In 1938, the Austrian ethologist Karl von Frisch made his first report on the existence of the chemical alarm signal known as Schreckstoff (fright substance) in minnows. An alarm signal is a response produced by an individual, the "sender", reacting to a hazard that warns other animals, the receivers, of danger. This chemical alarm signal is released only when the sender incurs mechanical damage, such as when it has been caught by a predator, and is detected by the olfactory system. When this signal reaches the receivers, they perceive a greater predation risk and exhibit an antipredator response. Since populations of fish exhibiting this trait survive more successfully, the trait is maintained via natural selection. While the evolution of this signal was once a topic of great debate, recent evidence suggests schreckstoff evolved as a defense against environmental stressors such as pathogens, parasites, and UVB radiation and that it was later co-opted by predators and prey as a chemical signal.
Background Chemical alarm systems have been identified in a number of different taxa, including gastropods, echinoderms, amphibians and fishes. One of the most well-studied chemical alarm signals is schreckstoff, the use of which is widespread in the superorder Ostariophysi (e.g., minnows, characins, catfishes, etc.). About 64% of all freshwater fish species and 27% of all fish species worldwide are found in the ostariophysan superorder, which highlights the widespread use and importance of this chemical alarm system in fishes.
Schreckstoff in ostariophysans The production of schreckstoff has been shown to be metabolically expensive and is therefore part of a conditional strategy that can only be employed by individuals with access to sufficient resources. One putative active ingredient in schreckstoff is hypoxanthine-3N-oxide (H3NO), which may be produced in club cells which will henceforth be referred to as "alarm substance cells". The nitrogen oxide functional group was found to be the main chemical trigger of antipredator behavior in receivers. Schreckstoff is a mixture, and fragments of a glycosaminoglycan, chondroitin sulfate, are able to trigger fear responses. The precursor polysaccharide is a component of mucus, and fragments are proposed to be produced during injury. Like schreckstoff obtained from skin extract, chondroitin sulfate activates a subset of olfactory sensory neurons. Production of and responses to schreckstoff change over the course of ontogeny. For example, young brook sticklebacks (Culaea inconstans) are more likely to be caught in minnow traps that have been baited with conspecific skin extracts than adults. This result indicates young brook sticklebacks do not make the association between schreckstoff and the potential presence of a predator as readily as adults. Whether this association strengthens over time as a result of learning or physiological development remains unclear. In addition to changes across ontogeny, the degree to which schreckstoff is produced varies within the breeding season. Male fathead minnows (Pimephales promelas) cease production of schreckstoff during the breeding season, but still exhibit antipredator behaviors in response to schreckstoff during this time. Schreckstoff production may be halted at this time because male fathead minnows often incur mechanical damage while building their nests. It would be detrimental to a male to produce schreckstoff while building a nest, as it would inadvertently repel females, thereby decreasing the likelihood of obtaining a mate. By ceasing schreckstoff production during the breeding season, males circumvent this problem. The cessation of alarm substance cell production appears to be controlled by androgens.
Hypotheses for the evolution of schreckstoff A number of different hypotheses have been proposed for the evolution of schreckstoff. The first hypothesis is that the evolution of schreckstoff has been driven by kin selection. Support for this hypothesis would include evidence that individuals live in groups of closely related kin and that the release of chemical alarm signals increases the likelihood that related individuals will avoid predation. The second hypothesis, predator attraction, suggests the release of schreckstoff may attract additional predators which will interfere with the predation event, increasing the likelihood that the prey will escape and survive the attack. This hypothesis assumes predators will be attracted to schreckstoff and will interfere with one another either through competition for the captured prey or through predation of one another. It additionally assumes, despite the fact that the prey has already incurred mechanical damage, it is possible for the prey to escape and recover from the attack. Testing and validating these assumptions would provide support for the predator attraction hypothesis. The third hypothesis proposes that schreckstoff has an immune function, providing protection against pathogens, parasites and/or UVB radiation. For this hypothesis to be supported, a correlation between alarm substance cell production and the presence of pathogens and parasites would need to be observed. Direct evidence that schreckstoff inhibits the growth of aquatic pathogens and parasites would provide additional support for the immunity hypothesis. Another hypothesis is that schreckstoff is a breakdown product of mucus and club cells, induced by injury. Selection for the alarm response is primarily at the level of the receiver.
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