Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza

Biological control of different species of pest with various species of generalist predators can potentially disrupt the control of pests through predator-predator interactions. We evaluate the impact of three species of generalist predatory mites on the biological control of green peach aphids, Myzus persicae (Sulzer) with the aphidophagous gall midge Aphidoletes aphidimyza (Rondani). The predatory mites tested were Neoseiulus cucumeris (Oudemans), Iphiseius degenerans (Berlese) and Amblyseius swirskii Athias–Henriot, which are all commonly used for pest control in greenhouse sweet pepper. All three species of predatory mites were found to feed on eggs of A. aphidimyza, even in the presence of abundant sweet pepper pollen, an alternative food source for the predatory mites. In a greenhouse experiment on sweet pepper, all three predators significantly reduced population densities of A. aphidimyza, but aphid densities only increased significantly in the presence of A. swirskii when compared to the treatment with A. aphidimyza only. This stronger effect of A. swirskii can be explained by the higher population densities that this predator reached on sweet pepper plants compared to the other two predator species. An additional experiment showed that female predatory midges do not avoid oviposition sites with the predator A. swirskii. On the contrary, they even deposited more eggs on plants with predatory mites than on plants without. Hence, this study shows that disruption of aphid control by predatory mites is a realistic scenario in sweet pepper, and needs to be considered when optimizing biological control strategies.     

Ecological considerations for biological control of aphids in protected culture

Several braconid and aphelinid parasitoids, midges, lacewings, and ladybird beetles are used to control aphids in greenhouses. Here, I review three topics as ecological bases for the biological control of aphids in a protected culture: the preliminary evaluation of biological control agents, natural enemy release strategies, and the effects of intraguild predation (IGP) on biological control. A comparison of several parasitoid species was conducted to select agents for the biological control of aphids; the intrinsic rate of natural increase was a useful criterion in the preliminary evaluation. To compare predators as biological control agents, the aphid-killing rate must be considered as a critical criterion, rather than reproductive criteria. The banker plant system (open rearing system) is used as a release method for Aphidius colemani and other natural enemies of aphids. Continuous release of parasitoid adults, which is the important characteristic of this method, has a stabilizing effect on population fluctuation in the aphid–parasitoid system. Two species of natural enemies can be used to control aphids in greenhouses. When one parasitoid and one predator are used simultaneously in a greenhouse, IGP of the parasitoid by the predator can occur, but the effect of IGP is less important in greenhouses than in the field.     

Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation

The combined release of species of generalist predators can enhance multiple pest control when the predators feed on different prey, but, in theory, predators may be excluded through predation on each other. This study evaluated the co-occurrence of the generalist predators Macrolophus pygmaeus Rambur and Orius laevigatus (Fieber) and their control of two pests in a sweet pepper crop. Both predators consume pollen and nectar in sweet pepper flowers, prey on thrips and aphids, and O. laevigatus is an intraguild predator of M. pygmaeus. Observations in a commercial sweet pepper crop in a greenhouse with low densities of pests showed that the two predator species coexisted for 8 months. Moreover, their distributions in flowers suggested that they were neither attracted to each other, nor avoided or excluded each other. A greenhouse experiment showed that the predators together clearly controlled thrips and aphids better than each of them separately. Thrips control was significantly better in the presence of O. laevigatus and aphid control was significantly better in the presence of M. pygmaeus. Hence, combined inoculative releases of M. pygmaeus and O. laevigatus seem to be a good solution for controlling both thrips and aphids in greenhouse-grown sweet pepper. The predators are able to persist in one crop for a sufficiently long period and they complement each other in the control of both pests. This study also provides further evidence that intraguild predation does not necessarily have negative effects on biological control.     

Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies

The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the U.S. since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse guild of insect predators feeds on soybean aphid in Michigan including the exotic coccinellid Harmonia axyridis, the native gall midge Aphidoletes aphidimyza and the native lacewing Chrysoperla carnea. In addition to feeding on A. glycines some members of this guild may also engage in intraguild predation. These interactions may produce positive, negative, or neutral impacts on A. glycines biological control. We explored the impact of intraguild predation on soybean aphid population dynamics by comparing aphid populations in microcosms with either A. aphidimyza larvae or C. carnea larvae alone, with both a H. axyridis adult and either A. aphidimyza or C. carnea larvae, and without predators. When H. axyridis was present with larval A. aphidimyza or C. carnea, the lady beetle acted as an intraguild predator. However, intraguild feeding did not result in a release of aphid populations compared with microcosms containing only the intraguild and aphid prey. A similar result was found in field cages. Cages allowing large predators had reduced numbers of A. aphidimyza and C. carnea larvae but also significantly fewer aphids compared with predator exclusion cages. Thus, in both lab and field studies the direct impact of H. axyridis on A. glycines overcame its negative impact as an intraguild predator. Together, these studies indicate that while the exotic H. axyridis does act as an intraguild predator and may contribute to local declines in A. aphidimyza and C. carnea, it is also currently important in overall biological control of A. glycines.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

Intraguild predation by the generalist predator Orius majusculus on the parasitoid Encarsia formosa

Intraguild predation of Orius majusculus (Reuter) (Heteroptera: Anthocoridae) on Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae), both natural enemies of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), was studied under laboratory conditions. The experiments quantified prey consumption by 5th instar nymphs and adults of O. majusculus offered unparasitised 3rd, early 4th or 4th instar B. tabaci nymphs or parasitised nymphs containing 2nd or 3rd larval instar or pupal parasitoids. In addition, prey preference of the two stages of O. majusculus for parasitised or unparasitised whitefly nymphs was studied using nine different prey combinations. Both predator stages readily preyed upon on both unparasitised and parasitised B. tabaci. In no-choice experiments, predation on 3rd instar E. formosa by adult predators was the highest, while predator nymphs preyed most on unparasitised 3rd instar B. tabaci and 2nd instar parasitoids. Predation of predator stages was lowest on 4th instar B. tabaci and E. formosa pupae. In all prey combinations, both stages of O. majusculus showed a significant preference for parasitised over unparasitised whitefly nymphs except for the combination of 5th instars of O. majusculus with early 4th instar whiteflies and E. formosa pupae. The results indicate that intraguild interactions between O. majusculus and E. formosa may have negative effects on biological control of B. tabaci.     

Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis

Coincidental intraguild predation is expected to be less disruptive to biological control than omnivorous intraguild predation, and strong intraguild predation is not expected to occur in natural systems. Coincidental intraguild predation in a foodweb involving introduced pest and natural enemy species was examined to determine whether intraguild predation would be disruptive of biological control services in soybean agroecosystems. Introduced natural enemies are important regulators of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations in North America. Seven-spotted lady beetles, Coccinella septempunctata L., and multicolored Asian lady beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), are key predators of soybean aphid in North America while the chalcidoid wasp, Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae), is the most common parasitoid of soybean aphid in Ontario, Canada. Predation of parasitized soybean aphids at two stages (newly parasitized aphids and mummified aphids) by adults and third instar larvae of both C. septempunctata and H. axyridis was examined in laboratory experiments. In choice experiments, all stages of lady beetles preferred non-parasitized aphids over mummified aphids. In cage experiments, third instar larvae and male and female adults of both lady beetles did not discriminate between newly parasitized and non-parasitized aphids. The influence of coincidental intraguild predation on the efficacy of parasitoids as biological control agents, and implications for soybean aphid management decisions based on natural enemies, are discussed.     

Different squash cultivars mediate performance of Aphis gossypii and its predator (Aphidoletes aphidimyza): Towards developing an IPM strategy

Different cultivars of plant species can affect the performance of aphids and their natural enemies. In this study, development and life table parameters of the cotton aphid, Aphis gossypii (Hem.: Aphididae) and its predatory midge, Aphidoletes aphidimyza (Dip.: Cecidomyiidae) were determined on four different squash cultivars (Rajaei, Elion, Clarita, and Chance) under laboratory conditions at 23 ± 2 °C, 70 ± 5% RH and 16:8 h L:D photoperiod. Adult longevity and total fecundity of A. gossypii differed with cultivar, with the highest value observed on Rajaei as the most susceptible host plant (21.93 ± 0.191 days and 74.37 ± 0.088 nymphs/female, respectively). Moreover, the intrinsic rate of increase (r) of the aphid on Rajaei and Elion (0.354 ± 0.008 day⁻¹ and 0.340 ± 0.009 day⁻¹, respectively) were significantly higher than two other cultivars. The predator reared on A. gossypii, feeding on Chance cultivar, had the lowest fecundity (51 ± 2.78 eggs/female) and the lowest r value (0.120 ± 0.011 day⁻¹) than those reared on other cultivars. These results attained from population projection estimation based on the age-stage, two-sex life table theory were in consistence with other findings which indicated the influence of different host plant cultivars on the performance of A. gossypii and its predator, A. aphidimyza. Combined use of resistant host plant cultivars together with biological control agents can be proposed as an efficient integrated pest management strategy.     

