Bombus dahlbomii

Commercially Introduced, Non-native Bumblebees

The most important and documented threat to the species at present is the invasion of European Bumblebee species introduced for crop pollination, in particular of Bombus terrestris (Morales et al. 2013). The driver of this threat is the global trade of non-native bumblebee species for pollination of agricultural field and greenhouse crops (Morales 2007, Stout and Morales 2009, Dafni et al. 2010). This commerce triggers the introduction of commercially reared bumblebee colonies outside their native range, along with their associated pathologies, and the additional threat that newly produced non-native queens will escape, find a mate, and become established. The pathogens introduced by commercial bumble bees, and the competition for resources from established feral colonies have become direct threats to the continued existence of B. dahlbomii.

The invasion and rapid spread of B. terrestris in Chile is continuously aided by permanent annual importation of thousands of commercial colonies. From 1997 to 2016, a yearly average of 16,651 colonies, 37,900 fertilised queens and 4,200 ovipositing queens have been imported to Chile, from different companies and geographic origins, including Belgium, The Netherlands, Israel, Slovakia, and Spain, reaching 39,000 colonies, 160,000 fertilised queens and 10,000 ovipositing queens in 2015 (Source: SAG Chile, date of data access: 14 June 2016).  Moreover, with the current existing regulations and recent requests for import authorized (Source: SAG Chile, Resolución N 2099/2016) these introductions will continue in the future. Strong propagule pressure (that is the combination of a high number of individuals of a non-native species involved in any one release event and the number of discrete release events) is one of the key factors favouring biological invasions (Colautti 2006). Here, the high number of colonies introduced on each shipment and the high frequency of introductions per year (Source: SAG Chile Date of data access: 14 June 2016) might subsidize the invasion of B. terrestris and its competitive and sanitary effects on B. dahlbomii.

This process has been documented in the The XII Region of Chile. Bombus terrestris was introduced in the XII Region during three consecutive years there (2011-2013) as part of a Project conducted by  the “Instituto de Investigaciones Agropecuarias” (INIA) to evaluate their pollination efficacy of Red Currant (Ribes rubrum) (Perez 2013, Estay and Mc Leod 2014). The first colonies were used under glasshouses conditions at INIA facilities in Kampenaike, Punta Arenas (Estay y Mc Leod 2014). Since then, commercial colonies have been continuously introduced by local growers for tomato pollination (Díaz Tavie, pers. comm., T. Salazar, pers. comm).

Feral colonies of B. terrestris have recently become established in the XII Region, including Tierra del Fuego, probably subsidized by these intentional local introductions. The first sightings of B. terrestris were documented in 2012 (Torres del Paine National Park, Diaz Tavie, pers. comm.) and the first photographic record in this Region was taken in 2014 (Puerto Natales, Diaz Tavie, pers. comm). These records coincide with observations of local owners of ornamental plant nursery, who agree that B. terrestris seems to have become established since at least 2014 near Punta Arenas (T. Salazar., pers. comm). Recent observations made by C. Morales (February 2016) and T. Salazar (March 2016) in the XII Region of Chile suggest that B. terrestris may be currently more abundant than B. dahlbomii, despite a relatively recent invasion.

Recently published studies confirm the rapid advance and current widespread distribution of B. terrestris. Schmid-Hempel et al. (2014) report that from field surveys in 2004 and from 2010-2012, by early 2010 B. terrestris was by far the dominant species in Central Chile from Santiago to Puerto Montt. In February 2011, no B. terrestris were found along the R.N. 26, road crossing the Patagonia steppe from the Andes to the Atlantic Ocean, however, in October 2011, just eight months later, this species was detected throughout this region.

Throughout the entire B. dahlbomii range, in sites where this species was formerly abundant and now is no longer observed or is very scarce, B. terrestris is extremely abundant (Morales et al. 2013, Schmid-Hempel et al. 2013, Geslin and Morales 2015, J. Montalva, L. Ruz, pers. obs., C. Avendaño, L. Vieli, Dr. Packer, pers. comm). All these studies together document that in less than 20 years the invasive bumblebee B. terrestris range has completely overlapped with B. dahlbomii (see the sections Population and Geographic Range).

