SciELO - Scientific Electronic Library Online

 
vol.87 número3Parásitos del cocinero Caranx caballus (Pisces: Carangidae) en tres localidades de las costas del Pacífico mexicano y su utilidad como marcadores biológicosIntegrando la estructura taxonómica en el análisis de la diversidad alfa y beta de los escarabajos Melolonthidae en la Faja Volcánica Transmexicana índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Revista mexicana de biodiversidad

versão On-line ISSN 2007-8706versão impressa ISSN 1870-3453

Rev. Mex. Biodiv. vol.87 no.3 México Set. 2016

http://dx.doi.org/10.1016/j.rmb.2016.07.011 

Ecología

Spider cyberdiversity (Araneae: Araneomorphae) in an ecotouristic tropical forest fragment in Xilitla, Mexico

Ciberdiversidad de arañas (Araneae: Araneomorphae) en un fragmento ecoturístico de selva tropical en Xilitla, México

Francisco A. Rivera-Quiroza  * 

Uriel Garcilazo-Cruza 

Fernando Álvarez-Padillaa  b 

a Laboratorio de Aracnología, Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, 04510 Mexico City, Mexico

b Department of Entomology, California Academy of Sciences, 55 Music Concourse Dr., San Francisco, CA 94118, USA

Abstract:

The diversity of araneomorph spiders in an ecoturistic tropical forest remnant of approximately 40 ha is described. A 1-ha plot with homogeneous vegetation was established. Six sampling methods covered all microhabitats, except tree canopy. Four expeditions were conducted from August 2011 to June 2012. In a total of 485 samples, 4,118 adult specimens representing 205 morphospecies were collected. Nonparametric richness estimates varied between 229 and 295 species. All collected morphospecies and species were documented with 2,233 digital images available at www.unamfcaracnolab.com. These images are intended to expedite species identification and to allow comparisons of taxa not formally described. Morphospecies identifications included: 91 species, 12 as similar to a described species, 86 to genus and 16 to family. Differences between seasonality and species collected revealed that March and June were similar in composition and were better represented in both number of species and adult specimens than August and November, although the collecting effort was the same. The similarity ranged between 0.35 and 0.71 among seasons.

Keywords: Arachnida; Faunistics; Biodiversity

Resumen:

Se describe la diversidad de arañas araneomorfas en un remanente ecoturístico de bosque tropical de aproximadamente 40 ha. Se estableció una parcela de 1 ha abarcando vegetación homogénea. Seis métodos de muestreo cubrieron todos los microhábitats disponibles excepto el dosel. Se efectuaron 4 expediciones de agosto de 2011 a junio de 2012. En un total de 485 muestras se recolectaron 4,118 especímenes adultos pertenecientes a 205 morfoespecies. Los estimadores de riqueza no paramétrica mostraron un rango de entre 229 y 295 especies. Todas las morfoespecies y especies recolectadas fueron documentadas con 2,233 imágenes digitales disponibles en la página www.unamfcaracnolab.com. Estas imágenes están encaminadas a acelerar la identificación de especies y a ayudar a comparar taxones sin describir. Las identificaciones de morfoespecies incluyeron 91 especies, 12 morfoespecies similares a taxones descritos, 86 géneros y 16 familias. Las diferencias entre estacionalidad y especies recolectadas revelaron que los muestreos realizados en marzo y junio fueron similares entre sí y se encontró una mayor cantidad de especies y especímenes adultos que los de agosto y noviembre, teniendo el mismo esfuerzo de colecta en todos los casos. La similitud de especies varió de 0.35 a 0.71 entre estaciones.

Palabras clave: Arachnida; Faunística; Biodiversidad

Introduction

Spiders inhabit almost all terrestrial ecosystems and are particularly diverse in the tropical and subtropical regions where most of the new species are expected to be found (Foelix, 2011). At the present there are more than 45,862 described species and Araneomorphae accounts for 93% of the total (WSC, 2016). It is estimated by taxonomic comparisons that between 2 and 5 times more species could be extant (Adis & Harvey, 2001; Coddington & Levi, 1991; Coddington, Giribet, Harvey, Prendini, & Walter, 2004; Platnick, 1999). Field data of 5 inventories from tropical forests worldwide averaged 274 species collected per ha, estimating an average richness of 403, with 812 species as the highest estimation from a Rainforest in Peru (Coddington, Agnarsson, Miller, Kuntner, & Hormiga 2009; Coddington, Griswold, Silva-Dávila, Peñaranda, & Larcher, 1991; Miller & Pham, 2011; Silva & Coddington, 1996; Sørensen, Coddington, & Scharff, 2002). Also the beta diversity is higher in tropical regions, a comparison between 2 spider inventories in Peru and Bolivia estimated only 5-20% shared species at similar elevation and 0.8-2.8% between elevations (Agnarsson, Coddington, & Kuntner, 2013). However, many more inventories would be required to estimate spider diversity and observe worldwide patterns using field data, therefore the taxonomic comparisons are our best estimate so far.

Faunistic inventories with spiders, as with other megadiverse taxa, present 2 main challenges: first, it is virtually impossible to collect all species in a particular area, and second, the large amount of time invested in the identification of specimens for taxonomically poorly documented and megadiverse taxa. Species richness estimators have been developed to address the first problem by extrapolating rarefaction curves, using species abundance distributions and non-parametric estimators that combine accumulation curves with the proportion of rare species in the sample (Colwell & Coddington, 1994; Colwell et al., 2012; Gotelli & Colwell, 2001). Also addressing this problem a pivotal advance happened for spiders when a standardized sampling protocol was proposed by Coddington et al. (1991) which combines several uniform techniques. This protocol has been used by several studies worldwide, incorporating more collecting techniques and new species richness estimators (Cardoso, 2009; Cardoso, Scharff, et al., 2008; Cardoso, Gaspar, et al., 2008; Coddington, Young, & Coyle, 1996; Coddington et al., 2009; Dobyns, 1997; Höfer & Brescovit, 2001; Miller & Pham, 2011; Scharff, Coddington, Griswold, Hormiga, & Bjørn, 2003; Sørensen, 2003; Toti, Coyle, & Miller, 2000).

The second problem has been addressed only recently, and although the taxonomic challenge of identifying species for poorly documented megadiverse taxa remains huge, considerable progress has been made thanks to the advances in digital imaging technology used to comprehensively document morphology, decreasing costs of DNA sequencing and web resources to share this information worldwide (Wheeler, 2008; Wilson, 2004). This new approach has been named cyberdiversity and has been proposed as a solution to the taxonomic impediment (Miller, Miller, Pham, & Beentjes, 2014). Some recent faunistic spider inventories have been pioneers in making available on the internet extensive image databases of all morphospecies (Ramírez, 2004), combining such databases with taxonomic descriptions for particular taxa (Miller, Griswold, & Yin, 2009) or providiong morpholocial data, DNA barcodes (www.digitalspiders.org) and evaluating how biodiversity changes in function of space, climate or other environmental variables (Miller et al., 2014).

