Outbreaks of Colony-Forming Pests in Tri-Trophic Systems: Consequences for Pest Control and the Evolution of Pesticide Resistance

Abstract

Ironically, pesticide applications in agriculture may result in the opposite of the intended reduction of the pest population. Following an initial treatment, the target population may resurge rapidly to greater than pre-treatment levels. In addition, populations of non-target species that were previously far below economic thresholds may increase greatly after applications and develop into pests of economic importance. Pesticide-induced outbreaks have been reported for very different groups of phytophagous arthropods and for several types of pesticides (Ripper 1956, Barbosa and Schultz 1987, Penman and Chapman 1988, Roush and Tabashnik 1990). This raises the question whether there are general principles underlying these outbreaks. One explanation for pesticide-induced outbreaks is that, for reasons rooted in their evolutionary past, phytophagous pest species are less susceptible to pesticides than their natural enemies. Hence, pesticide treatment will have a more drastic effect on natural enemies than on pests, resulting in outbreaks. However, this explanation ignores population dynamical effects on predator-prey balances. Furthermore, measurements of susceptibility to direct pesticide doses reveal that natural enemies are generally not more vulnerable to pesticides than their prey species (Hoy 1990) and may even show a trend towards lower predator susceptibility (Croft and Brown 1975). Thus, empirical support is lacking and (as we argue below) there is no good reason to expect that predatory arthropods would have been exposed to a narrower range of toxicants than their prey. A more sound explanation follows from consideration of the coupled population dynamics of predator and prey (May 1985, May and Dobson 1986). After pesticide application the densities of phytophagous arthropods are reduced. As soon as the harmful effects of the pesticide abate, conditions are favourable for herbivores: they suffer less predation and possibly experience reduced competition. Hence the numbers of pests and potential secondary pests will increase at a rate close to their maximum growth rate. Even if natural enemy densities are not directly affected, their densities will decrease after pesticide application since they are largely deprived of their main or only food source: phytophagous arthropods. Populations of predators can only increase after prey have attained sufficiently high densities. The increase in predator numbers therefore typically lags behind that of the pests. By the time the predators have returned to the pre-application densities, the pest populations have had the opportunity to increase unchecked for some time. The importance of food limitation to differential rates of recovery after pesticide application has been confirmed in a number of simulation studies (Tabashnik 1986 and 1990); even when the immediate mortality is similar for predator and prey, predator populations are more severely suppressed by pesticides than are pest populations (Waage et al. 1985). Pesticide induced outbreaks are often considered as transient events (Ripper 1956); after pesticide use is stopped, the ecosystem is expected to recover and predatorprey balances to restore. However, this need not be the case. Persistent outbreaks can result from the simultaneous existence of two stable states; one in which the predator controls the pest, and another in which the predator exists at very low levels, or is absent, and the pest is not controlled. After a small disturbance the system will return to its original state. For larger disturbances, however, the system may stabilize at either state, depending