Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations

Understanding the factors that influence the ability of predators to find and kill herbivores is central to enhancing their impact on prey populations, but few studies have tested the impact of these factors on predation rates in realistic foraging environments. Using the tri‐trophic system consisting of tomato, Solanum lycopersicum L. (Solanaceae), hornworm caterpillars, Manduca sexta L. (Lepidoptera: Sphingidae), and the predaceous stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae), we measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, we compared experienced vs. naive individuals under varying environmental contexts. Experienced predators were those with prior exposure to induced volatiles from the tomato–caterpillar association, whereas naive predators had not experienced tomato, only prey (caterpillars). We varied their environmental foraging matrix using either (1) tomato surrounded by basil (Ocimum basilicum L.; Lamiaceae) or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). We found that (1) experienced predators were more efficient than naive predators, capturing 28% more prey; (2) the tomato–basil combination did not affect predator–prey interactions; and (3) constitutive emission of synthetic MeSA caused a 22% reduction in P. maculiventris predation rate. These differences corresponded with distinct shifts in predator foraging; for example, experienced individuals were less stationary and exhibited unique behaviors such as stylet extension. Taken together, these results suggest that it is possible to improve the function of generalist predators in suppressing prey by coupling odors with food. However, constitutive emission of volatiles to attract natural enemies may ultimately camouflage neighboring plants, reducing the benefits of orientation to learned stimuli such as induced volatiles.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude‐specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space‐for‐time substitution to inform how predator–prey interaction may gradually evolve to long‐term warming.     

Density-dependent prey behaviours and mutable predator foraging modes induce Allee effects and over-prediction of prey mortality rates

1. Predator–prey models are often used to represent consumptive interactions between species but, typically, are derived using simple experimental systems with little plasticity in prey or predator behaviours. However, many prey and predators exhibit a broad suite of behaviours. Here, we experimentally tested the effect of density-dependent prey and predator behaviours on per capita relative mortality rates using Florida bass (Micropterus floridanus) consuming juvenile Bluegill (Lepomis macrochirus).
2. Experimental ponds were stocked with a factorial design of low, medium, and high prey and predator densities. Prey mortality, prey–predator behaviours, and predator stomach contents were recorded over or after 7 days. We assumed the mortality dynamics followed foraging arena theory. This pathologically flexible predator–prey model separates prey into invulnerable and vulnerable pools where predators can consume prey in the latter. As this approach can represent classic Lotka–Volterra and ratio-dependent dynamics, we fit a foraging arena predator–prey model to the number of surviving prey.
3. We found that prey exhibited density-dependent prey behaviours, hiding at low densities, shoaling at medium densities, and using a provided refuge at high densities. Predators exhibited ratio-dependent behaviours, using an ambush foraging mode when one predator was present, hiding in the shadows at low prey–high predator densities, and shoaling at medium and high prey–high predator densities. The foraging arena model predicted the mortality rates well until the high prey–high predator treatment where group vigilance prey behaviours occurred and predators probably interfered with one another resulting in the model predicting higher mortality than observed.
4. This is concerning given the ubiquity of predator–prey models in ecology and natural resource management. Furthermore, as Allee effects engender instability in population regulation, it could lead to inaccurate predictions of conservation status, population rebuilding or harvest rates.

     

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Associations between Non‐Lethal Injury,Body Size,and Foraging Ecology in an Amphibian Intraguild Predator

Theoretical treatments of intraguild predation and its effects on behavioral interactions regard the phenomenon as a size‐structured binary response wherein predation among competitors is completely successful or completely unsuccessful. However, intermediate outcomes occur when individuals escape intraguild (IG) interactions with non‐lethal injuries. While the effects of wounds for prey include compromised mobility and increased predation risk, the consequences of similar injuries among top predators are not well understood, despite the implications for species interactions. Using an amphibian IG predator, Ambystoma opacum (Caudata: Ambystomatidae), we examined associations between non‐lethal injuries and predator body size, foraging strategy, microhabitat selection, and intraspecific agonistic interactions. Wounds were common among IG predators, generally increasing in frequency throughout larval ontogeny. Non‐lethal injuries were associated with differences in predator body size and behavior, with injured predators exhibiting smaller body sizes, increased use of benthic microhabitats, reduced agonistic displays, and increased risk of intraspecific aggression. While such effects were not ultimately associated with reduced foraging success, non‐lethal injury could contribute to niche partitioning between injured and healthy predators via habitat selection, but injured predators likely continue to exert predatory pressure on IG and basal prey populations. Our results indicate that studies of top‐down population regulation should incorporate injury‐related modifications to both prey and predator behavior and size structure.     

