Ecological Impacts of Invasive Alien Species on Bees*

Apidologie 40 (2009) 388–409 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2009 www.apidologie.org DOI: 10.1051/apido/2009023 Review article

Ecological impacts of invasive alien species on bees*

Jane C. Stout1,CarolinaL.Morales2

1 School of Natural Sciences, Trinity College Dublin, Dublin 2, Republic of Ireland 2 Laboratorio Ecotono, INIBIOMA (CONICET-Universidad Nacional del Comahue), Pasaje Gutiérrez 1125, 8400, Bariloche, Río Negro, Argentina

Received 29 September 2008 – Revised 13 January 2009 – Accepted 15 January 2009

Abstract – We review direct and indirect impacts of invasive alien species (focussing on plants and insects) on native bees worldwide. Although there is a rapidly growing body of research into the effects of invasive alien plants on native plant pollination via disruption of native mutualisms, there has been little research on the impacts of invasive alien plants directly on bees. Such impacts are likely to vary according to the taxon of plant, the functional specificity of the native bees, and ecosystem context. Conversely, there have been more attempts to document impacts of invasive alien social bees on native bees. Most of these studies only indirectly evaluate competition for resources, have focused on a few native species and findings are sometimes contradictory. However, some studies showed strong negative impacts, suggesting that effects might be species-specific. Additionally, pathogen spillover and reproductive disruption due to interspecific mating has been demonstrated among some closely related taxa. Where we lack unequivocal evidence for impacts however, this should not be interpreted as lack of effect. We recommend that future studies are robustly designed and consider impacts on genetic, species (particularly solitary bees) and ecosystem biodiversity.

Apis mellifera / Bombus / non-native species / pollinator / plant invasion

1. INTRODUCTION the trade and transport of species, has led to a corresponding increase in research into the Alien species (exotic/non-native species in- impacts of invasive alien species (Lockwood troduced accidentally or intentionally by hu- et al., 2007). In addition to damage to human mans) that become invasive (i.e. recruit repro- health and economies (Pimentel et al., 2005), ductive offspring, often in large numbers and invasive alien species can in some cases dis- at considerable distances from parents, and rupt evolutionary process, and the composition thus can spread at a considerable rate, Traveset and functioning of local ecosystems (Parker and Richardson, 2006) are recognised as im- et al., 1999; Mooney and Cleland, 2001). In- portant drivers of global environmental change vasive alien species can have direct and in- (Sala et al., 2000; Levine and D’Antonio, direct impacts on native biodiversity (Parker 2003). Although only a small proportion of et al., 1999). The former occur when invasive ff alien species become invasive (Williamson, aliens consume or otherwise physically a ect 1996), the massive increase in the rate of bi- native species, and the latter when the inva- ff ological invasions due to rapid globalization sion a ects interactions among native species of economies in the last decade, accelerat- in the ecosystem, for example via competition ing both the rate and geographic pattern of for biotic resources, or via alteration of abiotic resource availability, either by competition or Corresponding author: J.C. Stout, when invasive aliens perform a novel ecosys- ff [email protected] tem function (Simberlo , 1991; White et al., * Manuscript editor: Tomas Murray 2006). In many cases, a combination of both

