Anuran amphibians in state of Paraná , southern Brazil

The state of Paraná, located in southern Brazil, was originally covered almost entirely by the Atlantic Forest biome, with some areas of Cerrado savanna. In the present day, little of this natural vegetation remains, mostly remnants of Atlantic Forest located in the coastal zone. While some data are available on the anurans of the state of Paraná, no complete list has yet been published, which may hamper the understanding of its potential anuran diversity and limit the development of adequate conservation measures. To rectify this situation, we elaborated a list of the anuran species that occur in state of Paraná, based on records obtained from published sources. We recorded a total of 137 anuran species, distributed in 13 families. Nineteen of these species are endemic to the state of Paraná and five are included in the red lists of the state of Paraná, Brazil and/or the IUCN. Two anuran species were categorized as Near Threatened by the IUCN and 27 species were listed as Data Deficient in one or more lists. According to IUCN 49.6% of the anuran species recorded had their population trends stable, 19% in declined, only 1.4% is increased and 20.4% had your population trends unknown. We also recorded the occurrence in Paraná of the exotic invader anuran Lithobates catesbeianus. We consider our list of species to be a relatively reliable estimate of the anuran diversity of the Brazilian state of Paraná, although new species records are expected, mainly because there are many regions that have not yet been sampled.


Introduction
Currently 6836 species of anuran amphibians are known to exist worldwide (Frost 2017).Just under a sixth (15.2%; 1039 species) of this total is found in Brazil (Segalla et al. 2016).This high species richness is partly related to the continental dimensions of the country and its considerable variation in altitude, as well as the enormous variety of tropical and subtropical habitats and ecosystems found in the different Brazilian biomes (Araújo et al. 2009), which provide a diversity of environments appropriate for anuran populations.In the Brazilian state of Paraná, most of these ecosystems are associated with the Atlantic Forest biome, although some areas of the Cerrado biome are also found in the state.Both these biomes have been classified as world biodiversity hotspots (Myers et al. 2000).Based on the modeling of the distribution data available for anuran species, Toledo & Batista (2012) estimated that as many as 147 anuran species may potentially occur in the state.Crivellari et al. (2014) recently listed the anurans that occur in the southern grasslands of Paraná, citing a total of 61 species.Up until now, however, no complete list of the anurans known to occur in the state of Paraná has been published.
While species lists for the country as a whole or for its different political divisions are important for the understanding of their biodiversity and provide an additional tool for the development of conservation measures, knowledge on the diversity of most groups of animals, through studies that provide species lists, is still incipient for most Brazilian states.Currently, lists of anuran amphibians are only available for the Brazilian states of Alagoas (Almeida et al. 2016), Espírito Santo (Almeida et al. 2011), Piauí (Roberto et al. 2013), Rio de Janeiro (Rocha et al. 2004), Rio Grande do Sul (Machado & Maltchik 2007), and São Paulo (Rossa-Feres et al. 2011), less than a quarter (23.1%) of the total number of Brazilian states.
In the present study, we estimated the number of anuran taxa that occur in the Brazilian state of Paraná based on a compilation of published records.We identified the endemic species, the taxa listed as threatened, near threatened and data deficient and the population trend of each species (sensu IUCN 2017).We also mapped the localities in Paraná where anuran inventories have been conducted.

Material and Methods
To identify the anuran species that occur in the Brazilian state of Paraná, we considered data obtained from papers published in journals based on a search of the Web of Science, Scielo, Scopus, and Google Scholar databases.The search terms used to identify the papers were amphib* AND Paraná, anur* AND Paraná and frog* AND Paraná.We consulted the papers cited as references in these articles.We terminated the search in November 06, 2017.We also did a supplementary search on the website SpeciesLink (2017) to know if there was still some anuran species collected in the state of Paraná that had not been registered by us through the publications accessed.To identify the endemic species of the Paraná state and the Atlantic Forest, we analyzed the known geographic distribution of each recorded species by Frost (2017).The current conservation status of each species was obtained from the Red List of Threatened Fauna of the state of Paraná (Segalla & Langone 2004), the Red List of Threatened Brazilian Fauna (MMA 2014), and the online version of the IUCN Red List of Threatened Species (IUCN 2017).The IUCN website was accessed to know the population trends of the anurans recorded in the present study (IUCN 2017).We followed the taxonomic nomenclature of Frost (2017).
