El Colegio de la Frontera Sur
Diversidad de arañas del suelo en cuatro tipos de vegetación
del Soconusco, Chiapas, México
TESIS
presentada como requisito parcial para optar al grado de Maestría en Ciencias en Recursos Naturales y Desarrollo Rural por
David Chamé Vázquez
2015
DEDICATORIA
A mi familia, de quien he aprendido a nunca rendirme, a levantarme una y otra vez no importando las veces que las dificultades nos hayan abatido y continuar en la persecución de nuestros sueños.
"Once more into the fray
Into the last good fight I'll ever know.
Live and die on this day.
Live and die on this day."
GMSG
Sin ti la vida sería una equivocación
AGRADECIMIENTOS
Al Consejo de Ciencia y Tecnología por la beca proporcionada para continuar con mis estudios de posgrado.
Al Dr. Guillermo Ibarra por sus enseñanzas, perseverancia y apoyo durante toda la tesis.
A la Dra. María Luisa Jiménez y al M en C. Héctor Montaño quienes contribuyeron en la dirección de la tesis y por sus atinados comentarios y sugerencias.
A Gabriela Angulo, Eduardo Chamé, Héctor Montaño y Gloria M. Suárez por su ayuda en el trabajo de campo y laboratorio lo que permitió culminar esta tesis.
Al M. en C. Juan Cisneros Hernández, Dra. Ariane Liliane Jeanne Dor Roques y
Dra. Lislie Solís Montero por sus comentarios y sugerencias que ayudaron a mejorar el presente documento.
Al M. en C. Francisco Javier Valle Mora por su asesoría estadística.
A G. Angulo, K. Bernal, E.F. Campuzano, L. Gallegos, F. Gómez, S. D. Moreno y G.
Sánchez por su desinteresada amistad y apoyo durante mi estancia en la colección.
INDICE
Página
Introducción 1
Capítulo de artículo enviado 4
Conclusiones 48
Literatura citada 49
INTRODUCCIÓN
La notable diversidad de ecosistemas y especies del estado de Chiapas es producto de su posición geográfica, amplitud latitudinal, complejidad fisiográfica e historia geológica
(González-Espinosa y Ramírez-Marcial, 2013). La región Soconusco está ubicada en el sureste del Estado de Chiapas, comprende 15 municipios y es importante desde el punto de vista socioeconómico y en recursos naturales. La región es ambientalmente heterogénea, está compuesta principalmente de llanuras y sierras, con elevaciones de hasta 4,080 msnm, sus suelos de profundos a delgados, pueden ser salitrosos o con rocas de origen volcánico. Los climas son cálidos, semi-cálidos y templados, todos con lluvias abundantes en verano (Gobierno de Chiapas, 2011). Esta inmensa heterogeneidad ambiental permite la existencia de múltiples comunidades vegetales y el desarrollo de diversas actividades agropecuarias, como la producción de cacao, café, plátano, mango, caña de azúcar, maíz, palma de aceite, entre otros (Fernández-Bello,
2008).
Las arañas son un componente importante de la diversidad biológica del
Soconusco, por su riqueza de especies y su amplia distribución, tanto en los hábitats naturales como en los modificados por el ser humano. Las arañas como depredadores, son elementos comunes y de gran importancia en el equilibrio ecológico de poblaciones de invertebrados en los bosques tropicales (Coddington y Levi, 1991). En sentido amplio las arañas han tomado relevancia como organismos controladores de plagas en agroecosistemas (Riechert y Bishop, 1990; Ibarra, et al., 2001). En otras regiones del continente americano algunas especies de Ctenidae, Lycosidae y Sparassidae han
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demostrado su utilidad y han sido utilizadas como organismos indicadores de disturbio humano (Bonaldo y Dias, 2010; Rego, Venticinque y Brescovit, 2005).
A pesar de su importancia y utilidad en estudios ecológicos existen pocos trabajos que indaguen a las arañas del suelo. En México, los trabajos conocidos se han realizado en algunos ecosistemas naturales como en selva baja caducifolia (Nieto-Castañeda,
2000); en bosque de Pinus-Quercus (Medina, 2002), en humedales de Baja California
(Nieto-Castañeda, 2004), en matorral desértico (Jiménez y Navarrete, 2010), en bosque mesófilo de montaña (Chamé-Vázquez, 2011), así como en agroecosistemas como cacaotales (Ruiz, 2004).
En México sólo existe un trabajo sobre la diversidad de arañas en un paisaje fragmentado en el sureste del país. Pinkus-Rendón, León-Cortés e Ibarra-Núñez (2006) estudiaron las arañas de un paisaje compuesto por 18 tipos de hábitats, y observaron que la riqueza de especies y la densidad de las arañas difirieron entre hábitats, con los valores de riqueza más altos en hábitats prístinos. Además, señalaron a la cobertura del bosque y la forma de vida de las plantas como las variables más importantes que afectaron la diversidad de arañas de la vegetación, pero no se encontró ninguna correlación entre las arañas del suelo y las variables ambientales analizadas. A diferencia del trabajo anterior, otros estudios han destacado la influencia de otros factores relevantes en la distribución de las arañas del suelo. El tipo de hojarasca, el grado de cobertura arbórea, el tipo de vegetación y la humedad a nivel del suelo afectan al ensamble de arañas, de acuerdo a la temporada del año (Ziesche y Roth, 2008). Sereda y colaboradores (2012) observaron que la distribución de cuatro especies dominantes de
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arañas, en un ambiente heterogéneo del suelo del bosque, estaba determinada por la cobertura de la hojarasca y cobertura de musgo. Entre otros factores determinantes también se han señalado: la proporción de área desprovista o cubierta con hojarasca, la cantidad de ramas o piedras, la forma de las hojas y profundidad de la hojarasca (Bultman y Uetz, 1982; Stevenson y Dindal, 1982; Uetz, 1975) y el tipo de suelo (Gasnier y Höfer,
2001).
Dado que la diversidad y composición de los ensambles de arañas del suelo pueden depender de las características estructurales del suelo y de la vegetación, estudios en regiones donde el paisaje es muy heterogéneo podrían brindar información relevante sobre las variables de mayor importancia que intervienen en la integración de los ensambles de arañas. Por ello, en este estudio analizamos las diferencias en la diversidad y composición de los ensambles de arañas en cuatro tipos de vegetación en la región Soconusco.
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CAPITULO DE ARTÍCULO ENVIADO
Carta de recepción de la revista “Agricultural and Forest Entomology” para el artículo “Soil spiders diversity in four plant communities in the Soconusco region, Chiapas, Mexico.”
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1 Title: Soil spiders diversity in four plant communities in the Soconusco region, Chiapas,
2 Mexico.
3
4
5 Authors’ names: David Chamé-Vázquez, Guillermo Ibarra-Núñez
6
7
8 Authors’ affiliations: El Colegio de la Frontera Sur (ECOSUR). Unidad Tapachula.
9 Carretera Antiguo Aeropuerto Km. 2.5, Tapachula, Chiapas 30700, México.
10
11
12 Contact information: Guillermo Ibarra-Núñez; [email protected]; tel (52) (962)
13 6289800 ext. 5420; Fax (52) (962) 6289800 ext. 5001
14
15 Runing title: Soil spiders diversity in four plant communities
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17 Keywords: agroecosystem, Araneae, assemblage structure, seasonality, soil spider,
18 species diversity
19
5
20 Abstract:
21 1. Environmental heterogeneity is one of the most important factors that explain
22 patterns of species diversity and composition.
23 2. We characterized the structure of soil spider assemblages in a landscape
24 dominated by agroecosystems such as: coffee, cocoa, mango and a medium
25 evergreen forest. Spiders were sampled using pitfall traps and leaf litter samples
26 processed in Berlese funnels.
27 3. We found 139 morphospecies, 105 genera and 39 families. We found differences
28 in diversity among sites and seasons (wet and dry seasons). The coffee
29 agroecosystem had the lowest (q=0) diversity and the mango plantation had the
30 highest (q=1) diversity. Coffee plantation was the only site without differences
31 between seasons. Abundance differed between sites (cacao site had more
32 individuals than mango site) but not between seasons. Structure of the spider
33 assemblage in the coffee plantation had the lowest similarity to the other sites,
34 while cocoa and medium evergreen forest were the more similar sites.
35 4. We could not establish relationships among the environmental factors evaluated
36 in this study and the diversity patterns of spider assemblages. Further research is
37 required to advance our knowledge about the factors that influence how soil
38 spider communities are structured in complex tropical landscapes.
