The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

Biological control of arthropod pests using banker plant systems: Past progress and future directions

The goal of banker plant systems is to sustain a reproducing population of natural enemies within a crop that will provide long-term pest suppression. The most common banker plant system consists of cereal plants infested with Rhopalosiphum padi L. as a host for the parasitoid Aphidius colemani L. Aphidius colemani continually reproduce and emerge from the banker plants to suppress aphid pests such as Aphis gossypii Glover and Myzus persicae Sulzer. Banker plant systems have been investigated to support 19 natural enemy species targeting 11 pest species. Research has been conducted in the greenhouse and field on ornamental and food crops. Despite this there is little consensus of an optimal banker plant system for even the most frequently targeted pests. Optimizing banker plant systems requires future research on how banker plants, crop species, and alternative hosts interact to affect natural enemy preference, dispersal, and abundance. In addition, research on the logistics of creating, maintaining, and implementing banker plant systems is essential. An advantage of banker plant systems over augmentative biological control is preventative control without repeated, expensive releases of natural enemies. Further, banker plants conserve a particular natural enemy or potentially the ‘right diversity’ of natural enemies with specific alternative resources. This may be an advantage compared to conserving natural enemy diversity per se with other conservation biological control tactics. Demonstrated grower interest in banker plant systems provides an opportunity for researchers to improve biological control efficacy, economics, and implementation to reduce pesticide use and its associated risks.     

Compatibility of flonicamid and a formulated mixture of pyrethrins and azadirachtin with predators for soybean aphid (Hemiptera: Aphididae) management

The invasive soybean aphid, Aphis glycines Matsumura, is an important pest in North American soybean production. Predators can play an important role in suppressing A. glycines. However, current A. glycines management practices rely primarily on broad-spectrum insecticides, which can adversely affect natural enemy populations. An alternative is the use of selective insecticides that control the targeted pest species, while having a reduced impact on natural enemies. In greenhouse and laboratory assays, we tested the effects of lambda-cyhalothrin, two rates of flonicamid, which is currently not registered for use in soybean, and a formulated mixture of pyrthrins and azadirachtin on A. glycines and its natural enemies, Chrysoperla rufilabris (Burmeister), Orius insidiosus (Say) and Hippodamia convergens (Guerin-Meneville). All insecticides significantly reduced A. glycines populations. Lambda-cyhalothrin was highly toxic to the natural enemies tested. Flonicamid showed the lowest toxicity to natural enemies, but the high rate did decrease survival of O. insidiosus. The mixture of pyrethrins and azadirachtin was toxic to larvae of C. rufilabris and adult O. insidiosus. Moreover, the mixture of pyrethrins and azadirachtin increased the developmental time of C. rufilabris. These results indicate potential for flonicamid and the mixture of pyrethrins and azadirachtin to increase compatibility between chemical and biological controls.     

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.     

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.     

