Introduction
Surveys of anuran communities provide basic information relevant for the taxonomy and distribution of species, and play a fundamental role in the development of species conservation and management plans (Silvano and Segalla, 2005; Toledo, 2009). These surveys are especially important in regions with high biodiversity and endemism, and those that present some level of threat to their remnants, such as the Atlantic Forest biome (Eterovick et al., 2005). The anurofauna
of the Atlantic Forest is one of the richest in the world, with 88% of the species being endemic to this biome (Haddad et al., 2013). Moreover, the Atlantic Forest is a biome that suffers mostly from habitat loss and fragmentation, remaining only about 11-16% of its original coverage, which is now highly fragmented in the landscape (Ribeiro et al., 2009). The deforestation problem is even more evident in some specific forest types, such as the semideciduous forest (SEF), target of the most drastic vegetation reduction due to rapid expansion of agricultural areas. It is estimated that only about 7% of the original area remains (Ribeiro et al., 2009).
Most of Paraná’s territory is covered by SEF, which houses a lower richness of anurans species than the dense ombrophilous forests, and higher than the mixed ombrophilous forest (e.g., Araucária Forest) (Rossa-Feres et al., 2017). In comparison with ombrophilous forests, SEF presents lower altitudinal and latitudinal gradients, and lower degree of environmental heterogeneity, especially of humid habitats, which possibly explains the reduced number of species that occur in this type of forest (Haddad and Prado, 2005; Brassaloti et al., 2010; Rossa-Feres et al., 2017). Specifically in the State of Paraná, anuran inventories
Anurans of anthropogenic areas and remnants of Semideciduous
Forest in western State of Paraná, Brazil
Peterson Trevisan Leivas1,*, Pedro de Oliveira Calixto1, Cristiane Hiert2 and Michel Varajão Garey3
1 Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná - UFPR, Caixa Postal 19031, CEP 81531-980, Curitiba, Paraná, Brasil.
2 Universidade Estadual do Centro-Oeste - UNICENTRO, Caixa Postal 3010, CEP 85040-080, Guarapuava, Paraná, Brasil.
3 Laboratório de Ecologia de Metacomunidades, Instituto Latino-Americano de Ciências da Vida e da Natureza, Universidade Federal da Integração Latino-Americana - UNILA, Av. Tarquínio Joslin dos Santos, 1000, CEP 85870-901, Foz do Iguaçu, Paraná, Brasil.
* Corresponding author. E-mail: ptleivas@gmail.com
Abstract. Here we present the first species list of anurans from western parts of the State of Paraná, Brazil, including many areas that had never been sampled before, as a contribution to the knowledge of the distribution of biodiversity. The regional species list was compiled based on new field records, museum collections and literature records in the counties of Cascavel, Céu Azul, Foz do Iguaçu, Matelância, Santa Tereza do Oeste, Santa Terezinha do Itaipu and São Miguel do Iguaçu. A total of 36 species were recorded in our study. Twenty-two species were recorded exclusively in the field, two only in museum collections and one species is only recorded in the literature. Hylidae and Leptodactylidae are the most well represented families out of the 10 recorded from museum and literature records with 20 and six species, respectively. Two species were globally classified as Near Threatened (Crossodactylus schmidti and Proceratophrys bigibbosa) and one species was regionally classified as Critically Endagered (Vitreona uranoscopa). Lithobates catesbeianus an exotic invasive species was recorded in four counties. Most of the recorded species occurred only in open area. The species richness observed in each county was lower than those found in other areas of semideciduous forest in the State of Paraná.
in SEF are even scarcer; only the counties of Londrina, Ortigueira, Telêmaco Borba and Três Barras do Paraná have anuran species lists (Bernarde and Anjos, 1999; Machado et al., 1999; Bernarde and Machado, 2000; Machado and Bernarde, 2002; Nazaretti and Conte, 2015; Santos and Conte, 2016).
