Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems

Biological control strategies that were developed for orchards and forests have had limited success in controlling pests in annual crop systems (ACSs). In this paper I will argue that an accurate characterization of the habitat template of ACSs will be a key feature for developing new strategies of biological control for field crops. I argue that ACSs are "predictably ephemeral" habitats that present a selective environment that is different from that commonly envisioned for disturbed or early successional habitats. By drawing on examples from natural ecosystems that are predictably ephemeral, I characterize the types of life cycles and life-history traits that are common in insects, that thrive in these types of environments. "Fugitive" or "colonizing" species that evolve in unpredictably disturbed environments usually allocate resources to numerous dormant or vagile propagules at the expense of parental survival. In contrast, many insects that exploit predictably ephemeral habitats respond to disturbance by dispersing to permanent refugia where they delay reproduction, overwinter, and then recolonize the following year. I refer to this strategy as "cyclic colonization" and document its ubiquity in natural and agroecosystems. Cyclic colonizers typically exhibit between-generation developmental flexibility in life-history traits. In many species, "establishment generations" have small or no wings, are behaviorally sedentary, grow rapidly, reproduce at an early age, and have high fecundities. In contrast, "over-wintering generations" are well adapted for dispersal to and from permanent habitats (long wings, behavioral tendency for flight, reproductively immature) and for winter survival. Cyclic colonizers are not, necessarily "r-selected", but rather have generations that alternate between relatively r- and K-selected life-history traits. Cyclic colonization explicitly relies on spatial heterogeneity, and therefore, effective biological control strategies in ACSs must include a landscape ethic that provides an abundance of permanent habitats that can act as reservoirs for indigenous and introduced enemies. The development of an optimal agricultural landscape for biological control in ACSs will require a metapopulation approach that focuses on annual cycles of colonization between permanent refugia and a patchwork of crop fields. Finally, given the ubiquity of cyclic colonization in ACSs, it seems that effective biological control will depend on an increased information base about the seasonal cycles, dispersal behavior, and overwintering ecology of indigenous and introduced natural enemies.