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Oecologia (2013) 172:667–677 DOI 10.1007/s00442-012-2541-3 PHYSIOLOGICAL ECOLOGY - ORIGINAL RESEARCH Traits underpinning desiccation resistance explain distribution patterns of terrestrial isopods André T. C. Dias • Eveline J. Krab • Janine Mariën • Martin Zimmer • Johannes H. C. Cornelissen • Jacintha Ellers David A. Wardle • Matty P. Berg • Received: 19 July 2012 / Accepted: 19 November 2012 / Published online: 7 December 2012 Ó Springer-Verlag Berlin Heidelberg 2012 Abstract Predicted changes in soil water availability regimes with climate and land-use change will impact the community of functionally important soil organisms, such as macro-detritivores. Identifying and quantifying the functional traits that underlie interspecific differences in desiccation resistance will enhance our ability to predict both macro-detritivore community responses to changing water regimes and the consequences of the associated species shifts for organic matter turnover. Using path analysis, we tested (1) how interspecific differences in desiccation resistance among 22 northwestern European terrestrial isopod species could be explained by three underlying traits measured under standard laboratory conditions, namely, body ventral surface area, water loss rate and fatal water loss; (2) whether these relationships were robust to contrasting experimental conditions and to the Communicated by Matthias Schaefer. Electronic supplementary material The online version of this article (doi:10.1007/s00442-012-2541-3) contains supplementary material, which is available to authorized users. A. T. C. Dias (&) E. J. Krab J. Mariën J. H. C. Cornelissen J. Ellers M. P. Berg Department of Ecological Science, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands e-mail: [email protected]; [email protected] M. Zimmer FB Organismische Biologie: Ökologie, Biodiversität & Evolution der Tiere, Paris-Lodron-Universität, Hellbrunner Str. 34, 5020 Salzburg, Austria D. A. Wardle Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden phylogenetic relatedness effects being excluded; (3) whether desiccation resistance and hypothesized underlying traits could explain species distribution patterns in relation to site water availability. Water loss rate and (secondarily) fatal water loss together explained 90 % of the interspecific variation in desiccation resistance. Our path model indicated that body surface area affects desiccation resistance only indirectly via changes in water loss rate. Our results also show that soil moisture determines isopod species distributions by filtering them according to traits underpinning desiccation resistance. These findings reveal that it is possible to use functional traits measured under standard conditions to predict soil biota responses to water availability in the field over broad spatial scales. Taken together, our results demonstrate an increasing need to generate mechanistic models to predict the effect of global changes on functionally important organisms. Keywords Detritivores Drought Functional traits Isopoda Soil moisture Water loss rate Introduction Climate and land-use change can greatly alter the structure and functioning of soil communities (Emmerling 1995; Bardgett and Wardle 2010; Moron-Rios et al. 2010; Blankinship et al. 2011). Soil detritivores are especially sensitive to changes in soil water availability, which can promote significant shifts in their abundance, vertical stratification, species richness and composition (Maraldo and Holmstrup 2010; Moron-Rios et al. 2010; Blankinship et al. 2011; Makkonen et al. 2011) and in turn alter essential soil processes (Briones et al. 2009). It is therefore expected that intensification of changes in precipitation patterns resulting 123 668 from climate change and artificial regulation of groundwater resources due to land-use change will strongly influence the abundance, community composition and functioning of these organisms. Macro-detritivores, such as isopods, millipedes and earthworms, are important regulators of the turnover of dead plant material (Lavelle 1997), with significant consequences for soil fertility, primary productivity and carbon turnover (Wardle 2002). Whether or not soil invertebrate communities will decline in abundance due to global changes (Barrett et al. 2008; David and Handa 2010; Blankinship et al. 2011) or how their functional composition will change has important implications for determining the overall impact of global changes on soil processes. The huge diversity of macro-detritivores (Schmalfuss 2003; Sierwald and Bond 2007) poses a challenge to ecologists with respect to synthesizing and applying current knowledge on species autecology to predict how changes in soil hydrological regimes influence their community structure. It has been proposed that ecological generality will improve with a shift from a nomenclatural approach focusing on species number and identity to a more functional approach focusing on species’ functional traits (McGill et al. 2006). Quantification of the variation in functional traits directly links organism performance to environmental conditions (Violle et al. 2007) and facilitates recognition of generalities in species responses to spatial or temporal variation therein (McGill et al. 2006). The functional approach has been mainly developed by plant ecologists, and some recent studies have successfully used functional traits to explain how animals respond to