Saving the diverse Malagasyamphibian fauna: where are we four years

after implementationof the Sahonagasy Action Plan?

FrancoAndreonea,AngusI.Carpenterb, JamiesonCopseyc,AngelicaCrottinid,GerardoGarciac,RichardK.B.Jenkinse,f, JörnKöhlerg,NirhyH.C.Rabibisoah,

HerilalaRandriamahazoi &ChristopherJ.Raxworthyj

a Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123 Torino, Italy;<franco.andreone@regione.piemonte.it>

b Centre for Ecology, Evolution and Conservation, School of Environmental Sciences,University of East Anglia, Norwich NR4 7TJ, United Kingdom

c Durrell Wildlife Conservation Trust, Les Augrès Manor, La Profonde Rue Trinity,Jersey JE3 5BP Channel Islands, United Kingdom

d Division of Evolutionary Biology, Institute of Zoology, University of Braunschweig, Spielmannstr. 8,38106 Braunschweig, Germany [Current address: CIBIO, Centro de Investigação

em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, R. Padre Armando Quintas,4485-661 Vairão, Portugal]

e Madagasikara Voakajy, BP 5181, Antananarivo 101, Madagascarf Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation,

University of Canterbury, Kent CT2 7NR,United Kingdom

g Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germanyh Amphibian Specialist Group/Conservation International, Explorer Business Park, Bâtiment C2,

Village des Jeux, Akorondrano,101 Antananarivo, Madagascar

i Amphibian Specialist Group / Madagascar Biodiversity Partnership, Antananarivo 101, Madagascarj Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street,

New York, 10024-5192, USA

We reviewed the actions carried out in the four years since the launch ofthe initiative ‘‘A Conservation Strategy for the Amphibians of Madagascar’’(ACSAM), which represents Madagascar’s contribution to the global amphi-bian conservation effort, to determine if progress has been consistent withexpectations. Of the targeted actions listed in the Sahonagasy Action Plan(SAP), 29 % have been fully implemented, 33 % partially implemented,whilst there was no evidence of progress for 38 %. We estimate that 41 %of the 1.4 million Euros needed in the first four years have been allocated todate. Difficulties encountered during this period included political instabi-lity, donor withdrawal from Madagascar and aligning research actions withconservation priorities; however, we expect all these issues will improveover the longer term. Until recently there was no confirmed evidence ofBatrachochytrium dendrobatidis fungus in Madagascar. Efforts are cur-rently underway to implement policies to reduce the risk of future Batra-chochytrium dendrobatidis introduction and dispersal across the island.In addition, no amphibians have dramatically declined or gone extinct overthe past four years, and ongoing survey works continue to discover newspecies.

Alytes, 2012, 29 (1¢4): 44-58.

Introduction

With more than 284 endemic frog species (number in December 2011), and many othersstill waiting to be described, Madagascar is one of the top hot spots for global amphibianspecies richness (Vieites et al., 2009). In 2005, the Global Amphibian Assessment (GAA)categorized 55 amphibians of Madagascar as threatened with extinction over a total numberof 220 species (thus corresponding to 25 %), based on the IUCN Red List Categories andCriteria (2001). Of these, nine species were classified as Critically Endangered (CR), 21 asEndangered (EN) and 25 as Vulnerable (VU) (Andreone et al., 2005). In a subsequent RedList update, Andreone et al. (2008b) revised this list to comprise 66 species: six CR, 31 ENand 29 VU. This list was subsequently approved by IUCN, and listed in the IUCN Red List(Anonymous, 2010), with a further addition in the CR category, which now comprises sevenspecies. The most recent update by IUCN (downloaded on 1st July 2011) revealed an overallnumber of 66 threatened species over 242 considered species (thus corresponding to 27.3 %).

The 2006 official launch of the initiative ‘‘A Conservation Strategy for the Amphibians ofMadagascar’’ (ACSAM) and the subsequent endorsement of the ‘‘Sahonagasy Action Plan’’(SAP) as Madagascar’s national amphibian action plan to implement the ACSAM, providedstakeholders and potential donors with a clear and consensual road-map for a five-yearperiod. Andreone & Randriamahazo (2008) identified eight priority strategic axes for theaction plan, ranging from field research and captive breeding to the development of a unifiednational research specimen collection. We are now in the final phase of the period covered bythe initial action plan, and we consider it important to evaluate the progress made towardsthese key targets.

