A trait-based framework for predicting foodborne pathogen risk from wild birds.

Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from farms, jeopardizing conservation efforts. However, it remains unclear which species, particularly birds, pose the greatest risk to food safety. Using >11,000 pathogen tests and 1565 bird surveys covering 139 bird species from across the western United States, we examined the importance of 11 traits in mediating wild bird risk to food safety. We tested whether traits associated with pathogen exposure (e.g., habitat associations, movement, and foraging strategy) and pace-of-life (clutch size and generation length) mediated foodborne pathogen prevalence and proclivities to enter farm fields and defecate on crops. Campylobacter spp. were the most prevalent enteric pathogen (8.0%), while Salmonella and Shiga-toxin producing Escherichia coli (STEC) were rare (0.46% and 0.22% prevalence, respectively). We found that several traits related to pathogen exposure predicted pathogen prevalence. Specifically, Campylobacter and STEC-associated virulence genes were more often detected in species associated with cattle feedlots and bird feeders, respectively. Campylobacter was also more prevalent in species that consumed plants and had longer generation lengths. We found that species associated with feedlots were more likely to enter fields and defecate on crops. Our results indicated that canopy-foraging insectivores were less likely to deposit foodborne pathogens on crops, suggesting growers may be able to promote pest-eating birds and birds of conservation concern (e.g., via nest boxes) without necessarily compromising food safety. As such, promoting insectivorous birds may represent a win-win-win for bird conservation, crop production, and food safety. Collectively, our results suggest that separating crop production from livestock farming may be the best way to lower food safety risks from birds. More broadly, our trait-based framework suggests a path forward for co-managing wildlife conservation and food safety risks in farmlands by providing a strategy for holistically evaluating the food safety risks of wild animals, including under-studied species.

Alternative prey and farming system mediate predation of Colorado potato beetles by generalists.

BACKGROUND: Biological control by generalist predators can be mediated by the abundance and biodiversity of alternative prey. When alternative prey draw predator attacks away from the control target, they can weaken pest suppression. In other cases, a diverse prey base can promote predator abundance and biodiversity, reduce predator-predator interference, and benefit biocontrol. Here, we used molecular gut-content analysis to assess how community composition altered predation of Colorado potato beetle (Leptinotarsa decemlineata (Say)) by Nabis sp. and Geocoris sp. Predators were collected from organic or conventional potato (Solanum tuberosum L.) fields, encouraging differences in arthropod community composition. RESULTS: In organic fields, Nabis predation of potato beetles decreased with increasing arthropod richness and predator abundance. This is consistent with Nabis predators switching to other prey species when available and with growing predator-predator interference. In conventional fields these patterns were reversed, however, with potato beetle predation by Nabis increasing with greater arthropod richness and predator abundance. For Geocoris, Colorado potato beetle predation was more frequent in organic than in conventional fields. However, Geocoris predation of beetles was less frequent in fields with higher abundance of the detritus-feeding fly Scaptomyza pallida Zetterstedt, or of all arthropods, consistent with predators choosing other prey when available. CONCLUSION: Alternative prey generally dampened predation of potato beetles, suggesting these pests were less-preferred prey. Nabis and Geocoris differed in which alternative prey were most disruptive to feeding on potato beetles, and in the effects of farm management on predation, consistent with the two predator species occupying complementary feeding niches. © 2021 Society of Chemical Industry.

Selection for high levels of resistance to double-stranded RNA (dsRNA) in Colorado potato beetle (Leptinotarsa decemlineata Say) using non-transgenic foliar delivery.

Insecticidal double-stranded RNAs (dsRNAs) silence expression of vital genes by activating the RNA interference (RNAi) mechanism in insect cells. Despite high commercial interest in insecticidal dsRNA, information on resistance to dsRNA is scarce, particularly for dsRNA products with non-transgenic delivery (ex. foliar/topical application) nearing regulatory review. We report the development of the CEAS 300 population of Colorado potato beetle (Leptinotarsa decemlineata Say) (Coleoptera: Chrysomelidae) with > 11,100-fold resistance to a dsRNA targeting the V-ATPase subunit A gene after nine episodes of selection using non-transgenic delivery by foliar coating. Resistance was associated with lack of target gene down-regulation in CEAS 300 larvae and cross-resistance to another dsRNA target (COPI ß; Coatomer subunit beta). In contrast, CEAS 300 larvae showed very low (~ 4-fold) reduced susceptibility to the Cry3Aa insecticidal protein from Bacillus thuringiensis. Resistance to dsRNA in CEAS 300 is transmitted as an autosomal recessive trait and is polygenic. These data represent the first documented case of resistance in an insect pest with high pesticide resistance potential using dsRNA delivered through non-transgenic techniques. Information on the genetics of resistance and availability of dsRNA-resistant L. decemlineata guide the design of resistance management tools and allow research to identify resistance alleles and estimate resistance risks.