Article published by EDP Sciences Impacts of invasive alien species on bees 389 direct and indirect processes affect native bio- et al., 2009) and the impacts of these processes diversity and the services it provides. on native bees have been studied on a range of A key ecosystem service that has the poten- scales. For example, recent research has sug- tial to be interrupted by the arrival of novel gested that landscape structure and land use species is pollination. This area has received management have important impacts on native a lot of recent research attention for sev- bees (Brosi et al., 2008; Osborne et al., 2008) eral reasons. Firstly, there is widespread con- and that organic farming can improve bee cern about loss of pollination services, both species abundance (Tscharntke et al., 2005; for wild plants and crops (Biesmeijer et al., Holzschuh et al., 2007). However, the impacts 2006; Klein et al., 2007); but see (Ghazoul, of invasive alien species on native bees are far 2005), and investigations into the drivers of from clear (Traveset and Richardson, 2006). pollinator loss are regarded as high priority We lack knowledge as to the extent at which (Steffan-Dewenter and Westphal, 2008). Sec- alien invasions affect population density of bee ondly, some high-profile invasions have re- species, and about how alien invasions affect ceived considerable media and research atten- composition of pollinator communities at dif- tion, for example the spread of Africanized ferent spatial and temporal scales (Bjerknes honeybees in the Americas (Schneider et al., et al., 2007). 2004; Moritz et al., 2005). Thirdly, because In this review, we aim to provide critical as- pollinators perform a vital ecosystem func- sessment of hypotheses and evidence for im- tion, impacts of alien species invasion can have pacts of invasive alien species that directly or knock-on effects on entire communities. indirectly affect native bees in order to identify Bees are arguably the most important polli- threats and to determine research and conser- nator group and threats to wild bees have been vation priorities in this area. Specifically, we more widely studied than impacts on other will consider impacts of invasive alien plants, pollinator taxa (Kenis et al., 2009; Murray bees and parasites on native bee behaviour, re- et al., 2009). Native (often referred to as production, populations and communities and “wild” bees, although this term strictly in- the ecological services they provide. cludes non-native domesticated species that have “escaped” into the wild) are very important for wild plant and crop pollination (Losey 2. IMPACTS OF INVASIVE ALIEN and Vaughan, 2006). Klein et al. (2007) esti- PLANTS mated that 35% of global crop production re- lies on animal pollinators and 87/115 of the Alien plant invasions are common in virtu- leading food crops worldwide require animal ally every terrestrial ecosystem on earth. The pollination. Many producers rely on domesti- number of plant introductions has climbed cated bees, but with worldwide declines in the steadily since the late eighteenth century most important domesticated bee (Apis mellif- (Pyšek et al., 2003), and in Europe, established era), the importance of native wild bees is be- alien plants are most common in nutrient-rich coming increasingly recognised. In the north- and/or man-made habitats (including urban eastern United States of America (New Jersey and agricultural ones) (Lambdon et al., 2008). and Pennsylvania), it has been predicted that A large proportion of alien plants have been in- native bees provide sufficient pollination for troduced as ornamental species, for example in watermelon crops in the absence of domesti- Australia (Groves, 1998; Reichard and White, cated honeybees (Winfree et al., 2007), con- 2001) and Europe (Lambdon et al., 2008), and firming the important role that native bees per- thus many produce showy, eye-catching flow- form in modern agro-ecosystems. ers, which also often makes them attractive to Habitat change, loss and fragmentation as- animal visitors. sociated with agricultural intensification are Many invasive alien plants are visited thought to pose the main risks to native bees (Valentine, 1978; Butz Huryn and Moller, (Kremen et al., 2002;Goulsonetal.,2008; 1995; Chittka and Schurkens, 2001; Moragues Steffan-Dewenter and Westphal, 2008; Murray and Traveset, 2005; Jesse et al., 2006;Stokes 390 J.C. Stout, C.L. Morales et al., 2006; Stout et al., 2006; Totland reduce visitation and hence their pollination et al., 2006; Lopezaraiza-Mikel et al., 2007; success) or non-existent (alien plants have no Bartomeus et al., 2008a; Tepedino et al., 2008) impacts on native ones). Indeed, studies so and pollinated (Parker, 1997;Richardsonetal., far have found a range of results (Tab. I), 2000; Stout, 2007) by native bees. These even for the same invasive alien plant species plants are attractive to native bees for many interacting with native taxa in different geo- reasons: some produce a massive floral dis- graphic localities. For example, Carpobrotus play, have prolific nectar production, and often spp. in California (Aigner, 2004), the Balearic appear at high density or dominate the flower Islands (Moragues and Traveset, 2005), and community in invaded sites (Ghazoul, 2002; north-eastern Spain (Bartomeus et al., 2008b) Bjerknes et al., 2007). In addition, many in- have varying impacts on different taxa of na- vasive alien plants fill a phenological gap of tive plants (Tab. I). In addition, interactions be- flower resources for bees, extending their for- tween the same alien and native plant species aging season. As a result, invasive alien plants at different locations have found contradictory have the potential to impact not only on indi- results. For example, the presence of Impa- vidual foraging behaviour, but also on colony tiens glandulifera decreased visitation to and success of social species, population size and seed set of Stachys palustris in Central Eu- distribution of native bees, bee community rope (Chittka and Schurkens, 2001) whilst structure and entire plant-pollinator networks Lopezaraiza Mikel (2006) found a facilitative (Aizen et al., 2008). In addition, by affecting effect on insect visitation in the UK, which var- the native plant communities, invasive alien ied with native plant density. Nienhuis et al. plants are likely to have indirect effects on na- (unpubl. data), on the other hand, found no im- tive pollinator communities. pact of varying I. glandulifera density on visitation, pollen deposition or seed set in S. palustris in a heavily invaded site in Ireland. Indeed, 2.1. Indirect impacts via effects on plant spatio-temporal variation in findings may well communities be due to not only plant (alien and native) but also pollinator density (Muñoz and Cavieres, Invasive alien plants can cause a reduc- 2008), which has not been fully addressed in tion in native plant abundance and/or diver- field studies so far. sity within a community (Pyšek and Pyšek, What is surprising, however, is that few 1995; Martin, 1999), although the mecha- studies have investigated the impacts of inva- nisms for impacts are not always clear (Levine sion by alien plants on the structure of pollina- et al., 2003). Invasive alien plants affect native tor communities, instead focussing on the im- plants via physical mechanisms (e.g. allelopa- pacts on native plant pollination (but see Aizen thy, smothering, strangling) or competition for et al., 2008). Knock-on effects of changes in abiotic resources (e.g. nutrients, light, space, plant community composition could have dra- water) (Lodge, 1993; Levine et al., 2003; Vilà matic implications for native pollinators, par- and Weiner, 2004). In addition, competition ticularly specialist species which are not able for biotic resources, such as pollination ser- to utilize the invasive alien plant because of vices, can cause changes to community com- temporal, morphological or nutritional restric- position in invaded habitats. tions (Fig. 1). For them, loss of their native Much of the research on the impacts of host plants (assuming this occurs due to alien invasive alien plants on plant-pollinator in- plant invasion) may severely reduce their fit- teractions has focussed on the indirect im- ness. A negative feedback would then oper- pacts of alien plants on native plant pollination ate whereby the decline of these specialist (Bjerknes et al., 2007). Impacts can be posi- pollinator species may result in pollination tive (alien plants facilitate pollination of native limitation of the specialised native plants they species by acting as “magnets” and drawing pollinate, although so few plant-pollinator in- pollinators into a plant community), negative teractions are so tightly specialised that this (alien plants compete with native plants and is unlikely to present widespread problems Impacts of invasive alien species on bees 391

Table I. Impacts of alien plants on native plant pollination. In all cases the main pollinators of the native plants are bees, except * where Diptera are the main pollinators.

Alien plant species Native plant species Location Impacts on native plant Authors Impatiens Stachys palustris Central Europe Negative on visitation and seed set Chittka and glandulifera Schurkens, 2001 Impatiens Several Britain Facilitation for visitation, possible Lopezaraiza- glandulifera competition for pollen deposition Mikel et al., 2007 Impatiens Stachys palustris Britain Facilitation for visitation, depending on Lopezaraiza glandulifera native plant density Mikel, 2006 Lythrum salicaria Impatiens capensis, Ontario, Canada Negative on seed and fruit set Grabas and Eupatorium Laverty, 1999 perfoliatum, Eupatorium maculatum Lythrum salicaria Lythrum alatum USA Negative on seed set Brown B.J. et al., 2002 Carpobrotus Lotus Balearic islands competitive effect (Lotus), facilitative Moragues and acinaciformis cytisoides, Cistus effect (C. salviifolius and Anthyllis), no Traveset, 2005 salviifolius, effect (C. monspeliensis)–effects not Anthyllis cytisoides, consistent over time Cistus monspeliensis Carpobrotus Dithyrea maritima, California, North No impact Aigner, 2004 acinaciformis Cakile maritima America

Carpobrotus Asphodelus aestivus, Majorca, Spain Low levels of pollen deposition on Jakobsson et al. edulis and C. affine Dorycnium hirsutum, stigmas, negative impact on seed set 2007 acinaciformis Helichrysum stoechas of H. stoechas Carpobrotus Several Spain Facilitation (Carpobrotus) and Bartomeus et al., affine acinaciformis competition (Opuntia) 2008b and Opuntia stricta Rhododendron Several Ireland Varied on visitation across locations and Dietzsch and Stout ponticum within flowering season unpubl. data Heracleum Non-native Mimulus Denmark Enhanced visitation to native when close Nielsen et al., 2008 mantegazzianum guttatus to alien but not seed set Phacelia Melampyrum Norway Visitation reduced, no impact on seed set Totland et al., 2006 tanacetifolia pratense Euphorbia esula* Linum lewisii USA, N America Variation in impacts on pollinator Larson et al., 2006 ssp. lewisii, Oxytropis visitation, reduced pollen deposition lambertii ssp. lambertii Chromolaena Dipterocarpus Thailand decreased visitation by butterflies but Ghazoul, 2004 odorata obtusifolius compensated by increased bird/moth pollination – no impact on seed set Solanum Glaucium flavum Lesvos, Greece Reduced visitation Petanidou et al., elaeagnifolium unpubl. data

