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.Funding provided by: National Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000001Award Number: DEB-1556885Funding provided by: U.S. Department of DefenseCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000005Award Number: NDSEG FellowshipField surveys of plant-pollinator interactions: We conducted this work in the California Central Valley at five replicated wildflower plantings neighboring almond orchards which we sampled in 2017 and 2018. We also sampled 15 montane meadows in the Central Sierra Nevada in 2019. In both ecosystems, we surveyed pollinators and their visits to flowering plants over multiple sample rounds. For network analyses, we excluded bees not identified to morphospecies (~3% of all specimens). Because we were exclusively interested in documenting bee competition, we also excluded non-bee floral visitors from network analyses. Assessing pollen diet composition In the lab, we counted and identified pollen grains on the bodies of collected bee specimens, focusing on scopal loads. We calculated pollen fidelity as the number of pollen grains from the plant species from which the specimen was caught divided by the total number of pollen grains in the swabbed sample. We calculated pollen diversity using the Shannon-Weiner diversity index. Quantifying pollen resource depletion In both systems, at the end of each sampling day, we measured pollen and nectar availability in the field using one to three flowers on 10–20 "open-pollinated" plants and 10-20 unvisited control plants which were bagged on site arrival (between 6h30 and 7h30) and prior to pollinator activity. We measured pollen availability as the proportion of dehisced anthers with pollen visible to the naked eye and measured nectar availability using 1µL capillary tubes. Network metrics: For each site and sample round in each year and system, we generated unique plant x pollinator visitation networks. In total, we generated 40 networks across two years of sampling for our Central Valley sites and 48 networks for our Sierra sites. For each network, we used the bipartite package and R to calculate pollinator specialization (d'), complementary specialization (H2'), and perceived apparent competition (PAC). Because PAC is sensitive to the relative abundance of competing species, we compared observed values of PAC against PAC values calculated using null networks. To perform this comparison, we generated 500 randomized null networks using the r2rtable method, which resamples interactions but keeps row and column sums constant and compared observed metrics against null network metrics using Z-scores. To complement calculations of PAC between honey bees and native bees, we also calculated the mean PAC value for all pairwise comparisons of native bees against other native bees. For more details about methods and statistical tests used to analyse these data, please see the associated publication