Non-consumptive Effects Research Articles

Biological and Physiological Changes in Spodoptera frugiperda Larvae Induced by Non-Consumptive Effects of the Predator Harmonia axyridis

The effects of predatory natural enemies on their prey or hosts involve both consumption and non-consumptive effects. This study investigated the non-consumptive effects of the predator, Harmonia axyridis (Coleoptera: Coccinellidae) on 1st, 2nd and 3rd instar larvae of Spodoptera frugiperda. We exposed larvae of different instars to the predator and assessed various parameters using a combination of biological and biochemical methods. Exposure to the predator significantly affected the growth and development of the S. frugiperda caterpillars. Firstly, the developmental duration of S. frugiperda larvae in the 1st–3rd instars and the pupal stage were notably prolonged. Moreover, we observed significant effects on pupal mass, pupal abnormality rate and emergence rate. These non-consumptive effects were gradually weakened with an increase in the larval stage exposed to the predator. Antioxidant enzyme activities including catalase (CAT) peroxidase (POD) and superoxide dismutase (SOD) activity increased significantly. Additionally, organismal triglyceride, trehalose and glycogen content were significantly altered by non-consumptive effects, while protein content showed no significant change. Spodoptera frugiperda larvae increased the activity of antioxidant enzymes in response to potential predators to mitigate oxidative stress and reduce cellular and tissue damage. This resources redistribution towards survival may inhibit growth and development of the species and further exacerbate these non-consumptive effects. These findings highlight the importance of considering non-consumptive effects in pest-management strategies to optimize control measures in agricultural systems.

Large mammal behavioral defenses induced by the cues of human predation.

Large mammals respond to human hunting via proactive and reactive responses, which can induce subsequent nonconsumptive effects (NCEs). Thus, there is evidence that large mammals exhibit considerable behavioral plasticity in response to human hunting risk. Currently, however, it is unclear which cues of human hunting large mammals may be responding to. We conducted a literature review to quantify the large mammal behavioral responses induced by the cues of human hunting. We detected 106 studies published between 1978 and 2022 of which 34 (32%) included at least one measure of cue, typically visual (n = 26 of 106, 25%) or auditory (n = 11 of 106, 10%). Space use (n = 37 of 106, 35%) and flight (n = 31 of 106, 29%) were the most common behavioral responses studied. Among the 34 studies that assessed at least one cue, six (18%) measured large mammal behavioral responses in relation to proxies of human hunting (e.g. hunting site or season). Only 14% (n = 15 of 106) of the studies quantified an NCE associated with an animal's response to human hunting. Moreover, the association between cues measured and antipredator behaviors is unclear due to a consistent lack of controls. Thus, while human hunting can shape animal populations via consumptive effects, the cues triggering these responses are poorly understood. There hence remains a need to link cues, responses, NCEs, and the dynamics of large mammal populations. Human activities can then be adjusted accordingly to prevent both overexploitation and unintended NCEs in animal populations.

Navigating the landscape of fear: Fruit flies exhibit distinct antipredator and antiparasite defensive behaviors.

Most organisms are at risk of being consumed by a predator or getting infected by a parasite at some point in their life. Theoretical constructs such as the landscape of fear (perception of risk) and nonconsumptive effects (NCEs, costly responses sans predation or infection) have been proposed to describe and quantify antipredator and antiparasite responses. How prey/host species identify and respond to these risks determines their survival, reproductive success and, ultimately, fitness. Most studies to date have focused on either predator-prey or parasite-host interactions, yet habitats and ecosystems contain both parasitic and/or predatory species that represent a complex and heterogenous mosaic of risk factors. Here, we experimentally investigated the behavioral responses of a cactophilic fruit fly, Drosophila nigrospiracula, exposed to a range of species that include parasites (ectoparasitic mite), predators (jumping spiders), as well as harmless heterospecifics (nonparasitic mites, ants, and weevils). We demonstrate that D. nigrospiracula can differentiate between threat and non-threat species, increase erratic movements and decrease velocity in the presence of parasites, but decrease erratic movements and time spent grooming in the presence of predators. Of particular importance, flies could distinguish between parasitic female mites and nonparasitic male mites of the same species, and respond accordingly. We also show that the direction of these NCEs differs when exposed to parasitic mites (i.e., risk of infection) versus spiders (i.e., risk of predation). Given the opposing effects of predation versus infection risk on fly behavior, we discuss potential trade-offs between parasite and predator avoidance behaviors. Our findings illustrate the complexity of risk assessment in a landscape of fear and the fine-tuned NCEs that arise in response. Moreover, this study is the first to examine these behavioral NCEs in a terrestrial system.

