The amphibians of the state of Rio de Janeiro , Brazil : an updated and commented list

The amphibian fauna of the state of Rio de Janeiro, in southeatern Brazil, is characterized by high species richness and rates of endemism, and is still insufficiently known. A first list of amphibian species with occurrence in the state was published in 2004 and reported 166 taxa, but since then many new records, descriptions of new taxa, and revalidations and synonymizations of species have consistently improved the knowledge about the state’s amphibian biodiversity. Thus, a re‐ view and update of that list was deemed necessary. We herein present an updated and commented list of amphibian species occurring in the state of Rio de Janeiro based on a survey of the literature. We recorded the occurrence of a total of 201 species of amphibians (197 anurans and four caecilians) in Rio de Janeiro, with 54 of them (ca. 27%) considered to be endemic of the state. Our study presents an increase in species richness of 21% since the publication of the previous list, indicating a consistent advance in knowledge of the composition of the amphibian fauna in the state. In spite of its relatively small territorial exten‐ sion (total area ca. 43,800 km2), the state of Rio de Janeiro contains nearly 20% of the amphibian species known to occur in Brazil and around 40% of those occurring in the Atlantic Forest biome. Thus, that state constitutes an important reservoir of amphibian biodiversity in the Atlantic Forest biome and in Brazil, as a whole. Key-Words. Anura; Atlantic Forest; Conservation; Gymnophiona; Species list.


INTRODUCTION
The Brazilian Atlantic Forest is one of the world's most threatened biomes, with only ca.12% of its original forest cover remaining nowadays (Ribeiro et al., 2009), and is considered one of the world's 35 biodiversity hotspots (Mittermeier, 2005).The state of Rio de Janeiro, with around 43,800 km² of total area and situated between 20-24°S and 45-41°W, is the Brazilian state that preserves the greatest proportional percentage (20.3% of its territory) of Atlantic Forest remnants (Bergallo et al., 2009).A combination of the state's geographic location with its heterogeneous landscape (ranging from sea-level to mountain peaks over 2,000 m high) favors the occurrence of multiple phytophysiognomies (mangroves, restingas, umbrophilous forests, semi-deciduous forests, high-altitude fields, and inselbergs).This, in turn, maintains high rates of biodiversity and endemism for different groups of the fauna and flora (Jenkins & Pimm, 2006;Nascimento & Campos, 2011).
Within the last twelve years or so there has been a considerable increase in studies with molecular phylogenetics of amphibians, resulting in extensive nomenclatural changes at the familial, subfamilial and generic levels (e.g., Faivovich et al., 2005;Frost et al., 2006;Grant et al., 2006;Hedges et al., 2008;Guayasamin et al., 2009;Wilkinson et al., 2011;Padial et al., 2014;Castroviejo-Fisher et al., 2015).Considering such changes, together with the aforementioned increase in the amount of information regarding the amphibian fauna of Rio de Janeiro after more than a decade since the list of Rocha et al. (2004) came out, we think that list needs to be reevaluated and updated.Thus, we here present a revised and updated list of the amphibian species reported to occur in the state of Rio de Janeiro.

MATERIALS AND METHODS
The current knowledge about the composition and species richness of amphibians occurring in the state of Rio de Janeiro, in southeast Brazil, was evaluated based on a survey of the literature.Extensive searches were carried out on the websites Web of Science of the Institute for Scientific Information (http://apps.isiknowledge.com) and Google Scholar (http://scholar.google.com.br) using the following combinations of key words: "Anura* and Rio de Janeiro", "amphibia* and Rio de Janeiro", "herpeto* and Rio de Janeiro", "new and anura and Rio de Janeiro".Additionally, databases of the sites Amphibian Species of the World (http://research.amnh.org/vz/herpetology/amphibia) and IUCN (International Union for Conservation of Nature: www.iucnredlist.org),as well as issues of the journal Herpetological Review were also mined for records.All the above sources were searched between June 2014 and December 2015, and searches were directed towards works published from 2004 onwards.We avoided including undescribed species or taxa of uncertain taxonomic status (i.e., treated in the literature as "sp.", "aff." or "cf.") in our list, except in a few particular cases (see Results and Discussion).Scientific nomenclature used throughout the present work follows Frost (2017), unless stated otherwise (see below).Duellman et al. (2016) recently reviewed the systematics of the speciose family Hylidae and proposed a number of taxonomic changes.These include the elevation of the three recognized hylid subfamilies to family level, adoption of the unranked name Arboranae for the clade formerly known as Hylidae, new subfamilial arrangements, and partitioning of some genera (including Phyllomedusa and Scinax).As those proposed changes are still too recent and are potentially controversial (due to the splitting of monophyletic taxa; see Vences et al., 2013), we prefer not to adopt them here, since we are not sure if they will be widely accepted.
Concerning their conservation status (sensu IUCN), the species under some level of threat were classified as data deficient (DD), near threatened (NT), endangered (EN), vulnerable (VU), critically endangered (CR), or extinct (EX).Classification of species in these categories at both the global and national levels followed IUCN (2016) and the Official National List of Species of the Fauna Threatened with Extinction (issued in 2014 by the Brazilian Ministry of Environment -MMA), respectively.