disturbance (Moretti et al. 2009; Langlands et al. 2011). However, the importance of functional traits for predicting responses of detritivore communities to changes in either macro- or micro-climate has not yet been studied. Climate change is expected to increase the frequency and intensity of both drought periods and extreme precipitation events (IPCC 2008), subjecting detritivore communities to a greater temporal variability of soil water availability. This variability is expected to have a strong impact on soil communities as both drought and flooding are considered to be important stress factors for detritivores (Plum 2005; David and Handa 2010). Here, we focus on resistance to desiccation, which varies greatly among macro-detritivore species (Haacker 1968; White and Zar 1968). Desiccation resistance measured under standard laboratory conditions has been suggested to be a useful trait for predicting detritivore responses to decreases in water availability, since it can explain abundance patterns in dry habitats (David and Handa 2010) and microhabitat preferences (Edney 1951; White and Zar 1968). However, progress in using this trait from published studies has been hampered by the lack of comparative studies and standard protocols for measuring desiccation resistance, as well as by a poor understanding of the 123 Oecologia (2013) 172:667–677 mechanisms that underpin interspecific variation. Identifying and quantifying the functional traits that underlie interspecific differences in desiccation resistance will enable more general inferences about the response of detritivore species to changes in water availability. In the study reported here, we used terrestrial isopods as a model system to investigate whether desiccation resistance and the traits underpinning this resistance can explain species distribution patterns along moisture gradients. Terrestrial isopods are important members of detritivore communities, with more than 3,500 species distributed worldwide (Schmalfuss 2003). Over evolutionary time, the colonization of contrasting terrestrial habitats in which soil water regimes range from semi-aquatic to desert conditions has led to considerable variation among isopod species in desiccation resistance (Warburg 1993; Schmalfuss 2003). However, little is known about which traits are strong candidates as causal drivers of desiccation resistance. Data are currently available for only a few species (Warburg 1993), and there have been even fewer explicit species comparisons (Edney 1951; White and Zar 1968). A study by Tsai et al. (1998) on two Ligia species demonstrated that intraspecific variation in desiccation resistance for the two species was explained primarily by water loss rate, which in turn is determined by body size (Fig. 1a). Fatal water loss (i.e. maximum water loss tolerance) also explained part of the variation in desiccation resistance but was independent of body size. In our study we asked whether these traits also explain interspecific differences in desiccation resistance. We specifically tested the following hypotheses: (1) interspecific variation in desiccation resistance is explained by underlying traits such as body surface area, water loss rate and fatal water loss (as shown in the path model in Fig. 1a), (2) the results of this model do not change qualitatively when measurements are made at contrasting water availabilities or when phylogenetic relatedness effects are excluded and (3) desiccation resistance and the traits underlying this resistance can explain species distribution over soil moisture gradients. To test these hypotheses, we measured desiccation resistance and hypothesized underlying traits for 22 dominant northwestern European terrestrial isopod species belonging to nine different families. We then used our trait measurements to explain species distribution patterns in relation to site moisture level using a previously published database. Materials and methods Species collection and traits measurements Adult individuals of 22 terrestrial isopod species (suborder Oniscidea) from nine families naturally occurring in the Oecologia (2013) 172:667–677 669 (a) A WL R F (b) A -0.89** WL -0.93** 2 R R2=0.80 X = 1.13; P = 0.77 GFI = 0.97 R2=0.90 AGFI = 0.91 0.15* F (c) 2 -0.53** A WL -0.67** R2=0.28 R R2=0.57 X = 1.29; P = 0.73 GFI = 0.97 AGFI = 0.89 0.36* F Fig. 1 Path diagrams showing: a hypothesized causal relationships between traits explaining interspecific variability in desiccation resistance in terrestrial isopods (based on Tsai et al. 1998), b fitted model with species trait attributes and c with phylogenetically independent contrasts. A Surface area, WL water loss rate, F fatal water loss, R desiccation resistance. Trait attributes were logtransformed to improve normality and linearity. Path coefficients, goodness-of-fit index (GFI) and adjusted goodness-of-fit index (AGFI) are shown for each model (*P \ 0.05, **P \ 0.01). Direct effect of surface area on desiccation resistance was not significant whether species trait attributes or phylogenetically independent contrasts were used. See ESM 6 for alternative models including the direct effect of surface area Netherlands, comprising 71 % of the 30 indigenous Dutch species (Berg et al. 2008), were collected. The collected individuals were kept in plastic pots containing moist plaster of Paris and litter from the site of origin. Animals were stored in a climate room maintained at 15 °C, 75 % air relative humidity (RH) and 12:12 