R. Jan F. Smith

Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus

AbstractThe importance of chemical cues in predator-prey interactions has recently received increasing attention from ecologists. The sources of chemicals to which prey species respond often originate as cues released by the predator (reviewed by Kats and Dill, this issue). Alternatively, cues may be released by other prey animals when they detect or are attacked by a predator. Such cues, known as chemical alarm signals, are particularly common in aquatic systems. These signals provide the basis of our current review. Short-term behavioural responses of prey animals to alarm signals have received the most attention. Behavioural responses of prey resemble those exhibited to known predators, and are therefore likely to make receivers less vulnerable to predation. More recently, studies have shown that benefits to alarm signal receivers extend beyond the immediate behavioural response of nearby conspecifics over a few minutes. For example, alarm signals are important in mediating the learning of unknown pred...

Alarm signals in fishes

Summarythe evolutionary questions surrounding alarm signalling remain unresolved, but we should now have a better understanding of the elements that must be considered in the balance sheet. The amplification that may occur in alarm signalling may be a key to understanding its evolution. The benefit to receivers will often go far beyond the response of a few nearby schoolmates over a few minutes, the response that has traditionally been measured. Distant fish may receive the signal by secondary transmission, and individuals that are not even present at the time may learn about predator stimuli through cultural transmission. These effects, such as learned response to predator odour or avoidance of an area, may persist for days or much longer, and work on invertebrates implies that there may be the potential for changes in morphology and life history. Thus one signal, such as release of alarm pheromone, could alter predation risk for many individuals over long periods of time. Anything that increases the total benefit to receivers will affect the evolutionary balance sheet. Increase in number of benefits and beneficiaries of a signal will increase the likelihood that the sender will receive adequate kin-selection benefits to drive the evolution of alarm displays. Likewise, to have many individuals avoiding predation would increase the post-signal benefits, such as reduced predation in the region (Trivers, 1971), to senders that survived.Similarly, anything that decreases the cost or increases the direct benefit to the sender will favour alarm signalling. Alarm signals that do double duty as predator deterrents, or aposematic displays, and distress signals that call in mobbers or secondary predators will have lower net cost than signals that only exist to warn others. It may be common for the senders display to evolve primarily in response to direct benefits to the sender while the reaction of conspecific receivers is selected by their survival. Selection on receivers that reduces their response threshold will make signalling cheaper for the sender.The variety of life histories and biological adaptations in the fishes, combined with the potential of several different, independently evolved alarm signals should provide many avenues of approach and potential research subjects for examining the evolution of these systems.There have been many interesting effects reported in other groups of animals that may occur in fishes and which would extend both the biological interest of these systems and their generality. I have mentioned the morphological and life cycle responses found in invertebrates. Birds show deceitful alarm signalling (Munn, 1986; Moller, 1988), in which senders give false alarm calls to distract receivers from food or other resources. Audience effects occur in domestic chickens (Marler, 1986); they are more likely to give an alarm call if with a companion than when alone. Vervet monkeys assess the reliability of individual signallers and tend to ignore signals from untrustworthy individuals (Cheney and Seyfarth, 1988). Birds can acquire and transmit the identity of individual predators that prey on their species, in contrast to other individuals of the same predatory species that do not (Conover, 1987).The many effects of alarm signalling that have been documented or proposed in fishes or other organisms indicate that this phenomenon must be taken into account in any examination of foraging tactics or predator-prey interaction or any of the several areas of decision making that could be influenced by information on predation risk. Alarm signalling is probably much more widespread than was previously thought. Alarm pheromones are not just an obscure feature of the ostariophysans, although that group alone includes over 6000 species, but also occur in various forms in darters (150 species), gobies (2000 species), sculpins (300 species) and perhaps others. Distress sounds occur in over 24 families (Myrberg, 1981). Alarm calls occur in at least some holocentrids (60 species) and possibly in cods (only 55 species, but some economic value). Visual alarm signals have been reported in gobies (2000 species) and bioluminescent displays in a batrachoidid (65 species). Yet only a small fraction of fishes have been carefully examined for alarm or distress signalling. If we multiply the range of effects by the number of potential species involved, we have a subject area of some general importance in understanding the interactions between prey and predators.The prime requirement in this field, as in so many others, is for carefully designed studies, particularly in the wild, that take account of the whole suite of possible effects that may occur in alarm signalling. These studies should try to include all the participants in the system, including the predator(s), the signaller, and the various classes of receivers. They should also consider both the ultimate and proximate factors at work in each system. Very often proximate mechanisms can tell us important things about the ultimate factors that may be possible.

Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning

Individuals that live in groups may have the opportunity to learn to recognize unfamiliar predators by observing the fright responses of experienced individuals in the group. In intraspecific trials, naive fathead minnows, Pimephales promelas, gave fright responses to chemical stimuli from predatory northern pike, Esox lucius, when paired with pike-experienced conspecifics but not when paired with pike-naive conspecifics. These pike-conditioned minnows retained the fright responses to pike odour when tested alone, indicating that learning had occurred, and transmitted their fright responses to pike-naive minnows in subsequent trials. Brook stickleback, Culaea inconstans, are found in mixed-species aggregations with fathead minnows and are also vulnerable to predation by northern pike. In a series of interspecific tests, pike-naive brook stickleback gave fright responses to chemical stimuli from northern pike when paired with pike-experienced minnows but not when paired with pike-naive minnows. Pike-conditioned stickleback also retained the fright responses when tested alone and subsequently also transmitted the fright responses to pike-naive minnows. Individuals may benefit from observations of the fright responses of conspecifics or heterospecifics by (1) being alerted to the immediate presence of unfamiliar predators and (2) learning to recognize unfamiliar predators as a potential threat.

THE EVOLUTION OF CHEMICAL ALARM SIGNALS: ATTRACTING PREDATORS BENEFITS ALARM SIGNAL SENDERS

A wide variety of organisms possess damage-released alarm pheromones that evoke antipredator responses in conspecifics. Understanding the evolution of such involuntary alarm signals has been perplexing because it is difficult to see direct benefits to the sender, notwithstanding benefits derived from warning relatives. Recently, it has been proposed that the alarm pheromone, or Schreckstoff, of Ostariophysan fishes may function in a fashion analogous to distress calls of many birds and mammals. The alarm pheromone may attract secondary predators to the proximity of the primary predation event, and, once there, the secondary predators may disrupt the predation event, thus allowing the prey greater opportunity to escape. Previous findings have established that the alarm pheromone of fathead minnows (Pimephales promelas) attracts predators, including northern pike (Esox lucius) to an area. In this study we demonstrate that the probability that fathead minnows will escape after being captured by a northern pike is significantly increased through interference by a second pike. Taken with the previous findings that alarm pheromone attracts predators, these results are the first to provide empirical evidence of benefits to senders of an involuntary alarm signal.

Intraspecific and Cross‐Superorder Responses to Chemical Alarm Signals by Brook Stickleback

Fathead minnows (Pimephales promelas) and brook stickleback (Culaea inconstans) are often sympatric, occupy similar microhabitats, and share common predators. Therefore, individuals that detect alarm signals of both conspecifics and heterospecifics should gain antipredator benefits. We conducted a series of experiments to determine the extent to which these species respond to chemical alarm signals from conspecifics and heterospecifics. In laboratory experiments, brook stickleback responded to chemical stimuli from injured conspecifics with increased shoaling, but did not increase shoaling following exposure to chemical stimuli from injured swordtails (Xiphophorus helleri), an unfamiliar tropical fish that is not closely related to either stickleback or fathead minnows. These data are the first to document a chemical alarm signal for fishes in the order Gasterosteiformes. Brook stickleback also exhibited fright responses to extracts from injured fathead minnows in both laboratory and field tests. Stickleback did not exhibit a fright reaction following exposure to chemical stimuli from fathead minnows that had been treated with testosterone to decrease the concentration of alarm substance cells. This result suggests that the minnow alarm pheromone is the active component rather than some other constituent of the minnow skin extracts. In contrast to the response of the stickleback, fathead minnows did not respond to extracts from brook stickleback with a fright response. These data suggest that brook stickleback may benefit from close proximity with fathead minnows by gaining early warning of danger.

