Ruth Hazzard

Herbivory reduces plant interactions with above- and belowground antagonists and mutualists

Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.

Using trap crops for control of Acalymma vittatum (Coleoptera: Chrysomelidae) reduces insecticide use in butternut squash.

ABSTRACT Striped cucumber beetle, Acalymma vittatum F., is the primary insect pest of cucurbit crops in the northeastern United States. Adult beetles colonize squash crops from field borders, causing feeding damage at the seedling stage and transmitting bacterial wilt Erwinia tracheiphila Hauben et al. 1999. Conventional control methods rely on insecticide applications to the entire field, but surrounding main crops with a more attractive perimeter could reduce reliance on insecticides. A. vittatum shows a marked preference for Blue Hubbard squash (Cucurbita maxima Duchesne) over butternut squash (C. moschata Poir). Given this preference, Blue Hubbard squash has the potential to be an effective perimeter trap crop. We evaluated this system in commercial butternut fields in 2003 and 2004, comparing fields using perimeter trap cropping with Blue Hubbard to conventionally managed fields. In 2003, we used a foliar insecticide to control beetles in the trap crop borders, and in 2004, we compared systemic and foliar insecticide treatments for the trap crop borders. We found that using a trap crop system reduced or eliminated the need to spray the main crop area, reducing insecticide use by up to 94% compared with conventional control methods, with no increase in herbivory or beetle numbers. We surveyed the growers who participated in these experiments and found a high level of satisfaction with the effectiveness and simplicity of the system. These results suggest that this method of pest control is both effective and simple enough in its implementation to have high potential for adoption among growers.

Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem.

Plants interact with a variety of other community members that have the potential to indirectly influence each other through a shared host plant. Arbuscular mycorrhizal fungi (AMF) are generally considered plant mutualists because of their generally positive effects on plant nutrient status and growth. AMF may also have important indirect effects on plants by altering interactions with other community members. By influencing plant traits, AMF can modify aboveground interactions with both mutualists, such as pollinators, and antagonists, such as herbivores. Because herbivory and pollination can dramatically influence plant fitness, comprehensive assessment of plant–AMF interactions should include these indirect effects. To determine how AMF affect plant–insect interactions, we grew Cucumis sativus (Cucurbitaceae) under five AMF inoculum treatments and control. We measured plant growth, floral production, flower size, and foliar nutrient content of half the plants, and transferred the other half to a field setting to measure pollinator and herbivore preference of wild insects. Mycorrhizal treatment had no effect on plant biomass or floral traits but significantly affected leaf nutrients, pollinator behavior, and herbivore attack. Although total pollinator visitation did not vary with AMF treatment, pollinators exhibited taxon-specific responses, with honey bees, bumble bees, and Lepidoptera all responding differently to AMF treatments. Flower number and size were unaffected by treatments, suggesting that differences in pollinator preference were driven by other floral traits. Mycorrhizae influenced leaf K and Na, but these differences in leaf nutrients did not correspond to variation in herbivore attack. Overall, we found that AMF indirectly influence both antagonistic and mutualistic insects, but impacts depend on the identity of both the fungal partner and the interacting insect, underscoring the context-dependency of plant–AMF interactions.

Comparison of Perimeter Trap Crop Varieties: Effects on Herbivory, Pollination, and Yield in Butternut Squash

ABSTRACT Perimeter trap cropping (PTC) is a method of integrated pest management (IPM) in which the main crop is surrounded with a perimeter trap crop that is more attractive to pests. Blue Hubbard (Cucurbita maxima Duch.) is a highly effective trap crop for butternut squash (C. moschata Duch. ex Poir) attacked by striped cucumber beetles (Acalymma vittatum Fabricius), but its limited marketability may reduce adoption of PTC by growers. Research comparing border crop varieties is necessary to provide options for growers. Furthermore, pollinators are critical for cucurbit yield, and the effect of PTC on pollination to main crops is unknown. We examined the effect of five border treatments on herbivory, pollination, and yield in butternut squash and manipulated herbivory and pollination to compare their importance for main crop yield. Blue Hubbard, buttercup squash (C. maxima Duch.), and zucchini (C. pepo L.) were equally attractive to cucumber beetles. Border treatments did not affect butternut leaf damage, but butternut flowers had the fewest beetles when surrounded by Blue Hubbard or buttercup squash. Yield was highest in the Blue Hubbard and buttercup treatments, but this effect was not statistically significant. Native bees accounted for 87% of pollinator visits, and pollination did not limit yield. There was no evidence that border crops competed with the main crop for pollinators. Our results suggest that both buttercup squash and zucchini may be viable alternatives to Blue Hubbard as borders for the main crop of butternut squash. Thus, growers may have multiple border options that reduce pesticide use, effectively manage pests, and do not disturb mutualist interactions with pollinators.

