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.     

Antipredator responses of koomal (Trichosurus vulpecula hypoleucus) against introduced and native predators

Antipredator behavior studies generally assess prey responses to single predator species although most real systems contain multiple species. In multi-predator environments prey ideally use antipredator responses that are effective against all predator species, although responses may only be effective against one predator and counterproductive for another. Multi-predator systems may also include introduced predators that the prey did not co-evolve with, so the prey may either fail to recognize their threat (level 1 naiveté), use ineffective responses (level 2 naiveté) or succumb to their superior hunting ability (level 3 naiveté). We analyzed microhabitat selection of an Australian marsupial (koomal, Trichosurus vulpecula hypoleucus) when faced with spatiotemporal differences in the activity/density levels of one native (chuditch, Dasyurus geoffroii) and two introduced predators (red fox, Vulpes vulpes; feral cat, Felis catus). From this, we inferred whether koomal recognized introduced predators as a threat, and whether they minimized predation risk by either staying close to trees and/or using open or dense microhabitats. Koomal remained close to escape trees regardless of the predator species present, or activity/density levels, suggesting koomal employ this behavior as a first line of defense. Koomal shifted to dense cover only under high risk scenarios (i.e., with multiple predator species present at high densities). When predation risk was low, koomal used open microhabitats, which likely provided benefits not associated with predator avoidance. Koomal did not exhibit level 1 naiveté, although further studies are required to determine if they exhibit higher levels of naiveté (2–3) against foxes and cats.     

Predation risk assessment by green frog (<Emphasis Type="Italic">Rana clamitans</Emphasis>) tadpoles through chemical cues produced by multiple prey

Many prey assess predation risk through predator chemical cues. Numerous studies have shown that (1) prey sometimes respond to chemical cues produced by heterospecifics and (2) that many species are capable of associative learning. This study extends this research by focusing on predation risk assessment and antipredator behavior in environments containing chemical cues produced by multiple prey species. The results show that green frog (Rana clamitans) tadpoles (1) assess risk from the chemical cue produced during predation by a heterospecific (gray tree frog, Hyla versicolor, tadpoles) and (2) can exhibit similarly strong behavioral responses to a mix of conspecific and heterospecific cues compared to conspecific cue alone, depending on their conditioning environment. I then discuss how the prey choice of the predators and the relative abundances of the prey species should influence the informational value of heterospecific cues.     

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.     

Do mountain log skinks (<Emphasis Type="Italic">Pseudemoia entrecasteauxii</Emphasis>) modify their behaviour in the presence of two predators?

Prey often adopt antipredator strategies to reduce the likelihood of predation. In the presence of predators, prey may use antipredator strategies that are effective against a single predator (specific) or that are effective against several predators (nonspecific). Most studies have been confined to single predator environments although prey are often faced with multiple predators. When more than one predator is present, specific antipredator behaviours can conflict and avoidance of one predator may increase vulnerability to another. To test how prey cope with this dilemma, I recorded the behaviours of lizards responding to the nonlethal cues of a bird and snake presented singly and simultaneously. Lizards use specific and conflicting antipredator tactics when confronted with each predator, as evidenced by refuge use. However, when both predators were present, lizards refuge use was the same as in the predator-free environment, indicating that they abandoned refuge use as a primary mechanism for predator avoidance. In the presence of both predators, they reduced their overall movement and time spent thermoregulating. This shift in behaviour may represent a compromise to minimize overall risk, following a change in predator exposure. This provides evidence of plasticity in lizard antipredator behaviour and shows that prey responses to two predators cannot be accurately predicted from what is observed when only one predator is present.Communicated by W. Cooper     

Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects?

The threat-sensitivity hypothesis predicts that prey individuals will increase antipredator behaviors as apparent predator risk increases. An implicit assumption of the threat-sensitivity hypothesis is that predator risk is additive. In other words, all characteristics of a predator that indicate risk should contribute in an additive way to determine the degree of risk-sensitive behavior. We tested this assumption in the laboratory by presenting live predators (green sunfish, Lepomis cyanellus) to groups of western mosquitofish (Gambusia affinis). We examined effects of predator diet, hunger level, and size on predator avoidance and inspection behavior of mosquitofish. Both predator diet and predator hunger level were significant and additive determinants of distance maintained from a predator, resulting in a graded response to combinations of these predator cues. In contrast, whereas predator diet was the most important determinant of general avoidance distances, predator hunger level was more important in determining mosquitofish vertical distribution and inspection behavior. Thus, the relationship between predator cue and the antipredator behavior that it elicits is dependent on which cues and behaviors are examined. Our data suggest that during risky behaviors, such as predator inspection, mosquitofish rely mainly on visual cues (behavior differences between hungry and satiated predators), whereas general avoidance behavior is determined by additive responses from visual and chemical cues.     