Risky Business: Predator Chemical Cues Mediate Morphological Changes in Freshwater Snails.

Many prey organisms respond to the nonconsumptive effects of predators by altering their physiology, morphology, and behavior. These inducible defenses can create refuges for prey by decreasing the likelihood of consumption by predators. Some prey, as in marine mollusks, have been shown to alter their morphology in response to the presence of size-limited predation. To extend this work, we exposed pointed campeloma snails (Campeloma decisum) to chemical cues from a natural predator, the rusty crayfish (Faxonius rusticus), to better understand how snail morphology changes under the threat of predation. The total force needed to crush shells, total shell length, aperture width, and total weight, along with changes to these 3 body measurements, were recorded for each individual and used to quantify morphological changes as a function of risk. Snails exposed to crayfish chemical cues had shells that required significantly more force to crush their shells than controls (P=0.023). Total shell length was greater in crayfish-exposed snails than in control snails (P=0.012), and snails in the crayfish treatment also showed significantly more change in shell length than control snails (P=0.007). Similarly, aperture width was significantly greater in exposed snails (P=0.011). However, exposed snails exhibited significantly less change in aperture width than controls (P=0.03). Finally, we found that snails exposed to crayfish weighed significantly more than snails in the control (P=0.008). Thus, the results of this study show that morphology of gastropods is altered in the presence of predators, and this may be an antipredator tactic directly related to predation risk.

Asymmetrical predation intensity produces divergent antipredator behaviours in primary and secondary prey.

It is widely recognized that predators can influence prey through both direct consumption and by inducing costly antipredator behaviours, the latter of which can produce nonconsumptive effects that cascade through trophic systems. Yet, determining how particular prey manage risk in natural settings remains challenging as empirical studies disproportionately focus on single predator-prey dyads. Here, we contrast foraging strategies within the context of a primary and secondary prey to explore how antipredator behaviours emerge as a product of predation intensity as well as the setting in which an encounter takes place. We studied the effects of spotted owls (Strix occidentalis) on two species experiencing asymmetrical risk: dusky-footed woodrats (Neotoma fuscipes; primary prey) and deer mice (Peromyscus spp.; alternative prey). Woodrats are most abundant within young forests, but predominantly captured by owls foraging within mature forests; in contrast, deer mice occur in high densities across forest types and seral stages and are consumed at lower per-capita rates overall. We deployed experimental foraging patches within areas of high and low spotted owl activity, created artificial risky and safe refuge treatments, and monitored behaviour throughout the entirety of prey foraging bouts. Woodrats were more vigilant and foraged less within mature forests and at riskier patches, although the effect of refuge treatment was contingent upon forest type. In contrast, deer mice only demonstrated consistent behavioural responses to riskier refuge treatments; forest type had little effect on perceived risk or the relative importance of refuge treatment. Thus, habitat can interact with predator activity to structure antipredator responses differently for primary versus secondary prey. Our findings show that asymmetrical predation can modulate both the magnitude of perceived risk and the strategies used to manage it, thus highlighting an important and understudied contingency in risk effects research. Evaluating the direct and indirect effects of predation through the paradigm of primary and secondary prey may improve our understanding of how nonconsumptive effects can extend to population- and community-level responses.

Resilience to changes in salinity and predator diversity in representative Gulf of Mexico estuarine fish predator-prey interactions

