ABSTRACT: The western or European honey bee (Apis mellifera) is the primary managed pollinator • in US agricultural systems, and its importance for food production is widely recognized. However, the role of A. mellifera as an introduced species in natural areas is potentially more complicated. The impact of A. mellifera on native insect pollinators can depend on broad community context, as can the relative effectiveness of A. mellifera in pollination of both native and nonnative plant species outside of agricultural systems. Apis mellifera is highly generalist and able to interact with hundreds of native The Role of Honey plant species following its naturalization. It is unlikely to wholly replace native pollinators as visitors of specialized plant species, and its behavioral characteristics tend to reduce A. mellifera’s per-visit Bees as Pollinators efficiency, even when its overall effectiveness is high. Preliminary results of our case study exploring the importance of A. mellifera vs. native bees as pollinators of native plants in Hawaiʻi indicate that A. mellifera is less important than native Hylaeus bees as a flower visitor of focal native plant species. In in Natural Areas light of current global declines in A. mellifera populations, maintenance of a diversity of pollinators and pollinator habitat are critical conservation needs in natural areas.

Index terms: Apis mellifera, competition, mutualistic networks, native bees, pollination

Clare E. Aslan1,6,7 1Landscape Conservation Initiative INTRODUCTION the importance of A. mellifera as a polli­ Northern Arizona University nator of native Hawaiian plants. Finally, Flagstaff, AZ 86005 Pollination serves as the backbone of com­ we discuss the global implications of A. plex ecological systems (Heithaus 1974) mellifera naturalization on native species. 2 and is essential to agricultural production Widespread population declines among Christina T. Liang (Bommarco et al. 2013). To boost pollina­ both native and nonnative pollinators could Ben Galindo3 tion and fruit production, European honey impact both food security and native eco­ Kimberly Hill4 bees (Apis mellifera Linnaeus) have been logical community dynamics (Meffe 1998; 5 introduced to agricultural systems world­ Steffan-Dewenter et al. 2005; Biesmeijer Walter Topete wide (Moritz et al. 2005). Following these et al. 2006; Potts et al. 2010). The relative introductions, A. mellifera has repeatedly influence of A. mellifera on pollination in 2USDA Forest Service naturalized and spread, now occurring in natural areas will be an important deter­ Pacific Southwest Research Station natural areas in most parts of the globe minant of how current pollinator declines 60 Nowelo St. (Moritz et al. 2005). impact native biodiversity and could guide Hilo, HI 96720 land managers in determining how to man­ The establishment of the nonnative A. age A. mellifera colonies in natural areas. 3Southwestern University mellifera as a pollinator and forager carries Georgetown, TX the potential to alter mutualistic and com­ REVIEW: Honey Bees in Natural petitive interaction networks worldwide Systems 4SUNY College of Environmental (Traveset and Richardson 2006). Apis Science and Forestry mellifera may directly boost native plant Upon naturalization and spread into natural Syracuse, NY fitness through pollination, or indirectly systems, A. mellifera becomes a mem­ reduce native plant fitness by pollinating ber of complex ecological communities 5University of Houston nonnative invasive plant species (Kato structured by mutualism, competition, Houston, TX et al. 1999). By competing with native and resource flows. This integration of A. pollinators for resources, A. mellifera mellifera has occurred worldwide, follow­ 6Conservation Science Partners may reduce native pollinator fitness (Paini ing introductions from its native Europe, Truckee, CA 96161 2004). More subtle impacts are possible as Asia, and Africa. In North America, A. well; A. mellifera may differ from native mellifera was introduced as early as 1622, • bees in spatial and/or temporal pattern of with subsequent introductions beginning in pollen transport, in nectar foraging, or the 1859 (Whitfield et al. 2006). The unique quantity of pollen dispersed vs. consumed ecology of A. mellifera contributes to (Freitas 1997; Freitas and Paxton 1998). the success of the species. Apis mellifera Here, we review these factors to evaluate exhibits a complex society characterized 7 Corresponding author: clare.aslan@nau. the role of A. mellifera in native communi­ by the simultaneous presence of several edu; 928-523-2487 ties and the importance of the species as a generations within a colony, cooperation pollinator in natural areas. Additionally, to in offspring care, and division of labor illustrate the conservation implications of into queens, drones, and workers. Older Natural Areas Journal 36:478–488 this topic, we present a brief case study and workers forage for pollen and nectar, and early results of ongoing research exploring the dance communication between A.