Complete implementation of the SAP was estimated to cost almost 1.8 million Eurosover a five-year period, but only a fraction of these funds have been raised so far. Madagascarwas plunged into a political crisis in 2009 that led to the suspension of donor activity frommany of the traditional funding sources for biodiversity conservation (Randriamalala &Liu, 2010). An increase in illegal logging in key biodiversity areas such as the MasoalaPeninsula and Marojejy (Schuurman & Lowry, 2009) and other environmental crimes(Barrett & Ratsimbazafy, 2009), have been linked to the limited capacity of the newgovernment of Madagascar to enforce the laws managing the use of natural resources. Ofcourse, this poses a significant difficulty for the conservation of natural environments on theisland (Freudenberger, 2010). Until recently, there was no evidence of the presence ofthe chytrid fungus Batrachochytrium dendrobatidis (Bd) (Weldon & Du Preez, 2008).Government support is needed to implement the chytrid-monitoring program. For thisreason, efforts are currently underway to implement new agreed policies to reduce the risk offuture dispersal and mass mortalities.

Here, we provide an evaluation of the activities carried out within the SAP, includingachievements and funds raised for each of the conservation priorities in the four years sincethe launch of the ACSAM Initiative. A more detailed review is beyond the scope of thisarticle, but we assess here the overall progress made towards reaching these objectives.

Andreone et al. 45

Material and methods

To assess the results and progress made since launching ACSAM, we referred to theconservation priority axes highlighted by the SAP. For each of these priorities (summarized intab. 1), we listed the funds originally estimated to achieve full implementation, and estimatedthe level of implementation for each of the actions within each priority using the followingthree categories: (1) full implementation (Yes); (2) partial implementation (Partially); and (3)no implementation to date (No).

We also provided comments and preliminary economic considerations affecting thesuccess of the intended investment. We estimated the total funding provided through grantsand/or indirect funding by the SAP for the four-year time period (2007¢2010) in terms ofoverall achieved performance for each priority. We assigned 100 % to the ‘‘Yes’’ category,50 % to ‘‘Partially’’ and a 0 % for ‘‘No’’, based on the estimated euro cost to achieve fullimplementation per priority.

Results

Full implementation of activities listed for all eight major priorities was reported in 29 %of cases, a further 33 % were underway and 38 % had yet to begin (tab. 1, fig. 1). Examiningeach conservation action in detail, the highest proportion of implemented activities wasassociated with trade and disease (fig. 2). Encouragingly, all activities in the focal area priority(selection and management of areas specifically devoted to amphibian conservation) havebeen initiated. Least progress was reported for captive breeding, monitoring potential impactsof climate change and unification of national herpetological collections. We estimate that41 % (594,000 Euros) of the required total funds (1,440,000 Euros) had been allocated (viadirect and indirect actions) during the four-year period (tab. 1, fig. 2).

Discussion

Overall performance, coordination and awareness

Having developed a program of needed actions for amphibian conservation, we considerthat a lack of funding and insufficient coordination have been the main limitations toimplementing the SAP. The estimated invested sum to date represents only a fraction of thenecessary financial backing, and mostly comes from indirect funds that support conservationin important sites for amphibians but are not channeled to saving frogs per se. Moreover, thecombination of the global recession and the political instability in Madagascar produced achallenging environment for fund-raising, especially for a generally overlooked biodiversitypriority like amphibian conservation. Large organizations, including governments and envi-ronmental NGOs, do not consider the biodiversity importance of frogs (and the threats facing

46 ALYTES 29 (1¢4)

Andreone et al. 47

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Fig. 1. ¢ Percentage of accomplishment of actions outlined in the Sahonagasy Action Plan. Numbers arethe total number of actions in each category.

Fig. 2. ¢ Comparison of the estimated funds raised and required to implement the Sahonagasy ActionPlan (Andreone & Randriamahazo, 2008).

Andreone et al. 49

them) among their biodiversity priorities. By comparison, in Madagascar, bird and primateconservation usually benefit from a much larger coordinated action of different stakeholders(and admittedly a higher international profile for these animals).

Regarding coordination, a relevant question can be posed: is scientific research onamphibians in Madagascar aligned with the conservation priorities identified in the SAP, orare academics more strongly guided by other factors (e.g., donor and grant priorities,scientific fashions, or home institution performance review criteria)? Soul-searching byconservation scientists has questioned whether academic research in high impact journals hasa significant, or indeed any, impact on conservation (Meijaard & Sheil, 2007; Sunderlandet al., 2009). In line with this, in a recent assessment of the impact of forest and habitatdegradation in Madagascar, the authors drew attention to the need for more applied studiesthat address directly how species respond to environmental change, and called for a reducedemphasis on purely academic research topics (Irwin et al., 2010).