light:dark ratio for at least 1 week and a maximum of 6 weeks before starting the measurements, allowing them to acclimate to the experimental conditions. Because different species were collected during five field trips to distinct locations from March to September 2010 [see Electronic Supplementary Material (ESM) 1], we used site controls to evaluate the degree to which the variation in trait values was due to betweenspecies differences versus within-species differences among sites. For this purpose, we collected the most abundant species, Porcellio scaber, in each site as a site control. We also collected P. scaber from the garden of the Hortus Botanicus at VU University in Amsterdam (52:33°N, 4:86°E) on every field collecting day to serve as a time control. We are aware that using only one species as a control could influence conclusions about trait variability across sites and time because this partly depends on which species we select, but P. scaber was the only species that occurred at sufficient densities in all sites visited. To standardize the initial conditions before measuring desiccation resistance, individuals from each species were kept isolated in small cylinders (diameter 2 cm, height 3 cm) with moist plaster of Paris in the bottom and no food for 3 days. These individual cylinders were placed in a closed glass box (20 9 30 9 25 cm) on top of a of 10-cm layer of moist sand that covered a water-saturated plaster of Paris element, ensuring constant humid conditions close to 100 % RH. This procedure allowed the animals to replenish any possible water deficit, so measurements started when they had approximately the maximal possible body water content. During this period, animals also evacuated most of their gut content which prevented defecation during the measurements and therefore changes in mass not related to water loss. This starvation period did not affect the survival of the isopods. For the more abundant species, two or three individuals were kept in the glass box (approximately 100 % RH) after the starvation period; none of these animals died before the end of the desiccation resistance measurements. Isopods were exposed to relatively dry but realistic conditions, i.e. 85 % RH, to record their water loss rate, fatal water loss and survival time. This humidity level was chosen to represent a moderate stress condition, just below the threshold above which isopods are able to absorb water vapour (91–93 % RH; Wright and Machin 1990). The humidity level was acquired using a glycerol–water solution with a specific gravity of 1.11 or 42 % volume (White and Zar 1968). Falcon tubes (50 ml) were filled with 20 ml of glycerol solution. In each tube, a platform made of plastic mesh (width 2 mm) was placed about 1 cm above the solution surface; the chamber containing the animal to be measured was then placed on this platform. The bottom of the plastic open-top chambers was made of mesh (width 0.5 mm), allowing airflow between the animal and the glycerol–water solution. Before we started the measurements, the chambers were acclimatized inside the Falcon tubes with the glycerol–water solution overnight to ensure no changes of mass during the experiment due to the adherence of water on the chamber walls. We measured 6–13 individuals per species depending on the number of animals collected in the field. At the start of each measurement, we placed a single individual in the open-top chamber to record their initial fresh mass (to the nearest 1 lg; model Supermicro; Sartorius AG, Göttingen, Germany) and immediately returned the chamber with the animal to the Falcon tube. This procedure allowed us to record changes in the isopod’s mass with minimal 123 670 disturbance. We re-weighed the isopods at regular intervals, the length of which varied from 15 min to 3 h depending on the species. Before weighing the isopods, we checked if they were alive. Using tweezers, we gently flipped the isopods onto their back. Individuals that were unable to flip back to the normal position and did not present leg and antenna movements were considered to be dead. All animals were followed until they died. Dead isopods were weighed and immediately frozen at -20 °C for further analyses. A schematic overview of the experimental setup can be found in the ESM 2. The average survival time (hours) was used as an estimate of desiccation resistance (i.e. the capacity of an organism to withstand dry conditions). Water loss rate was calculated by the slope of the linear regression between water mass and time and was expressed as the proportion of initial water content that was lost per hour. The relationship between water mass and time was linear for all species with R2 varying from 0.75 to 0.99. Fatal water loss was expressed as the proportion of the initial water content that was lost at the time of death (see ESM 3 for details on the calculation of traits). For individuals that died overnight, we used the median of the values of the last measurement in the afternoon and the first in the morning to calculate the above-mentioned traits. To measure body size, we removed isopods from the freezer and left them to thaw for 5 min, after which we took pictures of their ventral surface using a stereomicroscope (Leica model Wild M8; Leica Microsystems, Wetzlar, Germany) equipped with a digital camera (Leica model DC 200). We measured the length and width (to the nearest 0.1 mm) of each individual using the software Axio Vision 4.8 and calculated the