Herpetology Notes, volume 9: 15-21 (2016) (published online on 17 February 2016)

Anuran richness in remnants of Araucaria Forest, Paraná, Brazil

Peterson T. Leivas1,* and Cristiane Hiert2

Abstract. The State of Paraná is located in the Atlantic Forest biome and its Anuran diversity has not been sufficiently explored. Our goal was to describe the composition of anuran species in areas of Araucaria Forest in the county of Campo Largo, state of Paraná, Brazil. We made the list of species based on field records (32 sampling events) through seasonal sampling in five areas of Campo Largo. We registered 21 species distributed in seven families and the registered richness represents 15% of the species known for the state and 4% of the total anuran richness known for the Atlantic Forest (529 species).

Introduction population decline and species loss (Young et al., 2001; Stuart et al., 2004; Silvano and Segalla, 2005). The threat The Neotropical region holds the greatest richness of on anurans in this biome is related to anthropogenic anurans in the world, and within the region, Brazil is the factors that lead to habitat destruction (e.g. real estate country with the highest richness of species (988 species) occupation, agricultural expansion) and degradation of (Segalla et al., 2014). Of these, 40% were described in native biota (e.g. species introduction and presence of the last 26 years (Pyron and Wiens, 2011). The increase pathogens) (Silvano and Segalla, 2005). in the knowledge of species, although associated with a Of the forest formations of the Atlantic Forest in the number of factors, lies mainly in the survey of unstudied state of Paraná, the Araucaria Forest is reduced to less places and the development of studies. than 0.8% of its original area (Morellato and Haddad, From the brazilian biomes, the Atlantic Forest biome 2000), and knowledge on the anuran fauna of the first is considered to be the most diverse with 529 species plateau is restricted to a few locations in the east slope of of anurans, from which 60% are endemic (Haddad et the Serra do Mar mountains (e.g. Conte and Machado, al., 2013). However, it is believed that data on richness 2005; Conte and Rossa-Feres, 2006, 2007; Cunha et al., and endemism of this biome is underestimated, due 2010). Considering the threat and the gap in knowledge to samplings gaps and lack of knowledge on the across much of the state, we aimed to describe the taxonomy of the species (Haddad et al., 2013). Despite composition of anuran species in areas of Araucaria of the scarcity of knowledge on the diversity and the Forest in Campo Largo, Paraná, Brazil. importance of this biome for the maintenance of the brazilian biodiversity, the anuran fauna of the Atlantic Material and Methods Forest is under intense threat, with increasing records of We conducted the study in five points of Araucaria Forest in Campo Largo, Paraná, Brazil. The region is located in the first plateau of Paraná, about 920m of altitude, has Subtropical Temperate climate classified 1 Universidade Federal do Paraná (UFPR). Departamento de as Cfb according to Koppen (Maack, 2012). Zoologia. Caixa postal 19020. CEP 81531-980. Curitiba, PR, The regional landscape is a mosaic of forest fragments Brasil. with areas of agriculture, livestock and recreation 2 Universidade Estadual do Centro-Oeste (UNICENTRO). Departamento de Biologia,. Caixa postal 3010, 85040-080. activities. We selected five sampling areas, based on Guarapuava, Paraná, Brazil. the characteristics of the vegetation structure, presence *Corresponding author e-mail: [email protected] of hydric resources and degree of anthropization 16 Peterson T. Leivas & Cristiane Hiert

