Predator cue and prey density interactively influence indirect effects on Basal resources in intertidal oyster reefs

Predators can influence prey abundance and traits by direct consumption, as well as by non-consumptive effects of visual, olfactory, or tactile cues. The strength of these non-consumptive effects (NCEs) can be influenced by a variety of factors, including predator foraging mode, temporal variation in predator cues, and the density of competing prey. Testing the relative importance of these factors for determining NCEs is critical to our understanding of predator-prey interactions in a variety of settings. We addressed this knowledge gap by conducting two mesocosm experiments in a tri-trophic intertidal oyster reef food web. More specifically, we tested how a predatory fish (hardhead catfish, Ariopsis felis) directly influenced their prey (mud crabs, Panopeus spp.) and indirectly affected basal resources (juvenile oysters, Crassostrea virginica), as well as whether these direct and indirect effects changed across a density gradient of competing prey. Per capita crab foraging rates were inversely influenced by crab density, but they were not affected by water-borne predator cues. As a result, direct consumptive effects on prey foraging rates were stronger than non-consumptive effects. In contrast, predator cue and crab density interactively influenced indirect predator effects on oyster mortality in two experiments, with trait-mediated and density-mediated effects of similar magnitude operating to enhance oyster abundance. Consistent differences between a variable predator cue environment and other predator cue treatments (no cue and constant cue) suggests that an understanding of the natural risk environment experienced by prey is critical to testing and interpreting trait-mediated indirect interactions. Further, the prey response to the risk environment may be highly dependent on prey density, particularly in prey populations with strong intra-specific interactions.     

Visual and olfactory location of biotopes, prey patches, and individual prey by the ladybeetleChilocorus nigritus

Foraging behaviour of the predatorChilocorus nigritus (Fabricius) (Coleoptera: Coccinellidae) at the three spatial levels of biotope, prey patch and individual prey, was studied in the laboratory, and related to behaviour in the field. Vertically oriented parallel lines were more attractive than the same shapes in a horizontal position. A simulated horizon with a tree line was preferred to a simulated flat horizon. They were attracted to a tree image for the first 2 h of exposure, but were less attracted after longer exposure, possibly due to habituation. Leaf shape was recognised, and simple ovate leaves were preferred to compound bipinnate leaves and to squares. These responses were associated with biotope selection for feeding and aggregation at aestivation sites. The location of prey patches by adults involved prey odour but the location of such sites by larvae did not. Adults detected individual prey visually and olfactorily over short distances but physical contact with prey was required for detection by larvae. Location of individual prey and prey patches by adults and larvae was facilitated by alternation between intensive and extensive search. The differences in the ability of larvae and adults to locate prey, stem from the adults being the active locators of biotope and patch, whereas the comparatively immobile larvae depend on their parents’ ability for long-range location of prey. Two hypotheses concerning coccinellid foraging behaviour are proposed. Firstly, the duration of response to a visual cue is related to the distance over which such a cue may be perceived. It follows that habituation to closer range cues occurs more rapidly than to longer range cues. Secondly, visual cues used by adults at the different spatial levels of prey location, and the location of mates and aggregation sites, have the same or similar shape. These results also provide guidelines for orchard management to maximise the biocontrol value of this species.     

Unidirectional prey-predator facilitation: apparent prey enhance predators' foraging success on cryptic prey

Food availability can strongly affect predator-prey dynamics. When change in habitat condition reduces the availability of one prey type, predators often search for other prey, perhaps in a different habitat. Interactions between behavioural and morphological traits of different prey may influence foraging success of visual predators through trait-mediated indirect interactions (TMIIs), such as prey activity and body coloration. We tested the hypothesis that foraging success of stream-dwelling cutthroat trout (Onchorhyncus clarki) on cryptically coloured, less-active benthic prey (larval mayfly; Paraleptophebia sp.) can be enhanced by the presence of distinctly coloured, active prey (larval stonefly shredder; Despaxia augusta). Cutthroat trout preyed on benthic insects when drifting invertebrates were unavailable. When stonefly larvae were present, the trout ate most of the stoneflies and also consumed a higher proportion of mayflies than under mayfly only treatment. The putative mechanism is that active stonefly larvae supplied visual cues to the predator that alerted trout to the mayfly larvae. Foraging success of visual predators on cryptic prey can be enhanced by distinctly coloured, active benthic taxa through unidirectional facilitation to the predators, which is a functional change of interspecific interaction caused by a third species. This study suggests that prey-predator facilitation through TMIIs can modify species interactions, affecting community dynamics.     

