Food web context modifies predator foraging and weakens trophic interaction strength.

Trophic interaction modifications (TIM) are widespread in natural systems and occur when a third species indirectly alters the strength of a trophic interaction. Past studies have focused on documenting the existence and magnitude of TIMs; however, the underlying processes and long-term consequences remain elusive. To address this gap, we experimentally quantified the density-dependent effect of a third species on a predator's functional response. We conducted short-term experiments with ciliate communities composed of a predator, prey and non-consumable 'modifier' species. In both communities, increasing modifier density weakened the trophic interaction strength, due to a negative effect on the predator's space clearance rate. Simulated long-term dynamics indicate quantitative differences between models that account for TIMs or include only pairwise interactions. Our study demonstrates that TIMs are important to understand and predict community dynamics and highlights the need to move beyond focal species pairs to understand the consequences of species interactions in communities.

Infection risk associated with carnivore carcasses may govern trophic interactions between maggots and insectivorous passerine birds.

Infection risk by pathogenic agents motivates hosts to avoid using resources with high risks. This, in turn, results in increased availability of these resources for other species that are more tolerant of infections. For instance, carcasses of mammalian carnivores are frequently avoided by conspecific or closely related carnivores, allowing them to be almost exclusively used by maggots. This may lead to novel interactions with other species. This study investigated the consumption of maggots from carnivore carcasses by non-corvid passerines. We successfully monitored 66 raccoon carcasses in Hokkaido, Japan, from 2016 to 2019. Vertebrates only scavenged 14 carcasses before maggot dispersal; the other 52 carcasses produced abundant maggots that regularly fed at least 12 species of non-corvid passerines. Surprisingly, predation occurred at a distance from the carcasses, mainly after maggot dispersal for pupation, despite the higher efficiency of feeding on maggot masses on the carcasses. Birds are likely to reduce the potential risk of infection from the carcass and/or from maggots on the carcasses. Overall, only 1% of maggots were consumed. Our results suggest that necrophagous flies could benefit from the infection risk associated with carnivore carcasses, which may decrease scavenging by other carnivores and constrain maggot consumption by insectivorous birds.

Effects of predation risk on parasite-host interactions and wildlife diseases.

Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock-on effects, such as trophic cascades, on the wider ecosystem. While such indirect effects stemming from the fear of predation have received extensive attention for herbivore-plant and predator-prey interactions, much less is known about how they alter parasite-host interactions and wildlife diseases. In this synthesis, we present a conceptual framework for how predation risk-as perceived by organisms that serve as hosts-can affect parasite-host interactions, with implications for infectious disease dynamics. By basing our approach on recent conceptual advances with respect to predation risk effects, we aim to expand this general framework to include parasite-host interactions and diseases. We further identify pathways through which parasite-host interactions can be affected, for example, through altered parasite avoidance behavior or tolerance of hosts to infections, and discuss the wider relevance of predation risk for parasite and host populations, including heuristic projections to population-level dynamics. Finally, we highlight the current unknowns, specifically the quantitative links from individual-level processes to population dynamics and community structure, and emphasize approaches to address these knowledge gaps.

Predation risk-mediated indirect effects promote submerged plant growth: Implications for lake restoration.

Biological manipulation, involving fish stockings, is commonly used to counteract the deterioration of submerged vegetation in eutrophic lakes. Nevertheless, the non-consumptive effects (NCEs) of stocked carnivorous fish are often overlooked. Using a controlled experimental system, we investigated the NCEs of a native carnivorous fish, snakehead (Channa argus), on two key biological factors, herbivore-dominated grass carp (Ctenopharyngodon idella) and disturbance-dominated loach (Misgurnus anguillicaudatus), influencing submerged plants growth. Additionally, we conducted a meta-analysis on predation risk and primary productivity. The results reveal that predation risk induces oxidative stress damage and affects grass carp growth. Non-significant changes in cortisol and glucose may be linked to predation risk prediction. Simultaneously, predation risk reduces fish feeding and disturbance behavior, relieving pressure on submerged plants to be grazed and disturbed, thereby supporting plant development. The presence of submerged plants, in turn, enhances loach activity and influences water body characteristics through negative feedback. Furthermore, the meta-analysis results indicate the facilitative effect of predation risk on primary producers. Our findings contribute to the understanding of biological manipulation theory. We demonstrate that the predation risk associated with introducing carnivorous fish can promote the growth of submerged plants through behaviorally mediated indirect effects. This highlights the potential utility of predation risk in lake restoration efforts.

