Predicting disease dynamics requires a community perspective, incorporating multi‐species interactions involving hosts, pathogens, vectors, and consumers. In systems where pathogens are dependent on ...a vector for transmission from one host to another, predators can indirectly influence disease risk through direct effects on vectors. These effects may be consumptive if predators reduce vector abundance by capturing and killing vectors, or non‐consumptive if predators induce anti‐predator behavioral responses by vectors. Studies are accumulating that document cascading effects of predators on vector‐borne disease risk, but the mechanisms underlying these effects are often uncertain. Using a previously developed epidemiological model as a framework, I outline several mechanistic pathways by which predators can have consumptive and non‐consumptive effects on vectors, and present theoretical predictions about the cascading influence of these pathways on pathogen prevalence. I then review selected examples from the literature of vector‐borne plant pathogen systems where particular mechanistic pathways have been implicated. Together, the model predictions and the literature review reveal that, depending on the particular mechanisms at work, predators may reduce, leave unaffected, or even increase pathogen prevalence. In general, the consumptive effects of predators on vectors result in consistent reductions in pathogen prevalence. However, the non‐consumptive effects of predators that arise as a result of changes in pathogen transmission rates, vector birth rates, and non‐predation vector mortality rates are more variable, with the potential for context‐dependency and counter‐intuitive outcomes. Interactions among pathways are also possible, such that the magnitude of consumptive effects can depend upon the strength of non‐consumptive effects and vice versa. I conclude by highlighting the importance of teasing apart the various mechanistic pathways by which predators may indirectly influence pathogen prevalence, and clarifying the relationships among them, to accurately predict the consequences of predation for disease risk and the usefulness of biological control of vectors for suppression of plant pathogens.
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Evolution of resistance to transgenic crops producing toxins from Bacillus thuringiensis (Bt) threatens the sustainability of the technology. Examination of resistance mechanisms has largely focused ...on characterization of mutations in proteins serving as Bt toxin binding sites. However, insect microbial communities have the potential to provide host resistance to pesticides in a myriad of ways. Previous findings suggest the killing mechanism of Bt relies on enteric bacteria becoming pathogenic in the disrupted gut environment of the insect following Bt intoxication. Thus, here we hypothesized that resistance to Bt would alter the microbiome composition of the insect. Previous studies have manipulated the microbiome of susceptible insects and monitored their response to Bt. In our study, we characterized the associated bacterial communities of Bt‐resistant and ‐susceptible western corn rootworms, a widespread pest of maize in the United States. We found resistant insects harbor a bacterial community that is less rich and distinct from susceptible insects. After feeding on Bt‐expressing maize, susceptible insects exhibited dysbiosis of the associated bacterial community, whereas the community within resistant insects remained relatively unchanged. These results suggest resistance to Bt produces alterations in the microbiome of the western corn rootworm that may contribute to resistance. We further demonstrated that by itself, feeding on Bt toxin‐expressing seedlings caused a shift in the microbiota. This work provides a broader picture of the effect stressors have on microbiome composition, and the potential heritable changes induced as a result of intense selection.
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Drought events have the potential to mediate tri-trophic interactions. Changes in plant quality influence herbivore performance, which affects prey availability and quality for natural enemies. ...Parasitoid wasps are particularly vulnerable to these changes since their development is inextricably linked to that of their prey. However, we know little about the indirect effects of plant water limitation on parasitoid performance, especially the consequences of mild water limitation. This study investigated the ability of a parasitoid wasp (Aphidius colemani Viereck (Hymenoptera: Braconidae)) to suppress aphid (Rhopalosiphum padi L. (Hemiptera: Aphididae)) populations on well-watered, mildly stressed, or highly stressed wheat (Triticum aestivum L. (Poales: Poaceae)). We then investigated the role that aphid body size and behavioral interactions might play in wasp acceptance of aphid hosts. We found improved aphid suppression under mild and high-water limitation, but the underlying mechanisms were different. Mild-stress appeared to maximize parasitoid performance, as indicated by the highest mummy production. Aphids were larger when feeding on mildly stressed plants than on any other treatment, which suggests improved aphid quality for parasitoids. Improved aphid suppression under high-stress may have been driven by enhanced nonconsumptive effects. Despite improved aphid suppression, mummy formation was lowest on highly stressed plants. High-stress conditions have been shown to negatively affect aphid performance, so improved aphid suppression may be driven by poor aphid performance exacerbating the cost of interactions with parasitoids, such as stinging. No differences were observed in parasitoid foraging behaviors such as antennation or stinging across any treatments. This study highlights the importance of plant water stress intensity in affecting outcomes of parasitoid–host interactions.
