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Alytes, 2012, 29 (1¢4): 44-58.

Saving the diverse Malagasy amphibian fauna: where are we four years after implementation of the Sahonagasy Action Plan? Franco Andreonea, Angus I. Carpenterb, Jamieson Copseyc, Angelica Crottinid, Gerardo Garciac, Richard K. B. Jenkinse,f, Jörn Köhlerg, Nirhy H. C. Rabibisoah, Herilala Randriamahazoi & Christopher J. Raxworthyj a

Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123 Torino, Italy; <> 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, Madagascar f 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, Germany h 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, Madagascar j Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, 10024-5192, USA b

We reviewed the actions carried out in the four years since the launch of the initiative ‘‘A Conservation Strategy for the Amphibians of Madagascar’’ (ACSAM), which represents Madagascar’s contribution to the global amphibian conservation effort, to determine if progress has been consistent with expectations. 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 to date. Difficulties encountered during this period included political instability, donor withdrawal from Madagascar and aligning research actions with conservation priorities; however, we expect all these issues will improve over the longer term. Until recently there was no confirmed evidence of Batrachochytrium dendrobatidis fungus in Madagascar. Efforts are currently underway to implement policies to reduce the risk of future Batrachochytrium dendrobatidis introduction and dispersal across the island. In addition, no amphibians have dramatically declined or gone extinct over the past four years, and ongoing survey works continue to discover new species.

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Introduction With more than 284 endemic frog species (number in December 2011), and many others still waiting to be described, Madagascar is one of the top hot spots for global amphibian species richness (Vieites et al., 2009). In 2005, the Global Amphibian Assessment (GAA) categorized 55 amphibians of Madagascar as threatened with extinction over a total number of 220 species (thus corresponding to 25 %), based on the IUCN Red List Categories and Criteria (2001). Of these, nine species were classified as Critically Endangered (CR), 21 as Endangered (EN) and 25 as Vulnerable (VU) (Andreone et al., 2005). In a subsequent Red List update, Andreone et al. (2008b) revised this list to comprise 66 species: six CR, 31 EN and 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 seven species. The most recent update by IUCN (downloaded on 1st July 2011) revealed an overall number 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 of Madagascar’’ (ACSAM) and the subsequent endorsement of the ‘‘Sahonagasy Action Plan’’ (SAP) as Madagascar’s national amphibian action plan to implement the ACSAM, provided stakeholders and potential donors with a clear and consensual road-map for a five-year period. Andreone & Randriamahazo (2008) identified eight priority strategic axes for the action plan, ranging from field research and captive breeding to the development of a unified national research specimen collection. We are now in the final phase of the period covered by the initial action plan, and we consider it important to evaluate the progress made towards these key targets. Complete implementation of the SAP was estimated to cost almost 1.8 million Euros over a five-year period, but only a fraction of these funds have been raised so far. Madagascar was plunged into a political crisis in 2009 that led to the suspension of donor activity from many of the traditional funding sources for biodiversity conservation (Randriamalala & Liu, 2010). An increase in illegal logging in key biodiversity areas such as the Masoala Peninsula and Marojejy (Schuurman & Lowry, 2009) and other environmental crimes (Barrett & Ratsimbazafy, 2009), have been linked to the limited capacity of the new government of Madagascar to enforce the laws managing the use of natural resources. Of course, this poses a significant difficulty for the conservation of natural environments on the island (Freudenberger, 2010). Until recently, there was no evidence of the presence of the chytrid fungus Batrachochytrium dendrobatidis (Bd) (Weldon & Du Preez, 2008). Government support is needed to implement the chytrid-monitoring program. For this reason, efforts are currently underway to implement new agreed policies to reduce the risk of future dispersal and mass mortalities. Here, we provide an evaluation of the activities carried out within the SAP, including achievements and funds raised for each of the conservation priorities in the four years since the launch of the ACSAM Initiative. A more detailed review is beyond the scope of this article, but we assess here the overall progress made towards reaching these objectives.


