Damage-released Alarm Cues Research Articles

A field test of the “graveyard hypothesis” reveals avoidance of chemical but not visual cues in Bahamian queen conch (Aliger gigas)

Queen conch (Aliger gigas) are large gastropod molluscs harvested for their meat, shells, and pearls and as they are generally easy to collect by hand, they are vulnerable to overfishing. In The Bahamas, fishers often clean (or “knock”) their catch and dispose of the shells away from collection sites, forming midden heaps or “graveyards”. Although queen conch are motile and found throughout shallow water habitats, live animals are rarely observed in the vicinity of middens, giving rise to a common belief that conch actively avoid graveyards, possibly by moving offshore. Here, we experimentally evaluated avoidance behaviours of queen conch to chemical (tissue homogenate) and visual (shells) cues indicative of harvesting activity using replicated aggregations of six size-selected small (< 14 cm shell length) and large (> 14 cm) conch at Eleuthera Island. Large conch were consistently more likely to move, and to move farther, than small conch, independent of treatment. Small conch, however, demonstrated greater occurrence of movement in response to chemical cues vs seawater controls, while conch of both sizes demonstrated equivocal responses to visual cues. Collectively, these observations suggest that more economically desirable large conch may be less vulnerable to capture during successive harvest events than smaller juveniles due to their greater propensity to move, and that chemical cues consistent with damage-released alarm cues may play a greater role in eliciting avoidance behaviour than the visual cues typically associated with queen conch graveyards. Data AvailabilityData and R code are archived and freely available at Open Science Framework (https://osf.io/x8t7p/; DOI: 10.17605/OSF.IO/X8T7P).

Behavioural responses to con- and heterospecific alarm cues by an alien and a coexisting native fish

The monkey goby Neogobius fluviatilis is an invasive Ponto-Caspian fish that enters habitats of the native gudgeon Gobio gobio in European freshwaters, likely belonging to the same prey guild. Their abilities to detect and avoid predation have been poorly understood, although these traits may contribute to the competitive advantage and drive the invasion success of the goby. We tested intra- and interspecific responses of fish from sympatric populations to damage-released alarm cues (skin extract) in laboratory. Both species of fish responded to conspecific and heterospecific cues, but their responses to conspecifics were more diverse (changed social distancing among individuals, reduced vertical and horizontal movement) than those elicited by heterospecifics (changed social distancing only). Moreover, the fish differed in their anti-predation behaviour: the gudgeon increased whilst the monkey goby decreased inter-individual distances and only the gudgeon exhibited thigmotaxis and reduced mobility in response to the conspecific cues. Interspecific differences show that the species exhibit distant anti-predation strategies. This might be associated with their phylogenetic distance and/or higher differentiation of their ecological niches than commonly assumed. Besides, our results suggest that alien species be included in the interspecific exchange of information in local fish assemblages.

Does donor group size matter? The response of guppies (Poecilia reticulata) and convict cichlids (Amatitlania nigrofasciata) to disturbance cues from conspecific and heterospecific donors

Prey are under immense pressure to make context-specific, behavioural decisions. Prey use public information to reduce the costs associated with making inappropriate decisions. Chemical cues are commonly used by aquatic vertebrates to assess local threats and facilitate behavioural decision making. Previous studies on chemosensory assessment of risk have largely focused on damage-released alarm cues, with the cues released by disturbed or stressed prey (i.e., disturbance cues) receiving less attention. Disturbance cues are “early-warning signals” common among aquatic vertebrates that may warn conspecific and heterospecific prey guild members of potential risk. Initially, we conducted a series of laboratory studies to determine (i) if guppies (Poecilia reticulata Peters, 1859) produce and respond to disturbance cues and (ii) if relative concentration (donor group size) determines response intensity. Secondly, we examined if guppies and convict cichlids (Amatitlania nigrofasciata (Günther, 1867)) show similar response patterns to their own vs. heterospecific disturbance cues. Our results suggest that guppies exhibit increased predator avoidance behaviour to conspecific disturbance cues (relative to water from undisturbed conspecifics) and increased donor group size lead to stronger antipredator responses. However, although guppies and cichlids respond to each other’s disturbance cues, we found no effect of donor group size towards heterospecific disturbance cues. Our results suggest that disturbance cues are not generalized cues and present a degree of species-specificity.

