Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil

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1 Herpetology Notes, volume 10: (2017) (published online on 29 May 2017) Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil Karoline Ceron 1,2, *, Elaine Maria Lucas 3,4 and Jairo José Zocche 1 Abstract. We provide a list of amphibians from Parque Estadual da Serra Furada, located in Orleans and Grão-Pará municipalities, in Santa Catarina state, southern Brazil. Monthly sampling was carried out from August 2014 to July 2015, using visual and acoustic surveys. Twenty-seven species of anurans belonging to nine families were recorded on six distinct sites between forest trails, swamps, and streams, with 13 reproductive modes reported. Including all sites, 13 species were abundant, and five of them were considered rare. The greatest richness was recorded in the swamp, while forest trail and stream areas showed the greatest taxonomic distinctness. The high number of reproductive modes is a result of structural characteristics of the sampled areas, providing different microenvironments for anuran reproduction, a characteristic of the Atlantic Forest biome, emphasizing the importance of these environments in amphibian conservation. Keywords: Amphibians, Atlantic Forest, biodiversity, protected area, Neotropical region Introduction Brazil is one of the countries with the highest richness of amphibians in the world, with 1080 species (Segalla et al., 2016). The Atlantic Forest is an endangered morphoclimatic domain, classified as a hotspot (Myers et al., 2000), with 529 species of anurans (Haddad et al., 2013), one of the greatest biodiversity and endemism areas of the world. The original coverage of this morphoclimatic domain included almost the entire Brazilian coast; from the northern of Rio Grande do Norte state to north of Rio Grande do Sul (IBGE, 2012). Today, the remnants cover less than 13% of the original territory (Fundação SOS Mata Atlântica & INPE, 2015). Santa Catarina is a south Brazilian state inserted in the Atlantic Forest area with less than 30% of its original cover, with a predominance of vegetation in the medium and advanced successional stages (Sevegnani & Schroeder, 2013). Approximately 80% of the fragments are smaller than 50 ha, revealing a high degree of fragmentation of the remaining forest of the State (Vibrans et al., 2012). The study area comprises a phytoecological region of montane rainforest, 1 Laboratório de Ecologia de Paisagem e de Vertebrados, Programa de Pós-Graduação em Ciências Ambientais, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil. 2 Universidade Federal de Mato Grosso do Sul, Programa de Pós-Graduação em Ecologia e Conservação, Instituto de Biociências, Cidade Universitária, Campo Grande, MS, Brazil. 3 Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria UFSM, Palmeira das Missões-RS, Brazil. 4 Programa de Pós-Graduação em Ciências Ambientais. Universidade Comunitária da Região de Chapecó, Chapecó- SC, Brazil. * Corresponding author adenomera@gmail.com Figure 1. Map showing the study site in the state of Santa Catarina, Southern Brazil.

2 288 Karoline Ceron et al. Figure 2. Sampling sites in the Parque Estadual da Serra Furada, Orleans and Grão-Pará municipalities, Santa Catarina state, Brazil. Where (A) Swamp, (B) Forest, (C) Stream and (D) Dry stream. which originally covered 31% of Santa Catarina, with latitudinal and altitudinal variations, a high rate of rainfall, constant temperatures throughout the year (Klein, 1978; IBGE, 2012), and a great diversity, the result of those characteristics. These highly fragmented remnants are composed of pioneer and secondary plant species (Schorn et al., 2012; Vibrans et al., 2013). In the south of Santa Catarina, the montane rainforest is under pressure from agricultural activities, livestock, and the presence of cities and roads, which contributes greatly to the fragmentation and isolation (Sevegnani et al., 2013). Although amphibians play an important role in the functioning of ecosystems, this importance is not widely recognized as it is for other groups (e.g., mammals and birds) (Cunha & Rego, 2005). Information about the abundance and richness of amphibians is very important to understand population fluctuations (Lucas, 2008). Regarding amphibians, large areas still need inventories and many localities have been investigated by subsampling (Silvano & Segalla, 2005). Studies in the Santa Catarina state are incipient and lack information in all territories except on the western and central coasts (Garcia, 1996; Garcia & Vinciprova; 1998; Garcia et al., 2003; Lucas & Fortes, 2008; Lingnau, 2009; Lucas & Garcia, 2011; Lucas & Marocco, 2011; Bastiani et al., 2012; Bastiani & Lucas, 2013), while the southern region presents few studies (Ceron et al., 2016). The aim of this study is to characterize the anuran community, including species richness, taxonomic distinctness, constancy of occurrence, and reproductive modes, in sites of Atlantic Forest in Parque Estadual da Serra Furada, southern Santa Catarina, and southern Brazil. Material and Methods Study site The study was conducted in the Parque Estadual da Serra Furada (PAESF), municipalities of Orleans e Grão- Pará, in southern Santa Catarina state, southern Brazil (28º S, 49º W). Altitudes ranged from 360 to 1000 m (Figure 1).

