Sublethal exposure to fungicides can affect honey bees (Apis mellifera L.) in ways that resemble malnutrition. These include reduced brood rearing, queen loss, and increased pathogen levels. We examined the effects of oral exposure to the fungicides boscalid and pyraclostrobin on factors affecting colony nutrition and immune function including pollen consumption, protein digestion, hemolymph protein titers, and changes in virus levels. Because the fungicides are respiratory inhibitors, we also measured ATP concentrations in flight muscle. The effects were evaluated in 3- and 7-d-old worker bees at high fungicide concentrations in cage studies, and at field-relevant concentrations in colony studies. Though fungicide levels differed greatly between the cage and colony studies, similar effects were observed. Hemolymph protein concentrations were comparable between bees feeding on pollen with and without added fungicides. However, in both cage and colony studies, bees consumed less pollen containing fungicides and digested less of the protein. Bees fed fungicide-treated pollen also had lower ATP concentrations and higher virus titers. The combination of effects we detected could produce symptoms that are similar to those from poor nutrition and weaken colonies making them more vulnerable to loss from additional stressors such as parasites and pathogens.
Free-ranging herbivores have yearly life cycles that generate dynamic resource needs. Honey bee colonies also have a yearly life cycle that might generate nutritional requirements that differ between times of brood rearing and colony expansion in the spring and population contraction and preparation for overwintering in the fall. To test this, we analyzed polyfloral mixes of spring and fall pollens to determine if the nutrient composition differed with season. Next, we fed both types of seasonal pollens to bees reared in spring and fall. We compared the development of brood food glands (i.e., hypopharyngeal glands - HPG), and the expression of genes in the fat body between bees fed pollen from the same (in-season) or different season (out-of-season) when they were reared. Because pathogen challenges often heighten the effects of nutritional stress, we infected a subset of bees with Nosema to determine if bees responded differently to the infection depending on the seasonal pollen they consumed. We found that spring and fall pollens were similar in total protein and lipid concentrations, but spring pollens had higher concentrations of amino and fatty acids that support HPG growth and brood production. Bees responded differently when fed in vs. out of season pollen. The HPG of both uninfected and Nosema-infected spring bees were larger when they were fed spring (in-season) compared to fall pollen. Spring bees differentially regulated more than 200 genes when fed in- vs. out-of-season pollen. When infected with Nosema, approximately 400 genes showed different infection-induced expression patterns in spring bees depending on pollen type. In contrast, HPG size in fall bees was not affected by pollen type, though HPG were smaller in those infected with Nosema. Very few genes were differentially expressed with pollen type in uninfected (4 genes) and infected fall bees (5 genes). Pollen type did not affect patterns of infection-induced expression in fall bees. Our data suggest that physiological responses to seasonal pollens differ between bees reared in the spring and fall with spring bees being significantly more sensitive to pollen type especially when infected with Nosema. This study provides evidence that seasonal pollens may provide levels of nutrients that align with the activities of honey bees during their yearly colony cycle. The findings are important for the planning and establishment of forage plantings to sustain honey bees, and in the development of seasonal nutritional supplements fed to colonies when pollen is unavailable.
Varroa mites are a serious pest of honey bees and the leading cause of colony losses. Varroa have relatively low reproductive rates, so populations should not increase rapidly, but often they do. Other factors might contribute to the growth of varroa populations including mite migration into colonies on foragers from other hives. We measured the proportion of foragers carrying mites on their bodies while entering and leaving hives, and determined its relationship to the growth of varroa populations in those hives at two apiary sites. We also compared the estimates of mite population growth with predictions from a varroa population dynamics model that generates estimates of mite population growth based on mite reproduction. Samples of capped brood and adult bees indicated that the proportion of brood cells infested with mites and adult bees with phoretic mites was low through the summer but increased sharply in the fall especially at site 1. The frequency of capturing foragers with mites on their bodies while entering or leaving hives also increased in the fall. The growth of varroa populations at both sites was not significantly related to our colony estimates of successful mite reproduction, but instead to the total number of foragers with mites (entering and leaving the colony). There were more foragers with mites at site 1 than site 2, and mite populations at site 1 were larger especially in the fall. The model accurately estimated phoretic mite populations and infested brood cells until November when predictions were much lower than those measured in colonies. The rapid growth of mite populations particularly in the fall being a product of mite migration rather than mite reproduction only is discussed.
