Long-Term Functional Dynamics of an Aphidophagous Coccinellid Community Remain Unchanged despite Repeated Invasions

Aphidophagous coccinellids (ladybeetles) are important providers of herbivore suppression ecosystem services. In the last 30 years, the invasion of exotic coccinellid species, coupled with observed declines in native species, has led to considerable interest in the community dynamics and ecosystem function of this guild. Here we examined a 24-year dataset of coccinellid communities in nine habitats in southwestern Michigan for changes in community function in response to invasion. Specifically we analyzed their temporal population dynamics and species diversity, and we modeled the community’s potential to suppress pests. Abundance of coccinellids varied widely between 1989 and 2012 and became increasingly exotic-dominated. More than 71% of 57,813 adult coccinellids captured over the 24-year study were exotic species. Shannon diversity increased slightly over time, but herbivore suppression potential of the community remained roughly constant over the course of the study. However, both Shannon diversity and herbivore suppression potential due to native species declined over time in all habitats. The relationship between Shannon diversity and herbivore suppression potential varied with habitat type: a positive relationship in forest and perennial habitats, but was uncorrelated in annual habitats. This trend may have been because annual habitats were dominated by a few, highly voracious exotic species. Our results indicated that although the composition of the coccinellid community in southwestern Michigan has changed dramatically in the past several decades, its function has remained relatively unchanged in both agricultural and natural habitats. While this is encouraging from the perspective of pest management, it should be noted that losses of one of the dominant exotic coccinellids could result in a rapid decline in pest suppression services if the remaining community is unable to respond.     

Landscape composition influences patterns of native and exotic lady beetle abundance

Aim Coccinellid beetles are important predators that contribute to pest suppression in agricultural landscapes. Since the introduction of the exotic coccinellids Coccinella septempunctata L. and Harmonia axyridis Pallas into the USA, several studies have reported a decline of native Coccinellidae in agroecosystems. We aimed to investigate the influence of landscape composition on native and exotic coccinellid abundance within soybean fields. Location Iowa, Michigan, Minnesota and Wisconsin. Methods As part of a 2‐year study (2005–06) on the biological control of the soybean aphid, Aphis glycines Matsumura, we examined coccinellid communities in 33 soybean fields using yellow sticky card traps. Landscape heterogeneity and composition were measured at multiple spatial scales ranging 1–3.5 km from focal soybean fields where coccinellid sampling took place. Results Exotic species made up 90% of the total coccinellid community in Michigan soybean fields followed by Wisconsin (84%), Minnesota (66%) and Iowa (57%). Harmonia axyridis was the dominant exotic coccinellid in all states comprising 45–62% of the total coccinellid community, followed by C. septempunctata (13–30%). Two additional exotic species, Hippodamia variegata (Goeze) and Propylea quatuordecimpunctata (L.) were also found in the region. Overall, the most abundant native coccinellid was Hippodamia convergens Guerin‐Meneville; however, its abundance varied across the region, comprising 0% (Michigan) to 28% (Iowa) of the total coccinellid community. Landscape structure significantly influenced the composition of coccinellid communities in soybean agroecosystems. We found that native coccinellids were most abundant in low‐diversity landscapes with an abundance of grassland habitat while exotic coccinellids were associated with the abundance of forested habitats. Main conclusion We propose that grassland dominated landscapes with low structural diversity and low amounts of forested habitat may be resistant to exotic coccinellid build‐up, particularly H. axyridis and therefore represent landscape‐scale refuges for native coccinellid biodiversity.     

The heterogeneity and composition of agricultural landscapes influence native and exotic coccinellids in alfalfa fields

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Changes in carabid beetle diversity within a fragmented agricultural landscape

The distribution of carabid and cicindelid (Coleoptera: Carabidae) beetles in five distinct habitats (riparian, mature orchard, pine windbreak, young orchard, natural veld), within Tambuti Citrus Estate (Swaziland) was examined by pitfall trapping over 18 months. Habitats with high vegetation and litter cover had the highest species diversity and larger specimens, e.g. riparian border and pine windbreak, while the lowest diversity was observed in intensively managed mature citrus orchards. While species such as Tefflus delagorguei Guérin occurred in all the habitats sampled, certain species illustrated habitat specificity; e.g. Dromica ambitiosa Péringuey was observed only in the pine windbreaks while Haplotrachelus sp. Chaudoir occurred mainly in the vegetated riparian and natural veld habitats. Four unidentified carabid beetles were exclusive to the riparian border habitat. This habitat was the only one with a distinct assemblage of species in the agricultural mosaic studied. Multivariate analyses were used to assess the role of soil and environmental variables in relation to the ground beetle diversity within the agricultural mosaic studied.     

