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. 2016 Nov 28;7(4):69. doi: 10.3390/insects7040069

Positive and Negative Impacts of Non-Native Bee Species around the World

Laura Russo 1
Editor: Mary L Cornelius1
PMCID: PMC5198217  PMID: 27916802

Abstract

Though they are relatively understudied, non-native bees are ubiquitous and have enormous potential economic and environmental impacts. These impacts may be positive or negative, and are often unquantified. In this manuscript, I review literature on the known distribution and environmental and economic impacts of 80 species of introduced bees. The potential negative impacts of non-native bees include competition with native bees for nesting sites or floral resources, pollination of invasive weeds, co-invasion with pathogens and parasites, genetic introgression, damage to buildings, affecting the pollination of native plant species, and changing the structure of native pollination networks. The potential positive impacts of non-native bees include agricultural pollination, availability for scientific research, rescue of native species, and resilience to human-mediated disturbance and climate change. Most non-native bee species are accidentally introduced and nest in stems, twigs, and cavities in wood. In terms of number of species, the best represented families are Megachilidae and Apidae, and the best represented genus is Megachile. The best studied genera are Apis and Bombus, and most of the species in these genera were deliberately introduced for agricultural pollination. Thus, we know little about the majority of non-native bees, accidentally introduced or spreading beyond their native ranges.

Keywords: bees, competition, genetic introgression, impacts, invasive species, pollination, species introductions

1. Introduction

The accidental introduction of some invasive insects can decimate ecosystems [1] or cause billions of dollars of environmental [2], crop [3], or building damage [4]. The majority of these insects are not noted for their potential positive impacts. On the other hand, some insects have been deliberately introduced for the services they provide to humans, without full consideration for their potential negative impacts. These insects may spread beyond the areas where they have been deliberately introduced and even become invasive pests in some cases [5]. Bees are one such group of insects, often introduced for their pollination services, but also with the potential to have negative economic and environmental impacts.

Bee species have been both introduced accidentally and deliberately around the world. Perhaps the most well-known of these introduced bee species is the European Honeybee (Apis mellifera), the most managed bee in the world, but over 70 other species have become established outside of their native ranges. There is increasing concern about the potential negative effects of these introduced bees, and there have even been efforts to eradicate them in some areas [6]. However, most attention is focused on the highly abundant and widely introduced species, including A. mellifera and Bombus terrestris as well as the managed solitary bee, Megachile rotundata.

Most non-native bee species are accidentally introduced and the potential negative and positive impacts to their introductions have not been explored. Learning about the potential impacts of introduced bees is particularly important as new species are still being proposed for domestication, and ranges will continue to change naturally and through human transportation. The purpose of this review is to collate information on all recorded non-native bee species around the world, and to discuss some of the potential outcomes of their introductions. I reviewed over 450 papers (266 of those papers are cited in this manuscript: 145 in the main text and tables and the remainder in the supplementary tables) addressing the distributions and impacts of introduced bees around the world, and present recorded positive and negative impacts here.

2. Non-Native Bee Species

For the purposes of this paper, a non-native species is defined as having one or more populations outside of its historical range. Non-native species can have both negative and positive impacts [7]. Non-native species with recognized negative impacts which are difficult to control are often referred to as “invasive” and some bee species with non-native populations are referred to in this way. However, because of the widely recognized beneficial impacts of bees, and the fact that they are often deliberately introduced, not all non-native bee species are considered invasive. Thus, I will simply refer to them as non-native species here.

The literature reviewed by the author included 80 recorded non-native bee species from 30 genera around the world (Table 1). These non-native bees are unevenly distributed among the 7 bee families, suggesting attributes of some bee families might make them more likely to have adventive or invasive species. Melittidae and Stenotritidae are not represented by any recorded non-native species. The mining bee family, Andrenidae, is only represented by one non-native species (Andrena wilkella), while both Colletidae and Halictidae have 8 non-native representatives. Indeed, the non-native bees are dominated by representatives of the families Megachilidae (33 non-native species) and Apidae (30 non-native species), though some of the other families have fewer species overall and are thus less likely to have invasive representatives. With 13 non-native species, Megachile is the best represented genus.

Table 1.

A list of non-native bee species around the world, sorted by family and including their probable method of introduction (deliberately introduced: I; accidentally introduced: A; naturally expanding or shifting range: N), year of introduction, origin, and known areas of introduction. Question marks (?) represent uncertainty in the timing or distribution of introduced and native range. This often occurs when the bee fauna of a given area has only recently been studied and in some cases the non-native species has potentially been present for a long time.

Colletidae (8) Non-native Species Year From Found in Reference
Chilicola rostrata A 2008 Argentina Chile [8]
Hylaeus (Prosopis) variegates A 1990 North Africa New York City pers. comm. S. Droege
Hylaeus albonitens A 1995 Australia Hawaii [9]
Hylaeus hyalinatus A 1990 Europe New York City, S Ontario, New Jersey, Pennsylvania [10,11]
Hylaeus leptocephalus A 1900 Europe US, S Canada [9,11,12]
Hylaeus punctatus A 1980 Europe US, Chile, Canada, Argentina, Brazil [11]
Hylaeus strenuus A 2007 Asia Hawaii [13,14]
Hyleoides concinna A 1980 Australia New Zealand [15]
Andrenidae (1)
Andrena wilkella A 1900s Europe and N Asia NE US and S Canada [11,12,16]
Halictidae (8)
Halictus tectus A 2000 Europe to Mongolia Philadelphia, Baltimore, Washington, DC [12]
Lasioglossum eleutherense A 1990 Bahamas and Cuba Florida pers. comm. S. Droege
Lasioglossum imbrex A 2013 US Hawaii [17,18]
Lasioglossum impavidum A 2003 W US Hawaii [9]
Lasioglossum leucozonium A 1900s Europe and North Asia US and S Canada [11,16]
Lasioglossum microlepoides A 2013 continental US Hawaii [17,18]
Lasioglossum zonulum A ? Europe and S China North America [11]
Nomia melanderi I 1970 North America New Zealand [19]
Megachilidae (33)
Afranthidium (Immanthidium) repetitum A 2000 Africa Australia [20]
Anthidium manicatum A 1960 Europe, N Africa, Near East Chile, Brazil, Argentina, Uruguay, the US, Canada, New Zealand, Siberia, Peru, Suriname, Paraguay [11,12,16]
Anthidium oblongatum A 1990 Europe and Near East NE US and S Canada [11,12]
Anthidium vigintiduopunctatum A 2006 South America, Ecuador, Peru Galapagos, Fiji? [21,22]
Chelostoma campanularum A 1960 Europe and Near East New York, Connecticut, and S Ontario [11,23]
Chelostoma rapunculi A 1960 Europe and Near East New York and S Ontario [11,23]
Coelioxys coturnix A 2000 Europe, North Africa, Mediterranean, India? E US pers. comm. S. Droege
Heriades truncorum A 2010 Europe and Near East Maryland pers. comm. S. Droege
Hoplitis adunca 2016 Europe, Asia, Africa Britain [24]
Hoplitis anthocopoides A 1960 Europe US, S Ontario [11,25]
Lithurgus bractipes A ? ? Fiji [26]
Lithurgus chrysurus A 1970 Europe, Near East, N Africa Pennsylvania and New Jersey [12]
Lithurgus huberi A 1907 Asia South America, Argentina [27,28,29]
Lithurgus scabrosus A 1907 Europe Hawaii, Vanuatu [9]
Megachile apicalis A 1930 Europe, N Africa, Near/Middle East US, Canada [11,12]
Megachile australis A SE Asia Vanuatu, Samoa [26]
Megachile chlorura A 1988 Philippines Hawaii [9]
Megachile concinna A 1940 Africa West Indies, Mexico, US, Argentina [12]
Megachile ericetorum A 2000 Europe, Near East, China S Ontario and New York [11]
Megachile fullawayi A 1921 Guam Hawaii [30]
Megachile gentilis A ? W US Hawaii [9,31]
Megachile lanata A 1700–1800 India and China West Indies and N South America, Florida, Antilles, Hawaii [32]
Megachile rotundata I,A 1920–1940 Europe to China North America to N Mexico, New Zealand, Chile, Argentina, Australia, Canada, Denmark [11,12,19,33]
Megachile rufipennis A 1511–1867 Old World Antilles [32]
Megachile sculpturalis A 1990 Far east China, Korea, Japan US, S Canada, Europe [11,12,34,35]
Megachile timberlakei A 2010 Hawaii? Galapagos [9,22,36]
Megachile umbripenne A 2013 S Asia Fiji, Samoa, Hawaii? [9,26]
Osmia caerulescens A 1800s Europe, N Africa, Near East, India US, S Canada, New Zealand [11,12]
Osmia cornifrons I 1960 East China, Japan US, Denmark, Korea [12]
Osmia cornuta I 1980 Europe, N Africa, Near East establishment not documented [37]
Osmia ribifloris I 1991 W US Maine/E US, establishment uncertain [38]
Osmia taurus A 2000 East China, Japan E US, Michigan [16] Gibbs et al in prep
Pseudoanthidium nana A 2000 Europe and Near East NE US pers. comm. S. Droege
Apidae (30)
Amegilla pulchra A ? Australia Fiji [39]
Anthophora villosula I 1980 Japan E US [12]
Apis cerana A 2007 Asia Australia, Russia, Iran (Crane 1995), Papua New Guinea (Bradbear and MacKay 1995), Samoa, Fiji, Vanuatu [40]
Apis dorsata A ? Asia Japan [41]
Apis florea I 1985 Oman, Asia, Indonesia Iraq, Sudan (Glaiim 2005) [42,43,44,45]
Apis mellifera I 1620 N Europe, Meditteranean globally introduced [11,12]
Bombus hortorum I 1885 UK New Zealand [19]
Bombus hypnorum N 2001 Europe UK [46,47]
Bombus impatiens I 2003 North America Chile, Mexico, Central America, Canada [33,48]
Bombus lucorum 1981 Europe, China Iceland [19]
Bombus ruderatus I 1885 UK New Zealand, Chile, Argentina, Patagonia, Canary Islands [19,33,49]
Bombus subterraneous I 1885 UK New Zealand [19]
Bombus terrestris I 1885 UK Chile, China, Israel, Japan, Mexico, South Africa, South Korea, New Zealand, Tasmania, and Taiwan [19,33,49,50,51]
Braunsapis puangensis A 2003 Asia, india Fiji [52,53,54,55]
Centris nitida A 2000 SW US, Mexico, central, S America Florida [56]
Ceratina arizonensis A 1950 W US Hawaii [9]
Ceratina cobaltina A 1970 Mexico Texas pers. comm. S. Droege
Ceratina dallatorreana A 1940 Meditteranean California [57]
Ceratina dentipes A 1909 Turkey, Cyprus, S Asia, Australia Vanuatu, Fiji, Samoa, Cook Islands, Hawaii, Japan, Mauritius [9]
Ceratina smaragdula I 1960 Pakistan, India, SE Asia Hawaii, Australia [9]
Euglossa dilemma A 2000 Mexico and Central America Florida [58]
Peponapis pruinosa N ? Mexico North America [59]
Plebia frontalis I? 2010 Mexico, Central, South America California pers. comm. S. Droege
Triepeolus remigatus N ? Mexico North America pers. comm. S. Droege
Xenoglossa strenua N ? Mexico North America pers. comm. S. Droege
Xylocopa appendiculata A 2010 Japan and China California [60]
Xylocopa augusti A 2013 Argentina Chile [61]
Xylocopa sonorina I ? W US Samoa, Hawaii, Guam, Northern Marianas Islands, Japan [9,41,62]
Xylocopa tabaniformis parkinsoniae A 1990 South Texas W US pers. comm. S. Droege
Xylocopa tranquebarorum A 2005 Asia Japan [63]