Threat-sensitive learning of predators by larval mosquitoes <Emphasis Type="Italic">Culex restuans</Emphasis>

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Innate antipredator responses of Arctic charr (<Emphasis Type="Italic">Salvelinus alpinus</Emphasis>) depend on predator species and their diet

The ability to discriminate between more dangerous and less dangerous predators can have serious fitness advantages for fish juveniles. This is especially true for hatchery-reared fish young used for stocking, because their post-release mortality is often much higher than that of wild-born conspecifics. We tested whether two coexisting fish predators and their different diets induce innate behavioral responses in predator-naive Arctic charr (Salvelinus alpinus) young originating from an endangered hatchery-bred population used for re-introductions. We predicted the antipredator responses of charr to be stronger towards chemical cues of brown trout (Salmo trutta) and pikeperch (Stizostedion lucioperca) than towards odorless control water. More pronounced antipredator behavior was predicted in treatments with predators fed on charr than when their diet consisted of another sympatric salmonid, European grayling (Thymallus thymallus), or when they were food-deprived. The Arctic charr young showed strong antipredator responses in all brown trout treatments, whereas odors of the less likely predator pikeperch were avoided with conspecific diet only. Freezing was the most sensitive antipredator behavior, as it was completely absent in control treatments. We found considerable individual variation in the amount and strength of antipredator responses. Although almost half of the charr failed to show antipredator behavior towards the piscivores, those with the innate ability showed highly sensitive recognition of predator odors. Our results indicate that the innate antipredator behavior of the juvenile fish is already finely tuned to respond specifically to chemical cues from different fish predators and even their diets.Communicated by J. Krause     

Risk level of chemical cues determines retention of recognition of new predators in Iberian green frog tadpoles

In aquatic environments, many prey rely on chemosensory information from injured (alarm cues) or stressed conspecifics (disturbance cues) to assess predation risk. Alarm cues are considered as a sign of higher risk than disturbance cues. These cues could be used by prey to learn potential new predators. In this study, we tested whether Iberian green frog tadpoles (Pelophylax perezi) exhibited antipredator responses to alarm and disturbance cues of conspecifics and whether tadpoles could associate new predators with alarm or disturbance cues. Tadpoles reduced their activity in the presence of disturbance cues, but only weakly when compared with their response to alarm cues. Also, tadpoles learned to recognize new predators from association with alarm or disturbance cues. However, the period of retention of the learned association was shorter for disturbance than alarm cues. Our results indicate that tadpoles are able to modify their antipredatory behavior according to (1) the degree of risk implied by the experimental cues (2) their previous experience of chemical cues of the predator.     

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.     

Risk vs. reward: how predators and prey respond to aging olfactory cues

Many animals use olfaction to find food and avoid predators, and must negotiate environments containing odors of varying compositions, strengths, and ages to distinguish useful cues from background noise. Temporal variation in odor cues (i.e., “freshness”) seems an obvious way that animals could distinguish cues, yet there is little experimental evidence for this phenomenon. Fresh cues provide a more reliable indicator of donor presence than aged cues, but we hypothesize that the benefits of responding to aged cues depend on whether the cue indicates the proximity of a predator or a potential meal. As prey cannot remain eternally risk averse in response to predator odor, we predict that antipredator responses should diminish as predator cues age. In contrast, animals searching for food should investigate aged prey cues if investigation costs are sufficiently low and the potential benefit (a meal) sufficiently high; thus, we predict that predators will maintain interest in aged prey cues. We tested these ideas using free-ranging rats (Rattus spp.) in two separate experiments; firstly assessing giving-up densities in the presence of predator odor, and secondly examining investigation rates of prey odors. As predicted, giving-up densities dropped once predator odor had aged, but investigation rates remained similar for aged and fresh prey odor. Thus, rats used temporal variation in odor cues to evaluate the cost–benefit relationship of responding to predator and prey odors. We suggest that the ecological significance of variable cue age needs more research and should be considered when interpreting behavioral responses to olfactory information.     

A review of predator diet effects on prey defensive responses

Numerous studies have examined how predator diets influence prey responses to predation risk, but the role predator diet plays in modulating prey responses remains equivocal. We reviewed 405 predator–prey studies in 109 published articles that investigated changes in prey responses when predators consumed different prey items. In 54 % of reviewed studies, prey responses were influenced by predator diet. The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators. Further, prey can alleviate costs or accrue greater benefits using diet cues as secondary sources of information to fine tune responses to predators and to learn novel risk cues from exotic predators or alarm cues from sympatric prey species. However, the ability to draw broad conclusions regarding use of predator diet cues by prey was limited by a lack of research identifying molecular structures of the chemicals that mediate these interactions. Conclusions are also limited by a narrow research focus. Seventy percent of reviewed studies were performed in freshwater systems, with a limited range of model predator–prey systems, and 98 % of reviewed studies were performed in laboratory settings. Besides identifying the molecules prey use to detect predators, future studies should strive to manipulate different aspects of prey responses to predator diet across a broader range of predator–prey species, particularly in marine and terrestrial systems, and to expand studies into the field.     

Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies

The antipredator behaviour of prey organisms is shaped by a series of threat-sensitive trade-offs between the benefits associated with successful predator avoidance and a suite of other fitness-related behaviours such as foraging, mating and territorial defence. Recent research has shown that the overall intensity of antipredator response and the pattern of threat-sensitive trade-offs are influenced by current conditions, including variability in predation risk over a period of days to weeks. In this study, we tested the hypothesis that long-term predation pressure will likewise have shaped the nature of the threat-sensitive antipredator behaviour of wild-caught Trinidadian guppies (Poecilia reticulata). Female guppies were collected from two populations that have evolved under high- and low-predation pressure, respectively, in the Aripo River, Northern Mountain Range, Trinidad. Under laboratory conditions, we exposed shoals of three guppies to varying concentrations of conspecific damage-released chemical alarm cues. Lower Aripo (high-predation) guppies exhibited the strongest antipredator response when exposed to the highest alarm cue concentration and a graded decline in response intensity with decreasing concentrations of alarm cue. Upper Aripo (low-predation) guppies, however, exhibited a nongraded (hypersensitive) response pattern. Our results suggest that long-term predation pressure shapes not only the overall intensity of antipredator responses of Trinidadian guppies but also their threat-sensitive behavioural response patterns.     

Different antipredator behaviour in two anuran tadpoles: effects of predator diet

Recent investigations have indicated that animals are able to use chemical cues of predators to assess the magnitude of predation risk. One possible source of such cues is predator diet. Chemical cues may also be important in the development of antipredator behaviour, especially in animals that possess chemical alarm substances. Tadpoles of the common toad (Bufo bufo) are unpalatable to most vertebrate predators and have an alarm substance. Tadpoles of the common frog (Rana temporaria) lack both these characters. We experimentally studied how predator diet, previous experience of predators and body size affect antipredator behaviour in these two tadpole species. Late-instar larvae of the dragonfly Aeshna juncea were used as predators. The dragonfly larvae were fed a diet exclusively of insects, R. temporaria tadpoles or B. bufo tadpoles. R. temporaria tadpoles modified their behaviour according to the perceived predation risk. Depending on predator diet, the tadpoles responded with weak antipredatory behaviour (triggered by insect-fed predators) or strong behaviour (triggered by tadpole-fed predators) with distinct spatial avoidance and lowered activity level. The behaviour of B. bufo in predator diet treatments was indistinguishable from that in the control treatment. This lack of antipredator behaviour is probably related to the effective post-encounter defenses and more intense competitive regime experienced by B. bufo. The behaviour of both tadpole species was dependent on body size, but this was not related to predator treatments. Our results also indicate that antipredator behaviour is largely innate in tadpoles of both species and is not modified by a brief exposure to predators. Received: 22 August 1996 / Accepted after revision: 31 January 1997     

Defense mechanisms and antipredator behavior in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus

The congeneric spiny lobsters Panulirus argus and P. guttatus co-occur throughout the Caribbean Sea, where they may share the coral reef habitat. Despite their phylogenetic closeness, both species have many different life-history traits that may partially explain their coexistence. However, even though both species may face the same predators, their defense mechanisms and antipredator strategies had not been compared. We compared the performance between species in 18 morphological and behavioral defense mechanisms commonly expressed by most spiny lobsters, including predator-avoidance mechanisms (activity schedule, sheltering behavior, delay to disturbance, and effect of conspecific damage-released scents on shelter choice) as well as antipredator mechanisms (body size, several parameters of the escape response and limb autospasy, clinging strength, antennal strength, and cooperative defense). As hypothesized, both species expressed all these defense mechanisms (except cooperative defense, shown only by P. argus), reflecting their phylogenetic closeness, but performed significantly differently in most, in accordance with their particular ontogenetic traits. Their comparative performance in individual defense mechanisms as well as the antipredator strategies displayed by groups of lobsters of each species in the presence of a common predator (the triggerfish Balistes vetula) showed that, in general, the defensive behavioral type of P. argus is more bold and that of P. guttatus more shy. Therefore, their distinct defensive behaviors contribute to their niche differentiation.     

