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Altitudinal distribution of alpha, beta, and gamma diversity of pseudoscorpions (Arachnida) in Oaxaca, Mexico
Acta Oecologica 103 (2020) 103525
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Original article
Altitudinal distribution of alpha, beta, and gamma diversity of pseudoscorpions (Arachnida) in Oaxaca, Mexico
T
Violeta Saraí Jiménez-Hernándeza, Gabriel Alfredo Villegas-Guzmána,b, José Arturo Casasola-Gonzálezc, Carlos Fabián Vargas-Mendozad,∗ a
Laboratorio de Acarología, Departamento Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación Carpio y Plan de Ayala S/n, Col. Casco de Santo Tomás C.P, 11340, Ciudad de México, Mexico b Laboratorio de Conservación de Fauna Silvestre, Universidad Autónoma Metropolitana Iztapalapa, San Rafael Atlixco No. 186, Col. Vicentina, C.P, 09340, Delegación Iztapalapa, Ciudad de México, Mexico c Instituto de Estudios Ambientales, Universidad de La Sierra Juárez, Av. Universidad S/n. Ixtlán de Juárez. C.P, 68725, Oaxaca, Mexico d Laboratorio de Variación Biológica y Evolución, Departamento Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación Carpio y Plan de Ayala S/n, Col. Casco de Santo Tomás C.P, 11340, Ciudad de México, Mexico
A R T I C LE I N FO
A B S T R A C T
Keywords: Species richness Species abundance Santiago comaltepec Diversity Altitudinal gradient
In this study, we describe the spatial and temporal variation in the diversity of pseudoscorpions along an altitudinal gradient in Santiago Comaltepec, Oaxaca, Mexico. Four altitudinal levels were selected (150, 989, 2177, and 2990 m a.s.l.). Species were recorded through monthly sampling from April 2016 to April 2017. Alpha and beta diversities were estimated at every altitude, and gamma diversity was calculated for the entire gradient; diversity was then related to temperature and precipitation. The highest species richness was observed at 989 m a.s.l. and the lowest at 2990 m a.s.l. The months with the lowest number of species and specimens were January, March, and April. The highest Shannon index value was observed at 989 m a.s.l. (H′ = 1.724) and the lowest at 2177 m a.s.l. (H′ = 0.692). Gamma diversity was 2.15 and was mainly affected by the average alpha diversity. Alpha diversity was higher during the dry season and was slightly regulated by precipitation. Moreover, higher species replacement was observed in the dry season than in the wet season, which was mainly associated with changes in temperature. Overall, with the increase in altitude, the diversity of pseudoscorpions decreases.
1. Introduction
has not been properly studied for all groups of organisms (Rahbek, 1995; Gaston and Spicer, 2004). In order to understand the spatial variation patterns of biodiversity with respect to the structure of the landscape, the various components of species diversity must be evaluated, i.e., a) the species richness of a community (alpha diversity), b) the degree of change in species composition across different communities (beta diversity), and c) the species richness of all communities in a landscape (gamma diversity) (Whittaker, 1972; Moreno, 2001; Koleff, 2005; Magurran and McGill, 2011). The altitudinal distribution of arthropods has not been widely studied and pseudoscorpions, in particular, have received very little attention (Muchmore, 1976, 1990; Olson, 1994; Aguiar et al., 2006; Richardson and Richardson, 2013). Pseudoscorpions are small arachnids, measuring between 1 and 12 mm, that live in moss and leaf litter, under logs, stones, bark, and in bird, rodent, and insect nests; they are cryptic predators of small arthropods. Pseudoscorpions are mainly distributed in tropical and subtropical
The distribution of biodiversity along environmental gradients (latitude, longitude, and altitude) has received considerable research attention (Olson, 1994; Sanders, 2002; Gaston and Spicer, 2004; Aguiar et al., 2006; Richardson and Richardson, 2013). Based on these studies, several patterns of species richness have been proposed (Stevens, 1992; Sanders, 2002; McCain and Bracy-Knight, 2013). There are two common models of species distribution: the first predicts a monotonic decrease in the number of species with altitude, and the second predicts a hump-shaped pattern, with a peak in the middle of the gradient (Stevens, 1992; Rahbek, 1995; Lomolino, 2001; Gaston and Spicer, 2004). Changes in species abundance and composition are generally related to changes in temperature and humidity with elevation (Malumbres-Olarte et al., 2018). Although species abundance and distribution are known to be closely related, the nature of this relationship
∗
Corresponding author. E-mail addresses: [email protected], [email protected] (C.F. Vargas-Mendoza).
https://doi.org/10.1016/j.actao.2020.103525 Received 11 July 2019; Received in revised form 6 January 2020; Accepted 17 January 2020 Available online 21 February 2020 1146-609X/ © 2020 Elsevier Masson SAS. All rights reserved.
Acta Oecologica 103 (2020) 103525
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and dry leaves hanging from plants, for 2 h along each transect. Specimens were taken directly from these microhabitats using fine-tip tweezers and placed in containers with 80% ethanol (Muchmore, 1990). Pseudoscorpions were processed following Hoff's technique (1949) with Wirth and Marston (1968) modifications. Taxonomic identification was performed under a phase-contrast microscope (Carl Zeiss, Ulm, Germany) with reference to specialized literature (e.g., Chamberlin, 1931a,b; Chamberlin and Chamberlin, 1945; Hoff, 1956; Muchmore, 1990; Harvey, 1992; Harvey et al., 2006; Harvey and Muchmore, 2013). The specimens were deposited in the collection “Dra. Isabel Bassols Batalla” of the Acarology Laboratory of the Escuela Nacional de Ciencias Biológicas of the Instituto Politécnico Nacional, Mexico City, Mexico.
regions (Chamberlin, 1931a,b; Hoff, 1949; Weygoldt, 1969; Muchmore, 1990). There are 3799 species worldwide (Harvey, 2013), of which 167 are found in Mexico (Harvey et al., 2006; Francke, 2013; VillegasGuzmán, 2015). In Oaxaca, 43 species have been recorded (Flores-Luna, 2006; Villegas-Guzmán et al., 2006; Harvey and Muchmore, 2013), of which 21 are found in Sierra Norte de Oaxaca (Villegas-Guzmán et al., 2006; Jiménez-Hernández, 2016; Jiménez-Hernández et al., 2018). To date, only two studies have related the diversity of pseudoscorpions to altitude (Hoff, 1959; Sato, 1983). On one hand, it is thought that the highest species diversity is found at intermediate elevations, and on the other, that pseudoscorpions follow three range size distribution patterns namely, a) restricted distribution, below 900 m, b) intermediate level, between 900 m and 1300 m, c) high altitude, between 1100 m and 2300 m (Sato, 1983). This study aims to describe the spatial and temporal variation of pseudoscorpion diversity along an altitudinal gradient in Sierra Norte de Oaxaca, Mexico. In contrast to previous studies, this research was conducted in a tropical area. We compared differences and similarities in the patterns of species richness and attempted to elucidate: 1) α and β diversities at different altitudes; 2) the relationships between α and β diversities, and temperature and precipitation at the sampling sites; and 3) gamma diversity variation across the altitudinal gradient over a oneyear cycle.
2.3. Data analysis 2.3.1. Alpha diversity (α) The total number of species (S), the Shannon-Weaver (H′) index, Pielou's equitability (J′) index, and individual rarefaction estimates for each index were estimated (Magurran, 1988, 2004; Moreno et al., 2011). In addition, Hill numbers were calculated following Moreno et al. (2011) and a plot of the Rényi index was developed using the parameter α in order to verify which localities were non-comparable (if the lines of localities crossed, those diversity indices were deemed noncomparable) (Tothmeresz, 1995). Non-parametric species richness was calculated using Chao2 and Clench estimators, using ESTIMATE v9.1 software (Colwell, 2006). Shannon-Weaver (H′) index values were compared between localities using a Hutcheson's t-test (Zar, 1999; Magurran, 1988, 2004). Correlations between diversity and weather variables, i.e., temperature and precipitation, were calculated for each locality. Monthly averages were obtained for a one-year cycle at different gathering points using historical data from 1970 to 2000 (WORLDCLIM v2 - Global Climate Data), with a spatial resolution of 30 arcseconds (approximately 1 km resolution at the equator) (Fick and Hijmans, 2017). Subsequently, the Shannon-Weaver index was estimated for each locality and for the study period (April 2016 to April 2017) in order to identify the month with the highest alpha diversity (α).
