Diversity and habitat use by snakes and lizards in coastal environments of southernmost Brazil

Diversidade e uso do ambiente por serpentes e lagartos em ambientes costeiros do extremo sul brasileiro

ARTICLES

Diversity and habitat use by snakes and lizards in coastal environments of southernmost Brazil

Diversidade e uso do ambiente por serpentes e lagartos em ambientes costeiros do extremo sul brasileiro

Maurício Beux dos Santos^I,*; Mauro Cesar Lamim Martins de Oliveira^II; Alexandro Marques Tozetti^III

^ILaboratório de Ecologia de Vertebrados Terrestres, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande - FURG, Campus Carreiros, Av. Itália, Km 8, CEP 96201-900, Rio Grande, RS, Brasil

IILaboratório de Ictiologia, Instituto de Oceanografia, Universidade Federal do Rio Grande - FURG, Campus Carreiros, CP 474, CEP 96201-900, Rio Grande, RS, Brasil

^IIIUniversidade do Vale do Rio dos Sinos - UNISINOS, Av. Unisinos, 950, CEP 93022-000, São Leopoldo, RS, Brasil

ABSTRACT

This study examined species composition differences among snake and lizard assemblages from coastal dunes and restinga habitats in southernmost Brazil. Animals were collected between April 2009 and March 2010 using pitfall traps, artificial shelters, and time-constrained searches in grasslands areas susceptible to flooding. Species richness was higher in the restinga, but lower than the observed in other Brazilian biomes, possibly associated with more unstable microclimate conditions and low habitat complexity (vertical and horizontal distribution of the vegetation) in this habitat. This hypothesis is supported by the fact that the most abundant species of both snakes and lizards have fossorial habits. The assemblage of snakes is apparently mainly determined by abiotic characteristics of the habitat, while the assemblage of lizards, by vegetation cover.

Keywords: diversity, lizards, restinga, sand dunes, snakes.

RESUMO

O estudo teve como objetivo avaliar a composição de espécies de serpentes e lagartos em ambientes costeiros no extremo sul brasileiro. Foram feitas amostragens sistematizadas em hábitats de dunas e restingas entre abril de 2009 e março de 2010 por meio de armadilhas de interceptação e queda, abrigos artificiais e procuras visuais. O ambiente de restinga revelou uma maior riqueza de espécies do que as dunas. As taxocenoses revelaram uma menor riqueza do que a observada em outros biomas brasileiros, o que parece estar associado às condições microclimáticas menos estáveis e à baixa complexidade estrutural desses habitats (distribuição vertical e horizontal da vegetação). Essa hipótese parece ser reforçada pelo fato de tanto para serpentes quanto para lagartos as espécies mais abundantes apresentam hábitos fossoriais. Aparentemente a taxocenose de serpentes é determinada predominantemente pelas características abióticas (microclima) do habitat enquanto que a de lagartos pelo padrão de cobertura vegetal.

Palavras-chave: diversidade, dunas, lagartos, restinga, serpentes.

Introduction

In the last decades, several studies on assemblages of snakes and lizards have been conducted in the Neotropics, broadening the understanding of the diversity patterns of these groups (Di-Bernardo et al. 2007). However, the number of studies is still low when compared to those in Europe, North America, and Australia (Seigel & Collins 1993). This also occurs in Brazil, which houses a large diversity of Squamata (Di-Bernardo et al. 2007). Currently, 241 Brazilian species of lizard and 371 species of snakes have been described (Bérnils 2010). Unfortunately, generalizations on the patterns of regional diversity of Squamata in Brazil are limited, as most studies available focus on forest habitats (e.g. Marques & Sazima 2004, Bernarde & Abe 2006, Sawaya et al.2008) and most recently in Cerrado (e.g. Colli et al. 2002, Costa et al. 2007, Sawaya et al.2008). In Rio Grande do Sul state, samplings have been concentrated in the Pampa, Araucaria forest, central depression, and northern coastal region (Maciel et al.2003, Santos et al. 2005, Zanella & Cechin 2006, Winck et al. 2007).