478 Natural Areas Journal Volume 36 (4), 2016 mellifera individuals boosts foraging ef­ quantitative effectiveness of a pollinator pollinators have declined in abundance fectiveness (Okada et al. 2012). Individual depends on visitation frequency as well found that the primary pollinator of the workers forage across varied locations and as the abundance of pollen transferred. native Metrosideros polymorpha Gaudich. seasons, exhibit great flexibility in flight Effectiveness relates the overall visits of a was now A. mellifera, although native bees performance, and can carry substantial pollinator to seed set (Motten et al. 1981). are present and interacting with the tree loads during flight (Harrison and Fewell Furthermore, effectiveness must be evalu­ as well (Hanna et al. 2013). Native bees 2002). Mature A. mellifera colonies can ated in comparison to pollination received are the primary visitors to the declining range from 20,000 to 70,000 worker bees by native pollinators; in theory this is the Acacia carneorum Maiden in Australia, (Lee and Winston 1987). By contrast, the pollination context within which a given but A. mellifera is the primary visitor to vast majority of native bees in systems focal plant species evolved. Hypothetically its abundant congener A. ligulata A. Cunn. where A. mellifera has naturalized are it is an indicator of the quantity of pollen ex Benth., which displays high fecundity solitary. As a result of its sociality and transfer required to maintain population (Gilpin et al. 2014). In China native bumble behavior, A. mellifera makes up a very growth rate. Although A. mellifera is a sin­ bees deposited more pollen during their first high proportion of pollinator individuals gle introduced species, the sheer abundance floral visit to the endemic plantPedicularis in any natural area where it is found. The of A. mellifera in most systems can trans­ densispica Franchet ex Maximowicz, but presence of A. mellifera therefore exerts form patterns of pollination in a region, A. mellifera significantly elevated overall a strong influence on pollination patterns giving A. mellifera a disproportionate effect seed set for the species by increasing (stemming from foraging distance and on community dynamics. This abundance out-crossing (transfer of pollen between foraging preferences) in inhabited sites results in a high number of visits and, plants) (Sun et al. 2013). In Spain, native (e.g., Steffan-Dewenter and Tscharntke probabilistically, a high occurrence of seeds Crataegus monogyna L. and Vaccinium 2000; Jha and Vandermeer 2009), even attributable to A. mellifera visits (Rader et myrtillus L. displayed higher fruit set when though A. mellifera is a single species and al. 2009). Efficiency, on the other hand, is an A. mellifera apiary was located closer native bees may comprise dozens or hun­ generally assessed as the amount of seed to the plants, although this effect was not dreds of species in a particular locale. The set resulting from each visit: a high-effi­ observed for Prunus avium L. (Cayuela et introduction of A. mellifera has altered the ciency pollinator can generate high seed al. 2011). Native bees and A. mellifera were behavioral and ecological characteristics set with fewer individual visits (Rader et equally effective pollinators when fruit set of pollinators within both the agricultural al. 2009). Some studies have demonstrated was examined following single visits from and natural landscape. low efficiency of A. mellifera as a pollina­ each potential pollinator for Psychotria tor of native plants. This is because each carthagenensis (Faria and Araujo 2015), Apis mellifera is able to partner with a individual visit results in lower seed set and also for Dillwynia juniperina Lodd. large number of plant species because of than a visit by native bees, although effec­ in Australia (Gross 2001). The endemic its morphology and behavior, making it a tiveness may be high (Westerkamp 1991; herb P. densispica exhibited enhanced re­ supergeneralist interactor (Giannini et al. Osorio-Beristain et al. 1997; Spira 2001). production and constant outcrossing rates 2015). Direct competition for resources Very different patterns have been observed following introduction of A. mellifera, between A. mellifera and native bees may elsewhere; the efficiency of A . mellifera suggesting that A. mellifera was as effective also indirectly impact the fitness of native visits to two native species of Jatropha in a pollinator as the native bumblebee (Xia plants through declines in native bees Brazil, for example, was extremely high et al. 2007). Both A. mellifera and native (Abrol 2012). An early review identified (100% and 85%, respectively) (Neves and bees adjust their foraging in response to unrelated correlates of A. mellifera intro­ Viana 2011). This result was attributable seasonal floral changes that occur in the duction impacting both native plants and to the generalist floral characteristics of native tree Magnolia grandiflora L. (Allain native bees, and claimed a lack of evidence Jatropha: the flowers are easily accessible et al. 1999). The native shrub Dillwynia of direct negative effects on native biota to A. mellifera due to their size and shape. sieberi Steud. was visited primarily by A. from introductions of A. mellifera (Huryn Such generalist characteristics are likely mellifera in revegetated pastures, whereas 1997). Since then, a large number of to sustain pollination for many plants in native pollinators dominated in remnant studies have explored the various roles of transformed ecosystems by enabling them native woodland patches; total seed set was A. mellifera in natural areas, finding that to interact with nonnative visitors such as A. similar between the two site types (Lomov effects vary widely by context, and we mellifera (Schweiger et al. 2010). Similarly, et al. 2010). As these examples illustrate, A. review these studies here. A. mellifera was the most frequent visitor to mellifera has been shown to be an effective the California native Triteleia laxa Benth. pollinator of some native plants. Effectiveness and Efficiency of Honey and appeared to be responsible for most Bees as Interactors with Individual seed set (Chamberlain and Schlising 2008). In other cases, A. mellifera appears to be Native Plant Species an ineffective pollinator of native plant In Brazil, A. mellifera is the principle species. Compared to visitation by A. The effectiveness of A. mellifera as a pol­ pollinator of the native plant Melochia mellifera, more seed set was produced by linator of native plants varies enormously tomentosa L. (Machado and Sazima 2008). native pollinator visitation to the native among plant species and systems. The One study in Hawaiian forests where avian plant Phacelia parryi Torrey in California