The Hylidae family was the richest in species (58 species, 42.3% of the total), while Alsodidae, Centrolenidae, Craugastoridae, Hemiphractidae and Ranidae were the least diverse, each one represented by a single species (0.7% of the total) (Table 1).The most diverse genus was Boana, with 13 species, 9.5% of the total recorded for the state.The most frequently recorded species in published studies were Boana faber (Wied-Neuwied, 1821) and Scinax fuscovarius (Lutz, 1925), each one recorded in 18 studies, and Dendropsophus minutus (Peters, 1872) and Ischnocnema henselii (Peters, 1870), both recorded in 17 studies.By contrast, out of 137 recorded species, 32 (23.3%) were cited in only a single study, nine of them (28.1%) are endemic to Paraná, and a further eight (25%) are also found only in the neighboring states of Santa Catarina or São Paulo.
We also reported the occurrence of the exotic invader anuran Lithobates catesbeianus (Shaw 1802) (Ranidae), known as the bullfrog.We found five studies that recorded the occurrence of this anuran species in the state of Paraná (Table 1).
Five (3.6%) anuran species are listed as threatened in the red lists of Paraná, Brazil and/or IUCN (Table 1): Brachycephalus pernix, Dendropsophus anceps (Lutz, 1929), Limnomedusa macroglossa (Duméril & Bibron, 1841), Boana semiguttata (Lutz, 1925)  Based on IUCN (2017), the population trends of 68 (49.6%) anuran species recorded in the present study are stable (Table 1).Most of these species belongs to the family Hylidae (40 species, 58.8% of the total number of registered species), representing 69% of the recorded hylids, and Leptodactylidae (17 species, 25.0% of the total number of registered species), representing 65.4% of the recorded leptodactylids.By contrast, 26 species (19% of the total number of registered species) have declining populations, including nine hylids (15.5% of hylid species) and five leptodactylids (19.2% of leptodactylids species), and two species have increasing populations (1.4% of the total number of registered species), Rhinella schneideri (Werner, 1894) and Lithobates catesbeianus.A further 28 (20.4%)species recorded for Paraná have unknown population trends, nine species from the family Brachycephalidae (6.6% of the total number of registered species, 60% of the brachycephalids) and seven species from the family Bufonidae (5.1% of the total number of registered species, 58.3% of the bufonids).The remaining 11 anuran species (8.1% of the total number of registered species) have yet to be assessed by the IUCN.Two recently described anuran species (Brachycephalus coloratus and B. curupira) have not yet been assessed by the IUCN and therefore, we have not been able to access their population trends.

Discussion
The 137 anuran species recorded in the present study for the Brazilian state of Paraná is close to the 147 species predicted for the state by Toledo & Batista (2012), and thus appears to be a relatively reliable estimate.In that study, the authors constructed a Brazilian list of species based on range distribution shapes (shadow maps analysis), including species occurrences by Brazilian states, and therefore, we assume that species recorded by them to Paraná but not registered in our study do not occur in the state; these anuran species are: Ischnocnema manezinho (Garcia, 1996), Melanophryniscus spectabilis Caramaschi & Cruz, 2002, Rhinella granulosa (Spix, 1824), Cycloramphus diringshofeni Bokermann, 1957, Proceratophrys appendiculata (Günther, 1873), Fritziana goeldii (Boulenger, 1895), Dendropsophus elianeae (Napoli & Caramaschi, 2000)  recorded in Paraná require revision.For example, eight species were identified "aff.","cf." or "gr." in the articles consulted.One of them is Adenomera cf.bokermanni, cited by Santos-Pereira et al. ( 2016), and A. aff.bokermanni by Armstrong & Conte (2010) and Garey & Hartmann (2012).This species was originally described as Adenomera bokermanni by Heyer (1973), type locality in the municipality of Paranaguá, state of Paraná, and it seems very likely that the taxon cited in more recent studies corresponds to this species, given that these records refer to localities extremely close to the type locality of A. bokermanni, that is, municipalities of Morretes (Armstrong & Conte 2010) and Guaraqueçaba (Garey & Hartmann 2012, Santos-Pereira et al. 2016).Ischnocnema spanios (cited as "cf." in Santos-Pereira et al. 2016) is known to occur only from the minicipalyti of Boracéia (type locality of this species, Heyer, 1985) to the municipality of São Paulo (L.Malagoli, pers.comm.).Santos-Pereira et al. ( 2016) collected an anuran of the genus Cycloramphus, which they