作物多样性对大豆蚜的控蚜效应

【目的】研究大豆蚜发生为害及大豆与多种作物间邻作种植对大豆蚜的控制作用,为大豆蚜的可持续综合治理提供理论依据。【方法】采用系统调查的方法,研究大豆蚜和天敌田间种群动态;通过田间罩笼、人工接蚜和释放天敌的方法,研究捕食性天敌对大豆蚜种群的控制作用;在佳木斯地区进行大豆与早熟马铃薯间作,牡丹江地区进行黄瓜-大豆-玉米、甜葫芦-大豆-玉米、烟草-大豆-香瓜、甜菜-大豆-玉米等多作物带状穿插种植模式,以单作大豆田为对照,对不同种植模式的大豆田大豆蚜与天敌进行调查,研究作物多样性对大豆蚜的控制作用。【结果】2009年6月中下旬大豆蚜开始侵入大豆田,3~5周后田间有蚜株率达到100%,大豆蚜种群发生高峰期在7月下旬至8月上旬,9月上旬在田间逐渐消失。草蛉、瓢虫和寄生蜂等为蚜虫天敌优势种;按大豆蚜与天敌数量之比700︰1,释放异色瓢虫和叶色草蛉成虫7 d后,蚜虫种群减退率分别为54.78%和78.79%;大豆与早熟马铃薯间作,在大豆蚜种群迅速增长期早熟马铃薯收获(7月20日)后第5天,豆田蚜虫天敌总数是收获前的2.6倍,与同期单作大豆田相比,间作田大豆蚜种群数量降低了51.3%。大豆与甜葫芦、香瓜、烟草和玉米等作物进行多样性间作种植,在大豆蚜田间发生高峰期,单作豆田益害比为1︰65.2,多样性种植区的大豆田益害比为1︰26~1︰42,与单作大豆田相比,间作田大豆蚜种群数量降低40.7%~83.5%。【结论】2009年大豆蚜的种群高峰期为8月3日,田间的天敌优势种类为草蛉、瓢虫和寄生蜂。早熟马铃薯与大豆间作,在大豆蚜种群迅速增长期间收获早熟马铃薯,大量蚜虫天敌转移至间作的大豆田,从而形成对大豆蚜的控制。大豆与其它经济作物间邻作,大豆田天敌昆虫与蚜虫的益害比明显提高,表明利用农田作物多样性能充分发挥自然天敌的生物控害作用。     

A nematode,fungus, and aphid interact via a shared host plant: implications for soybean management

Soybean, Glycine max (L.) Merrill (Fabaceae), is an introduced crop to America and initially benefited from a small number of pests threatening its production. Since its rapid expansion in production beginning in the 1930s, several pests have been introduced from the native range of soybean. Our knowledge of how these pests interact and the implications for management is limited. We examined how three common economic soybean pests, the nematode Heterodera glycines Ichinohe (Nematoda: Heteroderidae), the fungus Cadophora gregata Harrington & McNew (Incertae sedis), and the aphid Aphis glycines Matsumura (Hemiptera: Aphididae), interact on soybean cyst nematode‐susceptible (SCN‐S) and soybean cyst nematode‐resistant cultivars carrying the PI 88788 resistance source (SCN‐R). From 2008 to 2010, six soybean cultivars were infested with either a single pest or all three pests in combination in a micro‐plot field experiment. Pest performance was measured in a ‘single pest’ treatment and compared with pest performance in the ‘multiple pest’ treatment, allowing us to measure the impact of SCN resistance and the presence of other soybean pests on each pest’s performance. Performance of H. glycines (80% reduction in reproduction) and A. glycines (19.8% reduction in plant exposure) was reduced on SCN‐R cultivars. Regardless of cultivar, the presence of multiple pests significantly decreased the performance of A. glycines, but significantly increased H. glycines performance. The presence of multiple pests decreased the performance of C. gregata on SCN‐S soybean cultivars (20.6% reduction in disease rating).     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.     

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.     

Temporal relationships between the generalist predator,Orius insidiosus,and its two major prey in soybean

The generalist predator, Orius insidiosus (Say) is an important early-season predator of the soybean aphid, Aphis glycines Matsumura, a newly invasive pest of major concern in soybean crop management. We conducted a 3 year, multiple field study to characterize the dynamic relationships between the predator, the pest, and alternative prey in soybean. Using field sampling data, we showed that thrips were the only alternative prey to be well-established in fields prior to O. insidiosus arrival and were likely to promote predator colonization of soybean fields prior to the arrival of soybean aphid. The predator displayed a reproductive numerical response to thrips in one of the 3 years and a primarily aggregative response in another year. The predator did not respond numerically to soybean aphid in the majority of fields. Experimental manipulations of thrips populations in field plots temporarily reduced thrips densities but had a minimal effect on O. insidiosus densities, suggesting that the predator is resilient against temporary reductions in a major resource. In the 2 years O. insidiosus populations were well-established in fields prior to soybean aphid arrival, soybean aphid remained at low levels throughout the season. In the year soybean aphid arrived early with respect to the growing season and before O. insidiosus populations were established, soybean aphid reached outbreak levels in all fields. Future research efforts on the factors determining soybean aphid population dynamics need to address the relative importance of early-season soybean aphid colonization and generalist predator population dynamics on the potential for soybean aphid population outbreaks.     

