TY - JOUR
AU - Knapp,, Michal
AB - Abstract Geographic variation in body size has fascinated biologists since the 19th century as it can provide insight into the evolution of the body size of various organisms. In this study, we investigated body size variation in eight carabid species/subspecies (Coleoptera: Carabidae) along elevational gradients in six Central European mountain ranges. First, we examined elevational variation in body size and whether female and male body sizes differed in their responses to elevation. Second, we examined intrapopulation variation in body size along an elevational gradient, and we compared the degrees of intrapopulation variation between males and females. The investigated species either followed a converse Bergmann’s cline (Carabus auronitens auronitens Fabricius 1792; Carabus linnei Panzer 1810; Pterostichus melanarius (Illiger, 1798); Pterostichus pilosus (Host, 1789)) or their size was unaffected by elevation (Carabus auronitens escheri Palliardi, 1825; Carabus sylvestris sylvestris Panzer, 1796; Carabus sylvestris transsylvanicus Dejean, 1826; Pterostichus burmeisteri Heer, 1838). Females were the larger sex in all the investigated species, but the degree of sexual size dimorphism differed between species. In general, the degree of sexual size dimorphism showed no change with elevation. The degree of intrapopulation variation in body size slightly increased with elevation in C. sylvestris sylvestris and P. pilosus. Overall, the intrapopulation variation in body size significantly differed among the investigated carabid species. The existing literature on intrapopulation variation in the body size of insects is limited, but further investigation of this issue could provide a better understanding of the mechanisms that generate geographical clines. converse Bergmann’s rule, altitudinal gradient, geographical cline, intrapopulation variation, sexual size dimorphism Body size is a crucial characteristic of all living organisms because of its close relationship with other life-history traits (Chown and Gaston 2010, Yom-Tov and Geffen 2011). Larger individuals often exhibit increased survival under unfavorable conditions, such as water and food limitation, and they are better able to cope with adverse temperatures when overwintering (Blanckenhorn et al. 2007, Kingsolver and Huey 2008, Kovacs and Goodisman 2010, Teder et al. 2010). Many studies have shown a strong positive relationship between body size and fecundity in females (Honěk 1993, Marshall et al. 2013, Pincheira-Donoso and Hunt 2015) as well as between body size and mating success in males (Savalli and Fox 1998, Romero-Alcaraz and Ávila 2000, Arriaga-Osnaya et al. 2017). However, the advantages of larger body size are sometimes outweighed by the disadvantages, so insects do not always grow to their maximum possible size (Blanckenhorn 2000). For example, the longer development time needed to attain a larger body size is linked to higher predation risk during preimaginal development (Nylin and Gotthard 1998). Moreover, suboptimal environmental conditions can limit the benefits resulting from a large body size (Gotthard et al. 2007, Teuschl et al. 2007). Thus, selection pressure on body size can differ under various biotic and abiotic conditions, so spatial variation in body size is expected. The best-known pattern of geographical variation in body size is Bergmann’s rule (Bergmann 1847), which posits that endothermic species from high latitudes are larger than related species from lower latitudes, and a lower surface to volume ratio in larger animals was proposed as the underlying mechanism. Increasing body size with increasing latitude or elevation should also be observed at the species level, i.e., when populations are investigated along a geographical gradient (Blackburn et al. 1999). Bergmann’s rule has also been investigated in ectotherms, but in this case, the term ‘Bergmann’s cline’ is more precise (Ray 1960, Blanckenhorn and Demont 2004, Shelomi 2012) as different mechanisms generate geographical variation in body size in ectotherms compared to endotherms. Blanckenhorn and Demont (2004) observed species-specific patterns with latitude representing a continuum from increasing body size (Bergmann’s cline) to decreasing body size (converse Bergmann’s cline). Season length and the voltinism of a given species, which are related to the duration of preimaginal development, seem to be the main drivers of geographical size clines in terrestrial arthropods (Horne et al. 2015, Zeuss et al. 2017). In addition to abiotic factors, such as temperature, the body size of ectotherms can be affected by biotic factors, e.g., food quantity or quality, that vary along geographical gradients (Okuzaki and Sota 2017). In particular, large univoltine species tend to follow a converse Bergmann’s cline while smaller polyvoltine species tend to follow Bergmann’s cline. Moreover, underlying mechanisms responsible for intraspecific geographical variation in insect body size are not well known. Geographical clines could be a result of local adaptation, i.e., genetically determined, and/or phenotypic plasticity, i.e., plastic response to environmental conditions during juvenile development (Stillwell 2010). In addition to variation in size among populations, significant variation also exists between individuals within a particular population. Sex-related differences in body size commonly exist between males and females, which is termed ‘sexual size dimorphism’ (Teder and Tammaru 2005, Teder 2014), and such differences in body size are believed to arise when different selection pressures differentially act on males and females (Blanckenhorn 2000). Strong fecundity selection, i.e., selection for larger females that produce more eggs, results in female-biased sexual size dimorphism in most insect species (Teder 2014). As selection pressures can change along a geographical gradient, the degree of sexual size dimorphism may vary as well (Stillwell and Fox 2007, Laiolo et al. 2013). In addition, sex-specific phenotypic plasticity could be very important in insects (Teder and Tammaru 2005, Stillwell et al. 2010), so varying conditions along a geographical gradient, e.g., temperature or food availability, can result in varying degrees of sexual size dimorphism. Males generally seem to exhibit steeper geographical clines than females (Blanckenhorn et al. 2006). However, patterns can be taxon-specific, and data on carabid beetles are limited (e.g., Ikeda et al. 2012). Differences between individuals of the same sex are an additional source of intrapopulation variation that has only rarely been investigated in insects (Chown and Gaston 2010, Gouws et al. 2011, Mega 2014), and information on elevational clines in intrapopulation variation is almost non-existent (but see Bai et al. 2016, Baranovská and Knapp 2018). A meta-analysis