Ant Community Organization Along Elevational Gradients in a Temperate Ecosystem

Insect. Soc. DOI 10.1007/s00040-014-0374-2 Insectes Sociaux

RESEARCH ARTICLE

Ant community organization along elevational gradients in a temperate ecosystem

A. Bernadou • X. Espadaler • A. Le Goff • V. Fourcassie´

Received: 20 February 2014 / Revised: 27 September 2014 / Accepted: 9 October 2014 Ó International Union for the Study of Social Insects (IUSSI) 2014

Abstract The aim of our study was to characterize the decreased with elevation. A signiﬁcant nested pattern was factors that shape the pattern of change in ant species observed, indicating that the species found in the poorest richness and community structure along altitudinal gradi- site represented a subset of those found at the richest one. ents in two valleys located on the northern and southern side Ants collected at mid- and high-elevation sites had a wider of the Pyrenees. During three summers, we sampled 20 sites altitudinal range than those collected at low-elevation sites, distributed across two Pyrenean valleys ranging in elevation thus complying with Rapoport’s rule. Our results suggest from 1,009 to 2,339 m using pitfall traps and hand collec- that, although elevation strongly inﬂuences the organization tion. We employed diversity index, degree of nestedness of of ant communities, ecological factors such as temperature ant assemblages, ordination method, and multiple regres- and local habitat features (sun exposure, vegetation density) sion analysis to examine the effects of various environ- are the main factors explaining the pattern of ant diversity mental factors on ant species communities. In total, 41 ant along altitudinal gradients. species were found in the two valleys. The number of species was 26 % lower in the valley located on the northern Keywords Ants Á Community ecology Á side than in that located on the southern side. At the valley Elevation gradient Á Andorra Á France Á Pyrenees scale, the number of ant species, as well as the evenness,

Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00040-014-0374-2) contains supplementary material, which is available to authorized users. Mountains cover approximately one-quarter of the land surface of the Earth (Ko¨rner, 2007;Ko¨rner et al., 2011) and & A. Bernadou ( ) Á A. Le Goff Á V. Fourcassie´ represent 11.4 % of the protected areas of the Earth surface Universite´ de Toulouse, UPS Centre de Recherches sur la Cognition Animale, 118 Route de Narbonne, 31062 Toulouse (Kollmair et al., 2005). They have generally a high rate of Cedex 9, France endemism and species diversity (Kollmair et al., 2005) and e-mail: [email protected] this probably explains why many biodiversity hotspots are located, at least in part, in highland or mountainous areas A. Bernadou Á A. Le Goff Á V. Fourcassie´ CNRS Centre de Recherches sur la Cognition Animale, 118 (Myers et al., 2000). Mountainous areas with their altitu- Route de Narbonne, 31062 Toulouse Cedex 9, France dinal gradients are characterized by rapid changes in climate, soil, or vegetation over relatively short distances. X. Espadaler They are therefore the ideal place for exploring the eco- Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Facultat de Cie`ncies, Universitat Auto`noma de logical mechanisms underlying spatial patterns in species Barcelona, E-08193 Bellaterra, Spain richness (Ko¨rner, 2007). A widespread pattern observed in both plants and ani- Present Address: mals in mountainous areas is a linear and monotonic decline A. Bernadou Evolution, Behaviour and Genetics-Biology I, University of of species richness with elevation (Rahbek, 2005). Other Regensburg, Universita¨tsstraße 31, 93053 Regensburg, Germany studies suggest, however, that a second pattern, with a peak 123 A. Bernadou et al. of species richness at mid elevation, may also be common (Bernard, 1946; Ovazza, 1950; Soulie´, 1962; Espadaler, (Rahbek, 2005 for a review). Both of these patterns are 1979; Sommer and Cagniant, 1988a, b; but see Arnan et al., found in insects (Olson, 1994; Sanders et al., 2010). How- 2009; Bernadou et al., 2013b for more recent studies). ever, the mechanisms and factors responsible for these The aim of our study was to characterize the pattern of patterns still remain poorly understood (Rahbek, 2005; change in ant diversity along altitudinal gradients in the Dunn et al., 2009b). The variation in species richness with Pyrenees and to relate this change to environmental and altitudinal gradients is indeed not easily interpreted as ecological factors. We sampled 20 sites distributed across several factors (e.g., sunlight, temperature, barometric two Pyrenean valleys characterized by contrasted climatic pressure, rainfall, available area) are known to co-vary with conditions: one valley is located in Andorra, on the southern elevation (Ko¨rner, 2007; Sundqvist et al., 2013), which side of the Pyrenees, while the other is located in France, on makes their respective roles difficult to decipher. For the northern side. Our study addresses three interrelated example, climatic factors such as temperature and precipi- questions: (1) Does ant diversity vary between the two tation have been shown to be consistently correlated with valleys and with elevation? (2) Does elevation affect the species richness in several studies (Kaspari et al., 2000; distribution of ant species and the composition of their Sanders et al., 2003, 2007; Dunn et al., 2009a). In general, communities? and (3) Do climatic and/or landscape vari- warmer and more productive sites support more species than ables influence the pattern of species richness along cooler or less productive sites. However, other factors such altitudinal gradients? as spatial heterogeneity or habitat complexity have also been highlighted as relevant for explaining the structure of species assemblages. For example, the distribution of ants Materials and methods and their functional groups can be significantly affected by land-cover variables (Bernadou et al., 2013a), the spatial Study area and study sites heterogeneity generated by fire (Parr and Andersen, 2008) or habitat fragmentation (Vasconcelos et al., 2006). All The Pyrenees extend over the border between France and these factors can interact with each other to drive spatial Spain, along an east–west direction from the Mediterranean variation and shape species richness. Sea to the Atlantic Ocean over a length of approximately Ants are one of the most represented groups of animals in 430 km and a width of 100–140 km. The two sides of the most terrestrial ecosystems (Ho¨lldobler and Wilson, 1990). range present important climatic contrasts. While the Most of the studies on ant assemblage patterns along ele- northern side has an oceanic climate, with rainfall through- vational gradients published in the literature during the last out the year, mild winters and cool summers, the southern two decades have focused on tropical regions (e.g., Peters side, in contrast, has a more continental climate, with very et al., 2014) or on temperate regions of North America (e.g., cold winters and dry summers, high solar radiation and large Sanders et al., 2003, 2007). Studying new biogeographic variations in temperature (Go´mez et al., 2003). regions and thus working with ant assemblages from dif- Two valleys were sampled in this study: the Madriu- ferent species pools, functional or phylogenetic groups and Perafita-Claror, in the Principality of Andorra, and the Pique influenced by different evolutionary histories may help to valley, in France (Fig. 1—distance between the valleys is highlight the mechanisms that could have shaped ant bio- about 80 km). The Madriu-Perafita-Claror valley is a glacial diversity along elevational gradients, and also to investigate valley located in the southeast part of Andorra which has whether these mechanisms are the same across continents. been registered in 2004 as World Heritage for its cultural A case in point is the mountainous areas of Europe which landscape by UNESCO because of the persistence of pas- hitherto have been poorly investigated, in particular the toralism and a strong mountain culture dating back to the Pyrenees. These mountains have always been of great 13th century (http://www.unesco.org, see Madriu-Perafita- interest for naturalists because they are characterized by a Claror valley). It covers an area of 4,247 ha, which repre- relatively high rate of endemism of both animal (Martinez sents nearly 10 % of the territory of the Principality of Rica and Recoder, 1990; for arthropods: Deharveng, 1996; Andorra. The valley is oriented along an east–west axis and Brown et al., 2009) and plant species (Villar and Denda- extends along an altitudinal gradient ranging from 1,055 to letche, 1994; Villar et al., 1997). The Pyrenees present 2,905 m. The Pique valley is a glacial valley, predominantly particular interests for myrmecologists because they are oriented along a north–south axis, extending along an alti- located at the boundary of two climatic zones, the temperate tudinal gradient ranging from 650 to 3,116 m and covering one and the Mediterranean one, in which ants have not yet an area of 8,251 ha. It is part of the Natura 2000 sites (http:// been adequately sampled (Jenkins et al., 2011). Indeed, www.natura2000.fr/-FR7300881). most papers on the Pyrenean ant fauna have been published We sampled ants at 20 sites (9 sites in the Madriu valley before the 80s and consist primarily of lists of species and 11 sites in the Pique valley) in July–August 2005 to 123 Ant community organization