Prey-mediated effects of mCry51Aa2-producing cotton on the predatory nontarget bug Orius majusculus (Reuter)

Genetically engineered (GE) cotton, MON 88702, is protected against certain sucking pests, such as plant bugs and thrips, by producing mCry51Aa2, a modified protein from Bacillus thuringiensis (Bt). Predatory pirate bugs (Orius spp.), natural enemies contributing to biological pest control, are also sensitive to the insecticidal protein when exposed continuously to high concentrations. We evaluated effects of MON 88702 on Orius majusculus when fed prey types with different mCry51Aa2 concentrations. When neonates were provided exclusively Tetranychus urticae spider mites reared on MON 88702 (high mCry51Aa2 content), adverse effects on predator survival and development were confirmed, compared with specimens fed prey from near-isogenic non-Bt cotton. When fed a mixture of T. urticae and Ephestia kuehniella eggs (mCry51Aa2-free), predator life table parameters were similar to the treatment where eggs were fed exclusively. When mCry51Aa2-containing spider mites were provided for a limited time at the beginning or the end of juvenile development, effects were less pronounced. While pirate bug nymphs showed similar consumption rates for prey from Bt and non-Bt cotton, choice experiments revealed a preference for E. kuehniella eggs over spider mites. Lepidopteran larvae (Spodoptera littoralis, high mCry51Aa2 content) or cotton aphids (Aphis gossypii, mCry51Aa2-free) reared on MON 88702 as alternative prey did not result in adverse effects on O. majusculus. Our study suggests limited risk of mCry51Aa2-producing cotton for O. majusculus, because its sensitivity for the Bt protein is relatively low and its natural food consists of diverse prey species with varying concentrations of Bt protein.     

5种生物杀虫剂对4种天敌昆虫的安全性评价

【目的】生物杀虫剂及天敌昆虫的应用是绿色防控的发展方向,但有关生物杀虫剂对天敌昆虫的安全性尚不明确。研究生物杀虫剂对天敌昆虫的影响可以为更好地协调使用生物杀虫剂和天敌昆虫提供理论依据。【方法】在实验室条件下采用药膜法和滤纸膜片法测定了5种生物杀虫剂(苦参碱、桉油精、鱼藤酮、除虫菊素、橄榄鲨)在田间推荐使用浓度下,对4种天敌昆虫(丽蚜小蜂、东亚小花蝽、食蚜瘿蚊、巴氏新小绥螨)的致死率。【结果】除虫菊素对丽蚜小蜂、东亚小花蝽、巴氏新小绥螨的影响较大,致死率均达到100%;鱼藤酮对丽蚜小蜂、食蚜瘿蚊、巴氏新小绥螨的影响均较大,致死率在98.65%以上;橄榄鲨对丽蚜小蜂、东亚小花蝽、食蚜瘿蚊的影响较小,致死率均小于30%;苦参碱对丽蚜小蜂的影响最大,致死率达100%,对食蚜瘿蚊和巴氏新小绥螨的影响较小,致死率分别为15.56%和15.91%;桉油精对巴氏新小绥螨的影响最大,致死率达100%,对东亚小花蝽和食蚜瘿蚊的影响较小,致死率分别为15.91%和6.67%。【结论】这5种生物杀虫剂中,橄榄鲨对丽蚜小蜂、东亚小花蝽、食蚜瘿蚊安全,桉油精对东亚小花蝽、食蚜瘿蚊安全,苦参碱对食蚜瘿蚊、巴氏新小绥螨安全,鱼藤酮对东亚小花蝽安全,除虫菊素对食蚜瘿蚊安全。     

Comparison of the predation capacities of two soil-dwelling predatory mites,Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae), on three thrips species