Effect of predation risk on parasite transmission from first to second intermediate trematode hosts.

Predators can affect parasite-host interactions when directly preying on hosts or their parasites. However, predators may also have non-consumptive indirect effects on parasite-host interactions when hosts adjust their behaviour or physiology in response to predator presence. In this study, we examined how chemical cues from a predatory marine crab affect the transmission of a parasitic trematode from its first (periwinkle) to its second (mussel) intermediate host. Laboratory experiments revealed that chemical cues from crabs lead to a threefold increase in the release of trematode cercariae from periwinkles as a result of increased periwinkle activity. This positive effect on transmission was contrasted by a 10-fold reduction in cercarial infection rates in the second intermediate host when we experimentally exposed mussels to cercariae and predator cues. The low infection rates were caused by a substantial reduction in mussel filtration activity in the presence of predator cues, preventing cercariae from entering the mussels. To assess the combined net effect of both processes, we conducted a transmission experiment between infected periwinkles and uninfected mussels. Infection levels of mussels in the treatments with crab cues were sevenfold lower than in mussels without crab chemical cues. This suggests that predation risk effects on mussel susceptibility can counteract the elevated parasite release from first intermediate hosts, with negative net effects on parasite transmission. These experiments highlight that predation risk effects on parasite transmission can have opposing directions at different stages of the parasite's life cycle. Such complex non-consumptive predation risk effects on parasite transmission may constitute an important indirect mechanism affecting prevalence and distribution patterns of parasites in different hosts across their life cycle.

A rodent herbivore reduces its predation risk through ecosystem engineering.

Predator-prey interactions are ubiquitous and powerful forces that structure ecological communities.1-3 Habitat complexity has been shown to be particularly important in regulating the strength of predator-prey interactions.4-6 While it is well established that changes in habitat structure can alter the efficacy of predatory and anti-predatory behaviors,7-9 little is known about the consequences of engineering activity by prey species who modify the external environment to reduce their own predation risk. Using field surveys and manipulative experiments, we evaluated how habitat modification by Brandt's voles (Lasiopodomys brandtii) influences predation risk from a principal avian predator (shrike; Lanius spp.) in a steppe grassland, located in Inner Mongolia, China. We found that voles actively modify habitat structure by cutting down a large, unpalatable bunchgrass species (Achnatherum splendens) in the presence of shrikes, a behavior that disappeared when these avian predators were excluded experimentally. The damage activities of these voless dramatically decreased the volume of unpalatable grasses, which in turn reduced visitations by shrikes and thus mortality rates. Our study shows that herbivorous prey that act as ecosystem engineers can directly reduce their own predation risk by modifying habitat structure. Given the ubiquity of predation risks faced by consumers, and the likely ability of many consumers to alter the habitat structure in which they live, the interplay between predation risk and ecosystem engineering may be an important but unappreciated mechanism at play in natural communities.

Community-wide consequences of nonconsumptive predator effects on a foundation species.