Fig. 1 Map showing a the location of the Pyrenees in Europe and b the location of the two valleys in France (Pique valley) and Andorra (Madriu valley) in which ants were sampled

2007 along an altitudinal gradient ranging from 1,300 to immediately and were left in place for 5–8 days (Supple- 2,300 m, and from 1,000 to 2,300 m, for the Madriu and mentary material Appendix A). The pitfalls could not be the Pique valley, respectively. Sampling could not be operated on the same year for both valleys or for the same achieved at lower elevations, because of high anthropo- length of time because adverse meteorological condition genic pressure below 1,300 m in the Madriu valley, and made the access to some of the transects too difficult. below 1,000 m in the Pique valley. Locations higher than However, this did not bias our data because there was no 2,300 m were not sampled because it is known that the ant correlation between the duration of pitfall activity and the species richness beyond this elevation is very low (Glaser, proportion of observed versus estimated species richness 2006). Whenever possible, for the different elevations (Spearman’s rank correlation, r = 0.13, P = 0.58, see sampled, at least one site on the southern slope and one site Appendix A and Table 1). Pitfall trapping was supple- on the northern slope were chosen for the Madriu valley, mented by hand collecting around each sampling point. and one site on the eastern slope and one site on the Hand collecting consisted of one person (the same western slope for the Pique valley. Appendix A of the throughout the whole sampling period—A.B.) picking up supplementary material gives the main characteristics of all visible ants on the ground and in the vegetation within a the sampling sites (GPS coordinates, dominant vegetation, 2 m radius around each pitfall during three minutes. All ants environmental variables and habitat characterization) in collected were placed in plastic vials filled with 90° ethanol the two valleys. and, once in the laboratory, were identified to the species level by two of the co-authors of the paper (A.B. and X.E.) Sampling methods and species identification using available keys (Collingwood, 1979; Seifert, 2007).

