The Plight of the Bumblebee

Major pollinators apart from the honeybee are suffering steep decline worldwide, chief among them the bumblebee, and neonicotinoid pesticides are a major culprit that should be banned. Prof. Joe Cummins

There has been a  huge amount written about the  decline of the honeybee,  Apis mellifera , but relatively scant attention has been paid  to other important pollinators that have also been affected simultaneously, in particular,  the bumblebee, Bombus terrestris, which has been experiencing a precipitous global decline. The bumble bee, an important pollinator, has received much less attention than the honeybee because the bumblebee does not produce   marketable quantities of honey.

Is the bumblebee doomed?

As early as six years ago, there was clear evidence that the bumblebee was in deep trouble in North America.  A survey of bumblebee species reached the following conclusion [1]: “The bumblebee subgenus Bombus is represented by five species in North America. Of these, one, B. franklini, may be extinct, and two others, the western B. occidentalis and the eastern B. affinis, appear to be in steep decline. For all of these species, habitat loss and degradation and extensive pesticide use are threats faced daily. However, circumstantial evidence indicates that the principal cause for these population declines is the introduction of exotic disease organisms and pathogens via trafficking in commercial bumblebee queens and colonies for greenhouse pollination of tomatoes.”

In 2009 the decline in Midwestern North American bumblebee was documented and large scale agricultural intensification implicated as the cause [2]. A 2010 report showed that the relative abundances of four species have declined by up to 96 percent and that their geographic ranges contracted by 23–87 percent within the last 20 years [3]. It also showed that declining populations have significantly higher infection levels of the microsporidian pathogen Nosema bombi and lower genetic diversity compared with co-occurring populations of the stable (non-declining) species. It concluded [3]: “Higher pathogen prevalence and reduced genetic diversity are, thus, realistic predictors of these alarming patterns of decline in North America, although cause and effect remain uncertain.”

A number of causes have been put forward for the decline of the bumble bee, these include intensification of land use, introduction of pathogen-bearing bees, pathogens from honey bees, inbreeding, and exposure to pesticides.  Before discussing those causes, I describe the lifestyle of the bumblebee.

Lifestyle of the bumble bee

The bumblebee may look like a large economy-sized honeybee, but it has a distinctly different lifestyle [4]. Most species live in small colonies, usually underground, often in an old mouse hole. The queen lays her eggs in a hollow nest of moss or grass at the beginning of the season. The larvae are fed on pollen and honey, and develop into workers. All the bees die at the end of the season except fertilized females, which hibernate and produce fresh colonies in the spring. Bumblebees form colonies. These colonies are usually much less extensive than those of honeybees. This is due to a number of factors including: the small physical size of the nest cavity, a single female is responsible for the initial construction and reproduction that happens within the nest; and the restriction of the colony to a single season (in most species). Often, mature bumblebee nests will hold fewer than 50 individuals. Bumblebee nests may be found within tunnels in the ground made by other animals, or in tussock grass. Bumblebees sometimes construct a wax canopy (“involucrum”) over the top of their nest for protection and insulation. Bumblebees do not often preserve their nests through the winter, though some tropical species live in their nests for several years (and their colonies can grow quite large, depending on the size of the nest cavity). In temperate species, the last generation of summer includes a number of queens that overwinter separately in protected spots.

The queens can live up to one year, possibly longer in tropical species. Bumblebee nests are first constructed by over-wintered queens in the spring (in temperate areas). Upon emerging from hibernation, the queen collects pollen and nectar from flowers and searches for a suitable nest site. The characteristics of the nest site vary among bumblebee species, with some species preferring to nest in underground holes and others in tussock grass or directly on the ground. Once the queen has found a site, she prepares wax pots to store food, and wax cells into which eggs are laid. These eggs then hatch into larvae, which cause the wax cells to expand isometrically into a clump of brood cells.

