Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil

Transcription

1 Herpetology Notes, volume 11: (2018) (published online on 31 August 2018) Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil Arlete B. Outeiral 1, Rafael L. Balestrin 1,2, Lize H. Cappellari 1,3, Thales de Lema 1, and Vanda L. Ferreira 4,* 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 Species composition, structure (abundance and species richness), and function are essential attributes of biodiversity (Noss, 1990; Magurran, 2004) and maintaining them are the basic objectives of global biodiversity conservation strategies (Wilson, 1992). Thus, conservation of biological diversity is based on traditional diversity measurements, such as inventories, descriptions of natural history and ecology (Gaston, 1996), and measurements of functional and phylogenetic diversity (Petchey and Gaston, 2006; Cavender-Bares et al., 2009; Cianciaruso et al., 2009; Stegen and Hurlbert 2011; Lopez et al., 2016), as well as factors and processes 1 Pontifícia Universidade Católica do Rio Grande do Sul, Faculdade de Biociências, Programa de Pós-graduação em Zoologia, Av. Ipiranga, 6681, Partenon, CEP , Porto Alegre, RS, Brazil. 2 Fieldwork Consultoria Ambiental Ltda, Rua Gonçalves Dias, 729, Apto. 503, Seminário, CEP , Curitiba, PR, Brazil. 3 Universidade da Região da Campanha, Rua General Osório, 522, CEP , Caçapava do Sul, RS, Brazil. 4 Universidade Federal de Mato Grosso do Sul, Instituto de Biociências, Laboratório de Pesquisa em Herpetologia, Cx.P. 549, CEP , Campo Grande, MS, Brazil. * Corresponding author. vandalferreira@gmail.com that affect and maintain them (Stegen et al., 2013), and combinations thereof (Hurlbert and Jetz, 2007; Stegen and Hurlbert, 2011; Paglia et al., 2012). Although taxonomic studies on regional fauna are considered important, relatively little is known about the diversity of Brazilian fauna (Lewinsohn and Prado, 2002), which holds true for snakes. Although snakes represent 35% of all reptiles worldwide (Roll et al., 2017; Uetz, 2017) and more than 50% of Brazilian reptile species (Costa and Bérnils, 2015, 2018), with high variation in community composition and phylogenetic diversity (Moura et al., 2017), they have been poorly studied. The distribution of this diverse reptile group is fundamental 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 challenges, as this ecosystem is neglected (Overbeck et al., 2007) and threatened on a global and local scale (Pillar and Vélez, 2010). It has high levels of biodiversity (Boldrini, 2009) and endemism (Bencke, 2009), but is experiencing alterations of its natural ecosystems (Bencke, 2009; Pillar and Vélez, 2010; Oliveira et al., 2017). Thus, considering the region s biological importance and the need to understand local communities, the local snake species composition and richness are described, and an annotated checklist for Campos Sulinos, located in Southern Brazil, is given.

2 734 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 Study site. The study was conducted at Dom Feliciano, Encruzilhada do Sul, in the municipalities of São Jerônimo and Barão do Triunfo, at the Serra do Sudeste, in the state of Rio Grande do Sul (RS), Brazil. The largest sampling effort was conducted at two sites, hereafter referred to as area 1 ( S W) and area 2 ( S O), Datum WGS84, located in portions of the Campos Sulinos ecosystem (Figure 1). This subtropical region 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). The regional topography comprises mountains with gradually increasing altitudes from south to north, from less than 100 meters on the southern edge to over 600 meters in the north (Rambo, 1994). The vegetation comprises a mosaic of transitional grassland and Semideciduous Seasonal Forest zones. The grassland formation exhibits a similar physiognomy to the Savannah, which, when invaded by native shrubs, is called campos grossos. Fragments of Semideciduous Seasonal Forest are present in more humid areas, mainly slopes and valleys (Quadros and Pillar, 2002). However, the original vegetation has been altered by forest removal Figure 2. Climactic data at Serra do Sudeste, RS, Brazil. Data: INMET. Station Encruzilhada do Sul #