2. Materials and methods 2.1. Study area The study area was a northeast-facing hillside, with an elevation of almost 3000 m a.s.l., located in Santiago Comaltepec (17°34′N, 96°33′W), a municipality of Sierra Norte de Oaxaca, México (Ayuntamiento de Santiago Comaltepec, 2010) Santiago Comaltepec has an altitudinal gradient that includes variation in slope, soil factors, and vegetation types (INAFED (Instituto Nacional para el Federalismo y el Desarrollo Municipal), 2016). A range of sites were selected, separated by an interval of approximately 1000 m. Samples sites were accessed from highway 175, Oaxaca-Tuxtepec, in the direction of Golfo de Mexico. Sites of the same elevation were separated by large horizontal distances (14–20 km) due to the inaccessibility of closer localities. All transects were located in apparently undisturbed forest at least 500 m from the highway edge, except for Soyolapam (Fig. 1). The sites included: 1) Soyolapam (17°41′40.4″N, 96°16′14.6″W) at 150 m a.s.l., with patches of tropical rainforest and secondary herbaceous and shrub vegetation areas; 2) El Mameyal (17°40′31.5″N, 96°19′22.2″W) at 989 m a.s.l., corresponding to a transition zone between the cloud forest and the tropical rainforest; 3) El Relámpago (17°35′30″N, 96° 23′56.0″W) located at 2177 m a.s.l. and characterized by a cloud forest; and 4) Cerro Pelón (17°34′28.4″N, 96°30′15.5″W) located at 2990 m a.s.l., characterized by a dwarf shrubland and open temperate forest with some Pinus hartwegii.
2.3.2. Beta diversity (β) Three estimators of beta diversity were used: Sörensen (βSor), Simpson (βSim), and nestedness (βNested) dissimilarity indices, according to Baselga (2010). With these indices, beta diversity turnover and nestedness were partitioned. An analysis of similarities (ANOSIM) was also conducted to evaluate differences between localities using PAST v3.16 (Koleff, 2005; Hammer et al., 2017). To determine which of the two variables—temperature or precipitation—affect species replacement, a paired matrix was created using the differences in these variables (temperature difference = ToC localityi - ToC localityj; precipitation difference = locality precipitationi - locality precipitationj) for each locality and sampling month. These data were used to perform a Cochran-Mantel-Haenszel test (Mantel and Haenszel, 1959), using PAST v3.16 (Hammer et al., 2017).
2.2. Sampling Pseudoscorpions were sampled every month from April 2016 to April 2017. A transect 200 m long and 10 m wide was established at every study locality. Specimens were collected using three methods: 1) pitfall traps, 2) leaf litter collection, and 3) direct capture (Hoff, 1949; Muchmore, 1990; Ranius, 2002; Márquez-Luna, 2005). For the pitfall traps, five traps were placed along each transect, 40 m apart, containing a 1:1 mixture of 80% ethanol and ethylene glycol. For the leaf litter, three samples of leaf litter and soil weighing approximately 800 g were collected randomly, and were stored in plastic bags and transported to the laboratory, where they were processed using the Berlese-Tullgren funnel technique. Direct capture consisted of searching for pseudoscorpions under bark, in logs and leaf sheaths, and underneath stones
2.3.3. Gamma diversity (γ) Gamma diversity was obtained by adding alpha and beta average diversities (Moreno, 2001). Total monthly temperature and precipitation were correlated with the gamma diversity values obtained for each sampling month using Spearman's correlation coefficients, using PAST v3.16 software (Hammer et al., 2017). 3. Results A total of 742 specimens were collected, of which 354 were adults (48%) and 388 were nymphs (52%). Twenty-three species were found 2
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Fig. 1. Study area and pitfall trap locations. The subscript indicates the trap number (1–5). A. Cerro Pelón; B. El Relámpago; C. El Mameyal; D. Soyolapam.
Fig. 2. Altitudinal distribution of pseudoscorpions in the hillside studied. Species sizes represent their abundance.
3
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Fig. 3. Abundance of individuals using A) Rarefaction Species Richness and B) Shannon exp (H′).
P-values of 0.21 at El Relámpago (2177 m a.s.l.) and 0.25 at El Mameyal (989 m a.s.l.), suggest that species richness was likely to be greater than observed at localities between those altitudes (Fig. 3). The highest species richness was observed at 989 m a.s.l. and the lowest at 2990 m a.s.l. (Table 1). At 150 m a.s.l. (Soyolapam), the highest diversity was seen in September 2016, when precipitation started to decrease. The months with the highest diversity were January 2017, April 2016, April 2017, and October 2016 (Table 1), while in May 2016 and July 2016 no specimens were found at 989 m a.s.l. (El Mameyal). At 2177 m a.s.l. (El Relámpago), February was the only month with records and the H′ value was 1.11. Finally, at 2990 m a.s.l. (Cerro Pelón), there were two peaks, one in November (H′ = 0.68) and one in March (H′ = 0.64). No presence was recorded in the other months (Table 1). The Hutcheson's t-test showed that diversity at 989 m a.s.l. (El Mameyal) was significantly higher than that of other localities (Cerro Pelón: t = −4.63, P < 0.001; El Relámpago: t = −7.26, P < 0.001; and Soyolapam: t = 2.32, P = 0.02) (Table 2). At 150 m a.s.l., diversity was higher than at localities above 2000 m a.s.l. (Cerro Pelón: t = −3.83, P = 0.0014 and El Relámpago: t = −6.35, P < 0.001). Conversely, diversity at localities higher than 1000 m a.s.l. was lower than that at localities below 1000 m a.s.l. (t = 0.16; P = 0.87) (Table 2). The correlation coefficient (r) for α diversity and
along the altitudinal gradient (Fig. 2). However, only 18 different species were identified, belonging to 16 genera and 10 families. 3.1. Effect of altitude on alpha diversity (α) According to Chao 2, good sampling efficiency was obtained at three localities (Fig. 3): 77% in Cerro Pelón (2990 m a.s.l.); 83% in El Mameyal (989 m a.s.l.); and 100% in Soyolapam (150 m a.s.l.). In contrast, 47% of the estimated richness was obtained at El Relámpago (2177 m a.s.l.). Three of the four sampling localities showed good estimations of species richness, according to the Shannon-Weaver index and rarefaction results (Fig. 4). Species richness and the abundance of pseudoscorpions were distributed homogenously at the extremes of the altitudinal gradient (150 and 2990 m a.s.l.), reflecting greater equitability (Table 1). Hill numbers showed that high diversity existed below 1000 m a.s.l. (Table 1) and diversity was lower above 1000 m a.s.l. The Rényi index plot (Supplementary material) showed that the only comparable locations were those above and below 1000 m a.s.l.; between these intervals, localities were not comparable because their lines crossed. The Clench equation showed a coefficient of determination of 0.99 for all localities. A P-value (slope) close to 0.1 at the extremes of the gradient suggested an complete inventory of species at those altitudes. 4
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Fig. 3. (continued)
Pelón (βSimpson = 1.000), and those with the greatest nestedness were El Mameyal with Cerro Pelón (βnested = 0.750; Table 4). In terms of species replacement, the months from May to August (the beginning to the middle of the wet season) were found to have the highest replacement, and conversely, April (βaverage = 0.76) had the least replacement. The Cochran-Mantel-Haenszel test resulted in a correlation coefficient of rdif.pp = −0.006, P = 0.58 for precipitation and rdif.temp = 0.17, P = 0.0023 for temperature. The latter is a weak, but significant, positive correlation, i.e., species replacement was slightly higher when the temperature difference was higher. In the former, no association was found, i.e., pseudoscorpion β diversity was not determined by monthly variation in precipitation.
precipitation at 150 m a.s.l. was significative (rsoyolapam = −0.42; P = 0.045) but no significant correlations were found at any of the other localities, for either precipitation or temperature (Table 3).
3.2. Beta diversity (β) Similar pseudoscorpion communities were those found at El Mameyal (989 m a.s.l.) and Soyolapam (150 m a.s.l.), followed by Cerro Pelón (2990 m a.s.l.) and Soyolapam. The community at El Relámpago (2177 m a.s.l.) showed the least similarity to those at other localities (Table 4). The ANOSIM results showed similar patterns (mean rank within = 1224; mean rank between = 1296; P = 0.0004; Table 4). Values of beta diversity were high when comparing all localities with each other (βSörensen = 0.664 ± 0.085). Approximately 50% of this diversity was due to turnover (βSimpson = 0.337 ± 0.160) and 50% to nestedness (βnested = 0.326 ± 0.113); this means that beta diversity is influenced by species replacement and loss (Baselga, 2010). The communities with the greatest turnover were El Relámpago and Cerro
3.3. Gamma diversity (γ) along the altitudinal gradient Gamma diversity along the altitudinal gradient had a value of 2.15 and was affected by the average alpha diversity (1.17; 54%), and by the average beta diversity (0.98; 46%). This means that the number of species in each locality was slightly higher than the species 5
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Table 1 Diversity recorded at localities along an altitudinal gradient. A) q0: species richness; q1: Shannon-Weber index exponential (eH’); q2: inverse of Simpson dominance index (1/∑ p i2; pi = species frequency). B) Monthly alpha diversity.
