The intersection of bee and flower sexes: pollen presence shapes sex-specific bee foraging associations in sunflower.

Foraging preferences are known to differ among bee taxa, and can also differ between male and female bees of the same species. Similarly, bees can prefer a specific flower sex, particularly if only one sex provides pollen. Such variation in foraging preferences could lead to divergent bee communities visiting different flower sexes of a plant species. We sampled bees visiting sunflowers to characterize bee species richness, abundance, and sex ratios on pollen-fertile and pollen-sterile cultivars. We asked whether female or male bees were more abundant on sunflowers, whether female bees were more abundant on pollen-fertile or pollen-sterile cultivars, and whether pollen presence predicted the sex of sampled bees. We further asked whether the bee community differed between pollen-fertile and pollen-sterile cultivars. Females of most bee species were more abundant on sunflowers compared to males, and females were usually more abundant on pollen-fertile cultivars. In three bee species, pollen presence was predictive of a bee's sex, with females more abundant on pollen-fertile cultivars than males. Further, the bee community differed significantly between pollen-fertile and pollen-sterile cultivars, with two bee species functioning as indicators for pollen-fertile sunflowers. Our results demonstrate that a bee's sex shapes foraging associations on sunflowers and influences abundance between pollen-fertile and pollen-sterile cultivars, and that pollen-fertile and pollen-sterile cultivars are visited by different bee communities. Bee sexes and flower pollen presence may be under-appreciated factors shaping pollination services in both agricultural and natural ecosystems, and could be important considerations for pollination of crops with pollen-fertile and pollen-sterile flowers.

Sunflower-Associated Reductions in Varroa Mite Infestation of Honey Bee Colonies.

Landscapes can affect parasite epidemiology in wild and agricultural animals. Honey bees are threatened by loss of floral resources and by parasites, principally the mite Varroa destructor and the viruses it vectors. Existing mite control relies heavily on chemical treatments that can adversely affect bees. Alternative, pesticide-free control methods are needed to mitigate infestation with these ectoparasites. Many flowering plants provide nectar and pollen that confer resistance to parasites. Enrichment of landscapes with antiparasitic floral resources could therefore provide a sustainable means of parasite control in pollinators. Floral rewards of Asteraceae plants can reduce parasitic infection in diverse bee species, including honey and bumble bees. Here, we tested the effects of sunflower (Helianthus annuus) cropland and pollen supplementation on honey bee resistance to macro- and microparasites. Although sunflower had nonsignificant effects on microparasites, We found that increased sunflower pollen availability correlated with reduced Varroa mite infestation in landscapes and pollen-supplemented colonies. At the landscape level, each doubling of sunflower crop area was associated with a 28% reduction in mite infestation. In field trials, late-summer supplementation of colonies with sunflower pollen reduced mite infestation by 2.75-fold relative to artificial pollen. United States sunflower crop acreage has declined by 2% per year since 1980, however, suggesting reduced availability of this floral resource. Although further research is needed to determine whether the observed effects represent direct inhibition of mite fecundity or mite-limiting reductions in honey bee brood-rearing, our findings suggest the potential for sunflower plantings or pollen supplements to counteract a major driver of honey bee losses worldwide.

Manipulation of multiple floral traits demonstrates role in pollinator disease transmission.

Plants modulate multitrophic ecological interactions, and variation in plant traits can affect these interactions. Pollinators are exposed to pathogens at flowers and acquire or transmit pathogens at different rates on different plant species, but the traits mediating those interactions are almost entirely unknown. We experimentally manipulated five plant traits that span scales including flower, inflorescence, and plant, to determine their effects on pathogen transmission between foraging bees. Specifically, we manipulated two morphological traits (corolla lip length and flower orientation within an inflorescence) and three resource distribution traits (inflorescence nectar, plant patch nectar, and plant aggregation) in tents to test how plant traits affect bee pathogen transmission. We also quantified foraging behavior and fecal deposition patterns as potential mechanisms driving differences in transmission, and assessed trait manipulation consequences for bee reproduction. We found that pathogen transmission was reduced when we trimmed the corolla lip, evenly dispersed nectar distribution within an inflorescence, or aggregated plants in space. Some traits also affected bee reproduction; tents with trimmed corollas had more larval production than control tents, and tents with evenly distributed nectar across plant patches had more larval production than tents with clumped resources. Thus, some trait manipulations both reduced transmission and increased bee microcolony reproduction, although our design does not allow us to discern whether these are related or separate effects. Taken together, our results demonstrate causal effects of several floral traits on pathogen transmission and pollinator reproduction, indicating the importance of intraspecific plant trait variation for pollinator health and population dynamics.

