Plastic response to a proxy cue of predation risk when direct cues are unreliable

Responses to proximate cues that directly affect fitness or cues directly released by selective agents are well-documented forms of phenotypic plasticity. For example, to reduce predation risk, prey change phenotype in response to light level (e.g., moon phase) when light affects predation risk from visual predators, and to chemical cues (kairomones) released by predators. Less well understood is the potential for organisms to perceive predation risk through "proxy cues": proximate cues that correlate with, but do not directly affect predation risk. Previous field studies indicate that body and spine length of an invasive cladoceran in Lake Michigan, Bythotrephes longimanus (the spiny water flea), increase during the growing season, coincident with a decrease in clutch size. Although the cause of seasonal trait changes is not known, changes are associated with warmer water temperature and increased predation risk from gape-limited fish (i.e., fish whose ability to consume Bythotrephes is limited by mouth size). Using a laboratory experiment, we found no effect of fish (Perca flavescens) kairomones on Bythotrephes morphology or life history. In contrast, higher water temperature led to longer absolute spine and body length, increased investment in morphological defense of offspring (measured as the ratio of spine-to-body length), and decreased clutch size and age at reproduction. These plastic responses are unlikely to be adaptive to temperature per se, but rather our findings indicate that temperature serves as a proxy cue of fish predation risk. Temperature correlates with risk of gape-limited fish predation due to growth of fish from larval stages incapable of consuming Bythotrephes early in the season, to larger sizes by midseason increasingly capable of consuming Bythotrephes, but limited by gape size to consuming smaller individuals. We argue that for Bythotrephes, temperature is a more reliable cue of predation risk than fish kairomones, because fish kairomones are present throughout the season due to continual presence of non-gape-limited adult fish, to which plastic response would have little effect. Organisms may, therefore, not only respond to changes in an environmental factor because the factor directly affects risk, but also when the environmental factor serves as a proxy signaling change in predation risk.