by Teder et al. (2008) showed that relative variation in body size is generally lower in environments where individuals attain a larger final body size, indicating that, within a population, variation due to insect developmental plasticity is higher under suboptimal conditions, e.g., at high elevations or latitudes. However, intrapopulation variation in nature could not only be a result of developmental plasticity but could also reflect adaptations to local conditions. One can easily imagine that intrapopulation variation will differ between males and females. For example, strong fecundity selection can force females to maximize their body size, whereas male fitness is not as strongly affected by body size so more variable males can persist within a population. A tendency towards such a trend was observed for the carrion beetle Silpha carinata Herbst, 1783 (Coleoptera: Silphidae) (Baranovská and Knapp 2018), but data for other species are largely absent. In the present study, we conducted a thorough investigation of elevational size clines in several Central European carabid beetles. First, we examined changes in body size along an elevational gradient and whether female and male body sizes differ in response. We hypothesized that both female and male body sizes decrease with increasing elevation as all the studied carabids are large, univoltine species. We also expected that body size clines will be steeper in males compared to females as female body size could be under stronger selection pressure; i.e., females are forced to be larger even under suboptimal conditions. Second, we examined intrapopulation variation in body size along an elevational gradient and compared the degrees of intrapopulation variation between males and females. We hypothesized that intrapopulation variation increases with elevation, as high-elevation sites represent more stressful conditions, and that males are more variable than females within a given population. Third, we compared differences in intrapopulation variation between species, and we hypothesized that intrapopulation variation differs between species because such variation can be linked to species traits, e.g., niche width. We predicted higher intrapopulation body size variation for generalist species compared to habitat specialists. Materials and Methods Study Species In this study, we used carabid species that could be caught in sufficient numbers across elevational transects in selected mountain ranges (Table 1). In total, we collected more than 6,000 carabids, of which 4,189 beetles were measured: 262 individuals of Carabus auronitens auronitens Fabricius, 1792; 109 C. auronitens escheri Palliardi, 1825; 1,329 C. linnei Panzer, 1810; 366 C. sylvestris sylvestris Panzer, 1793; 422 C. sylvestris transsylvanicus Dejean, 1826; 219 Pterostichus burmeisteri Heer, 1838; 767 P. melanarius (Illiger, 1798) and 715 P. pilosus (Host, 1789; see Supp. Table S1). All studied species are large (with body lengths > 12 mm), univoltine species, and some are even semivoltine at higher elevations. The size of carabid beetles is quite variable within species; in some, the difference between the minimum and maximum body length can be up to 40% (Hůrka 1996). Females are generally the larger sex in carabids, but the degree of sexual size dimorphism is relatively limited (up to 15% difference between male and female lengths; M. Knapp, unpublished data). All species/subspecies except P. melanarius, P. pilosus, C. auronitens auronitens, and C. sylvestris transsylvanicus strongly prefer forested stands and thus only individuals originating from the preferred habitat type were measured (Table 2). Table 1. Summarizing information on sites sampled in this study Transect Mountain range Number of sampling sites Elevational range (m a.s.l.) JES1 Jeseníky Mts. 3 400–1,000 KRK Krkonoše Mts. 3 400–1,000 KRU Krušné Hory Mts. 3 400–1,000 JES2 Jeseníky Mts. 3 1,220–1,400 BAB Babia Góra Mts. 9 792–1,703 TAT High Tatras Mts. 18 1,008–1,963 BIE Bieszczady Mts. 20 697–1,218 Transect Mountain range Number of sampling sites Elevational range (m a.s.l.) JES1 Jeseníky Mts. 3 400–1,000 KRK Krkonoše Mts. 3 400–1,000 KRU Krušné Hory Mts. 3 400–1,000 JES2 Jeseníky Mts. 3 1,220–1,400 BAB Babia Góra Mts. 9 792–1,703 TAT High Tatras Mts. 18 1,008–1,963 BIE Bieszczady Mts. 20 697–1,218 View Large Table 1. Summarizing information on sites sampled in this study Transect Mountain range Number of sampling sites Elevational range (m a.s.l.) JES1 Jeseníky Mts. 3 400–1,000 KRK Krkonoše Mts. 3 400–1,000 KRU Krušné Hory Mts. 3 400–1,000 JES2 Jeseníky Mts. 3 1,220–1,400 BAB Babia Góra Mts. 9 792–1,703 TAT High Tatras Mts. 18 1,008–1,963 BIE Bieszczady Mts. 20 697–1,218 Transect Mountain range Number of sampling sites Elevational range (m a.s.l.) JES1 Jeseníky Mts. 3 400–1,000 KRK Krkonoše Mts. 3 400–1,000 KRU Krušné Hory Mts. 3 400–1,000 JES2 Jeseníky Mts. 3 1,220–1,400 BAB Babia Góra Mts. 9 792–1,703 TAT High Tatras Mts. 18 1,008–1,963 BIE Bieszczady Mts. 20 697–1,218 View Large Table 2. Effects of elevation, sex and their interaction on the body size of eight carabid species/subspecies Species Habitat preference Number of sites Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus auronitens auronitens Both habitats 6 387.4 <0.001 20.7 <0.001 0.1 0.766 Carabus auronitens escheri Spruce forest 17 215.6 <0.001 1.2 0.281 1.0 0.323 Carabus linnei Spruce forest 34 3401.7 <0.001 4.3 0.038 3.2 0.076 Carabus sylvestris sylvestris Spruce forest 5 118.7 <0.001 1.7 0.194 0.0 0.904 Carabus sylvestris transsylvanicus Both habitats 11 106.3 <0.001 0.3 0.567 0.0 0.932 Pterostichus burmeister Spruce forest 5 96.1 <0.001 0.5 0.475 0.2 0.690 Pterostichus melanarius Both habitats 9 399.2 <0.001 12.2 <0.001 0.5 0.471 Pterostichus pilosus Both habitats 39 321.1 <0.001 46.5 <0.001 0.2 0.690 Species Habitat preference Number of sites Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus auronitens auronitens Both habitats 6 387.4 <0.001 20.7 <0.001 0.1 0.766 Carabus auronitens escheri Spruce forest 17 215.6 <0.001 1.2 0.281 1.0 0.323 Carabus linnei Spruce forest 34 3401.7 <0.001 4.3 0.038 3.2 0.076 Carabus sylvestris sylvestris Spruce forest 5 118.7 <0.001 1.7 0.194 0.0 0.904 Carabus sylvestris transsylvanicus Both habitats 11 106.3 <0.001 0.3 0.567 0.0 0.932 Pterostichus burmeister Spruce forest 5 96.1 <0.001 0.5 0.475 0.2 0.690 Pterostichus melanarius Both habitats 9 399.2 <0.001 12.2 <0.001 0.5 0.471 Pterostichus pilosus Both habitats 39 321.1 <0.001 46.5 <0.001 0.2 0.690 Habitat preference indicating the origin of investigated specimens (habitat of their sampling; spruce forest or hay meadow) and number of sites with occurrence of a given species are shown. Results of LMM are reported. Mountain range identity was employed as a random effect in the model. Body size is represented by elytron length. Significant terms are