Intraguild predation among plant pests: western flower thrips larvae feed on whitefly crawlers

Omnivores obtain resources from more than one trophic level, and choose their food based on quantity and quality of these resources. For example, omnivores may switch to feeding on plants when prey are scarce. Larvae of the western flower thrips Frankiniella occidentalis Pergande (Thysanoptera: Thripidae) are an example of omnivores that become predatory when the quality of their host plant is low. Western flower thrips larvae usually feed on leaf tissue and on plant pollen, but may also attack eggs of predatory mites, their natural enemies, and eggs of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), one of their competitors. Here, we present evidence that western flower thrips larvae prey on Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), another competitor for plant tissue. We tested this on two host plant species, cucumber (Cucumis sativa L.), considered a host plant of high quality for western flower thrips, and sweet pepper (Capsicum annuum L.), a relatively poor quality host. We found that western flower thrips killed and fed especially on whitefly crawlers and that the incidence of feeding did not depend on host-plant species. The developmental rate and oviposition rate of western flower thrips was higher on a diet of cucumber leaves with whitefly crawlers than on cucumber leaves without whitefly crawlers, suggesting that thrips do not just kill whiteflies to reduce competition, but utilize whitefly crawlers as food.     

Evaluation of Dicyphus hersperus (Heteroptera: Miridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomato

The effectiveness of inoculative releases of the mirid predator Dicyphus hesperus Knight for control of Frankliniella occidentalis (Pergande) on greenhouse tomatoes was evaluated in terms of suppression of the population densities of F. occidentalis and associated fruit damage in the presence of the predator over two seasonal trials. An inoculative release of one D. hesperus per plant (approximately 0.1:10 predator:prey ratio) at a high F. occidentalis population density (140 thrips per plant) suppressed the thrips population density to a significantly lower level, compared with the nonrelease greenhouse, but not below a thrips level that caused economic fruit damage. As the predator:prey ratio increased to approximately 0.5:10 D. hesperus:F. occidentalis, the mean percentage of the thrips-damaged fruit in the D. hesperus release greenhouse decreased to 1.6%. However, the amount of fruit feeding by D. hesperus was highly correlated to the availability of prey (or predator:prey ratio) under greenhouse conditions. D. hesperus-induced fruit damage occurred when the predator:prey ratio was >1:10 D. hesperus:F. occidentalis. Considering the potential risk of fruit damage by D. hesperus and the need for effective control of F. occidentalis, a 0.5-1:10 D. hesperus:F. occidentalis ratio is recommended when the thrips population density is in the range of 60-150 thrips per plant.     

Prey temporarily escape from predation in the presence of a second prey species

1. Indirect interactions between populations of different prey species mediated by a shared predator population are known to affect prey dynamics. 2. Depending on the temporal and spatial scale, these indirect interactions may result in positive (apparent mutualism), neutral or negative effects (apparent competition) of the prey on each other's densities. Although there is ample evidence for the latter, evidence for apparent mutualism is scarce. 3. The effectiveness of using one species of predator for biological control of more than one pest species depends on the occurrence of such positive or negative effects. 4. We used an experimental system consisting of the two prey species Western flower thrips (Franklineilla occidentalis Pergande) and greenhouse whitefly (Trialeurodes vaporariorum Westwood) and a shared predator, the phytoseiid mite Amblyseius swirskii Athias‐Henriot. We released all three species on the same plant and studied their dynamics and distribution along rows of plants. 5. We expected that the more mobile prey species (thrips) would escape temporarily in the presence of the other prey species (whitefly) by dispersing from plants with the predator. The predator was expected to disperse slower in the presence of two prey species because of the higher availability of food. 6. Evidence was found for slower dispersal of predators and short‐term escape of thrips from predation when whiteflies were present, thus confirming the occurrence of short‐term apparent mutualism. 7. The apparent mutualism resulted in a cascade to the first trophic level: a higher proportion of fruits was damaged by thrips in the presence of whiteflies. 8. We conclude that apparent mutualism can be an important phenomenon in population dynamics, and can significantly affect biological control of pest species that share a natural enemy.     

Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes

In theory, selection favours predators that select prey in order to maximise reproductive success. We studied the association between preference and performance of the generalist predator Orius laevigatus with respect to two prey species: spider mites ( Tetranychus urticae ) and western flower thrips ( Frankliniella occidentalis ). Under ample prey supply, the predators had higher maximum reproductive success (measured as intrinsic population growth rate r ) on thrips than on spider mites; hence thrips represent a higher prey quality to the bugs. This was at odds with the observed preference of the predatory bug for plants (patches) with high densities of spider mites to plants with moderate densities of thrips in release-recapture experiments. Thus, prey quality does not suffice to explain the preference of predators for plants with prey. The quality of a patch as an oviposition site (i.e. the number of eggs produced on a patch per bug per day) also did not match preference patterns. Hence, patch preference was not correlated to prey quality or oviposition rate on prey patches. However, patch productivity, i.e. the total number of offspring surviving until adulthood that can be produced by one female on a patch, was correlated with preference. This was further tested by offering the predators a choice between plants with high densities of spider mites and plants with high densities of thrips in an independent set of release-recapture experiments. These two types of prey patches were found equivalent in terms of patch productivity. Indeed, the predators showed no preference for either of the two types of patches, which is in agreement with our predictions. This suggests that the predatory bugs select patches based on patch productivity rather than on prey quality or oviposition rate on a patch.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator

To test the hypothesis that pest species diversity enhances biological pest control with generalist predators, we studied the dynamics of three major pest species on greenhouse cucumber: Western flower thrips, Frankliniella occidentalis (Pergande), greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and two-spotted spider mites, Tetranychus urticae Koch in combination with the predator species Amblyseius swirskii Athias-Henriot. When spider mites infested plants prior to predator release, predatory mites were not capable of controlling spider mite populations in the absence of other pest species. A laboratory experiment showed that predators were hindered by the webbing of spider mites. In a greenhouse experiment, spider mite leaf damage was lower in the presence of thrips and predators than in the presence of whiteflies and predators, but damage was lowest in the presence of thrips, whiteflies and predators. Whitefly control was also improved in the presence of thrips. The lower levels of spider mite leaf damage probably resulted from (1) a strong numerical response of the predator (up to 50 times higher densities) when a second and third pest species were present in addition to spider mites, and (2) from A. swirskii attacking mobile spider mite stages outside or near the edges of the spider mite webbing. Interactions of spider mites with thrips and whiteflies might also result in suppression of spider mites. However, when predators were released prior to spider mite infestations in the absence of other pest species, but with pollen as food for the predators, we found increased suppression of spider mites with increased numbers of predators released, confirming the role of predators in spider mite control. Thus, our study provides evidence that diversity of pest species can enhance biological control through increased predator densities.     

Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits

In northeast Spain, the most common predators found in tomato fields and greenhouses are the mirids Macrolophus caliginosus Wagner and Dicyphus tamaninii Wagner. Natural colonization occurs during the growing season and both species prey on whiteflies. Because D. tamaninii can damage tomato fruits during periods of prey scarcity, a semifield experiment was carried out to evaluate whether the presence of M. caliginosus affects damage produced by D. tamaninii. In a tomato greenhouse, 60 plants were individually caged and distinct predator treatments were introduced: D. tamaninii, D. tamaninii + eggs of Ephestia kuehniella Zeller, D. tamaninii + M. caliginosus, M. caliginosus alone, and a control without any insect. Damage to tomato fruits was recorded (>25% of the fruit) in all the treatments with D. tamaninii, whereas no significant damage was detected with M. caliginosus alone. Finally, no intraguild predation was detected between both mirid species.     

