DOI: 10.25338/b8393n
title: Honey bee introductions displace native bees and decrease pollination of a native wildflower

description: 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 the 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.
description: <strong>Field methods</strong>: In 2019, we selected
 15 meadows, each &gt;500 m apart, which varied in honey bee abundance
 across space and time due to their proximity to four seasonal apiaries.
 Across these meadows, we surveyed pollinator visitation patterns from May
 – July. To assess the overall abundance of honey bees and native bees, we
 netted active flower visitors while walking 100 m transects for two
 30-minute periods (one between 8:00-12:00 and one between 12:00-16:00). To
 assess honey bee and native bee visitation rates to C. quamash, we
 conducted timed observations of 8-12 flowering C. quamash focal plants,
 noting all visitors in a 10-minute period. All focal plant observations
 occurred from 11:00-13:00, in-between morning and afternoon netting
 transects. At the end of each sampling day, we measured pollen and nectar
 availability in one to three flowers on each of 10-20 open-pollinated C.
 quamash plants and 10-20 unvisited control plants which were bagged on
 site arrival. 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.
 <strong>Measuring pollination and seed set</strong>:
 At the end of each sampling day, we collected one style from a flower on
 twelve pre-marked C. quamash plants and mounted styles on fuchsin-tinted
 gelatin slides. We counted the number of conspecific and heterospecific
 pollen grains on stigmas using a compound light microscope. Seventy-two
 hours following pollinator observations and after the initiation of pollen
 tube growth, we collected a second style from these same pre-marked plants
 into 70% ethanol. In the lab, we softened styles with 8M NaOH at 35º C for
 1 hour and stained pollen tubes by placing softened styles in a solution
 of 0.05% aniline blue in 0.1M KH2PO4 for 24 hours. We squashed styles
 beneath cover slips on microscope slides and counted pollen tubes near the
 base of styles using epifluorescence microscopy. Two weeks after
 conducting pollinator observations we collected fruits from these same
 plants and assessed seed set per fruit by scoring ovules as fertilized or
 unfertilized. <strong>Single-visit effectiveness
 and controlled honey bee visit experiments</strong>: To assess the
 relative quality of honey bee visits and their direct contribution to C.
 quamash pollination, we performed two field experiments. In 2019, we
 conducted a controlled multiple-visit experiment to isolate the direct
 relationship between increasing honey bee visits and C. quamash
 pollination in one of the meadows where hives were introduced. In 2020, we
 returned to a different meadow, where honey bee abundance was more
 moderate, and assessed the single-visit pollination effectiveness of honey
 bees and other insect visitors. In both years, we bagged a selection of
 plants to prevent visitation and conducted observations from 7:00 until
 16:00 across several days. For controlled honey bee visit experiments, we
 allowed a randomly assigned number of honey bee visits (between zero and
 twenty) to freshly opened flowers and all other visitors were excluded
 (i.e., swatted away). For single-visit effectiveness experiments, we
 allowed a single visit from different visitors, noting the pollinator
 identity and aspects of its visit behavior. Because we did not want to
 impact an insect’s visit by capturing it, our identifications were done in
 the field. We grouped visitors into several broad categories: Large-bodied
 Andrena spp., Apis mellifera, Bombus spp., Halictus spp., Osmia spp.,
 “Small dark bees”, and syrphid flies. The category “Small dark bees”
 comprised primarily Lasioglossum spp. and small-bodied Andrena spp. For
 both field experiments, we re-bagged plants to prevent further visitation
 after experimental visits had concluded, collected fruits two weeks later,
 and counted fertilized ovules. <strong>Data
 structure</strong>: please see metadata (included in the download as
 a README.md file) for more information about variable names and their
 interpretation.