Volume 36 (4), 2016 Natural Areas Journal 479 (Bruckman and Campbell 2014), native native community pollination, knowledge faced with the need to balance pollination bird visitation to the native Kniphofia for many systems is too limited to draw management (perhaps by management of linearifolia Baker in South Africa (Duffy confident comparisons. A. mellifera colonies) and nonnative plant et al. 2013), native hummingbird visitation species control. to the native cactus Melocactus intortus Honey Bees as Pollinators of Link and Otto in Puerto Rico (Fagua and Nonnative Plant Species in Natural The Position of Honey Bees Ackerman 2011), and native parrot visi­ Areas in Pollination Networks and tation to the native Eucalyptus globulus Communities Labill. in Tasmania (Hingston et al. 2004). Because of its highly generalist behavior Exclusion of birds reduced seed set of and morphology, A. mellifera often pol­ Apis mellifera can interact with large the native Australian shrub Brachyloma linates nonnative plant species, with the numbers of species and potentially alter the ericoides (Schltdl.) Sond., but exclusion of potential to facilitate spread rates (Stokes composition of ecological communities, A. mellifera did not (Celebrezze and Paton et al. 2006). Such dynamics could affect but its role varies widely across time and 2004). Apis mellifera appeared relatively natural areas by increasing invasiveness of space. For Eucryphia cordifolia Behr & F. ineffective at promoting outcrossing of rare nonnative plants requiring management. Muell., a native tree in Chile, only three plant individuals of Persoonia spp. (Rymer These effects have been documented in out of 137 pollinators were observed in et al. 2005). Apis mellifera was found to highly disturbed locations such as in Aus­ every year of a ten-year study; A. mellifera steal 99% of the pollen grains of the native tralia and New Zealand (Goulson 2003). dominated at times, but not always (Smith- Clusia arrudae Planchon & Triana, and Pollination by A. mellifera is responsible Ramírez et al. 2014). Spatial variation there was a negative correlation between for the spread of the invasive Lantana may be important, as well. In native and frequency of A. mellifera visits and seed camara L. in Australia (Goulson and introduced ranges of Hedysarum coronar­ set (Carmo et al. 2004). For the native plant Derwent 2004). In Tasmania, the invasive ium D., a perennial native to Spain, seed Melastoma affine L. in Australia, A. mellif­ ecosystem engineer Lupinus arboreus set and pollinator richness were greater in era deposited less pollen and removed more Sims is pollinated by A. mellifera (Stout the native than the introduced range, but pollen than native bees and also disturbed et al. 2002). When the nonnative Acacia pollen loads on A. mellifera were equivalent the foraging of native pollinators (Gross saligna (Labill.) H.L.Wendl. was present in the two locations (Montero-Castaño et and Mackay 1998). in South African study sites, visitation to al. 2014). the native Roepera fulva L. was reduced; Effectiveness of A. mellifera compared to A. mellifera is largely responsible for Some studies of communities have shown native pollinators is often unknown (e.g., the high floral visitor overlap, and thus that A. mellifera was the most frequent Kaiser-Bunbury and Müller 2009). For a pollination competition, between the two flower visitor, such as in a Garry oak suite of endemic Cunoniaceae plants in species (Gibson et al. 2013). In Kansas, the ecosystem in Canada and an endemic New New Caledonia, A. mellifera is a common invasive Lespedeza cuneata (Dum.Cours.) Caledonian ecosystem (Kato and Kawakita flower visitor along with native insects, G.Don, but not its native congeners, was 2004; Parachnowitsch and Elle 2005). birds, bats, and geckos (Hopkins et al. visited frequently by A. mellifera (Woods However, A. mellifera visited only a small 2015), but the effectiveness of A. mellifera et al. 2012). In California and Oregon, proportion of all local floral species in a compared to that of native visitors has not A. mellifera is the principal pollinator of regrowth forest patch in Brazil (Pedro and been explored. In Australia, A. mellifera the nonnative Centaurea solstitialis L. De Camargo 1991), in forested systems began foraging on Eucalyptus costata (Barthell et al. 2001; Mciver et al. 2009; in the Philippines (Fajardo and Cervancia Behr & F. Muell. flowers earlier in the Swope and Parker 2010), a major rangeland 2003), in wildflower gardens in Montana day than native pollinators, but collected invader. In South Africa, A. mellifera is (Pearce et al. 2012), and in New Zealand pollen rather than nectar. The overall im­ the primary pollinator of nonnative Arau­ honey production (Huryn 1997). By con­ pact on E. costata reproduction of a switch jia sericifera Brot. (Coombs and Peter trast, 23 out of 43 native plants were visited to pollination by A. mellifera rather than 2010). Examining a broad community of by A. mellifera in managed field margins in native pollinators is unclear (Horskins and interacting native and nonnative species, Michigan (Tuell et al. 2008). Fragmented Turner 1999). On Tenerife, an island with nonnative pollinators including A. mellif­ systems in the Argentinian chaco serrano a restricted number of individual plants era were significantly more likely to visit were dominated by A. mellifera, with due to small land area, plants at a site with nonnative than native plants (Morales and smaller fragments exhibiting increasing high occurrence of A. mellifera demon­ Aizen 2006). Similar effects have been occurrence of A. mellifera relative to native strated rapid nectar depletion and higher observed in many systems; pollination by insect species (Aizen and Feinsinger 1994). frequency of visits to multiple flowers A. mellifera and other exotic pollinators Similar context dependence was observed on the same plant; seed set and viability, likely exacerbates plant invasions in many for pollination of Schinus terebinthifolius however, appeared unaffected (Dupont natural areas (Hanley and Goulson 2003). (Cham. and Schlecht.) F. Muell., which et al. 2004). Although the importance of Therefore, the interaction between A. mel­ was visited predominantly by A. mellifera A. mellifera in natural areas can only be lifera and nonnative plants is a necessary in beach grass shrubland but by native satisfactorily evaluated with reference to consideration for natural area managers halictid bees in restinga forest (Cesario