Linking agricultural practices, mycorrhizal fungi, and traits mediating plant-insect interactions

Agricultural management has profound effects on soil communities. Activities such as fertilizer inputs can modify the composition of arbuscular mycorrhizal fungi (AMF) communities, which form important symbioses with the roots of most crop plants. Intensive conventional agricultural management may select for less mutualistic AMF with reduced benefits to host plants compared to organic management, but these differences are poorly understood. AMF are generally evaluated based on their direct growth effects on plants. However, mycorrhizal colonization also may alter plant traits such as tissue nutrients, defensive chemistry, or floral traits, which mediate important plant-insect interactions like herbivory and pollination. To determine the effect of AMF from different farming practices on plant performance and traits that putatively mediate species interactions, we performed a greenhouse study by inoculating Cucumis sativus (cucumber, Cucurbitaceae) with AMF from conventional farms, organic farms, and a commercial AMF inoculum. We measured growth and a suite of plant traits hypothesized to be important predictors of herbivore resistance and pollinator attraction. Several leaf and root traits and flower production were significantly affected by AMF inoculum. Both conventional and organic AMF reduced leaf P content but increased Na content compared to control and commercial AMF. Leaf defenses were unaffected by AMF treatments, but conventional AMF increased root cucurbitacin C, the primary defensive chemical of C. sativus, compared to organic AMF. These effects may have important consequences for herbivore preference and population dynamics. AMF from both organic and conventional farms decreased flower production relative to commercial and control treatments, which may reduce pollinator attraction and plant reproduction. AMF from both farm types also reduced seed germination, but effects on plant growth were limited. Our results suggest that studies only considering AMF effects on growth may overlook changes in plant traits that have the potential to influence interactions, and hence yield, on farms. Given the effects of AMF on plant traits documented here, and the great importance of both herbivores and pollinators to wild and cultivated plants, we advocate for comprehensive assessments of mycorrhizal effects in complex community contexts, with the aim of incorporating multispecies interactions both above and below the soil surface.

Buttercup Squash Provides a Marketable Alternative to Blue Hubbard as a Trap Crop for Control of Striped Cucumber Beetles (Coleoptera: Chrysomelidae)

ABSTRACT Winter squash is a vital agricultural commodity worldwide. In the Northeastern United States, the primary insect pest is the striped cucumber beetle, Acalymma vittatum F. Using a Blue Hubbard squash (Cucurbita maxima Duchesne) perimeter trap crop system can reduce insecticide use by >90% in butternut squash (C. moschata Poir), the primary winter squash grown in this region. Despite the savings in insecticide costs, growers may be reluctant to give up field space for a perimeter crop of Blue Hubbard squash, which comprises only 5% of the winter squash market in New England as compared with 19% for buttercup squash. Finding a more marketable trap crop would lower the barrier for adoption of this system. We tested eight varieties of three species of cucurbits for attractiveness to beetles relative to Blue Hubbard and butternut squash, and chose buttercup squash as the most promising replacement. We compared the effect of a buttercup border, Blue Hubbard border, or control (no border) on beetle numbers, herbivory, insecticide use, pollination, and pollen limitation in the main crop. We found that buttercup squash performed equally well as Blue Hubbard as a trap crop, with 97% reduction in total insecticide use compared with control fields. Honey bees (Apis mellifera L.) and squash bees (Peponapis pruinosa Say) were the predominant pollinators, and border treatments did not affect visitation. Hand pollination did not increase reproduction or yield, indicating that natural pollination was sufficient for full yield. This study confirms the effectiveness of perimeter trap crop systems and offers growers a more marketable trap crop for managing cucumber beetle damage.