The interaction of soybean aphids and soybean cyst nematodes on selected resistant and susceptible soybean lines

Soybean aphids, Aphis glycines Matsumura, and soybean cyst nematodes, Heterodera glycines Ichinohe, are economic pests of soybean, Glycine max (L.) Merr., in the north‐central United States. Combined, these pests may account for 20–50% of yield reductions in a soybean crop. Only limited information is available concerning the interaction of these two pests on soybean production. During the summers of 2006 and 2007, we conducted a field‐experiment near Urbana, IL, to evaluate the effect of resistant and susceptible soybean lines on the development and reproduction of both pests in combination with each other. We also examined how each pest, as well as their interaction, affected the yield of susceptible and resistant soybean lines. Soybean plants grown within caged plots were infested with soybean aphids and soybean cyst nematodes; cumulative aphid days and soybean cyst nematode egg densities were determined at the end of each growing season. Soybean aphids were able to survive on all four soybean lines in both years of this study; however, aphid‐resistant lines generally had fewer cumulative aphid days than aphid‐susceptible lines. Likewise, nematode‐resistant lines typically had fewer eggs than nematode‐susceptible lines. During both years, we failed to observe a significant interaction between these two pests on the reproduction of one another. Yield data from 2006 was inconclusive; however, results from 2007 suggest that yield‐loss when soybean aphids and soybean cyst nematodes occur jointly is not significantly greater than when these two pests occur independently. The relationship between these two pests, and our inability to observe an interaction, are discussed.     

Reaping benefits from an invasive species: role of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in natural biological control of <Emphasis Type="Italic">Aphis glycines</Emphasis> in North America

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an invasive species present in numerous agroecosystems in North America. Despite adverse impacts as a threat to native biodiversity, a nuisance household invader and a pest in fruit production, H. axyridis also plays a beneficial role as a major component of assemblages of generalist predators in several agricultural crops. Here, we review the role of H. axyridis as a natural enemy of Aphis glycines Matsumura (Hemiptera: Aphididae), an invasive pest of soybean, Glycine max (L.) Merrill (Fabales: Fabaceae), in North America. Harmonia axyridis is often the most abundant predator species attacking A. glycines in soybean agroecosystems. This predator has the potential to both prevent and suppress A. glycines outbreaks. Further studies are needed to fully understand and utilize the potential of H. axyridis as a natural enemy in the management of A. glycines and other agricultural pests in agroecosystems worldwide.     

Effect of flower identity and diversity on reducing aphid populations via natural enemy communities

Floral plantings are often used in agriculture to attract pollinator communities, but they also play an important role in recruiting and establishing natural communities for natural pest control. Inconsistent effects of floral plantings for pest control may be a result of an absence of mechanistic insights and a reliance on the idea that simply increasing flower diversity will benefit these services. A more tailored set of flower species may be needed to benefit the natural enemies through provision of nectar and alternative prey. We used an outside pot experiment to investigate the effect of three flower plants (Fagopyrum esculentum, Vicia faba, and Trifolium pratense) on reducing aphid pests on four different plant cultivars of barley (Hordeum vulgare), over two years. We grew the four cultivars of barley alone, next to a single flower or next to a mixture of flowers, and observed aphid and natural enemy colonization across the growing season. Aphid population sizes were reduced on all barley cultivars grown next to a flower with stronger pest suppression when all flowers were present. Each flower species recruited a different community of non‐barley aphids that, in turn, varied in their ability to establish the natural enemy populations and subsequently the ability to reduce barley aphid populations. Overall, increased pest suppression in the mixed treatments was a result of numerous weaker interactions between different flower, aphid, and natural enemy species, rather than a few dominant interactions. Natural enemy communities could be enhanced by incorporating flower species that vary in their ability to attract and host alternative prey (i.e., non‐pest aphids) as well as suitable nectar provisioning. We can use our knowledge of ecological interactions to tailor floral plantings to increase the effectiveness of pest control services.     