Stomach fullness modulates prey size choice in the frillfin goby,Bathygobius soporator

Behaviours related to foraging and feeding in predator–prey systems are fundamental to our understanding of food webs. From the perspective of a predator, the selection of prey size depends upon a number of factors including prey vulnerability, prey size, and the predator's motivation to eat. Thus, feeding motivation and prey visual cues are supposed to influence predator decisions and it is predicted that prey selection by visual cues is modulated by the predator's stomach fullness prior to attacking a prey. This study was conducted using an animal model from the rocky shores ecosystem, a predatory fish, the frillfin goby Bathygobius soporator, and a benthic prey, the mottled shore crab Pachygrapsus transversus. Our results demonstrate that frillfin gobies are capable of visually evaluating prey size and that the size evaluation process is modulated by the level of stomach fullness. Predators with an empty stomach (0% fullness) attacked prey that was larger than the predicted optimal size. Partially satiated predators (50% stomach fullness) selected prey close to the optimal size, while fully satiated predators (100% stomach fullness) showed no preference for size. This finding indicates an integrative response of the predator that depends on the input of both internal and external sensory information when choosing prey. Predator perceptions of visual cues (prey size) and stomach fullness modulate foraging decisions. As a result, a flexible feeding behaviour emerges, evidencing a clearly adaptive response in line with optimal foraging theory predictions.     

The Relationship Between Foraging Ecology and Lizard Chemoreception: Can a Snake Analogue (Burton’s Legless Lizard,Lialis burtonis) Detect Prey Scent?

In lizards and snakes, foraging mode (active vs. ambush) is highly correlated with the ability to detect prey chemical cues, and the way in which such cues are utilized. Ambush-foraging lizards tend not to recognize prey scent, whereas active foragers do. Prey scent often elicits strikes in actively-foraging snakes, while ambushers use it to select profitable foraging sites. We tested the influence of foraging ecology on the evolution of squamate chemoreception by gauging the response of Burton's legless lizard ( Lialis burtonis Gray, Pygopodidae) to prey chemical cues. Lialis burtonis is the ecological equivalent of an ambush-foraging snake, feeding at infrequent intervals on relatively large prey, which are swallowed whole. Captive L. burtonis did not respond to prey odour in any manner: prey chemical cues did not elicit elevated tongue-flick rates or feeding strikes, nor were they utilized in the selection of ambush sites. Like other ambushing lizards, L. burtonis appears to be a visually oriented predator. In contrast, an active forager in the same family, the common scaly-foot ( Pygopus lepidopodus ), did tongue-flick in response to odours of its preferred prey. These results extend the correlation between lizard foraging mode and chemosensory abilities to a heretofore-unstudied family, the Pygopodidae.     

Prey Detection in Two Tit Species,Parus ater and P. cristatus

We studied the prey-detection response of two related tit species (Parus ater, coal tit, and P. cristatus, crested tit) which occur in similar habitats and which are separated by microhabitat use and mode of locomotion. Specifically, we tested whether the two species differ in their ability to detect cryptic prey, with the hypothesis that coal tits perform better because of their longer stays in microhabitat patches. We expected that interspecific differences and the flexible responses within species to different levels of prey crypticity both depend on search intensity. In the experiments, tits had to forage in four different prey conditions: conspicuous + small, conspicuous + large, cryptic + small, and cryptic + large. Capture success, the time needed to detect prey, and stare duration were measured. Both species were less successful with cryptic than with conspicuous prey and did worst with small and cryptic prey. They also needed more time for detection and stared longer when prey was cryptic. When prey had been overlooked, preceding stare durations were shorter than those ending in successful searches. There were clear differences between the species in performance, with the crested tit doing worse. Coal tits, on average, were more successful in detecting prey, returned less frequently to already emptied patches, detected prey faster and yet they stared more briefly. The within-species results support current notions on predator search, but the differences between species cannot be explained with the same mechanisms. We discuss these findings in the context of the foraging ecology of these species and conclude that crested tits use different cues to detect prey and/or search a larger area per unit time.     