480 Natural Areas Journal Volume 36 (4), 2016 and Gaglianone 2013). Cresson and nonnative A. mellifera (Tuell 2009). A lengthy study of native bee popu­ et al. 2008). lations on Barro Colorado Island following The generality of A. mellifera is pervasive colonization of the island by A. mellifera in networks. In mutualisms such as polli­ Broad community context affects the role of found no measurable competitive effect of nation, a specialist interactor is one that A. mellifera. In the Seychelles, A. mellifera the nonnative (Roubik and Wolda 2001). interacts with one, or perhaps a restricted altered plant linkage and interaction even­ guild of partner species. Generalist in­ ness in networks including large numbers Competition between A. mellifera and teractors (whether plants or pollinators) of nonnative plants (Kaiser-Bunbury et al. native pollinators is likely to be highest will interact with many and diverse 2011). For coflowering Asclepias species, when the ecological requirements of the species, with supergeneralist interactors visitation frequency and, by extension, two groups are similar (Dohzono and A. interacting with a very high diversity of pollinator importance of A. mellifera vs. Yokoyama 2010). In New Caledonia, mellifera is “ubiquitous,” and competes partners. Generalization is more common native insect species varied by plant species with native bees for nectar and pollen than specialization in pollination (Johnson even among such similar plants (Theiss et al. 2007). In burned and unburned sites, (Donovan et al. 2013). In protected areas in and Steiner 2000; Waser 2006). In shru­ nonnative A. mellifera and B. terrestris as Israel, A. mellifera introduction resulted in bland ecosystems in Mexico, A. mellifera well as native bees were primary visitors decreased frequency of floral visitation by dominated the pollinator community in to Satureja thymbra L., and seed set was native bees (Shavit et al. 2009). Proximity both a conservation area and a disturbed high in both habitats (Potts et al. 2001). In to A. mellifera hives reduced reproductive area (Campos-Navarrete et al. 2013). Apis disturbed islands within the Bonin Islands, success and altered the foraging strategy mellifera performed the majority of flower A. mellifera dominated visitation to both of native Bombus occidentalis Greene in­ visits in a frequently disturbed cerrado-at­ native and nonnative flowers and were dividuals (Thomson 2004). Niche overlap lantico forest site, perhaps demonstrating seasonally dependent on nonnative flowers; between A. mellifera and native Melipona the capacity of the species to quickly this contrasted with intact native communi­ bees in Brazil indicated competition for recolonize after disturbance (Polatto and ties on less disturbed islands, which were nectar (Wilms and Wiechers 1997). For Chaud-Netto 2013). In a Pantanal, Brazil, dominated by native bees (Kato et al. 1999). two Sideroxylon tree species in Mauritius, network, the most generalist bee species Depending on its abundance, the role of A. mellifera was a low-efficiency pollinator was A. mellifera, visiting 27 out of 63 plant A. mellifera varies across communities, but depleted nectar each day, likely interfer­ species (Boff et al. 2013). but its generality gives it the potential ing with the native mutualism (Hansen et to heavily influence the structure of any al. 2002). Apis mellifera could also impact In network calculations, A. mellifera given network. native bees through pathogen transmission exhibits high centrality, uniting multiple and reproductive interference, but these modules with its generalist interaction have been less studied than competition behavior (Santos et al. 2012). In the Impact of Honey Bees on Native (Stout and Morales 2009). When natural Brazilian caatinga, A. mellifera strongly Pollinators area managers are concerned about native affected network structure by reducing pollinators, it may be important to consider modularity and increasing nestedness (San­ When competing for limiting resources, A. broad availability of flowering plants and tos et al. 2012). Modularity measures the mellifera may be expected to impact native densities of A. mellifera to determine how amount to which a network of interactors pollinators (Thomson 2004; Traveset and much the non-native bee may compete is divided into a number of natural subsets Richardson 2006; Shavit et al. 2009). Tests with natives. wherein species interact much more with of such effects, once again, indicate that each other than with species outside the context matters. Habitat fragmentation was As our review demonstrates, the role of subset (Olesen et al. 2007). Nestedness associated with declines in native insects A. mellifera in natural ecosystems and refers to the tendency of specialist species and increases in A. mellifera abundance communities is context-dependent. When to interact with generalists (James et al. in Argentina, but there was not strong ev­ evaluating the impact of A. mellifera in a 2012). A. mellifera impacts these metrics idence in that system that A. mellifera itself particular system, natural area managers by partnering with a high proportion of contributed to the native bee decline (Aizen must consider effects on native plants, the species in the system, changing the and Feinsinger 1994). In Brazil, however, nonnative plants, and native pollinators. linkages of native species with one anoth­ studies have indicated that declines in Those impacts will vary according to the er. In study systems in Brazil and South native bees may be due at least in part to abundance of A. mellifera, the level of Africa, A. mellifera was the most abundant competition with A. mellifera (Martins et ecological similarity between A. mellifera species, again generating high nestedness al. 2013) and that depletion of Spondias and native pollinators, and the relative via its generalist behavior (Dubet da Silva mombin L. pollen by A. mellifera reduced effectiveness of A. mellifera vs. native Mouga et al. 2012; Gibson et al. 2012). native bee foraging benefit (Carneiro and pollinators for particular plant species of In a common garden in the eastern US, Martins 2012). Niche overlap between A. concern. Apis mellifera pollinates some pollination of native plants was heavily mellifera and native bumble bees depended native plants successfully, even replacing dominated by native Bombus impatiens on total floral resource availability (Franco extinct pollinators in certain cases, but

