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Environmental factors affecting the distribution of land snails in the Atlantic Rain Forest of Ilha Grande, Angra dos Reis, RJ, Brazil/Fatores ambientais afetando a distribuicao de moluscos terrestres na Mata Atlantica da Ilha Grande, Angra dos Reis, RJ, Brasil.

1. Introduction

Studies of the relationship between the distribution and abundance of terrestrial molluscs and environmental factors are scarce (Hermida et al., 1995; Barker and Mayhill, 1999; Millar and Waite, 2002; Horsak et al., 2007), and there are no published data on Brazilian land snails. Despite the importance of such research for developing appropriate conservation strategies (Lange and Mwinzi, 2003; Horsak et al., 2007), much of the literature on land molluscs focuses on taxonomy, with ecological studies being few and far between (Tattersfield et al., 2001).

Land snails have an important role in the ecosystems in which they live: they contribute to litter decomposition and concentration of soil calcium and are an important food source for other animals (Lange, 2003). Their generally short life span (i.e. a few months or years) and their limited powers of dispersal make them excellent bioindicators (Watters et al., 2005).

The Atlantic Rain Forest is a biodiversity hotspot (Myers et al., 2000). Although the land snails account for a significant component of faunistic endemism in this region, it has been poorly studied (Thome et al., 2006). Our study attempted to address this gap in knowledge by investigating the relationship between species composition and the environmental variation for the land snails of two hillsides on Ilha Grande (Angra dos Reis, Rio de Janeiro), which forms part of the Atlantic Rain Forest.

[FIGURE 1 OMITTED]

2. Material and Methods

The study was conducted on two hillsides on Ilha

Grande (23[degrees]05'-23[degrees]15' S and 44[degrees]05'-44[degrees]23' W), Angra dos Reis (RJ) (Figure 1): Jararaca's Trail (oceanic hillside) and Pico do Papagaio's Trail (continental hillside).

Sampling was carried out from December 2004 to March 2005. On each hillside, five plots were sampled at 100 m elevation intervals between 100 to 500 m, with each plot being located at least 50 m from the main trail to minimise edge effects (Tattersfield et al., 2001; Santos et al., 2006). Each of the plots was sampled by collecting litter and carrying out time searches for shells and live animals (Getz and Uetz, 1994; Emberton et al., 1996).

Litter was collected down to the soil surface from ten quadrats of 25 x 75 cm, stored in labelled plastic bags, and later, transported to the laboratory of the Centro de Estudos Ambientais e Desenvolvimento Sustentavel (CEADS) at Vila Dois Rios, Ilha Grande, where it was searched for snails with the naked eye. All specimens detected were observed under a stereomicroscope (maximum magnification of 70x), and morphotypes separated and quantified. The time searches involved seven people sampling for 30 minutes, totalling 3.5 man hours per plot.

The following environmental variables were measured for each of the quadrats in a plot: litter depth, atmospheric temperature (maximum, average and minimum), soil temperature, relative air humidity (maximum, average and minimum), luminosity, canopy closure, litter moisture (leaf and branch), number of individuals and morphotypes of herbaceous plants up to 50 cm height, number of individuals and morphotypes of individuals of herbaceous plants up to 50 cm height (Menez, 2002).

We used cluster analysis to assess the similarity in species composition among plots. As the groups formed in the biological cluster analysis, the collection areas were grouped to perform a discriminant analysis using environmental data.

A Pearson correlation matrix was constructed for the environmental variables to see if there was a high intercorrelation among them. When two variables were highly inter-correlated (value > 0.65 in module), one was excluded from the discriminant analysis (Klecka, 1982) in order to minimise overestimating their effect. The variables excluded from both hillsides were: average atmospheric temperature, number of morphotype of plants from 50 cm to one metre in height and minimum relative air humidity. The minimum atmospheric temperature and number of morphotype of herbaceous plants up to 50 cm high were excluded for the oceanic hillside, and moisture of the branches in the litter was excluded for the continental hillside.

[FIGURE 2 OMITTED]

To compare the environmental data of the two hillsides we used Analysis of Variance.

3. Results

On the oceanic hillside we collected 523 specimens and 33 species. The most abundant family was Systrophiidae (42%). The most abundant species were Happiella sp. (15.5%), Stephanoda sp. (14%) and Habroconus semenlini Moricand, 1846 (11%). The species Radiodiscus sp. A, Megaspira sp., Bulimulidae A, Rhinus sp. A, Systrophiidae A and Streptartemon crossei (Pfeiffer, 1867) were exclusive of this hillside (Table 1). The Cluster Analysis yielded three clear groups: group A consisting of the plot at 100 m asl, group B with the plots at 200, 300 and 400 m asl and group C with the plot at 500 m asl (Figure 2a).