Predators can exert nonconsumptive effects (NCEs) on prey, which often take place through prey behavioural adjustments to minimise predation risk. As NCEs are widespread in nature, interest is growing to determine whether NCEs on a prey species can indirectly influence several other species simultaneously, thus leading to changes in community structure. In this study, we investigate whether a predator can exert NCEs on a foundation species and indirectly affect community structure. Through laboratory experiments, we first tested whether the predatory marine snail Acanthina monodon exerts negative NCEs on larviphagy (consumption of pelagic larvae) and phytoplankton filtration rates of the mussel Perumytilus purpuratus, an intertidal foundation species. These hypotheses stem from the notion that mussels may decrease feeding activities in the presence of predator cues to limit detection by predators. Afterwards, a field experiment tested whether the presence of A. monodon near mussel beds leads to higher colonisation rates of invertebrates that reproduce through pelagic larvae (expected under a lower larviphagy in P. purpuratus) and to a lower algal biomass on P. purpuratus shells (expected under a lower metabolite excretion in the mussels), thereby changing the community structure of the species typically found in P. purpuratus beds. The laboratory experiments revealed that waterborne cues from A. monodon limit the larviphagy and filtration rates of P. purpuratus. In turn, the field experiment showed that A. monodon cues led to greater abundances of barnacles and bivalves and a lower algal biomass in P. purpuratus beds, thus altering community structure. Overall, this study shows that a predator can indirectly affect community structure through NCEs on an invertebrate foundation species. As invertebrate foundation species are ubiquitous worldwide, understanding predator NCEs on these organisms could help to better understand community regulation in systems structured by such species.

Parasites and Their Impact on Ecosystem Nutrient Cycling.

Consumer species alter nutrient cycling through nutrient transformation, transfer, and bioturbation. Parasites have rarely been considered in this framework despite their ability to indirectly alter the cycling of nutrients via their hosts. A simple mathematical framework can be used to assess the relative importance of parasite-derived nutrients in an ecosystem.

Ecosystem engineering strengthens bottom-up and weakens top-down effects via trait-mediated indirect interactions.

Trophic interactions and ecosystem engineering are ubiquitous and powerful forces structuring ecosystems, yet how these processes interact to shape natural systems is poorly understood. Moreover, trophic effects can be driven by both density- and trait-mediated interactions. Microcosm studies demonstrate that trait-mediated interactions may be as strong as density-mediated interactions, but the relative importance of these pathways at natural spatial and temporal scales is underexplored. Here, we integrate large-scale field experiments and microcosms to examine the effects of ecosystem engineering on trophic interactions while also exploring how ecological scale influences density- and trait-mediated interaction pathways. We demonstrate that (i) ecosystem engineering can shift the balance between top-down and bottom-up interactions, (ii) such effects can be driven by cryptic trait-mediated interactions, and (iii) the relative importance of density- versus trait-mediated interaction pathways can be scale dependent. Our findings reveal the complex interplay between ecosystem engineering, trophic interactions, and ecological scale in structuring natural systems.

Contrasting complexity of adjacent habitats influences the strength of cascading predatory effects.

Although cascading effects of top predators can help structure communities, their influence may vary across habitats that differentially protect prey. Therefore, to understand how and to what degree habitat complexity can affect trophic interactions in adjacent habitats, we used a combination of a broad regional-scale survey, manipulative field trials, and an outdoor mesocosm experiment to quantify predator-prey interaction strengths across four trophic levels. Within estuaries of the southeastern USA, bonnethead sharks (Sphyrna tiburo) hunt blue crabs on mudflats and adjacent oyster reefs, two habitats with vastly different aboveground structure. Using 12-h tethering trials of blue crabs we quantified habitat-dependent loss rates of 37% on reefs and 78% on mudflats. We hypothesized that the sharks' predatory effects on blue crabs would cascade down to release a lower-level mud crab predator, which subsequently would increase juvenile oyster mortality, but that the cascade strength would be habitat-dependent. We experimentally manipulated predator combinations in split-plot mesocosms containing reef and mudflat habitats, and quantified oyster mortality. Bonnetheads exerted strong consumptive and non-consumptive effects on blue crabs, which ceased eating oysters in the sharks' presence. However, mud crabs, regardless of shark and blue crab presence, continued to consume oysters, especially within the structural refuge of the reef where they kept oyster mortality high. Thus, bonnetheads indirectly boosted oyster survival, but only on the mudflat where mud crabs were less active. Our work demonstrates how structural differences in adjacent habitats can moderate trophic cascades, particularly when mesopredators exhibit differential use of structure and different sensitivities to top predators.

