Moby-bass: suction feeding by predators limits direct release of alarm cues in fishes

Chemical alarm cues alert aquatic prey to the presence of an actively foraging predator. There is a large literature based upon responses to alarm cues derived from skin extract because it is anticipated that prey skin is damaged when prey are attacked by a predator. However, many predators feed by suction feeding whereby prey are quickly drawn into the buccal cavity and swallowed whole with little, if any, direct contact between the teeth of the predator and the skin of the prey. Here, we test if predation by suction feeding releases chemical information in sufficient quantity to elicit an antipredator response in conspecific prey. In tests of individual zebrafish Danio rerio, we found that odor of crushed zebrafish produced a clear antipredator behavioral response, but water collected immediately adjacent to staged predation events between a largemouth bass Micropterus salmoides (122-145 mm TL) and adult zebrafish (39 mm TL) did not elicit alarm behavior and did not differ from behavioral responses to blank water or bass odor (on a diet of earthworms). In a second experiment, zebrafish were swallowed by largemouth bass and then retrieved seconds later through gastric lavage, which produced zebrafish that were alive and completely intact with minimal epidermal damage. Published relationships between bass length, gape size, and the geometry of suction feeding suggest that in a hypothetical population of largemouth bass feeding on adult zebrafish or fathead minnows, the majority of predation events by piscivorous fish probably would not release detectable levels of prey alarm cue. Accounting for the role of feeding mechanics by fish predators requires a recalibration of the literature on risk assessment by small prey fishes. Chemically mediated antipredator behaviors against suction-feeding predators may occur primarily via post-ingestion dietary cues or disturbance cues released near the moment of attack. Significance statement Skin extract is commonly used to simulate predation and experimentally manipulate the perception of predation risk because it is generally assumed that epidermal tissue is damaged during predation. The resulting chemicals released by damaged skin induce nearby prey to engage in antipredator behavior. This study attempted to demonstrate behavioral responses to alarm cue released during staged predation events but was unable to do so, likely because of the mode of ingestion by the predator-suction feeding. Prey retrieved by gastric lavage from the gut of predators immediately after ingestion confirmed that the epidermis is largely intact when prey are swallowed by suction feeding. Because most fish predators employ suction feeding, this study calls for a recalibration of how chemical cues mediate predator-prey interactions in aquatic ecosystems. Release of alarm cues by fish predation cannot be assumed to occur in most cases. Chemical labeling by dietary cues or disturbance cues likely plays a larger role than previously appreciated for acquired predator recognition.

Automated summary

This study investigates whether predation by suction feeding releases enough chemical information to trigger an anti-predator response in prey. The results show that there is no detectable alarm behavior-inducing substance in the water surrounding the predation events between zebrafish and largemouth bass. Additionally, prey retrieved through gastric lavage after being swallowed intact by the bass confirms that the prey's skin remains largely intact during suction feeding. Therefore, this study calls for a recalibration of how chemical cues mediate predator-prey interactions in aquatic ecosystems.