Mexico is considered the world's fifth most diverse country (Llorente-Bousquets & Ocegueda, 2008). This diversity is product of the convergence of the Nearctic and Neotropical biotas combined with a rough topography defined as the Mexican Transition Zone (Espinosa-Organista, Ocegueda-Cruz, Aguilar-Zúñiga, Flores-Villela, & Llorente-Bousquets, 2008). The first description of a mexican spider was done by Lucas (1833), since then, most of the taxonomic work of the Mexican araneofauna has been done mainly by European and American arachnologists: Becker (1878, 1886), Koch (1836,1847), Peckham and Peckham (1883, 1909), Simon (1884, 1909), Gertsch (1933), Muma and Gertsch (1964), Levi (1953, 2005), Platnick (1972), and Bolzern, Platnick, and Berniker (2015). These authors published approximately 150 taxonomic works since then for the Mexican fauna (WSC, 2016); the references mentioned above include the first and last relevant papers on this topic. The most important taxonomic studies with spiders in the country are more than a century old and still useful references for this fauna (Cambridge, 1889, 1897; Keyserling, 1880, 1893).

The first spider catalog for Mexico reported 1,598 species (Hoffman, 1976). Since then 3 catalogs have been published reporting approximately 2,300 species (Francke, 2013; Jiménez, 1996; Jiménez & Ibarra-Núñez, 2008). According to data extracted from the World Spider Catalog (2016) there are currently 2,159 described species in 69 families occurring in Mexico representing ca. 4.7% of the world spider fauna.

A search in Web of Science v. 5.21 using the keywords Araneae or spider and biodiversity or faunistic, gave 263 results worldwide of which at least 18 are focused in the diversity of Araneae species for Mexico. In the last 24 years there have been several faunistic studies on the Mexican araneofauna restricted to a group or guild (Arana-Gamboa, Pinkus-Rendón, & Rebollar-Téllez, 2014; Bizuet-Flores, Jiménez-Jiménez, Zavala-Hurtado, & Corcuera, 2015; Corcuera, Valverde, Zavala-Hurtado, de la Rosa, & Duran-Barrón, 2010; Corcuera et al., 2015; Jiménez & Navarrete, 2010; Méndez-Castro & Rao, 2014), focuses on synantropic species (Desales-Lara, Francke, & Sánchez-Nava, 2013; Rodríguez-Rodríguez, Solís-Catalán, & Valdez-Mondragón, 2015; Salazar-Olivo & Solís-Rojas, 2015), or have an agroecological view (Ibarra-Núñez & García-Ballinas, 1998; Lucio-Palacio & Ibarra-Núñez, 2015; Marín & Perfecto, 2013). Studies that represented most of the spider diversity that inhabits a certain area by using a mixture of methods provide valuable information regarding ecological comparisons and species lists (Gómez-Rodríguez & Salazar-Olivo, 2012; Ibarra-Núñez, Maya-Morales, & Chame-Vázquez, 2011; Jiménez, 1991; Jiménez, Nieto-Castañeda, Correa-Ramírez, & Palacios-Cardiel, 2015; Maya-Morales, Ibarra-Núñez, León-Cortés, & Infante, 2012; Pinkus-Rendón, León-Cortés, & Ibarra-Núñez, 2006). However, comparisons with most of these studies are difficult because they used different collecting protocols, sample effort units and plot areas; regardless than standardized protocols for the group had been proposed and applied worldwide (Coddington et al., 1991, 1996, 2009; Dobyns, 1997; Scharff et al., 2003; Silva & Coddington, 1996; Sørensen et al., 2002; Toti et al., 2000). Furthermore this protocol is flexible enough to evaluate and incorporate other environmental variables and collecting techniques; the only requirements are specifying the area of the plot and using comparable sampling effort units (Cardoso, 2009; Cardoso, Gaspar, et al., 2008; Coddington et al., 2009; Ibarra-Núñez, Maya-Morales, & Chame-Vázquez, 2011; Maya-Morales et al., 2012).

Taxonomic comparisons between the Mexican inventories that included a list of the species collected obtained an average of 52% identified species. This represents a problem for direct comparisons, in particular for the unidentified morphospecies and the ones that remain as “circa” or “affinis”. Three alternatives exist for comparing unidentified taxa: wait until the new taxa are described, visit the collections where the specimens are deposited or illustrate all morphospecies with digital images available online.

The first 2 solutions have the disadvantage of waiting until formal descriptions are produced and the time and resources required for visiting the collections. The third solution makes these data immediately available and free for the scientific community or any institution with special interest in it. It also expedites the species identification process, provide identification voucher specimens and allow direct comparisons with other inventories for unidentified morphospecies that are otherwise difficult to reconcile with other studies or remain uninformative.

This last solution has never been implemented in México therefore the objectives of this paper are: to create an online image database documenting all morphospecies and species of the studied locality linked to their diversity data in the context of the new taxonomy (Wheeler, 2008), to estimate the species richness using nonparametric estimators and to analyze the impact of seasonality on the species composition.

Materials and methods

The study was conducted in the municipality of Xilitla, San Luis Potosí. This zone is part of the Sierra Madre Oriental having an altitude ranging from 600 to 2,000 m a.s.l. It is characterized by tropical vegetation; nonetheless almost half of the municipality vegetation has been transformed for agricultural use (Inegi, 2014). Spiders were collected in a 1 ha plot with homogeneous vegetation located approximately 2 km north of Xilitla (21°23′50″ N, 98°59′38″ W) inside the “Jardín Escultórico Edward James”. This site has a relatively well preserved area of 30 ha of tropical vegetation that is used primarily for ecotouristic activities.

