Consequences of plant invasions on compartmentalization and species' roles in plant-pollinator networks

Abstract

Compartmentalization-the organization of ecological interaction networks into subsets of species that do not interact with other subsets (true compartments) or interact more frequently among themselves than with other species (modules)-has been identified as a key property for the functioning, stability and evolution of ecological communities. Invasions by entomophilous invasive plants may profoundly alter the way interaction networks are compartmentalized. We analysed a comprehensive dataset of 40 paired plant-pollinator networks (invaded versus uninvaded) to test this hypothesis. We show that invasive plants have higher generalization levels with respect to their pollinators than natives. The consequences for network topology are that-rather than displacing native species from the network-plant invaders attracting pollinators into invaded modules tend to play new important topological roles (i.e. network hubs, module hubs and connectors) and cause role shifts in native species, creating larger modules that are more connected among each other. While the number of true compartments was lower in invaded compared with uninvaded networks, the effect of invasion on modularity was contingent on the study system. Interestingly, the generalization level of the invasive plants partially explains this pattern, with more generalized invaders contributing to a lower modularity. Our findings indicate that the altered interaction structure of invaded networks makes them more robust against simulated random secondary species extinctions, but more vulnerable when the typically highly connected invasive plants go extinct first. The consequences and pathways by which biological invasions alter the interaction structure of plant-pollinator communities highlighted in this study may have important dynamical and functional implications, for example, by influencing multi-species reciprocal selection regimes and coevolutionary processes.

Keywords: biological invasions of mutualistic interaction networks; exotic species; nestedness; pollination; robustness; specialization.

Figure 1.

Mean (±1 s.e.) modularity (M) of ‘uninvaded’ plant–pollinator networks and networks invaded by one or several alien plant species plotted against the seven study systems. M is a measure of the degree to which a network is organized into clearly delimited modules. ‘Uninvaded’ networks contained no aliens (16 networks) or a significantly lower proportion of alien plant species (study system 3) than ‘invaded’ networks. Information about study systems is given in the electronic supplementary material, S1a. Open circles, uninvaded; filled circles, invaded.

Figure 2.

Relationship between species generalization of the principal invader plant, measured as standardized degree (SD), and modularity (M) of invaded plant–pollinator networks.

Figure 3.

Example of the modular structure of (a) an uninvaded plant–pollinator network and (b) a network invaded by an alien plant invader (Carpobrotus affine acinaciformis; large red square). Interaction networks represent Mediterranean shrubland communities sampled at two locations at Cap de Creus, Spain (for details, see [21]). Plants are represented by squares, whereas pollinators by circles. Different colours represent different topological species' roles: peripheral species (yellow), connector (green), module hub (pink) and network hub (red).

Figure 4.

Mean (±1 s.e.) module size (i.e. the number of species forming a module) of modules of uninvaded plant–pollinator networks (n = 92), modules of invaded networks not containing alien plant species (n = 68), and modules of invaded networks containing alien plant species (n = 32).

Figure 5.

Proportion of topological species' roles in uninvaded (open circles) and invaded plant–pollinator networks (filled circles). Roles are defined according to their position in the parameter space of within-module degree z and between-module connectivity c: a network hub (z > 2.5, c > 0.62) is highly linked to species within its own module and is well connected to species of other modules, making it important for the coherence of both, its own module and the entire network; a module hub (z > 2.5, c ≤ 0.62) plays an important role within its own module while weakly connected to species of other modules; a connector (z ≤ 2.5, c > 0.62) species is important for among-module connectivity, and consequently network coherence, but plays an inferior role within its own module; a peripheral species (z ≤ 2.5, c ≤ 0.62) plays a topologically inferior role in the network [8].