Better the devil you know? How familiarity and kinship affect prey responses to disturbance cues

Prey can greatly improve their odds of surviving predator encounters by eavesdropping on conspecific risk cues, but the reliability of these cues depends on both previous accuracy as well as the cue's relevance. During a predator chase, aquatic prey release chemical disturbance cues that may vary in their reliability depending on the individuals receiving them. Thus, prey may rely differentially on disturbance cues from familiar individuals (due to previous experience) or from kin (due to their relatedness). We examined the responses of wood frog (Lithobates sylvaticus) tadpoles to disturbance cues from familiar versus unfamiliar conspecifics and kin versus non-kin. In accordance with our prediction, tadpoles responded differently to disturbance cues from familiar versus unfamiliar conspecifics. Tadpoles receiving disturbance cues from unfamiliar individuals displayed a fright response, whereas tadpoles ignored disturbance cues from familiar individuals. Tadpoles may have habituated to familiar cues since they were unaccompanied by a true threat, hence rendering these cues functionally unreliable. Tadpoles responded similarly to disturbance cues from related and unrelated individuals suggesting they were similarly reliable and this mirrors the matching reliability of prey responses to damage-released alarm cues from kin and non-kin. Our findings shed light on a seldom-studied chemical communication system in aquatic prey.

Field verification of chondroitin sulfate as a putative component of chemical alarm cue in wild populations of fathead minnows (Pimephales promelas)

Chemical characterization of damage-released alarm cues in ostariophysan fishes has lagged far behind the study of the ecological role that these cues play in behavioral decision-making of prey fishes. Chondroitin sulfate has been identified as a putative component of alarm cue based on two laboratory studies of zebrafish, Danio rerio, and the northern studfish, Fundulus catenatus. The fathead minnow, Pimephales promelas, is a model organism in the study of chemically mediated predator–prey interactions, in part because they can be studied in the laboratory and under field conditions. Here, we conducted a field experiment on wild populations of fathead minnows, to test for area avoidance of chondroitin sulfate relative to conspecific skin extract (containing alarm cues = positive control) or water (negative control). We repeated the experiment in two small lakes in central Minnesota using minnow traps containing blocks of sponge with one of the three test cues. We found that fathead minnows avoided traps chemically labeled with conspecific alarm cue more than control traps labeled with water, and that the number of minnows caught in traps labeled with chondroitin sulfate was intermediate between alarm cue traps and water traps. These data are consistent with laboratory findings that chondroitin sulfate is a component of alarm cue, but that other species-specific compounds are needed for a full behavioral response.

Migratory-stage sea lamprey Petromyzon marinus stop responding to conspecific damage-released alarm cues after 4 h of continuous exposure in laboratory conditions.

This study investigated the length of avoidance response of migratory-stage sea lamprey Petromyzon marinus exposed continuously to conspecific damage-released alarm cues for varying lengths of time in laboratory stream channels. Ten replicate groups of P. marinus, separated by sex, were exposed to either deionized water control or to P. marinus extract for 0, 2 or 4 h continuously. Petromyzon marinus maintained their avoidance response to the conspecific damage-released alarm cue after continuous exposure to the alarm cue for 0 and 2 h but not 4 h. Beyond being one of the first studies in regards to sensory-olfactory adaptation-acclimation of fishes to alarm cues of any kind, these results have important implications for use of conspecific alarm cues in P. marinus control. For example, continuous application of conspecific alarm cue during the day, when P. marinus are inactive and hiding, may result in sensory adaptation to the odour by nightfall when they migrate upstream.

Habituation of adult sea lamprey repeatedly exposed to damage-released alarm and predator cues

Predation is an unforgiving selective pressure affecting the life history, morphology and behaviour of prey organisms. Selection should favour organisms that have the ability to correctly assess the information content of alarm cues. This study investigated whether adult sea lamprey Petromyzon marinus habituate to conspecific damage-released alarm cues (fresh and decayed sea lamprey extract), a heterospecific damage-released alarm cue (white sucker Catostomus commersonii extract), predator cues (Northern water snake Nerodia sipedon washing, human saliva and 2-phenylethylamine hydrochloride (PEA HCl)) and a conspecific damage-released alarm cue and predator cue combination (fresh sea lamprey extract and human saliva) after they were pre-exposed 4 times or 8 times, respectively, to a given stimulus the previous night. Consistent with our prediction, adult sea lamprey maintained an avoidance response to conspecific damage-released alarm cues (fresh and decayed sea lamprey extract), a predator cue presented at high relative concentration (PEA HCl) and a conspecific damage-released alarm cue and predator cue combination (fresh sea lamprey extract plus human saliva), irrespective of previous exposure level. As expected, adult sea lamprey habituated to a sympatric heterospecific damage-released alarm cue (white sucker extract) and a predator cue presented at lower relative concentration (human saliva). Adult sea lamprey did not show any avoidance of the Northern water snake washing and the Amazon sailfin catfish extract (heterospecific control). This study suggests that conspecific damage-released alarm cues and PEA HCl present the best options as natural repellents in an integrated management program aimed at controlling the abundance of sea lamprey in the Laurentian Great Lakes.

