Understory spider diversity in two remnants of tropical montane cloud forest in Chiapas, Mexico
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J Insect Conserv
DOI 10.1007/s10841-011-9391-x
ORIGINAL PAPER
Understory spider diversity in two remnants of tropical montane
cloud forest in Chiapas, Mexico
Julieta Maya-Morales • Guillermo Ibarra-Núñez •
Jorge L. León-Cortés • Francisco Infante
Received: 6 August 2010 / Accepted: 5 March 2011
Ó Springer Science+Business Media B.V. 2011
Abstract We evaluated the spider diversity of a tropical Introduction
montane cloud forest understory in two nearby sites with
different degree of human disturbance at the Biosphere Tropical montane cloud forests (TMCF) are characterized
Reserve Volcán Tacaná, Chiapas, Mexico. The study was by a very humid atmosphere due to a constant presence of
conducted over a 24 days period distributed in 6 months in clouds or mist that promotes abundant evergreen vegeta-
2009, covering dry and rainy seasons. A total of 8,370 tion, including trees in several levels, covered with mosses,
spiders (1,208 adults and 7,162 juveniles) were collected. ferns, a variety of epiphytes, and a soil cover of bushes and
Determined specimens (7,747) represented 112 species and herbs. This type of forests concentrate high levels of bio-
morphospecies, 71 genera and 22 families. The results diversity in relation to the surface occupied and a great
showed that human disturbance has an influence on spider proportion of their biota are endemic or threatened species
communities: species richness was significantly higher in (Bubb et al. 2004; Stadtmuller 1987; Williams-Linera
the preserved site as regards to the disturbed site. Despite 2007). In Mexico, the TMCF occupy between 0.4 and 0.8%
their proximity, the composition of spider communities of the total land cover (Challenger 1998; Williams-Linera
showed only a moderate similarity between the two sites. 2007) but it holds about 12% of the 3,000 plant species,
No differences in abundance were found among sites when where more than 30% are endemic (Rzedowski 1996). Due
considering the whole sample, but sites differed clearly to its reduced extension, insularity, fragmented and dis-
when seasons were analyzed separately. The rainy season turbed condition, the TMCF are one of the most threatened
had a negative effect on the abundance of spiders in the types of vegetation in Mexico (Acosta 2004). Selective
preserved site. Although the spider community structure logging (for fuel wood and timber) and extensive rising of
was very similar between sites, there was a trend towards a livestock (sheep and cattle) are the most frequent anthro-
greater species evenness in the preserved site for the whole pogenic disturbance activities within this type of forests in
sampling period and for the dry season. southeast Mexico (Ramı́rez-Marcial 2003; Ramı́rez-Mar-
cial et al. 2001; Williams-Linera 2007). The effects of
Keywords Araneae Species richness anthropogenic disturbances on TMCF have been studied
Human disturbance Season effects for diverse plant groups and fungi (Garcı́a and Toledo
2008; Heredia and Arias 2008; Mehltreter 2008; Newton
et al. 2009; Ramı́rez-Marcial et al. 2001; Rüger et al. 2008;
J. Maya-Morales G. Ibarra-Núñez (&) F. Infante Williams-Linera and López-Campos 2008), but in the case
Departamento de Entomologı́a Tropical, El Colegio de la
of animal groups, these studies have been focused mostly
Frontera Sur, Carr. Antiguo Aeropuerto km 2.5,
Tapachula, 30700 Chiapas, Mexico on vertebrates (Gallina et al. 2008; González and Murrieta
e-mail: gibarra@ecosur.mx 2008; Pineda and Halffter 2004; Pineda et al. 2005; Sosa
et al. 2008; Tejeda and Gordon 2008) and on some insect
J. L. León-Cortés
groups (Deloya and Ordoñez 2008; Deloya et al. 2007;
Departamento de Ecologı́a y Sistemática Terrestre, El Colegio
de la Frontera Sur, Carr. Panamericana y Av. Periférico Sur S/N, Hernández and Dzul 2008; Pineda et al. 2005; Valenzuela
San Cristóbal de las Casas, 29290 Chiapas, Mexico et al. 2008). Spiders are a very diverse, ubiquitous and
