Partner choice in ectomycorrhizal mutualism.

Abstract

Mycorrhizae are a mutualism between fungi and plants, where fungi transfer nutrients to plants and plants provide photosynthate to the fungi. I addressed mechanisms that structure mycorrhizal fungal community along a light-intensity gradient, and the consequence of the community structure to plant growth. I hypothesized that, in each light environment plants choose the species composition of fungi that maximizes their growth. First I formalized this 'plant choice' hypothesis in an economics model, where maximizing fitness requires that plants equalize marginal costs of trading with different species of fungi. If this occurs, and the carbon payment that fungi require for nutrient delivery increases disproportionately with increasing amounts of nutrient delivered, then plant choice fosters fungal coexistence, structures fungal communities, and changes fungal community structure with changing light availability. Second, I tested five predictions of the plant choice hypothesis, using the association between <italic>Abies balsamea</italic> seedlings and two co-dominant species of ectomycorrhizal fungi (<italic>Cenococcum</italic> sp. and <italic>Lactarius</italic> sp). (1) Fungal community structure should be correlated with, and caused by light availability to the plant. (2) Plant should be colonized by a non-random light-dependent subset of available fungi. (3) Mycorrhizal fungi should negatively interact with each other. (4) Plants should not choose mycorrhizal fungi that act as parasites. (5) Plant should associate with the fungi that support the highest plant growth. Predictions 1--3 were supported: (1) <italic>Cenococcum</italic> relative abundance significantly decreased, and <italic>Lactarius</italic> relative abundance significantly increased in response to increasing light availability in field surveys and experiments. (2) Relative abundance of <italic>Cenococcum</italic> on the seedlings did not reflect <italic>Cenococcum </italic> availability in the soil, and <italic>Cenococcum</italic> was over-represented on shaded seedlings. (3) In a controlled experiment, the presence of <italic> Lactarius</italic> strongly inhibited <italic>Cenococcum</italic> colonization of unshaded seedlings. However, predictions 4--5 were strongly rejected: <italic>Cenococcum </italic> behaved as a parasite when in high abundance, and <italic>Lactarius </italic>-dominated seedlings had below average growth in high light where <italic> Lactarius</italic> was the dominant fungus. Therefore, plant choice was rejected as the dominant fungal community-structuring mechanism, because the composition of fungal community was not optimal for plant growth. Instead, I hypothesize that the fungal community is structured by fungal competition.