The sea lamprey, Petromyzon marinus, exhibits a spectacular alarm response to the odor emitted from decayed conspecifics that may differ substantially in function from the well-characterized system in ostariophysan fishes. Here, we report a series of three laboratory experiments designed to characterize the behavioral responses of migratory-phase lampreys to a set of odors derived from conspecific and heterospecific tissues, determine whether sex or sexual maturation alters these responses, and ascertain if the putative alarm substance derives from a particular region of the body. A number of the findings were consistent with the prevailing predator-avoidance paradigm for fish alarm substances released from the skin after predator attack in that: (1) dilute odors derived from freshly ground skin were highly repellent; (2) the substance is contained in the organism early in life; (3) the odor derived from a close relative was avoided whereas those of a distant relative were not; and (4) upon sexual maturity female response to the alarm substance was attenuated. Two interesting patterns arose that differed substantially from the prevailing paradigm: (1) conspecific odors remained repellent after 96 h of aerobic decay; and (2) the cue was emitted from multiple areas of the body, not just the skin, and the repellency of the odor derived from any tissue increased in accordance with its mass. A persistent cue emitted from several sources suggests a broader ecological function than the detection and avoidance of a predator.

Establishing how invasive animals perceive and manage the threat of predation improves our understanding of why certain species rapidly invade unfamiliar environs where others do not. The threat-sensitive response hypothesis predicts that prey that modulate their antipredator behavior in response to the perceived intensity of the threat will have a selective advantage. We investigated the behavioral and olfactory antipredator responses of migrating invasive sea lamprey to varying concentrations of a conspecific alarm cue in the laboratory and field. We hypothesized the odor indicates the presence and location of predation risk on river shorelines, allowing sea lamprey to either alter their migratory path and/or movement timing to reduce exposure to the predator. Migratory sea lampreys exhibited threat-sensitivity in space-use both in the laboratory and nature by increasingly avoiding areas as the concentration of alarm cue increased when safe space was available (areas without the alarm cue). The intensity of the avoidance at higher concentrations was greater in the field. Electrophysiological recordings from the olfactory organ confirmed a concomitant increase in signal output to the olfactory bulb of the brain when exposed to increased alarm cue concentrations. However, increasing the alarm cue concentration did not alter the animal’s motivation to move upstream in either avoidable risk or unavoidable risk scenarios. Exposure to alarm cue affected decisions regarding how to move, but not whether to move. Knowledge of how the animal uses the cue in nature reveals ways to use the cue to manipulate movement and achieve conservation goals.

The detection of predation risk without direct engagement with a predator is an important driver of prey movement strategies. Consequently, the application of alarm cues may prove an effective tool in guiding the movements of fishes targeted for control or conservation. However, failure to contemplate the sensory, physiological and cognitive outcomes of repeated or persistent exposure to the cue will likely lead to poor performance of management practices. Using a series of behavioural tests and physiological recordings from the olfactory organ, we examined the timing of onset and recovery of the alarm response in sea lamprey (Petromyzon marinus L.) when exposed continuously or sporadically to its alarm cue. In the laboratory, sea lamprey exhibited short-term, reversible attenuation of the alarm response over 2–4 h with continuous exposure. The alarm response spontaneously recovered after 30–60 min of removal from the cue. In long-duration free-swimming tests, where the animals were allowed to move into and out of the odour plume volitionally, repeated but sporadic encounter with the alarm cue over 5 h did not alter the alarm response. Electro-olfactogram recordings from the main olfactory epithelium indicated that olfactory sensory neurons quickly adapt to alarm cue and recovered within 15 min. Our findings strongly implicate habituation as the mechanism that induces reduction in the alarm response and provide insight into the design of effective management practices that seek to use fish alarm cues as repellents.