A parasite's modification of host behavior reduces predation on its host

Parasite modification of host behavior is common, and the literature is dominated by demonstrations of enhanced predation on parasitized prey resulting in transmission of parasites to their next host. We present a case in which predation on parasitized prey is reduced. Despite theoretical modeling suggesting that this phenomenon should be common, it has been reported in only a few host–parasite–predator systems. Using a system of gregarine endosymbionts in host mosquitoes, we designed experiments to compare the vulnerability of parasitized and unparasitized mosquito larvae to predation by obligate predatory mosquito larvae and then compared behavioral features known to change in the presence of predatory cues. We exposed Aedes triseriatus larvae to the parasite Ascogregarina barretti and the predator Toxohrynchites rutilus and assessed larval mortality rate under each treatment condition. Further, we assessed behavioral differences in larvae due to infection and predation stimuli by recording larvae and scoring behaviors and positions within microcosms. Infection with gregarines reduced cohort mortality in the presence of the predator, but the parasite did not affect mortality alone. Further, infection by parasites altered behavior such that infected hosts thrashed less frequently than uninfected hosts and were found more frequently on or in a refuge within the microcosm. By reducing predation on their host, gregarines may be acting as mutualists in the presence of predation on their hosts. These results illustrate a higher‐order interaction, in which a relationship between a species pair (host–endosymbiont or predator–prey) is altered by the presence of a third species.     

Complex dynamics of a predator–prey–parasite system: An interplay among infection rate,predator's reproductive gain and preference

Parasites are considered as an important factor in regulating their host populations through trait-mediated effects. On the other hand, predation becomes particularly interesting in host–parasite systems because predation can significantly alter the abundance of parasites and their host population. The combined effects of parasites and predator on host population and community structure therefore may have larger effect. Different field experiments confirm that predators consume disproportionately large number of infected prey in comparison to their susceptible counterpart. There are also substantial evidences that predator has the ability to distinguish prey that have been infected by a parasite and avoid such prey to reduce fitness cost. In this paper we study the predator–prey dynamics, where the prey species is infected by some parasites and predators consume both the susceptible and infected prey with some preference. We demonstrate that complexity in such systems largely depends on the predator's selectivity, force of infection and predator's reproductive gain. If the force of infection and predator's reproductive gain are low, parasites and predators both go to extinction whatever be the predator's preference. The story may be totally different in the opposite case. Survival of species in stable, oscillatory or chaotic states, and their extinction largely depend on the predator's preference. The system may also show two coexistence equilibrium points for some parameter values. The equilibrium with lower susceptible prey density is always stable and the equilibrium with higher susceptible prey density is always unstable. These results suggest that understanding the consequences of predator's selectivity or preference may be crucial for community structure involving parasites.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

Sustainability of exploited ecologically interdependent species

This paper examines the application of maximum sustainable yield (MSY) policy in ecosystem and indicates when the ecosystem based fisheries management approach is required for conservation purpose. To describe the possible impacts of applying global MSY policy in an ecosystem, we have considered both specialist and generalist prey–predator models with different fishing efforts. It is found that harvesting both prey and predator species in specialist prey–predator systems, to achieve global maximum sustainable total yield (MSTY) under independent efforts, will cause the extinction of the predator species. In contrast, the global MSTY may exist in a generalist prey–predator system. If global MSTY does not exist, then it is due to the extinction of predator species. Hence, the prey species never goes to extinction under independent efforts and this scenario is quite different from the one found under combined harvesting effort.     

