Herpetology Notes, volume 10: 287-296 (2017) (published online on 29 May 2017)

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

Karoline Ceron1,2,*, Elaine Maria Lucas 3,4 and Jairo José Zocche1

Abstract. We provide a list of 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 of anurans belonging to nine families were recorded on six distinct sites between 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 biome, emphasizing the importance of these environments in conservation.

Keywords: Amphibians, Atlantic Forest, biodiversity, protected area, Neotropical region

Introduction 2012). Today, the remnants cover less than 13% of the original territory (Fundação SOS Mata Atlântica & Brazil is one of the countries with the highest richness INPE, 2015). of amphibians in the world, with 1080 species (Segalla Santa Catarina is a south Brazilian state inserted et al., 2016). The Atlantic Forest is an endangered in the Atlantic Forest area with less than 30% of its morphoclimatic domain, classified as a hotspot (Myers original cover, with a predominance of vegetation et al., 2000), with 529 species of anurans (Haddad in the medium and advanced successional stages et al., 2013), one of the greatest biodiversity and (Sevegnani & Schroeder, 2013). Approximately 80% of endemism areas of the world. The original coverage the fragments are smaller than 50 ha, revealing a high of this morphoclimatic domain included almost the degree of fragmentation of the remaining forest of the entire Brazilian coast; from the northern of Rio Grande State (Vibrans et al., 2012). The study area comprises do Norte state to north of Rio Grande do Sul (IBGE, 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. Figure 1. Map showing the study site in the state of Santa * Corresponding author e-mail: [email protected] Catarina, Southern Brazil. 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 Santa Catarina state are incipient and lack information latitudinal and altitudinal variations, a high rate of in all territories except on the western and central coasts rainfall, constant temperatures throughout the year (Garcia, 1996; Garcia & Vinciprova; 1998; Garcia et (Klein, 1978; IBGE, 2012), and a great diversity, the al., 2003; Lucas & Fortes, 2008; Lingnau, 2009; Lucas result of those characteristics. These highly fragmented & Garcia, 2011; Lucas & Marocco, 2011; Bastiani et remnants are composed of pioneer and secondary plant al., 2012; Bastiani & Lucas, 2013), while the southern species (Schorn et al., 2012; Vibrans et al., 2013). In region presents few studies (Ceron et al., 2016). The aim the south of Santa Catarina, the montane rainforest is of this study is to characterize the anuran community, under pressure from agricultural activities, livestock, including species richness, taxonomic distinctness, and the presence of cities and roads, which contributes constancy of occurrence, and reproductive modes, in greatly to the fragmentation and isolation (Sevegnani et sites of Atlantic Forest in Parque Estadual da Serra al., 2013). Furada, southern Santa Catarina, and southern Brazil. Although amphibians play an important role in the functioning of ecosystems, this importance is not widely Material and Methods recognized as it is for other groups (e.g., mammals and Study site birds) (Cunha & Rego, 2005). Information about the abundance and richness of amphibians is very important The study was conducted in the Parque Estadual da to understand population fluctuations (Lucas, 2008). Serra Furada (PAESF), municipalities of Orleans e Grão- Regarding amphibians, large areas still need inventories Pará, in southern Santa Catarina state, southern Brazil and many localities have been investigated by sub- (28º11’07”77S, 49º23’31”80W). Altitudes ranged from sampling (Silvano & Segalla, 2005). Studies in the 360 to 1000 m (Figure 1). Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil 289

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

interval (Figure 6). Despite the track into the forest Discussion having shown less richness, it presented values of The 27 species recorded in the present study taxonomic distinctness and variation in taxonomic corresponded to 20% of the 135 species listed for distinctness of species in the average of 95% probability Santa Catarina state, considering Lucas (2008), funnels. However, despite the swamp having shown the Ribeiro et al. (2015), and more recent studies, as well highest richness, it had the lowest value of taxonomic as approximately 5.1% of the 529 recorded species in distinctness of all the environments analyzed. the Atlantic Forest (Haddad et al., 2013). The species Anurans of Parque Estadual da Serra Furada, Santa Catarina, Southern Brazil 291