Larval Sea Lampreys (&lt;i&gt;Petromyzon marinus&lt;/i&gt;) Do Not Emigrate from a Risky Habitat Under Semi-natural Conditions

Sea Lamprey (Petromyzon marinus), invaded the upper Great Lakes in the early 20th century, precipitating abrupt declines ina number of native fish species. A recently proposed alternative method for the behavioural manipulation of Sea Lamprey populations is the use of conspecific damage-released alarm and predator cues as potential repellents. We examined whether larval Sea Lamprey (Petromyzon marinus) ammocoetes can be manipulated to emigrate from an area by labeling their habitat “risky” with the regular release of chemosensory alarm cues over several days. in a semi-natural laboratory environment, we exposed eight replicate groups of eight ammocoetes twice a day, for 7 days, to deionized water (control), ammocoete whole-body extract (damage-released alarm cue), and 2-phenylethylamine HCl (predator cue). None of the experimental stimuli induced emigration from the experimental arena. This approach does not hold any promise for ammocoete behavioural manipulation in the context of a Sea Lamprey integrated management program.

The behavioural response of adult Petromyzon marinus to damage-released alarm and predator cues.

Using semi-natural enclosures, this study investigated (1) whether adult sea lamprey Petromyzon marinus show avoidance of damage-released conspecific cues, damage-released heterospecific cues and predator cues and (2) whether this is a general response to injured heterospecific fishes or a specific response to injured P. marinus. Ten replicate groups of 10 adult P. marinus, separated by sex, were exposed to one of the following nine stimuli: deionized water (control), extracts prepared from adult P. marinus, decayed adult P. marinus (conspecific stimuli), sympatric white sucker Catostomus commersonii, Amazon sailfin catfish Pterygoplichthys pardalis (heterospecific stimuli), 2-phenylethylamine (PEA HCl) solution, northern water snake Nerodia sipedon washing, human saliva (predator cues) and an adult P. marinus extract and human saliva combination (a damage-released conspecific cue and a predator cue). Adult P. marinus showed a significant avoidance response to the adult P. marinus extract as well as to C. commersonii, human saliva, PEA and the adult P. marinus extract and human saliva combination. For mobile P. marinus, the N. sipedon washing induced behaviour consistent with predator inspection. Exposure to the P. pardalis extract did not induce a significant avoidance response during the stimulus release period. Mobile adult female P. marinus showed a stronger avoidance behaviour than mobile adult male P. marinus in response to the adult P. marinus extract and the adult P. marinus extract and human saliva combination. The findings support the continued investigation of natural damage-released alarm cue and predator-based repellents for the behavioural manipulation of P. marinus populations in the Laurentian Great Lakes.

Contaminant-specific targeting of olfactory sensory neuron classes: Connecting neuron class impairment with behavioural deficits

The olfactory system of fish comprises several classes of olfactory sensory neurons (OSNs). The odourants l-alanine and taurocholic acid (TCA) specifically activate microvillous or ciliated OSNs, respectively, in fish. We recorded electro-olfactograms (EOG) in fathead minnows (Pimephales promelas; a laboratory-reared model species) and wild yellow perch (Perca flavescens) whose olfactory chambers were perfused with either l-alanine or TCA to determine if OSN classes were differentially vulnerable to contaminants, in this case copper or nickel. Results were consistent in both species and demonstrated that nickel targeted and impaired microvillous OSN function, while copper targeted and impaired ciliated OSN function. This result suggests that contaminant-specific effects observed in model laboratory species extrapolate to wild fish populations. Moreover, fathead minnows exposed to copper failed to perceive a conspecific alarm cue in a choice maze, whereas those exposed to nickel could respond to the same conspecific cue. These results demonstrate that fathead minnows perceive conspecific, damage-released alarm cue by ciliated, but not microvillous, OSNs. Fish living in copper-contaminated environments may be more vulnerable to predation than those in clean lakes owing to targeted effects on ciliated OSNs.