The majority (73%) of the bee species with non-native populations were likely accidentally introduced, while a minority (18%) were deliberately introduced, and a small number (5%) naturally expanded their ranges. The introduction history of the remainder is still uncertain. The majority (69%) of all non-native bee species nest in stems, twigs, existing cavities, or holes they bore into wood, while a smaller number (26%) nest in the ground, and very few (5%) have exposed nests. The proportion of bees that nest in stems, twigs, or other cavities increases to 77% when only accidentally introduced species are considered. Ten of the non-native species are suspected to be oligolectic and have likely been transported with their plant hosts. There are only two cleptoparasitic species represented among the non-native bees, though some non-native Sphecodes have been found in Hawaii (pers. comm. S. Droege).

Islands have the largest number of introduced bees, and indeed, 27 of the 80 non-native bee species are only non-native on islands (not counting Australia as an island). These non-native bee species sometimes become the most diverse and abundant component of the otherwise depauperate bee fauna of island ecosystems. For example, the Galapagos Islands have only one native bee species, but two non-native bee species have been introduced [22]. In the southwest Pacific islands of Fiji, Samoa, and Vanuatu, there is some evidence to indicate that most, if not all, apid and megachilid bees have been introduced by humans [26,64]. A similar situation likely exists in French Polynesia [39]. On the Hawaiian Islands, which likely have only 69 native bee species, there are 14 non-native bee species recorded [9,17].

There are likely many more unrecorded introduced bee species. This list is dominated by species introduced to North America; 34 of the 80 species are only reported as non-native in North America, including Hawaii (25 excluding Hawaii). A total of 55 bee species (69%) have been recorded as introduced to North America and it is unclear whether North America is truly more vulnerable to invasion or whether there is a sampling bias. As a contrast, there are relatively few non-native bees recorded in the well-studied European bee fauna.

3. Impacts

Outside of the genera Apis and Bombus, empirical evidence for impacts is sparse; for 25 species researchers have suggested hypothetical impacts, but have not measured impacts empirically. For an additional 29 species, there are neither hypothetical nor empirical impacts in the literature. For 13 species, there are potential negative impacts, but no potential positive impacts recorded in the literature, and, conversely, there are 11 species for which only potential positives are recorded. Thus, for more than two thirds of the non-native bee species distributed around the world, we have no empirical evidence of any impact of their introduction. This is not equivalent to evidence for the absence of an impact, though such evidence would be less likely to be published [65]. Moreover, it is more difficult to obtain evidence for some impacts than others. For example, it is easier to demonstrate that a non-native bee can pollinate an invasive weed than to show it competes with native bees, as the former can be directly measurable (Figure 1).

Figure 1.

Figure 1

Non-native bees on non-native plants, including (A) Megachile sculpturalis on Carduus acanthoides; (B) Anthidium manicatum on Linaria reticulata; (C) Osmia cornifrons on Pachysandra terminalis; and (D) Anthidium manicatum on Carduus acanthoides. Photographs by the author.

4. Negative Impacts

Goulson [19] conducted a review of the potential negative impacts of 17 non-native bees, which he listed as competition for floral resources or nesting sites, transmission of pathogens or parasites, affecting the seed set of native plants, and pollinating invasive plant species. However, many bee species were introduced after 2000 (Figure S1) and several additional negative impacts have been mentioned in the literature, including alteration of pollination networks, damage to buildings, and genetic introgression through hybridization of managed populations/species with wild populations/species.

4.1. Apis/Bombus

Because entire reviews have been written just on the impacts of the introduced species from the Apis and Bombus genera (e.g., [66,67,68,69]), I have collated selected references for these genera in separate tables in the supplementary materials. Despite the abundance of research on these two genera, the literature is still mixed on their potential impacts and the results of many studies are either inconclusive or contradictory [66]. For example, there is both abundant evidence that honeybees can reduce the pollination of native plants, and also that they can improve the pollination of native plants (Tables S1 and S2). Some also argue that introduced Apis only have negative impacts on other members of their own genus [70]. The negative impact of genetic introgression has only been recorded for Apis/Bombus, and there seems to be some strong empirical support for this potential outcome in Bombus terrestris. Though there is some empirical support for all negative impacts (except damage to buildings) across these two genera, there are also some studies that record the absence of competition, pollination of invasive weeds, and decreasing the fitness of native plants. The only category where there is plenty of empirical support and no contradicting studies is the spread of parasites and pathogens introduced along with Apis/Bombus species (Table S1).

4.2. Other Genera

The strongest evidence for negative impacts in non-Apis/Bombus species is in competition for floral resources, transmission of parasites and pathogens, and pollination of invasive weeds. However, there is little empirical evidence that these non-native bees compete for floral resources and there is empirical evidence demonstrating a lack competition in several cases (Table 2). There only seems to be evidence for nesting competition with native species in the genus Megachile and the potential economic negative of damage to buildings has only been hypothetically recorded for Lithurgus chrysurus [71,72], though some other wood boring species may also have this potential. There is no empirical support for the potential of these non-Apis/Bombus species to degrade pollination networks or to negatively affect the pollination of native plant species, but there is some concern in the literature that several species will have this effect, particularly on islands [26].

Table 2.

Potential negative impacts of non-Apis or Bombus species, including competition for nesting sites and floral resources, co-introduction with pathogens or parasites, pollination of invasive weeds, alteration of resident pollination networks, damage to buildings, and changing pollination of native plant species. Bold and underlined text refers to citations with an empirical component while unbolded text refers to papers that refer to impacts only from a hypothetical standpoint. Light grey shading indicates species for which neither positive nor negative impacts have been recorded, while dark grey indicates species for which only positive impacts have been recorded. “But see” refers to manuscripts that show evidence or describe the opposite of the effect.

