INTRODUCTION
Introduced and invasive species are fundamentally altering the structure
of ecological communities (Elton 1958; Gallardo et al. 2015;
O’Dowd et al. 2003; Soulé 1985), leading to increased species
extinctions and biodiversity loss (Bellard et al. 2016; Capinhaet al. 2015). In addition to shifting community composition,
exotic species can impact ecosystem functioning through changes in the
growth and fitness of primary producers and become costly agricultural
pests (Cameron et al. 2016; Paini et al. 2016). However,
the impacts of exotic species may be more nuanced when they engage in
keystone mutualisms like pollination. In these cases, there is potential
for direct negative impacts through competition with native species for
shared resources (Mallinger et al. 2017; Thomson & Page 2020)
but also potential to benefit other species through interactions that
increase primary productivity (Vilà et al. 2011) and plant
reproduction (Hanna et al. 2013). Indeed, recent meta-analyses of
the invasive species literature largely ignore exotic mutualists (Mollotet al. 2017) and we are only beginning to understand the impacts
of invasive species on mutualistic interactions (Geslin et al.2017; Valdovinos et al. 2018).
The impacts of exotic species are even more contentious when the
introduced species is actively managed for recognized benefits to
humanity. For example, growing demand for agricultural pollination has
led to steady increases in managed populations of the European honey bee
(Apis mellifera ) (Aizen & Harder 2009), which has become a
dominant floral visitor in many plant communities worldwide (Herrera
2020; Hung et al. 2018). Despite mounting evidence that honey
bees compete with wild bees for floral resources (Cane & Tepedino 2016;
Carneiro & Martins 2012; Thomson & Page 2020) with potential
consequences for plant-pollinator interactions (Geslin et al.2017; Valdovinos et al. 2018; Valido et al. 2019) and wild
bee reproduction (Hudewenz & Klein 2015; Thomson 2004), the importance
of honey bees as pollinators has led beekeeping to be promoted and even
subsidized in some natural habitats (Geslin et al. 2017).
However, the importance of honey bees does not automatically imply that
honey bee introductions will benefit plant populations (Ollertonet al. 2012). Indeed, we currently lack robust studies
investigating how honey bee introductions impact pollination and this
knowledge gap limits our ability to inform conservation policies that
safeguard plant and pollinator populations.
Assessing the overall impact of honey bee introductions on pollination
is complicated because abundant honey bees can influence pollination
directly, through their flower visits, but also indirectly, by
competitively influencing visits from other pollinators. Pollination is
expected to increase with increased floral visitation and honey bees
visit flowers frequently (Hung et al. 2018). However, a handful
of studies have documented direct negative effects of high visitation
rates by introduced pollinators, whereby increased visits increase
pollen deposition but also damage stigmas (Sáez et al. 2014) or
lead to clogging of styles with growing pollen tubes (Magrach et
al . 2017), ultimately reducing successful reproduction. Honey bees can
also damage flowers while nectar robbing, increasing floral abortion
(Carbonari et al. 2009). In addition to visit numbers, the
relative quality of visits (i.e., pollination effectiveness) also
influences pollination (King et al. 2013), and honey bees can be
ineffective at depositing the pollen they extract (Wilson & Thomson
1991). Though seemingly less dramatic than direct floral damage,
ineffective pollinators can indirectly decrease pollination by reducing
pollen available for deposition by more effective visitors (Harder &
Barrett 1995; Harder & Thomson 1989; Minnaar et al. 2019).
Furthermore, regardless of their relative pollination effectiveness,
honey bees can deplete floral rewards that attract pollinators (Carneiro
& Martins 2012; Paton 1993), thus diminishing other pollinator visits
(Hansen et al. 2002; Vaughton 1996).
These direct and indirect effects can add to one another, or they can
cancel each other out if effects are of opposite sign but similar
magnitude (Strauss 1991). Quantifying both direct and indirect impacts
is needed to understand overall fitness consequences for plants, but few
studies of honey bee introductions carefully partition direct and
indirect effects. Indeed, across 29 studies of honey bee effects on
pollination identified by Mallinger et al. (2017), all but four
were purely correlative studies and none investigated both direct and
indirect effects of honey bee abundance simultaneously. Studies that
investigate both direct and indirect effects could shed light on how
impacts vary across systems. For example, the generally positive direct
effect of honey bee visits may be of greater importance in the absence
of competition; in cases where native pollinators have become rare or
locally extinct, honey bees often increase pollination (Hanna et
al. 2013; Lomov et al. 2010) and can even “rescue” plant
populations from reproductive failure in isolated habitat fragments
(Dick 2001). However, negative indirect effects may occur and even
outweigh direct effects when honey bees competitively displace native
pollinators, especially when honey bees are ineffective substitutes
(Page et al. 2021).
In this study, we investigated whether honey bee introductions in
montane meadows competitively displace native bees and impact
pollination of Camassia quamash (Liliaceae), an herbaceous
perennial plant which is an important floral resource for native bees
(Parachnowitsch & Elle 2005) and culturally important within indigenous
communities in North America (Carney et al. 2021; Turner &
Kuhnlein 1983). We sampled meadows in the Tahoe National Forest, an area
where U.S. policy changes may soon allow for increased hive densities
(U.S. Code of Federal Regulations 2013). Using observational data of
plant-pollinator interactions, experimental honey bee introductions, and
a series of pollination experiments across multiple years we asked: (i)
Does increased honey bee abundance in meadows affect native bee
visitation and indirectly influence C. quamash pollination?; (ii)
What is the direct effect of increasing honey bee visits on
pollination?; (iii) Does honey bee abundance affect pollen and nectar
availability in C. quamash flowers?; and (iv) Do honey bees and
native bees vary in their single-visit pollination effectiveness?