RESULTS AND DISCUSSION
Based on our literature survey and on the previous list of Rocha et al. (2004), we compiled a list of 201 species of amphibians (197 belonging to the Order Anura and four to the Order Gymnophiona) reported to occur in the state of Rio de Janeiro, of which 54 (26.9%) are considered endemic to the state (Table 1).A total of 40 species were added to the amphibian list of Rocha et al. (2004), whereas five (Allobates carioca, Bokermannohyla clepsydra, Cycloramphus lutzorum, Ischnocnema gr.lactea, and I. nigriventris; see below) were removed from the list based on our revision.The present updated list thus represents an increase of 21% in the number of species reported for the state of Rio de Janeiro after thriteen years.This evidences a consistent improvement in knowledge of the composition and richness of the amphibian fauna of the state, driven by an increase in local faunal inventories and in systematic studies during the last decade.The description of 26 new amphibian species known to occur in the state of Rio de Janeiro within the 2004-2015 period, as well as the discovery of species that still remain to be formally described (e.g., Siqueira et al., 2011a, b;Bittencourt-Silva & Silva, 2013) reinforce the notion that many amphibian species inhabiting the Atlantic Forest remain unknown (Pimm et al., 2010).
Most of the new records added herein to the previous list of Rocha et al. (2004) represent descriptions of new species or revalidations of taxa previously in synonymy, as well as new occurrence records for the state.However, two of the new additions to the list represent "old" (pre-2004) records that have been apparently overlooked by Rocha et al. (2004): Scinax angrensis (as noted by Carvalho-e-Silva et al., 2008), a species that is actually endemic to the state, and Brachycephalus hermogenesi, whose occurrence in the municipality of Paraty had been reported in the original description (Giaretta & Sawaya, 1998).
Scinax x-signatus (Spix, 1824) is a problematic taxon, as its imprecise type locality, succinct description by Spix (1824) and presumably lost holotype preclude this name from being confidently applied to any existing population of treefrogs at present (Pombal et al., 1995;Sturaro & Peloso, 2014).Scinax x-signatus was not included by Rocha et al. (2004) in their list of the state's amphibians, despite Izecksohn & Carvalho-e-Silva (2001) having included this taxon among the amphibian species occurring in the municipality of Rio de Janeiro.Additionally, several recent studies have reported frogs identified as Scinax x-signatus, Scinax aff.x-signatus, or Scinax cf.x-signatus from various localities throughout the state (e.g., Abrunhosa et al., 2006;Silva et al., 2008;Salles et al., 2009; Table 1.List of species of amphibians reported from the state of Rio de Janeiro, southeastern Brazil.Species considered endemic to the state are marked with an 'X' .Categories of threat are given at both global and national levels, as follows: data deficient (DD), near threatened (NT), endangered (EN), vulnerable (VU), critically endangered (CR) and extinct (EX).(*) species added to the list of Rocha et al. (2004); (**) species present on the list of Rocha et al. (2004) that had since undergone nomenclatural change or re-identification.
Like the case mentioned above, we found other instances in which species not listed by Rocha et al. (2004) have been reported or suggested to occur in Rio de Janeiro by other authors.We investigated these potential new records and found that none of them were reliable.One of them concerns Boana bischoffi (Boulenger, 1887), whose range is given by Frost (2017) as "from Rio de Janeiro to Rio Grande do Sul", without citing sources.Nevertheless, according to Marcelino et al. (2009), who analyzed morphological variation of B. bischoffi across its geographic distribution range, this species does not extend northwards beyond the northern coast of São Paulo state.Thus, we opted for keeping this taxon off the list due to lack of solid evidence of its occurrence in the state of Rio de Janeiro.