Top predators negate the effect of mesopredators on prey physiology.

Predation theory and empirical evidence suggest that top predators benefit the survival of resource prey through the suppression of mesopredators. However, whether such behavioural suppression can also affect the physiology of resource prey has yet to be examined. Using a three-tier reef fish food web and intermittent-flow respirometry, our study examined changes in the metabolic rate of resource prey exposed to combinations of mesopredator and top predator cues. Under experimental conditions, the mesopredator (dottyback, Pseudochromis fuscus) continuously foraged and attacked resource prey (juveniles of the damselfish Pomacentrus amboinensis) triggering an increase in prey O2 uptake by 38 ± 12·9% (mean ± SE). The visual stimulus of a top predator (coral trout, Plectropomus leopardus) restricted the foraging activity of the mesopredator, indirectly allowing resource prey to minimize stress and maintain routine O2 uptake. Although not as strong as the effect of the top predator, the sight of a large non-predator species (thicklip wrasse, Hemigymnus melapterus) also reduced the impact of the mesopredator on prey metabolic rate. We conclude that lower trophic-level species can benefit physiologically from the presence of top predators through the behavioural suppression that top predators impose on mesopredators. By minimizing the energy spent on mesopredator avoidance and the associated stress response to mesopredator attacks, prey may be able to invest more energy in foraging and growth, highlighting the importance of the indirect, non-consumptive effects of top predators in marine food webs.

Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance.

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey.

Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host-parasite interactions.

Host-parasite interactions are subject to strong trait-mediated indirect effects from other species. However, it remains unexplored whether such indirect effects may occur across soil boundaries and connect spatially isolated organisms. Here, we demonstrate that, by changing plant (milkweed Asclepias sp.) traits, arbuscular mycorrhizal fungi (AMF) significantly affect interactions between a herbivore (the monarch butterfly Danaus plexippus) and its protozoan parasite (Ophryocystis elektroscirrha), which represents an interaction across four biological kingdoms. In our experiment, AMF affected parasite virulence, host resistance and host tolerance to the parasite. These effects were dependent on both the density of AMF and the identity of milkweed species: AMF indirectly increased disease in monarchs reared on some species, while alleviating disease in monarchs reared on other species. The species-specificity was driven largely by the effects of AMF on both plant primary (phosphorus) and secondary (cardenolides; toxins in milkweeds) traits. Our study demonstrates that trait-mediated indirect effects in disease ecology are extensive, such that below-ground interactions between AMF and plant roots can alter host-parasite interactions above ground. In general, soil biota may play an underappreciated role in the ecology of many terrestrial host-parasite systems.

Temporal constraints on predation risk assessment in a changing world.

Habitat degradation takes various forms and likely represents the most significant threat to our global biodiversity. Recently, we have seen considerable attention paid to increasing global CO2 emissions which lead to ocean acidification (OA). Other stressors, such as changing levels of ultraviolet radiation (UVR), also impact biodiversity but have received much less attention in the recent past. Here we examine fundamental questions about temporal aspects of risk assessment by coral reef damselfish and provide critical insights into how OA and UVR influence this assessment. Chemical cues released during a predator attack provide a rich source of information that other prey animals use to mediate their risk of predation and are the basis of the majority of trait-mediated indirect interactions in aquatic communities. However, we have surprisingly limited information about temporal aspects of risk assessment because we lack knowledge about how long chemical cues persist after they are released into the environment. Here, we showed that under ambient CO2 conditions (~385 µatm), alarm cues of ambon damselfish (Pomacentrus amboinensis) did not degrade within 30 min in the absence of ultraviolet radiation (UVR), but were degraded within 15 min when the CO2 was increased to ~905 µatm. In experiments that used filters to eliminate UVR, we found minimal degradation of alarm cues within 30 min, whereas under ambient UVR conditions, alarm cues were completely degraded within 15 min. Moreover, in the presence of both UVR and elevated CO2, alarm cues were broken down within 5 min. Our results highlight that alarm cues degrade surprisingly quickly under natural conditions and that anthropogenic changes have the potential to dramatically change rates of cue degradation in the wild. This has considerable implications for risk assessment and consequently the importance of trait-mediated indirect interactions in coral-reef communities.