identified as C. cf.asper, although vouchers were juveniles (MNRJ 87917-87918), which hampered the identification of the species.The occurrence of Hylodes aff.asper by the first time by Garey & Hartmann (2012) in the municipality of Guaraqueçaba may have been a mistake.Some years previously, Lingnau et al. (2008) described this species from a nearby municipality in the state of Paraná, Morretes, which is less than 90 km from Guaraqueçaba, and discussed the geographic distribution of Hylodes asper (Müller, 1924).For many years, herpetologists believed that the geographic range of H. asper extends from the state of Santa Catarina to the state of Rio de Janeiro, although this species has often been confused with H. perplicatus (Miranda-Ribeiro, 1926) or H. cardosoi Lingnau, Canedo & Pombal, 2008.The geographic range of H. asper is now restricted to an area from the state of Rio de Janeiro to Paranapiacaba, municipality of Santo André in the state of São Paulo, while H. cardosoi, but not H. asper, is found in the south of state of São Paulo (Lingnau et al. 2008).Therefore, we believe that the record of Hylodes aff.asper from Salto Morato, municipality of Guaraqueçaba, does in fact refers to H. cardosoi, but unfortunately, there are no voucher specimens or vocal records that might help confirm this hypothesis.Boana stellae (Kwet, 2008) is known only from the southern slope of the Araucaria Plateau in the center of the state of Rio Grande do Sul (Kwet 2008).Ololygon perpusillus is apparently restricted to the municipality of Rio de Janeiro (Peixoto 1987).Elachistocleis cesarii is known from northeastern Brazil, in the states of Ceará, Sergipe, and Bahia, central Brazil, in the states of Mato Grosso, Goiás, and Federal District, and southeastern Brazil, in the states of Minas Gerais, Espírito Santo, Rio de Janeiro and São Paulo (Caramaschi 2010).It is important to note that Fritziana gr.fissilis was recorded in two separate studies at the same locality, municipality of Guaraqueçaba, on the northern coast of the state of Paraná (Garey & Hartmann 2012, Santos-Pereira et al. 2016).In this case, further fieldwork will be required to confirm the occurrence of the species in the state of Paranábecause the genus Fritziana requires a taxonomic review and the specimens cannot be assigned reliably to a specific species at the present time.
In addition to these taxonomically problematic anurans, several other species assigned to Paraná by Frost (2017) were not included in our list.As we found no other reliable evidence or records of the occurrence of these species in Paraná, we did not include them in our inventory.These species are Boana curupi (Garcia, Faivovich & Haddad, 2007), Bokermannohyla claresignata (Lutz & Lutz, 1939), Trachycephalus imitatrix (Miranda-Ribeiro, 1926), Cycloramphus izecksohni Heyer, 1983 andBoana crepitans (Wied-Neuwied, 1824).In the case of B. claresignata, the only evidence is the record of Lutz (1973), who found tadpoles similar to those described for the species, but don't recorded any adult individual.Garcia et al. (2007) assumed that B. curupi occurs in Paraná, due to its association with the Paraná and Uruguay rivers, but we don't find any record of this anuran in the state of Paraná.Lutz (1973) found that the T. imitatrix specimens from southern Brazil (the "southern" form) were relatively large in size, and had a distinct type of iris, which is consistent with the description of T. dibernardoi Kwet & Solé, 2008.The analysis of the specimens from the municipality of Telêmaco Borba revealed the larger body size and dorsal markings typical of T. dibernardoi (Conte et al. 2010).In addition, the description of T. dibernardoi for the region near Curitiba (Kwet & Solé 2008) refers to a voucher specimen from a survey of the Fazenda Rio Grande (DZSJRP 8810; Conte & Rossa-Feres 2007), where this anuran was confused with T. imitatrix (Conte et al. 2010).Given this evidence, we concluded that T. dibernardoi, rather than T. imitatrix, occurs in Paraná, as recorded by Lutz (1973), and that the occurrence of T. imitatrix recorded by Conte & Rossa-Feres (2006, 2007) at São José dos Pinhais and Fazenda Rio Grande does in fact refer to T. dibernardoi.In the case of C. izecksohni, Frost (2017) only mentioned that the species occurs in the Serra do Mar coastal range, in the states of São Paulo, Paraná and Santa Catarina.Frost (2017) considered B. crepitans to occur in northern Brazil, with an allopatric population in the northeast, ranging as far south as Paraná and Santa Catarina.On these last two localities, we found available information about this anuran species only from the referred website.