There is also the case of Phyllomedusa megacephala (Miranda- Ribeiro, 1926), a species whose occurrence in Rio de Janeiro has been considered probable (Brandão, 2002).It was described (as Bradymedusa megacephala) based on a single specimen of uncertain provenance [given as "Rio de Janeiro?" by Miranda- Ribeiro (1926)].After comparing the holotype of P. megacephala with other specimens collected more recently, Caramaschi (2006) concluded that the type did not come from Rio de Janeiro and that the species occurs only in the Espinhaço mountain range in the state of Minas Gerais.Therefore, we do not include this taxon on the list.
Finally, Adenomera bokermanni (Heyer, 1973) was reported by Almeida-Gomes et al. (2014) from the municipality of Cachoeiras de Macacu.However, according to Fouquet et al., (2014) 'true' A. bokermanni has a relatively restricted distribution limited to coastal forests in the states of Paraná and northern Santa Catarina, in southern Brazil.They mention that many individuals of Adenomera from other localities that have been previously attributed to A. bokermanni (including most of the original type series) are in fact referable to the recently described A. thomei.This latter species, originally described from a lowland site in the state of Espírito Santo (Almeida & Angulo, 2006), was found by Fouquet et al. (2014) to have a relatively broad distribution, encompassing much of the states of Espírito Santo and Rio de Janeiro, as well as southeast São Paulo and southern Minas Gerais.The occurrence of A. thomei in the state of Rio de Janeiro has also been reported by Martins et al. (2014), who recorded the species in the municipality of Saquarema.Thus, we believe that the species reported by Almeida-Gomes et al. (2014) was in fact A. thomei and thus we do not add A. bokermanni to the list.
Our addition or removal of some species from the previous list of Rocha et al. (2004) result from taxonomic revisions (synonymizations/revalidations), re-evaluations of their occurrence records, or nomenclatural changes to the species' epithets that have been published since 2004.We list and comment those cases below.
The species listed as "Eleutherodactylus gr.lacteus (Miranda- Ribeiro, 1923)" by Rocha et al. (2004) is probably meant to be Ischnocnema lactea.This species is prob-lematic, however, and needs to be reviewed in order to define its actual status and geographic distribution (T.Silva-Soares, pers. comm.).As I. lactea was described from a site in the state of São Paulo and attribution of this name to other populations at present is considered problematic, we exclude this species from the list pending resolution of its taxonomic status.
Ischnocnema nigriventris (Lutz, 1925) was originally described based on specimens from "Serra de Cubatão" (state of São Paulo) and "Itatiaia" (state of Rio de Janeiro) (Lutz, 1925).Presumably based on the latter record, the species was included in the list of Rocha et al. (2004).Since then, Berneck et al. (2013) have reviewed the species based on the existing syntypes and on newly collected material, concluding that I. nigriventris occurs only in the state of São Paulo.Berneck et al. (2013) argue that the record from Itatiaia was based on a specimen that is presently lost, and apparently not conspecific with the remaining syntypes (as previously suggested by Heyer, 1985).Thus, we herein remove this species from the list of amphibians occurring in the state of Rio de Janeiro.Baldissera et al. (2004) reviewed the Bufo crucifer (now Rhinella crucifer) group and resurrected Bufo ornatus Spix, 1824 (now Rhinella ornata).According to that work, all records of R. crucifer from the state of Rio de Janeiro should be attributed to R. ornata.However, R. crucifer (sensu Baldissera et al., 2004) was subsequently reported from different localities in Rio de Janeiro (Marques et al., 2006;Silveira et al., 2009;Almeida-Gomes et al., 2010), confirming the presence of both species in the state.Additionally, Silveira et al. (2009) presented the first records of another member of the R. crucifer complex, R. pombali (Baldissera, Caramaschi & Haddad, 2004), for the state of Rio de Janeiro.However, recent molecular studies have found no support for the validity of R. pombali (Thomé et al., 2010(Thomé et al., , 2012)), and it was concluded that this taxon was based on R. crucifer × R. ornata hybrids (Thomé et al., 2012).As R. pombali is currently an invalid taxon, it is not included herein in the list.