Dicyphus tamaninii as a beneficial insect and pest in tomato crops in Catalonia,Spain

The mirid bugDicyphus tamaninii Wagner, is common in Catalonia in vegetable crops which have not been sprayed with insecticide. To study the feeding habits of this bug in tomato crops, several treated and untreated tomato plots were set up at Cabrils Experimental Station (North of Barcelona) during 1983, 1984 and 1985. The results indicate thatTrialeurodes vaporariorum Westwood populations are greatly affected by the mirid bug when no, or only a few, insecticide sprays are applied. However, the bug heavily damaged tomato fruits in unsprayed plots, where bug numbers were high and whitefly numbers low. It seems that tomato fruit is only preferred when whitefly numbers are extremely low. Similar results were obtained in 1984 in a preliminary experiment using cages to exclude the bug.      

Biological control of thrips and whiteflies by a shared predator: Two pests are better than one

We studied the capacity of one species of predator to control two major pests of greenhouse crops, Western flower thrips (Frankliniella occidentalis (Pergande)) and the greenhouse whitefly (Trialeurodes vaporariorum (Westwood)). In such a one-predator–two-prey system, indirect interactions can occur between the two pest species, such as apparent competition and apparent mutualism. Whereas apparent competition is desired because it brings pest levels down, apparent mutualism is not, because it does the opposite. Because apparent competition and apparent mutualism occurs at different time scales, it is important to investigate the effects of a shared natural enemy on biological control on a time scale relevant for crop growth. We evaluated the control efficacy of the predatory mites Amblyseius swirskii (Athias-Henriot) and Euseius ovalis (Evans) in cucumber crops in greenhouse compartments with only thrips, only whiteflies or both herbivorous insects together. Each of the two predators controlled thrips, but A. swirskii reduced thrips densities the most. There was no effect of the presence of whiteflies on thrips densities. Whitefly control by each of the two predators in absence of thrips was not sufficient, yet better with E. ovalis. However, whitefly densities in presence of thrips were reduced dramatically, especially by A. swirskii. The densities of predators were up to 15 times higher in presence of both pests than in the single-pest treatments. Laboratory experiments with A. swirskii suggest that this is due to a higher juvenile survival and developmental rate on a mixed diet. Hence, better control may be achieved not only because of apparent competition, but also through a positive effect of mixed diets on predator population growth. This latter phenomenon deserves more attention in experimental and theoretical work on biological control and apparent competition.     

Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons

This work presents the results of an investigation that aimed to evaluate the effectiveness of releases of the omnivorous predator Macrolophus caliginosus Wagner (Heteroptera, Miridae) in the control of Bemisia tabaci Gennadius (Homoptera, Aleyrodidae) on greenhouse melon. Two greenhouse trials were performed, one in spring and one in summer. Adults of M. caliginosus were released at two release rates (two and six per plant) in an initial infestation of 10 adult whitefly per plant. The high release rate did control the whitefly populations. Results of the lower release ratio did not work in the second trial, presumably due to excessive pruning of the crop that may have affected predator establishment. No damaged fruits were recorded. Laboratory trials were also done to examine the effects of plant and variable prey availability on predator fertility and survivorship. Results showed that low-prey availability significantly reduced survivorship and fertility of M. caliginosus, and explained why predator establishment was the same for both predator release rates.     

Population abundance and movement of Frankliniella species and Orius insidiosus in field pepper

1 A recent study revealed the capacity of the Orius insidiosus to suppress populations of Frankliniella spp. in field pepper during the spring when thrips are rapidly colonizing and reproducing. In this study, population abundance in pepper during spring, summer, and autumn was determined to understand better predator/prey dynamics under local conditions. Local movement between pepper flowers also was quantified to examine how population attributes of the predator allow suppression of rapidly moving populations of prey. 2 Randomized complete block experiments established in the autumn of 1998 and the spring of 1999 included treatments of biological and synthetic insecticides, which altered the population densities of predator and prey. Numbers of O. insidiosus in relation to prey were sufficient in 1998 to prevent build‐up of thrips populations. In 1999, populations of thrips were unable to recover from near extinction owing to persistence of the predator. The predator rapidly recolonized plots treated with insecticide. 3 Greenhouse plants of the same age as field plants were used to monitor movement by predators and prey. Movement by F. occidentalis was limited, whereas F. tritici and F. bispinosa moved rapidly to the greenhouse plants. The males of each thrips species moved more rapidly than the females. There was evidence that rapid movement assisted F. tritici and F. bispinosa in avoiding predation, but O. insidiosus also moved very rapidly to the greenhouse plants. This attribute explains the predator's ability to suppress thrips rapidly even when populations are rapidly colonizing and reproducing in the flowers.     

Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper

Zoophytophagous predators of the family Miridae (Heteroptera), which feed both on plant and prey, often maintain a close relationship with certain host plants. In this study, we aimed to select a suitable mirid predatory bug for aphid control in sweet pepper. Four species were compared: Macrolophus pygmaeus (Rambur), Dicyphus errans (Wolff), Dicyphus tamaninii Wagner and Deraeocoris pallens (Reuter). They were assessed on their establishment on sweet pepper plants with and without supplemental food (eggs of the flour moth Ephestia kuehniella Zeller and decapsulated cysts of the brine shrimp Artemia franciscana Kellogg) and on their effects on aphids with releases before and after aphid infestations. None of the predator species was able to control an established population of aphids on sweet pepper plants; however, the predators M. pygmaeus and D. tamaninii could successfully reduce aphid populations when released prior to an artificially introduced aphid infestation. The best results were achieved with M. pygmaeus in combination with a weekly application of supplemental food. Hence, our results demonstrate that the order and level of plant colonization by mirid predators and aphids determines how successful biological control is. Further studies are needed to evaluate the performance of mirid predatory bugs in sweet pepper crops in commercial greenhouses with multiple pests and natural enemies, in particular to understand how increased variation in food sources affects their feeding behaviour and preferences.     

稻田穗期主要捕食性天敌对两种盲蝽集团内捕食的初步研究

【目的】集团内捕食是影响农业系统广食性天敌对靶标害虫控制作用的重要因素,全面揭示稻田广食性天敌对稻飞虱重要天敌黑肩绿盲蝽Cyrtorhinus lividipennis Reuter和中华淡翅盲蝽Tytthus chinensis(St?l)(半翅目:盲蝽科)的集团内捕食作用有助于更好地保护利用天敌。【方法】建立以两种盲蝽为猎物对象的种特异性二重定量PCR系统,检测比较不同抗性品种穗期田间主要捕食者对两种盲蝽的集团内捕食作用。【结果】(1)本研究建立的二重定量PCR具有的物种专化性,两种检测靶标灵敏度高且相似,可用于田间捕食者猎物分析;(2)感虫水稻品种上捕食者对盲蝽的捕食强度高于抗性水稻品种;不同种类捕食者对盲蝽的集团内捕食强度有显著差异;捕食者对黑肩绿盲蝽集团内捕食强度显著高于中华淡翅盲蝽。【结论】捕食性盲蝽在稻田生态系统遭遇集团内捕食,其集团内捕食强度与水稻品种抗性、捕食者种类和猎物丰富度有关。     

Pollen subsidies promote whitefly control through the numerical response of predatory mites

Several studies have shown that biological control of pests can be improved by supplying extra food to natural enemies. This increases population levels of the enemies, resulting in decreases in pest densities. In theory, however, supplying food can also have negative effects on biological control. We specifically tested for such negative effects, using a predator–prey system consisting of the whitefly Bemisia tabaci (Gennadius) and a predatory mite Amblyseius swirskii (Athias-Henriot). This predator attacks eggs and young instars of the whitefly, but also feeds on pollen. We added pollen to populations of predators and whiteflies on isolated cucumber plants. Although the set-up of our experiments would favour the occurrence of a negative effect of the addition of pollen on biological control, we found increased control throughout the experiment. This shows that the control of whiteflies by A. swirskii can be improved by supplementing the predators with pollen.     