ventral surface area using the formula of the ellipse area. We are aware that this measurement does not encompass the total surface area where transpiration occurs, but it does cover the largest part of the transpiring surface (Warburg 1993). Moreover, as the morphology of isopods is relatively similar among species, this measurement should be a good surrogate of the ‘‘real’’ surface area. The high power of this variable on explaining water loss rate (see ‘‘Results’’) confirms that. We then oven-dried the isopods at 60 °C until constant mass and recorded the dry mass. Additionally, to test if our results were consistent under different experimental conditions, we compared water loss rate values measured at 85 and 36 % RH. The measurements at more extreme drought conditions, 36 % RH, 15 °C and 12:12 light:dark ratio had been performed in 2005 for 24 species comprising 20 species in common with the sampling in 2010. Most of the species had been collected from the same sites in 2005 as in 2010 (ESM 1). The measurements under 36 % RH had followed the same protocol as described above, except that we carried out the 123 Oecologia (2013) 172:667–677 measurements only until the animals lost about 30 % of the initial water content. This resulted in much faster experiments (\1 day). Species distribution We searched the literature for data on the distribution of terrestrial isopod species that fulfilled two sampling criteria: (1) sampling should not be biased toward a given group of species (e.g. by using pitfalls), and (2) sampling should provide information on water availability for the species records. We found only one data set with such characteristics comprising species in common with our own data set. Vilisics et al. (2007) compiled information on 126 site records describing isopod communities in nine major geographic regions across Hungary. Field sampling was carried out by direct search (20–40 min per site) where species presences were recorded. Sampling sites were classified into three moisture levels—dry, moist and wet. Sites were assigned to these categories according to the authors’ expert knowledge of the local environmental conditions. We are aware that this is only an approximate categorization of water availability. However, we believe that the classification of the sites into three levels of water availability should provide sufficient resolution to test whether this environmental factor can filter species according to their trait values. Future studies, with more detailed measurements of water availability, could improve this approach through providing a more complete description of the relationship between water availability and traits underlying desiccation resistance. Statistical analyses One-way analysis of variance (ANOVA) was used to test for interspecific differences in surface area, water loss rate, fatal water loss and desiccation resistance. Box–Cox transformation was performed using the car package in R 2.12 to improve data normality and homogeneity of variances. Because the control populations of P. scaber and other pilot experiments did not show any difference between males and females for the traits that we considered, sex was not considered as a factor in the statistical analyses. We used path analysis to test the hypothesis about the causal relationships between species traits. We hypothesized that desiccation resistance is determined by water loss rate and fatal water loss and that water loss rate is determined by surface area (Fig. 1a). We also tested an alternative model that included a direct effect of surface area on desiccation resistance (i.e. due to mechanisms not specified in the model). Maximum likelihood was used to estimate path coefficients in R 2.0.1 and the SEM package. Oecologia (2013) 172:667–677 The chi-square statistic (v2) was used to test if the observed covariance matrix differed from that predicted by the model. A significant difference between matrices indicates a low probability that the observed data was generated by the hypothesized causal model and the model should therefore be rejected. We used the goodness-of-fit index (GFI) and adjusted goodness-of-fit index (AGFI) to evaluate the fit between observed covariance matrix and that predicted by the models. We considered values of [0.9 to be a very good fit and values of C0.8 to be a good fit. To test whether relationships between traits were consistent when phylogenetic effects were excluded from the analysis, we constructed a phylogenetic tree based on 18S rRNA and used phylogenetically independent contrasts (Felsenstein 1985) to re-run the same models as described above. The final phylogeny, the details on the molecular work and on how the tree was constructed can be found in ESM 4. We first tested for the phylogenetic signal of the traits by comparing the variance of the standardized contrasts (VarCont) in the phylogeny with the variance of contrasts generated by a randomization test (i.e. trait values swapped across the tips of the tree; Blomberg and Garland 2002; Webb et al. 2008). We then calculated phylogenetically independent contrasts (PIC) for the four studied traits and reran the path models. Since our phylogeny was not completely resolved we followed the approach described by Pagel (1992) to deal with polytomies. The phylogenetic signal and PIC were calculated using the software Phylocom (Webb et al. 2008). Weighted least square regressions were used to investigate the relationship between the data on traits