Goodwin and Steiner’s 1997 Submission to AQIS and Environment Australia concerning the introduction of Bombus terrestris for biological pollination of horticultural crops in Australia contains a very substantial review of research on issues relating to bumblebee and other Hymenopteran introductions around the world. There are a few omissions however, and several papers have since been published which should be noted.

B. terrestris

An up to date literature review should begin with an old report in the Agricultural Gazette of Tasmania:

In 1909, after seeking advice from the U.S. Department of Agriculture and the Board of Agriculture, London, the Council of Agriculture, Tasmania ordered 25 bumble bee queens (species unknown) from New Zealand and released them in Tasmania at Falmouth (east coast), the Botanical Gardens (Hobart) and Gunns Plains (northwest coast). The advice favoured importation of long-tongued Bombus spp. , which does not include B. terrestris. No further reference to the project or its outcome appears in succeeding volumes of the Agricultural Gazette of Tasmania.

In the intervening period there are many papers on how bumblebees forage overseas, but most of them do not relate to Australian plants or native bees. The next relevant reference is Arretz and Macfarlane’s (1986) paper on B. ruderatus. They point out that bumblebees were introduced into Chile from New Zealand in 1983 and B. ruderatus, a long-tongued species, was chosen as part of an Organization of American States aid project to pollinate red clover. Chile does have its own bumblebees, but they were considered to be unsuitable for development as a major pollinator of red clover, because of factors such as timing of colony development, preferred nest sites in wooded areas, and insufficient numbers.

My own study done in 1995-96, measured population counts and production of reproductives of some successful colonies. 18 feral colonies found in and around Hobart were transferred to nest boxes, where colony development could be monitored. Only one of the 18 original nest sites could be classified as "semi-bush" but it was still within 0.5 km of suburban gardens. All of the colonies produced queens, and I found Tasmanian bumblebee nests to be on a par with the largest European nests, but not as large as New Zealand nests. This may be because the species is still in the process of getting established in this region. There is evidence of two generations produced during warmer months of the year, much as in New Zealand, where mild winters allow queens who emerge in late spring/early summer (without an intervening diapause over winter) to begin nests and successfully raise another generation of reproductives. I found the rate of dispersal through the island averaged 12.5 km/year at that time. Of course, external influences such as predatory habits of birds, availability of food, competition from other insects and deliberate introduction by people into new areas make the rate of spread unpredictable.

The HRDC report by Pomeroy and others (including myself) in 1997 cited in the Goodwin-Steiner submission was published in slightly different form in the Journal of Apicultural Research (Buttermore et al. 1999). We found that the population was sufficiently inbred for diploid male production to be a factor in commercial rearing, and speculated that Tasmanian bumblebees had perhaps started from a single introduced, inseminated queen. By the way, artificial insemination of bumblebees is now possible, and the technique was kindly demonstrated to me by Boris Baer, at ETH, Zürich (Baer & Schmid-Hempel 1999). His supervisor there is Paul Schmid-Hempel, and there is a possibility of collaboration with Geoff Allan (UTAS) and myself for micro-satellite analysis of the Tasmanian bumblebee population, to establish its genetic diversity conclusively.

In 1996, Andrew Hingston began an Honours project studying the impact of bumblebees on Tasmanian ecosystems which led to a thesis in 1997 and three published papers to date. Andrew and Peter McQuillan, in the Australian Journal of Ecology , reported on a summer, 1996-97 survey of native vegetation near Hobart. Bumblebees were found to be established in high numbers in a variety of vegetation types from coastal heath, through sclerophyll forest, and subalpine shrubberies up to an altitude of 1100 m. As a result, Andrew and Peter hypothesize that bumblebees have the potential to spread through much of Tasmania and temperate, mesic regions of mainland Australia. They reported that B. terrestris is highly polylectic, foraging on at least 66 native plant species from 21 families. While the most heavily visited plant species produced abundant nectar, the lack of predation on bumblebees also allowed them to forage economically on small flowers in clusters. This foraging profile overlapped with those of all anthophilous insect families, all bee subgenera, and all species of nectarivorous birds that were encountered. Therefore, B. terrestris has the potential to compete with most native anthophiles and commercial honeybees. Because B. terrestris forages from some plant taxa which are not visited by the European honeybee, the results show that bumblebees are in some degree impacting on plant-pollinator relationships which have previously been free from the effects of exotic bees. In a second 1998 paper published in the Victorian Naturalist, they report on a comparison of nectar robbing by B. terrestris between two populations of Common Heath, Epacris impressa, (Epacridaceae). Robbing was more frequent in the population with longer corollas, resulting in most open flowers being pierced. This has implications for Victorian flowers of the same species, as they have, on average, longer corolla tubes than those of Tasmania.