Sampling was carried out by 6 collectors during 4 expeditions (4 days each) from August, 2011 to June, 2012. The dates for these field trips were: August 27-31, 2011; November 14-18, 2011; March 23-30, 2012; and June 10-15, 2012. Approximately 120 samples were obtained per expedition using 6 methods: looking up, looking down, cryptic, beating, Berlese funnels and pitfall traps (Cardoso, 2009; Coddington et al., 1991; Miller et al., 2014; Scharff et al., 2003; Sørensen et al., 2002; Toti et al., 2000) allocating more effort for direct methods at night following both our experience and specialized literature suggestions. Direct methods included looking up, looking down, cryptic and beating, the first 2 were implemented during night, while the other 2 were done during the day. Samples of these methods were taken randomly inside the plot taking as effort unit 1hour per sample ranging from 20 to 30 samples of each method per expedition. Non-direct methods included sifted leaf litter processed with a Berlese funnel and pitfall traps. These were implemented as follows: funnel extraction consisted of 12 samples -1.5 l each - of sifted leaf litter per expedition. Samples were processed in 12 Berlese funnels for 3 days under a 60 W light bulb. Finally 31 pitfall traps per expedition were placed randomly inside the plot.

Each sample was labeled with expedition code, collector, method, and replicate number and preserved in 96% ethanol. Adult specimens are important because only the genital features are reliable to identify species or sort different morphospecies. In most tropical inventories juvenile spiders are not identified because these faunas are so little known that attempting to identify immature specimens using morphology will result in errors produced by associating immature and adults that are not conspecific or splitting the same morphospecies in more than 1. In many cases, even adult specimens may be impossible to identify (Coddington et al., 1996, 2009; Miller & Pham, 2011; Scharff et al., 2003; Sørensen et al., 2002; Toti et al., 2000). A solution to this problem not implemented here is the use of DNA barcodes to associate immatures and adults without ambiguity (Barret & Hebert, 2005; Prendini, 2005; Raso, Sint, Rief, Kaufmann, & Traugot, 2014; Slovik & Blagoev, 2012). Adult specimens were sorted to morphospecies and determined to genus and family using the Ubick, Paquin, Cushing, and Roth (2005) and Jocque and Dippenaar-Schoeman (2006) identification keys, and several papers provided by various internet sources (BHL, 2014; among other resources). Specimens and samples were organized using Microsoft Excel and this databse is available at www.unamfcaracnolab.com/WPGS_XIL/Xilitla.html.

Digital images where done with the following microscopes and digital cameras: Leica MZ16A, Nikon SMZ1000 for external morphology and Leica DM4000M for internal genital anatomy. Digital cameras were a Leica DFC500 and a Nikon DS-U2 for external anatomy and Nikon DXM1200 digital for structure of internal genitalia. The female internal genitalia were digested using pancreatin (Álvarez-Padilla & Hormiga, 2007), cleared using clove oil and mounted in semipermanent preparations (Coddington, 1983). Voucher specimens are deposited at the Laboratorio de Aracnología, Facultad de Ciencias, Universidad Nacional Autónoma de México and the California Academy of Sciences. Images for each morphospecies included approximately 15 standard views that covered most of their somatic and genital anatomy. An average 20 digital images were taken by standard view and combined with the program Helicon Focus 5.3 using the default values except radius set up at 44 and smoothing setup at 1. Rendering Method A was used for external anatomy and rendering Method B for cleared genitals. In some cases levels and contrast of the images were modified using Adobe Photoshop CS2 version 9.0. A selection of 2,238 images for all morphospecies is available online at www.unamfcaracnolab.com (Álvarez-Padilla Laboratory, 2014). Several arachnologists contributed with the species and genus identification speeding up the process, they are included in the Acknowledgements section and referenced with their respective identification on the website.

Species richness nonparametric estimation and the similarity analysis between seasons were performed with the program EstimateS 9.1.0 (Colwell, 2013). This program includes abundance based (Chao 1 and ACE), incidence based estimators (Chao 2, ICE, both Jacknifes and bootstrap). To asses if there were differences between the seasonality and the species collected at each expedition. Also the Shannon-Wiener diversity index was obtained for each of the expeditions and compared pair wise using the Hutcheson T-test (Hutcheson, 1970).

Results

A total of 485 samples were obtained from which 86 were beating, 45 berlese, 89 criptic, 82 looking down, 87 looking up and 96 pitfall traps capturing 10,661 spiders of which 4,118 were adults (38.6% of the total) representing 205 species and 39 families (Appendix 1). Almost 56% of the species found remained unidentified and many of these are expected to be new. Taxonomic identifications included 91 morphospecies identified to species level, 12 as confer or similar to a described species, 86 identified to genus and 16 only to family level. Each species was documented with an average of 15 images when both sexes were found and 8 images when only 1 sex was available. These standard views were: cephalotorax anterior view, habitus dorsal, lateral and ventral views for both sexes (total 8 images), 4 views on average to document male genital anatomy and three images for the female genitalia. Species richness estimations based on abundance data gave between 256 species with ACE and 290 with Chao 1; of these 2 estimations only Chao 1 calculates 95% confidence intervals that varied between 246 and 376. Incidence based estimations obtained 280 species with Chao 2, ICE 253, 229 bootstrap and 260 and 295 with Jacknife 1 and 2, respectively. Only Chao 2 computes confidence intervals that ranged between 242 and 356 species. A total of 55 species were singletons and 18 doubletons, 55 species were also represented only once in a sample (uniques) and 20 represented in only 2 samples (duplicates). The highest species estimation was given by Jackknife 2 with 294 species and the lowest with 229 was given by bootstrap (Table 1). The species accumulation curves exhibit stable behavior after the 100 samples but do not present a clear asymptote, likewise the singleton and doubleton curves did not intersect, an observation consistent with the proportion of rare species (Fig. 1).

Table 1 Observed and estimated species richness. 

  Species SD
Samples 485  
Individuals 4120  
Observed richness 205  
Singletons 55 -
Doubletons 18 -
Uniques 55 -
Duplicates 20 -
ACE 255.85 0
ICE 253.3 0
Chao 1 289.01 31.45
Chao 1 95% CI lower bound 246.31 -
Chao 1 95% CI upper bound 375.86 -
Chao 2 280.47 27.83
Chao 2 95% CI lower bound 242.48 -
Chao 2 95% CI upper bound 356.95 -
Jack 1 259.89 9.2
Jack 2 294.78 0
Bootstrap 229.03 0

Figure 1 Species accumulation and estimation curves. Data only includes adult specimens collected in 1hectare plot. Six non-parametric estimators based on: abundance (Chao 1, ACE), incidence (Chao 2, ICE) and resampling (Jackknife 2, Bootstrap) included. Singletons and doubletons are also graphed. 

Comparisons between the species lists in relation to seasonality obtained that the expeditions of March and June were the richest with 136 and 135 species, respectively sharing 87; followed by November with 106 and August with 88 species sharing 57. Shannon-Wiener diversity index per expedition were August 3.38; November 3.75; March 3.72 and June 4.03. Pair wise differences between these expeditons were evaluated using a Hutchenson t-test showing that only March and November expeditions (t (1998.6) 0.41 < p = 1.64) were significantly different between them. Most rare species were found in March and June with 23 and 17 singletons, respectively; whereas August and November had 7 and 8 singletons.