derived from our measurements and the species distribution data across the three moisture levels derived from Vilisics et al. (2007). Within each of the moisture levels we calculated the relative frequency of each species present, i.e. the number of occurrences of a given species divided by the total number of occurrences for all species within that moisture level. This represents how frequently each species (and its respective trait values) is observed within each level. We used this relative frequency to weigh the regression between trait values and moisture level. To evaluate which part of the gradient had filtered the trait values, we also used correlation analysis to test for relationships between trait values and the frequency of species across the moisture levels, where frequency at each moisture level was calculated as the number of occurrences of a given species at that level divided by its total number of occurrences at all three levels. This provides a relative measure of how often a given species is found at each moisture level. Using species as replicates, we then determined the Pearson correlation coefficient between species trait values and species relative frequency for each of the moisture classes. Correlation was tested by re-sampling techniques. 671 Results Ventral surface area, water loss rate, desiccation resistance and fatal water loss differed significantly among species (ANOVA, F21,200 = 295, P \ 0.001; F21,200 = 226, P \ 0.001; F21,200 = 151, P \ 0.001; F21,200 = 2.88, P \ 0.001, respectively; Fig. 2). The first three abovementioned traits showed great variation among species, while fatal water loss showed a much lower variation with values of around 0.47 ± 0.05 [mean ± standard deviation (SD), proportion] of the initial water content. The controls also showed significant differences among samples in surface area and water loss rate, but not in desiccation resistance or fatal water loss (ANOVA, F8,76 = 19.9, P \ 0.001; F8,67 = 2.28, P = 0.03; F8,67 = 1.31, P = 0.26; F8,67 = 0.16, P = 0.99, respectively; see ESM 5). Although significant, differences among controls in surface area and water loss rate showed much lower magnitude than the differences between species. These two traits showed a variation of one order of magnitude among species (Fig. 2), while among control populations, surface area varied only from 11.0 to 38.6 mm2 and water loss rate varied from 0.007 to 0.012 mg mg-1 h-1. These results indicate that the interspecific variation in these isopods is substantially greater than intraspecific variability. Our path model showed a strong fit between observed data and model predictions (Fig. 1b), corroborating the hypothesis that interspecific variation in desiccation resistance is explained by water loss rate and fatal water loss, with water loss rate as the main driver of desiccation resistance. The accepted model explained 90 and 80 % of the variation in desiccation resistance and water loss rate, respectively. The direct effect of surface area on desiccation resistance was not statistically significant (P = 0.80; see ESM 6 for alternative model), indicating that surface area affects desiccation resistance only indirectly, via changes in water loss rate. The structure of the model indicates that it is possible to use water loss rate and, indirectly, surface area as surrogates for desiccation resistance in isopods. All of the studied traits showed a significant phylogenetic signal (surface area: VarCont = 2.675, P = 0.002; water loss rate: VarCont = 0.006, P \ 0.001; desiccation resistance: VarCont = 3.002, P = 0.001; fatal water loss: VarCont = 0.009, P = 0.007). However, the path model using PIC for traits also showed a strong fit between the observed data and model predictions (Fig. 1c), indicating that the hypothesized relationships between traits are not only caused by a shared evolutionary history. However, the model using traits’ PICs explained a lower percentage of the variation of desiccation resistance and water loss rate: 57 and 28 %, respectively. Again, the direct effect of surface area on desiccation resistance was not statistically 123 Oecologia (2013) 172:667–677 Water loss rate (mg mg hr-1) Water loss rate (mg mg-1 hr-1) Surface area (m mm2) 672 Relative humidity (%) a oceanica Ligia Oniscus asellus adillidium vulgare Arma Porccellio spinicornis Porccellio scaber helipus rathkii Trach adillidium opacum Arma ma caelatum Elum adillidium pictum Arma oscia muscorum Philo dium hypnorum Ligid cellium conspersum Porc adillidium pulchellum Arma adillidium album Arma Andrroniscus dentiger yarthrus hoffmannseggi Platy honiscus pusillus Trich Hapllophthalmus danicus oniscus patiencei Mikto honiscoides sarsi Trich honiscoides albidus Trich atrichoniscoides leydigii Meta Fatal water loss (proportion) Desiccation resiistance (hr) Fig. 3 Reaction norm of water loss rate measured at 36 and 85 % RH (both at 15 °C) for 20 isopod species. Lines link the average values of water loss rate for the same species measured at different relative humidities Fig. 2 Trait attributes [mean ± standard deviation (SD, bars)] for 22 terrestrial isopod species. The four traits analysed are: ventral surface area, water loss rate as the proportion of initial water content lost per hour, desiccation resistance at 85 % relative humidity (RH) and fatal water loss as the proportion of initial water content that was lost at the time of death. Species are sorted by surface area 123 significant (P = 0.54; see ESM 