39
40
6
41 Introduction
42 Biodiversity is defined as the variety of living organisms on earth and implies three
43 traditional levels: intraspecific, interspecific and ecosystem diversity (Dirzo & Mendoza,
44 2008; Swingland, 2001). A historic, partial and descriptive measurement of the diversity
45 has typically been the number of species present of a site or habitat. However, the
46 simple task of count the number of species at a site requires a huge effort (Dirzo &
47 Mendoza, 2008; Swingland, 2001).
48
49 Anthropogenic activities such as natural resource exploitation and habitat modification or
50 destruction are the principal causes of biodiversity loss (Dirzo & Mendoza, 2008). These
51 activities may cause species extinction, including those species that have never been
52 discovered, named and without any knowledge of their function in the ecosystem
53 (Wennekes et al., 2012). In this context, the importance of conducting studies that
54 explain diversity patterns, spatial and seasonal variations has been emphasized,
55 particularly as there is no consensus on the theories that explain diversity gradients and
56 how communities are structured (Hsieh & Linsenmair, 2012; Wennekes et al., 2012).
57
58 Environmental heterogeneity is one of the most important factors that explain distribution
59 patterns of species diversity and this relationship can be either positive or negative
60 (Stein et al., 2014). Heterogeneity is defined as a non-random, unequal distribution of
61 the objects that can take many forms and combinations; therefore, the analysis of this
62 pattern is fundamental for the understanding of ecological processes and complex
63 systems functionality (Farina, 2006; Kolasa & Rollo, 1991). Environmental heterogeneity
7
64 is characteristic of a landscape mosaic, it exists at any scale and it is divided into three
65 categories: spatial, temporal and functional (Farina, 2006).
66
67 Spiders, as a predators group, are common and play an important role in the ecological
68 equilibrium of invertebrate populations in tropical forests (Coddington & Levi, 1991).
69 Furthermore, spiders are natural enemies of agroecosystem pest populations (Riechert
70 & Bishop, 1990; Ibarra et al., 2001) and are biological indicators of anthropogenic
71 disturbance (Bonaldo & Dias, 2010; Rego et al., 2005), thus they are potentially
72 sensitive to environmental heterogeneity.
73
74 Other studies indicate that the quantity and quality of leaf litter, degree of tree cover,
75 vegetation type, soil humidity, and moss cover influence on soil spider distribution
76 (Sereda et al., 2012; Ziesche & Roth, 2008). Other factors of the soil such as proportion
77 of bare soil or covered by leaf litter, branches or stones, leaf shape, leaf litter depth
78 (Bultman & Uetz, 1982; Stevenson & Dindal, 1982; Uetz, 1975), soil type (Gasnier &
79 Hofer, 2001) as well as seasonality (Hsieh & Linsenmair, 2012) also determine soil
80 spider distribution.
81
82 Despite their importance and value in ecological studies, few studies have focused on
83 soil spiders in Mexico (Ibarra-Núñez et al., 2011). In addition, the majority of research
84 has been conducted in natural ecosystems and little is known about spider abundance
85 and diversity in agroecosystems. These studies usually focus on quantify the spider
86 diversity only in one type of ecosystem at a time, with the exception of one study that
87 evaluated spider diversity in a fragmented landscape (Pinkus-Rendón et al., 2006).
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88 Given that the diversity and composition of spider assemblages can depend on the
89 structural characteristics of plant communities, studies undertaken in regions where the
90 landscape presents a high degree of heterogeneity can provide us relevant information
91 about the variables that determine the spider assemblages. In the present study, we
92 analysed the differences in the diversity and composition of spider assemblages in four
93 plant communities, in the Soconusco region of the state of Chiapas located at southeast
94 of Mexico. We also analysed seasonal changes in spider assemblages and the
95 relationship with tree cover and microclimate conditions at each site.
96
97 Materials and Methods
98 Study Area
99 The Soconusco region is located in the southeast of the state of Chiapas, Mexico. It
100 presents altitudes range from sea level on the coastal plain to 4,064 m.a.s.l. on the
101 Sierra Madre mountain. There is a diversity of climates along this altitudinal gradient:
102 warm subhumid climate with summer rains at lower levels, a warm humid climate with
103 abundant summer rains at intermediate foothills and a temperate climate at the highest
104 mountainous parts. Precipitation in this region fluctuate between 1,200 - 3,000 mm
105 during the rainy season (from May to October), and between 5 - 800 mm during the dry
106 season (from November to April). The types of plant communities are medium and high-
107 stature evergreen forest, low deciduous forest, pine-oak forest and cloud forest.
108 Besides, there is also a wide variety of agroecosystems that include: cocoa, coffee,
109 banana, mango, sugar cane, corn and oil palm among others (Fernández-Bello, 2008).
110 This study was carried out at four sites within the Soconusco region, each one
111 representing a plant community of economic importance for the region: coffee (CF),
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112 cocoa (CA) and mango (MA) and a remnant of the original vegetation: medium
113 evergreen forest (SM). The CF site is located in the community of Alpujarras in the
114 municipality of Cacahoatán (15°4'20.76"N and 92°9'57.00"W, at an altitude of 1,069
115 m.a.s.l.). The MA site is located in the village of Eisleben in the municipality of
116 Tapachula (14°44'36.10"N and 92°17'0.40"W, at 47 m.a.s.l.). The CA site is located in
117 the town of Huehuetan in the municipality of the same name (15°0'1.80"N and
118 92°26'52.26"W, at 20 m.a.s.l.), and finally the SM site is located on the outskirts of the
119 city of Tapachula (14°54'24.84"N and 92°18'29.40"W, at 124 m.a.s.l.). The sites are
120 separated by a minimum distance of 18 km (Figure 1). Each site differed in vegetation
121 stratification (horizontal and vertical) and composition. The CF is a shade coffee
122 plantation of Coffea arabica L. which shrubs reach a height of 1 to 2 metres. The trees
123 that provide shade are mainly Inga spp. Both coffee and shade trees are subject to
124 periodical pruning. In the CA site there is a medium stratum composed of cacao trees (2
125 to 5 m height) that grow under the shade of fruit and timber trees. The management of
126 this site includes 2 or more pruning cycles during each year, weeding and irrigation via
127 artificial channels. The MA is a plantation of mango (Mangifera indica L.) with scarce
128 understorey and herbaceous layers, although in this plantation those layers are more
129 abundant when it compared to a mechanized mango plantation. The SM site presents
130 herbaceous, shrub and tree layers. In addition, this site had a higher diversity of tree
131 species composition. This site is surrounded by a cattle pasture matrix while sites CA
132 and CF present a less contrasting contiguous matrixes. Another important characteristic
133 of the SM site is a greater heterogeneity of leaf litter composition as well as variation of
134 leaf litter depth. In contrast, site MA had a homogeneous and shallow leaf litter layer.
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135 While sites CF and CA display a deeper and more heterogeneous leaf litter layer than
136 site MA.
137
138 Climatic Variables and Canopy Cover
139 During the study period, temperature and relative humidity were measured slightly
140 above ground level every 30 minutes using a datalogger (LASCAR model EL-USB-2) at
141 each site. The estimation of tree cover percentage was carried out using planar
142 photography according to Korhonen & Heikkinen (2009). The percentage was the mean
143 of 40 photographs per site (five photographs on each side of each transect) that were
144 taken during May, 2014. The images were processed using MATLAB version 8.0 and a
145 modification of the Canopy Analysis script (Lobet et al., 2013).
146
147 Spider sampling
148 Four transects, each one with 50 m of length and separated at least by 25 m were
149 established at each site. We sampled every month in two periods: the dry season
150 (February-March) and rainy season (June-July-August), in order to assess seasonal
151 variations in spider assemblages.
152
153 Five pitfall traps were placed in each transect (removed after 72 hours) and 3 leaf litter
154 samples were taken. Each trap, buried at ground level, had 8 cm of diameter and
155 contained 200 ml of an aqueous solution of 50% propylene glycol. A fixed cover was
156 placed 3 cm above the trap to reduce plant residues and rain. Each leaf litter sample
157 comprised a 50 x 50 cm of area, alternating the side of the transect where the sample
158 was taken each sampling date in order to avoid previously sampled zones (previously
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159 marked with plastic tape). Each sample of leaf litter was processed in a Berlese funnel
160 over a period of two to three days to extract the spiders. The collected specimens were
161 placed in containers with 80% alcohol and subsequently quantified and identified to
162 species or morphospecies level. Species determination was carried out initially using
163 family and genus keys (Jocque & Dippenaar-Schoeman, 2007; Ubick et al., 2005) and
164 then specialized literature. Specimens were deposited in the Colección de Arácnidos del
165 Sureste de México (CASEM) at the El Colegio de la Frontera Sur (ECOSUR). The
166 spiders were collected under the scientific collection license number FAUT-0198 from
167 the Dirección de General de Vida Silvestre, SEMARNAT (SGPA/DGVS/00102/14 13
168 January 2014).
169
170 Data Analysis
171 The majority of the statistical analyses were performed with R software (R Core Team
172 2014). In order to compare the percentage of tree canopy cover between sites, we used
173 a Kruskal-Wallis test followed by multiple comparisons using the “kruskal” function in the
174 “agricolae” software package (Mendiburu, 2014). Prior to the analysis, an angular
175 transformation was applied to the percentage values. In order to compare temperature
176 and humidity among sites, a multivariate analysis of variance (MANOVA) and an
177 analysis of canonical variables were applied using the “candisc” package (Friendly &
178 Fox, 2013).
179
180 We determined species diversity and composition by site, season and as a whole. To
181 estimate the sampling completeness of each type of vegetation, the non-parametric
182 Chao 1 estimator was applied using the “estimateR” function in the “vegan” software
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183 package (Oksanen et al., 2015). The Chao 1 estimator uses the number of singletons
184 (number of species represented by one individual) and doubletons (number of species
185 represented by two individuals) to estimate the number of missing or unobserved
186 species. Other studies consider it this estimator to be robust (Hsieh & Linsenmair, 2012;
187 Sørensen et al., 2002).
188
189 Diversity among sites and seasons was evaluated by rarefaction and extrapolation
190 curves, using Hill’s first two numbers (a family of diversity measures to quantify diversity
191 in units of equivalent numbers of equally abundant species), according to Chao et al.
