Loss of functional diversity and network modularity in introduced plant-fungal symbioses

Abstract

The introduction of alien plants into a new range can result in the loss of co-evolved symbiotic organisms, such as mycorrhizal fungi, that are essential for normal plant physiological functions. Prior studies of mycorrhizal associations in alien plants have tended to focus on individual plant species on a case-by-case basis. This approach limits broad scale understanding of functional shifts and changes in interaction network structure that may occur following introduction. Here we use two extensive datasets of plant-fungal interactions derived from fungal sporocarp observations and recorded plant hosts in two island archipelago nations: New Zealand (NZ) and the United Kingdom (UK). We found that the NZ dataset shows a lower functional diversity of fungal hyphal foraging strategies in mycorrhiza of alien as compared with native trees. Across species this resulted in fungal foraging strategies associated with alien trees being much more variable in functional composition compared with native trees, which had a strikingly similar functional composition. The UK data showed no functional difference in fungal associates of alien and native plant genera. Notwithstanding this, both the NZ and UK data showed a substantial difference in interaction network structure of alien trees compared with native trees. In both cases, fungal associates of native trees showed strong modularity, while fungal associates of alien trees generally integrated into a single large module. The results suggest a lower functional diversity (in one dataset) and a simplification of network structure (in both) as a result of introduction, potentially driven by either limited symbiont co-introductions or disruption of habitat as a driver of specificity due to nursery conditions, planting, or plant edaphic-niche expansion. Recognizing these shifts in function and network structure has important implications for plant invasions and facilitation of secondary invasions via shared mutualist populations.

Keywords: Bipartite interaction networks; ectomycorrhizal symbiosis; foraging strategies; functional traits; invasion ecology; network modularity; second-genome; soil ecology..

Figure 1

Functional composition of ectomycorrhizal fungal exploration types on native and alien tree genera in New Zealand by tree genus. Native genera names labelled in blue, aliens in red. Four alien tree genera with fewer than eight observations were excluded from functional analysis.

Figure 2

Multivariate visualization of functional similarity of fungal communities on native (blue) and alien (red) tree genera in New Zealand, based on data presented in Figure 1. The native genera Kunzea and Leptospermum overlap. Native tree genera had functionally similar communities of associated fungi, while alien tree genera had widely variable functional composition.

Figure 3

Functional composition of ectomycorrhizal fungal exploration types on native and alien tree genera in the UK by tree genus. Native genera names labelled in blue, aliens in red.

Figure 4

Multivariate visualization of functional similarity of fungal communities on native (blue) and alien (red) tree genera in the UK based on data presented in Figure 2.

Figure 5

Interaction network of tree genera and ectomycorrhizal fungi in New Zealand (left) and the UK (right), showing plant–plant modules by the colour of the vertex. Native plant genera are indicated by circles, alien plants by squares, labelled with the first three letters of the genus except in the UK network, where PiS = Pinus sylvestris, and PiX = alien Pinus spp. Each link represents a fungal species either linking plant species or forming a self–self link (loops), with link width proportional to the square root of the number of observations (scaled 1/10th in the UK network compared with NZ network). The colour of the links indicates fungal-fungal modules (not discussed).