Bottom‐up processes drive reproductive success in an apex predator

One of the central goals of the field of population ecology is to identify the drivers of population dynamics, particularly in the context of predator–prey relationships. Understanding the relative role of top‐down versus bottom‐up drivers is of particular interest in understanding ecosystem dynamics. Our goal was to explore predator–prey relationships in a boreal ecosystem in interior Alaska through the use of multispecies long‐term monitoring data. We used 29 years of field data and a dynamic multistate site occupancy modeling approach to explore the trophic relationships between an apex predator, the golden eagle, and cyclic populations of the two primary prey species available to eagles early in the breeding season, snowshoe hare and willow ptarmigan. We found that golden eagle reproductive success was reliant on prey numbers, but also responded prior to changes in the phase of the snowshoe hare population cycle and failed to respond to variation in hare cycle amplitude. There was no lagged response to ptarmigan populations, and ptarmigan populations recovered quickly from the low phase. Together, these results suggested that eagle reproduction is largely driven by bottom‐up processes, with little evidence of top‐down control of either ptarmigan or hare populations. Although the relationship between golden eagle reproductive success and prey abundance had been previously established, here we established prey populations are likely driving eagle dynamics through bottom‐up processes. The key to this insight was our focus on golden eagle reproductive parameters rather than overall abundance. Although our inference is limited to the golden eagle–hare–ptarmigan relationships we studied, our results suggest caution in interpreting predator–prey abundance patterns among other species as strong evidence for top‐down control.     

Do phytoseiid mites select the best prey species in terms of reproductive success?

Optimal foraging theory predicts that predators prefer those prey species that are most rewarding in terms of reproductive success, which is dependent on prey quality and prey availability. To investigate which selection pressures may have moulded prey preference in an acarine system consisting of two prey species and three predator species, we tested whether prey preference of the predators is matched by the associated reproductive success.The predators involved areAmblyseius finlandicus (Oudemans),Am. potentillae (Garman) andTyphlodromus pyri Scheuten. The prey species are the apple rust mite (Aculus schlechtendali (Nalepa)) and the fruit-tree red spider mite (Panonychus ulmi (Koch)).Reproductive success was assessed in terms of intrinsic rate of increase and for one predator also in terms of diapause induction. All three predator species reached highest reproductive success on the same prey species: apple rust mite. This was most pronounced for the predatorAm. finlandicus, because its larval stage suffered severe mortality when feeding onP. ulmi.An independent study on prey preference of the three predator species (Dicke et al., 1988) revealed thatAm. finlandicus prefersAc. schlechtendali toP. ulmi, whereas the other two predator species have the reverse preference.Thus, on the basis of current data, prey preference ofAm. finlandicus can be understood in terms of reproductive success. However, this is not so for prey preference ofT. pyri andAm. potentillae. Investigations needed for a better understanding of prey preference of the last-named two predator species are discussed.     

Top–down limits on prey populations may be more severe in larger prey species,despite having fewer predators

Variation in the vulnerability of herbivore prey to predation is linked to body size, yet whether this relationship is size‐nested or size‐partitioned remains debated. If size‐partitioned, predators would be focused on prey within their preferred prey size range. If size‐nested, smaller prey species should become increasingly more vulnerable because increasingly more predators are capable of catching them. Yet, whether either of these strategies manifests in top–down prey population limitation would depend both on the number of potential predator species as well as the total mortality imposed. Here we use a rare ecosystem scale ‘natural experiment’ comparing prey population dynamics between a period of intense predator persecution and hence low predator densities and a period of active predator protection and population recovery. We use three decades of data on herbivore abundance and distribution to test the role of predation as a mechanism of population limitation among prey species that vary widely in body size. Notably, we test this within one of the few remaining systems where a near‐full suite of megaherbivores occur in high density and are thus able to include a thirtyfold range in herbivore body size gradient. We test whether top–down limitation on prey species of particular body size leads to compositional shifts in the mammalian herbivore community. Our results support both size‐nested and size‐partitioning predation but suggest that the relative top–down limiting impact on prey populations may be more severe for intermediate sized species, despite having fewer predators than small species. In addition we show that the gradual recovery of predator populations shifted the herbivore community assemblage towards large‐bodied species and has led to a community that is strongly dominated by large herbivore biomass.     