Biodiversity Loss following the Introduction of Exotic Competitors: Does Intraguild Predation Explain the Decline of Native Lady Beetles?

Exotic species are widely accepted as a leading cause of biodiversity decline. Lady beetles (Coccinellidae) provide an important model to study how competitor introductions impact native communities since several native coccinellids have experienced declines that coincide with the establishment and spread of exotic coccinellids. This study tested the central hypothesis that intraguild predation by exotic species has caused these declines. Using sentinel egg experiments, we quantified the extent of predation on previously-common (Hippodamia convergens) and common (Coleomegilla maculata) native coccinellid eggs versus exotic coccinellid (Harmonia axyridis) eggs in three habitats: semi-natural grassland, alfalfa, and soybean. Following the experiments quantifying egg predation, we used video surveillance to determine the composition of the predator community attacking the eggs. The extent of predation varied across habitats, and egg species. Native coccinellids often sustained greater egg predation than H. axyridis. We found no evidence that exotic coccinellids consumed coccinellid eggs in the field. Harvestmen and slugs were responsible for the greatest proportion of attacks. This research challenges the widely-accepted hypothesis that intraguild predation by exotic competitors explains the loss of native coccinellids. Although exotic coccinellids may not be a direct competitor, reduced egg predation could indirectly confer a competitive advantage to these species. A lower proportion of H. axyridis eggs removed by predators may have aided its expansion and population increase and could indirectly affect native species via exploitative or apparent competition. These results do not support the intraguild predation hypothesis for native coccinellid decline, but do bring to light the existence of complex interactions between coccinellids and the guild of generalist predators in coccinellid foraging habitats.     

Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective

Coccinellids (ladybird beetles) exhibit considerable diversity in habitat and dietary preference and specificity. This is evident even when comparing species within some coccinellid genera. Resource limitation and competition are suggested as of greatest importance in the evolution of coccinellid habitat preferences. Dietary and habitat specialization has probably occurred in some lineages within broader preferences possessed by generalist ancestors, to avoid the costs associated with migration between habitats and prey switching. Feeding in atypical habitats, on alternative food, when optimal prey are scarce, is likely to have been of great importance in facilitating evolutionary shifts to novel diets and habitats. The broad host ranges of many coccinellid parasitoids and observed interspecific differences in parasitoid prevalence resulting from physiological differences between coccinellid species argue that enemy free space has been of limited importance in habitat and prey shifts in this group. Rapid change may occur in coccinellid foraging patterns, perhaps due to conditioning, and coccinellids may swiftly adapt to new habitats through selection acting on the expression pre-existing traits. Diet, as a determinant of coccinellid migration and gene flow, is likely to affect probable modes of speciation in different coccinellid groups. Parapatric speciation and possibly sympatric speciation are suggested as of possible importance in the genesis of new coccinellid species through prey and habitat shifts.     

Intraguild predation and native lady beetle decline

Coccinellid communities across North America have experienced significant changes in recent decades, with declines in several native species reported. One potential mechanism for these declines is interference competition via intraguild predation; specifically, increased predation of native coccinellid eggs and larvae following the introduction of exotic coccinellids. Our previous studies have shown that agricultural fields in Michigan support a higher diversity and abundance of exotic coccinellids than similar fields in Iowa, and that the landscape surrounding agricultural fields across the north central U.S. influences the abundance and activity of coccinellid species. The goal of this study was to quantify the amount of egg predation experienced by a native coccinellid within Michigan and Iowa soybean fields and explore the influence of local and large-scale landscape structure. Using the native lady beetle Coleomegilla maculata as a model, we found that sentinel egg masses were subject to intense predation within both Michigan and Iowa soybean fields, with 60.7% of egg masses attacked and 43.0% of available eggs consumed within 48 h. In Michigan, the exotic coccinellids Coccinella septempunctata and Harmonia axyridis were the most abundant predators found in soybean fields whereas in Iowa, native species including C. maculata, Hippodamia parenthesis and the soft-winged flower beetle Collops nigriceps dominated the predator community. Predator abundance was greater in soybean fields within diverse landscapes, yet variation in predator numbers did not influence the intensity of egg predation observed. In contrast, the strongest predictor of native coccinellid egg predation was the composition of edge habitats bordering specific fields. Field sites surrounded by semi-natural habitats including forests, restored prairies, old fields, and pasturelands experienced greater egg predation than fields surrounded by other croplands. This study shows that intraguild predation by both native and exotic predators may contribute to native coccinellid decline, and that landscape structure interacts with local predator communities to shape the specific outcomes of predator-predator interactions.     