highlighted in bold. Detailed results including R2-values and coefficients are shown in Supp. Table S3. View Large Table 2. Effects of elevation, sex and their interaction on the body size of eight carabid species/subspecies Species Habitat preference Number of sites Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus auronitens auronitens Both habitats 6 387.4 <0.001 20.7 <0.001 0.1 0.766 Carabus auronitens escheri Spruce forest 17 215.6 <0.001 1.2 0.281 1.0 0.323 Carabus linnei Spruce forest 34 3401.7 <0.001 4.3 0.038 3.2 0.076 Carabus sylvestris sylvestris Spruce forest 5 118.7 <0.001 1.7 0.194 0.0 0.904 Carabus sylvestris transsylvanicus Both habitats 11 106.3 <0.001 0.3 0.567 0.0 0.932 Pterostichus burmeister Spruce forest 5 96.1 <0.001 0.5 0.475 0.2 0.690 Pterostichus melanarius Both habitats 9 399.2 <0.001 12.2 <0.001 0.5 0.471 Pterostichus pilosus Both habitats 39 321.1 <0.001 46.5 <0.001 0.2 0.690 Species Habitat preference Number of sites Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus auronitens auronitens Both habitats 6 387.4 <0.001 20.7 <0.001 0.1 0.766 Carabus auronitens escheri Spruce forest 17 215.6 <0.001 1.2 0.281 1.0 0.323 Carabus linnei Spruce forest 34 3401.7 <0.001 4.3 0.038 3.2 0.076 Carabus sylvestris sylvestris Spruce forest 5 118.7 <0.001 1.7 0.194 0.0 0.904 Carabus sylvestris transsylvanicus Both habitats 11 106.3 <0.001 0.3 0.567 0.0 0.932 Pterostichus burmeister Spruce forest 5 96.1 <0.001 0.5 0.475 0.2 0.690 Pterostichus melanarius Both habitats 9 399.2 <0.001 12.2 <0.001 0.5 0.471 Pterostichus pilosus Both habitats 39 321.1 <0.001 46.5 <0.001 0.2 0.690 Habitat preference indicating the origin of investigated specimens (habitat of their sampling; spruce forest or hay meadow) and number of sites with occurrence of a given species are shown. Results of LMM are reported. Mountain range identity was employed as a random effect in the model. Body size is represented by elytron length. Significant terms are highlighted in bold. Detailed results including R2-values and coefficients are shown in Supp. Table S3. View Large Field Sampling and Body Size Measurements Carabids were collected using pitfall traps along seven elevational transects in the following Central European mountain ranges: the Krkonoše Mts., Krušné Hory Mts., Jeseníky Mts., Babia Góra Mts., Bieszczady Mts., and High Tatras Mts. (Fig. 1). Within each sampled site (elevation), two habitat types (spruce forest and hay meadow) were sampled if available. In the case of the highest elevations, only open habitat sites were sampled (these sites were above the tree line). The pitfall traps installed in the Krkonoše, Jeseníky and Krušné Hory Mts. were baited with fish and filled with propylene glycol as a preservation fluid (for details, see Knapp et al. 2016). Sampling sites were established at three elevations (400, 700, and 1,000 m a.s.l.) in each of these Czech mountain ranges. In Poland (Babia Góra Mts. and Bieszczady Mts.) and Slovakia (High Tatras) as well as the Jeseníky Mts. (second transect), transects consisted of sites unevenly distributed along elevational gradients between 697 m a.s.l. and 1963 m a.s.l. (for details, see Table 1). Along these transects, unbaited pitfall traps filled with formaldehyde as a preservation fluid were employed. Distances between sampling sites within each mountain range ranged from ca. 500 m to ca. 15 km (sites were commonly situated a few km from each other). Summarizing information on all sampling sites is available in Table 1. As all the investigated carabid species, except Pterostichus melanarius, are flightless (some P. melanarius individuals can fly), i.e., their dispersal distances are at the scale of hundreds of meters, only very limited gene flow is expected between sampling sites. Moreover, patches of habitats preferred by particular species are fragmented in almost all the investigated mountain ranges (the landscapes consist of forest-meadow mosaics, and species spillover between contrasting habitats is very limited in carabids). Sample collection was related to several research and monitoring projects and in most cases occurred within areas under different levels of nature protection. Therefore, all field research was undertaken with official permission of the appropriate nature protection bodies of all three countries in which the mountain areas were sampled. Fig. 1. View largeDownload slide Map illustrating the geographical locations of sampled sites. From West to East: the Krušné Hory Mts., Krkonoše Mts., Jeseníky Mts., Babia Góra Mts., High Tatras Mts., and Bieszczady Mts. The information on the presence of particular carabid species in our samples from different sites is visualized by various colors corresponding to the species (for details, see the legend within the figure). Centroids of pie graphs in small panels indicate sampling site locations (if sites were too close to each other, precise site locations are indicated by guiding lines). Fig. 1. View largeDownload slide Map illustrating the geographical locations of sampled sites. From West to East: the Krušné Hory Mts., Krkonoše Mts., Jeseníky Mts., Babia Góra Mts., High Tatras Mts., and Bieszczady Mts. The information on the presence of particular carabid species in our samples from different sites is visualized by various colors corresponding to the species (for details, see the legend within the figure). Centroids of pie graphs in small panels indicate sampling site locations (if sites were too close to each other, precise site locations are indicated by guiding lines). In this study, we used elytron length as a measure of body size, and it was measured using a digital caliper with 0.01-mm precision. An undamaged elytron was separated from the body and placed on a sheet of paper, and its maximum length was measured. In total, structural body size, i.e., elytron length, was measured for 2,008 females and 2,182 males (for details, see the raw data included in Supp. Table S1). Elytron length is tightly correlated with total body length and other measures of structural body size in carabid beetles (Knapp and Knappová 2013). Therefore, elytron length is frequently used measure in studies focused on evolution of beetle body size (e.g., Baranovská and Knapp 2018, Tseng and Pari 2019). Data Analyses Elevational variation in body size was separately tested for each species using a linear mixed-effects model (LMM), and significance was evaluated using a type II Wald χ2-test. Elytron length was employed as a response variable in these models. Sex, elevation and an interaction term between sex and elevation were included as independent variables, and mountain range identity and population identity were treated as random effects to account for the shared origin of individuals collected from a given mountain range and the same site. Elevation was standardized to allow the regression slopes for particular