Non-native Species Nesting Sites Floral Resources Pathogens/Parasites Invasive Weeds Alteration of Pollination Networks Damage to Buildings Change Pollination
Colletidae
Chilicola rostrata
Hylaeus albonitens [76]
Hylaeus hyalinatus [77]
Hylaeus leptocephalus
Hylaeus punctatus
Hylaeus strenuus [14]
Hylaeus (Prosopis) variegates ¥
Hyleoides concinna [15]
Andrenidae
Andrena wilkella
Halictidae
Halictus tectus
Lasioglossum eleutherense
Lasioglossum imbrex
Lasioglossum impavidum [76]
Lasioglossum leucozonium
Lasioglossum microlepoides
Nomia melanderi
Megachilidae
Afranthidium repetitum
Anthidium manicatum [73] but see [78] [73] [73,78]
Anthidium oblongatum
Anthidium vigintiduopunctatum
Chelostoma campanularum **
Chelostoma rapunculi **
Coelioxys coturnix
Heriades truncorum
Hoplitis adunca
Hoplitis anthocopoides **
Lithurgus bractipes [26]
Lithurgus chrysurus ** [71,72]
Lithurgus huberi **
Lithurgus scabrosus [26]
Megachile apicalis ** [19,79],[80] [81]
Megachile australis [26]
Megachile concinna ** [82]
Megachile ericetorum
Megachile fullawayi
Megachile gentilis
Megachile lanata
Megachile rotundata ** [79] but see [83],[84],[85] But see [84] [19],[86] [19] but see [84]
Megachile rufipennis
Megachile sculpturalis [87,88] [89,90] [90]
Megachile timberlakei [22] [22] [22] [22]
Megachile umbripenne [26]
Osmia caerulescens
Osmia cornifrons [86]
Osmia cornuta ¥
Osmia ribifloris
Osmia taurus
Pseudoanthidium nana **
Apidae
Amegilla pulchra [39]
Anthophora plumipes
Braunsapis puangensis [52] [28,52],[91]
Centris nitida But see [56] [92]
Ceratina arizonensis [76]
Ceratina cobaltina ¥
Ceratina dallatorreana
Ceratina dentipes [76]
Ceratina smaragdula [76]
Euglossa dilemma [93,94]
Peponapis pruinosa **
Plebia frontalis ¥
Triepeolus remigatus
Xenoglossa strenua
Xylocopa appendiculata [60]
Xylocopa augusti
Xylocopa sonorina [39] [62,95]
Xylocopa tabaniformis parkinsoniae
Xylocopa tranquebarorum [63,96,97]

** oligolectic; ¥ establishment uncertain.

If hypothetical impacts can be considered a measure of the relative amount of concern about the introduction of a given species, the European Wool Carder bee (Anthidium manicatum), is the most concerning of the non-Apis/Bombus introduced bees. Indeed, the range of this species has increased rapidly in recent years, and it seems to be approaching a global distribution [73]. There is evidence that the non-native Osmia cornifrons and O. cornuta and their native congener O. lignaria can share some parasites [74,75], though the potential for the introduced bee to spread the parasite to native bee species has not been explored. In contrast, the most empirical evidence for negative impacts seems to be for the globally introduced managed Alfalfa Leaf Cutter Bee (Megachile rotundata) and the accidentally introduced Taiwanese bamboo carpenter bee (Xylocopa tranquebarorum).

5. Positive Impacts

To the best of my knowledge the positive impacts of introduced bees have not been reviewed although the pollination services provided by diverse communities of bees are well known [98,99,100,101] and the interactions between native and non-native bees might even be beneficial in some cases [102]. Non-native bees can have positive impacts by pollinating agricultural crops, acting as biological control agents, rescuing native plant species whose native pollinators have been lost, increasing resilience to human disturbance and climate change, encouraging scientific investigations through lab rearing, serving as bio-indicators, and promoting the study of natural history.

5.1. Apis/Bombus

As with negative impacts, the positive impacts of the Apis and Bombus genera are reviewed in the supplemental materials (Table S2). They can have the same positive impacts as the other bee genera and, as with the negative impacts, are better studied in general. The majority of these bees were deliberately introduced for their pollination services to agriculture, which are widely recognized. However, their ease of management has also led to their utility as study species for scientific research. They have also been demonstrated to rescue native plant species when their native pollinators are in decline, though their role in the decline of these native pollinators is unclear (Table S1). It is also possible that their impacts on native pollinators are confounded with human disturbance, as several of these species are more resilient to human impacts.

5.2. Other Genera

In the non-Apis/Bombus genera, the strongest evidence for positive impacts comes unsurprisingly from the potential to be agricultural pollinators. There is likely a publication bias for this effect, as it confers an economic benefit to humans [103]. Several non-native bee species were deliberately introduced for their pollination services (Table 1), but this is also listed as a hypothetical benefit for many accidentally introduced bee species (Table 3).

Table 3.

Potential positive impacts of non-Apis or Bombus species, including agricultural pollination, biocontrol of pest species, ability to encourage scientific research in lab-reared studies, as bioindicators, or for studies of natural history, and resilience to human disturbance and climate change. Bold and underlined text refers to citations with an empirical component while unbolded text refers to papers that refer to impacts only from a hypothetical standpoint. Light grey shading indicates species for which neither positive nor negative impacts have been recorded, while dark grey indicates species for which only negative impacts have been recorded. “But see” refers to manuscripts that show evidence or describe the opposite of the effect.

Non-native Species Agricultural Pollination Biocontrol Lab Reared Bioindicators Natural History Resilience
Colletidae
Chilicola rostrata
Hylaeus albonitens
Hylaeus hyalinatus [77]
Hylaeus leptocephalus
Hylaeus punctatus
Hylaeus strenuus
Hylaeus (Prosopis) variegates ¥
Hyleoides concinna
Andrenidae
Andrena wilkella [31] [107]
Halictidae
Halictus tectus
Lasioglossum eleutherense
Lasioglossum imbrex
Lasioglossum impavidum
Lasioglossum leucozonium [108] *
Lasioglossum microlepoides
Nomia melanderi [103],[109,110]
Megachilidae
Afranthidium repetitum
Anthidium manicatum [111]
Anthidium oblongatum
Anthidium vigintiduopunctatum [26]
Chelostoma campanularum **
Chelostoma rapunculi **
Coelioxys coturnix
Heriades truncorum [112]
Hoplitis adunca
Hoplitis anthocopoides **
Lithurgus bractipes [26]
Lithurgus chrysurus **
Lithurgus huberi **
Lithurgus scabrosus [26]
Megachile apicalis **
Megachile australis [26]
Megachile concinna ** [113]
Megachile ericetorum
Megachile fullawayi
Megachile gentilis [31]
Megachile lanata
Megachile rotundata ** [26,31],[38],[73,109,114],[115],[116] [116,117,118,119] [120]
Megachile rufipennis
Megachile sculpturalis
Megachile timberlakei
Megachile umbripenne [26]
Osmia caerulescens
Osmia cornifrons [109,114,121],[122,123,124] [125,126,127]
Osmia cornuta ¥ [109],[128],[129] [130] [131] [104]
Osmia ribifloris [19],[38]
Osmia taurus
Pseudoanthidium nana **
Apidae
Amegilla pulchra
Anthophora plumipes [132]
Braunsapis puangensis [52,133] [52,53,133]
Centris nitida [56]
Ceratina arizonensis
Ceratina cobaltina ¥
Ceratina dallatorreana
Ceratina dentipes
Ceratina smaragdula [134]
Euglossa dilemma [135]
Peponapis pruinosa ** [59]
Plebia frontalis ¥
Triepeolus remigatus
Xenoglossa strenua [136]
Xylocopa appendiculata
Xylocopa augusti
Xylocopa sonorina [31]
Xylocopa tabaniformis parkinsoniae
Xylocopa tranquebarorum

* Dissertation; ** oligolectic; ¥ establishment uncertain.

Because deliberately introduced species are generally easy to manage and rear in a laboratory setting, many of these provide an additional benefit to science and are often used for pesticide, genetic, and behavioral studies. In the case of Osmia cornuta, they have even shown to be potentially useful for the application of biocontrol to manage invasive pest species in crops [13] or bioindicators for environmental quality [104]. Many other bee species have the potential to provide this benefit, particularly those that readily nest in hollow tubes as a high proportion of introduced bees do.