Big bees spread disease: body size mediates transmission of a bumble bee pathogen.

Trait variation can have important consequences for the outcomes of species interactions. Even though some traits vary as much within species as across related species, models and empirical studies typically do not consider the role of intraspecific trait variation for processes such as disease transmission. For example, many pollinator species are in decline because of a variety of stressors including pathogens, but the role of intraspecific trait variation in mediating disease dynamics is rarely considered. For example, pollinator body size could affect pathogen transmission via differences in resistance, foraging behavior and physiology. We tested effects of body size on pollinator pathogen transmission using the common eastern bumble bee Bombus impatiens in field tents, introducing an infected "donor" microcolony of large or small workers with an uninfected average-sized "recipient" microcolony and allowing bees to forage for 9-16 d. Small donor bees had nearly 50% higher infection intensity (cells/0.02  µL) than large donor bees, but large donor bees were twice as likely to transmit Crithidia bombi to recipient bees. Both behavioral and physiological mechanisms may underlie this apparent paradox. Compared to small bees, large bees foraged more and produced more feces; simulations showed that foraging and defecation rates together had stronger effects on transmission than did donor infection intensity. Thus, effects of bee size on contact rates and pathogen supply may play significant roles in disease transmission, demonstrating the multifaceted impacts of traits on transmission dynamics.

Plants trap pollen to feed predatory arthropods as an indirect resistance against herbivory.

Plants commonly employ indirect resistance to reduce herbivory by provisioning predatory arthropod populations with additional resources. Numerous predatory arthropods consume pollen that is entrapped on dense, wooly trichomes of plants. Over two seasons, we supplemented pollen on the wooly leaves of turkey mullein, Croton setiger, in natural populations to determine if pollen entrapped on leaves supplements predatory arthropods and reduces herbivore populations and damage to the plant. Pollen supplementation increased the abundance of predatory spiders in both years and omnivorous Orius bugs in 1 yr but had no effect on predatory hemipterans. Pollen supplementation reduced the abundance of herbivorous fleahoppers. Pollen supplementation decreased the amount of leaf damage experienced by plants over the season, suggesting that pollen entrapment may act as an indirect resistance. While C. setiger plants have little control over the amount of pollen on their surfaces, pollen adds to the diet of predatory arthropods that reduce herbivory, thus attraction of predators may be an adaptive benefit of leaf structures such as wooly trichomes that entrap pollen.

Effects of wildfire on floral display size and pollinator community reduce outcrossing rate in a plant with a mixed mating system.

PREMISE OF THE STUDY: Wildfire changes the demography, morphology, and behavior of plants, and may alter the pollinator community. Such trait changes may drastically alter the outcome of pollination mutualisms on plants; however, the direct role of fire on these mutualisms is poorly known. METHODS: Following a pair of fires in the northern California coast range chaparral, we censused floral visitor communities of Trichostema laxum (Lamiaceae), quantified visiting bee behavior, and estimated outcrossing rates using a widespread Mendelian recessive floral polymorphism across a matrix of populations in burned and unburned sites. We also compared pre- and postfire floral visitation in two populations. RESULTS: Outcrossing rates were significantly lower in burned areas; however, our data suggest that the much larger size of plants in burned areas, not burn status itself, drove this pattern. Large-bodied bees dominated floral visitor communities after fire, likely recruiting to the abundant postfire floral resources. These bees visited more flowers per plant than did the smaller bees prevalent before fire and in unburned areas, likely increasing selfing through geitonogamy (within-plant pollination), an effect made possible by the far larger size of plants in burned areas. CONCLUSIONS: Outcrossing rates dropped substantially after wildfires because of changes in the pollinators, plant display size, and their interactions. Reductions in outcrossing following fire may have important implications for population resilience and evolution in a changing climate with more frequent fires.