Recognising the gap in knowledge regarding the anuran community across much of Paraná, we aimed to describe the composition of anuran species in anthropogenic areas and remnants of SEF in parts of western Paraná, specifically in the counties of Cascavel, Céu Azul, Foz
do Iguaçu, Matelândia, Santa Tereza do Oeste, Santa Terezinha do Itaipu, and São Miguel do Iguaçu in southern Brazil. With this work we hope to reduce the Wallacean shortfall (e.g., geographic distribution data) about amphibians (Hortal et al., 2015).
Material and Methods
Study area.—We sampled an area of the geological formation at Serra Geral in the Paraná basin, which holds the third plateau in western Paraná. According to the Köppen-Geiger classification, the climate of the area is Cfa, which means subtropical humid mesothermal with hot summers, infrequent frosts and trend of concentration of rainfalls during the summer months with no defined rainy season (Maack, 2012).
The region is inserted in the Atlantic Forest biome, covered by SEF, mainly at an intermediate stage of forest succession (Ribeiro et al., 2009). In the limit between western and central Paraná there are portions of Araucaria forest, forming a region of ecotone between these two floristic formations. The regional landscape is a mosaic of forest fragments, including the greatest forest remnant of SEF (e.g., Iguaçu National Park), including cultivation, livestock, and urban areas.
Data collection.—The regional species list was compiled based on field records, data from specimens deposited in museums and literature records for seven counties in western Paraná, southern Brazil, named: Cascavel, Céu Azul, Foz do Iguaçu, Matelândia, Santa Tereza do Oeste, Santa Terezinha do Itaipu and São Miguel do Iguaçu (Figure 1, Table 1). For the field data, we sampled forest remnants and open areas (farmlands Figure 1. Map of the study area showing the counties sampled
(light gray), State of Paraná in dark gray. Numbers indicate the county name as following: Cascavel (1), Céu Azul (2), Foz do Iguaçu (3), Matelândia (4), Santa Tereza do Oeste (5), Santa Terezinha do Itaipu (6) and São Miguel do Iguaçu (7). The abreviations of countries as following: Argentina (AR); Brazil (BR); Bolivia (BO); Paraguay (PY); and Uruguay (UY).
1
Table 1. Sampled areas in counties of western State of Paraná, Brazil, detailing geographic
1
coordinates (Céu Azul, Foz do Iguaçu and Santa Tereza do Oeste are the central coordinates of county), 2
type of area, type of sampled environments and number of sampled areas (NSE). O = open area; F = 3
forest; Df = dam in forest; Do = dam in open area; Swf = swamp in forest; Swo = swamp in open area; Pf 4
= pond in forest; Po = pond in open area; St = stream in forest. 5
6
7
County Geographic coordinates Area Environment NSE
Cascavel -25.02 S/-53.55 W F Df, Swf, St, F 7
Céu Azul -25.15 S/-53.84 W F, O Swo, St, Pf, F 9
Foz do Iguaçu -25.51 S/-54.58 W F, O Swf, Swo, Pf, Po, St 16
Matelândia -25.20 S/-54.02 W F, O Df, Do, Swo, St 9
Santa Tereza do Oeste -25.05 S/-53.61 W F, O Sw, St, Pf, Po 8
Santa Terezinha de Itaipú -25.39 S/-54.34 W F, O Do, Swo, F, St 11
São Miguel do Iguaçu -25.37 S/-54.31 W F Df, Swf, St 8
Table 1. Sampled areas in counties of western State of Paraná, Brazil, detailing geographic coordinates (Céu Azul, Foz do Iguaçu and Santa Tereza do Oeste are the central coordinates of county), type of area, type of sampled environments and number of sampled areas (NSE). O = open area; F = forest; Df = dam in forest; Do = dam in open area; Swf = swamp in forest; Swo = swamp in open area; Pf = pond in forest; Po = pond in open area; St = stream in forest.
and urban areas) in these counties. We selected the sampling sites based on the structural features of water bodies in order to sample the largest possible variety of environments (Table 1). Two people (PTL, CH and MVG) performed the sampling in all counties, both during the day (9:00 – 17:00) and twilight and night (17:30 - 22:30h).