192 (2014). The final comparisons were made using the double of the reference sample
193 size, in other words the number of individuals with the lower abundance was used as a
194 reference (Chao et al., 2014). The curves were generated by implementing iNext in R
195 (Hsieh et al., 2014).
196
197 The relative abundance of spider families at each site were compared (families with 20
198 or fewer individuals were grouped into one category). A nested analysis of variance
199 (ANOVA) and a post hoc test (Tukey multiple comparisons) were used to determine any
200 differences in abundance among sites and between seasons. Prior to the ANOVA test,
201 the abundances were log transformed in order to meet the assumptions of the analysis.
202 Assemblage structure, based on species abundance, was analyzed by graphic
203 categorization. This was implemented by creating dispersion graphics for each site,
204 divided into four sections by using the frequency percentage mean on the X axis and 2%
205 of the total species abundance on the Y axis (Barba et al., 2010; Maya-Morales et al.,
206 2012).
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207 To examine similarity in the composition and structure of the spider assemblages for
208 different vegetation types, NMDS (nonmetric multidimensional scaling) was used as a
209 multivariate technique, for which a similarity matrix was previously calculated using the
210 Bray-Curtis index. Subsequently, the NMDS was calculated 100 times using different
211 initial configurations to obtain the minimum stress, using the “bestnmds” function within
212 the “labdsv” software package (Bordcar et al., 2011; Roberts, 2013)
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214 Results
215 Environmental Variables
216 We found differences in mean temperature and humidity among sites (MANOVA, Pillai’s
217 trace=0.97, F=141.2, df= 3,888, P<0.05). The analysis of canonical variables (Table 1,
218 Fig. 2), revealed that the CF site clearly differed from the remaining sites, with the lowest
219 mean daily temperature and the highest mean daily relative humidity. The percentage of
220 tree cover also differed among sites (X2 = 8.32, df=3, P<0.05); multiple comparisons
221 revealed a difference between the MA and SM sites (Table 2).
222
223 Abundance and Species Composition
224 In total, 3406 spiders were collected from all sites during both seasons. As 326
225 specimens corresponded to early development phases and consequently lacked the
226 necessary morphological characteristics for correct identification to species level, these
227 were excluded from the subsequent analysis.
228
229 Of the 3080 identified spiders, approximately 65% (2011) were juveniles, 22% (685)
230 females and 12% (384) males, representing 139 species, 105 genera and 39 families, of
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231 which there are possibly 12 new species and a new genus belonging to the Linyphiidae
232 family (Appendix 1). Salticidae is the family with the highest number of species (24),
233 followed by Theridiidae (21), Linyphiidae (13) and Oonopidae (10). The most abundant
234 families were Lycosidae (503 specimens), followed by Ochyroceratidae (452),
235 Linyphiidae (388), Theridiidae (320) and Oonopidae (285). The most abundant species
236 in the entire study was a ochyroceratid spider: Theotima minutissimus (Petrunkevitch,
237 1929) with 445 specimens.
238
239 Species Richness and Sampling Completeness
240 Observed values of species richness were: the SM site presented the highest number of
241 species (63 spp), followed by MA (58), CA (57) and finally CF (32). The percentage of
242 singletons was highest at the CA site (37%) followed by the SM site (35%), MA (33%)
243 and finally CF (9%). The richness estimations indicated an expected number of 32.6
244 species for the CF site, 76.1 for CA, 79.4 for MA and 88.7 for SM. The completeness
245 values of the samples were greater than 70% in all sites (SM=71%, MA=73%, CA=74%
246 and CF=98%) indicating a comprehensive inventory according to the levels suggested
247 by Cardoso (2009).
248
249 Diversity Comparisons
250 When the obtained diversity values by rarefaction were compared (q=0) it was observed
251 that only the CF site, the least diverse, differed from the others, (Fig. 3a). When
252 considering the relative abundance of the species (q=1), there were no differences
253 between the CF and CA sites (Fig. 3b), both recorded the lowest levels of diversity. The
254 MA site presented an estimated diversity (q=1) equal to a theoretical community of
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255 23.28 species, where each species had the same abundance. This site was 1.3 times
256 more diverse than the SM site, 1.9 times more diverse than the CA site and 2.25 times
257 more diversity than CF site (Fig. 3b). In contrast, SM presented 1.7 times the diversity
258 found at site CF and 1.5 times the diversity at site CA, while site CF presented only 0.88
259 of the diversity recorded at site CA.
260
261 When comparing estimated diversity (q=0) between the dry and rainy seasons, only
262 sites CA and SM had higher diversity during the dry season (Fig. 4a). Considering
263 abundance (q=1) and the differences observed for q=0, site MA recorded greater
264 diversity during the dry season than rainy season (three times more than in the rainy
265 season in site SM, more than twice in CA and 1.7 times in MA, Fig 4b).
266
267 When the sites were compared according to season, sites CA and MA differed in
268 diversity (q=0 y q=1) during the wet season (Fig. 5a). During the dry season, site CF had
269 lower diversity (q=0 y q=1) than the remaining sites; however, for diversity of order 1,
270 site CA differs from site SM but not from site MA (Fig. 5b).
271
272 Abundance and Graphic Categorization
273 The numbers of individuals per site were: 517 in MA, 525 in CF, 890 in SM and 1148 in
274 CA. No differences in seasonal abundance were found but there were differences
275 between sites (nested ANOVA: Season F=0.0268, df=1, P>0.05; Site F=15.22, df=3,
276 P<0.05; Site: Transect F=6.12, df=12, P>0.05); only spider abundance at the CA site
277 differed from the MA site. Differences were observed in abundance distribution by family
278 at each site (Fig. 6). For example, the Ochyroceratidae is the dominant family at the CA
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279 site, Lycosidae at the CF site, Titanoecidae at the MA site and Linyphiidae at the SM
280 site.
281
282 Graphic categorization revealed differences between sites. Each site possess a
283 particular structure when taking into account the frequency and abundance of each
284 species (Fig. 7). Castianeira sp4 was the only constant species (i.e. very frequent but
285 not very abundant) at the CF site. This site presented seven dominants species with the
286 remaining species categorized as rare (low frequency and low abundance).
287 Furthermore, site CF does not share any of its dominant species with the remaining
288 sites. However, when the other sites are compared, these shared several dominant
289 species and contained a higher number of constant species. Spider assemblage
290 structure differed among sites as is shown in the ordination graphic, where transects
291 from the same site clearly resemble more each other than those of the other sites (Fig.
292 8). The spider assemblage structure of the CF site is clearly very different from the
293 remaining sites, while CA and SM had a higher similarity.
294
295 Discussion
296 Differences in temperature and humidity among sites are attributed to changes in
297 altitude (Körner, 2007). We observed this pattern as CF site recorded the lowest
298 temperature and the highest humidity that differed from the rest of the sites. This
299 differences are probably due to variations in altitude; while CF site is at approximately
300 1,069 m.a.s.l., the remaining sites do not pass 129 m.a.s.l. The only difference in
301 canopy cover was between sites MA and SM; this does not imply any similitude in all
302 other variables of canopy structure since two o more sites could have no differences in
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303 the amount of canopy cover but could present differences in structural heterogeneity
304 (canopy composition, above ground height, density and foliage thickness) as a result of
305 the dynamic history of the forest stand (Lieberman et al., 1989).