123J Insect Conserv abundant group of arthropods that predate on diverse Materials and methods invertebrates, and most of them live in strictly defined environments or on particular strata of a given habitat Study area (Foelix 1996). Studies have shown that spiders can dis- criminate among several environmental conditions, as The study site (Talquián, Unión Juárez, Chiapas) is located habitats with distinct plant architecture, or litter with dif- within the Biosphere Reserve Volcán Tacaná. Two sites of ferences in deep and complexity (Halaj et al. 1998; Noel TMCF (separated 800 m) were chosen based on different and Finch 2010; Rubio et al. 2008; Wise 1993), they can conditions of human disturbance, one relatively preserved display preferences for certain types of habitats (Hodge (15°050 14.800 N, 92°050 5500 W, 2,021 m asl) and a second 1987; Riechert and Tracy 1975), and react to disturbances one relatively disturbed (15°050 37.800 N, 92°060 05.700 W, in the environment (Balfour and Rypstra 1998; Gibson 2,048 m asl) (Fig. 1). The main elements of the forest in et al. 1992; Haughton et al. 1999; Marc et al. 1999; Rypstra the region are species of Matudaea, Inga, Clethra, Pith- et al. 1999; Warui et al. 2005; Willet 2001). Thus spiders ecolobium, Ilez, Podocarpus, Osmanthus, Decrela and fulfill the criteria of Kremen et al. (1993) to be reliable Olmediella (Miranda 1975). The climate is temperate indicator assemblages (‘‘suits of species that respond humid with abundant rains in summer (from May to readily to environmental change in ways that are easily October) and with total annual precipitations of 4,000 mm measured or observed’’) they constitute a helpful group to and a mean annual temperature of 15.3°C (INEGI 1981). detect habitat disturbances, be by natural causes or by human intervention. The objective of this study was to Vegetation assess the relative impact of human disturbances and natural environmental variation (seasonal) on spider As a reference of the level of disturbance of the study sites, assemblage composition and structure, in two contiguous we recorded the following data for the trees with basal sites of a TMCF in Chiapas, Mexico. Given the condition diameter C5 cm: (1) number of trees, (2) basal diameter of of this diverse and sensitive group, the results of this paper trees, (3) number of trees with visible tracks of cuts made will provide insights into the immediate effects of human with human tools, and (4) a measure of canopy cover in disturbance on key arthropod groups, a taxon that has been each site, based on 90 photographs at 1 m above of the rather neglected in conservation assessments in the ground level. All vegetation data were obtained in an area Neotropics. of 1,800 m2 per site. Fig. 1 Location of the study sites in the Biosphere Reserve Volcán Tacaná, Chiapas, southern Mexico 123
J Insect Conserv
Sampling and identification of spiders there were five samples per site, 30 samples per season and
60 samples per site for the whole study. To evaluate the
Each site was sampled 12 times in two periods (corre- inventory completeness, the estimated species richness was
sponding to the dry and rainy seasons), 3 months (six calculated using EstimateS software version 8.0 (Colwell
samplings) per period, from January to March and from 2007) after 100 randomizations of data. We used only the
June to August 2009. In each site, three 50 m transect strips nonparametric estimators Chao 1 and ACE (Magurran
were established separated by at least 25 m. Along each 2004) to construct species accumulation curves (Gotelli
transect, a circular sampling point (5 m diameter) was and Colwell 2001). To compare species richness values of
established every 10 m for a total of five points per transect, sites, individual-based rarefaction curves were computed
15 per site. Three methods were used, one for each transect. using EcoSim software version 7.0 (Gotelli and Entsminger
Hand collecting consisted in locating visually and catching 2004) to standardize datasets on the basis of number of
spiders, investing 20 min looking through the vegetation individuals and ensure valid comparisons of species rich-
per sampling point, 10 min for high vegetation (from the ness between sites (Gotelli and Colwell 2001). To analyze
waist to the maximum reach of the arm) and 10 min for low the similarity across sites we computed the Sørensen
vegetation (from the ground to waist level) (modified from qualitative index and the Bray-Curtis quantitative index
Coddington et al. 1991), for a total of 40 h of searching (Magurran 2004). These indices were used for comparisons
effort. Vegetation beating was carried out by shaking and between sites per season and for seasons of each site.
