Effects of Body Size, Trophic Mode and Larval Habitat on Diptera Stoichiometry: a Regional Comparison

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Effects of Body Size, Trophic Mode and Larval Habitat on Diptera Stoichiometry: a Regional Comparison Oikos 118: 615Á623, 2009 doi: 10.1111/j.1600-0706.2009.17177.x, # 2009 The Authors. Journal compilation # 2009 Oikos Subject Editor: Ulrich Brose. Accepted 29 October 2008 Effects of body size, trophic mode and larval habitat on Diptera stoichiometry: a regional comparison Peter A. Hamba¨ck, James Gilbert, Katie Schneider, Holly M. Martinson, Gundula Kolb and William F. Fagan P. A. Hamba¨ck ([email protected]) and G. Kolb, Dept of Botany, Stockholm Univ., SEÁ106 91 Stockholm, Sweden. Á J. Gilbert, K. Schneider, H. M. Martinson and W. F. Fagan, Dept of Biology, Univ. of Maryland, College Park, MD 20742, USA. Ecological stoichiometry has emerged as a tool for exploring nutrient demand and evolutionary responses to nutrient limitation. Previous studies of insects have found predictable variability in stoichiometry, both in relation to body size and trophic mode, at ordinal levels or higher. Our study further examines the evolutionary and ecological lability in these traits by comparing the effects of body size, trophic mode (larval and adult) and larval habitat on the stoichiometry of insects within one order (Diptera). The study also expands on previous work by analyzing trophic mode both at coarse (detritivore, herbivore, predator) and fine (high- vs low- nutrient quality resources within trophic categories) scales and by comparing nutrient stoichiometry in two geographical regions, Sweden and Arizona. As predicted, adults feeding on nectar or pollen had the lowest body N content in the dataset. Additionally, for Diptera with predatory larvae, species low N diets had lower body N content than those with high N diets. However, body N content was not consistently lower for all species with low N resources, as species feeding on plant material were indistinguishable in stoichiometry from predators with high N diets. We suggest that these results emerge because larval resource exploitation is poorly understood in herbivorous Diptera species. Body P content for Swedish Diptera decreased with body size for all trophic modes, and the only difference among trophic modes was that blood feeders had higher P content than other groups. The regional comparison further showed that the allometry of body P content is a labile trait that may vary at regional scales, as there was no allometric scaling of body P content in the Arizona data set, in contrast to the Swedish data set. These results are not easily explained by existing theoretical frameworks, but instead point to a general context-dependence of P stoichiometry, which should now be a focus for future work. A foundation of ecological stoichiometry is that organisms individuals with a high N demand (Elser et al. 2000a, should evolve to adjust their nutrient demands to the Jaenike and Markow 2003, Boersma and Elser 2006). availability of limiting nutrients (Elser et al. 2000c, Second, smaller species, irrespective of trophic mode, Baudouin-Cornu et al. 2001, Sterner and Elser 2002, Frost appear to have a higher body P content than larger species et al. 2005, Kay et al. 2005), suggesting that relative (Woods et al. 2004), presumably because the higher growth nutrient demands can be explored by comparing chemical rate in smaller species puts a higher demand on P-rich composition across taxa (Berendse 1994). Such compar- ribosomal RNA (Elser et al. 2003, Vrede et al. 2004, Kay isons have a long history in aquatic and marine sciences, but et al. 2005, Gillooly et al. 2005). have only recently been explored among terrestrial insects Previous analyses of terrestrial insects have mainly been (Markow et al. 1999, Fagan et al. 2002, Jaenike and performed on literature data consisting of fortuitous Markow 2003, Schade et al. 2003, Woods et al. 2004, collections from a multitude of spatial locations and biomes Davidson 2005, Martinson et al. 2008). Though these (but see Fagan and Denno 2004, Woods et al. 2004). As a studies suggest that the pattern is perhaps more complex on result, not all insect groups are equally represented, or land, they also show that ecological stoichiometry indeed represented in sufficient numbers for more detailed ana- seems able to explain large-scale variability in the chemical lyses. Consequently, comparisons have only been possible composition of terrestrial insects. First, a broad pattern across broad taxonomic groupings (ordinal levels or higher) appearing from previous analyses of published data on the and only few studies (Jaenike and Markow 2003, Bertram nitrogen (N) content of insects suggests that herbivores have et al. 2008) have examined variation in both body N and P a lower body N content than predators (Fagan et al. 2002). content for terrestrial insects at lower taxonomic levels. This lower body N content of herbivorous insects is Strong selective pressures should have consistent effects suggested to occur because feeding on a less nitrogen-rich across all phylogenetic levels; however, highly related species food source, such as most plant tissue, has selected against are much less independent than anciently diverged orders. 