Date Published: February 11, 2019
Publisher: Public Library of Science
Author(s): Keenan M. L. Mack, Maarten B. Eppinga, James D. Bever, Takeshi Miki.
Both ecological theory and empirical evidence suggest that negative frequency dependent feedbacks structure plant communities, but integration of these findings has been limited. Here we develop a generic model of frequency dependent feedback to analyze coexistence and invasibility in random theoretical and real communities for which frequency dependence through plant-soil feedbacks (PSFs) was determined empirically. We investigated community stability and invasibility by means of mechanistic analysis of invasion conditions and numerical simulations. We found that communities fall along a spectrum of coexistence types ranging from strict pair-wise negative feedback to strict intransitive networks. Intermediate community structures characterized by partial intransitivity may feature “keystone competitors” which disproportionately influence community stability. Real communities were characterized by stronger negative feedback and higher robustness to species loss than randomly assembled communities. Partial intransitivity became increasingly likely in more diverse communities. The results presented here theoretically explain why more diverse communities are characterized by stronger negative frequency dependent feedbacks, a pattern previously encountered in observational studies. Natural communities are more likely to be maintained by strict negative plant-soil feedback than expected by chance, but our results also show that community stability often depends on partial intransitivity. These results suggest that plant-soil feedbacks can facilitate coexistence in multi-species communities, but that these feedbacks may also initiate cascading effects on community diversity following from single-species loss.
Understanding the maintenance of biodiversity through the coexistence of apparent competitors is one of the central challenges in ecology. Ecological theory suggests that negative frequency dependent feedbacks preventing exclusion of the least fit species is a necessary requirement for coexistence [1,2]. In plant communities, such feedbacks were traditionally thought to be the result of competition for abiotic resources [3–5]. However, recent evidence suggests that biotic interactions, particularly interactions with soil micro-organisms, can generate frequency dependent negative feedback that plays an important role in plant community structure [6,7]. As a plant grows, its presence at a particular site promotes compositional shifts in the microbial community under and around it and the composition of that microbial community in turn feeds back on the growth and reproduction of that plant, its neighbors and/or the next plant to grow at that site. This particular type of frequency dependent feedback is referred to as plant-soil feedback (PSF). The analyses of PSFs have proven a useful framework for investigating how soil organisms affect plant community dynamics.
Previous analytical models show that frequency dependent feedbacks can facilitate plant coexistence in simple two-species communities [11,12,18]. The general framework presented here extends the conditions for plant coexistence mediated by frequency dependent feedbacks beyond two species. Kulmatiski et al. (2011) used a three-species plant-soil feedback model to illustrate coexistence without strict pair-wise negative feedback, but a comprehensive analysis was beyond the scope of that study. Eppinga et al. (2018) present an analytical solution to the conditions for coexistence via plant soil feedbacks in multispecies communities that identified the possibility of intransitive networks. Our theoretical analyses of multispecies communities more completely describe qualitatively new community structures that can generate species coexistence. Through intransitivity, multispecies communities can coexist when individual pairs of species would not otherwise. We found that communities structured by strict pair-wise negative feedbacks and those structured by strict intransitivity are the end points of a continuous spectrum of community coexistence types. As the richness of communities increases, more intermediate community types, which are stabilized by a combination of strict pair-wise negative feedbacks and intransitivity, become theoretically possible. We found that where a community lies on this continuum has important consequences for its stability to perturbation (Fig 6). For instance, communities completely structured by pair-wise negative feedbacks will be extremely robust to extinction since the loss of any given species will not affect the coexistence of the other species in the community (Fig 6). On the other hand, a community completely structured by intransitivity will be much more susceptible to extinction since the loss of any given species may result in a cascading extinction of competitors. We found that communities randomly assembled with greater richness were more likely to be at least partially structured through intransitivity (Fig 5), and therefore would be more vulnerable to cascading extinction events, which is consistent with previous results using a Lotka-Volterra model . As richness increases, the average dominant eigenvalue becomes less negative, meaning that strict pair-wise negative feedback becomes less and less common as the number of species in randomly assembled community increases. This could explain why we found that communities assembled from previously published feedback studies were more likely than randomly assembled communities to coexist through strict pair-wise negative feedbacks rather than intransitivity (Fig 5). Interestingly, we found that the enhanced stability of observed communities was partly due to indirect interactions, rather than more negative average pair-wise feedbacks (Fig 6A). Non-random patterns of interaction strengths, contributing to network stability has previously been identified in real food webs [52,53]. This study suggests that plant-soil feedbacks provide a similar mechanism for stability in competitive networks.