The Role of Natural Enemy Foraging Guilds in Controlling Cereal Aphids in Michigan Wheat

Insect natural enemies (predators and parasitoids) provide important ecosystem services by suppressing populations of insect pests in many agricultural crops. However, the role of natural enemies against cereal aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. The objectives of this research were to characterize the natural enemy community in wheat fields and evaluate the role of different natural enemy foraging guilds (foliar-foraging versus ground-dwelling predators) in regulating cereal aphid population growth. We investigated these objectives during the spring and summer of 2012 and 2013 in four winter wheat fields on the Michigan State University campus farm in East Lansing, Michigan. We monitored and measured the impact of natural enemies by experimentally excluding or allowing their access to wheat plants infested with Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae). Our results indicate that the natural enemy community in the wheat fields consisted mostly of foliar-foraging and ground-dwelling predators with relatively few parasitoids. In combination, these natural enemy groups were very effective at reducing cereal aphid populations. We also investigated the role of each natural enemy foraging guild (foliar-foraging versus ground-dwelling predators) independently. Overall, our results suggest that, in combination, natural enemies can almost completely halt early-season aphid population increase. Independently, ground-dwelling predators were more effective at suppressing cereal aphid populations than foliar-foraging predators under the conditions we studied. Our results differ from studies in Europe and the US Great Plains where foliar foraging predators and parasitoids are frequently more important cereal aphid natural enemies.     

Influence of drought on interactions between Rhopalosiphum padi and ground dwelling predators – A mesocosm study

Climate change will lead to extreme droughts, but it is difficult to predict how this will affect crop pests. In particular, it is unclear how interactions between natural enemies and pests will be influenced. In the field, bird cherry-oat aphids (Rhopalosiphum padi (L.)) have been observed to reside close to, or below the ground surface during dry conditions. We hypothesized that this will increase the niche overlap between R. padi and ground-dwelling predators such as carabid beetles and wolf spiders and that aphid numbers will therefore decline during dry conditions. A fully factorial mesocosm experiment was conducted testing the combined effects of drought and predator presence on aphid position and abundance on barley (Hordeum vulgare) plants. In support of our hypothesis, we found that (a) aphids moved below ground during dry conditions, (b) predators reduced aphid numbers, but only during dry conditions, and (c) predators reduced the proportion of aphids below ground in dry conditions. This increased predation effect during dry conditions was, however, compensated for by a corresponding increase in aphid performance on the plants and so the net effect of drought on aphid numbers ended up being neutral. Thus, pests can be affected by drought in complex ways via a combination top-down and bottom-up mechanisms. Predicting how pest populations will be affected by droughts in the future is thus a formidable research challenge.     

Non-additive effects of multiple natural enemies on aphid populations

The question of whether multiple natural enemies often interact to produce lower host mortality than single enemies acting alone has not yet been resolved. We compared the effects of four different combinations of natural enemies-parasitoids, predators, parasitoids plus predators, and no enemies-on caged aphid populations on marsh elder, Iva frutescens, in west-central Florida. Using starting densities of natural enemies commonly found in the field, we showed that parasitoid wasps reduced aphid population densities more than predatory ladybird beetles. The addition of predators to cages containing parasites reduced the ability of parasitoids to decrease aphid population densities. Because the experiments ran only over the course of one generation, such a reduction in the effectiveness of parasites is likely caused by interference of predators with parasitoid behavior. Parasitism in the cages containing both parasitoids and predators was reduced when compared to percent parasitism in parasitoid-only cages, but this could also be due to predation. Our experiments showed that ladybird beetles prey on parasitized aphids. Thus over the long-term, the effectiveness of parasites is impaired by the interference of predators on ovipositing parasitoids and by the predation of parasitized aphids. The effects of natural enemies in this system are clearly non-additive.     

