Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Bombus terrestris
(bumble bee)

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Datasheet

Bombus terrestris (bumble bee)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Host Animal
  • Preferred Scientific Name
  • Bombus terrestris
  • Preferred Common Name
  • bumble bee
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • This species is native to the western Palaearctic region (central and southern Europe, North Africa, Madeira and the Canary Islands, east to Afghanistan). It is found in all the countries around the Mediterranean Sea...

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Pictures

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PictureTitleCaptionCopyright
Bombus terrestris, the 'buff-tailed bumblebee', feeding on an introduced and invasive thistle flower (Cirsium vulgare). Lillydale, northern Tasmania, December 2010.  Bumble bees are introduced pests in Tasmania and tend to pollinate a range of European invasive weeds, as per the thistle in the picture.
TitleAdult on a thistle flower head
CaptionBombus terrestris, the 'buff-tailed bumblebee', feeding on an introduced and invasive thistle flower (Cirsium vulgare). Lillydale, northern Tasmania, December 2010. Bumble bees are introduced pests in Tasmania and tend to pollinate a range of European invasive weeds, as per the thistle in the picture.
CopyrightSabine T. Perrone/BSASP Pty. Ltd.
Bombus terrestris, the 'buff-tailed bumblebee', feeding on an introduced and invasive thistle flower (Cirsium vulgare). Lillydale, northern Tasmania, December 2010.  Bumble bees are introduced pests in Tasmania and tend to pollinate a range of European invasive weeds, as per the thistle in the picture.
Adult on a thistle flower headBombus terrestris, the 'buff-tailed bumblebee', feeding on an introduced and invasive thistle flower (Cirsium vulgare). Lillydale, northern Tasmania, December 2010. Bumble bees are introduced pests in Tasmania and tend to pollinate a range of European invasive weeds, as per the thistle in the picture.Sabine T. Perrone/BSASP Pty. Ltd.

Identity

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Preferred Scientific Name

  • Bombus terrestris (Linnaeus, 1758)

Preferred Common Name

  • bumble bee

Other Scientific Names

  • Apis terrestris Linnaeus, 1758
  • Bombus audax Harris, 1776
  • Bombus canariensis Pérez, 1895
  • Bombus maderensis Erlandsson, 1979
  • Bombus terreftris Linnaeus, 1758

International Common Names

  • English: large earth bumble bee

Local Common Names

  • France: le bourdon terrestre
  • Germany: Dunkle Erdhummel
  • UK: buff tailed bumble bee; buff tailed bumblebee; buff-tailed humble-bee; bumblebee

Summary of Invasiveness

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This species is native to the western Palaearctic region (central and southern Europe, North Africa, Madeira and the Canary Islands, east to Afghanistan). It is found in all the countries around the Mediterranean Sea except Egypt (Rasmont et al., 2008) and extends to the north up to the latitude of Helsinki and east to Altai (Pekkarinen and Kaarnam, 1994). Bumble bees are highly valued pollinators worldwide and substantially add to the value of crop production (Goulson, 2003a). B. terrestris has been introduced into New Zealand (e.g. Gurr, 1957; MacFarlane and Gurr, 1995), Tasmania (Cardale, 1993; Stout and Goulson, 2000), Brazil (Thorp, 2003), Chile (Torretta et al., 2006), Mexico (Stout and Goulson, 2000; Winter et al., 2006), and Japan (Washitani, 1998; Inoue et al., 2008). It appears that it was also introduced into mainland Australia (New South Wales) without persisting (W. Froggatt in Franklin, 1913). Recently it has spread from Chile to Argentina (Torretta et al., 2006).