Thus, the threat posed by the B. terrestris invasion can certainly affect the global population of B. dahlbomii. Hypothesized mechanisms underlying this observed ecological replacement may include pathogen transmission (Arbetman et al. 2013, Schmid-Hempel et al. 2014, Arismendi et al. 2016), although competition for resources cannot be discarded (Morales et al. 2013, Schmid-Hempel et al. 2014).


Pathogen Transmission and spread

Recent studies report that B. dahlbomii harbours various bumblebee internal pathogenic parasites (namely, Crithidia bombi, Nosema bombi, Locustacarus buchneri and Apicystis bombi). Overall, the timing of detection and patterns of prevalence suggest a role of invasive bumblebees in either co-introducing diseases or novel variants of pre-existing diseases or amplifying their spread, two hypotheses that need to be tested. Schmid-Hempel et al. (2014) performed various large scale surveys of the bumblebee fauna and bumblebee parasites in 2004 and from 2010 to 2012 covering the whole geographical range of B. dahlbomii, from Central Chile to the southern continental tip of South America. They reported infections of Crithidia bombi, a trypanosome protozoa which parasitizes bumble bees, in B. dahlbomii (18.5% prevalence) as well as in the two invasive bumblebee species (B. ruderatus and B. terrestris) in southern Chile. Genetically, the populations of C. bombi sampled in 2004 in B. dahlbomii and B. ruderatus were less diverse, and distinct from the ones sampled later, which were genetically similar among the three bumblebee species; supporting the hypothesis that Crithidia bombi was first introduced by B. ruderatus and then enriched by the later introduction of B. terrestris (Schmid-Hempel et al. 2014). Moreover, infection of C. bombi in B. terrestris was very high near Bariloche, Argentina in 2009, while the pathogen was absent from contemporaneous samples of native bumblebee species collected in other regions of Argentina not invaded by this species (Plischuk and Lange 2009).

Schmid-Hempel et al. (2014) also found that both invasive species carried the microsporidian Nosema, a pathogen  known to affect the survival and fecundity of bumblebees, although in low prevalence (B. ruderatus = 6.5%, n=77, B. terrestris = 2% n = 993), but this parasite was not detected in B. dahlbomii (n=128) nor in the native species more typical from the eastern side of the central Andes in Argentina, B. opifex (n=28) (Schmid-Hempel et al. 2014). However, Vallejos (2013) found Nosema bombi, both in B. dahlbomii (3.4% prevalence, N=176) and in B. terrestris (13,6%, N=88) sampled in South Chile in 2011. In our interpretation, the higher prevalence of N. bombi found by Vallejos (2013) may relate to the fact that he collected both B. dahlbomii and B. terrestris simultaneously in the same flowering plants in Valdivia city in 2011, thus increasing the chance of horizontal transmission. On the contrary, Schmid-Hempel (2014) sampled B. dahlbomii during a longer time lapse (2004, 2010-12), and over vast regions, including many sites still free of B. terrestris (see Fig. 2 and Table 2, Schmid-Hempel et al. 2014). This interpretation is consistent with a potential co-introduction of N. bombi by introduced bumblebees, and/or an increase of N. bombi infections in B. dahlbomii in the presence of B. terrestris, two hypothesis that remain to be tested.

