Non-consumptive Effects Of Predators Research Articles

Habitat use of sympatric prey suggests divergent anti-predator responses to recolonizing gray wolves.

The non-consumptive effects of predators on prey are now widely recognized, but the need remains for studies identifying the factors that determine how particular prey species respond behaviorally when threatened with predation. We took advantage of ongoing gray wolf (Canis lupus) recolonization in eastern Washington, USA, to contrast habitat use of two sympatric prey species-mule (Odocoileus hemionus) and white-tailed (O. virginianus) deer-at sites with and without established wolf packs. Under the hypothesis that the nature and scale of responses by these ungulates to wolf predation risk depend on their divergent flight tactics (i.e., modes of fleeing from an approaching predator), we predicted that (1) mule deer would respond to wolves with coarse-scale spatial shifts to rugged terrain favoring their stotting tactic; (2) white-tailed deer would manage wolf risk with fine-scale shifts toward gentle terrain facilitating their galloping tactic within their current home range. Resource selection functions based on 61 mule deer and 59 white-tailed deer equipped with GPS radio-collars from 2013 to 2016 revealed that habitat use for each species was altered by wolf presence, but in divergent ways that supported our predictions. Our findings add to a growing literature highlighting flight behavior as a viable predictor of prey responses to predation risk across multiple ecosystem types. Consequently, they suggest that predators could initiate multiple indirect non-consumptive effects in the same ecosystem that are transmitted by divergent responses of sympatric prey with different flight tactics.

Total Non-Consumptive Effects of Fish on Pelobates fuscus and Hyla orientalis Tadpoles in Pond Enclosure Experiments.

Most research on non-consumptive predator effects on amphibian larvae has been conducted in laboratory or mesocosm designs. Here, Pelobates fuscus and Hyla orientalis tadpoles were separately exposed to non-lethal (free-moving, but with tied mouthparts) common carp Cyprinus carpio for one week in enclosures placed in a pond densely stocked with fish. Tadpoles exposed to nonlethal fish did not differ in mortality, body mass, or, except for deeper tail fin depth in P. fuscus, morphological plasticity from controls kept in a fishless pond. Hyla orientalis tadpoles recovered from the fish treatment were subsequently enclosed until metamorphosis in either the pond with fish or the fishless pond. Metamorphs from the pond containing fish were heavier, and did not differ in survivorship or development time from their counterparts initially kept in the fish treatment and then transferred to the fishless pond or from controls kept the entire time under fish-free conditions. The lack of apparent metamorphic costs is consistent with previous experiments on anuran larvae, but the morphological defenses induced (or their absence) are not. In the fish-dominated pond, carp indirectly affected tadpole developmental responses by generating turbidity, through adverse impacts on submerged vegetation and predatory insects, and by increasing food resource (unicellular algae) levels. While the present study does not question the validity of laboratory and mesocosm experiments on the costs of non-consumptive predator effects on amphibian larvae, their outcomes cannot easily be extrapolated to ecologically complex natural habitats.

Consumptive and non-consumptive effects of predatory arthropods on billbug (Coleoptera: Dryophthoridae) pests in turfgrass

Generalist predators affect pest populations through direct consumption or by non-consumptive effects, whereby predators induce changes in prey behavior which represent a cost to prey. A diverse community of predatory arthropods has been described in turfgrass, contributing to the direct mortality of pests including black cutworm, fall armyworm, and Japanese beetle. Billbugs are a major pest of turfgrass in the Intermountain West, but the composition of the local predatory arthropod community and whether predators aid in billbug suppression through consumptive or non-consumptive effects is unknown. First, we catalogued the predatory arthropod community on Utah and Idaho golf courses using linear pitfall traps. Then, we assessed adult billbug consumption by resident predators in the field. Using a series of lab assays, we assessed the most abundant predators’ consumption of billbug life stages, including adults, sentinel waxworm larvae at varied soil depths, and eggs in turf stems. Finally, we assessed the non-consumptive effects of these abundant predators on adult billbug activity (mating, oviposition, thanatosis). We found that the predatory arthropod community consisted primarily of carabids (Pterostichus melanarius, Harpalus sp., Amara aenea, and Anisodactylus sp.) and spiders (lycosids), representing 60% and 28% of all predators, respectively. In the field and in lab assays, adult billbug mortality from predation was generally low at <6%. While predators readily consumed sentinel larvae in petri dish arenas, larvae escaped predation at 1 cm soil depth. The greatest consumptive effects of predators were on billbug eggs, with Anisodactlylus sp. feeding on 46% of eggs. Predator exposure reduced overall billbug activity by 56%, and for hunting billbugs, specifically, reduced mating activity by 28%. Our new understanding of the consumptive and non-consumptive effects of predators on billbugs supports the importance of conservation biocontrol in turfgrass and assists in planning for enhancement of specific predators.