B. terrestris is not considered invasive in its ‘native’ range. Following recent establishment, B. terrestris is considered by some to be invasive in Japan and Tasmania, Australia (which has no native bumble bees) (Winter et al., 2006; Hingston, 2006; Ings et al., 2006). Australia, USA and Canada are prohibiting the import of B. terrestris. China, South Africa, the Canary Islands and Norway, do not allow B. terrestris to be imported either (Velthuis and van Doorn, 2006; Winter et al., 2006); the Japanese government has included B. terrestris in its Invasive Alien Species Act (Velthuis and van Doorn, 2006). In New South Wales (Australia), the alteration of natural pollination dynamics caused by the presence of B. terrestris in other countries has prompted its listing as a “Key Threatening Process”, and in Victoria, Australia, it is listed as a “Potentially Threatening Process”, and B. terrestris importation is also prohibited in all states.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Hymenoptera
  •                         Family: Apidae
  •                             Genus: Bombus
  •                                 Species: Bombus terrestris

Notes on Taxonomy and Nomenclature

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B. terrestris is the most intensely studied non-Apis bee. It is one of the most abundant and widespread bumble bee species in the western Palaearctic. It is a geographically variable species with a wide distribution in Europe, the near east and northern Africa, the Mediterranean Islands, Canary Islands and Madeira. It is now widely domesticated and large numbers of colonies from different subspecies are transported from country to country (Velthuis, 2002). This leads to more and more mixing between populations (Ings et al., 2005b).

Based on morphological and coat colour pattern differences, species and subspecies have been recognized. B. terrestris,Bombus maderensis and Bombus canariensis have been regarded both as conspecific and as separate species. Erlandsson (1979) argued that the dark individuals from the Canary Islands, previously placed within B. terrestris by, for example Krüger (1954; 1956), are a separate species; B. canariensis. Erlandsson in turn, argued that individuals from Madeira, previously placed within B. terrestris by Bischoff (1937), are a separate species; B. maderensis. Rasmont (1984) also regards these three taxa as separate species, but Pekkarinen and Kaarnam (1994) treat them as conspecific. Work by Estoup et al. (1996) has found that although mainland populations do not vary significantly among themselves in mitochondrial genes, all island populations studied show significant differences from the mainland populations. Other characteristics, including coat colour, behaviour and learning performance, led Rasmont et al. (2008) and Coppée et al. (2008) to differentiate several subspecies of B. terrestris.

Description

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Bumble bees are social insects (eusocial), and the vast majority have an annual life cycle. Mated queens emerge from hibernation in the spring, and attempt to found a nest in which they rear daughter workers. In optimum conditions, the number of workers may reach 300 to 500 in some species by mid-summer, when new queens and males are reared. These leave the and nest, mate and the new queens enter hibernation, while the rest of the population dies off. B. terrestris form annual colonies and new colonies are initiated each spring by mated solitary queens (Goulson, 2003b). In warmer areas, colonies may reach large sizes, with colonies of more than 1000 individuals being recorded in Tasmania (Buttermore, 1997).

Distribution

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B. terrestris is widely distributed in the western Palaearctic region. Its distribution is typically Mediterranean, extending from the Canary Islands in the west, to the Altai in the East, and from the Anti-Atlas Mountains of Morocco in the south to southern Finland in the north (Rasmont, 1983; Estoup et al., 1996; Rasmont et al., 2008). B. terrestris is found to the latitude of Helsinki and east to the Altai, from ca. 30° to 60° N (Pekkarinen and Kaarnam, 1994). It is not found in Egypt and is absent from high alpine levels, the deserts and the arid, sub-desertic steppes (Rasmont et al., 2008). Within its wide distribution, there are important subspecific differences in morphological characters (e.g. coat colour and behaviour, learning performance), which underline the genetic differentiation among subspecies (Coppée et al., 2008).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentNativeRasmont et al., 2008
AzerbaijanPresentNativeRasmont et al., 2008
Georgia (Republic of)PresentNativeRasmont et al., 2008
IranPresentNativeRasmont et al., 2008In the north
IsraelPresentNativeVelthuis, 2002
JapanPresentIntroduced Invasive Washitani and Matsumura, 1998; Inoue et al., 2008
KazakhstanPresentNativeRasmont et al., 2008
LebanonPresentNativeRasmont et al., 2008
PakistanPresentNativeRasmont et al., 2008
SyriaPresentNativeRasmont et al., 2008
TurkeyPresentNativeVelthuis, 2002
UzbekistanPresentNativeRasmont et al., 2008

