Prey Cues Research Articles

Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage

To date, little attention has been devoted to possible complementary effects of multiple forms of public information similar information on the foraging behaviour of predators. In order to examine how predators may incorporate multiple information sources, we conducted a series of predator attraction trials in the Lower Aripo River, Trinidad. Four combinations of visual (present or absent) and chemical cues (present or absent) from each of two prey species were presented. The occurrences of three locally abundant predatory species present within a 1 m radius of cue introduction sites were recorded. The relative attractiveness of cue type to each predator was directly related to their primary foraging modes, with visual ambush predators demonstrating an attraction to visual cues, benthivores to chemical cues, and active social foragers demonstrating complementary responses to paired cues. Predator species-pair counts were greatest in response to cues from the more abundant prey species, indicating that individuals may adopt riskier foraging strategies when presented with more familiar prey cues. These differences in predator attraction patterns demonstrate complementary effects of multiple sensory cues on the short-term habitat use and foraging behaviour of predators under fully natural conditions.

Chemical prey cues influence the urban microhabitat preferences of Western black widow spiders, Latrodectus hesperus

Spiders are important predators in terrestrial ecosystems, and several spider species have been shown to use chemical cues to locate prey. However, the extent to which chemical prey cues actually drive habitat use by individual spiders remains unclear. In this study we tested whether Western black widow spiders, Latrodectus hesperus Chamberlin & Ivie 1935, can detect chemical cues left by potential prey items and adjust their habitat preferences (i.e., web building behavior and refuge choice) accordingly. Using outdoor enclosures, we gave mature female widows the choice of microhabitat (rocks) previously housing cricket prey versus control rocks lacking cricket cues. Our results showed a significant preference by black widows to build their webs in areas that contain chemical prey cues. We discuss the implications of this finding for our understanding of urban black widow habitat use, population dynamics, and the potential for urban infestations.

Volatile metabolites.

Volatile organic compounds (volatiles) comprise a chemically diverse class of low molecular weight organic compounds having an appreciable vapor pressure under ambient conditions. Volatiles produced by plants attract pollinators and seed dispersers, and provide defense against pests and pathogens. For insects, volatiles may act as pheromones directing social behavior or as cues for finding hosts or prey. For humans, volatiles are important as flavorants and as possible disease biomarkers. The marine environment is also a major source of halogenated and sulfur-containing volatiles which participate in the global cycling of these elements. While volatile analysis commonly measures a rather restricted set of analytes, the diverse and extreme physical properties of volatiles provide unique analytical challenges. Volatiles constitute only a small proportion of the total number of metabolites produced by living organisms, however, because of their roles as signaling molecules (semiochemicals) both within and between organisms, accurately measuring and determining the roles of these compounds is crucial to an integrated understanding of living systems. This review summarizes recent developments in volatile research from a metabolomics perspective with a focus on the role of recent technical innovation in developing new areas of volatile research and expanding the range of ecological interactions which may be mediated by volatile organic metabolites.

Olfactory Experience Modifies Semiochemical Responses in a Bark Beetle Predator

A typical feature of forest insect pests is their tendency to undergo large fluctuations in abundance, which can jeopardize the persistence of their predaceous natural enemies. One strategy that these predators may adopt to cope with these fluctuations would be to respond to sensory cues for multiple prey species. Another possible adaptation to temporal variation in the prey community could involve the learning of prey cues and switching behavior. We conducted three experiments to investigate the ability of the generalist bark beetle predator Thanasimus dubius (F.) (Coleoptera: Cleridae) to respond to different prey signals and to investigate the effect of olfactory experience. We first conducted a field choice test and a wind tunnel experiment to examine the kairomonal response of individual predators toward prey pheromone components (frontalin, ipsenol, ipsdienol, sulcatol) along with the pine monoterpene α-pinene, which is a volatile compound from the host of the prey. We also presented semiochemically naive predators with two prey pheromone components, frontalin and ipsenol, alone or associated with a reward. Our results showed that T. dubius populations are composed of generalists that can respond to a broad range of kairomonal signals. Naive T. dubius also were more attracted to ipsenol following its association with a reward. This work constitutes the first evidence that the behavior of a predatory insect involved in bark beetle population dynamics is influenced by previous olfactory experience, and provides a potential explanation for the pattern of prey switching observed in field studies.