Finally, many of these non-native species have been accidentally spread by humans because they flourish in human-modified landscapes. These bee species have the potential to supplement pollination services where native species have been lost and demonstrate resilience to human disturbance and climate change. Indeed, several of the listed species have only been recorded in urban areas (e.g., Anthidium oblongatum [105], Pseudanthidium nana (pers. comm. S. Droege)). Bees capable of handling human disturbance and habitat degradation might not only provision crop species with pollination services, but also have the potential to rescue native plant species whose more sensitive native pollinators have been lost [106], though this has not yet been listed as a potential benefit of non-Apis/Bombus genera.

6. Discussion

Though much research has been done on the impacts of bees in the Apis and Bombus genera, much less is known about the impacts of non-native bees in other genera. This is partly due to the fact that many of these bees have either only recently been introduced (e.g., [24]), or only recently been discovered as non-native [11]. It is particularly important to understand these impacts as bees continue to be accidentally introduced by humans, and expand their distributions in response to disturbance and climate change. As other authors have noted (e.g., [19]), conducting experiments to demonstrate some of the aforementioned impacts can be challenging, but with multiple studies in disparate locations, we can get a better understanding of the overall context dependence of negative and positive species impacts.

Future research should explore the impacts of bees beyond their roles as pollinators or competitors in ecological communities, for example, as prey in altered trophic webs. A sudden influx of a highly abundant food source, even if it is novel, might have implications for some predators [137]. It may change the population dynamics of insectivorous birds, generalist insect predators, or insects that prey solely on bees, such as beewolves [138]. There may also be interesting impacts of non-native bees on public perception of important ecological issues [139].

As is sometimes the case with introduced species [140], some of the bee species that are considered invasive in their introduced range have become quite rare in their native range, such as Bombus ruderatus [141] and B. subterraneous [142]. The management options for these bees in their introduced range are more complicated because conservation in their native range is also a concern. Indeed, some breeding programs for reintroduction of these Bombus species are being developed in their non-native range in New Zealand [143].

7. Conclusions

Invasive non-native bees present a complex topic because their negative impacts may be inextricably tied to the pollination services they provide to humans and the potential positive impacts they have in their role as pollinators. Whether or not they can have a dramatic effect on native communities and ecosystems or whether anthropogenic impacts such as habitat degradation are driving changes in community structure is unknown and probably understudied [85,144]. However, concerns about non-native bees exist, especially when their ranges expand rapidly, and for the majority of introduced bee species little or nothing is known. Thus, their role in novel ecosystems should be addressed, weighing both positive and negative influences they have on native species.

Acknowledgments

I would to acknowledge help from the many researchers who contributed observations or references on non-native bees, including Alfredo Valido, Sam Droege, Amber D. Tripodi, Jonathan B. Koch, Michael Orr, Elias H. Bloom, Jason Gibbs, Russel Barsh, Rufus Isaacs, Evan A. Sugden, Jim Cane, Jack Neff, Heather Moylett, Colin Phifer, Richard Orr, and Don Harvey. Thanks to Joe Keller and Eric Allen for friendly reviews. This work was funded by the Pennsylvania State University and National Science Foundation (grant #DMS-1313115).

Supplementary Materials

The following are available online at http://www.mdpi.com/2075-4450/7/4/69/s1. Table S1: Selected references of potential negative impacts of Apis or Bombus species; Table S2: Selected references for potential positive impacts of Apis or Bombus species. Figure S1: Frequency histogram of first collection records for introduced bee species. Note that dates of introduction are approximated and for most species have not been carefully studied.

Conflicts of Interest

The author declares no conflict of interest.