High reproductive rates result in high predation risks: a mechanism promoting the coexistence of competing prey in spatially structured populations

I tested the hypothesis that spatial structure provides a trade-off between reproduction and predation risk and thereby facilitates predator-mediated coexistence of competing prey species. I compared a cellular automata model to a mean-field model of two prey species and their common predator. In the mean-field model, the prey species with the higher reproductive rate (the superior competitor) always outcompeted the other species (the inferior competitor), both in the presence of and the absence of the predator. In the cellular automata model, both prey species, which differed only in their reproductive rates, coexisted for a long time in the presence of their common predator at intermediate levels of predation. At low predation rates, the superior competitor dominated, while high predation rates favored the inferior competitor. This discrepancy in the results of the different models was due to a trade-off that spontaneously emerged in spatially structured populations; that is, the more clustered distribution of the superior competitor made it more susceptible to predation. In addition, coexistence of competing prey species declined with increasing dispersal ranges of either prey or predator, which suggests that the trade-off that results from spatial structure becomes less important as either prey or predator disperse over a broader range.     

Increasing isolation reduces predator:prey species richness ratios in aquatic food webs

The number of species that live in a habitat typically declines as that habitat becomes more isolated. However, the influence of habitat isolation on patterns of food web structure, in particular the ratio of predator to prey species richness, is less well understood. We placed aquatic mesocosms at varying distances from ponds that acted as sources of potential colonists; then we examined how isolation affected the ratio of predator:prey species richness in the communities that assembled. In the final sampling, a total of 21 species (12 prey and 9 predators) of insects, crustaceans, and amphibians had colonized the mesocosms. We found that total species richness, as well as the richness of predators and prey, declined with increasing isolation. However, predator richness declined more rapidly than prey richness with increasing isolation, which lead to decreasing predator:prey ratios. This result conflicts with prior demonstrations of invariant predator:prey ratios in freshwater communities.     

Implications of shared predation for space use in two sympatric leporids

Spatial variation in habitat riskiness has a major influence on the predator–prey space race. However, the outcome of this race can be modulated if prey shares enemies with fellow prey (i.e., another prey species). Sharing of natural enemies may result in apparent competition, and its implications for prey space use remain poorly studied. Our objective was to test how prey species spend time among habitats that differ in riskiness, and how shared predation modulates the space use by prey species. We studied a one‐predator, two‐prey system in a coastal dune landscape in the Netherlands with the European hare (Lepus europaeus) and European rabbit (Oryctolagus cuniculus) as sympatric prey species and red fox (Vulpes vulpes) as their main predator. The fine‐scale space use by each species was quantified using camera traps. We quantified residence time as an index of space use. Hares and rabbits spent time differently among habitats that differ in riskiness. Space use by predators and habitat riskiness affected space use by hares more strongly than space use by rabbits. Residence time of hare was shorter in habitats in which the predator was efficient in searching or capturing prey species. However, hares spent more time in edge habitat when foxes were present, even though foxes are considered ambush predators. Shared predation affected the predator–prey space race for hares positively, and more strongly than the predator–prey space race for rabbits, which were not affected. Shared predation reversed the predator–prey space race between foxes and hares, whereas shared predation possibly also released a negative association and promoted a positive association between our two sympatric prey species. Habitat riskiness, species presence, and prey species’ escape mode and foraging mode (i.e., central‐place vs. noncentral‐place forager) affected the prey space race under shared predation.     

Individual base model of predator-prey system shows predator dominant dynamics

Individual base model of predator-prey system is constructed. Both predator and prey species have age structure and cohorts of early reproductive age have competitive advantage. The model has linear functional response in predation behavior and includes the effect of interference among predators and delay of population growth from resource intake, not by functional response but by calculation procedure. Each foraging action is calculated successively and surplus or scarce of acquired resources is interpreted into population size through individual birth and death. This model shows that biomass of prey killed by predator is dependent on demand of predator and that heterogeneity in predator population is essential in persistency and stability of predator-prey system. Heterogeneity of predator makes predator individuals of less competing ability die rapidly. Rapid death of weak individuals causes rapid decrease of total demand of predator and that makes enough room for survived predators. Therefore, the biomass of killed prey is dependent on predator's demand. As young or infant population of predator are the more vulnerable to shortage of prey, and when many of them cannot survive to reproductive age, they can stabilize the system by wasting excessive prey with only temporal numerical increase of predator population.     

Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay

Recent studies of aquatic food webs show that parasite diversity is concentrated in nodes that likely favour transmission. Various aspects of parasite diversity have been observed to be correlated with the trophic level, size, diet breadth, and vulnerability to predation of hosts. However, no study has attempted to distinguish among all four correlates, which may have differential importance for trophically transmitted parasites occurring as larvae or adults. We searched for factors that best predict the diversity of larval and adult endoparasites in 4105 fish in 25 species studied over a three-year period in the Bothnian Bay, Finland. Local predator–prey relationships were determined from stomach contents, parasites, and published data in 8,229 fish in 31 species and in seals and piscivorous birds. Fish that consumed more species of prey had more diverse trophically transmitted adult parasites. Larval parasite diversity increased with the diversity of both prey and predators, but increases in predator diversity had a greater effect. Prey diversity was more strongly associated with the diversity of adult parasites than with that of larvae. The proportion of parasite species present as larvae in a host species was correlated with the diversity of its predators. There was a notable lack of association with the diversity of any parasite guild and fish length, trophic level, or trophic category. Thus, diversity is associated with different nodal properties in larval and adult parasites, and association strengths also differ, strongly reflecting the life cycles of parasites and the food chains they follow to complete transmission.     

Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission

While the recent inclusion of parasites into food‐web studies has highlighted the role of parasites as consumers, there is accumulating evidence that parasites can also serve as prey for predators. Here we investigated empirical patterns of predation on parasites and their relationships with parasite transmission in eight topological food webs representing marine and freshwater ecosystems. Within each food web, we examined links in the typical predator–prey sub web as well as the predator–parasite sub web, i.e. the quadrant of the food web indicating which predators eat parasites. Most predator– parasite links represented ‘concomitant predation’ (consumption and death of a parasite along with the prey/host; 58–72%), followed by ‘trophic transmission’ (predator feeds on infected prey and becomes infected; 8–32%) and predation on free‐living parasite life‐cycle stages (4–30%). Parasite life‐cycle stages had, on average, between 4.2 and 14.2 predators. Among the food webs, as predator richness increased, the number of links exploited by trophically transmitted parasites increased at about the same rate as did the number of links where these stages serve as prey. On the whole, our analyses suggest that predation on parasites has important consequences for both predators and parasites, and food web structure. Because our analysis is solely based on topological webs, determining the strength of these interactions is a promising avenue for future research.     

Indirect effects between shared prey: Predictions for

Suppression of a target prey by a predator can depend on its surrounding community, including the presence of nontarget, alternative prey. Basic theoretical models of two prey species that interact only via a shared predator predict that adding an alternative prey should increase predator numbers and ultimately lower target pest densities as compared to when the target pest is the only prey. While this is an alluring prediction, it does not explain the numerous responses empirically observed. To better understand and predict the indirect interactions produced by shared predation, we explore how additional prey species affect three broad ecological mechanisms, the predator's reproductive, movement, and functional responses. Specifically, we review current theoretical models of shared predation by focusing on these mechanisms, and make testable predictions about the effects of shared predation. We find that target predation is likely to be higher in the two prey system because of predator reproduction, especially when: predators are prey limited, alternative or total prey density is high, or alternative prey are available over time. Target predation may also be greater because of predator movement, but only under certain movement rules and spatial distributions. Predator foraging behavior is most likely to cause lower target predation in the two-prey system, when per capita predation is limited by something other than prey availability. It is clear from this review that no single theoretical generalization will accurately predict community-level effects for every system. However, we can provide testable hypotheses for future empirical and theoretical investigations of indirect interactions and help enhance their potential use in biological control.     

