Carbon allocation and competition maintain variation in plant root mutualisms

Abstract

Plants engage in multiple root symbioses that offer varying degrees of benefit. We asked how variation in partner quality persists using a resource-ratio model of population growth. We considered the plant's ability to preferentially allocate carbon to mutualists and competition for plant carbon between mutualist and nonmutualist symbionts. We treated carbon as two nutritionally interchangeable, but temporally separated, resources-carbon allocated indiscriminately for the construction of the symbiosis, and carbon preferentially allocated to the mutualist after symbiosis establishment and assessment. This approach demonstrated that coexistence of mutualists and nonmutualists is possible when fidelity of the plant to the mutualist and the cost of mutualism mediate resource competition. Furthermore, it allowed us to trace symbiont population dynamics given varying degrees of carbon allocation. Specifically, coexistence occurs at intermediate levels of preferential allocation. Our findings are consistent with previous empirical studies as well the application of biological market theory to plantroot symbioses.

Keywords: biological market theory; cheating; preferential allocation; resource competition; species coexistence.

Figure 1

The nonmutualist outcompetes the mutualist for construction carbon (C_*N  < C*_M) due to the cost of mutualism borne to the mutualist. The mutualist outcompetes the nonmutualist for preferentially allocated carbon (C_*M  < C*_N), due to the fidelity of the plant to the mutualist

Figure 2

Competitive dynamics of the nonmutualist and mutualist competing for construction and allocation carbon. (a) In the absence of preferential allocation of carbon (f = 0), ${\widehat{\mathrm{C}}}_{\mathit{aN}}^{\ast }={\widehat{\mathrm{C}}}_{\mathit{cN}}^{\ast }$, resulting in a zero net growth isocline (ZNGI) with a slope of −1. Similarly, ${\widehat{\mathrm{C}}}_{\mathit{aM}}^{\ast }={\widehat{\mathrm{C}}}_{\mathit{cM}}^{\ast }$, which results in a ZNGI with a slope of −1, but which is higher than the nonmutualist ZNGI because of the cost of mutualism. In this scenario, the nonmutualist will always have competitive superiority. (b) In the presence of preferential allocation, ${\widehat{\mathrm{C}}}_{\mathit{aN}}^{\ast }>{\widehat{\mathrm{C}}}_{\mathit{cN}}^{\ast }$, creating a ZNGI for the nonmutualist with a slope of $\frac{-1}{(1-f)}$. The mutualist and nonmutualist ZNGIs cross such that C_*cN < C_*cM and C_*aM < C_*aN, allowing for a condition for coexistence of mutualist and nonmutualist symbionts. Dotted lines represent consumption vectors, which are placed perpendicular to each ZNGI to indicate that allocated carbon and construction carbon are consumed in proportion to their availability