At each of the 20 sites, we used a variation of the ALL Environmental variables and habitat characterization protocol (Agosti et al., 2000) to sample the ants. A 200 m long line transect was traced and sampling points were For each sampling point within a transect, we evaluated the placed on this line every 10 m (yielding a total of 20 sam- presence of a canopy as 0 (absence—no canopy above the pling points per site). Two collection methods were used to sampling point, no trees around the pitfall), 1 (sparse—the sample the ants at each sampling point (Bernadou et al., sampling point is covered by a canopy with many gaps, one 2013a): pitfall traps (diameter 35 mm, height 70 mm) and to three trees surround the pitfall) or 2 (dense—the sampling hand collection. The pitfall traps were set in action point is covered by a close canopy, several trees are present

123 A. Bernadou et al.

Table 1 Ant species richness (S), number of species occurrences, Simpson’s index of diversity (1-D) and species richness estimators (ICE = Incidence-based coverage estimator, Chao2, Jack2 = 2nd order jackknife) for the different transects of the two Pyrenean valleys sampled Valleys Alt. (m) S Occurrences 1-D ICE Chao2 ± SD Jack2 Mean ± SD %

Madriu valley 38 479 0.94 41.13 39.42 ± 1.93 42.02 40.86 ± 1.32 93.00 1351 25 106 0.93 31.75 27.85 ± 3.05 32.83 30.81 ± 2.61 81.14 1471 16 91 0.90 16.77 16.48 ± 1.24 18.85 17.37 ± 1.29 92.11 1612 12 84 0.85 14.63 12.95 ± 1.74 15.84 14.47 ± 1.45 82.93 1941 7 36 0.76 7.48 7.00 ± 0.24 8.00 7.49 ± 0.50 93.45 2036 13 43 0.81 27.11 19.65 ± 6.79 24.24 23.67 ± 3.76 54.92 2067 5 34 0.73 5.00 5.00 ± 0.07 5.00 5.00 ± 0.00 100.0 2280 7 43 0.79 7.40 7.00 ± 0.44 8.85 7.75 ± 0.97 90.32 2280 7 28 0.74 9.17 7.32 ± 0.89 8.99 8.49 ± 1.02 82.44 2339 2 14 0.13 2.00 2.00 ± 0.34 3.85 2.61 ± 1.06 76.62 Pique valley 28 356 0.92 29.62 28.60 ± 1.18 30.01 29.41 ± 0.72 95.20 1009 14 47 0.89 17.08 15.43 ± 2.14 18.84 17.12 ± 1.70 81.77 1044 5 12 0.66 10.17 7.85 ± 4.18 10.55 9.52 ± 1.46 52.52 1124 9 18 0.82 14.28 10.14 ± 1.77 12.99 12.47 ± 2.11 72.17 1422 10 30 0.88 10.76 10.48 ± 1.24 12.85 11.36 ± 1.29 88.02 1426 13 40 0.88 17.49 17.75 ± 5.76 21.40 18.88 ± 2.18 68.85 1544 6 20 0.79 6.41 6.00 ± 0.24 7.00 6.47 ± 0.50 92.73 1641 5 21 0.67 5.89 5.00 ± 0.16 5.14 5.34 ± 0.47 93.63 1922 10 66 0.85 10.54 10.00 ± 0.16 10.14 10.23 ± 0.28 97.75 1997 4 32 0.62 4.00 4.00 ± 0.04 3.15 3.71 ± 0.49 100.0 2283 6 38 0.67 7.46 6.95 ± 2.12 9.70 8.03 ± 1.46 74.65 2299 4 32 0.58 4.77 4.00 ± 0.41 5.85 4.87 ± 0.92 82.08 The means (±SD) correspond to the means of the three species richness estimators with their standard deviation. The percentage indicates the percentage of ant species collected (compared to the maximum number of species predicted by the 3 species richness estimators) in the different transects around the pitfall). We then calculated for each transect a collected at a sampling site by a pitfall trap and/or hand mean canopy index. For each transect, we noted the mean collection. Consequently, the theoretical maximum species elevation and general exposure of all sampling points. occurrence in a transect is 20. Moreover, since alate indi- Exposure was divided into two categories: ‘‘favorable’’ viduals in ants may travel considerable distances during (mostly southern exposure) or ‘‘unfavorable’’ (mostly nuptial ﬂight, all quantitative results in this paper are based northern exposure) (Supplementary material, Appendix A). on the worker caste. We used two climatic variables in our analysis, namely annual mean temperature (°C) and annual precipitation Sampling effort and species richness (mm). These two climatic variables were selected because they have been shown to consistently correlate with ant To estimate the total sampling effort for the two valleys and species richness (Sanders et al., 2007; Dunn et al., 2009a). for each transect within each valley, individual-based rare- They were obtained from 2 GIS data layers (30-arc seconds) faction curves were used (Gotelli and Colwell, 2001). These from the WorldClim 1.4 database (Hijmans et al., 2005) curves allow to compare species richness for equivalent (Supplementary material, Appendix A). levels of sampling effort. Rarefaction curves were calculated using Coleman’s method (100 replicates) in the Data analysis program EstimateS 7.5.2 (Colwell, 2005). To estimate total ant species richness at the valley and transect levels and to Because ants are social insects, a single sample may contain evaluate the completeness of our samples, three richness a high abundance of a rare species. Our analyzes are estimators were calculated: incidence-based coverage esti- therefore based on the species occurrence in the samples mator (ICE), Chao2 and Jacknife2 (the latter two non- rather than on the number of individuals. A sampling point parametric estimators were calculated with 100 thus corresponds to the presence/absence of various species permutations).

