Clarissa R. Mathews

Effect of floral and extrafloral resources on predation of Aphis spiraecola by Harmonia axyridis on Apple

Flowering companion plants and plants producing extrafloral nectar are being proposed to enhance biological control in apple (Malus domestica Borkh.) orchards. This experiment evaluated the impact of floral and extrafloral resources on predation of spirea aphid (Aphis spiraecola Patch) on apple by adult Harmonia axyridis (Pallas) under greenhouse conditions. Predation of spirea aphids was not affected by the presence of flowering buckwheat (Fagopyrum esculentum) as compared with either buckwheat with flowers removed or an uninfested apple shoot. However, there was a significant reduction in predation of spirea aphids on an apple shoot in the presence of a peach shoot with extrafloral nectar glands compared with either a peach shoot of the same cultivar without nectar glands or an uninfested apple shoot. These findings demonstrate that alternative food resources potentially could interfere with rates of biological control and, therefore, need to be carefully evaluated before incorporating in an orchard design. More studies are needed to adequately gauge the net effects of adding floral or extrafloral resources in orchards for conservation biological control.

Conservation Biological Control of Rosy Apple Aphid, Dysaphis plantaginea (Passerini), in Eastern North America

Abstract Because of the potentially serious damage rosy apple aphid, Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), can cause to apple fruit and branch development, prophylactic insecticides are often used for control. If biological control could be relied on, the amount of pesticide applied in orchards could be reduced. This study examined biological control of rosy apple aphid in eastern West Virginia and the potential for enhancement through conservation biological control, in particular, the effect of interplanting extrafloral nectar-bearing peach trees. By 20 d after first bloom, only 2% of fundatrices initially present survived to form colonies based on regression of data from 687 colonies. Exclusion studies showed that many of the early colonies were probably destroyed by predation; the major predator responsible seemed to be adult Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Mortality before apple bloom was most important in controlling rosy apple aphid population growth but by itself is not sufficiently reliable to prevent economic injury. Interplanting of extrafloral nectar-bearing trees did not increase biological control, and interplanting with 50% trees with extrafloral nectar glands reduced biological control. The number of leaf curl colonies in the 50% interplanted orchards was lower than in monoculture orchards, suggesting a preference of alate oviparae for more diverse habitats, supporting the resource concentration hypothesis but not at a level sufficient to prevent injury. Predation and parasitism after the formation of leaf curl colonies was not adequate to control rosy apple aphid populations.

A comparison of conventional and alternative understory management practices for apple production: multi-trophic effects

Modification of the soil for agricultural production is commonly studied as it relates to plant health and productivity, but the implications at other trophic levels are often over-looked. This study addressed the effects of orchard understory management at several trophic levels to understand potential impacts on the whole system. The soil in a newly planted Golden Delicious apple (Malus domestica Bork.) orchard was modified with four treatments: (1) mulch layer of composted poultry manure, (2) mulch layer of synthetic fiber, (3) conventional herbicide, and (4) hand-weeded control. These treatments were evaluated for their impact on edaphic and arboreal arthropods, substrate microclimate and weed growth, and apple tree vigor during the first year of growth (1998). Understory treatment affected edaphic arthropods at three trophic levels: detritivore, herbivore, and predator. Compost mulch significantly increased both edaphic detritivores and predators. Edaphic herbivores were less abundant in plots treated with synthetic mulch. No effect was found for arboreal herbivores, but aphidophagous Aphidoletes aphidimyza (Cecidomyiidae) larvae were more abundant on trees in compost-treated plots. Host-plant growth and leaf quality (% N) were also affected by soil management, with a higher average trunk diameter and lower average leaf nitrogen (%) in compost-treated plots, despite equivalent N-input in all four treatments. Both mulches (compost and synthetic) resulted in lower soil temperatures and higher soil moistures and suppressed weed growth 10-fold better than either conventional herbicide or hand weeding. The results indicate that soil modification affects organisms at several trophic levels, and therefore, could hold important implications for the orchard ecosystem as a whole. Overall, mulching with composted manure benefited the whole orchard system the most and was superior to conventional herbicide as an understory management practice.