After the first or second group of workers emerge, they take over the task of foraging and the queen spends most of her time laying eggs and caring for larvae. The colony grows progressively larger and at some point will begin to produce males and new queens. The point at which this occurs varies among species and is heavily dependent on resource availability and other environmental factors. Unlike the workers of more advanced social insects, bumblebee workers are not reproductively sterile and are able to lay haploid eggs (with one set of chromosomes) that develop into viable male bumble bees. Only fertilized queens can lay diploid eggs (with two sets of chromosomes) that mature into workers and new queens. New queens and males leave the colony after maturation. Males in particular are forcibly driven out by the workers. Away from the colony, the new queens and males live off nectar and pollen and spend the night on flowers or in holes. The queens are eventually mated, often more than once, and search for suitable location for diapause (dormancy).

Bumblebees generally visit flowers that form recognizable groups according to pollinator type. They can visit patches of flowers up to 1–2 kilometers from their colony. Bumblebees will also tend to visit the same patches of flowers every day, as long as nectar and pollen continue to be available, a habit known as pollinator or flower constancy. While foraging, bumblebees can reach ground speeds of up to 15 metres per second (54 km/h). Once they have collected nectar and pollen, they return to the nest and deposit the harvested nectar and pollen into brood cells, or into wax cells for storage. Unlike honey bees, bumblebees only store a few days’ worth of food and so are much more vulnerable to food shortage.

Land use

The decline of bumblebee worldwide was brought to light when the impact of particular land use practices was deemed to require fuller study to pinpoint those practices that would benefit the survival of the bumblebee [5].  Organic farming practices increased bumblebee species richness over conventional farming practices [6]. Agricultural landscapes with organic crops support bumblebee density by 150 percent over conventional farming [7].  Pollinator species such as the bumble bee that nest below ground were found to be more adversely effected by tillage than pollinators that nest above ground [8]. It was clear that organic farming practices generally support survival of the bumble bee.

Pesticides

The levels of insecticides that kill bees outright may be much higher than the levels interfering with foraging ability of the bees. Neonicotinoid insecticides are used throughout the world; there is clear laboratory evidence that the neonicotinoid insecticides imidacloprid, thiamethoxam and thiacloprid interfered with reproduction and foraging of the bumblebee [9]. Insecticides used to control pests on canola crops were found toxic to the bumblebee, these include imidacloprid, clothianidin, deltamethryn, spinosad and novaluron [10]. Lower bumblebee species richness was found in the more intensively farmed basin with higher pesticide loads [11]. The naturally derived insecticide spinosad was also found to interfere with bumble bee foraging when applied at sub-lethal doses [12].  Bacillus thuringiensis aizawai (Xentari) proved lethal to the bumblebee when applied in water. In contrast, Bt kurstaki (Dipel) was not toxic to the bumblebee. It seems clear that agricultural insecticides are a threat to the bumblebee [13], and they should be regulated to prevent bee decline.

There is now good evidence that sublethal levels of pesticides weaken the immune system of the honeybee, leaving them much more susceptible to disease agents such as the parasites Nosema [14]  (see also [15] Ban Neonicotinoid Pesticides to Save the Honeybee, SiS 49). It is likely that the bumble bee exposed to sub lethal levels of neonicotinoid insecticides may also be more sensitive to infection, as well as suffer from behavioural impairment, but the relevant research has not been done. Parasites and pathogens can spread rapidly between colonies and also between the honeybee and the bumblebee.

Viruses

RNA viruses contribute to colony collapse, and also expand the viral host range, which could lead to a deeper impact on the health of the ecosystem. Analyses showed that these viruses are disseminating freely among the pollinators via the flower pollen itself. Notably, in cases where honeybee apiaries affected by CCD harboured honeybees with Israeli Acute Paralysis virus (IAPV), nearby non-Apis hymenopteran pollinators also had IAPV, while those near apiaries without IAPV did not. In containment greenhouse experiments, IAPV moved from infected honeybees to bumblebees and from infected bumblebees to honeybees within a week, demonstrating that the viruses could be transmitted from one species to another. This study adds to our present understanding of virus epidemiology and may help explain bee disease patterns and pollinator population decline in general [16].