Do weaver ants affect arthropod diversity and the natural‐enemy‐to‐pest ratio in horticultural systems?

High biodiversity is an important component of sustainable agricultural systems, and previous studies have found that increases in the diversity of the natural enemies of pests are associated with decreases in pest populations. Weaver ants are well known for their highly territorial and aggressive behaviour and for their control efficiency of many insect pests in tropical crop trees. Because of this, the ants have been used as a key component in integrated pest management (IPM) programmes for tropical crop trees. In implementing the IPM programmes, we received a number of enquiries related to whether weaver ants have negative effects on arthropod diversity and other natural enemies in orchard systems due to their aggressive behaviour. To answer these questions, we regularly sampled canopy arthropods in cashew and mango orchards in the Northern Territory of Australia in 1996, 2002 and 2003. We sampled, using a vacuum sampler, orchards with and without weaver ants. Cashew and mango plots with abundant weaver ants had similar or higher canopy arthropod and natural enemy diversity and similar ratios of natural enemies to insect pests, compared with plot where the weaver ant was absent. The study also showed that the application of insecticides reduced arthropod diversity and the ratio of natural enemies to insect pests in a mango orchard. However, insecticide spray did not affect natural enemy diversity and abundance, which may be related to a high immigration rate of natural enemies in small plots surrounded by areas that were not sprayed.     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.     

Habitat linkages in conservation biological control: Lessons from the land–water interface

Terrestrial landscapes, including those with embedded agroecosystems, are a mosaic of cover types varying in size. Creating or maintaining habitats that support natural enemy populations to combat agricultural pests is the primary method of conservation biological control. Non-crop habitats can be managed in an attempt to maximize the exchange of natural enemies with adjacent agroecosystems with the expectation that they will suppress damaging pest outbreaks. Despite this goal, current habitat management relying on natural enemy spillover into crops has been unreliably effective at reducing pest abundance or increasing crop yield. Furthermore, the expansion and intensification of agriculture and changes in global climate patterns threaten the foundations of conservation biological control in future agroecosystems. However, the aquatic–terrestrial interface offers a natural boundary similar to the one between agroecosystems and their neighboring non-crop habitats that can provide useful insights to the challenges facing growers. Research of the exchanges between water and land suggests general biological and physical processes that govern the movement of organisms between disparate habitats. We propose that like aquatic insects moving from water to land, natural enemy dispersal from non-crop donor habitats into recipient crop patches on the landscape is a function of (1) the production of natural enemies in the source habitat which establishes the abundance of organisms that can disperse, (2) how and why mobile natural enemies disperse themselves into neighboring recipient habitats, and (3) the configuration of donor and recipient habitats on the landscape. We suggest that conservation biological control practitioners can focus on these main components of natural enemy production and dispersal to predict the effectiveness of conservation biological control measures and guide their adaptation to future global change.     

Alate immigration disrupts soybean aphid suppression by predators

Natural enemies suppress many aphid populations, and yet, population outbreaks sometimes occur. The reasons predation fails to suppress such outbreaks are not clearly understood. While manipulating predators to examine their role in soybean aphid population growth, a natural immigration of soybean aphids occurred that enabled us to compare the roles immigration and predation played in population growth. Using predator exclusion cages, we found that predation on the top of the plant accounted for 42.3 ± 11.4% (mean ± SE) reduction in aphid population growth rates. When 90–100% of the canopy was exposed, predation failed to reduce aphid population growth because winged immigrants colonized plants, with an observed 6‐fold increase in alates compared to plants completely covered or exposing only the top nodes (approximately 10% of the total canopy). We conclude that reproduction by immigrants contributed to population growth rates sufficiently to compensate for predation. These results demonstrate that immigration can counteract high levels of predation and lead to aphid population growth rates that could result in outbreak population densities.     