3 Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil 735 and the alteration of the South Brazilian campos for use in agriculture, pastures, and pine and eucalyptus plantations (MMA, 2000; Jurinitz and Jarenkow, 2003; Overbeck et al., 2007; Pillar et al., 2009). Data collection. The study was carried out from January 2000 to April 2006, with a gap from July 2003 to March Sampling in area 1 was carried out from January 2000 to June 2003 (42 months) and in area 2 from April 2004 to April 2006 (25 months). The sampling and capture efforts in area 1 were conducted using the following methods: - Resident collectors (RC): During 42 months, 17 plastic containers were distributed to residents from different locations within the two study areas, for depositing dead or incidentally slaughtered specimens (for example, during plantation soil management). The biological collections from municipal and state schools were visited and specimens were identified and quantified. - Active search (TCS) (adapted from Campbell and Christman, 1982, time constrained search-tcs, and Martins and Oliveira, 1998): Consisted of slow walks on trails, roads, through crops, and habitats surrounding homes, checking potential shelters (burrows, under rocks, fallen logs, and abandoned lumber) over 30 months (January 2000 at July 2002). Capture effort through AS was 2,120 observer-hours, about 70.5 hours/month. Snake detection rates were calculated using the ratio between the total number of captured or sighted individuals and the total number of hours invested in the method (Martins and Oliveira, 1998). - Search using automobile (SA): Searches with vehicles were carried out over 30 consecutive months. On average, every search was performed for forty minutes at a speed of 40 km/h, with a total of 12 observer-hours/month. The snake detection rate of SA was calculated by the ratio between the total number of snakes and the total number of travel hours by car. - Pitfall traps with drift fences (PTDF): Six sets of traps arranged in two rows (800 meters apart) were installed in open formations and forest areas. Each set consisted of L plastic containers (five containers per set), buried at 10 m intervals and connected by a 1 m high fence (plastic mesh). The containers were left open for 30 months and were inspected three times per week in the winter and on alternate days in the summer. The capture rate was calculated as the ratio between the number of captured snakes and the number of months multiplied by the number of containers (sampling effort) and was, therefore, expressed as the number of snakes/ container/month. - Scientific collection (SC): The collection from the Science and Technology Museum (Museu de Ciências e Tecnologia MCP) at the Rio Grande do Sul Pontifical Catholic University was used to obtain additional information about regional snake fauna. Area 2 was sampled through RC, using 13 containers for 22 months, and AS for 25 months in open habitats characterized by rock substrate covered mainly by native grassland and shrubs (95% sampling effort) (Figure 2), with a total investment of 1,385.8 person-hours, or 55.5 h/month. Voucher specimens were deposited at the aforementioned MCP and the reptile collection at the Federal University of Mato Grosso do Sul (ZUFMS REP). The specimen capture and collection authorization was permitted by the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA) License 024/ RS, proc /00-81 and License 142/04 proc / The updated list of synonyms is available in Uetz (2017) and Arteaga et al. (2018). The body was measured using the snout vent length (SVL), measuring from the tip of the nose (snout) to the cloaca (vent), excluding the tail. Snake macro and micro-habitats (environment and substrate) were classified based on Cadle and Greene (1993). Adult individuals were considered sexually mature based on gonad analysis. For males, the convoluted condition of the vas deferens was considered, while for females the presence and condition of the follicles (secondary or vitellogenic) or eggs were taken into account. The follicles were considered vitellogenic, with a size greater than or equal to 10 mm (Shine, 1977) or using the size determined in other studies (Marques and Puorto, 1998; Martins and Oliveira, 1998; Aguiar and Di-Bernardo, 2005; Balestrin and Di Bernardo, 2005; Santos-Costa et al., 2006). The recruitment period of juveniles was both indirectly and directly inferred (Almeida-Santos et al., 2014; Rebelato et al., 2016) based on, for example, the time of detection of wild individuals with a body size comparable with that of new-borns, occurrence of eggs/embryos or pleated oviducts, indicating recent egg deposition and hatching and birth events. The morphometric features of each species and ecology were reviewed (e.g. Pontes, 2007; Pizzatto et al., 2008; Lopéz et al., 2013; Gouveia et al., 2017). Diet was determined

