Free Access
Volume 41, Number 1, January-February 2010
Page(s) 1 - 13
Published online 04 August 2009

© INRA/DIB-AGIB/EDP Sciences, 2010


Biological invasions resulting from the introduction of non-native organisms generate potentially large economic and ecological costs (Pimentel, 2002; Perrings et al., 2005; Pimentel et al., 2005). Despite this, strong economic pressures are driving the introduction of non-native pollinators, particularly honeybees and bumblebees, throughout the world (Delaplane and Mayer, 2000; Thorp 2003; Velthuis and van Doorn, 2006). Given the scale of these introductions, as well as documented population declines in many natural pollinators across the globe (Kearns et al., 1998; Sarospataki et al., 2005; Steffan-Dewenter et al., 2005; Williams, 2005; Biesmeijer et al., 2006), and the potential invasiveness of social insects (Moller, 1996; Schneider et al., 2004), it is surprising that relatively few studies have actually attempted to monitor the establishment and spread of non-native pollinators (Ruz, 2002; Diniz et al., 2003; Matsumura, 2003; Inari et al., 2005; Schmid-Hempel et al., 2007). A common feature of these, and other studies on invasive organisms, is that they concern introduced species. However, the introduction of non-native subspecies (or populations) is more likely to impact on population diversity through hybridisation and introgression, and possibly competitive exclusion (Schneider et al., 2004; Moritz et al., 2005), than the introduction of non-native species.

Bumblebees provide an excellent model system to explore these risks further. After honeybees, bumblebees are the most important species for crop pollination (Delaplane and Mayer, 2000). Furthermore, the trade in bumblebees involves introductions of both non-native species and subspecies (Inari et al., 2005; Hingston, 2006; Ings et al., 2006; Inoue et al., 2008; Rasmont et al., 2008).

One of the most important commercially reared bumblebee species, particularly for the European and Asian markets, is Bombus terrestris (L). Worldwide, nearly one million colonies of B. terrestris are being used by growers each year (Velthuis and van Doorn, 2006). To date, B. terrestris has been imported into over 57 countries, including 16 outside of its native range (Ings, 2007). In fact, B. terrestris has now become established in the wild in at least two of these countries as the result of recent commercial introductions: Japan (Matsumura, 2003; Inari et al., 2005; Inoue et al., 2008) and Chile (Ruz, 2002). B. terrestris also became well established in New Zealand following purposeful introductions during late 19th and early 20th centuries, and more recently has spread into Tasmania, although it is not known whether the latter introduction was intentional or accidental (Schmid-Hempel et al., 2007). Within Europe, the situation is more complex because the commercial trade in B. terrestris involves introduction of non-native subspecies (Ings et al., 2005b; Velthuis and van Doorn, 2006) which could have consequences for the natural population diversity of the species in Europe (Ortiz-Sánchez, 1993; Estoup et al., 1996; Widmer et al., 1998).

There are nine subspecies of B. terrestris found within Europe and N. Africa (Rasmont et al., 2008). The continental (e.g. French and German) and island (e.g. Sardinian) populations are recognised as distinct subspecies because they differ significantly in their genotype (Estoup et al., 1996; Widmer et al., 1998) and phenotype; e.g. coat colour and colour preferences (Chittka et al., 2004), pheromones (Coppée et al., 2008), and behaviourally related traits such as foraging ability (Ings et al., 2005a; Ings et al., 2006). In fact, bumblebee breeders have utilised this diversity during the commercialisation of bumblebees by carefully selecting the best suited subspecies for their breeding programs (Velthuis, 2002; Velthuis and van Doorn, 2006). One of these was B. t. sassaricus Tournier, 1890, which naturally occurs in Sardinia. The initial breeding program was very successful and thousands of colonies of B. t. sassaricus were produced and shipped outside their native range into southern mainland Europe, including southern France, between 1989 and 1996 to pollinate tomatoes (Ings et al., 2005a; Velthuis and van Doorn, 2006). Since then, commercial breeders have largely been producing and exporting B. t. dalmatinus (Velthuis and van Doorn, 2006).

