Introduced social bees reduce nectar availability during the breeding season of the swift parrot (Lathamus discolor)
Andrew B. Hingston A D and Simon Wotherspoon B C
+ Author Affiliations
- Author Affiliations
A School of Land and Food, University of Tasmania, Private Bag 78, Hobart, Tas. 7001, Australia.
B School of Mathematics and Physics, University of Tasmania, Private Bag 37, Hobart, Tas. 7001, Australia.
C Present address: Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tas. 7001, Australia.
D Corresponding author. Email: hingston@utas.edu.au
Pacific Conservation Biology 23(1) 52-62 https://doi.org/10.1071/PC16025
Submitted: 16 June 2016 Accepted: 13 August 2016 Published: 3 October 2016
Abstract
Numerous pollinators are declining across the world. One of these, the swift parrot (Lathamus discolor) is a critically endangered Australian bird that feeds largely on the nectar and pollen of Eucalyptus trees. The Swift Parrot Recovery Plan includes competition for food from introduced social bees as a threatening process, although little evidence exists in support of this. Here, we present the strongest evidence yet to support this theory. We examined nectar standing crops in the species of trees that are important to swift parrots during their breeding season, Tasmanian blue gum (Eucalyptus globulus) and black gum (E. ovata). By comparing the amounts of nectar between flowers exposed to visitors and those bagged to exclude visitors throughout the day, we discovered that introduced honey bees (Apis mellifera) and bumble bees (Bombus terrestris) consumed most of the nectar and that exposed flowers often contained little nectar. Honey bees were the more common species, but bumble bees had greater per capita rates of nectar consumption. However, at low densities these bees had no effect on standing crops of nectar, and in such situations some nectar could be harvested by managed honey bees without reducing nectar availability for swift parrots. Although this study suggests that introduced social bees may pose a threat to swift parrots, further work is needed to determine whether our results are indicative of the impacts of bees across greater scales of time and space and whether these affect the reproductive success and conservation status of the swift parrot.
Additional keywords: biological invasions, nectarivorous birds, parrot conservation, pollination crisis, social Hymenoptera.
References
Abe, T., Makino, S., and Okochi, I. (2008). Why have endemic pollinators declined on the Ogasawara Islands? Biodiversity and Conservation 17, 1465–1473.| Why have endemic pollinators declined on the Ogasawara Islands?Crossref | GoogleScholarGoogle Scholar |
Allchin, R., Kirkpatrick, J., and Kriwoken, L. (2013). On not protecting the parrot: impact of conservation and planning legislation on an endangered species in Tasmania. Journal of International Wildlife Law and Policy 16, 81–104.
| On not protecting the parrot: impact of conservation and planning legislation on an endangered species in Tasmania.Crossref | GoogleScholarGoogle Scholar |
Bashford, R. (2001). The spread and impact of the introduced vespine wasps Vespula germanica (F.) and Vespula vulgaris (L.) (Hymenoptera: Vespidae: Vespinae) in Tasmania. Australian Entomologist 28, 1–12.
Bauer, D. M., and Wing, I. S. (2010). Economic consequence of pollinator declines: a synthesis. Agricultural and Resource Economics Review 39, 368–383.
Blair, A. C., and Wolfe, L. M. (2007). The association between floral longevity and pollen removal, pollen receipt, and fruit production in flame azalea (Rhododendron calendulaceum). Canadian Journal of Botany 85, 414–419.
| The association between floral longevity and pollen removal, pollen receipt, and fruit production in flame azalea (Rhododendron calendulaceum).Crossref | GoogleScholarGoogle Scholar |
Boland, D. J., Brooker, M. I. H., Chippendale, G. M., Hall, N., Hyland, B. P. M., Johnston, R. D., Kleinig, D. A., and Turner, J. D. (1984). ‘Forest Trees of Australia.’ (Thomas Nelson Australia & CSIRO: Melbourne.)
Bond, H. W., and Brown, W. L. (1979). The exploitation of floral nectar in Eucalyptus incrassata by honeyeaters and honeybees. Oecologia 44, 105–111.
| The exploitation of floral nectar in Eucalyptus incrassata by honeyeaters and honeybees.Crossref | GoogleScholarGoogle Scholar |
Brown, P. B. (1989). The swift parrot Lathamus discolor (White). A report on its ecology, distribution and status, including management considerations. Department of Lands, Parks and Wildlife, Hobart.