Species richness Number of specimens Pielou equitability (J′) Hill numbers q0 q1 q2
2990 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
3 15 0.664
5 71 0.430
15 258 0.637
9 398 0.694
3 2.075 1.718
5 1.998 1.509
15 5.607 3.683
9 4.591 3.412
B) Alpha diversity Month
2999 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
April 2016 May 2016 June 2016 July 2016 August 2016 September 2016 October 2016 November 2016 December 2016 January 2017 February 2017 March 2017 April 2017
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.683 0.000 0.000 0.000 0.637 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.105 0.000 0.000
1.677 0.000 0.956 0.000 0.956 1.386 1.642 1.011 0.637 1.887 1.066 1.420 1.673
0.000 0.000 0.000 0.000 0.000 0.614 0.562 0.500 0.637 0.500 1.071 1.428 1.292
Table 2 Student's t-test (modified by Hutcheson) values for different elevations. Significant differences are in bold.
2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
2990 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
t = 0.161 p = 0.873 t = −4.635 p = 0.00018 t = −3.831 p = 0.0014
t = −7.259 p < 0.001 t = −6.35 p < 0.001
t = 2.325 p = 0.0205
150 m a.s.l.
highest diversity between 900 and 1300 m a.s.l. This finding is probably related to vegetation type, since the shape and structure of terrestrial communities are defined mainly by vegetation (Stevens, 1992). El Mameyal (989 m a.s.l.) is a transition zone between cloud forests and tropical rainforest, which explains why this locality had the highest species richness; the variation of the plant communities defines the diversity of pseudoscorpions. Furthermore, these types of vegetation produce a large amount of leaf litter, which, when accumulated, creates ideal temperature and humidity conditions, providing the shelter and food necessary for pseudoscorpion survival and reproduction (Weygoldt, 1969; Aguiar et al., 2006). Our results are in contrast to those of Hoff (1949, 1956, 1959), who found the highest pseudoscorpion diversity between 1828 and 2438 m a.s.l. These differences may be to the fact that Hoff's study was conducted in a temperate zone, and our study was in a tropical area. However, both studies recorded six families and three species at the same altitudinal level, suggesting that the communities are not so different. Although environmental variables (precipitation and temperature) had little impact on alpha diversity, our data showed that precipitation was a determining factor, to some extent, of the species diversity at the lowest locality. According to Lomolino (2001), local weather and environmental factors (temperature, precipitation, seasonality, and soil characteristics) vary along altitudinal gradients and influence species
Fig. 4. Incidence estimator's curves for localities. X axis represents the percentage sampling effort and Y axis is the percentage of richness estimated.
replacement. The highest values for the monthly gamma diversity were seen in March (γ = 1.68) and February (γ = 1.67). Finally, gamma diversity showed no significant correlation with temperature, but it did show a negative correlation with precipitation (rs = −0.672; P = 0.015; R2 = 0.452), with the highest values observed during the dry months. 4. Discussion Our results show that pseudoscorpion diversity decreases at higher altitudes. The highest alpha diversity was found at an altitude of 989 m a.s.l., which is similar to that recorded by Sato (1983), who found the 6
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Altitudinally adjacent localities had the highest similarity (150–989 m a.s.l.). This similarity is likely due to the floristic composition shared by these localities (cloud forests and tropical rainforests), which can also influence species replacement. Habitat preferences may also be important in species replacement. Five species were found in three localities, and we can divide them into two groups: Paratemnoides pallidus, Tyrannochthonius alabamensis, and Ideoblothrus maya, at 2177, 989, and 150 m a.s.l. (Fig. 2); and Americhernes reductus and Lustrochernes grossus, found at 2900, 989, and 150 m a.s.l. (Fig. 2). Species were found at different abundances in each locality but despite this, they were generally found in the same habitats, e.g., L. grossus was found underneath bark and logs, which coincides with previous reports (Hoff, 1956, 1959; Muchmore, 1990; Silva-Briano et al., 2010; Córdova-Tabares and Villegas-Guzmán, 2013). According to Cowles, this species is found up to 1200 m a.s.l. in Arizona, USA, although in this study it was found at 3000 m. A similar pattern was observed with Americhernes reductus, which was found underneath tree bark and decaying trunks. This species has been recorded underneath the bark of red mangroves in Florida and Belize (Muchmore, 1976), which coincides with the habitat preference seen in this study. The locality with the highest turnover was El Relámpago, at 2177 m a.s.l., which could be due to the high species abundance found here in February 2017;this temporal effect could explain the replacement. Moreover, although alpha diversity was not affected by temperature, beta diversity was (rdif.temp = 0.17; p = 0.0023), which is likely related to seasonality and replacement (Cabra-García et al., 2012). Thus, we consider that the replacement patterns observed could be due to the displacement of pseudoscorpions in search of food or shelter for their new offspring (Weygoldt, 1969). Gamma diversity result along the altitudinal gradient showed that alpha diversity was higher than beta diversity. According to Halffter and Moreno (2005), gamma diversity is strongly influenced by the alpha diversity of the richest community, which in this case was El Mameyal. Otherwise, beta diversity—via complementarity—would be the main factor influencing gamma diversity. The values reported here are difficult to compare against other studies because there are no equivalent estimates for pseudoscorpions. However, if we consider total species richness, a study of the diversity of non-spider arachnids (including pseudoscorpions) in the River Cauca basin found 27 species (Cabra-García et al., 2012); this value is similar to the 23 species found in our study. Additional studies from the neotropical region show between 1 and 50 samples, Chernetidae stand out as the family with the highest number of genera and species (Ceballos, 2004; Villegas-Guzmán and Gaona, 2019; Villegas-Guzmán, 2015). High Chernetidae richness was also present at our study site and agrees with the of Hoff (1959). The highest gamma diversity values were found in March (γ = 1.684) and February (γ = 1.669), during the dry season; beta diversity was higher in March and alpha was higher in February. Gamma diversity values could also be affected by reproductive cycles, as the increase in gamma diversity coincided with the beginning of the presence of protonymphs, deutonymphs, and tritonymphs—products of the reproductive cycle. In March and April, the greatest number of nymphs were found, which affected gamma diversity values. Similar declines in invertebrate species richness and abundance at high elevations have been documented elsewhere (e.g., Olson, 1994; Aguiar et al., 2006; Richardson and Richardson, 2013), but it is not always clear how spatial variation patterns are related to biodiversity.
Table 3 Pearson correlation of environmental variables for the period between April 2016 and April 2017. r = correlation coefficient, r2 = coefficient of determination, p = probability. Significant differences are in bold. Temperature
2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
Precipitation 2
r
r
P
r
r2
p
−0.14 −0.30 −0.23 −0.42
0.02 0.09 0.05 0.18
0.64 0.32 0.45 0.15
−0.32 −0.25 −0.35 −0.55
0.10 0.07 0.13 0.30
0.28 0.39 0.23 0.045
Table 4 (A) Values for beta diversity and nesting between βSörensen, overall beta diversity; βSimpson, dissimilitude due to species turnover between communities; βnested, nestedness of the assemblages. (B) Similarity of ANOSIM test for the different localities. Only P-values are shown. (A)
βSörensen
βSimpson
βnested
2999–2177 m a.s.l. 2999–989 m a.s.l. 2999–150 m a.s.l. 2177–989 m a.s.l. 2177–150 m a.s.l. 989–150 m a.s.l. Mean
1.000 0.750 0.500 0.600 0.714 0.417 0.664 ± 0.085
1.000 0.000 0.000 0.200 0.600 0.222 0.337 ± 0.160
0.000 0.750 0.500 0.400 0.114 0.194 0.326 ± 0.113
(B) 2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
2999 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
0.343
0.000 0.002
0.016 0.062 0.466
densities to a declining degree with the increase in elevation (Aguiar et al., 2006). Regarding seasonality, higher species richness was recorded in the cold and dry season (November to April) than in the warm and wet season (May to October). Weygoldt (1969) and Gabbutt (1969) mention that temperature could have an effect on reproductive process. Most pseudoscorpion species prefer warm temperatures (above 20 °C), although others (e.g., Neobisium carcinoides) reproduce at low temperatures (15–18 °C), which matches our findings. In the case of precipitation, there are no data to relate it to the richness and diversity of pseudoscorpions; it is only known that they prefer humid places (Weygoldt, 1969). In this study, our results showed that the species distributed along the altitudinal gradient had one reproductive cycle (univoltine species). The maximum densities of nymphs were found in March (104 specimens: 52 protonymphs, 37 deutonymphs, and 15 tritonymphs) and April (93 specimens: 53 protonymphs, 25 deutonymphs, and 15 tritonymphs), with the highest number at the lowest altitude (150 m a.s.l.; 262 nymphs: 111 protonymphs, 103 deutonymphs, and 48 tritonymphs). However, at an altitude of 2990 m a.s.l., no nymphs were captured, probably due to the low temperatures and strong winds registered in that area throughout the study period. Additionally, it is likely that the reproductive season begins when precipitation decreases—September to November—since pseudoscorpions complete their cycle in a 3- to 4-month period (Weygoldt, 1969), similar to that reported by Félix-Angulo (2018) in Mexican subtropical zones. Average β diversity was high, which means that the communities along the altitudinal gradient were quite different, and the partitioning of beta diversity showed that loss and replacement were equally important. It is important to note that the highest species replacement was seen during the dry season, which is mainly linked to changes in temperature; during the wet season, there was no species replacement.