6 for an alternative model). More details on the results of the phylogenetic analyses can be found in ESM 4. All species showed increased water loss rate at 36 % RH when compared to measurements made at 85 % RH (values are given in ESM 1) with few changes in the rank order of species (i.e. few lines crossing in Fig. 3). This is also indicated by a high correlation between the two measurements (rSpearman = 0.94; n = 20; P \ 0.001). The relationship between desiccation resistance and both water loss rate and surface area were best described by a power function (Fig. 4). The very good fit of the equation for water loss rate indicates that this is a better surrogate of desiccation resistance than surface area. The residuals of the equation for surface area were not similar along the observed range of surface area values. Residuals are particularly high for species larger than 10 mm2. This increase in residuals can be a consequence of the way surface area was measured because the error of the measurement is likely to increase with the square root of the length and width measurements. Our data set had 11 species in common with Vilisics et al. (2007) for the measurements made under 36 % RH and eight for the measurements under 85 % RH; we therefore present the results using traits measured under 36 % RH. Site moisture level showed a positive Fig. 4 Power functions describing the relationship of desiccation resistance to water loss rate (F1,21 = 2,207, P \ 0.001) and body surface area (F1,21 = 68.8, P \ 0.001) among 22 terrestrial isopod species, with each point representing the average value for a single species 673 Desiccation resistance (hr) Oecologia (2013) 172:667–677 y = 0.415 x -1.043 2 R = 0.99 y = 1.629 x 0.997 2 R = 0.75 Surface area Water loss rate (mm2) (mg mg-1 hr-1) Discussion This is the first study to comprehensively reveal the functional traits underlying macro-detritivore responses to in situ soil water availability by showing relationships between standardized measurements of morpho-physiological traits and species distribution patterns across a soil moisture gradient. We revealed that differences in body water loss rate serves as the main mechanism behind interspecific variation in isopod desiccation resistance. Our findings contribute to the increasing need to generate empirically tested, mechanistic predictions on the effect of global changes, especially impacts of extreme weather events, on functionally important organisms such as detritivores. Functional traits underpinning desiccation resistance The physiological ability of an organism to show resistance to unfavourable conditions can be determined by physiological avoidance and tolerance strategies. In our study, Log10(1 + water loss rate) 0.15 Log10(1 + surface area) relationship with water loss rate (F1,24 = 6.8, P = 0.015, R2 = 0.19) and a negative relationship with body surface area (F1,24 = 5.0, P = 0.035, R2 = 0.14) but only when weighting for relative frequency within moisture levels was performed (Fig. 5, solid lines). Moreover, species water loss rate was negatively correlated with frequency on dry sites (r = -0.52, P = 0.039) and positively with frequency on wet sites (r = 0.83, P = 0.002). While species body surface area was negatively correlated with frequency in wet sites (r = -0.67, P = 0.021), frequency in moist sites did not show a significant correlation with any of the traits. The traits measured at 85 % RH showed the same patterns described above, although relationships were not significant (ESM 7), possibly due to the lower number of species with available data. a b 0.10 0.05 1.5 1.0 0.5 b a Dry Moist Wet Fig. 5 Relationship between site moisture level and two isopod traits, i.e. water loss rate and body surface area. The Y-axis value for each point represents the average trait value for a single species. The area of the symbols is proportional to the relative frequency of the species at a given moisture level (i.e. number of occurrences of the species at a moisture level divided by the total number of occurrences at this level). Relationships between traits and moisture levels were significant when weighting traits by the relative frequency of species (solid lines), but not when simple regression was used (dashed lines). Letters indicate two species that are specifically mentioned in the ‘‘Discussion’’: a Haplophthalmus mengii, b H. danicus water loss rate (avoidance) and fatal water loss (tolerance) explained 90 % of the interspecific variation in desiccation resistance, with water loss rate being the main factor explaining such variation. The low interspecific variation in fatal water loss found here is a common pattern in 123 674 Oecologia (2013) 172:667–677 arthropods in general, for example, 40–54 % for ants (Hood and Tschinkel 1990) and 42–52 % for weevils (Chown 1993). This low interspecific variation also corroborates the notion that morpho-physiological avoidance strategies (i.e. adaptations that influence water loss rate) are the main mechanism determining desiccation resistance among terrestrial arthropods (Villani et al. 1999). However, physiological tolerance might play an important role in determining differences in desiccation resistance between soil invertebrate taxa. Earthworms, for example, can show much higher values for fatal water loss (70–75 %; Roots 1956). Therefore, future studies should quantify the relative importance of water loss rate and fatal water loss in determining differences in desiccation