Southern Brazil, especially the southernmost region of Rio Grande do Sul state houses 21 species of lizards and 75 species of snakes (Brasil 2004, 2008, Quintela et al. 2006, Quintela & Loebmann 2009) and most of them are poorly studied. The municipality of Rio Grande, in Rio Grande do Sul state, harbors one of the largest continuous and relatively well-preserved areas of coastal grasslands, which are characterized by a mosaic of sand dunes and restingas. These two habitats differ, regarding patterns of plant cover and daily temperature variation (Cordazzo & Seeliger 1987, Calliari & Klein 1993). Despite the physical proximity between dunes and restinga, their characteristics might impose different limits for their use by snakes and lizards (Rocha & Sluys 2005). Thus, the present study was aimed at examining differences in species composition and relative abundance in assemblages of snakes and lizards in areas of dunes and restinga in southernmost Brazil.

Materials and Methods

1. Study area

Samplings were conducted in a continuous area of coastal grasslands of approximately 14700 ha, located at sea level (Figure 1a), known as Balneário Cassino (32º 07' 54.65" S and 52º 20' 53.36" O), municipality of Rio Grande, Rio Grande do Sul, Brazil. The climate is humid subtemperate with an average annual temperature of 18.1 ºC (Maluf 2000). Seasons are well defined, with occasional dry periods in the spring and average annual rainfall of 1162 mm (Maluf 2000). During this study, between April 2009 and March 2010, the hottest months were January and February (average air temperature = 25.4 ºC) and the coldest months were June and July (average air temperature = 11.2 ºC). In the study period total rainfall was 1371 mm, with November and February being the wettest (∑ = 527.9 mm) and July and March the driest months (∑ = 63.3 mm; Figure 2). Climate data were obtained from weather station #83995 of Rio Grande (EM 83995-INMET).

 

Two distinct habitats were sampled: (1) coastal grasslands associated with coastal dunes (hence termed "dune habitat"; Figure 1b) and (2) coastal grasslands associated with restinga (termed "restinga habitat"; Figure 1c).

The vegetation in the dune habitat consists of grasses and shrubs [e.g. Panicum racemosum (P. Beauv.) and Senecio crassiflorus (Poir.), Calliari & Klein (1993)]. Because of the ground cover and sandy soil, daily temperatures in the dunes vary widely (0-40 ºC, Calliari & Klein 1993). The vegetation in the restinga habitat is composed of predominantly shrubs and trees [e.g. Lithraea brasiliensis Marchandand Chrysophyllum marginatum (Hook. & Arn.), which provide significant amounts of leaf litter (Dorneles & Waechter 2004). The higher density and taller vegetation in the restinga provide more micro-climatic stability, and therefore the daily temperature variation is not as wide as in the dunes (Rocha & Sluys 2005).

2. Field work

The study was carried out between April 2009 and March 2010. The following methods were used to capture snakes and lizards:

a) Pitfall traps with drift fence (PDF) - consisted of 40 m lines with four buckets connected by a 50 cm high nylondrift fence (for details see Sawaya et al.2008). Three groups were set up at least 600 m apart in each examined habitat (dunes and restingas). Each group consisted of two lines of buckets, totaling 12 lines, 480 m of drift fence and 48 buckets (24 in each examined habitat). To minimize the effects of plant cover heterogeneity among groups, we selected visually similar areas regarding density and structure of the vegetation. Uncovered buckets were inspected during a period of five consecutive days, repeated every 15 days, totaling 120 sampling days. After 12 months of collection, 5.760 pitfall traps were monitored;

b) Artificial shelters (AS) - We installed three shelters for each line of traps, two located at the opposite sides of the line and one in the center (approximately 5 m from buckets), totaling 36 artificial shelters. Each AS consisted of a wood board of 1 m² and approximately 6 mm thick, placed on the ground after clearing the vegetation (Parmelee & Fitch 1995). The inspection of shelters was carried out simultaneously to PDF, totaling 5.184 inspections throughout the study;

c) Time constrained visual searches (TCVS) - we conducted 20 hours/man of search per month equally distributed between dune and restinga habitats, totaling 240 hours/man (Martins & Oliveira 1998); and

d) Incidental encounters (IC) - This method was used exclusively to complement the list of species and included animals found during activities other than those previously described.