Figure 3. Continued.

accumulation curve has stabilized, indicating that various strata of vegetation can be exploited by these sampling was sufficient to record most species present arboreal amphibians (Kopp & Eterovick, 2006; Afonso in the area, and few additional species would be added & Eterovick, 2007) and the great number of related with increased sampling effort. Still, the species species in this family (Segalla et al., 2016). accumulation curve rarely stabilizes fully, especially The high number of species classified as constants in tropical ecosystems (Santos, 2003). Hylidae was the (n = 13) was due to the abundant presence of anurans richest family, with 13 species, confirming the richness with large thermal tolerance (e.g., Boana bischoffi) and pattern of this family in Neotropical assemblages (Both the frequent presence of anurans in forest environments et al., 2008; Lucas & Fortes, 2008; Wachlevski et al., (streams and tracks into the forests), where the climate 2014). The large proportion of hylids may be related to is more stable in cooler months (Holling, 1973). Among the large number of vocalization sites available, as the the species considered rare are those with explosive 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 2015. 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) 23 92 A x x Bufonidae Dendrophryniscus berthalutzae Izecksohn, 1994 “1993” 8 50 A x x Rhinella abei (Baldissera-Jr,Caramaschi & Haddad, 2004) 1 17 R x x Rhinella icterica (Spix, 1824) 2 100 A x x Centrolenidae Vitreorana uranoscopa (Müller, 1924)* 25 58 A x Hemiphractidae Fritziana aff. fissilis 36 58 A x x Hylidae Aplastodiscus ehrhardti (Müller, 1924)* 5 75 A x x Aplastodiscus perviridis A. Lutz in B. Lutz, 1950 5 25 C x Boana bischoffi (Boulenger, 1887) 1 100 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, 1950 24 25 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, 1995 1 50 A x Trachycephalus mesophaeus (Hensel, 1867) 1 8 R x Hylodidae Hylodes meridionalis (Mertens, 1927) 3 58 A x Leptodactylidae Adenomera araucaria Kwet & Angulo, 2003 32 17 R x Leptodactylus gracilis (Duméril& Bibron, 1841) 30 25 C x Leptodactylus latrans (Steffen, 1815) 11 17 R x x Leptodactylus plaumanni Ahl, 1936 30 33 C x Physalaemus nanus (Boulenger, 1888) 11 50 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 13 - - 19 10 15

reproduction (T. mesophaeus), which reproduce for a Among the 27 reproductive modes recorded in the few days, often at high densities (Wells, 1977), and litter Atlantic Forest (Haddad & Prado, 2005), 13 were species (A. araucaria), which are more difficult to see recorded in this study. The diversity of the recorded with the methodologies used in this study. reproduction modes is a feature of the amphibian 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 one most often recorded in the Atlantic Forest (Pombal structural characteristics of different areas, which provide & Haddad, 2005; Conte & Rossa-Feres, 2007; Santos different microenvironments (Haddad & Prado, 2005). et al., 2008). This allows for a wide range of reproduction modes, None of the species recorded in this study are cited from the most simplistic (mode 1– eggs and exotrophic on the Brazilian Official Threatened Fauna Species List tadpoles in still water) up to the most demanding modes, (MMA, 2014); however, three species were listed in 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