Volume 36 (4), 2016 Natural Areas Journal 481 it interferes with effective pollination of we present here preliminary data relevant of 1510 minutes, and V. reticulatum Sm. for other native plants. The pollination needs to three cooccurring native plant species a total of 1530 minutes. Plants flowered on a of a given natural system, the conservation in early successional mesic forest on the rolling basis, therefore observations moved status of native pollinators, and the relative Island of Hawai’i. among flowering plants on each succeeding occurrence of specialist vs. generalist pol­ observation day. In all, 32 M. polymorpha METHODS linators may all be important determinants individuals and 231 flowers were observed, of the relative costs vs. benefits of A. mel­ 45 S. tameiameiae individuals and 663 To quantify the relative importance of A. lifera introductions and may influence A. flowers were observed, and 41 V. reticu­ mellifera vs. native species as pollinators mellifera management decisions. latum individuals and 1224 flowers were of native plant species in Hawai’i, we performed flower visitation observations observed. Each 10-minute observation period was divided into a 1-minute scan CASE STUDY: Honey Bees vs. for three common Hawaiian plant spe­ cies: endemic Metrosideros polymorpha sample and a 9-minute focal individual Native Bees as Pollinators of Native observation period (Aslan 2011; Aslan et Gaudich. (ʻōhiʻa, Myrtaceae), endemic al. 2014). During the scan sample, focal Hawaiian Plants Styphelia tameiameiae (Cham. and Schlt­ plants were observed from a fixed point to dl.) F. Muell. (pūkiawe; Ericaceae), and determine the total number of individuals The Hawaiian Islands have been heavily native Vaccinium reticulatum Sm. (ʻōhelo impacted by humans and exhibit very high of each species of flower visitor interacting ʻai; Ericaceae). For all of these species, we extinction rates (e.g., Hadfield et al. 1993; with the focal flowers. During the focal had casually observed visitation of both A. Boyer 2008). Hawai’i is the most isolated individual observation period, individual mellifera and native bee species (especially archipelago on the planet (Price 2004); visitors were observed, and the observer Hylaeus spp.) before conducting the pres­ only a restricted suite of species have been recorded the number of flowers visited as ent study. We quantified flower visitation able to colonize Hawai’i on their own, well as visitor behavior (pollen or nectar by A. mellifera and other pollinators using resulting in a limited diversity of native foraging, nectar robbing, etc.) during those systematic visitation observations. All ob­ species within any given functional group visits. New focal individuals were selected servations were performed over six weeks (Eldredge and Evenhuis 2003). This low and observed in sequence as long as they in the summer of 2015 at a montane mesic diversity leaves a high number of vacant were present until the 9-minute period had forest site on Mauna Loa Volcano, Hawaiʻi niches, allowing rapid diversification and ended, at which point the observation block Island, at approximately 1200 m elevation. adaptive radiation and the evolution of ended and a new block began with a new Because these data were collected in one unique forms and specialized interactions scan sampling period. flowering season and one study site, we (Price and Clague 2002). Hawaiian pol­ consider them to be preliminary; our next lination was historically dominated by a step is to expand these data collection Analysis restricted number of native bees, butterflies, methods to a wider diversity of endemic and moths, and a remarkably high propor­ plants, additional field sites, and multiple Flower visitation observation data were tion of native plants are bird-pollinated years of data collection. Additionally, we used to calculate Pollinator Importance (Wagner et al. 1999). Due to habitat loss, report here solely observational flower (adapted from Renne et al. 2000; Aslan invasion of exotic predators, and rampant visitation data, determined to be effective et al. 2014; Aslan 2015), a systematic introduced disease, native pollinators in in some systems (Vázquez et al. 2005) method of comparing visitor importance Hawai’i have experienced high extinction and ineffective in others (King et al. 2013) (sensu Renne et al. 2000) and identifying rates (Cox and Elmqvist 2000). Given at identifying pollinators; to supplement important visitors as those that visited such widespread extinction among native these observations and further explore the large numbers of flowers or were present pollinators, A. mellifera may be critical role of particular visitor groups, we are in high abundance. Pollinator Importance to reproduction of a diversity of endemic currently performing controlled pollination (FPI) is calculated as the average number and native plants. However, because A. treatments on flowers of these species to of visiting individuals of each flower vis­ mellifera is highly generalist and differs evaluate fruit and seed set in the absence behaviorally from native pollinators, it is itor group per minute from scan samples, and presence of A. mellifera visitation. unlikely that A. mellifera wholly replaces multiplied by the total number of flowers endemic pollinators as a partner of all plant visited by each individual per minute, for species. Furthermore, current declines in A. Flower Visitation Observations each plant/flower visitor combination. This mellifera populations in Hawai’i could in­ total flower visitation is then divided by dicate that A. mellifera’s relative abundance Observations took place in July and August the total average number of open flowers in pollinator communities may decline in 2015. Plants were observed in 10-minute observed. We examined resulting FPI val­ the future. We set out to understand the blocks by four observers. Metrosideros ues to determine which visitors emerged relative importance of A. mellifera vs. polymorpha Gaudich. was observed for as most important, and compared those native species as pollinators of a diversity a total of 1610 minutes, S. tameiameiae values using a simple one-way analysis of native plant species in Hawai’i, and (Cham. and Schlecht.) F. Muell. for a total of variance for each focal plant species.

