Herbivory and plant species coexistence: Community regulation by an outbreaking phytophagous insect

Most general theories proposed to explain the trophic structure of communities ignore the possibility that insect outbreaks can severely damage vegetation and reduce the abundance of dominant plant species over vast areas. Specialist chrysomelid beetles can irrupt and defoliate goldenrods (Solidago spp.), a group of widespread, long-lived, herbaceous perennials. We examined the long-term effects (10 yr) of suppressing insects, using insecticide in replicated plots on the structure and diversity of an old field dominated by the goldenrod, Solidago altissima. An outbreak of the chrysomelid beetle, Microrhopala vittata, that specializes on S. altissima, occurred during the experiment and persisted several years. Damage caused by this outbreak dramatically reduced the biomass, density, height, survivorship, and reproduction of S. altissima. Herbivore exclusion caused the formation of dense stands of goldenrods with a twofold increase in both standing crop biomass and litter. The understory in these dense stands had significantly lower plant abundance, species richness, flowering shoot production, and light levels; these conditions persisted for years following the outbreak. Thus, M. vittata functioned as a keystone species. Furthermore, insect herbivory indirectly increased the abundance of invading trees, thereby increasing the rate of succession, by speeding the transition of this old field to a tree-dominated stage. We conducted two follow-up experiments to test the hypothesis that insects altered community dynamics by their indirect effect on Litter accumulation and light availability in the understory. In the first experiment, we tied back the canopy to increase light into the understory and removed litter in both the insecticide-treated and control plots. We found little effect of removing Litter. By contrast, increasing understory light levels significantly increased understory forb abundance and species richness. In the second experiment, we placed rosettes of Hieracium pratense, the dominant understory forb, under nine levels of shade cloth, ranging from 95% shade to full sun. Flowering-shoot production was a linear function of light availability (r(2) = 0.92; P < 0.0001). We concluded that insect herbivores indirectly promoted plant species richness and coexistence, primarily by augmenting light availability to suppressed understory species. Insect herbivory may often play a strong role in goldenrod stands, because outbreaks will likely occur at least once, if not more, during the period when goldenrods are dominant. Furthermore, our findings provide compelling evidence for two general mechanisms whereby insect herbivory promotes plant species diversity and coexistence. The first mechanism operates during outbreaks when insects act as keystone species. The second mechanism can operate at less than outbreak levels and occurs whenever insect damage augments light to a sufficient degree to enhance the fecundity of suppressed nonhost species. If this increase in fecundity increases recruitment of subordinate species, then insect herbivory will promote plant species coexistence and diversity. Our data suggest that there is a continuum in the influence of insect herbivory on plant communities from the more subtle, but important, effects of herbivory on the fecundity of nonhost species to the devastating influence of outbreaks. Also, our results demonstrate that long-term experiments are required to elucidate the role of insect herbivores. Finally, we propose that insect outbreaks are common enough in many community types, particularly forests, to warrant explicit consideration in theories of trophic regulation, particularly in terrestrial communities inhabited by long-lived plant species.