Africa

AlgeriaPresentNativeRasmont et al., 2008
LibyaPresentNativeRasmont et al., 2008
MoroccoPresentNativeRasmont et al., 2008
Spain
-Canary IslandsPresentIntroducedWidmer et al., 1998

North America

MexicoPresentIntroducedStout and Goulson, 2000; Flanders et al., 2003; Winter et al., 2006Shipments into Jalisco in 1995 and 1996 for greenhouse tomato pollination

South America

ArgentinaPresentIntroducedTorretta et al., 2006
BrazilPresentIntroducedCosta and Lordello, 1988; Thorp, 2003
ChilePresentIntroducedTorretta et al., 2006Introduced for pollination

Europe

AlbaniaPresentNativeRasmont et al., 2008
AndorraPresentNativeRasmont et al., 2008
AustriaPresentNativeRasmont et al., 2008
BelgiumPresentNativeRasmont et al., 2008
BulgariaPresentNativeEstoup et al., 1996
CroatiaPresentNativeRasmont et al., 2008
CyprusPresentNativeRasmont et al., 2008
Czech RepublicPresentNativeRasmont et al., 2008
Czechoslovakia (former)PresentNativeRasmont et al., 2008
DenmarkPresentNativeRasmont et al., 2008
EstoniaPresentNativeRasmont et al., 2008
FinlandPresentPekkarinen and Kaarnam, 1994
FrancePresentNativeEstoup et al., 1996
-CorsicaPresentNativeEstoup et al., 1996
GermanyPresentNativeRasmont et al., 2008
GreecePresentNativeEstoup et al., 1996
HungaryPresentNativeRasmont et al., 2008
IcelandPresentNativeHanley-Nicholls, 2008
IrelandPresentNativeRasmont et al., 2008
ItalyPresentNativeEstoup et al., 1996
LatviaPresentNativeRasmont et al., 2008
LiechtensteinPresentNativeRasmont et al., 2008
LithuaniaPresentNativeRasmont et al., 2008
LuxembourgPresentNativeRasmont et al., 2008
MacedoniaPresentNativeRasmont et al., 2008
MaltaPresentNativeRasmont et al., 2008
MoldovaPresentNativeRasmont et al., 2008
MonacoPresentNativeRasmont et al., 2008
MontenegroPresentNativeRasmont et al., 2008
NetherlandsPresentNativeRasmont et al., 2008
NorwayPresentNativeRasmont et al., 2008
PolandPresentNativeEstoup et al., 1996
PortugalPresentNativeRasmont et al., 2008
-MadeiraPresentIntroducedWidmer et al., 1998Could be a subspecies
RomaniaPresentNativeRasmont et al., 2008
Russian FederationPresentPresent based on regional distribution.
-Central RussiaPresentNativeRasmont et al., 2008
-Southern RussiaPresentNativeRasmont et al., 2008
San MarinoPresentNativeRasmont et al., 2008
SerbiaPresentNativeRasmont et al., 2008
SlovakiaPresentNativeRasmont et al., 2008
SloveniaPresentNativeRasmont et al., 2008
SpainPresentNativeEstoup et al., 1996
SwedenPresentNativeRasmont et al., 2008
SwitzerlandPresentNativeEstoup et al., 1996
UKPresentNativeRasmont et al., 2008
UkrainePresentNativeRasmont et al., 2008
Yugoslavia (former)PresentNativeRasmont et al., 2008
Yugoslavia (Serbia and Montenegro)PresentNativeRasmont et al., 2008

Oceania

AustraliaPresentPresent based on regional distribution.
-TasmaniaPresentCardale, 1993; Semmens et al., 1993; Stout and Goulson, 2000
New ZealandPresentIntroduced Invasive Hopkins, 1914; Gurr, 1957; MacFarlane and Gurr, 1995