Foraging success of juvenile pike Esox lucius depends on visual conditions and prey pigmentation

Young-of-the-year pike Esox lucius foraging on copepods experienced different foraging success depending on prey pigmentation in water visually degraded by brown colouration or algae. Both attack rate and prey consumption rate were higher for E. lucius foraging on transparent prey in brown water, whereas the opposite was true in algal turbid water. Pigments in copepod prey may have a cryptic function in brown water instead of a photo-protective function even if prey-size selectivity was stronger than selection based on pigmentation in juvenile E. lucius.     

Olfactory and visual plant cues as drivers of selective herbivory

Food quality is an important consideration in the foraging strategy of all animals, including herbivores. Those that can detect and assess the nutritional value of plants from afar, using senses such as smell and sight, can forage more efficiently than those that must assess food quality by taste alone. Selective foraging not only affects herbivore fitness but can influence the structure and composition of plant communities, yet little is known about how olfactory and visual cues help herbivores to find preferred plants. We tested the ability of a free‐ranging, generalist mammalian browser, the swamp wallaby Wallabia bicolor, to use olfactory and visual plant cues to find and/or browse differentially on Eucalyptus pilularis seedlings grown under different nutrient conditions. Low‐nutrient seedlings differed from high‐nutrient seedlings, having lighter coloured leaves, red stems and lower biomass and nitrogen content. In the absence of visual cues, wallabies used odour to differentiate vials containing cut seedlings. They visited and investigated patches with high‐nutrient seedling odour most, followed by patches with low‐nutrient seedling odour, and patches with no added odour least. However, when visual and olfactory cues of seedlings were present, wallabies reversed their foraging response and were more likely to browse low‐ than high‐nutrient seedlings. This browsing difference, in turn, disappeared when long‐range visual cues were reduced by pinning seedlings horizontal to the ground. We suggest that visual cues overrode the effects of olfactory cues on browsing patterns of intact seedlings. Our study shows that herbivores can respond to odours of higher nutrient plants but in ecologically realistic scenarios they use a variety of visual and olfactory cues, with a context‐dependent outcome that is not always selection of high nutrient food. Our results demonstrate the importance of testing the sensory abilities of herbivores in realistic multi‐sensory settings to understand their function in selective foraging.     

Population and behavioural responses of native prey to alien predation

The introduction of invasive alien predators often has catastrophic effects on populations of naïve native prey, but in situations where prey survive the initial impact a predator may act as a strong selective agent for prey that can discriminate and avoid it. Using two common species of Australian small mammals that have persisted in the presence of an alien predator, the European red fox Vulpes vulpes, for over a century, we hypothesised that populations of both would perform better where the activity of the predator was low than where it was high and that prey individuals would avoid signs of the predator’s presence. We found no difference in prey abundance in sites with high and low fox activity, but survival of one species—the bush rat Rattus fuscipes—was almost twofold higher where fox activity was low. Juvenile, but not adult rats, avoided fox odour on traps, as did individuals of the second prey species, the brown antechinus, Antechinus stuartii. Both species also showed reduced activity at foraging trays bearing fox odour in giving-up density (GUD) experiments, although GUDs and avoidance of fox odour declined over time. Young rats avoided fox odour more strongly where fox activity was high than where it was low, but neither adult R. fuscipes nor A. stuartii responded differently to different levels of fox activity. Conservation managers often attempt to eliminate alien predators or to protect predator-naïve prey in protected reserves. Our results suggest that, if predator pressure can be reduced, otherwise susceptible prey may survive the initial impact of an alien predator, and experience selection to discriminate cues to its presence and avoid it over the longer term. Although predator reduction is often feasible, identifying the level of reduction that will conserve prey and allow selection for avoidance remains an important challenge.     

Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence

Anti-predator behaviors often entail foraging costs, and thus prey response to predator cues should be adjusted to the level of risk (threat-sensitive foraging). Simultaneously dangerous predators (with high hunting success) should engender the evolution of innate predator recognition and appropriate anti-predator behaviors that are effective even upon the first encounter with the predator. The above leads to the prediction that prey might respond more strongly to cues of dangerous predators that are absent, than to cues of less dangerous predators that are actually present. In an applied context this would predict an immediate and stronger response of ungulates to the return of top predators such as wolves (Canis lupus) in many parts of Europe and North America than to current, less threatening, mesopredators. We investigated the existence of innate threat-sensitive foraging in black-tailed deer. We took advantage of a quasi-experimental situation where deer had not experienced wolf predation for ca. 100 years, and were only potentially exposed to black bears (Ursus americanus). We tested the response of deer to the urine of wolf (dangerous) and black bear (less dangerous). Our results support the hypothesis of innate threat-sensitive foraging with clear increased passive avoidance and olfactory investigation of cues from wolf, and surprisingly none to black bear. Prey which have previously evolved under high risk of predation by wolves may react strongly to the return of wolf cues in their environments thanks to innate responses retained during the period of predator absence, and this could be the source of far stronger non-consumptive effects of the predator guild than currently observed.     

Predator pheromone elicits a temporally dependent non-consumptive effect in prey

1. The influence of predator cues on the behaviour of prey is well supported in the literature; however, a clear understanding of how predator cues affect prey in variable environmental conditions and over longer time scales is needed to better understand the underlying mechanisms. Here, we measure how predator odors affect herbivore colonization, abundance, oviposition, and plant damage across two growing seasons.
2. The study system consisted of Leptinotarsa decemlineata (Colorado potato beetle) as prey, and the aggregation pheromone of live Podisus maculiventris (spined soldier bug) as the predator cue in a potato field.
3. In 2016, the amount of feeding damage by early beetle colonists was lower in predator odor-treated plots, reducing plant damage by 22%. Larval abundance was also reduced in treated plots in 2016. Beetle abundance and damage in 2017 was similar in the treatment and control plots. Two mechanisms were investigated to better understand why prey response to the predator odor treatment weakened over the first season, including changes in predator odor cue strength and prey habituation. Predator odor cue strength emerged as a likely explanation, as dispensers, which released a synthetic predator pheromone over the entire season, reduced the probability of finding damage more consistently than the live predator treatment.
4. These results suggest that temporal patterns of predator cue release and strength may drive prey response across the season, underscoring the importance of cue release-rate and consistency in both species interactions and for the future application of modifying insect behaviour using non-consumptive effects in agricultural systems.

     

Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters

Structural features of habitat are known to affect the density of predators and prey, and it is generally accepted that complexity provides some protection from the environment and predators but may also reduce foraging success. A next step in understanding these interactions is to decouple the impacts of both spatial and trophic ingredients of complexity to explicitly explore the trade-offs between the habitat, its effects on foraging success, and the competition that ensues as predator densities increase. We quantified the accumulation of spiders and their prey in habitat islands with different habitat complexities created in the field using natural plants, plant debris and plastic plant mimics. Spiders were observed at higher densities in the complex habitat structure composed of both live plants and thatch. However, the numerically dominant predator in the system, the wolf spider Pardosa milvina, was observed at high densities in habitat islands containing plastic mimics of plants and thatch. In a laboratory experiment, we examined the interactive effects of conspecific density and habitat on the prey capture of P. milvina. Thatch, with or without vertical plant structure, reduced prey capture, but the plastic fiber did not. Pairwise interactions among spiders reduced prey capture, but this effect was moderated by thatch. Taken together, these experiments highlight the flexibility of one important predator in the food web, where multiple environmental cues intersect to explain the role of habitat complexity in determining generalist predator accumulation.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.     