On the continental hillside we collected 458 specimens and 32 species. The most abundant family was Diplommatinidae (34%), followed by Systrophiidae (32%). The more abundant species were Adelopoma sp. (34%), Happiella sp. (16%) and Opeas beckianum (Pfeiffer, 1846) (8.5%). The species Ptychodon sp. A, Ptychodon sp. B, Stephanoda sp. A, Stephanoda sp. B and Systrophiidae B were exclusive of this hillside (Table 1). Again, three groups were generated by the Cluster Analysis: group A with the plot at 100 m asl, group B with the plot at of 200 m asl and group C joining the plots at 300, 400 and 500 m asl (Figure 2b).

Except for litter depth and number of herbaceous plant from 50 cm to one metre high, the measured environmental variables were significantly different between the hillsides (Table 2).

The result of Discriminant Analysis significantly distinguished the biological groups from the oceanic hillside (Wilks' lambda = 0.111; Df = 11, 2, 47; p = 0.0000) (Figure 3) and from the continental side (Wilks' lambda = 0.021; Df = 12, 2, 47; p = 0.0000) (Figure 4).

The relative air humidity, the litter depth, the atmospheric temperature and soil temperature determined the biological groups found on both hillsides. The luminosity and the canopy closure also determined the biological groups found on the continental hillside (Table 3).

4. Discussion

Systrophiidae was the most abundant family on the two hillsides, corroborating previous results from Ilha Grande (Santos and Monteiro, 2001) and from the Lower Urubamba Forest, Peru (Ramirez et al., 2001). Systrophiidae seems to be found frequently and often abundantly across Central and South America from Mexico to Argentina and Chile (Hausdorf, 2006). Species richness was similar for both hillsides, but the composition and abundance of species varied. This is probably related to differences in environmental variables between the studied hillsides, differences in disturbance history and naturally patchy distribution of species. Adelopoma sp. and Stephanoda sp. showed high abundance, apparently because of their gregarious behaviour in the present collection site.

There was significant environmental variation between the two hillsides, with all variables being different except for litter depth and number of individuals of herbaceous plants up to 50 cm height. Environmental variation may reflect the fact that the hillsides face in different directions, with humid winds from the sea resulting in higher rates of precipitation on the oceanic hillside (Rocha et al., 2003), and this may influence the other environmental variables measured.

The environmental factors which were associated with variation in species composition between the two hillsides were atmospheric temperature, litter depth, soil temperature and relative air humidity. It is well known that snails depend on water or high humidity for an active life (Baker, 1958) being relatively susceptible to desiccation, which tends to restrict them (Getz, 1974). Moist conditions are necessary for land-snail respiration and reproduction (Coney et al., 1982) and for the production of mucus, which is vital for locomotion (Cameron, 1970). Our results agree with Boycott's (1934) pioneering work on land snails as well as with studies carried out over the last decade in several countries (Millar and Waite, 2002; Martin and Sommer, 2004; Tattersfield et al., 2006; Horsak et al., 2007). According to Emberton et al. (1999) snail diversity can be explained by the increased humidity of the environment. The influence of litter depth on the communities of terrestrial molluscs was also reported by Getz and Uetz (1994) and Cameron (1986).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

Two additional environmental variables, luminosity and canopy closure, were associated with the composition of the land-snail fauna of the continental hillside. These variables are related, and are likely to have a substantial impact on land snail distributions through their influence on humidity and atmospheric temperature. Similar results were found by Shimek (1930), Millar and Waite (2002), Lange and Mwinzi (2003) and Martin and Somer (2004) for canopy closure, and by Nekola (2003) for luminosity.

Shimek (1930) stated that an association exists between vegetation type and distribution of molluscs. A similar result was found by Emberton et al. (1996), Baker and Mayhill (1999), Millar and Waite (2002) and Martin and Somer (2004). However, this study did not find a consistent relationship between the distribution of molluscs with the number and the abundance of morphotypes of herbaceous plants, which could be partially explained by the heterogeneity of the Atlantic Forest.

Our study showed that despite similar species richness, the two hillsides are characterised by differences in land-snail composition and abundance, which are associated to distinct environmental conditions on the two hillsides. The luminosity and the canopy closure also determined the biological groups found on the continental hillside. The relative air humidity, the litter depth, the atmospheric and soil temperature affected the distribution of land snails on both studied hillsides.