The identification of specimens was based on available identification keys (Quintela & Loebmann 2009, Achaval & Olmos 2003), as well as consultation of materials from collections of other institutions. Nomenclature followed the Brazilian List of Reptiles of the Sociedade Brasileira de Herpetologia (Bérnils 2010).

3. Data analysis

Catches taken by TCVS and IC were used only for making the list of local species. To evaluate the efficiency of PDF and AS (the only methods that allow controlled sampling effort), an average curve of species accumulations (collector's curve) was calculated with the software Estimates 8.2.0 (Colwell 2009), adjusted for 1000 iterations. The final average curve represented the average values of its points. The data obtained for each group of traps and their corresponding shelters, during a period of five days were considered one sample, with a total of 138 samples (6 groups and 23 sample periods).

Five richness estimators were tested for precision: Chao 1 and 2, Jacknife 1 and 2 and ACE. Chao 1 was chosen for stabilizing quickly and constancy of the extrapolated value for 1000 random iterations calculated with the software Estimates 8.2.0 (Colwell 2009). To examine the participation of each species in the assemblage composition, we also calculated dominance with the rarefaction method using the software Ecosim (Gotelli & Entsminger 2001), adjusted for 1000 iterations. Number of captures obtained for the two habitats were compared with the Mann-Withney test (exclusively for species with more than 10 captures, sensu Zar 1999).

Were used a cluster analysis using the Sorensen's index of similarity to compare the species composition of the study area with those of other habitats. In the comparison, only species with genus and species epithets were included. Assemblages of snakes and lizards were analyzed separately due to ecological differences and to facilitate comparisons with other studies. The species composition was compared with those of other localities and biomes according to the classification by IBGE (Instituto... 2011). For snakes, the following studies were compared: Amazon rainforest - Martins (1991); Atlantic rainforest - Zanella & Cechin (2006), Hartmann et al. (2009) and Borges-Martins et al. (2007); Cerrado - Sawaya et al. (2008) and Souza et al. (2010); Caatinga - Loebmann & Hadaad (2010); Pantanal - Strüssmann & Sazima (1993); Coastal environment of Uruguay - Carreira et al. (2005); Argentine Chaco - Leynaud & Bucher (1999); Pampa - Santos et al. (2005), Quintela & Loebmann (2009) and this study. For lizards, we selected: Amazon rainforest - Ilha & Dixo (2010) and Silva et al. (2011); Atlantic rainforest - Carvalho et al. (2007), Costa et al. (2009), Silva-Soares et al. (2011), Freire (1996) and Teixeira (2001); Cerrado - Valdujo et al. (2009) and Cintra et al. (2009); Chaco region in Argentina - Cabrera (2009) and Álvarez et al. (2009); Coastal environment of Uruguay - Carreira et al. (2005); Pampa - Santos et al. (2005), Quintela & Loebmann (2009) and this study.

Results

1. Snakes

1.1. Richness and dominance

Thirteen species from two families, Dipsadidae (12 species and 98.1% of captures) and Viperidae (one species, 1.79% of captures; Table 1), were captured. The three most abundant genera were Liophis (three species, 56.3% of captures), Xenodon (one species, 18.75% of captures) and Phalotris (one species, 98.21% of captures; Table 1).

