Evolution and Ecology of Parasite Avoidance.

Parasite avoidance is a host defense that reduces the contact rate with parasites. We investigate avoidance as a primary driver of variation among individuals in the risk of parasitism and the evolution of host-parasite interactions. To bridge mechanistic and taxonomic divides, we define and categorize avoidance by its function and position in the sequence of host defenses. We also examine the role of avoidance in limiting epidemics and evaluate evidence for the processes that drive its evolution. Throughout, we highlight important directions to advance our conceptual and theoretical understanding of the role of avoidance in host-parasite interactions. We emphasize the need to test assumptions and quantify the effect of avoidance independent of other defenses. Importantly, many open questions may be most tractable in host systems that have not been the focus of traditional behavioral avoidance research, such as plants and invertebrates.

Oviposition-site shift in phytophagous mites reflects a trade-off between predator avoidance and rainstorm resistance.

Predators can reduce prey population densities by driving them to undertake costly defences. Here, we report on a remarkable example of induced antipredator defence in spider mites that enhances the risk to rainstorms. Spider mites live on the undersides of host plant leaves and usually oviposit on the leaf undersurface. When they are threatened by predatory mites, they oviposit on three-dimensional webs to avoid egg predation, although the cost of ovipositing on webs has not yet been clearly determined. We prepared bean plants harbouring spider mite (Tetranychus kanzawai) eggs on either leaf surfaces or webs and exposed them to rainstorms outdoors. We found that fewer eggs remained on webs than on leaf surfaces. We then examined the synergistic effect of wind and rain by simulating both in the laboratory. We conclude that ovipositing on webs comes at a cost, as eggs are washed off the host plants by wind and rain. This may explain why spider mite populations decrease drastically in the rainy season, although they inhibit leaf undersides where they are not directly exposed to rainfall.

Behaviorally-mediated trophic cascade attenuated by prey use of risky places at safe times.

The mere threat of predation may incite behavioral changes in prey that lead to community-wide impacts on productivity, biodiversity, and nutrient cycling. The paucity of experimental manipulations, however, has contributed to controversy over the strength of this pathway in wide-ranging vertebrate systems. We investigated whether simulated gray wolf (Canis lupus) presence can induce behaviorally-mediated trophic cascades, specifically, whether the 'fear' of wolf olfactory cues alone can change deer foraging behavior in ways that affect plants and soils. Wolves were recently removed from the Cedar Creek Ecosystem Science Reserve (Minnesota, USA), such that consumptively mediated predator effects were negligible. At 32 experimental plots, we crossed two nested treatments: wolf urine application and herbivore exclosures. We deployed camera traps to quantify how white-tailed deer (Odocoileus virginianus) adjusted their spatiotemporal habitat use, foraging, and vigilance in response to wolf cues and how these behavioral changes affected plant productivity, plant communities, and soil nutrients. Weekly applications of wolf urine significantly altered deer behavior, but deer responses did not cascade to affect plant or soil properties. Deer substantially reduced crepuscular activity at wolf-simulated sites compared to control locations. As wolves in this area predominantly hunted during mornings and evenings, this response potentially allows deer to maximize landscape use by accessing dangerous areas when temporal threat is low. Our experiment suggests that prey may be sensitive to 'dynamic' predation risk that is structured across both space and time and, consequentially, prey use of risky areas during safe times may attenuate behaviorally-mediated trophic cascades at the predator-prey interface.

The ecological consequences of a pandemic.

The COVID-19 pandemic has altered human behaviour in profound ways, prompting some to question whether the associated economic and social impacts might outweigh disease impacts. This fits into a burgeoning ecological paradigm suggesting that for both predator-prey and parasite-host interactions, non-consumptive effects (avoidance) can be orders of magnitude stronger than consumptive effects (sickness and death). Just as avoidance of predators and parasites imposes substantial costs on prey and hosts, altered behaviour to reduce the transmission of COVID-19 has impacted human fitness and wellbeing. But the effects of infectious disease avoidance do not stop there; non-consumptive effects of predators and parasites often trigger cascading indirect effects in natural systems. Similarly, shifts in human behaviour due to COVID-19 have triggered myriad indirect effects on species and the environment, which can be positive, negative or neutral. We urge researchers to recognize that the environmental impacts associated with lockdowns are indirect effects of the virus. In short, the global response to COVID-19 suggests that the non-consumptive effects of a pathogen, and resulting indirect effects, can be profound.

Healthy but smaller herds: Predators reduce pathogen transmission in an amphibian assemblage.