Locustacarus buchneri, a parasitic mite known to affect bumblebees, was found in B. dahlbomii and in invasive bumblebees by two independent studies. Vallejos (2013) found L. buchneri in B. dahlbomii ( 0.6% prevalence, n=176) and B. terrestris (14%, n=88), in Valdivia city in 2011. More recently, Arismendi et al. (2016) found this pathogen at high prevalence in B. dahlbomii (23% of the 52 samples infected), as well as in the invasive B. terrestris (41% n=232) and B. ruderatus (30% n=94). The sequences of the parasite from the three hosts shared 100% identity among themselves and >98% identity with other sequences of L. buchneri reported in Belgium, the Netherlands, and >99% in Japan. Moreover, the L. buchneri infesting B. dahlbomii and invasive B. terrestris and B. ruderatus in Chile are more closely related than any other haplotypes reported in the Netherlands and Japan suggesting a potential horizontal transmission of this pathogen from the invasive bumble bees to B. dahlbomii (Arismendi et al. 2016). These authors suggest that L. buchneri may spread from commercial bumble bees (especially B. terrestris) to the native B. dahlbomii, since non-native and native species overlap and interact extensively throughout Chile (Montalva et al. 2011). The overall high prevalence of L. buchneri in B. dahlbomii compared to other native species whose ranges do not overlap with invading B. terrestris and B. ruderatus is remarkable, and suggests that the invading bumble bees may be the source of this pathogen, though a causal effect has not been clearly documented.

However, Plischuck et al.(2013) did not find infections of L. buchnerii in B. dahlbomii (n=2), B. ruderatus (n=8), or B. terrestris (n=704) sampled in Argentina. Although a low sample size may explain the lack of detection in the two former species, the lack of infected B. terrestris samples in Argentina contradicts the findings of Vallejos (2013) and Arismendi et al. (2016) in Chile, suggesting that further research on the epidemiology of this disease and the role of invasive species on its introduction and spread is needed.

Finally, there is evidence that the highly lethal bumblebee pathogen Apicystis bombi, detected in B. terrestris populations of southern Argentina but not in other native bumblebees of other regions of Argentina (Plischck and Lange 2009), shares the same haplotypes with Apicystis of bumblebees collected in Europe (Maharranov et al. 2013). This pathogen was further detected in B. dahlbomii and B. ruderatus sampled after but not before B. terrestris invasion, suggesting that the pathogen might have been co-introduced with invasive B. terrestris, from which it might have jumped to B. dahlbomii and B. ruderatus (Arbetman et al. 2013).

Although the pathogenic effects of all of these parasites on B. dahlbomii remain unknown, C. bombi has been shown to sterilize founding queens of B. terrestris (Brown, Schmid-Hempel andSchmid-Hempel 2003), leading to failure during colony founding and severely compromised reproductive success. This effect might be stronger in a species like B. dahlbomii that may not have encountered this parasite prior to invasion by B. terrestris and B. ruderatus (Otterstatter and Thomson 2008); a hypothesis that remains to be tested.

It is likely that only a novel, rather abundant, sufficiently virulent parasite should have the rapid effects that could have induced the observed population decline of B. dahlbomii in such a short time (Schmid-Hempe et al. 2014). The pathologies and known virulence of A. bombi and C. bombi would likely qualify for this. Likewise, the mite L. buchnerii invades, parasitizes, and reproduces in the tracheae and air sacs of adult bees (Yoneda et al. 2008, cited in Arismendi et al. 2016), affecting the host’s physiology, lifespan and behaviour (Otterstatter and Whidden 2004, Otterstatter et al. 2005). Urgent research is required to determine the direct effect of C. bombii, A. bombii, L. buchnerii and N. bombi on B. dahlbomii, as well as their combined effects, along with the interaction with other potential stressors like the direct and indirect competition for resources with invasive congeners.


Competitive effects of B. terrestris on B. dahlbomii

Bombus terrestris has larger colonies, emerges earlier from hibernation, has a longer season of activity than B. dahlbomii (Morales et al. 2013). Thus competitive displacement seems plausible (Schmid-Hempel et al. 2014), although it has not been experimentally demonstrated, partly because of the rapid collapse of B. dahlbomii subpopulations after B. terrestris invasion.

