Preparation of Virus-Enriched Inoculum for Oral Infection of Honey Bees (<em>Apis mellifera</em>)

Honey bees are of great ecological and agricultural importance around the world but are also subject to a variety of pressures that negatively affect bee ...

University of Illinois

Declines in honey bee health have been attributed to multiple interacting environmental stressors; among the most important are forage/nutrition deficits and parasites and pathogens. Recent studies suggest poor honey bee nutrition can exacerbate the negative impacts of infectious viral and fungal diseases, and conversely, that common honey bee parasites and pathogens can adversely affect bee nutritional physiology. This sets up the potential for harmful feedbacks between poor nutrition and infectious disease that may contribute to spiraling declines in bee health. We suggest that improving bees' nutritional resilience should be a major goal in combating challenges to bee health; this approach can buffer bees from other environmental stressors such as pathogen infection.

Feedbacks between nutrition and disease in honey bee health.

Honeybee population declines have been linked to multiple stressors, including reduced diet diversity and increased exposure to understudied viral pathogens. Despite interest in these factors, few experimental studies have explored the interaction between diet diversity and viral infection in honeybees. Here, we used a mixture of laboratory cage and small semi-field nucleus hive experiments to determine how these factors interact. In laboratory experiments, we found that high-quality diets (polyfloral pollen and high-quality single-source pollen) have the potential to reduce mortality in the face of infection with Israeli acute paralysis virus (IAPV). There was a significant interaction between diet and virus infection on mortality, even in the presence of high virus titres, suggesting that good diets can help bees tolerate virus infection. Further, we found that extreme stress in the form of pollen starvation in conjunction with IAPV infection increase exiting behaviour from small experimental hives. Finally, we showed that higher-quality pollen diets have significantly higher iron and calcium content, suggesting micronutrient deficiencies could be an under-explored area of bee nutrition.

Interacting stressors matter: diet quality and virus infection in honeybee health.

Parts of Europe and the United States have witnessed dramatic losses in commercially managed honey bees over the past decade to what is considered an unsustainable extent. The large-scale loss of bees has considerable implications for the agricultural economy because bees are one of the leading pollinators of numerous crops. Bee declines have been associated with several interactive factors. Recent studies suggest nutritional and pathogen stress can interactively contribute to bee physiological declines, but the molecular mechanisms underlying interactive effects remain unknown. In this study, we provide insight into this question by using RNA-sequencing to examine how monofloral diets and Israeli acute paralysis virus inoculation influence gene expression patterns in bees.

Transcriptomic responses to diet quality and viral infection in Apis mellifera.

Intensive agriculture can contribute to pollinator decline, exemplified by alarmingly high annual losses of honey bee colonies in regions dominated by annual crops (e.g., midwestern United States). As more natural or seminatural landscapes are transformed into monocultures, there is growing concern over current and future impacts on pollinators. To forecast how landscape simplification can affect bees, we conducted a replicated, longitudinal assessment of honey bee colony growth and nutritional health in an intensively farmed region where much of the landscape is devoted to production of corn and soybeans. Surprisingly, colonies adjacent to soybean fields surrounded by more cultivated land grew more during midseason than those in areas of lower cultivation. Regardless of the landscape surrounding the colonies, all experienced a precipitous decline in colony weight beginning in August and ended the season with reduced fat stores in individual bees, both predictors of colony overwintering failure. Patterns of forage availability and colony nutritional state suggest that late-season declines were caused by food scarcity during a period of extremely limited forage. To test if habitat enhancements could ameliorate this response, we performed a separate experiment in which colonies provided access to native perennials (i.e., prairie) were rescued from both weight loss and reduced fat stores, suggesting the rapid decline observed in these agricultural landscapes is not inevitable. Overall, these results show that intensively farmed areas can provide a short-term feast that cannot sustain the long-term nutritional health of colonies; reintegration of biodiversity into such landscapes may provide relief from nutritional stress.

Native habitat mitigates feast-famine conditions faced by honey bees in an agricultural landscape.