resistance among contrasting detritivore taxa. Body size affected desiccation resistance only indirectly—through changes in the water loss rate. The surface area to volume ratio, which varies allometrically with body size, has been suggested as an important factor influencing soil arthropod water balances (Villani et al. 1999). The cuticle of isopods is more permeable than that of most terrestrial arthropods, and transpiration across the integument, especially across the ventral surface, is a major source of water loss for isopods even at relatively high humidity (Warburg 1989, 1993). We observed that the water loss rate was highly constant over time for all species at both values of RH, both before and after the animals died (ESM 3). This observations suggests that water loss is a passive process in terrestrial isopods and that a larger body size could therefore contribute significantly to reduce water loss rate simply by reducing the surface area to volume ratio. Although body size explained 80 % of the variation in water loss rate, other morphological adaptations are also important to reduce water loss rate. For instance, Ligidium hypnorum and Androniscus dentiger, two species without pleopodal lungs, have much higher water loss rates and, consequently, lower desiccation resistance than species with pleopodal lungs and similar body size (such as Armadillidium album and A. pulchellum; Fig. 2). The evolution of pleopodal lungs was an important step in the colonization of terrestrial habitats (Schmidt and Wägele 2001) because the pleopods are the main site of water loss (Warburg 1993). As different adaptations can affect water loss rate, a considerable amount of variation in this trait cannot be explained by body size alone. Consequently, the use of body size as an indirect surrogate to desiccation resistance can lead to erroneous conclusions, especially when species of similar size are compared. negligible compared to the interspecific variability, leading to consistent and meaningful species ranking. However, this assumption has rarely been tested (Albert et al. 2010; Hulshof and Swenson 2010). Although our site control populations of P. scaber showed significant differences in surface area and water loss rate, the magnitude of this intraspecific variability was much lower than that of the interspecific variation. Also, the tight correspondence of species ranking based on measurements of water loss rate made in 2005 and in 2010 indicates that species ranking was robust when different populations were sampled. However, intraspecific variability should not be neglected. We were able to explain differences between species using the same traits as those used by Tsai et al. (1998) to explain intraspecific variability for two Ligia species. This result suggests that water loss rate can be used as a surrogate for desiccation resistance at the individual level, irrespective of the species under study. The variability between individuals of the same species is essential to the process of natural selection, and whether soil invertebrates are able to adapt to climate and land-use change remains largely untested. The few studies investigating the presence of adaptive variation in desiccation resistance for soil invertebrates provide results that are both positive (Holmstrup and Loeschcke 2003; Bahrndorff et al. 2006) and negative (Maraldo et al. 2008; Maraldo et al. 2009). More detailed studies on the intraspecific variability of desiccation resistance could reveal its potential importance to the adaptation of detritivores to environmental changes. Trait variation among versus within species Our results show that species traits measured under standardized laboratory conditions can be used to predict desiccation resistance at different experimental or natural conditions. The fact that traits measured in individuals When working with species average trait values, it is generally assumed that the intraspecific variability is 123 Phylogenetic signal We showed that desiccation resistance has a strong phylogenetic signal that reflects the evolutionary history of colonization of terrestrial habitats, with ancestral species showing lower desiccation resistance and derived species a higher resistance. All other functional traits that we measured also showed strong phylogenetic signals. However, the acceptance of the path model using phylogenetically independent contrasts indicates that the relationships between the traits could not be explained by phylogeny alone, suggesting that these relationships do not only reflect ancient divergences (as revealed through a strong phylogenetic signal) but have evolved repeatedly in the course of phylogenetic history as a result of convergent evolution. Applying the functional approach to macro-detritivore communities Oecologia (2013) 172:667–677 collected in The Netherlands could explain the distribution pattern of species in Hungary indicates that this approach can be applied to broad spatial scales. Animal ecologists have applied habitat preferences as surrogates for traits to explain species distributions (e.g. Purse et al. 2012). However, this approach has been challenged as species interactions can lead to a mismatch between species occurrences and their physiological optima (Ellers et al. 2010). We argue that the use of morpho-physiological traits, as we adopted here, is a better approach as it provides a direct, mechanistic link between organism performance and environmental conditions. Still, a