Predators and pathogens are fundamental components of ecological communities that have the potential to influence each other via their interactions with victims and to initiate density- and trait-mediated effects, including trophic cascades. Despite this, experimental tests of the healthy herds hypothesis, wherein predators influence pathogen transmission, are rare. Moreover, no studies have separated effects mediated by density vs. traits. Using a semi-natural mesocosm experiment, we investigated the interactive effects of predatory dragonfly larvae (caged or lethal [free-ranging]) and a viral pathogen, ranavirus, on larval amphibians (grey treefrogs and northern leopard frogs). We determined the influence of predators on ranavirus transmission and the relative importance of density- and trait-mediated effects on observed patterns. Lethal predators reduced ranavirus infection prevalence by 57%-83% compared to no-predator and caged-predator treatments. The healthy herds effect was more strongly associated with reductions in tadpole density than behavioural responses to predators. We also assessed whether ranavirus altered the responses of tadpoles to predators. In the absence of virus, tadpoles reduced activity levels and developed deeper tails in the presence of predators. However, there was no evidence that virus presence or infection altered responses to predators. Finally, we compared the magnitude of trophic cascades initiated by individual and combined natural enemies. Lethal predators initiated a trophic cascade by reducing tadpole density, but caged predators and ranavirus did not. The absence of a virus-induced trophic cascade is ostensibly the consequence of limited virus-induced mortality and the ability of infected individuals to continue interacting within the community. Our results provide support for the healthy herds hypothesis in amphibian communities. We uniquely demonstrate that density-mediated effects of predators outweigh trait-mediated effects in driving this pattern. Moreover, this study was one of the first to directly compare trophic cascades caused by predators and pathogens. Our results underscore the importance of examining the interactions between predators and pathogens in ecology.

Ecology of fear: environment-dependent parasite avoidance among ovipositing Drosophila.

Habitat avoidance is an anti-parasite behaviour exhibited by at-risk hosts that can minimize exposure to parasites. Because environments are often heterogeneous, host decision-making with regards to habitat use may be affected by the presence of parasites and habitat quality simultaneously. In this study we examine how the ovipositing behaviour of a cactiphilic fruit fly, Drosophila nigrospiracula, is affected by the presence of an ectoparasitic mite, Macrocheles subbadius, in conjunction with other environmental factors - specifically the presence or absence of conspecific eggs and host plant tissue. We hypothesized that the trade-off between site quality and parasite avoidance should favour ovipositing at mite-free sites even if it is of inferior quality. We found that although flies avoided mites in homogeneous environments (86% of eggs at mite-free sites), site quality overwhelmed mite avoidance. Both conspecific eggs (65% of eggs at infested sites with other Drosophila eggs) and host plant tissue (78% of eggs at infested sites with cactus) overpowered mite avoidance. Our results elucidate the context-dependent decision-making of hosts in response to the presence of parasites in variable environments, and suggest how the ecology of fear and associated trade-offs may influence the relative investment in anti-parasite behaviour in susceptible hosts.

The control of risk hypothesis: reactive vs. proactive antipredator responses and stress-mediated vs. food-mediated costs of response.

Inducible defences against predators evolve because they reduce the rate of direct predation, but this benefit is offset by the cost (if any) of defence. If antipredator responses carry costs, the effect of predators on their prey is partitioned into two components, direct killing and risk effects. There is considerable uncertainty about the strength of risk effects, the factors that affect their strength, and the mechanisms that underlie them. In some cases, antipredator responses are associated with a glucocorticoid stress response, and in other cases they are associated with trade-offs between food and safety, but there is no general theory to explain this variation. Here, I develop the control of risk (COR) hypothesis, predicting that proactive responses to predictable and controllable aspects of risk will generally have food-mediated costs, while reactive responses to unpredictable or uncontrollable aspects of predation risk will generally have stress-mediated costs. The hypothesis is grounded in laboratory studies of neuroendocrine stressors and field studies of food-safety trade-offs. Strong tests of the COR hypothesis will require more studies of responses to natural variation in predation risk and the physiological consequences of these responses, but its explanatory power can be illustrated with existing case studies.

Predictive power of food web models based on body size decreases with trophic complexity.

Food web models parameterised using body size show promise to predict trophic interaction strengths (IS) and abundance dynamics. However, this remains to be rigorously tested in food webs beyond simple trophic modules, where indirect and intraguild interactions could be important and driven by traits other than body size. We systematically varied predator body size, guild composition and richness in microcosm insect webs and compared experimental outcomes with predictions of IS from models with allometrically scaled parameters. Body size was a strong predictor of IS in simple modules (r2  = 0.92), but with increasing complexity the predictive power decreased, with model IS being consistently overestimated. We quantify the strength of observed trophic interaction modifications, partition this into density-mediated vs. behaviour-mediated indirect effects and show that model shortcomings in predicting IS is related to the size of behaviour-mediated effects. Our findings encourage development of dynamical food web models explicitly including and exploring indirect mechanisms.