4 736 Arlete B. Outeiral et al. Table 1. List of species, sampling method and vouchers registered at Serra do Sudeste, RS, Brazil. RC: Resident collectors, TCS: Time Constrained Search, SA: Search using automobile, PTDF: Pitfall traps with drift fences, SC: Scientific Collection. Numbers in parentheses indicate the amount of species per area or family. Family/Tribe/Species Area 1 (30) Area 2 (24) Collection method RC TCS SA PTDF SC RC TCS Leptotyphlopidae Stejneger 1892 (1) Epictini Adalsteinsson et al Epictia munoai (Orejas-Miranda 1961) 27 8 Colubridae Oppel 1811 (3) Chironius bicarinatus (Wied 1820) Mastigodryas bifossatus (Raddi 1820) Tantilla melanocephala (Linnaeus 1758) Dipsadidae Bonaparte 1838 (25) Dipsadini Bonaparte 1838 Atractus reticulatus (Boulenger 1885) 1 Dipsas aff. neuwiedi 1 Dipsas neuwiedi (Ihering 1911) 1 1 Dipsas ventrimaculatus (Boulenger 1885) Echinantherini Zaher et al Taeniophallus occipitalis (Jan 1863) Taeniophallus poecilopogon (Cope 1863) 3 7 Elapomorphini Jan 1862 Elapomorphus sp. 15 Phalotris lemniscatus (Duméril et al. 1854) 1 2 Hydropisini Dowling 1975 Helicops infrataeniatus (Jan 1865) 3 4 Philodryadini Cope 1886 Philodryas aestiva (Duméril et al. 1854) Philodryas agassizii (Jan 1863) Philodryas olfersii (Lichtenstein 1823) Philodryas patagoniensis (Girard 1858) Pseudoboini Baley 1967 Boiruna maculata (Boulenger 1896) 1 Oxyrhopus rhombifer Duméril et al Phimophis aff. guerini 1 Tachymenini Bailey 1967 Gomesophis brasiliensis (Gomes1918) 1 Thamnodynastes hypoconia (Cope 1860) 1 Thamnodynastes strigatus (Günther 1858) Tomodon dorsatus Duméril et al Xenodontini Bonaparte 1845 Erythrolamprus jaegeri (Günther 1858) 2 1 Erythrolamprus poecilogyrus (Wied 1824) Erythrolamprus semiaureus (Cope 1862) Xenodon dorbignyi (Duméril et al. 1854) 1 1 Xenodon merremii (Wagler in Spix 1824) Elapidae Boie 1827 (1) Micrurus altirostris (Cope 1859) Viperidae Oppel 1811 (3) Bothrops alternatus Duméril et al Bothrops pubescens (Cope 1870) Crotalus durissus terrificus (Laurenti 1768) 2 6 Species richness (33)

5 Xenodontini Bonaparte 1845 Erythrolamprus jaegeri (Günther 1858) 2 1 Erythrolamprus poecilogyrus (Wied 1824) Erythrolamprus semiaureus (Cope 1862) Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil Xenodon dorbignyi (Duméril et al. 1854) Xenodon merremii (Wagler in Spix 1824) Table 1. Continued. Elapidae Boie 1827 (1) Micrurus altirostris (Cope 1859) Viperidae Family/Tribe/Species Oppel 1811 (3) Area 1 (30) Area 2 (24) Bothrops alternatus Duméril et al Collection method RC TCS SA PTDF SC 1 RC TCS Bothrops pubescens (Cope 1870) Crotalus durissus terrificus (Laurenti 1768) 2 6 Species richness (33) Abundance Detection rate (see Materials and Methods) 0,04 1 0,09 1 0,16 2 0, snakes/observer-hour snakes/container/month based on direct observations in the environment and stomach content analysis. Behavioural descriptions of individuals followed Marques et al. (2001), Sawaya et al. (2008) and Hartmann et al. (2009). Results A total of 871 individuals belonging to 33 snake species were recorded, with three species exclusively registered through scientific collections (Bothrops alternatus, Gomesophis brasiliensis, and Thamnodynastes hypoconia) (Table 1, Appendix 1). None of the species in this community were endemic or considered threatened with extinction in the Pampas biome, but three records were important, since Dipsas aff. neuwiedi, Elapomorphus sp. (Figure 3) and Phimophis aff. guerini (Figure 4 and 5) are probably new taxa and are being studied. In addition, two of the species are reported in Brazil only in the state of Rio Grande do Sul (Taeniophallus poecilopogon and Erythrolamprus semiaureus) (see Costa and Bérnils, 2018). The individual detection rate varied among methods (Table 1). For RC, more than half the number of specimens and 76% of species richness were captured when compared to the other methods while TCS captured 26% and PTDF 16% of abundance. The TCS in area 2 resulted in a 2.5 higher capture rate compared to area 1. The effort employed with method PTDF resulted the highest capture rate of individuals for area 1. Richness records using different methods were distinct and complementary for the sampling of this assemblage. Terrestrial and diurnal snakes were most frequently detected. Snakes were more active in the warmer months (spring-summer) than in the colder months (autumnwinter), since temperate subtropical climates have little variation in precipitation throughout the year and severe winters (Figure 2). Regarding diet, anurans and lizards were the most important prey. Half of the 20 most abundant snake species had a diet composed of anurans, while a third of the species ate lizards. These food items represented 21% and 18%, respectively, of the diet of individuals with stomach contents. On average, 43% of individuals had food items in their stomach (n = 181). Information about natural history and morphometry are presented for some species in the annotated list, according to Costa and Bérnils (2015, 2018) and Arteaga et al. (2018), based on our survey work: Leptotyphlopidae Stejneger 1892 Epictia munoai (Orejas-Miranda 1961): Relative abundance of 4% (n = 35), mean SVL 110 mm ( mm, n = 24). Fossorial macro-habitat, found only in open areas, under rocks, during AS activity. Adults were found from August to November and juveniles in September (n = 2). Diet composed (43.8% of individuals with food in stomach) exclusively of termite (Isoptera) and ant (Hymenoptera) adults and larvae. Oviparous. During handling, some individuals placed and pressed the spine of the tail tip against the collector s hand. Colubridae Oppel 1811 Tantilla melanocephala (Linnaeus 1758): Relative abundance of 6.7%, mean SVL 220 mm ( mm, n = 34). Semi-fossorial, found only in open areas, mostly located under rocks (72%), reaching about 50 cm depth (n = 1). Diet (43.7% of individuals with food in stomach) composed exclusively of centipedes. Oviparous females (n = 2) with eggs (n = 2) in December and one juvenile recorded in February. Males with folded ducts in September (n = 3), October (n = 3), and November (n = 1). Behaviour of exposing the ventral face of the mid-posterior region of the body, cloacal

6 738 Arlete B. Outeiral et al. the ventral face of the mid-posterior region of the body, cloacal discharge, striking, and biting. Elapomorphini Jan 1862 Figure 3. Elapomorphus sp. specimen in captivity, recorded at the Serra do Sudeste region, RS, Brazil. Photographed by RL Balestrin. discharge, and winding around the collector s hand or finger. Dipsadidae Bonaparte 1838 Dipsadini Bonaparte 1838 Dipsas ventrimaculatus (Boulenger 1885): Relative abundance of 5.3% (n = 45). Mean SVL 342 mm ( mm, n = 45). Terrestrial, found in open and forested areas. Diet composed (17.6% of individuals with food in stomach) of slugs of the family Veronicellidae (n = 5) as verified by stomach contents (MCP and 17949). Oviparous. Females with vitellogenic follicles were found in September (n = 1), October (n = 1), November (n = 2) and January (n = 2). Males with folded ducts were found in October (n = 1), January (n = 3), April (n = 2) and two juveniles were found in January. When handling, some individuals exhibited cloacal discharge, dorsal flattening, curling up, and hiding the head under their own body. Echinantherini Zaher et al Taeniophallus occipitalis (Jan, 1863): Relative abundance of 3.1%, mean SVL 331 mm ( mm, n = 15). The majority (94%) were captured from PTDF in forested areas. Diet composed (100% of individuals with food in stomach) of Tantilla melanocephala and Cercosaura schreibersii (Wiegmann 1834) (n = 5). Oviparous, females were found with follicles in September and December and one juvenile in March. Some individuals exhibited a behaviour of exposing Elapomorphus sp. (Figure 3): Relative abundance of 1.7%. Species with cryptic macro-habitats, was found exclusively in rock outcrops (Figure 4). Compared to other species of this genus, Elapomorphus sp. has a relatively small body size. It exhibits a colourful