Community science data suggests that urbanization and forest habitat loss threaten aphidophagous native lady beetles

1. Community scientists have illustrated rapid declines of several aphidophagous lady beetle (Coccinellidae) species. These declines coincide with the establishment of alien coccinellids. We established the Buckeye Lady Beetle Blitz program to measure the seasonal occupancy of coccinellids within gardens across a wide range of landscape contexts. Following the Habitat Compression Hypothesis, we predicted that gardens within agricultural landscapes would be alien‐dominated, whereas captures of natives would be higher within landscapes encompassing a high concentration of natural habitat.
2. Within the state of Ohio, USA, community scientists collected lady beetles for a 7‐day period across 4 years in June and August using yellow sticky card traps. All identifications were verified by professional scientists and beetles were classified by three traits: status (alien or native), mean body length, and primary diet. We compared the relative abundance and diversity of coccinellids seasonally and determined if the distribution of beetles by size, status, and diet was related to landscape features.
3. Alien species dominated the aphidophagous fauna. Native aphidophagous coccinellid abundance was positively correlated with forest habitat while alien species were more common when gardens were embedded within agricultural landscapes. Urbanization was negatively associated with both aphidophagous alien and native coccinellids.
4. Synthesis and Applications: Our census of native coccinellid species within residential gardens—a widespread and understudied habitat—was enabled by volunteers. These data will serve as an important baseline to track future changes within coccinellid communities within this region. We found that native coccinellid species richness and native aphidophagous coccinellid abundance in gardens were positively associated with forest habitat at a landscape scale of 2 km. However, our understanding of when and why (overwintering, summer foraging, or both) forest habitats are important remains unclear. Our findings highlight the need to understand how declining aphidophagous native species utilize forest habitats as a conservation priority.

     

Habitat Specificity and Variation of Coleopteran Assemblages Between Habitats in a Southern African (Swaziland) Agricultural Landscape

Assessment of Coleopteran diversity and abundance was carried out in the lowveld region of Swaziland by pitfall trapping in five distinct habitats. Additionally, the study was to ascertain if any of the families collected illustrated habitat fidelity. 18 coleopteran families, comprising 2903 individuals were collected, with an additional 29 unidentified specimens, totalling 2932 beetles. Numerically, the top five families were the Scarabaeidae (2425), Carabidae (211), Tenebrionidae (149), Nitidulidae (37) and Curculionidae (22). 66.6% of all specimens collected were harboured within the pine windbreak while the lowest number (2.6%) was collected from the mature citrus orchard. The highest proportion (77%) of scarabaeid beetles collected occurred within the pine windbreak. Habitat specificity was illustrated by one family, Meloidae, which was found only in the young orchard. Community analysis was further carried out to ascertain distribution patterns of the dominant coleopteran families. Three scarabaeid species were found only in the pine windbreak while three carabid species occurred only in the indigenous savanna. Significant differences between habitats were observed in the number of beetles collected while no significant differences were observed in terms of the number of families observed in each habitat (p<0.05). Results indicate that conservation of the various habitat patches within the mosaic studied could facilitate conservation of whole communities rather than individual species thus facilitating effective conservation of the agricultural landscape.     

Alkaloids provide evidence of intraguild predation on native coccinellids by <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in the field

Over a period of less than 5 years, Belgium was thoroughly invaded by the multicolored Asian coccinellid, Harmonia axyridis. At the same time, a decline of some native coccinellid species was observed in tree habitats. One hypothesis about the cause of this decline was that it might have been due to intraguild predation (IGP) by H. axyridis. In natural conditions, IGP between coccinellids can be tracked by using defensive compounds. Exogenous alkaloids in H. axyridis were therefore examined by gas chromatography-mass spectrometry (GC–MS), using individuals sampled from lime trees that were also occupied by other species of coccinellids. Harmonia axyridis was the dominant species at all life stages, in terms of both numbers of sites occupied and local abundance. The GC–MS analysis of H. axyridis larvae revealed traces of exogenous alkaloids from 19 of the 20 sites and, in nine of those 19 sites, more than 30% of the larvae analyzed contained exogenous alkaloids. Three alkaloids were detected: adaline from Adalia spp., calvine from Calvia spp. and propyleine from Propylea quatuordecimpunctata. Predation by H. axyridis on two different coccinellid species was also detected in the same larva, reinforcing the status of H. axyridis as a top predator. A generalized linear model indicated that IGP frequency was positively influenced by two variables: the abundance of extraguild and intraguild prey; and the interaction between these two variables. Our results therefore support the hypothesis that IGP by H. axyridis on native coccinellids in tree habitats has led to the decline of several of these species.     