5. Conclusion To the best of our knowledge, this study is the first to analyze the altitudinal distribution of pseudoscorpions from tropical forest to temperate forest. Our results showed that diversity decreased with altitude, and elevations below 1000 m a.s.l. presented more species diversity, richness, and composition, i.e., community structure (Rahbek, 1995; Grytnes and Vetaas, 2002). 7
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Pseudoscorpion communities showed a nested pattern at 2990 m a.s.l. This distribution pattern can be linked to precipitation and vegetation more than temperature. The gamma diversity (total diversity) was explained mainly by high local species richness (alpha diversity of localities) and to a lesser extent by the composition and replacement of species between sites (beta diversity). The composition and structure of the pseudoscorpion communities along the altitudinal gradient reflect the different forces (stochastic or deterministic) that drive them.
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University of Oslo Noruega, pp. 264. Harvey, M.S., Muchmore, W.B., 2013. The systematics of the pseudoscorpion family ideoroncidae (pseudoscorpiones: neobisioidea) in the new world. J. Arachnol. 41, 229–290. Harvey, M.S., 1992. The phylogeny and classification of the pseudoscorpionida (chelicerata: arachnida). Invertebr. Systemat. 6, 1373–1435. Harvey, M.S., 2013. Order pseudoscorpiones pp. 85-96. In: In: Zhang, Z.Q. (Ed.), Animal Biodiversity: an Outline of Higher-Level Classification and Survey of Taxonomic Richness (Addenda 2013), vol. 3703. pp. 1–82 Zootaxa. Harvey, M.S., Díaz, R.B., Muchmore, W.B., González, A.P., 2006. Pseudalbiorix, a new genus of ideoroncidae (pseudoscorpiones, neobisioidea) from Central America. J. Arachnol. 34, 610–626. https://doi.org/10.1636/s05-28.1. Hoff, C.C., 1949. The pseudoscorpions of Illinois. Bull. Illinois Nat. 24, 413–498. Hoff, C.C., 1956. Pseudoscorpions of the family Chernetidae from New Mexico. Am. Mus. Novit. 1800, 1–63. Hoff, C.C., 1959. 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Pseudoscorpions from Florida and the Caribbean area. 5. Americhernes, a new genus based upon Chelifer oblongus Say (Chernetidae). Fla. Entomol. 59, 151–163. https://doi.org/10.2307/3493964. Muchmore, W.B., 1990. Pseudoescorpions pp. 503-527. In: Dindal, D.L. (Ed.), Soil Biology Guide. John Wiley & Sons, New York, pp. 1376. Olson, D.M., 1994. The distribution of leaf litter invertebrates along a Neotropical altitudinal gradient. J. Trop. Ecol. 10, 129–150. https://doi.org/10.1017/ S0266467400007793. Rahbek, C., 1995. The elevational gradient of species richness: a uniform pattern? Ecography 18, 200–205. Ranius, T., 2002. Population ecology and conservation of beetles and pseudoscorpions living in hollow oaks in Sweden. Anim. Biodivers. Conserv. 25, 53–68. Richardson, B.A., Richardson, M.J., 2013. Litter-based invertebrate communities in forest floor and bromeliad microcosms along an elevational gradient in Puerto Rico. In: In: González, G., Willig, M.R., Waide, R.B. 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Author contributions VSJH, GAVG, JACG conceived the study and conducted fieldwork. VSJH and CFVM were responsible for data analysis and the interpretation of results. VSJH and GAVG carried out species identification. VSJH, GAVG, JACG, and CFVM wrote the manuscript. Acknowledgments The authors of this work would like to acknowledge and thank the municipal and communal authorities of Santiago Comaltepec, Oaxaca, for allowing them to enter and work in its forest areas; Mexico's National Council of Science and Technology (CONACyT 621564, Mexico), the Instituto Politécnico Nacional (20195362, Mexico) through scholarships for Violeta Jiménez Hernández; and Jesús López Santiago, Viridiana Vásquez Jiménez, María Elena López Martínez, and Selene Hernández Santiago for their fieldwork support. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.actao.2020.103525. References Aguiar, N.O., Gualberto, T.L., Franklin, E., 2006. A medium-spatial scale distribution pattern of Pseudoscorpionida (Arachnida) in a gradient of topography (altitude and inclination), soil factors, and litter in a central Amazonia forest reserve, Brazil. Braz. J. Biol. 66, 791–802. https://doi:10.1590/s1519-69842006000500004. Asc (Ayuntamiento de Santiago Comaltepec), 2010. Plan municipal de desarrollo. Santiago Comaltepec, Ixtlán, Oaxaca. [pdf] Available at: https://www.finanzasoaxaca. gob.mx/pdf/inversion_publica/pmds/08_10/458.pdf accessed 8 August 2016. Baselga, A., 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecol. Biogeogr. 19 (1), 134–143. https://doi.org/10.1111/j.1466-8238.2009. 00490.x. In this issue. Cabra-García, J., Bermúdez-Rivas, C., Osorio, A.M., Chacón, P., 2012. Cross-taxon congruence of α and β diversity among five leaf litter arthropod groups in Colombia. Biodivers. Conserv. 21, 1493–1508. https://doi.org/10.1007/s10531-012-0259-5. Ceballos, A., 2004. Pseudoscorpionida. In: In: Llorente-Bousquets, J., Morrone, J.J., Ordóñez, O.Y., Vargas-Fernández, I. (Eds.), Biodiversidad, Taxonomía y Biogeografía de Artrópodos de México: hacia una síntesis de su conocimiento, vol. 4. Facultad de Ciencias, UNAM, Mexico, pp. 790 417-429. Chamberlin, J.C., 1931a. The Arachnid Order Chelonethida. Stanford University Press, pp. 284. Chamberlin, J.C., 1931b. A synoptic revision of the generic classification of the Chelonethid family Cheliferidae Simon (Arachnida). Can. Entomol. 64, 289–294. Chamberlin, J.C., Chamberlin, R.V., 1945. The genera and species of the Tridenchthoniidae (Dithidae): a family of the arachnid order Chelonethida. Bull. Univ. Utah 35, 5–66. https://doi.org/10.1136/ard.2007.082081. Colwell, R.K., 2006. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 9.1. http://viceroy.colorado.edu/estimates/, Accessed date: 15 May 2017. Córdova-Tabares, V.M., Villegas-Guzmán, G.A., 2013. Nuevos registros de pseudoescorpiones (Arachnida: pseudoescorpiones) en Chiapas, México. Acta Zool. Mex. 29, 596–613. Félix-Angulo, A.G., 2018. Diversidad de pseudoescorpiones (Arachnida: pseudoscorpiones) en bosque de Mangle en la localidad el Conchal, Culiacán, Sinaloa. Bol. Soc. Mex. Ento. 4, 5–8. Fick, S.E., Hijmans, R.J., 2017. Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. http://worldclim.org/version2 accessed 09 september 2017. Flores-Luna, E., 2006. Estudio preliminar de los pseudoescorpiones (Arachnida: Pseudoescorpiones) de Oaxaca, México. Memoria de Residencia Profesional. Instituto Tecnológico del Valle de Oaxaca, pp. 62. Francke, O.F., 2013. Biodiversidad de Arthropoda (Chelicerata: aracnida ex Acari) en
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ciudad de México y sus alrededores. Entomol. Mex. 2, 76–81. Villegas-Guzmán, G.A., Flores-Luna, E., Vásquez-Dávila, M.A., 2006. Nuevos registros de pseudoescorpiones (Arachnida: pseudoescorpiones) de Oaxaca, México. In: In: Estrada-Venegas, E.G., Romero-Napoles, J., Equihua-Martinez, A., Luna-Leon, C., Rosas-Acevedo, J. (Eds.), Entomol. Mex 5. pp. 127–132 Mexico. Villegas-Guzmán, G.A., Gaona, S., 2019. Primer registro de pseudoescorpiones (Arachnida: pseudoscorpiones) de Guanajuato, México. DUGESIANA 26, 173–178. Weygoldt, P., 1969. The Biology of Pseudoscorpiones. Harvard Universiy Press, Cambrige, Masachusetts, pp. 145. Whittaker, R.H., 1972. Evolution and measurement of species diversity. Taxon 21 (2/3), 213–251. https://doi.org/10.2307/1218190. Wirth, W.W., Marston, N., 1968. A method for mounting small insects on microscope slides in Canada balsam. Ann. Entomol. Soc. Am. 61, 783–784. Zar, J.H., 1999. Biostatistical Analysis. Pearson Education India, pp. 944.