2010, and February (summer) and May (autumn) of 2011. In each season, we sampled during eight days, so that each area was inspected during two nights. The areas 2 and 3 were inspected during the same nights due to the proximity and low environment complexity of the areas; still, the data will be presented separately. The sampling effort for each area was of eight nights (32 sampling events). We used the methods of visually and aurally oriented active search (Crump and Scott, 1994) using four pre- determined transects in forest and reproductive sites (Crump and Scott, 1994). Two people performed the methods during twilight and night (17:30 - 22:30h). The transects and the breeding sites were sampled during 2 hours/day each, totaling an effort of 4 hours/day each area and 20h of sampling per field season/person. For some species the morphological diagnosis was confirmed by analysis of the advertisement calls described in the literature. The species were: henselii according Gehara et al. (2013), Vitreorana uranoscopa according Haga et al. (2014) Figure 1. Map showing the five studied areas, in Araucaria and Physalaemus lateristriga according Cassini et al. Forest phytogeographic domain, in the county of Campo (2010). Vocalizations were recorded with a external Largo, Paraná, Brazil. directional microphone (Yoga HT 81), coupled to a H2n digital audio recorder positioned at a maximum distance of 1 m to the calling males. We analyzed the calls using Raven 1.2 software (16 bits of resolution, 44 kHz of frequency sampling, FFT and frame length of 256 samples). (disturbance), so that: Area 1 (25 º 23’49 “S, 49 º 31’51” To evaluate the sampling, we performed a curve of W): a slightly disturbed area comprising a permanent sampling sufficiency based on the number of species pond with marginal shrubby and woody vegetation, recorded during the sampling days, considering all the two swamps with shrubby vegetation in the interior, a stream and a river inside the forest fragment; Area 2 (25 º 24’38 “S, 49 º 29’35” W): an disturbed area with two permanent ponds with marginal woody vegetation and a small forest fragment; Area 3 (25 º 25’40 “S,49 º 28’36” W): an area in the interior of the forest fragment with a predominance of Paraná Pine tree (Araucaria angustifolia), with two small streams and a swamp region with shrubby and herbaceous vegetation; Area 4 (25 º 26’01 “S, 49 º 28’24” W): an area of wetland slightly disturbed with predominant shrubby and woody vegetation, consisting on flooded soil with several watercourses (streams); Area 5 (25 º 29’48 “S, 49 º 23’22” W): area in the borders of a dam, comprising a great reservoir, two permanent ponds bordered by shrubby vegetation and forest fragment with a stream within it (Figure 1). Figure 2. Species accumulation curve, obtained in the 32 field We sampled the areas in four seasons during the sampling days for the survey of anuran fauna of Campo Largo, months of August (winter) and November (spring) of PR. Anuran richness in remnants of Araucaria Forest, Paraná, Brazil 17 sampled areas. We used the Jackknife II estimator to day). However, the curve did not stabilized completely, verify if the total richness registered in the field is close indicating an increase in the number of species with the to the estimated richness (Gotelli and Cowell, 2010). The increase of the sampling effort (Figure 2). The recorded estimates were calculated from 1000 randomizations in richness was 21 species, which is close to the estimated the software EstimateS version 8.2.0 (Colwell, 2009). richness (26 species). To make the species list, we used the nomenclature The species were distributed into seven families: proposed by Frost (2015). Species diversity to each (one species), Bufonidae (two species), community was estimated by Fisher’s alpha diversity Centrolenidae (one species), Hylidae (10 species), index in the PAST program version 2.17b (Hammer et Leptodactylidae (five species), Odontophrynidae (one al., 2001). species) and Ranidae (one species) (Table 1 and Figure 3). Eleven species (50% of the species) occurred in Results more than two areas, five species (23% of the species) The curve of sampling sufficiency tends to stabilize occurred in two areas and six species (27% of the species) from the third sampling (between the 17th and 24th occurred in only one area (Table 1). The areas with the

Table 1. Table of anuran species recorded in Campo Largo within the vegetation domain of Araucaria Forest.