The first step in assessing the potential impacts of introducing non-native subspecies is to determine if they are able to establish themselves in the wild (i.e. establish colonies outside greenhouses) and spread beyond the areas into which they have been directly introduced. The importation of B. t. sassaricus into France provides an excellent opportunity to do this. Although the natural population of B. t. sassaricus is geographically isolated from the mainland French populations, climatic conditions of N. Sardinia and Mediterranean France are quite similar. Furthermore, a comprehensive survey of the bumblebees of France was undertaken by Rasmont (1988) prior to importation of B. t. sassaricus. He established that three subspecies of B. terrestris naturally coexist in southern France: B. t. terrestris (L. 1758), B. t. lusitanicus (Krüger 1956 [= ferrugineus auct. nec. Schmiedeknecht, 1878]) and B. t. dalmatinus Dalla Torre (1882) (Fig. 1). They exhibit the same annual cycle as B. t. sassaricus and B. t. xanthopus (Kriechbaumer, 1870) from Corsica (Ferton, 1901; Krausse, 1910), i.e. they have two generations per year, one in the spring and another in the autumn/winter (Rasmont, 1985; Duhayon and Rasmont, 1993). Finally, distinct differences in coat colour patterns of Sardinian and mainland subspecies (described fully in the methods) allow them to be readily distinguished in the field.

thumbnail Figure 1

The natural distribution of B. terrestris subspecies. The shaded area indicates the range over which B. terrestris occurs and the arrows point to the approximate centres of distribution of the nine subspecies. This figure was reproduced with permission from Rasmont et al. (2008).

Therefore, in this study we use long-term observations of B. terrestris in southern France (covering a 15 year period since the initial importation of B. t. sassaricus) coupled with recent targeted surveys, to track the potential establishment and spread of an introduced non-native bumblebee subspecies.


2.1. Study subspecies

Five subspecies of Bombus terrestris L. occur along the southern coast of France and on the Tyrrhenian islands (Sardinia, Corsica and Elba): B. t. dalmatinus, B. t. terrestris, B. t. lusitanicus, B. t. sassaricus and B. t. xanthopus. The subspecies from the islands show highly distinct colour patterns from those on the mainland (Rasmont et al., 2008). In particular, the Sardinian subspecies of B. terrestris can easily be distinguished from all other subspecies found in southern France. The native French subspecies (B. t. terrestris, B. t. lusitanicus and B. t. dalmatinus) have a black coat with a yellow collar at the front of the thorax, a yellow band on the front of the abdomen (which has a white tip), and black legs (although B. t. lusitanicus has black legs with reddish-brown hair). However, B. t. sassaricus females (workers and queens) have no yellow band on the thorax and the cuticle on their legs is conspicuously reddish-brown. These characters therefore make field identification of B. t. sassaricus easy (Fig. 1). Subspecies of B. terrestris are able to hybridise in the laboratory and in the wild (Rasmont and Adamski, 1996; Rasmont and Quaranta, 1997; Rasmont et al., 2008). We have observed intermediate forms of the three native subspecies in France, indicating that they also hybridise naturally, if infrequently. Coat coloration seems to be controlled by a single locus (Velthuis and van Doorn, 2006) and the red colouration of the legs of B. t. sassaricus is carried forward into hybrids, with 50% of males from hybrid matings and all F1 workers maintaining this character (Chittka and Wells, 2004; Velthuis and van Doorn, 2006).

2.2. Area surveyed

During the course of this study (1988–2004) we surveyed all departments of Continental France adjacent to the Mediterranean, from West to East: Pyrénées-Orientales (Postcode 66), Aude (11), Hérault (34), Gard (30), Bouches-du-Rhône (13), Vaucluse (84), Var (83) and Alpes-Maritimes (06) (see Figs. 25). This area encompasses the entire range of the autumn/winter generation of B. terrestris in continental France (Rasmont, 1985; Duhayon and Rasmont, 1993).

thumbnail Figure 2

Pre 1988 observations of native B. terrestris subspecies in southern France prior to the importation of B. t. sassaricus.

thumbnail Figure 3

Observations of B. terrestris subspecies made between 1988 and 2002. NB. B. t. sassaricus was recorded at four localities (see Fig. 5).

thumbnail Figure 4

Records of B. terrestris subspecies collected during 2004. NB. no B. t. sassaricus were found.

thumbnail Figure 5

Location of B. t. sassaricus records collected between 1993 and 1998.

