Environmental impacts on native bumble bee pollinators in an agricultural landscape of western Oregon

Bumble bees provide vital pollination services in both native and agricultural landscapes. However, in recent years, bumble bee populations have experienced global population declines. The primary causes of these declines have been attributed to the environmental impacts of pathogens, pesticide use and habitat fragmentation. While research has examined the impacts of pathogens, there is limited information on the effects of pesticides and habitat fragmentation on native bumble bees. Hence, the objectives of my dissertation research were to: 1) assess the toxicological impacts of pesticides used in two important bee-pollinated crops on queens and workers; 2) determine the impacts of forage resource availability on bumble bee colonies; 3) examine pollen foraging behavior of bumble bees in a late season mass-flowering agricultural landscape; and 4) document observations on trends towards bivoltinism in three western North American bumble bees. This research was conducted in the lab using wild and lab reared colonies, and in an agricultural landscape in the Willamette Valley of Western Oregon. In pesticide bioassays the impacts of residual toxicity of five classes of pesticides used in highbush blueberry and red clover cropping systems, were tested on queen and worker bumble bees, respectively. The results indicated variation in responses to the same insecticide by queens and workers, and to the same class of compounds by workers. Also, toxic effects were documented for both queens and workers to pesticides considered to be "safe" for bees. The impacts of forage resource availability were evaluated by exposing bumble bee colonies to four quantities of pollen, four quantities of nectar and three feeding frequencies of pollen. The study documented an inverse relationship between larvae and workers to resource type and availability. In addition, the type of larval mortality displayed by colonies, larval ejection or within clump mortality, was dependent on worker mortality. The individual and colony-level pollen foraging behavior of bumble bees was examined by placing colonies in red clover. Observations in the field on forager abundance, and at the colony-level on the duration and number of pollen trips and weight of stored pollen documented that red clover is an important resource for bumble bees. Pollen analysis revealed that in addition to red clover, Himalayan blackberry was also a key forage resource for bumble bees. Red clover resources at the end of the season may also benefit bumble bees by allowing for the creation of a second generation. Observations on both field and lab-reared queens document a trend towards bivoltinism in three species of western North American bumble bees. Agricultural habitats are vital for sustaining bumble bee populations. However, given the potential for pesticide impacts and temporal availability of flowering plants, these landscapes must be managed to provide maximum benefit to bumble bees. Results from this research should assist growers and researchers in developing landscape management and production practices geared toward the conservation and enhancement of native Bombus spp. populations in western Oregon.Keywords: environmental factors, agriculture, pollinator, Bombu

Context-Dependent Medicinal Effects of Anabasine and Infection-Dependent Toxicity in Bumble Bees

Background Floral phytochemicals are ubiquitous in nature, and can function both as antimicrobials and as insecticides. Although many phytochemicals act as toxins and deterrents to consumers, the same chemicals may counteract disease and be preferred by infected individuals. The roles of nectar and pollen phytochemicals in pollinator ecology and conservation are complex, with evidence for both toxicity and medicinal effects against parasites. However, it remains unclear how consistent the effects of phytochemicals are across different parasite lineages and environmental conditions, and whether pollinators actively self-medicate with these compounds when infected. Approach Here, we test effects of the nectar alkaloid anabasine, found in Nicotiana, on infection intensity, dietary preference, and survival and performance of bumble bees (Bombus impatiens). We examined variation in the effects of anabasine on infection with different lineages of the intestinal parasite Crithidia under pollen-fed and pollen-starved conditions. Results We found that anabasine did not reduce infection intensity in individual bees infected with any of four Crithidia lineages that were tested in parallel, nor did anabasine reduce infection intensity in microcolonies of queenless workers. In addition, neither anabasine nor its isomer, nicotine, was preferred by infected bees in choice experiments, and infected bees consumed less anabasine than did uninfected bees under no-choice conditions. Furthermore, anabasine exacerbated the negative effects of infection on bee survival and microcolony performance. Anabasine reduced infection in only one experiment, in which bees were deprived of pollen and post-pupal contact with nestmates. In this experiment, anabasine had antiparasitic effects in bees from only two of four colonies, and infected bees exhibited reduced—rather than increased—phytochemical consumption relative to uninfected bees. Conclusions Variation in the effect of anabasine on infection suggests potential modulation of tritrophic interactions by both host genotype and environmental variables. Overall, our results demonstrate that Bombus impatiens prefer diets without nicotine and anabasine, and suggest that the medicinal effects and toxicity of anabasine may be context dependent. Future research should identify the specific environmental and genotypic factors that determine whether nectar phytochemicals have medicinal or deleterious effects on pollinators

Effects of 5 ppm anabasine treatment on <i>Crithidia</i> infection intensity in <i>Bombus impatiens</i> across three experiments.

<p>(A) Parasite Variation Experiment that tested effects of anabasine on infection of individual bees with one of four <i>Crithidia</i> lineages and reared individually. (B) Life History Experiment in which bees were reared in microcolonies of three workers. (C) Pollen Deprivation Experiment in which individual bees were deprived of pollen. Significance of terms in generalized linear mixed-effects models were tested by χ² tests. <i>Crithidia</i> cell counts were ln(x+1)-transformed to better conform to model assumptions. Marginal cell length refers to length of the right forewing marginal cell, used to estimate bee size (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0183729#sec010" target="_blank">Materials and Methods</a>). Colony refers to the bee’s experimental colony of origin.</p

Effects of <i>Crithidia</i> infection on microcolony performance in the Life History Experiment.

<p>Microcolonies were observed daily for (A) deaths, (B) time to first egg production, and (C) time to first honeypot construction. Line type represents infection treatment (solid lines for uninfected microcolonies; dotted lines for infected microcolonies). Line color represents anabasine treatment (red lines for 30% sucrose control; blue lines for 30% sucrose with 5 ppm anabasine). Crosses represent events (i.e., deaths, egg production, or honeypot construction) or censoring due to removal of the microcolony from the experiment.</p