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Conservation of Brazilian Amphibians

DEBORA L. SILVANO AND MAGNO V. SEGALLA


Secretaria de Biodiversidade e Florestas, Ministrio do Meio Ambiente, Bras 70068-900, DF, Brasil, e lia email deborasilvano@uol.com.br Instituto H rus de Desenvolvimento e Conservao Ambiental, Rua Dr. Manoel Pedro 495/906, Curitiba 80035-030, Paran, Brasil o ca a

Abstract: Brazil is the world leader in amphibian diversity, with 765 species, most of which have been described in the last 40 years. The Brazilian Official List of Threatened Species and the results of a workshop for the Global Amphibian Assessment indicate that 26 species are threatened. The majority of these occur in the Atlantic Forest, one of the worlds biodiversity hotspots. The main threat to amphibians is the destruction of their habitats through deforestation, conversion into agricultural land, mining, wildfires, and infrastructure development and urbanization. In Brazil little is known about other causes of amphibian decline observed worldwide, such as pesticides, infectious diseases, climate change, invasive species, or wildlife trade. Brazilian conservation policies include such important legal instruments as the Official List of Threatened Species and the selection of priority areas for conservation measures in all of Brazils major biomes. Although there is little information on geographic distributions and the natural history and ecology of the large majority of the currently recognized species, a number of important regional studies for amphibian conservation are under way. New species are discovered each year.
Conservaci n de Anfibios Brasile os o n

Resumen: Brasil es el lder mundial en diversidad de anfibios, con 765 especies, la mayora de las cuales
han sido descritas en los ultimos 40 a os. La Lista Brasile a Oficial de Especies Amenazadas y los resultados n n de un taller para la Evaluaci n Global de Anfibios indican que 26 especies est n amenazadas, la mayora de o a ellas ocurre en el Bosque Atl ntico, uno de los sitios de importancia para la biodiversidad global. La principal a amenaza a los anfibios es la destrucci n de sus h bitats por la deforestaci n, conversi n a tierras agrcolas, o a o o minera, fuego no controlado, desarrollo de infraestructura y urbanizaci n. En Brasil se conoce poco sobre otras o causas de la declinaci n de anfibios observadas en todo el mundo, como pesticidas, enfermedades infecciosas, o cambio clim tico, especies invasoras o comercio de vida silvestre. Las polticas Brasile as de conservaci n a n o incluyen importantes instrumentos legales como la Lista Oficial de Especies Amenazadas y la selecci n de o areas prioritarias para la conservaci n en todos lo biomas principales de Brasil. Existe escasa informaci n o o sobre la distribuci n geogr fica y la historia natural y ecologa de la gran mayora de las especies reconocidas o a actualmente, aunque se est desarrollando un importante n mero de estudios regionales para la conservaci n a u o de anfibios. Cada a o se descubren nuevas especies. n

Species Diversity
From the 1960s to the present, 313 species of Brazilian amphibians were described, doubling the number described in the previous 200 years. Ninety-seven species have been described in the last 10 years. (This includes only species with Brazilian type localities, not those de-

scribed from specimens obtained in other countries but occurring in Brazil.) The Earth Summit Rio-92 inspired intensive worldwide efforts to compile information on biological diversity (Lewinsohn & Prado 2002). The Global Biodiversity report of the World Conservation Monitoring Center (Groombridge 1992) indicated that Brazil is home to

Paper submitted November 19, 2004; revised manuscript accepted December 29, 2004.