123 Ant community organization

Community structure: diversity and evenness BINMATNEST with the recommended default parameters and based our p values on 1,000 simulated matrices. Because species richness does not encompass all the char- A Spearman’s rank correlation test was used to evaluate the acteristics of a species assemblage (e.g., evenness), we influence of the altitudinal range of the species on the degree chose to calculate Simpson’s index (D) which can also be of nestedness of the assemblages. We considered the species expressed as 1-D (Magurran, 2004). To test the correlation order of the maximally nested matrix obtained by BIN- between this index and elevation for each valley, we used MATNEST and their respective altitudinal range and the modified t test developed by Dutilleul (1993) to control compared it to the same altitudinal range values classified in for potential effects of spatial autocorrelation (package: a decreasing order. A significant correlation coefficient SpatialPack; Osorio and Vallejos, 2014). Studies in Finland would suggest a possible influence of elevation on the for- (Savolainen et al., 1989) have indicated that the structure of mation of the nested structure and that the most common ant communities can be largely determined by the territorial species are those that are distributed along the largest alti- species of the wood ant group (in this study: Formica rufa, tudinal range. As for the NODF metric, it was run for each F. lugubris and F. pratensis). Since species of this group valley with two different null models (ER and CE; Gui- were present at our study sites, we used the modified t test maraes and Guimaraes, 2006; Almeida-Neto et al., 2008) and (Dutilleul, 1993) to calculate the correlation between the we based our p values on the maximum number of null model abundance of the species belonging to the wood ant group replicates (1,000) allowed by the software ANINHADO (expressed as the total number of sample points where the (Guimaraes and Guimaraes, 2006; Almeida-Neto et al., species were present) and the total number of species or 2008). their abundance recorded for each transect. To assess visually the differences in ant species composition between the different transects of the two valleys, we Species spatial distribution and community composition used a non-metric multidimensional scaling (NMDS) (package: VEGAN (Oksanen et al., 2005), R 2.11.0 soft- We estimated the altitudinal range of each species as the ware, http://www.r-project.org). NMDS was run for difference between the maximum and minimum elevations k (= number of dimensions) ranging from one to six at which the species was found. The mean altitudinal location dimensions and the optimal number of dimensions was of a species was calculated by weighting the elevations at found by examining a scree plot of stress vs. k dimensions. which the species was found by its occurrence at these dif- Stress values lower than 20 indicate that the ordination is a ferent elevations. If the presence of a species was not good representation of the original distance matrix values. recorded at a particular transect but was noted at the transect NMDS was computed with the Bray–Curtis distance index immediately above and below, it was assumed that this on the matrix of species presence/absence. A cluster ana- species was nonetheless present and its occurrence was noted lysis on the sampling site dissimilarity matrix (computed as 1 (Bru¨hl et al., 1999). Species occurrence within the dif- with the Bray–Curtis distance index) was achieved to dis- ferent genera was also represented for the two valleys tinguish groups of similar transects. The function Simprof according to the elevation of the transects. To characterize (package: clustsig; Whitaker and Christman, 2014) was then community composition, we calculated the level of nested- used to assess the number of significant clusters obtained ness of the two valleys: a significant nested pattern indicates with the cluster analysis. Cluster analysis and Simprof were that the species found in the poorest site represents a subset of computed using Ward’s clustering method. those found at the richest one (Patterson, 1987). To assess the level of nestedness of the community, we first calculated the Patterns and correlates of diversity along altitudinal matrix Temperature metric (T) with the binary matrix nest- gradients edness temperature calculator BINMATNEST (Rodrı´guez- Girone´s and Santamarıá, 2006). The nestedness temperature We used Generalized Linear Models with a Poisson error (T) varies from 0 for a perfectly nested matrix to 100 for a structure to examine the relationship between environmental random species distribution pattern. Since this metric is variables and species richness. In a preliminary exploration known to inflate somewhat the Type I error with increasing of our data set, we found a strong and significant correlation matrix size, we also calculated a second metric based on between two environmental variables: namely annual mean overlap and decreasing fill, the NODF metric, with the temperature and annual precipitation (Spearman’s rank software ANINHADO 3.0 (Guimaraes and Guimaraes, correlation, r =-0.98, P \ 0.001). To minimize collinearity 2006; Almeida-Neto et al., 2008). The NODF metric is problems, we therefore excluded annual precipitation from indeed more robust against matrix shape and matrix size than our models and tested only temperature and mean canopy the Temperature metric calculated by BINMATNEST index (numeric variables), and exposure (categorical vari- (Almeida-Neto et al., 2008; Ulrich et al., 2009). We ran able) as independent environmental variables. Since tempe- 123 A. Bernadou et al. rature decreased with elevation in the same way as mean were found at the 400 sampling points in the two valleys. canopy index, we centered these two variables on their These species belong to 8 ant genera that were all shared mean to reduce collinearity. We did not test elevation as between the two valleys. The two valleys have 25 species in independent variable because ants do not respond to eleva- common; 13 species were found in the Madriu valley only tion per se; elevation is only a surrogate for a variety of and 3 species in the Pique valley only. factors that shape diversity gradients (Ko¨rner, 2007). In addition, annual mean temperature and elevation were Sampling effort and species richness strongly and significantly correlated in our dataset (Spear- man’s rank correlation, r =-0.96, P \ 0.001). Five Individual-based rarefaction curves were approximately different models that use different combinations of inde- asymptotic for the two valleys (Fig. 2a), in particular for the pendent and interaction variables were tested (Table 2). The Pique valley, indicating that our sampling effort was cor- first model tests if species richness changes with temperature rect. The nonparametric richness estimators indicated that and the valley sampled. Because both valleys present between 90 % (Jack2 = 42.02 species) and 97 % important climatic contrasts, the interaction between the (mean ± SD: Chao2 = 39.42 ± 1.93 species) of the factors, valley and temperature, was included in the model. expected maximum number of species were collected in the The second model is identical to the first one except that it Madriu valley, and between 93 % (Jack2 = 30.01 species) takes into account the fact that species richness can peak at and 97 % (Chao2 = 28.60 ± 1.18 species) in the Pique intermediate elevations (see Sanders et al., 2003). The third valley (Table 1). When the curves of the two valleys are model tests if species richness is influenced only by habitat rarefied to the lower number of individuals collected (i.e., factors (i.e., canopy index and exposure) and valley. The 356 occurrences, corresponding to the Pique valley), the fourth model is a combination of models 1 and 3, and the fifth highest species richness was recorded in the Madriu valley model is a combination of models 2 and 3. We used multiple (Fig. 2a). model inference to evaluate the quality of the models The number of species collected at each transect varied (Burnham and Anderson, 2002). Because of our reduced between 25 at 1,351 m and 2 at 2,339 m, and between 14 at sample size, we used AICc instead of AIC. The set of ‘‘best’’ 1,009 m and 4 at 1,997 and 2,299 m, for the Madriu and models amongst all candidate models was based on both Pique valley, respectively (Table 1). Although for most DAICc, i.e., the difference between the AICc of each model transects, the number of species given by the rarefaction and that of the best fitting model (i.e., that with the lowest curves and the estimators converged well (Fig. 2b, c; AICc) and on AICc weights (Burnham and Anderson, 2002; Table 1), which suggests sampling completeness, the con- Burnham et al., 2011). vergence and the asymptotic phase of the rarefaction curves was less clear for some of the transects—in particular for the transects located at low elevations (1,044, 1,124 and Results 1,426 m in the Pique valley) and for those located at high elevations (2,036 and 2,339 m for the Madriu valley and In total, 41 species corresponding to 835 occurrences (see 2,283 m for the Pique valley). Whereas for these six tran- Table 1 and Appendix B of Supplementary material for the sects, on average less than 67 % (minimum: 52.52 %, results obtained with the two different sampling methods) maximum: 76.62 %; Table 1) of the expected number of