306
307 According to methodology used in this study to estimate climate and canopy cover data
308 we can’t relate these with the diversity and abundance patterns observed. However, two
309 studies conducted in the same region of this study discuss the relationship between
310 environmental and structural variables in specific spider communities. Pinkus-Rendón et
311 al. (2006) did not found a relationship between tree cover, plant life forms, leaf litter
312 depth, proportion of bare soil, grass, leaf litter and soil spider diversity or abundance
313 during any of the seasons evaluated; however, they found a positive relationship during
314 the wet season between epigeal spider, tree cover and plant life form diversity. Hajian-
315 Forooshani et al. (2014) presented evidence that tree cover, coffee grove tree density,
316 and altitude influence the diversity and abundance of spiders from tree canopy. In
317 addition, many studies have highlighted a relationship between environmental or
318 seasonal heterogeneity and the structure of soil spider assemblages (Ziesche & Roth,
319 2008; Sereda et al., 2012; Bultman & Uetz, 1982; Mineo et al., 2010).
320
321 The values for completeness provide sufficient sustenance for the analysis derived from
322 the data obtained. Cardoso (2009) considers that achieving 100% of completeness is
323 impractical for arthropods because the sampling required an immense effort. Other
324 studies have obtained completeness values similar to ours (Azevedo et al., 2014;
325 Coddington et al., 2009; Hsieh & Linsenmair, 2011; Maya-Morales et al., 2012;
326 Sørensen et al., 2002). However, the percentage of obtained singletons (with the
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327 exception of the CF site), correspond to the mean of other studies on arthropod diversity
328 (Azevedo et al., 2014; Coddington et al., 2009; Hsieh & Linsenmair, 2011). This
329 indicates an undersampling bias for these sites where singletons represent
330 approximately a third of all the spider community species. It has been suggested that
331 rarity measured as frequency is a consequence of phenological or edge effects (Scharff
332 et al., 2003) and it is possible that some of these effects are also responsible for the
333 high number of singletons found at the three sites previously mentioned. The CF site
334 had the highest sampling integrity (indicated by the percentage of completeness and
335 singletons) but had the lowest abundance and lowest richness of all sites. We could not
336 explain these differences nor how much are them related with differences among sites
337 as agronomic management, lanscape contrast and altitude among others.
338
339 High species richness of the families Salticidae, Theridiidae and Linyphiidae has also
340 been observed by other authors for different habitats in tropical regions (Ibarra-Núñez et
341 al., 2011; Dias et al., 2005; Indicatti et al., 2005; Rodrigues et al., 2010). Moreover, most
342 families in each assemblage are represented by few species and individuals, a
343 characteristic mentioned in other studies within the tropical region (Ibarra-Núñez et al.,
344 2011; Mineo et al., 2010; Indicati et al., 2005).
345
346 When we considered the spider assemblages of each site, the low species richness and
347 diversity observed in site CF, are possibly related to the altitude. Hajian-Forooshani et
348 al. (2014) observed that altitude was the most important variable that contributed to
349 differences in richness of canopy spiders but they considered also the impact of habitat
350 type and landscape heterogeneity in those groups of spiders that appear to be
19
351 insensitive to altitudinal gradients. The highest estimated diversity (q=1) of site MA,
352 could be related to the presence of shrub and herbaceous strata that increased ground-
353 level heterogeneity. This is particularly relevant, especially because several authors
354 ascribe the formation of different spider communities to different plant community
355 structure (Bowden & Buddle, 2010; Foord et al., 2008; Jiménez-Valverde & Lobo, 2007).
356
357 Reductions in diversity at the sites CA and SM (q=0) and CA, SM y MA (q=1) during the
358 rainy season, without any variations in respective abundances, are difficult to explain. A
359 possible explanation is an increase in humidity at both the soil and leaf litter levels as
360 one of the factors that caused this difference. However, this would affect abundance
361 first, something that we did not found this study. The reasons for seasonal variations in
362 diversity at the above sites are unknown; however, the fact that seasonality does not
363 appear to affect diversity at the CF site is even more intriguing. A posible explanation
364 may be that this site is traditionally managed with coffee bushes grown in the shade
365 provided by several tree species, resulting in a much less variable microclimate than a
366 monoculture agroecosystem subject to direct sunlight (Barradas & Fanjul, 1986). The
367 steeper slopes at the CF site could also contribute to a less variable microclimate, as
368 steeper slopes allow greater soil drainage, moderating extreme variation in humidity in
369 contrast with the other sites. Other studies have indicated a discernible change in
370 species diversity between seasons for soil spiders (Mineo et al., 2010), understorey
371 spiders (Maya-Morales et al., 2012) and canopy spiders (Hsieh & Linsenmair, 2012).
372
373 Although our results suggest that there is no difference in total abundance between
374 seasons, differences between sites were evident. Contrary to our results, other studies
20
375 demonstrated a seasonal variation in abundance. For example Mineo et al. (2010)
376 observed an increase in soil spider abundance during the rainy season in three Brazilian
377 savannahs, while in a study of cloud forest in Mexico, Maya-Morales et al. (2012) did not
378 observe any seasonal variations in abundance of understorey spiders in a perturbed
379 site, while in a preserved site there was more abundance during the dry season. The
380 depth of leaf litter could explain why CA site had higher abundance than MA site.
381 Theotima minutissimus, a small weaver spider was the dominant species in the CA site
382 with the deepest litter layer, contrasting with the dominance of the running spiders
383 Goeldia mexicana and Teminius hirsutus in the shallow leaf litter of the MA site. Wagner
384 et al. (2003) observed a vertical stratification of abundance that depended on hunting
385 strategies, where running and weaver spiders were abundant in the upper and
386 medium/lower strata respectively and a concurrent spider size decreased along a
387 continuum from the upper to the lower strata. In addition, climate factors or those related
388 to vegetation or landscape structure could influence the observed differences in
389 abundance at each site.
390
391 We obtained more specimens from the leaf litter processed using Berlese funnels (2411
392 specimens) than with the pitfall traps (669 specimens), although the latter is considered
393 the typical sampling technique used in studies of soil spiders (Patrick & Hansen, 2013).
394 Nevertheless, Sabu and Shiju (2010) considered both sampling techniques as
395 complementary for capturing ground-dwelling arthropods. Other studies consider only
396 adult specimens to analyze diversity, but in this study we included also juveniles as
397 Jimenez-Valverde & Lobo (2006) assert that the inclusion of juveniles allows a reliable
398 estimation in diversity studies (Jimenez-Valverde & Lobo, 2006).
21
399 In the structure of spider assemblages (i.e. abundance and species composition), the
400 CF site had one constant species and does not share any dominant species with the
401 remaining sites, although it shares other species. The sites CA, MA and SM shared
402 dominant species such as Ctenus calcaratus and Dictyna sp1, and also shared some
403 constants and rare species. For example, the Lycosidae family is present at all sites,
404 with two dominant species in three sites: Pirata sp1 (CF), Schizocosa sp1 (SM and CA);
405 however, this family is rare at the MA site. The higher similarity among transects of the
406 same site and the higher similarity among CA, SM and MA could be explained by the
407 distance among transects and sites, since environmental similarity among sites
408 decreases as the distance among them increases and the spatial configuration of the
409 landscape and time could sort the species by differences on dispersal abilities (Nekola &
410 White, 1999).
411
412 Undoubtedly, we are still far from understanding the factors that are involved in
413 community structuring, elements that certainly differ according to taxonomic group
414 (Fukami, 2009). In this study, similitudes and differences in species assemblages could
415 be related to specific environmental conditions that are present at each site. Samu,
416 Sunderland & Szinetár (1999) indicate the existence of many scale-dependent variables
417 that affect survival, reproduction and dispersion of spiders in agroecosystems.
418 Furthermore, other studies have suggested the importance of the life-history of each
419 species (Jimenez & Navarrete, 2010) and disturbance (Ibarra-Núñez & Chamé-Vázquez
420 unpublished data) in order to explain the structure of assemblages. Undoubtedly, the
421 factors that appear to regulate the space-time patterns of soil biota are principally
22
422 related to environmental heterogeneity, since this heterogeneity provides possibilities for
423 resource or habitat specialization, in other words niche-partitioning (Berg, 2009).
424 However, some studies indicate that the spatial distribution of some spider species
425 could be explained also by biological interactions, as inter and intraspecific predation
426 (Dor & Hénaut, 2011; Wise, 1993).
427
428 Although our study possesses many limitations, such as the fact that a satisfactorily
429 relationship could not be established between several variables and the spider
430 assemblages, ours the results showed patterns of family richness that are consistent
431 with other studies carried out in tropical regions. Furthermore, forest mass heterogeneity
432 has a definite influence on the structure of spider assemblages while seasonal and
433 landscape heterogeneity shapes spider diversity and abundance. In effect, the lowest
434 diversity presented by the CF site is probably determined by altitude. Certainly, aspects
435 of future research should focus on both the unravelling of spatial and seasonal
436 heterogeneity into separate elements and taking into consideration the effect of spatial
437 scale, to comprehend to what extent do multiple factors structure spider communities.