101–116. Sanders, N.J., 2002. Elevational gradients in ant species richness: area, geometry, and Rapoport's rule. Ecography 25, 25–32. https://doi.org/10.1034/j.1600-0587.2002. 250104.x. Sato, H., 1983. Altitudinal distribution of soil pseudoscorpions at Mt Fuji. Edaphologia 28, 13–22. Silva-Briano, M., Adabache-Ortiz, A., Gómez-Torres, y G., 2010. Introducción al conocimiento de los pseudoescorpiones del estado de Aguascalientes. Investig. Ciencia Univ. Autónoma Aguascalientes 50, 5–9. Stevens, G.C., 1992. The elevational gradient in altitudinal range: an extension of Rapoport's latitudinal rule to altitude. Am. Nat. 140, 893–911. https://doi.org/10. 1086/285447. Tothmeresz, B., 1995. Comparison of different methods for diversity ordering. J. Veg. Sci. 6, 283–290. https://doi.org/10.2307/3236223. Villegas-Guzmán, G.A., 2015. Pseudoescorpiones (Arachnida: pseudoscorpiones) de la
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Original article
Altitudinal distribution of alpha, beta, and gamma diversity of pseudoscorpions (Arachnida) in Oaxaca, Mexico
T
Violeta Saraí Jiménez-Hernándeza, Gabriel Alfredo Villegas-Guzmána,b, José Arturo Casasola-Gonzálezc, Carlos Fabián Vargas-Mendozad,∗ a
Laboratorio de Acarología, Departamento Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación Carpio y Plan de Ayala S/n, Col. Casco de Santo Tomás C.P, 11340, Ciudad de México, Mexico b Laboratorio de Conservación de Fauna Silvestre, Universidad Autónoma Metropolitana Iztapalapa, San Rafael Atlixco No. 186, Col. Vicentina, C.P, 09340, Delegación Iztapalapa, Ciudad de México, Mexico c Instituto de Estudios Ambientales, Universidad de La Sierra Juárez, Av. Universidad S/n. Ixtlán de Juárez. C.P, 68725, Oaxaca, Mexico d Laboratorio de Variación Biológica y Evolución, Departamento Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación Carpio y Plan de Ayala S/n, Col. Casco de Santo Tomás C.P, 11340, Ciudad de México, Mexico
A R T I C LE I N FO
A B S T R A C T
Keywords: Species richness Species abundance Santiago comaltepec Diversity Altitudinal gradient
In this study, we describe the spatial and temporal variation in the diversity of pseudoscorpions along an altitudinal gradient in Santiago Comaltepec, Oaxaca, Mexico. Four altitudinal levels were selected (150, 989, 2177, and 2990 m a.s.l.). Species were recorded through monthly sampling from April 2016 to April 2017. Alpha and beta diversities were estimated at every altitude, and gamma diversity was calculated for the entire gradient; diversity was then related to temperature and precipitation. The highest species richness was observed at 989 m a.s.l. and the lowest at 2990 m a.s.l. The months with the lowest number of species and specimens were January, March, and April. The highest Shannon index value was observed at 989 m a.s.l. (H′ = 1.724) and the lowest at 2177 m a.s.l. (H′ = 0.692). Gamma diversity was 2.15 and was mainly affected by the average alpha diversity. Alpha diversity was higher during the dry season and was slightly regulated by precipitation. Moreover, higher species replacement was observed in the dry season than in the wet season, which was mainly associated with changes in temperature. Overall, with the increase in altitude, the diversity of pseudoscorpions decreases.
1. Introduction
has not been properly studied for all groups of organisms (Rahbek, 1995; Gaston and Spicer, 2004). In order to understand the spatial variation patterns of biodiversity with respect to the structure of the landscape, the various components of species diversity must be evaluated, i.e., a) the species richness of a community (alpha diversity), b) the degree of change in species composition across different communities (beta diversity), and c) the species richness of all communities in a landscape (gamma diversity) (Whittaker, 1972; Moreno, 2001; Koleff, 2005; Magurran and McGill, 2011). The altitudinal distribution of arthropods has not been widely studied and pseudoscorpions, in particular, have received very little attention (Muchmore, 1976, 1990; Olson, 1994; Aguiar et al., 2006; Richardson and Richardson, 2013). Pseudoscorpions are small arachnids, measuring between 1 and 12 mm, that live in moss and leaf litter, under logs, stones, bark, and in bird, rodent, and insect nests; they are cryptic predators of small arthropods. Pseudoscorpions are mainly distributed in tropical and subtropical
The distribution of biodiversity along environmental gradients (latitude, longitude, and altitude) has received considerable research attention (Olson, 1994; Sanders, 2002; Gaston and Spicer, 2004; Aguiar et al., 2006; Richardson and Richardson, 2013). Based on these studies, several patterns of species richness have been proposed (Stevens, 1992; Sanders, 2002; McCain and Bracy-Knight, 2013). There are two common models of species distribution: the first predicts a monotonic decrease in the number of species with altitude, and the second predicts a hump-shaped pattern, with a peak in the middle of the gradient (Stevens, 1992; Rahbek, 1995; Lomolino, 2001; Gaston and Spicer, 2004). Changes in species abundance and composition are generally related to changes in temperature and humidity with elevation (Malumbres-Olarte et al., 2018). Although species abundance and distribution are known to be closely related, the nature of this relationship
∗
Corresponding author. E-mail addresses: [email protected], [email protected] (C.F. Vargas-Mendoza).
https://doi.org/10.1016/j.actao.2020.103525 Received 11 July 2019; Received in revised form 6 January 2020; Accepted 17 January 2020 Available online 21 February 2020 1146-609X/ © 2020 Elsevier Masson SAS. All rights reserved.
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and dry leaves hanging from plants, for 2 h along each transect. Specimens were taken directly from these microhabitats using fine-tip tweezers and placed in containers with 80% ethanol (Muchmore, 1990). Pseudoscorpions were processed following Hoff's technique (1949) with Wirth and Marston (1968) modifications. Taxonomic identification was performed under a phase-contrast microscope (Carl Zeiss, Ulm, Germany) with reference to specialized literature (e.g., Chamberlin, 1931a,b; Chamberlin and Chamberlin, 1945; Hoff, 1956; Muchmore, 1990; Harvey, 1992; Harvey et al., 2006; Harvey and Muchmore, 2013). The specimens were deposited in the collection “Dra. Isabel Bassols Batalla” of the Acarology Laboratory of the Escuela Nacional de Ciencias Biológicas of the Instituto Politécnico Nacional, Mexico City, Mexico.
regions (Chamberlin, 1931a,b; Hoff, 1949; Weygoldt, 1969; Muchmore, 1990). There are 3799 species worldwide (Harvey, 2013), of which 167 are found in Mexico (Harvey et al., 2006; Francke, 2013; VillegasGuzmán, 2015). In Oaxaca, 43 species have been recorded (Flores-Luna, 2006; Villegas-Guzmán et al., 2006; Harvey and Muchmore, 2013), of which 21 are found in Sierra Norte de Oaxaca (Villegas-Guzmán et al., 2006; Jiménez-Hernández, 2016; Jiménez-Hernández et al., 2018). To date, only two studies have related the diversity of pseudoscorpions to altitude (Hoff, 1959; Sato, 1983). On one hand, it is thought that the highest species diversity is found at intermediate elevations, and on the other, that pseudoscorpions follow three range size distribution patterns namely, a) restricted distribution, below 900 m, b) intermediate level, between 900 m and 1300 m, c) high altitude, between 1100 m and 2300 m (Sato, 1983). This study aims to describe the spatial and temporal variation of pseudoscorpion diversity along an altitudinal gradient in Sierra Norte de Oaxaca, Mexico. In contrast to previous studies, this research was conducted in a tropical area. We compared differences and similarities in the patterns of species richness and attempted to elucidate: 1) α and β diversities at different altitudes; 2) the relationships between α and β diversities, and temperature and precipitation at the sampling sites; and 3) gamma diversity variation across the altitudinal gradient over a oneyear cycle.