Predators strongly influence ecological communities and subsequent ecosystem function by directly consuming prey individuals and indirectly by inciting alterations in prey behavior, termed non-consumptive effects (NCEs). Gulf of Mexico estuaries support complex food webs structured by numerous species interactions maintained in constant environmental flux from variation in salinity. Environmental variation presents a source of physiological stress for estuarine fish and plays a role in their distributions and subsequent interactions. Here, we present the results of a mesocosm experiment examining if acute changes in salinity disrupt NCEs of different predators on estuarine prey. We exposed Gulf killifish (Fundulus grandis) to visual and/or olfactory cues from a common estuarine predator, red drum (Sciaenops ocellatus), and from a freshwater predator that is a transient species in lower portions of estuaries, largemouth bass (Micropterus salmoides), under either decreasing, constant, or increasing salinity. Killifish decreased shoal size and movement in response to olfactory cues or both visual and olfactory cues compared to when they were exposed to no cues or visual cues, demonstrating variable perceived risk dependent on cue type. Behavioral response did not vary by predator species, implying a generalized response to different fish predators. Prey did not change behavior when exposed to decreasing salinity compared to constant salinity. However, prey movement increased with increasing salinity, indicating that salinity changes may provide cues to search for different habitats instead of a stressor. Our experiment indicates that estuarine predator-prey interactions may be resilient to acute salinity changes given the broad tolerances of euryhaline species.

Parasites and the ecology of fear: Nonconsumptive effects of ectoparasites on larvae reduce growth in simulated Drosophila populations.

Predators negatively affect prey outside of direct attack, and these nonconsumptive effects (NCEs) may cause over half the impacts of predators on prey populations. This "ecology of fear" framework has been extended to host-parasite interactions. The NCEs of parasites are thought to be small relative to those of predators. However, recent research shows ectoparasites exert NCEs on multiple life stages of Drosophila. In this study, we apply recent data to a matrix-based model of fly populations experiencing infection/consumption and NCEs from an ectoparasitic mite. We found the NCEs of parasites on larvae, which are not actively parasitized, decreased the size of simulated host populations. By contrast, the NCEs on adult flies increased population size through compensatory egg production. The negative NCEs on larvae outweighed the positive effects on adults to reduce population size. This study suggests that parasitic NCEs can suppress host populations independent of infection.

Bimodal response strategy in Daphnia to ambush predation risk.

Predation's consequences can manifest through either consumptive or nonconsumptive effects, but the prey response may also vary depending on the predator hunting strategy. Considerable attention has been paid to coursing predators, whereas less information is available regarding responses to ambush predators. To remedy this paucity, we utilized a three-dimensional tracking platform to record groups of Daphnia magna under predation risk from the ambush invertebrate predator red-eyed damselfly, Erythromma najas. This design allowed us to test individual antipredator responses in multiple metrics of swimming behaviors. We demonstrate that predation risk was greatest for those that swam at 85% of the available depth and averaged 8.1 mm/s. Examining the swimming behavior of each individual separately showed that predation risk did not affect any of the prey response metrics. Interestingly, however, Daphnia did conform to one of two strategies while under predation risk: either swim fast high up in the water column or swim slowly close to the bottom. Hence, this dichotomous behavior is driven by strategies combining speed and depth in different constellations. In a broader context, our findings highlight the importance of considering both the spatial and temporal dimensions of predation events in order to correctly detect antipredator responses.

Size‐specific reduction in kelp consumption by New Zealand urchins exposed to chemical cues from the red rock lobster

AbstractSea urchins can strongly reduce their mobility, exposure to predation, and feeding rates upon detection of chemical cues produced by predators, driving behavioral effects on grazing activity that may contribute to macroalgal community dynamics. However, the extent of chemically induced antipredator behaviors in urchins can vary by predator–prey species pair and ecological context and is therefore important to characterize in novel settings. Additionally, the effect of predator and prey size on urchin reactions to predator cues has rarely been considered, with the few existing examples yielding mixed conclusions. Here, we used a replicated split‐plot experiment to measure the effects of red rock lobsters (Jasus edwardsii) on consumption of macroalgae by the New Zealand sea urchin (Evechinus chloroticus) across a range of predator and prey body sizes. Overall, per‐capita consumption rates of kelp by urchins declined by 30% in the presence of lobsters, though feeding activity varied widely among individuals. Based on mass‐specific measurements of feeding rates, responses to predator cues appeared similar across all urchin sizes but only yielded distinguishable differences in the amount of kelp consumed in trials with larger urchins due to their considerably higher feeding capacity. Conversely, consumption rates of kelp by urchins had no apparent relationship with lobster size, likely due to chemical cue saturation in our experimental setting or a risk gradient that was insufficient to elicit a graded behavioral response. Our findings provide new evidence for a nonconsumptive effect of lobsters on feeding rates of an important grazer that can potentially reinforce the ecological role of this key predator in New Zealand kelp beds.

Risk Perception: Chemical Stimuli in Predator Detection and Feeding Behaviour of the Invasive Round Goby Neogobius melanostomus.