dorsal pattern, similar to some Phalotris Cope 1862 (P. lativittatus Ferrarezzi 1994, P. lemniscatus (Duméril, Bibron and Duméril 1854), P. multipunctatus Puorto and Ferrarezzi 1994) and Apostolepis Cope 1861 (A. albicollaris Lema 2002, A. barrioi Lema 1978, A. dimidiata (Jan 1862), A. quirogai Giraudo and Scrocchi 1998) species. However, it also has a series of characteristics that suggest that it could belong to a new genus. The head scalation is similar to those of the larger species of the subfamily: a) presence of internasal (IN) and double prefrontal (common to Elapomorphus Wiegmann 1828 and Coronelaps Reinhardt 1861; b) tendency to have a reduced IN, which is absent in all species of Apostolepis, and which may be partially or totally fused (anomaly) in E. quinquelienatus (Raddi 1820) and Coronelaps lepida (Reinhardt 1861) in specimens; c) decreasing trend from two to one postoculars (PS). Only in Apostolepis does 1 PS occur and d) presence of five supralabials (SL), common only in Apostolepis of the lineata group. Elapomorphus sp. at this site exhibit more than 200 ventrals (VE), like Apostolepis species, and approximately 50 subcaudals (SC). Some Apostolepis species exhibit such a high number of SCs, such as the nigrolineata group. The description of a new genus is in the process of being evaluated. Diet composed (35.7% of individuals with food in stomach) exclusively of Amphisbaena munoai Klappenbach Female with follicles in October (n = 1). Philodryadini Cope 1886 Philodryas olfersii (Lichteinstein, 1823): Relative abundance of 6.9%. Mean SVL 562 mm ( mm, n = 21). Semi-arboreal, found in forested and open areas (n = 20). Diet (26.5% of individuals with food in stomach) included birds (Columbina talpacoti (Temminck 1810) (Columbidae)), (Turdus sp. (Turdidae)) and rodents (undetermined species). Oviparous, females with follicles in October (n = 3), November (n = 1), December (n = 1), January (n =

7 Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil 739 2) and February (n = 3). Some individuals exhibited cloacal discharge, striking and biting. Philodryas patagoniensis (Girard 1858): Relative abundance of 16.4%. Mean SVL 611 mm ( mm, n = 81). Terrestrial, found in open and forested areas. Diversified diet (47.7% of individuals with food in stomach), feeds on snakes (Oxyrhopus rhombifer Duméril, Bibron and Duméril 1854 and Philodryas agassizi (Jan 1863)), anurans (Physalaemus cuvieri Fitzinger 1826), lizards (Ophiodes sp., Anguidae (n = 1), Cercosaura schreibersii (n = 2), Aspronema dorsivitatta (Cope 1862), Mabuyidae (n = 2), Contomastix lacertoides (Duméril and Bibron 1839), Teiidae (n = 3); birds (Columbina talpacoti (n = 2), Turdus sp. and unidentified passerines (n = 3)). Oviparous, females were found with vitellogenic follicles in October (n = 2), November (n = 2); December (n = 4) and January (n = 1). A female with 10 eggs was found in December. Displayed behaviour of attempted escape, cloacal discharge, striking, biting, and thanatosis. Pseudoboini Bailey 1967 Phimophis aff. guerini: With 8 supralabials (SL), 17 dorsal scales (DO); loreal long and in contact with the 2nd and 3rd SL, 5th SL merged with the lower postocular, ocular formula 2 1. Temporal formula: 2 3, modified rostral. The single captured specimen was kept in captivity (Figure 4), and fed with Contomastix lacertoides. Subsequently it was lost, with photographic records available (ZUFMS REP 02490). Tachymenini Bailey 1967 Tomodon dorsatus Duméril, Bribon and Duméril 1854: Relative abundance of 3.4%. Mean SVL 331 mm ( mm, n = 22). Terrestrial, found in open and forested areas. Specimens found in all months of the year except July. Exclusive diet (30.8% of individuals with food in stomach) of slugs of the family Veronicellidae. Viviparous, a juvenile was found in June. Some individuals exhibited dorsal flattening behaviour, triangulation of the head, mouth opening, striking, curling up and hiding the head. Xenodontini Bonaparte 1845 Xenodon merremii (Wagler in Spix 1824): Relative abundance of 3.4%, mean SVL 447 mm ( mm, n = 25). Terrestrial, found in open and forested areas. Adults absent only in winter (June to August). Juveniles detected in February, April, and October. Diet (80% of individuals with food in stomach, n = 4) includes Odontophrynus