However, in the case of Madagascar, almost all amphibian research activities to datehave had positive implications for conservation, largely through better describing the spatialand taxonomic diversity of endemic species, and new research initiatives have been betteroriented to the ACSAM priorities. Examples range from contributions on the definition ofcandidate species (Vieites et al., 2009; Padial et al., 2010), through descriptions of agestructure and life history traits (e.g., Guarino et al., 2010; Andreone et al., 2011; Tessa et al.,2011), to the conservation of Mantella aurantiaca breeding ponds (Randrianavelona et al.,2010).

For the research on Malagasy amphibians to be of maximum use to conservation, itneeds to be conducted in high priority sites and the results need to be communicated to thestakeholders who will actually do the conservation. A mechanism that has gained traction isthe implementation of electronic group lists that allow participants to interact and shareexperiences. The MadFauna-Herp@yahoogroups.com (together with some Facebook pagesand causes) has helped to raise awareness on amphibian conservation in Madagascar. Forexample, actions on the conservation of two CR species of the Ankaratra Massif after arecent burning event, Boophis williamsii and Mantidactylus pauliani, were implementedthrough Facebook advertising (Schuurmann & Andreone, 2010). Another important stepwas the realization of the dedicated Sahonagasy website (<http://www.sahonagasy.org>),where information on the activities, results of conservation campaigns and an extensivebibliography are provided.

In terms of program implementation, we also suggest an approach that collates theresults from ongoing conservation and research activities in a form that is accessible to a widerstakeholder audience. This could take the form of an annual or biennial report. Because aconsiderable part of amphibian research in Madagascar is led by overseas researchers basedat different institutions, and who publish in a range of scientific journals, it would also behelpful to summarise key findings in a single open-access document. Moreover, it would beappropriate to store French language abstracts of all scientific publications about Malagasyfrogs, and this could be easily done through the Sahonagasy website.

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Research and monitoring

Herpetologists in Madagascar continue to survey important areas for amphibians andtheir efforts are particularly fruitful in terms of taxonomic discoveries and, recently, inhighlighting the biodiversity importance of forests in the North and West (Köhler et al.,2005; Vences et al., 2008; Glaw et al., 2010).

A recurring theme that cuts across different SAP priorities (e.g., disease, climate changeand trade) is the need to establish monitoring programs. Amphibian inventories in Madagas-car have traditionally consisted of short visits to focal areas with an associated low power todetect rare or elusive species. Moreover, monitoring programs need to be carefully designed toensure that they have enough power to detect changes. Regular and long-term amphibianmonitoring is still in its preliminary phase in Madagascar.

Survey and monitoring work were not helped by the fact that nocturnal research(indispensable for any amphibian-oriented field work) was temporarily forbidden in someprotected sites, as a result of perceived dangers from illegal logging activity. In addition, theinterdiction of voucher collection in protected areas affected the taxonomic baseline neededfor developing biodiversity assessments, estimates and monitoring programs.

The next few years should see a revised evaluation of the representation of Madagascar’samphibians within the network of protected areas, as well as identifying areas for which thereremain insufficient data. This revision should also incorporate the changes in species extinc-tion risk as assessed on the IUCN Red List. This work will be further enhanced by theresumption of nocturnal research, allowing a full range of research activities to be conductedwithin protected areas. The delay in implementing a monitoring program is obviously alsoreducing our ability to detect and mitigate the impacts of climate change (Rabibisoa et al.,2008; Raxworthy, 2008; Raxworthy et al., 2008b).

Management of focal amphibian sites

Recent increased attention at some ‘‘focal amphibian sites’’ is resulting in new protectedareas created for the conservation of threatened frogs. This is a welcome move, but obviouslyneeds more support and development. Options for securing amphibian-friendly managementin focal amphibian sites are few, but more projects that seek to purchase land for conservationmay constitute a solution. Here we report three examples.

The Critically Endangered Mantella cowanii is one of the most threatened amphibians ofMadagascar (Andreone & Vences, 2008). Its distribution is restricted to the central, highlydegraded highlands of Madagascar, and the number of known populations is very small(Rabibisoa et al., 2009). A site next to Antoetra, where the species occurs, has been chosen asan area dedicated to the conservation of this species (Rabibisoa, 2008). The site is currentlymanaged by local authorities with the assistance of Conservation International and the NGOMan and the Environment (MATE). Activities within the area, such as planting native andessential oil plant and energy woods in the buffer zone deal with livelihoods, whilst conserva-tion efforts have resulted in the creation of fire breaks.

Andreone et al. 51

The Critically Endangered Mantella aurantiaca is restricted to a small area of easternMadagascar where its breeding ponds are severely threatened by forest loss and mining (Boraet al., 2008; Randrianavelona et al., 2010). The long-term future of M. aurantiaca isuncertain and none of the sites where it occurs are found within a strictly protected area.Conservation efforts since 2008 have focussed on establishing a new protected area atMangabe and engaging with stakeholders at other sites. A species conservation strategy waslaunched in February 2011 by the government of Madagascar that sets out the key steps overthe next five years to maintain this species in the wild.

