Embryonic antipredator defenses and behavioral carryover effects in the fathead minnow (Pimephales promelas)

Abstract

Most research on embryonic learning and behavior in aquatic vertebrates has focused on fitness benefits after hatching, but the ability of embryos to perceive and respond to environmental stimuli may also have immediate adaptive value. Here, we examined whether fathead minnow embryos, Pimephales promelas, detect and respond to cues indicative of predation risk, and whether the embryonic environment influences behavior after hatching. We compared the behavior of 5-day-old post-fertilization (dpf) embryos reared in the presence or absence of olfactory alarm cue, alone or in combination with the cues of a piscivorous predator (Bluegill sunfish, Lepomis macrochirus). Next, we reared larvae from the embryonic treatments to 21 dpf and tested them in two antipredator behavioral assays reflecting differences in the degree of immediate risk (predator avoidance vs attack evasion). Embryos that developed under perceived high-risk conditions exhibited reduced activity compared to those from low-risk environments. Larvae from high-risk environments also showed enhanced antipredator behavior, and evidence for embryonic predator learning. These data provide new insight into the learning capabilities and antipredator behaviors of aquatic vertebrate embryos.

Significance statement

Predators can have a dramatic influence on the fitness of individuals at all life stages, including before birth. During early development, as at other life stages, selection should favor the ability of individuals to perceive external cues indicative of predation and adjust their behavior appropriately. We reared embryos in the presence or absence of olfactory predation cues and observed behavior before and after hatching. Embryos from perceived ‘high-predation’ environments showed less-conspicuous behavior before and after hatching compared to those from ‘predation-free’ environments, suggesting that fish perceive, recognize, and respond to external risk cues before hatching—not just after, as is commonly shown. Embryos learned to identify a predator before hatching, but after hatching embryonic experience primarily affected behavior during the predator recognition and assessment stages of the predator–prey interaction, rather than during predator escape.