striking the vegetation inside each point with a sweeping net Differences in abundance between sites were analyzed by
(low vegetation, N = 30 hits) and a stick (higher vegeta- chi-square tests with contingency tables using JMP soft-
tion, N = 30 hits) with a collecting tray of 1 m2 placed ware version 4.0 (JMP 1989–2000). To analyze the struc-
below to recover the fallen material of the high vegetation, ture of the communities, rank-abundance curves were
for a total of 7,200 hits. Shelter traps were made with fallen drawn for each site and the data were analyzed for differ-
leaves of the local vegetation rolled to form a tube and put ences using Kolmogorov–Smirnov test (Magurran 2004).
each inside a plastic tube (2 cm in length and diameter 1 or We built up a graphical categorization relating frequency
1.5 cm) that were distributed in the vegetation found in each with abundance of each species for each site. In a graph
point. Twenty traps (10 of each size) were placed in each divided in four sections by the average of percent fre-
sampling point 2 weeks previous to a sampling event, on quency in the X axis, and the 2% of total abundance in the
the trunks of the trees, at the branches of the shrubs and the Y axis (Toti et al. 2000; Chen and Tso 2004), each species
herbs, and not higher than 2 m; 2,400 traps were used was classed as dominant (a species that recorded high
throughout the sampling. The sampling team included two frequency and high abundance), constant (high frequency
to four collectors per event. Collected specimens were and low abundance), temporal (high abundance and low
transferred to 80% ethanol and deposited in the Colección frequency) or rare (low frequency and low abundance).
de Arácnidos del Sureste de México (ECOTAAR), located
at El Colegio de la Frontera Sur, Tapachula, Chiapas. All
individuals caught were identified to family level. Adults Results
and most juveniles were sorted to morphospecies and
identified to genus and/or species level whenever possible. Vegetation
For simplicity, the term species will refer to both deter-
mined and undetermined morphospecies. The studied sites clearly differ in the number of trees with
cut (t = -3.863; df = 3; P = 0.0307) and in canopy cover
Data analysis (site: F = 44.196; df = 1,174, P = 0.003; transect (site):
F = 2.3; df = 4,174, P = 0.061). There were no signifi-
To evaluate the relative condition of disturbance within cant differences between sites for the number of trees
sites, we used a two-sample t-test for tree density values (t = 0.532; df = 3; P = 0.316), nor for the basal diameter
and for the number of trees with cuts. A Mann–Whitney values (W = 43856; P = 0.434) (Table 1).
test was applied to measures of basal diameter and a nested
analysis of variance (ANOVA) was used to compare the Spiders
measures of canopy cover between sites. These analyses
were computed using Minitab software version 15.1 A total of 8,370 spiders were collected in 60 samples,
(Minitab 2007). For analyses purposes, a sample was including 1,208 adults (618 females and 590 males) and
integrated with the data corresponding to three points of a 7,162 immatures. Of this total, 623 immature specimens
site (one per transect) in view to include the three sampling (7%) were not assigned to a species because they belong to
methods in each sample, so that for each sampling date genera with two or more species found in the sampling, or
123J Insect Conserv
Table 1 Vegetation variables recorded for the preserved and disturbed sites
Site No. of trees No. of trees with cuts Basal diameter (mean ± SD) Canopy cover (mean % ± SD)
Preserved 219 28 21.37 ± 21.93 87.27 ± 3.92
Disturbed 189 103 19.92 ± 15.85 72.78 ± 13.26
because being too young its morphologic characteristics preserved site and between 94 and 111 in the disturbed site.