Another iconic species, the Near Threatened ‘‘true’’ tomato frog Dyscophus antongilii(Raxworthy et al., 2008b) has an important urban nucleus in Maroantsetra, where thespecies inhabits some small ponds and canals (Tessa et al., 2007). During recent years, thespecies appears to have declined, although the driver of this apparent decline remainsunknown. For this reason, a small patch of land adjacent to one of the best known existingbreeding sites was purchased using funds obtained through BIOPAT, and will be managed bya local NGO, Antongil Conservation.

Diseases

Until recently, the lethal chytrid fungus was claimed to be absent from Madagascar. Thisstatement was based on a series of published (Weldon et al., 2008; Andreone et al, 2008) andunpublished data. Studies carried out on the suitability for Bd colonization unequivocallyshowed that Madagascar is particularly prone to its colonization (Lötters et al., 2008).Especially concerning is the fact that recent laboratory tests have clearly shown that Malagasyspecies are susceptible to Bd infections and may suffer varying degrees of mortality wheninfected (C. Weldon, personal communication). A recent paper by Rabemananjara et al.(2011) quoted the possible presence of Bd in a remote area of central-western Madagascar,but this needs confirmation.

Most of the recent actions carried out by the IUCN SSC Amphibian Specialist Group(ASG) in Madagascar were aimed at developing a national strategy to counteract Bd spread.This included a workshop on chytrid prevention held in eastern Madagascar during October2010, and the publication of a specific guideline, including a three-year monitoring program(Garcia, 2010; Rabibisoa & Raharivololona, 2010). This monitoring action is focused oneight sites chosen on the basis of the following criteria: (1) amphibian diversity (high speciesrichness and abundance implies high availability of hosts and high transmission rates betweenhosts); (2) tourist value (high visitation rate by tourists increases the chance of accidentalintroduction or diffusion of chytrid); (3) geographic distribution (the distribution of sitescover a large area of the island and include high elevation sites, which are prone to amphibianpopulation declines elsewhere); (4) baseline data ¢ it is advantageous to select sites wherebaseline data are available from similar former surveys; and (5) human resources (areas wherepeople are already involved in amphibian research). Sampling is being and will continue to beconducted during the amphibian breeding season, which coincides with the rainy season(November¢April), since this is the time when amphibians are most abundant. One survey isconducted at the beginning of the season and one near the end of the season, thus harnessing

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the opportunity to sample both early explosive breeders and juveniles that begin to emergetowards the latter half of the season.

Taking into account the importance of an early detection of Bd, we also encourage theherpetological community working in Madagascar to regularly screen amphibian tissuesamples for the detection of Bd. It will be important to investigate a wide range of sites,including high altitude sites with heavy anthropogenic pressure; we also advocate the need forBd screening in areas much more sensitive to potential introductions and human transit, suchas spots close to harbors, airports, etc.

Captive breeding

Captive breeding for conservation was indicated as a specific objective in the SAP (Buleyet al., 2008), but so far progress has been limited. Currently, captive breeding facilities arebeing built at Andasibe by the Association Mitsinjo; and a husbandry program for severalanalogue species belonging to different ecological guilds is being established in collaborationwith the University of Antananarivo (Pramuk & Edmonds, 2011). Because captive breedingis considered as one of the few viable options for preventing declines and extinctionsassociated to Bd infection, this issue needs to be given greater attention in Madagascar.

Trade and harvesting

Relatively few Malagasy amphibians are harvested for food or traded commercially aspets (Andreone et al., 2006; Jenkins et al., 2009), but a few large frog species are collected fordomestic consumption (e.g., Mantidactylus grandidieri, M. guttulatus, Boophis goudotii) andsome of the colourful Mantella spp., Dyscophus spp. and Scaphiophryne spp. are subject toexport for the international pet market (Andreone et al., 2006; Rabemananjara et al., 2008;Jenkins et al., 2009). Arguably, trade and harvesting still remains one of the areas where therehas so far been insufficient support from scientists. For example, Madagascar is regularlychallenged by the ‘‘Convention on International Trade in Endangered Species of Wild Faunaand Flora’’ (CITES) to defend its export quota for highly threatened species like Mantellaaurantiaca, and improved population data for wild frogs subjected to commercial collectingare needed.

Further areas of conservation implementation

Many of the other priority activities reported in the SAP are currently underway andeven though some of these would have happened regardless of the initiative, there is a strongfeeling that some of the projects might not have happened if the SAP framework had not beenin place.