References

  • 1.Lovett G.M., Weiss M., Liebhold A.M., Holmes T.P., Leung B., Lambert K.F., Orwig D.A., Campbell F.T., Rosenthal J., McCullough D.G., et al. Nonnative forest insects and pathogens in the United States: Impacts and policy options. Ecol. Appl. 2016;26:1437–1455. doi: 10.1890/15-1176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Kovacs K.F., Haight R.G., McCullough D.G., Mercader R.J., Siegert N.W., Liebhold A.M. Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecol. Econ. 2010;69:569–578. doi: 10.1016/j.ecolecon.2009.09.004. [DOI] [Google Scholar]
  • 3.Gray M.E., Sappington T.W., Miller N.J., Moeser J., Bohn M.O. Adaptation and Invasiveness of Western Corn Rootworm: Intensifying Research on a Worsening Pest. Annu. Rev. Entomol. 2009;54:303–321. doi: 10.1146/annurev.ento.54.110807.090434. [DOI] [PubMed] [Google Scholar]
  • 4.Pimentel D., Zuniga R., Morrison D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 2005;52:273–288. doi: 10.1016/j.ecolecon.2004.10.002. [DOI] [Google Scholar]
  • 5.Morales C.L.C., Arbetman M.M.P., Cameron S.A., Aizen M.A. Rapid ecological replacement of a native bumble bee by invasive species. Front. Ecol. Environ. 2013;11:529–534. doi: 10.1890/120321. [DOI] [Google Scholar]
  • 6.Wenner A., Thorp R., Barthell J. Biological control and eradication of feral honey bee colonies on Santa Cruz Island, California: A summary; Proceedings of the 7th California Islands Symposium Institute Foe Wildlife Studies; Arcata, CA, USA. 5–8 February 2008. [Google Scholar]
  • 7.Schlaepfer M.A., Sax D.F., Olden J.D. The Potential Conservation Value of Non-Native Species. Conserv. Biol. 2011;25:428–437. doi: 10.1111/j.1523-1739.2010.01646.x. [DOI] [PubMed] [Google Scholar]
  • 8.Montalva J., Packer L. First record of the bee Chilicola (Pseudiscelis) rostrata (Friese, 1906) (Colletidae: Xeromelissinae) in Chile: A recent adventive species to the country? Bol. Biodivers. Chile. 2012;7:63–65. [Google Scholar]
  • 9.Snelling R. Bees of the Hawaiian Islands, exclusive of Hylaeus (Nesoprosopis)(Hymenoptera: Apoidea) J. Kansas Entomol. Soc. 2003;76:342–356. [Google Scholar]
  • 10.Tonietto R., Ascher J.S. Occurrence of the Old World bee species Hylaeus hyalinatus, Anthidium manicatum, A. oblongatum, and Megachile sculpturalis, and the native species Coelioxys banksi, Lasioglossum michiganense, and L. zophops in Illinois (Hymenoptera: Apoidea: Colletidae, Halictidae, Megachilidae) Gt. Lakes Entomol. 2008;41:200–203. [Google Scholar]
  • 11.Sheffield C., Dumesh S., Cheryomina M. Hylaeus punctatus (Hymenoptera: Colletidae), a bee species new to Canada, with notes on other non-native species. J. Entomol. Soc. Ont. 2011;142:29–43. [Google Scholar]
  • 12.Donovall L.R., vanEngelsdorp D. A Checklist of the Bees (Hymenoptera: Apoidea) of Pennsylvania. J. Kansas Entomol. Soc. 2010;83:7–24. doi: 10.2317/JKES808.29.1. [DOI] [Google Scholar]
  • 13.Magnacca K.N., Nagamine W.T., Dathe H.H. Hylaeus strenuus (Hymenoptera: Colletidae), a new alien bee on O’ahu. Eldredge Bish. Museum Occas. Pap. 2009;109:23–24. [Google Scholar]
  • 14.Magnacca K., Nagamine W., Dathe H. Hylaeus strenuus (Hymenoptera: Colletidae), a new alien bee on O’ahu. In: Evenhuis N., Eldredge L., editors. Records of the Hawaii Biological Survey for 2009-2010. Volume 109. Bishop Museum; Honolulu, HI, USA: 2011. pp. 23–24. [Google Scholar]
  • 15.Donovan B. Occurrence of the Australian bee Hyleoides concinna (Hymenoptera: Colletidae) in New Zealand. N. Z. J. Zool. 1983;10:345–347. doi: 10.1080/03014223.1983.10423929. [DOI] [Google Scholar]
  • 16.Giles V., Ascher J. A survey of the bees of the Black Rock Forest preserve, New York (Hymenoptera: Apoidea) J. Hymenopt. Res. 2006;15:208–231. [Google Scholar]
  • 17.Magnacca K., King C. Assessing the Presence and Distribution of 23 Hawaiian Yellow-Faced Bee Species on Lands Adjacent to Military Installations on O’ahu and Hawai’i Island. Pacific Cooperative Studies Unit, University of Hawaii at Manoa; Honolulu, HI, USA: 2013. [Google Scholar]
  • 18.Magnacca K., Gibbs J., Droege S. Notes on alien and native bees (Hymenoptera: Apoidea) from the Hawaiian Islands. Occas. Pap. 2013;114:61–65. [Google Scholar]
  • 19.Goulson D. Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 2003;34:1–26. doi: 10.1146/annurev.ecolsys.34.011802.132355. [DOI] [Google Scholar]
  • 20.Baumann J., Walker K., Threlfall C. African Carder bee, “Afranthidium (Immanthidium) repetitum” (Hymenoptera: Megachilidae): A new exotic species for Victoria. Vic. Nat. 2016;133:21–25. [Google Scholar]
  • 21.Gonzalez V.H., Griswold T., Ayala R. Two new species of nocturnal bees of the genus Megalopta (Hymenoptera: Halictidae) with keys to species. Rev. Biol. Trop. 2010;58:255–263. doi: 10.15517/rbt.v58i1.5207. [DOI] [PubMed] [Google Scholar]
  • 22.Rasmussen C., Carríon A., Castro-Urgal R. Megachile timberlakei Cockerell (Hymenoptera: Megachilidae): Yet another adventive bee species to the Galápagos Archipelago. Pan-Pacific Entomol. 2012;88:98–102. doi: 10.3956/2012-04.1. [DOI] [Google Scholar]
  • 23.Eickwort G. Two European species of Chelostoma established in New York State (Hymenoptera: Megachilidae) Psyche (Stuttg) 1980;87:315–324. doi: 10.1155/1980/24124. [DOI] [Google Scholar]
  • 24.Notton D.G., Tang C.Q., Day A.R. Viper’s Bugloss Mason Bee, Hoplitis (Hoplitis) adunca, new to Britain (Hymenoptera, Megachilidae, Megachilinae, Osmiini) Br. J. Entomol. Nat. Hist. 2016;29:134–143. [Google Scholar]
  • 25.Eickwort G. Hoplitis anthocopoides, a European mason bee established in New York state (Hymenoptera: Megachilidae) Psyche. 1970;77:190–201. doi: 10.1155/1970/95408. [DOI] [Google Scholar]
  • 26.Groom S., Hayes S., Ngo H., Stevens M., Schwarz M. Recipe for disruption: Multiple recent arrivals of megachilid bees in Pacific archipelagos. J. Insect Conserv. 2014;18:613–622. doi: 10.1007/s10841-014-9665-1. [DOI] [Google Scholar]
  • 27.Gonzalez V., Engel M., Lucia M. Species status and new distribution records for Lithurgus huberi (Hymenoptera, Megachilidae, Lithurginae) J. Hymenopt. 2013;30:13. doi: 10.3897/jhr.30.4018. [DOI] [Google Scholar]
  • 28.Silva D., Gonzalez V., Melo G., Lucia M. Seeking the flowers for the bees: Integrating biotic interactions into niche models to assess the distribution of the exotic bee species Lithurgus huberi in South America. Ecological. 2014;273:200–209. doi: 10.1016/j.ecolmodel.2013.11.016. [DOI] [Google Scholar]
  • 29.Vélez-Espino L.A., McLaughlin R.L., Jones M.L., Pratt T.C. Demographic analysis of trade-offs with deliberate fragmentation of streams: Control of invasive species versus protection of native species. Biol. Conserv. 2011;144:1068–1080. doi: 10.1016/j.biocon.2010.12.026. [DOI] [Google Scholar]
  • 30.Timberlake P.H. The discovery of a fifth species of Megachile on Oahu. Proc. Hawaiian Entomol. Soc. 1921;4:551–557. [Google Scholar]
  • 31.Bohart G. Introduction of foreign pollinators, prospects and problems. Proc. 1st Int. Symp. Pollinat. 1962;7:181–188. [Google Scholar]
  • 32.Genaro J. Origins, composition and distribution of the bees of Cuba (Hymenoptera: Apoidea: Anthophila) Insecta Mundi. 2008;52:1–16. [Google Scholar]
  • 33.Ruz L. Bee pollinators introduced to Chile: A review. In: Kevan P., Imperatriz-Fonseca V., editors. Pollinating bees: The Conservation Link Between Agriculture and Nature. Ministry of Environment/Brasilia; Brasília, Brazil: 2002. pp. 155–167. [Google Scholar]
  • 34.Mangum W., Brooks R. First records of Megachile (Callomegachile) sculpturalis Smith (Hymenoptera: Megachilidae) in the continental United States. J. Kansas Entomol. Soc. 1997;70:140–142. [Google Scholar]
  • 35.Westrich P., Knapp A., Berney I. Megachile sculpturalis Smith 1853 (Hymenoptera, Apidae), a new species for the bee fauna of Germany, now north of the Alps. Eucera. 2015;9:3–10. [Google Scholar]
  • 36.Castro-Urgal M., Herrera H., Olesen J. Invaders of pollination networks in the Galápagos Islands. Proc. R. Soc. B-Biol. Sci. 2013;280:20123040. doi: 10.1098/rspb.2012.3040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Torchio P., Asensio E. The introduction of the European bee, Osmia cornuta Latr into the US as a potential pollinator of orchard crops, and a comparison of its manageability with Osmia. J. Kansas Entomol. Soc. 1985;58:42–52. [Google Scholar]