History of Introduction and Spread

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(Several subspecies of) B. terrestris has been introduced in many countries as a pollinator of greenhouses crops such as tomatoes and peppers. It has escaped from the greenhouses and formed feral populations in several countries where it has been exported to. In Israel, Dafni and Shmida (1996) reported that the numbers of honeybees and solitary bees declined during the last two decades on Mt. Carmel where the range of B.terrestris had expanded. In New Zealand [?], where it has been introduced and where conditions are similar to its native environment, B. terrestris has demonstrated a rapid rate of range expansion up to 90 kilometers per year (Hopkins, 1914). Everywhere it has been introduced, it is competing with native pollinators for nest sites and food resources, leading to a decrease of many native species (Hingston and McQuillan, 1998; 1999; Dafni and Schmida, 1996; Dafni, 1998; Hergstrom et al., 2002; Matsumura et al., 2004; Hingston, 2005; 2006; Inoue et al., 2007). In Britain, where the south-eastern European subspecies Bombus terrestris dalmitinus is imported each year in large quantities (Ings et al., 2006), there is a great risk of competition with the endemic Bombus terrestris audax. There is a high risk of introduction and transmission of parasites (Ings et al., 2005a) and out-competition, particularly because the introduced subspecies has superior foraging efficiency and reproductive rate (Ings et al., 2006).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Argentina Chile   Intentional release (pathway cause) Yes Torretta et al. (2006)
Chile Europe 1998 Intentional release (pathway cause) Yes Ruz (2002); Ruz and Herrera (2001) Ssp. audax
Israel Europe 1960s Intentional release (pathway cause) Yes Dafni (1998) Escaped from glasshouses
Japan Europe 1991 Intentional release (pathway cause) Yes Inari et al. (2005); Inoue et al. (2007); Matsumura et al. (2004); Nagamitsu et al. (2007) Ssp. terrestris and ssp. dalmatinus
Mexico Europe 1995 & 1996 Intentional release (pathway cause) Yes Flanders et al. (2003) Escaped from glasshouses
New Zealand England and Wales  1875 Intentional release (pathway cause) Yes Dumbleton (1949); Goulson and Hanley (2004); Gurr (1964); Hopkins (1914); MacFarlane and Gurr (1995) Subspecies Bombus audax
Tasmania 1992 Intentional release (pathway cause) Yes Buttermore (1997); Hingston et al. (2001); Semmens et al. (1993) Feral population of ssp. audax discovered near Hobart

Risk of Introduction

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There are other dangers associated with commercial trafficking of bumble bees. B. terrestris is now naturalised in several countries where it was first introduced for pollination of greenhouse crops. There are substantiated concerns regarding possible competitive effects of this species on native bumble bees and other native pollinators, which may in turn reduce the reproductive capacity of native plants (Hingston et al., 2002). Studies have shown that B. terrestris has four times the reproductive output of native species in Japan (Matsumara et al., 2004) and that there are considerable overlaps in forage use and timing of foraging (Inari et al., 2005). Some greenhouses are not secure and a recent study in Canada found that 73% of pollen carried by workers returning to commercial colonies originated from plants outside the greenhouse (Morandin et al., 2001; Whittington and Winston, 2004). B. terrestris was allowed into Mexico in 1995 and 1996 without the knowledge of the USA or Canadian regulatory agencies (Flanders et al., 2003). These bumble bees were infected with the microsporidian Nosema bombi, an internal parasite of bumble bees, prompting the destruction of the colonies intended for Jalisco, Mexico, and a retraction of import permits (Winter et al., 2006). The use of B. terrestris for greenhouse production in Mexico has since been replaced by Bombus impatiens, with up to 55,000 colonies sold per year (Velthuis and van Doorn, 2006), since importation by Koppert de Mexico in 2001 (Martinez Guzman, 2005).

Almost 1 million colonies of primarily B. terrestris and B. impatiens are reared annually in commercial facilities, largely for use in greenhouse tomato production, a multi-billion dollar industry worldwide. They are exported in over 15 countries where they are not native and could escape and naturalize. Moller (1996) identified B. terrestris as potentially highly invasive.