Figure 5. Curve of species accumulation, based on the Figure 6. The 95% probability funnels (dotted and solid line) monthly occurrence of anurans, recorded on six sampling sites for taxonomic distinctness (Delta +) (A) and variation in in Parque Estadual da Serra Furada, SC, from August 2014 to taxonomic distinctness (Lambda +) (B) for anurans recorded July 2015. Legend – Solid black line with asterisk: Observed on three sampling sites in Parque Estadual da Serra Furada, richness, Solid black line with square: Jacknife2 and Solid SC, from August 2014 to July 2015. Legend – F (track into the black line with rhomb: Bootstrap. forest), S (swamp), and ST (stream). 294 Karoline Ceron et al. the Official List of Endangered Fauna Species of Santa involving communities and populations, checking for Catarina as Vulnerable (VU): V. uranoscopa, A. ehrhardti possible declines and real threats to amphibians. and B. marginata (CONSEMA, 2011). Vitreorana uranoscopa was found vocalizing in the riparian forest Acknowledgements. KC is grateful to the Parque Estadual near to streams of clean water. In addition, we observed da Serra Furada managers and FATMA (Santa Catarina this species showing visual communication (limb lifting Environmental Foundation) for allowed the research on PAESF, as answers to the calls of others males) during the study. CAPES for scholarship, Luis Fernando Rocha Ugioni for valuable suggestions on the manuscript and André Freitas, Beatriz Boana marginata was found in streams and swamps of Fernarndes, Caio Feltrin, Daniela Bôlla, Diego Pavei, Fábio clean water on the rocks or in herbaceous vegetation, Hammen Lhanos, Humberto Martins, João Gava-Just, Marina calling mainly in cooler months. 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Sevegnani, L., Schroeder, E., Blumenau, Brazil, Edifurb. Appendix 1 – Voucher list Vibrans, A., Sevegnani, L., Gasper, A.L., Lingner, D.V. (2012): Inventário Florístico Florestal de Santa Catarina, Vol. I, The reference specimens can be found at MUESC Diversidade e conservação dos remanescentes florestais. under numbers Dendrophryniscus berthalutzae Blumenau, Brazil, Edifurb. (MUESC 1246, 1247), Vitreorana uranoscopa (MUESC Vibrans, A.C., McRoberts, R.E., Lingner, D.V., Nicoletti, A.L., 1251), Fritziana aff. fissilis (MUESC 1253), Scinax Moser, P. (2013): Extensão original e remanescentes da Floresta granulatus (MUESC 1257) and Hylodes meridionalis Ombrófila Densa em Santa Catarina. In: Inventário Florístico (MUESC 1258). Florestal de Santa Catarina Vol IV: Floresta Ombrófila Densa, p. 25–33, Vibrans, A., Sevegnani, L., Gasper, A.L., Lingner, D.V., Acoustic recordings can be found at Fonoteca Blumenau, Brazil, Edifurb. Neotropical Jacques Vielliard (FNJV) under numbers: Wachlevski, M., Erdtmann, L.K., Garcia, P.C.A. (2014): Anfíbios Aplastodiscus ehrhardti (FNJV 32396), Bokermannohyla anuros em uma área de Mata Atlântica da Serra do Tabuleiro, hylax (FNJV 32397), Boana bischoffi (FNJV 32398), Santa Catarina. Biotemas 27(2):97–107. Boana marginata (FNJV 32399), Ischnocnema henselii Wells, K.D. (1977): The social behavior of anuran amphibians. (FNJV 32400), Adenomera araucaria (FNJV 32401), Behaviour 25:666–693. Leptodactylus plaumanni (FNJV 32402), Physalaemus Zar, J.H. 1999. Biostatistical Analysis. New Jersey, USA, Prentice Hall International. nanus (FNJV 32403), Trachycephalus mesophaeus Zimmerman, B., Simberloff, D. (1996): An historical interpretation (FNJV 32404) and Vitreorana uranoscopa (FNJV of use by frogs in a Central Amazonian forest. Journal of 32405). Biogeography 23(1):27–46. Zimmerman, B.L. (1994): Audio strip transects. In: Measuring and monitoring biological diversity: standard methods for amphibians, p. 92–96, Heyer, R., Donnelly, M., Foster, M., McDiarmid, R. Washington, USA, Smithsonian Institution Press.

Accepted by Diego Santana