Soil-dwelling predatory mites are natural enemies of various soil pest insects and mites. Both Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) are commercialized natural enemies of thrips, but there is little information on the predation rate of these predatory mites on different thrips species. We compared their predation capacities on three thrips species, Frankliniella occidentalis, F. intonsa, and Thrips palmi, which are major pests of various horticultural plants. The predatory rate of G. aculeifer was higher than that of S. scimitus. Both predator species fed on more T. palmi thrips than F. occidentalis or F. intonsa thrips, which may be attributable to the smaller body size of T. palmi than the other thrips. Predation rates of female adults were 2.6–2.8 times higher than those of deutonymphs in both species. Predation rates were not separated according to the various developmental stages (i.e., second instar larva, pupa, or adult) of thrips; however, deutonymphs fed on fewer adults than larvae or pupae of F. occidentalis. Our results suggest that both G. aculeifer and S. scimitus are active predators that can prey during any of their developmental stages and on any species of thrips tested.     

Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper

The role of natural enemy diversity in biological pest control has been debated in many studies, and understanding how interactions amongst predators and parasitoids affect herbivore populations is crucial for pest management. In this study, we assessed the individual and combined use of two species of natural enemies, the parasitoid Aphidius ervi Haliday, and the predatory brown lacewing Micromus variegatus (Fabricius), on their shared prey, the foxglove aphid, Aulacorthum solani (Kaltenbach), on sweet pepper. We hypothesized that the presence of intraguild predation (IGP) and predator facilitation (through induced aphid dropping behaviour) might have both negative and positive effects on aphid control, respectively. Our greenhouse trial showed that overall, the greatest suppression of aphids occurred in the treatment with both the parasitoid and the lacewing. While the combination of lacewings and parasitoids significantly increased aphid control compared to the use of parasitoids alone, the effect was not significantly different to the treatment with only predators, although there was a clear trend of enhanced suppression. Thus, the combined effects of both species of natural enemies were between additive and non‐additive, suggesting that the combination is neither positive nor negative for aphid control. High levels of IGP, as proven in the laboratory, were probably compensated for by the strong aphid suppression provided by the lacewings, whether or not supplemented with some level of predator facilitation. For aphid management over a longer time scale, it might still be useful to combine lacewings and parasitoids to ensure stable and resilient aphid control.     

Functional and Numerical Responses of Three Species of Predatory Phytoseiid Mites (Acari: Phytoseiidae) to Thrips flavidulus (Thysanoptera: Thripidae)

Phytoseiid mites are considered the most effective natural enemies of pest mites. They also have been shown to attack pest thrips. It is unknown, however, whether phytoseiid mites can reduce high densities of Thrips flavidulus (Bagnall). We addressed this question by the study of functional and numerical responses. The aim of this research was to evaluate the potential predation success of the adults of three predatory mites, Neoseiulus cucumeris (Oudemans), Neoseiulus barkeri (Hughes), and Euseius nicholsi (Ehara & Lee), against the first-instar of T. flavidulus in a climatic chamber at five different temperatures. The results showed that the functional responses of those predators reflected the Holling type II functional response and were density dependent and positively related to temperature. For the three predatory mites, predation and successful attack rates increased with increasing temperature up to 26°C, reducing afterward. Handling time had the opposite trend. Reproductive ability also increased with an increase in temperature and prey consumption.     

Change in carbon stable isotope ratios of the predatory bug Orius majusculus after dietary shifts

Orius majusculus Reuter (Hemiptera: Anthocoridae) is an important component of the pest predatory complex in arable crops in Mediterranean areas. It moves between crops searching for prey, and improving knowledge on its dispersal abilities will help to develop conservation biological control strategies. Stable isotope ratios may be used as a tool for tracking insect movements, as the isotopic composition of insect tissues changes to reflect that of their diet when they undergo dietary shifts on moving between isotopically distinct crops. We carried out laboratory diet switch experiments with a stable isotope approach to infer information on dispersal of O. majusculus individuals among C3 and C4 crops to better understand isotopic field data collections. Switching the aphid food source caused a quick change in δ¹³C signatures, regardless of the original and final food source. Changes in the δ¹³C ratio of O. majusculus after diet switching fitted with an exponential model that showed similar turnover rates, and thus half‐lives, between shifting diets up to 20 days. Subsequently, whereas individuals feeding on C4 aphids did not survive, turnover rate decreased in individuals that switched from C4 to C3 aphids. However, δ¹³C traces from the original source remained in the predator until 25 days after switching, and this is enough time to help determine the movement of O. majusculus between crops in the field and to plan the timing of predator sampling and crop practices that may enhance predator ecological services. Orius majusculus that switched to a maize aphid diet showed different turnover rates between sexes, although this did not influence the pattern of switchover.     

