Snake Assemblage from Serra Do Sudeste, Pampas Biome, Southern Brazil
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Herpetology Notes, volume 11: 733-745 (2018) (published online on 31 August 2018) Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil Arlete B. Outeiral1, Rafael L. Balestrin1,2, Lize H. Cappellari1,3, Thales de Lema1, and Vanda L. Ferreira4,* Abstract. Serra do Sudeste, located in Southern Campos and included in the Pampas biome, has a high biological importance in Brazil. The vegetation is made up of a mosaic of pasture transition zones and Semideciduous Seasonal Forest, with most of the area strongly threatened. In this context, the aim of the present study was to assess the diversity of local snake communities using several capture methods. Natural history data, activity patterns, habitat use, and the diet of some species are discussed. The snake community is made up of 33 species, representing more than one third of the known species for the state of Rio Grande do Sul, and the highest species richness is observed in areas influenced by temperate climates in neotropical regions. Bothrops pubescens (Cope, 1870) and Philodryas patagoniensis (Girard, 1858) had the highest relative abundance. The active search and resident collector methods were the best sampling methods for measuring species richness. Key words. Pampas, Campos Sulinos, census, natural history, species inventory Introduction that affect and maintain them (Stegen et al., 2013), and combinations thereof (Hurlbert and Jetz, 2007; Stegen Species composition, structure (abundance and and Hurlbert, 2011; Paglia et al., 2012). Although species richness), and function are essential attributes taxonomic studies on regional fauna are considered of biodiversity (Noss, 1990; Magurran, 2004) and important, relatively little is known about the diversity maintaining them are the basic objectives of global of Brazilian fauna (Lewinsohn and Prado, 2002), biodiversity conservation strategies (Wilson, 1992). which holds true for snakes. Although snakes represent Thus, conservation of biological diversity is based on 35% of all reptiles worldwide (Roll et al., 2017; Uetz, traditional diversity measurements, such as inventories, 2017) and more than 50% of Brazilian reptile species descriptions of natural history and ecology (Gaston, (Costa and Bérnils, 2015, 2018), with high variation 1996), and measurements of functional and phylogenetic in community composition and phylogenetic diversity diversity (Petchey and Gaston, 2006; Cavender-Bares et (Moura et al., 2017), they have been poorly studied. The al., 2009; Cianciaruso et al., 2009; Stegen and Hurlbert distribution of this diverse reptile group is fundamental 2011; Lopez et al., 2016), as well as factors and processes to understanding the determinants of biodiversity. Moreover, existing protected areas, biodiversity significance sites and global conservation schemes do not adequately represent reptiles (Roll et al., 2017). Conservation efforts for Campos Sulinos face great 1 Pontifícia Universidade Católica do Rio Grande do Sul, Faculdade de Biociências, Programa de Pós-graduação em challenges, as this ecosystem is neglected (Overbeck Zoologia, Av. Ipiranga, 6681, Partenon, CEP 90619-900, et al., 2007) and threatened on a global and local Porto Alegre, RS, Brazil. scale (Pillar and Vélez, 2010). It has high levels of 2 Fieldwork Consultoria Ambiental Ltda, Rua Gonçalves Dias, biodiversity (Boldrini, 2009) and endemism (Bencke, 729, Apto. 503, Seminário, CEP 80240-340, Curitiba, PR, 2009), but is experiencing alterations of its natural Brazil. ecosystems (Bencke, 2009; Pillar and Vélez, 2010; 3 Universidade da Região da Campanha, Rua General Osório, Oliveira et al., 2017). Thus, considering the region’s 522, CEP 96570-000, Caçapava do Sul, RS, Brazil. 4 Universidade Federal de Mato Grosso do Sul, Instituto de biological importance and the need to understand local Biociências, Laboratório de Pesquisa em Herpetologia, Cx.P. communities, the local snake species composition and 549, CEP 79070-900, Campo Grande, MS, Brazil. richness are described, and an annotated checklist for * Corresponding author. E-mail: [email protected] Campos Sulinos, located in Southern Brazil, is given. 734 Arlete B. Outeiral et al. Figure 1. Study site in the Serra do Sudeste region, Rio Grande do Sul, Brazil. Open circles indicate municipalities and circles with points indicate areas where the largest sampling effort was conducted. 1: (1) Encruzilhada do Sul, (2) Dom Feliciano, (3) Barão do Triunfo, (4) São Jerônimo, (5) Area 1, (6) Area 2. Datum WGS84. Materials and Methods gradually increasing altitudes from south to north, from less than 100 meters on the southern edge to over 600 Study site.