The deformed wing virus of honeybee was observed in bumblebees where they pose as serious threat [17]. Honeybee workers can be recruited (by bumble bees) for the establishment of bumblebee nests. Nest establishment rates  in three western bumble bee species can be increased dramatically by the addition of either honey bee workers or workers from  a second related bumble bee species   at colony initiation [18].  The co-mingling of honey and bumble bees  in nest establishment shows how viruses may be  spread  by direct contact between bee genera as distantly related as , for example , pigs and people.

Parasites

Foraging bees discriminate rewarding from non-rewarding flowers on the basis of colour and odour. Natural and experimental infection by a protozoan parasite (Crithidia bombi, which lives exclusively within the gut tract), impaired the ability of foragers to learn the colour of rewarding flowers. Parasitic infection can thus disrupt central nervous system pathways that mediate cognitive processes in bumblebees and as a consequence, can reduce their ability to monitor floral resources and make economic foraging decisions. This infection-induced change to cognitive function in bumblebees suggests communication between the immune and nervous systems [19].

Automated video-tracking was used to quantify networks of physical contact among individuals within colonies of the social bumblebee Bombus impatiens. Network structure was found to determine pathogen transmission in naturally and artificially infected hives with Crithidia bombi in social insect colonies [20]. The fungal pathogen Nosema bombi was found to be transmitted horizontally among bumblebee adults, but the transmission was relatively low for the strains of pathogen studied [21]. Commercially-reared bumblebees, used extensively to pollinate greenhouse crops may allow escape of bees from the greenhouse (spill over). Spill over has allowed the gut parasite Crithidia bombi to invade several wild bumblebee species near greenhouses. Given the available evidence, it is likely that pathogen spill over from commercial bees is contributing to the decline of wild Bombus in North America [22].

Inbreeding depression and immunity

The small relatively isolated colonies of the bumblebee are subject to inbreeding as the population declines. When the queen mates with her brothers, the offspring may be subject to inbreeding depression (decrease in fitness and vigour). Such impact is observed in both animals and plants. One study showed that inbred offspring of the bumblebee were smaller but not highly unfit [23]; though another study in the same species did not detect inbreeding depression in size or immune response [24]. 

One mechanism whereby genetically impoverished populations may become extinct is through decreased immunocompetence and higher susceptibility to parasites. The impact of parasitism will increase, pushing threatened populations closer to extinction [25]. Bumblebees have a novel immune system control called density-dependent prophylaxis. Adult bumblebee workers exhibit rapid plasticity in their immune function in response to social context. Density-dependent prophylaxis does not depend upon larval conditions, and is likely to be a widespread and labile response to rapidly changing conditions in adult insect populations. Immune function increases in bumblebee workers as the colony ages (and increases in density). This has obvious ramifications for experimental analysis of immune function in insects, and serious implications for our understanding of the epidemiology and impact of pathogens and parasites in spatially structured adult insect populations [26]. 

Decline and conservation of bumble bees

The decline of the bumblebee was discussed in 2008 and remedies were put forward. Suggested measures include tight regulation of commercial bumblebee use and targeted use of environmentally comparable schemes to enhance floristic diversity in agricultural landscapes [27]. But these are not enough. 

Agricultural pesticides known to affect the behaviour and resistance to   pathogens  of the bumblebee should be banned. The viruses and parasites   known to infect bumble bee must be identified  and their spread should be restricted as much as possible. The immediate key to the conservation of the bumble bee  is the elimination of pesticides that impair their behaviour and resistance to pathogens from the bees environment.   Organic farms and wild areas should be set aside as refuges for the bees.  Urban bans on cosmetic pesticide use will provide vital refuges for bumblebees and honeybees as well. Currently, homeowners are deluged with advice for eliminating bumblebees and their habitats from urban property. The endangered bumblebee should be protected from intentional Bombuscide by law. Bumblebees and honeybees are inseparable inhabitants of our ecosystem, and both must be preserved.