Two main priorities need further attention, since there was no evident improvementduring the SAP’s time frame: ‘‘Priority 8’’ of tab. 1 (Development of a unified herpetologicalcollection). This priority involves the realization of a large and accessible scientific collection,

Andreone et al. 53

necessary to develop and implement a taxonomic resource for local and foreign scientists.Such a collection currently exists at Université d’Antananarivo, Département de BiologieAnimale (UADBA) (Ramilijaona Ravohoangimalala, 2008; Ramilijaona Ravohoangi-malala et al., 2008), and its size is constantly increasing. One of the major problems affectingthe management of this resource is that no permanent curatorial position has yet beenestablished, although the collegial management by university professors and students repre-sents a good compromise. The unification and/or shared management of the Universitycollection and the smaller collection held at the Parc Botanique et Zoologique de Tsimbazaza(PBZT) has not happened yet, in spite of the evident curatorial and scientific advantages thatthis action could bear. Such reluctance is probably due to the different institutional prioritiesand the desire to maintain institutional individuality, in spite of the evident advantages interms of scientific utilization.

Another priority still needing implementation is ‘‘Priority 4’’ of tab. 1 (Climate changeand amphibians). Although some of the scheduled actions were met, most still need to becarried out, including the monitoring of high elevation amphibian species and captivebreeding. The main impediment here has been the lack of funding from potential donors,which has resulted partly from the recent political instability in Madagascar. However, higherelevation sites in Madagascar have also historically not benefited much from funding fromenvironmental NGOs, presumably because the human pressures on these habitats are typi-cally lower, yet access and management logistics are more challenging.

Efforts to attract funding for these initiatives will continue. To conclude, we remainoptimistic that these outstanding actions on amphibian conservation in Madagascar will besignificantly implemented in the forthcoming years, and this evaluation should thus beconsidered as an attempt to measure progress towards meeting these objectives. An importantadditional issue to be considered in the future is the ASG becoming an association withjuridical status in Madagascar. This would allow the group to continue to direct its actionsand initiatives for amphibian conservation, but also, over the longer term, attract and managefunds in an independent and autonomous way.

Résumé

Nous passons en revue les actions menées lors des quatre années écoulées depuis lelancement de l’initiative ‘‘Une stratégie de conservation pour les amphibiens de Madagascar’’(ACSAM), qui constitue la contribution de Madagascar au programme mondial de conser-vation des amphibiens, afin de déterminer si les progrès ont été conformes aux attentes. Parmiles actions ciblées figurant dans le Plan d’Action Sahonagasy (SAP), 29 % ont été pleinementmises en œuvre, 33 % partiellement mises en œuvre, alors qu’il n’y avait pas de progrèsévidents pour les 38 % restants. Nous estimons que 41 % des 1,4 million d’euros nécessaires aucours des quatre premières années ont été attribués. Les difficultés rencontrées au cours decette période sont l’instabilité politique, le retrait des bailleurs de fonds en provenance deMadagascar et l’ajustement des actions de recherche avec les priorités de conservation, maisnous nous attendons à ce que tous ces problèmes puissent être résolus à plus long terme.Jusqu’à récemment, il n’existait aucune preuve confirmée de la présence à Madagascar du

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champignon Batrachochytrium dendrobatidis (Bd). Pour cette raison, des efforts sont en courspour mettre en œuvre de nouvelles actions afin de réduire le risque de sa diffusion. En outre,aucune espèce d’amphibiens n’a sérieusement diminué ou disparu au cours des quatredernières années, et les recherches en cours continuent à découvrir de nouvelles espèces.

Acknowledgements

We are indebted with the Parc Botanique et Zoologique de Tsimbazaza, Universitéd’Antananarivo, Madagascar National Parks, and the Direction des Eaux et Forêts forpermissions to work in Madagascar. Research, fieldwork and conservation measures weresupported by several organisations and groups, such as Acquario di Genova, Act for Nature,Amphibian Specialist Group, Andy Sabin Family Foundation, Association pour l’Etude et laConservation des Lémuriens, BIOPAT, Conservation International, Declining DeutscheGesellschaft für Herpetologie und Terrarienkunde, Disney Wildlife Conservation Fund,European Association of Zoos and Aquaria, Gondwana Conservation and Research, IUCNSmall Ecosystem Project Grant, Madagascar Fauna Group, Institut de Madagascar pour laConservation des Ecosystèmes Tropicaux, Mohammed bin Zayed Species ConservationFund, Museo Regionale di Scienze Naturali, Nando Peretti Foundation, the National ScienceFoundation, Van Thienhoven Foundation, World Association of Zoos and Aquariums, andWildcare Institute. Among the many people with whom we repeatedly discussed about theeffectiveness of amphibian conservation in Madagascar and whom we thank for their insightsare O. Behra, C. P. Blanc, A. Bollen, N. Cox, N. D’Cruze, K. Freeman, F. Glaw, J. Glos, V.Mercurio, R. A. Mittermeier, J. Noël, R. A. Nussbaum, I. Porton, F. Rabemananjara, J. E.Randrianirina, G. M. Rosa, A. Sarovy, S. N. Stuart, M. Vences, and C. Weldon. A. Anguloassisted during the preparation of a preliminary version of this paper.