3 Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil 289 The vegetation comprises remnants of submontane, montane, and high montane tropical rainforest (IBGE, 2012) at different degrees of conservation, ranging from the initial stage to the advanced stage of succession (FATMA, 2010). The climate, according to the Köppen classification system, is Cfa (Alvares et al., 2013) with average temperatures ranging from 17.0 to 19.3 C and minimum and maximum averages ranging from 12.0 to 15.1 C and from 23.4 to 25.9 C, respectively. Annual precipitation ranges from 1200 to 1700 mm, with rain events well-distributed throughout the year (Alvares et al., 2013). Data collection Field sampling was conducted monthly, during two consecutive days from August 2014 to July 2015 by active search (Crump, 1971), and visual and acoustic encounters (Zimmerman, 1994) at six distinct sites: swamp (n = two), track into the forest (n = two), and stream (n = two) (Figure 2). Sampling was conducted between 15:00 and 00:00 h, totalling 144 h of sampling. Each site was sampled three times on each sampling occasion, using a standardized sampling protocol for all areas. All species seen or heard were recorded. Habitats were also visited ad libitum during the day, on separate dates from samplings, to register casual daytime activities. When required, specimens were collected and deposited in the Museu de Zoologia Profª. Morgana Cirimbeli Gaidzinski (MUESC) at UNESC University, Criciúma municipality, state of Santa Catarina, Brazil. The individuals were manually captured, anesthetized and killed with a 5% lidocaine paste, then fixed in 10% formalin and preserved in 70% alcohol. Acoustic recordings were deposited in the Fonoteca Neotropical Jacques Vielliard (FNJV). The swamps are situated in open areas and are characterized by herbaceous vegetation, influenced by pasture and livestock. They have sizes of 345 m² and 315 m² with altitudes varying from 505 m to 600 m. Forest areas consist of tracks (360 m and 315 m) of medium successional stage on different altitudes (477 m and 815 m, respectively), evidenced by the high density of bromeliads. The streams are inserted into forests of medium/advanced successional stage, with a presence of herbaceous plants, such as Heliconia farinosa Raddi and Calathea monophylla (Vell.) Koernicke, in the riparian zone. The streams have tracks of 500 and 735 m in length, situated at 515 and 700 m altitude, and are influenced by the higher rainfall period, with a greater depth of water in the spring and summer. One stream (735 m in length) remains mainly dry in winter and autumn. Data analysis Sampling efficiency was evaluated by a species accumulation curve, constructed from the matrix of monthly data collected on species abundance. Calculations were performed based on 1000 randomizations using the non-parametric estimators Bootstrap and Jacknife 2 in the program EstimateS9.0 (Cowell, 2013). Each recorded species was classified according to the constancy of occurrence index (Dajoz, 1983) considered to be abundant (present in >50% of samples), common (present in 25% 50% of samples), or rare (present in <25% of samples). Reproductive modes of recorded frogs were classified according to the literature (Haddad & Prado, 2005; Haddad et al., 2008; Haddad et al., 2013). In order to verify the taxonomic distinctness between the sampled environments (track into the forest, stream, and swamp), the averages of taxonomic distinctness (Δ +) and the variation in taxonomic distinctness (Λ +) were calculated (Clarke & Warwick, 1998; 2001) with PRIMER software version 7.0 (PRIMER-E Ltd.). Results Twenty-seven species were recorded, belonging to nineteen genera and nine families (Table 1; Figure 3). Hylidae (13 spp., 48.4%) was the most represented family, followed by Leptodactylidae (four spp., 18.5%) and Bufonidae (three spp., 11.1%). The other families (Brachycephalidae, Centrolenidae, Hemiphractidae, Hylodidae, Microhylidae, and Odontophrynidae) were represented by one species each. Most species in this study were classified as abundant (n = 13), followed by common (n = nine) and rare species (n = five) (Table 1). Thirteen reproductive modes were observed (Figure 4), with exotrophic tadpoles in still water (mode 1) being the most frequent mode. Nine of the 27 studied species (33%) had this reproductive mode. The species accumulation curve showed that the sampling effort was sufficient to register 96.1% of species potentially present in the study area, according to the Bootstrap estimator (Figure 5). The areas with the highest species richness were swamps (n = 19 species), followed by streams (n = 15 species), and tracks into the forest (n = 10) (Table 1). The taxonomic distinctness values (Δ +) and variation in taxonomic distinctness (Λ +) for all environments were distributed within the limits of the 95% confidence