The behavioural response of migratory sea lamprey (Petromyzon marinus) to potential damage-released larval and migratory chemical alarm cues

We investigated the presence of damage-released alarm cues and the reactions they may cause in landlocked migratory sea lamprey (Petromyzon marinus) using semi-natural laboratory conditions during the day. In two separate experiments, migratory sea lampreys were exposed to stimuli prepared from the skinless carcasses and skin tissue of larval sea lamprey and from the skin tissue and muscle tissue of migratory sea lamprey. Migratory female sea lamprey swam significantly longer after being exposed to the stimulus prepared from the skinless carcass of larval sea lamprey. No significant changes were seen in the behaviour of the migratory female lamprey in response to larval skin extract or in the behaviour of male sea lamprey to any experimental extract in the larval extract experiment. In the second experiment that utilised migratory lamprey stimuli, neither male and nor female migratory sea lamprey showed a significant difference in their behavioural response among different treatments and controls. Our findings indicate that adult female sea lamprey respond strongly to damage-released alarm cues from larval sea lamprey; hence, the latter holds promise for sea lamprey behavioural manipulations for control purposes during the day. Further research is needed to examine responses to damage-released alarm cues at night, when migratory sea lampreys are more active.

Toxic Prey and Predator Avoidance: Responses of Toxic Newts to Chemical Stimuli from a Predator and Injured Conspecifics

Abstract Predator avoidance behavior minimizes predation risk because the prey never enters the perceptual field of the predator. For toxic species, avoiding potential predators indiscriminately is unlikely to be the best predator avoidance strategy because many predators will be incapable of consuming the toxin. We investigated the role of chemical-based avoidance behavior in predator-prey interactions between a toxic prey species, the Rough-skinned Newt (Taricha granulosa), and its major predator, the Common Garter Snake (Thamnophis sirtalis). Terrestrial newts avoided predator kairomones only when the predator had recently consumed a conspecific, but did not avoid damage-released alarm cues. These results indicate newts may be able to chemically differentiate between toxin-resistant and toxin-sensitive snakes in the same population and avoid only those snakes actively preying upon their cohort.

Sensory complementation and the acquisition of predator recognition by salmonid fishes

Following disturbance, some aquatic prey species release chemicals that act as a warning cue and increase vigilance in nearby conspecifics. Such disturbance cues evoke consistent low intensity anti-predator responses. In contrast, alarm cues from injured conspecifics often evoke stronger intensity responses in prey animals. In this study, we test the sensory complement hypothesis, which suggests that multiple cues act in an additive or synergistic fashion to provide additional information for risk assessment by prey. In the first experiment, we showed that juvenile rainbow trout pre-exposed to disturbance cues respond to a given concentration of damage-released alarm cues with a higher intensity of response than the trout that were pre-exposed to cues from undisturbed conspecifics. The two cues acted in an additive fashion. In the second experiment, we demonstrated that disturbance cues alone were not enough to elicit a conditioned response to the odour of a novel predator. We also showed that while disturbance cues elicit an increase in the response of trout to alarm cues, this increase does not translate into a stronger learned response to the predator when the predator odour is paired with alarm cues. Future studies should take into account sensory complementation to avoid underestimating the responses of prey to predators.

A note on alarm cues in juvenile African catfish, Clarias gariepinus Burchell: Indications for opposing behavioural strategies

Following exposure of African catfish to alarm cues, a relationship ( r p = 0.60, N = 10, P = 0.07) between feed efficiency (measured as residual feed intake) and the change in percentage of time spent swimming in response to damage-released alarm cues was observed. Feed-efficient animals responded with a decrease in percentage of time spent swimming ( P < 0.05) whereas feed-inefficient animals responded with an increase in percentage of time spent swimming ( P < 0.05). This study shows opposing behavioural strategies in African catfish in response to damage-released alarm cues being related to feeding efficiency.

Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): responses to alarm, disturbance, and predator cues.

Slimy sculpins (Cottus cognatus) are small benthic fish that commonly co-occur with predatory fishes throughout most of their range in North America. In two laboratory experiments we examined the nature and extent of responses of slimy sculpins to chemosensory cues from predatory brook trout (Salvelinus fontinalis) and chemical alarm cues released by conspecific sculpins. Sculpins responded to three different classes of chemical stimuli: (1) cues of predatory brook trout, (2) damage-released alarm cues from conspecific sculpins, and (3) disturbance cues from conspecific sculpins. Sculpins did not distinguish between trout fed different diets; however, the presence of damage-released alarm cues did enhance the intensity of response to the predator chemicals. A histological analysis of the skin of sculpins revealed the presence of large sacciform cells that may act as the source of chemical alarm signals.