Intraguild predation of Orius tristicolor by Geocoris spp. and the paradox of irruptive spider mite dynamics in California cotton

It is paradoxical when a community of several natural enemies fails to control a pest population when it can be shown experimentally that single members of the natural enemy community are effective control agents when tested individually. This is the case for spider mites, Tetranychus spp., in California cotton. Spider mites exhibit irruptive population dynamics despite that fact that experiments have shown that there are at least four predators (Galendromus occidentalis, Frankliniella occidentalis, Orius tristicolor, and Geocoris spp.) that, when tested singly, can suppress mite populations. One possible explanation for the paradox is intraguild predation, wherein one predator consumes another. Here, I evaluate the hypothesis that intraguild predation is a strong interaction among spider mite predators. I report manipulative field experiments, focal observations of freely foraging predators in the field, and population survey data that suggest that the minute pirate bug O. tristicolor, is subject to strong predation by other members of the predator community, and in particular by Geocoris spp. These results, combined with the results of prior work, suggest that pervasive intraguild predation among spider mite predators may explain the pest status of Tetranychus spp. in cotton.     

Selection for non-diapause inAmblyseius cucumeris andAmblyseius barkeri and exploration of the effectiveness of selected strains for thrips control

In Europe and North America the western flower thrips,Frankliniella occidentalis, is an important pest in various greenhouse crops, such as sweet pepper and cucumber. Two species of predatory mite are commercially applied for biological control of this pest:Amblyseius cucumeris andA. barkeri. Thrips control is generally successful from March onwards. During winter, however, thrips control by these predatory mites is less effective. An important reason for this is that the commercially applied strains of both mite species enter reproductive diapause under short-day photoperiods, whereas the western flower thrips does not enter diapause. In this paper we report on selection experiments for non-diapause in strains of both mite species, aimed at obtaining predators that do not enter diapause under light- and temperature conditions prevailing in winter. Additional experiments were done to estimate the potential of the selected lines as control agents ofF. occidentalis. Selection for non-diapause proved highly successful in both predatory mite species. In a New Zealand strain ofA. cucumeris diapause incidence decreased from 41% to 0% in about ten generations; in a Dutch strain ofA. barkeri diapause incidence decreased from 67% to 0% in about six generations. Furthermore, selection for non-diapause had no influence on predator performance, measured as predation rate and oviposition rate on a diet of first instar thirps larvae. Rates of predation and oviposition were the same for selected and unselected lines in both species; rates of predation and oviposition were higher forA. cucumeris than forA. barkeri. After 18 months under non-diapause conditions, no less than 92% of a sample of the selected non-diapause line ofA. cucumeris did not enter diapause when tested under diapause-inducing conditions. This indicates that ‘non-diapause’ is a stable trait in these predatory mites. Finally, a small-scale greenhouse experiment in a sweet pepper crop showed that the selected non-diapause line ofA. cucumeris established successfully under diapause-inducing short-day conditions.     

Review Behaviour and indirect interactions in food webs of plant-inhabiting arthropods