Habitat

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Bumble bees are among the most important pollinators of temperate zone plants because of their diverse body and proboscis sizes, ability to sonicate, dense pile, long activity periods, and adaptability to a wide variety of temperatures and climate types (Winter et al., 2006). Bumble bees are adapted to a diversity of climates and habitats, and are active even when light intensity is low. Due to their relatively large body sizes and dense pile, they are able to continue foraging even at temperatures as low as 10°C and as high as 32°C, with observations of Bombus terrestris dalmatinus at temperatures as low as 2°C (Winter et al., 2006). Their increased motility allows them to continue flower visits for most of the year, unlike honeybees, which are mostly inactive at temperatures below 16°C (Heinrich, 1979). Bumble bees can forage during adverse climatic conditions, even flying during light rain, visiting from 20-50 flowers per minute with high pollination efficiency.

Habitat List

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CategoryHabitatPresenceStatus
Littoral
Coastal areas Principal habitat
Terrestrial-managed
Cultivated / agricultural land Principal habitat
Managed forests, plantations and orchards Principal habitat
Managed grasslands (grazing systems) Secondary/tolerated habitat
Protected agriculture (e.g. glasshouse production) Secondary/tolerated habitat
Rail / roadsides Principal habitat
Urban / peri-urban areas Secondary/tolerated habitat
Terrestrial-natural/semi-natural
Natural forests Principal habitat
Natural grasslands Principal habitat
Riverbanks Principal habitat
Scrub / shrublands Secondary/tolerated habitat

Hosts/Species Affected

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Bumble bees are second only to honeybees as commercial pollinator insects. B. terrestris is a specialist pollinator of a number of European plant species, either because they require a bee of a certain size (e.g. foxglove, Digitalis spp.), weight (e.g. Scotch broom, Cytisus scoparius), or require buzz pollination to release pollen from poricidal anthers (e.g. many Solanaceae). This may facilitate an increase in the abundance and distribution of weed species in countries where European plants have been introduced. The presence of B. terrestris may also disrupt pollination of native plant species (Hingston and McQuillan, 1998).

B. terrestris is a highly polylectic bumble bee collecting from hundreds of different flower species. Rasmont (1988) listed 309 species from France and Belgium alone and Ruszkowski (1971) reports 570 flowers in Poland. In Turkey, Özbek (1997) listed 62 favourite plant taxa, and in Anatolia, Rasmont and Flagothier (1996) listed 29 visited plant species.
 
Bumble bees exhibit a tremendous variation in body size and proboscis length, and forage on a variety of floral resources. Most bumble bees have longer tongues than honeybees, allowing them to reach nectar even in deep, tubular flowers. They also exhibit a distinctive behaviour of sonication, or “buzz pollination”, which vibrates pollen from the poricidal anthers of plants such as tomatoes (Buchmann, 1983). This is why they have been chosen for greenhouse pollination of Solanaceae crops (Dag and Kammer, 2001; Morandin et al., 2001). Bumble bees rapidly contract their indirect flight muscles while curled around a tomato flower androecium and transmit vibrations into a flower’s anthers, resulting in rapid pollen ejection from its apical pores. Bumble bees can harvest pollen from “buzzed” tomato flowers 400 times faster than honeybees can. Whereas managed honeybees are also generalists that can pollinate a wide variety of native plants and managed crops, but they are less efficient and more temperature-restricted than bumble bees for many crops (Free and Butler, 1959; Holm, 1966; Alford, 1975; Goulson, 2003b; Pouvreau, 2004; Velthuis and van Doorn, 2006). Due to the honeybees’ inability to use sonication to collect pollen, they are not as useful for tomato pollination (Winter et al., 2006).

Biology and Ecology

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Genetics

Both males and gynes of different (and introduced) populations have the potential to interbreed with native bees (De Jonge, 1986; Chittka and Wells, 2004), resulting in intraspecific hybridization (Olden et al., 2004). Hybridization is threatening the natural genetic diversity of B. terrestris (Widmer et al., 1998) and is also a risk to non-native bees as some of their hybrids can become established, as in Chile (Ruz and Herrera, 2001) and Japan (Matsumura et al., 2004). Due to the production of large numbers of haploid offspring, B. terrestris is particularly amenable to genetic linkage mapping and QTL (quantitative trait loci) studies (Wilfert et al., 2008).
 
