Fishes learn aversions to a nudibranch’s chemical defense

Abstract

The nudibranch Doriopsilla pharpa was rejected as food when tethered in the field and when offered to 2 species of co-occurring crabs (the lesser blue crab Callinectes similus and the mud crab Panopeus herbstii) and 2 species of co-occurring fishes (the mummichog Fundulus heteroclitus and the striped blenny Chasmodes bosquianus) in the laboratory. When the fishes were offered squid-based artificial food containing nudibranch extracts (i.e. defended food), both species initially consumed this food, but rapidly developed aversions in subsequent feedings. Although both fishes rapidly learned to reject the food, they learned using different cues. The striped blenny Chasmodes bosquianus regurgitated following the initial feeding and then avoided all food made of squid regardless of whether or not it contained the extract. In contrast, the mummichog Fundulus heteroclitus did not regurgitate, and learned to avoid only food containing the extract; it still consumed squid-based food without the extract. Thus, the mummichog detected the deterrent chemical and avoided only defended food while the striped blenny was a less effective feeder, avoiding both defended and undefended food that tasted like squid. Bioassay-guided separation using the mummichog demonstrated that the sesquiterpene polygodial was responsible for the deterrent effects of the nudibranch extract. This metabolite also resulted in the striped blenny avoiding either squid-or tunabased food treated with this metabolite. KEY WORDS: Fish behavior · Predator-prey interactions · Chemical ecology · Oyster reefResale or republication not permitted without written consent of the publisher

Escape by Inking and Secreting: Marine Molluscs Avoid Predators Through a Rich Array of Chemicals and Mechanisms

“…Some predators learn to avoid sea slugs on the basis of odor. Fish are one example, and they learn in different ways to avoid the chemically defended nudibranch Doriopsilla pharpa (Long and Hay, 2006). One fish, the mummichog Fundulus heteroclitus, learns to specifically avoid sea hares via a sesquiterpene, polygodial.…”

“…One fish, the mummichog Fundulus heteroclitus, learns to specifically avoid sea hares via a sesquiterpene, polygodial. In the study by Long and Hay (2006), mummichogs initially ate food containing this compound and learned to avoid food containing it, but they continued to eat foods initially associated with this compound (specific learned aversion). Another fish, the striped blenny Chasmodes bosquianus, also initially ate food containing polygodial and learned quickly to avoid food containing it; however, this species avoided food that was initially associated with polygodial but no longer contained it (generalized learned aversion).…”

Chemical Defenses: From Compounds to Communities

“…Some marine natural products have been studied for their toxicity to nervous systems, but few of these investigations have determined how marine consumers sense and respond to these natural products (Derby, 2007). Even less understood is how these natural products affect a consumer's ability to learn and remember in predator-prey interactions (Lindquist and Hay, 1995;Long and Hay, 2006), and ultimately how resultant behavioral changes can impact the ecology of the organism. To stimulate further research on these topics, in this section we provide neuroecological examples that relate to the natural products we have discussed.…”

TRPA1 Mediates the Noxious Effects of Natural Sesquiterpene Deterrents

“…Polygodial is also found in ferns (pteridophytes), bryophytes (liverworts) (13,14), and even in animals. Studies on Mediterranean and Pacific sea slugs have shown that these animals synthesize polygodial as a chemodefensive agent to deter predatory fish (15,16). Thus, pungent sesquiterpenes are used as chemical defense agents across plant, fungal, and animal kingdoms.…”