Ecological plasticity governs ecosystem services in multilayer networks

Abstract

Agriculture is under pressure to achieve sustainable development goals for biodiversity and ecosystem services. Services in agro-ecosystems are typically driven by key species, and changes in the community composition and species abundance can have multifaceted effects. Assessment of individual services overlooks co-variance between different, but related, services coupled by a common group of species. This partial view ignores how effects propagate through an ecosystem. We conduct an analysis of 374 agricultural multilayer networks of two related services of weed seed regulation and gastropod mollusc predation delivered by carabid beetles. We found that weed seed regulation increased with the herbivore predation interaction frequency, computed from the network of trophic links between carabids and weed seeds in the herbivore layer. Weed seed regulation and herbivore interaction frequencies declined as the interaction frequencies between carabids and molluscs in the carnivore layer increased. This suggests that carabids can switch to gastropod predation with community change, and that link turnover rewires the herbivore and carnivore network layers affecting seed regulation. Our study reveals that ecosystem services are governed by ecological plasticity in structurally complex, multi-layer networks. Sustainable management therefore needs to go beyond the autecological approaches to ecosystem services that predominate, particularly in agriculture.

Fig. 1. Hive plots of carabid, weed and gastropod mollusc networks.

a The ‘composite network’ encompassing all species and their interactions across all the multilayer networks from all sites used in this study. Carabid (black circles), weed (green circles) and gastropod mollusc (red circles) species nodes are sized proportionally to their rank of how often they were found across all networks. Link colour indicates the herbivore (green) and carnivore (red) layers, with the colour intensity and thickness being proportional to the strength of the interaction across all networks. b Example networks selected to show the trade-off between the number of links to the weeds and to the gastropods. The images of the beetle, weed seeds and molluscs are reproduced under the standard royalty free licence of 123rf.com (vectorgalaxy © 123RF.com; Patrick Guenette © 123RF.com; yod67 © 123RF.com; Autt Khamkhaunchan © 123RF.com).

Fig. 2. Weed seed regulation increases with herbivory interaction frequency.

The level of weed regulation in relation to the log of the summed herbivory predation interaction frequency in each network for: (a) total weed regulation; (b) monocotyledon weed regulation; and, (c) dicotyledon weed regulation. Solid lines in (a), (b) and (c) are regressions from GLMMs (Methods, Table S1). The dotted line at 0 indicates the threshold where weed seedbanks decline between t₀ and t₁.

Fig. 3. Trade-offs between herbivory and carnivory links.

a The relationship between the sum of specialist herbivory frequency interaction frequency and sum of specialist carnivory interaction frequency, transformed to the log(x + 0.5) scale, for each network. The line shown represents a LOESS smoother with dashed standard errors. b The number of links to weeds and gastropods for the omnivore carabid nodes within each network. The line shown is a regression fitted using a GLMM (“Methods”, Table S1). c The estimated link turnover between networks across the herbivore/carnivore gradient using Bray–Curtis dissimilarity.

Fig. 4. Link plasticity among carabid species.

Density plot showing the relationship between the number of herbivore and carnivore links across all networks. Each blue-shaded square indicates the instances that an omnivore carabid had a particular number of links to gastropods and to weeds, with the depth of the blue shading indicating the frequency of observation across all networks, scaled between 0 and 1000. Some networks contained carabids acting as pure herbivores or carnivores in the networks, but most contained omnivores. A filled, black circle is used to denote the link composition observed in different networks for the most common carabid species, Pterostichus melanarius, which in some networks appeared as either an herbivore (having links only to weeds) or a carnivore (having links only to gastropods), but more often acted as a flexible omnivore.