Boana faber, Scinax fuscovarius, Dendropsophus minutus and Ischnocnema henselii were the anurans recorded most frequently in the studies analyzed.This reflects, in part, the wide geographic distribution of these species in Brazil (Frost 2017), as well as their life history strategies.In the case of the hylids, for example, populations are often associated with open areas or even disturbed habitats (Lucas & Fortes 2008;Almeida-Gomes et al. 2010, 2014), resulting in a greater tolerance of these species to anthropogenic impacts in the environment.In particular, I. henseli, which is found in the leaf litter, was considered to be one of the dominant species of the anuran community at Guaraqueçaba (Santos-Pereira et al. 2011), given the considerable variety of microhabitats found in the leaf litter of the forest floor.This suggests that I. henseli besides frequent, is also an abundant leaf-litter frog found in the forest floor, and this possibly also indicates a greater environmental tolerance by this frog.
By contrast, 32 (23.3%) of the 137 anuran species identified in the literature search were recorded in only one study, and most of these species are endemic to Paraná or occurs only also in the region that includes the neighboring states of Santa Catarina and São Paulo.While these records may reflect a relatively restricted distribution for these species, they may also be the result of subsampling in Paraná, given that research on anurans in this state is still incipient (Santos-Pereira 2016) with inventories of anuran species concentrated basically in two regions of state (see discussion below).The restricted occurrence of many species may also be related to the devastation of the state's forests, which has often impacted their structure, resulting in direct effects on their anuran species richness, including the possible eradication of the most sensitive forms.Only 11.7% of the original Atlantic Forest cover of  (Frost 2017).The species of this genus are found on the eastern coast of Brazil between the states of Bahia, in the northeast, and Santa Catarina, in the south (Frost 2017), with most occurring at altitudes of over 600 m in the Serra do Mar (Ribeiro et al. 2005, Alves et al. 2006).Many of these species have been described recently (Garey et al. 2012b, Ribeiro et al. 2015, 2017, Bornschein et al. 2016a), which emphasizes the importance of surveys in the least well-known remnants of Atlantic Forest, which are often found in relatively inaccessible areas of high altitude.The biodiversity corridors of the Atlantic Forest -the Central Atlantic Forest corridor, the Serra do Mar corridor, and the Northeast corridor (Rocha et al. 2003) -contain a considerable number of endemic vertebrates, including anuran amphibians, and the coast of Paraná is located within the largest continuous remnant of Atlantic Forest, which is part of the Serra do Mar corridor (Câmara 2005), which implies that the state may have more endemic anurans than currently known.This is consistent with the position of Pimm et al. (2010), who predicted that many endemic species of amphibians, birds, and mammals are yet to be discovered in the Brazil.
The type localities of the anuran species described from specimens collected in Paraná are concentrated in the east of the state.This probably reflects the greater research efforts in this region, where we recorded the highest number of localities with anuran inventories, and also to the principal remnants of native forest (Câmara 2005).Additionally, this can be reflected the flora inventories and the proximity of large urban centers or the presence of specialists in the taxonomic groups in these urban areas.Another factor is the presence (and density) of roads, which implies accessibility to natural areas (Pautasso 2007, Ficetola et al. 2013).
In the state of Paraná, the exotic invader anuran Lithobates catesbeianus has been recorded in 15 municipalities up until now (Santos-Pereira & Rocha 2015).In general, these municipalities are located within a 60 km radius of commercial frog farms, indicating that, in most cases, the invasion of natural areas by L. catesbeianus has resulted from the escape of captive individuals into the natural environment (Santos-Pereira & Rocha 2015).As the records show that L. catesbeianus is widely distributed in different regions of the state, it is possible that the actual area occupied by the bullfrog in the state of Paraná is much larger than currently thought.Further surveys in the state may provide new evidence on the extent of the area invaded by L. catesbeianus.