species to be compared for different elevational ranges (see above) as well as to enable comparisons with future studies (Schielzeth 2010). Standardization was performed by subtracting individual elevation values from the mean elevation for a given species and dividing this value by the standard deviation for the species. R2 values for all fixed effect terms in our LMM were computed using the ‘r2beta’ function of the ‘r2glmm’ package in R (Jaeger 2017). To examine intrapopulation variation in body size along an elevational gradient, our first dataset was limited to species with data available for five or more populations, of which each was represented by at least 12 individuals per sex. In total, 34 populations of four species were included in the analyses of elevational clines in intrapopulation variation in body size: 12 populations of C. linnei, 5 populations of C. sylvestris sylvestris, 6 populations of P. melanarius, and 11 populations of P. pilosus (Supp. Table S2). To enable proper comparisons of intrapopulation variation in body size among various populations that differed in their mean body size, intrapopulation variation was standardized by dividing the elytron length of each specimen by the respective population mean. Standardization was performed separately for males and females for each population and species, and these standardized data were used to compute variance for each population*sex combination for each species. The effect of elevation on intrapopulation variation in body size was analyzed separately for each species using LMM with sex as a covariate, elevation as an independent variable and population identity as a random effect. To analyze the effects of sex and species identity on intrapopulation variation, a larger dataset was employed that consisted of 42 populations satisfying our criterion of at least 12 individuals per sex. The dataset consisted of 2 populations of C. auronitens auronitens, 1 population of C. auronitens escheri, 12 populations of C. linnei, 5 populations of C. sylvestris sylvestris, 1 population of C. sylvestris transsylvanicus, 4 populations of P. burmeisteri, 6 populations of P. melanarius and 11 populations of P. pilosus (Supp. Table S2). To test for systematic differences in intrapopulation variation in body size between sexes across all species, an LMM was fitted with sex as an independent variable and population identity as a random effect. To compare intrapopulation variation in body size among species, an LMM was applied with sex as a covariate, species as an independent variable and population identity as a random effect. The resulting significance values are based on type II Wald χ2-test statistics. All statistical analyses were conducted in R 3.4.3 (R Development Core Team 2017) using the lme4 package (Bates et al. 2017) and the car package (Fox et al. 2017). Results Variation Between Populations The majority of the investigated species/subspecies followed a converse Bergmann’s cline; i.e., their body size decreased with increasing elevation (Fig. 2). The decrease in body size with elevation was significant for C. auronitens auronitens, C. linnei, P. melanarius, and P. pillosus, and a nonsignificant relationship was observed for C. auronitens escheri, C. sylvestris sylvestris, C. sylvestris transsylvanicus, and P. burmeisteri (Table 2). Interestingly, two subspecies of C. auronitens showed contrasting patterns, but it is important to note that only a few individuals were collected of the Carpathian subspecies C. auronitens escheri. None of the investigated carabid species/subspecies followed Bergmann’s cline, i.e., exhibited a significant increase in body size with elevation. For all the investigated species, a significant difference in body size was observed between sexes, with females being larger (Table 2). However, the degree of sexual size dimorphism differed between species and ranged from ca. 5% in C. sylvestris to ca. 14% in C. linnei. In general, the degree of sexual size dimorphism did not change along an elevational gradient; i.e., the interaction between elevation and sex was not significant, with the exception of marginal significance in C. linnei (Table 2). Fig. 2. View largeDownload slide Body size variation in carabid beetles along elevational gradients. Each symbol represents an individual beetle. Black triangles represent males, and gray circles represent females. Elytron length was used as the measure of body size. Fig. 2. View largeDownload slide Body size variation in carabid beetles along elevational gradients. Each symbol represents an individual beetle. Black triangles represent males, and gray circles represent females. Elytron length was used as the measure of body size. In general, differences among populations explained only a minor portion of the variation among individuals within a carabid species, so variation among individuals within a population was crucial (Fig. 2, Table 3, Supp. Table S3). Table 3. Results of LMM fitting the effects of elevation, sex and their interaction on intrapopulation variation in the body size of four carabid species Species Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus linnei 1.3 0.262 1.3 0.249 2.7 0.102 Carabus sylvestris sylvestris 0.2 0.656 4.7 0.030 3.7 0.054 Pterostichus melanarius 4.4 0.036 0.1 0.731 1.0 0.323 Pterostichus pilosus 0.1 0.750 2.7 0.098 0.2 0.669 Species Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus linnei 1.3 0.262 1.3 0.249 2.7 0.102 Carabus sylvestris sylvestris 0.2 0.656 4.7 0.030 3.7 0.054 Pterostichus melanarius 4.4 0.036 0.1 0.731 1.0 0.323 Pterostichus pilosus 0.1 0.750 2.7 0.098 0.2 0.669 Mountain range identity was employed as a random effect. Intrapopulation variation was expressed as the variance of standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Significant terms are highlighted in bold. View Large Table 3. Results of LMM fitting the effects of elevation, sex and their interaction on intrapopulation variation in the body size of four carabid species Species Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus linnei 1.3 0.262 1.3 0.249 2.7 0.102 Carabus sylvestris sylvestris 0.2 0.656 4.7 0.030 3.7 0.054 Pterostichus melanarius 4.4 0.036 0.1 0.731 1.0 0.323 Pterostichus pilosus 0.1 0.750 2.7 0.098 0.2 0.669 Species Sex Elevation Sex*elevation χ2 P-value χ2 P-value χ2 P-value Carabus linnei 1.3 0.262 1.3 0.249 2.7 0.102 Carabus sylvestris sylvestris 0.2 0.656 4.7 0.030 3.7 0.054 Pterostichus melanarius 4.4 0.036 0.1 0.731 1.0 0.323 Pterostichus pilosus 0.1 0.750 2.7 0.098 0.2 0.669 Mountain range identity was employed as a random effect. Intrapopulation variation was expressed as the variance of standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Significant terms are highlighted in bold. View Large Variation Within Populations The degree of intrapopulation variation in body size seems to slightly