Indigenous Natural Enemies Associated with Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Eastern Spain

The incidence of generalist indigenous natural enemies of the citrus leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera; Gracillariidae), was monitored during three growing seasons at two different orchards located in the major citrus-growing area of Spain. Composition of the parasitoid complex changed during the study period. However, the eulophids Cirrospilus near lyncus Walker and Pnigalio pectinicornis L. were consistently the predominant species. Despite the varying composition of the parasitoid complex, oviposition, host feeding, and predatory preferences of the natural enemies of the CLM clearly centered on third instar larvae. Incidence of beneficial fauna increased as the season progressed, reaching maximal values up to 70% of susceptible leafminers (mature larvae) at the end of the summer. Parasitism was significantly related to relative host density. However, predation showed no relationship to host availability but did so to flushing in one of the orchards. Incidence of indigenous natural enemies of the CLM should not be ignored when planning any introduction of exotic parasitoids, and their conservation should be taken into account when planning any citrus IPM strategy.     

Development and application of molecular gut‐content analysis to detect aphid and coccinellid predation by Harmonia axyridis (Coleoptera: Coccinellidae) in Italy

Despite their positive effect in reducing pest populations, exotic generalist predators sometimes become invasive and contribute to the displacement of indigenous species in the same trophic level. Although laboratory experiments have linked intraguild predation (IGP) to these interactions, field evidence and quantification of IGP are still lacking for most systems. The recent establishment of the exotic Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Italy raises concern about the detrimental effect that the ladybird could have on native coccinellids. Here we assessed, under laboratory conditions, the acceptability and suitability of eggs of 2 native ladybirds, Adalia bipunctata L. and Oenopia conglobata (L.), as prey items for H. axyridis larvae. Then we developed primers for molecular gut‐content analysis to detect predation by H. axyridis on the 2 ladybirds and on the aphid Eucallipterus tiliae L. Species‐specific 16S primers were developed for the 3 species and laboratory feeding trials were conducted to quantify the rate of prey DNA breakdown in the gut of H. axyridis. Moreover, to field evaluate primers, H. axyridis 4th instars (n = 132) were systematically collected from linden trees in northern Italy and screened for the presence of prey DNA. Seventy‐three percent and 7% of field collected H. axyridis were positive for aphid and coccinellid DNA, respectively. Predation upon aphid and A. bipunctata was lower than predicted if density dependent consumption was expected, while predation upon O. conglobata was significantly higher. Here, we provided the first evidence of IGP among feral populations of H. axyridis and indigenous ladybird beetles, occurring in Italy.     

Sources of variability in the transition from extensive to intensive search in coccinellid predators (Homoptera: Coccinellidae)

In an environment structured by habitats, prey patches, and prey, predators such as coccinellids have two movement modes. The extensive search and the intensive search which results from prey capture are adopted for patch localization and exploration, respectively. The variability of changes from extensive search to intensive search was studied in larvae of the aphidophagous coccinellidSemiadalia undecimpunctata to find out their possibility of adaptation to a fluctuating environment. The temporal organization of coccinellid movements appears far more complicated than the generally accepted succession of extensive search, feeding, and intensive search. Their paths are characterized by the presence of time intervals devoted to intensive search before feeding, a highly variable path response after prey consumption (larvae may adopt intensive search immediately, later, or never), and the alternation of time periods devoted to either extensive search or intensive search after prey ingestion. This interindividual variability suggests that coccinellids have the ability to adapt to heterogeneity or short-term changes in environmental conditions, particularly in prey distribution. These results are in favor of the use of these predators in biological control programs.     

Habitat degradation and introduction of exotic plants favor persistence of invasive species and population growth of native polyphagous fruit fly pests in a Northwestern Argentinean mosaic