  • 38.Stubbs C., Drummond F., Osgood E. Osmia ribifloris biedermannii and Megachile rotundata (Hymenoptera: Megachilidae) introduced into the lowbush blueberry agroecosystem in Maine. J. Kansas Entomol. Soc. 1994;67:173–185. [Google Scholar]
  • 39.Groom S.S.V.C., Stevens M.M.I., Ramage T., Schwarz M.P. Origins and implications of apid bees (Hymentopera: Apidae) in French Polynesia. Entomol. Sci. 2016 doi: 10.1111/ens.12230. [DOI] [Google Scholar]
  • 40.Koetz A. Ecology, behaviour and control of Apis cerana with a focus on relevance to the Australian incursion. Insects. 2013;4:558–592. doi: 10.3390/insects4040558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Mito T., Uesugi T. Invasive alien species in Japan: The status quo and the new regulation for prevention of their adverse effects. Glob. Environ. Res. 2004;8:171–191. [Google Scholar]
  • 42.Mogga J., Ruttner F. Apis florea in Africa: Source of the founder population. Bee World. 1988;69:100–103. doi: 10.1080/0005772X.1988.11098960. [DOI] [Google Scholar]
  • 43.El Shafie H.A.F., Mogga J.B.B., Basedow T. Studies on the possible competition for pollen between the honey bee, Apis mellifera sudanensis, and the imported dwarf honey bee Apis florea (Hym., Apidae) in North-Khartoum (Sudan) J. Appl. Entomol. 2002;126:557–562. doi: 10.1046/j.1439-0418.2002.00711.x. [DOI] [Google Scholar]
  • 44.Moritz R.F.A., Haddad N., Bataieneh A., Shalmon B., Hefetz A. Invasion of the dwarf honeybee Apis florea into the near East. Biol. Invasions. 2010;12:1093–1099. doi: 10.1007/s10530-009-9527-z. [DOI] [Google Scholar]
  • 45.Haddad N., Fuchs S., Hepburn H.R., Radloff S.E. Apis florea in Jordan: Source of the founder population. Apidologie. 2009;40:508–512. doi: 10.1051/apido/2009011. [DOI] [Google Scholar]
  • 46.Goulson D., Williams P. Bombus hypnorum (L.)(Hymenoptera: Apidae), a new British bumblebee? Br. J. Entomol. Nat. Hist. 2001;14:129–131. [Google Scholar]
  • 47.Betts C. Is Bombus hypnorum (Hymenoptera: Apidae) becoming the dominant early-season bumblebee? A back-garden study in east. Br. J. Entomol. Nat. Hist. 2015;28:185–191. [Google Scholar]
  • 48.Ratti C., Colla S. Discussion of the presence of an eastern bumble bee species (Bombus impatiens Cresson) in western Canada. Pan-Pac. Entomol. 2010;86:29–31. doi: 10.3956/2009-19.1. [DOI] [Google Scholar]
  • 49.Montalva J., Dudley L., Arroyo M. Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.) in Chile. J. Apic. Res. 2011;50:11–21. doi: 10.3896/IBRA.1.50.1.02. [DOI] [Google Scholar]
  • 50.Torretta J., Medan D., Abrahamovich A. First record of the invasive bumblebee Bombus terrestris (L.)(Hymenoptera, Apidae) in Argentina. Trans. Am. Entomol. Soc. 2006;132:285–289. [Google Scholar]
  • 51.Acosta A., Giannini T., Imperatriz-Fonseca V. Worldwide alien invasion: A methodological approach to forecast the potential spread of a highly invasive pollinator. PLoS ONE. 2016;11:e0148295. doi: 10.1371/journal.pone.0148295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Groom S., Tuiwawa M., Stevens M. Recent introduction of an allodapine bee into Fiji: A new model system for understanding biological invasions by pollinators. Insect Sci. 2015;22:532–540. doi: 10.1111/1744-7917.12136. [DOI] [PubMed] [Google Scholar]
  • 53.Shenoy M., Borges R. A novel mutualism between an ant-plant and its resident pollinator. Naturwissenschaften. 2008;95:61–65. doi: 10.1007/s00114-007-0289-0. [DOI] [PubMed] [Google Scholar]
  • 54.Silva C., Stevens M., Schwarz M. Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies. Insectes Soc. 2016;63:67–78. doi: 10.1007/s00040-015-0436-0. [DOI] [Google Scholar]
  • 55.Fuller S., Schwarz M., Tierney S. Phylogenetics of the allodapine bee genus Braunsapis: Historical biogeography and long-range dispersal over water. J. Biogeogr. 2005;32:2135–2144. doi: 10.1111/j.1365-2699.2005.01354.x. [DOI] [Google Scholar]
  • 56.Downing J., Liu H. Friend or foe? Impacts of the introduced tropical oil bee Centris nitida on a threatened and specialized native mutualism in Southern Florida. Biol. Invasions. 2012;14:2175–2185. doi: 10.1007/s10530-012-0223-z. [DOI] [Google Scholar]
  • 57.Daly H. Biological studies on Ceratina dallatorreana, an alien bee in California which reproduces by parthenogenesis (Hymenoptera: Apoidea) Ann. Entomol. Soc. Am. 1966;59:1138–1154. doi: 10.1093/aesa/59.6.1138. [DOI] [Google Scholar]
  • 58.Skov C., Wiley J. Establishment of the neotropical orchid bee Euglossa viridissima (Hymenoptera: Apidae) in Florida. Fla. Entomol. 2005;88:225–227. doi: 10.1653/0015-4040(2005)088[0225:EOTNOB]2.0.CO;2. [DOI] [Google Scholar]
  • 59.López-Uribe M., Cane J. Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proc. R. Soc. B Biol. Sci. 2016;283:1–9. doi: 10.1098/rspb.2016.0443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Dahlberg L., Hauser M., Yanega D. Japanese carpenter bee, Xylocopa appendiculata Smith 1852 (Hymenoptera: Apidae) potentially established in Santa Clara County, first record for North America. Pan-Pac. Entomol. 2013;89:226–229. doi: 10.3956/2013-22.1. [DOI] [Google Scholar]
  • 61.Montalva J., Allendes J., Lucia M. The large carpenter bee Xylocopa augusti (Hymenoptera: Apidae): New record for Chile. J. Melittol. 2013;12:1–6. doi: 10.17161/jom.v0i12.4480. [DOI] [Google Scholar]
  • 62.Barrows E. Robbing of exotic plants by introduced carpenter and honey bees in Hawaii, with comparative notes. Biotropica. 1980;12:23–29. doi: 10.2307/2387770. [DOI] [Google Scholar]
  • 63.Okabe K., Masuya H., Kawazoe K., Makino S. Invasion pathway and potential risks of a bamboo-nesting carpenter bee, Xylocopa tranquebarorum (Hymenoptera: Apidae), and its micro-associated mite introduced into Japan. Appl. Entomol. Zool. 2010;45:329–337. doi: 10.1303/aez.2010.329. [DOI] [Google Scholar]
  • 64.Groom S., Ngo H., Rehan S., Skelton P. Multiple recent introductions of apid bees into Pacific archipelagos signify potentially large consequences for both agriculture and indigenous ecosystems. Biol. Invasions. 2014;16:2293–2302. doi: 10.1007/s10530-014-0664-7. [DOI] [Google Scholar]
  • 65.Dickersin K. Publication bias: Recognizing the problem, understanding its origins and scope, and preventing harm. In: Rothstein H.R., Sutton A.J., Borenstein M., editors. Publication bias in meta-analysis: Prevention, Assessment and Adjustments. John Wiley & Sons; San Francisco, CA, USA: 2005. pp. 11–32. [Google Scholar]
  • 66.Paini D. Impact of the introduced honey bee (Apis mellifera)(Hymenoptera: Apidae) on native bees: A review. Austral Ecol. 2004;29:399–407. doi: 10.1111/j.1442-9993.2004.01376.x. [DOI] [Google Scholar]
  • 67.Dafni A., Kevan P., Gross C., Goka K. Bombus terrestris, pollinator, invasive and pest: An assessment of problems associated with its widespread introductions for commercial purposes. Appl. Entomol. Zool. 2010;45:101–113. doi: 10.1303/aez.2010.101. [DOI] [Google Scholar]
  • 68.Valido A., Rodríguez-Rodríguez M. Impacto de la introducción de la abeja doméstica (Apis mellifera, Apidae) en el Parque Nacional del Teide (Tenerife, Islas Canarias) Ecosistemas. 2014;23:58–66. doi: 10.7818/ECOS.2014.23-3.08. [DOI] [Google Scholar]
  • 69.Abrahamovich A., Telleria M., Díaz N. Bombus species and their associated flora in Argentina. Bee World. 2001;82:76–87. doi: 10.1080/0005772X.2001.11099505. [DOI] [Google Scholar]
  • 70.Moritz R., Härtel S., Neumann P. Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience. 2005;12:289–301. doi: 10.2980/i1195-6860-12-3-289.1. [DOI] [Google Scholar]
  • 71.Rust R., Cambon G., Grossa J. Nesting biology and foraging ecology of the wood-boring bee Lithurgus chrysurus (Hymenoptera: Megachilidae) J. Kansas. 2004;77:269–279. doi: 10.2317/0402.17.1. [DOI] [Google Scholar]
  • 72.Rozen J., Wyman E. Early nesting biology of the wood-nesting adventive bee, Lithurgus chrysurus Fonscolombe (Apoidea: Megachilidae: Lithurginae) Am. Museum Novit. 2014;3804:1–12. doi: 10.1206/3804.1. [DOI] [Google Scholar]