In Céu Azul, Foz do Iguaçu and Santa Tereza do Oeste only aquatic breeding sites were sampled (13 lotic and 20 lentic water bodies), applying a visual and acoustic active search (Crump and Scott, 1994) and sampling tadpoles using a hand dipnet (mesh 3mm2). Sampling was carried out between September 2014 and March 2018, which is the breeding season for the great majority of species in western Paraná. Each water body was sampled three times during this period. The first sampling was carried out between September and October, the second between November and December and the third between January and March. Each breeding sites were sampled during one hour applying both sampling methods, totalling an effort of three hours per breeding site.
In Cascavel, Matelândia, Santa Terezinha de Itaipú and São Miguel do Iguaçu anurans were sampled applying visual and acoustic active search methods (Crump and Scott, 1994) using four predetermined transects that crossed aquatic breeding sites (Crump and Scott, 1994). Transects with breeding sites were sampled during two hours during the day and two hours during the night, totalling an effort of four hours/day. In these counties we collected data in August (winter) and November (spring) 2010 and in February (summer), and May (autumn) 2011. Each area was sampled for two days in each season, totalising eight days of sampling per area.
Morphological diagnoses and analysis of the advertisement calls were performed to confirm the taxonomic identity of the species recorded (e.g. Vitreorana uranoscopa according Haga et al. 2014). Vocalizations were recorded with an external directional microphone (Yoga HT 81), coupled to an H2n digital audio recorder positioned at a maximum distance of 1 m to the calling males. Calls were analysed using Raven 1.2 software (16 bits of resolution, 44 kHz of frequency sampling, FFT and frame length of 256 samples). All specimens collected were anesthetized and killed, fixed in 10% formalin and stored in 70% ethanol (adults) or 10% formalin (tadpoles). All adult specimens and tadpoles are housed in Coleção de Anfíbios at Universidade Federal da Integração Latino-Americana (CA-UNILA) (Appendix 1).
Literature and museum data were also compiled. The bibliographic data includes published articles and the list of species collected in the management plan of Iguacu National Park. The search for articles was done on Google Scholar using the keywords “county name” AND “Amphibia”. For the compilation of museum data, herpetological collections were searched through the online database speciesLink, and records from the folowing collections were included: Museu de Ciências e Tecnologia of Pontifícia Universidade Católica do Rio Grande do Sul (MCP-PUCRS), Centro de Coleções Taxonômicas of Universidade Federal de Minas Gerais (UFMG-ICB), Coleção “Célio F. B. Haddad” of Universidade Estadual Paulista campus Rio Claro (CFBH), Coleção de Anfíbios adultos of Universidade Estadual Paulista campus São José do Rio Preto (DZSJRP) and Coleção de Anfíbios of Museu de Zoologia of Universidade Estadual de Campinas (ZUEC). In addition, the authors personally visited the collection of Museu de História Natural Capão da Imbuia (MHNCI).
Species nomenclature was updated following Frost (2017). Anuran threat status was determined according to international, national and regional criteria. Population trends and international threat status for each species were based on data available on the IUCN “Red List of Threatened Species version 2017.3” (IUCN, 2017). The national database follows Ordinance nº 444 of 17 December 2014 (Brasil, 2014) and regionally follows Livro Vermelho da Fauna Ameaçada no Estado do Paraná (Mikich and Bérnils, 2004).