4 290 Karoline Ceron et al. Figure 3. Some anurans recorded on the six sampling sites in Parque Estadual da Serra Furada, SC, from August 2014 to July 2015: (A) Ischnocnema henselii, (B) Dendrophryniscus berthalutzae, (C) Rhinella abei, (D) Rhinella icterica, (E) Vitreorana uranoscopa, (F) Fritziana aff. fissilis, (G) Aplastodiscus ehrhardti, (H) Aplastodiscus perviridis, (I) Bokermannohyla hylax, (J) Dendropsophus nahdereri, (K) Boana bischoffi, (L) Boana faber, (M) Boana marginata, (N) Phyllomedusa distincta, (O) Ololygon catharinae, (P) Scinax fuscovarius, (Q) Scinax granulatus, (R) Scinax perereca, (S) Trachycephalus mesophaeus, (T) Hylodes meridionalis, (U) Leptodactylus gracilis, (V) Leptodactylus latrans, (X) Physalaemus nanus and (Z) Proceratophrys boiei. interval (Figure 6). Despite the track into the forest having shown less richness, it presented values of taxonomic distinctness and variation in taxonomic distinctness of species in the average of 95% probability funnels. However, despite the swamp having shown the highest richness, it had the lowest value of taxonomic distinctness of all the environments analyzed. Discussion The 27 species recorded in the present study corresponded to 20% of the 135 species listed for Santa Catarina state, considering Lucas (2008), Ribeiro et al. (2015), and more recent studies, as well as approximately 5.1% of the 529 recorded species in the Atlantic Forest (Haddad et al., 2013). The species

5 Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil 291 Figure 3. Continued. accumulation curve has stabilized, indicating that sampling was sufficient to record most species present in the area, and few additional species would be added with increased sampling effort. Still, the species accumulation curve rarely stabilizes fully, especially in tropical ecosystems (Santos, 2003). Hylidae was the richest family, with 13 species, confirming the richness pattern of this family in Neotropical assemblages (Both et al., 2008; Lucas & Fortes, 2008; Wachlevski et al., 2014). The large proportion of hylids may be related to the large number of vocalization sites available, as the various strata of vegetation can be exploited by these arboreal amphibians (Kopp & Eterovick, 2006; Afonso & Eterovick, 2007) and the great number of related species in this family (Segalla et al., 2016). The high number of species classified as constants (n = 13) was due to the abundant presence of anurans with large thermal tolerance (e.g., Boana bischoffi) and the frequent presence of anurans in forest environments (streams and tracks into the forests), where the climate is more stable in cooler months (Holling, 1973). Among the species considered rare are those with explosive

6 292 Karoline Ceron et al. Table 1. Anurans recorded in six sampling sites in Parque Estadual da Serra Furada, SC, between August 2014 and July Where: OF = occurrence frequency; CI = constancy index (Dajoz, 1983), C (Common species), A (abundant species) and R (rare species). * Endangered species according CONSEMA (2011). Taxa RM OF (%) CI Swamp Forest Stream Brachycephalidae Ischnocnema henselii (Peters, 1872) A x x Bufonidae Dendrophryniscus berthalutzae Izecksohn, A x x Rhinella abei (Baldissera-Jr,Caramaschi & Haddad, 2004) 1 17 R x x Rhinella icterica (Spix, 1824) A x x Centrolenidae Vitreorana uranoscopa (Müller, 1924)* A x Hemiphractidae Fritziana aff. fissilis A x x Hylidae Aplastodiscus ehrhardti (Müller, 1924)* 5 75 A x x Aplastodiscus perviridis A. Lutz in B. Lutz, C x Boana bischoffi (Boulenger, 1887) A x x x Boana faber (Wied-Neuwied, 1821) 4 50 A x x Boana marginata (Boulenger, 1887)* 2 92 A x x x Bokermannohyla hylax (Heyer, 1985) 4 92 A x x Dendropsophus nahdereri (B. Lutz &Bokermann, 1963) 1 25 C x Ololygon catharinae (Boulenger, 1888) 1 42 C x Phyllomedusa distincta A. Lutz in B. Lutz, C x x Scinax fuscovarius (A. Lutz, 1925) 1 17 R