Behaviour and neural responses in crucian carp to skin odours from cross-order species

Many teleost species respond with fright reactions to olfactory cues from injured skin of conspecifics, but they may also display responses to skin extracts of heterospecific fish. In the present study, we exposed crucian carp to skin extracts of conspecifics and three cross-order species of fish (brown trout, pike, and perch). Behavioural experiments showed that conspecific skin extracts induced fright reactions in crucian carp; extracts of brown trout induced such behaviour less frequently, while extracts of perch and pike were poor inducers of fright responses. The olfactory bulb is chemo-topically organized, and different sub-sets of neurons respond to functionally related odorants that mediate distinct behaviours. Accordingly, behavioural responses to an alarm signal should be reflected by activation of the neurons mediating fright reaction. Extracellular recordings from single units in the olfactory bulb showed that the relay neurons activated by conspecific skin extracts were also activated by extracts of brown trout, whereas extracts of perch and pike less frequently activated these units. Thus, the difference in behavioural responses matched the differences in the neural responses, indicating that skin extracts of heterospecific fish are more likely to induce fright behaviour when the responding sub-set of olfactory neurons is similar to the sub-set responding to conspecific extracts. Our results suggest that responses to injured heterospecific fish rely on chemical resemblance between odorants from heterospecific and conspecific skin, and need not be based on any form of associative learning.