The omnivorous predator Macrolophus pygmaeus,a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants

The poinsettia thrips Echinothrips americanus Morgan is a relatively new pest that has spread rapidly worldwide and causes serious damage in both vegetable and ornamental plants. In this study, we investigated if and how effective this pest can be controlled in gerbera by the omnivorous predator Macrolophus pygmaeus (Rambur). Because herbivores on plants can interact through a shared predator, we also investigated how poinsettia thrips control is affected by the presence of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), a pest that commonly coexists with E. americanus in gerbera. In laboratory studies, we found that the predator M. pygmaeus fed on both pests when offered together. Olfactometer tests showed a clear preference of the predators for plants infested by whiteflies but not by thrips. In a greenhouse experiment, densities of both pests on single gerbera plants were reduced to very low levels by the predator, either with both pests present together or alone. Hence, predator‐mediated effects between whiteflies and thrips played only a minor role. The plant feeding of the shared predator probably reduced the dependence of predator survival and reproduction on the densities of the two pests, thereby weakening potential predator‐mediated effects. Thus, M. pygmaeus is a good candidate for biological control of both pests in gerbera. However, further research is needed to investigate pest control at larger scales, when the pests can occur on different plants.     

Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus

The effects of water stress (produced by water deprivation and prey feeding) on plant feeding were investigated in the omnivorous predator Dicyphus hesperus Knight (Hemiptera: Miridae). The objective was to determine if prey feeding aggravated water deficits and thus increased plant feeding. We measured plant feeding in a factorial experiment where female D. hesperus were prepared for experiments by providing or withholding water and/or prey for 24 h. We then evaluated the amount of plant feeding on Nicotiana tabacum seedlings by the direct observation of insects at three different densities of the prey, Ephestia kuehniella eggs. The amount of plant feeding, as measured by frequency of plant feeding bouts and time spent plant feeding during observation, was significantly greater for water‐deprived individuals than for those that had been provided with water. Individuals that had been provided with prey fed on plants at a significantly higher frequency than prey‐deprived individuals at two of the prey densities used in the experiment. These results support the hypothesis that plant feeding in zoophytophagous Hemiptera facilitates prey feeding by providing water that is essential for predation.     

Use of plant resources by an omnivorous predator and the consequences for effective predation

Plant-provided food may enhance survival and establishment of omnivorous predators on target crops but on the other hand they may adversely affect predation rates and thus their potential for biological control of target pests. However, it is not known how predation is affected by plant food quality and prey density. The omnivorous predator Macrolophus pygmaeus is commonly used in augmentative releases in greenhouse crops. Experiments have shown its ability to utilize plant resources; eggplant and pepper plant leaves are the most and least suitable, respectively. In this study we searched the effects of floral resources (pollen or flower) of eggplant or pepper plant on the predation rate of M. pygmaeus. We used experiments in dishes (leaves) and cages (plants) under a range of densities of its prey, the aphid Myzus persicae. We did not find evidence that the consumption rates and the type of the functional responses of M. pygmaeus were affected by the plant leaf (eggplant vs pepper plant) or the increase in the spatial scale (leaf vs plant). However, the presence of pollen or a flower of eggplant and to a lesser extent of pepper plant reduced the plateau of the functional response to aphid density and increased the handling time per prey. The extent of prey feeding replacement by flower resources was dependent on the interaction between plant species and prey density. It seems that there is a constant rate of prey consumption replacement at intermediate and high prey densities on eggplant but only at intermediate prey densities on pepper plant. These results indicate the interactions between plant and prey resources in diets of omnivores and may be useful for its efficacy in pest control on eggplant and pepper plant.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Plant architecture and prey distribution influence foraging behavior of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae)

The arrangement, number, and size of plant parts may influence predator foraging behavior, either directly, by altering the rate or pattern of predator movement, or, indirectly, by affecting the distribution and abundance of prey. We report on the effects of both plant architecture and prey distribution on foraging by the predatory mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae), on cucumber (Cucumis sativus L.). Plants differed in leaf number (2- or 6-leafed), and there were associated differences in leaf size, plant height, and relative proportions of plant parts; but all had the same total surface area. The prey, the twospotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), were distributed either on the basal leaf or on all leaves. The effect of plant architecture on predator foraging behavior varied depending on prey distribution. The dimensions of individual plant parts affected time allocated to moving and feeding, but they did not appear to influence the frequency with which predators moved among different plant parts. Overall, P. persimilis moved less, and fed upon prey longer, on 6-leafed plants with prey on all leaves than on plants representing other treatment combinations. Our findings suggest that both plant architecture and pattern of prey distribution should be considered, along with other factors such as herbivore-induced plant volatiles, in augmentative biological control programs.     

Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae)

Macrolophus pygmaeus (Heteroptera: Miridae) is an omnivourus predator used to control several pests of horticultural greenhouses. With the aim to explore the relationship between M. pygmaeus and different host plants compared with tomato, plant preferences and bio-cycle traits were studied using: Capsicum annuum, Calendula officinalis, Salvia officinalis, Parietaria officinalis and Solanum nigrum. Species were selected among natural host crop and wild plants. Plant preference was measured by multi-choice host plant selection and olfactometric bioassays. Bio-cycle traits were assessed on reproduction and on nymphal development with and without animal diet support. Among tested plants, P. officinalis was the least attractive under laboratory conditions. Furthermore the availability of prey was crucial for the successful establishment of M. pygmaeus on tested plants, suggesting the inability of nymphs to complete development to adulthood on a strictly phytophagous diet. Nevertheless, M. pygmaeus seemed to prefer plants where phytophagy provides a fitness benefit.     

Preference and consumption of Macrolophus pygmaeus preying on mixed instar assemblages of Myzus persicae

This study examines the effects of changes in the prey frequency and abundance on prey selection among the four instars of Myzus persicae by the predator Macrolophus pygmaeus under laboratory conditions. The central hypothesis was that M. pygmaeus will become more selective as prey density increases. It was also observed that M. pygmaeus can occasionally abandon a prey item that had already been killed (non-consumptive prey mortality). It was assumed that the frequency of this behavior would increase with the prey size and prey density. For these purposes prey selection was evaluated by simultaneously presenting all instars of M. persicae to the predator in equal proportions and at increasing densities. M. pygmaeus showed a higher predation rate and a higher preference for smaller prey instars at all prey densities. However, if the predation rate by the predator is expressed in terms of biomass consumed, then biomass gain was higher when feeding on the larger instars of M. persicae. The prey selectivity was indicated by the total prey mortality (consumptive plus non-consumptive prey mortality) as well as by the non-consumptive prey mortality, was associated with relatively high prey densities, depending on the prey instar. Therefore, we argued that the predatory impact of M. pygmaeus on the various instars of the aphid depends not only on prey traits but also on their relative abundance in a patch. Observed decreases in biomass gain from larger prey were likely the result of high prey availability at densities before saturation, which might have caused confusion in the predator’s prey selection.     

Fitness and predation potential of Macrolophus pygmaeus reared under artificial conditions

Abstract The biological parameters of Macrolophus pygmaeus Rambur after prolonged rearing in the absence of plant materials were compared with those of conventionally plant‐reared predators. When eggs of Ephestia kuehniella Zeller were provided as food, developmental and reproductive fitness of M. pygmaeus reared for over 30 consecutive generations using artificial living and oviposition substrates was similar to that of predators kept on tobacco leaves. Plantless‐reared fifth instars of the predator also had similar predation rates on second instars of the tobacco aphid, Myzus persicae nicotianae Blackman, as their peers maintained on plant materials. In a further experiment, predation on aphid prey by fifth instar M. pygmaeus fed one of two egg yolk‐based artificial diets was compared with that of nymphs fed E. kuehniella eggs. Despite their lower body weights, predators produced on either artificial diet killed similar numbers of prey as their counterparts reared on lepidopteran eggs. Our study indicates that artificial rearing systems may be useful to further rationalize the production of this economically important biological control agent.     

Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey‐related cues

Most terrestrial plants are associated with arbuscular mycorrhizal fungi but research on the effects of arbuscular mycorrhizal symbiosis on aboveground plant‐associated organisms is scarcely expanded to tri‐trophic systems. The arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. enhances fitness of the two‐spotted spider mite Tetranychus urticae Koch and its natural enemy, the predatory mite Phytoseiulus persimilis Athias‐Henriot, via changes in host plant and prey quality, respectively. In the present study, it is hypothesized that gravid P. persimilis are able to recognize arbuscular mycorrhiza‐enhanced prey quality and behave accordingly. In two experiments, on leaf arenas and in cages, P. persimilis is given a choice between prey patches deriving from mycorrhizal and non‐mycorrhizal bean plants (Phaseolus vulgaris L.) as feeding and oviposition sites. The use of cages allows the manipulation of distinct patch components acting as possible cues to guide predator foraging and oviposition behaviours, such as eggs produced and traces (webbing and faeces) left by the spider mite females. Both experiments show that P. persimilis preferentially resides close to prey fed on mycorrhizal plants. The cage experiment reveals that P. persimilis uses direct prey‐related cues, mainly derived from eggs, to discern prey quality and preferentially oviposits close to prey from mycorrhizal plants. This is the first study to document that predators recognize arbuscular mycorrhiza‐induced changes in herbivorous prey quality via direct prey‐related cues.     