2.3. Data analysis 2.3.1. Alpha diversity (α) The total number of species (S), the Shannon-Weaver (H′) index, Pielou's equitability (J′) index, and individual rarefaction estimates for each index were estimated (Magurran, 1988, 2004; Moreno et al., 2011). In addition, Hill numbers were calculated following Moreno et al. (2011) and a plot of the Rényi index was developed using the parameter α in order to verify which localities were non-comparable (if the lines of localities crossed, those diversity indices were deemed noncomparable) (Tothmeresz, 1995). Non-parametric species richness was calculated using Chao2 and Clench estimators, using ESTIMATE v9.1 software (Colwell, 2006). Shannon-Weaver (H′) index values were compared between localities using a Hutcheson's t-test (Zar, 1999; Magurran, 1988, 2004). Correlations between diversity and weather variables, i.e., temperature and precipitation, were calculated for each locality. Monthly averages were obtained for a one-year cycle at different gathering points using historical data from 1970 to 2000 (WORLDCLIM v2 - Global Climate Data), with a spatial resolution of 30 arcseconds (approximately 1 km resolution at the equator) (Fick and Hijmans, 2017). Subsequently, the Shannon-Weaver index was estimated for each locality and for the study period (April 2016 to April 2017) in order to identify the month with the highest alpha diversity (α).
2. Materials and methods 2.1. Study area The study area was a northeast-facing hillside, with an elevation of almost 3000 m a.s.l., located in Santiago Comaltepec (17°34′N, 96°33′W), a municipality of Sierra Norte de Oaxaca, México (Ayuntamiento de Santiago Comaltepec, 2010) Santiago Comaltepec has an altitudinal gradient that includes variation in slope, soil factors, and vegetation types (INAFED (Instituto Nacional para el Federalismo y el Desarrollo Municipal), 2016). A range of sites were selected, separated by an interval of approximately 1000 m. Samples sites were accessed from highway 175, Oaxaca-Tuxtepec, in the direction of Golfo de Mexico. Sites of the same elevation were separated by large horizontal distances (14–20 km) due to the inaccessibility of closer localities. All transects were located in apparently undisturbed forest at least 500 m from the highway edge, except for Soyolapam (Fig. 1). The sites included: 1) Soyolapam (17°41′40.4″N, 96°16′14.6″W) at 150 m a.s.l., with patches of tropical rainforest and secondary herbaceous and shrub vegetation areas; 2) El Mameyal (17°40′31.5″N, 96°19′22.2″W) at 989 m a.s.l., corresponding to a transition zone between the cloud forest and the tropical rainforest; 3) El Relámpago (17°35′30″N, 96° 23′56.0″W) located at 2177 m a.s.l. and characterized by a cloud forest; and 4) Cerro Pelón (17°34′28.4″N, 96°30′15.5″W) located at 2990 m a.s.l., characterized by a dwarf shrubland and open temperate forest with some Pinus hartwegii.
2.3.2. Beta diversity (β) Three estimators of beta diversity were used: Sörensen (βSor), Simpson (βSim), and nestedness (βNested) dissimilarity indices, according to Baselga (2010). With these indices, beta diversity turnover and nestedness were partitioned. An analysis of similarities (ANOSIM) was also conducted to evaluate differences between localities using PAST v3.16 (Koleff, 2005; Hammer et al., 2017). To determine which of the two variables—temperature or precipitation—affect species replacement, a paired matrix was created using the differences in these variables (temperature difference = ToC localityi - ToC localityj; precipitation difference = locality precipitationi - locality precipitationj) for each locality and sampling month. These data were used to perform a Cochran-Mantel-Haenszel test (Mantel and Haenszel, 1959), using PAST v3.16 (Hammer et al., 2017).
2.2. Sampling Pseudoscorpions were sampled every month from April 2016 to April 2017. A transect 200 m long and 10 m wide was established at every study locality. Specimens were collected using three methods: 1) pitfall traps, 2) leaf litter collection, and 3) direct capture (Hoff, 1949; Muchmore, 1990; Ranius, 2002; Márquez-Luna, 2005). For the pitfall traps, five traps were placed along each transect, 40 m apart, containing a 1:1 mixture of 80% ethanol and ethylene glycol. For the leaf litter, three samples of leaf litter and soil weighing approximately 800 g were collected randomly, and were stored in plastic bags and transported to the laboratory, where they were processed using the Berlese-Tullgren funnel technique. Direct capture consisted of searching for pseudoscorpions under bark, in logs and leaf sheaths, and underneath stones
2.3.3. Gamma diversity (γ) Gamma diversity was obtained by adding alpha and beta average diversities (Moreno, 2001). Total monthly temperature and precipitation were correlated with the gamma diversity values obtained for each sampling month using Spearman's correlation coefficients, using PAST v3.16 software (Hammer et al., 2017). 3. Results A total of 742 specimens were collected, of which 354 were adults (48%) and 388 were nymphs (52%). Twenty-three species were found 2
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Fig. 1. Study area and pitfall trap locations. The subscript indicates the trap number (1–5). A. Cerro Pelón; B. El Relámpago; C. El Mameyal; D. Soyolapam.
Fig. 2. Altitudinal distribution of pseudoscorpions in the hillside studied. Species sizes represent their abundance.
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Fig. 3. Abundance of individuals using A) Rarefaction Species Richness and B) Shannon exp (H′).
P-values of 0.21 at El Relámpago (2177 m a.s.l.) and 0.25 at El Mameyal (989 m a.s.l.), suggest that species richness was likely to be greater than observed at localities between those altitudes (Fig. 3). The highest species richness was observed at 989 m a.s.l. and the lowest at 2990 m a.s.l. (Table 1). At 150 m a.s.l. (Soyolapam), the highest diversity was seen in September 2016, when precipitation started to decrease. The months with the highest diversity were January 2017, April 2016, April 2017, and October 2016 (Table 1), while in May 2016 and July 2016 no specimens were found at 989 m a.s.l. (El Mameyal). At 2177 m a.s.l. (El Relámpago), February was the only month with records and the H′ value was 1.11. Finally, at 2990 m a.s.l. (Cerro Pelón), there were two peaks, one in November (H′ = 0.68) and one in March (H′ = 0.64). No presence was recorded in the other months (Table 1). The Hutcheson's t-test showed that diversity at 989 m a.s.l. (El Mameyal) was significantly higher than that of other localities (Cerro Pelón: t = −4.63, P < 0.001; El Relámpago: t = −7.26, P < 0.001; and Soyolapam: t = 2.32, P = 0.02) (Table 2). At 150 m a.s.l., diversity was higher than at localities above 2000 m a.s.l. (Cerro Pelón: t = −3.83, P = 0.0014 and El Relámpago: t = −6.35, P < 0.001). Conversely, diversity at localities higher than 1000 m a.s.l. was lower than that at localities below 1000 m a.s.l. (t = 0.16; P = 0.87) (Table 2). The correlation coefficient (r) for α diversity and
along the altitudinal gradient (Fig. 2). However, only 18 different species were identified, belonging to 16 genera and 10 families. 3.1. Effect of altitude on alpha diversity (α) According to Chao 2, good sampling efficiency was obtained at three localities (Fig. 3): 77% in Cerro Pelón (2990 m a.s.l.); 83% in El Mameyal (989 m a.s.l.); and 100% in Soyolapam (150 m a.s.l.). In contrast, 47% of the estimated richness was obtained at El Relámpago (2177 m a.s.l.). Three of the four sampling localities showed good estimations of species richness, according to the Shannon-Weaver index and rarefaction results (Fig. 4). Species richness and the abundance of pseudoscorpions were distributed homogenously at the extremes of the altitudinal gradient (150 and 2990 m a.s.l.), reflecting greater equitability (Table 1). Hill numbers showed that high diversity existed below 1000 m a.s.l. (Table 1) and diversity was lower above 1000 m a.s.l. The Rényi index plot (Supplementary material) showed that the only comparable locations were those above and below 1000 m a.s.l.; between these intervals, localities were not comparable because their lines crossed. The Clench equation showed a coefficient of determination of 0.99 for all localities. A P-value (slope) close to 0.1 at the extremes of the gradient suggested an complete inventory of species at those altitudes. 4
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Fig. 3. (continued)
Pelón (βSimpson = 1.000), and those with the greatest nestedness were El Mameyal with Cerro Pelón (βnested = 0.750; Table 4). In terms of species replacement, the months from May to August (the beginning to the middle of the wet season) were found to have the highest replacement, and conversely, April (βaverage = 0.76) had the least replacement. The Cochran-Mantel-Haenszel test resulted in a correlation coefficient of rdif.pp = −0.006, P = 0.58 for precipitation and rdif.temp = 0.17, P = 0.0023 for temperature. The latter is a weak, but significant, positive correlation, i.e., species replacement was slightly higher when the temperature difference was higher. In the former, no association was found, i.e., pseudoscorpion β diversity was not determined by monthly variation in precipitation.