(Waser et al., 1996). Generalist native polli- try in most plant-pollinator networks (Vázquez nators that are able to utilize the resources of and Aizen, 2004), plus other drivers of en- invasive alien plants may support native plant vironmental change (e.g. habitat loss, pollu- communities (Memmott and Waser, 2002)and tion, climate change), the impacts of invasive promote further invasion of the alien plant alien plants on native pollinator communities species (Stout, 2007)(Fig.1). Due to asymme- are diﬃcult to detect. 392 J.C. Stout, C.L. Morales

the British Isles. Alternatively, invasive alien flowers could require some specific handling skills that native bees do not possess. For example, native bees in Tasmania are unable to manipulate the flowers of invasive alien Lupi- nus arboreus because the latter require large, powerful bees to expose stamens and stigma (Goulson, 2003), and native halictid bees in Florida are unable to buzz pollinate the flowers of invasive alien Solanum torvum because of their inability to sonicate anthers (Liu and Pemberton, 2008). In these cases, the invasive alien plant species are avoided by native bees and so do not act as a useful food resource. It is more likely that generalist native bee Figure 1. Potential interactions between native and taxa are able to include invasive alien plant alien plants and bees in invaded ecosystems. (Inter- species in their diet, either by legitimate vis- actions among native species are not shown for clar- its to flowers, or via robbing (Inouye, 1980). ity.) Note that native specialist bees (those which Indeed, research has indicated that general- forage on one or a few host plants) and specialised ist bees are more common foraging on inva- plants (that can only be pollinated by one or a sive alien plants than specialists (Lopezaraiza- few pollinators) do not benefit from alien inva- Mikel et al., 2007; Tepedino et al., 2008). sion, whereas alien generalist bees and generalised Although concern has been expressed over the plants benefit the most. Interactions among alien bees and plants may result in the formation of inva- loss of specialist bee taxa (Biesmeijer et al., sion complexes. Black lines indicate direct impacts 2006; Fitzpatrick et al., 2007), the loss of gen- of plants on bees (by providing a forage resource) eralist bees could be far more detrimental to and broken grey lines indicate direct impacts of bees plant communities (Memmott et al., 2004). on pants (through pollination service). The broken This is because pollination networks are asym- black lines represent resource competition among metrical and therefore have ecological toler- native and alien species. ance to extinction of specialists (Memmott et al., 2004). Hence, if invasive alien plants support native generalist pollinators, they act 2.2. Direct impacts on bees as resource reservoirs in largely degraded landscapes (cf. Westphal et al., 2003). In turn, Very little research has focussed on the di- if generalist pollinators are well supported, rect impacts of invasive alien plants on native then native plants that are specialised for pol- pollinators, including bees. In order for native lination by one or a few generalist species bees to utilise invasive alien plants success- may benefit (Ashworth et al., 2004), and their fully as a forage resource, alien flowers need pollination positively facilitated (Aizen et al., to (i) be morphologically accessible, (ii) con- 2008). tain rewards of nutritional value, and (iii) be In terms of the nutritional value of invasive spatially and temporally available to native alien plant species for native bees, there has bees. Some alien plant species display flow- been very little direct research. The quantity ers specialised for pollination by animals other and quality of nectar and pollen produced by than bees, and so nectar and/or pollen rewards any plant is affected by resource availability in may not be accessible to native bee taxa. For the habitat, resource allocation by the plant, example, although Salvia splendens flowers the pollination syndrome to which the plant produce copious nectar, nectar is concealed belongs and, of course, genotypic constraints. deep within long corolla tubes (Corbet et al., Numerous studies have quantified nectar quan- 2001), making it difficult for native bees to tity and quality (in terms of sugar content) in access nectar where this species is grown in a huge range of plant taxa, but it is pollen that Impacts of invasive alien species on bees 393 provides most of the dietary nutrition of bees. considered as ecological equivalents to mass- Pollen varies in protein content among species flowering crops. For example, R. ponticum, (Roulston et al., 2000) and this affects the which produces a massive, short-term floral pollen foraging behaviour of honeybees (Cook display with copious nectar rewards (Stout, et al., 2003; Keller et al., 2005). If invasive 2007), facilitates the number of B. lucorum alien plants produce nectar and pollen of suf- and B. pascuorum colonies in invaded sites in ficiently high quantity and quality, they could Ireland by providing floral resources to found- act as important foraging resources, particu- ing colonies (Dietzsch et al., unpubl. data). larly in forage-depleted agri-environments. These latter two studies illustrate that general- On the other hand, if invasive alien plant ist bees benefit from the forage resources pro- rewards are not beneficial to native bees, but vided by invasive alien mass-flowering plants, even detrimental to them, they can have the but both highlight the short-term nature of opposite impact. For example, the nectar and these floral resources in the context of the pollen of the invasive alien Rhododendron entire colony cycle. In addition, no studies ponticum contain grayanotoxins which cause have yet estimated the impacts of invasive poisoning in humans (Koca and Koca, 2007). alien plants as potential forage resources on Although R. ponticum nectar apparently con- populations of specialised and solitary bees. tains relatively high levels of these toxins As well as the impacts that invasive alien (Koca and Koca, 2007), they have no impact plants could have on forage resources, we must on individual workers of native bumblebees also consider impacts on native bee nesting from Ireland (Bombus lucorum, Dietzsch et al., sites. For example, invasion by R. ponticum unpubl. data). This is probably due to the bum- and replacement of the native vegetation in blebees’ ability to metabolize or excrete the Vaccinium-dominated heathlands in the north toxins (cf. B. consobrinus and others which are western British Isles eliminates the microhab- tolerant to aconitine in Acotinum (monkshood) itats that form the nesting sites of declining across Europe (Ponchau et al., 2006)), or they heathland specialist species such as B. monti- may have sub-lethal effects. Interestingly, hon- cola (Edwards and Jenner, 2005). eybees rarely visit R. ponticum flowers in the In general, studies of impacts of inva- British Isles, which may indicate that they are sive alien plants on bee communities are deterred by these toxins. Indeed, other Rhodo- much harder to perform. Experimental ma- dendron species contain nectar that is toxic to nipulations of plants in order to assess im- honeybees (Carey et al., 1959). Furthermore, pacts on bee communities would require huge there has been no study of the impact of in- areas to take account of large bee forag- vasive alien plant pollen on larval growth and ing ranges (Beekman and Ratnieks, 2000; survival, either in the lab or the field. Cresswell et al., 2000; Goulson and Stout, The impacts of invasive alien plants on 2001; Knight et al., 2005;Westphaletal., native bees are relatively simple to study at 2006; Osborne et al., 2008). Alternatively, the individual level (changes in foraging be- natural sites (invaded and uninvaded) can be haviour, survival etc.), but more difficult to used, but it is difficult (and sometimes impos- study at the population and community levels. sible) to find appropriate independent repli- Populations of social bees may be studied us- cates for study. A particular problem is finding ing molecular techniques to determine sister- un-invaded or pre-invaded control sites with- ship and estimate colony abundance (Darvill out confounding the experimental design with et al., 2004; Knight et al., 2005) in invaded large-scale biogeochemical variation. For ex- landscapes. Recent studies have shown that ample, Lopezaraiza-Mikel et al. (2007) could mass flowering crops such as oil seed rape find no suitable un-invaded control sites for (Brassica napus) may positively influence the comparison with their invaded and experimen- number of B. pascuorum colonies in agri- tally cleared sites. Bartomeus et al. (2008b) cultural landscapes (Westphal et al., 2006; found similar pollinator community richness Herrmann et al., 2007). Invasive alien plants in invaded and uninvaded plots, but these with large, short-lived floral displays can be were only separated by around 300 m. Hence 394 J.C. Stout, C.L. Morales conclusions about the impacts of the invader their native range, as a consequence of inten- on the native community are difficult to draw tional releases and the trade of colonies, and since it is difficult to measure the true native at least 18 have become established (Donovan, community. In addition, if displacement of na- 1980; Goulson, 2003; Morales, 2007). A. mel- tive forage resources causes native specialist lifera and Bombus spp. have been introduced bees to disappear, there may be a time-lag dur- most widely, frequently and in higher numbers ing which this loss occurs, which may be diffi- than any other taxon. Currently, A. mellifera is cult to detect via short-term alien removal ex- the most widely distributed alien pollinator in periments. the world (Kearns et al., 1998), being present Invasive alien plants may have additional in all continents except Antarctica. However, indirect impacts on native bees if they pro- bumblebees are increasingly viewed as valu- mote the successful establishment and spread able pollinators of many crops, with more of super-generalist invasive alien pollinators than one million colonies produced annually (Aizen et al., 2008). Associations between in- (Velthuis and van Doorn, 2006). Since the troduced pollinators and plants can have pos- start of commercial rearing of bumblebees itive effects on both parties and form invader in 1987, they have been introduced to more complexes, for example such as those be- than 11 countries in South and North Amer- tween A. mellifera and Centaurea solstitialis ica, Australasia and Asia and they have fur- in western USA (Barthell et al., 2001), B. ter- ther invaded other countries in South Amer- restris and Lupinus arboreus in Tasmania and ica and Australasia (Morales, 2007). Although New Zealand (Stout et al., 2002), and A. mel- most studies on invasive alien bees have fo- lifera, B. ruderatus, Vespula germanica and cused on these two genera, and hereafter alien plants in the southern Andes, Argentina much of our discussion is on them, other in- (Morales and Aizen, 2006). Super-generalist vasive alien insects (especially other flower invasive alien bees can in turn have their own users, such as ants) might also potentially impacts on native bees. impact native bees, and they deserve further research attention. For example, studies have shown that invasive alien Argentine ants, 3. IMPACTS OF INVASIVE ALIEN Linepithema humile, can reduce the amount INSECTS of time native bees spend foraging on flowers Invasive alien insects have the potential to and can displace them altogether (Altshuler, exert considerable direct and indirect impacts 1999; Lach, 2008). As is the case with in- on native bees. Recent reviews vary consider- vasive alien plants, invasive alien social bees ably in their conclusions on whether existing have been introduced intentionally for polli- evidence does (Sudgen et al., 1996; Goulson, nation purposes and are associated strongly 2003; Morales, 2007) or does not (Donovan, with anthropized and highly disturbed habi- 1980; Butz Huryn, 1997;Paini,2004) sup- tats (Aizen and Feinsinger, 1994, 2003; Stout port negative impacts of invasive alien bees. and Goulson, 2000; Morales and Aizen, 2002; Previous reviews proposed that major eco- Inari et al., 2005). This not only facilitates logical impacts are mediated by (i) competi- their invasion, but makes the assessment of ffi tion for resources and nesting sites, (ii) trans- their ecological impact di cult, because dis- mission of pathogens, and (iii) reproductive turbance per se and invasion of alien bees are disruption via interspecific mating with na- frequently considered as confounding factors tive congeners (Goulson, 2003;Travesetand (Aizen and Feinsinger, 1994;Paini,2004). Richardson, 2006; Morales, 2007). In addi- Since Apis, Bombus and ants are social in- tion, invasive insects which cause a change sects, their invasive potential is increased by in the native plant community structure could the possibility of a single inseminated queen cause further indirect impacts on native bees. founding a new colony which is then capable To date, ca. 20 species of solitary (Nomia, of producing a high number of reproductive in- Osmia and Megachile) and social bees (Apis dividuals (Moller, 1996). This could then lead and Bombus) have been introduced outside to the invasion of an entire island or continent Impacts of invasive alien species on bees 395

