Non-native Bumblebees Research Articles

Limited introgression from non-native commercial strains and signatures of adaptation in the key pollinator Bombus terrestris.

Insect pollination is fundamental for natural ecosystems and agricultural crops. The bumblebee species Bombus terrestris has become a popular choice for commercial crop pollination worldwide due to its effectiveness and ease of mass rearing. Bumblebee colonies are mass produced for the pollination of more than 20 crops and imported into over 50 countries including countries outside their native ranges, and the risk of invasion by commercial non-native bumblebees is considered an emerging issue for global conservation and biological diversity. Here, we use genome-wide data from seven wild populations close to and far from farms using commercial colonies, as well as commercial populations, to investigate the implications of utilizing commercial bumblebee subspecies in the UK. We find evidence for generally low levels of introgression between commercial and wild bees, with higher admixture proportions in the bees occurring close to farms. We identify genomic regions putatively involved in local and global adaptation, and genes in locally adaptive regions were found to be enriched for functions related to taste receptor activity, oxidoreductase activity, fatty acid and lipid biosynthetic processes. Despite more than 30 years of bumblebee colony importation into the UK, we observe low impact on the genetic integrity of local B. terrestris populations, but we highlight that even limited introgression might negatively affect locally adapted populations.

Cross-mating between the alien bumblebee Bombus terrestris and two native Japanese bumblebees, B. hypocrita sapporensis and B. cryptarum florilegus, in the Nemuro Peninsula, Japan

The rapid naturalization of Bombus terrestris across the Nemuro Peninsula has led to a decline in two closely related native Japanese species, namely Bombus hypocrita sapporensis and Bombus cryptarum florilegus, both belonging to the common subgenus Bombus. Although it is widely believed that cross-mating of native and non-native species is influenced by the common male sex pheromone in this region, no study has been conducted to substantiate this claim. Thus, we investigated the cross-activities of male sex pheromones between native and non-native bumblebees, as well as the frequencies of cross-mating, using chemical and DNA assays. Our gas chromatography–electroantennographic detector analyses and behavioral tests revealed the presence of sex pheromonal cross-activities between B. terrestris and the two Japanese bumblebees species. Furthermore, DNA analyses revealed the occurrence of cross-mating between native and non-native species in the Nemuro Peninsula. Overall, these results indicate the immediate need for conservation measures to safeguard Japanese bumblebee populations in the Nemuro Peninsula.

A keystone mutualism promotes resistance to invasion.

It is not uncommon for one or a few species, and their interactions, to have disproportionate effects on other species in ecological communities. Such keystone interactions might affect how communities respond to the invasion of non-native species by preventing or inhibiting the establishment, spread or impact of non-native species. We explore whether a keystone mutualism among a hummingbird-mistletoe-marsupial promotes ecological resistance to an invasive pollinator, the bumblebee Bombus terrestris, by comparing data collected at sites prior to bumblebee invasion to data collected 11years after the invasion in sites with and without the keystone mutualism. We built pollination networks and focused on network motifs, regarded as building blocks of networks, to identify the central pollinators and estimate the change in their interactions after invasion of B. terrestris. We also estimated the interaction rewiring across the season in post-invasion networks and tested it as a possible mechanism explaining how the keystone mutualism increased ecological resistance to invasion. We found two times more species in post-invasion sites with the keystone mutualism than in post-invasion sites without the keystone mutualism. Moreover, we found that invasive bumblebee reduced the strength and interaction niche of the five central pollinator species while increasing its own strength and interaction niche, suggesting a replacement of interactions. Also, we found that the keystone mutualism promoted resistance to B. terrestris invasion by reducing its negative impacts on central species. In the presence of the keystone mutualism, central species had three times more direct interactions than in sites without this keystone mutualism. The higher interaction rewiring, after invasion of B. terrestris, in sites with the keystone mutualism indicates greater chances of central pollinators to form new interactions and reduces their competence for resources with the non-native bumblebee. Our results demonstrate that a keystone mutualism can enhance community resistance against the impacts of a non-native invasive pollinator by increasing species diversity and promoting interaction rewiring in the community. This study suggests that the conservation of mutualisms, especially those considered keystone, could be essential for long-term preservation of natural communities under current and future impacts of global change.

