Rooting theories of plant community ecology in microbial interactions

Abstract

Predominant frameworks for understanding plant ecology have an aboveground bias that neglects soil micro-organisms. This is inconsistent with recent work illustrating the importance of soil microbes in terrestrial ecology. Microbial effects have been incorporated into plant community dynamics using ideas of niche modification and plant-soil community feedbacks. Here, we expand and integrate qualitative conceptual models of plant niche and feedback to explore implications of microbial interactions for understanding plant community ecology. At the same time we review the empirical evidence for these processes. We also consider common mycorrhizal networks, and propose that these are best interpreted within the feedback framework. Finally, we apply our integrated model of niche and feedback to understanding plant coexistence, monodominance and invasion ecology.

Figure I

(a) Methods used to study plant-soil community feedbacks include two-phase conditioning experiments; (b) planting seedlings at varying distances from trees, and (c) observations of seedling size-distributions in mixed species forests.

Figure I

Examples of monodominant invasive and EcM plants: invasive Pinus contorta (lodgepole pine, left) and Ulex europaeus (common gorse, middle) in New Zealand, and the tropical monodominant Dicymbe corymbosum (right) in Guyana. Photo credits: P. contorta: I. Dickie, Ulex europaeus: D. Peltzer, Dicymbe corymbosum: Krista McGuire.

Figure 1

Soil microbes and resource partitioning. In (a) and (b), the levels of phosphorus (P) and nitrogen (N) required for persistence are represented by the thick colored lines for a blue (solid) and orange (dashed) species of plant. (a) represents the advantage conferred to the orange species through association with an arbuscular mycorrhizal (AM) fungus that increases access to soil P, which could confer competitive superiority to the orange species in the absence of costs. If the association with the AM fungus comes at a cost in N, then this trade-off could allow coexistence of a mycorrhizal plant species (orange) with a non-mycorrhizal plant species (blue) under a range of nutrient supply points (b). The orange (dashed) and blue (solid) arrows represent the rate of consumption of the two resources of the orange and blue species, respectively. (c) presents a hypothetical example of resource partitioning among two Eucalyptus tree species mediated by specific associations with two different species of ectomycorrhizal fungi with differential access to organic and inorganic pools of N.

Figure 2

Soil community feedback. (a) presents a conceptual representation of soil community feedback (modified from[49]). The presence of plant A can cause a change in the composition of the soil community, represented by S_A. This change in the soil community can directly alter the population growth rate of species A (represented by α_A) and it can alter the growth rate (α_B) of competing plant species B (with negative effect represented by the club symbol). Similarly, the presence of plant B can cause a change in the composition of the soil community (S_B) which can directly feed back (β_B) on the population growth rate of plant B or indirectly feed back on the growth rate of plant B through changes in the growth rate (β_A) of competing plant A. The net effect of soil community dynamics on plant species coexistence is determined by the sign and magnitude of an interaction coefficient = α_A− α_B− β_A+ β_B, which represents the net pairwise feedback[49]. (b) and (c) depict the direct negative feedback due to accumulation of pathogenic Pythium sp., as has been observed in Prunus serotina (black cherry) trees in North American forests[62]. The P. serotina seedling (b) exhibits chlorosis likely resulting from infection with Pythium sp. (c) depicts roots infected with Pythium sp. This direct negative feedback could contribute to coexistence with competing tree species when the deleterious effects of Pythium sp. are host-specific. (d) presents net pairwise negative feedback between Panicum sphaerocarpon and Plantago lanceolata generated by changes in composition of AM fungi[53]. Thickness of arrows represent the relative strengths of benefit between individual species of plants and AM fungi. Scutellospora calospora has high fitness with Plantago, but Plantago doesn't grow well with Sc. calospora. Rather, Plantago has highest growth rates in association with AM fungi, Archaeospora trappei and Acaulospora morrowiae, which themselves have high fitness in association with Panicum. The asymmetric fitness relationships generate negative feedback which can contribute to coexistence of these competing plant species. Spores of the AM fungi, Ar.trappei, Ac. morrowiae and Sc. calospora, are depicted. Photos of P. serotina seedling is credited to A. Packer, and roots and fungi are credited to J. Bever.

Figure 3

(a) represents microbially-mediated resource partitioning where plant A has greater access to resource 1 through association with symbiont X (similar to Figure 1b) while (b) represents microbially-mediated resource partitioning with plants host-specific symbionts which differentially access soil resources (similar to Figure 1c). In both of these scenarios, the dynamics of plant A will be determined by the product of the stabilizing effects of the resource partitioning and the destabilizing effects of the positive feedback. (c) represents the stabilizing effect of negative feedback with the destabilizing effect of microbially-mediated competitive dominance.