Table 2 Results of generalized linear models used to examine the relationships between ant species richness with temperature (T °C), exposure (EFavorable/Unfavorable) and mean canopy index (MCI) in the two Pyrenean valleys (VMadriu/Pique) in which ants were sampled Model description K AICc DAICc AICc weight

Species richness

1. T °C ? VM/P ? T °C 9 VM/P 4 109.474 0.000 0.8234

4. T °C ? EF/U ? MCI ? VM/P ? T °C 9 VM/P 6 112.973 3.499 0.1432 2 2 2. (T °C) ? T °C ? VM/P ? (T °C) 9 VM/P ? T °C 9 VM/P 6 115.967 6.493 0.0320 2 2 5. (T °C) ? T °C ? EF/U ? MCI ? VM/P ? (T °C) 9 VM/P ? T °C 9 VM/P 8 122.346 12.872 0.0013

3. EF/U ? MCI ? VM/P 4 130.501 21.027 0.0000 Five different candidate models using different combinations of independent variables and interactions were tested (for further details, see data analysis). These models were fitted with a Poisson distribution. For each model, the number of parameters of the model (K), the Akaike information criterion corrected for small sample sizes (AICc), DAICc, the difference between the AICc of the model of interest and the AICc of the best fitting model and the AICc weight which quantifies the plausibility of a model compared to the other ones, are given. Candidate models were arranged in ascending order of DAICc

123 Ant community organization

Fig. 2 Individual-based 40 rarefaction curves for the two (a) valleys in which ants were 30 sampled (a) and for each transect Madriu valley in the Madriu (b) and Pique Pique valley (c) valleys (Pyrenees). These 20 curves were used to compare ant species richness between the two valleys and among the different 10 sampling sites within each valley. They were calculated 0 using Coleman’s method in the program Estimate S 7.5.2. The 0 100 200 300 400 500 gray curves in (a) represent the 1351m standard deviation of the mean 25 1471m of 100 replicates; for the sake of (b) 1612m 1941m clarity, they were not 20 2036m represented in (b) and (c) 2067m 15 2280m 2280m 2339m 10

5 Number of species 0

0 20 40 60 80 100 120 20 1009m (c) 1044m 1124m 15 1422m 1426m 1544m 10 1641m 1922m 1997m 5 2283m 2299m 0 0 20 40 60 80 Occurrences species were collected, on average more than 89 % (mini- abundance of the species of the wood ant group (in this mum: 81.14 %, maximum: 100.00 %; Table 1) of the study: Formica rufa, F. lugubris and F. pratensis) for the species were collected for the 14 other transects. Madriu valley (species richness: r =-0.45, P = 0.08; abundance: r =-0.50, P \ 0.01, n = 9), but not for the Community structure: diversity and evenness Pique valley (species richness: r = 0.34, P = 0.28; abundance: r = 0.42, P = 0.19, n = 11). The species of the The value of the Simpson’s index varied with elevation from wood ant group were any way not very abundant in the 0.93 at 1351 m to 0.13 at 2339 m and from 0.89 at 1009 m to Pique valley (abundance was lower than 5 in 91 % of the 0.58 at 2299 m, for the Madriu and Pique valleys, respec- sampling sites). tively (Table 1). The correlation coefﬁcients between elevation and the values of Simpson’s index for both the Species spatial distribution and community composition Madriu and the Pique valleys were negative and non significant, although there was a strong tendency for the Pique The minimum–maximum elevations and mean altitudinal valley (Table 1, r =-0.63, P = 0.136, n = 9 and r = range of each species are indicated in Fig. 3a. Species -0.57, P = 0.07, n = 11, for the Madriu and the Pique val- gradually replace each other along the altitudinal gradient. leys, respectively). The low values of Simpson’s index Only a few species occurred at high elevation, the same for recorded at the most elevated sites can be explained by both a the two valleys (Myrmica sulcinodis, M. lobulicornis, lower number of species and a lower evenness of these species. Formica lemani and Temnothorax tuberum). At the genus The variation in ant species richness and abundance level, the abundance of species per genera in the two valleys among transects tended to be related to the variation in the differed with elevation (Fig. 3b). Tapinoma and Lasius