The feeding response of Pseudophycas barbata to multisensory prey cues in a low light environment

The nocturnal southern bastard cod Pseudophycis barbata was found to utilize chemo- and mechanosensory systems when hunting for prey under low light conditions. The sensory system used depended on whether prey produced a hydrodynamic signal.

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.

Multiple prey cues induce foraging flexibility in a trap-building predator

Predators must be behaviourally flexible to counter the temporal and spatial stochastic fluctuations and response variability of their prey. To ensure behaviours are adequate across environments, animals must regularly assess environmental cues. Spider orb webs are an example of a flexible foraging trait in a predator, as web architectural components vary in response to exposure to different prey types and prey traits. The cues used by orb web spiders to initiate changes in web architecture are not known. Current research predicts that prey nutrients and vibratory stimuli are potential candidates, but how they combine to affect spider foraging decisions is not clear. We performed experiments exposing the giant wood spider, Nephila pilipes, to different prey nutrients and vibratory stimuli. Spiders were fed either large profitable prey with high kinetic energy (crickets) or small prey with low kinetic energy (flies). In two treatments the prey nutrients and vibratory cues came from live prey, but in the other two treatments spiders received dead crickets with webs stimulated by flies and vice versa. The spiders fed on live flies built larger webs with more radii that were less stiff and had greater vibration damping. These web characteristics did not differ between the other three treatment groups. Our results show that in the absence of nutrient and vibratory cues from profitable prey, spiders alter their web architecture to build webs better able to capture the less profitable prey at a cost of more material investment, greater web visibility and reduced vibratory signal clarity.

Pygmy owl Glaucidium passerinum and the usage of ultraviolet cues of prey

Birds rely mainly on their vision when foraging. Many diurnal raptors use ultraviolet (UV) vision and ultraviolet‐reflecting vole scent marks to find suitable hunting areas, whereas nocturnal owls seem to lack this ability. We studied if the diurnal pygmy owl Glaucidium passerinum that uses voles and birds as its food can detect vole scent marks using UV‐vision. We conducted a laboratory experiment with eleven owls. Each individual owl had four options to choose from: (1) scent marks with UV light, (2) scent marks without UV light, (3) clean arena with UV light and (4) clean arena without UV light. The owls scanned the scent mark arena more often in the presence of UV light than other arenas. However, owls did not spend more time above the UV arena. We suggest that pygmy owls can detect near UV and use UV to gain information about prey like other diurnal raptors.

Complementary lateralisation in the exploratory and predatory behaviour of the common wall lizard (Podarcis muralis)

Several ectotherms show lateralisation, particularly visual lateralisation. Such brain specialisation has an ancient origin and is still present in living vertebrates. One important advantage is the possibility for lateralised animals to carry out two tasks at the same time, without altering the efficiency of either one. Recent studies on the common wall lizard (Podarcis muralis) found right eye/left hemisphere bias for attention to the cues of prey, and left eye/right hemisphere bias for controlling antipredatory and exploratory behaviours. However, these studies were independent of each other and therefore were not empirical demonstrations that the directions of visual lateralisation found in this species are present in the same individual, allowing the simultaneous performance of dual tasks. In our study the same Podarcis muralis individuals carried out one exploratory and one predatory test each. We allowed each lizard to move freely in a circular arena, with opaque walls, with either nothing or mealworm larvae in the centre. In the first case the test was an exploratory test, while in the second case it was a predatory one. The results indicated that lizards preferentially used the left eye to observe the environment—i.e., during exploration—and just tended to use the right eye during predation. Hence we conclude that in the Podarcis muralis lizard lateralisation is expressed in the same individual in opposite directions, in accordance with previous observations.