An average of 10.2 (±15.5) adult specimens per species were collected. Twenty were represented by 50 or more specimens, of these taxa Theridion sp. 1 (Theridiidae) (457) was the most abundant followed by Pirata pagicola Chamberlin, 1925 (290) (Lycosidae), Thymoites illudens Gertsch and Mulaik, 1936 (266) (Theridiidae) and Phrurolithidae sp. 1 (185); the abundance for the other 16 species ranged between 54 and 179 specimens (Fig. 2). The 185 taxa not included in this plot were represented by an average of 7.4 (±9.1) specimens per species including the singletons and doubletons mentioned above.

Figure 2 Histogram of the twenty more abundant species. Data includes abundance of all adult specimens per species collected in the inventory. 

The most abundant family was also Theridiidae with 1,432 specimens, followed by Pholcidae (304) and Lycosidae (295). Four families were represented only by 1 specimen (Agelenidae, Hahniidae, Philodromidae and Zorocratidae). Theridiidae was the richest family with 51 species representing 25% of the total followed by Salticidae and Araneidae with 25 each accounting together for the 23.1%. Thirteen families were represented only by 1 species (Appendix 1).

Discussion

More than 55% of the species collected in this inventoy remained as unidentified and are likely new. Some of these species were identified as related to a described species (aff. or cf.) indicating in the website the characteristics that are different between them. Whereas other species were only identified to genus and in some cases to family level (sp.) depending on the taxonomic problems particular of each taxon. The percentage of new species in relation to the total of species collected was compared in 14 studies that did not necessarily follow Coddington et al. (1991) protocol, but included a species list. Results ranged between 0 and 13.09% of unidentified species for temperate regions. In contrast, the percentage of unidentified taxa for tropical regions varies between 49.18 and 100% with an average of 43.6% unidentified taxa (Table 3).

Table 3 Percentages of undetermined species in spider inventories. 

Author Undet. spp. Geographic area
Dobyns (1997) 0.00% Ellicott Rock, USA
Scharff et al. (2003) 0.00% Hestehaven, Denmark
Toti et al. (2000) 5.46% Great Smoky Mountains, USA
Coddington et al. (1996) 5.68% Ellicott Rock, USA
Cardoso, Gasper, et al. (2008) 13.09% Mata da Albergaria, Portugal
Höfer and Brescovit (2001) 48.91% Reserva Ducke, Brazil
Ricetti and Bonaldo (2008) 49.18% Serra do Cachimbo, Brazil
This study 56.03% Xilitla, Mexico
Ibarra-Núñez et al. (2011) 64.47% Volcán Tacaná, Mexico
Raizer et al. (2005) 65.53% Bacia do Rio Paraguai, Brazil
Bonaldo and Dias (2010) 88.86% Porto Urucu, Brazil
Sørensen et al. (2002) 95.75% Uzungua Mountains, Tanzania
Silva and Coddington (1996) 100.00% Pakitza, Peru

When comparisons are attempted between published inventories the biggest problem is the high percentage of species that are either unidentified or the identification is doubtful, particularly for tropical regions with megadiverse taxa that are poorly documented. The tool provided by cyberdiversity (Miller et al., 2014) that directly address this problem is the publication of extensive image databases available on the internet coordinated with faunistic inventories. These databases allow direct comparisons of morphospecies that remain unidentified either because they are new or because the taxonomy of the group needs a thorough revision. In addition, these databases also provide voucher specimens that give evidence of the accuracy of the taxonomic determinations, illustrate interspecific geographic variations and expedite the process of new species recognition.

It has been estimated that 1 hectare of tropical forest may support between 300 and 800 species of spiders (Coddington et al., 1991, 2009). The present study reports a total of 205 species for a remnant of tropical forest. Similar studies done in Mexican territory have obtained similar richness ranging from 112 to 243 species (Bizuet-Flores et al., 2015; Jiménez et al., 2015; Maya-Morales et al., 2012). Inventories conducted in tropical areas of South America ranged between 121 and 352 species (Coddington et al., 2009; Nogueira, Pinto-da Rocha, & Brescovit, 2006; Raizer, Hilton, Indicatti, & Brescovit, 2005; Ricetti & Bonaldo, 2008; Silva & Coddington, 1996; Yanoviak, Kragh, & Nadkarni, 2003). For temperate ecosystems 123.5 (±51.1) species were collected, the highest richness was observed in a Quercus spp. forest in Portugal with 204, and the lowest in a scrubland in USA with 60 species (Cardoso, Scharff et al., 2008, Toti et al., 2000). Eighteen of these spider inventories worldwide that use comparable sampling protocols were analyzed collecting 211.1 (±SD 138.69) species (Table 2).

Table 2 Abundance, richness and estimated number of species of 18 spider inventories worldwide. 

Vegetation Abundance Richness Estimation Estimation Estimation Study
      (range) mean SD  
Coastal forest 8,710 66 74-88 81 7 Scharff et al. (2003)
Grassland 1,853 91 106-159 131.75 22.88 Toti et al. (2000)
Hardwood forest 1,629 89 117-128 122.67 5.51 Coddington et al. (1996)
Montane forest 5,233 149 165-201 183 18 Sørensen (2003)
Montane forest 9,096 170 183-215 195 6.93 Sørensen et al. (2002)
Pantanal 602 206 299 299 34 Raizer et al. (2005)
Quercus forest 10,808 204 232-260 242.75 12.84 Cardoso, Gaspar, et al. (2008)
Quercus forest 7,423 168 188-214 199 11.6 Cardoso, Henriques, et al. (2008)
Scrubland 3,059 115 116-192 160.11 22.83 Cardoso, Scharff, et al. (2008)
Scrubland 573 60 68-97 75.75 14.38 Toti et al. (2000)
Tropical forest 5,965 352 443 - - Coddington et al. (2009)
Tropical forest 3,912 506 - - - Höfer and Brescovit (2001)
Tropical forest 1,208 112 123-138 132.8 5.81 Maya-Morales et al. (2012)
Tropical forest 2,010 262 336-385 360.5 34.65 Miller and Pham (2011)
Tropical forest 3,148 121 - - - Nogueira et al. (2006)
Tropical forest 2,750 427 614 - - Ricetti and Bonaldo (2008)
Tropical forest 2,616 498 720-812 766.75 41.13 Silva and Coddington (1996)
Tropical forest 1,163 204 - - - Yanoviak et al. (2003)
Tropical forest 4,121 212 237-298 275 22.44 This study

Non-parametric estimators show that the 205 species found in this inventory represent between the 89.5% and 69.7% of the estimated species in the sampled area. This is consistent with other tropical inventories where usually between 50% and 85% of the araneofauna is found and the estimated curves do not present a clear asymptote (Bonaldo & Dias, 2010; Coddington et al., 1996, 2009; Maya-Morales et al., 2012; Miller & Pham, 2011; Ricetti & Bonaldo, 2008; Sørensen et al., 2002). As the samples accumulate in the inventory, it is less likely to add new species to the inventory, most of which will represent either rare species of the study site or vagrant species that do not belong to the studied community (Cardoso, 2009; Coddington et al., 2009; Jiménez-Valverde & Hortal, 2003; Moreno & Halffter, 2000).

