Intraguild predation and sublethal interactions between two zoophytophagous mirids,Macrolophus pygmaeus and Nesidiocoris tenuis

The omnivorous predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) are important biological control agents of pests on tomato crops. In this study, potential intraguild predation (IGP) interactions between the two species were investigated on tomato. We examined: (a) the within plant distribution of both species in the field, (b) the within plant distribution of each predatory species when co-occurred at high densities on tomato caged plants, (c) their behavioral interactions when enclosed in experimental arenas and (d) the development young and old nymphs of M. pygmaeus when enclosed together with N. tenuis adults. Results revealed that the two predators showed a different distribution pattern on the plants, with N. tenuis exploiting mostly the upper part, whereas M. pygmaeus were mostly observed on the 5th to the 7th leaf from the top. However, when the predators co-occurred, N. tenuis or M. pygmaeus individuals were recorded with increased numbers on the lower or the higher part of the plant, respectively. In the presence of N. tenuis adult young nymphs of M. pygmaeus completed their development to the adult stage, when alternative prey (lepidopteran eggs) was present on the plant, however failed to reach adulthood in the absence of alternative prey. A high percentage of the dead nymphs found with their body fluids totally sucked indicating predation by N. tenuis. However, large 4th instar nymphs of M. pygmaeus were much less vulnerable to N. tenuis than younger. The behavior of N. tenuis was affected by the presence of M. pygmaeus, but at a rate similar to that when two individuals of N. tenuis were enclosed together. Contacts between the predators were recorded in a similar frequency in mono- and heterospecific treatments, whereas aggressive behavior was not observed. This study shows that intraguild interactions between M. pygmaeus and N. tenuis occur but are not intensive. The potential implications of the outcomes for biological control are discussed.     

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.     

Resource quality,resource availability,and intraguild predation among omnivorous mirids

Intraguild predation (IGP) among predatory species can influence many plant-arthropod associations. However, the relevance of IGP is poorly understood for truly omnivorous species such as those that can complete development on both animal and plant diets. Here we test the hypothesis that IGP among two omnivorous mirids is more common when extraguild food is either absent or not suitable. Laboratory experiments were performed in experimental cages in order to determine the effect of intraguild prey densities and diet availability on direction and intensity of IGP between Dicyphus tamaninii and Macrolophus caliginosus (Heteroptera: Miridae). Intraguild predation was symmetrical between the two mirid species in the absence of alternative food. Increasing densities of intraguild prey enhanced drastically the incidence of IGP. Intraguild predation was reduced when mirids were in the presence of green or red tomato fruits, but the presence of any other extraguild resources had no impact on IGP level. However, when given before the experiments, all resources with the exception of tomato leaves significantly reduced IGP. A second experiment was performed on live plants to compare the results of the previous trials with that obtained in a more natural setting. No IGP was observed when both mirid species were present on a plant. However, development of the intraguild prey (the more vulnerable stage) was hindered by the presence of the intraguild predator. The potential of such results is discussed from community ecology and biological control perspective.     

Intraguild predation and competitive displacement between Nesidiocoris tenuis and Dicyphus maroccanus,two biological control agents in tomato pests

Dicyphus maroccanus Wagner and Nesidiocoris tenuis Reuter (Hemiptera: Miridae) are 2 biological control agents in tomatoes. Through the crop seasons, a natural shift in the occurrence of both mirids in favor of N. tenuis has been observed at the end of the cropping cycle in eastern Spain. To better optimize their conservation, the reasons for the observed change, such as intraguild interactions (IGP) or the influence of environmental conditions, are worth elucidating. To do this, we first studied the IGP of adult females on heterospecific nymphs in the laboratory. We next studied exploitative competition between adults and nymphs of each species when feeding on Ephestia kueniella Zeller (Lepidoptera: Pyralidae) eggs in the laboratory. Finally, to analyze the competitive displacement between both mirids, we conducted a semifield experiment in which both predators were released together. All experiments were conducted at 2 temperature regimes (20 and 25°C). Adult‐to‐nymph intraguild interactions occurred only at 25 ºC at very low levels, showing that N. tenuis attacked and consumed a greater proportion of heterospecific nymphs. Nesidiocoris tenuis was a better competitor than D. maroccanus when feeding on the shared prey in the presence of its heterospecific nymph at 25 ºC. In semifield conditions, N. tenuis showed a competitive advantage over D. maroccanus at both temperatures. We conclude that there is not direct interference between both species, however, N. tenuis has a greater ability to outcompete, since it is best adapted to higher temperatures and it is able to remove food sources for D. maroccanus.     