Root herbivory indirectly affects above‐ and below‐ground community members and directly reduces plant performance

There is a widespread recognition that above- and below-ground organisms are linked through their interactions with host plants that span terrestrial subsystems. In addition to direct effects on plants, soil organisms such as root herbivores can indirectly alter interactions between plants and other community members, with potentially important effects on plant growth and fitness. We manipulated root herbivory by Acalymma vittatum in Cucumis sativus to determine indirect effects on arbuscular mycorrhizal fungi, leaf herbivory, the leaf pathogen downy mildew and pollinators. We also manipulated pollen receipt by plants to determine whether root herbivory reduced plant reproduction through changes in pollinator visitation. Overall, root herbivory had strong net negative effects on plant growth and fitness, with 34% reductions in both leaf and fruit production by high root damage levels relative to control, despite reduced infection by downy mildew. High root herbivory also reduced floral visitation by 39%, apparently due to lower flower production, as flower size and scent were unaffected. Above-ground herbivory was not affected by root herbivores. Although root herbivory reduced pollinator visits, pollen receipt manipulations had no effect on fruit set, indicating that reduced pollinator service did not affect plant reproduction. Synthesis. Root herbivory had indirect effects on a range of community members, including mutualists and antagonists both above- and below-ground. Although reduced pathogen infection associated with root herbivory would be expected to benefit plants, root herbivory had an overall strong negative effect on plant growth and reproduction, indicating that direct negative effects over-rode any potential indirect benefits. Soil organisms such as root herbivores can indirectly alter interactions between plants and other community members. Here, root damage had indirect effects on a range of community members, including mutualists and antagonists both above- and below-ground. However, direct negative effects of root herbivory were more important for reducing plant growth and fitness.

Attracting mutualists and antagonists: Plant trait variation explains the distribution of specialist floral herbivores and pollinators on crops and wild gourds

UNLABELLED • PREMISE OF THE STUDY Floral traits play important roles in pollinator attraction and defense against floral herbivory. However, plants may experience trade-offs between conspicuousness to pollinators and herbivore attraction. Comparative studies provide an excellent framework to examine the role of multiple traits shaping mutualist and antagonist interactions.• METHODS To assess whether putative defensive and attractive traits predict species interactions, we grew 20 different Cucurbitaceae species and varieties in the field to measure interactions with pollinators and herbivores and in the greenhouse to assess trait variation. Cucurbits are characterized by the production of cucurbitacins, bitter nonvolatile terpenoids that are effective against generalist herbivores but can attract specialist beetles. We determined whether plant traits such as cucurbitacins predict herbivore resistance and pollinator attraction using an information-theoretic approach.• KEY RESULTS Mutualists and floral antagonists were attracted to the same cucurbit varieties once they flowered. However, rather than cucurbitacin concentration, we found that the size of the flower and volatile emissions of floral sesquiterpenoids explained both pollinator and floral herbivore visitation preference across cucurbit taxa. This pattern held across cucurbit taxa and within the Cucurbita genus.• CONCLUSIONS Surprisingly, floral sesquiterpenoid volatiles, which are associated with direct defense, indirect defense, and attraction, rather than defense traits such as cucurbitacins, appeared to drive interactions with both pollinators and floral herbivores across cucurbit taxa. Identifying the relevant plant traits for attraction and deterrence is important in this economically valuable crop, particularly if pollinators and floral herbivores use the same plant traits as cues.

Overwintering and seasonal patterns of feeding and reproduction in Phyllotreta cruciferae (Coleoptera: Chrysomelidae) in the Northeastern United States

Abstract The life history of the agricultural pest Phyllotreta cruciferae (Goeze), including location of overwintering sites, time of spring emergence, reproductive phenology, and seasonal changes in feeding and responsiveness to yellow sticky traps, was studied in the northeastern United States from 2001 to 2003 to provide growers with information to improve their management of flea beetle populations in Brassica crops. Samples of leaf litter, organic debris, and soil were collected from a variety of vegetation types to determine the location of flea beetle overwintering sites surrounding agricultural fields. Significantly more P. cruciferae were found in the leaf litter beneath shrubs and brush or in wooded areas than in grass, within-field debris, or in soil samples taken within each vegetation type. Weekly dissections of field-collected female beetles suggested the occurrence of a partial second generation by P. cruciferae in 2003. In laboratory assays of beetles collected weekly from Brassica fields in Massachusetts, both adult beetle feeding on Brassica foliage and beetle responsiveness to yellow sticky traps shows two peaks (June and August) that corresponded to the first and second generations. Beetle catch on yellow sticky traps was highly correlated (2002: R2 = 0.8; 2003: R2 = 0.6) with the mean number of feeding holes on injured plants.