Species coexistence through simultaneous fluctuation-dependent mechanisms

Abstract

Understanding the origins and maintenance of biodiversity remains one of biology's grand challenges. From theory and observational evidence, we know that variability in environmental conditions through time is likely critical to the coexistence of competing species. Nevertheless, experimental tests of fluctuation-driven coexistence are rare and have typically focused on just one of two potential mechanisms, the temporal storage effect, to the neglect of the theoretically equally plausible mechanism known as relative nonlinearity of competition. We combined experiments and simulations in a system of nectar yeasts to quantify the relative contribution of the two mechanisms to coexistence. Resource competition models parameterized from single-species assays predicted the outcomes of mixed-culture competition experiments with 83% accuracy. Model simulations revealed that both mechanisms have measurable effects on coexistence and that relative nonlinearity can be equal or greater in magnitude to the temporal storage effect. In addition, we show that their effect on coexistence can be both antagonistic and complementary. These results falsify the common assumption that relative nonlinearity is of negligible importance, and in doing so reveal the importance of testing coexistence mechanisms in combination.

Keywords: coexistence; environmental variability; relative nonlinearity; resource competition; storage effect.

Fig. 1.

Least-squares best fits of Monod growth functions in response to the availability of amino acids for the four focal nectar yeast species at low (Top), medium (Middle), and high (Bottom) osmotic pressure (10%, 30%, and 50% sucrose). Horizontal dashed lines represent the effective continuous mortality rate corresponding to an 80% instantaneous mortality event every 48 h, as implemented in the model simulations and competition experiments (Materials and Methods).

Fig. 2.

Simulations of resource competition between M. reukaufii (blue) and M. koreensis (light orange) at constant sucrose concentrations of 10% (A), 30% (B), and 50% (C) and fluctuating every 2 d between sucrose concentrations of 10% (white bars) and 50% (gray bars) (D).

Fig. 3.

Contribution of the storage effect ($\mathrm{\Delta }I$) and relative nonlinearity ($\mathrm{\Delta }N$) to the growth rate ($h{r}^{-1}$) of each species as an invader ($r_{inv}$) in pairwise competition, where $r_{inv}$ = average fitness differences + $\mathrm{\Delta }I$ + $\mathrm{\Delta }N$. (A) Pairs where coexistence is predicted because $r_{inv}>0$ for both species. In the case of M. koreensis (Mk) and M. reukaufii (Mr), $r_{inv}$ would be negative for M. koreensis without the contribution of $\mathrm{\Delta }N$, and negative for M. reukaufii without the contribution of $\mathrm{\Delta }I$. In the case of S. bombicola (Sb) and M. gruessii (Mg), M. gruessii would still have $r_{inv}>0$ without either mechanism, while persistence of S. bombicola requires one or both mechanisms. (B) Pairs where coexistence is not predicted because one species has $r_{inv}<0$. In all pairs, $\mathrm{\Delta }I$ is weak to nonexistent, while $\mathrm{\Delta }N$ is strongly equalizing (i.e., differences in $r_{inv}>0$ would be much larger without the contribution of $\mathrm{\Delta }N$).

Fig. 4.

Mixed (solid lines) and monoculture (dashed lines) times series for M. reukaufii (blue) and M. koreensis (light orange) at constant 10% (A and E), 30% (B and F), and 50% (C and G) and fluctuating 10–50% (D and H) sucrose. The fluctuating treatment was replicated in an additional eight microcosms (SI Appendix, Fig. S12).