Results
A total of 36 species were recorded in western Paraná, southern Brazil (Table 2). Twenty-two species were recorded exclusively in the field, two only in museum collections and one species was recorded only in the literature (Table 2). Only the MHNCI presented records of anurans from the study region, and all specimens collected are from Foz do Iguaçu (Appendix 1). In field, 33 anuran species representing ten families were recorded (Table 2). Hylidae was the richest family with 20 species (55.5%), followed by Leptodactylidae with six species (16.7%), Bufonidae and Odontophrynidae with two species (5.6% each one), and six families (Alsodidae, Centrolenidae, Hylodidae, Microhylidae, Phyllomedusidae, and Ranidae) with only one species (each one represents 2.8%). The ranid species Lithobates catesbeianus is an exotic and invasive species. Regarding the environmental occurrence, 17
Table 2. Anuran species recorded in the seven counties of western State of Paraná, southern Brazil: Cascavel (CS), Céu Azul (CA), Foz do Iguaçu (FI), Matelândia (MA), Santa Tereza do Oeste (SO), Santa Terezinha do Itaipu (SI), and São Miguel do Iguaçu (SM). Source of the species record in each county: field survey (1), museum collections (2), and literature (3). Population status according to the IUCN (2017): Stb (stable), Unk (Unknown), Dec (Decreasing) and Inc (Increasing). Environmental occurrence (Env): F (forest), O (open area), and B (both).(MA), Santa Tereza do Oeste (SO), Santa Terezinha do Itaipu (SI), and São Miguel do Iguaçu (SM). Source of the species record in each county: field survey (1), museum Table 2. Anuran species recorded in the seven counties of western State of Paraná, southern Brazil: Cascavel (CS), Céu Azul (CA), Foz do Iguaçu (FI), Matelândia
collections (2), and literature (3). Population status according to the IUCN (2017): Stb (stable), Unk (Unknown), Dec (Decreasing) and Inc (Increasing). Environmental occurrence (Env): F (forest), O (open area), and B (both).
County IUCN Env FAMILY/Taxon
CS CA FI MA SO SI SM ALSODIDAE
Limnomedusa macroglossa (Duméril and Bibron, 1841) 3 Stb F
BUFONIDAE
Rhinella ornata (Spix, 1824) 1 2,3 Unk F
R. schneideri (Werner, 1894) 1 1,2 1 1 1 1 Inc B
CENTROLENIDAE
Vitreorana uranoscopa (Müller, 1924) 1 Dec F
HYLIDAE
Aplastodiscus perviridis Lutz, 1950 1 1 2,3 Stb F
Boana albopunctata (Spix, 1824) 1 1 1 1 1 1 1 Stb B
B. bischoffi (Boulenger, 1887) 1 1 1 1 Stb O B. caingua (Carrizo, 1991) 1 2,3 1 Stb O B. faber (Wied-Neuwied, 1821) 1 1 1 1 Stb B B. prasina (Burmeister, 1856) 1 1 1 1 Stb O B. punctata (Schneider, 1799) 1 Stb O B. raniceps (Cope, 1862) 1 1 1 1 Stb O
B. semiguttata (A. Lutz, 1925) 3 Stb O
Dendropsophus minutus (Peters, 1872) 1 1 1 1 1 1 1 Stb B
D. nanus (Boulenger, 1889) 1 1 1,2,3 1 1 1 1 Stb O
D. sanborni (Schmidt, 1944) 1 1 Stb O
Itapotihyla langsdorffii (Duméril and Bibron, 1841) 1 Dec F
Lysapsus limellum Cope, 1862 1 Stb B
Ololygon berthae (Barrio, 1962) 2,3 Stb B
Scinax fuscovarius (Lutz, 1925) 1 1 1,2,3 1 1 1 1 Stb B
S. granulatus (Peters, 1871) 1 Stb O
S. perereca Pombal, Haddad, and Kasahara, 1995 1 1 1 Unk B
S. squalirostris (Lutz, 1925) 1 1 Stb O