(Chapman and Bourke, 2001). For instance, gathering resources, resource depletion, spa- 236, 214, and 1–5 queens founded the current tial or temporal correlations between native populations of alien bumblebees invading New and invasive alien bees, and, finally, changes Zealand (MacFarlane and Gurr, 1995), Chile in the patterns of abundance, activity, resource and Argentina (Arretz and MacFarlane, 1986; gathering, or diversity of native species, in Roig Alsina and Aizen, 1996;Ruz,2002)and relation to the natural or manipulated pres- Tasmania (Semmens et al., 1993; Buttermore ence of invasive alien bees. All these variables et al., 1998), respectively. Social bees can are easier to measure in the field (Goulson, also communicate the availability and loca- 2003; Thorp, 2003), but do not provide conclu- tion of resources to nest mates, which im- sive evidence on the existence of competition proves their foraging efficiency (Dornhaus and (Goulson, 2003;Paini,2004; Thomson, 2004; Chittka, 1999, 2001). As resource acquisition Velthuis and van Doorn, 2006). However, they is closely related to reproductive performance are valuable because they suggest a scenario of (Thomson, 2006), this efficiency might con- potential competition. Here we summarize the tribute to their invasive success. In addition, main conclusions of these studies, grouped by invasive alien bee species that have more suc- response variable and experimental approach. cessfully colonized new habitats have done so because they are generalists (Goulson, 2003). 3.1.1. Resource niche breadth and These traits are expected to increase their overlap chances of survival and establishment in invaded regions. Honeybees and bumblebees are generalist species, thus they can interact indirectly 3.1. Competition for resources via plant-pollinator interactions with a significant proportion of the local bee fauna Invasive alien insects and native bees might (Goulson, 2003). Indeed, studies have shown compete for resources, if (1) they experience that both honeybees and bumblebees’ forag- a substantial floral resource overlap, (2) re- ing niches overlap substantially with native sources are limiting, and (3) decreases in re- visitors (Goulson, 2003), and most of them source acquisition translate to a reduction of suggested that the impact on native bees was fitness of the less competitive or both com- either negative or unnoticeable (reviewed in peting species (usually expressed as a reduc- Paini, 2004; Morales, 2007). For example, tion in fecundity, survival, or population size). Paini and Roberts (2005) found considerable Experimental tests of the effect of invasive resource overlap between native oligolectic alien insects on any of these fitness mea- bees and invasive alien honeybees in Australia, sures provide the most direct and conclusive which led to a reduction in native bee fecun- evidence of competitive impacts of alien on dity. The use of resource overlap measures native bees (e.g. Thomson, 2004). However, seems justified because some studies have the difficulty in carrying out well designed found that the chances of having a detrimental manipulated experiments has precluded such impact increased with the degree of resource studies in most situations (Goulson, 2003; overlap. For instance, Goodell (2000) found Thorp, 2003; Thomson, 2006; Velthuis and that the performance of the native generalist van Doorn, 2006; Morales, 2007). Rather, megachilid Osmia pumilia, which had a higher most studies on the impact of invasive alien resource overlap with honeybees, was more insects on natives bees have inferred com- detrimentally affected than other native Osmia petitive impacts on the population dynam- species. In addition, potential for competition ics or fitness of native species from one or suggested by the observed similarity in visi- more of the following indirect measures (re- tation patterns between invasive alien A. mel- viewed in Goulson, 2003 for bees in general; lifera and native B. occidentalis was further Butz Huryn, 1997;Paini,2004 for honeybees; experimentally confirmed by a reduction in and Morales, 2007; for bumblebees): floral B. occidentalis colony reproductive success resource overlap, comparative efficiency in at decreasing distances of A. mellifera hives 396 J.C. Stout, C.L. Morales