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Material and methods To assess the results and progress made since launching ACSAM, we referred to the conservation priority axes highlighted by the SAP. For each of these priorities (summarized in tab. 1), we listed the funds originally estimated to achieve full implementation, and estimated the level of implementation for each of the actions within each priority using the following three 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 the success of the intended investment. We estimated the total funding provided through grants and/or indirect funding by the SAP for the four-year time period (2007¢2010) in terms of overall 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 full implementation 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). Examining each conservation action in detail, the highest proportion of implemented activities was associated with trade and disease (fig. 2). Encouragingly, all activities in the focal area priority (selection and management of areas specifically devoted to amphibian conservation) have been initiated. Least progress was reported for captive breeding, monitoring potential impacts of climate change and unification of national herpetological collections. We estimate that 41 % (594,000 Euros) of the required total funds (1,440,000 Euros) had been allocated (via direct 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 consider that a lack of funding and insufficient coordination have been the main limitations to implementing the SAP. The estimated invested sum to date represents only a fraction of the necessary financial backing, and mostly comes from indirect funds that support conservation in important sites for amphibians but are not channeled to saving frogs per se. Moreover, the combination of the global recession and the political instability in Madagascar produced a challenging environment for fund-raising, especially for a generally overlooked biodiversity priority like amphibian conservation. Large organizations, including governments and environmental NGOs, do not consider the biodiversity importance of frogs (and the threats facing

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

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


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them) among their biodiversity priorities. By comparison, in Madagascar, bird and primate conservation usually benefit from a much larger coordinated action of diďŹ&#x20AC;erent stakeholders (and admittedly a higher international profile for these animals). Regarding coordination, a relevant question can be posed: is scientific research on amphibians in Madagascar aligned with the conservation priorities identified in the SAP, or are academics more strongly guided by other factors (e.g., donor and grant priorities, scientific fashions, or home institution performance review criteria)? Soul-searching by conservation scientists has questioned whether academic research in high impact journals has a significant, or indeed any, impact on conservation (Meijaard & Sheil, 2007; Sunderland et al., 2009). In line with this, in a recent assessment of the impact of forest and habitat degradation in Madagascar, the authors drew attention to the need for more applied studies that address directly how species respond to environmental change, and called for a reduced emphasis on purely academic research topics (Irwin et al., 2010). However, in the case of Madagascar, almost all amphibian research activities to date have had positive implications for conservation, largely through better describing the spatial and taxonomic diversity of endemic species, and new research initiatives have been better oriented to the ACSAM priorities. Examples range from contributions on the definition of candidate species (Vieites et al., 2009; Padial et al., 2010), through descriptions of age structure 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, it needs to be conducted in high priority sites and the results need to be communicated to the stakeholders who will actually do the conservation. A mechanism that has gained traction is the implementation of electronic group lists that allow participants to interact and share experiences. The (together with some Facebook pages and causes) has helped to raise awareness on amphibian conservation in Madagascar. For example, actions on the conservation of two CR species of the Ankaratra Massif after a recent burning event, Boophis williamsii and Mantidactylus pauliani, were implemented through Facebook advertising (Schuurmann & Andreone, 2010). Another important step was the realization of the dedicated Sahonagasy website (<>), where information on the activities, results of conservation campaigns and an extensive bibliography are provided. In terms of program implementation, we also suggest an approach that collates the results from ongoing conservation and research activities in a form that is accessible to a wider stakeholder audience. This could take the form of an annual or biennial report. Because a considerable part of amphibian research in Madagascar is led by overseas researchers based at diďŹ&#x20AC;erent institutions, and who publish in a range of scientific journals, it would also be helpful to summarise key findings in a single open-access document. Moreover, it would be appropriate to store French language abstracts of all scientific publications about Malagasy frogs, 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 and their efforts are particularly fruitful in terms of taxonomic discoveries and, recently, in highlighting 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 change and trade) is the need to establish monitoring programs. Amphibian inventories in Madagascar have traditionally consisted of short visits to focal areas with an associated low power to detect rare or elusive species. Moreover, monitoring programs need to be carefully designed to ensure that they have enough power to detect changes. Regular and long-term amphibian monitoring 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 some protected sites, as a result of perceived dangers from illegal logging activity. In addition, the interdiction of voucher collection in protected areas affected the taxonomic baseline needed for developing biodiversity assessments, estimates and monitoring programs. The next few years should see a revised evaluation of the representation of Madagascar’s amphibians within the network of protected areas, as well as identifying areas for which there remain insufficient data. This revision should also incorporate the changes in species extinction risk as assessed on the IUCN Red List. This work will be further enhanced by the resumption of nocturnal research, allowing a full range of research activities to be conducted within protected areas. The delay in implementing a monitoring program is obviously also reducing 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 protected areas created for the conservation of threatened frogs. This is a welcome move, but obviously needs more support and development. Options for securing amphibian-friendly management in focal amphibian sites are few, but more projects that seek to purchase land for conservation may constitute a solution. Here we report three examples. The Critically Endangered Mantella cowanii is one of the most threatened amphibians of Madagascar (Andreone & Vences, 2008). Its distribution is restricted to the central, highly degraded 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 as an area dedicated to the conservation of this species (Rabibisoa, 2008). The site is currently managed by local authorities with the assistance of Conservation International and the NGO Man and the Environment (MATE). Activities within the area, such as planting native and essential oil plant and energy woods in the buffer zone deal with livelihoods, whilst conservation efforts have resulted in the creation of fire breaks.