x x Scinax granulatus (Peters, 1871) 1 25 C x x Scinax perereca Pombal, Haddad &Kasahara, A x Trachycephalus mesophaeus (Hensel, 1867) 1 8 R x Hylodidae Hylodes meridionalis (Mertens, 1927) 3 58 A x Leptodactylidae Adenomera araucaria Kwet & Angulo, R x Leptodactylus gracilis (Duméril& Bibron, 1841) C x Leptodactylus latrans (Steffen, 1815) R x x Leptodactylus plaumanni Ahl, C x Physalaemus nanus (Boulenger, 1888) A x Microhylidae Elachistocleis bicolor (Valenciennes in Guérin-Menéville, (1838) 1 25 C x Odontophrynidae Proceratophrys boiei (Wied-Neuwied, 1825) 2 33 C x x Richness reproduction (T. mesophaeus), which reproduce for a few days, often at high densities (Wells, 1977), and litter species (A. araucaria), which are more difficult to see with the methodologies used in this study. Among the 27 reproductive modes recorded in the Atlantic Forest (Haddad & Prado, 2005), 13 were recorded in this study. The diversity of the recorded reproduction modes is a feature of the amphibian

7 Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil 293 Figure 4. Some reproductive modes recorded in Parque Estadual da Serra Furada, SC, from August 2014 to July 2015.Where (A) Eggs of Rhinella icterica and (B) Boana marginata (Mode 2 eggs and exotrophic tadpoles in running water) and (C) eggs of Vitreorana uranoscopa (Mode 25 after hatching, exotrophic tadpoles that drop in running water). assemblage of the Atlantic Forest, resulting from the structural characteristics of different areas, which provide different microenvironments (Haddad & Prado, 2005). This allows for a wide range of reproduction modes, from the most simplistic (mode 1 eggs and exotrophic tadpoles in still water) up to the most demanding modes, such as mode 8 (eggs and endotrophic tadpoles in water accumulated in tree holes or in aerial plants), mode 2 (eggs and exotrophic tadpoles in running water), and mode 25 (after hatching, exotrophic tadpoles that drop into running water) (Haddad & Prado, 2005). Reproductive mode 1, the most frequent in this study, is the most widespread mode among amphibians and the one most often recorded in the Atlantic Forest (Pombal & Haddad, 2005; Conte & Rossa-Feres, 2007; Santos et al., 2008). None of the species recorded in this study are cited on the Brazilian Official Threatened Fauna Species List (MMA, 2014); however, three species were listed in Figure 5. Curve of species accumulation, based on the monthly occurrence of anurans, recorded on six sampling sites in Parque Estadual da Serra Furada, SC, from August 2014 to July Legend Solid black line with asterisk: Observed richness, Solid black line with square: Jacknife2 and Solid black line with rhomb: Bootstrap. Figure 6. The 95% probability funnels (dotted and solid line) for taxonomic distinctness (Delta +) (A) and variation in taxonomic distinctness (Lambda +) (B) for anurans recorded on three sampling sites in Parque Estadual da Serra Furada, SC, from August 2014 to July Legend F (track into the forest), S (swamp), and ST (stream).

8 294 the Official List of Endangered Fauna Species of Santa Catarina as Vulnerable (VU): V. uranoscopa, A. ehrhardti and B. marginata (CONSEMA, 2011). Vitreorana uranoscopa was found vocalizing in the riparian forest near to streams of clean water. In addition, we observed this species showing visual communication (limb lifting as answers to the calls of others males) during the study. Boana marginata was found in streams and swamps of clean water on the rocks or in herbaceous vegetation, calling mainly in cooler months. Aplastodiscus ehrardti was classified as abundant (in relation to its presence in samples), but this species was found at low frequencies, often vocalizing in the tree canopy close to streams. The populations of A. ehrardti are in decline, mainly because of deforestation and water pollution (Eterovick et al., 2005; Silvano & Segalla, 2005). Some studies in Brazil have shown that open areas have greater richness in relation to predominantly forest environments (Afonso & Eterovick, 2007; Lucas & Marocco, 2011; Bastiani & Lucas, 2013; this study). This pattern may be related to the evolution of neotropical anurans, which favor species that breed in lentic environments of open areas, a result of different pressures (e.g., predators, resources, competition, and disturbances) (Zimmerman & Simberloff, 1996; Hocking & Semlitsch, 2008). Because