Why fruit rots: theoretical support for Janzen's theory of microbe-macrobe competition

Abstract

We present a formal model of Janzen's influential theory that competition for resources between microbes and vertebrates causes microbes to be selected to make these resources unpalatable to vertebrates. That is, fruit rots, seeds mould and meat spoils, in part, because microbes gain a selective advantage if they can alter the properties of these resources to avoid losing the resources to vertebrate consumers. A previous model had failed to find circumstances in which such a costly spoilage trait could flourish; here, we present a simple analytic model of a general situation where costly microbial spoilage is selected and persists. We argue that the key difference between the two models lies in their treatments of microbial dispersal. If microbial dispersal is sufficiently spatially constrained that different resource items can have differing microbial communities, then spoilage will be selected; however, if microbial dispersal has a strong homogenizing effect on the microbial community then spoilage will not be selected. We suspect that both regimes will exist in the natural world, and suggest how future empirical studies could explore the influence of microbial dispersal on spoilage.

Keywords: carrion; competition; frugivory; fungus; metapopulations; yeast.

Figure 1.

The equilibrium numbers of fruits containing no microbial organisms (empty, E), or a colony of spoiling microorganisms (S) or a colony of non-spoilers (N), as a function of the parameter controlling the rate at which empty patches can be colonized by spoilers (c_S). The parameters c_N and e_N governing non-spoilers are both held at unity throughout. The four panels explore two levels of the remaining two parameters (the rate at which empty patches are introduced to the system Q, and the extinction rate of patches with spoilers on them e_S) in a factorial arrangement.