increase with elevation in C. sylvestris sylvestris and P. pilosus (the result was marginally significant for P. pilosus; Table 2), and no relationship was observed between intrapopulation variation in body size and elevation for C. linnei and P. melanarius (Table 3). A marginally significant effect of sex-specific elevational clines on intrapopulation variation in body size was found in C. sylvestris sylvestris; i.e., the variation in male size increased with elevation whereas that in female size did not vary with elevation (Fig. 3; Table 3). Intrapopulation variation did not significantly differ between females and males when the general pattern across species was investigated (LMM: χ2 = 0.36, P = 0.55), but a significant difference was detected in P. melanarius, in which females varied more than males within the same population (Table 3). Intrapopulation variation in body size differed significantly among the investigated carabid species (LMM: χ2 = 19.28, P = 0.007). The most pronounced variation was found in P. melanarius and C. auronitens, whereas the lowest variation was observed in P. burmeisteri and P. pilosus (Fig. 4). Fig. 3. View largeDownload slide Effect of elevation and sex on standardized intrapopulation variation in body size in four carabid species. Individual symbols correspond to the sampled populations. Values are presented separately for males (black triangles) and females (gray circles). Intrapopulation variation was expressed as the variance in standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Fig. 3. View largeDownload slide Effect of elevation and sex on standardized intrapopulation variation in body size in four carabid species. Individual symbols correspond to the sampled populations. Values are presented separately for males (black triangles) and females (gray circles). Intrapopulation variation was expressed as the variance in standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Fig. 4. View largeDownload slide Differences in intrapopulation variation in body size among carabid species/subspecies. Different letters (not shared) between species/subspecies indicate significant differences between species/subspecies based on Tukey post hoc tests. Mean values ± SEM are shown. Intrapopulation variation was expressed as the variance in standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Fig. 4. View largeDownload slide Differences in intrapopulation variation in body size among carabid species/subspecies. Different letters (not shared) between species/subspecies indicate significant differences between species/subspecies based on Tukey post hoc tests. Mean values ± SEM are shown. Intrapopulation variation was expressed as the variance in standardized data (the elytron length of each specimen was divided by the respective population mean; standardization was performed separately for males and females within a given population). Discussion Our results show that the investigated carabid species tend to follow a converse Bergmann’s cline rather than Bergmann’s cline, and we confirmed that female-biased sexual size dimorphism is common in carabids as females were significantly larger than males in all the investigated species. The degree of sexual size dimorphism appears to be quite constant along elevational gradients in carabids, and intrapopulation variation in body size exhibited signs of a slight increase with elevation in some species. There were significant differences between species in the degree of intrapopulation variation in body size, but generally, there was no difference in intrapopulation variation between males and females. It is important to note that intrapopulation variation in body size is responsible for a major component of the variability among individuals within species in our study system. Within species, it appears that most coleopterans follow a converse Bergmann’s cline; i.e., their body size decreases with increasing elevation/latitude (Blanckenhorn and Demont 2004, Shelomi 2012, Horne et al. 2018), and this pattern is also common in carabids (this study, Park 1949, Sota 1985, Sota 1996, Tsuchiya et al. 2012, Sukhodolskaya and Saveliev 2016, Okuzaki and Sota 2017). The investigated beetles are large, univoltine species with relatively long development time, so their preimaginal development is probably limited by season length. Semivoltine development is even possible for some species/populations, but detailed information is lacking (Hůrka 1996). Therefore, we recommend that future studies also focus on investigating the relationship between elevation and body size in small carabid species. Some of these smaller carabids have relatively short preimaginal development times (Saska and Honěk 2003). However, they are collected by pitfall traps less frequently, so an alternative sampling technique would need to be employed (Hancock and Legg 2012). It is also important to note that elevational gradients may be not fully comparable with latitudinal gradients. Recently, Horne et al. (2018) showed that body size along elevational gradients exhibits contrasting responses to latitudinal gradients and not the pattern predicted by the temperature-size rule in the laboratory. Thus, some variables can specifically vary with elevation; for example, the elevational cline in the body size of Carabus japonicus Motschulsky, 1857 (Coleoptera: Carabidae) seems to correspond to prey availability (Okuzaki and Sota 2017). Similarly, the oxygen concentration varies with elevation but not with latitude. The existing evidence indicates that lowered oxygen concentration can cause body size reduction especially in large insects (Harrison et al. 2010). However, effects of reduced oxygen availability are probably not strong enough to be the main driver of elevational gradients in body size observed in this study (at altitudes between 400 and 2,000 m a.s.l.). Observed differences among species and even among subspecies (body size variation of two subspecies of C. auronitens showed contrasting patterns; body size did not change with elevation in C. auronitens escheri but decreased with elevation in C. auronitens auronitens) can be explained by several reasons. Non-significant clines can result from insufficient sampling; e.g., only a few individuals of the Carpathian subspecies C. auronitens escheri were collected from high elevations. However, there are also biologically meaningful explanations such as the traits of investigated species and subspecies can differ. For example, Sota (1996) showed that overwintering in the larval stage can facilitate the survival of carabids under high-elevation conditions (promoting the transition from a univoltine to a semivoltine life cycle), and such species spanning large elevational ranges also exhibit steeper elevational clines in body size. However, probably the only species/subspecies investigated in our study that