Dropping to escape: a review of an under‐appreciated antipredator defence

Dropping is a common antipredator defence that enables rapid escape from a perceived threat. However, despite its immediate effectiveness in predator-prey encounters (and against other dangers such as a parasitoid or an aggressive conspecific), it remains an under-appreciated defence strategy in the scientific literature. Dropping has been recorded in a wide range of taxa, from primates to lizards, but has been studied most commonly in insects. Insects have been found to utilise dropping in response to both biotic and abiotic stimuli, sometimes dependent on mechanical or chemical cues. Whatever the trigger for dropping, the decision to drop by prey will present a range of inter-related costs and benefits to the individual and so there will be subtle complexities in the trade-offs surrounding this defensive behaviour. In predatory encounters, dropping by prey will also impose varying costs and benefits on the predator-or predators-involved in the system. There may be important trade-offs involved in the decision made by predators regarding whether to pursue prey or not, but the predator perspective on dropping has been less explored at present. Beyond its function as an escape tactic, dropping has also been suggested to be an important precursor to flight in insects and further study could greatly improve understanding of its evolutionary importance. Dropping in insects could also prove of significant practical importance if an improved understanding can be applied to integrated pest-management strategies. Currently the non-consumptive effects of predators on their prey are under-appreciated in biological control and it may be that the dropping behaviour of many pest species could be exploited via management practices to improve crop protection. Overall, this review aims to provide a comprehensive synthesis of the current literature on dropping and to raise awareness of this fascinating and widespread behaviour. It also seeks to offer some novel hypotheses and highlight key avenues for future research.

Community consequences of foraging under fear

Non-consumptive effects of predators within ecosystems can alter the behavior of individual prey species, and have cascading effects on other trophic levels. In this context, an understanding of non-consumptive predator effects on the whole prey community is crucial for predicting community structure and composition, hence biodiversity patterns. We used an individual-based, spatially-explicit modelling approach to investigate the consequences of landscapes of fear on prey community metrics. The model spans multiple hierarchical levels from individual home range formation based on food availability and perceived predation risk to consequences on prey community structure and composition. This mechanistic approach allowed us to explore how important factors such as refuge availability and foraging strategy under fear affect prey community metrics. Fear of predators affected prey space use, such as home range formation. These adaptations had broader consequences for the community leading to changes in community structure and composition. The strength of community responses to perceived predation risk was driven by refuge availability in the landscape and the foraging strategy of prey animals. Low refuge availability in the landscape strongly decreased diversity and total biomass of prey communities. Additionally, body mass distributions in prey communities facing high predation risk were shifted towards small prey animals. With increasing refuge availability the consequences of non-consumptive predator effects were reduced, diversity and total biomass of the prey community increased. Prey foraging strategies affected community composition. Under medium refuge availability, risk-averse prey communities consisted of many small animals while risk-taking prey communities showed a more even body mass distribution. Our findings reveal that non-consumptive predator effects can have important implications for prey community diversity and should therefore be considered in the context of conservation and nature management.

High Arctic lemmings remain reproductively active under predator-induced elevated stress.