did not allow a safe species assigment, so they were not The inventory completeness (ratio of observed to estimated
included in diversity analyses. The following analyses number of species) was lower for the preserved site
consider 7,747 individuals representing 22 families, 71 (77–85%) than for the disturbed site (78–90%) for most
genera, and 112 species (Table 2) (91 species represented estimators, except Jacknife 1 and Bootstrap, which showed
by adults). The proportion of species identified at the no difference between sites (Table 2). Based on Chao 1 and
species level was 36% (41 out of 112 species). Most genera ACE, at least 18 more species are to be expected for the
(53 out of 71, i.e. 74.6%) comprised only one species, some preserved site and between 10 and 13 more species for the
of them were represented just by juvenile specimens. Other disturbed site. When considering each season separately,
juveniles were discriminated as a distinct species based on the pattern of completeness (based on Chao 1 and ACE)
a combination of somatic characteristics (i.e. color pattern, remains comparable as for the whole study in both seasons,
form of abdomen, proportions of several structures) not lower in the preserved (dry 64 and 78%; rainy 81 and 77%)
shared with any other species. Of the total individuals 14% than in the disturbed site (dry 87 and 84%; rainy 88 and
were adults, with Linyphiidae being the most abundant 86%). For the whole study, the curves of Chao 1 and ACE
(421 individuals, 35% of the total of adults), followed by estimators for the disturbed site reach an asymptote, while
Theridiidae (328, 26%), Anyphaenidae (109, 9%), Ther- for the preserved site none of the curves did (Fig. 2a). This
idiosomatidae (81, 7%) and Tetragnathidae (70, 6%). pattern is consistent during the dry season, but it reverses in
the rainy season (Fig. 2b, c). When compared by rarefac-
Alpha diversity tion, the species richness for the total fauna (Fig. 3a) and
for each season (Fig. 3b, c) differs significantly between
For the whole study 94 species were recorded in the pre- the sites at a comparable level of number of individuals,
served site and 86 in the disturbed site; there were 26 with the preserved site recording the highest spider rich-
species (28%) exclusive to the preserved site and 18 (21%) ness in all cases. Concerning species richness, significant
to the disturbed site. In the dry season 19 out of 79 total differences were detected between seasons for each site.
species were exclusive to the preserved site and seven out The rainy season recorded the highest species richness for
of 64 to the disturbed site. In the rainy season 12 out of 79 both preserved and disturbed sites at the same number of
total species were exclusive to the preserved site and eight individuals (Fig. 4).
out of 72 to the disturbed site. For the whole sampling, the
estimators indicate between 103 and 122 species in the Beta diversity
Species composition similarity between sites (as indicated
Table 2 Measures of species richness estimates and percentage by Sørensen index, Table 3) was moderately high for each
(brackets) of completeness for each site
season as for the whole sampling, without exhibiting
Preserved site Disturbed site Total important differences between seasons. When comparing
species composition between seasons, the preserved site
No. of specimens 3,888 3,859 7,747
had a notable lower variation than the disturbed site. The
Observed richness 94 86 112
assemblage structure similarity between sites (as indicated
Number of singletons 19 16 22
by Bray-Curtis index, Table 3) was lower for the rainy than
Number of doubletons 10 11 11
for the dry season, but both sites showed the same level of
ACE 112 (84) 99 (87) 133 (84)
variability between seasons.
Chao 1 112 (84) 96 (90) 134 (84)
Chao 2 111 (85) 99 (87) 138 (81)
Abundance and structure
Jacknife 1 114 (83) 104 (83) 136 (82)
Jacknife 2 122 (77) 111 (78) 149 (75)
For the whole sampling we collected similar numbers
Bootstrap 103 (91) 94 (91) 123 (91) of spiders for preserved (N = 3,888) and disturbed
ICE 112 (84) 100 (86) 133 (84) (N = 3,859) sites. The disturbed site recorded also similar
123J Insect Conserv
140 Preserved - observed data Disturbed - observed data
(a)
Preserved - ACE Disturbed - ACE
120 Preserved - Chao 1 Disturbed - Chao 1
100
80
60
40
20
0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59
No. samples
140 (b)
120
100
80
60
40
20
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
No. samples
140 (c)
120
100
80
60
40
20
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
No. samples
Fig. 2 Accumulation curves of observed species richness and ACE and Chao 1 estimators of each study site for a the whole sampling, b the dry
season and c the rainy season