Expansion of agricultural land is one of the most significant human alterations to the global environment because it entails not only native habitat loss but also introduction of exotic species. These alterations affect habitat structure and arthropod dynamics, such as those among host plants, tephritid fruit flies, and their natural enemies. We compared abundance and dynamics of pest and non-pest tephritids and their natural enemies over a mosaic of habitats differing in structure, diversity and disturbance history on the Sierra de San Javier in Tucuman, Argentina. Our prediction was that conserved habitats would be more resistant to the establishment and spread of invasive tephritid species due in part to a greater abundance of natural enemies, a greater diversity of native species in the same family and trophic level, and a greater wealth of biotic interactions. We further predicted that native species with broad host ranges should be more sensitive to habitat loss yet more competitive in less disturbed habitats than generalist native and exotic species. We found that environmental degradation, and introduction and spread of exotic host plants strongly affected distribution patterns, abundance, and phenology of native and exotic tephritids. Monophagous tephritid species and several specialized parasitoids were more sensitive to habitat loss than polyphagous species and parasitoids exhibiting a wide host range. In contrast, native monophagous species and native parasitoids appeared to exclude the invasive Mediterranean fruit fly from conserved patches of native vegetation. Nevertheless, the Mediterranean fruit fly persisted in uncontested exotic host plants and thrived in highly degradeted urban landscapes.     

Effects of an invading coccinellid on native coccinellids in an agricultural landscape

Seven native coccinellid species inhabited alfalfa, corn, and small grain fields in eastern South Dakota prior to invasion and establishment of Coccinella septempunctata L. Six species occurred in all crops, however, Adalia bipunctata (L.) occurred only in corn. The structure of native coccinellid communities differed significantly for years prior to compared with years after establishment of C. septempunctata in fields of the three agricultural crops. Differences in community structure were accounted for mainly by reduced abundance of two species, C. transversoguttata richardsoni Brown and Adalia bipunctata (L.). Annual abundance of C. transversoguttata richardsoni averaged 20–32 times lower during post-invasion years than in years prior to invasion, depending on crop; while annual abundance of A. bipunctata averaged 20 times lower in corn after invasion. Addition of C. septempunctata to the community did not result in a significant increase in total abundance of coccinellids in the crops. Coccinellid abundance in agricultural crops may be limited by the total abundance of prey or by the availability of other requisites in the landscape as a whole. Therefore, introduction of a new species, while resulting in reductions in native species populations, may not increase total coccinellid abundance, and may therefore have no net effect on biological control of aphid pests.     

Use of Tropical Dry Forests and Agricultural Areas by Neotropical Bird Communities

Agricultural activities represent a global threat to biodiversity, yet little is known about the relative importance of different agricultural land uses in relation to their wildlife communities. We explored bird community structure, diversity, and composition in a landscape dominated by primary tropical dry forest, and in three agricultural systems (i.e., tree orchards, herbaceous cropfields, cattle pastures) to evaluate the way in which birds use different habitats within the landscape. Tropical dry forests had the highest species richness and community evenness, although the bird community in tree orchards was also relatively species rich and even. Cattle pastures had more bird species than cropfields but both habitats were comparatively species poor with low evenness. Our results are related to habitat structure and the spatial location of sites within the landscape matrix. Based on our observations, we recommend including native tree species within agricultural systems and surrounding areas to provide additional resources for birds. Finally, we suggest promoting natural recruitment of native trees and shrubs within cattle pastures to provide suitable habitat for species that use tropical dry forest plants. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Risk assessment of non-target effects caused by releasing two exotic phytoseiid mites in Japan: can an indigenous phytoseiid mite become IG prey?

Two exotic phytoseiid mites, Neoseiulus cucumeris and Amblyseius swirskii, are commercially available in Japan for the control of thrips and other pest insects. As part of a risk assessment of the non-target effects of releasing these two species, we investigated intraguild predation (IGP) between these exotic phytoseiid mites and an indigenous phytoseiid mite Gynaeseius liturivorus, which is promising as an indigenous natural enemy for the control of thrips in Japan. To understand IGP relations between the exotic and indigenous phytoseiid mites after use of the exotic mites for biological control, we investigated IGP between them in the absence of their shared prey. When an IG prey was offered to an IG predator, both exotic and indigenous females consumed the IG prey at all immature stages (egg, larva, protonymph, deutonymph), especially at its larval stages. The propensity for IGP in a no-choice test was measured by the survival time of IG prey corrected using the survival time of thrips offered to the IG predator. There was no significant difference in the propensity for IGP between N. cucumeris and G. liturivorus, but the propensity was significantly higher in A. swirskii than G. liturivorus. The propensity for IGP in a choice test was measured by the prey choice of the IG predator when a conspecific and a heterospecific larva were offered simultaneously as IG prey. Both exotic females consumed the heterospecific larva only. The indigenous female preferentially consumed the heterospecific larva when the heterospecific larva was N. cucumeris, but consumed the conspecific larva when the heterospecific larva was A. swirskii. We concluded that further investigation would be necessary for the exotic mites’ risk assessment, since the propensity for IGP of the two exotic females was similar to or higher than that of the indigenous female in both the no-choice and choice tests.     

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.     

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.