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Ecological Impacts of Invasive Alien Species on Bees*

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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 impor- tant 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 visi- tation, pollen deposition or seed set in S.
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