Publications

Wildflower habitats planted along field borders are a widely promoted strategy for supporting bees in agricultural landscapes. However, honeybees (Apis mellifera), which are often stocked at high densities in crop lands can compete with wild bees for pollen and nectar, potentially limiting the successfulness of wildflower plantings in supporting diverse bee communities. Using weekly samples of five study sites in Northern California we assessed how plants in pollinator-friendly seed mixes varied in their ability to provide bees with abundant and nutritious pollen under intense honeybee competition. We quantified pollen production, protein and lipid content, and end-of-day pollen availability for different plant species. We also sampled bee visits to flowers and assessed the composition of pollen on bee bodies. Using these data, we investigate how the nutritional quality of pollen in wildflower plantings and honeybee abundance impacted native bee pollen nutrition. Bees collected more nutritious pollen (i.e. pollen with more protein) from plantings with more nutritious plant species (i.e. sites with more high-protein plants). However, as honeybee abundance increased, the nutritional quality of native bee diets declined. We also detected important interactions between honeybee abundance and the nutritional quality of flowers in plantings, such that, for some bee taxa, there was no impact of competition on pollen diet quality in high-nutrition plantings. Synthesis and applications: Our study reveals that honeybee competition can reduce the nutritional quality of native bee diets. From an applied conservation perspective, we therefore recommend that honeybee introductions in natural areas be approached with extreme caution. However, our results also suggest that high-protein flower plantings could mitigate negative effects of honeybee competition in managed landscapes. Where simultaneous support of managed and wild bees is a key management objective, we recommend including high-protein plant species in plant mixes to support diverse bee populations.

1. Human-mediated species introductions provide real-time experiments in how communities respond to interspecific competition. For example, managed honey bees (Apis mellifera L.) have been widely introduced outside their native range and may compete with native bees for pollen and nectar. Indeed, multiple studies suggest that honey bees and native bees overlap in their use of floral resources. However, for resource overlap to negatively impact resource collection by native bees, resource availability must also decline, and few studies investigate impacts of honey bee competition on native bee floral visits and floral resource availability simultaneously. 2. In this study, we investigate impacts of increasing honey bee abundance on native bee visitation patterns, pollen diets, and nectar and pollen resource availability in two Californian landscapes, wildflower plantings in the Central Valley and montane meadows in the Sierra. 3. We collected data on bee visits to flowers, pollen and nectar availability, and pollen carried on bee bodies across multiple sites in the Sierra and Central Valley. We then constructed plant-pollinator visitation networks to assess how increasing honey bee abundance impacted perceived apparent competition (PAC), a measure of niche overlap, and pollinator specialization (d’). We also compared PAC values against null expectations to address whether observed changes in niche overlap were greater or less than what we would expect given the relative abundances of interacting partners. 4. We find clear evidence of exploitative competition in both ecosystems based on the following results, (1) honey bee competition increased niche overlap between honey bees and native bees, (2) increased honey bee abundance led to decreased pollen and nectar availability in flowers, and (3) native bee communities responded to competition by shifting their floral visits, with some becoming more specialized and others becoming more generalized depending on the ecosystem and bee taxon considered. 5. Although native bees can adapt to honey bee competition by shifting their floral visits, the coexistence of honey bees and native bees is tenuous and will depend on floral resource availability. Preserving and augmenting floral resources is therefore essential in mitigating negative impacts of honey bee competition.

Introduced species can have cascading effects on ecological communities, but indirect effects of species introductions are rarely the focus of ecological studies. For example, managed honey bees (Apis mellifera) have been widely introduced outside their native range and are increasingly dominant floral visitors. Multiple studies have documented how honey bees impact native bee communities through floral resource competition, but few have quantified how these competitive interactions indirectly affect pollination and plant reproduction. Such indirect effects are hard to detect because honey bees are themselves pollinators and may directly impact pollination through their own floral visits. The potentially huge but poorly understood impacts that non-native honey bees have on native plant populations combined with increased pressure from beekeepers to place hives in U.S. National Parks and Forests makes exploring impacts of honey bee introductions on native plant pollination of pressing concern. In this study, we used experimental hive additions, field observations, as well as single-visit and multiple-visit pollination effectiveness trials across multiple years to untangle the direct and indirect impacts of increasing honey bee abundance on the pollination of an ecologically important wildflower, Camassia quamash. We found compelling evidence that honey bee introductions indirectly decrease pollination by reducing nectar and pollen availability and competitively excluding visits from more effective native bees. In contrast, the direct impact of honey bee visits on pollination was negligible, and, if anything, negative. Honey bees were ineffective pollinators, and increasing visit quantity could not compensate for inferior visit quality. Indeed, although the effect was not statistically significant, increased honey bee visits had a marginally negative impact on seed production. Thus, honey bee introductions may erode longstanding plant-pollinator mutualisms, with negative consequences for plant reproduction. Our study calls for a more thorough understanding of the indirect effects of species introductions and more careful coordination of hive placements.

In our analysis of 168 pollination effectiveness studies, we found that honey bees were less effective than the average bee and rarely the most effective pollinator of plants they visit.