Literature cited

Anonymous [IUCN], 2010. ¢ IUCN Red List of Threatened Species. Version 2010.2.<http://www.iucnredlist.org>.

Andreone, F., Bungard, M. & Freeman, K., 2007. ¢ Threatened amphibians of Madagascar. Torino,Museo Regionale di Scienze Naturali: 1¢32.

Andreone, F., Cadle, J. E., Cox, N., Glaw, F., Nussbaum, R. A., Raxworthy, C. J., Stuart, S. N.,Vallan, D. & Vences, M., 2005. ¢ Species review of amphibian extinction risks in Madagascar:conclusions from the Global Amphibian Assessment. Conserv. Biol., 19: 1790¢1802.

Andreone, F., Carpenter, A. I., Cox, N., du Preez, L., Freeman, K., Furrer, S., Garcia, G.,Glaw, F., Glos, J., Knox, D., Koehler, J., Mendelson III, J. R., Mercurio, V., Mittermeier,R. A., Moore, R. D., Rabibisoa, N. H. C., Randriamahazo, H., Randrianasolo, H., Rasoa-mampionona Raminosoa, N., Ravoahangimalala Ramilijaona, O., Raxworthy, C. J.,Vallan, D., Vences, M., Vieites, D. R. & Weldon, C., 2008a. ¢ The challenge of conservingamphibian megadiversity in Madagascar. PLoS Biol., 6 (5): 943¢946.

Andreone, F., Cox, N. A., Glaw, F., Köhler, J., Rabibisoa, N. H. C., Randriamahazo, H.,Randrianasolo, H., Raxworthy, C. J., Stuart, S. N., Vallan, D. & Vences, M., 2008b. ¢Update of the Global Amphibian Assessment for Madagascar in light of new species discoveries,nomenclature changes, and new field information. In: F. Andreone (ed.), A conservation strategyfor the amphibians of Madagascar, Monog. Mus. reg. Sci. nat. Torino, 45: 419¢438.

Andreone et al. 55

Andreone F., Giacoma C., Guarino F. M., Mercurio V. & Tessa G., 2011. ¢ Age profile in nineMantella poison frogs from Madagascar, as revealed by skeletochronological analyses. Alytes, 27(3): 73¢84.

Andreone, F., Mercurio, V. & Mattioli, F., 2006. ¢ Between environmental degradation and interna-tional pet trade: conservation strategies for the threatened amphibians of Madagascar. Natura ¢Soc. ital. Sci. nat. e Mus. civ. Stor. nat. Milano, 95 (2): 81¢96.

Andreone, F. & Randriamahazo, H., 2008. ¢ Sahonagasy Action plan. Conservation programs for theamphibians of Madagascar. Bogota, Museo Regionale di Scienze Naturali, Conservation Interna-tional and IUCN/SSC Amphibian Specialist Group: 1¢96.

Andreone, F. & Vences M., 2008. ¢Mantella cowanii. IUCN Red List of Threatened Species. <www.iu-cnredlist.org>.

Barrett, M. A. & Ratsimbazafy, J., 2009. ¢ Luxury bushmeat trade threatens lemur conservation.Nature, 461: 470.

Bora, P., Dolch, R., Jenkins, R. K. B., Jovanovic, O., Rabemananjara, F. C. E., Randrianirina, J.,Rafanomezantsoa, J., Raharivololoniaina, L., Ramilijaona, O. R., Raminosoa, N. R., Ran-drianavelona, R., Raselimanana, A., Razafimahatratra, B., Razafindraibe, T. & Vences,M. 2008. ¢ Geographical distribution of three species of Malagasy poison frogs of high conser-vation priority: Mantella aurantiaca, M. crocea and M. milotympanum. Herp. Notes, 1: 39¢48.

Buley, K., Furrer, S. C., Garcia, G., Gibson, R. C., Gili, C., Mattioli, F. & Andreone, F., 2008. ¢8. Captive breeding and zoo actions / Elevage en captivité et activités des parcs zoologiques. In:Andreone & Randriamahazo (2008): 67¢75.