482 Natural Areas Journal Volume 36 (4), 2016 RESULTS Implications suggested that native Hylaeus bees were by far the most important visitors for both The visitor taxon with highest FPI across Because observations took place within species, followed by nonnative Syrphidae all three focal plant species was native a single season and because visitation spp., with A. mellifera as significantly less Hylaeus spp. bees (Figure 1). This result data alone can vary in significance based important (Figure 1). was largely driven by the tendency of Hy­ on system, we consider these results preliminary and will expand this study to laeus bees to visit multiple flowers within CONCLUSIONS a single observation (Table 1). FPI values encompass flower treatments as well as for A. mellifera and Hylaeus as visitors additional plant species in future seasons. The impact of A. mellifera on pollination of M. polymorpha were quite similar Nevertheless, these initial results imply in natural areas is context-dependent, and considerably greater than values for that the effectiveness of A. mellifera in this varying by focal plant species and by system is once again context-dependent. the other flower visitors (Lepidopteran ecological community. Apis mellifera For M. polymorpha, A. mellifera exhibited moths, Hymenopteran wasps, and nonna­ acts as an effective pollinator of gener­ the second greatest FPI, but its importance alist plants, in particular, and occupies a tive Syrphidae flies; and the native birds did not differ significantly from that of Vestiaria coccinea Forster and Himatione highly influential role in interaction net­ the native Hylaeus bees (Figure 1). This works but is likely to serve in many cases sanguinea Gmelin and nonnative Zosterops result contrasted somewhat with results as an imperfect replacement for native japonicas Temminck and Schlegel . For ) exploring pollination of M. polymorpha in pollinators. In some circumstances, such the Ericaceae species S. tameiameiae and a lower-elevation system further south on as for plants with specialist floral charac­ V. reticulatum, Hylaeus again exhibited Hawaiʻi Island, wherein A. mellifera was teristics requiring specialized morphology the highest FPI, with A. mellifera visiting found to be the most important pollinator or behavior on the part of pollinators, A. flowers much more rarely than Hylaeus. (Hanna et al. 2013); the relative importance mellifera may be ineffective compared One-way analysis of variance results re­ of A. mellifera in pollinator networks may with native pollinators; in other cases, vealed significant differences among FPI vary even over relatively short spatial the high abundance typical of A. mellifera only for S. tameiameiae (F = 22.63; P < distances and within ecosystem types and populations may generate high pollination 0.0001; df = 2). Due to large variances, between years. rates for certain native species. In some there were no significant differences in FPI systems, A. mellifera appears to compete for visitors of M. polymorpha (F = 0.104; Apis mellifera as a pollinator appeared with native pollinators for resources. This P = 0.996; df = 6) or V. reticulatum (F = even less important for S. tameiameiae is most likely when niche overlap is great 1.43; P = 0.262; df = 2). and V. reticulatum. Visitation observations and floral resources limited and is a phe-

Table 1. Components of flower visitation importance (FPI) for each visitor taxon to each focal native plant species. Overall FPI for each visitor taxon is calculated from presence (i.e., the average number of visitors of each taxon per unit time) and activity (i.e., the average number of flowers visited by each visitor). The native Hylaeus spp. bees exhibited the highest FPI for all three plant species.