solely overwinters in the adult stage is P. burmeisteri (Hůrka 1996), so the overwintering mode, per se, is not sufficient to explain the observed differences among species. Female-biased sexual size dimorphism is a common phenomenon in carabids (e.g., Sota et al. 2002, Lagisz 2008, Henríquez et al. 2009, Laparie et al. 2010, Tsuchiya et al. 2012), and this probably results from fecundity selection on females exceeding sexual selection on males; in carabids, the latter only rarely fight for females (Okuzaki et al. 2012). The degree of sexual size dimorphism differs between species (this study, Teder and Tammaru 2005, Teder 2014) and as documented for several insect species, it can also vary between populations within species (e.g., Blanckenhorn et al. 2006, Stillwell and Fox 2009, Laiolo et al. 2013, Levy and Nufio 2015). Differences in phenotypic plasticity between males and females have been proposed to be partly responsible for variation in sexual size dimorphism within species (Stillwell et al. 2010). Absenting variation in sexual dimorphism in carabid body size observed in our study could be explained by the positive relationship between sex-specific phenotypic plasticity and the degree of sexual size dimorphism, i.e., sex-specific plasticity is rare in species with less pronounced sexual size dimorphism, such as carabid beetles (Teder and Tammaru 2005). The lack of a sex-specific response to elevation can also be caused by similar plasticity in size responses to temperature in females and males (Hirst et al. 2015). This study provides a unique insight into patterns of intrapopulation variation in the body size of carabid beetles. Intrapopulation variation in body size can play a key role in understanding the evolution of insect body size (Gouws et al. 2011), but only a few studies have investigated this issue. We found that a substantial proportion of variation in body size among individuals within species occurs at an intrapopulation level. Large intrapopulation variation is probably linked to developmental plasticity caused by variation in food availability during larval development. All the investigated carabid species are carnivorous, and their prey is typically unevenly distributed in time and space, resulting in a variable energy income among individuals (Kotze et al. 2011). Food quality and quantity during the larval stage have been previously shown to be a significant source of variability in adult body size (e.g., Bommarco 1998, Sasakawa 2011). In our study system, the degree of intrapopulation variation in body size increased with elevation in some species (C. sylvestris sylvestris, P. pilosus) but did not vary in others (C. linnei, P. melanarius). Thus, our results are partially congruent with the tendency toward increased intrapopulation variation in insect body size under stressful environmental conditions (Teder et al. 2008). In contrast to our hypothesis and published results on the carrion beetle S. carinata (Baranovská and Knapp 2018), intrapopulation variation did not differ between males and females, and the pattern observed in P. melanarius was even opposite to that predicted, with intrapopulation variation being larger in females compared to males. Higher variation in female body size has been previously reported for carabids by Bell et al. (2017). P. melanarius together with C. auronitens also showed the highest degree of intrapopulation variation when compared to the other species investigated in this study, and the nonspecific environmental demands of these two species are a possible explanation. These generalist species are widely distributed in Central Europe (Hůrka 1996) and are able to inhabit both open and forest habitats and probably different microhabitats within certain sites. However, future research focused on differences in the degree of intrapopulation variation in body size between species is needed to disentangle the real drivers (evolutionary or ecological determinants). In conclusion, the converse Bergmann’s cline observed in most of the carabid species investigated in this study is in accordance with patterns predicted for large, terrestrial, univoltine insects. The lack of elevational clines in the degree of sexual size dimorphism in the investigated carabid species is probably due to similar responses of both sexes to changing environmental conditions. The degree of intrapopulation variation in body size slightly increased with elevation in some species, but no general trend was observed. However, there were significant differences in the degree of intrapopulation variation in body size among the investigated carabid species. The existing literature on intrapopulation variation in body size in insects is limited, but further investigation of this issue could elucidate the mechanisms generating geographical clines and determining the degree of sexual size dimorphism. Acknowledgments Sample collection was related to several research and monitoring projects in areas with different levels of nature protection and was performed with official permission from the appropriate nature protection bodies in the Czech Republic (Ministry of Environment CR; Krkonoše National Park, Jeseníky Protected Landscape Area), Poland (Babia Gora National Park, Bieszczady National Park), and Slovakia (Tatra National Park; Ministry of Environment SK), whose support is highly appreciated by the authors. We are grateful to Tiit Teder and three anonymous reviewers for insightful comments on a previous version of the manuscript, Věra Zaplatílková for her help in the field and Philippe Vernon for a general discussion of related topics. Advice on the statistical analyses was provided by Petr Chajma. This study was financially supported by grants 42110/1312/3123 and 42110/1312/3118 from the Internal Grant Agency of the Faculty of Environmental Sciences at the Czech University of Life Sciences, Prague. The field research was partly supported by the Czech Science Foundation, project 14-09231S. References Cited Arriaga-Osnaya , B. J. , J. Contreras-Garduño , F. J. Espinosa-García , Y. M. García-Rodríguez , M. Moreno-García , H. Lanz-Mendoza , H. Godínez-Álvarez , and R. Cueva del Castillo. 2017 . Are body size and volatile blends honest signals in orchid bees? Ecol. Evol . 7 : 3037 – 3045 . Google Scholar Crossref Search ADS PubMed Bai , Y. , J.-J. Dong , D.-L. Guan , J.-Y. Xie , and S.-Q. Xu . 2016 . Geographic variation in wing size and shape of the grasshopper Trilophidia annulata (Orthoptera: Oedipodidae): morphological trait variations follow an ecogeographical rule . Sci. Rep . 6 : 32680 . Google Scholar Crossref Search ADS PubMed Baranovská , E. , and M. Knapp . 2018 . Steep converse Bergmann’s cline in a carrion beetle: between- and within-population variation in body size along an elevational gradient . J. Zool . 