Predator Inspection Behaviour in a Characin Fish: an Interaction between Chemical and Visual Information?

Recent evidence suggests that predator inspection behaviour by Ostariophysan prey fishes is regulated by both the chemical and visual cues of potential predators. In laboratory trials, we assessed the relative importance of chemical and visual information during inspection visits by varying both ambient light (visual cues) and predator odour (chemical cues) in a 2 × 2 experimental design. Shoals of glowlight tetras (Hemigrammus erythrozonus) were exposed to a live convict cichlid (Archocentrus nigrofasciatus) predator under low (3 lux) or high (50 lux) light levels and in the presence of the odour of a cichild fed tetras (with an alarm cue) or swordtails (Xiphophorus helleri, with an alarm cue not recognized by tetras). Tetras exhibited threat‐sensitive inspection behaviour (increased latency to inspect, reduced frequency of inspection, smaller inspecting group sizes and increased minimum approach distance) towards a predator paired with a tetra‐fed diet cue, regardless of light levels. Similar threat‐sensitive inspection patterns were observed towards cichlids paired with a swordtail‐fed diet cue only under high light conditions. Our data suggest that chemical cues in the form of prey alarm cues in the diet of the predator, are the primary source of information regarding local predation risk during inspection behaviour, and that visual cues are used when chemical information is unavailable or ambiguous.     

Spatial variability in prey phenology determines predator movement patterns and prey survival

Species have phenological variation among local habitats that are located at relatively small spatial scales. However, less studies have tested how this spatial variability in phenology can mediate intra-/inter-specific interactions. When predators track phenological variation of prey among local habitats, survival of prey within a local habitat strongly influenced by phenological synchrony with their conspecifics in adjacent habitats. Theory predicts that phenological synchrony among local habitats increases prey survival in local habitat within spatially structured environments because the predators have to make a habitat choice for foraging. Consequently, total survival of prey at regional scale should be higher. By using a spatially explicit field experiment, we tested above hypothesis using a prey–predator interaction between tadpole (Rhacophorus arboreus) and newt (Cynops pyrrhogaster). We established enclosures (≈regional scale) consisting of two tanks (≈local habitat scale) with different degree of prey phenological synchrony. We found that phenological synchrony of prey between tanks within each enclosure decreased the mean residence time of the predator in each tank, which resulted in higher survival of prey at a local habitat scale, supporting the theoretical prediction. Furthermore, individual-level variation in predator residence time explained the between-tank variation in prey survival in enclosures with phenological synchrony, implying that movement patterns of the predator can mediate variation in local population dynamics of their prey. However, total survival at each enclosure was not higher under phenological synchrony. These results suggest the importance of relative timing of prey phenology, not absolute timing, among local habitats in determining prey–predator interactions.     

Signal evolution in prey recognition systems

In this paper a graphical model first developed in the context of kin recognition is adapted to the study of signalling in predator-prey systems. Antipredation strategies are envisioned as points along a signal-to-noise (S/N) axis, with concealing (low S/N) and conspicuous (high S/N) strategies being placed at opposite sides of this axis. Optimal prey recognition systems should find a trade-off between acceptance errors (going after a background cue as if it were a prey) and rejection errors (not going after a prey as if it were background noise). The model also predicts the types of cues the predator should use in opposite sides of the S/N axis.     