The variation of the diversity in each of the expeditions was compared using the Hutcheson test to evaluate statistically the seasonal differences in the spider community. Comparisons between the species lists in each expedition reveals March as the richest with 136 species and August as the least rich with 88 species. The relative abundance shows that March is also the month with more adult abundance (308) and November is the one with least adult representation (809). This could be correlated with the phenology of the different spiders groups during the year, independently of the collecting effort. Nevertheless it is recommended for arthropod inventories to sample at different times of the year increasing the probability of collecting adult specimens for most taxa.

As Cardoso (2009) suggests, different study sites require different number of samples per collecting method. In the case of Xilitla, the methods that covered the vegetation were the most effective, representing comprehensively the fauna they are designed for in a smaller number of samples than the methods that cover ground spiders and cryptic habitats as revealed by the steepness of the curves. Therefore, in order to increase the number of ground and wandering species, more effort should be put in these methods. These differences reflect the microhabitats where most of the spiders are found. However, the selection of collecting techniques for a given ecosystem follows their suitability; for example, collecting with sweeping nets in this forest remnant would be impossible due to the tangled vegetation. Therefore, it is important to consider that although in every inventory there are methods that are more efficient than others, covering most suitable microhabitats helps to have a better representation of the community sampled especially for rare species.

Acknowledgments

We would like to thank the following arachnologists for their taxonomic determinations: Wayne Maddison, Antonio Brescovit, Gustavo Hormiga, Darrell Ubick, Lina Almeida, Martin Ramirez, Facundo Labarque, Angelo Bolzern, Thiago Silva, Jimmy Cabra, Alexandre Bonaldo, Regianne Saturnino, and Lidianne Salvatierra. Also to the students that helped collecting and sorting the specimens: Miguel Hernández, Francisco J. Salgueiro, Diana E. Álvarez, Rigel S. González, and Omar Caballero. Special thanks to the Xilitla Foundation for allowing this inventory to take place inside the ecotouristic development Las Pozas. In addition, we thank Jeremy Miller and Charles Griswold for revising and editing the English on early versions of this manuscript, Patricia Santillán for helping us with the ecological analyses and the Editor Dr. Alejandro Valdéz and the anonymous reviewers for their comments and corrections. An undergraduate student grant was provided to F. A. Rivera and U. Gracilazo by the project UNAM-DGAPA PAPIIT IN213612 during the development of this spider inventory.

References

Adis and Harvey, 2001 Adis J, Harvey M. How many Arachnida and Myriapoda are there world-wide and in Amazonia. Studies on neotropical fauna and environment. 2001; 35:39-141 [ Links ]

Agnarsson et al., 2013 Agnarsson I, Coddington J.A, Kuntner M. Systematics: progress in the study of spider diversity and evolution. In D. Penney (Ed.), Spider research in the 21st century: trends and Perspectives. Manchester, UK: Siri Scientific Press; 2013. 58-111 [ Links ]

Álvarez-Padilla Laboratory, 2014 Álvarez-Padilla Laboratory. (2014). Araneomorphae of Mexico a digital images catalog v 2.0. Facultad de Ciencias, UNAM. Retrieved on: April 12, 2016 from http://www.unamfcarachnology.com. [ Links ]

Álvarez-Padilla and Hormiga, 2007 Álvarez-Padilla F, Hormiga G. A protocol for digesting internal soft tissues and mounting spiders for scanning electron microscopy. Journal of Arachnology. 2007; 35:538-42 [ Links ]

Arana-Gamboa et al., 2014 Arana-Gamboa N.R, Pinkus-Rendón R, Rebollar-Téllez M.A. Spatial and temporal diversity and structure of cursorial spiders (Arachnida: Araneae) in a fragmented landscape in Yucatán, Mexico. Southwestern Entomologist. 2014; 39:555-80 [ Links ]

Barrett and Hebert, 2005 Barrett R.D.H, Hebert P.D.N. Identifying spiders through DNA barcodes. Canadian Journal of Zoology. 2005; 83:481-91 [ Links ]

Becker, 1878 Becker L. Diagnoses de quelques aranéides nouvelles du Mexique. Annales de la Société Entomologique de Belgique. 1878; 21:77-80 [ Links ]

Becker, 1886 Becker L. Diagnoses de quelques arachnides nouvaux. Annales de la Société Entomologique de Belgique. 1886; 30:23-7 [ Links ]

BHL, 2014 BHL (Biodiversity heritage library). (2014). Retrieved on: April 12, 2016 from http://www.biodiversitylibrary.org/. [ Links ]

Bizuet-Flores et al., 2015 Bizuet-Flores M.Y, Jiménez-Jiménez M.L, Zavala-Hurtado A, Corcuera P. Diversity patterns of ground dwelling spiders (Arachnida: Araneae) in five prevailing plant communities of the Cuatro Cienegas Basin, Coahuila, México. Revista Mexicana de Biodiversidad. 2015; 86:153-63 [ Links ]

Bolzern et al., 2015 Bolzern A, Platnick N.I, Berniker L. Three new genera of soft-bodied goblin spiders (Araneae, Oonopidae) from México, Belize, and Guatemala. American Museum Novitates. 2015; 3824:1-59 [ Links ]

Bonaldo and Dias, 2010 Bonaldo A.B, Dias S.C. A structured inventory of spiders (Arachnida, Araneae) in natural and artificial forest gaps at Porto Urucu, Western Brazilian Amazonia. Acta Amazonica. 2010; 40:357-72 [ Links ]

Cambridge, 1889 Cambridge, O. P. (1889). Arachnida-Araneidea. Volume I. In Biologia Centrali Americana. Zoology, London. [ Links ]

Cambridge, 1897 Cambridge, F.O. P. (1897). Arachnida - Araneidea and Opiliones. Volume II. In Biologia Centrali-Americana. Zoology, London. [ Links ]

