The context dependence of non‐consumptive predator effects

Non‐consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator‐induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti‐predator behaviours, we conceptualise the multi‐stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey‐specific patterns of evasion success (‘evasion landscapes’) as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non‐consumptive predator–prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context‐dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Interspecific differences in antipredator strategies determine the strength of non‐consumptive predator effects on stream detritivores

Animal species differ considerably in their response to predation risks. Interspecific variability in prey behaviour and morphology can alter cascading effects of predators on ecosystem structure and functioning. We tested whether species‐specific morphological defenses may affect responses of leaf litter consuming invertebrate prey to sit‐and‐wait predators, the odonate Cordulegaster boltonii larvae, in aquatic food webs. Partly or completely blocking the predator mouthparts (mandibles and/or extensible labium), thus eliminating consumptive (i.e. lethal) predator effects, we created a gradient of predator‐prey interaction intensities (no predator < predator – no attack < predator – non‐lethal attacks < lethal predator). A field experiment was first used to assess both consumptive and non‐consumptive predator effects on leaf litter decomposition and prey abundances. Laboratory microcosms were then used to examine behavioural responses of armored and non‐armored prey to predation risk and their consequences on litter decomposition. Results show that armored and non‐armored prey responded to both acute (predator – non‐lethal attacks) and chronic (predator – no attack) predation risks. Acute predation risk had stronger effects on litter decomposition, prey feeding rate and prey habitat use than predator presence alone (chronic predation risk). Predator presence induced a reduction in feeding activity (i.e. resource consumption) of both prey types but a shift to predator‐free habitat patches in non‐armored detritivores only. Non‐consumptive predator effects on prey subsequently decreased litter decomposition rate. Species‐specific prey morphological defenses and behaviour should thus be considered when studying non‐consumptive predator effects on prey community structure and ecosystem functioning.     

Comparing the effects of GM and non‐GM soybean varieties on non‐target arthropods

In order to guarantee the safety of genetically modified (GM) soybean crops, it is important to assess the potential toxicity of their expressed insecticidal proteins to non‐target organisms. In the present study, the effects of the GM soybean Insulin‐like Growth Factor (IGF), which is tolerant to the herbicide glufosinate, on plant‐dwelling non‐target insects and arachnids were evaluated in soybean agroecosystems. For comparison, the non‐GM parental cultivar of soybean Gwangan‐kong was used as a control. Data were collected in 2016 and 2017 via surveying at Ochang and Jeonju, Korea. In total, 13,031 individual insects and arachnids, representing 64 families in 11 orders, were captured during the study. Firstly, the results indicate that the GM soybean IGF did not negatively affect plant‐dwelling non‐target insects and arachnids. However, the numbers of captured individuals on both IGF and Gwangan‐kong were higher at Ochang in 2017. The occurrence of insect pests, natural enemies, and other insects differed significantly according to region, region and survey year, and survey year, respectively. In addition, the dominance, diversity, evenness, and richness indices for the collected insects varied significantly among the regions and survey years regardless of soybean variety. The score from PROXSCAL multidimensional scaling using combined data showed that insects and arachnids in different natural environments were separated by their cultivation regions and years irrespective of soybean cultivars.     

Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non‐consumptive effects of predators

1. Density‐ and trait‐mediated indirect interactions (DMIIs and TMIIs, respectively) in food chains play crucial roles in community structure and processes. However, factors affecting the relative strength of these interactions are poorly understood, including in widespread and important freshwater rice ecosystems. 2. We studied the strength of DMIIs and TMIIs in a food chain involving a predator (the Reeve’s turtle Chinemys reevesii), its herbivorous prey (the apple snail Pomacea canaliculata) and a plant (rice Oryza sativa) in outdoor containers simulating rice fields. We also evaluated consumptive and non‐consumptive effects of the predator on the snail. We removed a fixed proportion of snails every 2 days to simulate prey consumption and introduced a caged turtle that was fed daily with snails to simulate non‐consumptive effects. 3. Direct consumptive effects increased growth of the remaining snails and their per capita feeding rate. Moreover, consumptive and non‐consumptive effects, and their interaction, affected the proportion of snails buried in the soil. This interaction was presumably because increasing food availability per snail induced their self‐burying behaviour. 4. Both DMIIs and TMIIs affected the number of rice plants remaining, whereas their interaction term was not significant. 5. In summary, density dependence and interactions between consumptive and non‐consumptive effects influenced snail growth and behaviour, respectively. However, no cascading effects of these complicated interactions on rice plants were detected.     