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502 species of amphibians. Lewinsohn and Prado (2002) counted about 600, but 731 species were listed and their status assessed at the World Conservation Unions (IUCN) Global Amphibian Assessment (GAA) held in 2003 (IUCN et al. 2004). Unsatisfied, the Brazilian Herpetological Society (SBH) attempted to compile a more comprehensive list of Brazilian amphibian species in 2004. The result placed Brazil at the top of the worlds amphibian diversity charts: 765 species in three orders, 13 families, and 98 genera (SBH 2004). Brazils list includes 737 anurans, 27 caecilians, and a single salamander. By comparison, Colombia has registered 698 species of amphibians and Ecuador has 447 (IUCN et al. 2004). The total number of species known for the New World is 3,046, of 5,743 amphibians worldwide. Nevertheless, Brazils amphibians, especially the caecilians and salamanders, are poorly known. Little information exists on their geographic distributions, natural history, life histories, or ecology. Enormous areas of Brazil have yet to be inventoried, and there are many localities where surveys have been insufficient. Many of the sites known for their particular richness have been studied for many years and coincide with protected areas or are otherwise easily accessed for periodic inventories. Additionally, numerous surveys and collections remain unpublished or in the gray literature. The paradox is that the opportunities and academic incentives for publishing species listswhether simple or annotatedare limited, even though they are vital to understanding Brazils biodiversity and the biogeography of the group, and to appreciating the appropriate strategies for their conservation (Haddad 1998). Taxonomic collections are evidently an important tool (Shaffer et al. 1998), but information on abundance is rare. It is therefore difficult to reconstruct the history that is vital to understanding current trends and declines. In addition, large numbers of unidentified specimens reside in museums and collections. All of these aspects frustrate attempts to obtain a comprehensive understanding of the composition, geography, and demographics of Brazils amphibian fauna, which are so necessary for its conservation.

Threatened Species
The first Brazilian threatened species list to include amphibians appeared in 1989. It registered a single species, Paratelmatobius gaigeae, with another eight recorded in an appendix of data deficient but possibly threatened (Bernardes et al. 1990). Hyla izecksohni, now categorized as critically endangered, and Phrynomedusa fimbriata, currently considered extinct according to the IUCN (2001) criteria and categories, were included. The most recent revision of the Official List of Species Threatened with Extinction was written in 2002 (IBAMA

2003). It listed 15 amphibians as threatened and 1 as extinct, all from the Atlantic Forest (Table 1). Ninety more were categorized as data deficient. Eight species were listed as critically endangered, 7 of which (Phyllomedusa ayeaye, Hyla cymbalum, Hyla izecksohni, Scynax alcatraz, Holoaden bradei, Paratelmatobius lutzi, and Odontophrynus moratoi) are known only from single sites in the states of Rio de Janeiro, So Paulo, and Minas a Gerais in the southeast. One (Melanophryniscus macrogranulosus) is known only from its type locality in the far south of Brazil. Four species were ranked as endangered: Adelophryne maranguapensis is restricted to the Serra de Maranguape in Cear; Physalaemus soaresi is rea stricted to the Horto Florestal de Santa Cruz, Itagua Rio , de Janeiro; Hylomantis granulosa occurs in a number of northeastern localities; and Thoropa petropolitana oc a curs in the Serra dos Orgos, Rio de Janeiro. The three vulnerable species were Adelophryne baturitensis, which is restricted to Serra de Baturit, Cear; Thoropa lutzi, e a which occurs in Rio de Janeiro, Esp rito Santo, and Minas Gerais; and Melanophryniscus dorsalis, which is found along the coast in Santa Catarina and Rio Grande do Sul. Phrynomedusa fimbriata, evidently extinct, was known only from Paranapiacaba, So Paulo, but has not been seen a for more than 80 years. Most of the species listed have restricted or highly fragmented rangesthey suffer from loss of habitat or have been extremely difficult to find. Until the 1980s, conservation efforts were largely restricted to the actions of the federal government. In the last two decades, the states themselves have become increasingly active in this sense, and a number have taken the initiative of drawing up their own threatened species lists, explicitly to support the setting of conservation priorities. The first state list of threatened amphibians was drawn up by the secretary of the environment of the state of Paran in 1995 (SEMA 1995), followed in the same year a by Minas Gerais (Machado et al. 1998) and later by So a Paulo (SEMA 1998), Rio de Janeiro (Bergallo et al. 2000a), and Rio Grande do Sul (Marques et al. 2002; Garcia & Vinciprova 2003). The state of Paran reviewed its 1995 a list in 2004 (Segalla & Langone 2004). In all, 34 amphibians have been categorized as threatened as a result of these state assessments. Forty-seven more were classified as near threatened or data deficient. In 2003 the IUCN, the Center for Applied Biodiversity Science at Conservation International, Conservation International of Brazil, and several other institutions organized a workshop specifically to map the geographic ranges and examine the status of the Brazilian amphibians (part of the GAA, a worldwide effort to assess all amphibian species against IUCNs [2001] Red List criteria [IUCN et al. 2004]; Table 1). National and international experts assessed 731 species. Six were considered critically endangered, 6 endangered, 12 vulnerable, 1 extinct, 21 near threatened, and 205 data deficient. They are listed as such on the IUCNs 2004 Red List (IUCN 2004).

