Comparative nectar-foraging behaviors and efficiencies of an alien and a native bumble bee

Resource preemption by alien organisms can contribute to their invasion success and the demise of functionally equivalent native species, particularly when opportunistic foraging by aliens results in more efficient exploitation. In forests of NW Patagonia, the only native bumble bee and major pollinator, Bombus dahlbomii, declined almost to extinction as the alien B. ruderatus increased in abundance since its first appearance about 17 years ago. To explore whether resource competition might have driven this displacement we studied the behavior and foraging efficiency of both bumble bees while they harvested nectar from flowers of Alstroemeria aurea, the main summer food resource in the forests of NW Patagonia. We compared the nectar content of flowers that bees selected, recently visited, and rejected with that of randomly-chosen neighboring flowers and assessed differences in visitation rates. The native bumble bee selects flowers with abundant nectar and mostly exploits nectar-rich flower patches by rejecting a higher proportion of flowers with little or no nectar. On the other hand, the alien bumble bee discriminated less with respect to sugar content per visited flower, but visited more flowers per minute. Workers of the native bumble bee harvested ~70% more sugar per unit of time than those of the alien species in absolute terms, and a similar amount when sugar harvested was expressed as a percentage of body mass. In contrast to expectation, the opportunistic foraging of the alien bumblebee was not more efficient and therefore cannot explain the ecological extinction of the native species through exploitative competition. These findings suggest that the displacement of the native species by the alien may be driven by other factors, such as the associated introduction of novel diseases or parasites.     

Pollination niche overlap between a parasitic plant and its host

Niche theory predicts that species which share resources should evolve strategies to minimise competition for those resources, or the less competitive species would be extirpated. Some plant species are constrained to co-occur, for example parasitic plants and their hosts, and may overlap in their pollination niche if they flower at the same time and attract the same pollinators. Using field observations and experiments between 1996 and 2006, we tested a series of hypotheses regarding pollination niche overlap between a specialist parasitic plant Orobanche elatior (Orobanchaceae) and its host Centaurea scabiosa (Asteraceae). These species flower more or less at the same time, with some year-to-year variation. The host is pollinated by a diverse range of insects, which vary in their effectiveness, whilst the parasite is pollinated by a single species of bumblebee, Bombus pascuorum, which is also an effective pollinator of the host plant. The two species therefore have partially overlapping pollination niches. These niches are not finely subdivided by differential pollen placement, or by diurnal segregation of the niches. We therefore found no evidence of character displacement within the pollination niches of these species, possibly because pollinators are not a limiting resource for these plants. Direct observation of pollinator movements, coupled with experimental manipulations of host plant inflorescence density, showed that Bombus pascuorum only rarely moves between inflorescences of the host and the parasite and therefore the presence of one plant is unlikely to be facilitating pollination in the other. This is the first detailed examination of pollination niche overlap in a plant parasite system and we suggest avenues for future research in relation to pollination and other shared interactions between parasitic plants and their hosts.     

Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set

The fecundity of insect-pollinated plants may not be linearly related to the number of flowers produced, since floral display will influence pollinator foraging patterns. We may expect more visits to plants with more flowers, but do these large plants receive more or fewer visits per flower than small plants? Do all pollinator species respond in the same way? We would also expect foragers to move less between plants when the number of flowers per plant are large, which may reduce cross-pollination compared to plants with few flowers. We examine the relationships between numbers of inflorescence per plant, bumblebee foraging behaviour and seed set in comfrey, Symphytum officinale, a self-incompatible perennial herb. Bumblebee species differed in their response to the size of floral display. More individuals of Bombus pratorum and the nectar-robbing B.?terrestris were attracted to plants with larger floral displays, but B. pascuorum exhibited no increase in recruitment according to display size. Once attracted, all bee species visited more inflorescences per plant on plants with more inflorescences. Overall the visitation rate per inflorescence and seed set per flower was independent of the number of inflorescences per plant. Variation in seed set was not explained by the numbers of bumblebees attracted or by the number of inflorescences they visited for any bee species. However, the mean seed set per flower (1.18) was far below the maximum possible (4 per flower). We suggest that in this system seed set is not limited by pollination but by other factors, possibly nutritional resources.     