Brown, J. H., Kodric-Brown, A., Whitham, T. G., and Bond, H. W. (1981). Competition between hummingbirds and insects for the nectar of two species of shrubs. The Southwestern Naturalist 26, 133–145.
| Competition between hummingbirds and insects for the nectar of two species of shrubs.Crossref | GoogleScholarGoogle Scholar |
Castro, S., Silveira, P., and Navarro, L. (2008). Effect of pollination on floral longevity and costs of delaying fertilization in the out-crossing Polygala vayredae Costa (Polygalaceae). Annals of Botany 102, 1043–1048.
| Effect of pollination on floral longevity and costs of delaying fertilization in the out-crossing Polygala vayredae Costa (Polygalaceae).Crossref | GoogleScholarGoogle Scholar | 18829587PubMed |
Cumber, R. A. (1953). Life cycle of the humble bee. New Zealand Science Review , 92–98.
Dafni, A., Kevan, P., Gross, C. L., and Goka, K. (2010). Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes. Applied Entomology and Zoology 45, 101–113.
| Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes.Crossref | GoogleScholarGoogle Scholar |
De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I., and Serrano, J. (2009). Biodiversity, conservation and current threats to European honeybees. Apidologie 40, 263–284.
| Biodiversity, conservation and current threats to European honeybees.Crossref | GoogleScholarGoogle Scholar |
Faegri, K., and van der Pijl, L. (1979). ‘The Principles of Pollination Ecology.’ (Pergamon Press: Oxford.)
Forster, I. W., and Hadfield, W. V. (1958). Effectiveness of honey bees and bumble bees in the pollination of Montgomery red clover. New Zealand Journal of Agricultural Research 1, 607–619.
| Effectiveness of honey bees and bumble bees in the pollination of Montgomery red clover.Crossref | GoogleScholarGoogle Scholar |
Fussell, M. (1992). Diurnal patterns of bee activity, flowering, and nectar reward per flower in tetraploid red clover. New Zealand Journal of Agricultural Research 35, 151–156.
| Diurnal patterns of bee activity, flowering, and nectar reward per flower in tetraploid red clover.Crossref | GoogleScholarGoogle Scholar |
Gartrell, B. D. (2002). Nutritional and physiological constraints on reproduction in the endangered swift parrot Lathamus discolor. Ph.D. thesis, University of Tasmania, Hobart.
Gartrell, B. D., and Jones, S. M. (2001). Eucalyptus pollen grain emptying by two Australian nectarivorous psittacines. Journal of Avian Biology 32, 224–230.
| Eucalyptus pollen grain emptying by two Australian nectarivorous psittacines.Crossref | GoogleScholarGoogle Scholar |
Gartrell, B. D., Jones, S. M., Brereton, R. N., and Astheimer, L. B. (2000). Morphological adaptations to nectarivory of the alimentary tract of the swift parrot Lathamus discolor. Emu 100, 274–279.
| Morphological adaptations to nectarivory of the alimentary tract of the swift parrot Lathamus discolor.Crossref | GoogleScholarGoogle Scholar |
González-Varo, J. P., Biesmeijer, J. C., Bommarco, R., Potts, S. G., Schweiger, O., Smith, H. G., Steffan-Dewenter, I., Szentgyörgyi, H., Woyciechowski, M., and Vilà, M. (2013). Combined effects of global change pressures on animal-mediated pollination. Trends in Ecology & Evolution 28, 524–530.
| Combined effects of global change pressures on animal-mediated pollination.Crossref | GoogleScholarGoogle Scholar |
Goulson, D., Peat, J., Stout, J. C., Tucker, J., Darvill, B., Derwent, L. C., and Hughes, W. O. H. (2002). Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Animal Behaviour 64, 123–130.
| Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?Crossref | GoogleScholarGoogle Scholar |
Grünewald, B. (2010). Is pollination at risk? Current threats to and conservation of bees. Gaia 19, 61–67.
Hansen, D. M., Olesen, J. M., and Jones, C. G. (2002). Trees, birds and bees in Mauritius: exploitative competition between introduced honey bees and endemic nectarivorous birds? Journal of Biogeography 29, 721–734.
| Trees, birds and bees in Mauritius: exploitative competition between introduced honey bees and endemic nectarivorous birds?Crossref | GoogleScholarGoogle Scholar |
Heinsohn, R., Webb, M., Lacy, R., Terauds, A., Alderman, R., and Stojanovic, D. (2015). A severe predator-induced population decline predicted for endangered, migratory swift parrots (Lathamus discolor). Biological Conservation 186, 75–82.
| A severe predator-induced population decline predicted for endangered, migratory swift parrots (Lathamus discolor).Crossref | GoogleScholarGoogle Scholar |
Hindwood, K. A., and Sharland, M. (1963). The swift parrot. Emu 63, 310–326.
| The swift parrot.Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B. (2006). Is the exotic bumblebee Bombus terrestris really invading Tasmanian native vegetation? Journal of Insect Conservation 10, 289–293.
| Is the exotic bumblebee Bombus terrestris really invading Tasmanian native vegetation?Crossref | GoogleScholarGoogle Scholar |
Hingston, 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.
| Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems?Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., and Piech, M. (2011). Parrots, people and plants: urban tree removal and habitat loss for the endangered swift parrot, Lathamus discolor. Papers and Proceedings of the Royal Society of Tasmania 145, 1–4.