part of the variation of species distribution could not be explained by traits underpinning desiccation resistance, possibly due to two main reasons. First, the data set is based on species presence and absence only. Environmental filters can have a stronger impact on the relative abundance than on species presence because even under unfavourable conditions species may persist with low abundances. Second, other factors, which may or may not be related to soil water availability, can affect species distributions. These limitations can be exemplified by Haplophthalmus mengii, the species showing lower surface area and higher water loss rate in Fig. 5. This species was found at a low frequency at the three moisture levels, but it is expected to have higher abundances on wet sites through being hygrophilous (Berg et al. 2008; Gregory 2009). In this case, adding data on relative abundance of species could improve the explanatory power of the studied traits. Additionally, this species inhabits clayish soils with high water holding capacity (Berg et al. 2008; Gregory 2009), which can buffer variations in water availability. In contrast, the congeneric species H. danicus typically inhabits soils with a high organic matter content that are moist but well drained (Berg et al. 2008; Gregory 2009), and it was only present in sites classified as moist and wet (Fig. 5). Determining how soil type preference is related to water availability or other requirements (i.e. nutrients, shelter) will be an important step towards a better understanding of detritivore species distribution. Another potential problem with using pure physiological traits to explain animal responses to environmental conditions is that changes in behaviour can obscure relationships between traits and the environment. For example, isopods with high water loss rates and small body size are able to move deeper into the soil through small cracks, thereby minimizing the risk of exposure to dry conditions. However, when changes in water availability regimes are strong enough to reduce the availability of suitable refuges, our results indicate that macro-detritivore communities differ considerably in terms of desiccation resistance. Recently, functional traits have been successfully used to explain community structure and species responses to 675 environmental change for different animal groups (Moretti et al. 2009; Schamp et al. 2010; Langlands et al. 2011; Makkonen et al. 2011; Wiescher et al. 2012). However, there is still no consensus on what the most important traits are and what is the best way to measure them. Standardization of trait measurements is a pressing issue for the full implementation of a functional trait approach. For example, the standardization of measurements of plant functional traits (Cornelissen et al. 2003) has enabled analyses of trait relationships on broad spatial scales (Diaz et al. 2004; Wright et al. 2004). Nowadays, trait values are available in several plant databases, including a huge global database (Kattge et al. 2011). However, animal ecologists have not yet reached a similar agreement on standard protocols for trait measurements. For soil fauna, the experimental conditions that we used (85 % RH, 15 °C) represent a moderate stress condition in the temperate region of Europe (David and Vannier 2001; Holmstrup and Loeschcke 2003; Kaersgaard et al. 2004). We suggest that this experimental set could be applied to a vast number of groups of soil organisms, including similar-sized animals, such as millipedes, as well as very small animals, such as springtails and mites. Ecological implications and extensions of this study The differences in desiccation resistance between terrestrial isopod species have important ecological implications. The negative relationship between site moisture level and body size suggests that a reduction in soil water availability will probably filter out—or at least reduce the relative abundance of—small species. It is still not clear if and how the variation in desiccation resistance and body size is related to the effects of isopods on soil processes. The mass ratio hypothesis (Grime 1998) states that the effect of a given species on ecosystem processes is proportional to its relative abundance in the community and has received increasing empirical support (Diaz et al. 2007; Quested et al. 2007; Mokany et al. 2008), although exceptions have also been reported (Wardle et al. 2008; Peltzer et al. 2009). Therefore, changes in community functional composition due to species filtering can potentially have strong impacts on ecosystem processes. If desiccation resistance is correlated with the effects of isopod species on soil processes, the directional changes in desiccation resistance of the isopod community due to environmental filtering is expected to have consequences for ecosystem processes (Suding et al. 2008; Webb et al. 2010). Nonetheless, the loss of species with particular trait attributes will decrease functional diversity with possible detrimental effects on ecosystem functions (Heemsbergen et al. 2004). Here, we identified traits related to the response of isopods to decrease in soil water availability. Future studies 123 676 should investigate whether our findings for isopods are consistent with those of other detritivore groups and whether water loss rate can be used to predict species desiccation resistance more generally across detritivore groups. 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