Visitor taxon Importance ± SE Presence ± SE Activity ± SE Plant species Metrosideros polymorpha Apis mellifera 0.13 ± 0.02 0.069 ± 0.0054 1.88 ± 0.14 Hylaeus spp. 0.14 ± 0.19 0.031 ± 0.006 4.49 ± 0.36 Vestiaria coccinea 0.0050 ± 0.05 0.00049 ± 3.94E-05 10.09 ± 1.82 Zosterops japonicus 0.013 ± 0.21 0.00093 ± 0 13.44 ± 4.22 Lepidopteran ± 0 0.00018 ± 0 0.34 ± 0 Himatione sanguinea 0.011 ± 0.17 0.0021 ± 0 5.50 ± 0.5 Hymenopteran wasps 0.0025 ± 0.038 0.00048 ± 0 5.22 ± 0 Styphelia tameiameiae Apis mellifera 0.017 ± 0.0024 0.0036 ± 0.00023 4.62 ± 0.57 Hylaeus spp. 0.25 ± 0.026 0.044 ± 0.0042 5.60 ± 0.23 Syrphidae 0.067 ± 0.013 0.015 ± 0.0016 4.45 ± 0.75 Vaccinium reticulatum Apis mellifera 0.0024 ± 0.00072 3.2 ± 0.8 0.00076 ± 0.00012 Hylaeus spp. 0.030 ± 0.0096 3.51 ± 0.6 0.0085 ± 0.0023 Syrphidae 0.0072 ± 0.0019 2.86 ± 0.6 0.0025 ± 0.00039

Volume 36 (4), 2016 Natural Areas Journal 483 Although its close ties to human agriculture have led to its successful spread around the globe, A. mellifera currently faces a number of emerging threats. Factors such as pesticide use, habitat loss, and disease and parasite introductions are likely culprits in current A. mellifera declines (Ball and Allen 1988; Genersch 2010; Johnson et al. 2010). Colony infestation by the Varroa destructor (Anderson & Trueman) mite reduces colony resource reserves during winter months and causes significant A. mellifera losses, especially in northern regions (Guzmán-Novoa et al. 2010), implying that in many cases A. mellifera will not persist in northern natural areas without active management. Extreme hab­ itat loss is also correlated with significant declines in diversity and abundance of bees (Winfree et al. 2009; Abrol 2012; Goulson et al. 2015). The predominance of plant monocultures in agriculture and resulting lack of pollen and nectar diversity have also been identified as potential stressors for A. mellifera (Decourtye et al. 2010). Proximity of forest habitats to agricultural areas boosted bee diversity in Costa Rica (Brosi et al. 2007). Where A. mellifera is native, the presence of game reserves appears to increase the density of hives, perhaps bolstering bee populations (Vaudo et al. 2012). Network analysis implies that plant species with fewer pollinator species are most at risk of negative impact from pollination disruption resulting from loss of those pollinator species (Spira 2001). The presence of natural areas and diverse native species appears essential to conservation of pollination as a service, whether mediated by A. mellifera or native pollinators.

Maintaining large, structurally-diverse expanses of habitat may be key to sus­ taining maximum richness of pollinator species (Kearns et al. 1998; Spira 2001). Figure 1. FPI of flower visitors to three native Hawaiian plant species, quantified via flower visitation Habitat can be maintained or increased by observations recording visitor presence and behavior. (a) For Metrosideros polymorpha, the most import­ planting native host plants (Dumroese et al. ant visitors were the native Hylaeus spp. bees, but A. mellifera was only marginally less important. (b) Hylaeus spp. bees were also the most important visitors for Styphelia tameiameiae, with much smaller 2016 this issue pps. 499-511), following importance attributed to A. mellifera. (c) Similarly, Hylaeus spp. bees were by far the most important best management practices with regard to visitors to Vaccinium reticulatum, with little visitation by A. mellifera. Bars represent mean importance nonnative plant species, forest conditions, ± standard error. and roadside and powerline corridors (Hanula et al. this issue pps. 427-439), nomenon that could restructure interaction on the floral characteristics of those plants and managing the timing and intensity networks and ecological communities. The and their communities as well as on the of ungulate grazing (DeBano et al. 2016 role of A. mellifera as a pollinator of rare diversity of the extant native pollinator this issue pps. 458-477). Apis mellifera or conservation-dependent plants depends community. is integrated into many natural areas and

484 Natural Areas Journal Volume 36 (4), 2016 interacts with hundreds of native plant etates nearby wild margins with native, Varroa jacobsoni. Annals of Applied Biol­ species, but its generality makes it unlikely pollinator-friendly annual and perennial ogy 113:237-244. to replicate the function of diverse commu­ flowers every spring and fall. Barthell, J.F., J.M. Randall, R.W. Thorp, and nities of native pollinators in natural areas. A.M. Wenner. 2001. Promotion of seed set Kimberly Hill is a student at the SUNY in yellow star-thistle by honey bees: Evi­ Natural area managers concerned about dence of an invasive mutualism. Ecological native plant reproduction should assess the College of Environmental Science and Applications 11:1870-1883. Forestry in the Natural Resources Man­ effectiveness of A. mellifera as a pollinator Biesmeijer, J.C., S.P.M. Roberts, M. Reemer, of target plant species when determining agement Program. She will graduate with R. Ohlemüller, M. Edwards, T. Peeters, A.P. how to manage A. mellifera populations. In a Bachelor’s of Science with focuses in Schaffers, S.G. Potts, R. Kleukers, and C.D. many cases, management efforts to boost Water Resources and Recreation Resource Thomas. 