The haploid karyotype of B. terrestris comprises 18 chromosomes, two more than those found in the honeybee Apis mellifera (Gadau et al., 2001). The physical genome size has been estimated at 625 Mb (Wilfert et al., 2006). The physical genome size of B. terrestris is, therefore, estimated to be 2.7 times larger than that of A. mellifera (Wilfert et al., 2008).
 
Four independent genetic linkage maps of B. terrestris have been published (see Gadau et al., 2001; Wilfert et al., 2006).
 
Wilfert et al. (2006) used recurring groups of microsatellites and homologous amplified fragment length polymorphism (AFLP) markers to extract a core of 14 homologous linkage groups from the independent linkage maps. The core map can serve as a reference between different mapping populations and experiments. This tool has been used to compare the genetic architecture of host susceptibility and other fitness-relevant traits across different natural populations (Wilfert et al., 2007). For more information see Wilfert et al. (2008).
 
Reproductive Biology
 
Most bumble bees are primitively eusocial; they live in monogynous colonies with reproductive division of labour and have an annual life cycle. The first bumble bees to be seen in spring are the queens – the queen is the only bumble bee to hibernate through the winter. The queen is much bigger than the workers, which appear later. As soon as the queen has found some nectar, to replenish her energy reserves, she starts looking for a suitable site to build her nest. The nest site is usually underground; an abandoned mouse burrow is often used. Inside, the queen first builds a nectar pot, which will sustain her during bad weather. She also begins to build up a pollen larder, which will feed her brood. The queen then lays a small batch of eggs. Once these hatch, she tends the larvae, feeding them with nectar and pollen. When the larvae are fully grown, they pupate, and about 2 weeks later the first worker bumble bees emerge. These workers will forage for nectar and pollen for the colony, and tend later generations of larvae. The queen can now concentrate on egg laying and does not need to leave the nest again. The workers are smaller than the queen, and will only live for a few weeks. The foraging range and frequency of workers depends on the quality and distribution of available forage, but most workers forage within a few hundred metres of their nest. Towards the end of the summer the queen lays some unfertilized eggs, which develop into male bees. Some eggs are also laid that receive extra food and pupate to become new queens. When the males emerge from the nest they do not return, foraging only for themselves. They seek out the new queens and mate with them. B. terrestris is thought to be a mainly singly-mating species. This is unusual for social insect queens where mating with several males (polyandry) has been shown to have several benefits. The lack of multiple mating by B. terrestris queens may be caused by male interference in the process. B. terrestris males plug the female's sexual tract with a sticky secretion during mating, which appears to temporarily reduce the female's ability to successfully mate with other males for several days. When the autumn cold weather sets in, all but the young queens will die. The latter seek out a safe place to hibernate and they are the only ones to survive the winter (Estoup et al. 1996; Schmid-Hempel and Schmid-Hempel, 2000).
 
Environmental Requirements
 
Bumble bees are adapted to a diversity of climates and habitats, and are active even when light intensity is low. Due to their relatively large body sizes and dense pile, they are able to continue foraging even at temperatures as low as 10°C and as high as 32°C, with observations of Bombus terrestris dalmatinus at temperatures as low as 2°C (Winter et al., 2006). Their increased motility allows them to continue flower visits for most of the year, unlike honeybees, which are mostly inactive at temperatures below 16°C (Heinrich, 1979). Bumble bees can forage during adverse climatic conditions, even flying during light rain, visiting from 20-50 flowers per minute with high pollination efficiency. Several species of Bombus, including Bombus affinis, emerge early in the spring and forage into the cool autumn weather of November (Laverty and Harder, 1988). Consequently, many early spring- and late autumn-flowering plants benefit from pollination services provided by members of this hardy genus.