304 : 243 – 251 . Google Scholar Crossref Search ADS Bates , D. , B. Bolker , S. Walker , H. Singmann , B. Dai , and F. Scheipl . 2017 . lme4: Linear Mixed-Effects Models using “Eigen” and S4 Contact. R package version 1.1–15 .https://cran.r-project.org/web/packages/lme4/index.html Bell , A. J. , I. D. Phillips , S. E. Nielsen , and J. R. Spence . 2017 . Species traits modify the species-area relationship in ground-beetle (Coleoptera: Carabidae) assemblages on islands in a boreal lake . PLoS One 12 : 1 – 16 . Bergmann , C . 1847 . Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse, Göttinger Stud . Vandenhoeck und Ruprecht , Göttingen, Germany . Blackburn , T. M. , K. J. Gaston , and N. Loder . 1999 . Geographic gradients in body size: a clarification of Bergmann’s rule . Divers. Distrib . 5 : 165 – 174 . Google Scholar Crossref Search ADS Blanckenhorn , W . 2000 . The evolution of body size: what keeps organisms small? Q. Rev. Biol . 75 : 385 – 407 . Google Scholar Crossref Search ADS PubMed Blanckenhorn , W. U. , and M. Demont . 2004 . Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr. Comp. Biol . 44 : 413 – 424 . Google Scholar Crossref Search ADS PubMed Blanckenhorn , W. U. , R. C. Stillwell , K. A. Young , C. W. Fox , and K. G. Ashton . 2006 . When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution . 60 : 2004 – 2011 . Google Scholar Crossref Search ADS PubMed Blanckenhorn , W. , J. Fanti , and C. Reim . 2007 . Size‐dependent energy reserves, energy utilization and longevity in the yellow dung fly . Physiol. Entomol . 32 : 372 – 381 . Google Scholar Crossref Search ADS Bommarco , R . 1998 . Stage sensitivity to food limitation for a generalist arthropod predator, Pterostichus cupreus (Coleoptera: Carabidae) . Environ. Entomol . 27 : 863 – 869 . Google Scholar Crossref Search ADS Chown , S. L. , and K. J. Gaston . 2010 . Body size variation in insects: a macroecological perspective . Biol. Rev. Camb. Philos. Soc . 85 : 139 – 169 . Google Scholar Crossref Search ADS PubMed Fox , J. , S. Weisberg , D. Adler , D. Bates , G. Baud-bovy , S. Ellison , D. Firth , M. Friendly , G. Gorjanc , S. Graves , et al. . 2017 . car: Companion to Applied Regression. R package version 2.1–6 . https://cran.r-project.org/web/packages/car/index.html Gotthard , K. , D. Berger , and R. Walters . 2007 . What keeps insects small? Time limitation during oviposition reduces the fecundity benefit of female size in a butterfly . Am. Nat . 169 : 768 – 779 . Google Scholar Crossref Search ADS PubMed Gouws , E. J. , K. J. Gaston , and S. L. Chown . 2011 . Intraspecific body size frequency distributions of insects . PLoS One 6 : 1 – 8 . Google Scholar Crossref Search ADS Hancock , M. H. , and C. J. Legg . 2012 . Pitfall trapping bias and arthropod body mass . Insect Conserv. Divers . 5 : 312 – 318 . Google Scholar Crossref Search ADS Harrison , J. F. , A. Kaiser , and J. M. VandenBrooks . 2010 . Atmospheric oxygen level and the evolution of insect body size . Proc. R. Soc. B Biol. Sci . 277 : 1937 – 1946 . Google Scholar Crossref Search ADS Henríquez , P. , D. S. Donoso , and A. A. Grez . 2009 . Population density, sex ratio, body size and fluctuating asymmetry of Ceroglossus chilensis (Carabidae) in the fragmented Maulino forest and surrounding pine plantations . Acta Oecol . 35 : 811 – 818 . Google Scholar Crossref Search ADS Hirst , A. G. , C. R. Horne , and D. Atkinson . 2015 . Equal temperature– size responses of the sexes are widespread within arthropod species . Proc. R. Soc. B Biol. Sci . 282 : 1 – 9 . Google Scholar Crossref Search ADS Honěk , A . 1993 . Intraspecific variation in body size and fecundity in insects: a general relationship . Oikos . 66 : 483 – 492 . Google Scholar Crossref Search ADS Horne , C. R. , A. G. Hirst , and D. Atkinson . 2015 . Temperature-size responses match latitudinal-size clines in arthropods, revealing critical differences between aquatic and terrestrial species . Ecol. Lett . 18 : 327 – 335 . Google Scholar Crossref Search ADS PubMed Horne , C. R. , A. G. Hirst , and D. Atkinson . 2018 . Insect temperature-body size trends common to laboratory, latitudinal and seasonal gradients are not found across altitudes . Funct. Ecol . 32 : 1 – 10 . Google Scholar Crossref Search ADS Hůrka , K . 1996 . Carabidae of the Czech and Slovak Republics (České a Slovenské republiky) . Kabourek , Zlín, Czech Republic . Ikeda , H. , Y. Tsuchiya , N. Nagata , M. T. Ito , and T. Sota . 2012 . Altitudinal life-cycle and body-size variation in ground beetles of the genus Carabus (subgenus Ohomopterus) in relation to the temperature conditions and prey earthworms . Pedobiologia (Jena) . 55 : 67 – 73 . Google Scholar Crossref Search ADS Jaeger , B . 2017 . Computes R Squared for Mixed (Multilevel) Models . r2glmm: Computes R Squared for Mixed (Multilevel) Models. R package version 0.1.2. https://cran.r-project.org/web/packages/r2glmm/index.html Kingsolver , J. G. , and R. B. Huey . 2008 . Size, temperature, and fitness: three rules . Evol. Ecol. Res . 10 : 251 – 268 . Knapp , M. , and J. Knappová . 2013 . Measurement of body condition in a common carabid beetle, Poecilus cupreus: a comparison of fresh weight, dry weight, and fat content . J. Insect Sci . 13 : 6 . Google Scholar Crossref Search ADS PubMed Knapp , M. , E. Baranovská , and P. Jakubec . 2016 . Effects of bait presence and type of preservative fluid on ground and carrion beetle samples collected by pitfall trapping . Environ. Entomol . 45 : 1022 – 1028 . Google Scholar Crossref Search ADS PubMed Kotze , D. , P. Brandmayr , A. Casale , E. Dauffy-Richard , W. Dekoninck , M. Koivula , G. L. Lövei , D. Mossakowski , J. Noordijk , W. Paarmann , et al. . 2011 . Forty years of carabid beetle research in Europe–from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation . Zookeys . 100 : 55 – 148 . Google Scholar Crossref Search ADS Kovacs , J. L. , and M. A. D. Goodisman . 2010 . Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons . Insectes Soc . 57 : 53 – 65 . Google Scholar Crossref Search ADS Lagisz , M . 2008 . Changes in morphology of the ground beetle Pterostichus oblongopunctatus F. (Coleoptera; Carabidae) from vicinities of a zinc and lead smelter . Environ. Toxicol. Chem . 27 : 1744 – 1747 . Google Scholar Crossref Search ADS PubMed Laiolo , P. , J. C. Illera , and J. R. Obeso . 2013 . Local climate determines intra- and interspecific variation in sexual size dimorphism in mountain grasshopper communities . J. Evol. Biol . 26 : 2171 – 2183 . Google Scholar Crossref Search ADS PubMed Laparie , M. , M. Lebouvier , L. Lalouette , and D. Renault . 2010 . Variation of morphometric traits in populations of an invasive carabid predator (Merizodus soledadinus) within a sub-Antarctic island . Biol. Invasions 12 : 3405 – 3417 . Google Scholar Crossref Search ADS Levy , R. A. , and C. R. Nufio . 2015 . Dispersal potential impacts size clines of grasshoppers across an elevation gradient . Oikos . 