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Table 1. Threatened Brazilian amphibians on the List of Brazilian Fauna Threatened with Extinction and according to the Global Amphibian Assessment (GAA). Species Bufonidae Atelopus spumarius Dendrophryniscus carvalhoi Melanophryniscus dorsalis Melanophryniscus macrogranulosus Melanophryniscus montevidensis Dendrobatidae Colostethus olfersioides Hylidae Hemiphractus johnsoni Hyla cymbalum Hyla izecksohni Hylomantis granulose Phrynomedusa fimbriata Phyllomedusa ayeaye Scinax alcatraz Leptodactylidae Adelophryne baturitensis Adelophryne maranguapensis Euparkerella robusta Euparkerella tridactyla Holoaden bradei Odontophrynus moratoi Paratelmatobius lutzii Physalaemus atlanticus Physalaemus soaresi Thoropa lutzi Thoropa petropolitana Microhylidae Chiasmocleis carvalhoi Dasypops schirchi Oreophrynella quelchii Brazilian official list 2002 GAA 2003 VU EN VU VU VU VU EN CR CR LC EX CR CR VU EN VU VU CR CR DD VU EN EN VU EN VU VU States Roraima, Amazonas, Amap, Par a a Esp rito Santo Rio Grande do Sul, Santa Catarina Rio Grande do Sul Rio Grande do Sul Alagoas, Bahia, Esp rito Santo, Minas Gerais, Rio de Janeiro, Sergipe Acre So Paulo a So Paulo a Pernambuco So Paulo a Minas Gerais So Paulo a Cear a Cear a Esp rito Santo Esp rito Santo Minas Gerais, Rio de Janeiro So Paulo a Minas Gerais So Paulo a Rio de Janeiro Esp rito Santo, Minas Gerais, Rio de Janeiro Esp rito Santo, Rio de Janeiro Bahia, Rio de Janeiro, So Paulo a Bahia, Esp rito Santo Roraima

VU VU DD

CR CR CR EX CR CR VU VU CR CR CR EN VU EN

Abbreviations: CR, critically endangered; EN, endangered; VU, vulnerable; EX, extinct; DD, data deficient; LC, least concern. Categories defined in IUCN (2001).

Combining the two assessmentsBrazils official list and that of the GAAwe arrive at a total of 26 threatened species and 1 extinct species in 16 Brazilian states (Table 1). Of those threatened, 23 occur in the Atlantic Forest and three in Amazonia. A recent analysis of the threatened amphibians throughout South America shows that although all countries have threatened species, they are concentrated in two distinct areas: the Cordilheira dos Andes, between Col mbia and Ecuador, and the central o region of the Atlantic Forest, between the states of Rio de Janeiro and So Paulo (Young et al. 2004). a A notable aspect of the threatened species lists is the large number of species considered data deficientthe Brazilian list contains 90 and IUCNs 2004 Red List has 189. The number of species in this category indicates directions and subjects for future studies. Two-thirds of the species on IUCNs list of data-deficient species have been described in the last 10 years. Information must be obtained as soon as possible on the status of these species to avoid their listing as threatened entirely, or largely, be-

cause of the lack of timely or appropriate measures for their protection.