In the last century, a global transformation of Earth's surface has occurred due to human activity with extensive agriculture replacing natural ecosystems. Concomitant declines in wild and managed bees are occurring, largely due to a lack of floral resources and inadequate nutrition, caused by conversion to monoculture-based farming. Diversified fruit and vegetable farms may provide an enhanced variety of resources through crops and weedy plants, which have potential to sustain human and bee nutrition. We hypothesized fruit and vegetable farms can enhance honey bee (Hymenoptera: Apidae, Apis mellifera Linnaeus) colony growth and nutritional state over a soybean monoculture, as well as support a more diverse wild bee community. We tracked honey bee colony growth, nutritional state, and wild bee abundance, richness, and diversity in both farm types. Honey bees kept at diversified farms had increased colony weight and preoverwintering nutritional state. Regardless of colony location, precipitous declines in colony weight occurred during autumn and thus colonies were not completely buffered from the stressors of living in a matrix dominated with monocultures. Contrary to our hypothesis, wild bee diversity was greater in soybean, specifically in August, a time when fields are in bloom. These differences were largely driven by four common bee species that performed well in soybean. Overall, these results suggest fruit and vegetable farms provide some benefits for honey bees; however, they do not benefit wild bee communities. Thus, incorporation of natural habitat, rather than diversified farming, in these landscapes, may be a better choice for wild bee conservation efforts.

Diversified Farming in a Monoculture Landscape: Effects on Honey Bee Health and Wild Bee Communities.

Anthropogenic changes create evolutionarily novel environments that present opportunities for emerging diseases, potentially changing the balance between host and pathogen. Honey bees provide essential pollination services, but intensification and globalization of honey bee management has coincided with increased pathogen pressure, primarily due to a parasitic mite/virus complex. Here, we investigated how honey bee individual and group phenotypes are altered by a virus of concern, Israeli acute paralysis virus (IAPV). Using automated and manual behavioral monitoring of IAPV-inoculated individuals, we find evidence for pathogen manipulation of worker behavior by IAPV, and reveal that this effect depends on social context; that is, within versus between colony interactions. Experimental inoculation reduced social contacts between honey bee colony members, suggesting an adaptive host social immune response to diminish transmission. Parallel analyses with double-stranded RNA (dsRNA)-immunostimulated bees revealed these behaviors are part of a generalized social immune defensive response. Conversely, inoculated bees presented to groups of bees from other colonies experienced reduced aggression compared with dsRNA-immunostimulated bees, facilitating entry into susceptible colonies. This reduction was associated with a shift in cuticular hydrocarbons, the chemical signatures used by bees to discriminate colony members from intruders. These responses were specific to IAPV infection, suggestive of pathogen manipulation of the host. Emerging bee pathogens may thus shape host phenotypes to increase transmission, a strategy especially well-suited to the unnaturally high colony densities of modern apiculture. These findings demonstrate how anthropogenic changes could affect arms races between human-managed hosts and their pathogens to potentially affect global food security.

Honey bee virus causes context-dependent changes in host social behavior.

Honey bees are key agricultural pollinators, but beekeepers continually suffer high annual colony losses owing to a number of environmental stressors, including inadequate nutrition, pressures from parasites and pathogens, and exposure to a wide variety of pesticides. In this review, we examine how two such stressors, pesticides and viruses, may interact in additive or synergistic ways to affect honey bee health. Despite what appears to be a straightforward comparison, there is a dearth of studies examining this issue likely owing to the complexity of such interactions. Such complexities include the wide array of pesticide chemical classes with different modes of actions, the coupling of many bee viruses with ectoparasitic  mites, and the intricate social structure of honey bee colonies. Together, these issues pose a challenge to researchers examining the effects pesticide-virus interactions at both the individual and colony level.

Pesticide-Virus Interactions in Honey Bees: Challenges and Opportunities for Understanding Drivers of Bee Declines.

To study how honey bees utilize forage resources and guide pollination management plans in crops, a multitude of methods have been developed, but most are time consuming, costly, and require specialized skills. Colored pan traps for monitoring activity-density are a simple, efficient, and cost-effective alternative; however, their usefulness for studying honey bees is not well described. We examined if trap color, location within a field, and the presence of managed colonies affected estimates of honey bee activity-density within soybean fields. Soybeans are visited by pollinators but do not require these visits for seed development. Pan traps, especially those colored blue, captured more honey bees when colonies were present. There were no differences in activity-density based on placement of traps within a field nor with increasing distance from colonies. Throughout the season, activity-density in soybeans was constant but tripled after soybean ceased blooming, suggesting spikes in pan trap captures may indicate periods of forage scarcity. Activity-density did not correlate with the population size of worker bees at a site, but did correlate with number of colonies present. We conclude that pan traps can be useful for assessing honey bee activity, particularly for estimating colony presence and identifying times of forage scarcity.

Adam G. Dolezal

Department of Entomology

University of Illinois

Preparation of Virus-Enriched Inoculum for Oral Infection of Honey Bees (Apis mellifera)

Adam G. Dolezal

.css-o250i3{font-size:18px;font-family:Open Sans,sans-serif;line-height:21.6px;}Department of Entomology

University of Illinois

Preparation of Virus-Enriched Inoculum for Oral Infection of Honey Bees (Apis mellifera)

Department of Entomology