Effect of pollen supplement on intraguild predatory interactions between two omnivores: The importance of spatial dynamics

Arthropods often engage in complex trophic interactions such as intraguild predation (IGP), true omnivory (i.e., feeding on plants and prey), and apparent competition. Theoretical treatments of the effects of such interactions on herbivore populations have been concerned almost entirely with equilibrium conditions. Yet these interactions are common in non-equilibrium settings such as agroecosystems, where they are likely to have a strong influence on pest populations. We therefore tested short-term effects of IGP and food supplementation on interactions between two predators (the phytoseiid mite Neoseiulus cucumeris and the anthocorid bug Orius laevigatus) and their shared prey, Frankliniella occidentalis, on strawberry plants. All three consumers feed on strawberry pollen, both mites and bugs prey on thrips, and the bug also feeds on the mites (IGP). Strong IGP on mites (IG prey) by the bugs (IG predator) was recorded in structurally-simple arenas. In a more complex setting (whole-plants), however, the intensity of IGP differed among plant structures. Likewise, pollen supplementation reduced both IGP and predation on thrips in a structurally simple setting. In the whole-plant experiment, IGP was more intense on pollen-bearing than pollen-free flowers. The study illustrated how spatial dynamics, generated when consumers track food sources differently in the habitat and possibly when herbivorous and IG prey alter their distribution to escape predation, led to site-specific configuration of interacting populations. The intensity of resulting trophic interactions was weakened by food supplementation and by increased complexity of the habitat.     

Intra-guild predation relaxes natural enemy impacts on herbivore populations

Abstract. 1. To investigate the role of intra-guild predation in mediating the impact of the natural enemy complex on herbivore populations, a manipulative field experiment was conducted using uncaged plots (islets of Spartina cordgrass) on a North American salt marsh. The densities (moderate or low) of two invertebrate predators, the generalist wolf spider Pardosa littoralis and the specialist mirid bug Tytthus vagus , were manipulated in a 2 × 2 factorial design, and the resulting treatment effects on the population growth of their herbivorous prey, Prokelisia planthoppers, were assessed.
2. The abundance of wolf spiders on experimental islets was unaffected by the presence of mirid bugs, however the density of mirid bugs was influenced very negatively by the presence of the wolf spider.
3. The negative effect of the wolf spider on mirid bugs most probably resulted from the intra-guild predation of mirids by spiders because planthopper limitation by the wolf spider alone was significantly greater than when both predators were present.
4. As a result of intra-guild predation, planthopper population growth was positive in the presence of both predators, despite the fact that each predator alone promoted a decrease in planthopper population growth.
5. Notably, the occurrence of intra-guild predation diminished top-down impacts on planthopper populations in a relatively simple food web where strong top-down effects were expected. This result, however, was limited to habitats on the marsh with simply structured vegetation lacking leaf litter.     

Do functional responses of predatory arthropods reach a plateau? A case study of Orius insidiosus with western flower thrips as prey

Parameters determining the functional and numerical response of Orius insidiosus to the density of second instar larvae of the western flower thrips (WFT), Frankliniella occidentalis, were estimated with the aim to be used in models calculating adequate release ratios of predators vs prey. Especially when the prey population must decrease immediately after predator release and the time to suppression must be short, it is of crucial importance to know whether the functional response reaches a plateau or keeps on increasing with prey density within the range of densities that are realistic for the prey. Such plateaus may arise from constraints on the time budget or from constraints on gut-fullness-associated motivation to attack the prey. Estimates of the plateau for O. insidiosus based on prey handling times by far exceed realistic values. In addition, motivation constraints did not apply, because the level of gut fullness above which attack ceases coincides with gut capacity. This implies that the predation rate keeps on increasing linearly with the square root of the density of WFT-larvae and does not reach a plateau within the realistic range of thrips densities (0–20 WFT per cm2). Such plateaus are likely to occur for smaller-sized predators and smaller-sized stages of the same predator and they may also occur when the prey stage offered has better capacities to escape or resist attack. We argue that the presence and level of plateaus in functional responses are of importance for determining initial predator-to-prey ratios.     