The Effect of Greenhouse Pollination Methods on Consumers’ Willingness to Pay for Tomatoes in Japan

AbstractSince 2017, the Japanese government has been phasing out the use of non-native bumblebees as greenhouse tomato pollinators due to their ecological risks. We used an online questionnaire to investigate whether pollination methods affect consumers’ willingness to pay (WTP) for tomatoes. We found that consumers valued the use of non-native bumblebees more than hormonal treatment and native more than non-native bees. Moreover, we found that informing consumers of the ecological risks increased WTP for native bumblebees and hormonal treatment. These results suggest that pollination method labeling may help protect ecosystems from the threat of non-native species.

Occurrence of bee viruses and pathogens associated with emerging infectious diseases in native and non-native bumble bees in southern Chile

The invasion of non-native bees to new ecological territories could spread novel pathogens causing emerging infectious diseases (EIDs) in native species. We provide novel information on the prevalence, load, and co-infection network of honey bee viruses, trypanosoma, microsporidia and neogregarinorida pathogens in native Bombus dahlbomii and non-native Bombus terrestris and Bombus ruderatus. Apicystis bombi and Crithidia bombi were highly prevalent (> 78%) in three bumble bee species, with high loads of these pathogens. Nosema bombi was detected only in B. terrestris (37%) and B. ruderatus (15%). Lotmaria passim was detected in low prevalence (< 6%) and low loads in three bumble bee species. Deformed wing virus (genotype A) was detected only in B. terrestris (20%) and B. ruderatus (6%). Black queen cell virus was detected in B. terrestris (34%), B. ruderatus (22%) and B. dahlbomii (23%). Chronic bee paralysis virus, Kashmir bee virus and Acute bee paralysis virus were detected with low prevalence (7%) and titers in the three bumble bee species. The proximity of apiaries and collection sites was not a significant factor in the presence of viruses in bumble bees. The three bumble species were found to be co-infected with Apicystis bombi and C. bombi; a significant positive correlation was found between these two parasites, especially in B. terrestris. Multiple infections with N. bombi, A. bombi, C. bombi and viruses in B. terrestris and B. ruderatus were also detected. This suggests that the invasion and successful establishment of exotic bumble bees in a new area also entails the possible establishment of the pathogens that they carry, which could also be present in native bee species. This finding evidences a potential link between the population decline of B. dahlbomii and the pathogens that were detected with high levels and prevalence.

Molecular detection of the tracheal mite Locustacarus buchneri in native and non-native bumble bees in Chile

Bumble bees (Bombus spp.) are considered one of the most important pollinators of native, non-native, and domesticated plants. Pathogens and parasites, such as the tracheal mite Locustacarus buchneri (Podapolipidae), are harmful to bumble bees. We developed primers based on the mitochondrial CO1 gene for the specific detection of L. buchneri directly from samples of native Bombus dahlbomii and non-native B. terrestris and B. ruderatus. PCR products amplified and sequenced for these primers shared 100 % identity among themselves and around 99–100 % identity with other sequences of L. buchneri reported in Belgium, the Netherlands, and Japan. Bombus terrestris was the most infected species (41 %), followed by B. ruderatus (31 %) and B. dahlbomii (23 %). This is the first report involving L. buchneri in native and non-native bumble bees in Chile. Our described PCR-based detection offers a feasible, specific, and rapid method for the screening of L. buchneri in any bumble bee species.

Parasites and genetic diversity in an invasive bumblebee.

Biological invasions are facilitated by the global transportation of species and climate change. Given that invasions may cause ecological and economic damage and pose a major threat to biodiversity, understanding the mechanisms behind invasion success is essential.Both the release of non-native populations from natural enemies, such as parasites, and the genetic diversity of these populations may play key roles in their invasion success.We investigated the roles of parasite communities, through enemy release and parasite acquisition, and genetic diversity in the invasion success of the non-native bumblebee, Bombus hypnorum, in the United Kingdom.The invasive B. hypnorum had higher parasite prevalence than most, or all native congeners for two high-impact parasites, probably due to higher susceptibility and parasite acquisition. Consequently parasites had a higher impact on B. hypnorum queens’ survival and colony-founding success than on native species. Bombus hypnorum also had lower functional genetic diversity at the sex-determining locus than native species. Higher parasite prevalence and lower genetic diversity have not prevented the rapid invasion of the United Kingdom by B. hypnorum. These data may inform our understanding of similar invasions by commercial bumblebees around the world.This study suggests that concerns about parasite impacts on the small founding populations common to re-introduction and translocation programs may be less important than currently believed.