123J Insect Conserv Fig. 3 Individual-based rarefaction curves depicting spider species richness for each study site with 95% confidence intervals for a the whole sampling, b the dry season and c the rainy season. Vertical lines indicate standardized sample size abundances between seasons, but in the preserved site there in the preserved site for Linyphiidae (X2 = 122.29; df = 1; were more individuals during the dry season in comparison P \ 0.0001) and Araneidae (X2 = 8.68; df = 1; P = with the rainy season (X2 = 101.62; df = 1; P \ 0.0001) 0.003), whereas the inverse occurred for Corinnidae (X2 = (Table 4). Theridiidae, Anyphaenidae, Tetragnathidae and 8.1; df = 1; P = 0.004) and Theridiosomatidae (X2 = 15.52; Linyphiidae were the most abundant families in both sites. df = 1; P \ 0.001). In the disturbed site two species The total abundance of spider families were dependent on recorded an abundance greater than 10%, Theridion the site (X2 = 321.03; df = 21; P \ 0.0001), and for some evexum Keyserling, 1884 (15%) and Anyphaena trifida families, the adult-juvenile proportions showed significant F.O.P.-Cambridge, 1900 (14%), while in the preserved differences between sites, with higher proportions of adults site only one species recorded a comparable abundance, 123
J Insect Conserv
Fig. 4 Individual-based
rarefaction curves depicting
spider species richness with
95% confidence intervals for the
dry and rainy seasons of
a preserved site and b disturbed
site. Vertical line indicates
standardized sample size
Table 3 Values of similarity indices between the preserved and disturbed (whole sampling, dry and rainy seasons), and between the dry and
rainy seasons data sets for each site
Index Total Dry season Rainy Preserved dry Disturbed dry
season versus rainy versus rainy
Sørensen 0.756 0.727 0.728 0.81 0.735
Bray-Curtis 0.583 0.586 0.549 0.592 0.587
Table 4 Spider abundance recorded for each site and season
both sites T. evexum was the dominant species and L. sim-
Season Preserved site Disturbed site Total plex maintains the third place, all other abundant species
change status, but some are in closer ranks in both sites
Dry season 2,380 1,923 4,303
(Anyphaena sp3, A. trifida, Theridiidae sp1, Ameridion
Rainy season 1,508 1,936 3,444
sp1) and others species, common in one site, were absent or
Total 3,888 3,859 7,747
much less common in the other (Erigoninae sp1, Epei-
rotypus sp1, Cyrtognatha sp1, Thymoites sp1, Linyphia
T. evexum (12%). From the 20 most abundant species in sp2, Wendilgarda mexicana Keyserling, 1886). Figure 5
each site (Fig. 5), only 11 species were common in both also shows a trend of a more equitable distribution of
sites, two of these were more abundant in the preserved site abundances for the preserved site in comparison with the
(Anyphaena sp3 and Leucauge simplex F.O.P.-Cambridge, disturbed site. Abundance rank distributions were similar
1903) and eight were more abundant in the disturbed site, between sites, with no statistical differences. Nonetheless,
with three of the latter ones having more than twice the the dominant and subdominant species in the disturbed site
number of individuals (A. trifida, Jalapyphantes cuerna- had a higher proportion that in the preserved site. The
vaca Gertsch and Davis, 1946 and Chrysometa sp1). In graphical categorization of the spiders showed that in the
123J Insect Conserv
Fig. 5 Comparison of the 20 Hentziectypus florens
most abundant spider species in
(a)
Trachelas sp1
a preserved site and b disturbed Metagonia asintal
site Chrysometa sp1
Ameridion sp1
Micrathena lenca
Trachelas sp2
Selenyphantes longispinosus
Mangora sp1
Species
Theridiosoma davisi
Theridiidae sp1
Jalapyphantes cuernavaca
Thymoites sp1
Cyrtognatha sp1
Anyphaena trifida
Epeirotypus sp1
Erigoninae sp1
Leucauge simplex
Anyphaena sp3
Theridion evexum
0 100 200 300 400 500 600
Individuals
Josa nigrifrons
(b)
Chrysometa sp3
Ameridion sp1
Araneus sp1
Theridion adjacens
Anyphaena sp5
Trachelas sp1
Chrysometa sp2
Hentziectypus florens
Species
Linyphia nigrita
Wendilgarda mexicana
Linyphia sp2
Selenyphantes longispinosus
Theridiidae sp1
Chrysometa sp1
Anyphaena sp3
Jalapyphantes cuernavaca
Leucauge simplex
Anyphaena trifida
Theridion evexum
0 100 200 300 400 500 600
Individuals
preserved site there were 12 ‘‘dominant’’ species (13% of a temperate forest in North America, Ibarra-Núñez (1990)
the total), 20 ‘‘constant’’ species (21%) and 62 ‘‘rare’’ with 65 species in coffee foliage in Chiapas, and Ibarra-
species (66%) (Fig. 6a), whereas in the disturbed site there Núñez et al. (2004) and Ibarra-Núñez (unpublished data)
were 13 ‘‘dominant’’ (15%), 13 ‘‘constant’’ (15%) and 60 with 94 species (juveniles included), in cocoa foliage in
‘‘rare’’ ones (70%) (Fig. 6b), showing a lower proportion Chiapas. However, this figure was below others such as
of constant species and a corresponding increase in domi- Sørensen (2003) with 114 species in Tanzania and Álvares
nant and rare species in the disturbed site. et al. (2004) with 153 in Brazil (only the data about adult