2006. Parallel declines in pollina­ native pollinator communities threatened and Protected Area Management. She is tors and insect-pollinated plants in Britain by habitat loss and environmental change currently a part of the Doris Duke Con­ and the Netherlands. Science 313:351-354. may be critical. servation Scholars Program at NAU and Boff, S., A.C. Araujo, and A. Pott. 2013. Bees is an Indigenous Environmental Leaders (Hymenoptera: Apoidea) and flowers in for the Future fellowship recipient at her natural forest patches of southern Pantanal. Biota Neotropica 13:46-56. ACKNOWLEDGMENTS college. Bommarco, R., D. Kleijn, and S.G. Potts. 2013. Ecological intensification: Harnessing eco­ Funding was provided by the Strategic Walter Topete is a junior at the University of Environmental Research and Development system services for food security. Trends in Houston pursuing a degree in biology with Ecology and Evolution 28:230-238. Program and the Doris Duke Conserva­ a minor in chemistry and energy and sus­ Boyer, A.G. 2008. Extinction patterns in the tion Scholars Program. We further thank tainability. As a Doris Duke Conservation avifauna of the Hawaiian Islands. Diversity the Doris Duke Charitable Foundation Scholar, he has interned and worked with and Distributions 14:509-517. and Doris Duke Conservation Scholars NAU’s Department of Forestry and Land­ Brosi, B.J., G.C. Daily, and P.R. Ehrlich. 2007. Program for the enormous logistical and scape Conservation Initiative in Arizona Bee community shifts with landscape con­ training support provided throughout the as well as on Hawaii’s Big Island. When text in a tropical countryside. Ecological Applications 17:418-430. field study. Thanks to Heather Coad and not tutoring students, he can be found on Kristen Potter for their invaluable logistical the rugby field or playing guitar. Bruckman, D., and D.R. Campbell. 2014. Floral and field elp.h neighborhood influences pollinator assem­ blages and effective pollination in a native plant. Oecologia 176:465-476. Clare Aslan is an Assistant Professor with LITERATURE CITED Campos-Navarrete, M.J., V. Parra-Tabla, J. the Landscape Conservation Initiative at Ramos-Zapata, C. Díaz-Castelazo, and E. Northern Arizona University and a Se­ Abrol, D.P. 2012. Consequences of introduced Reyes-Novelo. 2013. Structure of plant– Hymenoptera networks in two coastal shrub nior Scientist with Conservation Science honeybees upon native bee communities. Pp. 635–667 in D.P. Abrol, ed., Pollination sites in Mexico. Arthropod-Plant Interac­ Partners. Her research focuses on the im­ Biology. 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Apidologie 43:474-486. biodiversity, particularly in the face of seed-dispersal mutualisms between birds Cayuela, L., S. Ruiz-Arriaga, and C.P. Oz­ environmental change, working in Hawaiʻi and introduced plants in northern California, USA. Biological Invasions 13:2829-2845. ers. 2011. Honeybees increase fruit set in and California. Current projects investigate native plant species important for wildlife the persistence of endemic species as well Aslan, C.E, E.S. Zavaleta, B. Tershy, D. Croll, conservation. Environmental Management as the ecological impacts of non-native and R.H. Robichaux. 2014. Imperfect re­ 48:910-919. invasive wildlife species. placement of native species by non-native species as pollinators of endemic Hawaiian Celebrezze, T., and D.C. Paton. 2004. Do introduced honeybees (Apis mellifera, plants. Conservation Biology 28:478-488. Ben Galindo is a senior Environmental Hymenoptera) provide full pollination Aslan, C.E. 2015. 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Volume 36 (4), 2016 Natural Areas Journal 487 Santos, G.M. de M., C.M. Aguiar, J. Genini, C.F. the effect of exotic pollinators on exotic colony strength parameters in the Eastern Martins, F.C. Zanella, and M.A. Mello. 2012. weed population dynamics: Bumblebees Cape, South Africa. Journal of Insect Con­ Invasive Africanized honeybees change the and broom in Australia. Diversity and Dis­ servation 16:601-611. structure of native pollination networks in tributions 12:593-600. Vázquez D.P., W.F. Morris, and P. Jordano. Brazil. Biological Invasions 14:2369-2378. Stout, J.C., A.R. Kells, and D. Goulson. 2002. 2005. Interaction frequency as a surrogate Schweiger, O., J.C. Biesmeijer, R. Bommarco, Pollination of the invasive exotic shrub for the total effect of animal mutualists on T. Hickler, P.E. Hulme, S. Klotz, I. Kühn, Lupinus arboreus (Fabaceae) by introduced plants. Ecology Letters 8:1088-1094. bees in Tasmania. Biological Conservation M. Moora, A. Nielsen, R. Ohlemüller, T. 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Pollinator diversity and crop pollina­ Tuell, J.K., A.K. Fiedler, D. Landis, and R. Woods, T.M., J.L. Jonas, and C.J. Ferguson. tion services are at risk. Trends in Ecology Isaacs. 2008. Visitation by wild and managed 2012. The invasive Lespedeza cuneata and Evolution 20:651-652. bees (Hymenoptera: Apoidea) to eastern attracts more insect pollinators than native congeners in tallgrass prairie with variable Steffan-Dewenter. I., and T. Tscharntke. 2000. US native plants for use in conservation impacts. Biological Invasions 14:1045-1059. Resource overlap and possible competition programs. Environmental Entomology between honey bees and wild bees in central 37:707-718. Xia, J., S.G. Sun, and Y.H. Guo. 2007. Honey­ Europe. Oecologia 122:288-296. bees enhance reproduction without affecting Vaudo, A.D., J.D. Ellis, G.A. Cambray, and M. the outcrossing rate in endemic Pedicularis Stokes, K.E., Y.M. Buckley, A.W. Sheppard. Hill. 2012. 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