Evidence of exploitative competition between honey bees and native bees in two California landscapes.

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. 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. 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. 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. 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. In two California ecosystems, honey bee competition decreases pollen and nectar resource availability in flowers and alters native bee diets with potential implications for bee conservation and wildlands management.

Honey bee introductions displace native bees and decrease pollination of a native wildflower.

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.

A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors.

PREMISE: Many animals provide ecosystem services in the form of pollination including honeybees, which have become globally dominant floral visitors. A rich literature documents considerable variation in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators. METHODS: We conducted a hierarchical meta-analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. We paired SVE data with visitation frequency data for 69 of these studies. We used these data to ask three questions: (1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE? (2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors? (3) Is there a correlation between visitation frequency and SVE? RESULTS: Honeybees were significantly less effective than the most effective non-honeybee pollinators but were as effective as the average pollinator. The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent. CONCLUSIONS: Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators, and safeguarding pollination will benefit from conservation of non-honeybee taxa.

The importance of competition between insect pollinators in the Anthropocene.

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.

Pollinator effectiveness in a composite: a specialist bee pollinates more florets but does not move pollen farther than other visitors.

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.