D’Cruze, N., Henson, D., Olsson, A. & Emmett, D., 2009. ¢ The importance of herpetological surveywork in conserving Malagasy biodiversity. Are we doing enough? Herp. Rev., 40: 19¢25.

Freudenberger, K., 2010. ¢ Paradise lost? Lessons from 25 years of USAID Environment Programs inMadagascar. Washington, International Resources Group: 1¢122.

Garcia, G., 2010. ¢ Preparations for the battle against chytrid: building capacity for chytrid detection inMadagascar. Amphibian Ark Newsletter, 13. <www.amphibianark.org>.

Glaw, F., Köhler, J., De la Riva, I., Vieites, D. R. & Vences, M., 2010. ¢ Integrative taxonomy ofMalagasy treefrogs: combination of molecular genetics, bioacoustics and comparative morpho-logy reveals twelve additional species of Boophis. Zootaxa, 2383: 1¢82.

Guarino,F.M.,Tessa,G.,Mercurio,V.& Andreone,F., 2010. ¢Rapid sexual maturity and short lifespan in the blue-legged frog and the rainbow frog from the arid Isalo Massif, southern-centralMadagascar. Zool., 113 (6): 378¢384.

Irwin, M. T., Wright, P. C. W., Birkinshaw, C., Fisher, B. L., Gardner, C. J., Glos, J., Goodman,S. M., Loiselle, P., Rabeson, Raharison, J.-L., Raherilalao, M. J., Rakotondravony, D.,Raselimanana, A., Ratsimbazafy, J., Sparks, J. S., Wilme, L. & Ganzhorn, J. U., 2010. ¢Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol. Conserv.,143: 2351¢2362.

Jenkins, R. K. B., Rabearivelo, A., Andre, C. T. C. W. M., Randrianavelona, R. & Randrianan-toandro, J. C. 2009. ¢ The harvest of endemic amphibians for food in eastern Madagascar. Trop.Conserv. Sci., 2: 25¢33.

Köhler, J.,Vieites,D.R.,Bonett,R.M.,HitaGarcia,F.,Glaw,F., Steinke,D.& Vences,M., 2005.¢New amphibians and global conservation: a boost in species discoveries in a highly endangeredvertebrate group. BioScience, 55: 693¢696.

Lötters, S.,Rödder,D.,Bielby, J.,Bosch, J.,Garner,T. J.W.,Kielgast, J., Schmidtlein, S.,Veith,M., Walker, S., Weldon, C., Aanensen, D. M. & Fisher, M. C., 2008. ¢Meeting the challengeof conserving Madagascar’s megadiverse amphibians: addition of a risk-assessment for thechytrid fungus. PLoS Biol., 6 (online).

Meijaard, E. & Sheil, D., 2007. ¢ Is wildlife research useful for wildlife conservation in the tropics? areview from Borneo with global implications. Biodiversity & Conservation, 16: 3035¢3065.

Padial, J. M., Miralles, A., De la Riva, I. & Vences, M., 2010. ¢ The integrative future of taxonomy.Front. Zool.. 7 (1): 1¢16.

Pramuk, J. & Edmonds D., 2011. ¢ Establishing a captive breeding facility for Malagasy amphibians.Poster presented at the workshop hosted by Seattle’s Woodland Park Zoo, 8¢11 March 2011.<http://www.zaccconference.com>.

56 ALYTES 29 (1¢4)

Rabemananjara,F.C.E.,Raminsoa,N.R.,Ramilijaona,O.R.,Andreone,F.,Bora, P.,Carpenter,A. I., Glaw, F., Razafindrabe, T. J., Vallan, D., Vieites, D. & Vences, M., 2008. ¢Malagasypoison frogs in the pet trade: a survey of levels of exploitation of species in the genus Mantella. In:F. Andreone (ed.), A conservation strategy for the amphibians of Madagascar, Monog. Mus. reg.Sci. nat. Torino, 45: 67¢84.

Rabemananjara, F., Andreone, F. & Rabibisoa, N., 2011. Madagascar and chytrid news: needed andurgent action and close collaboration between stakeholders. Froglog 97: 33.

Rabibisoa,N., 2008. ¢ Plan d’action pour la conservation de Mantella cowani. Antananarivo, AmphibianSpecialist Group Madagascar & Conservation International: 1¢26.

Rabibisoa, N. & Raharivololona, L., 2010. ¢ Plan stratégique de prévention et de lutte contre l’intro-duction du chytride à Madagascar. Antananarivo, Conservation International & AmphibianSpecialist Group.