(Thomson, 2004). The proboscis length of A. (2004) found that honeybees stayed longer and mellifera and worker B. occidentalis is very visited more flowers per inflorescence than na- similar, which probably leads to similarities tive bees, depleting nectar in Echium wild- in flower visitation patterns (Inouye, 1977). pretii, suppressing visitation by native ani- Nevertheless, as Thomson (2006) warns, sub- mals due to exploitative competition. In the stantial temporal variability in niche esti- Bonin (Ogasawara) Islands, Kato et al. (1999) mates might seriously compromise conclu- found a negative relationship between the oc- sions based on these measures. currence of honeybees and native bees, partly attributable to pollen depletion in native plants 3.1.2. Comparative efficiency in resource by honeybees, but also partly due to distur- acquisition bance and invasion by alien flora. Resource ffi depletion has been argued to result in a sig- Invasive alien bees are more e cient in nificant asymmetry in competition in favor of the acquisition of resources than many na- invasive alien bees (Goulson, 2003 and refer- tive counterparts. For instance, in Chile B. ter- ences therein). This effect varies among na- restris spends less time per flower than native tive plant species and the abundance of alien B. dahlbomii (Ruz and Herrera, 2001). Since bees. Indeed, Horskins and Turner (1999)did most observations were performed on flow- not find that honeybees depleted resources of ers with short corollas, where short tongued anativeplant. bees visit flowers faster than long tongued bees (Inouye, 1980), this difference might reflect the differences in tongue length be- 3.1.4. Spatial and temporal association tween the alien (short tongue) and the na- between native and alien bees tive (long tongue length). In another study, alien subspecies of B. terrestris collected rel- Correlational studies have found mostly atively more nectar per unit time than na- negative (Aizen and Feinsinger, 1994; tive subspecies (Ings et al., 2005b), which in Goulson et al., 2002; Inari et al., 2005; turn translated into a better reproductive per- Yang, 2005; Thomson, 2006; Tepedino et al., formance (Ings et al., 2006). It is not clear 2007), but also null (Goulson et al., 2002; whether this is a result of long-term com- Thomson, 2006; Nagamitsu et al., 2007; mercial breeding or due to inherent differ- Tepedino et al., 2007)andtoalesserextent ences between the two subspecies. If resource positive (Nagamitsu et al., 2007) spatial overlap is substantial and alien bees gather re- associations between native and invasive alien ffi bees. Interestingly, even within the same sources more e ciently, they have the poten- ff tial to displace native bees due to depleting system, di erent studies (eg. Inari et al., common nectar sources (Ings et al., 2005b), 2005; Nagamitsu et al., 2007) or experimental which could be additionally exacerbated by approaches (e.g. Thomson, 2006; Tepedino their comparatively large numbers, particu- et al., 2007) have provided contrasting larlyinthecaseofA. mellifera. evidence, illustrating the risks in drawing conclusions from a single correlational study. For instance, despite experimental data for both 3.1.3. Resource depletion bumblebee foragers and colonies suggesting Honeybees and bumblebees might deplete significant competitive impacts (Thomson, nectar and pollen. In Arizona, Schaffer et al. 2004), Thomson (2006) found that only one (1983) experimentally demonstrated that hon- of seven analyses of correlational data showed eybees reduced the standing crop of nectar a significant negative relationship between of Agave schottii to the detriment of native A. mellifera and native Bombus abundance. bees. In New South Wales, Gross (2001)at- This apparent incongruence seems to be the tributed fewer visits by native bees recorded result of substantial temporal variability of in Dillwynia juniperina to honeybees de- correlational data (Thomson, 2006). Com- pleting the standing crop of nectar. Simi- petition might be absent or undetectable larly, in the Canary Islands, Dupont et al. if resources are not limited (Paini, 2004), Impacts of invasive alien species on bees 397 a condition that varies from year to year. For Thomson, 2004, 2006). In French Guiana, instance, Pleasants (1981) found that native a decrease in the abundance of native bees bumblebees in Colorado, USA, expanded was found in sites where Africanized bees their diet breadth to include honeybee-flowers were experimentally placed (Roubik, 1978), in a year of honeybee scarcity. but no evidence was found that the addi- Consistent temporal trends revealed by tion of Africanized A. mellifera colonies af- long-term studies can provide a much more fected the fecundity in two Megachile spp. reliable insight into the existence of compe- (Roubik, 1983). Similarly, in Australia, large tition (Roubik, 2001). Monitoring over many forage resource overlap was found between A. years did not show any clear declines in abun- mellifera and a native Megachile sp., but no dance or local extinction of native Melipona change in reproductive success in the native spp. since the arrival of the Africanized hon- bee was detected (Paini et al., 2005). Also in eybees (Wolda and Roubik, 1986; Roubik, Australia, increased brood rearing success but 1991; Roubik and Wolda, 2001). Conversely, also changes in sex ratios were found in the in South Argentina, ongoing yearly monitor- semi-social Exoneura asimillima placed in the ing of visitation frequency showed that since vicinity of honeybee hives (Sugden and Pyke, invasion of B. ruderatus in 1994 to 2006, the 1991). In a three-year study on four differ- visits by native B. dahlbomii steeply declined ent sites, Thomson (2004) found striking ev- simultaneously to an increase in visits by the idence of competitive suppression of native invasive species in a mainly undisturbed forest B. occidentalis by A. mellifera, as reflected (Morales, 2007; Morales and Aizen, in prepa- by decreased worker foraging activity, rate ration). of pollen acquisition, and reproductive suc- Correlations do not reveal causation, and cess of colonies experimentally placed close might indicate competitive exclusion only if to A. mellifera hives. Furthermore, colonies other potentially confounding factors have with greater foraging success had higher re- been taken in account (Paini, 2004; e.g. Aizen productive success, emphasizing the impor- and Feinsinger, 2003). For instance, positive tance of resource limitation in determining spatial correlations suggest similar resource or fitness (Thomson, 2004). However, since mea- habitat preferences; in turn, negative spatial sures of colony resource intake explained a correlations may reflect different habitat pref- relatively low amount of the observed vari- erences or competitive exclusion. Increasing ance in reproductive success, caution should invasive alien bee abundances are often associ- be taken in utilizing foraging behaviour alone ated with increasing anthropogenic habitat dis- to predict the importance of competitive ef- turbance, which may in turn explain declines fects (Thomson, 2004). in native bees (Aizen and Feinsinger, 1994; Thomson (2006) went a step further, and ff Butz Huryn, 1997; Goulson, 2003;Stean- found that competitive effects on colony re- Dewenter and Kuhn, 2003;Paini,2004). Nev- productive success were accurately estimated ertheless, it is also possible, that habitat distur- by experimental data on forager abundances, bance synergistically exacerbates the negative but the latter did not estimate competitive ef- impact of invasive alien on native bees, fects as strongly as those actually observed through asymmetric competition in a habitat for reproductive success. Since correlational favoring aliens, to the detriment of native bees. data mostly failed to predict the detrimental effects observed in the experimental study (see 3.1.5. Experimental manipulation of above), this suggests that the actual impact of alien bees invasive alien on native bees is stronger than inferred from estimations of niche overlap, Only a handful of studies have measured spatial and temporal correlations, or changes changes in fecundity, survival or population in native bees foraging activities, and high- densities of native bees after densities of A. lights how misleading a picture observational mellifera had been manipulated (e.g. Roubik, measures may paint of invasion impacts, par- 1978, 1982, 1983; Roubik and Wolda, 2001; ticularly over short time scales. 398 J.C. Stout, C.L. Morales