Non-consumptive effects of predation have rarely been assessed in wildlife populations even though their impact could be as important as lethal effects. Reproduction of individuals is one of the most important demographic parameters that could be affected by predator-induced stress, which in turn can have important consequences on population dynamics. We studied non-consumptive effects of predation on the reproductive activity (i.e., mating and fertilization) of a cyclic population of brown lemmings exposed to intense summer predation in the Canadian High Arctic. Lemmings were live-trapped, their reproductive activity (i.e., testes visible in males, pregnancy/lactation in females) assessed, and predators were monitored during the summers of 2014 and 2015 within a 9ha predator-reduction exclosure delimited by a fence and covered by a net, and on an 11ha control area. Stress levels were quantified non-invasively with fecal corticosterone metabolites (FCM). We found that FCM levels of lemmings captured outside the predator exclosure (n = 50) were 1.6 times higher than inside (n = 51). The proportion of pregnant/lactating adult females did not differ between the two areas, nor did the proportion of adult scrotal males. We found that lemmings showed physiological stress reactions due to high predation risk, but had no sign of reduced mating activity or fertility. Thus, our results do not support the hypothesis of reproductive suppression by predator-induced stress.

Nonconsumptive predator effects on prey demography: dogwhelk cues decrease benthic mussel recruitment

AbstractPredators often have nonconsumptive effects (NCEs) on prey behaviour, but the demographic consequences for prey remain poorly known. This is important to understand because demography influences the functional role of a species in its community. We used an intertidal predator–prey system to investigate predator NCEs on prey recruitment, a key demographic process for population persistence. Pelagic mussel larvae are known to avoid waterborne cues from dogwhelks, which prey on intertidal mussels. Through a field experiment done in Atlantic Canada, we manipulated the presence of dogwhelks in intertidal habitats during the mussel (Mytilus spp.) recruitment season. We measured mussel recruitment in collectors that could be reached by waterborne dogwhelk cues but not by dogwhelks themselves. We found that the nearby presence of dogwhelks significantly decreased mussel recruit density. A previous study done in the same habitats under the same experimental conditions showed that dogwhelk cues also limit the recruitment of barnacles, another prey item for dogwhelks. However, such NCEs were stronger than those observed for mussel recruitment, possibly because mussels have more opportunities to escape predation during their benthic existence. Thus, basic features of natural history might be useful to predict the intensity of predator NCEs on prey recruitment.

Predation and Competition Differentially Affect the Interactions and Trophic Niches of a Neotropical Amphibian Guild

Competition and predation alter individual traits of organisms, and these effects can scale-up to have consequences on community structure and dynamics. The relative importance of competition and predation will depend largely on the local assemblage of species, the type of predators, or the degree of niche segregation. We experimentally investigated the interplay of competition and predation on the structure and trophic level (measured via stable isotope analysis) of a seven-species Neotropical freshwater guild using a mesocosm approach in central Panama. We tested the effect of two types of predators (dragonfly nymphs or adult water bugs) in combination with the presence/absence of a common competitor, the red-eyed treefrog (Agalychnis callidryas), on four core species of tadpoles. We also distinguished between consumptive and non-consumptive effects of each type of predator by presenting them to tadpoles caged or freely roaming. Dragonfly larvae were more efficient predators than water bugs, but these effects were not uniform for all tadpole species. All amphibian species grew bigger when raised in the presence of an uncaged dragonfly nymph, presumably due to reduced competition through thinning, but tadpoles were smaller when exposed to caged dragonfly nymphs indicating the existence of non-consumptive predator effects as well. Predator presence also altered the relative trophic position of the different amphibian species, causing some tadpole species to increase and others to decrease their trophic status. Despite the presumed ecological similarity of tadpole species in the guild, the interplay of competition and predation had varying effects on the trophic status of nearly every species. Our results indicate that community composition can greatly affect the trophic level of larval amphibians, and that predation may have a greater role than competition in structuring Neotropical larval amphibian guilds.

Sensory signals and the reaction space in predator–prey interactions

Non-consumptive effects of predators (NCEs) often occur when prey alter their behavior in response to sensory signals indicative of predatory threats. The purpose of this study was to assess how the reaction to predation risk by prey changes with environmental context and predator hunting mode. We placed prey (crayfish) in two different environments (flow and no flow) in one of the three predator treatments (active predator [bass], sit-and-wait predator [catfish], no predator) and monitored the behavior of the crayfish in a resource patchy environment. Crayfish rely on chemically mediated behaviors including foraging, agonistic, and predator detection, and inhabit flow and no flow environments. Our results show predator hunting mode changes prey behavior, but only in flow water that would enhance the transmission of predator cues. The most significant interaction between predator treatment and environmental conditions was found with the active predator in flow habitats, but changes in stimulus transmission dynamics did not alter NCEs from a sit-and-wait predator.

