Omnivore diet composition alters parasite resistance and host condition.

Diet composition modulates animals' ability to resist parasites and recover from stress. Broader diet breadths enable omnivores to mount dynamic responses to parasite attack, but little is known about how plant/prey mixing might influence responses to infection. Using omnivorous deer mice (Peromyscus maniculatus) as a model, we examine how varying plant and prey concentrations in blended diets influence resistance and body condition following infestation by Rocky Mountain wood ticks (Dermacentor andersoni). In two repeated experiments, deer mice fed for 4 weeks on controlled diets that varied in proportions of seeds and insects were then challenged with 50 tick larvae in two sequential infestations. The numbers of ticks successfully feeding on mice declined by 25% and 66% after the first infestation (in the first and second experiments, respectively), reflecting a pattern of acquired resistance, and resistance was strongest when plant/prey ratios were more equally balanced in mouse diets, relative to seed-dominated diets. Diet also dramatically impacted the capacity of mice to cope with tick infestations. Mice fed insect-rich diets lost 15% of their body weight when parasitized by ticks, while mice fed seed-rich diets lost no weight at all. While mounting/maintaining an immune response may be energetically demanding, mice may compensate for parasitism with fat and carbohydrate-rich diets. Altogether, these results suggest that a diverse nutritional landscape may be key in enabling omnivores' resistance and resilience to infection and immune stressors in their environments.

Weeds Impose Unique Outcomes for Pests, Natural Enemies, and Yield in Two Vegetable Crops.

Weed management requires enormous labor investments from vegetable farmers, yet crops vary in how much weed pressure they can tolerate without yield loss. Moreover, until weeds reach a point where they threaten yield or approach seed production, they can increase biodiversity and provision food and habitat to attract predatory insects. In two related field experiments, we quantified impacts of weed presence and diversity on pests, predators, and biocontrol of both weed seeds and insect prey. We also measured yields of two vegetables that vary in competitiveness (eggplants and turnips) across two weed management treatments (weedy and weed-free), to determine productivity costs of tolerating weeds. Allowing weeds to grow adjacent to rows of eggplants increased abundances of predators and reduced pests. Surprisingly, relaxing weed management came at no cost to eggplant yield. In contrast, tolerating weeds in turnips had strong yield costs, and did not benefit predators or decrease pest pressure. On both crops, pests declined as weed diversity increased. Yet, weed treatments had no impact on consumption of weed seeds or sentinel prey by soil-surface insects, which were dominated by red imported fire ants. Our results suggest that highly competitive crops might benefit from stronger natural pest control when weeds are less-aggressively managed. However, herbivores and predators had unique responses to weeds that were crop-specific. To help farmers allocate limited weed management labor resources, future work should examine the relative competitiveness of a wider variety of vegetables over a gradient of weed pressure while measuring corresponding impacts on pest control.

Organic Farming Sharpens Plant Defenses in the Field.

Plants deploy a variety of chemical and physical defenses to protect themselves against herbivores and pathogens. Organic farming seeks to enhance these responses by improving soil quality, ultimately altering bottom up regulation of plant defenses. While laboratory studies suggest this approach is effective, it remains unclear whether organic agriculture encourages more-active plant defenses under real-world conditions. Working on the farms of cooperating growers, we examined gene expression in the leaves of two potato (Solanum tuberosum) varieties, grown on organic vs. conventional farms. For one variety, Norkotah, we found significantly heightened initiation of genes associated with plant-defense pathways in plants grown in organic vs. conventional fields. Organic Norkotah fields exhibited lower levels of nitrate in soil and of nitrogen in plant foliage, alongside differences in communities of soil bacteria, suggesting possible links between soil management and observed differences in plant defenses. Additionally, numbers of predatory and phloem-feeding insects were higher in organic than conventional fields. A second potato variety, Alturas, which is generally grown using fewer inputs and in poorer-quality soils, exhibited lower overall herbivore and predator numbers, few differences in soil ecology, and no differences in gene-activity in organic and conventional farming systems. Altogether, our results suggest that organic farming has the potential to increase plants' resistance to herbivores, possibly facilitating reduced need for insecticide applications. These benefits appear to be mediated by plant variety and/or farming context.

Better Together? Combining Cover Crop Mulches, Organic Herbicides, and Weed Seed Biological Control in Reduced-Tillage Systems.