2.3. Data collection

2.3.1. 1988-2002

Since 1988, PR made ad hoc visits of 1–2 months every year in the Mediterranean region of France (Fig. 3), typically in October, November, December, April, May, July and August. Most of these visits (April, May) involved intensive insect collection by students from the Université de Mons-Hainaut, as part of a Zoology and Ecology field course. The October-November trips were devoted to collecting queens for bumblebee breeding and the December and July observations were part of short collecting excursions during holidays. Bombus terrestris is in aestivation during August in the Mediterranean basin. During this time a total of 7 946 B. terrestris specimens were examined.

2.3.2. Survey of 2004

To follow up previous observations, and determine whether B. t. sassaricus had indeed become established in southern France, extensive searches were carried out in 2004 along the length of the French Mediterranean coastline (Fig. 4), from near Hyères (43° 08’ N 6° 07’ E) in the east to near Perpignan (42° 42’ N 2° 53’ E) in the west. Three visits were made to encompass different generations of B. terrestris. The first visit occurred in May (9th to 20th) to coincide with peak worker activity of the spring generation. A second survey was carried out near Montpellier and Perpignan in October (18th to 21st) to coincide with peak activity of nest founding queens after the first autumn rains. Finally, a return visit to the Montpellier region was made in December (19th to 23rd) to coincide with peak worker activity of colonies founded by the generation of queens observed in October.

During these periods over 100 flower rich sites at 32 locations were monitored by two observers for the presence of bumblebees. A total of 478 B. terrestris specimens were examined. We used either standard bee walks (e.g. Pollard, 1977; Banaszak, 1980) or fixed observations, depending on the habitat type. Bee walks entailed walking slowly (∼ 1 m s−1) along a linear habitat (e.g. roadside verge or flowering hedge) identifying and recording all visible bumblebees (typically within 2 m either side of the transect). For habitats where flowers were in discrete patches (e.g. flowering shrubs), individual patches (typically 4 by 4 m) were observed (10–20 minutes combined observation time per patch – up to 1 hour if bumblebees were detected). All sites were monitored during dry weather. During October and December, all bees were captured and marked, by placing a dot of white correction fluid (Tippex®) on the thorax, to avoid re-recording the same individuals.

When a bumblebee was observed it was scored as a queen, worker or male and identified as non-native B. t. sassaricus (all black thorax and red legs) or native French B. terrestris sl. (yellow banded thorax and black legs). Queens and workers of the native French B. terrestris showing distinct characteristics were further split into subspecies: B. t. terrestris (narrow yellow band on the thorax), B. t. dalmatinus (wide yellow band on its thorax) and B. t. lusitanicus (distinctive reddish-brown hairs on its legs).


3.1. Extensive surveys 1988 to 2002

3.1.1. Before importation of B. t. sassaricus (pre 1989)

The original survey by Rasmont (1988), which occurred largely before the mass import of B. t. sassaricus, revealed the co-occurrence of three native subspecies of B. terrestris (B. t. terrestris, B. t. dalmatinus and B. t. lusitanicus) in the Mediterranean coastal regions of France (Fig. 2). However, although 1 848 individuals (mainly those cited by Rasmont, 1985) were observed (Fig. 2) across all departments (66, 34, 30, 13, 84 and 83), no specimens of B. t. sassaricus were found (mean proportion in population = 0, upper 95% Confidence Interval (Wilson score interval: Newcombe1998) = 0.0021).

3.1.2. During importation of B. t. sassaricus (1989–1996)

During the second survey between 1988 and 2002, a further 7 946 B. terrestris were recorded across all surveyed departments (Fig. 3). The majority of these records (5 626 bees) were from the autumn/winter generation (recorded between September 21 and January 31) and were observed visiting Salpichroa origanifolia (Lam.) Baillon and Arbutus unedo L. A small number of B. t. sassaricus (6 in total between 1991 and 1994) were observed for the first time at three different locations in areas close (< 10 km) to commercial greenhouses (Tab. I, Fig. 5). One of the males observed in 1994 showed characteristics of both B. t. terrestris and B. t. sassaricus.