precipitation at 150 m a.s.l. was significative (rsoyolapam = −0.42; P = 0.045) but no significant correlations were found at any of the other localities, for either precipitation or temperature (Table 3).
3.2. Beta diversity (β) Similar pseudoscorpion communities were those found at El Mameyal (989 m a.s.l.) and Soyolapam (150 m a.s.l.), followed by Cerro Pelón (2990 m a.s.l.) and Soyolapam. The community at El Relámpago (2177 m a.s.l.) showed the least similarity to those at other localities (Table 4). The ANOSIM results showed similar patterns (mean rank within = 1224; mean rank between = 1296; P = 0.0004; Table 4). Values of beta diversity were high when comparing all localities with each other (βSörensen = 0.664 ± 0.085). Approximately 50% of this diversity was due to turnover (βSimpson = 0.337 ± 0.160) and 50% to nestedness (βnested = 0.326 ± 0.113); this means that beta diversity is influenced by species replacement and loss (Baselga, 2010). The communities with the greatest turnover were El Relámpago and Cerro
3.3. Gamma diversity (γ) along the altitudinal gradient Gamma diversity along the altitudinal gradient had a value of 2.15 and was affected by the average alpha diversity (1.17; 54%), and by the average beta diversity (0.98; 46%). This means that the number of species in each locality was slightly higher than the species 5
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Table 1 Diversity recorded at localities along an altitudinal gradient. A) q0: species richness; q1: Shannon-Weber index exponential (eH’); q2: inverse of Simpson dominance index (1/∑ p i2; pi = species frequency). B) Monthly alpha diversity.
Species richness Number of specimens Pielou equitability (J′) Hill numbers q0 q1 q2
2990 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
3 15 0.664
5 71 0.430
15 258 0.637
9 398 0.694
3 2.075 1.718
5 1.998 1.509
15 5.607 3.683
9 4.591 3.412
B) Alpha diversity Month
2999 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
April 2016 May 2016 June 2016 July 2016 August 2016 September 2016 October 2016 November 2016 December 2016 January 2017 February 2017 March 2017 April 2017
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.683 0.000 0.000 0.000 0.637 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.105 0.000 0.000
1.677 0.000 0.956 0.000 0.956 1.386 1.642 1.011 0.637 1.887 1.066 1.420 1.673
0.000 0.000 0.000 0.000 0.000 0.614 0.562 0.500 0.637 0.500 1.071 1.428 1.292
Table 2 Student's t-test (modified by Hutcheson) values for different elevations. Significant differences are in bold.
2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
2990 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
t = 0.161 p = 0.873 t = −4.635 p = 0.00018 t = −3.831 p = 0.0014
t = −7.259 p < 0.001 t = −6.35 p < 0.001
t = 2.325 p = 0.0205
150 m a.s.l.
highest diversity between 900 and 1300 m a.s.l. This finding is probably related to vegetation type, since the shape and structure of terrestrial communities are defined mainly by vegetation (Stevens, 1992). El Mameyal (989 m a.s.l.) is a transition zone between cloud forests and tropical rainforest, which explains why this locality had the highest species richness; the variation of the plant communities defines the diversity of pseudoscorpions. Furthermore, these types of vegetation produce a large amount of leaf litter, which, when accumulated, creates ideal temperature and humidity conditions, providing the shelter and food necessary for pseudoscorpion survival and reproduction (Weygoldt, 1969; Aguiar et al., 2006). Our results are in contrast to those of Hoff (1949, 1956, 1959), who found the highest pseudoscorpion diversity between 1828 and 2438 m a.s.l. These differences may be to the fact that Hoff's study was conducted in a temperate zone, and our study was in a tropical area. However, both studies recorded six families and three species at the same altitudinal level, suggesting that the communities are not so different. Although environmental variables (precipitation and temperature) had little impact on alpha diversity, our data showed that precipitation was a determining factor, to some extent, of the species diversity at the lowest locality. According to Lomolino (2001), local weather and environmental factors (temperature, precipitation, seasonality, and soil characteristics) vary along altitudinal gradients and influence species
Fig. 4. Incidence estimator's curves for localities. X axis represents the percentage sampling effort and Y axis is the percentage of richness estimated.
replacement. The highest values for the monthly gamma diversity were seen in March (γ = 1.68) and February (γ = 1.67). Finally, gamma diversity showed no significant correlation with temperature, but it did show a negative correlation with precipitation (rs = −0.672; P = 0.015; R2 = 0.452), with the highest values observed during the dry months. 4. Discussion Our results show that pseudoscorpion diversity decreases at higher altitudes. The highest alpha diversity was found at an altitude of 989 m a.s.l., which is similar to that recorded by Sato (1983), who found the 6
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Altitudinally adjacent localities had the highest similarity (150–989 m a.s.l.). This similarity is likely due to the floristic composition shared by these localities (cloud forests and tropical rainforests), which can also influence species replacement. Habitat preferences may also be important in species replacement. Five species were found in three localities, and we can divide them into two groups: Paratemnoides pallidus, Tyrannochthonius alabamensis, and Ideoblothrus maya, at 2177, 989, and 150 m a.s.l. (Fig. 2); and Americhernes reductus and Lustrochernes grossus, found at 2900, 989, and 150 m a.s.l. (Fig. 2). Species were found at different abundances in each locality but despite this, they were generally found in the same habitats, e.g., L. grossus was found underneath bark and logs, which coincides with previous reports (Hoff, 1956, 1959; Muchmore, 1990; Silva-Briano et al., 2010; Córdova-Tabares and Villegas-Guzmán, 2013). According to Cowles, this species is found up to 1200 m a.s.l. in Arizona, USA, although in this study it was found at 3000 m. A similar pattern was observed with Americhernes reductus, which was found underneath tree bark and decaying trunks. This species has been recorded underneath the bark of red mangroves in Florida and Belize (Muchmore, 1976), which coincides with the habitat preference seen in this study. The locality with the highest turnover was El Relámpago, at 2177 m a.s.l., which could be due to the high species abundance found here in February 2017;this temporal effect could explain the replacement. Moreover, although alpha diversity was not affected by temperature, beta diversity was (rdif.temp = 0.17; p = 0.0023), which is likely related to seasonality and replacement (Cabra-García et al., 2012). Thus, we consider that the replacement patterns observed could be due to the displacement of pseudoscorpions in search of food or shelter for their new offspring (Weygoldt, 1969). Gamma diversity result along the altitudinal gradient showed that alpha diversity was higher than beta diversity. According to Halffter and Moreno (2005), gamma diversity is strongly influenced by the alpha diversity of the richest community, which in this case was El Mameyal. Otherwise, beta diversity—via complementarity—would be the main factor influencing gamma diversity. The values reported here are difficult to compare against other studies because there are no equivalent estimates for pseudoscorpions. However, if we consider total species richness, a study of the diversity of non-spider arachnids (including pseudoscorpions) in the River Cauca basin found 27 species (Cabra-García et al., 2012); this value is similar to the 23 species found in our study. Additional studies from the neotropical region show between 1 and 50 samples, Chernetidae stand out as the family with the highest number of genera and species (Ceballos, 2004; Villegas-Guzmán and Gaona, 2019; Villegas-Guzmán, 2015). High Chernetidae richness was also present at our study site and agrees with the of Hoff (1959). The highest gamma diversity values were found in March (γ = 1.684) and February (γ = 1.669), during the dry season; beta diversity was higher in March and alpha was higher in February. Gamma diversity values could also be affected by reproductive cycles, as the increase in gamma diversity coincided with the beginning of the presence of protonymphs, deutonymphs, and tritonymphs—products of the reproductive cycle. In March and April, the greatest number of nymphs were found, which affected gamma diversity values. Similar declines in invertebrate species richness and abundance at high elevations have been documented elsewhere (e.g., Olson, 1994; Aguiar et al., 2006; Richardson and Richardson, 2013), but it is not always clear how spatial variation patterns are related to biodiversity.