Honey bee colonies have a yearly cycle that is supported nutritionally by the seasonal progression of flowering plants. In the spring, colonies grow by rearing brood, but in the fall, brood rearing declines in preparation for overwintering. Depending on where colonies are located, the yearly cycle can differ especially in overwintering activities. In temperate climates of Europe and North America, colonies reduce or end brood rearing in the fall while in warmer climates bees can rear brood and forage throughout the year. To test the hypothesis that nutrients available in seasonal pollens and honey bee responses to them can differ we analyzed pollen in the spring and fall collected by colonies in environments where brood rearing either stops in the fall (Iowa) or continues through the winter (Arizona). We fed both types of pollen to worker offspring of queens that emerged and open mated in each type of environment. We measured physiological responses to test if they differed depending on the location and season when the pollen was collected and the queen line of the workers that consumed it. Specifically, we measured pollen and protein consumption, gene expression levels (hex 70, hex 110, and vg) and hypopharyngeal gland (HPG) development. We found differences in macronutrient content and amino and fatty acids between spring and fall pollens from the same location and differences in nutrient content between locations during the same season. We also detected queen type and seasonal effects in HPG size and differences in gene expression between bees consuming spring vs. fall pollen with larger HPG and higher gene expression levels in those consuming spring pollen. The effects might have emerged from the seasonal differences in nutritional content of the pollens and genetic factors associated with the queen lines we used.
-Honey bees that consume pollen with sublethal levels of the fungicide Pristine® can have reduced pollen digestion, lower ATP synthesis, and in many ways resemble malnourished bees. Reduced nutrient acquisition in bees exposed to Pristine® might be due to the effects of this fungicide on the composition of gut microbial communities. Two experiments were conducted in two separate years to test for the effects of Pristine® on the composition and diversity of bacteria in nurse bee midguts. In the low-dose experiment, bees fed the fungicide had a reduced relative abundance of Gilliamella sp. and the number of bacterial taxa within each individual bee was lower. In the high-dose experiment, the fungicide treatment led to increased relative abundance of Lactobacillus sp. Firm 4 and Firm 5 relative to the control. Presence of the fungicide did not impact the distribution of bacteria among individuals on either the low-or high-dose experiments. Considerable differences in gut microbial communities existed between the two experiments perhaps due to environmental and dietary factors. The effects of Pristine® on the gut microbiota were inconsistent between experiments indicating that exposure rate and environmental conditions can influence the effects of this fungicide on gut microbial communities.respiration / nutrition / boscalid / pyraclostrobin / microbiome
Varroa destructor is an ectoparasitic mite of immature and adult honey bees that can transmit several single-stranded RNA viruses to its host. Varroa reproduce in brood cells, and mite populations increase as colonies produce brood in spring and summer. Mite numbers also can sharply rise, particularly in the fall, by the migration of varroa into hives on foragers. Colonies with high levels of varroa and viruses often die over the winter. Feeding colonies pollen might keep virus levels low and improve survival because of the positive effects of pollen on immunity and colony growth. We compared varroa and virus levels and overwinter survival in colonies with (fed) and without (unfed) supplemental pollen. We also measured the frequency of capturing foragers with mites (FWM) at colony entrances to determine its relationship to varroa and virus levels. Colonies fed supplemental pollen were larger than unfed colonies and survived longer. Varroa populations and levels of Deformed wing virus (DWV) rose throughout the season, and were similar between fed and unfed colonies. The growth of varroa populations was correlated with FWM in fed and unfed colonies, and significantly affected DWV levels. Increasing frequencies of FWM and the effects on varroa populations might reduce the positive influence of supplemental pollen on immune function. However, pollen feeding can stimulate colony growth and this can improve colony survival.
Varroa (Varroa destructor Anderson and Trueman) is an external parasite of honey bees (Apis mellifera L.) and a leading cause of colony losses worldwide. Varroa populations can be controlled with miticides, but mite-resistant stocks such as the Russian honey bee (RHB) also are available. Russian honey bee and other mite-resistant stocks limit Varroa population growth by affecting factors that contribute to mite reproduction. However, mite population growth is not entirely due to reproduction. Numbers of foragers with mites (FWM) entering and leaving hives also affect the growth of mite populations. If FWM significantly contribute to Varroa population growth, mite numbers in RHB colonies might not differ from unselected lines (USL). Foragers with mites were monitored at the entrances of RHB and USL hives from August to November, 2015, at two apiary sites. At site 1, RHB colonies had fewer FWM than USL and smaller phoretic mite populations. Russian honey bee also had fewer infested brood cells and lower percentages with Varroa offspring than USL. At site 2, FWM did not differ between RHB and USL, and phoretic mite populations were not significantly different. At both sites, there were sharp increases in phoretic mite populations from September to November that corresponded with increasing numbers of FWM. Under conditions where FWM populations are similar between RHB and USL, attributes that contribute to mite resistance in RHB may not keep Varroa population levels below that of USL.
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