438
23
439 Acknowledgements
440 We are grateful to G. Angulo, E.R. Chamé, H. Montaño and G.M. Suárez (ECOSUR) for
441 their help during the sampling and sorting of spiders. J. Valle-Mora (ECOSUR) provided
442 support for the statistical analysis. M.L. Jimenez (CIBNOR), J. Cisneros, A.L.J. Dor, H.
443 Montaño and L. Solís (ECOSUR) contributed with numerous comments that helped
444 improve the final version of this manuscript. The authors want to thanks to Consejo
445 Nacional de Ciencia y Tecnología for the scholarship to DCV.
24
Literature cited
Azevedo, G.H.F., Faleiro, B.T., Magalhães, I.L.F., Benedetti, A.R., Oliveira, U., Pena-
Barbosa, J.P.P., Santos, M.T.T., Vilela, P.F., de Maria, M. & Santos, A. J. (2014)
Effectiveness of sampling methods and further sampling for accessing spider
diversity: a case study in a Brazilian Atlantic rainforest fragment. Insect
Conservation and Diversity, 7, 381-391.
Barba, E, Juárez-Flores, J. & Estrada-Loreto, F. (2010) Distribución y abundancia de
crustáceos en humedales de Tabasco, México. Revista Mexicana de
Biodiversidad, 81(Suppl),153-163.
Barradas, V.L. & Fanjul, L. (1986) Microclimatic chacterization of shaded and open-
grown coffee (Coffea arabica L.) plantations in Mexico. Agricultural and Forest
Meteorology, 38, 101-112.
Berg, M.P. (2009) Spatio-temporal structure in soil communities and ecosystem
processes. Community Ecology: Processes, Models, and Applications (ed. by
Verhoef, H.A. & P.J. Morin), pp.69-80. Oxford University Press, New York.
Bonaldo, A.B. & Dias, S.C. (2010) A structured inventory of spiders (Arachnida,
Araneae) in natural and artificial forest gaps at Porto Urucu, Western Brazilian
Amazonia. Acta Amazonica, 40(2), 357-372.
Borcard, D., Gillet, F. & Legendre, P. (2011) Numerical Ecology with R. Springer-Verlag
New York: New York.
Bowden, J.J. & Buddle, C.M. (2010) Determinants of Ground-Dwelling Spider
Assemblages at a Regional Scale in the Yukon Territory, Canada. Ecoscience,
17(3), 287-297.
25
Bultman, T.L. & Uetz, G.W. (1982) Abundance and community structure of forest floor
spiders following litter manipulation. Oecologia, 55(1), 34-41.
Cardoso, P. (2009) Standardization and optimization of arthropod inventories-the case
of Iberian spiders. Biodiversity and Conservation, 18, 3949-3962.
Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K. & Ellison, A.M.
(2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling
and estimation in species diversity studies. Ecological Monographs, 84, 45-67.
Coddington, J.A. & Levi, H.W. (1991) Systematics and Evolution of Spiders (Araneae).
Annual Review of Ecology and Systematics, 22(1), 565-592.
Coddington, J.A., Agnarsson, I., Miller, J.A., Kuntner, M. & Hormiga, G. (2009)
Undersampling bias: the null hypothesis for singleton species in tropical arthropod
surveys. Journal of Animal Ecology, 78, 573-584.
Dias, M.D.F.D.R., Brescovit, A.D. & Menezes, M. De (2005) Aranhas de solo
(Arachnida: Araneae) em diferentes fragmentos florestais no sul da Bahia, Brasil.
Biota Neotropica, 5,141-150.
Dirzo, R. & Mendoza, E. (2008) Biodiversity. Encyclopedia of Ecology. (ed. by E.
Jorgensen & Fath, B.). Elsevier, Amsterdam.
Dor, A. & Hénaut, Y. (2011) Are cannibalism and tarantula predation factors in the
spatial distribution of the wolf spider Lycosa subfusca (Araneae Lycosidae)?
Ethology Ecology & Evolution, 23, 375-387.
Farina, A. (2006) Principles and Methods in Landscape Ecology.Springer Netherlands,
Dordrecht.
Fernández-Bello, E. (2008) La producción agropecuaria en el Soconusco e intercambio
con Centroamérica. La Frontera Sur. Reflexiones sobre el Soconusco, Chiapas, y
26
sus problemas ambientales, poblacionales y productivos. (ed. by J. E. Sánchez &
R. Jarquin). pp. 185–200. Senado de la República-ECOSUR, Mexico.
Foord, S.H., Mafadza, M.M., Dippenaar-Schoeman, A.S. & Van Rensburg, B.J. (2008)
Micro-scale heterogeneity of spiders (Arachnida: Araneae) in the Soutpansberg,
South Africa: a comparative survey and inventory in representative habitats.
African Zoology, 43(2), 156-174.
Friendly, M. & Fox, J. (2013) candisc: Visualizing Generalized Canonical Discriminant
and Canonical Correlation Analysis. R package
version 0.6-5. http://CRAN.R-project.org/package=candisc
Fukami, T. (2009) Community assembly dynamics in space. Community Ecology:
Processes, Models, and Applications (ed. by Verhoef, H.A. & P.J. Morin), pp.45-
54. Oxford University Press, New York.
Gasnier, T.R. & Höfer, H. (2001) Patterns of abundance of four species of wandering
spiders (Ctenidae, Ctenus) in a forest in central Amazonia. Journal of
Arachnology, 29(1), 95-103.
Hajian-Forooshani, Z., Gonthier, D. J., Marín, L., Iverson, A. L., & Perfecto, I. (2014)
Changes in species diversity of arboreal spiders in Mexican coffee
agroecosystems: untangling the web of local and landscape influences driving
diversity. PeerJ, 2, e623.
Hsieh, T.C., Ma, K.H. & Chao, A. (2014) iNEXT: An R package for interpolation and
extrapolation in measuring species diversity. [WWW document]. URL
http://chao.stat.nthu.edu.tw/blog/software-download/inext-r-package/ [accessed
on 5 January 2015].
27
Hsieh, Y.L. & Linsenmair, K.E. (2011) Underestimated spider diversity in a temperate
beech forest. Biodiversity and Conservation, 20(13), 2953-2965.
Hsieh, Y.L. & Linsenmair, K.E. (2012) Seasonal dynamics of arboreal spider diversity in
a temperate forest. Ecology and Evolution, 2(4), 768-777.
Ibarra-Núñez, G., García, J.A., Moreno, M.A., López, J.A., y Lachaud, J.P. (2001) Prey
analysis in the diet of some ponerine ants (Hymenoptera: Formicidae) and web-
building spiders (Araneae) in coffee plantations in Chiapas, Mexico. Sociobiology,
37(3B), 723-755.
Ibarra-Núñez, G., Maya-Morales, J. & Chame-Vázquez, D. (2011) Las arañas del
bosque mesófilo de montaña de la Reserva de la Biosfera Volcán. Revista
Mexicana de Biodiversidad, 82, 1183-1193.
Indicatti, R.P.; Candiani, D., Brescovit, A.D. & Japyassu, H. F. (2005) Diversidade de
aranhas (Arachnida, Araneae) de solo na bacia do reservatório do Guarapiranga,
São Paulo, São Paulo, Brasil. Biota Neotropica, 5(1a), 151-162.
Jimenez, M.L. & Navarrete, J.G. (2010) Fauna de arañas del suelo de una comunidad
árida-tropical en Baja California Sur, México. Revista Mexicana de Biodiversidad,
81, 417-426.
Jiménez-Valverde, A. & Lobo, J.M. (2006) Establishing reliable sampling protocols for
spider (Araneae, Araneidae & Thomisidae) assemblages: estimation of species
richness, seasonal coverage and effect of juvelines on species richness and
composition. Acta Oecologica, 30, 21-32.
Jiménez-Valverde, A. & Lobo, J.M. (2007) Determinants of local spider (Araneidae and
Thomisidae) species richness on a regional scale: Climate and altitude vs. habitat
structure. Ecological Entomology, 32, 113–122.
28
Jocque, R. & Dippenaar-Schoeman, A.S. (2007) Spider Families of the World. Royal
Museum for Central Africa, Tervuren.
Kolasa, J. & Rollo, C.D. (1991) Introduction: the heterogeneity of heterogeneity: a
glossary. Ecological Heterogeneity (ed. by Kolasa, J. & S.T.A. Pickett), pp.1-23.
Springer-Verlag, New York.
Korhonen, L. & Heikkinen, J. (2009) Automated analysis of in situ canopy images for the
estimation of forest canopy cover. Forest Science, 55(4), 323-334.
Körner, C. (2007) The use of “altitude” in ecological research. Trends in Ecology &
Evolution, 22(11), 569-74.
Lieberman, M., Lieberman, D. & Peralta, R. (1989) Forest are not just swiss cheese:
canopy stereogeometry of non-gaps in tropical forests. Ecology, 70(3), 550–552.