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The Critically Endangered Mantella aurantiaca is restricted to a small area of eastern Madagascar where its breeding ponds are severely threatened by forest loss and mining (Bora et al., 2008; Randrianavelona et al., 2010). The long-term future of M. aurantiaca is uncertain 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 at Mangabe and engaging with stakeholders at other sites. A species conservation strategy was launched in February 2011 by the government of Madagascar that sets out the key steps over the 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 the species inhabits some small ponds and canals (Tessa et al., 2007). During recent years, the species appears to have declined, although the driver of this apparent decline remains unknown. For this reason, a small patch of land adjacent to one of the best known existing breeding sites was purchased using funds obtained through BIOPAT, and will be managed by a local NGO, Antongil Conservation.

Diseases Until recently, the lethal chytrid fungus was claimed to be absent from Madagascar. This statement was based on a series of published (Weldon et al., 2008; Andreone et al, 2008) and unpublished data. Studies carried out on the suitability for Bd colonization unequivocally showed 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 Malagasy species are susceptible to Bd infections and may suffer varying degrees of mortality when infected (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 October 2010, and the publication of a specific guideline, including a three-year monitoring program (Garcia, 2010; Rabibisoa & Raharivololona, 2010). This monitoring action is focused on eight sites chosen on the basis of the following criteria: (1) amphibian diversity (high species richness and abundance implies high availability of hosts and high transmission rates between hosts); (2) tourist value (high visitation rate by tourists increases the chance of accidental introduction or diffusion of chytrid); (3) geographic distribution (the distribution of sites cover a large area of the island and include high elevation sites, which are prone to amphibian population declines elsewhere); (4) baseline data ¢ it is advantageous to select sites where baseline data are available from similar former surveys; and (5) human resources (areas where people are already involved in amphibian research). Sampling is being and will continue to be conducted 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 is conducted 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 emerge towards the latter half of the season. Taking into account the importance of an early detection of Bd, we also encourage the herpetological community working in Madagascar to regularly screen amphibian tissue samples 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 for Bd screening in areas much more sensitive to potential introductions and human transit, such as spots close to harbors, airports, etc. Captive breeding Captive breeding for conservation was indicated as a specific objective in the SAP (Buley et al., 2008), but so far progress has been limited. Currently, captive breeding facilities are being built at Andasibe by the Association Mitsinjo; and a husbandry program for several analogue species belonging to different ecological guilds is being established in collaboration with the University of Antananarivo (Pramuk & Edmonds, 2011). Because captive breeding is considered as one of the few viable options for preventing declines and extinctions associated 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 as pets (Andreone et al., 2006; Jenkins et al., 2009), but a few large frog species are collected for domestic consumption (e.g., Mantidactylus grandidieri, M. guttulatus, Boophis goudotii) and some of the colourful Mantella spp., Dyscophus spp. and Scaphiophryne spp. are subject to export 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 there has so far been insufficient support from scientists. For example, Madagascar is regularly challenged by the ‘‘Convention on International Trade in Endangered Species of Wild Fauna and Flora’’ (CITES) to defend its export quota for highly threatened species like Mantella aurantiaca, and improved population data for wild frogs subjected to commercial collecting are needed. Further areas of conservation implementation Many of the other priority activities reported in the SAP are currently underway and even though some of these would have happened regardless of the initiative, there is a strong feeling that some of the projects might not have happened if the SAP framework had not been in place. Two main priorities need further attention, since there was no evident improvement during the SAP’s time frame: ‘‘Priority 8’’ of tab. 1 (Development of a unified herpetological collection). This priority involves the realization of a large and accessible scientific collection,