Acknowledgements--This study is part of GKMN's Master's Dissertation at the Programa de Pos- Graduacao em Biologia at UERJ. SBS received financial support from Faperj (APQ1 E-26-110.430/2007 and APQ1 E-26/110.402/2010). We thank CNPq for GKMN's undergraduate scholarship (135134/20057); CAPES for GKMN's scholarship (2009-2013). IBAMA for the Sisbio license (10812-1); INEA for license (18/2007); Dr. R.S. Absalao (UFRJ) for helping in statistic analyses; Dr. D. Raheem (The Natural History Museum) for a critical reading of this manuscript; LEM Lacerda for the map; the team of the Laboratory of Malacology (UERJ) for helping with fieldwork and CEADS of UERJ for logistic support.

References

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Nunes, GKM. * and Santos, SB.

Programa de Pos-Graduacao em Ecologia e Evolucao--PPGEE, Laboratorio de Malacologia Limnica e Terrestre, Universidade do Estado do Rio de Janeiro--UERJ, Rua Sao Francisco Xavier, 524, PHLC, sala 224, CEP 20550-013, Rio de Janeiro, RJ, Brazil

* e-mail: gkmnunes@yahoo.com.br

Received November 30, 2010--Accepted February 1, 2011--Distributed February 29, 2012

(With 4 figures)
Table 1. Species collected abundance on two hillsides
at Ilha Grande, RJ, Brazil.

Species                     Oceanic hillside

                      1     2    3    4     5    Total

Alcadia sp.           0     8    3    0     6     17
Helicina sp.          0     3    2    4     5     14
Neocyclotus           1     8    10   4     0     23
  prominulus
  (d'Orbigny,
  1835)
Adelopoma sp.         0     4    3    1     6     14
Radiodiscus sp.       4     0    0    0     0      4
Radiodiscus sp. A     0     0    0    0     1      1
Ptychodon schuppi     0     0    7    0     4     11
  (Suter, 1900)
Ptychodon sp. A       0     0    0    0     0      0
Ptychodon sp. B       0     0    0    0     0      0
Stephanoda sp.        0     5    0    5    63     73
Stephanoda sp. A      0     0    0    0     0      0
Stephanoda sp. B      0     0    0    0     0      0
Lilloiconcha          3     2    1    4     2     12
  superba (Thiele,
  1927)
Habroconus            14    3    8    26    7     58
  semenlini
  Moricand, 1846
Leptinaria            0     1    0    0     0      1
  unilamellata
  (d' Orbigny,
  1835)
Lamellaxis            1     0    0    1     1      3
  gracilis (Hutton,
  1834)
Opeas beckianum       7     0    0    0     0      7
  (Pfeiffer, 1846)
Obeliscus sp.         2     1    1    1     0      5
Megaspira sp.         0     5    0    0     0      5
Bulimulidae A         0     0    0    0     5      5
Rhinus sp. A          2    14    3    1     0     20
Rhinus sp. B          0     0    0    0     2      2
Rhinus ciliatus       0     1    4    2     0      7
  (Gould, 1846)
Simpulopsis sp. A     0     1    0    0     0      1
Simpulopsis sp. B     0     0    2    0     0      2
Happia sp.            6     1    2    8     0     17
Happia vitrina        1     3    1    6     9     20
  (Wagner, 1827)
Happiella             1     4    4    0     2     11
  banghaasi
  (Thiele, 1927)
Happiella sp.         35   10    14   10   12     81
Miradiscops sp.       5    17    9    12    2     45
Systrophiidae A       7    18    13   10    0     48
Systrophiidae B       0     0    0    0     0      0
Scolodonta sp.        0     1    0    1     0      2
Streptartemon         0     1    0    0     0      1
  crossei
  (Pfeiffer, 1867)
Streptaxis sp.        0     1    1    1     0      3
Solaropsis            0     1    0    1     1      3
  brasiliana
  (Deshayes, 1831)
Zonitoides sp.        0     0    1    1     0      2
Veronicellidae        0     3    2    0     0      5
    Abundance         89   116   91   99   128    523
    Richness          14   24    20   19   16     33

Species                    Continental hillside

                      1     2    3    4    5    Total

Alcadia sp.           1     0    0    0    0      1
Helicina sp.          3     2    0    0    0      5
Neocyclotus           0     8    3    3    0     14
prominulus
(d'Orbigny,
1835)

Adelopoma sp.         0    140   6    0    10    156
Radiodiscus sp.       0     1    1    0    7      9
Radiodiscus sp. A     0     0    0    0    0      0
Ptychodon schuppi     0     1    1    0    0      2
(Suter, 1900)

Ptychodon sp. A       1    26    3    0    0     30
Ptychodon sp. B       0     2    0    1    0      3
Stephanoda sp.        0     1    0    1    1      3
Stephanoda sp. A      0     1    0    0    1      2
Stephanoda sp. B      0     1    1    0    0      2
Lilloiconcha          0     3    0    0    0      3
superba (Thiele,
1927)