Article first published 11/02/11

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References

1. Thorp RW and Shepherd MD. Profile: Subgenus Bombus. In Shepherd MD,  Vaughan DM, and Black SH (Eds). Red List of Pollinator Insects of North America. CD-ROM Version 1 (May 2005). Portland, OR: TheXerces Society for Invertebrate Conservation.
2. Grixti J, Wong L, Cameron S, Favret C. Decline of bumble bees (Bombus) in the North American Midwest Original Research Article Biological Conservation, 2009, 142,75-84.
3. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL Patterns of widespread decline in North American bumble bees.Proc Natl Acad Sci U S A. 2011, 108(2), 662-7.
4. Bumblebee Wikipedia 2011 http://en.wikipedia.org/wiki/Bumble_bee
5. Williams P, Osborne J. Bumble bee vulnerability and conservation worldwide.  Apidologie 2009 40,367-87.
6. Rundlöf M, Nilsson H, Smith H. Interacting effects of farming practice and landscape context on bumble bees.  Biological Conservation 2008 141, 417-26.
7. Holzschuh A, Steffan-Dewenter I, Tscharntke T. Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 2008, 117, 354–61.
8. Williams N, Crone E, Roulston T, Minckley R, Packer L, Potts S. Ecological and life-history traits predict bee species responses to environmental disturbances. Biological Conservation 2010,143, 2280-91.
9. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G. Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behaviour. Ecotoxicology 2010,19, 207-15.
10. Scott-Dupree CD, Conroy L, Harris CR. Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J Econ Entomol. 2009, 102(1), 177-82.
11. Brittain C, Vighi M, Bommarco R, Settele J, Potts E. Impacts of a pesticide on pollinator species richness at different spatial scales. Basic and Applied Ecology 2010, 11, 106-15.
12. Morandin L, Winston M, Franklin M, Abbott V. Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Management Science 2005, 61, 619–26.
13. Mommaerts V, Jans K, Smagghe1 G. Impact of Bacillus thuringiensis strains on survival, reproduction and foraging behaviour in bumblebees (Bombus terrestris). Pest Management Science 2010 ,66, 520–5.
14. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, Brillard J, Baldy A, Belzunces LP, Le Conte Y. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol. 2010, 12(3), 774-82.
15. Ho MW. Ban neonicotinoid pesticides to save the honeybee. Science in Society 49 (to appear).
16. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Vanengelsdorp D, Lipkin WI, Depamphilis CW, Toth AL, Cox-Foster DL.RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species.PLoS One. 2010, 5(12), e14357.
17. Genersch E, Yue C, Fries I, de Miranda JR Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invertebr Pathol. 2006, 91(1), 61-3.
18. Strange JP. Nest initiation in three North American bumble bees (Bombus): gyne number and presence of honey bee workers influence establishment success and colony size. J Insect Sci. 2010, 10, 130.
19. Gegear RJ, Otterstatter MC, Thomson JD.Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc Biol Sci. 2006, 273(1590), 1073-8.
20. Otterstatter MC, Thomson JD.Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 2007, 154(2), 411-21.
21. Rutrecht S, Klee J and Brown J. Horizontal transmission success of Nosema bombi to its adult bumble bee hosts: effects of dosage, spore source and host age. Parasitology 2007, 134, 1719-26.
22. Otterstatter MC, Thomson JD. Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS One 2008, 3(7), e2771.
23. Gerloff C, Schmid-Hempel P. Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 2005, 111, 67–80.
24. Gerloff C, Ottmer B, Schmid-Hempel P. Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology 2003,17, 582–9.
25. Whitehorn P, Tinsley M, Brown N, Darvill D, Goulson D. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc. R. Soc. B  2010 published online before print  doi:10.1098/rspb.2010.1550.
26. Ruiz-González MX, Moret Y, Brown MJ. Rapid induction of immune density-dependent prophylaxis in adult social insects. Biol Lett. 2009, 5(6), 781-3.
27. Goulson D, Lye GC, Darvill B. Decline and conservation of bumble bees .Annu Rev Entomol. 2008, 53, 191-208.