Rabibisoa, N., Randrianasolo, H., Anjeriniana, M., MacKinnon, J., Andriamamonjisoa, A.,Ramandimbison, Randrianantoandro, C. & Andreone, F., 2009. ¢New findings of harlequinmantella improve the conservation status of Madagascar’s most threatened frog. Froglog, 92: 5¢8.

Rabibisoa, N., Raxworthy, C. J & Andreone, F., 2008. ¢ 5. Climate change and amphibians /Changements climatiques et amphibiens. In: Andreone & Randriamahazo (2008): 43¢48.

Ramilijaona Ravoahangimalala, O., 2008. ¢ Rôle du Muséum du Département de Biologie Animalede l’Université d’Antananarivo dans la conservation de la biodiversité de Madagascar, avecspéciale référence aux amphibiens. In: F. Andreone (ed.), A conservation strategy for the amphi-bians of Madagascar, Monog. Mus. reg. Sci. nat. Torino, 45: 59¢66.

Ramilijaona Ravoahangimalala, O., Vences, M. & Andreone, F., 2008. ¢Development of a unifiedherpetological collection / Developpement d’une collection herpétologique unifiée. In: Andreone& Randriamahazo (2008): 76¢83.

Randriamalala, H. & Liu, Z., 2010. ¢ Rosewood of Madagascar: between democracy and conserva-tion. Madag. Conserv. Dev., 5 (1): 11¢22.

Randrianavelona,R.,Rakotonoely,H.,Ratsimbazafy, J.& Jenkins,R.K.B., 2010. ¢Conservationassessment of the Critically Endangered frog Mantella aurantiaca in Madagascar. Afr. J. Herp., 59:65¢78.

Raxworthy, C. J., 2008. ¢ Global warming and extinction risks for amphibians in Madagascar: apreliminary assessment of potential upslope displacement. In: F.Andreone (ed.), A conservationstrategy for the amphibians of Madagascar, Monog. Mus. reg. Sci. nat. Torino, 45: 67¢84.

Raxworthy, C. J., Pearson, R. G., Rabibisoa, N., Rakotondrazafy, A. M., Ramanamanjato, J.-B.,Raselimanana,A. P.,Wu, S.,Nussbaum,R.A.& Stone,D., 2008a. ¢Extinction vulnerability oftropical montane endemism from warming and upslope displacement: a preliminary appraisal forthe highest massif in Madagascar. Global Change Biology, 14: 1703¢1720.

Raxworthy,C.,Vences,M.,Andreone,F.& Nussbaum,R., 2008b. ¢Dyscophus antongilii. IUCN RedList of Threatened Species. Version 2010.4. <www.iucnredlist.org>.

Schuurman, D. & Andreone, F., 2010. ¢ Rampant logging, illegal collection and slash and burnagriculture driving Madagascar’s rare frogs towards extinction. Wildlife Extra.com<www.wildlifeextra.com/go/news/madagascar-frogs.html.#cr>.

Schuurman, D. & Lowry, P. P., II, 2009. ¢ The rosewood massacre. Madag. Conserv. Dev., 4: 98¢102.Sunderland, T., Sunderland-Groves, J., Shanley, P. & Campell, B., 2009. ¢ Bridging the gap: how

can information access and exchange between conservation biologists and field practitioners beimproved for better conservation outcomes. Biotropica, 41: 549¢554.

Tessa, G., Guarino, F. M., Giacoma, C., Mattioli, F. & Andreone, F., 2007. ¢ Longevity and bodysize in three populations of Dyscophus antongilii (Microhylidae, Dyscophinae), the tomato frogfrom north-eastern Madagascar. Acta herp., 2 (2): 139¢146.

Tessa,G.,Guarino,F.M.,Randrianirina, J.E.& Andreone,F., 2011. ¢The age structure in the falsetomato frog Dyscophus guineti from eastern Madagascar, compared to the closely related D.antongilii (Anura, Microhylidae). Afr. J. Herp., 60 (1): 84¢88.

Vences,M., Jovanovic,O.& Glaw, F., 2008. ¢Historical analysis of amphibian studies in Madagascar:an example for increasing research intensity and international collaboration. In: F. Andreone(ed.), A conservation strategy for the amphibians of Madagascar, Monog. Mus. reg. Sci. nat.Torino, 45: 47¢58.

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Vieites, D. R., Wollenberg, K. C., Andreone, F., Köhler, J., Glaw, F. & Vences, M., 2009. ¢ Vastunderestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory.PNAS, 106: 8267¢8272.

Weldon, C. & Du Preez, L., 2008. ¢ 4. Managing emerging amphibian diseases. Gestion des maladiesémergentes des amphibiens. In: Andreone & Randriamahazo (2008): 34¢42.

Corresponding editor: Ariadne Angulo.

© ISSCA 2012

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