Habroconus            0     4    1    3    0      8
semenlini
Moricand, 1846

Leptinaria            5     0    1    0    1      7
unilamellata
(d' Orbigny,
1835)

Lamellaxis            0     0    0    1    1      2
gracilis (Hutton,
1834)

Opeas beckianum       39    0    0    0    0     39
(Pfeiffer, 1846)

Obeliscus sp.         0     0    0    3    0      3
Megaspira sp.         0     0    0    0    0      0
Bulimulidae A         0     0    0    0    0      0
Rhinus sp. A          0     0    0    0    0      0
Rhinus sp. B          0     1    0    0    0      1
Rhinus ciliatus       1     1    0    0    0      2
(Gould, 1846)

Simpulopsis sp. A     1     0    1    0    1      3
Simpulopsis sp. B     0     0    1    0    0      1
Happia sp.            0     9    2    0    5     16
Happia vitrina        0     3    0    0    0      3
(Wagner, 1827)

Happiella             3     4    4    0    3     14
banghaasi
(Thiele, 1927)

Happiella sp.         8    22    24   7    13    74
Miradiscops sp.       2    26    3    2    2     35
Systrophiidae A       0     0    0    0    0      0
Systrophiidae B       6     0    0    0    0      6
Scolodonta sp.        0     2    1    0    0      3
Streptartemon         0     0    0    0    0      0
crossei
(Pfeiffer, 1867)

Streptaxis sp.        3     2    0    0    0      5
Solaropsis            1     0    0    0    1      2
brasiliana
(Deshayes, 1831)

Zonitoides sp.        2     1    0    0    0      3
Veronicellidae        0     0    0    0    1      1
Abundance             76   261   53   21   47    458
Richness              14   22    15   8    13    32

Table 2. Analysis of variance performed with the
environmental data comparing the two hillsides
on Ilha Grande, Angra dos Reis, RJ.

                                     F        p

Atmospheric temperature maximum      8.36   0.00#
Atmospheric temperature average     10.15   0.00#
Atmospheric temperature minimum     25.89   0.00#
Soil temperature                     4.90   0.02#
Relative air humidity maximum       16.11   0.00#
Relative air humidity average       13.21   0.00#
Relative air humidity minimum       74.82   0.00#
Luminosity                          15.85   0.00#
Litter depth                         0.16   0.68
Number of individuals of             0.39   0.53
  herbaceous plants *
Morphotype herbaceous plants *       4.32   0.04#
Number of individuals of            11.38   0.00#
  herbaceous plants **
Morphotype of herbaceous            10.47   0.00#
  plants **
Canopy closure                       6.17   0.01#
Litter moisture (leaf)             161.40   0.00#
Litter moisture (branch)            84.65   0.00#

* Up to 50 cm height; **: from 50 cm to one
metre height; bold numbers indicate p < 0.05.

Note: Numbers indicate p < 0.05 are indicated with #.

Table 3. Coefficients of the Canonical Discriminant Function
constructed from the biological groups on two hillsides on
Ilha Grande, RJ, Brazil.

                              Oceanic           Continental
                             hillside             hillside

                           D F 1     D F 2     D F 1     D F 2

Constant                   0.000     0.000     0.000     0.000
Atmospheric temperature    0.897#   1.575#     0.306     0.069
maximum

Atmospheric temperature      --       --      0.870#     0.052
minimum

Soil temperature           0.887#   -0.959#   -2.085#   -0.273
Relative air humidity      1.435#    0.213    1.093#     0.436
maximum

Relative air humidity      -0.11     0.080    -1.160#   -0.110
average

Luminosity                 0.494     0.303    -0.171    1.061#
Litter depth               0.112    0.561#     0.119    -0.653#
Number of individuals      0.371     0.220    -0.030    -0.282
of herbaceous plants *

Morphotype of herbaceous     --       --       0.070    -0.415
plants *

Number of individuals      0.228     0.155     -0.15    -0.442
of plants **

Canopy closure             0.303    -0.222    0.868#     0.104
Litter moisture (leaf)     0.247    -0.024      --        --
Litter moisture (branch)   0.394    -0.068     0.012    -0.036

* Up to 50 cm height; **: from 50 cm to one metre height; D F:
Discriminant function; bold numbers indicate high values.

Note: Numbers indicate high values are indicated with #.
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Title Annotation:ECOLOGY
Author:Nunes, G.K.M.; Santos, S.B.
Publication:Brazilian Journal of Biology
Date:Feb 1, 2012
Words:3771
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