Fear and lethality in snowshoe hares: the deadly effects of non‐consumptive predation risk

Predators play a critical, top–down role in shaping ecosystems, driving prey population and community dynamics. Traditionally, studies of predator‐prey interactions have focused on direct effects of predators, namely the killing of prey. More recently, the non‐consumptive effects of predation risk are being appreciated; e.g. the ‘ecology of fear’. Prey responses to predation risk can be morphological, behavioural, and physiological, and are assumed to come at a cost to prey fitness. However, few studies have examined the relationship between predation risk and survival in wild animals. We tested the hypothesis that predation risk itself could reduce survival in wild‐caught snowshoe hares. We exposed female snowshoe hares to a simulated predator (a trained dog) during gestation only, and measured adult survival and, in surviving females, their ability to successfully wean offspring. We show for the first time in a wild mammal that the risk of predation can itself be lethal. Predation risk reduced adult female survival by 30%, and had trans‐generational effects, reducing offspring survival to weaning by over 85% – even though the period of risk ended at birth. As a consequence of these effects the predator‐exposed group experienced a decrease in number, while the control group substantially increased. Challenges remain in determining the importance of risk‐induced mortality in natural field settings; however, our findings show that non‐lethal predator encounters can influence survival of both adults and offspring. Future work is needed to test these effects in free‐living animals.     

Consumptive and non‐consumptive effects of wolf spiders on cotton bollworms

Larvae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) that survive on genetically modified Bt cotton (Gossypium hirsutum L., Malvaceae) contribute to the risk of widespread resistance to Bt toxins. Current resistance management techniques include pupae busting, which involves deep tilling of the soil to kill overwintering pupae. Unfortunately, pupae busting runs counter to soil and water conserving techniques, such as minimum tillage. This problem could be relieved with biological control methods, whereby predators attack either larvae going to ground to pupate or moths emerging from the ground. We found that the wolf spider Tasmanicosa leuckartii (Thorell) (Araneae: Lycosidae), a common inhabitant of Australian cotton agroecosystems, is an effective predator of H. armigera, attacking and killing most larvae (66%) and emerging moths (77%) in simple laboratory arenas. Tasmanicosa leuckartii also reduced the number of emerging moths by 66% on average in more structurally complex glasshouse arenas. Males, females, and late‐instar juveniles of T. leuckartii were similarly effective. Tasmanicosa leuckartii also imposed non‐consumptive effects on H. armigera, as when a spider was present larvae in the laboratory areas spent less time on the cotton boll and more time on the soil and more mass was lost from the cotton boll. Increased loss of boll mass likely reflects changes in H. armigera foraging behavior induced by the presence of spiders (indirect non‐consumptive effects). Helicoverpa armigera spent more time as pupae when the spider was present in simple laboratory arenas, but not in more complex glasshouse enclosures. Overall, results indicate that T. leuckartii spiders can be effective predators of H. armigera late instars and moths but also suggest that, under some conditions, the presence of spiders could increase the damage to individual cotton bolls.     

Plant resistance attenuates the consumptive and non‐consumptive impacts of predators on prey

Plant resistance and predation have strong independent and interacting effects on herbivore survival, behavior, and patterns of herbivory. Historically, research has emphasized variation in the consumption of herbivores by enemies. Recent work, however, demonstrates that predators also elicit important changes in the traits of their prey, but we do not know how this is influenced by plant quality. In this study, we quantify how the consumptive and non‐consumptive effects of predators vary along a gradient of plant resistance using tomato plants (Solanum lycopersicum), tobacco hornworms (Manduca sexta), and predaceous stinkbugs (Podisus maculiventris). We manipulated resource quality using three tomato lines that vary in the expression of the jasmonate pathway, a phytohormonal pathway that is central in mediating resistance to insects. Resistant plants had higher levels of defensive proteins and glandular trichomes than low resistance plants. The consumptive and non‐consumptive effects of predators were quantified on the three tomato lines by comparing the impact of ‘lethal’ predators that both kill and scare prey with ‘risk’ predators whose mouthparts were surgically impaired to prevent killing. Across several field experiments, the total cascading effect of predators on plant damage was 80.4% lower on jasmonate‐overex‐pressing (highly resistant) plants compared to that on wild‐type or jasmonate‐insensitive (low resistance) plants. This dramatic attenuation of predator effects was due to a 66% reduction in consumption on high resistance plants, and also because of a 65% decline in non‐consumptive effects. Numerous studies in natural and agricultural habitats have documented that predator effects tend to be weaker on well‐defended plants; our results provide novel mechanistic insight into this pattern by demonstrating that plant resistance substantially weakens both the consumptive and non‐consumptive impacts of predators.     

