Bombus terrestris: Difference between revisions

Bombus terrestris
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hymenoptera
Family:	Apidae
Subfamily:	Apinae
Genus:	Bombus
Species:	B. terrestris
Binomial name
	Bombus terrestris; (Linnaeus, 1758)

Browse history interactively

← Previous edit Next edit →

Content deleted Content added

VisualWikitext

Inline

Revision as of 05:49, 21 October 2015

Bombus terrestris, the buff-tailed bumblebee or large earth bumblebee, is one of the most numerous bumblebee species in Europe. In addition, Bombus terrestris is the largest of the European bumblebee species.^[1] It is one of the main species used in greenhouse pollination, and consequently, can be found in many countries and areas where it is not native, such as Tasmania for example.^[2] Moreover, it is a eusocial insect that is characterized by unique Hymenopteran sex ratios, where male drones dominate most colonies. The queen of B. terrestris is often highly dominant over her colony and exhibits behaviors such as altering the sex ratio in her favor over the workers and controlling queen larval development with pheromones. However, after aggression breaks out in the nest, the workers can usually gain control of the nest and restart the colony cycle. The queen is monandrous and only mates with one male after leaving the nest, despite the potential genetic benefits from polyandrous mating. B. terrestris demonstrates noteworthy learning tactics with flower color and alloethism in foraging behaviors. They have also been implicated in a number of bee pathology studies.

Taxonomy and Phylogenetics

B. terrestris is part of the order Hymenoptera, which is composed of ants, bees, wasps, and sawflies. The family Apidae specifically consists of bees. It is also part of the subfamily Apinae, which includes most species of bees within the family most of which are solitary. There are 14 tribe lineages within Apinae, and B. terrestris is in the bumblebee tribe, Bombini. It is in the genus Bombus, which consists entirely of bumblebees, and the subgenus Bombus sensu stricto. There are two documented subspecies: Bombus terrestris terrestris and Bombus terrestris sassaricus. ^[3] Two closely related species, B. canariensis and B. maderensis, are thought to have evolved from European B. terrestris strains and then diverged on the Canary Islands and Maderia respectively.^[4]

Description and Identification

B. terrestris are pollen-storing bees that generally feed and forage on nectar and pollen.^[5] These bees can navigate their way back to the nest from a distance as far away as 13 km (8.1 mi), although most forage within 5 km of their nest.^[6] One mark and recapture study found their average foraging distance to be approximately 663 m.^[7] The queen is between 20–22 mm long, males range from 14–16 mm, and workers from 11–17 mm. The latter are characterized by their white-ended abdomens and look just like workers of the white-tailed bumblebee, B. lucorum, a close relative, apart from the yellowish bands of B. terrestris being darker in direct comparison. The queens of B. terrestris have the namesake buff-white abdomen tip ("tail"); this area is white like in the workers in B. lucorum.^[1] B. terrestris are unique compared to other bees in that their caste of workers exhibit a wide variation in worker size, with thorax sizes ranging from 2.3 to 6.9 mm in length and masses ranging from 68 to 754 mg.^[5]

Distribution and Habitat

B. terrestris is most commonly found throughout Europe and generally occupies temperate climates. Because it can survive in a wide variety of habitats, there are populations in the near East, the Mediterranean Islands, and Northern Africa as well.^[4] Nests are usually found underground, such as in abandoned rodent dens.^[8]^[9] Colonies form comb-like nest structures with egg cells each containing several eggs. The queen will layer these egg cells on top of one another. Colonies produce between 300-400 bees on average, with a large variation in the number of workers.^[3]

Colony Cycle

A solitary queen hatched from her abandoned colony initiates the colony cycle when she mates with a male and finds a nest, after which she lays a small batch of diploid eggs. Once these hatch, she tends the larvae, feeding them with nectar and pollen. When the larvae are grown, they pupate, and about two weeks later, the first workers emerge. This is known as the initiation phase of the colony.^[3] Workers will forage for nectar and pollen for the colony and tend later generations of larvae. The workers are smaller than the queen and only live for a few weeks. The foraging range and frequency of workers depends on the quality and distribution of available food, but most workers forage within a few hundred meters of their nest.^[10]

This first phase can last a variable amount of time in B. terrestris, after which the switch point is reached and the queen begins to lay some unfertilized eggs, which develop into males.^[3] When the male drones emerge from the nest, they do not return, foraging only for themselves. They seek out new queens and mate with them. Remaining diploid eggs receive extra food and pupate to become new queens. The queen can use pheromones to discourage the workers' inclination to invest more in these larvae, thereby ensuring that not too many become queens. The colony persists until the competition point is reached, when workers begin egg laying. At this point, outright aggression among workers and between the queen and workers begins. This is a predictable time point that occurs about 30 days into the colony cycle.^[3]

Usually, the worker-queen conflict will force the queen out and the new workers will become queenless. A "false queen" might take control of the colony for a short period.^[11] The colony cycle starts again when the newly hatched queens leave the nest in search of a mate and a nest for themselves in order to start a new colony.

Reproductive Behavior

Mating System

B. terrestris is thought to be a singly mating species. This is unusual for social insect queens because mating with several males (polyandry) has potential genetic benefits.^[12] The lack of multiple matings by B. terrestris queens may be partly due to male interference. B. terrestris males plug the female's sexual tract with a sticky secretion during mating, which appears to reduce the female's ability to successfully mate with other males for several days.^[13] While there may be genetic fitness benefits in colony heterogeneity from a polyandrous mating system, bumblebees are also likely to be monandrous due to social constraints and risks associated with multiple matings. Finding multiple mates might be energetically costly and expose the queen to higher predation risks. Additionally, while queens may prefer multiple matings to ensure more genetic variability and viable offspring, the queen-worker conflict dictates that workers will be more apt to raise larvae from a single male.^[12] This is due to haplodiploidy in Hymenopteran social insects in which males (drones) are haploid and females (workers and queens) are diploid. This confers greater genetic similarity between sister workers (relatedness of 0.75) than between mother and offspring (relatedness of 0.5), making kin selection stronger between sisters. This selective force would be reduced if workers were the offspring of multiple males, which might lead to increased conflict in the nest.

Worker Egg Laying

In addition to the queen, the workers can lay eggs for the colony brood. Since workers do not mate, all of their eggs are haploid and will develop into drones. There are multiple factors that determine whether a worker bee will become reproductively active. Workers born early in the first brood are more likely to become egg layers due to their increased size and age, which allows more time for ovarian development. Workers usually have to be at least 30 days old to become an egg layer. Individuals that spend less time foraging and more time near the queen are also more likely to become reproductive. Lastly, due to intense competition for the opportunity to reproduce, older workers often harass the queen by attacking her and buzzing loudly. Once this point is reached the colony is usually abandoned.^[14]

Sex Ratios

Due to the variability in the switch point of B. terrestris colonies, there are varying levels of sex ratios among nests. Early-switching colonies have a much larger number of males compared to workers and queens (17.4:1), which may give them a competitive advantage in mating with later emerging queens. Late-switching colonies have fewer males and a more even sex ratio of 1:3:1, thus indicating the queen's control over her colony (she prefers a 1:1 ratio, since she is equally related to both sons and daughters). On the other hand, workers prefer a 1:3 ratio, as they are more related to each other than to their mother. Although early and late switching colonies are usually balanced in the population, the overall demographic in one study was found to be male biased, resulting in an overall sex ratio of 4:1 (males to females).^[3] However, most studies show that this balance of bimodal sex determination between early and late-switching colonies creates the queen's preferred 1:1 sex ratio in B. terrestris populations.^[15] This is unusual for social insects, which usually have a 1:3 sex ratio indicative of worker colony control.

Reproductive Suppression

Queen Suppression

Queen bees can control oogenesis in worker bees via juvenile hormone (JH), which regulates egg development. Among queenless B. terrestris workers, the corpus allata, which secretes JH, was noticeably enlarged compared to queenright workers. JH concentrations were also higher in the hemolymph of queenless workers. This suggests that the presence of a queen is enough to prevent workers from laying eggs, which helps her maintain genetic control over her colony's brood. The mechanism through which the queen induces this behavior is likely through pheromones. ^[16]

Worker Suppression

While the queen controls much of the egg laying and larval development in the colony, it is likely that workers play a much bigger role in controlling egg laying than previously thought. Dominant workers will often inhibit younger workers from laying eggs.^[14]^[17] Workers have low levels of JH and ovarian development during the early stages of the colony cycle and also after the competition point. Workers introduced into queenright and queenless colonies experience similar levels of inhibition from fellow workers during the competition point, indicating the key role of worker policing of fellow nest mates later in the colony cycle. This suggests that worker reproductive development will be highest between early development and the competition point in the colony.^[17]

Social and Foraging Behavior

Dominance Hierarchy

Workers start out at the bottom of the dominance hierarchy in the social colony. As they age, they move closer to the position of queen. Queen-side workers are often egg layers and interact more frequently with the queen. This social position may pay off later, after the competition point is reached. When the queen is overthrown by the aggression of the workers, the most dominant worker will have the best likelihood of contributing more eggs to the colony brood and will perhaps climb to the position of “false queen.” The queen appears to maintain a constant distance of social dominance from her workers at all points in the cycle, suggesting that she is displaced by the sheer number of workers later in the cycle.^[11]

Foraging Behavior

Alloethism

B. terrestris bees exhibit alloethism in foraging behavior. Larger bees are more often found foraging outside the nest and will return to the nest with larger amounts of nectar and pollen. It is possible that larger bees might be able to withstand greater temperature variation, avoid predation, and travel larger distances making them selectively advantageous. Distinct social roles based on morphology might also be beneficial for individuals of the colonies, by making the colony operate more efficiently. Small bees can be reared more cheaply and kept for in-nest tasks, while only some larvae will be fed enough to become large foraging bees.^[5]

Food Alert

Individuals who return from the nest after a foraging run often recruit other bees in the colony to leave the nest and search for food. In B. terrestris, successful foragers will return to the nest and run around frantically and without a measurable pattern, unlike the ritualized dance of the honeybee. Although the mechanism by which this recruitment strategy functions is unclear, it is hypothesized that running around likely spreads a pheromone that encourages other bees to exit and forage by indicating the location and odor of food nearby.^[9]

Homing Ability

B. terrestris has an impressive homing range, where bees displaced from their nests can relocate the colony from up to 9.8 km away. However, the return often takes several days, indicating B. terrestris might be utilizing familiar foliage and natural landmarks to find the nest. This may be a tedious process if an individual is outside the conventional foraging range of the nest.^[18]