Given the low number of experimental stud- species for this resource (Donovan, 1980). In- ies that directly measured individual fitness, terspecific nest usurpation is characteristic of it is difficult to make any definite conclusion many bumblebee species (Sakagami, 1976) until more research is conducted. This situa- but we are not aware of any studies that specifi- tion is further complicated by the fact that in cally address nest competition among invasive regions where A. mellifera has invaded many alien and native species in the wild. B. ter- decades or even centuries ago, displacement restris queens experimentally introduced into or extinction of most vulnerable native species nest boxes containing incipient colonies of na- may have occurred before the experiments tive B. ignitus and B. hypocrita,usurpedtheB. took place (Paini, 2004).Thus,sofar,werely ignitus nest and killed its queen, whereas this mostly on indirect evidence to draw conclu- behavior was not observed with B. hypocrita sions about such situations. nests (Ono, 1997). However, this is clearly an Overall, there is no indisputable evidence area where further research is required. that invasive alien bees have a substantial and consistent competitive impact on native bees. This lack of unequivocal evidence should not 3.3. Transmission of pathogens be interpreted as a lack of effect. Most indirect evidence to date suggests negative impacts, One of the biggest threats associated with and the scarce direct evidence shows that in the invasion by alien bees is the spread of some cases, these negative impacts might be disease to native species. Invasive alien bees rather strong. can act as vectors of novel pathogens that can infect native con-specifics and other closely related species (Tab. II). The importation of 3.2. Competition for nesting sites commercial bee colonies is thought to be the source of exotic parasites and pathogens. Be- With the exception of Barthell et al. cause honeybee health is extensively dealt (1998), who found invasive alien insects (two with in numerous publications (including a Megachilid bees, Megachile apicalis and M. forthcoming Special Issue in Apidologie in rotundata, and the European earwig Forficula 2010), we limit our discussion to the im- auricularia), occupying more trap-nests than pacts of commercially imported bumblebees native bees in California, studies on compe- and their associated parasites. tition between invasive alien and native bees A diverse array of pathogens affect Bom- for nesting sites are even scarcer than studies bus spp. (Macfarlane et al., 1995;Schmid- on competition for resources. Often, the best Hempel, 1998; Schmid Hempel and Loosli, we can do is to infer potential competition on 1998), some of them with devastating ef- the basis of niche overlap. B. terrestris queens fects on infected colonies (e.g. the tripanoso- use nest sites that are similar to those used matid Crithidia bombi (Brown M.J.F. et al., by native Bombus species in different invaded 2000, 2003); the acarine Locustacarus buch- regions (e.g. B. hypocrita in Japan (Velthuis neri (Goka et al., 2001); the microsporid- and van Doorn, 2006); B. dahlbomii in Ar- ian Nosema bombi (Otti and Schmid-Hempel, gentina (Morales, 2007)) and by native B. ter- 2007), and the hymenopteran Melittobia restris subspecies in Europe, and so there is acasta (Estay, 2007)). These pathogens are huge potential for nest site competition. How- among the most important threats from in- ever, no study has addressed whether nest sites troduction of commercial colonies to native limit bumblebee populations in their native species because they thrive in conditions of ranges. In New Zealand, the availability of nest artificial rearing. Studies have demonstrated sites seems to be an important constraint to that commercial bumblebee colonies can hold bee population levels; nevertheless, wide dif- higher levels of infection than wild colonies ferences in nest site requirements among al- (Colla et al., 2006).Thustheescapeof most all species suggest that there is little or workers, and potentially the establishment of no competition between native and introduced feral bumblebee colonies from commercial Impacts of invasive alien species on bees 399

Table II. Evidence of pathogen/parasite transmission from non-native Bombus and Apis species imported for commercial crop pollination.