The cobblers stick to their lasts: pollinators prefer native over alien plant species in a multi-species experiment

The majority of plant species rely, at least partly, on animals for pollination. Our knowledge on whether pollinator visitation differs between native and alien plant species, and between invasive and non-invasive alien species is still limited. Additionally, because numerous invasive plant species are escapees from horticulture, the transition from human-assisted occurrence in urbanized habitats to unassisted persistence and spread in (semi-)natural habitats requires study. To address whether pollinator visitation differs between native, invasive alien and non-invasive alien species, we did pollinator observations for a total of 17 plant species representing five plant families. To test whether pollinator visitation to the three groups of species during the initial stage of invasion depends on habitat type, we did the study in three urbanized habitats and three semi-natural grasslands, using single potted plants. Native plants had more but smaller flower units than alien plants, and invasive alien plants had more but smaller flowers than non-invasive alien plants. After accounting for these differences in floral display, pollinator visitation was higher for native than for alien plant species, but did not differ between invasive and non-invasive alien plant species. Pollinator visitation was on average higher in semi-natural than in urbanized habitats, irrespective of origin or status of the plant species. This might suggest that once an alien species has managed to escape from urbanized into more natural habitats, pollinator limitation will not be a major barrier to establishment and invasion.     

A method for quantifying the gene flow that results from a single bumblebee visit using transgenic oilseed rape,Brassica napus L. cv. Westar

Genetically modified plants containing selectable markers offer a unique opportunity for pollination biologists to investigate some of the major, but intractable questions about paternity distributions and their causes. Here, a method is reported that uses transgenic plants to enable the quantification of the outcrossed fertilizations that result from a single pollinator visit. Gene flow mediated by worker bumblebees (Bombus terrestris) was studied among plants of oilseed rape (Brassica napus L. cv. Westar) where transgenic paternity in seeds of a non-transgenic plant was manifested as herbicide resistance. Overall, 91% of the resistant seeds resulted from the first four flowers that were visited after the bumblebee left the transgenic plant, and none was found beyond the 14th successively visited flower. The possibilities for developing the method to address various questions in pollination biology are discussed.     

Pollinator Shift and Reproductive Performance of the Qinghai–Tibetan Plateau Endemic and Endangered Swertia przewalskii (Gentianaceae)

Reproductive failure results in many plant species becoming endangered. However, little is known of how and to what extent pollinator shifts affect reproductive performance of endangered species as a result of the artificial introduction of alien insects. In this study we examined breeding systems, visitor species, visiting frequency and seed set coefficients of Swertia przewalskii in two years that had different dominant pollinator species (native vs. alien). Flowers of this species were protandrous and herkogamous and insects were needed for the production of seeds. The stigmatic receptivity of this species was shorter than for other gentians. No significant difference in seed set coefficient was found for hand-pollinated plants between the two years, indicating that pollinator shift only had a minor effect on this plant’s breeding system. The commonest pollinators in 2002 were native bumblebees, alien honeybees and occasional solitary bees, however, only alien honeybees were observed in 2004. The flower visitation rate in both years was relatively high, although the total visit frequency decreased significantly in 2004. The control flowers without any treatment produced significantly fewer seed sets in 2004 than in 2002. In the past decade the seed production of this species may have partly decreased due to pollination by alien honeybees, however, we suggest that they might have acted as alternative pollinators ensuring seed production of S. przewalskii when native pollinators were unavailable. The main reason that this plant is endangered is probably the result of habitat destruction, but changes in land use, namely intensified agricultural practice and unfavorable animal husbandry have also contributed to its decline. We recommend that in-situ conservation, including the establishment of a protected area, is the best way to preserve this species effectively.     