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.

Using NextRAD sequencing to infer movement of herbivores among host plants.

Herbivores often move among spatially interspersed host plants, tracking high-quality resources through space and time. This dispersal is of particular interest for vectors of plant pathogens. Existing molecular tools to track such movement have yielded important insights, but often provide insufficient genetic resolution to infer spread at finer spatiotemporal scales. Here, we explore the use of Nextera-tagmented reductively-amplified DNA (NextRAD) sequencing to infer movement of a highly-mobile winged insect, the potato psyllid (Bactericera cockerelli), among host plants. The psyllid vectors the pathogen that causes zebra chip disease in potato (Solanum tuberosum), but understanding and managing the spread of this pathogen is limited by uncertainty about the insect's host plant(s) outside of the growing season. We identified 1,978 polymorphic loci among psyllids separated spatiotemporally on potato or in patches of bittersweet nightshade (S. dulcumara), a weedy plant proposed to be the source of potato-colonizing psyllids. A subset of the psyllids on potato exhibited genetic similarity to insects on nightshade, consistent with regular movement between these two host plants. However, a second subset of potato-collected psyllids was genetically distinct from those collected on bittersweet nightshade; this suggests that a currently unrecognized source, i.e., other nightshade patches or a third host-plant species, could be contributing to psyllid populations in potato. Oftentimes, dispersal of vectors of pathogens must be tracked at a fine scale in order to understand, predict, and manage disease spread. We demonstrate that emerging sequencing technologies that detect genome-wide SNPs of a vector can be used to infer such localized movement.

Responses of Aphid Vectors of Potato leaf roll virus to Potato Varieties.

Potato leaf roll virus (PLRV) can reduce tuber yield and quality in potato. Green peach aphid (Myzus persicae [Sulzer]) and potato aphid (Macrosiphum euphorbiae [Thomas]) are the two most important potato-colonizing PLRV vectors in the Pacific Northwest. We compared My. persicae and Ma. euphorbiae densities and PLRV incidences among potato varieties in the field to clarify the relationships between aphid abundance and PLRV incidence in plants. Aphids were sampled weekly over three years in the potato varieties Russet Burbank, Ranger Russet, and Russet Norkotah in a replicated field trial. In all years, My. persicae was more abundant than Ma. euphorbiae, representing at least 97% of samples. My. persicae densities did not differ among potato varieties across years; very low numbers of Ma. euphorbiae precluded such statistical comparisons for this species. PLRV infection did not differ significantly among potato varieties, although the percent of PLRV-infected plants differed among years when all varieties were combined (46% in 2013, 29% in 2011, 13% in 2012). For Ranger Russet and Russet Norkotah, PLRV incidence was positively correlated with aphid abundance as well as proportion of PLRV-positive aphids. In Russet Burbank, only aphid abundance was positively correlated with PLRV infection. Our results suggest that the three most commonly grown potato varieties in our region do not differ in their susceptibility to PLRV infection, and that aphid density was a consistent indicator of the risk of infection by this virus across varieties. Both of these findings can be used to hone PLRV monitoring and modeling efforts.

The Red Queen in a potato field: integrated pest management versus chemical dependency in Colorado potato beetle control.

Originally designed to reconcile insecticide applications with biological control, the concept of integrated pest management (IPM) developed into the systems-based judicious and coordinated use of multiple control techniques aimed at reducing pest damage to economically tolerable levels. Chemical control, with scheduled treatments, was the starting point for most management systems in the 1950s. Although chemical control is philosophically compatible with IPM practices as a whole, reduction in pesticide use has been historically one of the main goals of IPM practitioners. In the absence of IPM, excessive reliance on pesticides has led to repeated control failures due to the evolution of resistance by pest populations. This creates the need for constant replacement of failed chemicals with new compounds, known as the 'insecticide treadmill'. In evolutionary biology, a similar phenomenon is known as the Red Queen principle - continuing change is needed for a population to persevere because its competitors undergo constant evolutionary adaptation. The Colorado potato beetle, Leptinotarsa decemlineata (Say), is an insect defoliator of potatoes that is notorious for its ability to develop insecticide resistance. In the present article, a review is given of four case studies from across the United States to demonstrate the importance of using IPM for sustainable management of a highly adaptable insect pest. Excessive reliance on often indiscriminate insecticide applications and inadequate use of alternative control methods, such as crop rotation, appear to expedite evolution of insecticide resistance in its populations. Resistance to IPM would involve synchronized adaptations to multiple unfavorable factors, requiring statistically unlikely genetic changes. Therefore, integrating different techniques is likely to reduce the need for constant replacement of failed chemicals with new ones.