From To Pathogen Location Reference B. terrestris Native conspecifics Nosema bombi Europe Schmid-Hempel, & congenerics 1998 B. terrestris Native conspecifics Locustacarus Japan Goka et al., 2001; & B. ignitus & congenerics buchneri Goka, 2006 B. impatiens Native conspecifics Crithidia bombi Canada Colla et al., 2006; & congenerics Otterstatter and Thomson, 2008 A. mellifera B. terrestris Deformed wing Europe Genersch et al., and B. pascuorum virus 2006 A. mellifera B. impatiens Aethina tumida North Hoffmann et al., America 2008* A. mellifera B. impatiens ** Aethina tumida Florida, Spiewok and USA Neumann, 2006 A. cerana A. mellifera Nosema ceranae Spain, Higes et al., 2006 Europe A. cerana A. mellifera Nosema ceranae Taiwan Huang et al., 2007 A. cerana A. mellifera Varroa destructor Asia Akratanakul and Burgett, 1975; de Jong et al., 1982 * Potential for transmission demonstrated, no evidence of host switch in the wild. ** Commercial colonies. colonies, or the infiltration of glasshouses by Detection of microorganisms and endopar- wild bees, could introduce pathogens to na- asites is very difficult in living bees (Thorp, tive conspecifics and congeners while forag- 2003). Therefore, in spite of quarantine con- ing on the same flowers (Durrer and Schmid- trols, infested commercial colonies have been Hempel, 1994). Indeed, in Ontario, Canada, introduced to some countries (Goka et al., native bumblebees in the proximity of green- 2001). Following interspecific transmission of houses hosting commercial colonies of bum- parasites, virulence on new hosts could be blebees were infected by C. bombi, whereas higher or lower, although more noticeable in there was no incidence of this pathogen in the former case (Bull, 1994). Furthermore, bumblebees collected at other sites in the re- it is postulated that the sudden decline of gion (Colla et al., 2006). Furthermore, the for- five North American bumblebee species might mer had concentrations of the microsporidia be related to N. bombi outbreak in bum- N. bombi three times higher than the latter blebee facilities that decimated the commer- (Colla et al., 2006). Recently, Otterstatter and cial colonies of B. occidentalis (Thorp and Thomson (2008) constructed a spatially ex- Shepherd, 2005; Winter et al., 2006; Williams plicit model of C. bombi infection spread- and Osborne, 2009). ing from commercial to wild bumblebees, There is a serious gap in our knowledge and found that although the forecasted “wave- about the reproductive effects, geographical front” of infection was not detected, the preva- distribution, epidemiology and evolutionary lence of C. bombi near greenhouses was con- ecology of most pathogens associated with sistent with their predictions. Bombus (Schmid-Hempel, 1998), and to a 400 J.C. Stout, C.L. Morales lesser extent with Apis. In light of the existing ences therein); nevertheless interspecifc mat- evidence, the improvement of methods for pre- ing between B. terrestris and B. hypocrita venting commercial bee escape (through mesh sapporoensis in the laboratory results in the screens in commercial greenhouses) and for production of inviable hybrids (Kanbe et al., detecting pathogens in living specimens, and 2008). Thus, despite the potential failure to the standardization of inspection protocols for produce hybrid progeny, interspecific mating importing and exporting colonies should be negatively affects the reproductive rate of na- high priorities (Morales, 2007). tive species due to a reduction of intraspecific matings, and in turn, of viable progeny (Kanbe et al., 2008). In addition queen mortality has 3.4. Reproductive disruption and been observed to increase after interspecific hybridization matings (e.g. Cuadriello et al., unpubl. data).

The rupture of biogeographical barriers that maintained isolated related species will have 3.5. Modification of native plant genetic consequences for both the invasive community structure alien and native species and/or subspecies. For example, commercial importation of A. mel- Invasive alien insects can mediate changes lifera ligustica and A. m. carnica around Eu- in native plant communities via disruption of rope has caused introgression of alleles into native- and promotion of alien-plant pollina- the native A. m. mellifera, completely replac- tion, with knock-on impacts on native plant ing the native sub-species in some areas, no- seed set, succession and community struc- tably Germany (De La Rúa et al., 2002, 2009; ture (Roubik, 1996; Yang, 2005; Kenta et al., Jensen et al., 2005). Similarly, in Europe, com- 2007), which can facilitate further impacts on mercial use of colonies of various B. terrestris native bees. For example, although A. mellif- subspecies (mostly B. terrestris dalmatinus era do not deplete the resources collected by (Velthuis and van Doorn, 2006)), could re- native pollinators of Clusia arrudae, a tropical sult in interbreeding between commercial and tree pollinated by resin-collecting Euffriesea native bees, and introgression into local sub- nigrohirta, honeybees do affect the pollination species such as B. terrestris audax in Britain of the species by removing virtually all pollen and Ireland and other subspecies elsewhere in from flowers (Mendes do Carmo et al., 2004). Europe (Ings et al., 2005a). Until recently, suit- Similarly, Gross and Mackay (1998) found able molecular markers have not been avail- that honeybees negatively affected pollination able to test whether this is indeed occurring, of Melastoma affine, a pioneer species in trop- but recent research has found evidence for in- ical Australian rainforests. In both cases, sup- trogression in the wild between commercial pression of native plant pollination has the and native B. terrestris in Poland (Rohde, un- potential to alter plant community structure, publ. data). which could have dramatic impacts on native In addition to hybridization and introgres- bees and pollinator communities. sion among subspecific bees, there may also be hybridization among species. For example, there is evidence of mating between in- 4. RESEARCH PRIORITIES vasive alien and native bumblebees belong- ing to the same subgenus: B. terrestris mates In order to prevent, assess and/or manage with its Japanese consubgenerics B. hypocrita impacts on native bees, further research is re- and B. ignitus (Ono, 1997; Goka et al., 2001), quired. Whilst it will not be possible to inves- and B. (Pyrobombus) impatiens with its con- tigate all impacts in all systems, we suggest subgeneric B. ephippiatus (Vergara, 2008). some priorities for study. Firstly, studies on For instance, 30% of native Bombus hyp- impacts of invasive alien plants and pollinators ocrita queens copulate with B. terrestris males should be extended to the landscape scale and in the field (Kanbe et al., 2008 and refer- should be long-term and observations should Impacts of invasive alien species on bees 401 be carried out at the species and commu- Invasive alien flowering plants are of- nity level (Walther-Hellwig et al., 2006). Im- ten introduced intentionally as ornamen- plicit within this, is to examine the impacts on tals (Dehnen-Schmutz and Williamson, 2006; solitary bees, particularly rare/specialist bee Milbau and Stout, 2008). Many nations need species, as well as on generalist and com- tighter restrictions (“biosecurity”) on the im- mon social species. Secondly, these studies portation, sale and planting of certain flow- need to be properly replicated in time and/or ering invaders. In this regard, some countries space (e.g. Thomson, 2004). Systems are nat- (e.g. New Zealand) are far ahead of others (e.g. urally variable and in order to generate use- many countries in the European Community ful conclusions, rigorous experimental design lack border restrictions with other EU coun- is required. Thirdly, the rapid rate of new in- tries). Educational programs aimed at pro- troductions, in particular by the exponential moting gardening with native flowering plants expansion of the bumblebee market (Velthuis would help to reduce alien importations and at and van Doorn, 2006), means that conduct- the same time increase public awareness of the ing detailed experimental studies of each alien value of local biota. species, in each native area may be imprac- With regards to imported commercial bees, tical. For this reason, determining measures all efforts should be made to license importa- to identify quickly the likely impacts of new tion and minimise bee escape and the subse- introductions is a key step to improve deci- quent spread of disease to native species and sion making, monitoring and rapid response populations. Bees do escape from commercial (Thomson, 2006). Fourthly, it is important to colonies used in the field and in glasshouses understand the pathology, virulence and cross- and so the potential for spread of disease, and infectivity of disease organisms like N. bombi, hybridization is substantial. In addition, from L. buchnerii, C. bombi and others (Thorp and the point of view of safety and nature protec- Shepherd, 2005), and to adjust the mecha- tion, local production, preferably of a locally nisms of detection of these pathogens in live pollinating species, should be encouraged. If bees in order to improve the quarantine mea- there is concern about dangers of introduc- sures. Finally, there is an urgent need to con- ing alien species, both the government and the sider the impacts of climate change on spa- farmers should invest in research (Velthuis and tial and temporal shifts in invasive alien and van Doorn, 2006). Finally, the most effective, native plants and pollinators and their interac- economical, and ecologically sound approach tions (Schweiger et al., unpubl. data). to managing invasive species is to prevent them from arriving (Windle and Chavarría, 2005). 5. CONSERVATION NEEDS