Threat of predation alters aggressive interactions among spotted salamander (Ambystoma maculatum) larvae.

Intraspecific aggression represents a major source of mortality for many animals and is often experienced alongside the threat of predation. The presence of predators can strongly influence ecological systems both directly by consuming prey and indirectly by altering prey behavior or habitat use. As such, the threat of attack by higher level predators may strongly influence agonistic interactions among conspecifics via nonconsumptive (e.g., behaviorally mediated) predator effects. We sought to investigate these interactions experimentally using larval salamanders (Ambystoma maculatum) as prey and dragonfly nymphs (Anax junius) as predators. Specifically, we quantified salamander behavioral responses to perceived predation risk (PPR) from dragonfly nymphs and determined the degree to which PPR influenced intraspecific aggression (i.e., intraspecific biting and cannibalism) among prey. This included examining the effects of predator exposure on the magnitude of intraspecific biting (i.e., extent of tail damage) and the resulting change in performance (i.e., burst swim speed). Salamander larvae responded to PPR by reducing activity and feeding, but did not increase refuge use. Predator exposure did not significantly influence overall survival; however, the pattern of survival differed among treatments. Larvae exposed to PPR experienced less tail damage from conspecifics, and maximum burst swim speed declined as tail damage became more extensive. Thus, escape ability was more strongly compromised by intraspecific aggression occurring in the absence of predation risk. We conclude that multitrophic indirect effects may importantly modulate intraspecific aggression and should be considered when evaluating the effects of intraspecific competition.

Nonconsumptive predator effects on prey demography

Nonconsumptive predator effects on prey demography

Nonconsumptive predator effects on prey: dogwhelk cues limit mussel recruitment and trigger mussel shell plasticity that hinders predation

Nonconsumptive predator effects on prey: dogwhelk cues limit mussel recruitment and trigger mussel shell plasticity that hinders predation

Fear of predation alters clone-specific performance in phloem-feeding prey

Fear of predation has been shown to affect prey fitness and behaviour, however, to date little is known about the underlying genetics of responses to predator-associated risk. In an effort to fill this gap we exposed four naïve clones of green peach aphid (Myzus persicae), maintained on the model crop Brassica oleracea, to different types of cues from aphid lion (Chrysoperla carnea). The respective predation risks, we termed Fear Factors, were either lethal (consumption by predator), or non-lethal (non-consumptive predator-associated cues: plant-tethered predator cadavers and homogenised shoot-sprayed or soil-infused blends of predator remains). Our results show that the non-lethal risk cues differentially impeded prey reproductive success that varied by clone, suggesting genotype-specific response to fear of predation. Furthermore, whether plants were perceived as being safe or risky influenced prey responses as avoidance behaviour in prey depended on clone type. Our findings highlight that intra-specific genetic variation underlies prey responses to consumptive and non-consumptive effects of predation. This allows selection to act on anti-predator responses to fear of predation that may ramify and influence higher trophic levels in model agroecosystems.

Keep calm and don't stop growing: Non-consumptive effects of a sympatric predator on two invasive Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides.

Predators shape prey populations by elimination of individuals (consumptive effects) and by inducing modifications in prey behaviour, physiology or morphology (NCE—non-consumptive effects). Due to the resource allocation to defence, decreased feeding and higher stress, the costs of predator NCEs can be considerable. Therefore, the resistance to NCEs may be crucial for population growth and interspecific competition. We tested the resistance of Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides to NCEs imposed by their predator, the racer goby Babka gymnotrachelus. As D. villosus is often avoided by predators in the presence of alternative food, we hypothesised that it would bear lower behavioural and physiological costs of anti-predator responses. We tested gammarid feeding in short-time experiments (2–4 h) with food (chironomid larvae) located at various distances from the stony shelter (to enforce food searching, Experiment I) or in the direct gammarid proximity (no searching needed, Experiment II). Moreover, we checked the predator effect on gammarid growth in a 2-week Experiment III. Both gammarids exposed to predators reduced feeding efficiency outside the shelter (Experiment I). Contrary to our expectations, the response of D. villosus was stronger. When food was provided in their direct proximity (Experiment II), the feeding of both species was unaffected by predators, indicating that a shelter supplied with food can reduce predator NCEs. The growth of P. robustoides was reduced in the presence of predators (Experiment III), whereas that of D. villosus was unaffected. Although D. villosus has a more effective defence strategy than P. robustoides, it bears similar or even higher behavioural costs of NCEs. However, it exhibits the higher resistance to the long-term predator presence, sustaining its growth rate under such conditions. This may be one of the factors contributing to the great invasion success of D. villosus, currently taking place in European fresh waters.

Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels.

Non-consumptive effects (NCEs) of predators are ubiquitous in food webs with well-detailed impacts on trophic cascades over multiple levels. However, integrating NCEs with other predator-mediated interactions, like intraguild predation, as well as context-specific habitat factors that shape top-down pressure, remains a challenge. Focusing on two common seed predators, mice (Peromyscus spp.) and carabid beetles (Coleoptera: Carabidae), we quantify trophic and behavioral consequences of predation risk and availability of refuge vegetation on both intraguild predators (mice) and intraguild prey (beetles). In a 2-year field experiment, we manipulated refuge habitat (red clover), small mammal access, and moonlight, which small mammals use as an indirect cue of predation risk. We found that avoidance of predation risk by mice in simulated moonlight reduced carabid activity density in vegetation by up to 50% compared to exposed habitat, but had no cascading effects on seed predation. We linked patterns observed in the field with behavioral mechanisms by observing beetle foraging activity, and found that exposure to both indirect and direct vertebrate predator cues reduced movement by 50%, consistent with predator-mediated activity reductions observed in the field. However, predation risk increased carabid seed consumption by 43%. Thus, weak effects of predation risk on seed removal in the field may be explained by overcompensatory seed feeding by beetles. This work demonstrates that predators elicit responses that cascade over multiple trophic levels, triggering behavioral changes in species lower on the food chain. These behavior-mediated cascades are controlled by their spatiotemporal context and have important downstream impacts on predator-prey dynamics.

THE EFFECTS OF ARTIFICIAL CRAB SPIDERS (THOMISIDAE: Misumenops spp.) ON Piper POLLINATOR BEHAVIOUR IN COSTA RICA: DIFFERENCES BETWEEN INSECT ORDERS

Communication drives ecosystem interactions, including the visual signals of plants used to attract pollinators. However, the effectiveness of flower color in attracting pollinators increases dishonest signalling by pollinator predators exploiting floral inflorescences as hunting niches. Negative pollinator associations with spiders on flowers may cause avoidance of specific plants, thus reducing plant fitness from decreased pollination, but this remains understudied. In this study, we used clay models to simulate crab spiders ( Misumenops spp.) on Piper plants in a paired design (spider vs. no spider) on the same plant to further investigate the role of pollinator predators on pollinator behaviour. Using this design, we compared avoidance and visitation of Piper plants, identified pollinators to order (and to insect, if possible, such as the case with bees, wasps, and ants in Hymenoptera), and observed individual insect behaviour towards spiders. Piper pollinators were more likely to be aware of spider treatments vs. controls and were also 5.01 times as likely to avoid spider treatments (p < 0.001). Visitation on controls was also higher, but this was not found to be significant (p = 0.800). Overall, nine orders of pollinators were observed visiting Piper plants, with Hymenopterans, Dipterans, and Coleopterans found to be the dominant orders observed with differences in visitation and avoidance, using Poisson distributions in generalized linear model analyses. This study provides a framework for investigating non-consumptive effects of predators on plant fitness.

Predator effects on reef fish settlement depend on predator origin and recruit density.