Exploratory behaviour and novel predator recognition: behavioural correlations across contexts

It was hypothesized that the exploratory behaviour of an individual measured in a novel environment could predict its behaviour in response to a novel predator. This study examined novel predator recognition in the western mosquitofish Gambusia affinis, a species with individual differences in risk‐taking, activity and exploration in novel environments. Prey responded with characteristic shoaling and avoidance in response to native predators, but did not show characteristic antipredator behaviour towards novel predators. Furthermore, G. affinis exhibited individual‐level behavioural correlations across contexts but only when prey were tested with native predators. This could be the result of native predatory selection on behavioural correlations in the prey species.     

Short‐term prey field lability constrains individual specialisation in resource selection and foraging site fidelity in a marine predator

Spatio‐temporally stable prey distributions coupled with individual foraging site fidelity are predicted to favour individual resource specialisation. Conversely, predators coping with dynamic prey distributions should diversify their individual diet and/or shift foraging areas to increase net intake. We studied individual specialisation in Scopoli's shearwaters (Calonectris diomedea) from the highly dynamic Western Mediterranean, using daily prey distributions together with resource selection, site fidelity and trophic‐level analyses. As hypothesised, we found dietary diversification, low foraging site fidelity and almost no individual specialisation in resource selection. Crucially, shearwaters switched daily foraging tactics, selecting areas with contrasting prey of varying trophic levels. Overall, information use and plastic resource selection of individuals with reduced short‐term foraging site fidelity allow predators to overcome prey field lability. Our study is an essential step towards a better understanding of individual responses to enhanced environmental stochasticity driven by global changes, and of pathways favouring population persistence.     

Interactions of multiple predators with different foraging modes in an aquatic food web

Top predators can have different foraging modes that may alter their interactions and effects on food webs. Interactions between predators may be non-additive resulting from facilitation or interference, whereas their combined effects on a shared prey may result in emergent effects that are risk enhanced or risk reduced. To test the importance of multiple predators with different foraging modes, we examined the interaction between a cruising predator (largemouth bass, Micropterus salmoides) and an ambush predator (muskellunge, Esox masquinongy) foraging on a shared prey (bluegill sunfish, Lepomis macrochirus) with strong anti-predator defense behaviors. Additive and substitution designs were used to compare individual to combined predator treatments in experimental ponds. The multiple predator interaction facilitated growth of the cruising predator in the combined predator treatments, whereas predator species had substitutable effects on the growth of the ambush predator. The combined predator treatments created an emergent effect on the prey; however, the direction was dependent on the experimental design. The additive design found a risk-reducing effect, whereas the substitution design found a risk-enhancing effect for prey fish. Indirect effects from the predators weakly extended to lower trophic levels (i.e., zooplankton community). Our results highlight the need to consider differences in foraging mode of top predators, interactions between predators, and emergent effects on prey to understand food webs.     

Does a top predator reduce the predatory impact of an invasive mesopredator on an endangered rodent?

The mesopredator release hypothesis (MRH) predicts that reduced abundance of top‐order predators results in an increase in the abundance of smaller predators (mesopredators) due to a reduction in intra‐guild predation and competition. The irruption of mesopredators that follows the removal of top‐order predators can have detrimental impacts on the prey of the mesopredators. Here we investigated the mechanisms via which the presence of a top‐order predator can benefit prey species. We tested predictions made according to the MRH and foraging theory by contrasting the abundances of an invasive mesopredator (red fox Vulpes vulpes) and an endangered prey species (dusky hopping mouse Notomys fuscus), predator diets, and N. fuscus foraging behaviour in the presence and absence of a top‐predator (dingo Canis lupus dingo). As predicted by the MRH, foxes were more abundant where dingoes were absent. Dietary overlap between sympatric dingoes and foxes was extensive, and fox was recorded in 1 dingo scat possibly indicating intra‐guild predation. Notomys fuscus were more likely to occur in fox scats than dingo scats and as predicted by the MRH N. fuscus were less abundant in the absence of dingoes. The population increase of N. fuscus following rainfall was dampened in the absence of dingoes suggesting that mesopredator release can attenuate bottom‐up effects, although it remains conceivable that differences in grazing regimes associated with dingo exclusion could have also influenced N. fuscus abundance. Notomys fuscus exhibited lower giving‐up densities in the presence of dingoes, consistent with the prediction that their perceived risk of predation would be lower and foraging efficiency greater in the presence of a top‐predator. Our results suggest that mesopredator suppression by a top predator can create a safer environment for prey species where the frequency of fatal encounters between predators and prey is reduced and the non‐consumptive effects of predators are lower.     