taxonomic distinctness analysis does not give much value to the richness of species but to the taxonomic hierarchy derived from it, areas with low richness, such as tracks into the forest, had high taxonomic distinctness. This result reinforces the importance of forest habitats for the conservation of amphibians, which are home to specialized and unique species. Despite the greater richness in the swamp area, it showed low taxonomic distinctness between species. Warwick & Clarke (1998) suggest that environments with some kind of degradation tend to have a lower average taxonomic distinctness than non-degraded sites. Despite its low taxonomic distinctness relative to other environments, the swamp showed high variation in taxonomic distinctness, which measures the evenness that rates are distributed on the taxonomic tree. This fact may be related to great richness in the swamp, well distributed between genera and families, in relation to other environments (Clarke & Warwick, 2001). Basic studies are very important for the characterization of the biodiversity in Santa Catarina state, especially in conservation units. At the same time, it is important to know the status of conservation and threatened species. However, there is still a need for long-term studies involving communities and populations, checking for possible declines and real threats to amphibians. Acknowledgements. KC is grateful to the Parque Estadual da Serra Furada managers and FATMA (Santa Catarina Environmental Foundation) for allowed the research on PAESF, CAPES for scholarship, Luis Fernando Rocha Ugioni for valuable suggestions on the manuscript and André Freitas, Beatriz Fernarndes, Caio Feltrin, Daniela Bôlla, Diego Pavei, Fábio Hammen Lhanos, Humberto Martins, João Gava-Just, Marina Olivo and Rafael Romagna for the help on fieldwork. References Karoline Ceron et al. Afonso, L.G., Eterovick, P.C. (2007): Spatial and temporal distribution of breeding anurans in streams in southeastern Brazil. Journal of Natural History 41: Alvares, C.A., Stape, J.L, Sentelhas, P.C., de Moraes, G., Leonardo, J., Sparovek, G. (2013): Köppen s climate classification map for Brazil. Meteorologische Zeitschrift 22(6): Bastiani, V. I. M., Garcia, P. C., Lucas, E. M. 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10 296 Sevegnani, L., Schroeder, E., Blumenau, Brazil, Edifurb. Vibrans, A., Sevegnani, L., Gasper, A.L., Lingner, D.V. (2012): Inventário Florístico Florestal de Santa Catarina, Vol. I, Diversidade e conservação dos remanescentes florestais. Blumenau, Brazil, Edifurb. Vibrans, A.C., McRoberts, R.E., Lingner, D.V., Nicoletti, A.L., Moser, P. (2013): Extensão original e remanescentes da Floresta Ombrófila Densa em Santa Catarina. In: Inventário Florístico Florestal de Santa Catarina Vol IV: Floresta Ombrófila Densa, p , Vibrans, A., Sevegnani, L., Gasper, A.L., Lingner, D.V., Blumenau, Brazil, Edifurb. Wachlevski, M., Erdtmann, L.K., Garcia, P.C.A. (2014): Anfíbios anuros em uma área de Mata Atlântica da Serra do Tabuleiro, Santa Catarina. Biotemas 27(2): Wells, K.D. (1977): The social behavior of anuran amphibians. Animal Behaviour 25: Zar, J.H Biostatistical Analysis. New Jersey, USA, Prentice Hall International. Zimmerman, B., Simberloff, D. (1996): An historical interpretation of habitat use by frogs in a Central Amazonian forest. Journal of Biogeography 23(1): Zimmerman, B.L. (1994): Audio strip transects. In: Measuring and monitoring biological diversity: standard methods for amphibians, p , Heyer, R., Donnelly, M., Foster, M., McDiarmid, R. Washington, USA, Smithsonian Institution Press. Appendix 1 Voucher list Karoline Ceron et al. The reference specimens can be found at MUESC under numbers Dendrophryniscus berthalutzae (MUESC 1246, 1247), Vitreorana uranoscopa (MUESC 1251), Fritziana aff. fissilis (MUESC 1253), Scinax granulatus (MUESC 1257) and Hylodes meridionalis (MUESC 1258). Acoustic recordings can be found at Fonoteca Neotropical Jacques Vielliard (FNJV) under numbers: Aplastodiscus ehrhardti (FNJV 32396), Bokermannohyla hylax (FNJV 32397), Boana bischoffi (FNJV 32398), Boana marginata (FNJV 32399), Ischnocnema henselii (FNJV 32400), Adenomera araucaria (FNJV 32401), Leptodactylus plaumanni (FNJV 32402), Physalaemus nanus (FNJV 32403), Trachycephalus mesophaeus (FNJV 32404) and Vitreorana uranoscopa (FNJV 32405). Accepted by Diego Santana