The round goby Neogobius melanostomus is a notoriously invasive fish originating from the Ponto-Caspian region that in recent decades has successfully spread across the globe. One of its primary impacts is direct predation; in addition, when entering new ecosystems, the round goby is likely to become a food resource for many higher native predators. However, little is known either about the indirect effects of predators on the round goby as prey or its feeding behaviour and activity. The non-consumptive effect of the presence of higher native predators presumably plays an important role in mitigating the impact of non-native round gobies as mesopredators on benthic invertebrate communities, especially when both higher- and mesopredators occupy the same habitat. We tested the food consumption probability and gut evacuation rates in round gobies in response to chemical signals from a higher predator, the European eel Anguilla anguilla. Gobies were placed individually in experimental arenas equipped with shelters and exposed to water from a tank in which (a) the higher predator had actively preyed on a heterospecific prey, earthworms Lumbricus sp. (the heterospecific treatment; HS); (b) the higher predator had fed on round gobies (the conspecific treatment; CS); or (c) the water was provided as a control treatment (C). To ensure exposure to the chemical stimuli, this study incorporated the application of skin extracts containing damaged-released alarm cues from the CS treatment; distilled water was used for the remaining treatments. No significant differences were observed in either the food consumption probability or gut evacuation rate in the tested treatments. Despite the lack of reaction to the chemical stimuli, round gobies did exhibit high evacuation rates (R = 0.2323 ± 0.011 h-1; mean ± SE) in which complete gut clearance occurred within 16 h regardless of the applied treatment. This rapid food processing suggests high efficiency and great pressure on resources regardless of the presence or not of a higher predator. These findings hint at the boldness of round gobies, which did not exhibit any pronounced threat sensitivity. This would seem to suggest great efficiency in food processing and a potential competitive advantage over local native species when colonising new ecosystems, irrespective of the presence of native predators. Our study did not detect any non-consumptive effect attributable to the higher predator, given that the feeding activity of the invasive round goby was not altered.

Population and community consequences of perceived risk from humans in wildlife

AbstractHuman activities catalyse risk avoidance behaviours in wildlife across taxa and systems. However, the broader ecological significance of human‐induced risk perception remains unclear, with a limited understanding of how phenotypic responses scale up to affect population or community dynamics. We present a framework informed by predator–prey ecology to predict the occurrence of non‐consumptive effects (NCE) and trait‐mediated indirect effects (TMIE) of anthropogenic disturbances. We report evidence from a comprehensive review of the different types of human‐induced behavioural and physiological phenotypic changes and their influence on vital rates and population parameters in wildlife. Evidence for human‐induced NCEs and TMIEs is mixed, with half of published studies finding a relationship between human activities, phenotypic change and population outcomes. The net effects of anthropogenic NCEs and TMIEs depend on the mismatch between the phenotypic response and the lethality of human activity. However, strong research biases in taxa, systems, human disturbance types and demographic measures prevent unified inference about the prevalence of population responses to human activities. Coexistence with and conservation of wildlife requires additional research linking human‐induced phenotypic change to population and community outcomes.

Rapid evolution of consumptive and non-consumptive predator effects on prey population densities, bioenergetics and stoichiometry.

Predators can strongly influence prey populations not only through consumptive effects (CE) but also through non-consumptive effects (NCE) imposed by predation risk. Yet, the impact of NCE on bioenergetic and stoichiometric body contents of prey, traits that are shaping life histories, population and food web dynamics, is largely unknown. Moreover, the degree to which NCE can evolve and can drive evolution in prey populations is rarely studied. A 6-week outdoor mesocosm experiment with Caged-Fish (NCE) and Free-Ranging-Fish (CE and NCE) treatments was conducted to quantify and compare the effects of CE and NCE on population densities, bioenergetic and stoichiometric body contents of Daphnia magna, a keystone species in freshwater ecosystems. We tested for evolution of CE and NCE by using experimental populations consisting of D. magna clones from two periods of a resurrected natural pond population: a pre-fish period without fish and a high-fish period with high predation pressure. Both Caged-Fish and Free-Ranging-Fish treatments decreased the body size and population densities, especially in Daphnia from the high-fish period. Only the Free-Ranging-Fish treatment affected bioenergetic variables, while both the Caged-Fish and Free-Ranging-Fish treatments shaped body stoichiometry. The effects of CE and NCE were different between both periods indicating their rapid evolution in the natural resurrected population. Both the Caged-Fish and Free-Ranging-Fish treatments changed the clonal frequencies of the experimental Daphnia populations of the pre-fish as well as the high-fish period, indicating that not only CE but also NCE induced clonal sorting, hence rapid evolution during the mesocosm experiment in both periods. Our results demonstrate that CE as well as NCE have the potential to change not only the body size and population density but also the bioenergetic and stoichiometric characteristics of prey populations. Moreover, we show that these responses not only evolved in the studied resurrected population, but that CE and NCE also caused differential rapid evolution in a time frame of 6 weeks (ca. four to six generations). As NCE can evolve as well as can drive evolution, they may play an important role in shaping eco-evolutionary dynamics in predator-prey interactions.