Relationships between soybean shoot nitrogen components and soybean aphid populations

Defining the relationships between soybean (Glycine max [L.] merr.) shoot nitrogen (N) components and soybean aphid (Aphis glycines Matsumura) populations will increase understanding of the biology of this important insect pest. In this 2-year field study, caged soybean plants were infested with soybean aphids (initial infestation of 0, 10, 50, or 100 aphids plant^?1) at the fifth node developmental stage. Soybean aphid populations, soybean shoot dry weight, and shoot concentrations of nitrate-N, ureide-N, and total N were measured starting at full bloom through full seed soybean development stages. Soybean aphid population as well as shoot concentration of ureide-N increased rapidly starting at full bloom, peaked at beginning seed, and dramatically decreased by full seed soybean reproductive stages. Regression analysis indicated significant relationships (P = 0.01; r = 0.71) between soybean aphid populations and shoot ureide-N concentration. Thus, soybean aphid population levels appear to coincide with shoot ureide-N concentrations in the soybean plant.     

Lack of strong refuges allows top-down control of soybean aphid by generalist natural enemies

Refuges have been shown to be important mediators of predator–prey interactions, and in particular, have been proposed as a potential mechanism allowing herbivore populations to reach outbreak levels. However, very little research on the role of refuges has been conducted in systems dominated by generalist predators. We investigated the existence of refuges from predation for the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) at multiple scales. This species invaded North America and in spite of previous studies demonstrating strong suppression by generalist natural enemies, its populations periodically cause significant economic losses. Using naturally occurring populations of soybean aphid and its natural enemies, we tested for the presence of A. glycines spatial and dynamic refuges at the within-field, single plant, and within-plant scale. At the within-field level, we found only weak and transient spatial patterns in aphid populations suggesting the lack of spatial refuges at this scale. Similarly, at the plant level we found no individual colonies that escaped predation and aphid suppression was 9- to 28-fold greater in comparison with caged controls regardless of initial aphid density. When high aphid populations were exposed to predation they were rapidly reduced to levels close to the average field density and showed reduced per capita growth rates, indicating an absence of dilution of predation risk at increased aphid density. Finally, we found a significant shift in the distribution of aphids to the lower portions of the plant in the presence of generalist predators, suggesting a partial refuge from predation at the within-plant scale. Overall, we found the naturally occurring community of generalist predators to exert strong top-down suppression of soybean aphid populations at multiple scales, and no evidence that the presence of refuges at the scales studied can lead to outbreak populations. The partial refuge from predation at the within-plant scale revealed in our study may have important consequences for the within-season population dynamics of A. glycines, since it may be associated with low plant quality tradeoffs, and therefore warrants further research.     

Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem

The suppression of agricultural pests has often been proposed as an important service of natural enemy diversity, but few experiments have tested this assertion. In this study we present empirical evidence that increasing the richness of a particular guild of natural enemies can reduce the density of a widespread group of herbivorous pests and, in turn, increase the yield of an economically important crop. We performed an experiment in large field enclosures where we manipulated the presence/absence of three of the most important natural enemies (the coccinellid beetle Harmonia axyridis, the damsel bug Nabis sp., and the parasitic wasp Aphidius ervi) of pea aphids (Acyrthosiphon pisum) that feed on alfalfa (Medicago sativa). When all three enemy species were together, the population density of the pea aphid was suppressed more than could be predicted from the summed impact of each enemy species alone. As crop yield was negatively related to pea aphid density, there was a concomitant non‐additive increase in the production of alfalfa in enclosures containing the more diverse enemy guild. This trophic cascade appeared to be influenced by an indirect interaction involving a second herbivore inhabiting the system – the cowpea aphid, Aphis craccivora. Data suggest that high relative densities of cowpea aphids inhibited parasitism of pea aphids by the specialist parasitoid, A. ervi. Therefore, when natural enemies were together and densities of cowpea aphids were reduced by generalist predators, parasitism of pea aphids increased. This interaction modification is similar to other types of indirect interactions among enemy species (e.g. predator–predator facilitation) that can enhance the suppression of agricultural pests. Results of our study, and those of others performed in agroecosystems, complement the broader debate over how biodiversity influences ecosystem functioning by specifically focusing on systems that produce goods of immediate relevance to human society.