Lobet G., Draye X. & Périlleux C. (2013) An online database for plant image analysis
software tools. Plant Methods, 9 (38) [WWW document]. URL
http://www.plantmethods.com/content/9/1/38 [accessed on 20 March 2014]
Maya-Morales, J., Ibarra-Núñez, G., León-Cortés, J. L. & Infante, F. (2012) Understory
spider diversity in two remnants of tropical montane cloud forest in Chiapas,
México. Journal of Insect Conservation, 16, 25-38.
Mendiburu, F. (2014) Agricolae: Statistical Procedures for Agricultural Research. R
package version 1.2-1. http://CRAN.R-project.org/package=agricolae
Mineo, M.F., Del-Claro, K. & Brescovit, A.D. (2010) Seasonal variation of ground
spiders in a Brazilian Savanna. Zoologia (Curitiba), 27(3), 353-362.
Nekola, J.C. & White, P.S. (1999) The distance decay of similarity in biogeography and
ecology. Journal of Biogeography, 26(4), 867-878.
29
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B.,
Simpson, G.L., Solymos, P., Stevens, M.H.H. & Wagner, H. (2015) vegan:
Community Ecology. Package. R package version 2.2-1. http://CRAN.R-
project.org/package=vegan
Patrick, L.B. & Hansen, A. (2013) Comparing ramp and pitfall traps for capturing
wandering spiders. Journal of Arachnology, 41(3), 404-406.
Pinkus-Rendón, M.A., León-Cortés, J.L. & Ibarra-Núñez, G. (2006) Spider diversity in a
tropical hábitat gradient in Chiapas, Mexico. Diversity and Distributions, 12, 61-
69.
R Core Team. 2014. R: A language and environment for statistical computing. version
3.2.0. http://cran.r-project.org/
Rego, F.N.A.A., Venticinque, E.M. & Brescovit, A.D. (2005) Densidades de aranhas
errantes (Ctenidae e Sparassidae, Araneae) em uma floresta fragmentada. Biota
Neotropica, 5(1A), 45-52.
Riechert, S.E. & Bishop, L. (1990) Prey control by an assemblage of generalist
predators: spiders in garden test systems. Ecology, 71, 1441-1450.
Roberts, D.W. (2013) labdsv: Ordination and Multivariate Analysis for Ecology. R
package version 1.6-1. http://CRAN.R-project.org/package=labdsv
Rodrigues, E.N.L., Mendoca Jr, M.S., Rosado, J.L.O. & Loeck, A.E. (2010) Soil spiders
in differing environments: Eucalyptus plantations and grasslands in the Pampa
biome, southern Brazil. Revista Colombiana de Entomología, 36(2), 277-284.
Sabu T.K. & Shiju, R.T. (2010) Efficacy of pitfall trapping, Winkler and Berlese extraction
methods for measuring ground-dwelling arthropods in moist-deciduous forests in
the Western Ghats. Journal of Insect Science, 10(98), 1-17
30
Samu, F., Sunderland, K.D. & Szinetár, C. (1999) Scale-Dependent Dispersal and
Distribution Patterns of Spiders in Agricultural Systems: A Review. Journal of
Arachnology, 27(1), 325-332
Scharff, N., Coddington, J.A., Griswold, C.E., Hormiga, G. & Bjørn, P.D.P. (2003) When
To Quit? Estimating Spider Species Richness in a Northern European Deciduous
Forest. Journal of Arachnology, 31, 246-273.
Sereda, E., Blick, T., Dorowb, W.H.O., Woltersa, V., & Birkhofer, K. (2012) Spatial
distribution of spiders and epedaphic Collembola in an environmentally
heterogeneous forest floor hábitat. Pedobiologia, 55, 241-245
Sørensen, L.L., Coddington, J.A., & Scharff, N. (2002) Inventorying and estimating
spider diversity using semi-quantitative sampling methods in an afrotropical
montane forest. Environmental Entomology, 31, 319-330.
Stein, A., Gerstner, K. & Kreft, H. (2014) Environmental heterogeneity as a universal
driver of species richness across taxa, biomes and spatial scales. Ecology
Letters, 17, 866-880.
Stevenson, B.G. & Dindal, D.L. (1982) Effect of leaf shape on forest litter spiders:
community organization and microhabitat selection of immature Enoplognatha
ovata (Clerck) (Theridiidae). Journal of Arachnology, 10(2), 165-178.
Swingland, I. R. (2001) Biodiversity, Definition of. Encyclopedia of Biodiversity (ed by
S.A. Levin), pp. 377-391.Academic Press, San Diego.
Ubick, D., Paquin, P., Cushing, P.E. & Roth, V. (2005) Spiders of North America: an
identification manual. American Arachnological Society, s.l.
31
Uetz, G.W. (1975) Temporal and spatial variation in species diversity of wandering
spiders (Araneae) in deciduous forest litter. Environmental Entomology, 4(5), 719-
724.
Wagner, J.D., Toft, S. & Wise, D.H. (2003) Spatial Stratification in litter depth by forest-
floor spiders. Journal of Arachnology, 31(1), 28-39.
Wennekes, P.L., Rosindell, J. & Etienne, R.S. (2012) The Neutral-Niche Debate: A
Philosophical Perspective. Acta Biotheoretica, 60, 257-271.
Wise, D.H. (1993) Spider in Ecological Webs. Cambridge University Press, Cambridge.
Ziesche, T.M. & Roth, M. (2008) Influence of environmental parameters on small-scale
distribution of soil-dwelling spiders in forests: What makes the difference, tree
species or microhabitat?. Forest Ecology and Management, 255, 738-752.
32
Tables Table 1. Unstandardized coefficients, structure and total variation explained by each canonical variable (Can) obtained in a canonical discriminant analysis used to separate mean temperature and mean humidity among sites.
Variable Can1 Can2 Mean daily temperature* -1.384 (-0.972) -0.170 (0.230) Mean daily humidity* -0.122 (0.408) -0.141 (-0.912) % of variance** 99.60 0.39 Eigenvalue 12.90 0.05 Squared canonical correlation 0.92 0.04 * canonical structure in parentheses ** proportion of discriminating ability
Table 2. Mean, standard deviation (sd) and rank mean of canopy cover per site. Significant differences are indicated by different lowercase letters (results of multiple comparisons after a Kruskal-Wallis test). Site abbreviations: cocoa (CA), coffee (CF), mango (MA) and a remnant of the original vegetation: medium-height evergreen forest (SM).
site mean sd mean rank CA 58.13 13.95 74.97ab CF 58.23 13.84 77.72ab MA 64.62 11.66 98.32a SM 57.50 12.38 70.97b
33
Figure legends
Figure 1. Location of the study sites within the Soconusco region. Site abbreviations: cocoa (CA), coffee (CF), mango (MA) and a remnant of the original vegetation: medium- height evergreen forest (SM).
Figure 2. Boxplot of canonical scores results of canonical discriminant analysis used to separate mean temperature and mean humidity among sites.
Figure 3. Sample-size-based rarefaction (solid lines) and extrapolation (dashed lines) of spider species diversity among sites, based on the Hill numbers. The 95% confidence intervals were obtained by a bootstrap method based on 50 replications. The reference sample of 1034 individuals is denoted by a vertical line. a) Comparison of spider species diversity for Hill numbers of order q=0. b) Comparison of spider species diversity for Hill numbers of order q=1.
Figure 4. Comparison of the sample-size-based rarefaction of spider species diversity between seasons for each site (dry vs rainy), based on the Hill numbers. The 95% confidence intervals (as error bars) were obtained by a bootstrap method based on 50 replications. a) Comparison of spider species diversity for Hill numbers of order q=0. b) Comparison of spider species diversity for Hill numbers of order q=1.
Figure 5. Comparison of the sample-size-based rarefaction of spider species diversity among sites for each season, based on the Hill numbers. The 95% confidence intervals (as error bars) were obtained by a bootstrap method based on 50 replications. a) Comparison of spider species diversity in rainy season for Hill numbers of order q=0 and q=1. b) Comparison of spider species diversity in dry season for Hill numbers of order q=0 and q=1.
Figure 6. Number of individuals belonging to each family of spider across sites. Site abbreviations: cocoa (CA), coffee (CF), mango (MA) and medium-height evergreen forest (SM).
Figure 7. Dispersion plot for each site, divided into four sections using the mean frequency percentage and the 2% of species abundance. a) cocoa (CA). b) coffee (CF). c) mango (MA). d) medium-height evergreen forest (SM). Numbers in parentheses indicate the amount of species per section. Numbers in the dominants section correspond to those noted for each species in the appendix.