Predator presence dramatically reduces copepod abundance through condition‐mediated non‐consumptive effects

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Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Determinants and co‐expression of anti‐predator responses in amphibian tadpoles: a meta‐analysis

A wide range of taxa respond to perceived predation risk (PPR) through inducible defenses, and many prey are capable of responding both behaviorally and morphologically to the same risk event. In cases where multiple defenses confer protection by independent means (i.e. they are mechanistically independent) responses will either be co‐expressed, or the expression of one defense will limit the capacity (or need) to respond along another axis. Our ability to generate a broad understanding of these patters has been limited, in part, by difficulties in comparing results across studies that employ distinct experimental protocols. Using the extensive literature on tadpole responses to PPR, we conducted a meta‐analysis to identify the ecological and experimental determinants of inducible defence expression. We then assessed whether the magnitude of response to PPR along behavioural versus morphological response axes was positively, or negatively, correlated. The most commonly quantified responses to perceived risk in tadpoles included reductions in movement and swimming behaviour, and altered tail morphology. Our analyses reveal that tadpole behavioural responses are strongly influenced by prey family, predator taxon, evolutionary history with the predator (native versus non‐native), amount of prey consumed by the predator, and how perceived risk was manipulated (e.g. presence versus absence of alarm cues). Tail morphology was similarly influenced by these factors, but also whether the target prey was palatable to predators. Thus, our results identify ecological and experimental features that critically influence the observed effect size in tadpole responses to PPR. A positive correlation between behavioural and morphological responses in studies where both were measured indicates that trait co‐specialization is the predominant pattern of defense deployment in larval amphibians. This positive relationship suggests that survival tends to be maximized in tadpoles through equivalent co‐activation of multiple independent axes of protection, opposed to maximal expression along any single axis. Synthesis Our understanding of plastic responses to perceived predation risk (PPR) has benefited substantially from the vast amount of experimental work examining inducible defences in anuran tadpoles. Indeed this research has illustrated the wide variety of ways that prey animals can respond to the same risk event. We conducted a metaanalysis to identify the key ecological and experimental determinants of inducible defence expression. We then show that, in most cases, behavioural and morphological responses to PPR tend to be co‐expressed suggesting that responding along one axis (moving behaviour) does not limit their ability to respond along another distinct axis (tail morphology).     

The association between stressors and telomeres in non‐human vertebrates: a meta‐analysis

Animal response to stressors such as harsh environmental conditions and demanding biological processes requires energy generated through increased mitochondrial activity. This results in the production of reactive oxygen species (ROS). In vitro and some in vivo studies suggest that oxidative damage of DNA caused by ROS is responsible for telomere shortening. Since telomere length is correlated with survival in many vertebrates, telomere loss is hypothesised to trigger cellular ageing and/ or to reflect the harshness of the environment an individual has experienced. To improve our understanding of stress‐induced telomere dynamics in non‐human vertebrates, we analysed 109 relevant studies in a meta‐analytical framework. Overall, the exposure to possible stressors was associated with shorter telomeres or higher telomere shortening rate (average effect size = ?0.16 ± 0.03). This relationship was consistent for all phylogenetic classes and for all a priori‐selected stressor categories. It was stronger in the case of pathogen infection, competition, reproductive effort and high activity level, which emphasises their importance in explaining intraspecific telomere length variability and, potentially, lifespan variability. Interestingly, the association between stressor exposure and telomeres in one hand, and oxidative stress in the other hand, covaried, suggesting the implication of oxidative stress in telomere dynamics.     