Predator–prey interactions: why do larger albatrosses eat bigger squid?

The relationship between predator sizes and prey sizes is well documented for terrestrial but rarely for marine ecosystems. We show that wandering albatrosses, the biggest albatross species, feed on larger cephalopod prey than those consumed by smaller albatrosses (grey-headed and black-browed albatrosses). This reflects differences in timing of breeding, foraging ecology and their feeding methods. Wandering albatrosses breed later in the year, during the austral winter, than smaller albatrosses (therefore catching older squid) and forage most of the year in Antarctic open waters, sub-Antarctic, subtropical and tropical waters, overlapping minimally with the smaller albatrosses' foraging range while breeding. Also, wandering albatrosses mostly scavenge whereas smaller albatrosses feed more on live prey. Prey ecology may also play a key role because many squid species might experience post-spawning mortality during the austral winter, becoming easily available to wandering albatrosses. Spawning in winter can be linked to predator avoidance (i.e. reduction in mortality in winter by avoiding pelagic predators) and would allow squid larvae to develop and take advantage of the high productivity (i.e. Antarctic phytoplankton bloom) in spring and at the beginning of summer. Thus, aspects of prey and predator ecology may combine to generate observed differences in prey size.     

Indirect cues in selecting a hunting site in a sit‐and‐wait predator

Sit‐and‐wait predators use relatively simple rules for their decisions to choose and leave a patch, such as using the direct presence of prey to select a hunting site. However, the direct presence of prey can only be used when there is a highly visited patch in the proximity of the predator. Therefore, it is plausible that sit‐and‐wait predators also exploit indirect cues of prey presence and, consequently, use associative learning to select a hunting site. The present study tests for the role of associative learning in a sit‐and‐wait predator species for which the ecology is well understood: Misumena vatia Clerck crab spiders. An ecologically relevant scenario is used by selecting flower colour as the conditioned stimulus and prey presence as the unconditioned stimulus. The results provide no evidence that M. vatia crab spiders use the association between flower colour and food presence for selecting a hunting site. After a training phase of being exposed to a colourful artificial flower highly visited by bees, spiders select a hunting site independently of its colour during the testing phase. Investigations of similar scope and ecological relevance are required with other sit‐and‐wait predators to identify the conditions promoting the use of associative learning for foraging site selection when animals face an unpredictable food supply.     

Prey density affects predator foraging strategy in an Antarctic ecosystem

Studying the effects of prey distribution on predator behavior is complex in systems where there are multiple prey species. The role of prey density in predator behavior is rarely studied in closed ecosystems of one predator species and one prey species, despite these being an ideal opportunity to test these hypotheses. In this study, we investigate the effect of prey density on the foraging behavior of a predatory species in an isolated Antarctic ecosystem of effectively a single predatory species and a single prey species. We use resource selection models to compare prey density in areas utilized by predators (obtained from fine‐scale GPS telemetry data) to prey density at randomly generated points (pseudoabsences) throughout the available area. We demonstrate that prey density of breeding Antarctic petrels (Thalassoica antarctica) is negatively associated with the probability of habitat use in its only predator, the south polar skua (Catharacta maccormicki). Skuas are less likely to utilize habitats with higher petrel densities, reducing predation in these areas, but these effects are present during chick rearing only and not during incubation. We suggest that this might be caused by successful group defense strategies employed by petrel chicks, primarily spitting oil at predators.     

Inside‐container effects drive mosquito community structure in Brazilian Atlantic forest

Metacommunity theory is a convenient framework in which to investigate how local communities linked by dispersal influence patterns of species distribution and abundance across large spatial scales. For organisms with complex life cycles, such as mosquitoes, different pressures are expected to act on communities due to behavioral and ecological partitioning of life stages. Adult females select habitats for oviposition, and resulting offspring are confined to that habitat until reaching adult stages capable of flight; outside‐container effects (OCE) (i.e., spatial factors) are thus expected to act more strongly on species distributions as a function of adult dispersal capability, which should be limited by geographic distances between sites. However, larval community dynamics within a habitat are influenced by inside‐container effects (ICE), mainly interactions with conspecifics and heterospecifics (e.g., through effects of competition and predation). We used a field experiment in a mainland‐island scenario to assess whether environmental, spatial, and temporal factors influence mosquito prey and predator distributions and abundances across spatial scales: within‐site, between‐site, and mainland‐island. We also evaluated whether predator abundances inside containers play a stronger role in shaping mosquito prey community structure than do OCE (e.g., spatial and environmental factors). Temporal influence was more important for predators than for prey mosquito community structure, and the changes in prey mosquito species composition over time appear to be driven by changes in predator abundances. There was a negligible effect of spatial and environmental factors on mosquito community structure, and temporal effects on mosquito abundances and distributions appear to be driven by changes in abundance of the dominant predator, perhaps because ICE are stronger than OCE due to larval habitat restriction, or because adult dispersal is not limited at the chosen spatial scales.     