The Value of Uncropped Field Margins For Foraging Bumblebees

The intensification of agriculture has led to declines in species diversity and abundance within groups of certain flora and fauna. Bumblebees (Bombus spp.) are one group where a decline has been documented, and it is thought to be attributable to a decrease in forage resources and potential nest sites. As bumblebees play an important role in the pollination of many entomophilous crops, this decline could impact on agricultural productivity. We examined the role of naturally regenerated field margins in providing forage plants on land where nectar resources are otherwise impoverished. The following question was addressed – Are naturally regenerated unsprayed field margins more attractive to foraging bumblebees and honeybees than cropped field margins managed as conservation headlands? Significantly more bees visited naturally regenerated field margins than cropped field margins. Honeybees (Apis mellifera), Bombus terrestris, and Bombus lapidarius were the most commonly observed bee species. Different wildflower species within the naturally regenerated margins varied greatly in relative number of visits received, and bumblebee species were found to prefer different flower species to honeybees. The potential role that naturally regenerated field margins could play in the conservation of bumblebee species, and the implications for other species of flora and fauna, are discussed.     

Worldwide migration of parasitic mites as a result of bumblebee commercialization

We investigated the status of infestation by a tracheal mite, Locustacarus buchneri, in natural populations of a Japanese native bumblebee species, Bombus hypocrita, collected on Hokkaido Island and in the Aomori prefecture between 1997 and 2001. We also investigated mite infestation in commercial colonies of the European bumblebee, Bombus terrestris, imported from the Netherlands and Belgium, and the Japanese native species, B. ignitus, imported from the Netherlands, between 1997 and 2001. We detected mites in natural populations of the two B. hypocrita subspecies and in the commercial colonies. Analysis of variations in 535 bp sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene showed that the mite haplotypes in the native populations and in the imported colonies did not overlap in 1997–1999, but in 2000–2001 some mites possessing European CO1 haplotypes were detected in the natural populations of Japanese native bumblebees. In addition, many mites possessing Japanese haplotypes were detected in the imported commercial colonies from Europe. Considering the fact that the Japanese native bumblebees, B. hypocrita, were once exported to Europe for commercialization, these results suggest that bumblebee commercialization has caused overseas migration and cross-infestation of parasitic mites among natural and commercial colonies. However, because the Japanese and European CO1 haplotypes were closely related, there was a possibility that the European haplotypes found in the mites in the Hokkaido Island revealed native variation. To clarify the status of mite invasion, further detailed analysis of genetic variation of the mite, using other genetic markers on additional samples, need to be performed.     

Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by ‘robotic’ crab spiders. As bees learnt to avoid ‘dangerous’ flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.     

Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees

Pollination success of plants is highly susceptible to the frequency of visits and foraging behavior of pollinators. Pollination of the nectarless flowers of Pedicularis species depends on bumblebee workers collecting pollen by vibrating the anthers (buzz pollination). However, little is known about the efficiency of the pollination system. Foraging behavior, pollen removal from anthers and pollen deposition on stigmas of P. chamissonis were studied to assess the effectiveness of buzz pollination in an alpine snowbed population of northern Japan. Although bumblebees tended to visit most of the flowers open at a given time within inflorescences during a single visit, pollen removal rate at the first visit was about 20%, and buzzing period decreased with increasing number of previous visits, resulting in a decreasing proportion of pollen removed per visit as the number of visits increased. These trends enable plants to provide pollen for more pollinators. The number of pollen grains deposited on stigmas was not saturated during the first visit and increased with additional visits. Irrespective of weak self-compatibility, evidence of interference between self and outcross pollen was lacking for seed production. Therefore, buzz pollination in P. chamissonis acts as a mechanism that improves the chance of cross-pollination upon multiple visits if pollinator visitation is frequent.     

Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania?