For the analysis of species richness, we only included captures obtained using PDF and AS. The species accumulation curve did not stabilize (Figure 3), indicating that new samplings would increase the number of snake species. Species richness was higher in the restinga (nine species) than in the dune habitat (six species). Additionally, the estimated richness (Chao1) of snakes was higher for the restinga (9.68 ± 3.04) than for dunes (5.93 ± 1.15).

The dominance observed for the dune habitat was lower (0.40) than that of the restinga (0.43). Although the number of captures in the dunes (n = 181) was higher than that of the restinga (n = 79), this difference was not significant (U = 2248.5, p = 0.574, n = 138). The same occurred when species were examined individually. In the dunes, the most abundant species were Liophis poecilogyrus (40.62% of captures), Xenodon dorbignyi (26.56% of captures) and Liophis jaegeri (12.6% of captures; Table 1). In the restinga, the three most abundant species were L. poecilogyrus (43.75% of captures), Phalotris lemniscatus (16.66% of captures) and L. jaegeri (12.5% of captures; Table 1). The snakes Boiruna maculata and Helicops infrataeniatus were observed only in the dunes, while Oxyrhopus rhombifer, Philodryas aestiva and Rhinocerophis alternatus, only in the restinga (Table 1).

1.2. Comparison of snake assemblages from other localities

The number of species found in this study (n = 13) was less than the total species in all areas compared (Table 2). The cluster analysis revealed that the snake assemblage described in the present study is most similar to those of the Coastal environment of Uruguay (Careira et al. 2005), Atlantic rainforest from south of Brazil and Pampa habitats (Table 2; Figure 4). Similarity was lowest when compared to assemblages of the Atlantic Rainforest in southeastern Brazil (Hartmann et al. 2009) and other open habitats (e.g. Cerrado, Pantanal and Chaco; Figure 4).

2. Lizards

2.1. Richness and dominance

We captured two hundred lizards from five species distributed in five families, Liolaemidae (64.5% of captures), Gymnophtalmidae (30% of captures), Scincidae (3% of captures), Teiidae (1.5% of captures) and Anguidae (1% of captures; Table 3). Specimens of the latter family represent a new species that is currently being described (M. Borges Martins, personal comment.).

The species accumulation curve (captures in AS and PDF) approached stability (Figure 5). The observed richness in the restinga habitat (five species) was higher than that of dunes (four species). Also, the estimated richness (Chao 1) of lizards was higher for the restinga (4.74 ± 1.08) than for the dune habitat (3.58 ± 0.61).

The dominance observed for the dunes was higher (0.66) than that of that of the restinga (0.57). The number of captures of lizards was significantly different between habitats (U = 1822, p = 0.001, n = 138), higher in the dunes (n = 147) than that in restinga (n = 52; Table 3). In both habitats, Liolaemus occipitalis was the most abundant species with 90 captures for the dunes and 30 for the restinga (41.34% of the total of captures), followed by Cercosauraschreibersii, with 45 captures in the dunes and 15 in the restinga (19.23% of the total of captures; Table 3).

For L. occipitalis (U = 1789.5, p = 0.011, n = 138) and C. schreibersii (U = 1894.5, p = 0.038, n = 138), the number of captures was higher in the dunes (n = 98 and 45, respectively) than in the restinga (n = 30 and 15; Table 3). The lizard L. occipitalis was only captured by PDF and Mabuya dorsivittata, only by AS. Cercosaura schreibersii had only two captures by PDF. All species of lizards were observed in both habitats, except for Tupinambis merianae, captured only in the restinga (Table 3).

2.2. Comparison with lizard assemblages from other localities

The number of species of lizards found in this study (n = 5) was lower than those found in compared studies (Table 4).

Cluster analysis revealed that the assemblage of lizards studied has greater similarity with areas of Pampa, Coastal environment of Uruguay and Eastern Chaco in Argentina (Table 4; Figure 6). The dendrogram revealed a distinction between open and forested habitats. Similarity was lowest between assemblages of forest and that of the present study.