Andrew and Peter published a third paper this year (1999) in the Australian Journal of Zoology where they reported the results of an study into the impact of B. terrestris on the foraging of two species of native bees, Chalicodoma (Megachilidae), on flowers of Gompholobium huegelii (Fabaceae). In that study, Chalicodoma spp. spent less time at each flower during the afternoon in quadrats where B. terrestris foraged than at quadrats from which B. terrestris was excluded, suggesting that standing crops of nectar were depleted by B. terrestris during the course of the day. The decline in resources was associated with reductions in number of flowers visited, and amount of time spent foraging, by Chalicodoma spp. Andrew and Peter hypothesize that the native bees avoided foraging in the quadrat where B. terrestris occurred, as a response to reduced foraging efficiency in that situation, implying that B. terrestris displaced these two species of Chalicodoma through competition for a limited resource. Further, the high densities at which B. terrestris occurred, together with its ability to forage at lower ambient temperatures than the native bees, exacerbated the impact. The possibility that this will adversely affect pollination in G. huegelii was also discussed.

Amots Dafni, in Bee World, (1998) has issued another warning on the threat of Bombus terrestris spread.

Trevor Semmens (1998) issued a supplementary list of new flowers visited by bumblebees in Tasmania. The aggregate list now stands at 216 plants: 20 natives and 196 introduced species.

A recent symposium (Ecological Society of America, Las Vegas, 10 November 1998) presented the issues involved in the history and future of pollinator management (Karen Strickler, University of Idaho, pers. comm.) Editors Strickler and James Cane, (USDA ARS, Logan, UT) hope that the forthcoming publication will help guide USDA APHIS in crafting appropriate regulations governing the growing trade in bees for agricultural pollination. As a result of that symposium, the following two pieces of personal correspondence, dated last December, were noted on BOMBUS-L, an electronic discussion list owned by Chris Plowright:

Dr Masato Ono, Professor, Tamagawa University, Japan is extremely worried about the possibility of transfer of disease from B. terrestris, and subsequent extinction of native Japanese bumblebees. So far, ongoing research projects on these potential problems are unpublished. I quote:

"These results (including nest usurpation & genetic pollution by B. terrestris against closely-related species of Japan) may change the minds of companies trading in bumblebees towards favoring commercial production of indigenous bumblebees as pollinators for growers.

 

"Based on worldwide experience of the harm caused by introduction of non-native species, such imports require very careful impact beforehand."

Adriaan van Doorn, Head R&D - Pollination, Department, Koppert Biological Systems points out the probably prohibitive costs which Ono’s proposals involve and I’ll paraphrase his response:

"…it is possible to rear some of the native Japanese species, for example, Bombus ignitus. However, production costs at this moment are some 5 times higher than for Bombus terrestris, [and] the colonies reach about half the size of a terrestris colony ([Therefore] about twice as many colonies are needed to pollinate a given area)…for the Japanese tomato grower, costs would become significantly higher (…up to 10 times) than they are now."

Two draft papers by Jane Stout and Dave Goulson (U. Southampton) on bumblebee distribution in Tasmania, and potential impact of the bees on Australian flora and fauna have been submitted respectively to Bee World and Journal of Applied Ecology.

Last September, in a paper presented to a meeting of specialists on insect pollination in greenhouses (in press), I reported on the results of a repeat experiment where laboratory reared broods of field-caught bumblebee queens were checked for the prevalence of diploid male production, an indication of inbreeding. The ratio of males to workers at the beginning of colony development was used as an indicator. As stated above, the previous 1996 experiment had shown the Tasmanian bumblebee population to be very inbred, with about 50% of adult-producing colonies producing initial sex ratios consistent with male diploidy, but two years later the level fell to about 38%. Rearing success rate was much improved: 67% v. 18% of fit queens raised at least one adult, and colonies were much more populous in this later trial. Whether this is a permanent change is unknown, but if it is, mooted importation of new genetic material may now not be necessary to sustain commercial breeding of B. terrestris in Tasmania.

