-term monitoring programs to assess potential ment of State, Volkswagen Foundation, Wildlife Conser- population changes in sensitive taxa or communities. We vation Society, and World Wide Fund for Nature. Spe- also envision interesting prospects for using new distri- cial thanks to the Museo Regionale di Scienze Naturali

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(Torino) and Conservation International (Madagascar) for antongilii and D. insularis.Pages 181–193 in M. J. Uricheck, editor. having kindly and generously supported the publication Proceedings of the 13th international herpetological symposium. of the color maps and plates. Many thanks also to D. Fis- International Herpetological Symposium, Inc., Salt Lake City, Utah. ESRI (Environmental Systems Research Institute) 2000. ArcView GIS chman and S. Krogh of Conservation International, who 3.2a. ESRI, New York. provided much-appreciated help in the spatial analysis of Ganzhorn, J. U., B. Rakotosamimanana, L. Hannah, J. Hough, L. Iyer, the species range maps. A. P. Raselimanana, an unknown S. Olivieri, S. Rajaobelina, C. Rodstrom, and G. Tilkin. 1997. Priori- referee, F. Hawkins, and G. Meffe provided useful com- ties for biodiversity conservation in Madagascar. Primate Report 48: ments and criticisms on an earlier draft of this paper. 1–81. Glaw, F., and M. Vences. 1994. 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