Bombus terrestris puts competitive pressures on B. dahlbomii. For example, presence of B. terrestris alters B. dahlbomii’s behaviour. Bombus terrestris primarily nectar robs Fuchsia magellanica flowers, and when it does, it precipitates a shift in B. dahlbomii's behaviour from legitimate visitation to secondary nectar robbing (Combs 2011, N. Rosenberger, pers. obs). All across their overlapping range, B. dahlbomii legitimately visits F. magellanica’s flowers, and it is one of the most frequent pollinators of populations growing in the area of Puerto Blest, Parque Nacional Nahuel Huapi: the eastern limit of the Valdivian Temperate Forest (Morales and Aizen 2002). However, a recent study in this area shows that after B. terrestris arrival to this area, B. dahlbomii frequently robs F. magellanica flowers using holes made by B. terrestris (N. Rosenberger, pers. obs). Preliminary comparisons of visitation to F. magellanica flowers before (2000-2001, Morales and Aizen 2002, 2006), and after (2015-2016, N. Rosenberger, in preparation) B. terrestris’ arrival does not show evidence of a local negative impact on B. dahlbomii’s overall visitation frequency to F. magellanica (Morales and Rosenberger, unpublished), however, the impacts of this phenomenon on diseases transmission through corolla holes, and on plant reproduction remain unknown.

On the contrary, a recent study focused on Vicia nigricans, a typically bumblebee pollinated plant, whose main pollinator was B. dahlbomii (Morales and Aizen 2002, Vazquez and Simberloff 2004), is increasingly visited by B. terrestris who chews through the corolla tube to access the floral nectaries thereby not providing any pollination services (Graham 2015). Bombus dahlbomii visitation frequency to V. nigricans flowers decreases in sites strongly invaded by B. terrestris. As a consequence, comparisons of populations trends across a broad geographic region suggest a consistent decline in visitation frequency to V. nigricans by B. dahlbomii, and a reduction in seed output after B. terrestris invasion (Chalcoff et al. 2015, Chalcoff et al. in prep).

Other focal threats that can affect local subpopulations are the increasing habitat loss and urbanization rate (in particular in Central Chile, Arroyo et al. 1999). Habitat fragmentation and disturbance seems to indirectly affect the species by favouring the spread of B. ruderatus (Aizen and Feinsinger 2003, Morales and Aizen 2002), and B. terrestris (Morales, pers. obs). Finally, global warming may negatively affect and probably accelerate the observed southward retraction observed at the northern part its range (Morales et al. in prep).

Many of the remaining Argentinian subpopulations as well as many of the Chilean subpopulations are located in National Parks and other Natural and Wildlife Reserves. However, if invasion of introduced bumblebees are the main drivers of its decline, solely protecting habitat will probably not be effective enough to revert this declining trend, because these invasive species also thrive in these habitats.

In addition there have been a lot of outreach activities (radio interviews, talks, etc.) and publications (Morales 2006a,b, 2007, 2009; Arbetman and Morales 2014) aimed to enhance the public awareness on this species.

In Argentina an educational brochure "El mangangá y la polinización de nuestrosbosques" has been designed by Carolina L. Morales and published with the support of the Cannon National Parks Science Scholar Program, the National Parks Administration of Argentina and the Universidad Nacional del Comahue.

In Chile a targeted campaign called "Salvenos Nuestro Abejorro" (Save our bumblebee) has been launched by Jose Montalva: https://salvemosnuestroabejorro.wordpress.com/. In addition, a proposal to classify and protect this species under the National Red Listing Scheme in Chile has been recently approved by the Ministry of Environment of Chile (http://www.mma.gob.cl/clasificacionespecies/listado_especies_12o_pac.htm). The final resolution will be officially published during 2016, and this classification is expected to trigger practical conservations measures.

Some proposed realistic actions needed to mitigate major threats to the taxon are to stop the ongoing importation of B. terrestris, control and eradicate the currently established populations of B. terrestris and B. ruderatus in areas where subpopulations of B. dahlbomii are still healthy (manual removal of colonies/mated queens), identify subpopulations of B. dahlbomii which are immune or resistant to pathogenic diseases that can be used for captive breeding and reintroduction programs, study rearing techniques specific to the native species, genetic analysis of populations where still abundant, to inform management programs. A possible action to reduce populations of invasive Bombus spp. might be to release sterilized drones or males to reduce the fecundity of the species as has been successful in other taxa.