Recent bumble bee declines have prompted the development of novel population monitoring tools, including the use of putatively non-lethal tarsal clipping to obtain genetic material. However, the potential side effects of tarsal clipping have only been tested in the worker caste of a single domesticated species, prompting the need to more broadly test whether tarsal clipping negatively affects sampled individuals. To determine if tarsal clipping reduces queen survivorship and colony establishment, we collected wild queens of Bombus vosnesenskii and clipped tarsi from a single leg of half the individuals. We reared captive queens and estimated survivorship and nest establishment success. We also clipped tarsi of workers from a subset of colonies across a range of body sizes. We found no consistent negative effect of clipping on queen survival. In the first year, clipped nest-searching queens suffered heavy mortality, but there was no effect on foraging queens. The following year, we found no effect of clipping on queen survival or establishment. Clipping did not reduce overall worker survival but reduced survivorship for those in the smallest size quartile.

Resource competition likely plays an important role in some insect pollinator declines and in shaping effects of environmental change on pollination services. Past research supports that competition for floral resources affects bee foragers, but mostly with observational evidence and rarely linking foraging with population change. An increasing number of studies ask whether resources limit pollinator populations, using field measurements of reproductive success, time series and models. Findings generally support positive effects of floral resources, but also highlight the potential importance of nest site availability and parasitism. In parallel, recent experiments strengthen evidence that competition reduces access to floral resources. Developing common currencies for quantifying floral resources and integrating analyses of multiple limiting factors will further strengthen our understanding of competitive interactions and their effects in the Anthropocene.

Background and Aims - Pendulous flowers (due to a flexible pedicel) are a common, convergent trait of hummingbird-pollinated flowers. However, the role of flexible pedicels remains uncertain despite several functional hypotheses. Here we present and test the ‘lever action hypothesis’: flexible pedicels allow pendulous flowers to move upwards from all sides, pushing the stigma and anthers against the underside of the feeding hummingbird regardless of which nectary is being visited. Methods - To test whether this lever action increased pollination success, we wired emasculated flowers of serpentine columbine, Aquilegia eximia, to prevent levering and compared pollination success of immobilized flowers with emasculated unwired and wire controls. Key Results - Seed set was significantly lower in wire-immobilized flowers than unwired control and wire control flowers. Video analysis of visits to wire-immobilized and unwired flowers demonstrated that birds contacted the stigmas and anthers of immobilized flowers less often than those of flowers with flexible pedicels. Conclusions - We conclude that flexible pedicels permit the levering of reproductive structures onto a hovering bird. Hummingbirds, as uniquely large, hovering pollinators, differ from flies or bees which are too small to cause levering of flowers while hovering. Thus, flexible pedicels may be an adaptation to hummingbird pollination, in particular due to hummingbird size. We further speculate that this mechanism is effective only in radially symmetric flowers; in contrast, zygomorphic hummingbird-pollinated flowers are usually more or less horizontally oriented rather than having pendulous flowers and flexible pedicels.

Bumble bees are among the best-studied bee groups worldwide, yet surprisingly we know almost nothing about their overwintering habitats nor the microsite characteristics that govern selection of these sites. This gap represents a critical barrier for their conservation, especially if preferred overwintering habitats differ from foraging and nesting habitats. Current conservation plans focus on foraging habitat, potentially creating a problem of partial habitats where improved forage might fail to prevent population declines due to limited overwintering sites. We provide the first data on the overwintering habitat for any western North American bumble bee. Our data suggest that overwintering and foraging habitats are likely distinct, and queens’ selection of overwintering sites may be shaped by environmental stressors of the year. In our study area, queens overwintered in litter beneath cypress trees, where no floral resources exist. Whether this separation of overwintering and foraging habitat holds for other bumble bee species remains to be discovered. Our data highlight the need to consider the whole life cycle for understanding population dynamics and conservation planning. This need is underscored by growing evidence for the decline of multiple North American bumble bee species

Premise - Variation in pollinator effectiveness may contribute to pollen limitation in fragmented plant populations. In plants with multiovulate ovaries, the number of conspecific pollen grains per stigma often predicts seed set and is used to quantify pollinator effectiveness. In the Asteraceae, however, florets are uniovulate, which suggests that the total amount of pollen deposited per floret may not measure pollinator effectiveness. We examined two aspects of pollinator effectiveness—effective pollen deposition and effective pollen movement—for insects visiting Echinacea angustifolia, a composite that is pollen limited in small, isolated populations. Methods - We filmed insect visits to Echinacea in two prairie restorations and used these videos to quantify behavior that might predict effectiveness. To quantify effective pollen deposition, we used the number of styles shriveled per visit. To quantify effective pollen movement, we conducted paternity analysis on a subset of offspring and measured the pollen movement distance between mates. Results - Effective pollen deposition varied among taxa. Andrena helianthiformis, a Heliantheae oligolege, was the most effective taxon, shriveling more than twice the proportion of styles as all other visitors. Differences in visitor behavior on a flowering head did not explain variation in effective pollen deposition, nor did flowering phenology. On average, visitors moved pollen 16 m between plants, and this distance did not vary among taxa. Conclusions - Andrena helianthiformis is an important pollinator of Echinacea. Variation in reproductive fitness of Echinacea in fragmented habitat may result, in part, from the abundance of this species.