Elucidating the relative strength of top-down and bottom-up forces in communities of phytophagus insects has been a major historical focus. Current consensus is that both forces play a role, but it ...is poorly known if these forces act differently on herbivores in the same assemblage and what factors underlie this variation. Using manipulative experiments with an assemblage of sap-feeding phytophagous insects (six species of planthoppers, leafhoppers, and heteropteran bugs) inhabiting intertidal Spartina marshes, we examined the association between herbivore behavior, risk of predation, and ultimately the relative impact of top-down (wolf spider predation) and bottom-up (host-plant nutrition) factors on the population density of each sap-feeding herbivore. A factorial experiment on open Spartina islets in the field (two levels of plant nutrition crossed with two levels of spider predation) showed that bottom-up and top-down manipulations differentially affected the various sap-feeders. Overall, bottom-up effects dominated in this sap-feeder community, whereby the density of all six sap-feeders increased when the nitrogen content of Spartina was elevated. By contrast, wolf-spider addition significantly suppressed populations of only the Prokelisia species and had little impact on the other four sap-feeder species in the community. Functional-response experiments and behavioral studies revealed that certain species (Prokelisia planthoppers) were at much higher risk of attack by wolf spiders than other sap-feeders in the assemblage and that risk of predation was associated with a species' particular "escape/defensive behavior." Moreover, risk of spider predation was roughly linked to the strength of top-down impacts in the field, because species with ineffective escape behaviors and a high risk of spider attack (Prokelisia planthoppers) were the only sap-feeders whose populations were suppressed by spider predation in the field. Thus, specific behavioral characteristics of the sap-feeders on Spartina influenced risk of predation and the relative strength of top-down and bottom-up impacts on their population dynamics. Notably, all herbivores in this system were positively influenced by elevated plant nutrition, only the common sap-feeder species (Prokelisia planthoppers) were adversely affected by spider predation, and it was the rarer sap-feeders in the assemblage that were least impacted by predation. These results call into question the overall pervasiveness of top-down forces and underscore the primacy of basal resources in structuring this community of phytophagous insects.
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The western corn rootworm, Diabrotica virgifera virgifera LeConte, is the most important insect of maize, Zea mays L., but knowledge of its interaction with water deficit on maize production is ...lacking. A series of greenhouse experiments using three infestation levels of the western corn rootworm, D. virgifera virgifera, under well-watered, moderately dry, and very dry soil moisture levels were conducted to quantify the interaction of western corn rootworm and soil water deficit on B73 × Mo17 maize growth and physiology. Three separate experiments were conducted. Soil moisture regimes were initiated 30 d postplanting for experiments using neonate and second-instar larvae and 30 d postinfestation in the experiment using eggs. In the neonate and second-instar experiments, there were no significant differences among western corn rootworm levels in their effects on leaf water potential, shoot dry weight, and root dry weight. The interaction of western corn rootworm and soil moisture significantly impacted the larval recovery in the neonate experiment, but no other significant interactions were documented between soil moisture levels and rootworm infestation levels. Overall, the results indicate that under the conditions of these experiments, the effect of water deficit was much greater on plants than the effect of western corn rootworm and that the interactions between water deficit and western corn rootworm levels minimally affected the measured parameters of plant performance.
In conservation biological control (CBC), we attempt to reduce pest problems by increasing the abundance and diversity of the natural enemy community. However, rather than consistently strengthening ...herbivore suppression, studies show that the conservation of natural enemy species richness sometimes weakens, or has no affect, on biological control. Evidence is mounting that this idiosyncratic mix of positive, negative, and neutral effects of enemy diversity is caused by niche complementarity, intraguild predation, and functional redundancy, respectively. While the balance of evidence suggests that the conservation of natural enemy diversity and biological control are compatible goals, CBC practitioners cannot ignore the fact that conserving intraguild predators can sometimes disrupt biological control. Recent studies have made important progress toward identifying the traits of enemies and their prey that promote intraguild predation, functional redundancy, and niche complementarity. However, intraguild predation has received more attention than niche complementarity, and more theoretical and empirical work is needed rectify this asymmetry. We suggest that a continued focus on natural enemy functional traits, particularly those that are expressed at larger spatiotemporal scales, will increase our ability to identify the “right” kind of diversity and may ultimately improve the practice of conservation biological control.
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Ecological stoichiometry provides a novel context for elucidating the occurrence of intraguild predation. Recent data show that predators on average have a higher nitrogen content and lower C:N ratio ...than potential herbivorous prey. Thus, many predators may be nitrogen limited, and intraguild predation may allow them to increase their nitrogen intake and growth by supplementing a diet of herbivores with more nitrogen-rich intraguild prey. We tested this hypothesis using an assemblage of salt-marsh-inhabiting arthropods. First, we determined the nitrogen content and C:N ratio of taxa in four trophic groups (plants, herbivores, omnivores, and predators). Second, we fed an intraguild predator, the wolf spider Pardosa, one of three diets (herbivores, intraguild prey, or an alternating mix of the two) and measured spider survival, growth, capture rate, and biomass and nitrogen intake. In general, body nitrogen content increased and C:N ratio decreased from lower to higher trophic levels for marsh-inhabiting species, with predators having a higher nitrogen content and lower C:N ratio than herbivores. Performance experiments showed that in one case Pardosa ingested more biomass and nitrogen and grew faster on a diet of intraguild prey (the planthopper egg predator Tytthus) than on a diet of herbivores (the planthopper Prokelisia dolus). This occurred because Pardosa captured more Tytthus than Prokelisia and not because Tytthus (a stoichiometric exception) was higher in nitrogen content. In another case, Pardosa grew slower on a diet of intraguild prey (the web-building spider Grammonota) than on a planthopper diet even though Grammonota was more nitrogen rich, a result we attribute to prey behavior and risk of predation. Mass gain and nitrogen intake in Pardosa were highly correlated with the biomass of prey consumed. However, after accounting for the biomass of prey consumed across all diet treatments, we found little evidence that either the nitrogen content or C:N stoichiometry of prey contributed to Pardosa's growth. Thus, there was little support for the hypothesis that the nitrogen stoichiometry of prey directly confers a performance advantage to Pardosa and in itself promotes intraguild predation. In this system, characteristics other than the nitrogen stoichiometry of prey play a significant role in prey capture and predator performance. Nonetheless, by supplementing their diet with readily captured intraguild prey, predators such as Pardosa can increase their nitrogen intake and performance.
