Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

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.

Olfactory assessment of predation risk in the aquatic environment

The aquatic environment is well suited for the transmission of chemical information. Aquatic animals have evolved highly sensitive receptors for detecting these cues. Here, I review behavioural evidence for the use of chemical cues by aquatic animals for the assessment of predation risk. Chemical cues are released during detection, attack, capture and ingestion of prey. The nature of the cue released depends on the stage of the predation sequence in which cues are released. Predator odours, disturbance pheromones, injury–released chemical cues and dietary cues all convey chemical information to prey. Prey use these cues to minimize their probability of being taken on to the next stage of the sequence. The evolution of specialized epidermal alarm substance cells in fishes in the superorder Ostariophysi represent an amplification of this general phenomenon. These cells carry a significant metabolic cost. The cost is offset by the fitness benefit of the chemical attraction of predators. Attempts of piracy by secondary predators interrupt predation events allowing prey an opportunity for escape. In conclusion, chemical cues are widely used by aquatic prey for risk assessment and this has resulted in the evolution of specialized structures among some taxa.

The ventral adhesive disc of the clingfish Gobiesox maeandricus: integumental structure and adhesive mechanisms

Light microscopy and scanning and transmission electron microscopy of the ventral adhesive disc of the northern clingfish, Gobiesox maeandricus, demonstrate that two distinct types of epidermis are present on the disc surface. Most of the disc is covered with cuboidal epithelium in which four cell types can be distinguished: acidophil cells, mucous cells, epithelial cells, and "alarm substance" cells. The surfaces of the epithelial cells feature whorled microridges typical of teleost epidermis. Near the margin of the disc, on the lateral fin rays, and in discrete raised patches inside the disc are papillae of stratified columnar epithelium. The surface cells of these papillae are microvillous and secrete a noncellular cuticle which is firmly anchored to the microvillous surface of the papillae. The cuticle is not adhesive. It contains keratin-like proteins but no mucins or mucoproteins are demonstrable histochemically. Connective tissue layers and muscle underlying the epidermis of the disc are arranged to provide structural integrity and shock absorption while allowing some flexibility to the disc and papillae. The adhesive force generated by the disc was demonstrated using a pressure transducer. Negative pressure decays over time and is periodically renewed by the fish. Thus suction is largely maintained passively and the disc's seal is subject to some leakage. The fish can also actively apply suction pressure when agitated but fatigues and cannot sustain high negative pressures for long. The epidermal papillae, coupled with the fish's ability to flex the disc, represent an additional gripping mechanism for irregular surfaces. The papillary surface cuticle apparently acts as an abrasion-resistant, frictional surface.

Epidermal club cells are not linked with an alarm response in reedfish, Erpetoichthys (= Calamoichthys) calabaricus

Club cells in the epidermis of reedfish, Erpetoichthys (= Calamoichthys) calabaricus (Pisces, Polypteriformes), are morphologically similar, perhaps homologous, to the "alarm substance cells" found in the skin of cypriniform fishes. Cypriniforms perform a fright reaction when they detect chemicals released from the damaged alarm substance cells of conspecifics. We examined the response of reedfish to conspecific skin extract and checked for a cross reaction to reedfish extract by a cypriniform fish, the zebra danio, Brachydanio rerio. Reedfish responded to conspecific skin extract with an increase in activity but this response did not resemble a fright reaction. Zebra danios responded to reedfish extract with a feeding response. We conclude that reedfish do not show a fright reaction to the skin extract of conspecifics. This suggests that if cypriniform alarm substance cells are homologous to reedfish club cells, their alarm pheromone function is a secondary adaptation.

Effect of hormone treatments on alarm substance cell counts in the pearl dace, Semotilus margarita

The seasonal loss of alarm substance cells that normally occurs in breeding male and female pearl dace, Semotilus margarita, could not be induced by treatment with androgen, estrogen, salmon gonadotropin, or prolactin. Treatment with carp pituitary did lead to a significant reduction in alarm substance cell numbers. Androgen treatment induced changes in tuberculation and mucous cell counts. Salmon gonadotropin and carp pituitary increased breeding colouration. Prolactin treatment increased mucous cell counts. The lack of response of pearl dace alarm substance cells to androgen contrasts with the situation in fathead minnows, Pimephales promelas, where seasonal alarm substance cell loss is under androgen control. The difference may reflect differences in the annual cycle of secondary sexual characteristics.