Experimental evidence of the importance of multitrophic structure for species persistence

Abstract

Ecological theory predicts that species interactions embedded in multitrophic networks shape the opportunities for species to persist. However, the lack of experimental support of this prediction has limited our understanding of how species interactions occurring within and across trophic levels simultaneously regulate the maintenance of biodiversity. Here, we integrate a mathematical approach and detailed experiments in plant-pollinator communities to demonstrate the need to jointly account for species interactions within and across trophic levels when estimating the ability of species to persist. Within the plant trophic level, we show that the persistence probability of plant species increases when introducing the effects of plant-pollinator interactions. Across trophic levels, we show that the persistence probabilities of both plants and pollinators exhibit idiosyncratic changes when experimentally manipulating the multitrophic structure. Importantly, these idiosyncratic effects are not recovered by traditional simulations. Our work provides tractable experimental and theoretical platforms upon which it is possible to investigate the multitrophic factors affecting species persistence in ecological communities.

Keywords: competition; mutualism; persistence; probability; species interactions.

Fig. 1.

Scheme of the two network topologies empirically evaluated. The community consisted of three plants (radish: R. raphinastrum, tomato: S. lycopersicon, field bean: V. fava) and three pollinators (bumblebees: B. terrestris, mason bees: O. bicornis, green bottle flies: L. sericata). This figure portrays the number of visits recorded as links (the thickness of the line is proportional to the link strength, i.e., number of pollinator visits) and the observed reproductive success (proportional to circle sizes). For our studied community, we constructed two network topologies of species interactions. (A) A fully nested interaction network. (B) The topology when the interaction between bumblebee and radish is experimentally prevented from the fully nested topology. Note that the thickness of links and size of nodes are different between the two topologies due to the manipulation and subsequent reorganization of the rest of the interaction strengths.

Fig. 2.

Effects of multitrophic structure within a trophic level. (A–C) A graphical representation of the community structure within the trophic level formed by plants in each of the empirical scenarios investigated: plants with no pollinators, plants with pollinators, and plants with pollinators with the bumblebee–radish interaction experimentally prevented. In the illustration, plants’ intrinsic growth rates are proportional to circle size and the strength of their interactions is proportional to thickness of arrows. Solid and dashed lines imply negative and positive interactions, respectively. (D–F) The simplex representation of the feasibility domain (the sum of intrinsic growth rates is normalized to one). The size of the feasibility domain (colored area) corresponds to the fraction of directions of intrinsic growth rates compatible with the persistence of the three species. Note that the feasibility domain is a function of the species interactions (shown in A). The solid dot corresponds to the direction of the vector of the observed intrinsic growth rates (also shown in A). Note that this simplex is the normalized projection in an $n-1$ dimensional space of the original parameter space of intrinsic growth rates. Each vertex then represents a basis vector of this parameter space, that is, $\left\{\mathrm{1,0,0}\right\}$, $\left\{\mathrm{0,1,0}\right\}$, or $\left\{\mathrm{0,0,1}\right\}$. Consequently, each vertex represents the position where one species in particular dominates the entire parameter space.

Fig. 3.

Effects of multitrophic structure across trophic levels. (A) The probability of persistence for each species estimated from a structural stability analysis. For each species we estimate the probability within each multitrophic structure: original fully nested structure (blue triangles), the in silico-manipulated structure (bumblebee–radish interaction set to zero; red squares), and the physically manipulated structure (bumblebee–radish interaction experimentally prevented from the original structure, orange circles). (B) The relative changes in persistence probability (i.e., effect) of the in silico-modified network structure (red squares), as compared with the relative changes in persistence probability of the experimentally modified network structures (orange circles) and the mean null probability expected under random interaction reorganization. Note that the in silico-modified network barely changes, while the observed experimental changes are often in opposite direction to the expected (mean) values derived from the null model.