Foraging strategies and patch distributions: intraguild interactions between Dicyphus hesperus and Encarsia formosa

Abstract 1. Competing foragers are affected by the distribution of resources, but can also affect resource distribution. Intraguild predators may affect the distribution of both the shared prey and the intraguild prey, which are also their competitors. 2. Variation in foraging strategies and their effects on resource distributions may influence the outcome of intraguild interactions between an intraguild predator and its intraguild prey. This was tested using whitefly Trialeurodes vaporariorum as the shared resource, the parasitoid Encarsia formosa as the intraguild prey, and Dicyphus hesperus, an omnivore, as the intraguild predator on tomato (Lycopersicon esculentum) and mullein (Verbascum thapsus) plants, within enclosures in a greenhouse. Treatments were established with and without the intraguild predator and at high and low intraguild prey densities. 3. The interaction between D. hesperus and E. formosa showed significant asymmetry, with D. hesperus populations being unaffected by E. formosa densities, although E. formosa populations were reduced by the inclusion of D. hesperus. However, the inclusion of D. hesperus diminished density‐dependent effects limiting E. formosa populations at high release densities. 4. Dicyphus hesperus reduced the average patch size and the proportion of patches occupied by whitefly. Increasing the release rate of E. formosa had no effect on any distributional measure. Based upon the foraging ecology of both species, the foraging activities of D. hesperus appear to have modified the patch distribution so that its foraging strategy becomes more successful than that of E. formosa. These properties may provide an important mechanism determining the outcome of species interactions.     

Voracity and prey preference of insidious flower bug (hemiptera: anthocoridae) for immature stages of soybean aphid (hemiptera: aphididae) and soybean thrips (thysanoptera: thripidae)

The generalist predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid, Aphis glycines Matsumura. Soybean thrips, Neohydatothrips variabilis (Beach), serve as an important prey resource for O. insidiosus in soybeans, sustaining the predator's population before the arrival of the soybean aphid. Although generalist predators can forage on a broad range of prey, they may show distinct preferences for particular prey, attacking prey at levels disproportionate to their relative numbers. To assess the preference of O. insidiosus for soybean aphid and soybean thrips, attack rates of nymphal and adult O. insidiosus were measured in the laboratory. For both adults and nymphs, the number of prey attacked increased as more prey were provided. For nymphs, the total number of prey attacked increased as the predator matured. In general, the number of prey attacked by adult predators was relatively constant as the predator aged. Both O. insidiosus nymphs and adults displayed a preference for soybean thrips, by disproportionately attacking soybean thrips over soybean aphid regardless of the relative densities of the two prey. We discuss implications of this preference on O. insidiosus life history characteristics and the potential impact on O. insidiosus-prey dynamics in the field.     

Non-consumptive effects of predatory mites on thrips and its host plant

Recent reviews on trait-mediated interactions in food webs suggest that trait-mediated effects are as important in triggering top–down trophic cascades as are density-mediated effects. Trait-mediated interactions between predator and prey result from non-consumptive predator effects changing behavioural and/or life history traits of prey. However, in biological control the occurrence of trait-mediated interactions between predators, prey and plants has been largely ignored. Here, we show that non-consumptive predator effects on prey cascade down to the plant in an agro-ecological food chain. The study system consisted of the predatory mites P. persimilis and N. californicus , the herbivorous non-target prey western flower thrips F. occidentalis and the host plant bean. Irrespective of predator species and risk posed to prey, the presence of predator eggs led to increased ambulation, increased mortality and decreased oviposition of thrips. Furthermore, the presence of predator eggs reduced leaf damage caused by thrips. To our knowledge this is the first experimental evidence suggesting a positive trophic cascade triggered by non-consumptive predator effects on non-target prey in an augmentative biological control system.