Table I

Detailed records of all sightings of B. t. sassaricus workers (W), queens (F) and males (M) observed during the 1988–2002 survey period which yielded 7946 sightings of B. terrestris.

3.1.3. After importation of B. t. sassaricus ceased (1998)

In 1998, two years after the last colonies of B. t. sassaricus were imported into France, several B. t. sassaricus workers were observed foraging alongside native subspecies in an isolated garden surrounded by forest close to Gonfaron, Var (Tab. I, Fig. 5) more than 30 km from the nearest commercial greenhouses (which typically occur along the coastal plains). However, despite frequent return visits in all seasons, no more B. t. sassaricus have been recorded at this location.

3.2. Survey of 2004

3.2.1. May

Bumblebee abundance was low in May 2004, with less than 200 B. terrestris being recorded, despite extensive searches being carried out at 75 flower rich patches during good weather. Furthermore, B. terrestris was only recorded at just over half (39 out of 75) of the flower rich patches surveyed (Fig. 4). Most records of B. terrestris were workers (152), although some queens (12) and a few males (7) were seen. All three native subspecies (B. t. terrestris, B. t. lusitanicus, B. t. dalmatinus and various intermediate forms (putative hybrids)) were recorded. However, no B. terrestris sassaricus, or F1 hybrids, were found in a total sample of 171 bees (mean proportion = 0, upper 95% Confidence Interval = 0.022).

3.2.2. October

A large number of queens (135) and a few males (20) of the three native subspecies were observed at six S. origanifolia and two A. unedo sites in October (Fig. 4). About 45% of the 60 queens recorded at the largest S. origanifolia location (Mas de St-Michel, near Aimargue) were B. t. lusitanicus, 33.3% B. t. terrestris and 16.7% B. t. dalmatinus. However, no B. terrestris sassaricus, or F1 hybrids, were found in a total sample of 155 bees (mean proportion = 0, upper 95% Confidence Interval = 0.024).

3.2.3. December

During the final survey in December, B. terrestris was recorded at all of the six locations near Montpellier. Mostly workers (135), a few males (16) and one queen were observed foraging on A. unedo, Erica multiflora L. and Rosmarinus officinalis L. About two thirds of bees recorded were either B. t. terrestris or B. t. dalmatinus (they were not separated on this occasion) with the remaining third being B. t. lusitanicus. However, no B. terrestris sassaricus, or F1 hybrids, were found in a total sample of 152 bees (mean proportion = 0, upper 95% Confidence Interval = 0.025).


This study is one of the first to document the escape, temporary establishment and apparently failed invasion of an imported subspecies. Extensive surveys of southern France carried out during the 1990’s revealed that males and queens (i.e. reproductively active castes) of the commercially imported, non-native subspecies B. t. sassaricus were escaping into the wild. More importantly, by 1998 B. t. sassaricus appeared to have become naturalised in at least one wild area of southern France far from greenhouses. However, in subsequent surveys we were unable to detect the presence of B. t. sassaricus, indicating that it has been unable to persist, possibly through competitive exclusion by the three native subspecies. Alternatively, B. t. sassaricus may be present in very low numbers or its appearance may have become indistinguishable from the other native subspecies as a result of frequent hybridisation.

The structure of B. terrestris populations is complex: insular forms (including B. t. sassaricus and B. t. xanthopus from the Tyrrhenian Islands and B. t. canariensis from the Canary Islands) are significantly genetically differentiated from mainland forms (Estoup et al., 1996; Widmer et al., 1998; Rasmont et al., 2008). Several of the subspecies are able to hybridise, both under laboratory (Ings et al. 2005b) and natural conditions (Rasmont and Adamski, 1996; Rasmont and Quaranta, 1997). Therefore, moving subspecies, especially insular ones, into regions where they are not native could have important implications for the genetic diversity of B. terrestris.