Whilst research is still required, conserva- 6. CONCLUSIONS tion measures should be put in place as a pre- caution in the intervening time. For example, Some invasive species provide benefits mass flowering invasive plants and simplifica- (including the economic and environmental tion of agricultural landscapes may increase benefits of increased pollination services) but competition among pollinators (Bronstein, others have negative impacts on native bees. 1995;Steffan-Dewenter and Kuhn, 2003). Impacts of invasive alien species on specialist Thus, habitats rich in native flowering species, and generalist bee taxa may differ, and prob- which provide plentiful pollen and nectar re- ably vary according to landscape context, and sources during the whole foraging season although it is difficult to test impacts experi- should be protected and promoted in restora- mentally in well designed and replicated ex- tion projects. These can support a larger diver- periments, this is what we should strive to sity of native bees, which benefits agriculture achieve. More research is required on all native (Hoehn et al., 2008) and the pollination of na- bees (Committee on the Status of Pollinators tive wild plants. in North America, National Research Council, 402 J.C. Stout, C.L. Morales

2007), but especially on solitary species and chen Verfügbarkeit der Belohnungen variiert. Ein specialists. Unfortunately, in many parts of indirekter Einfluss liegt vor, wenn invasive frem- the world, these studies are limited by tax- de Pflanzen die einheimische Pflanzengemeinschaft beeinflussen (entweder durch Wettbewerb um abio- onomic expertise, an issue which may be tische Ressourcen oder um biotische Ressourcen overcome to some extent by DNA barcod- einschließlich der Bestäubung) (Tab. I). Insgesamt ing (www.bee-bol.org). Finally, we need pre- können Beeinflussungen des individuellen Verhal- dictions of impacts not just on species, but tens und Überlebens relativ leicht bestimmt werden, on entire plant-pollinator-parasite communi- während dagegen Einflüsse auf Populationen oder ties, ecosystem services and ecosystem func- Gesellschaften wesentlich schwerer vorauszusehen sind und bislang nur wenig untersucht wurden. tioning. Der überwiegende Teil der Forschungen über die Auswirkung fremder invasiver Insekten auf die einheimischen Bienen hat sich auf die Auswirkungen von eingeführten sozialen Arten von Honigbienen ACKNOWLEDGEMENTS oder Hummeln bezogen, die um Ressourcen oder Nistplätze in Konkurrenz stehen, die Verbreitung We are grateful to the editors of this special issue von Pathogenen und Krankheiten verursachen oder for inviting us to write this article, to Mark Brown, die Populationsstruktur durch Hybridisation oder Introgression beeinflussen. Trotz erheblicher Auf- Anke Dietzsch, Caroline Nienhuis and Marc Kenis merksamkeit der Forschung gibt es wenig schlüs- for advice and comments on earlier drafts and to sige Nachweise für eine Kompetition zwischen David Inouye and an anonymous reviewer for sug- fremden und einheimischen Bienen um Futterres- gestions for improvements. sourcen, hauptsächlich weil Untersuchungen zur Kompetition schwierig durchzuführen und zu in- terpretieren sind. Allerdings haben einige Unter- Impacts écologiques d’espèces invasives étran- suchungen eine Verminderung der Fitness einhei- gères sur les abeilles. mischer Bienen bei Anwesenheit invasiver fremder Bienen nachgewiesen. Es gibt allerdings so gut wie Apis mellifera / Bombus / pollinisateur / espèce keine Untersuchungen zur Kompetition um ande- non indigène / espèce invasive / plante / parasite re Ressourcen als Futterressourcen, dies schließt / protection / conservation Nistplätze trotz ihres offensichtlichen kompetitiven Potentials ein. Kürzlich wurde offensichtlich, dass insbesondere in Nordamerika eine der größten von eingeführten Bestäubern ausgehenden Gefährdun- Zusammenfassung – Ökologische Folgen inva- gen ist, dass sie möglicherweise neuartige Patho- siver fremder Arten auf Bienen. Invasive frem- gene und Krankheiten auf die einheimischen Bie- de Arten sind wichtige Antreiber globaler Um- nen übertragen (Tab. II). Die Fähigkeit eingeführter weltveränderungen, indem sie direkt oder indirekt Arten mit einheimischen Arten zu hybridisieren ist auf die einheimische Biodiversität und die Öko- gut bekannt, und mit der Entwicklung molekulare- systemprozesse Einfluss nehmen. Die durch ein- re Marker zur Erkennung einer Introgression dürfte heimische Bienen erbrachten Bestäubungsleistun- das Ausmaß des Problems klarer werden. gen werden allgemein durch einen weiten Bereich Wir schlagen verschiedene Forschungsschwer- menschlicher Aktivitäten als gefährdet angesehen, punkte vor, nämlich dass (1) Untersuchungen des im Blickpunkt dieser zusammenfassenden Untersu- Ausmaßes der Auswirkungen sollten sowohl in chung stehen potentielle Gefährdungen durch in- zeitliches als auch räumlicher Hinsicht erweitert vasive Arten. Ziel des Artikels ist, den möglichen werden, in einem robusten Versuchsdesign struk- Einfluss invasiver fremder Arten auf die einheimi- turiert sein und repliziert werden, (2) besonde- schen Bienen abzuschätzen, um Gefährdungen be- re Aufmerksamkeit sollte den Auswirkungen auf stimmen und Forschungsprioritäten in diesem Ge- solitäre und spezialisierte Bienenarten zukommen, biet festlegen zu können. Wir berücksichtigten die (3) eine schnelle Erfassung potentieller Auswir- Auswirkungen invasiver fremder Pflanzen, Bienen kungen neuer Eindringlinge sollte zu einer ra- und Parasiten auf das Verhalten, die Populationen schen Entscheidungsfindung, Überwachung und und Gesellschaften einheimischer Bienen und die Entschärfung des Problems führen, (4) die Patho- Leistungen, die sie für das Ökosystem erbringen. logie, Virulenz und Kreuzinfektiösität von Patho- Invasive fremde Pflanzen können direkt oder in- genen und Parasiten muss besser verstanden wer- direkt auf die einheimischen Bienen Einfluss neh- den, und (5) die Auswirkungen weiterer Umweltän- men (Abb. 1). Direkter Einfluss beinhaltet die derungen auf Grund des Klimawandels müssen Bereitstellung von Blütenressourcen, wobei deren wegen der potentiellen räumlichen und zeitlichen Wert entsprechend ihrer morphologischen Zugäng- Verlagerungen bei invasiven und einheimischen lichkeit, Nährwert und der zeitlichen und räumli- Pflanzen und Bestäubern sowie ihrer Interaktionen Impacts of invasive alien species on bees 403

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