americanus (Duméril and Bibron 1841). Exhibited triangulation of the head, dorsal flattening, mouth opening, striking, curling up, hiding the head, and erratic movements. Elapidae Boie 1827 Micrurus altirostris (Cope 1859): Relative abundance of 7.8%, mean SVL 447 mm ( mm, n = 65). Semi-fossorial, found in open and forested areas. Adults found between October and May and juveniles in April (n = 2). Diet composed (36.2% of individuals with food in stomach) of Ophiodes sp (n = 3), Sauria (indeterminate species) and Amphisbaena munoai. Exhibited erratic movements, dorsal flattening, tail tip raising and rolling, head blows, striking and attempting to bite. Viperidae Oppel 1811 Figure 4. Phimophis aff. guerini specimen in captivity registered at the Serra do Sudeste region, RS, Brazil. Photographed by RL Balestrin. Bothrops pubescens (Cope 1870): Relative abundance of 23%. SVL of 565 mm ( mm, n = 53). Terrestrial, found in open and forested areas. Diet consisted (26.6% of individuals with food in stomach) of anurans: Physalaemus sp (n = 2), Leptodactylus chaquensis Cei 1950 (n = 1), indeterminate family of Anura (n = 1); birds (Columbina talpacoti and Turdus sp.), lizards: Contomastix lacertoides (n = 2), Scolopendridae (n = 2) and rodents (n = 13). An adult female (MCP 15936) was found in May, at a height of 1.30 meters, in a riparian forest. Viviparous, females with follicles in January (n = 2), February (n = 2), and

8 740 March (n = 3) and juveniles in April, May, and June. Behaviours included dorsal flattening, tail vibration, cloacal discharge, striking and attempting to bite. Discussion The snake species richness determined herein represents 37% of the known species in the state of Rio Grande do Sul (see Costa and Bérnils, 2018). This study expanded the species richness of scientific collections (10-fold) through the deposition of vouchers specimens. Furthermore, our results classify this area as having the highest snake species richness of any area influenced by temperate climates in the Neotropical region (Arzamendia and Giraudo, 2002; Carreira et al., 2005; Santos et al., 2005; Zanella and Cechin, 2006; Quintela et al., 2006; Winck et al., 2007; Quintela and Loebmann, 2009; Santos et al., 2012; Pazinato et al., 2013; Zanella et al., 2013; Gorleri at al. 2014; Bellini et al., 2015). This region comprises both grassland and mountainous areas with slopes and forested valleys (Rambo, 1994; Quadros and Pillar, 2002) resulting in high environmental and topographic complexity (Whittaker, 1975), which explains the high species richness when compared to other regions of the state. The active search (TCS) method did not allow for the sampling of absolute richness (33), but was efficient for capture of species richness (61%) and important for observing behavioural patterns. The combination of TCS and RC detected approximately 90% of species. Abundance was associated with months Figure 5. Aspect of open habitats in area 2, Serra do Sudeste region, RS, Brazil. The habitat is characterized by a rock substrate, covered mainly by native grassland and shrubs. Photographed by RL Balestrin. Arlete B. Outeiral et al. exhibiting monthly average temperatures below 15 C (i.e. between May and August), regardless of capture effort. This effect is most likely driven by searching of potential shelters, which allowed access to inactive snakes, which were theoretically vulnerable due to the milder temperatures of that season. The PTDF detection rate obtained was similar to rates obtained in the northern plateau (Zanella and Cechin, 2006), but much lower than in the Brazilian savannah (Cerrado) in southeastern Brazil, evaluated using similar methods (Cechin and Martins, 2000). These differences may be associated with the peculiarity of habitat attributes (e.g., temperature range, soil type, phytophysiognomies, humidity, topographical features), differences in the density of snake species or a combination of these factors (Lillywhite 1987, Oliveira and Martins, 2001; Di-Bernardo et al., 2007). Snake activity is usually seasonal (see Gregory and Stewart, 1975; Stevenson, 1985; Gibbons and Semlitsch, 1987) and determined by behavioural and physiological mechanisms, which are reflected to differences in detection probability between summer and