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.

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.

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.

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.

Buttercup squash provides a marketable alternative to blue hubbard as a trap crop for control of striped cucumber beetles (Coleoptera: Chrysomelidae).

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.

Potential of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) for biological control of European corn borer (Lepidoptera: Crambidae) in solanaceous crops.

We assessed the ability of Trichogramma ostriniae (Peng & Chen) to locate and parasitize Ostrinia nubilalis (Hübner) eggs in crops other than corn, and we evaluated the efficacy of inundative releases of the parasitoid in two solanaceous crops, pepper and potato. Despite a greater plant surface area to search, parasitism of O. nubilalis eggs was consistently higher in sweet corn than dicotyledonous crops such as pepper, snap bean, broccoli, potato, and melon, in choice and no-choice experiments. Nonetheless, in 2002 and 2003, we made four to five separate inundative releases of approximately 30,000-50,000 T. ostriniae per 0.02 ha in nine pepper fields in Virginia, Pennsylvania, and Massachusetts and compared O. nubilalis egg parasitization and fruit damage in those plots with spatially isolated nonrelease plots. Egg parasitization averaged 48.7% in T. ostriniae release plots, which was significantly higher than in nonrelease plots (1.9%). Also, cumulative pepper fruit damage averaged 8.7% in release plots, which was significantly less than in nonrelease plots (27.3%). In potatoes in 2002 and 2003, we made two releases of approximately 75,000 T. ostriniae per 0.2 ha in nine fields in Maine and Virginia and compared O. nubilalis damage in those plots with that in nonrelease plots. T. ostriniae releases significantly reduced the number of tunnel holes and number of O. nubilalis larvae in potato stems. We conclude that this parasitoid has great potential as a biocontrol agent for O. nubilalis in solanaceous crops.

Validation of a Commercial System for Remote Estimation of Wetness Duration.

To assess the accuracy of remote, real-time mathematical simulations of wetness duration and air temperature, hourly measurements of wetness duration and air temperature at 18 sites in the United States and Canada from May to September 1995 were compared with simulations for these sites provided by SkyBit, Inc. SkyBit simulations of mean, maximum, and minimum daily air temperatures varied from on-site measurements by less than 0.7°C but underestimated the duration of wet periods by an average of 3.4 h/day. At five of six stations tested, SkyBit underestimates of wetness duration were significantly (P < 0.01) larger on days when no rain was measured than on rainy days, indicating that simulations of dew-period duration were much less accurate than simulations of rain-period duration. The vast majority of hours SkyBit misclassified as dry occurred either when entire wet periods were missed (59.3%) or when the onset of a wet period was detected late (28.4%). The results suggest that revision of SkyBit wetness-simulation models should focus on reducing error rates during dew events. In simulations using two disease-warning models, TOM-CAST and Melcast, with mean values of measured and SkyBit-simulated wetness duration, SkyBit-simulated values resulted in fewer and later fungicide spray advisories than did measured values. The magnitude of these impacts varied with the magnitude of the simulation errors and with differences in the models' decision rules.