123 A. Bernadou et al.

(a) Madriu valley Pique valley

Mymica sulcinodis Temnothorax tuberum Formica lemani Myrmica lobulicornis Formica lugubris Formica pressilabris Tetramorium impurum Formica rufa Formica frontalis Formica decipiens Camponotus herculeanus Mymica sulcinodis Leptothorax acervorum Formica lemani Myrmica wesmaeli Myrmica lobulicornis Myrmica sabuleti Temnothorax tuberum Formica fusca Leptothorax acervorum Formica foreli Formica pressilabris Formica rufibarbis Tetramorium impurum Lasius grandis Formica lugubris Formica sanguinea Formica sanguinea Lasius flavus Leptothorax muscorum Myrmica schencki Myrmica ruginodis Lasius alienus Myrmica scabrinodis Myrmica scabrinodis Lasius mixtus Myrmica specioides Myrmica schencki Formica pratensis Lasius niger Tapinoma erraticum Lasius flavus Temnothorax unifasciatus Lasius platythorax Camponotus ligniperdus Myrmica rubra Myrmica ruginodis Formica rufa Temnothorax parvulus Formica cunicularia Temnothorax nylanderi Formica fusca Temnothorax nadigi Myrmica sabuleti Temnothorax affinis Lasius brunneus Myrmica rubra Temnothorax nadigi Leptothorax muscorum Tapinoma erraticum Lasius platythorax Lasius paralienus Lasius paralienus Formica pratensis Lasius brunneus Camponotus ligniperdus 1000 1250 1500 1750 2000 2250 2500 1000 1250 1500 1750 2000 2250 2500 Elevation (m) Elevation (m)

(b) Madriu valley Pique valley

2299 m Formica Tetramorium 2283 m Myrmica 2339 m Camponotus 1997 m Temnothorax 2280 m Leptothorax 1922 m Tapinoma 2280 m Lasius 1641 m 2067 m 1544 m

2036 m 1426 m

1941 m 1422 m

1612 m 1124 m

1471 m 1044 m

1351 m 1009 m

0 5 10 15 20 25 0 5 10 15 20 25 Species number Species number

Fig. 3 a Minimum–maximum elevations (black and gray lines) and was calculated by weighting the elevation at which the species was mean altitudinal location (black and gray circles) for all ant species found by its abundance in the different transects. b Altitudinal collected in the Madriu and Pique valleys. Ant species are ordered by distribution of ant genera among the different sampling sites of the their mean altitudinal range. The mean altitudinal range of a species Madriu and the Pique valleys

123 Ant community organization

NMDS1 -1.0 -0.5 0.0 0.5 1.0

P-1044

P-1641

P-1544 P-1124 M-2067 P-2299 P-1922

P-1422 M-2280 P-1426 P-2283 M-2280 P-1009 M-1941 P-1997 NMDS2 M-1351

M-1471 M-2036 M-2339

M-1612 -1.0 -0.5 0.0 0.5 1.0 Fig. 5 Relationship between species richness and temperature for the Madriu (solid circle) and Pique (solid triangle) valleys. This ﬁgure corresponds to model 1, which includes temperature, valleys and the interaction between temperature and valleys (see Table 2). Dotted lines indicate standard errors

a Spearman’s rank correlation test indicated that for the two valleys, the values of altitudinal range of each species arranged in the order obtained by BINMATNEST were significantly and positively correlated with the values of Information remaining (%) altitudinal range of each species arranged in decreasing 0.0 1.0 2.0 3.0 order (Madriu valley: r = 0.77, P \ 0.001 and Pique val- P-2283 P-1997 P-2299 P-1124 P-1422 P-1009 P-1426 P-1044 P-1641 P-1544 P-1922 M-1351 M-2280 M-1612 M-2280 M-1471 M-2036 M-2067 M-2339 M-1941 ley: r = 0.69, P \ 0.001). The nested structure of ant assemblages was thus underpinned by the altitudinal range Fig. 4 NMDS (upper graph) and cluster analysis (lower graph) of the 20 transects of the two valleys sampled in the Pyrenees. The first letter of the species: the species that have a large altitudinal range of the point label indicates the valley in which the transect was located are present at most sampling sites. (M for Madriu, P for Pique) and the four digits that follow the elevation The NMDS (stress = 13.07) revealed an altitudinal and of the transect. NMDS was computed with the Bray–Curtis distance environmental gradient in community composition. Sites index on the matrix of species presence/absence. Sites were grouped according to elevation (NMDS 1) and canopy openness (NMDS 2). A were grouped according to elevation (NMDS 1) and canopy cluster analysis was subsequently achieved to distinguish groups of openness (NMDS 2) (Fig. 4). The cluster analysis allows to similar transects. This analysis discriminates three groups of transects: distinguish two main groups of transects (Fig. 4 and Sup- those at low and high elevations and those at intermediate elevations plementary material Appendix C): the first corresponds to the transects at high elevation (approximately above genera were found mainly at low-elevation sites (Pique 1,900–2,000 m) and the second to the transects at low ele- valley), while genera such as Formica and Myrmica were vations. A third cluster gathering the remaining transects distributed along the whole altitudinal gradient (Fig. 3b). located at intermediate elevations can also be distinguished. The ant assemblages were significantly nested for the The difference in ant species composition between these Madriu valley (T = 12.07, P \ 0.001; NODF(Er) = 14.98, three clusters is significant (Simprof, P \ 0.05). P(Er) \ 0.001 and NODF(Ce) = 17.33, P(Ce) = 0.02). The results for the Pique valley were not as clear as for Patterns and correlates of diversity along altitudinal the Madriu valley since they depended on the metric used gradients to calculate matrix nestedness (T = 24.03, P = 0.02; NODF(Er) = 15.06, P(Er) = 0.25 and NODF(Ce) = 16.22, The ranking of the five candidate models based on DAICc is P(Ce) = 0.36). At least in the Madriu valley, therefore one presented in Table 2. Model 1 which includes temperature, can say that the species found at the poorest transects rep- valley and the interaction term between temperature and resent a subset of those found at the richest ones. Moreover, valley, received substantial support to explain the variation

