The importance of herbivore population density in multitrophic interactions in natural and agricultural ecosystems

Summary

Multitrophic interactions are an important aspect of evolution for insects on plants, with carnivorous insects comprising a large part of plant defense against herbivores. We explore a conflict between ecological and evolutionary aspects of tritrophic interactions. We reason that, by greatly lowering the densities of herbivores, carnivorous natural enemies can thwart the opportunities for selection of resistance to herbivory. With effective natural enemies, these opportunities should be fairly rare and restricted to odd periods of herbivore outbreak.

An example of a gallmidge outbreak and consequent population decline in a genetic experiment with willow saplings illustrates this idea. At the height of the outbreak, great additive genetic variance and heritability in resistance to the midge occurred among willow genotypes. With increasing mortality from natural enemies, gall densities decreased over several midge generations, and additive variance and heritability for willow resistance to the midge decreased in kind. At lowest gall densities heritability for resistance equalled zero. Endemic densities of the midge are usually much lower than even the lowest in the experiment, so heritability for resistance in nature is normally nil. Since no plants died, no selection took place among these saplings. However, seedlings can probably suffer heavy mortality from these galls. This is an example of an interspecific genotype by environment interaction, with herbivore density being the environmental factor that influences the expression of plant genotype. Without heritability, no response to selection and no evolution of resistance can take place. Thus, carnivorous natural enemies that suppress herbivore populations can protect plants ecologically but at the same time thwart opportunities for selection of herbivore resistance.