Honeybees, Apis mellifera, have been introduced by man throughout the globe. More recently, other bee species including various bumblebees (Bombus spp.) have been introduced to several new regions. Here we examine the impacts of honeybees and the bumblebee, Bombus terrestris, on native flower-visiting insects in Tasmania. To assess whether native insects have lower abundance or are excluded in areas that have been colonised by exotic bees, we quantified the abundance, diversity and floral preferences of flower-visiting insects at sites where bumblebees and honeybees were present, and compared them to sites where they were absent. This was achieved by hand searches at 67 sites, and by deploying sticky traps at 122 sites. Honeybees were by far the most abundant bee species overall, and dominated the bee fauna at most sites. There was considerable niche overlap between honeybees, bumblebees and native bees in terms of the flowers that they visited. Sites where bumblebees were established had similar species richness, diversity and abundance of native flower-visiting insects compared to sites where bumblebees were absent. In contrast, native bees were more than three times more abundant at the few sites where honeybees were absent, compared to those where they were present. Our results are suggestive of competition between honeybees and native bees, but exclusion experiments are needed to provide a definitive test.     

Worldwide Alien Invasion: A Methodological Approach to Forecast the Potential Spread of a Highly Invasive Pollinator

The ecological impacts of alien species invasion are a major threat to global biodiversity. The increasing number of invasion events by alien species and the high cost and difficulty of eradicating invasive species once established require the development of new methods and tools for predicting the most susceptible areas to invasion. Invasive pollinators pose serious threats to biodiversity and human activity due to their close relationship with many plants (including crop species) and high potential competitiveness for resources with native pollinators. Although at an early stage of expansion, the bumblebee species Bombus terrestris is becoming a representative case of pollinator invasion at a global scale, particularly given its high velocity of invasive spread and the increasing number of reports of its impacts on native bees and crops in many countries. We present here a methodological framework of habitat suitability modeling that integrates new approaches for detecting habitats that are susceptible to Bombus terrestris invasion at a global scale. Our approach did not include reported invaded locations in the modeling procedure; instead, those locations were used exclusively to evaluate the accuracy of the models in predicting suitability over regions already invaded. Moreover, a new and more intuitive approach was developed to select the models and evaluate different algorithms based on their performance and predictive convergence. Finally, we present a comprehensive global map of susceptibility to Bombus terrestris invasion that highlights priority areas for monitoring.     

Comparative efficiency of Nannotrigona perilampoides, Bombus impatiens (Hymenoptera: Apoidea), and mechanical vibration on fruit production of enclosed habanero pepper

The native bee Nannotrigona perilampoides Cresson (Apidae: Meliponini) has been evaluated with promising results in greenhouse pollination of Solanaceae in Mexico. However, no comparison has been done with imported bumble bees (Apidae: Bombini), which are the most common bees used for greenhouse pollination. We compared the foraging activity and fruit production of habanero pepper. Capsicum chinense Jacquin, by using N. perilampoides and Bombus impatiens Cresson in pollination cages. Both bee species collected pollen on a similar number of flowers per unit time, but N. perilampoides visited significantly more flowers per trip, lasted longer on each flower, and spent more time per foraging trip. Ambient temperature and light intensity significantly affected the foraging activity of N. perilampoides. Light intensity was the only environmental variable that affected B. impatiens. Except for the fruit set, there were not significant differences in the quality of fruit produced by both bee species; however, N. perilampoides and B. impatiens performed better than mechanical vibration for all the variables measured. The abortion of fruit caused the low fruit set produced by B. impatiens, and we speculate it might be due to an excessive visitation rate. Pollination efficiency per visit (Spear's pollination efficiency index) was similar for both bee species in spite of the significantly lower amount of pollen removed by N. perilampoides. We suggested that the highest number of flowers visited per foraging trip coupled with adequate amounts of pollen transported, and transferred between flowers, could explain the performance of N. perilampoides as a good pollinator of habanero pepper. Our experiments confirm that N. perilampoides could be used as an alternative pollinator to Bombus in hot pepper under tropical climates.     

