The Population Biology of Parasite-Induced Changes in Host Behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes adn Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for Ro, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasiteinduced changes in host behavior tend to increase Ro and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles. This contrasts with the case for a direct life cycle parasite where parasite-induced reductions in host fecundity and asexual reproduction are always destabilizing. The Consequences of these different patterns of dynamic interaction are discussed in terms of the evolution of complex life cycles in parasitic helminths and the intensity with which modification of host behavior should be expressed in different habitats. Although the available data tend to support the conclusions of the models, the whole area would benefit considerably from futher detailed field studies of specific parasite-host systems.