Table 3 Pearson correlation of environmental variables for the period between April 2016 and April 2017. r = correlation coefficient, r2 = coefficient of determination, p = probability. Significant differences are in bold. Temperature
2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
Precipitation 2
r
r
P
r
r2
p
−0.14 −0.30 −0.23 −0.42
0.02 0.09 0.05 0.18
0.64 0.32 0.45 0.15
−0.32 −0.25 −0.35 −0.55
0.10 0.07 0.13 0.30
0.28 0.39 0.23 0.045
Table 4 (A) Values for beta diversity and nesting between βSörensen, overall beta diversity; βSimpson, dissimilitude due to species turnover between communities; βnested, nestedness of the assemblages. (B) Similarity of ANOSIM test for the different localities. Only P-values are shown. (A)
βSörensen
βSimpson
βnested
2999–2177 m a.s.l. 2999–989 m a.s.l. 2999–150 m a.s.l. 2177–989 m a.s.l. 2177–150 m a.s.l. 989–150 m a.s.l. Mean
1.000 0.750 0.500 0.600 0.714 0.417 0.664 ± 0.085
1.000 0.000 0.000 0.200 0.600 0.222 0.337 ± 0.160
0.000 0.750 0.500 0.400 0.114 0.194 0.326 ± 0.113
(B) 2999 m a.s.l. 2177 m a.s.l. 989 m a.s.l. 150 m a.s.l.
2999 m a.s.l.
2177 m a.s.l.
989 m a.s.l.
150 m a.s.l.
0.343
0.000 0.002
0.016 0.062 0.466
densities to a declining degree with the increase in elevation (Aguiar et al., 2006). Regarding seasonality, higher species richness was recorded in the cold and dry season (November to April) than in the warm and wet season (May to October). Weygoldt (1969) and Gabbutt (1969) mention that temperature could have an effect on reproductive process. Most pseudoscorpion species prefer warm temperatures (above 20 °C), although others (e.g., Neobisium carcinoides) reproduce at low temperatures (15–18 °C), which matches our findings. In the case of precipitation, there are no data to relate it to the richness and diversity of pseudoscorpions; it is only known that they prefer humid places (Weygoldt, 1969). In this study, our results showed that the species distributed along the altitudinal gradient had one reproductive cycle (univoltine species). The maximum densities of nymphs were found in March (104 specimens: 52 protonymphs, 37 deutonymphs, and 15 tritonymphs) and April (93 specimens: 53 protonymphs, 25 deutonymphs, and 15 tritonymphs), with the highest number at the lowest altitude (150 m a.s.l.; 262 nymphs: 111 protonymphs, 103 deutonymphs, and 48 tritonymphs). However, at an altitude of 2990 m a.s.l., no nymphs were captured, probably due to the low temperatures and strong winds registered in that area throughout the study period. Additionally, it is likely that the reproductive season begins when precipitation decreases—September to November—since pseudoscorpions complete their cycle in a 3- to 4-month period (Weygoldt, 1969), similar to that reported by Félix-Angulo (2018) in Mexican subtropical zones. Average β diversity was high, which means that the communities along the altitudinal gradient were quite different, and the partitioning of beta diversity showed that loss and replacement were equally important. It is important to note that the highest species replacement was seen during the dry season, which is mainly linked to changes in temperature; during the wet season, there was no species replacement.
5. Conclusion To the best of our knowledge, this study is the first to analyze the altitudinal distribution of pseudoscorpions from tropical forest to temperate forest. Our results showed that diversity decreased with altitude, and elevations below 1000 m a.s.l. presented more species diversity, richness, and composition, i.e., community structure (Rahbek, 1995; Grytnes and Vetaas, 2002). 7
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Pseudoscorpion communities showed a nested pattern at 2990 m a.s.l. This distribution pattern can be linked to precipitation and vegetation more than temperature. The gamma diversity (total diversity) was explained mainly by high local species richness (alpha diversity of localities) and to a lesser extent by the composition and replacement of species between sites (beta diversity). The composition and structure of the pseudoscorpion communities along the altitudinal gradient reflect the different forces (stochastic or deterministic) that drive them.
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Author contributions VSJH, GAVG, JACG conceived the study and conducted fieldwork. VSJH and CFVM were responsible for data analysis and the interpretation of results. VSJH and GAVG carried out species identification. VSJH, GAVG, JACG, and CFVM wrote the manuscript. Acknowledgments The authors of this work would like to acknowledge and thank the municipal and communal authorities of Santiago Comaltepec, Oaxaca, for allowing them to enter and work in its forest areas; Mexico's National Council of Science and Technology (CONACyT 621564, Mexico), the Instituto Politécnico Nacional (20195362, Mexico) through scholarships for Violeta Jiménez Hernández; and Jesús López Santiago, Viridiana Vásquez Jiménez, María Elena López Martínez, and Selene Hernández Santiago for their fieldwork support. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.actao.2020.103525. References Aguiar, N.O., Gualberto, T.L., Franklin, E., 2006. A medium-spatial scale distribution pattern of Pseudoscorpionida (Arachnida) in a gradient of topography (altitude and inclination), soil factors, and litter in a central Amazonia forest reserve, Brazil. Braz. J. Biol. 66, 791–802. https://doi:10.1590/s1519-69842006000500004. Asc (Ayuntamiento de Santiago Comaltepec), 2010. Plan municipal de desarrollo. Santiago Comaltepec, Ixtlán, Oaxaca. [pdf] Available at: https://www.finanzasoaxaca. gob.mx/pdf/inversion_publica/pmds/08_10/458.pdf accessed 8 August 2016. Baselga, A., 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecol. Biogeogr. 19 (1), 134–143. https://doi.org/10.1111/j.1466-8238.2009. 00490.x. In this issue. Cabra-García, J., Bermúdez-Rivas, C., Osorio, A.M., Chacón, P., 2012. Cross-taxon congruence of α and β diversity among five leaf litter arthropod groups in Colombia. Biodivers. Conserv. 21, 1493–1508. https://doi.org/10.1007/s10531-012-0259-5. Ceballos, A., 2004. Pseudoscorpionida. In: In: Llorente-Bousquets, J., Morrone, J.J., Ordóñez, O.Y., Vargas-Fernández, I. (Eds.), Biodiversidad, Taxonomía y Biogeografía de Artrópodos de México: hacia una síntesis de su conocimiento, vol. 4. Facultad de Ciencias, UNAM, Mexico, pp. 790 417-429. Chamberlin, J.C., 1931a. The Arachnid Order Chelonethida. Stanford University Press, pp. 284. Chamberlin, J.C., 1931b. A synoptic revision of the generic classification of the Chelonethid family Cheliferidae Simon (Arachnida). Can. Entomol. 64, 289–294. Chamberlin, J.C., Chamberlin, R.V., 1945. The genera and species of the Tridenchthoniidae (Dithidae): a family of the arachnid order Chelonethida. Bull. Univ. Utah 35, 5–66. https://doi.org/10.1136/ard.2007.082081. Colwell, R.K., 2006. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 9.1. http://viceroy.colorado.edu/estimates/, Accessed date: 15 May 2017. Córdova-Tabares, V.M., Villegas-Guzmán, G.A., 2013. Nuevos registros de pseudoescorpiones (Arachnida: pseudoescorpiones) en Chiapas, México. Acta Zool. Mex. 29, 596–613. Félix-Angulo, A.G., 2018. Diversidad de pseudoescorpiones (Arachnida: pseudoscorpiones) en bosque de Mangle en la localidad el Conchal, Culiacán, Sinaloa. Bol. Soc. Mex. Ento. 4, 5–8. Fick, S.E., Hijmans, R.J., 2017. Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. http://worldclim.org/version2 accessed 09 september 2017. Flores-Luna, E., 2006. Estudio preliminar de los pseudoescorpiones (Arachnida: Pseudoescorpiones) de Oaxaca, México. Memoria de Residencia Profesional. Instituto Tecnológico del Valle de Oaxaca, pp. 62. Francke, O.F., 2013. Biodiversidad de Arthropoda (Chelicerata: aracnida ex Acari) en
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