winter. Therefore, the detection rate of snakes can be strongly influenced by the sampling period and employed methods (May et al., 1996; Cechin and Martins, 2000; Rocha et al., 2014, Eskew and Todd, 2017). The discrepancy between TCS in areas 1 and 2 was probably due to unsuccessful searches during three winter periods, including a period when temperatures were very low (average 12 C and minimum temperatures around or below of 10 C) in area 1 (see Materials and Methods and Figure 2). Furthermore, because area 1 was searched first, collector experience may have influenced the success (or failure) of the searches, i.e. in the detectability of individuals. Species richness is best assessed using various methods, since each method has advantages and limitations (Campbell and Christman, 1982; Zanella and Cechin, 2006; Ribeiro-Jr et al., 2008). Excluding SA, unique species were detected with each method, which can be explained by the high sampling effort and period (see Ribeiro-Jr et al., 2008). The community is characterized by the presence of snakes in both open and forested areas, as proposed by Bencke (2009), which suggests that the herpetofauna and other vertebrates of Campos Sulinos share species with the Atlantic Forest. Furthermore, Lema (1994, 2002) considers the Serra do Sudeste as a neighbouring Atlantic forest region, which allows dispersal of herpetofauna from forests. In this scenario, according to Lema (2002: 109), it is possible that snake species richness records would increase with further studies (Bérnils et al., 2007) with

9 Snake assemblage from Serra do Sudeste, Pampas Biome, southern Brazil 741 the possibility of two additional species, Elapomorphus quinquelineatus (Raddi 1820) and Bothrops cotiara (Gomes 1913). The latter is considered vulnerable in the state of Rio Grande do Sul (Di-Bernardo et al., 2003). Elapomorphus sp. individuals recorded in this study differ from E. quinquelineatus, and will probably be considered a new genus. Terrestrial and diurnal snakes were detected most frequently, corroborating Cadle and Greene (1993), who consider this habit characteristic of South American xenodontines, which comprise most of the taxa from different communities studied in neotropical areas. The main food items of the snake community studied herein were anurans and lizards, in agreement with the review by Cortés-Gomez et al. (2015), where 41% of anuran and 55% of lizard species were consumed by neotropical snakes. The behaviours exhibited by snakes were consistent with published observations (e.g., Borges-Martins et al., 2007, Sawaya et al., 2008). In conclusion, this portion of the Serra do Sudeste, even without records of threatened or endemic snake species (MMA, 2014; IUCN, 2016), represents one of the most snake-species-rich areas in the temperate/ subtropical Neotropics. High levels of plant diversity also characterize this area (Jurinitz and Jarenkow, 2003; Veldman et al., 2015; Stam, 2016). Accelerated human activities, particularly the removal of native vegetation, the introduction of exotic plant species (MMA, 2000), and unknown and misrepresented information about the ecological characteristics among scientists, policy makers, land managers, and the public (Veldman et al., 2015) are the main threats, requiring urgent and immediate planning and implementation of conservation action plans. In addition, if the distribution of snake diversity overlaps with the distribution of other tetrapods, these groups would also benefit from the conservation of this ecosystem. Acknowledgments: ABO and RLB were supported by fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), VLF was supported by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (Fundect # 247/2014). Authorizations were given by the Instituto Brasileiro do Meio Ambiente and logistics provided by Secretaria de Educação and Saúde e Meio Ambiente, of the Encruzilhada do Sul municipality. The authors would like to thank Glaúcia Pontes for the identity confirmation of the Dipsas aff. neuwiedi and Erythrolamprus semiaureus specimens, Matheus Neves for preparing the map and Jeffrey Himmelstein for the English review. We appreciate the valuable suggestions and comments made by Maria Cristina dos Santos Costa. 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