Size-structured food webs form integrated trophic systems where energy is being channelled from small to large consumers. Empirical evidence suggests that size structure prevails in aquatic ecosystems while in terrestrial food webs trophic level is largely independent of body size.Compartmentalisation 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 community-wide decline in trophic level with body mass in invertebrates and a remarkable non-linearity in community metabolism and trophic positions across all size classes. Specifically, we found that correlation between body mass and trophic level is positive in small-sized (protists, nematodes, arthropods below 1 µg in body mass), neutral in medium-sized (arthropods of 1 µg to 1 mg) and negative in 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, e.g. 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 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 is supported by a balance across individual size compartments.
1. Sympetrum fonscolombii dragonflies are believed to migrate seasonally. In the spring and early summer, the already-mature dragonflies arrive in Middle Asia for reproduction. In the late summer and autumn, summer-generation dragonflies migrate to the south. Their wintering places remain unknown. 2. Stable hydrogen (δ 2 H) and oxygen (δ 18 O) isotope analyses were conducted to confirm the migration of S. fonscolombii and determine the wintering area. Stable isotope composition of carbon (δ 13 C) and nitrogen (δ 15 N) in wings and legs was used to clarify the habitats in which dragonfly development took place. 3. Three cohorts of dragonflies collected in different regions of Middle Asia were used for analysis: (i) immigrants that arrived in the spring, (ii) residents that developed in Middle Asia, and (iii) transit dragonflies migrating to the south during autumn. 4. The average δ 2 H values in the wings were significantly higher in immigrants (−96‰) than in residents (−134‰) and transit individuals (−124‰). High δ 18 O and δ 15 N values in the tissue of immigrants confirmed their southerly origin. 5. Based on the species range and the global distribution of annual averages of δ 2 H and δ 18 O values in precipitation, the latitudinal migrations of S. fonscolombii were inferred to cover the area from the proposed natal regions of immigrants in SouthWest Asia (below ∼36 ∘ N) to Southern Ural and the south of Western Siberia in the north (54-55 ∘ N) with a maximum migration distance of more than 4000 km.
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