Leaf Extrafloral Nectaries Enhance Biological Control of a Key Economic Pest, Grapholita molesta (Lepidoptera: Tortricidae), in Peach (Rosales: Rosaceae)

Abstract Extrafloral nectaries (EFNs) in many plant species produce sugary secretions that commonly attract ants. This research determined the impact of peach (Prunus persica L. Batsch) EFNs on the biological control of the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), a key economic pest in peach orchards, and studied interactions of EFNs and ants. Studies (2002–2005) in peach orchards of the mid-Atlantic United States showed that ‘Lovell’ peach trees with EFNs supported more parasitic Hymenoptera in the spring and increased the parasitism of G. molesta larvae later in the season than those trees without EFNs. Ant exclusion experiments revealed that trees with EFNs harbored fewer G. molesta larvae when ants were permitted access to the tree canopies. Furthermore, the trees with EFNs had ≈90% less fruit injury by G. molesta, indicating that EFNs have a protective role for the fruit as well. The results show that the combined actions of ants and parasitic Hymenoptera confer an EFN-mediated protective effect spanning the whole fruit growing season. When EFNs are present, naturally occurring biological control agents can reduce damage by G. molesta in peach orchards without insecticide inputs. The EFNs are an important host-plant characteristic that should be retained in future peach cultivar selections as a means of enhancing biological control.

Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically <10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.

Identifying a Potential Trap Crop for a Novel Insect Pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Organic Farms.

Abstract The invasive brown marmorated stink bug, Halyomorpha halys, poses significant risk to organic farming systems because they rely on biological control, nonsynthetic inputs, and cultural tactics for pest management. This study evaluated the potential of five crop plants (sorghum, admiral pea, millet, okra, and sunflower) to be used as trap crops under organic production in four mid-Atlantic states. Stink bug (H. halys and endemic species) densities and host plant phenologies were recorded weekly (mid-June through September). Sorghum attracted significantly more H. halys than the other crops evaluated, followed by sunflower and okra. Seasonal average H. halys density was 1.5–4× higher on sorghum than the other crops (P < 0.05), depending on site. Endemic stink bugs were equally attracted to all crops except admiral pea. A significant effect of time was detected (P < 0.0001), with H. halys densities initially higher on sunflower; as the sunflower senesced, sorghum supported significantly higher average H. halys densities. While sunflower and sorghum phenologies differed, these crops together provided a 5-wk attraction period coinciding with peak H. halys activity. The efficacies of pheromone-baited traps, flaming, applying OMRI-approved insecticides (Azera and Venerate), and vacuuming to removing stink bugs were evaluated as a management tactic. Flaming was the most effective treatment against H. halys and endemic stink bugs. Our results suggest that a trap crop composed of sorghum and sunflower may be an effective management tool for the mid-Atlantic stink bug complex, including H. halys. Future research should address the appropriate size and placement of trap crop within the farm.

Interactions between Extrafloral Nectaries, Ants (Hymenoptera: Formicidae), and Other Natural Enemies Affect Biological Control of Grapholita molesta (Lepidoptera: Tortricidae) on Peach (Rosales: Rosaceae)

ABSTRACT Extrafloral nectaries (EFNs) are reported to benefit some plants when ants (Hymenoptera: Formicidae) use their secretions and fend off herbivores, but in some cases resulting competitive interactions may reduce biological control of specific herbivores. This research examined the interactions between ants and other natural enemies associated with the EFNs of peach [Prunus persica (L.) Batcsh] and the implications for biological control of a key pest, the oriental fruit moth [Grapholita molesta (Busck)]. Studies using sentinel G. molesta placed on peach trees (‘Lovell’ cultivar) with EFNs present and absent revealed that several natural enemy groups associated with the EFNs contribute to reductions in G. molesta eggs, larvae, and pupae in peach orchards. Ants on trees with EFNs antagonized the G. molesta egg parasitoid Trichogramma minutum (Riley), but the ants were crucial in reducing G. molesta in both the larval and pupal stages. Overall, individual trees with EFNs experienced higher ant and other (nonant) natural enemy densities and subsequent pest reductions, as compared with trees without EFNs. However, the implications of EFN-natural enemypest interactions to orchard-level biological control will likely depend on local G. molesta population dynamics.