Syrphid flies suppress lettuce aphids

Syrphid flies are abundant in lettuce fields, where their larvae are key predators of aphids. However, the presence of predators in the field does not always result in economically significant levels of prey suppression. Even when predators are numerous, their effects on prey population dynamics may be variable. Over a two year period we surveyed lettuce fields in coastal California, USA to test whether syrphid flies are capable of colonizing fields with aphids and suppressing aphid population growth. The survey showed that female syrphids oviposited more eggs at locations with more aphids, and that greater numbers of syrphid larvae resulted in lower rates of increase in the aphid populations. We also directly manipulated syrphid densities by adding syrphid eggs to uncaged lettuce plants, and these syrphid additions resulted in lower aphid population growth. This research shows that syrphid flies have the ability to suppress aphid populations in lettuce fields.     

Quantifying the impact of polyphagous invertebrate predators in controlling cereal aphids and in preventing wheat yield and quality reductions

Exclusion barriers were used to manipulate numbers of polyphagous invertebrate predators so that their impact on cereal aphids and consequently wheat yield and quality could be examined. Experiments were conducted within the framework of the LINK Integrated Farming Systems Project which allowed comparisons to be made between the integrated and conventional farming systems under examination on a study farm in Hampshire, UK. Only in 1995 were the numbers of aphids per tiller, the aphid peak and rate of increase to the peak significantly greater in the exclusion areas where the density of polyphagous predators had been reduced. The maximum increase in aphids as a result of excluding polyphagous predators was 31%, which was equivalent to 130 aphid days. However, the polyphagous predators did not reduce the number of tillers infested. The relatively low impact of polyphagous predators was attributed to the aphid population phenology and greater effects may have been found had aphids infested the crops earlier in their development. Sowing date was shown to govern the time over which a crop may be susceptible to yield loss from aphids, with later-drilled crops being more susceptible to late-summer aphid infestations. Aphid numbers rarely affected grain yield but were found to be related to some grain quality parameters, but reducing polyphagous predators had no direct impact on grain yield or quality even where the aphid burden increased. The peak period of activity and density differed between the species of Carabidae, Staphylinidae and Araneae consequently influencing their relationship with the aphids. Some negative correlations were found between these groups of polyphagous predators and aphids. Species composition and abundance differed between fields thereby influencing the level of aphid predation. The exclusion barriers were most effective at reducing numbers of Carabidae although numbers of Staphylinidae and Araneae were also reduced. The consequences for Integrated Crop Management are discussed.     

Differential effects of weather and natural enemies on coexisting aphid populations

Study of mechanisms responsible for regulating populations of living organisms is essential for a better comprehension of the structure of biological communities and evolutionary forces in nature. Aphids (Hemiptera: Sternorrhyncha) comprise a large and economically important group of phytophagous insects distributed worldwide. Previous studies determined that density-dependent mechanisms play an important role in regulating their populations. However, only a few of those studies identified specific factors responsible for the observed regulation. Time series data used in this study originated from the untreated control plots that were a part of potato (Solanum tuberosum L.) insecticide trials in northern Maine from 1971 to 2004. The data set contained information on population densities of three potato-colonizing aphid species (buckthorn aphid, Aphis nasturtii; potato aphid, Macrosiphum euphorbiae; and green peach aphid, Myzus persicae) and their natural enemies. We used path analysis to explore effects of weather and natural enemies on the intrinsic growth rates of aphid populations. Weather factors considered in our analyses contributed to the regulation of aphid populations, either directly or through natural enemies. However, direct weather effects were in most cases detectable only at P ≤ 0.10. Potato aphids were negatively affected by both fungal disease and predators, although buckthorn aphids were negatively affected by predators only. Parasitoids did not have a noticeable effect on the growth of any of the three aphid species. Growth of green peach aphid populations was negatively influenced by interspecific interactions with the other two aphid species. Differential population regulation mechanisms detected in the current study might at least partially explain coexistence of three ecologically similar aphid species sharing the same host plant.     