Foraging interactions between native and exotic bumblebees: enclosure experiments using native flowering plants

To assess the impact of Bombus terrestris invasion on the foraging efficiency of native Japanese bumblebees, consumption and acquisition of floral resources during foraging on flowers of native Japanese plant species were investigated using enclosures with three treatments: one with only B. terrestris (exotic), one with both B. terrestris and native Japanese bumblebee species (mixed), and one with only Japanese species (native), but with the bumblebee density held constant. Changes in the body mass of queens and the nest mass of colonies for two days did not significantly differ among four combinations of the species and treatment, B. terrestris in the exotic and mixed treatments and Japanese species in the mixed and native treatments. Thus, it is not clear that B. terrestris has higher foraging efficiency than native species and that B. terrestris individuals more negatively affect the foraging efficiency of native species than individuals of the native species themselves. The nectar standing crop of Cirsium kamtschaticum was smaller in the exotic treatment than in the mixed and native treatments. However, this may have been an artifact of differences in the numbers of flowers in the various treatments. T. Nagamitsu and T. Kenta contributed equally to this work     

Does Invasion of Exotic Plants Promote Invasion of Exotic Flower Visitors? A Case Study from the Temperate Forests of the Southern Andes

Habitat disturbance, particularly of human origin, promotes the invasion of exotic plants, which in turn might foster the invasion of alien-interacting animals. Here we assess whether the invasion of exotic plants – mostly mediated by habitat disturbance – facilitates the invasion of exotic flower visitors in temperate forests of the southern Andes, Argentina. We recorded visit frequencies and the identity of visitors to the flowers of 15 native and 15 exotic plant species occurring in different highly disturbed and less disturbed habitats. We identified three alien flower visitors, the hymenopterans Apis mellifera, Bombus ruderatus, and Vespula germanica. We found significantly more visitation by exotic insects in disturbed habitats. This pattern was explained, at least in part, by the association between alien flower visitors and flowers of exotic plants, which occurred more frequently in disturbed habitats. However, this general pattern masked different responses between the two main alien flower visitors. Apis mellifera exploited almost exclusively the flowers of a subset of herbaceous exotic plants that thrive under disturbance, whereas B. ruderatus visited equally flowers of both exotic and native plants in both disturbed and undisturbed habitats. We did not find any strong evidence that flowers of exotic plants were more generalist than those of native plants, or that exotic flower visitors were more generalist than their native counterparts. Our results suggest that alien plant species could facilitate the invasion of at least some exotic flower visitors to disturbed habitats. Because flowering plants as well as flower visitors benefit from this mutualism, this association may enhance, through a positive feedback, successful establishment of both exotic partners.     

Abundance,body size,and morphology of bumblebees in an area where an exotic species, <Emphasis Type="Italic">Bombus terrestris</Emphasis>, has colonized in Japan

An exotic bumblebee species, Bombus terrestris, has colonized in Japan and becomes dominant in some local communities. We examined the effects of land use and bumblebee abundance on the number and body size of bumblebees collected using window traps in a lowland area in the southern Ishikari district, Hokkaido. In 2004, we collected 922 bumblebees of six species using 70 traps at 17 sites. A statistical model fitted to the data demonstrated that dispersion from commercial B. terrestris colonies used in greenhouses positively affected the number of B. terrestris caught by each trap. This exotic species was abundant in sites where paddy fields were prevalent, but three native species, B. hypocrita, B. ardens, and B. diversus, were abundant in sites where farms and woodlands were widespread. The local abundance of B. terrestris was not associated negatively with the number and body size of native bumblebees. Thus, we did not find any competitive interactions between exotic and native bumblebees although habitat conditions seem to be common determinants of the bumblebee populations. A morphological analysis showed that B. terrestris had intermediate tongue length between B. hypocrita and B. ardens.     

Bumblebee-pollination and temporal change of the calyx tube length in Clematis stans(Ranunculaceae)

Clematis stans is dioecious semi-arboreal, with pale purple–blue, nodding, tubulous flowers in a paniculate inflorescence. Both male and female flowers produce nectar from the base of the calyx tube during a flowering period of 3 or 4 days, and are pollinated by two bumblebee species, Bombus diversus and B. honshuensis, with different proboscis lengths. When the flowers open, four sepals constructing a calyx tube separate at the top and their respective tips gradually curl up, so that a tubular part shortens. Observations at two field sites showed that B. diversus (with a longer proboscis) most often visits the flowers with a longer calyx tube, and B. honshuensis (with a shorter proboscis) the flowers with a shorter calyx tube, i.e., later in the flowering period. By changing the calyx tube length, the flowers of C. stans accept the two bumblebee species with different proboscis length as pollinators and thus increase the chance of pollination for each flower. It was also found that the two bumblebee species prefer the male flowers to the female flowers, although the female flowers secrete more nectar as a reward than male flowers. This is likely because they visit the male flowers to collect pollen grains in addition to nectar. Electronic Publication     

Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on <Emphasis Type="Italic">Bombus affinis</Emphasis> Cresson

Bumblebees (Bombus spp.) have been declining rapidly in many temperate regions of the Old World. Despite their ecological and economic importance as pollinators, North American bumblebees have not been extensively surveyed and their conservation status is largely unknown. In this study, two approaches were used to determine whether bumblebees in that region were in decline spatially and temporally. First, surveys performed in 2004–2006 in southern Ontario were compared to surveys from 1971 to 1973 in the same sites to look at changes in community composition, in one of the most bumblebee diverse areas of eastern North America. Second, the extent of range decline for a focal species (Bombus affinis Cresson) was estimated by surveying 43 sites throughout its known native range in eastern Canada and the United States. Our study documents an impoverishment of the bumblebee community in southern Ontario over the past 35 years. Bombus affinis in particular was found to have declined drastically in abundance not only in southern Ontario but throughout its native range. The loss of any bumblebee species may result in cascading impacts on native fauna and flora and reduce agricultural production. Implications for the conservation of this important group of pollinators are discussed.     

Increased tomato yield through pollination by native Australian Amegilla chlorocyanea (Hymenoptera: Anthophoridae)

Amegilla spp. (Hymenoptera: Anthophoridae) have been suggested as potential native Australian alternative to overseas used bumblebees (Bombus spp.) for pollination of tomato in greenhouses. In this study, we investigate the effectiveness of Amegilla chlorocyanea Cockerell as a greenhouse pollinator of tomato, Lycopersicon esculentum Mill. We show that (1) a single buzz by a female increases tomato weight by 11% compared with pollination by using an industrial pollination wand, (2) multiple buzzes increase tomato weight compared with a single buzz, and (3) unlimited flower visits lead to an increase in fruit weight of 21% compared with wand pollination. These results are comparable with those achieved by bumblebee pollination and demonstrate that A. chlorocyanea is a valid alternative to bumblebees for greenhouse tomato pollination in Australia.     

Successful pollination of the Neotropical crop Solanum quitoense by Bombus terrestris: behaviour,efficiency and yield

The South American lulo (Solanum quitoense Lam.) is a crop plant of the Andes of Ecuador and Colombia, pollinated by South American bumblebees, such as, Bombus atratus Franklin. The cultivation of lulo outside of its native range, for example in European glasshouses, requires the presence of efficient pollinators to enable high fruit set and yield. Until now, the suitability of Bombus terrestris L., native to Europe and commonly used in agriculture, has been untested for this purpose. In this study, the pollen‐collecting behaviour of B. terrestris when visiting lulo flowers was investigated. It was shown that B. terrestris adopted the lulo as a pollen source, and on average visited three flowers per minute, had five buzzing events per stay and foraged for 15 s on a single flower, independently of the previous number of visits and level of bruising to the anthers. The pollination efficiency of five different treatments was evaluated: (i) exclusion of bees, (ii) single and (iii) multiple visits of B. terrestris, (iv) self‐ and (v) cross‐pollination by hand. The results clearly demonstrated that, for fruit set, pollination is crucial. It was also found that lulo flowers can be successfully self‐pollinated, but give 25% fewer fruit set compared with pollination via multiple bumblebee visits, or cross‐pollination by hand. Fruit set, seed set and fruit size were as high with pollination by B. terrestris as with cross‐pollination by hand, indicating that this bumblebee is an appropriate pollinator for lulo. However, B. terrestris was conspicuously less effective when a flower was visited only once. Therefore, when growing lulos commercially, multiple bumblebee visits should be encouraged, but it is likely that the behaviour of B. terrestris would ensure this anyway. Our results indicate that B. terrestris is a suitable and efficient pollinator for the production of lulo fruits.