Organic vegetable farmers rely heavily on labor-intensive tillage for weed management, which adversely affects soil health and harms beneficial insects that consume crop pests and weed seeds. Using cover crop residues as a weed-suppressive mulch enables some reduction in tillage, and combining this tool with recently developed organic herbicides may further enhance weed suppression in vegetable production. However, organic herbicides may also adversely affect beneficial insects, and their nontarget effects are unknown. Here, we examine the combined impacts of cultural and chemical tools on weed cover while monitoring activity of beneficial epigeal insects and measuring rates of weed seed biological control to assess potential nontarget effects of organic herbicides. In a 2-yr experiment, we compared three cover crop mulch treatments and three organic herbicide treatments (capric/caprylic acid, corn gluten meal, and herbicide-free) in a reduced-tillage system. Organic herbicides led to no reductions in beneficial insect activity nor weed seed biocontrol. In both years, capric/caprylic acid herbicide and cover crop mulches reduced weed pressure relative to a fallow control treatment, whereas corn gluten meal had no effect. In year 2, a combination of cover crop mulch with organic herbicide had the greatest weed suppression relative to the fallow control. Integrated weed management is a perpetual challenge, but our results suggest that organic herbicides used in concert with cover crop mulch may enhance weed control and reduce the need for tillage, with limited collateral damage to natural enemies.

Organic Soils Control Beetle Survival While Competitors Limit Aphid Population Growth.

Soil chemistry and microbial diversity can impact the vigor and nutritive qualities of plants, as well as plants' ability to deploy anti-herbivore defenses. Soil qualities often vary dramatically on organic versus conventional farms, reflecting the many differences in soil management practices between these farming systems. We examined soil-mediated effects on herbivore performance by growing potato plants (Solanum tuberosum L.) in soils collected from organic or conventional commercial farm fields, and then exposing these plants to herbivory by green peach aphids (Myzus persicae Sulzer, Hemiptera: Aphididae) and/or Colorado potato beetles (Leptinotarsa decemlineata Say, Coleoptera: Chrysomelidae). Responses of the two potato pests varied dramatically. Survivorship of Colorado potato beetles was almost 3× higher on plants grown in organic than in conventional soils, but was unaffected by the presence of aphids. In contrast, aphid colony growth was twice as rapid when aphids were reared alone rather than with Colorado potato beetles, but was unaffected by soil type. We saw no obvious differences in soil nutrients when comparing organic and conventional soils. However, we saw a higher diversity of bacteria in organic soils, and potato plants grown in this soil had a lower carbon concentration in foliar tissue. In summary, the herbivore species differed in their susceptibility to soil- versus competitor-mediated effects, and these differences may be driven by microbe-mediated changes in host plant quality. Our results suggest that soil-mediated effects on pest growth can depend on herbivore species and community composition, and that soil management strategies that promote plant health may also increase host quality for pests.

Bacteria and Competing Herbivores Weaken Top-Down and Bottom-Up Aphid Suppression.

Herbivore suppression is mediated by both plant defenses and predators. In turn, plant defenses are impacted by soil fertility and interactions with soil bacteria. Measuring the relative importance of nutritional and microbial drivers of herbivore resistance has proven problematic, in part because it is difficult to manipulate soil-bacterial community composition. Here, we exploit variation in soil fertility and microbial biodiversity across 20 farms to untangle suppression of aphids (Brevicoryne brassicae) through bottom-up and top-down channels. We planted Brassica oleracea plants in soil from each farm, manipulated single and dual infestations of aphids alone or with caterpillars (Pieris rapae), and exposed aphids to parasitoid wasps (Diaeretiella rapae) in the open field. We then used multi-model inference to identify the strongest soil-based predictors of herbivore growth and parasitism. We found that densities of Bacillus spp., a genus known to include plant-growth-promoting rhizobacteria, negatively correlated with aphid suppression by specialist parasitoids. Aphid parasitism also was disrupted on plants that had caterpillar damage, compared to plants attacked only by aphids. Relative abundance of Pseudomonas spp. bacteria correlated with higher aphid growth, although this appeared to be a direct effect, as aphid parasitism was not associated with this group of bacteria. Non-pathogenic soil bacteria are often shown to deliver benefits to plants, improving plant nutrition and the deployment of anti-herbivore defenses. However, our results suggest that these plant growth-promoting bacteria may also indirectly weaken top-down aphid suppression by parasitoids and directly improve aphid performance. Against a background of varying soil fertility, microbial biodiversity, competing herbivores, and natural enemies, we found that effects of non-pathogenic soil microbes on aphid growth outweighed those of nutritional factors. Therefore, predictions about the strength of plant defenses along resource gradients must be expanded to include microbial associates.

Dual-guild herbivory disrupts predator-prey interactions in the field.

