Conservation status assessment of the amphibians and reptiles of Uruguay

The native species of amphibians and reptiles of Uruguay were categorized according to the IUCN Red List criteria. Out of 47 amphibian species, seven are listed as Critically Endangered (CR), five as Endangered (EN), one as Vulnerable (VU), three as Near Threatened (NT), and two as Data Deficient (DD); the remaining species are considered to be Least Concern (LC). Among the 64 species of reptiles evaluated, one is listed as Critically Endangered (CR), seven as Endangered (EN), two as Vulnerable (VU), one as Near Threatened (NT) and seven as Data Deficient (DD); the rest are considered to be Least Concern (LC). The use of these results as an additional criterion in the definition of protected areas in Uruguay will contribute towards the conservation of the aforementioned threatened species and their associated ecosystems.

The ultimate goal of conservation biology is to provide scientific concepts and data to design effective management strategies for the conservation of biodiversity.The design of a conservation system/ network must be based on sound knowledge of species' life histories, as well as an understanding of the functioning of ecosystems and the social component that interacts with natural environments (PRIMAK & RODRIGUES, 2001).Unfortunately, efforts and decisions regarding conservation are being taken based on a poor knowledge of the biology of species or the functioning of ecosystems, due to the asymmetries between the time required to generate such knowledge against the urgency of particular conservation actions (SOULÉ & ORIANS, 2001;MCCALLUM, 2007).
It was in this context that the IUCN (International Union for the Conservation of Nature) "Red List of Threatened Species" arose as a tool to help in the rapid assessment and monitoring of the conservation status of biodiversity using all available information (HILTON-TAYLOR, 2000).Based on this categorization method, 5,918 amphibians and 664 of the 8,240 known species of reptiles have been assessed on a global scale (IUCN, 2006b).As a result, 31 % of amphibian and 51 % of reptile species fell into one of the threat categories.In recent years (from 1996 until 2006), there has been a sustained increase in the number of species occupying each of the threat categories (IUCN, 2006a).
As in other regions of the world (see MILLER et al., 2007), evaluate the conservation status of amphibian and reptile species at a national level has been one of the main interests of Uruguayan herpetologists in the last years.That interest motivated the publication of several categorization schemes, such as those proposed by ACHAVAL & OLMOS (2007), MANEYRO & LANGONE (2001;amphibians), MORALES FAGUNDES & CARREIRA (2001;snakes), CARREIRA (2004;lizards), and CARREIRA et al. (2007, turtles) using the methodology of RECA et al. (1994), which has been widely applied in southern South America (GRIGERA & UBEDA, 2000).The process of elaboration of the Red Lists of Uruguay began with an initiative spearheaded by the Sociedad Zoológica del Uruguay.CANAVERO et al.With the participation of the IUCN Uruguayan Committee, two biodiversity groups were created to bring together the researchers working locally on each zoological group: Amphibia and Reptilia.Each of these working groups proposed initiatives to complete the categorization of both taxonomic groups at a regional (national) level using the IUCN criteria.Later, a Uruguayan Fauna Red List Workshop, sponsored by the IUCN Regional Office for South America (Quito, Ecuador), took place in November 2000 in Montevideo.A working agenda was set at this meeting, which resulted in the creation of the Red List of Amphibians and Reptiles of Uruguay following the categories and criteria suggested by IUCN (2003IUCN ( , 2006a)).
The aim of this work is to report the results of this assessment at national level.

MATERIAL AND METHODS
The categorization of amphibian and reptile species present in Uruguay followed the criteria established by the IUCN (2006a) and using the guidelines for the application of the IUCN Red List Categories and Criteria at regional levels (IUCN, 2003).Global categorizations for amphibians were taken from IUCN (2006b) and for reptiles from IUCN (2006a).Amphibians nomenclature and systematics followed FAIVOVICH et al. (2005), FROST et al. (2006), and GRANT et al. (2006).Common names for amphibians followed ACHAVAL & OLMOS (2007).The nomenclature and systematics of reptiles followed CARREIRA et al. (2005) with some modifications: the name for the genus Echinanthera Cope, 1894 is replaced by Taeniophallus Cope, 1895 (SCHARGEL et al., 2005) and Liophis miliaris semiaureus (Cope, 1862) is replaced by Liophis semiaureus (GIRAUDO et al., 2006).Common names for reptiles follow ACHAVAL & OLMOS (2007) and TIPTON (2005).
