ABSTRACT
Forest canopy is densely populated by phyto-, sapro-, and microbiphages, as well as predators and parasitoids. Eventually, many of crown inhabitants fall down, forming so-called 'arthropod rain'. Although arthropod rain can be an important food source for litter-dwelling predators and saprophages, its origin and composition remains unexplored. We measured stable isotope composition of the arthropod rain in a temperate mixed forest throughout the growing season. Invertebrates forming arthropod rain were on average depleted in 13C and 15N by 1.6 and 2.7, respectively, compared to the soil-dwelling animals. This difference can be used to detect the contribution of the arthropod rain to detrital food webs. Low average δ13C and δ15N values of the arthropod rain were primarily driven by the presence of wingless microhytophages, represented mainly by Collembola and Psocoptera, and macrophytophages, mainly aphids, caterpillars, and heteropterans. Winged arthropods were enriched in heavy isotopes relative to wingless specimens, being similar in the isotopic composition to soil-dwelling invertebrates. Moreover, there was no consistent difference in δ13C and δ15N values between saprophages and predators among winged insects, suggesting that winged insects in the arthropod rain represented a random assemblage of specimens originating in different biotopes, and are tightly linked to soil food webs.
ABSTRACT
Size-structured food webs form integrated trophic systems where energy is channeled from small to large consumers. Empirical evidence suggests that size structure prevails in aquatic ecosystems, whereas in terrestrial food webs trophic position is largely independent of body size. Compartmentalization of energy channeling according to size classes of consumers was suggested as a mechanism that underpins functioning and stability of terrestrial food webs including those belowground, but their structure has not been empirically assessed across the whole size spectrum. Here we used stable isotope analysis and metabolic regressions to describe size structure and energy use in eight belowground communities with consumers spanning 12 orders of magnitude in living body mass, from protists to earthworms. We showed a negative correlation between trophic position and body mass in invertebrate communities and a remarkable nonlinearity in community metabolism and trophic positions across all size classes. Specifically, we found that the correlation between body mass and trophic level is positive in the small-sized (protists, nematodes, arthropods below 1 µg in body mass), neutral in the medium-sized (arthropods of 1 µg to 1 mg), and negative in the large-sized consumers (large arthropods, earthworms), suggesting that these groups form compartments with different trophic organization. Based on this pattern, we propose a concept of belowground food webs being composed of (1) size-structured micro-food web driving fast energy channeling and nutrient release, for example in microbial loop; (2) arthropod macro-food web with no clear correlation between body size and trophic level, hosting soil arthropod diversity and subsidizing aboveground predators; and (3) "trophic whales," sequestering energy in their large bodies and restricting its propagation to higher trophic levels in belowground food webs. The three size compartments are based on a similar set of basal resources, but contribute to different ecosystem-level functions and respond differently to variations in climate, soil characteristics and land use. We suggest that the widely used vision of resource-based energy channeling in belowground food webs can be complemented with size-based energy channeling, where ecosystem multifunctionality, biodiversity, and stability are supported by a balance across individual size compartments.