Family Bufonidae
The species listed in Rocha et al. (2004) as "Bufo gr.margaritifer Laurenti, 1768" is, most probably, Rhinella hoogmoedi Caramaschi & Pombal, 2006, which is currently the only species of the R. margaritifera group known to occur in the state (Frost, 2017).Therefore, we substituted the former name by the latter.Lima et al. (2010) considered Heyer's (1983) record of Cycloramphus lutzorum Heyer, 1983 for the state of Rio de Janeiro as dubious, and implicitly restricted the species (which they rediscovered after nearly two decades without records) to the states of São Paulo and Paraná.Therefore, we remove C. lutzorum from the list of amphibians of Rio de Janeiro.

Family Hylidae
Aplastodiscus callipygius (Cruz & Peixoto, 1985) was synonymized with A. albosignatus (a species absent from the list of Rocha et al., 2004) by Berneck et al. (2016).Thus, we substituted the former name by the latter in our list.
Bokermannohyla clepsydra (Lutz, 1925) is known only from its type locality in the state of São Paulo (Frost, 2017) and is thus herein removed from the list.
Scinax dolloi (Werner, 1903) is a problematic taxon, as this name is not currently associated to any known frog population (Frost, 2017).Nevertheless, Caramaschi et al. (2013) concluded that its type locality (not given in the original description of Werner, 1903) is Maringá, in the Municipality of Itatiaia, and thus we included this species on the list.

Family Leptodactylidae
The species formerly known as Leptodactylus ocellatus (Linnaeus, 1758) is currently called L. latrans.According to Lavilla et al. (2010), the name Rana ocellata Linnaeus, 1758 does not represent a leptodactylid, but the Jamaican hylid Osteopilus brunneus (Gosse, 1851), and the oldest available name for the taxon then known as Leptodactylus ocellatus is Rana latrans Steffen, 1815.Nascimento et al. (2006) has shown that the correct name of the species to which the name Physalaemus fuscomaculatus (Steindachner, 1864) used to be formerly applied is P. marmoratus.Currently, Eupemphix fuscomaculatus Steindachner, 1864 is considered a junior synonym of Physalaemus biligonigerus Cope, 1861 (see Kolenc et al., 2011), a species that does not occur in Rio de Janeiro (Frost, 2017).Langone et al. (2015) reviewed the distribution range of Pseudopaludicola falcipes (Hensel, 1867) and concluded that this species is restricted to northern Argentina, Uruguay, and the extreme south of Brazil, with all previous Brazilian records outside that range (including those from Rio de Janeiro state) representing misidentifications.Therefore, we remove P. falcipes from the list of amphibians of Rio de Janeiro, observing that the identity of the Pseudopaludicola species occurring in the state is presently unknown, which we acknowledge by listing it as Pseudopaludicola sp.Peloso et al. (2014) synonymized the genus Syncope Walker, 1973 with Chiasmocleis Méhely, 1904, thus creating an instance of homonymy between Chiasmocleis carvalhoi (Nelson, 1975) (formerly in the genus Syncope) and Chiasmocleis carvalhoi Cruz, Caramaschi & Izecksohn, 1997.To solve the problem Peloso et al. (2014) renamed the latter species (i.e., the junior homonym) as C. lacrimae.Silveira et al. (2010) reported the first record of Elachistocleis ovalis (Schneider, 1799), and also of the genus Elachistocleis Parker, 1927, for the state of Rio de Janeiro, based on a specimen from the municipality of Itaperuna.Caramaschi (2010) considered E. ovalis a nomen dubium, and identified all specimens of Elachistocleis examined by him from the state of Rio de Janeiro (including the specimen reported by Silveira et al., 2010) as E. cesarii, a species that had just been revalidated by Toledo et al. (2010) for specimens from the state of São Paulo.Thus, the species of Elachistocleis occurring in Rio de Janeiro is currently referred to E. cesarii.