Consumptive and non‐consumptive effects of wolf spiders on cucumber beetles and cucumber plant damage

Biological control research often focuses on the ability of predators to reduce pest densities and protect crops through consumption. Less studied is their ability to protect crops by altering pest behaviour (non‐consumptive effects). Lab experiments were conducted to test predation rates of striped cucumber beetles (Acalymma vittatum; Coleoptera: Chrysomelidae) and spotted cucumber beetles (Diabrotica undecimpunctata howardi; Coleoptera: Chrysomelidae) by large (>10 mm) wolf spiders (Araneae: Lycosidae). Field experiments were conducted to examine how the physical presence and/or cues of spiders impact the behaviour and mortality of A. vittatum (specialist) and D. undecimpunctata (generalist) cucumber beetles as well as growth and damage of cucumber plants (Cucumis sativus; Cucurbitaceae). A. vittatum and D. undecimpunctata adults were added to caged cucumber plants without a spider, with spider cues only (spider removed before beetle inclusion), with spider only (spider introduced to plants immediately before beetle inclusion), and with spiders and their cues present (spiders introduced 24 hr in advance of beetle inclusion). A. vittatum responded to spider cues primarily by emigrating from plants. Contrarily, D. undecimpunctata did not display obvious responses, such as reduced feeding or increased emigration, to spider foraging and/or cues. Actively foraging lycosids increased A. vittatum mortality and reduced densities of D. undecimpunctata in the field when cucumber plants were flowering. This study highlights how non‐consumptive and consumptive effects can play a role in modifying pest populations, and how these effects can vary across species and plant growth stages.     

Non‐consumptive effects of a top‐predator decrease the strength of the trophic cascade in a four‐level terrestrial food web

The fear of predators can strongly impact food web dynamics and ecosystem functioning through effects on herbivores morphology, physiology or behaviour. While non‐consumptive predator effects have been mostly studied in three‐level food chains, we lack evidence for the propagation of non‐consumptive indirect effects of apex predators in four level food‐webs, notably in terrestrial ecosystems. In experimental mesocosms, we manipulated a four‐level food chain including top‐predator cues (snakes), mesopredators (lizards), herbivores (crickets), and primary producers (plants). The strength of the trophic cascade induced by mesopredators through the consumption of herbivores decreased in the presence of top‐predator cues. Specifically, primary production was higher in mesocosms where mesopredators were present relative to mesocosms with herbivores only, and this difference was reduced in presence of top‐predator cues, probably through a trait‐mediated effect on lizard foraging. Our study demonstrates that non‐consumptive effects of predation risk can cascade down to affect both herbivores and plants in a four‐level terrestrial food chain and emphasises the need to quantify the importance of such indirect effects in natural communities.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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A matrix‐based method of moments for fitting the multivariate random effects model for meta‐analysis and meta‐regression

Multivariate meta‐analysis is becoming more commonly used. Methods for fitting the multivariate random effects model include maximum likelihood, restricted maximum likelihood, Bayesian estimation and multivariate generalisations of the standard univariate method of moments. Here, we provide a new multivariate method of moments for estimating the between‐study covariance matrix with the properties that (1) it allows for either complete or incomplete outcomes and (2) it allows for covariates through meta‐regression. Further, for complete data, it is invariant to linear transformations. Our method reduces to the usual univariate method of moments, proposed by DerSimonian and Laird, in a single dimension. We illustrate our method and compare it with some of the alternatives using a simulation study and a real example.     

A meta‐analysis of the strength and nature of cytoplasmic genetic effects

Genetic variation in cytoplasmic genomes (i.e. the mitochondrial genome in animals, and the combined mitochondrial and chloroplast genomes in plants) was traditionally assumed to accumulate under a neutral equilibrium model. This view has, however, come under increasing challenge from studies that have experimentally linked cytoplasmic genetic effects to the expression of life history phenotypes. Such results suggest that genetic variance located within the cytoplasm might be of evolutionary importance and potentially involved in shaping population evolutionary trajectories. As a step towards assessing this assertion, here we conduct a formal meta‐analytic review to quantitatively assess the extent to which cytoplasmic genetic effects contribute to phenotypic expression across animal and plant kingdoms. We report that cytoplasmic effect sizes are generally moderate in size and associated with variation across a range of factors. Specifically, cytoplasmic effects on morphological traits are generally larger than those on life history or metabolic traits. Cytoplasmic effect sizes estimated at the between‐species scale (via interspecies mix‐and‐matching of cytoplasmic and nuclear genomes) are larger than those at the within‐species scale. Furthermore, cytoplasmic effects tied to epistatic interactions with the nuclear genome tend to be stronger than additive cytoplasmic effects, at least when restricting the data set to gonochorous animal species. Our results thus confirm that cytoplasmic genetic variation is commonly tied to phenotypic expression across plants and animals, implicate the cytoplasmic–nuclear interaction as a key unit on which natural selection acts and generally suggest that the genetic variation that lies within the cytoplasm is likely to be entwined in adaptive evolutionary processes.