Bistability and limit cycles in generalist predator–prey dynamics

Since generalist predators feed on a variety of prey species they tend to persist in an ecosystem even if one particular prey species is absent. Predation by generalist predators is typically characterized by a sigmoidal functional response, so that predation pressure for a given prey species is small when the density of that prey is low. Many mathematical models have included a sigmoidal functional response into predator–prey equations and found the dynamics to be more stable than for a Holling type II functional response. However, almost none of these models considers alternative food sources for the generalist predator. In particular, in these models, the generalist predator goes extinct in the absence of the one focal prey. We model the dynamics of a generalist predator with a sigmoidal functional response on one dynamic prey and fixed alternative food source. We find that the system can exhibit up to six steady states, bistability, limit cycles and several global bifurcations.     

How population loss through habitat boundaries determines the dynamics of a predator–prey system

The increased persistence of predator–prey systems when interactions are distributed through the space has been acknowledged by both empirical and theoretical studies. One salient feature of predator–prey interactions in heterogeneous space, for example, is the existence of cycles with reduced amplitude when compared with a homogeneous landscape. Although the role of spatial interactions in shaping the dynamics of predator–prey systems has been extensively studied, still very few works have focused on the effects of habitat loss and fragmentation on these systems. In this work, we study the population dynamics of a predator–prey system in a single finite habitat with flux at the boundaries. Species movement and growth are described through a reaction–diffusion model with Rosenzweig–MacArthur type local interactions. Conforming with the existing literature, we find that the reduction of habitat size, or increasing of species movement rates equivalently, has the potential to decrease the amplitude of oscillations and even bring the system to a steady coexistence equilibrium above a threshold. We observe, however, situations in which this trend is reversed. This occurs when species movement rates and response at patch boundaries interact to induce non-trivial patterns of species distributions. These distributions are characterized by anti-correlation between predator and prey, creating then spatial refugia for prey. Our results highlight the role of population loss through habitat boundaries in determining the dynamics of predator–prey interactions.     

Dynamics of predator and modular prey: effects of module consumption on stability of prey–predator system

In traditional models of predator–prey population dynamics, it is usually assumed that consumed prey are immediately removed from the population. However, in plant–herbivore interactions, damaged plants are generally alive after attacks by herbivores. This can result in successive or simultaneous attacks by multiple predators on a single prey item (here, the term prey is expanded to include plants). We constructed a mathematical model with two time scales, taking into account predation processes within a generation, considering post‐predation survival and the modularity of prey. We assumed that a prey item can be divided into modules and that it can be fed on by multiple predators or parasitized by multiple parasites at the same time. The model includes two essential factors: the modularity of prey for predators (n) and the detaching/attaching ratio of predators to prey (ε). Based on the formulae, we revealed a general property of realistic dynamics in plant–herbivore and host–parasite interactions. The analysis showed that the model could be approximated by models with the type I, type II or Beddington–DeAngelis functional responses by taking appropriate limits to the situations. When modularity is low or the detaching/attaching ratio is high, population dynamics tend to be stabilized. These stabilizing effects may be related to interference competition among predator individuals or increases in free prey modules and free predator individuals. In the limit of high modularity, the ratio of the attached prey modules to the total prey modules becomes negligible and the dynamics tend to be destabilized. However, if quantity and quality of prey modules are negatively correlated, the equilibrium is likely to be stabilized at high modularity as long as it remains feasible. These results suggest that considering post‐predation survival and modularity of prey is crucial to understand predator–prey interactions.     