spiders from low vegetation). Compared with the above
studies, the species richness is high considering that it was
Discussion collected from a single stratum of vegetation (no spiders
were sampled from soil or canopy), that sampling area was
The species richness found in the understory was higher not extensive (a total of 0.0589 ha for the two sites) and
than in previous similar studies as Coddington et al. (1996) that it was sampled in 24 days (12 for each site). The
with 89 species (adults only), in low vegetation and soil of percentage of identified species (36%) shows that there
123J Insect Conserv
Fig. 6 Graphical categorization (a)
of understory spider species in 1000
function of their frequency and
abundance for a preserved site 1
and b disturbed site. For 3 2
4
briefness, only the names of the 5
7 6
dominant species are listed:
1 = Theridion evexum, 11 9 8
Abundance (log)
2 = Anyphaena sp3, 100 Temporal 10 Dominant
12
3 = Leucauge simplex,
4 = Erigoninae sp1,
5 = Epeirotypus sp1,
6 = Anyphaena trifida,
7 = Cyrtognatha sp1,
8 = Thymoites sp1, 10
9 = Jalapyphantes cuernavaca,
10 = Theridiidae sp1,
11 = Theridiosoma davisi,
12 = Mangora sp1,
13 = Chrysometa sp1,
14 = Selenyphantes Rare Constant
longispinosus, 15 = Linyphia 1
0 10 20 30 40 50 60 70 80 90 100
sp2, 16 = Wendilgarda
mexicana, 17 = Linyphia Frequency (%)
nigrita, 18 = Hentziectypus (b)
florens, 19 = Chrysometa sp2 1000
1
6
3
9
2
13
16 10
15 14
Abundance (log)
100 Temporal 17 19 18 Dominant
10
Rare Constant
1
0 10 20 30 40 50 60 70 80 90 100
Frequency (%)
may be a significant proportion of new species and there- (2002), reaching the comprehensive (70–80%) inventory
fore a high degree of endemism, a distinctive feature of level of Cardoso (2009). So far no work with spiders in
TMCF. tropical regions has achieved a complete inventory.
Chao 1 richness estimator has been used as reference for As in other studies of tropical communities (Coddington
diversity studies of spiders (Coddington et al. 2009; et al. 1991, 1996, 2009; Silva and Coddington 1996;
Sørensen 2003; Sørensen et al. 2002) and was suggested Sørensen et al. 2002), the observed species accumulation
for the study of tropical communities because it performed curves for both sites did not reach the asymptote, indicating
better when most information is concentrated in the species that our sampling effort failed to record all species. How-
of low abundance values (singletons or doubletons) ever, the curves of the estimators for the disturbed site
(Coddington et al. 1996), as in this study. The level of reached an asymptote (both general and for each season,
completeness (C84% with Chao 1) was higher than or except ACE for the rainy season), indicating that sampling
comparable to other intensive studies such as Álvares et al. at this site was sufficient to estimate the richness accurately
(2004), Coddington et al. (2009), Dobyns (1997), Silva and (Coddington et al. 2009). Also, the disturbed site registered
Coddington (1996), Sørensen (2003) and Sørensen et al. higher percentages of completeness. The proportion of
123J Insect Conserv species represented by a single individual (singleton) has effects of light, wind and rain that affects the microclimate, been used as another indicator of the inventory complete- and therefore the community of spiders (Ozanne et al. ness. In tropical regions, the percentage of singletons 2000). The difference between sites is maintained in the recorded in various studies of spiders range from 13 to two seasons, even though there were significant variations 63%, with an average of 37% (Coddington et al. 2009). in relative abundance between the two sites. Rubio et al. Sørensen (2003) recorded 32% in a comparable TMCF site. (2008), also recorded differences in richness sustained Compared with these values, the percentages of singletons among seasons, between two sites in a subtropical dry obtained for both studied sites were relatively low, espe- forest in Argentina. cially considering that there are species represented only by Concerning the observed differences between conditions juveniles, which are not considered in most field assess- (preserved and disturbed) it is clear that (as there were no ments. Considering only adults, the percentage of single- replicates of sites) our conclusions are limited to these tons was 27% for the preserved site and 33% for the sites, nevertheless they agreed with other studies con- disturbed site, representing a better sampling than those cerning the relationship between vegetation structure and obtained in many of the studies cited in Coddington et al. spider diversity (Greenstone 1984; Hatley and MacMahon (2009). 