Non-Consumptive Effects of Harmonia axyridis on the Reproduction and Metabolism of Spodoptera frugiperda.

An increasing body of research has underscored the significant impact of non-consumptive effects on the dynamics of prey pests, encompassing growth, development, reproduction, and metabolism across various vertebrate and invertebrate taxa, rivaling the influence of consumption effects. In our investigation, we delved into the non-consumptive effects exerted by the natural predatory enemy Harmonia axyridis on the reproductive capacity and metabolism of Spodoptera frugiperda adults. Our findings revealed a substantial decrease in the reproductive ability of S. frugiperda adults when exposed to the non-consumptive effects of H. axyridis. Concurrently, we observed an elevation in hydrogen peroxide (H2O2) content and the activities of antioxidant enzymes such as superoxide dismutases (SODs), catalases (CATs), and peroxidases (PODs). Furthermore, notable alterations were detected in energy metabolism, characterized by heightened triglyceride levels and diminished glycogen and trehalose concentrations. These outcomes underscored the adaptive response of the pest aimed at mitigating non-consumptive adverse effects by augmenting antioxidant enzyme activity to counteract oxidative stress and minimize cellular damage. Nonetheless, this defensive mechanism entails a significant expenditure of energy resources, resulting in shifts in energy utilization. Elevated triglyceride levels and reduced glycogen and trehalose concentrations diminish available resources for reproductive processes, such as egg laying, ultimately culminating in decreased fecundity. This study contributes novel insights into the non-consumptive effects observed in insects, while also furnishing valuable insights into the mechanisms underlying insect stress responses.

Predator-prey interactions across hunting mode, spatial domain size, and habitat complexities.

Predator-prey interactions are a fundamental part of community ecology, yet the relative importance of consumptive and nonconsumptive effects (NCEs) (defined as a risk-induced response that alters prey fitness) has not been resolved. Theory suggests that the emergence and subsequent predominance of consumptive or NCEs depend on the given habitat's complexity as well as predator hunting mode and spatial domain sizes of both predator and prey, but their relative influence on the outcome of predator-prey interactions is unknown. We built agent-based models in NetLogo to simulate predator-prey interactions for three hunting modes-sit-and-wait, sit-and-pursue, and active-while concurrently simulating large versus small spatial domain sizes for both predators and prey. We studied (1) how hunting mode and spatial domain size interact to influence the emergence of consumptive or NCEs and (2) how, when NCEs do dominate, hunting mode and spatial domain separately or additively determine prey shifts in time, space, and habitat use. Our results indicate consumptive effects only dominate for active predators when prey habitat domains overlap completely with the predator's spatial domain and when sit-and-wait and sit-and-pursue predators and their prey both have large spatial domains. Prey are most likely to survive when they shift their time but most frequently shift their habitat. Our paper helps to better understand the underlying mechanisms that drive consumptive or NCEs to be most dominant.

The Impact of Predation Risks on the Development and Fecundity of Bactrocera dorsalis Hendel.