Learning

Bumblebees and honeybees are extremely influenced by an innate preference for blue and yellow color. When they have no training, they will often just visit flowers that naturally attract them. However, it is generally thought that bees will learn to visit more nectar rewarding flowers after experience associates the reward with the color of the petals. This has been demonstrated in B. terrestris, where bees trained on artificially colored flowers will pick a similar color to the one they were trained with when tested with an array of flower choices. If individuals were tested with flower colors significantly different than from what they were trained with, they just visited flowers most closely aligned with their innate color preferences.^[19] In addition to identifying specific colors for foraging purposes, it has also been shown that young worker bees have to learn complex motor skills in order to efficiently collect nectar and pollen from flowers. These skills might take several days to develop, as memory does not always hold perfectly on a day-to-day basis, sometimes deteriorating overnight.^[20]

Limitations on Foraging Precision

While bees are highly adept at discrimination tasks, they are still limited by the magnitude of difference needed in hue to properly carry out these tests. Error rates of color recognition decrease in B. terrestris when flower pigments are closer together on the color spectrum. This might have damaging effects on pollination efficiency if bees visit different flower species with similar, but distinct colors, which can only be mediated if the flowers have unique shapes.^[21]

Social Learning

While bees often forage alone, experiments demonstrate that young foragers might learn what flowers provide the most nectar more quickly when foraging with older workers. B. terrestris individuals have a faster learning curve for visiting unfamiliar, yet rewarding flowers, when they can see a conspecific foraging on the same species.^[22] The discovery of this type of associative learning is a novel insight into bee behavior and may supplement learning via color reward association.

Kin Selection

Worker-Queen Conflict

Conflict is expected between queen and workers over the sex ratio and reproduction of males in the colony, especially in monandrous colonies where workers are more related to their own sons and nephews than to their brothers.^[17] In early-switching colonies, workers might start laying eggs when they know it will be in their own genetic interests, perhaps from a cue that indicates the switch point has been reached and the queen is now laying haploid eggs. This might be delayed, because sex can only be differentiated in mature larvae by workers. In late-switching colonies (where the competition point still occurs at the same time in the cycle), workers may start laying eggs when they detect a change in the queen’s pheromone that indicate larvae are developing into new queens.^[15] Thus, the outcome of this conflict is mediated through the dominance of the queen and the information available to the workers. While it is assumed that queens usually win this conflict, it is still unclear because some studies have indicated that up to 80% of males are produced by workers.^[14] These asymmetries in the timing of egg lying and dominance in B. terrestris might explain why it often does not conform to predicted sex ratios and kin-selection hypotheses.

Worker-Worker Conflict

Although B. terrestris workers are most directly in competition with the queen for egg laying opportunities, they will still inhibit their sisters from laying eggs in order to have their own sons. This is beneficial to them because they will share more genes with their own son rather than their nephews.^[17]

Parasites and Disease

Effects of Foraging on Resistance

Foraging is considered energetically costly and it is possible that individuals that spend more time foraging suffer costs to their overall fitness. For example, B. terrestris is often vulnerable to parasitism by conopid flies in Central Europe, and it has been hypothesized that foragers might suffer higher incidences of parasites due to the increased metabolic costs of flying. This was demonstrated in a population in which foraging workers had significantly lower levels of encapsulation of an experimental parasitic egg when compared to non-foraging workers. This suggests that foragers have compromised immune systems due to increased energetic expenses and might be predisposed to fly parasites.^[23]

Effects of Polyandry on Resistance

While B. terrestris is a singly mating species, a polyandrous system would potentially be beneficial because it would be possible to attain greater genetic variability for resistance against disease. Accordingly, artificially increasing the number of mates a B. terrestris queen obtains through artificial insemination has shown that the increased genetic variability in her offspring confers greater resistance to the most common bumblebee parasite, Crithidia bombi. ^[12] However, the average reproductive success between one and multiple matings is not linear. Queens that mated once and mated four times had a higher fitness than those that mated twice.^[12] This suggests that there might be a fitness barrier to increased matings, which might be why colonies are usually monandrous.

Immunocompetence

Surprisingly, the immunocompetence, as measured by the ability to encapsulate a novel antigen, does not vary based on the local environment. Experimental studies demonstrate that B. terrestris have equal levels of encapsulation in poor and stable environments.^[24] This is unexpected, because immunity should be compromised in conditions where food supply is low in order to save energy. Perhaps encapsulation represents an invariable trait of bumblebees, or immunity is far too complex to characterize solely based on measurements of encapsulation.

Threats from Disease

Deformed wing virus (DMV) is normally a honeybee pathogen that results in reduced and crumpled wings, making those individuals inviable. This virus is thought to have spread to B. terrestris and in 2004 as many as 10% of queen bees bred commercially in Europe were found dead with deformed wings. This was confirmed as DMV when B. terrestris colonies tested positive for the presence of DMV RNA. This could indicate that DMV is a broad range pathogen among bees, or perhaps it has recently been infecting new hosts after transmission from honeybees.^[25]

Environmental Concerns

Invasive Species

While native to Europe, B. terrestris has been introduced as a greenhouse pollinator into many foreign ecosystems. The presence of B. terrestris is becoming an ecological concern in many communities in which it is not native. It is classified as an "invasive alien species" in Japan.^[26] For example, B. terrestris has a large niche overlap with local Japanese bee species in terms of flower resources and nest sites. B. terrestris queens competing for local underground nest sites are displacing B. hypocrita sapporoensis. However, B. pseudobaicalensis, which visits similar flowers but only forms nests above ground, has not seen a rapid decline in population numbers.^[8]

In 2008, the Australian government banned the live import of B. terrestris into Australia on the grounds that it would present a significant risk of becoming a feral species and thereby present a threat to native fauna and flora.^[27] In 2004, this bumblebee was classified as a 'Key Threatening Process' by the Scientific Committee of the New South Wales Department of Environment.^[28]

This species was introduced to Chile in 1998. It has since crossed into Argentina, and is spreading at about 275 km per year. Where it spreads, the only bumblebee native to southern South America, Bombus dahlbomii, disappears within weeks. Bombus ruderatus, a bee previously introduced in 1982, is also seriously affected. The cause is thought to be the parasite Apicystis bombi, an organism carried by the buff-tails, but which has no adverse effect on that species.^[29]

Colony Development in Changing Environments

In temperate areas, variable climates and environmental conditions occur during changing seasons. Lack of available food due to these unpredictable circumstances can often negatively affect colony growth, reproduction, and resistance to parasites. In poor environments with limited food, the few workers born are smaller than average. However, it appears that B. terrestris is well adapted to a changing environment, considering colony growth is higher under variable feeding conditions. Workers and reproductives are also heavier with a variable food supply when compared to stable food availability. This might indicate an adaptive strategy of increased provisioning to save for days it is hard to find food.^[24]

Pesticide Exposure

In their 2014 study published in Functional Ecology researchers using Radio-Frequency Identification (RFID) tagging technology on the bees, found that a sublethal exposure to either a neonicotinoid (imidacloprid) and/or a pyrethroid (?-cyhalothrin) over a four-week period caused an impairment of the bumblebee's ability to forage.^[30] Research published in 2015 showed that bees prefer solutions containing neonicotinoids, even though the consumption of these pesticides caused them to eat less food overall. This work implies that treating flowering crops with such pesticides presents a sizeable hazard to foraging bees.^[31]

Human Importance

Domestication

Since 1987, B. terrestris has been bred commercially for use as a pollinator in European greenhouse crops, particularly tomatoes—a task which was previously carried out by human hand.^[26]^[32] B. terrestris has been commercially reared in New Zealand since the early 1990s^[33]^[34] and is now used in at least North Africa, Japan, Korea, and Russia, with the global trade in bumblebee colonies probably exceeding 1 million nests per year.^[35]

Agriculture

B. terrestris are key commercial pollinators in Europe, which has driven researchers to investigate the influence of agricultural land on the foraging and survival of this species. Monoculture reduces biodiversity in farmland areas and likely decreases the number of flowering species bees can forage on. B. terrestris consequently exhibits greater nest growth in suburban areas than in farmland, because local suburban gardens promote more plant diversity for bees to feed from. Agriculture has a profound impact on many bumblebees and is causing widespread decline in several species. However, B. terrestris is still widespread, likely because it can forage at very long distances, making it less sensitive to changes in biodiversity and the environment.^[36]