1980; Langellotto and Denno 2004; Pinkus et al. 2006). Coddington et al. (1996) conceived the sample intensity As in the case of other studies of spiders (Rubio et al. index (ratio of number of individuals to observed species 2008; Silva and Coddington 1996; Toti et al. 2000), in our richness) and proposed 10:1 as an appropriate ratio. Sub- study the effect of change of season on species richness sequent studies consider that for sites with high diversity, a was consistent with a significant increase in the rainy relatively adequate sampling intensity must be not less than season for both sites. But in the case of the disturbed site, 30:1 (Cardoso et al. 2009; Sørensen et al. 2002). The this change involved a greater turnover of species between results of this study exceed those values when including all the two periods (in comparison with preserved site), which individuals, although when considering only adults, the showed a greater sensitivity of the spiders of this site to the ratio decreases significantly. The presence of very abun- season effects. dant species can inflate the value of the sample intensity Theridiidae is the richest family in the two sites, both in index without reaching an apparent asymptotic behavior in numbers of genera and species, followed by Linyphiidae the corresponding curve (Toti et al. 2000). For our data the and Araneidae. These results are consistent with other highest sample intensity index in the disturbed site coin- studies of tropical areas, where Theridiidae and Araneidae cides with the reach of the asymptote for the accumulation were among the most diverse (Ibarra-Núñez 1990; Ibarra- curve estimators. Núñez and Garcı́a 1998; Ibarra-Núñez et al. 1995; Silva The difference in species richness between sites, as and Coddington 1996; Sørensen 2004; Sørensen et al. shown by the rarefaction curves, was recorded even though 2002). Linyphiidae is usually rich in species in temperate the sites are close together, which facilitates the recoloni- habitats (Coddington et al. 1996; Toti et al. 2000) but not in zation of the disturbed site. In contrast, Chen and Tso tropical lowland regions, although some studies suggest (2004) whose study sites were not contiguous did not find that its occurrence increases with altitude (Russell and differences in species richness between sites with different Stork 1994; Sørensen 2004) as in the present study. level of disturbance. It appears that the absence of certain species in a given habitat might be due more to the lack of Beta diversity sustainability of the habitat than a limited ability of dis- persion (Samu et al. 1999). In this respect the differences in The similarity between spider communities becomes richness may be related to the effects caused by differences reduced when habitats have different structural complexity in the intensity of use of the two sites. The preserved site (Toti et al. 2000), when they inhabit different vegetation has a more pronounced slope and is farther to the nearest types (even if they are contiguous) (Rubio et al. 2008), or village, therefore is less accessible than the disturbed site, when distance between sites is relatively high ([20 km) where there are multiple paths that cross the area and a (Colwell and Coddington 1994; Sørensen 2004). In our greater mobility of people and domestic animals (horses, study, even when the sites are relatively close (800 m cows, pigs and chickens), yielding a different level of use apart) and have the same vegetation type, the similarity of vegetation that affects the integrity of the structure and between spider communities only reached moderate values, functioning of this forest remnant (Williams-Linera 2007). pointing out that differences in composition and structure The site with lower incidence of cut trees is considered to might be a consequence of different levels of disturbance in have greater complexity, even with a similar density each site. Rubio et al. (2008) showed that the change of between sites, because the cuts result in a lower density of season had an influence on fauna similarity, with the dry vegetation in the canopy, giving more exposure to the season having a lower similarity than the rainy reason. In 123
J Insect Conserv
our study the similarity between sites were alike for each reduction of the material retained on the site involved a
season, but the qualitative similarity between seasons reduction in the number of spiders collected. It is possible
for the preserved site was higher than that of the disturbed that the reduction of dry leaves retained on the site relates
site, suggesting a higher temporal stability in species to the different environmental conditions between the two
composition. sites, because although it is considered that the rains could
moist equally the dry leaves caught in the branches of
shrubs and trees in the two sites, the lower canopy cover in
Abundance and structure the disturbed site would allow greater penetration of sun-
light and wind to help dry the wet leaves in a greater degree
The proportion of adults found in this study (14%) is low than in the preserved site.