  • 73.Gibbs J., Sheffield C. Rapid range expansion of the Wool-Carder Bee, Anthidium manicatum (Linnaeus)(Hymenoptera: Megachilidae), in north america. J. Kansas Entomol. Soc. 2009;82:21–29. doi: 10.2317/JKES805.27.1. [DOI] [Google Scholar]
  • 74.Bosch J. Parasitism in wild and managed populations of the almond pollinator Osmia cornuta Latr.(Hymenoptera: Megachilidae) J. Apic. Res. 1992;31:77–82. doi: 10.1080/00218839.1992.11101266. [DOI] [Google Scholar]
  • 75.McKinney M., Park Y. Distribution of Chaetodactylus krombeini (Acari: Chaetodactylidae) within Osmia cornifrons (Hymenoptera: Megachilidae) nests: Implications for population. Exp. Appl. Acarol. 2013;60:153–161. doi: 10.1007/s10493-012-9629-7. [DOI] [PubMed] [Google Scholar]
  • 76.Magnacca K.N. Conservation status of the endemic bees of Hawai‘i, Hylaeus (Nesoprosopis) (Hymenoptera: Colletidae) Pac. Sci. 2007;61:173–190. doi: 10.2984/1534-6188(2007)61[173:CSOTEB]2.0.CO;2. [DOI] [Google Scholar]
  • 77.MacIvor J.S., Cabral J.M., Packer L. Pollen specialization by solitary bees in an urban landscape. Urban Ecosyst. 2014;17:139–147. doi: 10.1007/s11252-013-0321-4. [DOI] [Google Scholar]
  • 78.Soper J., Beggs J. Assessing the impact of an introduced bee, Anthidium manicatum, on pollinator communities in New Zealand. N. Z. J. Bot. 2013;51:213–228. doi: 10.1080/0028825X.2013.793202. [DOI] [Google Scholar]
  • 79.Barthell J., Frankie G. Invader effects in a community of cavity nesting megachilid bees (Hymenoptera: Megachilidae) Environ. Entomol. 1998;27:240–247. doi: 10.1093/ee/27.2.240. [DOI] [Google Scholar]
  • 80.Frankie G., Thorp R. Monitoring solitary bees in modified wildland habitats: Implications for bee ecology and conservation. Environ. Entomol. 1998;27:1137–1148. doi: 10.1093/ee/27.5.1137. [DOI] [Google Scholar]
  • 81.Mciver J., Thorp R., Erickson K. Pollinators of the invasive plant, yellow starthistle (Centaurea solstitialis), in north-eastern Oregon, USA. Weed Biol. Manag. 2009;9:137–145. doi: 10.1111/j.1445-6664.2009.00331.x. [DOI] [Google Scholar]
  • 82.Alvarez L., Lucia M., Aquino D. Nesting biology and associated insect enemies of the exotic leaf cutter bee Megachile (Eutricharaea) concinna (Hymenoptera: Megachilidae) in Argentina. J. Apic. Res. 2016;54:305–313. doi: 10.1080/00218839.2016.1159402. [DOI] [Google Scholar]
  • 83.Donovan B. Interactions between native and introduced bees in New Zealand. N. Z. J. Ecol. 1980;3:104–116. [Google Scholar]
  • 84.Woodward D. Monitoring for impact of the introduced leafcutting bee, Megachile rotundata (F.)(Hymenoptera: Megachilidae), near release sites in South Australia. Aust. J. Entomol. 1996;35:187–191. doi: 10.1111/j.1440-6055.1996.tb01385.x. [DOI] [Google Scholar]
  • 85.Howlett B., Donovan B. A review of New Zealand’s deliberately introduced bee fauna: current status and potential impacts. N. Z. Entomol. 2010;33:92–101. doi: 10.1080/00779962.2010.9722196. [DOI] [Google Scholar]
  • 86.Hedtke S., Blitzer E., Montgomery G., Danforth B. Introduction of non-native pollinators can lead to trans-continental movement of bee-associated fungi. PLoS ONE. 2015;10:e0130560. doi: 10.1371/journal.pone.0130560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Laport R., Minckley R. Occupation of active Xylocopa virginica nests by the recently invasive Megachile sculpturalis in upstate New York. J. Kansas Entomol. Soc. 2012;85:384–386. doi: 10.2317/0022-8567-85.4.384. [DOI] [Google Scholar]
  • 88.Parys K., Tripodi A., Sampson B. The Giant Resin Bee, Megachile sculpturalis Smith: New Distributional Records for the Mid-and Gulf-south USA. Biodivers. Data J. 2015;3:e6733. doi: 10.3897/BDJ.3.e6733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Mangum W., Sumner S. A survey of the North American range of Megachile (Callomegachile) sculpturalis, an adventive species in North America. J. Kansas Entomol. Soc. 2003;76:658–662. [Google Scholar]
  • 90.Quaranta M., Sommaruga A., Balzarini P. A new species for the bee fauna of Italy: Megachile sculpturalis continues its colonization of Europe. Bull. Insectol. 2014;67:287–293. [Google Scholar]
  • 91.Hodge S., Prasad A. Factors influencing the foraging activity of the allodapine bee Braunsapis puangensis on creeping daisy (Sphagneticola trilobata) in Fiji. J. Hymenopt. Res. 2013;35:56–69. doi: 10.3897/jhr.35.6006. [DOI] [Google Scholar]
  • 92.Liu H., Pemberton R. Pollination of an invasive orchid, Cyrtopodium polyphyllum (Orchidaceae), by an invasive oil-collecting bee, Centris nitida, in southern Florida. Botany. 2010;88:290–295. doi: 10.1139/B10-017. [DOI] [Google Scholar]
  • 93.Pemberton R., Liu H. Potential of invasive and native solitary specialist bee pollinators to help restore the rare cowhorn orchid (Cyrtopodium punctatum) in Florida. Biol. Conserv. 2008;141:1758–1764. doi: 10.1016/j.biocon.2008.04.016. [DOI] [Google Scholar]
  • 94.Liu H., Pemberton R. Solitary invasive orchid bee outperforms co-occurring native bees to promote fruit set of an invasive Solanum. Oecologia. 2009;159:515–525. doi: 10.1007/s00442-008-1232-6. [DOI] [PubMed] [Google Scholar]
  • 95.Howarth F. Impacts of alien land arthropods and mollusks on native plants and animals in Hawaii. University of Hawai‘i Press; Honolulu, HI, USA: 1985. [Google Scholar]
  • 96.Kawazoe K., Okabe K., Kawakita A. An alien Sennertia mite (Acari: Chaetodactylidae) associated with an introduced Oriental bamboo-nesting large carpenter bee (Hymenoptera: Apidae: Xylocopa) Entomol. Sci. 2010;13:303–310. doi: 10.1111/j.1479-8298.2010.00396.x. [DOI] [Google Scholar]
  • 97.Goka K., Okabe K., Takano A. Recent cases of invasive alien mites and ticks in Japan: Why is a regulatory framework needed? Exp. Appl. Acarol. 2013;59:245–261. doi: 10.1007/s10493-012-9609-y. [DOI] [PubMed] [Google Scholar]
  • 98.Kremen C., Williams N.M., Aizen M.A., Gemmill-Herren B., LeBuhn G., Minckley R., Packer L., Potts S.G., Roulston T., Steffan-Dewenter I., et al. Pollination and other ecosystem services produced by mobile organisms: A conceptual framework for the effects of land-use change. Ecol. Lett. 2007;10:299–314. doi: 10.1111/j.1461-0248.2007.01018.x. [DOI] [PubMed] [Google Scholar]
  • 99.Winfree R., Williams N.M., Dushoff J., Kremen C. Native bees provide insurance against ongoing honey bee losses. Ecol. Lett. 2007;10:1105–1113. doi: 10.1111/j.1461-0248.2007.01110.x. [DOI] [PubMed] [Google Scholar]
  • 100.Carvalheiro L.G., Veldtman R., Shenkute A.G., Tesfay G.B., Pirk C.W.W., Donaldson J.S., Nicolson S.W. Natural and within-farmland biodiversity enhances crop productivity. Ecol. Lett. 2011;14:251–259. doi: 10.1111/j.1461-0248.2010.01579.x. [DOI] [PubMed] [Google Scholar]
  • 101.Garibaldi L.A., Steffan-Dewenter I., Winfree R., Aizen M.A., Bommarco R., Cunningham S.A., Kremen C., Carvalheiro L.G., Harder L.D., Afik O., et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. 2013;339:1608–1611. doi: 10.1126/science.1230200. [DOI] [PubMed] [Google Scholar]
  • 102.Greenleaf S.S., Kremen C. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl. Acad. Sci. USA. 2006;103:13890–13895. doi: 10.1073/pnas.0600929103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103.Losey J.E., Vaughan M. The Economic Value of Ecological Services Provided by Insects. Bioscience. 2006;56:311. doi: 10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2. [DOI] [Google Scholar]
  • 104.Felicioli A., Bedini G., Soci M., Pinzauti M. Detection of lead in the environment by using the pedotrophic cell of Osmia cornuta (Hymenoptera, Megachilidae) Ann. Della Fac. 2006;59:263–273. [Google Scholar]
  • 105.O’Brien M., Swanson D., Monsma J. Anthidium oblongatum (Apoidea: Megachilidae) confirmed as a Michigan resident, with notes on other Michigan Anthidium species. Gt. Lakes Entomol. 2012;45:102–105. [Google Scholar]
  • 106.Sanguinetti A., Singer R. Invasive bees promote high reproductive success in Andean orchids. Biol. Conserv. 2014;175:10–20. doi: 10.1016/j.biocon.2014.04.011. [DOI] [Google Scholar]
  • 107.Packer L., Zayed A., Grixti J., Ruz L. Conservation genetics of potentially endangered mutualisms: Reduced levels of genetic variation in specialist versus generalist bees. Conserv. Biol. 2005;19:195–202. doi: 10.1111/j.1523-1739.2005.00601.x. [DOI] [Google Scholar]