Prey type, vibrations and handling interactively influence spider silk expression

The chemical and mechanical properties of spider major ampullate (MA) silks vary in response to different prey, mostly via differential expression of two genes - MaSp1 and MaSp2 - although the spinning process exerts additional influence over the mechanical properties of silk. The prey cues that initiate differential gene expression are unknown. Prey nutrients, vibratory stimuli and handling have been suggested to be influential. We performed experiments to decouple the vibratory stimuli and handling associated with high and low kinetic energy prey (crickets vs flies) from their prey nutrients to test the relative influence of each as inducers of silk protein expression in the orb web spider Nephila pilipes. We found that the MA silks from spiders feeding on live crickets had greater percentages of glutamine, serine, alanine and glycine than those from spiders feeding on live flies. Proline composition of the silks was unaffected by feeding treatment. Increases in alanine and glycine in the MA silks of the live-cricket-feeding spiders indicate a probable increase in MaSp1 gene expression. The amino acid compositions of N. pilipes feeding on crickets with fly stimuli and N. pilipes feeding on flies with cricket stimuli did not differ from each other or from pre-treatment responses, so these feeding treatments did not induce differential MaSp expression. Our results indicate that cricket vibratory stimuli and handling interact with nutrients to induce N. pilipes to adjust their gene expression to produce webs with mechanical properties appropriate for the retention of this prey. This shows that spiders can genetically alter their silk chemical compositions and, presumably, mechanical properties upon exposure to different prey types. The lack of any change in proline composition with feeding treatment in N. pilipes suggests that the MaSp model determined for Nephila clavipes is not universally applicable to all Nephila.

Behavioral evidence for eavesdropping on prey song in two Palearctic sibling bat species

Eavesdropping on prey communication signals has never before been reported for a Palearctic bat species. In this study, we investigated whether lesser and greater mouse-eared bats, Myotis blythii oxygnathus and Myotis myotis, find tettigoniid bushcrickets (Tettigoniidae) by eavesdropping on their mate-attraction song. Tettigoniids are known to be the most important prey item for M. blythii oxygnathus, while carabid beetles and other epigaeic arthropods are the most important prey for its sibling species, M. myotis, in many places in Europe. M. myotis locates walking beetles by listening for their rustling sounds. We compared these two species’ response to four acoustic prey cues: calling song of two tettigoniid species, the rustling sound made by walking carabid beetles, and a control tone. Individuals of both bat species attacked the speaker playing tettigoniid song, which clearly indicates that both species eavesdrop on prey-generated advertisement signals. There were, however, species differences in response. M. blythii oxygnathus exhibited stronger predatory responses to the calling song of two species of tettigoniid than to the beetle rustling sound or the control. M. myotis, in contrast, exhibited stronger predatory responses to the beetle rustling and to one tettigoniid species but not the other tettigoniid or the control. Our study (1) for the first time demonstrates eavesdropping on prey communication signals for Palearctic bats and (2) gives preliminary evidence for sensory niche partitioning between these two sympatric sibling bat species.

Socializing makes thick-skinned individuals: on the density of epidermal alarm substance cells in cyprinid fish, the crucian carp (Carassius carassius)

In cyprinid fish, density of epidermal club cells (i.e. alarm substance cells) has been found to vary between lakes with different predator fauna. Because predators can be labelled with chemical cues from prey, we questioned if club cell density could be controlled indirectly by predators releasing prey cues. In particular, we suspected a possible feedback mechanism between chemical alarm signals and their cellular source. We raised crucian carp singly and in groups of four. For both rearing types, fish were exposed to skin extracts of either conspecifics or brown trout (without club cells), and provided either low or high food rations. Independent of rearing type, condition factor and club cell density increased with food ration size, but no change was found in club cell density following exposure to conspecific alarm signals. However, the density of club cells was found significantly higher for fish raised in groups than for fish raised alone. We conclude that an increased condition factor results in more club cells, but crucian carp may also possess an awareness of conspecific presence, given by higher club cell densities when raised in groups. This increase in club cell density may be induced by unknown chemical factors released by conspecifics.