Life‐history parameters and predation capacity of Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) on eggs of Plutella xylostella (Lepidoptera: Plutellidae)

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Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem

Several models and experimental studies conducted in confined environments have shown that intraguild predation (IGP) can modulate population abundances and structure communities. A number of ecological and abiotic factors determine the nature and frequency of IGP. This study examined the effect of plant architecture and extraguild prey density, and their interactions, on the occurrence of IGP between two species of ladybird, Harmonia axyridis (Pallas) and Propylea quatuordecimpunctata L. (both Coleoptera: Coccinellidae). Theoretical concepts predict that IGP levels would increase with a decrease of both extraguild prey density and plant structural complexity. We conducted a factorial experiment in an open soybean field into which coccinellid larvae were introduced in experimental plots for a period of 5 days. We tested two levels of soybean aphid [Aphis glycines Matsumara (Hemiptera: Aphididae)] density, low and high (100 and 1 000 aphids per plot, respectively), and two levels of plant complexity, low (by removing half of the branches from the soybean plants) and high (by leaving plants intact). We used species‐specific molecular markers to detect the presence of P. quatuordecimpunctata in the digestive tract of H. axyridis. Molecular gut‐content analysis of H. axyridis revealed that rates of IGP were higher (20%) at low aphid density than at high aphid density (<6%). Decreased plant complexity did not impact the frequency of IGP. In accordance with existing literature, this study demonstrates that IGP is amplified at low extraguild prey density. We conclude that considering environmental factors, such as extraguild prey density, is crucial to improve our ability to predict the impact of intraguild predation on community structure and, from an applied perspective, biological control.     

Intra‐ and interspecific interactions between aphidophagous ladybirds: the role of prey in predator coexistence

Cannibalism (CANN) and intraguild predation (IGP) may provide energy and nutrients to individuals and eliminate potential competitors. These negative competitive interactions could also affect the coexistence of predatory species. The co‐occurrence of aphidophagous ladybird species in crops creates opportunities for CANN and IGP, especially when aphids become scarce. The Lotka–Volterra model predicts the coexistence of two species if intraspecific competition is stronger than interspecific interference interactions. Cycloneda sanguinea L. and Eriopis connexa (Germar) (both Coleoptera: Coccinellidae) coexist in sweet pepper crops in La Plata (Argentina) consuming mainly Myzus persicae (Sulzer) (Hemiptera: Aphididae). The present study used laboratory experiments to estimate levels of CANN and IGP by adults and larvae on eggs, and by adults on larvae, in both the presence and absence of prey (i.e., M. persicae), to explain the effect of prey on coexistence of these two predators. Levels of CANN by C. sanguinea and E. connexa were high in the absence of aphids, and decreased when prey was present. Intraguild predation was bidirectional and asymmetric. Adults and larvae of E. connexa were more voracious IG predators of C. sanguinea than vice versa, the former being the stronger IG predator and interference competitor. Eriopis connexa always won when larvae of the same instar were compared, whereas the larger larva always won when larvae were of different instars, regardless of species. In the presence of prey, CANN by both species decreased, but IGP by E. connexa on C. sanguinea remained high, suggesting that E. connexa could displace C. sanguinea via interspecific interference competition. Other factors potentially affecting the coexistence of C. sanguinea and E. connexa in sweet pepper crops are discussed.     

Nesidiocoris tenuis as a pest in Northwest Europe: Intervention threshold and influence of Pepino mosaic virus

The use of Nesidiocoris tenuis (Hemiptera: Miridae) as a biocontrol agent is controversial as it is considered a pest in Northwest European tomato greenhouses, due to its tendency to damage the plant and fruit. Necessary chemical plant protection products to control N. tenuis have toxic side effects on important beneficials like Macrolophus pygmaeus (Hemiptera: Miridae), which jeopardizes the whole IPM programme. In this study, several commercial tomato greenhouses were monitored for mirid populations. The relationship between the number of N. tenuis individuals and plant damage was assessed in function of availability of prey and interaction with M. pygmaeus. These greenhouse data were used to determine a practical density intervention threshold. Next, the hypothesis that a Pepino mosaic virus (PepMV) infection increases plant and fruit damage by N. tenuis (as has been shown for M. pygmaeus) was tested. Plant damage occurred when the average number of predatory bugs in the head of the plant exceeded 16 per ten plants. Plant damage increased in severity at increasing predatory bug densities, independent of the availability of prey and M. pygmaeus presence. Plant and fruit damage were not affected by the presence of PepMV, as was shown for fruit damage in previous studies for M. pygmaeus. Our study provides a practical density intervention threshold for growers in greenhouse crops. Simple monitoring of the number of predatory bugs in the head of the plant can be used to take specific biocontrol actions. It was also shown that only the predatory bug N. tenuis itself causes damage, and there is no interaction with PepMV.     