Fish predators reduce kelp frond loss via a trait-mediated trophic cascade.

Although trophic cascades were originally believed to be driven only by predators eating prey, there is mounting evidence that such cascades can be generated in large part via non-consumptive effects. This is especially important in cascades affecting habitat-forming foundation species that in turn, influence associated communities. Here, we use laboratory and field experiments to identify a trait-mediated indirect interaction between predators and an abundant kelp in a marine temperate reef system. Predation risk from a microcarnivorous fish, the señorita, suppressed grazing by the host-specific seaweed limpet, which in turn, influenced frond loss of the habitat-forming feather boa kelp. This trophic cascade was pronounced because minor amounts of limpet grazing decreased the strength required to break kelp fronds. Cues from fish predators mitigated kelp loss by decreasing limpet grazing; we found 86% of this indirect interaction between predator and kelp was attributed to the non-consumptive effect in the laboratory and 56% when applying the same effect size calculations to the field. In field manipulations, the non-consumptive effect of señorita was as strong as the total predator effect and most importantly, as strong as the uncaged, "open" treatment with natural levels of predators. Our findings demonstrate that the mere presence of this fish reduces frond loss of the feather boa kelp through a trait-mediated trophic cascade. Moreover, despite large volumes of water, current flow, and wave energy, we clearly demonstrate a strong non-consumptive effect via an apparent chemical cue from señorita, suggesting that chemically mediated trait-driven cascades may be more prevalent in subtidal marine systems than we are currently aware.

Moving beyond linear food chains: trait-mediated indirect interactions in a rocky intertidal food web.

In simple, linear food chains, top predators can have positive indirect effects on basal resources by causing changes in the traits (e.g. behaviour, feeding rates) of intermediate consumers. Although less is known about trait-mediated indirect interactions (TMIIs) in more complex food webs, it has been suggested that such complexity dampens trophic cascades. We examined TMIIs between a predatory crab (Carcinus maenas) and two ecologically important basal resources, fucoid algae (Ascophyllum nodosum) and barnacles (Semibalanus balanoides), which are consumed by herbivorous (Littorina littorea) and carnivorous (Nucella lapillus) snails, respectively. Because crab predation risk suppresses snail feeding rates, we hypothesized that crabs would also shape direct and indirect interactions among the multiple consumers and resources. We found that the magnitude of TMIIs between the crab and each resource depended on the suite of intermediate consumers present in the food web. Carnivorous snails (Nucella) transmitted TMIIs between crabs and barnacles. However, crab-algae TMIIs were transmitted by both herbivorous (Littorina) and carnivorous (Nucella) snails, and these TMIIs were additive. By causing Nucella to consume fewer barnacles, crab predation risk allowed fucoids that had settled on or between barnacles to remain in the community. Hence, positive interactions between barnacles and algae caused crab-algae TMIIs to be strongest when both consumers were present. Studies of TMIIs in more realistic, reticulate food webs will be necessary for a more complete understanding of how predation risk shapes community dynamics.

The biogeography of trophic cascades on US oyster reefs.

Predators can indirectly benefit prey populations by suppressing mid-trophic level consumers, but often the strength and outcome of trophic cascades are uncertain. We manipulated oyster reef communities to test the generality of potential causal factors across a 1000-km region. Densities of oyster consumers were weakly influenced by predators at all sites. In contrast, consumer foraging behaviour in the presence of predators varied considerably, and these behavioural effects altered the trophic cascade across space. Variability in the behavioural cascade was linked to regional gradients in oyster recruitment to and sediment accumulation on reefs. Specifically, asynchronous gradients in these factors influenced whether the benefits of suppressed consumer foraging on oyster recruits exceeded costs of sediment accumulation resulting from decreased consumer activity. Thus, although predation on consumers remains consistent, predator influences on behaviour do not; rather, they interact with environmental gradients to cause biogeographic variability in the net strength of trophic cascades.

Predatory fish sounds can alter crab foraging behaviour and influence bivalve abundance.