References

^ ^a ^b Bumblebee species, retrieved 4 October 2014
^ Semmens, T.D., E. Turner, and R. Buttermore. (1993). "Bombus terrestris (L.) (Hymenoptera: Apidae) now established in Tasmania". Australian Journal of Entomology. 32 (4): 346.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b ^c ^d ^e ^f Duchateau, M. J. and H. H. W. Velthuis (1988). "Development and reproductive strategies in Bombus terrestris colonies". Behavior. 107: 186–207.
^ ^a ^b 10. Widmer, A., P. Schmid-Hempel, and A. Estoup, and A. Scholl (1998). "Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira". Heredity. 81: 563–572. {{cite journal}}: horizontal tab character in |author= at position 4 (help)CS1 maint: multiple names: authors list (link) CS1 maint: numeric names: authors list (link)
^ ^a ^b ^c Goulson, D., J. Peat, J. C. Stout, J. Tucker, B. Darvill, L. C. Derwent, and W. O. H. Hughes (2002). "Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?". Animal Behaviour. 64: 123–130.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ Louisa Cheung (July 26, 2006). "Homing instinct of bees surprises". BBC News.
^ Walther-Hellwig, K. and R. Frankl (1999). "Foraging distances of Bombus muscorum, Bombus lapidarius, and Bombus terrestris (Hymenoptera, Apidae)". Journal of Insect Behavior. 13 (2): 2000.
^ ^a ^b Inoue, M.K., J. Yokoyama, and I. Washitani (2008). "Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae)". Journal of Insect Conservation. 12: 135–146.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b Dornhaus, A. and L. Chittka (2001). "Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications". Behavioral Ecology and Sociobiology. 50: 570–576.
^ Stephan Wolf & Robin F. A. Moritz (2008). "Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae)". Apidologie. 39 (4). EDP Sciences: 419–427. doi:10.1051/apido:2008020.
^ ^a ^b van Honk, C. and P. Hogeweg (1981). "The ontogeny of the social structure in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9 (2): 111–119.
^ ^a ^b ^c ^d Baer, B. and P. Schmid-Hempel (2001). "Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris". Evolution. 55 (8): 1639–1643.
^ Annette Sauter, Mark J. F. Brown, Boris Baer & Paul Schmid-Hempel (2001). "Males of social insects can prevent queens from multiple mating". Proceedings of the Royal Society B. 268 (1475): 1449–1454. doi:10.1098/rspb.2001.1680. PMC 1088762. PMID 11454287.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b ^c van Honk, C.G.J., P.F. Roseler, H.H.W. Velthuis, and J.C. Hoogeveen (1981). "Factors influencing the egg laying of workers in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9: 9–14.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b Bourke, A.F.G. and F.L.W. Ratnieks (2001). "Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae)". Proceedings of the Royal Society of London B. 268: 347–355.
^ Roseler, P. F. (1977). "Juvenile hormone control of oogenesis in bumblebee workers, B. terrestris". Journal of Insect Physiology. 23: 985–992.
^ ^a ^b ^c ^d Bloch, G. and A. Hefetz (1999). "Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queen right colonies". Behavioral Ecology and Sociobiology. 45: 125–135.
^ Goulson, D. and J. Stout (2001). "Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae)". Apidologie. 32: 105–111.
^ Gumbert, A (2000). "Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning". Behavioral Ecology and Sociobiology. 48 (1): 36–43.
^ Raine, N.E. and L. Chittka (2007). "Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris)". Naturwissenschaften. 94: 459–464.
^ Dyer, A.G. and L. Chittka (2004). "Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study". Journal of Comparative Physiology A. 190: 105–114.
^ Leadbeater, E. and L. Chittka (2007). "The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris)". Behavioral Ecology and Sociobiology. 61 (11): 1789–1796.
^ Konig, C. and P. Schmid-Hempel (1995). "Foraging and immunocompetence in workers of the bumblebee, Bombus terrestris L.". Proceedings of the Royal Society of London B. 260: 225–227.
^ ^a ^b Schmid-Hempel, R. and P. Schmid-Hempel (1998). "Colony performance and immunocompetence of a social insect, B. terrestris, in poor and variable environments". Functional Ecology. 22: 22–30.
^ Genersch, E., C. Yue, I. Fries, J. R. de Miranda (2006). "Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities". Journal of Insect Pathology. 91: 61–63.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b Matsumura, Chizuru; Jun Yokoyama; Izumi Wasitani (August 2004). "Invasion Status and Potential Ecological Impacts of an Invasive Alien Bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) Naturalized in Southern Hokkaido, Japan" (PDF). Global Environmental Research. AIRIES: 51–66.
^ "Bumblebee rejected for live import". Australian Government. 26 October 2008. Retrieved 1 January 2009. {{cite web}}: Cite has empty unknown parameter: |coauthors= (help)
^ Paul Adam (February 2004). "Introduction of the large earth bumblebee, Bombus terrestris - key threatening process listing". NSW Government. Retrieved 1 January 2009. {{cite web}}: Cite has empty unknown parameter: |coauthors= (help)
^ Goulson, Dave (2013). "Argentinian invasion!". Buzzword. 21: 17–18.
^ Gill, Richard J.; Raine, Nigel E. (7 July 2014). "Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure". Functional Ecology. doi:10.1111/1365-2435.12292. {{cite journal}}: |access-date= requires |url= (help)
^ Kessler, Sebastien C (7 May 2015). "Bees prefer foods containing neonicotinoid pesticides". Nature. 521. Macmillan Publishing Ltd: 74–76. ISSN 0028-0836. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
^ Anon. "Natural pollination". Koppert Biological Systems. Koppert B.V. Retrieved 18 September 2011.
^ Velthuis, H. H. W. and van Doorn, A. (April 2004) 'The breeding, commercialization and economic value of bumblebees.' in B. M. Freitas and J. O. P. Pereira (eds) Solitary Bees Conservation, Rearing and Management for Pollination. Federal University of Ceara, Brasil, pp. 135-149
^ http://biobees.co.nz/biology.html
^ Dave Goulson (2010). "Bumblebees. Behaviour, Ecology and Conservation" Oxford University Press.
^ Goulson, D., W.O.H. Hughes, L.C. Derwent, and J.C. Stout (2002). "Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats". Oecologia. 130: 267–273.{{cite journal}}: CS1 maint: multiple names: authors list (link)

External links

What Harm Could Exotic Bumblebees Do in Australia? - a report by Australian Native Bee Research Centre

[bee-1] Bumblebee species, retrieved 4 October 2014

[2] Semmens, T.D., E. Turner, and R. Buttermore. (1993). "Bombus terrestris (L.) (Hymenoptera: Apidae) now established in Tasmania". Australian Journal of Entomology. 32 (4): 346.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[Duchateau-3] ^ ^a ^b ^c ^d ^e ^f Duchateau, M. J. and H. H. W. Velthuis (1988). "Development and reproductive strategies in Bombus terrestris colonies". Behavior. 107: 186–207.

[Widmer-4] 10. Widmer, A., P. Schmid-Hempel, and A. Estoup, and A. Scholl (1998). "Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira". Heredity. 81: 563–572. {{cite journal}}: horizontal tab character in |author= at position 4 (help)CS1 maint: multiple names: authors list (link) CS1 maint: numeric names: authors list (link)

[Goulson-5] Goulson, D., J. Peat, J. C. Stout, J. Tucker, B. Darvill, L. C. Derwent, and W. O. H. Hughes (2002). "Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?". Animal Behaviour. 64: 123–130.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[6] Louisa Cheung (July 26, 2006). "Homing instinct of bees surprises". BBC News.

[7] Walther-Hellwig, K. and R. Frankl (1999). "Foraging distances of Bombus muscorum, Bombus lapidarius, and Bombus terrestris (Hymenoptera, Apidae)". Journal of Insect Behavior. 13 (2): 2000.

[Inoue-8] Inoue, M.K., J. Yokoyama, and I. Washitani (2008). "Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae)". Journal of Insect Conservation. 12: 135–146.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[Dornhaus-9] Dornhaus, A. and L. Chittka (2001). "Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications". Behavioral Ecology and Sociobiology. 50: 570–576.

[10] Stephan Wolf & Robin F. A. Moritz (2008). "Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae)". Apidologie. 39 (4). EDP Sciences: 419–427. doi:10.1051/apido:2008020.

[Honk-11] van Honk, C. and P. Hogeweg (1981). "The ontogeny of the social structure in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9 (2): 111–119.

[Baer-12] Baer, B. and P. Schmid-Hempel (2001). "Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris". Evolution. 55 (8): 1639–1643.

[13] Annette Sauter, Mark J. F. Brown, Boris Baer & Paul Schmid-Hempel (2001). "Males of social insects can prevent queens from multiple mating". Proceedings of the Royal Society B. 268 (1475): 1449–1454. doi:10.1098/rspb.2001.1680. PMC 1088762. PMID 11454287.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[van_Honk-14] van Honk, C.G.J., P.F. Roseler, H.H.W. Velthuis, and J.C. Hoogeveen (1981). "Factors influencing the egg laying of workers in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9: 9–14.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[Bourke-15] Bourke, A.F.G. and F.L.W. Ratnieks (2001). "Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae)". Proceedings of the Royal Society of London B. 268: 347–355.

[16] Roseler, P. F. (1977). "Juvenile hormone control of oogenesis in bumblebee workers, B. terrestris". Journal of Insect Physiology. 23: 985–992.

[Bloch-17] Bloch, G. and A. Hefetz (1999). "Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queen right colonies". Behavioral Ecology and Sociobiology. 45: 125–135.

[18] Goulson, D. and J. Stout (2001). "Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae)". Apidologie. 32: 105–111.

[19] Gumbert, A (2000). "Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning". Behavioral Ecology and Sociobiology. 48 (1): 36–43.

[20] Raine, N.E. and L. Chittka (2007). "Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris)". Naturwissenschaften. 94: 459–464.

[21] Dyer, A.G. and L. Chittka (2004). "Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study". Journal of Comparative Physiology A. 190: 105–114.

[22] Leadbeater, E. and L. Chittka (2007). "The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris)". Behavioral Ecology and Sociobiology. 61 (11): 1789–1796.

[23] Konig, C. and P. Schmid-Hempel (1995). "Foraging and immunocompetence in workers of the bumblebee, Bombus terrestris L.". Proceedings of the Royal Society of London B. 260: 225–227.

[Schmid-24] Schmid-Hempel, R. and P. Schmid-Hempel (1998). "Colony performance and immunocompetence of a social insect, B. terrestris, in poor and variable environments". Functional Ecology. 22: 22–30.

[25] Genersch, E., C. Yue, I. Fries, J. R. de Miranda (2006). "Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities". Journal of Insect Pathology. 91: 61–63.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[Matsumura-26] Matsumura, Chizuru; Jun Yokoyama; Izumi Wasitani (August 2004). "Invasion Status and Potential Ecological Impacts of an Invasive Alien Bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) Naturalized in Southern Hokkaido, Japan" (PDF). Global Environmental Research. AIRIES: 51–66.

[27] "Bumblebee rejected for live import". Australian Government. 26 October 2008. Retrieved 1 January 2009. {{cite web}}: Cite has empty unknown parameter: |coauthors= (help)

[28] Paul Adam (February 2004). "Introduction of the large earth bumblebee, Bombus terrestris - key threatening process listing". NSW Government. Retrieved 1 January 2009. {{cite web}}: Cite has empty unknown parameter: |coauthors= (help)

[29] Goulson, Dave (2013). "Argentinian invasion!". Buzzword. 21: 17–18.

[Gill_Raine_2014-30] Gill, Richard J.; Raine, Nigel E. (7 July 2014). "Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure". Functional Ecology. doi:10.1111/1365-2435.12292. {{cite journal}}: |access-date= requires |url= (help)

[Neonicotinoids-31] Kessler, Sebastien C (7 May 2015). "Bees prefer foods containing neonicotinoid pesticides". Nature. 521. Macmillan Publishing Ltd: 74–76. ISSN 0028-0836. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)

[32] Anon. "Natural pollination". Koppert Biological Systems. Koppert B.V. Retrieved 18 September 2011.

[33] Velthuis, H. H. W. and van Doorn, A. (April 2004) 'The breeding, commercialization and economic value of bumblebees.' in B. M. Freitas and J. O. P. Pereira (eds) Solitary Bees Conservation, Rearing and Management for Pollination. Federal University of Ceara, Brasil, pp. 135-149

[34] ttp://biobees.co.nz/biology.html

[35] Dave Goulson (2010). "Bumblebees. Behaviour, Ecology and Conservation" Oxford University Press.