For all the species, all the IUCN criteria were analyzed.However, as a consequence of the type of available information for each taxon, the criteria applied in the support of the categories among amphibian species were those related to the geographic distribution (criterion B) quantified as the extent of occurrence (B1) or the area of occupancy (B2).Other important variables such as habitat fragmentation, continuous decline in the extent of presence (observed, inferred or projected), area, habitat extent and/or quality and number of localities or subpopulations, were also taken into account within these two sub-criteria (B1 and B2).In addition to criterion B, the reduction in population size (A) and restricted or very small population (D) criteria were also applicable in the reptile assessment (for more detailed description of the IUCN criteria, see IUCN, 2006a).
In the case of amphibians and the majority of reptile species, excluding sea turtles, we consider that all species have breeding populations and that Uruguayan populations may experience a negligible "rescue effect" from populations outside the country (BROWN & KODRIC-BROWN, 1977;HANSKI & GYLLENBERG, 1993).Thus, based on the conceptual scheme for assigning an IUCN Red List Category at the regional level (IUCN, 2003), and because it is unlikely that individuals from extra-regional populations would be able to survive and reproduce within the region, we suggest that, in these cases, the assigned regional category be left unchanged.Since sea turtles (Caretta caretta (Linnaeus, 1758), Chelonia mydas (Linnaeus, 1758), Lepidochelys olivacea (Eschscholtz, 1829), Dermochelys coriacea (Vandelli, 1761)) are considered as visitors, and the conditions outside and within the region are deteriorating (step 2e and 2f in IUCN, 2003), the assigned regional category should be left unchanged (IUCN, 2003).
We compared the percentages of each threat category for Uruguayan amphibians and reptiles at both global and regional (national) scales (sensu IUCN, 2006a) (Figs.1-4).

RESULTS AND DISCUSSION
Of the 47 native amphibian and 64 native reptile species evaluated, 23 species were classified in a threat category (CR, EN, VU), four were Near Threatened (NT) and nine were considered as Data Deficient (DD).So, a total of 75 species could be considered as Least Concern (LC), this represents 67.6 % of herpetofauna from Uruguay (Tabs.I, II).
The conservation status of the amphibians of Uruguay appears to be critical due to the relatively high proportion of Critically Endangered species (CR = 14.9 %), which is twice that of the global average (7.4 %) (STUART et al., 2004), and Endangered species (EN =10.6 %).On a different note, the low proportion of Data Deficient taxa (DD = 4.3 % vs. 24.1 % globally) reflects a relatively welldeveloped knowledge of the distribution of the Uruguayan amphibian fauna.
It is important to point out that 12.7 % of the Uruguayan amphibian species were recorded or described during the last six years (Scinax aromothyella Faivovich, 2005, Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920), Rhinella achavali (Maneyro, Arrieta & Sá , 2004); Physalaemus cuvieri (Fitzinger, 1826), Hypsiboas albopunctatus (Spix, 1824), Leptodactylus furnarius Sazima & Bokermann, 1978) (CANAVERO et al., 2001;KWET et al., 2002;MANEYRO et al., 2004;BORTEIRO et al., 2005;PRIGIONI et al., 2005;MANEYRO & BEHEREGARAY, 2007).The above mentioned species are known from very few localities, but their categorization was very different because of the unequal knowledge about their life history and local populations.For instance, we have good records on the life history of Hypsiboas albopunctatus, Leptodactylus furnarius, and Physalaemus cuvieri (see IUCN, 2006b), all of these species have southernmost distribution limits in the territory of Rivera in northern Uruguay.In Uruguay, they have been found in very well sampled localities, and thus their relative abundances could be estimated.For example, less than twelve specimens of P. cuvieri were recorded in a particular locality, although this locality was surveyed intensively during two years (Raúl Maneyro, pers. comm.).On the other hand, the abundance of L. furnarius recorded in a given locality in the course of one year was thirty times lower than that of a syntopic species Leptodactylus gracilis (Duméril & Bibron, 1841) (N L. furnarius = 11; N L. gracilis = 375), based on catalog information of the Vertebrate Collection of the Faculty of Sciences (Universidad de la República, Uruguay).These localities are situated in regions with forestry production and close to urban zones (ACHKAR et al., 2004).This fact allows us to categorize Hypsiboas albopunctatus, Leptodactylus furnarius, and Physalaemus cuvieri in the CR category.On the other hand, species such as Melanophryniscus pachyrhynus (with one record, BORTEIRO et al., 2005) and Scinax aromothyella (PRIGIONI et al., 2005;BORTEIRO et al., 2007;KOLENC et al., 2007), also recently recorded (as mentioned above), were categorized as DD because of the lack of knowledge of their life history traits and the absence of other local data.