124 : 610 – 619 . Google Scholar Crossref Search ADS Marshall , J. M. , M. A. Miller , J. P. Lelito , and A. J. Storer . 2013 . Latitudinal variation in body size of Agrilus planipennis and relationship with fecundity . Agric. For. Entomol . 15 : 294 – 300 . Google Scholar Crossref Search ADS Mega , N. O . 2014 . The adult body size variation of Dryas iulia (Lepidoptera, Nymphalidae, Heliconiinae) in different populations is more influenced by temperature variation than by host-plant availability during the seasons . Entomol. Sci . 17 : 376 – 387 . Google Scholar Crossref Search ADS Nylin , S. , and K. Gotthard . 1998 . Plasticity in life-history traits . Annu. Rev. Entomol . 43 : 63 – 83 . Google Scholar Crossref Search ADS PubMed Okuzaki , Y. , and T. Sota . 2017 . Factors Related to Altitudinal Body Size Variation in the Earthworm-Eating Ground Beetle Carabus japonicus . Zoolog. Sci . 34 : 229 – 234 . Google Scholar Crossref Search ADS PubMed Okuzaki , Y. , Y. Takami , Y. Tsuchiya , and T. Sota . 2012 . Mating behavior and the function of the male genital spine in the ground beetle Carabus clathratus . Zoolog. Sci . 29 : 428 – 432 . Google Scholar Crossref Search ADS PubMed Park , O . 1949 . Application of the converse Bergmann principle to the carabid beetle, Dicaelus purpuratus . Physiol. Zool . 22 : 359 – 372 . Google Scholar Crossref Search ADS PubMed Pincheira-Donoso , D. , and J. Hunt . 2015 . Fecundity selection theory: concepts and evidence . Biol. Rev . 44 : 341 – 356 . R Development Core Team . 2017 . R Internals . R Dev. Core Team . 1 : 63 . Ray , C . 1960 . The application of Bergmann’s and Allen’s rules to the poikilotherms . J. Morphol . 106 : 85 – 108 . Google Scholar Crossref Search ADS PubMed Romero-Alcaraz , E. , and J. M. Ávila . 2000 . Landscape heterogeneity in relation to variations in epigaeic beetle diversity of a Mediterranean ecosystem. Implications for conservation . Biodivers. Conserv . 9 : 985 – 1005 . Google Scholar Crossref Search ADS Sasakawa , K . 2011 . Laboratory studies on larval food habits of two syntopic, related, granivorous ground beetles Amara chalcites and A. congrua (Coleoptera: Carabidae): a comparison with stable isotope analysis . Appl. Entomol. Zool . 46 : 511 – 518 . Google Scholar Crossref Search ADS Saska , P. , and A. Honěk . 2003 . Temperature and development of central European species of Amara (Coleoptera: Carabidae) . Eur. J. Entomol . 100 : 509 – 515 . Google Scholar Crossref Search ADS Savalli , U. , and C. Fox . 1998 . Sexual selection and the fitness consequences of male body size in the seed beetle Stator limbatus . Anim. Behav . 55 : 473 – 483 . Google Scholar Crossref Search ADS PubMed Schielzeth , H . 2010 . Simple means to improve the interpretability of regression coefficients . Methods Ecol. Evol . 1 : 103 – 113 . Google Scholar Crossref Search ADS Shelomi , M . 2012 . Where are we now? Bergmann’s rule sensu lato in insects . Am. Nat . 180 : 511 – 519 . Google Scholar Crossref Search ADS PubMed Sota , T . 1985 . Limitation of reproduction by feeding condition in a carabid beetle, Carabus yaconinus . Res. Popul. Ecol. (Kyoto) 27 : 171 – 184 . Google Scholar Crossref Search ADS Sota , T . 1996 . Altitudinal variation in life cycles of carabid beetles: life-cylce strategy and colonization in alpine zones . Arct. Alp. Res . 28 : 441 . Google Scholar Crossref Search ADS Sota , T. , Y. Takami , K. Kubota , and R. Ishikawa . 2002 . Geographic variation in body size of carabid beetles: patterns resulting from climatic adaptation and interspecific interaction . Entomol. Sociate Japan . 5 : 88 – 97 . Stillwell , R. C . 2010 . Are latitudinal clines in body size adaptive? Oikos . 119 : 1387 – 1390 . Google Scholar Crossref Search ADS PubMed Stillwell , R. C. , and C. W. Fox . 2007 . Environmental effects on sexual size dimorphism of a seed-feeding beetle . Oecologia . 153 : 273 – 280 . Google Scholar Crossref Search ADS PubMed Stillwell , R. C. , and C. W. Fox . 2009 . Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity . Oikos . 118 : 703 – 712 . Google Scholar Crossref Search ADS Stillwell , R. C. , W. U. Blanckenhorn , T. Teder , G. Davidowitz , and C. W. Fox . 2010 . Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution . Annu. Rev. Entomol . 55 : 227 – 245 . Google Scholar Crossref Search ADS PubMed Sukhodolskaya , R. , and A. Saveliev . 2016 . Body Size Variation of Ground Beetles (Coleoptera: Carabidae) in Latitudinal Gradient . Period. Biol . 118 : 273 – 280 . Google Scholar Crossref Search ADS Teder , T . 2014 . Sexual size dimorphism requires a corresponding sex difference in development time: a meta-analysis in insects . Funct. Ecol . 28 : 479 – 486 . Google Scholar Crossref Search ADS Teder , T. , and T. Tammaru . 2005 . Sexual size dimorphism within species increases with body size in insects . Oikos . 108 : 321 – 334 . Google Scholar Crossref Search ADS Teder , T. , T. Tammaru , and T. Esperk . 2008 . Dependence of phenotypic variance in body size on environmental quality . Am. Nat . 172 : 223 – 232 . Google Scholar Crossref Search ADS PubMed Teder , T. , T. Esperk , T. Remmel , A. Sang , and T. Tammaru . 2010 . Counterintuitive size patterns in bivoltine moths: late-season larvae grow larger despite lower food quality . Oecologia . 162 : 117 – 125 . Google Scholar Crossref Search ADS PubMed Teuschl , Y. , C. Reim , and W. U. Blanckenhorn . 2007 . Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies . J. Evol. Biol . 20 : 87 – 103 . Google Scholar Crossref Search ADS PubMed Tseng , M. , and S. S. Pari . 2019 . Body size explains interspecific variation in size–latitude relationships in geographically widespread beetle species . Ecol. Entomol . 44 : 151 – 156 . Google Scholar Crossref Search ADS Tsuchiya , Y. , Y. Takami , Y. Okuzaki , and T. Sota . 2012 . Genetic differences and phenotypic plasticity in body size between high- and low-altitude populations of the ground beetle Carabus tosanus . J. Evol. Biol . 25 : 1835 – 1842 . Google Scholar Crossref Search ADS PubMed Yom-Tov , Y. , and E. Geffen . 2011 . Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls . Biol. Rev. Camb. Philos. Soc . 86 : 531 – 541 . Google Scholar Crossref Search ADS PubMed Zeuss , D. , S. Brunzel , and R. Brandl . 2017 . Environmental drivers of voltinism and body size in insect assemblages across Europe . Glob. Ecol. Biogeogr . 26 : 154 – 165 . Google Scholar Crossref Search ADS © The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Changes in the Body Size of Carabid Beetles Along Elevational Gradients: A Multispecies Study of Between- and Within-Population Variation
JO - Environmental Entomology
DO - 10.1093/ee/nvz036
DA - 2019-06-07
UR - https://www.deepdyve.com/lp/oxford-university-press/changes-in-the-body-size-of-carabid-beetles-along-elevational-SJ3DOTwfM6
SP - 583
VL - 48
IS - 3
DP - DeepDyve
ER -