Organic agriculture promotes evenness and natural pest control.

Human activity can degrade ecosystem function by reducing species number (richness) and by skewing the relative abundance of species (evenness). Conservation efforts often focus on restoring or maintaining species number, reflecting the well-known impacts of richness on many ecological processes. In contrast, the ecological effects of disrupted evenness have received far less attention, and developing strategies for restoring evenness remains a conceptual challenge. In farmlands, agricultural pest-management practices often lead to altered food web structure and communities dominated by a few common species, which together contribute to pest outbreaks. Here we show that organic farming methods mitigate this ecological damage by promoting evenness among natural enemies. In field enclosures, very even communities of predator and pathogen biological control agents, typical of organic farms, exerted the strongest pest control and yielded the largest plants. In contrast, pest densities were high and plant biomass was low when enemy evenness was disrupted, as is typical under conventional management. Our results were independent of the numerically dominant predator or pathogen species, and so resulted from evenness itself. Moreover, evenness effects among natural enemy groups were independent and complementary. Our results strengthen the argument that rejuvenation of ecosystem function requires restoration of species evenness, rather than just richness. Organic farming potentially offers a means of returning functional evenness to ecosystems.

Increasing enemy biodiversity strengthens herbivore suppression on two plant species.

Concern over biodiversity loss, especially at higher trophic levels, has led to a surge in studies investigating how changes in natural enemy diversity affect community and ecosystem functioning. These studies have found that increasing enemy diversity can strengthen, weaken, and not affect prey suppression, demonstrating that multi-enemy effects on prey are context-dependent. Here we ask how one factor, plant species identity, influences multi-enemy effects on prey. We focused on two plant species of agricultural importance, potato (Solanum tuberosum), and collards (Brassica oleracea L.). These species share a common herbivorous pest, the green peach aphid (Myzus persicae), but vary in structural and chemical traits that affect aphid reproductive rates and which may also influence inter-enemy interactions. In a large-scale field experiment, overall prey exploitation varied dramatically among the plant species, with enemies reducing aphid populations by approximately 94% on potatoes and approximately 62% on collards. Increasing enemy diversity similarly strengthened aphid suppression on both plants, however, and there was no evidence that plant species identity significantly altered the relationship between enemy diversity and prey suppression. Microcosm experiments suggested that, on both collards and potatoes, intraspecific competition among natural enemies exceeded interspecific competition. Enemy species showed consistent and significant differences in where they foraged on the plants, and enemies in the low-diversity treatment tended to spend less time foraging than enemies in the high-diversity treatment. These data suggest that increasing enemy diversity may strengthen aphid suppression because interspecific differences in where enemies forage on the plant allow for greater resource partitioning. Further, these functional benefits of diversity appear to be robust to changes in plant species identity.

Species identity dominates the relationship between predator biodiversity and herbivore suppression.

Agricultural pest suppression is an important ecosystem service that may be threatened by the loss of predator diversity. This has stimulated interest in the relationship between predator biodiversity and biological control. Multiple-predator studies have shown that predators may complement or interfere with one another, but few experiments have determined if the resulting effects on prey are caused by changes in predator abundance, identity, species richness, or some combination of these factors. We experimentally isolated the effect of predator species richness on the biological control of an important agricultural pest, the green peach aphid. We found no evidence that increasing predator species richness affects aphid biological control; overall there was no strong complementarity or interference among predator species that altered the strength of aphid suppression. Instead, our experiments revealed strong effects of predator species identity, because predators varied dramatically in their per capita consumption rates. Our results are consistent with other multiple-predator studies finding strong species-identity effects and suggest that, for the biological control of aphids, conservation strategies that directly target key species will be more effective than those targeting predator biodiversity more broadly.