Plant defenses often mediate whether competing chewing and sucking herbivores indirectly benefit or harm one another. Dual-guild herbivory also can muddle plant signals used by specialist natural enemies to locate prey, further complicating the net impact of herbivore-herbivore interactions in naturally diverse settings. While dual-guild herbivore communities are common in nature, consequences for top-down processes are unclear, as chemically mediated tri-trophic interactions are rarely evaluated in field environments. Combining observational and experimental approaches in the open field, we test a prediction that chewing herbivores interfere with top-down suppression of phloem feeders on Brassica oleracea across broad landscapes. In a two-year survey of 52 working farm sites, we found that parasitoid and aphid densities on broccoli plants positively correlated at farms where aphids and caterpillars rarely co-occurred, but this relationship disappeared at farms where caterpillars commonly co-occurred. In a follow-up experiment, we compared single and dual-guild herbivore communities at four local farm sites and found that caterpillars (P. rapae) caused a 30% reduction in aphid parasitism (primarily by Diaeretiella rapae), and increased aphid colony (Brevicoryne brassicae) growth at some sites. Notably, in the absence of predators, caterpillars indirectly suppressed, rather than enhanced, aphid growth. Amid considerable ecological noise, our study reveals a pattern of apparent commensalism: herbivore-herbivore facilitation via relaxed top-down suppression. This work suggests that enemy-mediated apparent commensalism may override constraints to growth induced by competing herbivores in field environments, and emphasizes the value of placing chemically mediated interactions within their broader environmental and community contexts.

Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels.

Non-consumptive effects (NCEs) of predators are ubiquitous in food webs with well-detailed impacts on trophic cascades over multiple levels. However, integrating NCEs with other predator-mediated interactions, like intraguild predation, as well as context-specific habitat factors that shape top-down pressure, remains a challenge. Focusing on two common seed predators, mice (Peromyscus spp.) and carabid beetles (Coleoptera: Carabidae), we quantify trophic and behavioral consequences of predation risk and availability of refuge vegetation on both intraguild predators (mice) and intraguild prey (beetles). In a 2-year field experiment, we manipulated refuge habitat (red clover), small mammal access, and moonlight, which small mammals use as an indirect cue of predation risk. We found that avoidance of predation risk by mice in simulated moonlight reduced carabid activity density in vegetation by up to 50% compared to exposed habitat, but had no cascading effects on seed predation. We linked patterns observed in the field with behavioral mechanisms by observing beetle foraging activity, and found that exposure to both indirect and direct vertebrate predator cues reduced movement by 50%, consistent with predator-mediated activity reductions observed in the field. However, predation risk increased carabid seed consumption by 43%. Thus, weak effects of predation risk on seed removal in the field may be explained by overcompensatory seed feeding by beetles. This work demonstrates that predators elicit responses that cascade over multiple trophic levels, triggering behavioral changes in species lower on the food chain. These behavior-mediated cascades are controlled by their spatiotemporal context and have important downstream impacts on predator-prey dynamics.

Ground beetle (Coleoptera: Carabidae) phenology, diversity, and response to weed cover in a turfgrass ecosystem.

Despite being fragmented and highly disturbed habitats, urban turfgrass ecosystems harbor a surprising diversity of arthropods. The suitability of turf as arthropod habitat, however, likely depends on the extent and types of pesticides and fertilizers used. For example, moderate levels of weed cover in low-input lawns may provide alternative food resources. We conducted a 2-yr field study to: 1) characterize the ground beetle (Carabidae) species assemblage in turfgrass, and 2) assess the direct and indirect effects of lawn management on carabid communities. Weed cover and beetle activity were compared among four lawn management programs: 1) consumer/garden center, 2) integrated pest management (IPM), 3) natural organic, and 4) no-input control. Nearly 5,000 carabid beetles across 17 species were collected with the predator Cyclotrachelus sodalis LeConte numerically dominating the trap catch (87% and 45% of individuals in 2005 and 2006, respectively). Populations of C. sodalis underwent a distinct peak in activity during the third week of June, whereas omnivorous and granivorous species tended to occur at far lower levels and were less variable over the season. We found no evidence for direct effects of lawn management on carabid species diversity; however, we detected an indirect effect mediated by variation in weed cover. Seed-feeding species were positively correlated with turf weeds early in 2006, whereas strictly predaceous species were not. Thus, turf management programs that lead to changes in plant species composition (i.e., herbicide regimes) may indirectly shape epigeal arthropod communities more strongly than the direct effects of insecticide use.