Prey‐specific foraging tactics in a web‐building spider

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Autotomy and its Effects on Wolf Spider Foraging Success

Few studies have attempted to determine how physical injury affects predators. One of the ways that physical injury can be expressed is by autotomy or the voluntary loss of a body part. Here, we examined whether the loss of specific legs affects the foraging success of the wolf spider Rabidosa santrita (predator) on another species, Pardosa valens (prey). We also wanted to identify whether the loss of legs in both the predator and prey would impact the outcome of a predation event. Both predator and prey were collected from a creek bed at Portal, AZ, in 2012. Predators were randomly assigned groups where all prey items were intact or all prey had one randomly chosen leg IV removed. Within these groups, predators were organized into a control, leg I autotomy, or leg IV autotomy treatment. All predators had their pre‐ and post‐foraging running speed determined. Predators were introduced into chambers with five prey items and allowed to forage for 1 h. The leg position autotomized or the comparison of pre‐ and post‐foraging trials had no effect on predator running speed. Additionally, there was no significant effect of either predator or prey leg treatment on the total proportion of prey items captured by the end of the foraging trials. Survival analyses indicated that intact prey items tended to have a higher survival rate when predators were missing a leg IV than when predators were intact. When both the predator and prey were missing legs, no significant difference in prey survival rates was detected. We suggest that for predators that inhabit complex, heterogeneous habitats and are classified as ambush predators, the loss of a limb may affect prey capture success, especially when the prey is intact, but that increased sample size is necessary to determine whether this trend is significant.     

Variation in foraging success among predators and its implications for population dynamics

The effects of the expected predation rate on population dynamics have been studied intensively, but little is known about the effects of predation rate variability (i.e., predator individuals having variable foraging success) on population dynamics. In this study, variation in foraging success among predators was quantified by observing the predation of the wolf spider Pardosa pseudoannulata on the cricket Gryllus bimaculatus in the laboratory. A population model was then developed, and the effect of foraging variability on predator–prey dynamics was examined by incorporating levels of variation comparable to those quantified in the experiment. The variability in the foraging success among spiders was greater than would be expected by chance (i.e., the random allocation of prey to predators). The foraging variation was density‐dependent; it became higher as the predator density increased. A population model that incorporates foraging variation shows that the variation influences population dynamics by affecting the numerical response of predators. In particular, the variation induces negative density‐dependent effects among predators and stabilizes predator–prey dynamics.     

Oxygen minimum zone: An important oceanographic habitat for deep‐diving northern elephant seals,Mirounga angustirostris

Little is known about the foraging behavior of top predators in the deep mesopelagic ocean. Elephant seals dive to the deep biota‐poor oxygen minimum zone (OMZ) (>800 m depth) despite high diving costs in terms of energy and time, but how they successfully forage in the OMZ remains largely unknown. Assessment of their feeding rate is the key to understanding their foraging behavior, but this has been challenging. Here, we assessed the feeding rate of 14 female northern elephant seals determined by jaw motion events (JME) and dive cycle time to examine how feeding rates varied with dive depth, particularly in the OMZ. We also obtained video footage from seal‐mounted videos to understand their feeding in the OMZ. While the diel vertical migration pattern was apparent for most depths of the JME, some very deep dives, beyond the normal diel depth ranges, occurred episodically during daylight hours. The midmesopelagic zone was the main foraging zone for all seals. Larger seals tended to show smaller numbers of JME and lower feeding rates than smaller seals during migration, suggesting that larger seals tended to feed on larger prey to satisfy their metabolic needs. Larger seals also dived frequently to the deep OMZ, possibly because of a greater diving ability than smaller seals, suggesting their dependency on food in the deeper depth zones. Video observations showed that seals encountered the rarely reported ragfish (Icosteus aenigmaticus) in the depths of the OMZ, which failed to show an escape response from the seals, suggesting that low oxygen concentrations might reduce prey mobility. Less mobile prey in OMZ would enhance the efficiency of foraging in this zone, especially for large seals that can dive deeper and longer. We suggest that the OMZ plays an important role in structuring the mesopelagic ecosystem and for the survival and evolution of elephant seals.