Behavioral responses to light gradients, olfactory cues, and prey in larvae of two North Pacific gadids (Gadus macrocephalus and Theragra chalcogramma)

The growth and survival of larvae can be significantly enhanced through close association with patches of high prey concentration. However, the taxis and kinesis responses used by larvae to locate and maintain residence in micro-patches remains poorly understood. In this study, the behavioral responses of Pacific cod (Gadus macrocephalus) and walleye pollock (Theragra chalcogramma) larvae (45–100 dph) to light, prey scent, and prey were examined. Both species displayed an ontogenetic shift in response to a horizontal light gradient, with small larvae (11–13 mm SL) exhibiting a positive phototaxis and large larvae (23–32 mm SL) exhibiting a negative phototaxis. Whether this reversal is related to ontogenetically appropriate foraging cues or some other aspect of the environment remains to be determined. Neither species displayed significant behavioral responsiveness to the introduction of olfactory prey cues at either size. The aggregating (taxis) response of large larvae to introduction of live prey was stronger than that of small larvae, possibly due to increased reaction distances and encounter rates. In addition, both species exhibited a kinesis response of reducing the frequency of swimming bouts in response to introduction of live prey. These results suggest that the scale of prey patchiness and the physical factors that determine patch encounter rates are a significant determinant of larval growth and survival in the early feeding stages of marine fishes.

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to "label" predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.

Dragline deposition patterns among male and female Hogna helluo (Araneae, Lycosidae) in the presence of chemical cues from prey

Prey are able to show adaptive antipredator responses in the presence of silk from the wolf spider Hogna helluo (Walckenaer 1837). Hogna helluo also is attracted to chemical cues associated with previously consumed prey. Consequently H. helluo may benefit by modifying its silk deposition when encountering prey cues to avoid detection. Silk is an important medium for female wolf spiders to attract prospective mates, whereas silk is putatively less important for males to attract females. Females also consume much more food than males after maturity; therefore, male and female H. helluo may differ in the relative costs and benefits of silk deposition with respect to improved feeding efficiency. We tested whether field-caught male and female Hogna helluo changed silk deposition patterns in the presence of excreta deposited by domestic crickets, Acheta domesticus, (Linnaeus). Hungry male and female H. helluo were allowed to deposit silk for four hours in containers either previously occupied by five crickets for 24 h or devoid of cues (n 5 36). We found no significant decrease in silk dragline deposition among males or females in the presence of prey cues; however, female spiders showed a significant decrease in the number of attachment disks produced in the presence of cricket cues whereas males did not. Our results suggest that Hogna helluo do change silk deposition patterns in the presence of crickets, but that these changes are sex-specific.

Importance of light, temperature, zooplankton and fish in predicting the nighttime vertical distribution of Mysis diluviana

The opossum shrimp Mysis diluviana (formerly M. relicta) performs large amplitude diel vertical migrations in Lake Ontario and its nighttime distribution is influenced by temperature, light and the distribution of its predators and prey. At one location in southeastern Lake Ontario, we measured the vertical distribution of mysids, mysid predators (i.e. planktivorous fishes) and mysid prey (i.e. zooplank- ton), in addition to light and temperature, on 8 occasions from May to September, 2004 and 2005. We use these data to test 3 different predictive models of mysid habitat selection, based on: (1) laboratory- derived responses of mysids to different light and temperature gradients in the absence of predator or prey cues; (2) growth rate of mysids, as estimated with a mysid bioenergetics model, given known prey densities and temperatures at different depths in the water column; (3) ratio of growth rates (g) and mor- tality risk (μ) associated with the distribution of predatory fishes. The model based on light and temper- ature preferences was a better predictor of mysid vertical distribution than the models based on growth rate and g:μ on all 8 occasions. Although mysid temperature and light preferences probably evolved as mechanisms to reduce predation while increasing foraging intake, the response to temperature and light alone predicts mysid vertical distribution across seasons in Lake Ontario.

Effects of turbidity on the spontaneous and prey-searching activity of juvenile Atlantic cod (Gadus morhua).