Fig. 8. Ordination plot of four transect for each vegetation type, based on multidimensional scaling of the spider assemblages result of 100 iterations, stress: 6.6%. Site abbreviations: cocoa (CA), coffee (CF), mango (MA) and medium-height evergreen forest (SM).
34
Fig. 1
35
Fig. 2
36
Fig. 3b Fig.
Fig. 3a Fig. 3a
37
Fig. 4b
Fig. 4a
38
Fig. 5b Fig. 5a
39
Fig. 6
40
Fig. 7a Fig. 7b
Fig. 7c Fig. 7d
41
Fig. 8
42
Appendix List of spider species collected per season (R: Rainy and D: Dry season) within Soconusco region in Chiapas, Mexico. Site abbreviations: cocoa (CA), coffee (CF), mango (MA) and medium-height evergreen forest (SM).
CA CF MA SM Code Family/Species R D R D R D R D Anyphaenidae 1 Anyphaena sp. 1 ------1 2 Anyphaena sp. 2 - 1 ------3 Anyphaeninae sp. 1 - - - - - 1 - - Araneidae 4 Edricus productus O. Pickard-Cambridge, 1896 ------1 - 5 Gen. sp. 1 1 ------6 Mangora sp. 1 - - - - 1 1 - - 7 Mangora sp. 2 ------5 8 Pronous sp. 1 - 1 - - - - - 1 Caponiidae 9 Nops sp. 1 1 ------Clubionidae 10 Clubiona sp. 1 - 1 - - - - - 1 11 Elaver sp. 1 - 1 ------Corinnidae 12 Castianeira sp. 1 ------4 13 Castianeira sp. 2 ------1 14 Castianeira sp. 3 2 2 2 - 1 1 - 2 15 Castianeira sp. 4 5 2 3 5 3 - 2 4 16 Castianeira sp. 5 ------1 17 Castianeira sp. 6 - - 1 - - - - - 18 Creugas sp. 1 ------2 - 19 Creugas sp. 2 1 ------20 Mazax pax Reiskind, 1969 23 5 - - 1 3 8 4 Ctenidae 21 Acanthoctenus sp. 1 1 ------22 Ctenus calcaratus F. O. P.-Cambridge, 1900 31 23 - - 2 13 11 13 23 Ctenus sp. 1 - - 12 12 - - - - 24 Cupiennius sp. 1 5 2 - - - - - 2 Ctenizidae 25 Ummidia zebrina (F. O. Pickard-Cambridge, 1897) ------4 - Deinopidae 26 Deinopis longipes F. O. Pickard-Cambridge, 1902 - - - - - 1 - -
43
CA CF MA SM Code Family/Species R D R D R D R D Dictynidae 27 Dictyna sp. 1 18 7 - - 1 35 7 47 28 Mallos sp. 1 - - - - - 1 - - 29 Tivyna sp. 1 ------1 Dipluridae 30 Ischnothele digitata (O. Pickard-Cambridge, 1892) - 1 - - - 1 - - Gnaphosidae 31 Camillina sp. 1 - 2 - - - - 1 4 32 Cesonia lugubris (O. P.-Cambridge, 1896) 22 9 - - 6 3 1 16 33 Gnaphosa sp. 1 ------1 Hahniidae 34 Neoantistea sp. 1 29 40 - - - - 4 2 Leptonetidae 35 Darkoneta sp. 1 ------1 1 Linyphiidae 36 Agyneta sp. 1 13 6 - - - - 20 6 37 Agyneta sp. 2 - - 2 3 - - - - 38 Agyneta sp. 3 18 11 ------39 Agyneta sp. 4 - - - - - 7 - - 40 Gen. 1 sp. 1 ------203 33 41 Gen. 1 sp. 2 - - - - 4 5 - - 42 Gen. 2 sp. 1 ------1 - 43 Gen. 6 sp. 1 - - 1 1 - - - - 44 Gen. 7 sp. 1 - - - - 1 - - - 45 Gen. 8 sp. 1 ------1 46 Pocobletus coroniger Simon, 1894 - 1 - - - 21 - 2 47 Tenneseellum sp. 1 - - 3 - - - - - 48 Walckenaeria sp. 1 5 9 1 4 1 5 - - Lycosidae 49 Hogna sp. 1 - - - - - 1 - - 50 Pirata sp. 1 - - 93 103 - - - - 51 Schizocosa sp. 1 139 43 1 9 - - 61 40 52 Trochosa sp. 1 - 2 - - - 4 - 1 53 Trochosa sp. 2 - - 6 - - - - - Mimetidae 54 Mimetus sp. 1 - - - - 1 - - - Miturgidae 55 Teminius hirsutus (Petrunkevitch, 1925) - - - - 6 71 - 1 Mysmenidae 56 Calodipoena sp. 1 - 1 3 - - 6 2 6
44
CA CF MA SM Code Family/Species R D R D R D R D Nesticidae 57 Eidmannella pallida (Emerton, 1875) 3 ------Ochyroceratidae 58 Ochyrocera sp. 1 - - 5 2 - - - - 59 Theotima minutissimus (Petrunkevitch, 1929) 338 85 - - - - 22 - Oecobiidae 60 Oecobius cellariorum (Dugès, 1836) - - - 1 - 4 - - Oonopidae 61 Brignolia parumpunctata (Simon, 1893) 43 35 - - 32 16 3 9 62 Costarina sp. 1 - - 5 10 - - 3 - 63 Escaphiella sp. 1 1 ------1 64 Gen. sp. 1 ------5 7 65 Gen. 2 sp. 1 ------2 - 66 Gen. 3 sp. 1 1 1 - - 3 1 - - 67 Gen. 4 sp. 1 - - 2 - - - - - 68 Ischnothyreus peltifer (Simon, 1891) 30 16 - - 9 9 2 2 69 Triaeris stenaspis Simon, 1891 6 9 2 4 - - 8 6 70 Yumates sp. 1 2 ------Oxyopidae 71 Oxyopes chiapas Brady, 1975 - 2 - - 2 5 - - Pholcidae 72 Anopsicus sp. 1 ------97 28 73 Anopsicus sp. 2 - - 4 1 - - - - 74 Anopsicus sp. 3 - - - 1 - - - - 75 Metagonia asintal Huber, 1998 1 3 - - - 2 1 11 Phrurolithidae 76 Piabuna sp. 1 - - 22 15 - - - - Pisauridae 77 Tinus sp. 1 - 2 - - 2 1 - - Salticidae 78 Aillutticus sp. 1 1 4 ------79 Akela charlottae Peckham & Peckham, 1896 9 6 - - 1 1 - - 80 Corythalia sp. 1 - - - - - 1 - - 81 Corythalia sp. 2 - - 6 1 - - - - 82 Cylistella sp. 1 ------1 83 Dendriphantini sp. 1 - - - - - 1 - - 84 Euophryinae sp. 1 ------1 - 85 Freya longispina (F. O. Pickard-Cambridge, 1901) 1 - - - 1 - - - 86 Freya regia (Peckham & Peckham, 1896) - 3 ------87 Gen. sp. 1 - - - - 3 11 - - 88 Gen. 2 sp. 1 - - - - 2 2 - -
45
CA CF MA SM Code Family/Species R D R D R D R D Salticidae 89 Gen. 5 sp. 1 - - - - 1 1 - - 90 Gen. 7 sp. 1 - - - - 1 4 - - 91 Gen. 8 sp. 1 - 2 ------92 Gen. 9 sp. 1 ------1 3 93 Gen. 10 sp. 1 ------1 94 Habronattus sp. 1 4 1 - - - 12 - 7 95 Lyssomanes sp. 1 ------1 96 Marpissinae sp. 1 ------1 97 Metacyrba venusta (Chickering, 1946) 1 - - - 2 2 - - 98 Mexigonus sp. 1 - - 4 6 - - - - 99 Thiodina sp. 1 - - - - - 1 - - 100 Zygoballus tibialis F. O. Pickard-Cambridge, 1901 - - - - - 3 - - 101 Zygoballus maculatus F. O. Pickard-Cambridge, 1901 - 1 ------Scytodidae 102 Scytodes sp. 1 ------4 36 103 Scytodes sp. 2 - - - - 1 - - - Sparassidae 104 Olios sp. 1 - - - - - 1 - - Tengellidae 105 Gen. sp. 1 ------8 12 Tetragnathidae 106 Glenognatha spherella Chamberlain & Ivie, 1936 2 1 4 11 - - 1 1 107 Leucauge venusta (Walckenaer, 1841) - 1 - - - 1 1 - Theraphosidae 108 Theraphosinae sp. 1 1 - 3 - - - 2 2 Theridiidae 109 Chrosiothes sp. 1 - 2 ------110 Dipoena anas Levi, 1963 - 1 ------111 Dipoena lana Levi, 1953 1 1 ------112 Enoplognatha sp. 1 - - - - 2 1 - - 113 Euryopis lineatipes O. Pickard-Cambridge, 1893 1 - - - - 3 - - 114 Euryopis spinigera O. Pickard-Cambridge, 1895 4 19 - - - 11 1 6 115 Gen. 1 sp. 1 - - - - 1 - - - 116 Gen. 1 sp. 2 - - - - 1 - - - 117 Gen. 1 sp. 3 - - - - - 2 - - 118 Gen. 1 sp. 4 ------1 1 119 Gen. 1 sp. 5 - - 1 1 - - - - 120 Gen. 2 sp. 1 - - - - - 1 - - 121 Stemmops bicolor O. Pickard-Cambridge, 1894 - - 3 3 - - - -
46