Trachycephalus dibernadoi Kwet and Soulé 2008 1 Stb F
HYLODIDAE
Crossodactylus schmidti Gallardo, 1961 1 1 Dec F
LEPTODACTYLIDAE
Leptodactylus fuscus (Schneider, 1799) 1 1 1 1 1 1 Stb O
L. latrans (Steffen, 1815) 1 3 1 1 1 Stb B
L. mystacinus (Burmeister, 1861) 2,3 1 1 Stb O
L. podicipinus (Cope, 1862) 2 1 Stb O
Physalaemus aff. gracilis (Boulenger, 1883) 1 Stb O
Physalaemus cuvieri Fitzinger, 1826 1 1,2,3 1 1 1 Stb O
MICROHYLIDAE
Elachistocleis bicolor (Guérin-Méneville, 1838) 1 1 1 Stb O
ODONTOPHRYNIDAE
Proceratophrys avelinoi Mercadal de Barrio and Barrio, 1993 1 Unk F
P. bigibbosa (Peters, 1872) 1,2 Dec F
PHYLLOMEDUSIDAE
Phyllomedusa tetraploidea Pombal and Haddad, 1992 1 Stb B
RANIDAE
Lithobates catesbeianus (Shaw, 1802) 1 1 1 1 Inc O
Figure 2. Some of the anuran species recorded for western Paraná, Brazil. (a) Rhinella schneideri, (b) Aplastodiscus perviridis, (c) Boana caingua, (d) B. faber, (e) B. prasina, (f) B. punctata, (g) B. raniceps, (h) Dendropsophus sanborni, (i) Phyllomedusa
tetraploidea, (j) Scinax granulatus, (l) S. squalirostris, (k) Leptodactylus fuscus, (m) L. podicipinus, (n) Physalaemus cuvieri, (o) P. aff. gracilis, and (p) Proceratophrys avelinoi.
occur in open areas, nine occur only in forest, and 10 species occur in both environments (Table 2).
According to the IUCN, the majority of species found are classified as Least Concern (LC), and only Crossodactylus schmidti and Proceratophrys bigibbosa are classified as Near Threatened (NT). No species from western Paraná is listed as endangered in the Brazilian National Red List. In Paraná State Red List, Vitreorana uranoscopa is categorized as Data Deficient (DD) and Limnomedusa macroglossa as Critically Endangered (CE). Regarding the population status of the species, most species were considered stable (72% of species), four species have declining populations (11%), three species have unknown population status (8%), two species (6%), L. catesbeianus and Rhinella schneideri with increasing population size. Physalaemus aff. gracilis has an uncertain taxonomy and therefore is not included in the IUCN list (Table 2; IUCN 2017). Discussion
The anurofauna of western Paraná accounts for 23% of the amphibian species of this state (Toledo & Batista, 2012) and 6% of the known species that occur in the Atlantic Forest (Haddad et al., 2013). The species richness observed in each county was lower than that found in other areas of semideciduous forest in Paraná state, such as Telêmaco Borba and Ortigueira counties (27 species; Machado and Bernarde, 2002), Parque Estadual Mata dos Godoy in Londrina county (24 species; Bernarde & Anjos, 1999, Machado et al., 1999), and Parque Estadual do Rio Guarany in Três Barras county (23 species; Bernarde and Machado, 2000). It is quite possible that the sampling effort of the present study was not enough to record all the species from these seven counties located in western Paraná. However, this is the first anuran species list of this region, so with the increase of sampling effort, especially in the Iguaçu National Park and other counties of Paraná River bank, more species should be added to the list.
