Size compartmentalization of energy channeling in terrestrial belowground food webs

Abstract

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.

Feeding habits and multifunctional classification of soil‐associated consumers from protists to vertebrates

“…The full classification is more complex and includes 148 trophic groups (see Table S1). Even at this more detailed resolution, trophic groups were often characterised by feeding on several resources, emphasising the prevalence of multichannel feeding in soil consumers (Scheu & Setälä, 2002;Digel et al, 2014;Wolkovich, 2016;Potapov et al, 2021b) (Fig. 1) and contrasting with traditional soil food-web reconstructions with distinct resource-based energy channels (Hunt et al, 1987;de Ruiter, Neutel & Moore, 1994).…”

Multifunctionality of belowground food webs: resource, size and spatial energy channels

“…Even though my reconstruction did not include biomasses, it recovered several expected patterns in the ratios of secondary to primary energy fluxes (S/P) based solely on feeding interaction strengths. For example, top-down control was higher (larger S/P ratios) in microand meso-than in macro-food webs (Potapov et al, 2019b(Potapov et al, , 2021b and it was higher for plant-based than for soil-based energy channels (Fig. 7A,B).…”

“…(4) Size classes of soil consumers Consumers, from protists to large invertebrates, may span from few micrometres to dozens of centimetres in body length and over 12 orders of magnitude in body mass in a single soil community (Mulder et al, 2008;Potapov et al, 2021b). Body size is a very general trait that affects a number of organism characteristics including metabolism, growth rate and trophic interaction partners among others (Brown et al, 2004;Woodward et al, 2005).…”

“…(B) Multichannel reconstruction captures widespread generalism in resource preferences with resource-based energy channels being to a large extent reticulated (Digel et al, 2014;Wolkovich, 2016) and consumers being clustered also in body size and spatial energy channels (Potapov et al, 2021b). plantations increases the plant energy channel in soil food webs (Klarner et al, 2017;Susanti et al, 2019) and reduces the bacterial, but not the fungal, energy channel (Susanti et al, 2019).…”

“…This functional complexity calls for a holistic approach to describing soil communities across consumers of different body sizes, similar to the size spectrum approach commonly used in marine ecosystems (Blanchard et al, 2017). There have been several conceptual and empirical attempts to apply the size spectrum approach to terrestrial belowground communities (Mulder, 2006;Petchey & Belgrano, 2010;Turnbull, George & Lindo, 2014), but they provide only simplified information because terrestrial food webs have more complex size structures than marine ones (Potapov et al, 2019a(Potapov et al, , 2021b. The food-web framework is, however, a promising way of describing the functioning of terrestrial food webs because it unites the functional, biodiversity and stability aspects of biological systems (Hines et al, 2015;Barnes et al, 2018).…”