Relative importance of predators and parasitoids for cereal aphid control

Field experiments with manipulations of natural enemies of plant-feeding insects may show how a diverse enemy group ensures an important ecosystem function such as naturally occurring biological pest control. We studied cereal aphid populations in winter wheat under experimentally reduced densities of: (i) ground-dwelling generalist predators (mostly spiders, carabid and staphylinid beetles); (ii) flying predators (coccinellid beetles, syrphid flies, gall midges, etc.) and parasitoids (aphidiid wasps), and a combination of (i) and (ii), compared with open controls. Aphid populations were 18% higher at reduced densities of ground-dwelling predators, 70% higher when flying predators and parasitoids were removed, and 172% higher on the removal of both enemy groups. Parasitoid wasps probably had the strongest effect, as flying predators occurred only in negligible densities. The great importance of parasitism is a new finding for aphid control in cereal fields. In conclusion, a more detailed knowledge of the mechanisms of natural pest control would help to develop environmentally sound crop management with reduced pesticide applications.     

Effects of Aphis fabae Scop, and of its attendant ants and insect predators on yields of field beans (Vicia faba L.)

Predators (mainly coccinellid adults and larvae and syrphid larvae), although few, were important in decreasing numbers of Aphis fabae on a small plot of field beans during the early stages of infestation in a year favourable to the aphid. At the same time, ants (Lasius niger L.), attending aphids on other plants on the same plot, effectively protected the aphids from predators for about 2 weeks, enabling the attended aphids to multiply faster than the unattended. When all aphid populations started to decline, predators became more numerous and accelerated the decline on both sets of plants. Bean plants without aphids yielded fifty-six seeds per plant; those with aphids but free from ants gave seventeen; and those with ant-attended aphids, eight seeds per plant. The damage and loss of yield was caused by the large aphid populations that developed when the pods were maturing, and not by the fewer aphids present when the plants were in flower. It appears that small, temporary infestations during flowering might increase the yield of field beans.     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.     

Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Virus mediated trophic interactions between aphids and their natural enemies

Microbial endosymbionts alter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae (i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level, the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virus enhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.     

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.     

Predator avoidance behavior in the pea aphid: costs,frequency, and population consequences

Induced prey defenses can be costly. These costs have the potential to reduce prey survival or reproduction and, therefore, prey population growth. I estimated the potential for predators to suppress populations of pea aphids (Acyrthosiphon pisum) in alfalfa fields through the induction of pea aphid predator avoidance behavior. I quantified (1) the period of non-feeding activity that follows a disturbance event, (2) the effect of frequent disturbance on aphid reproduction, and (3) the frequency at which aphids are disturbed by predators. In combination, these three values predict that the disturbances induced by predators can substantially reduce aphid population growth. This result stems from the high frequency of predator-induced disturbance, and the observation that even brief disturbances reduce aphid reproduction. The potential for predators to suppress prey populations through induction of prey defenses may be strongest in systems where (1) predators frequently induce prey defensive responses, and (2) prey defenses incur acute survival or reproductive costs. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

自然天敌对苗蚜和伏蚜控制作用的定量分析

【目的】为了合理利用自然天敌,定量评价棉田自然天敌对苗蚜和伏蚜的控制作用。【方法】采用接虫罩笼法结合系统调查。【结果】发现苗蚜的主要自然天敌是龟纹瓢虫Propylaea japonica Thunberg和异色瓢虫Harmonia axyridis Pallas,大部分时间能够有效的控制苗蚜种群在防治指标以下,控害指数高达91%;伏蚜主要自然天敌是蜘蛛、草蛉和龟纹瓢虫,由于其种群数量太少,益害比低,对伏蚜控害指数始终低于20%,无法有效的控制伏蚜种群。【结论】结果提示,应根据苗蚜和伏蚜自然天敌控制作用不同,制定合理的保护利用自然天敌的策略。     