Predators are dependent on the capture of prey to meet their energetic and nutritive requirements, which brings the risk of predation to prey. The predation risk is divided into consumptive and non-consumptive effects. Non-consumptive effects may manifest through altered growth and ontogenetic trajectories in prey species, a dynamic modulated by olfactory or other sensory cues from predators. Bactrocera dorsalis Hendel represents a major invasive threat to global horticulture. While earlier research was primarily centered on the consumptive interactions between B. dorsalis and its natural enemies, the potential consequences of non-consumptive interactions on the development of B. dorsalis have been overlooked. In this study, we investigated the impact of predation risk effects, induced by both visual exposure to the predatory mantis Hierodula patellifera Serville and its associated odor, on the life history traits of B. dorsalis. Female B. dorsalis demonstrated a reduced developmental time in the presence of a caged predator (H. patellifera) or predator odors, but showed significantly increased fecundity. Conversely, males displayed no significant change in developmental time. Additionally, neither the female nor male body weight at death was significantly influenced by the predation risk from the caged predator or predator odors. This study investigated the effects of predation risk on the development and reproduction of B. dorsalis, emphasizing the potential importance of odor risk in biological and pest control.

Behavioral trade-offs and multitasking by elk in relation to predation risk from Mexican gray wolves.

Predator non-consumptive effects (NCE) can alter prey foraging time and habitat use, potentially reducing fitness. Prey can mitigate NCEs by increasing vigilance, chewing-vigilance synchronization, and spatiotemporal avoidance of predators. We quantified the relationship between Mexican wolf (Canis lupus baileyi) predation risk and elk (Cervus canadensis) behavior. We conducted behavioral observations on adult female elk and developed predation risk indices using GPS collar data from Mexican wolves, locations of elk killed by wolves, and landscape covariates. We compared a priori models to determine the best predictors of adult female behavior and multitasking. Metrics that quantified both spatial and temporal predation risk were the most predictive. Vigilance was positively associated with increased predation risk. The effect of predation risk on foraging and resting differed across diurnal periods. During midday when wolf activity was lower, the probability of foraging increased while resting decreased in high-risk areas. During crepuscular periods when elk and wolves were most active, increased predation risk was associated with increased vigilance and slight decreases in foraging. Our results suggest elk are temporally avoiding predation risk from Mexican wolves by trading resting for foraging, a trade-off often not evaluated in behavioral studies. Probability of multitasking depended on canopy openness and an interaction between maternal period and predation risk; multitasking decreased prior to parturition and increased post parturition in high-risk areas. Openness was inversely related to multitasking. These results suggest adult female elk are altering the type of vigilance used depending on resource availability/quality, current energetic needs, and predation risk. Our results highlight potentially important, but often-excluded behaviors and trade-offs prey species may use to reduce the indirect effects of predation and contribute additional context to our understanding of predator-prey dynamics.

Variation in farming damselfish behaviour creates a competitive landscape of risk on coral reefs.

Interspecific interactions are fundamental drivers of animal space use. Yet while non-consumptive effects of predation risk on prey space use are well-known, the risk of aggressive interactions on space use of competitors is largely unknown. We apply the landscape of risk framework to competition-driven space use for the first time, with the hypothesis that less aggressive competitors may alter their behaviour to avoid areas of high competitor density. Specifically, we test how aggressive risk from territorial algal-farming damselfishes can shape the spatial distribution of herbivore fish competitors. We found that only the most aggressive damselfish had fewer competitors in their surrounding area, demonstrating that individual-level behavioural variation can shape spatial distributions. In contradiction to the landscape of risk framework, abundances of farming damselfish and other fishes were positively associated. Our results suggest that reef fishes do not simply avoid areas of high damselfish abundance, but that spatial variation in aggressive behaviour, rather than of individuals, created a competitive landscape of risk. We emphasize the importance of individual-level behaviour in identifying patterns of space use and propose expanding the landscape of risk framework to non-predatory interactions to explore cascading behavioural responses to aggressive risk.

Ghosts of parasites past influence current non-consumptive effects in Drosophila nigrospiracula