[36] Goulson, D., W.O.H. Hughes, L.C. Derwent, and J.C. Stout (2002). "Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats". Oecologia. 130: 267–273.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[1]

[2]

[3]

[4]

[5]

[6]

[7]

[8]

[9]

[10]

[11]

[12]

[13]

[14]

[15]

[16]

[17]

[18]

[19]

[20]

[21]

[22]

[23]

[24]

[25]

[26]

[27]

[28]

[29]

[30]

[31]

[32]

[33]

[34]

[35]

[36]

@@ Line 15: / Line 15: @@
 }}
-'''''Bombus terrestris''''', the '''buff-tailed bumblebee''' or '''large earth bumblebee''' is one of the most numerous [[bumblebee]] [[species]] in [[Europe]]. In addition, ''Bombus terrestris'' is the largest of the European bumblebee species.<ref name ="bee">{{citation|url=http://www.bumblebee.org/key.htm |title=Bumblebee species |accessdate=4 October 2014 }}</ref> It is one of the main species used in greenhouse [[pollination]], and consequently, can be found in many countries and areas where it is not native; [[Tasmania]] for example.<ref>{{cite journal | author = Semmens, T.D., E. Turner, and R. Buttermore. |title = ''Bombus terrestris'' (L.) (Hymenoptera: Apidae) now established in Tasmania | journal = Australian Journal of Entomology | year = 1993 | volume = 32 | issue = 4| pages =346}}</ref> Moreover, it is a [[Eusociality|eusocial]] insect that is characterized by unique Hymenopteran sex ratios, where male drones dominate most colonies. The queen of ''B. terrestris'' is often highly dominant over her colony and exhibits behaviors such as altering the sex ratio in her favor over the workers and controlling queen larval development with pheromones. However, after aggression breaks out in the nest, the workers can usually gain control of the nest and restart the colony cycle. The queen is monandrous and only mates with one male after leaving the nest, despite the potential genetic benefits from polyandrous mating. ''B. terrestris'' demonstrates noteworthy learning tactics with flower color and alloethism in foraging behaviors. They have also been implicated in a number of bee pathology studies.
+'''''Bombus terrestris''''', the '''buff-tailed bumblebee''' or '''large earth bumblebee,''' is one of the most numerous [[bumblebee]] [[species]] in [[Europe]]. In addition, ''Bombus terrestris'' is the largest of the European bumblebee species.<ref name ="bee">{{citation|url=http://www.bumblebee.org/key.htm |title=Bumblebee species |accessdate=4 October 2014 }}</ref> It is one of the main species used in greenhouse [[pollination]], and consequently, can be found in many countries and areas where it is not native, such as [[Tasmania]] for example.<ref>{{cite journal | author = Semmens, T.D., E. Turner, and R. Buttermore. |title = ''Bombus terrestris'' (L.) (Hymenoptera: Apidae) now established in Tasmania | journal = Australian Journal of Entomology | year = 1993 | volume = 32 | issue = 4| pages =346}}</ref> Moreover, it is a [[Eusociality|eusocial]] insect that is characterized by unique Hymenopteran sex ratios, where male drones dominate most colonies. The queen of ''B. terrestris'' is often highly dominant over her colony and exhibits behaviors such as altering the sex ratio in her favor over the workers and controlling queen larval development with pheromones. However, after aggression breaks out in the nest, the workers can usually gain control of the nest and restart the colony cycle. The queen is monandrous and only mates with one male after leaving the nest, despite the potential genetic benefits from polyandrous mating. ''B. terrestris'' demonstrates noteworthy learning tactics with flower color and alloethism in foraging behaviors. They have also been implicated in a number of bee pathology studies.
 ==Taxonomy and Phylogenetics==
-''B. terrestris'' is part of the order [[Hymenoptera]], which is composed of ants, bees, wasps, and sawflies and the family [[Apidae]], which specifically consists of bees. It is also part of the subfamily [[Apinae]], which includes most species of bees within the family most of which are solitary. There are 14 tribe lineages within [[Apinae]], and ''B. terrestris'' is in the bumblebee tribe, [[Bombini]]. It is in the genus ''[[Bombus]]'', which consists entirely of bumblebees, and the subgenus ''Bombus sensu stricto''. There are two documented subspecies: ''Bombus terrestris terrestris'' and ''Bombus terrestris sassaricus.'' <ref name="Duchateau">{{cite journal | author = Duchateau, M. J. and H. H. W. Velthuis | year = 1988 |  title = Development and reproductive strategies in Bombus terrestris colonies | journal =[[Behavior]] | volume = 107 | issue = | pages = 186–207}}</ref> Two closely related species, ''B. canariensis'' and ''B. maderensis'', are thought to have evolved from European ''B. terrestris'' strains and then diverged on the Canary Islands and Maderia respectively.<ref name = "Widmer">{{cite journal | author = 10.	Widmer, A., P. Schmid-Hempel, and A. Estoup, and A. Scholl| year = 1998 |title = Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira | journal = Heredity | volume = 81 | pages = 563–572}}</ref>
+''B. terrestris'' is part of the order [[Hymenoptera]], which is composed of ants, bees, wasps, and sawflies. The family [[Apidae]] specifically consists of bees. It is also part of the subfamily [[Apinae]], which includes most species of bees within the family most of which are solitary. There are 14 tribe lineages within [[Apinae]], and ''B. terrestris'' is in the bumblebee tribe, [[Bombini]]. It is in the genus ''[[Bombus]]'', which consists entirely of bumblebees, and the subgenus ''Bombus sensu stricto''. There are two documented subspecies: ''Bombus terrestris terrestris'' and ''Bombus terrestris sassaricus.'' <ref name="Duchateau">{{cite journal | author = Duchateau, M. J. and H. H. W. Velthuis | year = 1988 |  title = Development and reproductive strategies in Bombus terrestris colonies | journal =[[Behavior]] | volume = 107 | issue = | pages = 186–207}}</ref> Two closely related species, ''B. canariensis'' and ''B. maderensis'', are thought to have evolved from European ''B. terrestris'' strains and then diverged on the Canary Islands and Maderia respectively.<ref name = "Widmer">{{cite journal | author = 10.	Widmer, A., P. Schmid-Hempel, and A. Estoup, and A. Scholl| year = 1998 |title = Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira | journal = Heredity | volume = 81 | pages = 563–572}}</ref>
 ==Description and Identification==
-''B. terrestris'' are pollen-storing bees that generally feed and forage on nectar and pollen.<ref name = "Goulson">{{cite journal | author = Goulson, D., J. Peat, J. C. Stout, J. Tucker, B. Darvill, L. C. Derwent, and W. O. H. Hughes | year = 2002 | title = Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? | journal = Animal Behaviour | volume = 64 | pages = 123–130}}</ref> These bees can navigate their way back to the nest from a distance as far away as {{convert|13|km|mi|abbr=on}}, although most forage within 5&nbsp;km of their nest,<ref>{{cite news |url=http://news.bbc.co.uk/1/hi/sci/tech/5215022.stm |title=Homing instinct of bees surprises |publisher=[[BBC News]] |date=July 26, 2006 |author=Louisa Cheung}}</ref> with one mark and recapture study finding the average foraging distance to be approximately 663 m.<ref>{{cite journal | author = Walther-Hellwig, K. and R. Frankl | year = 1999 | title = Foraging distances of ''Bombus muscorum'', ''Bombus lapidarius'', and ''Bombus terrestris'' (Hymenoptera, Apidae) | journal = Journal of Insect Behavior | volume = 13 | issue =2 | pages =2000}}</ref> The queen is between 20–22&nbsp;mm long, males range from 14–16&nbsp;mm, and workers from 11–17&nbsp;mm. The latter are characterized by their white-ended abdomens and look (apart from their yellowish bands being darker in direct comparison) just like those of the white-tailed bumblebee, ''[[Bombus lucorum|B. lucorum]]'', a close relative. The queens of ''B. terrestris'' have the namesake [[buff (colour)|buff]]-white [[abdomen]] ("tail") tip; this area is white like in the workers in ''B. lucorum.''<ref name ="bee"/> ''B. terrestris'' are unique compared to other bees in that their caste of workers exhibits a wide variation in worker size with thorax sizes ranging from 2.3 to 6.9&nbsp;mm and masses ranging from 68 to 754&nbsp;mg.<ref name = "Goulson"/>
+''B. terrestris'' are pollen-storing bees that generally feed and forage on nectar and pollen.<ref name = "Goulson">{{cite journal | author = Goulson, D., J. Peat, J. C. Stout, J. Tucker, B. Darvill, L. C. Derwent, and W. O. H. Hughes | year = 2002 | title = Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? | journal = Animal Behaviour | volume = 64 | pages = 123–130}}</ref> These bees can navigate their way back to the nest from a distance as far away as {{convert|13|km|mi|abbr=on}}, although most forage within 5&nbsp;km of their nest.<ref>{{cite news |url=http://news.bbc.co.uk/1/hi/sci/tech/5215022.stm |title=Homing instinct of bees surprises |publisher=[[BBC News]] |date=July 26, 2006 |author=Louisa Cheung}}</ref> One mark and recapture study found their average foraging distance to be approximately 663 m.<ref>{{cite journal | author = Walther-Hellwig, K. and R. Frankl | year = 1999 | title = Foraging distances of ''Bombus muscorum'', ''Bombus lapidarius'', and ''Bombus terrestris'' (Hymenoptera, Apidae) | journal = Journal of Insect Behavior | volume = 13 | issue =2 | pages =2000}}</ref> The queen is between 20–22&nbsp;mm long, males range from 14–16&nbsp;mm, and workers from 11–17&nbsp;mm. The latter are characterized by their white-ended abdomens and look just like workers of the white-tailed bumblebee, ''[[Bombus lucorum|B. lucorum]]'', a close relative, apart from the yellowish bands of ''B. terrestris'' being darker in direct comparison. The queens of ''B. terrestris'' have the namesake [[buff (colour)|buff]]-white [[abdomen]] tip ("tail"); this area is white like in the workers in ''B. lucorum.''<ref name ="bee"/> ''B. terrestris'' are unique compared to other bees in that their caste of workers exhibit a wide variation in worker size, with thorax sizes ranging from 2.3 to 6.9&nbsp;mm in length and masses ranging from 68 to 754&nbsp;mg.<ref name = "Goulson"/>
 ==Distribution and Habitat==
-''B. terrestris'' is most commonly found throughout Europe and generally occupies temperate climates. Because it can survive in a wide variety of habitats, there are populations in the near East, the Mediterranean Islands, and Northern Africa as well.<ref name = "Widmer"/> Nests are usually found underground, such as in abandoned rodent dens.<ref name = "Inoue">{{cite journal |author =Inoue, M.K., J. Yokoyama, and I. Washitani | year = 2008 | title = Displacement of Japanese native bumblebees by the recently introduced ''Bombus terrestris'' (L.) (Hymenoptera: Apidae) | journal = Journal of Insect Conservation | volume = 12 | pages = 135–146 }}</ref><ref name = "Dornhaus">{{cite journal | author = Dornhaus, A. and L. Chittka | year = 2001 | title = Food alert in bumblebees (''Bombus terrestris''): possible mechanisms and evolutionary implications | journal = Behavioral Ecology and Sociobiology | volume = 50 | pages = 570–576}}</ref> Colonies form comb-like nest structures with eggcells, each containing several eggs. The queen will layer these eggcells on top of one another. Colonies produce between 300-400 bees on average with a large variation in the number of workers.<ref name="Duchateau"/>