Apis mellifera

In Australia, research on the impact of the introduced honeybee on the long term viability of the native biota has been ongoing since at least the early ‘eighties, and three essays on the subject were featured in a special, 1997 issue of the Victorian Naturalist. The Goodwin-Steiner submission cites two of those papers but misses the third, an essay by David Paton on honeybees and the disruption of plant-pollinator systems in Australia. In that particular journal issue was also an introduction by Tim New, which recalls the 1989 National Workshop on ‘Commercially managed Honey Bees in the Australian environment’ . Tim writes: "at that meeting…there was a perceived need for critical appraisal of some previous key studies, and for sound experimental research to test hypotheses on possible adverse or competitive effects (involving both exploitation or resources and interference with other species)." This is perhaps the situation we now find ourselves facing with bumblebees.

Earlier Australian studies, too numerous to mention, are cited in the bibliographies that follow those three papers and their introduction. However a survey by George & Jennifer Ettershank wasn’t listed. The Ettershanks examined the interactions between honeybees and native insects on Tasmanian leatherwood trees before the advent of bumblebees to the state.

Leatherwoods (Eucryphia lucida and E. milliganii, are typical understorey tree species in the cool temperate rainforests and mixed forests of western Tasmania. Much of these forests lie within the Tasmanian Wilderness World Heritage Area and State Forests. E. lucida is more extensive at lower altitudes, and is the major honey-producing species in the state. E. milliganii is a sub-alpine species and of minor importance as a honey source. The Ettershanks attempted to ascertain the range of native insects that utilise leatherwoods as a nectar or pollen source, to estimate the utilisation of the resource, and to determine if interactions could be observed between foraging Apis mellifera and native insects. The sequence of development of the flowers and the quantity and quality of nectar were also studied, together with some aspects of growth and distribution of Eucryphia lucida.

A very diverse insect fauna was found to be associated with the flowers of both species of leatherwoods. Many of the common insects were also found on other plant species.

Visitations by native insects and by honeybees (both feral and managed) were quite low.

At the flowers, no behavioural interaction of honeybees (either feral or managed) with native insects were observed. No interspecific interactions were seen except between insects and arthropod predators.

Feral honeybees were seen at all locations sampled, as much as 25-30 km from commercial beekeeping sites.

Steven Mallick, funded by the Tasmanian Parks & Wildlife Service, began a three year study investigating the impacts of commercial honeybees on the native flower visiting fauna of Tasmania’s leatherwood forests (Dreissen, 1998). His study area is located in northwest Tasmania where the fauna of several sites with established commercial apiaries are being compared with fauna at control sites. In addition, the impact of introducing an apiary to "pristine" sites without prior apiary use is being investigated. The results of this study should be of value in the ongoing debate as to the potential deleterious impacts of commercial apiaries within conservation areas in Tasmania but also may be of value on some of the aspects needed for bumblebee research.

In addition, there is a report in preparation for World Wide Fund for Nature (Australia) by Mike Schwarz, Caroline Gross, Penny Kukuk & D. Hobbs: "An Assessment of Competition Between Honeybees & Australian Native Bees". They conclude:

"Our results do not provide clear cut evidence for negative impacts of honeybees on the native bee Exoneura bicolor. However, our findings include a variety of results that strongly suggest that honeybees do have an impact on the ecology of native allodapine bees. This raises the question of whether the ‘positive’ effects detected by our study might have negative consequences for natural ecosystems, or whether only ‘beneficial’ or neutral effects arise. This question has not been raised by previous studies of honeybees in Australia ecosystems...

 

"…Consequently, we recommend that in areas where ecosystems are to be conserved in pristine states honeybees should be excluded. However, in ecosystems where perturbations are regarded as permissible (e.g.. forests which are used for timber harvesting or which have a low conservation status) then there may be a lesser case for excluding honeybees."

 

Disease/Parasite introduction

Alford in his 1975 book on bumblebees, noted that they might very occasionally be vectors of micro-organisms, e.g. fireblight, Erwinia amylovora, a serious disease of apple and pear trees. He also listed the known enemies and nest commensals, including larger predators. However, Rod Macfarlane says that most of the larger bumblebee enemies that evolved in the Northern Hemisphere are not present in Australia or New Zealand.