123 A. Bernadou et al. in species richness (see Table 2 and Appendix D of Sup- Sanders et al., 2003 ca 900–2225 m). Finally, the selected plementary material, Fig. 5). Model 4, which includes not models show a significant interaction between valley and only temperature and valley but also slope exposure and temperature: the number of species was higher in the mean canopy index can also be considered as plausible. Madriu than in the Pique valley at low and middle elevation, Taken together, these two models have an AICc weight of but then converges towards the same value in both valleys 96 % (Table 2). Model 1 is approximately 5.7 times more for higher elevation. This may be explained by the fact that likely to be the best approximating model than model 4 at high elevation the environmental features are more (Table 2). The models with only habitat factors (model 3) or homogenous between the two valleys than at low elevations. with squared temperature and habitat factors (model 5) had Therefore, there are less local variations in temperature and low support (AIC weight\0.01, Table 2). the effect of temperature on species richness may be expressed in the same way in the two valleys. At least two explanations can be proposed to explain the Discussion decrease we observed in ant species richness with increasing elevation. The first is related to the ‘‘abundance–extinction’’ Our results show that ant species richness was lower on the mechanism proposed by Kaspari et al. (2000) and Sanders northern side (Pique valley) than on the southern side et al. (2007, 2010). Temperature determines in part the (Madriu valley) of the Pyrenees and decreased along the actual evapotranspiration of a site (AET, Sanders et al., altitudinal gradient. This suggests that the pattern of ant 2010), which can be considered as an indirect measure of species richness between the two valleys and between the net primary productivity (Kaspari et al., 2000). Conse- transects within each valley was driven mainly by temper- quently, sites with higher temperature are able to support ature: warmer sites harbor more species than cooler ones. larger population sizes, thus reducing the probability of a Despite the overriding effect of temperature in both valleys, species to become locally extinct. In our study, warmer species richness was driven at a smaller scale by local sites, at low elevations, had indeed higher species richness habitat features, i.e., the absence/presence of canopy above than colder sites, at high elevations. Ant species richness is the sampling sites and the slope exposure. The decrease in also likely to correlate positively with temperature and ant species richness along altitudinal gradients was primary productivity at the level of a mountain range in the accompanied by a species turnover in the communities so same way as it does at the level of a continent (Kaspari et al., that the composition of ant communities of high elevation 2000; Dunn et al., 2009a, Kumschick et al., 2009). This may differs from that of low elevation. Although a species explain the discrepancy in species richness that we observed turnover exists, a significant nested pattern was observed, in our study between the Madriu and Pique valleys. In fact, indicating that the species found in the poorest transect one may expect a difference in species richness and com- represent a subset of those found at the richest one. position from the warmer Mediterranean (Sommer and The number of ant species collected in the two valleys Cagniant, 1988a, b) to the cooler Atlantic climate when (41 species) represents more than 19 % of the total number moving westwards in the Pyrenees. of species found in France (213 species, see Casevitz- A second explanation that could account for the decline Weulersse and Galkowski, 2009) and around 13.5 % of that in species richness with elevation is linked to the direct recorded in the Iberian Peninsula (300 species; Espadaler, effect of temperature on the activity of ants (Retana and pers. comm.). The model selection procedure indicated that Cerda, 2000). In fact, the second best model that explained ant species richness decreased with annual mean tempera- the variation in species richness retained not only temper- ture. This result has already been reported for mountain ature and valley but also the terms related to the habitat ranges located on other continents (e.g., Lessard et al., 2007; characteristics: species richness decreased with increasing Sanders et al., 2007, 2010). The selected models show in values of canopy index. Sites with dense canopy cover are addition that the number of species differed significantly expected to be cooler than sites exposed to direct sunlight between the two valleys: it was 26 % lower in the Pique (Lassau and Hochuli, 2004; Lassau et al., 2005). Since ants than in the Madriu valley. This occurred in spite of the fact are thermophilic animals, a reduction in ground temperature that the sampling points were distributed over a larger could reduce their foraging activity and consequently altitudinal range in the Pique than in the Madriu valley. In increases the probability for ant colonies to disappear. It both valleys, however, we failed to find a peak of species would be worth exploring how temperature along eleva- richness at mid elevation. This could be due to the reduced tional gradient in the two valleys we studied interacts with range of elevations at which we sampled. Most of the access to food resources, allows (or not) the coexistence of studies in which a peak in species richness at mid elevation dominant and subordinate species and, ultimately, contri- was shown are indeed based on samples collected across a bute to shaping ant communities (Cerda et al., 1998a, b; wider altitudinal range (Sanders, 2002 ca 150–4400 m; Retana and Cerda, 2000). 123 Ant community organization