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Within food webs, vectors of plant pathogens interact with individuals of other species across multiple trophic levels, including predators, competitors, and mutualists. These interactions may in ...turn affect vector-borne pathogens by altering vector fitness and behavior. Predators, for example, consume vectors and reduce their abundance, but often spur movement of vectors as they seek to avoid predation. However, a general framework to predict how species interactions affect vectors of plant pathogens, and the resulting spread of vector-borne pathogens, is lacking. Here we developed a mathematical model to assess whether interactions such as predation, competition, and mutualism affected the spread of vector-borne plant pathogens with nonpersistent or persistent transmission modes. We considered transmission mode because interactions affecting vector–host encounter rates were expected to most strongly affect nonpersistent pathogens that are transmitted with short feeding bouts; interactions that affect vector feeding duration were expected to most strongly affect persistent pathogens that require long feeding bouts for transmission. Our results show that interactions that affected vector behavior (feeding duration, vector–host encounter rates) substantially altered rates of spread for vector-borne plant pathogens, whereas those affecting vector fitness (births, deaths) had relatively small effects. These effects of species interactions were largely independent of transmission mode, except when interactions affected vector–host encounter rates, where effects were strongest for nonpersistent pathogens. Our results suggest that a better understanding of how vectors interact with other species within food webs could enhance our understanding of disease ecology.
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Feeding-induced plant resistance is a well-documented phenomenon for leaf-chewing insects. Furthermore, feeding-induced resistance provides the mechanistic basis for many cases of delayed ...interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap-feeding insects. The results we present here for salt marsh-inhabiting planthoppers (Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant-mediated interspecific competition between two sap-feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant-mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage-free islets of cordgrass in the field. Feeding-induced reductions in host-plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia planthoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant-mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding-depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding-induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contemporaneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.
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1. Antagonistic interactions among invertebrate predators such as intraguild predation and cannibalism have the potential to dampen top-down impacts on shared prey at lower trophic levels. Two ...abundant spider predators, the large wolf spider Pardosa littoralis and the small sheet-web builder Grammonota trivitatta co-occur on the salt marshes of eastern North America where they both attack planthoppers (Prokelisia spp.), the dominant herbivores on the marsh. Experiments both in the laboratory and field were used to assess the incidence of intraguild predation and cannibalism in these spiders and elucidate how such antagonistic interactions influence planthopper suppression. 2. Functional response experiments showed that with an increase in planthopper prey density, Grammonota captured more prey but not a higher proportion of that offered. Pardosa exhibited the same response when Grammonota were offered as intraguild prey. Both functional responses were type I over the range of prey densities offered. 3. Grammonota is moderately cannibalistic, and the presence of planthopper prey reduced the incidence of cannibalism. 4. Factorial experiments in the laboratory showed that Pardosa but not Grammonota reduced planthopper prey populations when prey density was low. By contrast, at high prey densities, both Pardosa and Grammonota had significant adverse effects on planthopper populations. Moreover, there was an interactive effect such that Grammonota reduced planthopper populations relatively more when Pardosa was absent than when it was present. 5. There was direct evidence for the intraguild predation of Grammonota by Pardosa such that fewer Grammonota survived in the presence of Pardosa than when it was absent. This result occurred whether planthopper prey were abundant or not. 6. Field releases of Grammonota in open plots resulted in significant but small decreases in the density of planthopper prey, both nymphs and adults. 7. Enhancing densities of Pardosa in open plots resulted in Grammonota suppression. The intraguild predation of Grammonota at this enhanced Pardosa density, however, did not preclude Pardosa from significantly reducing planthopper populations.8. Although there was evidence that Grammonota reduced planthopper populations and that the intraguild predation of Grammonota by Pardosa occurred, the strength of these interactions was relatively weak given the low consumption rate of planthoppers by Grammonota (< 3 day-1) and Grammonota by Pardosa (approximately = 2 day-1). Thus, weak asymmetric intraguild predation among spiders on the marsh likely dampens but does not eliminate the ability of Pardosa to exert significant top-down control on planthopper populations.
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