+''B. terrestris'' is most commonly found throughout Europe and generally occupies temperate climates. Because it can survive in a wide variety of habitats, there are populations in the near East, the Mediterranean Islands, and Northern Africa as well.<ref name = "Widmer"/> Nests are usually found underground, such as in abandoned rodent dens.<ref name = "Inoue">{{cite journal |author =Inoue, M.K., J. Yokoyama, and I. Washitani | year = 2008 | title = Displacement of Japanese native bumblebees by the recently introduced ''Bombus terrestris'' (L.) (Hymenoptera: Apidae) | journal = Journal of Insect Conservation | volume = 12 | pages = 135–146 }}</ref><ref name = "Dornhaus">{{cite journal | author = Dornhaus, A. and L. Chittka | year = 2001 | title = Food alert in bumblebees (''Bombus terrestris''): possible mechanisms and evolutionary implications | journal = Behavioral Ecology and Sociobiology | volume = 50 | pages = 570–576}}</ref> Colonies form comb-like nest structures with egg cells each containing several eggs. The queen will layer these egg cells on top of one another. Colonies produce between 300-400 bees on average, with a large variation in the number of workers.<ref name="Duchateau"/>
 ==Colony Cycle==
-A solitary queen hatched from her abandoned colony will initiate the colony cycle when she mates with a male and finds a nest, after which she will lay a small batch of [[Ploidy|diploid]] eggs. Once these hatch, she tends the larvae, feeding them with nectar and pollen. When the larvae are grown, they pupate, and about two weeks later, the first worker bumblebees emerge. This is known as the initiation phase of the colony.<ref name="Duchateau"/> Workers will forage for nectar and pollen for the colony and tend later generations of larvae. The workers are smaller than the queen and only live for a few weeks. The foraging range and frequency of workers depends on the quality and distribution of available food, but most workers forage within a few hundred meters of their nest.<ref>{{cite journal | author = Stephan Wolf & Robin F. A. Moritz | title = Foraging distance in ''Bombus terrestris'' L. (Hymenoptera: Apidae) | journal =[[Apidologie]] | volume = 39 | issue = 4 | pages = 419–427 | publisher = EDP Sciences | year = 2008 | url = http://www.apidologie.org/articles/apido/abs/2008/04/m07103/m07103.html |doi=10.1051/apido:2008020}}</ref>
+A solitary queen hatched from her abandoned colony initiates the colony cycle when she mates with a male and finds a nest, after which she lays a small batch of [[Ploidy|diploid]] eggs. Once these hatch, she tends the larvae, feeding them with nectar and pollen. When the larvae are grown, they pupate, and about two weeks later, the first workers emerge. This is known as the initiation phase of the colony.<ref name="Duchateau"/> Workers will forage for nectar and pollen for the colony and tend later generations of larvae. The workers are smaller than the queen and only live for a few weeks. The foraging range and frequency of workers depends on the quality and distribution of available food, but most workers forage within a few hundred meters of their nest.<ref>{{cite journal | author = Stephan Wolf & Robin F. A. Moritz | title = Foraging distance in ''Bombus terrestris'' L. (Hymenoptera: Apidae) | journal =[[Apidologie]] | volume = 39 | issue = 4 | pages = 419–427 | publisher = EDP Sciences | year = 2008 | url = http://www.apidologie.org/articles/apido/abs/2008/04/m07103/m07103.html |doi=10.1051/apido:2008020}}</ref>
-This first phase can last a variable amount of time in ''B. terrestris'', after which the switch point is reached and the queen begins to lay some unfertilized eggs, which develop into male bees.<ref name="Duchateau"/> When the male drones emerge from the nest, they do not return, foraging only for themselves. They seek out new queens and mate with them. Remaining diploid eggs receive extra food and pupate to become new queens, though the queen can use pheromones to discourage to some extent  the workers' inclination to invest more in larvae around this time, thereby ensuring that not too many become queens. The colony persists until the competition point is reached, when workers begin egg laying. At this point, outright aggression among workers and between workers and the queen begins. This is a very predictable point that occurs at about 30 days into the colony cycle.<ref name="Duchateau"/>
+This first phase can last a variable amount of time in ''B. terrestris'', after which the switch point is reached and the queen begins to lay some unfertilized eggs, which develop into males.<ref name="Duchateau"/> When the male drones emerge from the nest, they do not return, foraging only for themselves. They seek out new queens and mate with them. Remaining diploid eggs receive extra food and pupate to become new queens. The queen can use pheromones to discourage the workers' inclination to invest more in these larvae, thereby ensuring that not too many become queens. The colony persists until the competition point is reached, when workers begin egg laying. At this point, outright aggression among workers and between the queen and workers begins. This is a predictable time point that occurs about 30 days into the colony cycle.<ref name="Duchateau"/>
-Usually the worker-queen conflict will force the queen out and the new workers will become queenless. A "false queen" might take control of the colony for a short period.<ref name = "Honk">{{cite journal | author = van Honk, C. and P. Hogeweg | year = 1981 | title = The ontogeny of the social structure in a captive Bombus terrestris colony | journal = Behavioral Ecology and Sociobiology | volume = 9 | issue = 2 | pages = 111–119}}</ref> The colony cycle starts again when the newly hatched queens leave the nest in search of a mate and a nest for themselves to start a new colony.
+Usually, the worker-queen conflict will force the queen out and the new workers will become queenless. A "false queen" might take control of the colony for a short period.<ref name = "Honk">{{cite journal | author = van Honk, C. and P. Hogeweg | year = 1981 | title = The ontogeny of the social structure in a captive Bombus terrestris colony | journal = Behavioral Ecology and Sociobiology | volume = 9 | issue = 2 | pages = 111–119}}</ref> The colony cycle starts again when the newly hatched queens leave the nest in search of a mate and a nest for themselves in order to start a new colony.
 ==Reproductive Behavior==
@@ Line 41: / Line 41: @@
 ===Mating System===
-''B. terrestris'' is thought mainly to be a singly mating species. This is unusual for social insect queens where mating with several males ([[polyandry]]) has potential genetic benefits.<ref name = "Baer">{{cite journal | author = Baer, B. and P. Schmid-Hempel | year = 2001 | title = Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, ''Bombus terrestris'' | journal = Evolution | volume = 55 | issue = 8 | pages = 1639–1643 }}</ref> The lack of multiple matings by ''B. terrestris'' queens may be partly caused by male interference. ''B. terrestris'' males plug the female's sexual tract with a sticky secretion during mating, which appears to reduce the female's ability to successfully mate with other males for several days.<ref>{{cite journal | author=Annette Sauter, Mark J. F. Brown, Boris Baer & Paul Schmid-Hempel | year=2001 |title=Males of social insects can prevent queens from multiple mating |journal=[[Proceedings of the Royal Society B]] |volume=268 |issue=1475 |pages=1449–1454 |doi=10.1098/rspb.2001.1680 |pmid=11454287 |pmc=1088762}}</ref> While there may be genetic fitness benefits in colony [[heterogeneity]] from a polyandrous mating system, bumblebees are also likely monandrous due to social constraints and risks associated with multiple matings. Finding multiple mates might be energetically costly and expose the queen to higher predation risks. Additionally, while queens may prefer multiple matings to ensure more genetic variability and viable offspring, the queen-worker conflict dictates that workers will be more apt to raise larvae from a single male.<ref name = "Baer"/> This is due to [[haplodiploidy]] in Hymenopteran social insects in which males (drones) are haploid and females (workers and queens) are diploid. This confers greater genetic similarity between sister workers (75%) than between mother and offspring (50%), making kin selection stronger between sisters. This selective force would be reduced if workers were the offspring of multiple males, which might lead to increased conflict in the nest.
+''B. terrestris'' is thought to be a singly mating species. This is unusual for social insect queens because mating with several males ([[polyandry]]) has potential genetic benefits.<ref name = "Baer">{{cite journal | author = Baer, B. and P. Schmid-Hempel | year = 2001 | title = Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, ''Bombus terrestris'' | journal = Evolution | volume = 55 | issue = 8 | pages = 1639–1643 }}</ref> The lack of multiple matings by ''B. terrestris'' queens may be partly due to male interference. ''B. terrestris'' males plug the female's sexual tract with a sticky secretion during mating, which appears to reduce the female's ability to successfully mate with other males for several days.<ref>{{cite journal | author=Annette Sauter, Mark J. F. Brown, Boris Baer & Paul Schmid-Hempel | year=2001 |title=Males of social insects can prevent queens from multiple mating |journal=[[Proceedings of the Royal Society B]] |volume=268 |issue=1475 |pages=1449–1454 |doi=10.1098/rspb.2001.1680 |pmid=11454287 |pmc=1088762}}</ref> While there may be genetic fitness benefits in colony [[heterogeneity]] from a polyandrous mating system, bumblebees are also likely to be monandrous due to social constraints and risks associated with multiple matings. Finding multiple mates might be energetically costly and expose the queen to higher predation risks. Additionally, while queens may prefer multiple matings to ensure more genetic variability and viable offspring, the queen-worker conflict dictates that workers will be more apt to raise larvae from a single male.<ref name = "Baer"/> This is due to [[haplodiploidy]] in Hymenopteran social insects in which males (drones) are haploid and females (workers and queens) are diploid. This confers greater genetic similarity between sister workers (relatedness of 0.75) than between mother and offspring (relatedness of 0.5), making kin selection stronger between sisters. This selective force would be reduced if workers were the offspring of multiple males, which might lead to increased conflict in the nest.
 [[File:Bombus terrestris queen face HC1.jpg|thumb|''B. terrestris'' queen]]
@@ Line 47: / Line 47: @@
 ===Worker Egg Laying===
-In addition to the queen, the workers can lay eggs for the colony brood. Since workers do not mate, all of their eggs are haploid and will develop into drones. There are multiple factors that determine whether a worker bee will obtain a reproductively active fate. Workers born early in the first batch of eggs are more likely to become egg layers due to their increased size and age, which allows more time for ovarian development. Workers usually have to be at least 30 days old to become an egg layer. Individuals that spend less time foraging and more time near the queen are also more likely to become reproductive. Lastly, due to intense competition for the opportunity to reproduce, older workers often harass the queen by attacking her and buzzing loudly. Once this point is reached the colony is usually abandoned.<ref name = "van Honk">{{cite journal | author = van Honk, C.G.J., P.F. Roseler, H.H.W. Velthuis, and J.C. Hoogeveen | year = 1981 | title = Factors influencing the egg laying of workers in a captive ''Bombus terrestris'' colony | journal = Behavioral Ecology and Sociobiology | volume = 9 | pages = 9–14}}</ref>
