Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.

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Thousands of fish species belonging to the Superorder Ostariophysi possess specialized club cells in their epidermis. Damage to the cells, as would occur during a predator attack, releases chemical substances that evoke antipredator responses in nearby shoalmates. These chemical substances have often been referred to as alarm substances and the cells that release them as alarm cells. Understanding the evolution of the cells in an alarm context has been difficult. The fish needs to be captured prior to the chemicals being released, hence the benefit to the receiver is unclear. Recent studies have suggested that the club cells are part of the immune system and are maintained by natural selection owing to the benefits that they confer against pathogens, parasites, and general injury to the epidermis. In the present study, we gave fathead minnows intraperitoneal injections of cortisol, a known immunosuppressant, or injections of a control substance (corn oil). We found that fish exposed to cortisol had suppressed immune systems (as measured by a respiratory burst assay) and that they also reduced their investment in club cells. This is the best evidence to date indicating that the club cells of Ostariophysan fishes are part of the innate immune system and that the alarm function of the cells evolved secondarily. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 891–897.

Ecological theory predicts that the timing of the transition between life-history stages should vary with the costs and benefits associated with each stage. For example, the timing of hatching or metamorphosis may vary with the predation risk in each stage. Predator-induced changes in hatching time are well documented in some taxa but have not been reported in fishes. We provide the first empirical evidence that a species of fish can alter its hatching time in response to predator cues. We showed that fathead minnows, Pimephales promelas Rafinesque, 1820, exposed to chemical cues from virile crayfish, Orconectes virilis (Hagen, 1870), foraging on minnow embryos hatch sooner than those exposed to a blank control. Moreover, in the presence of cues from virile crayfish feeding on minnow embryos, the hatchlings exhibited a change in morphology because they had significantly shorter total lengths. There was a significant positive correlation between hatchling size and length of the developmental period, except in the high predation threat treatment. By hatching earlier, the fathead minnows escaped predation from virile crayfish that were actively foraging on fathead minnow eggs. Hatching at a smaller size, however, may make the fry more vulnerable to other predators.