Behavioural and physiological responses of limpet prey to a seastar predator and their transmission to basal trophic levels.

Besides the well-documented behavioural changes induced by predators on prey, predator-induced stress can also include a suite of biochemical, neurological and metabolic changes that may represent important energetic costs and have long-lasting effects on individuals and on the demography of prey populations. The rapid transmission of prey behavioural changes to lower trophic levels, usually associated with alteration of feeding rates, can substantially change and even reverse direction over the long term as prey cope with the energetic costs associated with predation-induced stress. It is therefore critical to evaluate different aspects and assess the costs of non-consumptive predator effects on prey. We investigated the behavioural and physiological responses of an herbivorous limpet, Fissurella limbata, to the presence of chemical cues and direct non-lethal contact by the common seastar predator, Heliaster helianthus. We also evaluated whether the limpets feeding behaviour was modified by the predator and whether this translated into positive or negative effects on biomass of the green alga, Ulva sp. Our experimental results show the presence of Heliaster led to increased movement activity, increased distances travelled, changes in time budget over different environmental conditions and increased feeding rate in the keyhole limpets. Moreover, additional experiments showed that, beyond the increased metabolic rate associated with limpet increased activity, predator chemical cues heighten metabolic rate as part of the induced stress response. Changes in individual movement and displacement distances observed through the 9-day experiment can be interpreted as part of the escape response exhibited by limpets to reduce the risk of being captured by the predator. Increased limpet feeding rate on algae can be visualized as a way individuals compensate for the elevated energetic costs of movement and heightened metabolic rates produced by the predator-induced stress, which can lead to negative effects on abundance of the lower trophic level. We suggest that in order to understand the total non-consumptive effect of predators in natural communities, it is necessary to evaluate not only short-term behavioural responses, but also the costs associated with the multiple interdependent pathways triggered by predator-induced stress, and determine how individuals cope with these costs in the long term.

Predator identity and trait-mediated indirect effects in a littoral food web.

Perturbations to the density of a species can be propagated to distant members of a food web via shifts in the density or the traits (i.e. behavior) of intermediary species. Predators with differing foraging modes may have different effects on prey behavior, and these effects may be transmitted differently through food webs. Here we test the hypothesis that shifts in the type of predator present in a food web indirectly affect the prey's resource independent of changes in the density of prey. We assessed the importance of predator identity in mediating the grazing effects of the freshwater snail Physa integra on its periphyton resources using field and mesocosm studies. Field observations showed that Physa used covered habitats more in ponds containing fish than in ponds containing crayfish or no predators at all. A field experiment confirmed that snail behavior depended on predator identity. Physa placed near caged pumpkinseed sunfish (Lepomis gibbosus) selected covered habitats, but Physa placed near caged crayfish (Orconectes rusticus) moved to the surface of the water. The effects of predator identity on periphtyon were then examined in a mesocosm experiment, using caged predators. Habitat use of Physa was similar to their habitat use in the field experiment. In the presence of caged sunfish, periphyton standing crop in covered habitats was reduced to 34% of the standing crop in the presence of crayfish. In contrast, periphyton in near-surface habitats was 110% higher in the presence of fish than in the presence of crayfish. Thus, the effects of predator identity on Physa behavior cascaded through the food web to affect the abundance and spatial distribution of periphyton.