+In addition to the queen, the workers can lay eggs for the colony brood. Since workers do not mate, all of their eggs are haploid and will develop into drones. There are multiple factors that determine whether a worker bee will become reproductively active. Workers born early in the first brood are more likely to become egg layers due to their increased size and age, which allows more time for ovarian development. Workers usually have to be at least 30 days old to become an egg layer. Individuals that spend less time foraging and more time near the queen are also more likely to become reproductive. Lastly, due to intense competition for the opportunity to reproduce, older workers often harass the queen by attacking her and buzzing loudly. Once this point is reached the colony is usually abandoned.<ref name = "van Honk">{{cite journal | author = van Honk, C.G.J., P.F. Roseler, H.H.W. Velthuis, and J.C. Hoogeveen | year = 1981 | title = Factors influencing the egg laying of workers in a captive ''Bombus terrestris'' colony | journal = Behavioral Ecology and Sociobiology | volume = 9 | pages = 9–14}}</ref>
 ===Sex Ratios===
-Due to the variability in the switch point of ''B. terrestris'' colonies, there are varying levels of sex ratios among nests. Early-switching colonies have a much larger number of males (17.4:1), which may give them a competitive advantage in mating with later emerging queens. Late switching colonies have fewer males and a more even sex ratio of 1.3:1, thus indicating the queen's control over her colony as she would prefer a 1:1 ratio since she is equally related to both sons and daughters. On the other hand, workers would prefer a 1:3 ratio as they are more related to each other than to their mother. Although early and late switching colonies are usually balanced in the population, the overall demographic in this study was found to be male biased, resulting in an overall sex ratio of 4:1, males to females.<ref name="Duchateau"/> However, most studies show that this balance of bimodal sex determination between early and late-switching colonies creates the queen's preferred 1:1 sex ratio in ''B. terrestris'' populations.<ref name = "Bourke">{{cite journal | author = Bourke, A.F.G. and F.L.W. Ratnieks | year = 2001 | title = Kin-selected conflict in the bumble-bee ''Bombus terrestris'' (Hymenoptera: Apidae) | journal = Proceedings of the Royal Society of London B | volume = 268 | pages = 347–355}}</ref> This is unusual for social insects, which usually have a 1:3 sex ratio indicative of worker colony control.
+Due to the variability in the switch point of ''B. terrestris'' colonies, there are varying levels of sex ratios among nests. Early-switching colonies have a much larger number of males compared to workers and queens (17.4:1), which may give them a competitive advantage in mating with later emerging queens. Late-switching colonies have fewer males and a more even sex ratio of 1:3:1, thus indicating the queen's control over her colony (she prefers a 1:1 ratio, since she is equally related to both sons and daughters). On the other hand, workers prefer a 1:3 ratio, as they are more related to each other than to their mother. Although early and late switching colonies are usually balanced in the population, the overall demographic in one study was found to be male biased, resulting in an overall sex ratio of 4:1 (males to females).<ref name="Duchateau"/> However, most studies show that this balance of bimodal sex determination between early and late-switching colonies creates the queen's preferred 1:1 sex ratio in ''B. terrestris'' populations.<ref name = "Bourke">{{cite journal | author = Bourke, A.F.G. and F.L.W. Ratnieks | year = 2001 | title = Kin-selected conflict in the bumble-bee ''Bombus terrestris'' (Hymenoptera: Apidae) | journal = Proceedings of the Royal Society of London B | volume = 268 | pages = 347–355}}</ref> This is unusual for social insects, which usually have a 1:3 sex ratio indicative of worker colony control.
 ===Reproductive Suppression===
@@ Line 61: / Line 61: @@
 ====Worker Suppression====
-While the queen controls much of the egg laying and larval development in the colony, it is likely that workers play a much bigger role in controlling egg laying than previously thought. Dominant workers will often inhibit younger workers from laying eggs.<ref name = "van Honk"/><ref name = "Bloch">{{cite journal | author = Bloch, G. and A. Hefetz | year = 1999 | title = Regulation of reproduction by dominant workers in bumblebee (''Bombus terrestris'') queen right colonies | journal = Behavioral Ecology and Sociobiology | volume = 45 | pages = 125–135}}</ref> Workers have low levels of JH and ovarian development during the early stages of the colony cycle and also after the competition point. Workers introduced into queenright and queenless colonies experience similar levels of inhibition from fellow worker sisters during the competition point, indicating the key role of worker policing of fellow nest mates later in the colony cycle. This suggests that worker reproductive development will be highest between early development and the competition point in the colony.<ref name = "Bloch"/>
+While the queen controls much of the egg laying and larval development in the colony, it is likely that workers play a much bigger role in controlling egg laying than previously thought. Dominant workers will often inhibit younger workers from laying eggs.<ref name = "van Honk"/><ref name = "Bloch">{{cite journal | author = Bloch, G. and A. Hefetz | year = 1999 | title = Regulation of reproduction by dominant workers in bumblebee (''Bombus terrestris'') queen right colonies | journal = Behavioral Ecology and Sociobiology | volume = 45 | pages = 125–135}}</ref> Workers have low levels of JH and ovarian development during the early stages of the colony cycle and also after the competition point. Workers introduced into queenright and queenless colonies experience similar levels of inhibition from fellow workers during the competition point, indicating the key role of worker policing of fellow nest mates later in the colony cycle. This suggests that worker reproductive development will be highest between early development and the competition point in the colony.<ref name = "Bloch"/>
 ==Social and Foraging Behavior==
@@ Line 67: / Line 67: @@
 ===Dominance Hierarchy===
-Workers start out at the bottom of the dominance hierarchy in the social colony. As they age, they move up closer to the position of the queen. Queen-side workers are often egg layers and interact more frequently with the queen. This social position may pay off later, after the competition point is reached. When the queen is overthrown by the aggression of the workers, the most dominant worker will have the best likelihood of contributing more eggs to the colony brood and perhaps climb to the position of “false queen.”  The queen appears to maintain a constant distance of social dominance from her workers at all points in the cycle, suggesting that she is displaced by the sheer number of workers later in the cycle.<ref name = "Honk"/>
+Workers start out at the bottom of the dominance hierarchy in the social colony. As they age, they move closer to the position of queen. Queen-side workers are often egg layers and interact more frequently with the queen. This social position may pay off later, after the competition point is reached. When the queen is overthrown by the aggression of the workers, the most dominant worker will have the best likelihood of contributing more eggs to the colony brood and will perhaps climb to the position of “false queen.”  The queen appears to maintain a constant distance of social dominance from her workers at all points in the cycle, suggesting that she is displaced by the sheer number of workers later in the cycle.<ref name = "Honk"/>
 [[File:Courgette bloem met gewone aardhommel (Cucurbita pepo and Bombus terristris).jpg |thumb|Queen and worker on ''[[Cucurbita pepo]]'' flower]]
@@ Line 79: / Line 79: @@
 ====Food Alert====
-Individuals who return from the nest after a foraging run often recruit other bees in the colony to leave the nest and search for food. In ''B. terrestris'', successful foragers will return to the nest and run around frantically and without a measurable pattern, unlike the ritualized dance of the honeybee. Although the mechanism by which this is an effective recruitment strategy is unclear, it is hypothesized that running around likely spreads a pheromone that encourages other bees to exit and forage by indicating the location and odor of food nearby.<ref name ="Dornhaus"/>
+Individuals who return from the nest after a foraging run often recruit other bees in the colony to leave the nest and search for food. In ''B. terrestris'', successful foragers will return to the nest and run around frantically and without a measurable pattern, unlike the ritualized dance of the honeybee. Although the mechanism by which this recruitment strategy functions is unclear, it is hypothesized that running around likely spreads a pheromone that encourages other bees to exit and forage by indicating the location and odor of food nearby.<ref name ="Dornhaus"/>
 ====Homing Ability====
-''B. terrestris'' has an impressive homing range, where bees displaced from their nests can relocate the colony from up to 9.8&nbsp;km away. However, the return often takes several days indicating ''B. terrestris'' might be utilizing familiar foliage and natural landmarks to find the nest, which may be a tedious process if an individual is outside the conventional foraging range of the nest.<ref>{{cite journal |author = Goulson, D. and J. Stout | year = 2001 | title = Homing ability of the bumblebee ''Bombus terrestris'' (Hymenoptera: Apidae) | journal = Apidologie | volume = 32 | pages = 105–111}}</ref>
+''B. terrestris'' has an impressive homing range, where bees displaced from their nests can relocate the colony from up to 9.8&nbsp;km away. However, the return often takes several days, indicating ''B. terrestris'' might be utilizing familiar foliage and natural landmarks to find the nest. This may be a tedious process if an individual is outside the conventional foraging range of the nest.<ref>{{cite journal |author = Goulson, D. and J. Stout | year = 2001 | title = Homing ability of the bumblebee ''Bombus terrestris'' (Hymenoptera: Apidae) | journal = Apidologie | volume = 32 | pages = 105–111}}</ref>
 ===Learning===
-Bumblebees and honeybees are extremely influenced by innate preferences for blue and yellow color. When they have no training, they will often just visit flowers that naturally attract them. However, it is generally thought that bees will learn to visit more nectar rewarding flowers after experience associates the reward with the color of the petals. This has been demonstrated in ''B. terrestris'' where bees trained on artificially colored flowers will pick a similar color to the one they were trained with when tested with an array of flower choices. Though if individuals were tested with flower colors significantly different than from what they were trained with, they just visited flowers most closely aligned with their innate color preferences.<ref>{{cite journal | author = Gumbert, A | year = 2000 | title = Color choices by bumble bees (''Bombus terrestris''): Innate preferences and generalization after learning | journal = Behavioral Ecology and Sociobiology | volume = 48 | issue = 1 | pages = 36–43 }}</ref> In addition to identifying specific colors for foraging purposes, it has also been shown that young worker bees have to learn complex motor skills in order to efficiently collect nectar and pollen from flowers. These skills might take several days to develop, as memory does not always hold perfectly on a day-to-day basis, sometimes deteriorating overnight.<ref>{{cite journal |author = Raine, N.E. and L. Chittka | year = 2007 | title = Pollen foraging: learning a complex motor skill by bumblebees (''Bombus terrestris'') | journal = Naturwissenschaften | volume = 94 | pages = 459–464 }}</ref>