Discussion

Despite the intense sampling effort and the combination of capture methods, the non-stabilization of the collector's curve suggests that the species richness of snakes in the study area is still higher than that recorded. The numbers of species found in this study represents 68% of the snake species and 62% of the lizard species previously recorded in the municipality (Quintela et al. 2006). This indicates the importance of dune and restinga habitats for the region. The relatively low species richness compared to other Brazilian assemblages might be due to historical factors (Seeliger 1997), an abiotic filter created by the wide daily temperature variation, as well as the harsh winter for tropical standards (Maluf 2000). These factors associated to strong coastal winds (Calliari & Klein 1993), make these habitats less susceptible for the colonization by ectotherms. Consequently, the lower richness observed in dunes compared to restinga (for snakes as well as lizards) might be associated to more severe microclimatic conditions in dunes (e.g. insolation and wide daily temperature variation) and also the lower heterogeneity in plant cover.. On the other hand this configuration should be driven by historical factors. A biogeographic approach should be helpful for subsequent studies in similar habitats.

Interestingly, two fossorial snakes were the dominant species in dunes (X. dorbignyi) as well as restinga (P. lemniscatus). The ability to bury might increase the adaptability to dune and restinga habitats, both subjected to abrupt temperature variations at the ground surface (Tozetti et al. 2009, Oliveira et al. 2001). The dominance of semi-fossorial (L. occipitalis)and cryptic (C. schreibersii) species was also observed for lizards. The sandy substrate possible favors L. occipitalis, which buries itself in the sand and builds shelters (Santos et al. 2010, Bujes & Verrastro 1998). In contrast, C. schreibersii, instead of burying itself, uses logs and stones as shelter (Doan 2003, pers. obs.). Although this behavior could increase its affinity for therestinga, where the leaf litter and additional accumulated plant material provide more shelters, this was not observed. The use of artificial shelters might have increased the capture of individuals of these species in the dunes (where the availability of natural shelters is low), masking differences in abundance between habitats.

The cluster analysis suggests that the type of vegetation has a secondary role in the structure of snake assemblages examined. This is supported by the higher similarity of the study area to some assemblages from forests than to those from open habitats such as Pampa or Pantanal. However, the similarity with other Coastal environments suggest a stronger abiotic influence in the structure of communities, which is supported by the similarity observed between the study area and the Coastal environment of Uruguay (Carreira et al. 2005). In both areas, the climatic conditions and the marine influence are similar. This abiotic filter, less favorable to ectotherms, might also be responsible for the relatively low species richness compared to other Brazilian assemblages.

Conversely, lizard assemblages showed a stronger association with plant cover. Similarity was higher with the Pampa, where climatic conditions are distinct from those of the Coastal environments (Maluf 2000, Santos et al. 2005). Additionally, despite the coastal influence in areas of the Atlantic Forest, the assemblages from this biome were different from that of the study area. Although the Atlantic Forests included restinga habitats, plant cover consists of an arboreal component more developed than that of the study area (Freire 1996, Teixeira 2001, Carvalho et al. 2007). This divergence suggests that plant cover pattern represent a primary filter, wich overlaps the abiotic factors in the structure of the lizard assemblages compared.

Our findings also revealed an intrinsic heterogeneity of the communities of some groups of Squamata in habitats that comprise the Brazilian coastal grasslands. Despite low endemic rates, the coastal grasslands of southernmost Brazil contain biotic and abiotic characteristics that act as important filters in the structure of snakes and lizards communities.

Acknowledgements

The authors are thankful to the researchers Alexandre Hartmann and Lucas Ott Tavaves for field work assistance, and to CNPq, FAPERGS, and Capes for financial support to conduct this study and a Master's fellowship.

Received 20/09/2011

Revised 24/06/2012

Accepted 10/08/2012

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Publication Dates

• Publication in this collection
  08 Nov 2012
• Date of issue
  Sept 2012

History

• Received
  20 Sept 2011
• Accepted
  10 Aug 2012
• Reviewed
  24 June 2012