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necessary to develop and implement a taxonomic resource for local and foreign scientists. Such a collection currently exists at Université d’Antananarivo, Département de Biologie Animale (UADBA) (Ramilijaona Ravohoangimalala, 2008; Ramilijaona Ravohoangimalala et al., 2008), and its size is constantly increasing. One of the major problems affecting the management of this resource is that no permanent curatorial position has yet been established, although the collegial management by university professors and students represents a good compromise. The unification and/or shared management of the University collection 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 that this action could bear. Such reluctance is probably due to the different institutional priorities and the desire to maintain institutional individuality, in spite of the evident advantages in terms of scientific utilization. Another priority still needing implementation is ‘‘Priority 4’’ of tab. 1 (Climate change and amphibians). Although some of the scheduled actions were met, most still need to be carried out, including the monitoring of high elevation amphibian species and captive breeding. 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, higher elevation sites in Madagascar have also historically not benefited much from funding from environmental NGOs, presumably because the human pressures on these habitats are typically lower, yet access and management logistics are more challenging. Efforts to attract funding for these initiatives will continue. To conclude, we remain optimistic that these outstanding actions on amphibian conservation in Madagascar will be significantly implemented in the forthcoming years, and this evaluation should thus be considered as an attempt to measure progress towards meeting these objectives. An important additional issue to be considered in the future is the ASG becoming an association with juridical status in Madagascar. This would allow the group to continue to direct its actions and initiatives for amphibian conservation, but also, over the longer term, attract and manage funds in an independent and autonomous way.

Résumé Nous passons en revue les actions menées lors des quatre années écoulées depuis le lancement de l’initiative ‘‘Une stratégie de conservation pour les amphibiens de Madagascar’’ (ACSAM), qui constitue la contribution de Madagascar au programme mondial de conservation des amphibiens, afin de déterminer si les progrès ont été conformes aux attentes. Parmi les actions ciblées figurant dans le Plan d’Action Sahonagasy (SAP), 29 % ont été pleinement mises en œuvre, 33 % partiellement mises en œuvre, alors qu’il n’y avait pas de progrès évidents pour les 38 % restants. Nous estimons que 41 % des 1,4 million d’euros nécessaires au cours des quatre premières années ont été attribués. Les difficultés rencontrées au cours de cette période sont l’instabilité politique, le retrait des bailleurs de fonds en provenance de Madagascar et l’ajustement des actions de recherche avec les priorités de conservation, mais nous 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 cours pour 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 quatre dernières années, et les recherches en cours continuent à découvrir de nouvelles espèces.

Acknowledgements We are indebted with the Parc Botanique et Zoologique de Tsimbazaza, Université d’Antananarivo, Madagascar National Parks, and the Direction des Eaux et Forêts for permissions to work in Madagascar. Research, fieldwork and conservation measures were supported 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 la Conservation des Lémuriens, BIOPAT, Conservation International, Declining Deutsche Gesellschaft für Herpetologie und Terrarienkunde, Disney Wildlife Conservation Fund, European Association of Zoos and Aquaria, Gondwana Conservation and Research, IUCN Small Ecosystem Project Grant, Madagascar Fauna Group, Institut de Madagascar pour la Conservation des Ecosystèmes Tropicaux, Mohammed bin Zayed Species Conservation Fund, Museo Regionale di Scienze Naturali, Nando Peretti Foundation, the National Science Foundation, Van Thienhoven Foundation, World Association of Zoos and Aquariums, and Wildcare Institute. Among the many people with whom we repeatedly discussed about the effectiveness of amphibian conservation in Madagascar and whom we thank for their insights are 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. Angulo assisted during the preparation of a preliminary version of this paper.

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ALYTES 29 (1¢4)

Vieites, D. R., Wollenberg, K. C., Andreone, F., Köhler, J., Glaw, F. & Vences, M., 2009. ¢ Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. PNAS, 106: 8267¢8272. Weldon, C. & Du Preez, L., 2008. ¢ 4. Managing emerging amphibian diseases. Gestion des maladies émergentes des amphibiens. In: Andreone & Randriamahazo (2008): 34¢42. Corresponding editor: Ariadne Angulo.

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