—The study was conducted at Dom meters in the north (Rambo, 1994). The vegetation Feliciano, Encruzilhada do Sul, in the municipalities comprises a mosaic of transitional grassland and of São Jerônimo and Barão do Triunfo, at the Serra Semideciduous Seasonal Forest zones. The grassland do Sudeste, in the state of Rio Grande do Sul (RS), formation exhibits a similar physiognomy to the Brazil. The largest sampling effort was conducted at Savannah, which, when invaded by native shrubs, is two sites, hereafter referred to as “area 1” (30°25.38’S called “campos grossos”. Fragments of Semideciduous 52°18.69’W) and “area 2” (30°22.26’S 52°18.12’O), Seasonal Forest are present in more humid areas, mainly Datum WGS84, located in portions of the Campos slopes and valleys (Quadros and Pillar, 2002). However, Sulinos ecosystem (Figure 1). This subtropical region the original vegetation has been altered by forest removal experiences hot summer temperatures that exceed 22ºC, with the driest months experiencing about 30 mm of rainfall (Nimer, 1990). However, in upland areas at higher altitudes, the climate is temperate (Köppen, 1948; Nimer, 1990; Kottek et al., 2006, Barros et al., 2015), with mild summers and evenly distributed rainfall (1,100 to 2,000 mm/year) (Figure 2). Upland areas lack a dry season, with the average temperatures of the hottest month not exceeding 22º C, with severe and frequent frosts (Nimer, 1990; Belomo et al., 1990; Rambo, 1994; Quadros and Pillar 2002), and winters with minimum average temperature lower than 10º C (Figure 2) and at least 350 to 400 hours of temperatures below 7.2° C between May and September (Almeida et al., 2012). Figure 2. Climactic data at Serra do Sudeste, RS, Brazil. Data: The regional topography comprises mountains with INMET. Station Encruzilhada do Sul # 83964. Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil 735 and the alteration of the South Brazilian “campos” for captured snakes and the number of months multiplied use in agriculture, pastures, and pine and eucalyptus by the number of containers (sampling effort) and plantations (MMA, 2000; Jurinitz and Jarenkow, 2003; was, therefore, expressed as the number of snakes/ Overbeck et al., 2007; Pillar et al., 2009). container/month. - Scientific collection (SC): The collection from Data collection.—The study was carried out from the Science and Technology Museum (Museu de January 2000 to April 2006, with a gap from July 2003 Ciências e Tecnologia – MCP) at the Rio Grande do to March 2004. Sampling in area 1 was carried out Sul Pontifical Catholic University was used to obtain from January 2000 to June 2003 (42 months) and in additional information about regional snake fauna. area 2 from April 2004 to April 2006 (25 months). The sampling and capture efforts in area 1 were conducted Area 2 was sampled through RC, using 13 containers using the following methods: for 22 months, and AS for 25 months in open habitats - Resident collectors (RC): During 42 months, 17 characterized by rock substrate covered mainly by native plastic containers were distributed to residents from grassland and shrubs (95% sampling effort) (Figure 2), different locations within the two study areas, for with a total investment of 1,385.8 person-hours, or 55.5 depositing dead or incidentally slaughtered specimens h/month. (for example, during plantation soil management). Voucher specimens were deposited at the The biological collections from municipal and state aforementioned MCP and the reptile collection schools were visited and specimens were identified at the Federal University of Mato Grosso do Sul and quantified. (ZUFMS REP). The specimen capture and collection - Active search (TCS) (adapted from Campbell and authorization was permitted by the Brazilian Institute Christman, 1982, time constrained search-TCS, of the Environment and Renewable Natural Resources and Martins and Oliveira, 1998): Consisted of slow (IBAMA) License 024/ RS, proc. 02023.02286/00-81 walks on trails, roads, through crops, and habitats and License 142/04 proc. 02010.003277/04-32. surrounding homes, checking potential shelters The updated list of synonyms is available in Uetz (burrows, under rocks, fallen logs, and abandoned (2017) and Arteaga et al. (2018). The body was lumber) over 30 months (January 2000 at July 2002). measured using the snout vent length (SVL), measuring Capture effort through AS was 2,120 observer-hours, from the tip of the nose (snout) to the cloaca (vent), about 70.5 hours/month. Snake detection rates were excluding the tail. Snake macro and micro-habitats calculated using the ratio between the total number (environment and substrate) were classified based of captured or sighted individuals and the total on Cadle and Greene (1993). Adult individuals were number of hours invested in the method (Martins considered sexually mature based on gonad analysis. and