Climate

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ClimateStatusDescriptionRemark
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Means of Movement and Dispersal

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Evidence points to the fact that B. terrestris is able to naturalize easily, even with limited numbers of founding queens (Buttermore et al., 1998) and can spread quickly once introduced. In New Zealand [?], where B. terrestris has been introduced and conditions are similar to its native environment, the bumble bee has demonstrated a rapid rate of range expansion up to 90 kilometers per year (Hopkins, 1914). It maintains higher population densities than semi-social and solitary bees across a broad range of habitats and geographical regions, and is a generalist forager (Goulson, 2003a,b), allowing B. terrestris populations to potentially occupy a wide diversity of niches also used by different species of pollinator (Winter et al., 2006).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Horticulture Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Mail Yes

Impact Summary

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CategoryImpact
Cultural/amenity Positive
Environment (generally) Positive and negative

Economic Impact

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The commercial production of bumble bees has developed into a thriving branch of agribusiness, generating an estimated yearly economic value of US$1.25 billion in pollination services in the USA alone (Ghazoul, 2005). The benefits to growers include reduced costs from not having to pollinate mechanically using shaker tables or by hand with electronic vibrating wands, ease in monitoring bumble bee activity, increased fruit yields, little or no need for pesticides, and improved fruit quality leading to higher sales prices (Velthuis and van Doorn, 2006). Bumble bees, notably several subspecies of Bombus terrestris, have been shipped throughout the world in vast numbers since the late 1980s, and around countries in Europe, where they are now competing with local native populations, leading some to extinction (Goka et al., 2001; Goulson, 2003a). Five species of bumble bees are used commercially, Bombus impatiens and Bombus occidentalis in Northern America, Bombus ignitus and Bombus lucorum in East Asia, and B. terrestris in Europe, South America, Asia, and New Zealand. Commercially-reared bumble bees can escape from greenhouses in relatively large proportions (Morandin et al., 2001) if growers are not cautious in preventing their accidental release. The use of non-native bumble bee species is a major ecological concern as they have been shown to escape and naturalize quickly (Ruz and Herrera, 2001; Hingston et al., 2002; Matsumura et al., 2004; Velthuis and van Doorn, 2006). Introduced pollinators could change the local flora by increasing the pollination rate of exotic weeds, causing increased costs in weed control programmes and threaten native pollinators by increasing competition (Goulson, 2003a,b). Furthermore, imported bumble bees carry parasites that potentially threaten native bumble bee and honeybee populations (Goka et al., 2001), potentially causing even more stress and losses to endemic species and populations.

Environmental Impact

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Worldwide, there are over 250 species of bumble bees (Michener, 2000), which form the monophyletic genus Bombus within the family Apidae (Hymenoptera) (Kawakita et al., 2004). Native bumble bees face threats from introduced parasites and diseases, including Nosema bombi, the microorganism Crithidia bombi, the tracheal mite Locustacarusbuchneri, and hymenopteran brood parasitoids such as Melittobia acasta and Melittobia chalybii, which can be difficult to detect when inspecting commercial colonies and may be spread from commercial to wild colonies by greenhouse production facilities (Winter et al., 2006).

Infected bumble bees can readily transmit intestinal parasites between individuals (Durrer and Schmid-Hempel, 1994). Disease transmission between commercial and wild populations of bumble bees has been demonstrated in field studies (Colla et al., 2006). At least seven species of North American bumble bees have disappeared from much of their native range since the late 1990s and may now be extinct (Thorp, 2005). A study of pathogen spillover from commercial bumble bees to wild populations in Canada demonstrated that N. bombi was three times more prevalent among bumble bees foraging near greenhouses than it was in areas without them (Colla et al., 2006).

In new environments, B. terrestris may threaten populstions of native pollinators not only by introducing new diseases, but also by competing for resources, or by disrupting genetic adaptations by hybridizing with native species.

The use of non-native bumble bee species is a major ecological concern (Velthuis and van Doorn, 2006). Introduced pollinators could change the local flora, e.g., by increasing the pollination rate of exotic weeds, and threaten native pollinators by increasing competition (Goulson, 2003a,b). These concerns are reinforced by results showing that even the introduction of non-native subspecies, such as Bombus terrestris sassaricus from Southern Europe to Western Europe, could lead to the displacement of native bees (Ings et al., 2005a).