 Area Sampling Family/ Species 1 2 3 4 5 1 2 3 4 Brachycephalidae Ischnocnema henselii (Peters, 1870) Bufonidae Rhinella abei (Baldissera-Jr, Caramaschi & Haddad, 2004) R. icterica (Spix, 1824) Centrolenidae Vitreorana uranoscopa (Müller, 1924) Hylidae Aplastodiscus albosignatus (A.Lutz & B. Lutz, 1938) A. perviridis Lutz, 1950 Dendropsophus minutus (Peters, 1872) Hypsiboas albopunctatus (Spix, 1824) H. bischoffi (Boulenger, 1887) H. faber (Wied-Neuwied, 1821) H. prasinus (Burmeister, 1856) Scinax perereca Pombal, Haddad & Kasahara, 1995 S. fuscovarius (Lutz, 1925) Phyllomedusa distincta Lutz, 1950 Leptodactylidae Leptodactylus latrans (Steffen, 1815) L. notoaktites Heyer, 1978 Physalaemus cuvieri Fitzinger, 1826 P. aff. gracilis P. lateristriga (Steindachner, 1864) Odontophrynidae Proceratophrys boiei (Wied-Neuwied, 1824) Ranidae Lithobates catesbeianus (Shaw, 1802) TOTAL 19 11 8 11 14 13 18 19 8 18 Peterson T. Leivas & Cristiane Hiert

Figure 3. Some of the anuran species registered in Campo Largo, PR. A = Rhinella abei; B = R. icterica; C = Vitreorana uranoscopa; D = Aplastodiscus albosignatus; E = A. perviridis; F = Hypsiboas albopunctatus; G = Dendropsophus minutus; H = H. bischoffi; I = H. faber; J = H. prasinus; L = S. fuscovarius; M = Phyllomedusa distincta; N = Leptodactylus latrans and O = L. notoaktites. Photo by Peterson T. Leivas and Cristiane Hiert. Anuran richness in remnants of Araucaria Forest, Paraná, Brazil 19

Figure 3. Continued.

greatest richness of species were 1 and 5, with 19 and area 5 (α = 3.07±0.5), area 2 (α = 2.74±1.3) and area 3 14 species respectively. Areas 2 and 4 have richness (α = 2.02±1.8) respectively of 11 species each, and area 3 has the lowest richness with eight species (Table 1). The biological diversity the areas were area 1 (α = 4.57 ±0.3), area 4 (α = 3.75 ±1.7), 20 Peterson T. Leivas & Cristiane Hiert

Discussion chytridiomycosis, a disease pointed as one of the main threats to (Schloegel et al., 2009). The richness of species represents 15% of the species In this study we provide data of basic species inventory registered for the state of Paraná (n = 142) (Conte et al., from five sites in Araucaria Forest southern Brazil. Our 2010) and is lower than the known richness for areas results increased the know distribution records of anura with the same phytogeographic and climatic domain, in for Araucaria Forest. Also we recorded L. catesbeianus, the counties of Tijucas do Sul (23 species) (Conte and species that can directly impact native species through Machado, 2005) and Fazenda Rio Grande (32 species) predation (Leivas et al., 2012). Together these data (Conte and Rossa-Ferres, 2007). Ours results (curve of reinforces the need of inventory-based actions, as these sampling sufficiency and richness estimator) indicates data are the basic unity of biodiversity. this richness is underestimated occurring an increase in richness with performing greater sampling effort. Acknowledgements. Peterson T. Leivas received a doctoral Small differences in regional phytogeographic patterns Grant from the Coordenação de Aperfeiçoamento de Pessoal de can promote differences in local richness of species Nivel Superior - CAPES. (Huston, 1994; Conte and Rossa-Ferres, 2007; Cunha et al., 2010; Silva et al., 2012). Thus, the areas studied in References Fazenda Rio Grande and Tijucas do Sul are located in regions of ecotone, that present greater environmental Armstrong, C.G., Conte, C.E. (2010): Taxocenose de anuros heterogeneity when compared to non-ecotone regions. (Amphibia: Anura) em uma área de Floresta Ombrófila Densa no sul do Brasil. Biota neotropica 10(1): 39-46. 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Accepted by Clarissa Canedo