Kevan & Laverty (1990) warned about the possibility of spreading Varroa mites (a serious pest of honeybees) by other insects, including bumblebees, although it is not thought to be a critical problem according to Chris Plowright. One virus has been linked to both honeybees and bumblebees. This is linked to the Varroa mite Barbara Ball, (Rothamstead Experimental Station pers. comm.) and causes acute paralysis syndrome of queens (Bailey & Ball, 1994). Van den Eijnde & Vette in 1993 showed that the protozoan Nosema bombi did not infect honeybees nor did N. apis cross-infect bumblebees. Although the review by Macfarlane and others in 1995 was cited in the Goodwin-Steiner submission, the actual reference was omitted. One of the main points of that review was that honeybees and bumblebees share very few pathogens due to their different life styles.

I believe that covers the more important references not discussed in the Goodwin-Steiner submission, but if there are others to add, please let me know.

References

Alford, D.V. (1975) Bumblebees. Davis-Poynter, London. 352 p.

 

Arretz, P. V. and Macfarlane, R. P. (1986) The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World 67: 15-22.

 

Baer, B. & Schmid-Hempel, P. (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397: 151-153.

 

Bailey, L. & Ball, B.V. (1994) Honey bee viruses. In: Encyclopedia of Virology, Academic Press, London pp. 654-660.

 

Buttermore, R. E. (1997) Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in southern Tasmania. Australian Journal of Entomology 36: 251-254.

 

Buttermore, R. E. (1999) Further developments concerning rearing (inbred Tasmanian bumblebees. Proceedings of the Specialists’ Meeting on Insect Pollination in Greenhouses (in press).

 

________, R. E., Pomeroy, N., Hobson, W., Semmens, T. and Hart, R. (1998) Assessment of the genetic base of Tasmanian bumble bees (Bombus terrestris) for development as pollination agents. Journal of Apicultural Research 37: 23-25.

 

Dafni, A. (1998) The threat of Bombus terrestris spread. Bee World, 79: 113-114.

 

Driessen, M. (1998) News from the World Heritage Area Zoologist. Invertebrata March 1998 No. 10: 5. Queen Victoria Museum & Art Gallery, Launceston.

 

Eijnde, J. van den & Vette, N. (1993) Nosema infection in honeybees (Apis mellifera L.) and bumblebees (Bombus terrestris L.). Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 4: 205-208.

 

Ettershank, G. & Ettershank, J.A., (1992) Tasmanian Leatherwoods (Eucryphia spp.) - floral phenology and the insects associated with flowers. Tasmanian NRCP Technical Report No. 11. Forestry Commission, Tas. and DASET, Canberra.

 

Hingston, A.B. (1997). The impact of the large earth bumblebee, Bombus terrestris (L.) (Apidae: Apoidea) on Tasmanian ecosystems. University of Tasmania at Hobart Honours Thesis, 450 pp.

 

_______, A.B. and McQuillan, P.B. (1998) Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems? Australian Journal of Ecology 23: 539-549.

 

_______, A.B. and McQuillan, P.B. (1998) Nectar robbing in Epacris impressa (Epacridaceae) by the recently introduced bumblebee Bombus terrestris (Apidae) in Tasmania. The Victorian Naturalist 115(4): 230-233.

 

_______, A.B and McQuillan, P.B. (1999) Displacement of Tasmanian megachilid bees by the recently introduced bumblebee Bombus terrestris (Linnaaeus, 1758) (Hymenoptera : Apidae) threaten Australian ecosystems? Australian Journal of Zoology 47: 59-65.

 

Kevan, P.G. & Laverty, T.M. (1990) A brief survey and caution about importing alternative pollinators into Canada. Canadian Beekeeping 15(8): 176.

 

Macfarlane, R.P., Jerzy, J.L. & Lipa, H.J. (1995) Bumble bee pathogens and internal enemies. Bee World 76(3): 130-148.

 

New, T.R. (1997) Significance of honey bees in the Australian environment: setting the scene. Victorian Naturalist 114: 4-7.

 

Paton, D.C. (1997) Honey Bees Apis mellifera and the disruption of plant-pollinator systems in Australia. Victorian Naturalist 114: 23-29.

 

Pomeroy, N., Hobson, W., Buttermore, R.E., Semmens, T. & Hart, R., (1997) Assessment of the genetic base of Tasmanian bumble bees for development as pollination species. HRDC Report, Project No: HG 631.

 

Semmens, T. (1998) New flowers visited by bumble bees. Invertebrata November 1998 No. 12: 9. Queen Victoria Museum & Art Gallery, Launceston.