Rapid ecological replacement of a native bumble bee by invasive species

Despite rising global concerns over the potential impacts of non‐native bumble bee (Bombus spp) introductions on native species, large‐scale and long‐term assessments of the consequences of such introductions are lacking. Bombus ruderatus and Bombus terrestris were sequentially introduced into Chile and later entered Argentina's Patagonian region. A large‐scale survey in Patagonia reveals that, in 5 years post‐arrival, the highly invasive B terrestris has become the most abundant and widespread Bombus species, and its southward spread is concurrent with the geographic retraction of the only native species, Bombus dahlbomii. Furthermore, a 20‐year survey of pollinators of the endemic herb Alstroemeria aurea in northern Patagonia indicates that B ruderatus and B terrestris have replaced B dahlbomii, formerly the most abundant pollinator. Although the decline's underlying mechanisms remain unknown, the potential roles of exploitative competition and pathogen co‐introduction cannot be ruled out. Given that invasive bumble bees can rapidly extirpate native congeners, further introductions should be discouraged.

Impacts of the Use of Nonnative Commercial Bumble Bees for Pollinator Supplementation in Raspberry

Evidence for pollinator declines has led to concern that inadequate pollination services may limit crop yields. The global trade in commercial bumble bee (Bombus spp.) colonies provides pollination services for both glasshouse and open-field crops. For example, in the United Kingdom, commercial colonies of nonnative subspecies of the bumble bee Bombus terrestris L. imported from mainland Europe are widely used for the pollination of raspberries, Rubus idaeus L. The extent to which these commercial colonies supplement the services provided by wild pollinators has not been formally quantified and the impact of commercial bumble bees on native bees visiting the crop is unknown. Here, the impacts of allowing commercially available bumble bee colonies to forage on raspberry canes are assessed in terms of the yield of marketable fruit produced and the pollinator communities found foraging on raspberry flowers. No differences were found in the abundance, diversity, or composition of social bee species observed visiting raspberry flowers when commercial bumble bees were deployed compared with when they were absent. However, weight of marketable raspberries produced increased when commercial bees were present, indicating that wild pollinator services alone are inadequate for attaining maximum yields. The findings of the study suggests that proportional yield increases associated with deployment of commercial colonies may be small, but that nevertheless, investment in commercial colonies for raspberry pollination could produce very significant increases in net profit for the grower. Given potential environmental risks associated with the importation of nonnative bumble bees, the development of alternative solutions to the pollination deficit in raspberry crops in the United Kingdom may be beneficial.

Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.) in Chile

SummaryIn the present work, we update floral associations and geographical distribution for four species of Bombus present in Chile, two native (B. dahlbomii and B. funebris) and two introduced species (B. terrestris and B. ruderatus). We also examine possible associations among native or introduced bees with native or introduced plant species. We found a significant non-random plant association among non-native bumble bee species and non-native plant species. Because of the distributional overlap between B. dahlbomii with the two non-native bee species, it is likely that B. dahlbomii interacts with these non-native bees.

Effects of aposematic coloration on predation risk in bumblebees? A comparison between differently coloured populations, with consideration of the ultraviolet

It has been proposed that sympatric bumblebee species form mimicry rings to profit from learnt avoidance behaviour by predators. This hypothesis can be tested by comparing the predation rates of local bumblebees with those of imported non-native bumblebees, whose coat colour is different from that of local bees, so that their coloration is unfamiliar to local predators. To test whether populations of non-native bumblebees suffer higher worker loss rates during foraging, we conducted transplant experiments in the UK, Germany and Sardinia. The loss rates of foraging workers of four Bombus terrestris populations (Bombus terrestris canariensis, Bombus terrestris terrestris, Bombus terrestris sassaricus and Bombus terrestris dalmatinus) were compared, evaluating data from 989 foragers, whose flight times were monitored precisely (over 8258 h of foraging). While all of these workers display a bright UV-reflecting abdominal tip, the colours in other body parts differ strongly to the eyes of avian predators. The hypothesis that foragers from the non-native bumblebee populations, which differ in coloration from the local native population, would suffer higher predation risk was not upheld. In contrast, in one location (Sardinia) the native population had the highest loss rate. The consistent population rank order we found in terms of forager losses indicates that such losses are more prominently affected by factors other than the familiarity of local predators with aposematic colour patterns.