Increasing turbidity in coastal waters in the North Atlantic and adjacent seas has raised concerns about impacts on Atlantic cod (Gadus morhua) using these areas as nurseries. A previous experiment (Meager et al. 2005 Can. J. Fish. Aquat. Sci. 62, 1978-1984) has shown that turbidity (up to 28 beam attenuation m-1) had little effect on the foraging rate of juvenile cod. Although this was attributed to cod using chemoreception in conjunction with vision to locate prey, foraging rates may also be maintained by increased activity. Higher activity, however, is energetically costly and may offset benefits from increased foraging return. We examined the effects of turbidity on prey searching and spontaneous activity of juvenile cod in the laboratory, by measuring activity with and without prey cues. Activity of juvenile cod was nonlinearly affected by turbidity and was lower at intermediate turbidity, regardless of the presence of prey odour. Activity increased over time when prey odour was present and decreased when absent, but the effects of prey odour were similar across all turbidity levels. Position in the tank was unaffected by turbidity or prey odour. Reduced activity at intermediate turbidities is likely to offset longer prey-search times. At high turbidity (greater than 17m-1), both longer prey-search times and higher activity indicate that increased energetic costs are probable.

The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey

Ecological and phylogenetic factors determine which sensory modalities organisms use in their day-to-day activities. Among lizards, empirical studies indicate a tight association between foraging strategies and the ability to detect chemical cues from prey. Consequently, ambush insectivores do not detect food chemicals and these differences have a phylogenetic basis, as ambush lizards mainly belong to the Iguania clade. These data contrast, however, with the widespread uses of chemoreception in the Iguania genus Liolaemus, which are mostly insectivorous ambush predators. Moreover, observations from different Liolaemus species suggest a capability to find prey through chemoreception. In order to clarify the abilities of Liolaemus to detect chemical cues from prey, the chemoreceptive behavior of the insectivorous ambush predator, L. lemniscatus, was studied. Lizards were given the choice between areas with and without chemical cues from a food item (mealworms). Results show that test animals stayed for longer, moved more, and did more chemical exploration (tongue flicks) in the area where chemical cues from mealworms were present. Furthermore, in this area, more individuals displayed behaviors that suggest maintenance and defense of the prey patch. Thus, L. lemniscatus is the first insectivorous Iguania reported to be able to detect chemical cues from prey. Although I propose a mechanism for acquiring chemical detection of prey cues in Liolaemus, I also remark that it is necessary to reanalyze both the abilities to detect and use chemical foraging cues in Iguania at large, and the methodologies traditionally used to study these issues.

Turbidity and foraging rate in threespine sticklebacks: the importance of visual and chemical prey cues

AbstractIn aquatic habitats turbidity can affect the foraging efficiency of visual predators, directly influencing their capacity to detect prey. In a laboratory study we tested the effect of different loads of suspended sediment upon the foraging rates of threespine sticklebacks (Gasterosteus aculeatus). We compared the foraging rates of fish under a series of different turbidity treatments, testing fish originating from four habitats within a single drainage basin that differed in a number of environmental parameters including turbidity. Although we found habitat specific differences in foraging rates, these did not correspond to local turbidity levels. The findings of a follow up experiment revealed habitat-specific variation in boldness, which may be indirecly linked to the observed differences in foraging rate. The main finding of our study was that turbidity alone had no impact upon their prey capture rates, but that high turbidity in combination with saturation with prey odour extract caused prey capture rates to fall significantly. This suggests that olfactory cues can be more important than visual cues in determining foraging performance in this species, potentially influencing how they cope with naturally occurring periods of turbidity, and how they adapt to human-induced eutrophication.

Relationships between chemosensory behaviour and foraging mode within lacertid lizards

We assess associations between chemosensory capacity and foraging mode within lacertid lizards. Species of Lacertidae differ considerably in indices of foraging mode, and therefore seem well suited to test the adaptive nature of a coupling between foraging and sensory ecology. We observed tongue-flick (TF) rates of members from eight species in the field and in experimental conditions with no prey stimuli, with chemical stimuli, with visual stimuli and with both chemical and visual stimuli. All species increased TF rates in response to both purely visual and purely chemical prey cues, and the increase was most pronounced when both types of stimuli were offered simultaneously. Absolute TF rates in experimental conditions differed considerably among species, and species means obtained in experimental situations correlated closely with those observed in the field. Species that spend a relatively large amount of their time budget actively searching for food tend to use their vomeronasal system more frequently. Although all species in our study retained the capacity of recognizing prey chemicals, our data corroborate the idea of a functional link between an active foraging style and the usage of chemical information.