The risk of predation can have large effects on ecological communities via changes in prey behaviour, morphology and reproduction. Although prey can use a variety of sensory signals to detect predation risk, relatively little is known regarding the effects of predator acoustic cues on prey foraging behaviour. Here we show that an ecologically important marine crab species can detect sound across a range of frequencies, probably in response to particle acceleration. Further, crabs suppress their resource consumption in the presence of experimental acoustic stimuli from multiple predatory fish species, and the sign and strength of this response is similar to that elicited by water-borne chemical cues. When acoustic and chemical cues were combined, consumption differed from expectations based on independent cue effects, suggesting redundancies among cue types. These results highlight that predator acoustic cues may influence prey behaviour across a range of vertebrate and invertebrate taxa, with the potential for cascading effects on resource abundance.

Prey state shapes the effects of temporal variation in predation risk.

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as 'trophic heat' during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length.

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.

Enemy-Risk Effects in Parasitoid-Exposed Diamondback Moth Larvae: Potential Mediation of the Interaction by Host Plants.

Enemy-risk effects (i.e., non-consumptive effects) describe the non-lethal fitness costs incurred by animals when they perceive a risk of predation. These effects can result from fear-associated changes in behavior and physiology. Diamondback moth larvae (Plutella xylostella) are known to violently wriggle backwards and drop from their host plants, usually suspending themselves with a silk thread, when threatened by predators and parasitoids. Here, we investigated the developmental costs associated with this behavior when larvae were exposed to its specialist parasitoid wasp (Diadegma insulare). Additionally, the structural and chemical properties of plants are well-known to influence predation and parasitism rates of herbivorous insects. Yet, few studies have examined the influence of plants on enemy-risk effects. Therefore, we examined the developmental costs associated with parasitism risk on two host plants. Diamondback moth larvae were placed on either cabbage or Virginia pepperweed plants and exposed to gravid parasitoids with truncated ovipositors, which prevented piercing of the host cuticle without affecting host searching and attacking behaviors. On Virginia pepperweed, risk of parasitism resulted in reduced larval weight gain, longer development time, and smaller adult size compared to larvae that were not exposed to parasitoids. However, on cabbage, parasitoid exposure prolonged development time but had no significant effects on larval weight gain and adult size. On both plants, parasitoid-exposed larvae were found feeding on older foliage than younger foliage. Our findings demonstrate that the enemy-escape behavior of diamondback moths has developmental costs and that plants may mediate the intensity of these enemy-risk effects.

Extending the ecology of fear: Parasite-mediated sexual selection drives host response to parasites.

The 'ecology of fear' describes the negative effects natural enemies have on potential victims even when those victims are not consumed or infected. Although recent work has demonstrated parasites have non-consumptive effects (NCE) on potential hosts, how these effects vary within host populations is not well understood. We investigated how NCE vary based on host risk of infection and relative cost of infection by measuring the metabolic rate (MR) of naive Drosophila nigrospiracula exposed to an ectoparasite, Macrocheles subbadius. We tested two mutually exclusive hypotheses: 1) asymmetrical costs of infection drive adaptions for stronger responses to parasite exposure; or 2) asymmetrical risks of infection drive adaptions for stronger responses to parasite exposure. In this system, male flies have higher costs of infection relative to female flies due to parasite-mediated sexual selection; similarly, virgin females experience higher costs of infection relative to mated females. Risk of infection also varies among flies because mites preferentially infect female flies over males, and mites preferentially infect mated females over virgin females. Our results were compatible with the hypothesis that costs of infection drive the strength of response to mite risk. Female flies responded to parasite exposure with a 15.1% increase in MR, while exposed males showed a stronger response with a 31.3% increase in MR. Mated females increased their MR by 34.8% during mite exposure whereas virgin females experienced an increase of 61.2%. Our findings suggest that NCE of parasites can vary based on state-dependent costs of infection.

Larval predation in malaria vectors and its potential implication in malaria transmission: an overlooked ecosystem service?

The role of aquatic predators in controlling the anopheline aquatic stage has been known for decades. Recently, studies have highlighted that exposition to predation stress during aquatic development can have a profound impact on life-history traits (e.g. growth rate, fecundity and longevity) and consequently on the ability of adults to transmit human malaria parasites. In this study, we present a review aiming to contextualize the role of Anopheles larvae predators as an ecosystem factor interacting with the malaria pathogen through its vector, i.e. the female adult Anopheles. We first envisage the predator diversity that anopheline vectors are susceptible to encounter in their aquatic habitats. We then focus on mosquito-predator interactions with a special mention to anti-predator behaviors and prey adaptations developed to deal with the predation threat. Next, we address the direct and indirect effects of larval predation stress on mosquito populations and on individual life-history traits, which strongly suggest some carry-over effect of the impact of larval predation on vectorial capacity. The last part addresses the impact of human activities on larval predation. Concluding remarks highlight gaps in the knowledge of anopheline bio-ecology which may constitute avenues for researchers in the future.