Measuring host plant selection and retention of Halyomorpha halys by a trap crop.

Trap cropping may exploit a pests dispersal and host selection behavior in order to protect a desired crop. Here, we used a combination of visual sampling, immunomarking, and harmonic radar to assess host plant selection and retention time of the highly mobile and invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), as it moves within and between a polyculture trap crop of sorghum and sunflower, and a bell pepper cash crop. Visual sampling demonstrated no significant differences in H. halys densities across crops, whereas dislodging stink bugs to collect for protein analysis revealed ca. 4× more bugs in the trap crop plants than in the peppers. In total 145 H. halys were collected and of these 6% were doubly marked with proteins, demonstrating that minimal movement occurred between the two planting systems. Tracking tagged H. halys with harmonic radar revealed that the trap crop retained adult H. halys within the plots 1.5× longer and reduced their movement by nearly half compared with bugs released in the pepper cash crop. The data suggest the trap crop of sunflower plus sorghum has the potential to attract and arrest the invasive H. halys, demonstrating that trap cropping may operate as an effective management tool.

Comparison of Peach Cultivars for Provision of Extrafloral Nectar Resources to Harmonia axyridis (Coleoptera: Coccinellidae)

Abstract Incorporating nonprey sugar resources into apple orchards is a potential means of enhancing biological control services, but little is known about the impacts of extrafloral nectars on aphidophagous coccinellids. We explored peach Prunus persica (L.) Batsch extrafloral nectar as a supplemental resource for Harmonia axyridis (Pallas), a key aphid predator in the mid-Atlantic United States. Extrafloral nectar quantity, temporal production, and carbohydrate profile were assessed for four peach cultivars in orchard and greenhouse culture. Seasonal densities of H. axyridis visiting extrafloral nectaries were estimated, and the propensity of beetles to feed upon extrafloral nectar was compared by cultivar in the laboratory. We also compared survival of newly eclosed adult pairs that were starved or fed aphids with or without extrafloral nectar. Peach extrafloral nectar contained six carbohydrates, with sucrose dominant for all cultivars, but extrafloral nectar production varied significantly by cultivar and collection date, with ‘Lovell’ yielding higher average seasonal volume than the other cultivars. Harmonia axyridis continuously foraged on peach trees lacking prey, and beetle abundance was positively correlated with the number of leaves actively producing extrafloral nectar. In laboratory assays, newly emerged adult beetles preferentially selected and consumed extrafloral nectar of Lovell peach shoots. Furthermore, when prey were initially unavailable to adult H. axyridis, the beetles were sustained by extrafloral nectar and experienced longer survival compared with beetles without the supplemental resource. Collectively, these results suggest that peach extrafloral nectar is a beneficial resource that could potentially sustain H. axyridis in orchards when prey are scarce.

Compost tea reduces egg hatch and early-stage nymphal development of Halyomorpha halys (Hemiptera: Pentatomidae)

Abstract The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is an invasive pest causing significant agricultural losses in the USA, particularly among USDAcertified organic agricultural operations that are prohibited from using synthetic pesticides. Recent research indicates that for optimal development, nymphs of H. halys require gut microbial symbionts that are acquired from the egg mass. This research investigated the impact of ‘compost teas,’ biologically-active organic matter emulsions that are commonly applied as foliar sprays for pathogen management in organic agriculture, on H. halys during early stages of development. We compared H. halys development after misting egg masses and neonates with reversed osmosis water (control), or with a 50/50 mixture of compost teas derived from poultry manure and mushroom waste. The compost tea treatment significantly affected hatch (%) for egg masses of H. halys that were treated initially within 24–30 h of deposition, resulting in a 13% reduction in hatch, as compared to the control. Furthermore, significant 2-fold increases in mortality were found for 1st and 2nd instars in the compost tea group, as compared to those in the control group. For egg masses initially treated later (i.e., 2–3 days after deposition), the compost tea treatment resulted in a significant 3-fold increase in mortality (%) for 1st instars, compared to the control. These findings suggest that compost tea holds potential for developing an organic management tactic for H. halys and warrant future investigation of potential underlying mechanisms, including antagonistic interactions with microbial gut symbionts and antibiotic compounds that could penetrate the egg chorion.