Survival trade-offs between two predator-induced phenotypes in Pacific treefrogs (Pseudacris regilla)

In many organisms, specific predator species induce defensive phenotypes that are qualitatively different from the phenotypes induced by other predator species. This differential induction implies that there is no optimal phenotype that works best against all predators. However, few studies have actually tested the hypothesis that each predator-induced phenotype provides the highest survival rate in encounters with the predator that induced that phenotype. In this experiment, I reared Pacific treefrog (Pseudacris regilla) larvae with chemical cues from two different predators (bluegill sunfish and predaceous diving-beetle larvae), and without predator cues. The Pacific treefrog larvae in the three treatments differed in their morphology and foraging behavior. I then exposed tadpoles from each treatment to free-foraging predaceous diving beetles and bluegill sunfish. Tadpoles survived best when exposed to the predator whose cues they were reared with, and worst when exposed to the other predator. In both predator environments, the tadpoles reared in the nonpredator control treatment had intermediate survival between the two predator-induced groups. Thus, there is no generalized "antipredator" response to these predators; rather, there was a clear trade-off in survival abilities between the predators.     

Local interactions between predators and prey call into question commonly used functional responses

Commonly used functional response models (Holling’s type I and type II models) assume that the encounter rate of a predator increases linearly with prey density, provided that the predator is searching for prey. In other other words, aN (a is the baseline encounter rate and N is prey density) describes the encounter rate. This study examined whether the models are adequate when predators and prey interact locally by using a spatially explicit individual based model because local interactions affect the spatial distribution of predators and prey, which also affects the encounter rate. Predators were assumed to possess a spatial perception range that influenced their foraging behavior (e.g., if a prey is in the perception range, the predator moves towards the prey). The effect of antipredator behavior by prey was also examined. The results suggest that prey and predator densities as well as handling time affect the baseline rate (i.e., parameter a) as opposed to the common assumption that the parameter is constant. The nature of model deviations depended on both the antipredator behavior and the predators’ perception range. Understanding these deviations is important as they qualitatively affect community dynamics.     

Predator identity and additive effects in a treehole community

Multiple predator species can interact as well as strongly affect lower trophic levels, resulting in complex, nonadditive effects on prey populations and community structure. Studies of aquatic systems have shown that interactive effects of predators on prey are not necessarily predictable from the direct effects of each species alone. To test for complex interactions, the individual and combined effects of a top and intermediate predator on larvae of native and invasive mosquito prey were examined in artificial analogues of water-filled treeholes. The combined effects of the two predators were accurately predicted from single predator treatments by a multiplicative risk model, indicating additivity. Overall survivorship of both prey species decreased greatly in the presence of the top predator Toxorhynchites rutilus. By itself, the intermediate predator Corethrella appendiculata increased survivorship of the native prey species Ochlerotatus triseriatus and decreased survivorship of the invasive prey species Aedes albopictus relative to treatments without predators. Intraguild predation did not occur until alternative prey numbers had been reduced by approximately one-half. Owing to changes in size structure accompanying its growth, T. rutilus consumed more prey as time progressed, whereas C. appendiculata consumed less. The intermediate predator, C. appendiculata, changed species composition by preferentially consuming A. albopictus, while the top predator, T. rutilus, reduced prey density, regardless of species. Although species interactions were in most cases predicted from pairwise interactions, risk reduction from predator interference occurred when C. appendiculata densities were increased and when the predators were similarly sized.     

Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues

Summary. Predation is a pervasive selective agent highly variable in space and time. Due to the costs associated with antipredator responses, prey would be at a selective advantage if they respond to predation threats with an intensitfy matching the threat posed by the predator. Many aquatic organisms have been shown to use chemical alarm cues present in the water to assess the level of risk in their environment. This includes mosquito larvae which show antipredator responses to conspecific alarm cues. In this study, we investigated the nature of the responses of larval mosquitoes Culex restuans to those cues. In our initial observations, we showed pond/population differences in the response intensity of C. restuans to alarm cues. In experiment 1, we showed that the response intensity to alarm cues could be increased by increasing the background level of risk in the mosquitoes’ environment (by adding salamander predators) and once turned on, the response intensity to alarm cues was likely maintained for the remainder of the mosquitoes’ aquatic life. In experiments 2 and 3, we investigated if the increase in response intensity to alarm cues was directly correlated with the level of background risk in the mosquitoes’ environment. When given increasing levels of background risk, mosquito larvae subsequently showed a graded response to conspecific alarm cues. This series of experiments demonstrates that the response intensity of larval mosquitoes to a standard concentration of alarm cues is not fixed, but rather dependent on the background level of risk in the environment. An understanding of the background level of risk is particularly important for comparing antipredator responses of prey between habitats.