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Capable of securing and ingesting a wide range of food
  • Highly mobile locally
  • Fast growing
  • Has propagules that can remain viable for more than one year

Uses List

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Environmental

  • Commercial pollinator

Diagnosis

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Currently in the USA, bumble bee rearing facilities are inspected by national and state veterinary services, but often the importing countries are only prepared to identify diseases and pests affecting honeybees, and regulatory agency personnel may be insufficiently trained or understaffed to handle proper inspection procedures (Velthuis and van Doorn, 2006). Internal parasites affecting bumble bees can be quite difficult to detect, particularly at low levels of infection when colonies may otherwise appear healthy. There are no current international standards for inspection that would prevent the further spread of diseases and parasites (Winter et al., 2006).

Detection and Inspection

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B. terrestris is a relatively large, primitively eusocial bee native to Europe. B. terrestris is generally more heavily built and hairier than the honeybee, Apis mellifera. B. terrestris queens are 30-35 mm long; workers are more variable in size, ranging from 8-22 mm long; and males are similar in size and appearance to large workers. B. terrestris are black with one yellow or ochre band across the front of the thorax and a second yellow or ochre band across the abdomen. The tip of the abdomen is either buff or white.

Note that colour patterning is highly variable within and among Bombus species and subspecies, and cannot be used alone for species identification. Additional genetic analysis is needed to identify specimens at the species level.

Similarities to Other Species/Conditions

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The world bumble bee (Bombus) fauna consists of approximately 250 known species; most of them are found in temperate parts of the northern hemisphere. Several distinct populations occur in the natural range of B. terrestris that show distinct colour and size variations (Chittka et al., 2004; Rasmont et al., 2008). Genetic studies have shown that several distinct subspecies exist, some of which can be considered as distinct species altogether. Examples include populations from Sardinia hosting Bombus terrestris sassaricus, the Canary Islands with Bombus terrestris canariensis, and the British Isles with Bombus terrestris audax (Estoup et al., 1996; Widmer et al., 1998). Rasmont et al. (2008) recognise nine morphological subspecies in B. terrestris: ssp. terrestris; ssp. africanus (North Africa), ssp. audax (British Isles), ssp. calabricus (Italy and Sicily), ssp. canariensis (Canary Islands), ssp. dalmatinus (Balkans, Urals and Asia), ssp. lusitanicus, ssp. sassaricus (Sardinia) and ssp. xanthopus (Corsica). For taxonomic differences and distribution within subspecies see the papers from Widmer et al. (1998); Rasmont et al. (2008); Coppée et al. (2008); the website of the Natural History Museum, London devoted to bumble bees (http://www.nhm.ac.uk/research-curation/research/projects/bombus/bo.html) and Professor David Goulson’s (Stirling University) webpage (http://www.sbes.stir.ac.uk/people/goulson/index.html).

Prevention and Control

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Invasive Species Management

There is no known control of B. terrestris once it has been introduced and/or has escaped in the natural environment. The only management strategy is through exclusion and restriction of importation into new areas or countries where it is not endemic and can impact on the local environment. Currently the best option is to promote the commercial use of native bumble bees within their countries of origin, rather than import the exotic species (B. terrestris) with the potential for damaging consequences. 

Control
 
Successful rearing and use of other species of bumble bees in their native areas, in North America in particular, have shown that alternatives are possible within the world distribution range of bumble bees (Thorp, 2003). Alternatives are being explored in Japan (Ono, 1997) and more recently in Mexico (Winter et al., 2006). It is imperative to promote the commercial use of native bumble bees within their countries of origin, rather than import exotic species, such as B. terrestris, with the potential for damaging consequences.
 
Movement Control
 
In the USA, regulations are in place to restrict the importation of honeybees (import permitted only from Australia, New Zealand and Canada), but not for non-Apis pollinators such as the bumble bees (Winter et al., 2006). Bumble bee queens can be imported provided that they are disease- and parasite-free. Other countries have local (province/state) regulations that permit the movement of certain bee species and bumble bees as long as they are healthy (e.g. Europe, Canada, Mexico).

References

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Links to Websites

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WebsiteURLComment
Natural History Museum, Londonhttp://www.nhm.ac.uk
Stirling University, Biological & Environmental Sciences - Professor David Goulson's webpagehttp://www.sbes.stir.ac.uk/people/goulson/index.html

Contributors

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27/07/10 Original text by:

CRCNPB Australia, CRC for National Plant Biosecurity, Canberra, Australia

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