The red lists consulted during the present study revealed several inconsistencies in the conservation status of the anuran species identified in the state of Paraná.Some of these discrepancies may be the result of a certain asynchrony between the regional, national and global assessments (Rodríguez et al. 2000).The conservation status of nonendemic species will also vary according to the scale of analysis, even though it should be consistent among the state, national and global red lists (Brito et al. 2010).This indicates the existence of discrepancies between the national and global lists, given that two species endemic to the state of Paraná (B.pernix and I. paranaensis) are listed as DD by the IUCN, although I. paranaensis is not even listed by the Brazilian government.Similarly, Pseudis cardosoi is listed by the IUCN, but does not appear on the lists for Paraná or Brazil.In the specific case of the State list, the publication is more than 10 years old (Segalla & Langone 2004), and requires revision, whereas on a broader scale, species not endangered in Paraná may be under threat in other states.As the regional lists are not updated regularly, they tend to provide outdated assessments of conservation status.This situation may reduce the effectiveness of these lists as guidelines for conservation practices, given that most measures are currently based on the evaluation of the extinction risk of the species (Miller et al. 2006).It is important to note that the regional lists are important conservation tools, given that most measures are implemented on a local scale (Possingham et al. 2002).Half of the anuran species recorded by us in this study that were categorized as data deficient in Paraná list or by the IUCN are endemic of this state.This reinforces the need for further research into the viability of their populations and the habitats they occupy, and their potential risk of extinction.
Based on the assessment of the IUCN (2017), most of the anuran species recorded in the present study -predominantly hylids -have stable populations.This is probably at least partly due to the fact that these are among the most abundant species in anuran communities, in particular in the Atlantic Forest (e.g., Conte & Rossa-Feres 2006, Almeida-Gomes et al. 2010, Santos-Pereira et al. 2016).For example, the three species recorded most frequently in the publications analyzed in the present study (Boana faber, Dendropsophus anceps and Scinax fuscovarius) are known to be very common species (IUCN 2017), and S. fuscovarius is common even in deforested areas.The majority of leptodactylids have stable populations, and many of them [e.g., Adenomera marmorata Steindachner, 1867, Physalaemus cuvieri Fitzinger, 1826 and Leptodactylus mystaceus (Spix, 1824)], are common throughout their geographic ranges ( IUCN 2017).Populations are declining in 26 species, which may reflect impacts on the ecosystems in which these anurans are found, in particular the high deforestation rates recorded throughout the state of Paraná.For example, Aplastodiscus ehrhardti (Müller, 1924), Proceratophrys brauni Kwet &Faivovich, 2001 andScythrophrys sawayae (Cochran, 1953) are relatively common species and their populations, while classified as declining by the IUCN, are stable in suitable habitats.Other example is Pleurodema bibroni, a rare species that occurs in widely scattered populations, being probably extinct in Montevideo Department, Uruguay, because of habitat destruction (IUCN 2017).The populations of only two anuran species listed here (Rhinella schneideri and Lithobates catesbeianus) are thought to be increasing (IUCN 2017).Lithobates catesbeianus is widespread in Paraná (Santos-Pereira & Rocha 2015).This species is known worldwide from thousands of localities and is usually very abundant with increasing populations (IUCN 2017).In 28 cases, mostly brachycephalids and bufonids, population trends are unclear, although some brachycephalids, such as Brachycephalus brunneus, B. ferruginus, B. izecksohni, Ischnocnema henselii and I. sambaqui, are locally abundant ( IUCN 2017).No data are available on the population trends of other brachycephalids, i.e., B. pombali and I. spanios (IUCN 2017).The populations of the Brachycephalus species are typically restricted to fragments of hill forests (Pombal et al. 1998, Ribeiro et al. 2005, Alves et al. 2006), separated by valleys, which isolates the populations (Pie et al. 2013) and makes them difficult to survey effectively.In the case of the bufonids, Dendrophryniscus stawiarskyi, for example, is known only from three specimens collected in the early 1980s, and there is currently no information on its population status, while the species of the genus Melanophryniscus, M. alipioi and M. tumifrons (Boulenger, 1905), are extremely difficult to survey, although the former species is commonly encountered during the breeding season (IUCN 2017).This possibly is due to the fact that the anuran species of this genus show explosive breeding, reproducing in small and ephemeral water bodies (e.g.Cairo et al. 2008, Laufer et al. 2015).Given this scenario, we identified three main variables that are important for the evaluation of the population viability of anurans -the abundance of the species, the difficulty of capturing specimens and the quality of the environment inhabited by the population.