Discovery of both male and queen B. t. sassaricus close to commercial greenhouses in the 1990’s showed that they were escaping in to the wild. B. t. sassaricus will hybridise with B. t. xanthopus in southern Corsica, although hybrids are very rare (Rasmont and Adamski, 1996), so it is conceivable that hybridisation would be a problem in southern France. However, only one male showing mixed characters, i.e. a putative hybrid, was discovered near to greenhouses during this study (Tab. I).

Although low numbers of B. t. sassaricus were observed outside greenhouses, large quantities (thousands) of B. t. sassaricus colonies were used in southern France over 8 years (1989–1996). Release of a few individuals from each colony every year (possibly several times a year) would represent a high propagule pressure, which is known to increase the probability of establishment by alien species (Kolar and Lodge, 2001). Furthermore, B. terrestris appears to be able to establish viable populations from a very small pool of foundress queens (Buttermore et al., 1998). Southern France also provides B. t. sassaricus with suitable habitats containing important biota necessary to sustain its autumn/winter generation. Notably, extensive A. unedo populations, a common food plant for B. t. sassaricus in northern Sardinia (Krausse, 1910), are present in the Massif des Maures to the north-west of Saint Tropez and the Massif de l’Arboussas to the north-west of Montpellier. We therefore expected that B. t. sassaricus should readily become established in southern France.

Our expectations were met to some extent in 1998 when workers of B. t. sassaricus were observed foraging in an isolated area of the Massif des Maures. This observation occurred nearly two years after the importation of B. t. sassaricus ceased, and was more than 30 kilometres from the nearest commercial greenhouses. Clearly B. t. sassaricus had established feral colonies in the region and had persisted for at least 2 years. However, no further observations of B. t. sassaricus, or visible F1 hybrids, have been made since, despite continued visits to the same area and extensive surveys along the south coast of France (between Hyères in the east and Perpignan in the west: Fig. 4). This leads us to ask why no more B. t. sassaricus were seen again.

A problem with surveys is that it is easier to show presence than it is to conclusively show absence. Survey effort, i.e. area covered, observation hours and number of observations is important. In our study, the surveys undertaken between 1988 and 2002, when a few specimens of B. t. sassaricus were observed, covered a larger area and involved many more observations (7 946 compared to 493) than the 2004 survey. It is therefore possible that B. t. sassaricus were missed in the 2004 surveys. Furthermore, low bumblebee densities occurred during the surveys in May 2004: B. terrestris was only recorded at 39 out of 75 suitable habitat patches. This scarcity, which may have been a consequence of the extreme dryness in 2003, might have affected our ability to detect B. t. sassaricus. However, our surveys incorporated areas close to commercial greenhouses, where feral colonies are most likely to be found (Inari et al., 2005), and areas where B. t. sassaricus had previously been recorded (e.g. near Aimargue). The surveys also targeted areas of habitat containing favoured food plants of B. t. sassaricus (e.g. A. unedo in the Massif des Maures and near Montpellier). The surveys in October and December also increased the total area covered and the number of bees identified. Yet, no B. t. sassaricus or its F1 hybrids were seen, even amongst the large number of queens that were recorded near Aimargue. More importantly, the upper estimate for the proportion of B. t. sassaricus present in the population of B. terrestris, i.e. those potentially missed was only 0.8% for the combined 2004 survey.

It is possible that no B. t. sassaricus were found because hybridisation with other subspecies during the last decade has led to loss of the distinctive colouration of B. t. sassaricus. Coat colouration seems to be controlled by a single locus (Velthuis and van Doorn, 2006), so continued mixing with other native subspecies over at least 16 generations (two generations per year) could remove colour variation from the resident population. Yet, the three native subspecies recorded in this study still maintained their natural colour forms despite low levels of hybridisation among subspecies. Therefore, although southern France appears to be a B. terrestris hybrid zone (only B. t. terrestris is present in central and northern France), a reasonably large degree of reproductive isolation must be occurring, for example through non-random mating (Ings et al., 2005b; Coppée et al., 2008). Clearly the only way to fully resolve this issue would be to sample the population of B. terrestris close to historical importation sites and to use molecular techniques to determine subspecies membership and/or presence of hybrids beyond the F1 generation, if it is still possible.