Forage use and niche partitioning by non-native bumblebees in New Zealand: implications for the conservation of their populations of origin

Bumblebees were introduced into New Zealand from the UK approximately 120 years ago and four species became established. Two of these, Bombus terrestris and B. hortorum, are common in Europe whilst two, B. ruderatus and B. subterraneus, have experienced declines, and the latter is now extinct in the UK. The presence of these species in New Zealand presents an opportunity to study their ecology in a contrasting environment. Forage visits made by bumblebees in New Zealand were recorded across a season. Ninety-six percent of visits were to six non-native forage plants (Cirsium vulgare, Echium vulgare, Hypericum perforatum, Lotus corniculatus, Lupinus polyphyllus and Trifolium pratense). All but L. polyphyllus are European plant species, and three are noxious weeds in New Zealand. Several of these plants have decreased in abundance in the UK, providing a potential explanation for the declines of B. ruderatus and B. subterraneus in Britain. In contrast to studies conducted elsewhere, B. ruderatus, B. terrestris and B. hortorum did not differ in diet breadth and overlap in forage use was high, probably due to the reduced diversity of bumblebee forage plants present in New Zealand. Diel partitioning of forage use between the species was observed, with foraging activity of B. hortorum greatest in the morning and evening, B. ruderatus greatest in the middle of the day and B. terrestris intermediate between the two. These patterns correspond to the climatic preferences of each species as evidenced by their geographic ranges. Implications for bumblebee conservation in the UK are discussed.

Competition for flower resources and nest sites between Bombus terrestris (L.) and Japanese native bumblebees

The non-native bumblebee, Bombus terrestris, has recently become naturalized in Japan and is now dominant in some local communities. Here, we review previous studies reporting the effects of B. terrestris on native bees in both Japan and other countries. We also introduce our work to assess possible competitive exclusion by examining potential niche overlap, resource limitation for bumblebees, and the reproductive capacity of B. terrestris. Previous studies have reported the high niche overlap and some declines of native bees, indicating that competitive exclusion may be occurring. However, there is no indisputable evidence for this invader's ecological impacts on native species through competitive exclusion. Our studies showed that in terms of niche overlap for limited nest sites, two native species, B. hypocrita sapporoensis and B. diversus tersatus, were most likely to be affected through competitive exclusion. Feral colonies of B. terrestris produced a mean of 90.2 gynes and showed high reproductive capacity, which would presumably allow the species to outcompete native bumblebees. Field surveys demonstrated that these two native species have declined accompanied by an increase in B. terrestris. The present study provides strong circumstantial evidence for competitive exclusion of native bumblebees owing to the establishment of B. terrestris.

Impacts of non-native bumblebees in Western Europe and North America

The earliest deliberate introductions of bumblebees to areas outside of their native range occurred over 100 years ago. Transportation of bumblebees accelerated in the late 1980s following the development of techniques for mass rearing them, and their widespread adoption as the preferred pollinator for a range of glasshouse crops, primarily tomatoes. There is now a worldwide trade in one species, Bombus terrestris dalmatinus, originating from south east Europe. Within North America, which does not allow the importation of B. terrestris, the trade is primarily in Bombus impatiens. Trade in B. t. dalmatinus threatens the integrity of other subspecies within Europe, such as B. t. audax which is endemic to Britain and Ireland. However, there is a conspicuous absence of data as to whether B. t. dalmatinus has established in the wild outside its native range, and whether it interbreeds with native subspecies. Perhaps a more significant risk associated with trade in bumblebees is the accidental spread of parasites, and the subsequent risk that native bumblebee species may be exposed to parasites for which they have little resistance. There is circumstantial evidence that catastrophic declines of several North American bumblebee species may have been triggered by the accidental introduction of pathogens from Europe. Even if commercial bumblebee colonies are reared locally, the high densities at which they are kept mean that glasshouse nests are likely to act as reservoirs for spread of disease to wild bumblebee populations nearby. There is clearly the need for tight quarantining of bee colonies before transportation, and a moratorium should be placed on the transport of bumblebees in cases where native species suitable for commercial rearing are readily available.