+Bumblebees and honeybees are extremely influenced by an innate preference for blue and yellow color. When they have no training, they will often just visit flowers that naturally attract them. However, it is generally thought that bees will learn to visit more nectar rewarding flowers after experience associates the reward with the color of the petals. This has been demonstrated in ''B. terrestris,'' where bees trained on artificially colored flowers will pick a similar color to the one they were trained with when tested with an array of flower choices. If individuals were tested with flower colors significantly different than from what they were trained with, they just visited flowers most closely aligned with their innate color preferences.<ref>{{cite journal | author = Gumbert, A | year = 2000 | title = Color choices by bumble bees (''Bombus terrestris''): Innate preferences and generalization after learning | journal = Behavioral Ecology and Sociobiology | volume = 48 | issue = 1 | pages = 36–43 }}</ref> In addition to identifying specific colors for foraging purposes, it has also been shown that young worker bees have to learn complex motor skills in order to efficiently collect nectar and pollen from flowers. These skills might take several days to develop, as memory does not always hold perfectly on a day-to-day basis, sometimes deteriorating overnight.<ref>{{cite journal |author = Raine, N.E. and L. Chittka | year = 2007 | title = Pollen foraging: learning a complex motor skill by bumblebees (''Bombus terrestris'') | journal = Naturwissenschaften | volume = 94 | pages = 459–464 }}</ref>
 ====Limitations on Foraging Precision====
-While bees are highly adept at discrimination tasks, they are still limited by the magnitude of difference needed in hue to properly carry out these tests. Error rates of color recognition go down in ''B. terrestris'' when flower pigments are closer together on the color spectrum. This might have damaging effects on pollination efficiency if bees visit different flower species with similar, but distinct colors, which can only be mediated if the flowers have unique shapes.<ref>{{cite journal |author = Dyer, A.G. and L. Chittka | year = 2004 | title = Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (''Bombus terrestris'') as a case study | journal = Journal of Comparative Physiology A | volume = 190 | pages = 105–114}}</ref>
+While bees are highly adept at discrimination tasks, they are still limited by the magnitude of difference needed in hue to properly carry out these tests. Error rates of color recognition decrease in ''B. terrestris'' when flower pigments are closer together on the color spectrum. This might have damaging effects on pollination efficiency if bees visit different flower species with similar, but distinct colors, which can only be mediated if the flowers have unique shapes.<ref>{{cite journal |author = Dyer, A.G. and L. Chittka | year = 2004 | title = Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (''Bombus terrestris'') as a case study | journal = Journal of Comparative Physiology A | volume = 190 | pages = 105–114}}</ref>
 ====Social Learning====
-While bees often forage alone, experiments demonstrate that young foragers might learn what flowers provide the most nectar more quickly when foraging with older workers. ''B. terrestris'' individuals have a faster learning curve for visiting unfamiliar, yet rewarding flowers when they can see a conspecific foraging on the same species.<ref>{{cite journal | author = Leadbeater, E. and L. Chittka | year = 2007 | title = The dynamics of social learning in an insect model, the bumblebee (''Bombus terrestris'') | journal = Behavioral Ecology and Sociobiology | volume = 61 | issue = 11 | pages = 1789–1796}}</ref> The discovery of this type of associative learning is a novel insight into bee behavior and may supplement learning via color reward association.
+While bees often forage alone, experiments demonstrate that young foragers might learn what flowers provide the most nectar more quickly when foraging with older workers. ''B. terrestris'' individuals have a faster learning curve for visiting unfamiliar, yet rewarding flowers, when they can see a conspecific foraging on the same species.<ref>{{cite journal | author = Leadbeater, E. and L. Chittka | year = 2007 | title = The dynamics of social learning in an insect model, the bumblebee (''Bombus terrestris'') | journal = Behavioral Ecology and Sociobiology | volume = 61 | issue = 11 | pages = 1789–1796}}</ref> The discovery of this type of associative learning is a novel insight into bee behavior and may supplement learning via color reward association.
 [[File:Bombus terrestris 00001.png|thumb]]
@@ Line 107: / Line 107: @@
 ===Worker-Worker Conflict===
-Although ''B. terrestris'' workers are most directly in competition with the queen for egg laying opportunities, they will still inhibit their sisters from laying eggs in order to have their own sons, which they will share the most genes with than their nephews.<ref name = "Bloch"/>
+Although ''B. terrestris'' workers are most directly in competition with the queen for egg laying opportunities, they will still inhibit their sisters from laying eggs in order to have their own sons. This is beneficial to them because they will share more genes with their own son rather than their nephews.<ref name = "Bloch"/>
 ==Parasites and Disease==
@@ Line 113: / Line 113: @@
 ===Effects of Foraging on Resistance===
-Foraging is considered energetically costly and it is possible that individuals that spend more time foraging suffer costs to their overall fitness. For example,'' B. terrestris'' is often vulnerable to parasitism by [[Conopidae|conopid flies]] in Central Europe and it has been hypothesized that foragers might suffer higher incidences of parasites due to the increased metabolic costs of flying. This was demonstrated in a population in which foraging workers had significantly lower levels of encapsulation of an experimental parasitic egg when compared to non-foraging workers. This suggests that foragers have compromised immune systems due increased energetic expenses and might be predisposed to fly parasites.<ref>{{cite journal | author = Konig, C. and P. Schmid-Hempel | year = 1995 | title = Foraging and immunocompetence in workers of the bumblebee, Bombus terrestris L. | journal = Proceedings of the Royal Society of London B | volume = 260 | pages = 225–227}}</ref>
+Foraging is considered energetically costly and it is possible that individuals that spend more time foraging suffer costs to their overall fitness. For example,'' B. terrestris'' is often vulnerable to parasitism by [[Conopidae|conopid flies]] in Central Europe, and it has been hypothesized that foragers might suffer higher incidences of parasites due to the increased metabolic costs of flying. This was demonstrated in a population in which foraging workers had significantly lower levels of encapsulation of an experimental parasitic egg when compared to non-foraging workers. This suggests that foragers have compromised immune systems due to increased energetic expenses and might be predisposed to fly parasites.<ref>{{cite journal | author = Konig, C. and P. Schmid-Hempel | year = 1995 | title = Foraging and immunocompetence in workers of the bumblebee, Bombus terrestris L. | journal = Proceedings of the Royal Society of London B | volume = 260 | pages = 225–227}}</ref>
 ===Effects of Polyandry on Resistance===
-While ''B. terrestris'' is a singly mating species, it might be beneficial to mate with multiple males in a polyandrous system to attain greater genetic variability for resistance against disease. Accordingly, artificially increasing the number of mates a ''B. terrestris'' queen obtains through artificial insemination has shown that the increased genetic variability in her offspring confers greater resistance to the most common bumblebee parasite, ''[[Crithidia]] bombi.'' <ref name = "Baer"/> However, the average reproductive success between one and multiple matings is not linear. Queens that mated once and mated four times had a higher fitness than those that mated twice.<ref name = "Baer"/> This suggests that there might be a fitness barrier to increased matings, which might be why colonies are usually monandrous.
+While ''B. terrestris'' is a singly mating species, a polyandrous system would potentially be beneficial because it would be possible to attain greater genetic variability for resistance against disease. Accordingly, artificially increasing the number of mates a ''B. terrestris'' queen obtains through artificial insemination has shown that the increased genetic variability in her offspring confers greater resistance to the most common bumblebee parasite, ''[[Crithidia]] bombi.'' <ref name = "Baer"/> However, the average reproductive success between one and multiple matings is not linear. Queens that mated once and mated four times had a higher fitness than those that mated twice.<ref name = "Baer"/> This suggests that there might be a fitness barrier to increased matings, which might be why colonies are usually monandrous.
 ===Immunocompetence===
-Surprisingly, the [[immunocompetence]], as measured by the ability to encapsulate a novel antigen, does not vary based on the local environment. Experimental studies demonstrate that ''B. terrestris'' have equal levels of encapsulation in poor and stable environments.<ref name ="Schmid">{{cite journal | author = Schmid-Hempel, R. and P. Schmid-Hempel | year = 1998 | title = Colony performance and immunocompetence of a social insect, ''B. terrestris'', in poor and variable environments | journal = Functional Ecology | volume = 22 | pages = 22–30}}</ref> This is unexpected, because immunity should be compromised in conditions where food supply is low to save energy, but perhaps encapsulation represents an invariable trait of bumblebees or immunity is far too complex to characterize solely based on measurements of encapsulation.
+Surprisingly, the [[immunocompetence]], as measured by the ability to encapsulate a novel antigen, does not vary based on the local environment. Experimental studies demonstrate that ''B. terrestris'' have equal levels of encapsulation in poor and stable environments.<ref name ="Schmid">{{cite journal | author = Schmid-Hempel, R. and P. Schmid-Hempel | year = 1998 | title = Colony performance and immunocompetence of a social insect, ''B. terrestris'', in poor and variable environments | journal = Functional Ecology | volume = 22 | pages = 22–30}}</ref> This is unexpected, because immunity should be compromised in conditions where food supply is low in order to save energy. Perhaps encapsulation represents an invariable trait of bumblebees, or immunity is far too complex to characterize solely based on measurements of encapsulation.