Cardoso, 2009 Cardoso P. Standardization and optimization of arthropod inventories, the case of Iberian spiders. Biodiversity Conservation. 2009; 18:3949-62 [ Links ]

Cardoso et al., 2008a Cardoso P, Gaspar C, Pereira L.C, Silva I, Henriques S.S, da Silva R.R, et al. Assessing spider species richness and composition in Mediterranean cork oak forests. Acta Oecologica. 2008; 33:114-27 [ Links ]

Cardoso et al., 2008b Cardoso P, Henriques S.S, Gaspar C, Crespo L.C, Carvalho R, Schmidt J.B, et al. Species richness and composition assessment of spiders in a Mediterranean scrubland. Journal of Insect Conservation. 2008; 13:45-55 [ Links ]

Cardoso et al., 2008c Cardoso P, Scharff N, Gaspar C, Henriques S.S, Carvalho R, Castro P.H, et al. Rapid biodiversity assessment of spiders (Araneae) using semi-quantitative sampling: a case study in a Mediterranean forest. Insect Conservation and Diversity. 2008; 1:71-84 [ Links ]

Coddington, 1983 Coddington J. A temporary slide mount allowing precise manipulation of small structures. Verhandlungen des naturwissenschaftlichen Vereins Hamburg. 1983; 26:291-2 [ Links ]

Coddington et al., 2009 Coddington J.A, Agnarsson I, Miller J.A, Kuntner M, Hormiga G. Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. Journal of Animal Ecology. 2009; 78:573-84 [ Links ]

Coddington et al., 2004 Coddington J.A, Giribet G, Harvey M.S, Prendini L, Walter D.E. Arachnida. In J. Cracraft, & M. J. Donoghue (Eds.), Assembling the tree of life. Oxford, UK: Oxford University Press; 2004. [ Links ]

Coddington et al., 1991 Coddington, J. A., Griswold, C. E., Silva-Dávila, D., Peñaranda, E., & Larcher, S. F. (1991). Designing and testing sampling protocols to estimate biodiversity in tropical ecosystems. In E.C. Dudley (Ed.), The unity of evolutionary biology. Proceedings of the fourth international congress of systematic and evolutionary biology. University of Maryland, College Park, USA. 1990; (pp. 44-60). [ Links ]

Coddington and Levi, 1991 Coddington J.A, Levi H.W. Systematics and evolution of spiders (Araneae). Annual Review of Ecology, Evolution and Systematics. 1991; 22:565-92 [ Links ]

Coddington et al., 1996 Coddington J.A, Young L.H, Coyle F.A. Estimating spider species richness in a Southern Appalachian cove hardwood forest. Journal of Arachnology. 1996; 24:111-28 [ Links ]

Colwell, 2013 Colwell R.K. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's guide and application. Retrieved on: April 12, 2016 from http://purl.oclc.org/estimates. 2013. [ Links ]

Colwell et al., 2012 Colwell R.K, Chao A, Gotelli N.J, Lin S.Y, Mao C.X, Chazdon R.L, et al. Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology. 2012; 5:3-21 [ Links ]

Colwell and Coddington, 1994 Colwell R.K, Coddington J.A. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society, B. 1994; 345:101-18 [ Links ]

Corcuera et al., 2015 Corcuera P, Valverde P.L, Jiménez-Jiménez M.A, Ponce-Mendoza A, De la Rosa G, Nieto-Castañeda I.G. Ground spider guilds and functional diversity in native pine woodlands and Eucalyptus plantations. Environmental Entomology. 2015; 45:292-300 [ Links ]

Corcuera et al., 2010 Corcuera P, Valverde P.L, Zavala-Hurtado J.A, de la Rosa G, Duran-Barrón C.G. Non weaving spiders on native woodlands and Eucalyptus plantations in Western Mexico: diversity and distribution patterns. Journal of Insect Conservation. 2010; 14:711-9 [ Links ]

Desales-Lara et al., 2013 Desales-Lara M.A, Francke O.F, Sánchez-Nava P. Diversity of spiders (Arachnida: Araneae) in anthropogenic habitats. Revista Mexicana de Biodiversidad. 2013; 84:291-305 [ Links ]

Dobyns, 1997 Dobyns J.R. Effects of sampling intensity on the collection of spiders (Araneae) species and the estimation of species richness. Pest Mananging and Sampling. 1997; 26:150-62 [ Links ]

Espinosa-Organista et al., 2008 Espinosa-Organista D, Ocegueda-Cruz S, Aguilar-Zúñiga C, Flores-Villela O, Llorente-Bousquets J. El conocimiento biogeográfico de las especies y su regionalización natural. In J. Sarukhan (Ed.), Capital natural de México, Vol. I. Conocimiento actual de la biodiversidad. México, D.F: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad; 2008. 33-65 [ Links ]

Foelix, 2011 Foelix R. Biology of spiders. 3rd. Edition. EUA: Oxford University Press; 2011. [ Links ]

Franke, 2013 Franke O. Biodiversidad de Arthropoda (Chelicerata: Arachnida ex Acari) en México. Revista Mexicana de Biodiversidad. 2013; 85:408-18 [ Links ]

Gertsch, 1933 Gertsch W.J. Notes on American spiders of the family Thomisidae. American Museum Novitates. 1933; 593:1-22 [ Links ]

Gómez-Rodríguez and Salazar-Olivo, 2012 Gómez-Rodríguez J.F, Salazar-Olivo C.A. Arañas de la región montañosa de Miquihuana, Tamaulipas: listado faunístico y registros nuevos. Dugesiana. 2012; 19:1-8 [ Links ]

Gotelli and Colwell, 2001 Gotelli N.J, Colwell R.K. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters. 2001; 4:379-91 [ Links ]

Höfer and Brescovit, 2001 Höfer H, Brescovit A.D. Species and guild structure of a Neotropical spider assemblage (Araneae) (Reserva Florestal Adolpho Ducke, Manaus, Amazonas, Brazil). Andrias. 2001; 15:99-120 [ Links ]

Hoffman, 1976 Hoffman A. Relación bibliográfica preliminar de las arañas de México (Arachnida: Araneae). México, D.F: Publicacion especial, Instituto de Biología UNAM; 1976. [ Links ]

Hutcheson, 1970 Hutcheson K. A test for comparing diversities based on Shannon formula. Journal of Theoretical Biology. 1970; 29:151-4 [ Links ]