Foraging tactics and prey-selection patterns of omnivorous and carnivorous calanoid copepods

The foraging tactics and prey-selection patterns of omnivorous and carnivorous calanoid copepods are reviewed. Calanoid foraging tactics are envisioned as falling along several closely coupled continua reflecting swimming behavior, feeding behavior, and dietary habit. The consequences of these foraging tactics on prey-selection patterns are explored in the context of a graphical model. It is hypothesized that the prey-selection patterns of calanoid copepods are determined, to a large extent, by calanoid foraging tactics and the size relationships of predator and prey.     

Response of mirid predators to synthetic herbivore‐induced plant volatiles

Zoophytophagous plant bugs feed on plant tissue as a source of water and nutrients, besides feeding on prey. By phytophagy, mirid predators activate plant defense responses through different pathways, resulting, among others, in the release of herbivore‐induced plant volatiles (HIPVs). These compounds could repel herbivores and attract parasitoids and predators, and synthetic versions could potentially be used in biological control. Nevertheless, little is known about the influence of synthetic volatiles on mirid attraction. Using Y‐tube olfactometer trials, we evaluated the responses of Nesidiocoris tenuis (Reuter), Macrolophus pygmaeus (Rambur), and Dicyphus bolivari Lindberg (Hemiptera: Miridae), important natural enemies used to control various greenhouse pests, to 10 synthetic versions of HIPVs released from tomato (Solanum lycopersicum L., Solanaceae) plants induced by N. tenuis and M. pygmaeus. Nesidiocoris tenuis responded to five of the 10 HIPVs, whereas M. pygmaeus and D. bolivari responded to four of the 10 HIPVs. Two green leaf volatiles, (Z)‐3‐hexenyl propanoate and (Z)‐3‐hexenyl acetate, and the ester methyl salicylate (MeSA) were attractive to all three mirid predator species. Our results demonstrate that the volatiles released by tomato plants activated by N. tenuis and M. pygmaeus phytophagy are attractive to their conspecifics and also to D. bolivari. Further studies should evaluate the potential of these compounds to attract predatory mirids in the field.     

Predatory hoverflies select their oviposition site according to aphid host plant and aphid species

The hoverfly Episyrphus balteatus De Geer (Diptera: Syrphidae) is an abundant and efficient aphid‐specific predator. Several aphidophagous parasitoids and predators are known to respond positively to aphid‐infested plants. Semiochemicals from the latter association usually mediate predator/parasitoid foraging behavior toward sites appropriate for offspring fitness. In this study, we investigated the effect of aphid host plant and aphid species on foraging and oviposition behavior of E. balteatus. Behavioral observations were conducted using the Noldus Observer v. 5.0, which allows observed insect behavior to be subdivided into different stages. Additionally, the influence of aphid species and aphid host plant on offspring fitness was tested in a second set of experiments. Acyrthosiphon pisum Harris and Megoura viciae Buckton were equally attractive for E. balteatus whereas Aphis fabae Scopoli (all Homoptera: Aphididae) were less attractive. These results were correlated with (i) the number of eggs laid, which was significantly higher for the two first aphid species, and (ii) the fitness of hoverfly larvae, pupae, and adults. Two solanaceous plant species, Solanum nigrum L. and Solanum tuberosum L. (Solanaceae), which were infested with Myzus persicae Sulzer (Homoptera: Aphididae), were also compared using the same approach. Discrimination between these two M. persicae host plants was observed, with S. tuberosum being preferred as an oviposition site by the predatory hoverfly. Larval and adult fitness was correlated with the behavioral observations. Our results demonstrated the importance of the prey–host plant association on the choice of the oviposition site by an aphid predator, which is here shown to be related to offspring fitness.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Effect of plants on the searching efficiency of a generalist predator: the importance of predator-prey spatial association

In most studies of tritrophic interactions, the effect of plants on predators is confounded with changes in prey and predator behaviors after an encounter event. Here, we estimate how the effect of plants on prey distribution (in the absence of the predator) and on predator foraging behavior (in the absence of prey) may influence predation rate of Orius insidiosus (Say) (Heteroptera: Anthocoridae) in 11 plant by prey species combinations. The within-leaf distributions of O. insidiosus and its prey overlapped most on bean plants. The predator's foraging behavior (e.g., walking speed, turning rate) also differed among plant species. Simulations, using the prey distribution data and predator's foraging patterns on leaf surfaces of each plant species, show that, overall, the searching efficiency of O. insidiosus was higher on leaves of bean and corn than of tomato. However, the predator's searching efficiency was not consistent within plant species. Thus, the combined effect of plants directly on the predator and indirectly through the prey influenced the predator's searching efficiency.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Plant and Prey Consumption Cause a Similar Reductions in Cannibalism by an Omnivorous Bug