While we identified an additional 10 anuran species during the survey of the scientific collections available in the SpeciesLink database, we did not include these species in our inventory of the anurans of the state of Paraná.The record of Allobates brunneus, for example, is almost certainly erroneous, given that the genus Allobates is not found in Paraná (Verdade & Rodrigues 2007).While it may be possible that Vitreorana eurygnatha occurs in Paraná, we found only a single specimen in the Brazilian National Museum of Natural History (NMNH), so at this time, we prefer to exercise caution, and not confirm that the species occurs in Paraná.Similarly, we have classified Aplastodiscus cochranae, A. leucopygius, Crossodactylus gaudichaudii, Leptodactylus chaquensis and Physalaemus biligonigerus as tentative occurrences, pending the confirmation of the taxonomic identification of the specimens.In the specific case of Boana polytaenia, we consider the identification doubtful, given that Cruz & Caramaschi (1998) did not refer to the occurrence of the species in Paraná in their review [the only species of this complex known unequivocally to occur in the state of Paraná, at the present time, and that was included in our list, is Boana jaguariavensis (Caramaschi, Cruz & Segalla, 2010)].It seems likely the record of Ololygon brieni does in fact refers to O. littoralis (Pombal & Gordo 1991).Finally, it does seem likely that Pseudopaludicola falcipes occurs in Paraná, given that this species is cited by Frost (2017).
The inventories of anurans in the state of Paraná have been concentrated primarily in the metropolitan region of the Curitiba city, in the eastern extreme, and the central-northern region of the state, while there are severalgeographic distribution gaps in most of the state.This concentration of research in the north and east of the state reflects the proximity of its principal universities, including the Federal University of Paraná, in the Curitiba city, and the State universities of Londrina and Maringá, both located in the central-northern region.The metropolitan region of Curitiba, which extends as far as the Atlantic coast, also encompasses several other institutions, including universities and museums, and a major portion of the largest continuous remnant of Atlantic Rainforest found in Brazil.This region also contains a number of protected areas, which may stimulate the interest of researchers seeking well-preserved environments and faunal communities.It is interesting to note that there has been no inventory of anurans in the Foz do Iguaçu micro-region, in western Paraná, which includes the Iguaçu National Park, one of Brazil's first national parks, created in 1939.
This study was the first attempt to compile a comprehensive inventory of the anuran fauna of the Brazilian state of Paraná.We consider our list of species to be a relatively reliable estimate of the anuran diversity of the state, although we do expect new species to be added to the list, in particular because many areas have yet to be sampled adequately.In addition to the need for more extensive surveys, especially in areas that have yet to be sampled adequately, a number of forms require taxonomic review.We also emphasize the need for the conservation of the state's remaining natural habitats, as well as further research on the invasion of the region by the exotic frog, Lithobates catesbeianus, especially in relation to the escape and dispersal of animals from local frog farms.
and Ischnocnema paranaensis.Brachycephalus pernix is classified as Critically Endangered (CR) in Paraná and Brazil and L. macroglossa only in Paraná, while B. semiguttata and I. paranaensis are listed as Endangered (EN) in Brazil and in Paraná, respectively.Moreover, Crossodactylus schmidti Gallardo, 1961 and Pleurodema bibroni Tschudi, 1838 are listed as Near Threatened (NT) by the IUCN.A further 27 species (19.2% of the total) are listed as Data Deficient (DD) in Paraná and/or by the IUCN.Two of the species endemic to Paraná (B.pernix and I. paranaensis) are listed as Critically Endangered, corresponding to 10.5% of the anuran species endemic to the state.

Table 1 .
Anuran amphibians in the state of Paraná, southern Brazil, including geographical distribution in Brazil, endemism for the state of Paraná (both sensu
Paraná now remains, and it has the highest historic rate of deforestation of any state of the Brazil (Fundação SOS Mata Atlântica & Instituto Nacional de Pesquisas Espaciais 2015).Eleven (57.9%) of the 19 endemic species recorded in the present study are brachycephalids, and nine of these are Brachycephalus species, which is 26.5% of the 34 species currently recognized for this genus