In the present study, the regional categories of two nearly endemic species (Melanophryniscus montevidensis (Philippi, 1902) and M. orejasmirandai Prigioni & Langone, 1986) did not agree with the Global Amphibian Assessment (GAA) by IUCN (2006b) (Tab.I).This is a consequence of the newly acquired, highly detailed information on the distribution and natural history of these species provided by specialists working at the national level (KOLENC et al., 2003;KWET et al., 2005; Figures 1-4.The pie charts represent the percentages of amphibians and reptiles on each threat category evaluated at the global and local scale: 1, amphibians at the global scale; 2, amphibians of Uruguay; 3, reptiles at the global scale (until now, only 664 of the 8,420 species described have been evaluated); 4, reptiles of Uruguay (EX, extinct; CR, critically endangered; EN, endangered; VU, vulnerable; NT, near threatened; DD, data deficient; LC, least concern).The differences observed between the national and global analyses as they pertain to Uruguay might be due to two main causes.First, the geographical location of Uruguay is transitional between northern, subtropical and southern, cooler temperate biogeographical realms.Because the geographical distribution (and more specifically, the extent of presence) is a highly weighted variable in IUCN (2006a) categories, those species barely reaching Uruguay at their southernmost distributions (Hypsiboas albopunctatus, Leptodactylus chaquensis Cei, 1950, L. furnarius, L. podicipinus (Cope, 1862), Lysapsus limellus Cope, 1862, Physalaemus cuvieri, Leptophis ahaetulla marginatus (Cope, 1862)) can mistakenly be included in a threatened category.
Second, many of the localities occupied by species placed in a threat category are situated in regions with an established forest industry, rice and soybean fields or zones where urban growth and development have recently accelerated (ACHKAR et al., 2004).Examples of threatened amphibian species with distributions restricted to areas with forestry impact are: Rhinella achavali, Hypsiboas albopunctatus, Leptodactylus furnarius, Melanophryniscus devincenzii Klappenbach, 1968, M. orejasmirandai, M. pachyrhynus, M. sanmartini Klappenbach, 1968, Physalaemus cuvieri, and Scinax aromothyella.Species occurring in rice-crops zones are: Leptodactylus chaquensis, L. podicipinus, Lysapsus limellus, and Chthonerpeton indistinctum (Reinhardt & Lütken, 1862).In areas of accelerated urban development, we find Argenteohyla siemersi (Mertens, 1937), Ceratophrys ornata (Bell, 1843), Melanophryniscus montevidensis, Physalaemus fernandezae (Müller, 1926), and Pleurodema bibroni Tschudi, 1838.This situation also holds for reptiles because several species in the threat categories are observed in areas with similar anthropogenic development (i.e.Calamodontophis paucidens, Taeniophallus poecilopogon (Cope, 1864)).The single rattlesnake species present in Uruguay (Crotalus durissus terrificus (Laurenti, 1768)) constitutes an example of a species that, like those mentioned above, shows no apparent conservation threats at a global level, while at the national scale its distribution has been notoriously reduced, presently restricted to a few localities in the north of the country (CARREIRA et al., 2005).Habitat destruction and fragmentation are repeatedly invoked factors in species categorization, whereas information regarding population sizes and dynamics is very scarce, except for the sea turtles and Caiman latirostris (BORTEIRO et al., 2006).Sea turtles comprise a particular case because they do not reproduce in Uruguayan beaches, although the Uruguayan maritime space is an important feeding area for the sea turtle populations of the southern Atlantic (LÓPEZ-MENDILAHARSU et al., 2006).