CA CF MA SM Code Family/Species R D R D R D R D 122 Stemmops questus Levi, 1955 8 3 1 2 4 2 7 - 123 Theridion sp. 1 - - 5 3 - - - - 124 Thymoites boquete (Levi, 1959) - 2 69 44 - - - - 125 Thymoites delicatulus (Levi, 1959) ------1 126 Thymoites maderae (Gertsch & Archer, 1942) - 4 - - - 49 - 7 127 Thymoites notabilis (Levi, 1959) ------4 26 128 Thymoites sp. 1 - - 2 2 - - - - 129 Thymoites sp. 2 1 - - - - - 1 5 Theridiosomatidae 130 Epeirotypus sp. 1 ------1 Thomisidae 131 Synema sp. 1 - - - - - 3 - 1 Titanoecidae 132 Goeldia mexicana (O. P.-Cambridge, 1896) - - - - 52 30 - 8 Trachelidae 133 Trachelas bispinosus F. O. P.-Cambridge, 1899 - - 4 7 - - - - 134 Trachelas sp. 1 - - - - - 1 - - Uloboridae 135 Ariston sp. 1 - - - - - 1 - - 136 Philoponella semiplumosa (Simon, 1893) - - - - - 4 - - 137 Uloborus campestratus Simon, 1893 - 1 ------138 Uloborus sp. 1 - - - - - 2 - - Zodariidae 139 Ishania sp. 1 - - 2 2 - - - - 773 375 272 253 148 369 504 386
47
CONCLUSIONES
La comunidad de arañas presentes en los cuatro sitios se compone de 139
morfoespecies, 105 géneros y 39 familias. Las familias más diversas en todo el
estudio fueron Salticidae seguida de Theridiidae, Linyphiidae y Oonopidae. Sin
duda estas familias aportan muchas especies a los ensambles de arañas en la
región tropical. Es notable la abundancia de la familia Ochyroceratidae en el sitio
CA y en todo el estudio (Theotima minutissimus resultó ser la especie más
abundante en todo el estudio con 445 ejemplares). Otras familias abundantes
fueron Lycosidae, Linyphiidae, Theridiidae y Oonopidae.
Las diferencias observadas en la diversidad y abundancia en los ensambles de
arañas sugieren que algunas variables de los tipos de vegetación estudiados
influyen sobre ellas. Los cambios detectados en la diversidad entre temporadas
indicarían que algunos factores climáticos afectan también a los ensambles de
arañas. El sitio CF fue el menos diverso (q=0), no presentó alguna diferencia en
su diversidad entre lluvias y secas, además fue el más diferente en cuanto a su
composición de especies.
No obstante con el fin de analizar los múltiples factores que estructuran las
comunidades de arañas se requieren estudios con diseños de muestreo que
permitan descomponer la heterogeneidad espacial y temporal y al mismo tiempo
que consideren el efecto de la escala.
48
LITERATURA CITADA
Bonaldo, A.B. y Dias, S.C., 2010. A structured inventory of spiders (Arachnida, Araneae)
in natural and artificial forest gaps at Porto Urucu, Western Brazilian Amazonia. Acta
Amazonica, 40(2), pp.357-372.
Bultman, T.L. y Uetz, G.W., 1982. Abundance and community structure of forest floor
spiders following litter manipulation. Oecologia, 55(1), pp.34-41.
Chamé-Vázquez, D., 2011. Arañas de Suelo del Bosque Mesófilo de Montaña,
Conservado y Alterado en el Soconusco, Chiapas, México. Tesis de licenciatura.
Universidad de Ciencias y Artes de Chiapas.
Coddington, J.A. y Levi, H.W., 1991. Systematics and Evolution of Spiders (Araneae).
Annual Review of Ecology and Systematics, 22(1), pp.565-592.
Fernández-Bello, E., 2008. La producción agropecuaria en el Soconusco e intercambio
con Centroamérica. En: J. E. Sánchez & R. Jarquin, eds. La frontera sur. Reflexiones
sobre el Soconusco, Chiapas, y sus problemas ambientales, poblacionales y
productivos. Mexico: Senado de la República-ECOSUR, pp. 185–200.
Gasnier, T.R. y Höfer, H., 2001. Patterns of abundance of four species of wandering
spiders (Ctenidae, Ctenus) in a forest in central Amazonia. Journal of Arachnology,
29(1), pp.95-103.
Gobierno de Chiapas, 2011. Programa regional de desarrollo: región X Soconusco. [pdf]
s.l.: s.n. Disponible en: < http://www.haciendachiapas.gob.mx/planeacion/planes_
desarrollo_muni.asp> [Consultado 20 Noviembre 2013].
49
González-Espinosa, M. y Ramírez-Marcial, N., 2013. Comunidades vegetales terrestres.
En: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO),
ed. 2013. La biodiversidad en Chiapas: Estudio de Estado. Mexico, DF: Comisión
Nacional para el Conocimiento y Uso de la Biodiversidad y Gobierno del Estado de
Chiapas. pp.21-42
Ibarra-Núñez, G., García, J.A., Moreno, M.A., López, J.A., y Lachaud, J.P., 2001. Prey
analysis in the diet of some ponerine ants (Hymenoptera: Formicidae) and web-
building spiders (Araneae) in coffee plantations in Chiapas, Mexico. Sociobiology,
37(3B), pp.723-755.
Jiménez, M.L. y Navarrete, J.G., 2010. Fauna de arañas del suelo de una comunidad
árida-tropical en Baja California Sur, México. Revista Mexicana de Biodiversidad, 81,
pp.417–426.
Medina, S.F., 2002. Las arañas y su distribución temporal en un bosque de San Martín
Cachihuapan, Municipio de Villa del Carbón, Estado de México. Tesis de
Licenciatura. Facultad de Estudios Superiores, Iztacala. UNAM.
Nieto-Castañeda, I.G., 2000. Inventario de arañas de algunas localidades de los estados
de Puebla y Morelos en la parte alta del Balsas. Tesis de licenciatura. Facultad de
Estudios Superiores Zaragoza, UNAM.
Nieto-Castañeda, I.G., 2004. Arañas edáficas (Caponiidae, Gnaphosidae, Lycosidae,
Oonopidae: Arachnida Araneae) asociadas a los humedales de Baja California Sur,
México. Tesis de Maestría. Centro de Investigaciones Biológicas del Noroeste, S.C.
Pinkus-Rendón, M.A., León-Cortés, J.L. e Ibarra-Núñez, G., 2006. Spider diversity in a
tropical habitat gradient in Chiapas, Mexico. Diversity and Distributions, 12, pp.61–
69.
50
Rego, F.N.A.A., Venticinque, E.M. y Brescovit, A.D., 2005. Densidades de aranhas
errantes (Ctenidae e Sparassidae, Araneae) em uma floresta fragmentada. Biota
Neotropica, 5(1A), pp.45-52.
Riechert, S.E. y Bishop, L., 1990, Prey control by an assemblage of generalist predators:
spiders in garden test systems. Ecology, 71, pp.1441-1450.
Ruiz, A., 2004. Diversidad de arañas de suelo en una plantación de cacao, Mpio. Tuxtla
Chico, Chiapas, México. Tesis de licenciatura. Universidad de Ciencias y Artes de
Chiapas.
Sereda, E., Blick, T., Dorowb, W.H.O., Woltersa, V. y Birkhofer, K., 2012. Spatial
distribution of spiders and epedaphic Collembola in an environmentally
heterogeneous forest floor habitat. Pedobiologia, 55, pp.241–245.
Stevenson, B.G. y Dindal, D.L., 1982. Effect of leaf shape on forest litter spiders:
community organization and microhabitat selection of immature Enoplognatha ovata
(Clerck) (Theridiidae). Journal of Arachnology, 10(2), pp.165-178.
Uetz, G.W., 1975. Temporal and spatial variation in species diversity of wandering spiders
(Araneae) in deciduous forest litter. Environmental Entomology, 4(5), pp.719-724.
Ziesche, T.M. y Roth, M., 2008. Influence of environmental parameters on small-scale
distribution of soil-dwelling spiders in forests: What makes the difference, tree species
or microhabitat?. Forest Ecology and Management, 255, pp.738-752.
51