Behavioural responses of free‐ranging western grey kangaroos (Macropus fuliginosus) to olfactory cues of historical and recently introduced predators

Predation risk influences foraging decisions and time allocation of prey species, and may result in habitat shifts from potentially dangerous to safer areas. We examined a wild population of western grey kangaroos (Macropus fuliginosus) to test the efficacy of predator faecal odour in influencing time allocated to different behaviours and inducing changes in habitat use. Kangaroos were exposed to fresh faeces of a historical predator, the dingo (Canis lupus dingo), a recently introduced predator, the red fox (Vulpes vulpes), a herbivore (horse, Equus caballus) and an unscented control simultaneously. Kangaroos did not increase vigilance in predator‐scented areas. However, they investigated odour sources by approaching and sniffing; more time was spent investigating fox odour than control odours. Kangaroos then exhibited a clear anti‐predator response to predator odours, modifying their space use by rapidly escaping, then avoiding fox and dingo odour sources. Our results demonstrate that wild western grey kangaroos show behavioural responses to predator faeces, investigating then avoiding these olfactory cues of potential predation risk, rather than increasing general vigilance. This study contributes to our understanding of the impact of introduced mammalian predators on marsupial prey and demonstrates that a native Australian marsupial can recognize and respond to the odour of potential predators, including one that has been recently introduced.     

Predator hunting modes and predator–prey space games

Predators and prey are often engaged in a game where their expected fitnesses are affected by their relative spatial distributions. Game models generally predict that when predators and prey move at similar temporal and spatial scales that predators should distribute themselves to match the distribution of the prey's resources and that prey should be relatively uniformly distributed. These predictions should better apply to sit-and-pursue and sit-and-wait predators, who must anticipate the spatial distributions of their prey, than active predators that search for their prey. We test this with an experiment observing the spatial distributions and estimating the causes of movements between patches for Pacific tree frog tadpoles (Pseudacris regilla), a sit-and-pursue dragonfly larvae predator (Rhionaeschna multicolor), and an active salamander larval predator (Ambystoma tigrinum mavortium) when a single species was in the arena and when the prey was with one of the predators. We find that the sit-and-pursue predator favors patches with more of the prey's algae resources when the prey is not in the experimental arena and that the prey, when in the arena with this predator, do not favor patches with more resources. We also find that the active predator does not favor patches with more algae and that prey, when with an active predator, continue to favor these higher resource patches. These results suggest that the hunting modes of predators impact their spatial distributions and the spatial distributions of their prey, which has potential to have cascading effects on lower trophic levels.     

Can prey behaviour induce spatially synchronic aggregation of solitary predators?

Spatio-temporal patterns of predator aggregations within their settlement areas (i.e. temporary settling zones used during dispersal or, more generally, foraging patches) were studied. By integrating the main behavioural rules of juveniles of Spanish imperial eagles Aquila adalberti during dispersal with the temporal availability of the eagles' main prey, we have developed several individual-based models under different simulation scenarios. The results suggest that the spatially synchrony of the aggregation patterns that we observed were derived from a combination of behavioural responses of the prey and the distances between available settlement areas. These results are discussed in the context of predator–prey relationships, optimal foraging and self-organizing processes.     

Effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird beetle

The effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird, Harmonia axyridis , were investigated by using a 2 × 2 factorial design in large scale cages. Prey density influenced prey consumption of the ladybirds, and the frequency with which predation occurred was quite different between the prey distributions. The ladybirds consumed a relatively constant and small number of aphids when the prey were uniformly distributed, whereas the number of prey consumed per day when predation occurred was large and much more variable when the prey were contagiously distributed. At high prey density, the number of prey consumed was highest during the first day of the experiment; thereafter, only 10–20 aphids were consumed during the following 3 days. However, these patterns of prey consumption were not observed at low prey density. The percentage of aphids that remained on the host plants when the experiments were terminated was higher at low prey density than at high prey density, suggesting that predator foraging efficiency at low prey density was lower than at high prey density. Ladybirds foraging for high prey density were more frequently observed on the plants with aphids than ladybirds foraging for low prey density. Prey distribution also influenced the frequency of residence of ladybirds on the plants. The different predation patterns observed in the two spatial distributions, in which prey consumption was much more variable for the contagious distribution, might be explained by the difference in prey encounter rate of the predator between the distributions. This study indicated that the ladybirds had limited ability to search out prey over large spatial scales.