  • 108.Adamson N., Fell R., Mullins D., Kennedy L. An Assessment of non-Apis Bees as fruit and Vegetable Crop Pollinators. Virginia Polytechnic Institute and State University; Blacksburg, VA, USA: 2011. [Google Scholar]
  • 109.Cane J. Ground-nesting bees: The neglected pollinator resource for agriculture. Acta Hortic. 1997;437:309–324. doi: 10.17660/ActaHortic.1997.437.38. [DOI] [Google Scholar]
  • 110.Cane J. A native ground-nesting bee (Nomia melanderi) sustainably managed to pollinate alfalfa across an intensively agricultural landscape. Apidologie. 2008;39:315–323. doi: 10.1051/apido:2008013. [DOI] [Google Scholar]
  • 111.Payne A., Schildroth D., Starks P. Nest site selection in the European wool-carder bee, Anthidium manicatum, with methods for an emerging model species. Apidologie. 2011;42:181–191. doi: 10.1051/apido/2010050. [DOI] [Google Scholar]
  • 112.Praz C., Müller A., Dorn S. Specialized bees fail to develop on non-host pollen: Do plants chemically protect their pollen. Ecology. 2008;89:795–804. doi: 10.1890/07-0751.1. [DOI] [PubMed] [Google Scholar]
  • 113.Parker F., Torchio P., Nye W. Utilization of additional species and populations of leafcutter bees for alfalfa pollination. J. Apic. Res. 1976;15:89–92. doi: 10.1080/00218839.1976.11099840. [DOI] [Google Scholar]
  • 114.Kearns C.A., Inouye D.W., Waser N.M. Endangered Mutualisms: The Conservation of Plant-Pollinator Interactions. Annu. Rev. Ecol. Syst. 1998;29:83–112. doi: 10.1146/annurev.ecolsys.29.1.83. [DOI] [Google Scholar]
  • 115.Brading P., El-Gabbas A., Zalat S., Gilbert F. Biodiversity economics: the value of pollination services to Egypt. Egypt. J. Biol. 2009;11:46–51. [Google Scholar]
  • 116.Pitts-Singer T., Cane J. The Alfalfa leafcutting bee, Megachile rotundata: The World’s most intensively managed solitary bee. Annu. Rev. Entomol. 2011;56:221–237. doi: 10.1146/annurev-ento-120709-144836. [DOI] [PubMed] [Google Scholar]
  • 117.Stephen W., Osgood C. The induction of emergence in the leaf-cutter bee Megachile rotundata, an important pollinator of alfalfa. J. Econ. Entomol. 1965;58:284–286. doi: 10.1093/jee/58.2.284. [DOI] [Google Scholar]
  • 118.Cane J., Neff J. Predicted fates of ground-nesting bees in soil heated by wildfire: Thermal tolerances of life stages and a survey of nesting depths. Biol. Conserv. 2011;144:2631–2636. doi: 10.1016/j.biocon.2011.07.019. [DOI] [Google Scholar]
  • 119.Pitts-Singer T., Buckner J. Structural Examination of the Dufour’s Gland of the Solitary Bees Osmia lignaria and Megachile rotundata (Hymenoptera: Megachilidae) Ann. Entomol. Soc. Am. 2012;105:103–110. doi: 10.1603/AN11046. [DOI] [Google Scholar]
  • 120.Cane J., Tepedino V. Gauging the effect of honey bee pollen collection on native bee communities. Conserv. Lett. 2016 doi: 10.1111/conl.12263. [DOI] [Google Scholar]
  • 121.Abel C., Wilson R. The use of diverse plant species for increasing Osmia cornifrons (Hymenoptera: Megachilidae) in field cages. J. Kansas Entomol. Soc. 1998;71:23–28. [Google Scholar]
  • 122.West T., McCutcheon T. Evaluating Osmia cornifrons as pollinators of highbush blueberry. Int. J. Fruit Sci. 2009;9:115–125. doi: 10.1080/15538360902991303. [DOI] [Google Scholar]
  • 123.Matsumoto S., Maejima T. Several new aspects of the foraging behavior of Osmia cornifrons in an apple orchard. Psyche A J. Entomol. 2010;53:4633–4641. [Google Scholar]
  • 124.Biddinger D., Joshi N., Rajotte E., Halbrendt N. An immunomarking method to determine the foraging patterns of Osmia cornifrons and resulting fruit set in a cherry orchard. Apidologie. 2013;44:738–749. doi: 10.1007/s13592-013-0221-x. [DOI] [Google Scholar]
  • 125.Wilson R., Abel C. Storage conditions for maintaining Osmia cornifrons (Hymenoptera: Megachilidae) for use in germplasm pollination. J. Kansas Entomol. Soc. 1996;69:270–272. [Google Scholar]
  • 126.Biddinger D., Robertson J., Mullin C., Frazier J. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski) PLoS ONE. 2013;8:e72587. doi: 10.1371/journal.pone.0072587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127.Lee K., Yoon H., Jin B. Osmia cornifrons vitellogenin: cDNA cloning, structural analysis and developmental expression. Entomol. Res. 2015;45:94–101. doi: 10.1111/1748-5967.12098. [DOI] [Google Scholar]
  • 128.Vicens N., Bosch J. Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on “red Delicious” apple. Environ. Entomol. 2000;29:235–240. doi: 10.1603/0046-225X(2000)029[0235:PEOOCA]2.0.CO;2. [DOI] [Google Scholar]
  • 129.Nogué S., Long P., Eycott A., Nascimento L. de Pollination service delivery for European crops: Challenges and opportunities. Ecol. Econ. 2016;128:1–7. doi: 10.1016/j.ecolecon.2016.03.023. [DOI] [Google Scholar]
  • 130.Maccagnani B., Giacomello F., Fanti M., Gobbin D. Apis mellifera and Osmia cornuta as carriers for the secondary spread of Bacillus subtilis on apple flowers. BioControl. 2009;54:123. doi: 10.1007/s10526-008-9163-z. [DOI] [Google Scholar]
  • 131.Lozo J., Berić T., Terzić-Vidojević A. Microbiota associated with pollen, bee bread, larvae and adults of solitary bee Osmia cornuta (Hymenoptera: Megachilidae) Bull. Entomol. Res. 2015;105:470–476. doi: 10.1017/S0007485315000292. [DOI] [PubMed] [Google Scholar]
  • 132.Bond D., Kirby E. Anthophora plumipes (Hymenoptera: Anthophoridae) as a pollinator of broad bean (Vicia faba major) J. Apic. Res. 1999;38:199–203. doi: 10.1080/00218839.1999.11101010. [DOI] [Google Scholar]
  • 133.Silva D., Groom S., Silva C. Potential pollination maintenance by an exotic allodapine bee under climate change scenarios in the Indo-Pacific region. J. Appl. Entomol. 2016 doi: 10.1111/jen.12337. [DOI] [Google Scholar]
  • 134.Ali H., Alqarni A., Shebl M., Engel M. Notes on the nesting biology of the small carpenter bee Ceratina smaragdula (Hymenoptera: Apidae) in northwestern Pakistan. Florida Entomol. 2016;99:89–93. doi: 10.1653/024.099.0116. [DOI] [Google Scholar]
  • 135.Pemberton R., Wheeler G. Orchid bees don’t need orchids: Evidence from the naturalization of an orchid bee in Florida. Ecology. 2006;87:1995–2001. doi: 10.1890/0012-9658(2006)87[1995:OBDNOE]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 136.Minter L.M., Bessin R.T. Evaluation of Native Bees as Pollinators of Cucurbit Crops under Floating Row Covers. Environ. Entomol. 2014;43:1354–1363. doi: 10.1603/EN13076. [DOI] [PubMed] [Google Scholar]
  • 137.Pintor L.M., Byers J.E. Do native predators benefit from non-native prey? Ecol. Lett. 2015;18:1174–1180. doi: 10.1111/ele.12496. [DOI] [PubMed] [Google Scholar]
  • 138.Stubblefield J.W., Seger J., Wenzel J.W., Heisler M.M. Temporal, Spatial, Sex-Ratio and Body-Size Heterogeneity of Prey Species Taken by the Beewolf Philanthus sanbornii (Hymenoptera: Sphecidae). Philos. Trans. R. Soc. Lond. B Biol. Sci. 1993;339:397–423. doi: 10.1098/rstb.1993.0039. [DOI] [PubMed] [Google Scholar]
  • 139.Smith T., Saunders M. Honey bees: The queens of mass media, despite minority rule among insect pollinators. Insect Conserv. Divers. 2016;9:384–390. doi: 10.1111/icad.12178. [DOI] [Google Scholar]
  • 140.Marchetti M.P., Engstrom T. The conservation paradox of endangered and invasive species. Conserv. Biol. 2016;30:434–437. doi: 10.1111/cobi.12642. [DOI] [PubMed] [Google Scholar]
  • 141.Bartlett M., Hale R., Hale M. Habitat quality limits gene flow between populations of Bombus ruderatus in the South Island, New Zealand. Conserv. Genet. 2016;17:703–713. doi: 10.1007/s10592-016-0816-7. [DOI] [Google Scholar]
  • 142.Howlett B., Donovan B., Read R., Hale R. Rearing Bombus subterraneus for re-introduction into Great Britain. Weta. 2009;37:10–12. [Google Scholar]
  • 143.Lye G., Kaden J., Park K., Goulson D. Forage use and niche partitioning by non-native bumblebees in New Zealand: Implications for the conservation of their populations of origin. J. Insect Conserv. 2010;14:607–615. doi: 10.1007/s10841-010-9287-1. [DOI] [Google Scholar]
  • 144.Wehling W., Flanders R. The Risks of International Trade in Bees: Laws and Regulations on the Import, Movement and Release of Bees in the United States. Bee Res. Virus Eur. 2005;6:301–309. [Google Scholar]

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