compared with other studies where spiders were sampled The distribution of spider abundance of both sites cor-
using pitfall traps (Dias et al. 2005: 69.4%; Indicatti et al. responds to that recorded in other tropical areas, where
2005: 66.8 and 76.8%; see also Álvares et al. 2004), but there is a large proportion of rare species (Coddington et al.
when the sampling of spiders is focused on the vegetation 1996, 2009). Although the rank-abundance analysis
layer, without use of pitfall traps (as in this study), the revealed no differences in the structure of the two com-
proportion of adults is much lower, whether in temperate munities, other data indicate that the preserved site has a
(Brierton et al. 2003: 0.05% of adults; Mason et al. 1997: greater evenness, which coincides with the results of Floren
17.2%) or in tropical sites (Ibarra-Núñez 1990: 8.0%; and Deeleman (2005) where a disturbed tropical forest
Moreno-Molina et al. 2001: 19.5%). Although there are no showed high dominance in comparison with a primary
differences for the total abundance of the two sites, sig- forest. The graphs of the 20 most abundant species of each
nificant differences were observed between the abundance site show different curves with a more pronounced differ-
of adults. Cardoso et al. (2007, 2009) found that habitats ence between dominant and subdominant in the disturbed
with higher tree cover density have higher richness of site. In addition, the results of the graphical categorization
spiders, and suggested that structurally simpler habitats in abundance and frequency showed a greater proportion of
provide less protection against extreme changes in envi- constant species in the preserved site compared to the
ronmental factors, resulting in a lower proportion of adults. disturbed site, which coincidentally had the highest species
This difference is maintained during the dry season but turnover. Overall, these differences suggest a different
disappears in the rainy season. The preserved site had structure of the two communities of spiders, possibly
conditions favoring a greater number of individuals resulting from prevailing structural and environmental
reaching the adulthood (over the entire sample and for the conditions at each site.
dry season), and the rainy season modifies the conditions in The disturbance affects negatively some species while
the disturbed site, allowing parity with the preserved site, others are more tolerant to changes and even favored.
but the latter shows greater stability with minimal variation Within the first group the most affected species were
between the two periods. Epeirotypus sp1, Cyrtognatha sp1, Erigoninae sp1, Thy-
The different seasonal changes in abundance of spiders moites sp1, whose abundance decreased significantly from
for each site, suggests an interaction between the level of the preserved to the disturbed site, so they could be con-
disturbance and environmental conditions. This may be a sidered as susceptible to disruptions in TMCF of Volcán
result of individual species changes (increases or decrea- Tacaná. The increase or decrease in populations is related
ses) from one season to another, but can also be a potential to the reproductive cycle and in tropical regions, the spi-
effect of environmental changes on the conditions of the ders may have multivoltine or univoltine life cycles (Lubin
two sites, which in turn affect the efficiency of some 1978), but often the most abundant peaks are located
methods of collection from one season to another. In the around the time with more abundant resources (i.e. rainy
preserved site the efficiency of the baiting method was 50% season). However, contrary to what was observed in
lower during the rainy season compared to the dry season, another study where the rainy season has a positive influ-
whereas the disturbed site only showed a 3% decrease in ence in abundance due to increased resources (Robinson
efficiency. This change was particularly noted for the et al. 1974), the rainy season appears to be a critical period
amount of dry leaves recovered from samples of the col- for spiders of TMCF of Volcán Tacaná in the preserved site
lecting tray, which was reduced significantly in the rainy because, in spite of maintaining the highest species rich-
season in the preserved site, in reference with the dry ness, its abundance was reduced. As mentioned above, the
season, meanwhile there was no significant decrease in the reduction in the abundance of preserved site is possibly
disturbed site. The dry leaves recovered by this method, related to a decrease of the dry leaves. Four families were
function as shelter for many species of spiders or as web the most abundant at the two sites (Theridiidae, Anypha-
support for small species, similar to leaf litter, so the enidae, Tetragnathidae and Linyphiidae). Theridiidae is
123J Insect Conserv
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gratitude to two anonymous reviewers who suggested valuable
y conservación. Instituto de Ecologı́a, Xalapa, México,
improvements to the manuscript. Spider specimens were collected in
pp 123–134
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