If we conclude, as our data suggest, that B. t. sassaricus was briefly established in the wild in France but was not able to persist as a pure subspecies, we are prompted to ask: why not? B. terrestris has readily become established in several countries outside its native range as result of intentional or accidental introductions (e.g. in New Zealand: Hopkins, 1914; Chile: Ruz, 2002; and Japan: Inari et al., 2005). However, the key difference in these countries is that B. terrestris is a non-native species that may be able to utilise a slightly different niche to native species, whereas in France it is a non-native subspecies which shares a very similar niche to the native subspecies already present. Furthermore, in Tasmania, B. terrestris is able to utilise both native and introduced plants (Hingston, 2005). Thus, niche availability, which is believed to be important in invasion success (Shea and Chesson, 2002; Le Breton et al., 2005), is perhaps a limiting factor in France.

B. t. xanthopus seems to have been able to cross the 33 km distance between the Capraia and the Elba Islands, where it hybridizes with B. t. terrestris (Rasmont and Quaranta, 1997). B. t. sassaricus is easily able to cross the 12 km from Sardinia to Corsica where it hybridises, albeit rarely, with the native Corsican subspecies B. t. xanthopus. However, B. t. sassaricus has not been able to gain a foothold in Corsica, and hybrids are restricted to the southern coast (Rasmont and Adamski, 1996). This suggests that vagrant B. t. sassaricus and hybrid offspring are competitively excluded by the native B. t. xanthopus. Niche overlap between B. t. sassaricus and the three subspecies native to the French mainland is likely to be the same. In contrast, in New Zealand and Tasmania there are no native species of bumblebee, although B. terrestris may have to compete with other native bees for floral resources (Hingston and McQuillan, 1999). Furthermore, it has been suggested that introduced bumblebees in these countries rely heavily on plants introduced from Europe that are not utilised by the native bee fauna (Stout et al., 2002; Goulson and Hanley, 2004).

Our long-term study has documented the brief establishment and apparently failed invasion of a non-native bumblebee subspecies in France. B. t. sassaricus is no longer present, or its population density is negligible in comparison to native subspecies. We conclude that the inability of imported B. t. sassaricus to become properly established in France reflects competitive exclusion by the three native subspecies. However, a number of questions regarding the impact of the release of non-native subspecies into the wild remain open and need to be addressed in the future. In particular, it is necessary to use molecular techniques (e.g. Murray et al., 2008) to confirm that B. t. sassaricus has not disrupted the native subspecies gene pool.


TI was supported by the University of London Central Research Fund (grant CRFT1C7R) and the Natural Environment Research Council (grant NE/D012813/1). LC was supported by a grant from the British Ecological Society (SEPG 2267) and PR was supported by the Belgian Fonds National de la Recherche Scientifique and Fonds de la Recherche Fondamentale et Collective (mainly grant 2.4.564.06.F). We would like to thank Jean-Noël Tasei and two anonymous reviewers for their helpful comments on an earlier version of the manuscript.


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All Tables

Table I

Detailed records of all sightings of B. t. sassaricus workers (W), queens (F) and males (M) observed during the 1988–2002 survey period which yielded 7946 sightings of B. terrestris.

All Figures

thumbnail Figure 1

The natural distribution of B. terrestris subspecies. The shaded area indicates the range over which B. terrestris occurs and the arrows point to the approximate centres of distribution of the nine subspecies. This figure was reproduced with permission from Rasmont et al. (2008).

In the text
thumbnail Figure 2

Pre 1988 observations of native B. terrestris subspecies in southern France prior to the importation of B. t. sassaricus.

In the text
thumbnail Figure 3

Observations of B. terrestris subspecies made between 1988 and 2002. NB. B. t. sassaricus was recorded at four localities (see Fig. 5).

In the text
thumbnail Figure 4

Records of B. terrestris subspecies collected during 2004. NB. no B. t. sassaricus were found.

In the text
thumbnail Figure 5

Location of B. t. sassaricus records collected between 1993 and 1998.

In the text