Parasites can indirectly impact hosts through non-consumptive effects (NCEs) via changes in behaviour, morphology, and/or physiology. These responses can be understood in terms of the ecology of fear (ectoparasites) or the ecology of disgust (endoparasites) framework. We tested the hypothesis that NCEs of parasite exposure (e.g., parasite avoidance and defense) trade off with other important behaviours such as feeding and resting. We predicted that when exposed to parasites (without infection), hosts will increase their defensive behaviors at the expense of feeding. We also posited that history of exposure (without infection), or previous infection would impact the expression of these NCEs. The study system involves a cactophilic fruit fly (Drosophila nigrospiracula) and a naturally occurring parasitic mite (Macrocheles subbadius). First, we assessed how prior mite exposure affected fly behaviour in response to current parasite exposure. Mite presence resulted in increased grooming and movement, but exposure history did not affect these behaviours. However, the interaction between previous and current exposure influenced host feeding and resting behaviours. We found that previously exposed flies increased feeding and decreased resting upon a secondary mite exposure. In a second experiment, we tested the role of infection history on current parasite exposure. Compared with naïve flies, previously infected flies were expected to increase defensive behaviours upon secondary exposure. Flies increased defensive and ambulatory behaviour in the presence of mites, and consequently less time was spent resting but feeding was unaffected. None of the behaviours measured were affected by previous infection status. In general, current parasite exposure resulted in NCEs. Moreover, our results showed that previous exposure (without infection) to parasites may have an even stronger effect upon secondary exposure than infection history. Our study highlights the importance of the ecology of fear and the role that exposure and infection history plays in generating NCEs of parasitism.

Do recolonising wolves trigger non‐consumptive effects in European ecosystems? A review of evidence

Predators can affect ecosystems through non‐consumptive effects (NCE) on their prey, which can lead to cascading effects on the vegetation. In mammalian communities, such cascading effects on whole ecosystems have mainly been demonstrated in protected areas, but the extent to which such effects may occur in more human‐dominated landscapes remains disputable. With the recolonisation of wolves Canis lupus in Europe, understanding the potential for such cascading processes becomes crucial for understanding the ecological consequences of wolf recovery and making appropriate management recommendations. Here, we investigate the evidence for non‐consumptive effects of wolves on their wild ungulate prey and cascading effects on the vegetation in European landscapes. We reviewed empirical studies reporting wild ungulate responses to wolves involving spatio‐temporal behaviour at large and fine spatial scales, activity patterns, vigilance, grouping, physiological effects, and effects on the vegetation. We reveal that non‐consumptive effects of wolves in Europe have been studied in few regions and with focus on regions with low human impact, are highly context‐dependent, and might often be overruled by human‐related factors. Hence, we highlight the need for a description of human influence in NCE studies. We discuss challenges in NCE research and the potential for advances in future research on NCE of wolves in a human‐dominated landscape. We emphasise the need for wildlife management to restore ecosystem complexity and processes, to allow non‐consumptive predator effects to occur.

A theory for context-dependent effects of mammalian trampling on ecosystem nitrogen cycling.

Large mammalian herbivores substantially impact ecosystem functioning. As their populations are dramatically altered globally, disentangling their consumptive and non-consumptive effects is critical to advance mechanistic understanding and improve prediction of effects over ecosystem and Earth-system spatial extents. Mathematical models have played an important role in clarifying potential mechanisms of herbivore zoogeochemistry, based mostly on their consumptive effects as primary consumers and recyclers of organic and inorganic matter via defecation and urination. Trampling is a ubiquitous effect among walking vertebrates, but the consequences and potential mechanisms of trampling in diverse environments remain poorly understood. We derive a novel mathematical model of large mammalian herbivore effects on ecosystem nitrogen cycling, focusing on how trampling and environmental context impact soil processes. We model herbivore trampling with a linear positive or negative additive effect on soil-mediated nitrogen cycling processes. Combining analytical and numerical analyses, we find trampling by large mammalian herbivores is likely to decrease nitrogen mineralisation rate across diverse environments, such as temperate grassland and boreal forest. These effects are mediated by multiple potential mechanisms, including trampling-induced changes to detritivore biomass and functioning (e.g. rate of organic matter consumption). We also uncover scenarios where trampling can increase nitrogen mineralisation rate, contingent on the environment-specific relative sensitivity of detritivore mineral-nitrogen release and detritivore mortality, to trampling. In contrast to some consumptive mechanisms, our results suggest the pace of soil nitrogen cycling prior to trampling has little influence over the direction of the trampling net effect on nitrogen mineralisation, but that net effects may be greater in slow-cycling systems (e.g. boreal forests) than in fast-cycling systems (e.g. grasslands). Our model clarifies the potential consequences of previously overlooked mechanisms of zoogeochemistry that are common to all terrestrial biomes. Our results provide empirically testable predictions to guide future progress in empirical and theoretical studies of herbivore effects in diverse environmental contexts. Resolving ecological contingencies around animal consumptive and non-consumptive effects will improve whole-ecosystem management efforts such as restoration and rewilding.