Principal Threats
Reports of declines in amphibian populations began to appear from different parts of the world in the second half of the 1980s. The main cause is undoubtedly habitat destruction, but the prevalence of pathological chytrid fungi is also a significant cause (Young et al. 2004). Additionally factors (such as water pollution and contamination from agrotoxic chemicals, climate change, invasive species, ultraviolet radiation, and illegal wildlife trade) act alone or synergistically (Young et al. 2001, 2004). The results of the GAA show that, as a group, amphibians are considerably more threatened than either birds or mammals (Stuart et al. 2004). Relatively few publications address amphibian population declines in Brazil (Heyer et al. 1988; Weygoldt 1989;

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Bertoluci & Heyer 1995; Guix et al. 1998; Pombal & Haddad 1999; Izecksohn & Carvalho-e-Silva 2001; Eterovick et al. 2005), although there are many anecdotal and informal reports of abundant species becoming scarce. Population declines in Brazil are poorly documented and understood because of a lack of knowledge of the species biology, little or no long-term monitoring, and, not least, the enormous size of Brazil and the complexity and diversity of its amphibian species and their habitats. Most reports of declines come from the Atlantic Forest, one of the worlds biodiversity hotspots (Myers et al. 2000). The Atlantic Forest reports include high-elevation populations in the Serra do Mar in So Paulo (Heyer et a al. 1988; Bertoluci & Heyer 1995; Young et al. 2004); in Santa Teresa, Esp rito Santo ( Weygoldt 1989); in Tijuca and Teres polis in Rio de Janeiro (Heyer et al. 1988; Weyo goldt 1989; Izecksohn & Carvalho-e-Silva 2001; Young et al. 2004); in the Itatiaia National Park in the Serra da Mantiqueira (Heyer et al. 1988; Guix et al. 1998; Pombal & Haddad 1999); and in montane Atlantic Forest in Paran (Young et al. 2004; Eterovick et al. 2005) and Cear a a (Eterovick et al. 2005). Fire seems to have caused declines in Linhares, Esp rito Santo (Papp & Papp 2000). Eterovick et al. (2005) have offered the first reports of declines for two species in areas of high elevation in the Cerrado in the Serra do Cip , Minas Gerais. In all, there are reports of o declines and disappearances for 30 species in the Atlantic Forest. This is, however, an incomplete and preliminary assessment, and there are no doubts that a major increase in monitoring and research efforts is needed to obtain a more realistic understanding of the scope and seriousness of the situation. In Brazil habitat loss is the most visible and probably the main threat to amphibians. Deforestation, the advance of the agricultural frontier, mining, wildfires, and development projects (e.g., dams, highways, industry, housing) are the main causes of habitat loss. Although varying in extent, all Brazilian biomes are now severely affected, especially the Atlantic Forest, where fragmented forest remnants constitute the 8% that remains (SOS Mata Atlntica a 2002). The Cerrado (bush savanna of Central Brazil) is also a hotspot, and amphibian habitats have been widely destroyed throughout (Myers et al. 2000; Sala et al. 2000). Little is known of its amphibian fauna (Colli et al. 2002; Diniz-Filho et al. 2004). Recent estimates indicate that only 34% of the original vegetation remains and that it will disappear completely over the next 30 years under present development regimes. Habitat losses here are primarily a result of traditional crops giving way to enormous mechanized plantations of soybean, cotton, corn, millet, sorghum, and sunflowers (Machado et al. 2004). Approximately 88% of the Amazonian forests remain (WWF-Brasil 2004), although annual deforestation is as high as 20,000 km2 , and enormous areas are becoming