Bumblebees, humble pollinators or assiduous invaders? A population comparison of foraging performance in Bombus terrestris

Worldwide trade in non-native bumblebees remains largely unrestricted despite well-documented cases where introductions of non-native bees have gone dramatically wrong. Within Europe, indiscriminate importation of non-native populations of bumblebees (Bombus terrestris) for the pollination of glasshouse crops continues on a massive scale. However, no risk assessment has been conducted for these introductions, perhaps because B. terrestris is considered a native species, so shipping populations from one region to another has been implicitly assumed to present no risk. This view is clearly unjustified because Bombus terrestris populations differ significantly in their genetic makeup as demonstrated by strong differences in coat colour and behavioural traits. Therefore, for the first time we compare an important competitive trait, namely foraging performance, between commercially available B. terrestris populations in contrasting environments. We test whether commercially reared populations differ in their nectar foraging performance and whether this is influenced by both their source environment and the one they are introduced into. We do this by means of a reciprocal transplant experiment. Strong, consistent inter-population differences in performance occurred irrespective of test location: Canary Island bees (B. t. canariensis) were superior to Sardinian bees (B. t. sassaricus), which were generally superior to mainland European bees (B. t. terrestris). These inter-population differences in performance were largely explained by inter-population variation in forager size, with larger bees being superior foragers. However, even when body size was accounted for, "native" bees were not superior to transplanted non-native bees in all but one case. We conclude that non-native populations, especially those with large foragers, can be highly competitive foragers. This could lead to their establishment and displacement of native bees. Therefore, we recommend that unregulated movements of non-native B. terrestris populations within Europe should not be carried out without a full risk assessment.

Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical México.

The acclimation, foraging behavior, and pollination efficiency of stingless bees of the species Nannotrigona perilampoides Cresson were evaluated in tomato (Lycopersicon esculentum Mill.) plants cultivated in two greenhouses. The greenhouses were divided into three areas of 16 m2, and one of the following treatments was used for pollination: stingless bees (SB), mechanical vibration (MV), and no pollination (NP). Observations were conducted once a week from 0800 to 1600 hours during 2 mo. The acclimation of the bees to the greenhouses was estimated by the number of bees that did not return to the hive (lost bees) and by comparing the population of the colonies (brood and adults). The foraging activity of the bees across the day was evaluated by comparing the number of foragers per hour. The influence of environmental variables on the foraging activity was also analyzed. The pollination efficiency was compared among treatments through the percentage of fruit set, weight of individual fruit, kilograms of fruit produced per square meter, and the number of seed per fruit. The bees started foraging on the flowers approximately 7 d after the colonies were introduced to the greenhouse. There was a decline in the population of the colonies across the experiment, but colonies did not die out. Correlations of environmental variables with the foraging activity of the bees showed that none of them had a significant influence on pollen foraging. However, water collection was positively correlated with the temperature and negatively correlated with the humidity inside the greenhouse. The estimation of the pollination efficiency per treatment showed that there were significant differences in fruit set in SB (83 +/- 4.2) and MV (78.5 +/- 6.4) compared with NP (52.6 +/- 7.6). However, the average weight of the fruit was similar for the three treatments (65 g). There were significant differences for seed number in SB (200 +/- 15.3) and MV (232 +/- 21.4) compared with NP (120 +/- 16.6). The productivity in kilograms of fruit per square meter was higher in SB (5.72 +/- 0.61) and MV (5.66 +/- 0.58 kg) compared with NP (3.34 +/- 0.72). The number of seed was positively correlated with the weight of the fruit. We conclude that the use of Nannotrigona testaceicornis Rondani, for pollinating greenhouse tomatoes in tropical climates, could be an alternative to the use of highly defensive African-derived Apis mellifera or non-native bumble bees (Bombus spp.). However, more research is needed to evaluate the cost/benefit on large-scale greenhouse pollination using N. perilampoides Cresson against other bee species and pollination methods.