Assessing changes in arthropod predator–prey interactions through DNA‐based gut content analysis—variable environment,stable diet

Analysing the structure and dynamics of biotic interaction networks and the processes shaping them is currently one of the key fields in ecology. In this paper, we develop a novel approach to gut content analysis, thereby deriving a new perspective on community interactions and their responses to environment. For this, we use an elevational gradient in the High Arctic, asking how the environment and species traits interact in shaping predator–prey interactions involving the wolf spider Pardosa glacialis. To characterize the community of potential prey available to this predator, we used pitfall trapping and vacuum sampling. To characterize the prey actually consumed, we applied molecular gut content analysis. Using joint species distribution models, we found elevation and vegetation mass to explain the most variance in the composition of the prey community locally available. However, such environmental variables had only a small effect on the prey community found in the spider's gut. These observations indicate that Pardosa exerts selective feeding on particular taxa irrespective of environmental constraints. By directly modelling the probability of predation based on gut content data, we found that neither trait matching in terms of predator and prey body size nor phylogenetic or environmental constraints modified interaction probability. Our results indicate that taxonomic identity may be more important for predator–prey interactions than environmental constraints or prey traits. The impact of environmental change on predator–prey interactions thus appears to be indirect and mediated by its imprint on the community of available prey.     

The underrated importance of predation in transmission ecology of direct lifecycle parasites

Most parasites with complex life cycles exploit trophic webs to pass from host to host in order to develop and, eventually, reproduce. Thus predation constitutes the necessary route for transmission. Conversely, the transmission of parasites that use a single host to develop and reproduce should be, in principle, not particularly affected by host trophic ecology. Here I challenge this view, showing that predation may be relevant also for direct lifecycle parasites. I used a large dataset of fish trophic interactions to investigate if the degree of monogenean species overlap in predators and prey deviated from randomness. I demonstrated that predators and prey often share more monogenean parasite genera than explained by host habitat ecology, geographical distribution and phylogeny. This suggests that predation may play an important role in promoting monogenean host range expansion. In addition, a non‐negligible proportion of considered prey–predator pairs showed a significantly high overlap in their monogenean parasites at the species level. This may indicate a tendency of some monogenean parasites to evolve transmission strategies targeted towards host interactions. If this hypothesis is true, these monogenean parasites would be much more vulnerable to co‐extinction than previously thought. Synthesis Predation is not expected to play an important role in the ecology and evolution of simple life cycle parasites. Yet, several predator fish tend to share with their prey more monogenean parasites than one would expect predicted from their geographical distribution, habitat preference, and or phylogenetic relationships. This suggests that some monogenean parasites have evolved transmission strategies more targeted towards host interactions than towards species‐specific traits. If this hypothesis is supported, it would have strong implications on host–parasite evolutionary ecology, primarily, suggesting the existence of peculiar situations where some parasites have evolved high specialized host finding behaviors to expand their host range.     

Antagonistic species interaction drives selection for sex in a predator–prey system

The evolutionary maintenance of sexual reproduction has long challenged biologists as the majority of species reproduce sexually despite inherent costs. Providing a general explanation for the evolutionary success of sex has thus proven difficult and resulted in numerous hypotheses. A leading hypothesis suggests that antagonistic species interaction can generate conditions selecting for increased sex due to the production of rare or novel genotypes that are beneficial for rapid adaptation to recurrent environmental change brought on by antagonism. To test this ecology‐based hypothesis, we conducted experimental evolution in a predator (rotifer)–prey (algal) system by using continuous cultures to track predator–prey dynamics and in situ rates of sex in the prey over time and within replicated experimental populations. Overall, we found that predator‐mediated fluctuating selection for competitive versus defended prey resulted in higher rates of genetic mixing in the prey. More specifically, our results showed that fluctuating population sizes of predator and prey, coupled with a trade‐off in the prey, drove the sort of recurrent environmental change that could provide a benefit to sex in the prey, despite inherent costs. We end with a discussion of potential population genetic mechanisms underlying increased selection for sex in this system, based on our application of a general theoretical framework for measuring the effects of sex over time, and interpreting how these effects can lead to inferences about the conditions selecting for or against sexual reproduction in a system with antagonistic species interaction.