LEARNED RECOGNITION OF PREDATION RISK BY Enallagma DAMSELFLY LARVAE (ODONATA, ZYGOPTERA) ON THE BASIS OF CHEMICAL CUES

We studied two populations of damselfly larvae (Enallagma boreale): one population cooccurred with a predatory fish (northern pike, Esox lucius); the other did not. Damselflies that cooccurred with pike adopted antipredator behavior (reduced activity) in response to chemical stimuli from injured conspecifics, and to chemical stimuli from pike, relative to a distilled water control. Damselflies from an area where pike do not occur responded only to chemical stimuli from injured conspecifics. In a second set of experiments, we conditioned pike-naive damselflies to recognize and respond to chemical stimuli from pike with antipredator behavior. Damselfly larvae that were previously unresponsive to pike stimuli learned to recognize pike stimuli after a single exposure to stimuli from pike and injured damselflies or pike and injured fathead minnows (Pimephales promelas). The response to injured fathead minnows was not a general response to injured fish because damselfly larvae did not respond to chemical stimuli from injured swordtails (Xiphophorus helleri), an allopatric fish. Taken together, these data suggest a flexible learning program that allows damselfly larvae to rapidly acquire the ability to recognize local predation risk based on chemical stimuli from predators, conspecifics, and heterospecific members of their prey guild.

Differential learning rates of chemical versus visual cues of a northern pike by fathead minnows in a natural habitat

We stocked 39 juvenile pike, Esox lucius, into a previously pike free pond which contained a population of approximately 78 000 fathead minnows, Pimephales promelas. Fathead minnows sampled prior to pike stocking did not show a stereotypic fright response to either visual or chemical cues from pike. After stocking pike, we sampled minnows every two days for a period of two weeks. Minnows sampled six days after stocking still did not show a fright response to the sight of a pike, but those sampled eight days after stocking did exhibit a significant fright response, indicating that acquired predator recognition based on vision occurred between six and eight days. Minnows sampled two days after stocking did not show a fright response to chemical cues of a pike. Those sampled four days after did, however, exhibit a significant fright response, indicating that acquired predator recognition based on chemical cues occurred between two and four days. These data indicate that acquired predator recognition occurs very rapidly and that the rate of learning of predator identity differs for chemical versus visual cues.

Reactions of Gammarus lacustris to Chemical Stimuli from Natural Predators and Injured Conspecifics

We exposed the freshwater amphipod Gammarus lacustris, to chemical stimuli from injured conspecifics and to chemical stimuli from two types of natural predators: dragonfly larvae (Aeshna eremita) and northern pike (Esox lucius). Exposure to all three stimuli caused G. lacustris to reduce significantly its level of activity relative to activity recorded in response to a distilled water control. The similarity in responses to chemicals associated with predators and to injured conspecifics suggests the presence of an alarm pheromone within the body tissues of G. lacustris. In response to chemical stimuli from pike, G. lacustris tended to reduce its time in the water column and spend more time near the bottom of the test aquaria. However, no such trend was apparent in response to chemical stimuli from dragonfly larvae. The differences in response to chemical stimuli from pike and larval dragonflies suggest that G. lacustris does not have a rigid behavioral response to predation risk; instead, antipredator behavior may be modified to maximize avoidance of predators that are active in different microhabitats.

The role of experience in risk assessment: Avoidance of areas chemically labelled with fathead minnow alarm pheromone by conspecifics and heterospecifics

Abstract:In two field experiments, we investigated risk avoidance behaviour by individual fathead minnows (Pimephales promelas Rafinesque) and brook stickleback (Culaea inconstans Kirtland) in resp...

Localized defecation by pike: a response to labelling by cyprinid alarm pheromone?

Fathead minnows (Pimephales promelas) that have never encountered a predatory pike (Esox lucius), are able to detect conspecific alarm pheromone in a pikes diet if the pike has recently consumed minnows. It remains unclear how this minnow alarm pheromone is secreted by pike and if a pike is able to avoid being labelled as a potential predator by localizing these cues away from its foraging range. The first experiment determined that minnow alarm pheromone is present in pike feces when pike are fed minnows. Individual fathead minnows exhibited a fright response to a stimulus of pike feces if the pike had been fed minnows, but not if the pike had been fed swordtails, which lack alarm pheromone. Individual minnows also exhibited a fright reaction to alarm pheromone in the water (which contained no feces) housing pike which had been fed minnows, suggesting that alarm pheromone is also released in urine, mucous secretions and/or via respiration. The second experiment determined that test pike spent a significantly greater proportion of time in the “home area” of the test tanks (i.e. where they were fed) but the majority of feces were deposited in the opposite end of the test tank. By localizing their defecation away from the home or foraging area, pike may be able to counter the effects of being labelled as a predator by the alarm pheromone of the prey species.