With the increased use of biological control agents, artificial food webs are created in agricultural crops and the interactions between plants, herbivores and natural enemies change from simple tritrophic interactions to more complex food web interactions. Therefore, herbivore densities will not only be determined by direct predator–prey interactions and direct and indirect defence of plants against herbivores, but also by other direct and indirect interactions such as apparent competition, intraguild predation, resource competition, etc. Although these interactions have received considerable attention in theory and experiments, little is known about their impact on biological control. In this paper, we first present a review of indirect food web interactions in biological control systems. We propose to distinguish between numerical indirect interactions, which are interactions where one species affects densities of another species through an effect on the numbers of an intermediate species and functional indirect interactions, defined as changes in the way that two species interact through the presence of a third species. It is argued that functional indirect interactions are important in food webs and deserve more attention. Subsequently, we discuss experimental results on interactions in an artificial food web consisting of pests and natural enemies on greenhouse cucumber. The two pest species are the two-spotted spider mite Tetranychus urticae and the western flower thrips, Frankliniella occidentalis. Their natural enemies are the predatory mite Phytoseiulus persimilis, which is commonly used for spider mite control and the predatory mites Neoseiulus cucumeris and Iphiseius degenerans and the predatory bug Orius laevigatus, all natural enemies of thrips. First, we analyse the possible interactions between these seven species and we continue by discussing how functional indirect interactions, particularly the behaviour of arthropods, may change the significance and impact of direct interactions and numerical indirect interactions. It was found that a simple food web of only four species already gives rise to some quite complicated combinations of interactions. Spider mites and thrips interact indirectly through resource competition, but thrips larvae are intraguild predators of spider mites. Some of the natural enemies used for control of the two herbivore species are also intraguild predators. Moreover, spider mites produce a web that is subsequently used by thrips to hide from their predators. We discuss these and other results obtained so far and we conclude with a discussion of the potential impact of functional indirect and direct interactions on food webs and their significance for biological control.     

Plant quality effects on intraguild predation between Orius laevigatus and Aphidoletes aphidimyza

To understand the influence of plant quality on intraguild predation and consequently on the suppression of a shared prey population as well as on plant yield, the interactions between Aphis gossypii Glover (Hemiptera: Aphididae) (shared prey), Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) (intermediate predator), and Orius laevigatus Fieber (Hemiptera: Anthocoridae) (top predator) were investigated in 25‐day experiments on cucumber, Cucumis sativus L. (Cucurbitaceae) at various N fertilization levels (90, 150, and 190 p.p.m.) in microcosm set‐ups under greenhouse conditions. The final aphid population size was significantly affected by an interactive effect of N fertilization and predator application. Regardless of the N fertilization levels, O. laevigatus alone was more effective in aphid suppression than A. aphidimyza alone. In addition, the risk for aphids of being predated upon by both predators together was significantly reduced in the low and medium‐N fertilization levels, whereas it was additive in the high‐N fertilization treatment. The A. aphidimyza population was suppressed by O. laevigatus in both the 90 and 150 p.p.m. N treatments. However, there was no intraguild predation of O. laevigatus on A. aphidimyza at the 190 p.p.m. N level. Total plant yield depended on predator treatments and N fertilization levels, with the highest yield produced at the 150 p.p.m. N fertilization level in treatments with either O. laevigatus alone or with both predators together. Our results demonstrate that the weak asymmetric intraguild predation among A. aphidimyza and O. laevigatus does not influence the ability of both predators together to diminish bottom‐up effects on aphid populations and the yield losses associated with aphid infestations.     

Aphid suppression by natural enemies in mulched cereals

Large populations of natural enemies are the basis for natural pest control. Effects of mulch on predator–prey interactions in arable fields are poorly known, despite its potential to enhance ground‐dwelling predators and thereby reduce pest infestations. We studied the densities of predators and parasitoids, and their impact on cereal aphids in the presence and absence of mulch. Released populations of the bird cherry aphid, Rhopalosiphum padi (L.) (Homoptera: Aphididae), and two naturally occurring aphid species, were monitored under experimentally reduced densities of: (i) ground‐dwelling predators, (ii) flying predators and parasitoids, and (iii) with straw mulch. The three treatments were applied in a 2 × 2 × 2 factorial design in a field of spring wheat (Triticum aestivum L.). The exclusion of ground‐dwelling predators increased aphid populations by 55% in June and 40% in July, respectively. Mulched plots had 25% lower aphid densities in June. This was presumably due to enhanced densities of spiders (Araneida) in mulched plots. The exclusion of flying predators and parasitoids led to 94% higher aphid populations in late July (109 vs. 56 individuals per 100 shoots), irrespective of mulch or ground predator manipulation. This was attributed to the larvae of gall midges Aphidoletes cf. aphidimyza (Rondani) (Diptera: Cecidomyiidae) and hoverflies (Diptera: Syrphidae). The results indicate that a scarcity of predators and a bare soil surface renders crops more susceptible to arthropod pests. Farming schemes should aim at enhancing both ground‐dwelling and flying predators for elevated levels of natural pest control.