Reciprocal intraguild predation between two mirid predators,Cyrtorhinus lividipennis and Tytthus chinensis (Hemiptera: Miridae)

Interactions between predator species shape ecological communities and are crucial in the relationship between biodiversity and ecosystem functioning. They contribute to improving the natural biological control. Cyrtorhinus lividipennis Reuter and Tytthus chinensis Stål (Hemiptera: Miridae) are important natural enemies of brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae), the most destructive rice pest in Asia. Comparative functional responses of both sexes of the two mirids at different development stages were estimated and the direction, symmetry, as well as intensity of intraguild predation (IGP) were studied in the laboratory. Prey preferences of the two mirid species and the influence of alternative prey on functional responses were also evaluated. The mirids exhibited reciprocal IGP in addition to consuming eggs of BPH. All predator–prey combinations exhibited a type II functional response. Females and fourth instar nymphs of C. lividipennis showed greater voracity for eggs of BPH than of T. chinensis. The two mirids were more voracious to intraguild prey than to extraguild prey. Alternative prey released the functional responses of C. lividipennis to both intra- and extraguild prey. In contrast, alternative prey had no effect on the functional response of T. chinensis. RIGP was symmetrical in the absence of extraguild prey. And in the presence of extraguild prey that was common in the field, resulted in different responses by the mirids.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

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.     

Intraguild predation among the predatory mites Amblyseius eharai,Amblyseius cucumeris and Amblyseius barkeri

Predator species with the same prey interact not only by competition for food and space but also by intraguild predation (IGP). The impact of IGP on introduced phytoseiid mites and native species in the context of biological control is a matter of considerable debate. Amblyseius eharai is the dominant native citrus species in central China, while Amblyseius cucumeris and Amblyseius barkeri are candidates for importation. All three species can feed on the spider mite Panonychus citri, which is the main pest in citrus. This study investigated, in the laboratory, possible IGP among these species in the absence and presence of P. citri, respectively. IGP in different densities of shared prey and intraguild (IG) prey was also studied. All three species consumed heterospecific larvae and eggs but not adults, and the IGP rate of larvae was significantly higher than that of eggs in the absence of shared prey. Additionally, the IGP rate of each group was reduced dramatically in the presence of both shared and IG prey when compared to the absence of shared prey. This occurs most likely because the three species prefer to feed on their natural prey P. citri, rather than on IG prey. Our results showed that A. eharai seems to be a more voracious IG predator than A. cucumeris. A. eharai was much more prone to IGP than A. barkeri.     

Asymmetrical intraguild predation between natural enemies of the citrus mealybug

The ability of a predator to discriminate against parasitized prey determines the extent of asymmetrical intraguild predation, which is often crucial for the outcome of biological control. Anagyrus nr. pseudococci (Girault) (Hymenoptera: Encyrtidae), a parasitoid of the citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), suffers from intraguild predation by coccinellids occurring in the same habitat. The level of intraguild predation on A. nr. pseudococci by Nephus includens (Kirsch) (Coleoptera: Coccinellidae) at different immature stages has been investigated with and without simultaneous offer of extraguild prey. Larvae of A. nr. pseudococci appeared to face increased intraguild predation at early developmental stages, whereas mummification provided adequate protection against the predatory coccinellid. Different predation levels on unparasitized vs. parasitized hosts at various developmental stages in choice assays indicated that N. includens preferences might be determined not solely by palatability of the prey but also by its ability to protect itself.     

Predation and reproduction of the generalist predator Nabis pseudoferus preying on Tuta absoluta

The damsel bug, Nabis pseudoferus Remane (Hemiptera: Namidae), is a generalist predator of small arthropods, including key insect pests of vegetable crops. In this study, we characterized the predation and development of various N. pseudoferus life stages when preying on the eggs and first- and fourth-instar nymphs of the invasive South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). These findings were compared to those of the bug’s common prey, cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Of the life stages tested, females showed the highest predation rate on all tested prey, due to their high longevity, large body, and great energy requirements for reproduction. The predator’s oviposition rate was clearly influenced by prey type, and was highest when feeding on fourth instars of T. absoluta. Considering the zoophytophagy of most of the life stages of other mirid species of tomato, and the lower propensity of N. pseudoferus to feed on plants, these results show that this species can be considered as a key indigenous natural enemy for sustainable pest control packages against T. absoluta in newly invaded areas.     

Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is an omnivorous generalist predator which is augmentatively released and conserved for control of whiteflies (Hemiptera: Aleyrodidae) and Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crops. Eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) are often provided as factitious prey to improve the establishment of N. tenuis after its release. We first tested different amounts of E. kuehniella eggs per plant to optimize N. tenuis establishment and then investigated whether the amount of eggs that optimized N. tenuis establishment might be reduced by adding sugars (hydrocapsules filled with 0.5 m sucrose) under walk‐in cage and commercial greenhouse conditions. These experiments demonstrated that the addition of sugar to the diet of N. tenuis could half the amount of E. kuehniella eggs required to establish N. tenuis. Under greenhouse conditions, the progeny of N. tenuis per plant did not differ significantly between E. kuehniella alone or the half amount of E. kuehniella plus hydrocapsules. These results demonstrated that the sugar could partially substitute for E. kuehniella eggs improve establishment of N. tenuis and suggest that natural sugars such as nectar and honeydew might also beneficial.     

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.     

Predation by <Emphasis Type="Italic">Nesidiocoris tenuis</Emphasis> on <Emphasis Type="Italic">Bemisia tabaci</Emphasis> and injury to tomato

Tomato is the most important vegetable crop in Spain. The mirid bug Nesidiocoris tenuis (Reuter) commonly appears in large numbers in protected and open-air tomato crops where little or no broad-spectrum insecticides are used. Nesidiocoris tenuis is known to be a predator of whiteflies, thrips and several other pest species. However, it is also considered a pest because it can feed on tomato plants, causing necrotic rings on stems and flowers and punctures in fruits. Our objectives were to evaluate predation by N. tenuis on sweetpotato whitefly Bemisia tabaci Gennadius under greenhouse conditions and establish its relationship to N. tenuis feeding on tomato. Two different release rates of N. tenuis were compared with an untreated control (0, 1 and 4 N. tenuis plant⁻¹) in cages of 8 m². Significant reductions of greater than 90% of the whitefly population and correspondingly high numbers of N. tenuis were observed with both release rates. Regression analysis showed that necrotic rings on foliage caused by N. tenuis were best explained by the ratio of B. tabaci nymphs:N. tenuis as predicted by the equation y = 15.086x − 0.6359.

New records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) predation by Brazilian Hemipteran predatory bugs

The tomato borer Tuta absoluta, native to western South America, is an extremely devastating pest in tomato crops in most of South America, Europe and Africa North of the Sahel, causes yield losses up to 100% and decreases fruit quality in open field and greenhouse crops if control methods are not applied. In Brazil two other important lepidopteran pests – Neoleucinodes elegantalis and Helicoverpa zea – occur in tomato, as well as thrips, whiteflies and aphids. For control of these pests, frequent applications of pesticides of up to 5 times per week are needed, and these resulted in the appearance of resistant populations to a number of active ingredients and decimation of natural enemies. Biological control may offer a better, safer and more sustainable opportunity for pest management. Mirid predatory bugs are currently used with success in southern Europe to control T. absoluta and other pests. In Brazil, four Hemipteran predatory bugs, not yet known to attack T. absoluta, were found to successfully prey on eggs and larvae of this pest. The first results on their predation capacity, development, survival and reproduction on T. absoluta on tomato plants are presented.     

Preference and Prey Switching in a Generalist Predator Attacking Local and Invasive Alien Pests

Invasive pest species may strongly affect biotic interactions in agro-ecosystems. The ability of generalist predators to prey on new invasive pests may result in drastic changes in the population dynamics of local pest species owing to predator-mediated indirect interactions among prey. On a short time scale, the nature and strength of such indirect interactions depend largely on preferences between prey and on predator behavior patterns. Under laboratory conditions we evaluated the prey preference of the generalist predator Macrolophus pygmaeus Rambur (Heteroptera: Miridae) when it encounters simultaneously the local tomato pest Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and the invasive alien pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). We tested various ratios of local vs. alien prey numbers, measuring switching by the predator from one prey to the other, and assessing what conditions (e.g. prey species abundance and prey development stage) may favor such prey switching. The total predation activity of M. pygmaeus was affected by the presence of T. absoluta in the prey complex with an opposite effect when comparing adult and juvenile predators. The predator showed similar preference toward T. absoluta eggs and B. tabaci nymphs, but T. absoluta larvae were clearly less attacked. However, prey preference strongly depended on prey relative abundance with a disproportionately high predation on the most abundant prey and disproportionately low predation on the rarest prey. Together with the findings of a recent companion study (Bompard et al. 2013, Population Ecology), the insight obtained on M. pygmaeus prey switching may be useful for Integrated Pest Management in tomato crops, notably for optimal simultaneous management of B. tabaci and T. absoluta, which very frequently co-occur on tomato.