It should be noted as a caveat that the use of the restricted altitudinal range. This is consistent with Rapo- Wordclim database only allows a crude approximation of port’s rule applied to elevational gradients (Stevens, 1992). the mean annual temperature at the transect scale. The This rule states that species living at higher elevations must temperatures experienced by ants at a local scale are prob- be able to tolerate more variability in environmental con- ably somewhat different. More accurate measures of ditions, and as a consequence, must have relatively larger temperature could have been provided by the use of tem- elevational ranges. perature loggers placed at different locations along the The nested pattern we observed is important for con- transects (see for example: Fridley, 2009). servation management because it could help to target the At the genus level, the composition of ant communities sites to preserve in priority. However, this calls for a word varied along elevational gradients (Fig. 3b). According to of caution. In fact, although ant assemblages in this study Machac et al. (2011), species found at low elevations tend to (and others) are significantly nested, this does not mean that be evenly dispersed across phylogeny, while those at high they are perfectly nested, i.e., that the richest transects elevations tend to be phylogenetically clustered. The most harbor all the species present in the poorest transects common genera found at high elevations by these authors (Fischer and Lindenmayer, 2005). In fact, ant assemblages were Formica, Myrmica and Temnothorax, the same as in in mountainous areas are imperfectly nested because of a this study. This suggests that the pattern they observed could species turnover between high and low elevations; sites be consistent across temperate regions, which indeed seems with a few species are thus as important to conserve as sites to be confirmed by the study of Lessard et al. (2011). As with many species (Fischer and Lindenmayer, 2005). This suggested by Machac et al. (2011), some of the species distinction is important in conservation biology when it found at high elevation (e.g., Formica lemani and Myrmica comes to the question of preserving all the sites or just the sulcinodis) could possess behavioral or physiological traits richest sites. that facilitate or enhance cold resistance. To conclude, our results suggest that the organization of Our results support the idea that the structure of ant ant communities in the Pyrenees change with elevation and communities could be determined by the presence of terri- that ecological factors such as temperature and local habitat torial species of the wood ant group in the Madriu valley. features (sun exposure, vegetation density) are the main Such a relationship has been reported for the Pyrenees by factors explaining the pattern of ant diversity along altitu- Arnan et al. (2009) who found that areas with a high dinal gradients. These results concord with those of other abundance of F. lugubris were characterized by a low ant studies recently achieved in mountain ranges located in the species diversity. Surprisingly, however, this was not the USA (e.g., Lessard et al., 2007; Sanders et al., 2007), sug- case in the Pique valley and this was probably due to the low gesting that the mechanisms shaping ant biodiversity along occurrence of the species of the Formica (s.str.) group in the altitudinal gradients are common across continents (e.g., sites sampled in this valley. Our results also show that ant Janzen et al., 1976). species gradually replace each other along altitudinal gradients (Fig. 3a). The cluster analysis performed on the Acknowledgments We thank M. Leponce, J.-P. Lessard, L. Legal dissimilarity matrix clearly distinguished two main groups and P.S. Oliveira for constructive comments on previous versions of this paper. A.B. was financed by a doctoral grant from the Fundacio´ of ant assemblages, one at high and another at low elevation, Cre`dit Andorra and by a grant ‘‘Germaine Cousin’’ from the French with a boundary between the two groups around Entomological Society. Part of this work was supported by the pro- 1,900–2,000 m. A third but smaller group can be distin- gram ‘‘Entomological Inventory of the Madriu-Perafita-Claror Valley’’ guished at intermediate elevations. According to Sanders funded by the Department of Agriculture of the Principality of Andorra. et al. (2003), such a break around 2,000 m could correspond to a change in the dominant vegetation. Because of their nesting or feeding habits (e.g., Formica species), vegetation might provide indirectly important resources to the ants and References could thus partly drive their distribution. A significant nested pattern was found for the Madriu Agosti D., Majer J.D., Alonso L.E. and Schultz T.R. 2000. ANTS - valley, indicating that species composition at the poorest Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian Institution Press, Washington and London transects represents a subset of those found at the richest Almeida-Neto M., Guimaraes P., Guimaraes P.R., Loyola R.D. and ones. Nestedness seems to be a common pattern in ants Ulrich W. 2008. A consistent metric for nestedness analysis in (Vasconcelos et al., 2006; Lessard et al., 2007). In our study, ecological systems: reconciling concept and measurement. Oikos it was underpinned by the altitudinal range of the species: 117: 1227–1239 Arnan X., Gracia M., Comas L. and Retana J. 2009. Forest manage- ants collected at mid and high elevations have a wide alti- ment conditioning ground ant community structure and compo- tudinal range and are present at most sampling sites, sition in temperate conifer forests in the Pyrenees Mountains. whereas those collected at low elevations have a more Forest Ecol. Manag. 258: 51–59 123 A. Bernadou et al.

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