increasingly vulnerable to wildfires (Fearnside 2005). As in the other biomes, little information is available on the status of the amphibians occurring there (Azevedo-Ramos & Galatti 2002). The chytrid fungus (Batrachochytrium dendrobatidis) is an important cause of amphibian declines (Young et al. 2004). Although it has yet to be documented in Brazil, it has been recorded in other South American countries (Ron & Merino 2000; Bonaccorso et al. 2003; Mazzoni et al. 2003; Hanselmann et al. 2004). The fungus affects mainly species associated with streams at mid to high elevations (Berger et al. 1998; Longcore et al. 1999). Most of the amphibian declines recorded in Brazil have been of high-elevation species, but there have been no efforts to locate the fungus as a possible cause. Likewise, little or nothing is known about the effects of pesticides or other agrotoxic chemicals, climate change, invasive species, or the extent or seriousness of wildlife trade in amphibians. Throughout the country, pesticide use is largely indiscriminate and uncontrolled; climate change effects have been identified in some regions; and although little has been published, there are records of alien invasive species (e.g., Rana catesbeiana) in the south and southeast, which may be affecting native amphibian populations (Guix 1990; Borges-Martins et al. 2002). Additionally, although known to occur, there is no quantitative data on trade in Brazilian amphibians.

Conservation and Research Initiatives


Species declines and extinctions in South America occur because many of the countries in the region lack adequate and effective conservation policies (Junc 2001). a The rapid declines of numerous amphibians underscore the need for a rapid expansion of research programs and emergency strategies for their conservation, especially in regions where little information is available on their diversity, distribution, and abundance, as in Brazil (Young et al. 2001). Because of this, Brazils 1989 threatened species listalthough including only one amphibian species served to draw attention to the large number believed to be in trouble but for which there was too little information (IBAMA 1989; Bernardes et al. 1990). The 2002 revision resulted in 15 amphibians being listed as threatened nationwide (IBAMA 2003). The threatened species list is having considerable impact in Brazil, providing as it does the backbone for all environmental legislation that touches on biodiversity conservation. A number of states also have taken the initiative of drawing up official threatened species lists, generating publications that provide valuable syntheses and incentives for research and conservation measures (Rylands 1998; Bergallo et al. 2000a, 2000b). Garcia and Vinciprova (2003), for example, reviewed amphibian

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diversity and presented information on the threats to and distribution and status of 10 amphibians considered vulnerable in the state of Rio Grande do Sul. The Brazilian government held five major workshops from 1998 to 2000. These workshops defined priority areas for biodiversity conservation and conservation measures in five major biomes as part of the Project for the Conservation and Sustainable Use of Brazilian Biological Diversity (MMA 2002). In all, 180 priority areas were identified for amphibian and reptiles combined, most (101) in the Atlantic Forest and southern grasslands. Forty-six priority areas were identified in Amazonia, 19 in the Caatinga, and 14 in the Pantanal and Cerrado. Azevedo-Ramos and Galatti (2002) review our current understanding of amphibian diversity in the Brazilian Amazon and indicate the need for protected areas in a number of regions so as to take in diverse habitats along north-south and east-west axes as a means of maximizing the numbers of species covered in areas where species turnover is high even over short distances. In Amazonia, patterns of endemism and the occurrence of threatened species do not stand alone as the best indicators for locating protected areas for amphibians. When determining priority areas for inventories and the location of new protected areas for amphibians, patterns of development; the degradation, destruction, and conversion of habitats; and the existence of already established protected areas must also be considered. Following a macroscale biogeographical analysis, DinizFilho et al. (2004) recently proposed a regional system of areas potentially important for the conservation of anuran amphibians in the Cerrado. They identified 10 regions in Central Brazil where conservation efforts and inventories should be concentrated. The rates of deforestation and the advance of the agricultural frontier in the Amazon and the Cerrado underscore the need for urgent action for the conservation of numerous restricted-range and endemic species. Based on the results of the GAA (summarized in Stuart et al. 2004), Young et al. (2004) suggest a number of measures for amphibian conservation in South America. They stress the importance of strict habitat protection but also make recommendations on needed public policies, captive breeding, environmental education, research on infectious diseases, and surveys. They also suggest new research approaches for the species-by-species identification of key problems that are causing amphibian decline.

Literature Cited
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Acknowledgments
We thank A. B. Rylands for his comments, revisions, and the version in English, and D. Church for his critical review.

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Conservation Biology Volume 19, No. 3, June 2005