Cannibalism is usually more intense when other food sources are scarce, be it prey or plant-based foods. We hypothesized that feeding on plants would reduce cannibalism to a lesser extent than feeding on prey, because plants are considered nutritionally inferior compared to prey. We used the omnivorous bug Orius laevigatus Say (Heteroptera: Anthocoridae) to test this prediction. Starved female bugs were individually held with five second-instar conspecific nymphs and offered (i) Helicoverpa armigera eggs (prey); (ii) pollen (plant); (iii) H. armigera eggs and pollen (prey+plant); or (iv) no eggs or pollen. Fewer cannibalistic events and shorter feedings on conspecifics were recorded in the presence of pollen, prey or both than in their absence. Data therefore do not support our hypothesis that cannibalism is differentially affected by foods of different nutritional values. It seems that omnivorous feeding habits enable predators to sustain themselves on plant sources in the absence of prey, without the need to resort to cannibalism.     

Strategies of zooplanktivory shape the dynamics and diversity of littoral plankton communities: a mesocosm approach

Planktivorous fish can exert strong top‐down control on zooplankton communities. By incorporating different feeding strategies, from selective particulate feeding to cruising filter feeding, fish species target distinct prey. In this study, we investigated the effects of two species with different feeding strategies, the three‐spined stickleback (Gasterosteus aculeatus (L.)) and roach (Rutilus rutilus (L.)), on a low‐diversity brackish water zooplankton community using a 16‐day mesocosm experiment. The experiment was conducted on a small‐bodied spring zooplankton community in high‐nutrient conditions, as well as a large‐bodied summer community in low‐nutrient conditions. Effects were highly dependent on the initial zooplankton community structure and hence seasonal variation. In a small‐bodied community with high predation pressure and no dispersal or migration, the selective particulate‐feeding stickleback depleted the zooplankton community and decreased its diversity more radically than the cruising filter‐feeding roach. Cladocerans rather than copepods were efficiently removed by predation, and their removal caused altered patterns in rotifer abundance. In a large‐bodied summer community with initial high taxonomic and functional diversity, predation pressure was lower and resource availability was high for omnivorous crustaceans preying on other zooplankton. In this community, predation maintained diversity, regardless of predator species. During both experimental periods, predation influenced the competitive relationship between the dominant calanoid copepods, and altered species composition and size structure of the zooplankton community. Changes also occurred to an extent at the level of nontarget prey, such as microzooplankton and rotifers, emphasizing the importance of subtle predation effects. We discuss our results in the context of the adaptive foraging mechanism and relate them to the natural littoral community.     

Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology

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The interaction between spatial heterogeneity and genetic feedback in laboratory predator-prey systems

Summary A hybrid experimental design combining laboratory populations and computer simulation was used to study the relative influence of spatial heterogeneity, genetic feedback and predator foraging behavior on the stability of predator-prey systems. Houseflies, Musca domestica, maintained in multicellular or single-cell population cages were used as predator feeding on chemical solutions contained in small glass vials. Feeding, mortality and dispersal of the predators occurred within the cages, but reproduction of the predators and prey as well as dispersal of the prey was controlled by a computer program. Genetic change in the prey was determined partially by the computer model which associated chemical solutions with particular genotypes, and partially by the predators, whose foraging behavior influenced the fitness of each genotype. Three treatments were compared: a genetically polymorphic prey population in a spatially homogeneous environment, a monomorphic prey population in a heterogeneous environment, and a polymorphic prey population in a heterogeneous environment. With the parameters used, the latter treatment, involving an interaction between spatial heterogeneity and genetic feedback, was the most stable. Without genetic feedback in the prey, spatial heterogeneity was insufficient to overcome the destabilizing influence of the predator's foraging behavior. Without spatial heterogeneity, genetic feedback was insufficient to overcome the destabilizing effect of preferential feeding by the predators on palatable prey. The prey population evolved sufficient resistance to cause extinction of the predator population. The results support the hypothesis that population regulation by genetic feedback in predator-prey systems is less likely when predators feed preferentially on susceptible prey and that spatial heterogeneity, by decreasing the relative accessibility of susceptible prey and hence altering the predator's foraging strategy, may increase the likelihood of regulation through genetic feedback.