 ===Threats from Disease===
@@ Line 127: / Line 127: @@
 [[File:Deformed Wing Virus in worker bee.JPG |thumb|Honeybee infected with deformed wing virus]]
-[[Deformed wing virus]] (DMV) is normally a [[Apis mellifera|honeybee]] pathogen that results in reduced and crumpled wings, making those individuals inviable. This virus is thought to have spread to ''B. terrestris'' and in 2004 as many as 10% of queen bees bred commercially in Europe were found dead with deformed wings. This was confirmed as DMV when ''B. terrestris'' colonies tested positive for the presence of DMV RNA. This could indicate that DMV is a broad range pathogen among bees or perhaps it has recently been infecting new hosts after transmission from honeybees.<ref>{{cite journal | author = Genersch, E., C. Yue, I. Fries, J. R. de Miranda | year = 2006 | title = Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (''Bombus terrestris'' and ''Bombus pascuorum'') with wing deformities | journal = Journal of Insect Pathology | volume = 91 | pages = 61–63}}</ref>
+[[Deformed wing virus]] (DMV) is normally a [[Apis mellifera|honeybee]] pathogen that results in reduced and crumpled wings, making those individuals inviable. This virus is thought to have spread to ''B. terrestris'' and in 2004 as many as 10% of queen bees bred commercially in Europe were found dead with deformed wings. This was confirmed as DMV when ''B. terrestris'' colonies tested positive for the presence of DMV RNA. This could indicate that DMV is a broad range pathogen among bees, or perhaps it has recently been infecting new hosts after transmission from honeybees.<ref>{{cite journal | author = Genersch, E., C. Yue, I. Fries, J. R. de Miranda | year = 2006 | title = Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (''Bombus terrestris'' and ''Bombus pascuorum'') with wing deformities | journal = Journal of Insect Pathology | volume = 91 | pages = 61–63}}</ref>
 ==Environmental Concerns==
@@ Line 133: / Line 133: @@
 ===Invasive Species===
-While native to Europe, ''B. terrestris'' has been introduced as a greenhouse pollinator into many foreign ecosystems. The presence of B. terrestris is becoming an ecological concern in many communities in which it is not native. It is classified as an "invasive alien species" in Japan.<ref name="Matsumura"/> For example, ''B. terrestris'' has a large niche overlap with local Japanese bee species in flower resources and nest sites. ''B. terrestris'' queens competing for local underground nest sites are displacing ''B. hypocrita sapporoensis''. However, ''B. pseudobaicalensis'', which visits similar flowers, but only forms nests above ground has not seen a rapid decline in population numbers.<ref name = "Inoue"/>
+While native to Europe, ''B. terrestris'' has been introduced as a greenhouse pollinator into many foreign ecosystems. The presence of B. terrestris is becoming an ecological concern in many communities in which it is not native. It is classified as an "invasive alien species" in Japan.<ref name="Matsumura"/> For example, ''B. terrestris'' has a large niche overlap with local Japanese bee species in terms of flower resources and nest sites. ''B. terrestris'' queens competing for local underground nest sites are displacing ''B. hypocrita sapporoensis''. However, ''B. pseudobaicalensis'', which visits similar flowers but only forms nests above ground, has not seen a rapid decline in population numbers.<ref name = "Inoue"/>
 In 2008, the Australian government banned the live import of ''B. terrestris'' into Australia on the grounds that it would present a significant risk of becoming a feral species and thereby present a threat to native fauna and flora.<ref>{{cite web | last = | first = | authorlink = Minister for the Environment, Heritage and the Arts | coauthors = | title = Bumblebee rejected for live import  | work = | publisher = Australian Government | date = 26 October 2008 | url = http://www.environment.gov.au/minister/garrett/2008/mr20081026.html| doi = | accessdate = 1 January 2009 }}</ref> In 2004, this bumblebee was classified as a 'Key Threatening Process' by the Scientific Committee of the New South Wales Department of Environment.<ref>{{cite web |author= Paul Adam | authorlink = | coauthors = | title = Introduction of the large earth bumblebee, ''Bombus terrestris'' - key threatening process listing | work = | publisher = NSW Government | date = February 2004 | url = http://www.environment.nsw.gov.au/determinations/BombusTerrestrisKtpDeclaration.htm | doi = | accessdate = 1 January 2009 }}</ref>
@@ Line 141: / Line 141: @@
 ===Colony Development in Changing Environments===
-In temperate areas, variable climates and environmental conditions occur during changing seasons. Lack of available food due to these unpredictable circumstances can often negatively affect colony growth, reproduction, and resistance to parasites. In poor environments with limited food, the few workers born are smaller than average. However, it appears that ''B. terrestris'' is well adapted to a changing environment considering colony growth is higher under variable feeding conditions. Workers and reproductives are also heavier with a variable food supply when compared to stable food availability. This might indicate an adaptive strategy of increased provisioning to save for days it is hard to find food.<ref name ="Schmid"/>
+In temperate areas, variable climates and environmental conditions occur during changing seasons. Lack of available food due to these unpredictable circumstances can often negatively affect colony growth, reproduction, and resistance to parasites. In poor environments with limited food, the few workers born are smaller than average. However, it appears that ''B. terrestris'' is well adapted to a changing environment, considering colony growth is higher under variable feeding conditions. Workers and reproductives are also heavier with a variable food supply when compared to stable food availability. This might indicate an adaptive strategy of increased provisioning to save for days it is hard to find food.<ref name ="Schmid"/>
 ===Pesticide Exposure===
@@ Line 151: / Line 151: @@
 ===Domestication===
-Since 1987, ''B. terrestris'' has been bred commercially for use as a pollinator for European greenhouse crops, particularly tomatoes—a task which was previously carried out by human hand.<ref name="Matsumura">{{cite journal|last=Matsumura|first=Chizuru |author2=Jun Yokoyama|author3=Izumi Wasitani|date=August 2004|title=Invasion Status and Potential Ecological Impacts of an Invasive Alien Bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) Naturalized in Southern Hokkaido, Japan|journal=Global Environmental Research|publisher=AIRIES|pages=51–66|url=http://www.airies.or.jp/publication/ger/pdf/08-01-06.pdf}}</ref><ref>{{cite web|url=http://www.koppert.com/Pollination/?snsrc=aws_af0698a370efeb5d62f7ead745f106678343564925&snkw=pollination&gclid=COib-bPopqsCFesLtAodzl_7zw|title=Natural pollination|last=Anon|work=Koppert Biological Systems|publisher=Koppert B.V.|accessdate=18 September 2011}}</ref> ''B. terrestris'' has been commercially reared in New Zealand since the early 1990s<ref>Velthuis, H. H. W. and van Doorn, A. (April 2004) 'The breeding, commercialization and economic value of bumblebees.' in B. M. Freitas and J. O. P. Pereira (eds) ''Solitary Bees Conservation, Rearing and Management for Pollination.'' Federal University of Ceara, Brasil, pp. 135-149</ref><ref>http://biobees.co.nz/biology.html</ref> and is now used in at least North Africa, Japan, Korea, and Russia, with the global trade in bumblebee colonies probably exceeding 1 million nests per year.<ref>[[Dave Goulson]] (2010). "Bumblebees. Behaviour, Ecology and Conservation" Oxford University Press.</ref>
+Since 1987, ''B. terrestris'' has been bred commercially for use as a pollinator in European greenhouse crops, particularly tomatoes—a task which was previously carried out by human hand.<ref name="Matsumura">{{cite journal|last=Matsumura|first=Chizuru |author2=Jun Yokoyama|author3=Izumi Wasitani|date=August 2004|title=Invasion Status and Potential Ecological Impacts of an Invasive Alien Bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) Naturalized in Southern Hokkaido, Japan|journal=Global Environmental Research|publisher=AIRIES|pages=51–66|url=http://www.airies.or.jp/publication/ger/pdf/08-01-06.pdf}}</ref><ref>{{cite web|url=http://www.koppert.com/Pollination/?snsrc=aws_af0698a370efeb5d62f7ead745f106678343564925&snkw=pollination&gclid=COib-bPopqsCFesLtAodzl_7zw|title=Natural pollination|last=Anon|work=Koppert Biological Systems|publisher=Koppert B.V.|accessdate=18 September 2011}}</ref> ''B. terrestris'' has been commercially reared in New Zealand since the early 1990s<ref>Velthuis, H. H. W. and van Doorn, A. (April 2004) 'The breeding, commercialization and economic value of bumblebees.' in B. M. Freitas and J. O. P. Pereira (eds) ''Solitary Bees Conservation, Rearing and Management for Pollination.'' Federal University of Ceara, Brasil, pp. 135-149</ref><ref>http://biobees.co.nz/biology.html</ref> and is now used in at least North Africa, Japan, Korea, and Russia, with the global trade in bumblebee colonies probably exceeding 1 million nests per year.<ref>[[Dave Goulson]] (2010). "Bumblebees. Behaviour, Ecology and Conservation" Oxford University Press.</ref>
 ===Agriculture===
-''B. terrestris'' are key commercial pollinators in Europe, which has driven researchers to investigate the influence of agricultural land on the foraging and survival of this species. Monoculture reduces biodiversity in farmland areas and likely decreases the number of flowering species bees can forage on. ''B. terrestris'' bees consequently exhibit greater nest growth in suburban areas than in farmland, because local suburban gardens promote more plant diversity for bees to feed from. Agriculture has a profound impact on many bumblebees and is causing widespread decline in several species. However, ''B. terrestris'' is still widespread, likely because it can forage at very long distances, making it less sensitive to changes in biodiversity and the environment.<ref>{{cite journal | author = Goulson, D., W.O.H. Hughes, L.C. Derwent, and J.C. Stout | year = 2002 | title = Colony growth of the bumblebee, ''Bombus terrestris'', in improved and conventional agricultural and suburban habitats | journal = Oecologia | volume = 130 | pages = 267–273}}</ref>
+''B. terrestris'' are key commercial pollinators in Europe, which has driven researchers to investigate the influence of agricultural land on the foraging and survival of this species. Monoculture reduces biodiversity in farmland areas and likely decreases the number of flowering species bees can forage on. ''B. terrestris'' consequently exhibits greater nest growth in suburban areas than in farmland, because local suburban gardens promote more plant diversity for bees to feed from. Agriculture has a profound impact on many bumblebees and is causing widespread decline in several species. However, ''B. terrestris'' is still widespread, likely because it can forage at very long distances, making it less sensitive to changes in biodiversity and the environment.<ref>{{cite journal | author = Goulson, D., W.O.H. Hughes, L.C. Derwent, and J.C. Stout | year = 2002 | title = Colony growth of the bumblebee, ''Bombus terrestris'', in improved and conventional agricultural and suburban habitats | journal = Oecologia | volume = 130 | pages = 267–273}}</ref>
 ==References==