615 Hence, examining the same general patterns within an Sommaggio 1999, Oosterbroek 2006). In a few cases, we insect order is a more conservative test of the evolutionary excluded specimens where the diet information was not significance of ecological stoichiometry. We therefore seek resolved or reliable at the level of identification. This was to characterize the extent to which stoichiometric signals in encountered particularly in the Muscidae and related trophic level, body size, and phylogeny persist even among families, both because they often show large variability closely related taxa. Moreover, we may also expect large among species in diet and because they are, at times, differences among sites or biomes in stoichiometric com- difficult to identify to species. We also pooled nectar and position, due to differences in nutrient availability, season- pollen feeders (hereafter floral feeders), due to lack of more ality, and subsequent growth rate limitations (Watts et al. specific information. For each species, we recorded the dry 2006). For instance, Daphnia has higher body P content in body mass (mg) and quantified body C, N and P content. regions with a shorter growing season and a concomitant For a few species we had limited specimens to analyze all stronger selection for higher growth rate (Elser et al. 2000b, three nutrients, and then substituted a specimen from a Woods et al. 2003). Such spatial variability, however, closely related and ecologically similar species. In all cases, cannot be tested in compiled databases for terrestrial insects specimens were starved overnight prior to analysis to because taxa have not been collected along large environ- minimize diluting effects of gut contents (Fagan et al. mental gradients. 2002). In total, the dataset of Swedish Diptera includes In this study, we help fill this important gap by (larval trophic mode) 50 predator/parasite, 13 herbivore, comparing the elemental composition among taxa within and 41 detritivore species, or (adult trophic mode) 49 floral the insect order Diptera (flies) between the moist temperate feeders, 16 detritivores, 4 blood feeders, 16 predators and region of southern Sweden (new data) and the dry desert of 15 species that are believed not to feed as adults. The Arizona (data from Woods et al. 2004). We focus on comparative dataset of Woods et al. (2004) from the Diptera for three reasons: 1) because of the large variability Sonoran Desert was classified only by larval trophic mode in trophic mode among Diptera families, both among and included only larval detritivores (8) and predators (11) larvae (including predators, parasites, herbivores, and species. detritivores) and adults (including nectar feeders, blood Our analysis suggested a weak association of larval feeders, predators and detritivores): 2) because the order trophic mode with adult body N content (Results), in includes both terrestrial and aquatic species: and 3) because contrast to previous studies. Because this trophic signal may extensive laboratory studies on Drosophila have well- have been obscured by large variation in resource stoichio- characterized the relationship between stoichiometry and metry within trophic categories, we subdivided the predator growth (Markow et al. 1999, Jaenike and Markow 2003, and detritivore groups for the N-analysis based on more Watts et al. 2006). As descriptors of trophic mode we use specific diet information (fine trophic mode). A similar both larval diet, as the diet during this stage is most closely subdivision of herbivore species was not possible due to a connected to individual growth rates, and adult diet, as this low sample size and because diets were quite similar among is the stage that is assayed for stoichiometry. Using the species. Adult trophic modes were not further subdivided. Swedish data set, we examined the variation in N and P Species with predatory larvae were subdivided into two content with body size, between main trophic modes, and fine trophic modes, based on the average N content of their between larval habitats (terrestrial vs aquatic). For N alone, main food items. The group of predators feeding on a low we subdivided each main trophic mode to investigate N diet included species attacking aphids (6.6% N; further the relationship between species’ body N and the Syrphidae and Chloropidae), leafhoppers (9.3% N; Pipun- N content of their main food items. All analyses were culidae) and isopods (7.1% N; Rhinophoridae). These prey performed within a phylogenetic framework using the latest items are N-poor when compared with the average body N Diptera supertree (Yeates et al. 2006). The Arizona data set content of arthropods, at 10.5% (data from Fagan et al. is smaller and only contains information on P content. 2002, Martinson et al. 2008). The predator group with a Hence, in the comparison between geographic data sets, we high N diet included species feeding primarily on insect only examined the allometric and trophic mode variation larvae, gastropods (10Á11% N; Sciomyzidae), lumbricids on P content.
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