Ibarra-Núñez and García-Ballinas, 1998 Ibarra-Núñez G, García-Ballinas J.A. Diversidad de tres familias de arañas tejedoras (Araneae: Araneidae, Tetragnathidae, Theridiidae) en cafetales del Soconusco, Chiapas, México. Folia Entomologica Mexicana. 1998; 102:11-20 [ Links ]

Ibarra-Núñez et al., 2011 Ibarra-Núñez G, Maya-Morales J, Chame-Vázquez D. Las arañas del bosque mesófilo de montaña de la Reserva de la Biosfera Volcán Tacaná, Chiapas, México. Revista Mexicana de Biodiversidad. 2011; 82:1183-93 [ Links ]

Inegi, 2014 Inegi (Instituto Nacional de Geografía y Estadística). (2014). Retrieved on: April 12, 2016 from http://www3.inegi.org.mx/sistemas/mexicocifras/default.aspx?e=24. [ Links ]

Jiménez, 1991 Jiménez M.L. Araneofauna de las islas Revillagigedo, México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. Serie Zoología. 1991; 62:417-92 [ Links ]

Jiménez, 1996 Jiménez M.L. Araneae. In J. Llorente-Bousquets, A. N. García-Aldrete, & E. González (Eds.), Biodiversidad, taxonomía y biogeografía de artrópodos de México: hacia una síntesis de su conocimiento. México, D.F: Universidad Nacional Autónoma de México; 1996. 83-101 [ Links ]

Jiménez and Ibarra-Nuñez, 2008 Jiménez M.L, Ibarra-Nuñez G. Arañas (Aracnidos). In S. Ocegueda, & J. Llorente-Bousquets (Eds.), Capital natural de México. Conocimiento actual de la biodiversidad. (CD 1) (Vol. I) Catálogo taxonómico de especies de México. México, D.F.: Comisión Nacional para el Conocimiento y uso de la Biodiversidad; 2008. [ Links ]

Jiménez and Navarrete, 2010 Jiménez M.L, Navarrete J.G. Fauna de arañas del suelo de una comunidad árido tropical en Baja California Sur, México. Revista Mexicana de Biodiversidad. 2010; 81:417-26 [ Links ]

Jiménez et al., 2015 Jiménez M.L, Nieto-Castañeda I.G, Correa-Ramírez M.M, Palacios-Cardiel C. Spiders of oases in the southern region of the Baja California Peninsula, Mexico. Revista Mexicana de Biodiversidad. 2015; 86:319-31 [ Links ]

Jiménez-Valverde and Hortal, 2003 Jiménez-Valverde A, Hortal J. Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Revista Ibérica de Aracnología. 2003; 8:151-61 [ Links ]

Jocque and Dippenaar-Schoeman, 2006 Jocque R, Dippenaar-Schoeman A.S. Spider families of the World. Belgium: Royal Museum for Central Africa; 2006. [ Links ]

Keyserling, 1880 Keyserling, E. (1880). Die Spinnen Amerikas, I. Laterigradae. Nürnberg. [ Links ]

Keyserling, 1893 Keyserling, E. (1893). Die Spinnen Amerikas. Epeiridae. Nürnberg. [ Links ]

Koch, 1836 Koch, C. L. (1836). Die Arachniden. Nürnberg. [ Links ]

Koch, 1847 Koch, C. L. (1847). Die Arachniden. Nürnberg. [ Links ]

Levi, 1953 Levi H.W. New and rare Dipoena from Mexico and Central America (Araneae Theridiidae). American Museum Novitates. 1953; 1639:1-11 [ Links ]

Levi, 2005 Levi H.W. The orb-weaver genus Mangora of Mexico, Central America, and the West Indies (Araneae: Araneidae). Bulletin of the Museum of Comparative Zoology at Harvard College. 2005; 158:139-82 [ Links ]

Llorente-Bousquets and Ocegueda, 2008 Llorente-Bousquets J, Ocegueda S. Estado del conocimiento de la biota. In J. Sarukhan (Ed.), Capital natural de México Vol I. Conocimiento actual de la biodiversidad. México, D.F: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad; 2008. 283-322 [ Links ]

Lucas, 1833 Lucas H. Description de l’Epeira mexicana. Magasin de Zoologie. 1833; 3:1-2 [ Links ]

Lucio-Palacio and Ibarra-Núñez, 2015 Lucio-Palacio C.R, Ibarra-Núñez G. Arboreal spiders from cocoa plantations with different management type in Chiapas, México. Revista Mexicana de Biodiversidad. 2015; 86:143-52 [ Links ]

Marín and Perfecto, 2013 Marín L, Perfecto I. Spider diversity in coffee agroecosystems: the influence of agricultural intensification and aggressive ants. Environmental Entomology. 2013; 42:204-13 [ Links ]

Maya-Morales et al., 2012 Maya-Morales J, Ibarra-Nuñez G, León-Cortés J.L, Infante F. Understory spider diversity in two remnants of tropical montane cloud forest in Chiapas, Mexico. Journal of Insect Conservation. 2012; 16:25-38 [ Links ]

Méndez-Castro and Rao, 2014 Méndez-Castro E.F, Rao D. Spider diversity in epiphytes: Can shade coffee plantations promote the conservation of cloud forest assemblages?. Biodiversity and Conservation. 2014; 23:2561-77 [ Links ]

Miller et al., 2009 Miller J.A, Griswold C.E, Yin C.M. The symphytognathoid spiders of the Gaoligongshan, Yunnan, China (Araneae: Araneoidea): Systematics and diversity of micro-orbweavers. ZooKeys. 2009; 11:9-195 [ Links ]

Miller et al., 2014 Miller J.A, Miller J.H, Pham D.S, Beentjes K.K. Cyberdiversity: improving the informatic value of diverse tropical arthropod inventories. PLOS ONE. 2014; 9(12):e115750 [ Links ]

Miller and Pham, 2011 Miller J.A, Pham D.S. Landscape biodiversity of tropical forest spider communities in Vietnam (Arachnida: Araneae). Treubia. 2011; 38:53-70 [ Links ]

Moreno and Halffter, 2000 Moreno C.E, Halffter G. Assessing the completeness of bat biodiversity inventories using species accumulation curves. Journal of Applied Ecolology. 2000; 37:149-58 [ Links ]

Muma and Gertsch, 1964 Muma M.H, Gertsch W.J. The spider family Uloboridae in North America north of Mexico. American Museum Novitates. 1964; 2196:1-43 [ Links ]

Nogueira et al., 2006 Nogueira A, Pinto-da Rocha R, Brescovit A.D. Comunidade de aranhas orbitelas (Araneae, Arachnida) na região da Reserva Florestal do Morro Grande, Cotia, São Paulo, Brasil. Biota Neotropica. 2006; 6:1-24 [ Links ]