During major life-history transitions, animals often experience high mortality rates due to predation, making predator avoidance particularly advantageous during these times. There is mixed evidence from a limited number of studies, however, regarding how predator presence influences settlement of coral-reef fishes and it is unknown how other potentially mediating factors, including predator origin (native vs. nonnative) or interactions among conspecific recruits, mediate the non-consumptive effects of predators on reef fish settlement. During a field experiment in the Caribbean, approximately 52% fewer mahogany snapper (Lutjanus mahogoni) recruited to reefs with a native predator (graysby grouper, Cephalopholis cruentata) than to predator-free control reefs and reefs with an invasive predator (red lionfish, Pterois volitans) regardless of predator diet. These results suggest that snapper recruits do not recognize nonnative lionfish as a threat. However, these effects depended on the density of conspecific recruits, with evidence that competition may limit the response of snapper to even native predators at the highest recruit densities. In contrast, there was no effect of predator presence or conspecific density on the recruitment of bicolor damselfish (Stegastes partitus). These context-dependent responses of coral-reef fishes to predators during settlement may influence individual survival and shape subsequent population and community dynamics.

Predation risk influences feeding rates but competition structures space use for a common Pacific parrotfish.

In terrestrial systems it is well known that the spatial patterns of grazing by herbivores can influence the structure of primary producer communities. On coral reefs, the consequences of varied space use by herbivores on benthic community structure are not well understood, nor are the relative influences of bottom-up (resource abundance and quality), horizontal (competition), and top-down (predation risk) factors in affecting spatial foraging behaviors of mobile herbivorous fishes. In the current study we quantified space use and feeding rates of the parrotfish, Chlorurus spilurus, across a strong gradient of food resources and predator and competitor abundance across two islands with drastically different fisheries management schemes. We found evidence that while feeding rates of this species are affected by direct interference competition and chronic predation risk, space use appears to be primarily related to exploitative competition with the surrounding herbivore community. We found no evidence that predation risk influences diurnal foraging space use in this small bodied parrotfish species. Additionally, we found the influence of chronic predation risk on feeding rates of this species to be less dramatic than the results of recent studies that used model predators to measure acute behavioral responses of other species of herbivorous fishes. Our results indicate that the non-consumptive effects of predators on the foraging behaviors of coral reef herbivores may be less dramatic than previously thought.

Fear Mediates Trophic Cascades: Nonconsumptive Effects of Predators Drive Aquatic Ecosystem Function.

Predators control prey populations and influence communities and the functioning of ecosystems through a combination of consumptive and nonconsumptive effects. These effects can be locally confined to one ecosystem but can also be extended to neighboring ecosystems. In this study, we investigated the nonconsumptive effects of terrestrial avian predators on the communities of aquatic invertebrates inhabiting bromeliads and on the functioning of these natural ecosystems. Bromeliads with stuffed birds placed nearby showed a decrease in aquatic damselfly larvae abundance and biomass, and we can infer that these changes were caused by antipredator responses. These larvae, which are top predators in bromeliad ecosystems, changed the composition of the entire aquatic invertebrate community. While total species richness, mesopredator richness, and shredder abundance increased in the presence of birds, scraper biomass decreased, possibly as a consequence of the increase in mesopredator richness. High scraper biomass in the absence of birds may have accelerated detrital decomposition, making more nutrients available for bromeliads, which grew more. These results show that nonconsumptive effects triggered by terrestrial predators can cascade down to lower trophic levels and dramatically affect the functioning of aquatic ecosystems, which can in turn alter nutrient provision to terrestrial ecosystems.

Are males more scared of predators? Differential change in metabolic rate between males and females under predation risk

The non-consumptive effects of predation contribute to reduce preys' fitness. In this way, predation imposes a cost to animals, not only through direct consumption, but also as an energetic cost. One way used to estimate this cost in the past has been to measure the production of CO2 to estimate the change in metabolic rate because of predation. It has been proposed that this change is mediated by the insect stress neurohormone octopamine. Here we study the change in metabolic rate of the black field cricket (Teleogryllus commodus), and how the production of CO2 varies when a chemical cue from a sympatric predator is added. We hypothesised that after the addition of a predatory cue, the metabolic rate will increase. Moreover, since the pressure of predation is stronger on females, we propose that females will have a greater increase in the CO2 produce as consequence of the added cues from the predator. Our results confirmed our first hypothesis, showing an almost two-fold increase in CO2 when the predatory cue was added. However, males were the ones that showed a greater increase, in opposition to our second hypothesis. We put these results in the context of the escape theory and, in particular, the “landscape of fear” hypothesis. Also, because the timing between the increase of metabolic rate we measure here and the release of octopamine reported in previous studies do not match, we reject the idea that octopamine causes the increase in metabolism.