The conservation status of most species is Least Concern (IUCN, 2017), which is probably related to the wide geographic distribution of these species (e.g., Aplastodiscus perviridis, Dendropsophus nanus, Leptodactylus latrans) (Haddad et al., 2013; Frost, 2017), and/or more generalist in relation to habitat use, for example, some species are commonly found in urban environments, such as Leptodactylus fuscus, Rhinella schneideri and Scinax fuscovarius (Haddad et al., 2013). Crossodactylus schmidti, Limnomedusa macroglossa and Proceratophrys bigibbosa are the only endangered
species in western Paraná. Crossodactylus schmidti occurs in streams inside forests and L. macroglossa occurs in open and forested areas on rocky soil along rivers both in mesophytic semideciduous and Araucaria forests (Conte et al., 2009; Santos et al., 2009; Caldart et al., 2010; Haddad et al., 2013). Proceratophrys bigibbosa occurs in mountainous regions and Araucaria forest plateau, and breeds in small streams (Kwet and Faivovich, 2001). The major threats to these species are deforestation, forest fragmentation and soil and water pollution, and the presence of the exotic Lithobates catesbeianus (Silvano et al., 2004a; 2004b). Moreover, four species recorded only in the Iguaçu National Park are in population decline: C. schmidti, Itapotihyla langsdorffii, P. bigibbosa, and Vitreorana uranoscopa. Searches for other populations of these species in forest fragments located in western Paraná should be considered a priority. These findings provide evidence of the effects of fragmentation on these species. In addition, the acquisition of information about natural history is essential to develop conservation strategies, especially for data deficient species (e.g., V. uranoscopa) or under some degree of threat (e.g., C. schmidti, P. bigibbosa, and L. macroglossa) (Mikich and Bérnils, 2004; IUCN, 2017).
Western Paraná, excluding Iguaçu National Park, is one of the most deforested and fragmented regions of the state (Ribeiro et al., 2009) where there are only small forest fragments and few studies on biodiversity. This study represents an important contribution to understanding the distribution of biodiversity in this region. Species lists are essential to reduce the Wallacean shortfall, and this is the starting point for the development of conservation strategies.
Acknowledgements. We thank the Instituto Chico Mendes
de Conservação da Biodiversidade (ICMBio) for providing collection permits (SISBIO/40772 and 42012). MVG thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Proc. 422537/2016-0) and UNILA (edital PRPPG 109/2017) for financial support. POC thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a research fellowship (132606/2016-0). PTL thank Fundação Araucária, Fundação Grupo Boticário de Proteção a Natureza and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support. We thanks Jéssica de L. Jeziorny, Fátima R. B. Fernández, Fatima B. Penayo, Tarik A. Kardush, Lara J. G. de Sousa, Jean P. S. da Silva and Derlis J. V. Ayala for valuable assistance in the field.
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Appendix 1 – Voucher List
Museu de História Natural Capão da Imbuia (MHNCI):
Brazil, State of Paraná, Foz do Iguaçu: Aplastodiscus perviridis: 2902. Boana caingua: 2900. Dendropsophus nanus: 2904–2908. Leptodactylus mystacinus: 2899; 8577. Leptodactylus podicipinus; 8573; 8574; 8576. Ololygon berthae; 2903. Physalaemus cuvieri; 8584; 8597; 8603–8606; 8608–8610; 8912–8916. Proceratophrys bigibbosa: 8579–8583; 8588–8593. Rhinella ornata: 8561–8564. Rhinella schneideri: 8565–8568. Scinax fuscovarius: 2901; 8570–8572; 8578; 8595; 8596.
Coleção de Anfíbios da Universidade Federal da Integração Latino-Americana (CA-UNILA):
Brazil, State of Paraná, Céu Azul: Aplastodiscus perviridis: 007. Crossodactylus schmidti: 0003-005; 008-010. Hypsiboas faber: 006.
Brazil, State of Paraná, Foz do Iguaçu: Boana albopunctata: 012; 075; 177; 236-238. Boana raniceps: 86-87; 182-184. Dendropsophus minutus: 076-077; 088-089; 168-173. Dendropsophus nanus: 79-82; 99-103; 162-167. Elachistocleis bicolor: 140-145; 174; 206. Itapotihyla langsdorffi: 048-049. Leptodactylus fuscus: 104; 148; 157; 197; 224. Leptodactylus podicipinus: 92; 151-153; 187-191; 243-244. Physalaemus cuvieri: 178; 215. Proceratophrys bigibbosa: 013. Rhinella ornata: 161. Rhinella schneideri: 83-85; 179-181. Scinax fuscovarius 014; 044; 121-122; 124-126. Scinax squalirostris: 078; 105-110. Trachycephalus dibernadoi: 061.
Brazil, State of Paraná, Santa Tereza do Oeste: Leptodactylus latrans: 045.
