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?