Ecosystem engineering strengthens bottom-up and weakens top-down effects via trait-mediated indirect interactions

Abstract

Trophic interactions and ecosystem engineering are ubiquitous and powerful forces structuring ecosystems, yet how these processes interact to shape natural systems is poorly understood. Moreover, trophic effects can be driven by both density- and trait-mediated interactions. Microcosm studies demonstrate that trait-mediated interactions may be as strong as density-mediated interactions, but the relative importance of these pathways at natural spatial and temporal scales is underexplored. Here, we integrate large-scale field experiments and microcosms to examine the effects of ecosystem engineering on trophic interactions while also exploring how ecological scale influences density- and trait-mediated interaction pathways. We demonstrate that (i) ecosystem engineering can shift the balance between top-down and bottom-up interactions, (ii) such effects can be driven by cryptic trait-mediated interactions, and (iii) the relative importance of density- versus trait-mediated interaction pathways can be scale dependent. Our findings reveal the complex interplay between ecosystem engineering, trophic interactions, and ecological scale in structuring natural systems.

Keywords: bottom-up effects; density-mediated indirect effects; ecosystem engineering; top-down effects; trait-mediated indirect effects.

Figure 1.

Effects of sheep grazing (control versus grazed plots) on plant community structure in large-scale experimental plots in August 2014 showing: (a–d) plant cover, (e–h) plant densities, and (i–l) plant heights for all plants combined (Total) and the three plant groups (L. chinensis, other grasses, and forbs). An asterisk (*) indicates significant differences between treatments. Error bars represent ±1 s.e.

Figure 2.

Effects of sheep grazing on (a) A. bruennichi spider density and web density (web and spider densities are equivalent), (b) Euchorthippus grasshopper density, (c) mean area and (d) mean height of A. bruennichi webs, and (e) predation successes of A. bruennichi on Euchorthippus in large-scale control and grazed plots in August 2014. An asterisk (*) indicates significant differences between treatments. Error bars represent ±1 s.e.

Figure 3.

Effects of sheep grazing and forb removal on A. bruennichi spider and Euchorthippus grasshopper behaviours and interactions in microcosm experiments in August 2014 showing: A. bruennichi (a) mean web area, (b) mean web height, and (c) per capita predation rates on Euchorthippus; and Euchorthippus (d) feeding, (e) walking, and (f) jumping frequencies. Different letters above the bars indicate significant differences among treatments. Error bars represent ±1 s.e.

Figure 4.

Community interaction web showing the effects of ecosystem engineering from sheep grazing on east-Asian steppe communities. In the absence of sheep (panel a), forbs strongly influence interactions (interaction modifications, indicated as black dashed lines) (i) between Euchorthippus grasshoppers and their host L. chinensis grass by interfering with grasshopper foraging and weakening plant–herbivore interactions (indicated as black ‘−’), and (ii) between grasshoppers and their A. bruennichi spider predators by facilitating grasshopper walking and jumping behaviours that drive grasshoppers into spider webs and strengthen predator–prey interactions (indicated as black ‘+’). In the presence of sheep (panel b with sheep effects indicated in red), selective grazing of sheep strongly reduces forb abundance and height (indicated as ‘−↓’ next to the forb group) which alters the arena for these interactions, weakening the forb's facilitative effects on predator–prey interactions and its interference effects on plant–herbivore interactions (indicated as ‘−↓’ applied to the two red dashed lines). The overall effect of ecosystem engineering by sheep is an increase in strength of bottom-up (indicated as a thicker solid line in black between L. chinensis and Euchorthippus) and decrease in strength of top-down effects (indicated as a thinner solid line in black between A. bruennichi and Euchorthippus) mediated by interaction modifications.