Another threat for biodiversity that has been detected in the last years in Uruguay, but that perhaps could have an impact comparable to habitat loss and environmental contamination, is the introduction of alien species and diseases (ALFORD & RICHARDS, 1999).MAZZONI et al. (2003) reported the presence of an infectious disease parasite, the fungus Batrachochytrium dendrobatidis, in a North American bullfrog farm near Montevideo.Later, LAUFER et al. (2008) reported the presence of the North American bullfrog (Lithobates catesbeianus) in the wild; such an occurrence has been found to have negative effects on native amphibian species via competition and predation (ADAMS, 2000;BLAUSTEIN & KIESECKER, 2002;BOONE et al., 2004).Both invasions pose a risk to the native amphibian species because L. catesbeianus can act as a vector and a reservoir (HANSELMANN et al., 2004) for pathogenic microorganisms, especially Batrachochytrium dendrobatidis, which is responsible for chytridiomycosis, an emerging infectious disease associated to global amphibian declines (PECHMANN & WILBUR, 1994;LONGCORE et al., 1999;LIPS et al., 2001;YOUNG et al., 2001;COLLINS & STORFER, 2003;DASZAK et al., 2003;SEMLITSCH, 2003;STUART et al., 2004).The occurrence of both the invading species and the parasite in the Uruguayan national territory is almost unknown, but given the serious risk that both species represent (the fungus and the bullfrog), we call for an immediate response from the scientific community and the local authorities.
It is important to consider that several species of reptiles and amphibians have been recently recorded for Uruguay, and because of that, updated information on the distribution and natural history of these species is scarce and fragmented.The species recently added to the Uruguayan fauna are Rhinella achavali (MANEYRO et al., 2004), Melanophryniscus pachyrhynus (BORTEIRO et al., 2005), Physalaemus cuvieri (MANEYRO & BEHEREGARAY, 2007), Scinax aromothyella (PRIGIONI et al., 2005), Atractus reticulatus (Boulenger, 1885) (CARREIRA et al., 2004) and Waglerophis merremi (Wagler, 1824) (CARREIRA et al., 2005).We believe it is important to set as priority goals for the near future the gathering of information for evaluating the species that are currently in the Data Deficient category (DD) as well as encouraging those actions that will promote the protection of the species included in threat categories.In particular, IUCN Red List categories are useful to define priority areas for conservation, and for that reason, the existence of Data Deficient taxa raises questions that are difficult to answer in order to provide timely and informed actions towards biodiversity protection.
Finally, taking in mind the information stated above, we are allowed to recommend that the "in situ" conservation strategies seem to be the most appropriate for the Uruguayan herpetofauna.The most relevant factor related to herpetofauna conservation in Uruguay is the habitat destruction and fragmentation (as a consequence of urbanization and agrarial macroindustriesafforestation, soybean and rice crops).So, the results of the present article (and its continuous update) should be taken in account both in the definition of conservation units (e.g.National System of Protected Areas and other initiatives) and in the enrironmental management of the areas destinated to agro-sylvo production.

Table I .
Amphibians of Uruguay with global and national threat categorizations for each species.Species are grouped by taxonomic families and the scientific and common names are provided.For a detailed description of the IUCN codes that define criteria, seeIUCN  (2006a).

Table II .
Reptiles of Uruguay with global and national threat categorizations for each species.Species are grouped by taxonomic families and the scientific and common names are provided.For a detailed description of the IUCN codes that define criteria, seeIUCN (2006a).