Family Microhylidae
The records of Stereocyclops incrassatus Cope, 1870 in the state of Rio de Janeiro are currently considered to represent S. parkeri (see Frost, 2017).Previously in the synonymy of S. incrassatus (see Carvalho, 1948), S. parkeri was treated as a valid taxon by Bokermann (1966) without comment, and this has been followed by most subsequent authors since then (e.g., Izecksohn & Carvalho-e-Silva, 2001;Haddad et al., 2013).

Conservation remarks
Fifty-four amphibian species are presently considered endemic of the state of Rio de Janeiro, corresponding to 27% of the state's amphibian richness (Table 1).These include Ischnocnema guentheri (sensu stricto), which was recently considered a microendemic species and is now restricted to the municipality of Rio de Janeiro, with records from elsewhere representing I. henselii and four undescribed cryptic species (Gehara et al., 2013).Also, 16 species (8% of the state's amphibians) are currently considered to be under some level of threat (excluding those categorized as DD) at either the global or national level, or both (Table 1).Some of these, and even a few that are classified as DD, have not been recorded for decades and are possibly extinct, as is the case of Aplastodiscus musicus, Holoaden bradei and Thoropa petropolitana.Although conservation strategies tend to prioritize threatened species, IUCN has recommended to give similar attention to the species considered as "data deficient" (DD), though this is still not being properly done (Pimenta et al. 2005;Siqueira et al. 2013).Species labeled as "DD" currently represent 19% (N = 38) of the amphibian fauna of Rio de Janeiro (Table 1) and, considering that the threat status of several recently described species have not yet been evaluated by the IUCN (2016), this number tends to increase.
Exotic invasive species constitute the second greatest threat to biodiversity, after habitat destruction (Rocha et al., 2011).In the state of Rio de Janeiro, the American bullfrog, Lithobates catesbeianus, remains the only known exotic amphibian occurring in natural habitats.Since 2004, there have been a number of new records of occurrence of the American bullfrog in different parts of the state (Salles et al., 2009;Almeida-Gomes et al., 2014;Pontes et al., 2015).This anuran, native to the eastern and central regions of the United States, is believed to be expanding its distribution in the state of Rio de Janeiro (Rocha et al., 2004;van Sluys et al., 2009), which points to the necessity of monitoring of its populations and of management programs for removal of individuals from natural habitats.
Scinax nasicus, a species typical of open habitats such as Cerrados, has been recently reported from the municipality of Porto Real, representing the easternmost record of the species and the one closest to the coast (Pederassi et al., 2015).The finding of this species in an area that is currently practically devoid of forest remnants suggests that deforestation may be favoring the colonization and/ or range expansion of open-habitat anuran species in the state, as previously reported for the viperid snake Crotalus durissus Linnaeus, 1758 (Bastos et al., 2005).
Recently, a total of 1,080 species of amphibians were reported to occur in Brazil (Segalla et al., 2016) and 543 species were reported for the Atlantic Forest biome (Haddad et al., 2013).Thus, the state of Rio de Janeiro, in spite of its relatively small territorial extension, contains approximately 19% of the amphibian species known to occur in Brazil and nearly 40% of the Atlantic Forest amphibian species.Nevertheless, the list reported herein for Rio de Janeiro is likely still far from exhaustive, judging by the numerous recent reports of undescribed species from throughout the state, including members of genera such as Brachycephalus (Siqueira et al., 2011a(Siqueira et al., , b, 2013)), Ischnocnema (Siqueira et al., 2011b;Gehara et al., 2013), Euparkerella (Fusinatto et al., 2013), Adenomera (Fouquet et al., 2014), Fritziana (Siqueira et al., 2011b;Castroviejo-Fisher et al., 2015), Aplastodiscus (Berneck et al., 2016), andScinax (Bittencourt-Silva &Silva, 2013).This indicates that the current amphibian richness recorded for the state is still an underestimate, and is likely to increase in the years to come following the intensification of taxonomic studies and of local herpetofaunal surveys.The state of Rio de Janeiro thus constitutes an important reservoir of amphibian (and, especially, anuran) biodiversity in the Atlantic Forest biome and of Brazil, as a whole.