Peckham and Peckham, 1883 Peckham G.W, Peckham E.G. Descriptions of new or little known spiders of the family Attidae from various parts of the United States of North America. Milwaukee: Natural History Society or Wisconsin. Cramer, Aikens & Cramer Milwaukee Perss; 1883. [ Links ]

Peckham and Peckham, 1909 Peckham G.W, Peckham E.G. Revision of the Attidae of North America. Transactions of the Wisconsin Academy of Sciences, Arts and Letters. 1909; 16:355-655 [ Links ]

Pinkus-Rendón et al., 2006 Pinkus-Rendón M.A, León-Cortés J.L, Ibarra-Núñez G. Spider diversity in a tropical habitat gradient in Chiapas, México. Diversity and Distributions. 2006; 12:61-9 [ Links ]

Platnick, 1972 Platnick N.I. Notes on the pepinensis group of the crab spider genus Ebo (Araneae: Thomisidae). Psyche, Cambridge. 1972; 79:58-60 [ Links ]

Platnick, 1999 Platnick N.I. Dimensions of biodiversity: targeting megadiverse groups. In J. Cracraft, & F. T. Grifo (Eds.), The living planet in crisis: biodiversity science and policy. New York: Columbia University Press; 1999. 33-52 [ Links ]

Prendini, 2005 Prendini L. Comment on “Identifying spiders through DNA barcodes”. Canadian Journal of Zoology. 2005; 83:498-504 [ Links ]

Raizer et al., 2005 Raizer J.J, Hilton F, Indicatti R.P, Brescovit A. Comunidade de aranhas (Arachnida, Araneae) do pantanal norte (Mato Grosso, Brasil) e sua similaridade com a araneofauna amazônica. Biota Neotropica. 2005; 5:125-40 [ Links ]

Ramírez, 2004 Ramírez, M. (2004). Spider biodiversity inventory carried out at Doi Inthanon during the “Biodiversity inventory theory and design-short course”. Retrieved on: April 12, 2016 from http://aracnologia.macn.gov.ar/ThaiPlot/. [ Links ]

Raso et al., 2014 Raso L, Sint D, Rief A, Kaufmann R, Traugot M. Molecular identification of adult and juvenile linyphiid and theridiid spiders in Alpine Glacier Foreland communities. PLOS ONE. 2014; 9:e101755 [ Links ]

Ricetti and Bonaldo, 2008 Ricetti J, Bonaldo A.B. Spiders diversity and richness estimates in four vegetations types of Serra do Cachimbo, Para, Brazil. Iheringia. Série Zoologia. 2008; 98:88-99 [ Links ]

Rodríguez-Rodríguez et al., 2015 Rodríguez-Rodríguez E.S, Solís-Catalán P.K, Valdez-Mondragón A. Diversity and seasonal abundance of anthropogenic spiders (Arachnida: Araneae) in different urban zones of the city of Chilpancingo, Guerrero, Mexico. Revista Mexicana de Biodiversidad. 2015; 86:962-71 [ Links ]

Salazar-Olivo and Solís-Rojas, 2015 Salazar-Olivo C.A, Solís-Rojas C. Araneofauna urbana (arachnida: araneae) de Ciudad Victoria, Tamaulipas, México. Acta Zoológica Mexicana Nueva Serie. 2015; 31:55-66 [ Links ]

Scharff et al., 2003 Scharff N, Coddington J.A, Griswold C.E, Hormiga G, Bjørn P.P. When to quit? Estimating spider species richness in a northern European deciduous forest. Journal of Arachnology. 2003; 31:246-73 [ Links ]

Silva and Coddington, 1996 Silva D, Coddington J.A. Spiders of Pakitza (Madre de Dios, Peru): Species richness and notes on community structure. In D. E. Wilson, & A. Sandoval (Eds.), The biodiversity of Southeastern Peru. Washington, D.C: Smithsonian Institution; 1996. 253-311 [ Links ]

Simon, 1884 Simon E. Description d’une espèce nouvelle du genre Cryptothele L. Koch. Annales de la Société Entomologique de Belgique. 1884; 28:301-2 [ Links ]

Simon, 1909 Simon E. Sur l’araignée Mosquero. Comptes Rendus de l’Académie des Sciences Paris. 1909; 148:736-7 [ Links ]

Slowik and Blagoev, 2012 Slowik J, Blagoev G.A. A survey of spiders (Arachnida: Araneae) of Prince of Wales Island, Alaska; combining morphological and DNA barcode identification techniques. Insecta Mundi. 2012; 251:1-12 [ Links ]

Sørensen, 2003 Sørensen L.L. Stratification of the spider fauna in a Tanzanian forest. In Y. Basset, V. Novotny, & S. E. Miller (Eds.), Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge: Cambridge University Press; 2003. 92-101 [ Links ]

Sørensen et al., 2002 Sørensen L.L, Coddington J.A, Scharff N. Inventorying and estimating sub-canopy spider diversity using semi-quantitative sampling methods in an afromontane forest. Environmental Entomology. 2002; 31:319-30 [ Links ]

Toti et al., 2000 Toti D.S, Coyle F.A, Miller J.A. A structured inventory of Appalachian grass bald and heath bald spider assemblages and a test of species richness estimator performance. Journal of Arachnology. 2000; 28:329-45 [ Links ]

Ubick et al., 2005 Ubick D, Paquin P, Cushing P.E, Roth V. Spiders of North America: an identification manual. USA: American Arachnologcal Society; 2005. [ Links ]

Wheeler, 2008 Wheeler Q.D. The new taxonomy. In The Systematics Association Special Volume Series 76. New York: CRC Press; 2008. [ Links ]

Wilson, 2004 Wilson E.O. Taxonomy as a fundamental discipline. Philosophical Transactions of the Royal Society B. 2004; 359:739 [ Links ]

WSC, 2016 World Spider Catalog (2016). Natural History Museum Bern. Retrieved on: April 12, 2016 from http://wsc.nmbe.ch, version 17.0. [ Links ]

Yanoviak et al., 2003 Yanoviak S.P, Kragh G, Nadkarni N.M. Spider assemblages in Costa Rican cloud forests: effects of forest level and forest age. Studies on Neotropical Fauna and Environment. 2003; 38:145-54 [ Links ]

** Peer Review under the responsibility of Universidad Nacional Autónoma de México.

Appendix 1. Species list and adult abundances.

Descargar anexo en formato PDF

Received: December 03, 2015; Accepted: May 19, 2016

* Corresponding author. E-mail address: rivera.andres37@gmail.com (F.A. Rivera-Quiroz).

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License