Mixed messages across multiple trophic levels: the ecology of bark beetle chemical communication systems

Summary. Chemical, physiological and behavioral components of pheromone communication have been described for a number of bark beetle species, yet our understanding of how these signals function under natural conditions remains relatively limited. Development of ecologically based models is complicated by the multiple functions and sources of variability inherent in bark beetle semiochemistry. This discussion addresses four ecological issues of chemical signaling in bark beetles: the effects of aggregation on individual fitness, the possibility of cheating, how plants can defend themselves against herbivores that employ aggregation pheromones, and the implications of variability in chemical communication systems to predator avoidance. An analysis of published data from thirteen scolytid – conifer systems indicates that the net benefit and optimal colonization density vary with host condition and beetle species. When beetles attack live trees, the benefit of cooperative host procurement exceeds losses due to competition for the limited substrate, at least up to moderate densities. When beetles colonize dead tissue, however, the effect of subsequently arriving beetles on initial colonizers is almost entirely negative. This suggests that aggregation originated as exploitation of senders, but evolved into manipulation of receivers. It is also proposed that the optimal colonization density which typifies each species or population may offer a more objective and less value–laden index of behavior than current labels such as “aggressiveness”. Beetles can maximize the relative benefits of group attack by incorporating instantaneous measures of host resistance into their colonization behavior, and by adjusting oviposition with colonization density. This system may provide opportunities for cheating. However a number of factors may select against a fixed strategy of cheating, including the linkage between tree allelochemistry and beetle semiochemistry, the reduced quality of substrate available to late arrivers, the short adult lifespans of most bark beetles, differential exposure to some predators, the difficulty of locating signalers during extensive endemic periods, and the low costs incurred during host assessment. However, the possibility that beetles employ flexible, density – dependent strategies deserves heightened attention. The ability of bark beetles to collectively exhaust host defenses poses a particular problem for plant defense. It is argued here that the ideal defense should include both direct resistance mechanisms against invading beetles, and indirect mechanisms that inhibit chemical communication. Evidence for the latter mechanism is explored. The ability of predators to efficiently exploit aggregation pheromones as kairomones in prey finding poses significant risk to bark beetles. It is proposed that minor alterations in pheromone components may provide colonizers with partial escape from such natural enemies while maintaining intraspecific functionality. Traditional interpretations emphasized the fidelity and consistency of pheromones, but under natural conditions chemical signals are modified by unpredictable features of the biotic and abiotic environment. Although we typically view variation in pheromonal signals as experimental noise or simple deviations from a population norm, such variation may reflect evolutionary dynamics. Complex ecological interactions may impose trade-offs between the clarity versus diversity of their signals. Received 3 July 2000; accepted 8 January 2001