The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour

1. The effects of predator species, aphid density, aphid age, diel period, and habitat complexity on the dropping behaviour of the pea aphid Acyrthosiphon pisum were assessed in a series of laboratory and field-cage experiments.
2. The presence of foliar-foraging predators significantly increased the proportion of aphids that dropped from alfalfa plants. In the absence of predators, less than 7% of the aphids dropped. Dropping more than doubled (14%) when one of three hemipteran predators , N. americoferus, G. punctipes or O. insidiosus , was present. Nearly 60% of the aphids dropped when the ladybird beetle, Coccinella septempunctata , was present.
3. Adult aphids showed a significantly higher propensity to drop than immature aphids, regardless of the presence or absence of predators. Aphid density had no effect on dropping behaviour.
4. Neither diel period nor habitat complexity had an effect on aphid dropping behaviour. Aphids were significantly more likely to drop in the presence of predators during either the day or night and from either early or late regrowth alfalfa.
5. A review of the factors affecting dropping behaviour, including those elucidated in this study, indicates that the propensity to drop from a plant is influenced by three factors: the risk of predation on the plant, the quality of the resource to be abandoned, and the risk of mortality in the new microhabitat.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

Genetically based population variation in aphid association with ants and predators

A species’ genotype can have extended consequences for the structure of the surrounding community, but few studies have investigated the extended consequences of genetic variation in animals. Accordingly, I examined the importance of genetically based variation among five populations of the ant-tended aphid Aphis asclepiadis for its interactions with both ants and predators. In a common environment, aphid source population accounted for 23 and 17% of the variation in the occurrence of ants and predators, respectively. Ant exclusion increased predator abundance, accounting for 25% of variation, but there was no detectable influence of ants on aphid abundance. There was an indication that aphid source populations varied in honeydew quality, but this was uncorrelated with rates of ant attendance. This study provides the first evidence for genetic variation in aphids for attractiveness to ants, and underscores the important link between intra-specific genetic variation in aphids and the processes governing arthropod community structure.     

Within-Plant Bottom-Up Effects Mediate Non-Consumptive Impacts of Top-Down Control of Soybean Aphids

There is increasing evidence that top-down controls have strong non-consumptive effects on herbivore populations. However, little is known about how these non-consumptive effects relate to bottom-up influences. Using a series of field trials, we tested how changes in top-down and bottom-up controls at the within-plant scale interact to increase herbivore suppression. In the first experiment, we manipulated access of natural populations of predators (primarily lady beetles) to controlled numbers of A. glycines on upper (i.e. vigorous-growing) versus lower (i.e. slow-growing) soybean nodes and under contrasting plant ages. In a second experiment, we measured aphid dispersion in response to predation. Bottom-up and top-down controls had additive effects on A. glycines population growth. Plant age and within-plant quality had significant bottom-up effects on aphid size and population growth. However, top-down control was the dominant force suppressing aphid population growth, and completely counteracted bottom-up effects at the plant and within-plant scales. The intensity of predation was higher on upper than lower soybean nodes, and resulted in a non-consumptive reduction in aphid population growth because most of the surviving aphids were located on lower plant nodes, where rates of increase were reduced. No effects of predation on aphid dispersal among plants were detected, suggesting an absence of predator avoidance behavior by A. glycines. Our results revealed significant non-consumptive predator impacts on aphids due to the asymmetric intensity of predation at the within-plant scale, suggesting that low numbers of predators are highly effective at suppressing aphid populations.     

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.     

Detection of aphid remains in predatory insects and spiders by ELISA

An ELISA was developed which would detect and quantify ingested aphids in predators found in and around cereal crops. The detection limit of the assay was less than one hundredth of an homogenised adult aphid. Tests with 13 species of aphid showed that those which had been used as the principal immunogens reacted most strongly in the assay. Nearly a hundred species of invertebrates, both predators and alternative prey, have been tested in the assay and no evidence of significant cross-reaction was found with any of these species or with a number of samples of plant material on which aphids may be found. Aphid material could still be detected in predators which had been stored for up to 7 days in 4% formalin or 70% ethanol.