Hingston, A. B., and Potts, B. M. (1998). Floral visitors of Eucalyptus globulus ssp. globulus in eastern Tasmania. Tasforests 10, 125–137.
Hingston, A. B., and Potts, B. M. (2005). Pollinator activity can explain variation in outcrossing rates within individual trees. Austral Ecology 30, 319–324.
| Pollinator activity can explain variation in outcrossing rates within individual trees.Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., Marsden-Smedley, J., Driscoll, D. A., Corbett, S., Fenton, J., Anderson, R., Plowman, C., Mowling, F., Jenkin, M., Matsui, K., Bonham, K. J., Ilowski, M., McQuillan, P. B., Yaxley, B., Reid, T., Storey, D., Poole, L., Mallick, S. A., Fitzgerald, N., Kirkpatrick, J. B., Febey, J., Harwood, A. G., Michaels, K. F., Russell, M. J., Black, P. G., Emmerson, L., Visoiu, M., Morgan, J., Breen, S., Gates, S., Bantich, M., and Desmarchelier, J. M. (2002). Extent of invasion of Tasmanian native vegetation by the exotic bumblebee Bombus terrestris (Apoidea: Apidae). Austral Ecology 27, 162–172.
| Extent of invasion of Tasmanian native vegetation by the exotic bumblebee Bombus terrestris (Apoidea: Apidae).Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., Gartrell, B. D., and Pinchbeck, G. (2004a). How specialized is the plant–pollinator association between Eucalyptus globulus ssp. globulus and the swift parrot Lathamus discolor? Austral Ecology 29, 624–630.
| How specialized is the plant–pollinator association between Eucalyptus globulus ssp. globulus and the swift parrot Lathamus discolor?Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., Potts, B. M., and McQuillan, P. B. (2004b). The swift parrot Lathamus discolor (Psittacidae), social bees (Apidae), and native insects as pollinators of Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany 52, 371–379.
| The swift parrot Lathamus discolor (Psittacidae), social bees (Apidae), and native insects as pollinators of Eucalyptus globulus ssp. globulus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., Potts, B. M., and McQuillan, P. B. (2004c). Pollination services provided by various size classes of flower visitors to Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany 52, 353–369.
| Pollination services provided by various size classes of flower visitors to Eucalyptus globulus ssp. globulus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Hingston, A. B., Herrmann, W., and Jordan, G. J. (2006). Reproductive success of a colony of the introduced bumblebee Bombus terrestris (L.) (Hymenoptera: Apidae) in a Tasmanian National Park. Australian Journal of Entomology 45, 137–141.
| Reproductive success of a colony of the introduced bumblebee Bombus terrestris (L.) (Hymenoptera: Apidae) in a Tasmanian National Park.Crossref | GoogleScholarGoogle Scholar |
IUCN (2015). The IUCN Red List of Threatened Species. Version 2015-4. Available at: www.iucnredlist.org [accessed 16 April 2016].
Kanbe, Y., Okada, I., Yoneda, M., Goka, K., and Tsuchida, K. (2008). Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften 95, 1003–1008.
| Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aisLvL&md5=c773f922f5e202135367c989f590fdd7CAS | 18594790PubMed |
Kato, M. (1992). Endangered bee fauna and its floral hosts in the Ogasawara Islands. Japanese Journal of Entomology 60, 487–494.
Kato, M., Shibata, A., Yasui, T., and Nagamasu, H. (1999). Impact of introduced honeybees, Apis mellifera, upon native bee communities in the Bonin (Ogasawara) Islands. Researches on Population Ecology 41, 217–228.
| Impact of introduced honeybees, Apis mellifera, upon native bee communities in the Bonin (Ogasawara) Islands.Crossref | GoogleScholarGoogle Scholar |
Kearns, C. A., and Inouye, D. W. (1993). ‘Techniques for Pollination Biologists.’ (University Press of Colorado: Colorado.)
Mallick, S., James, D., Brereton, R., and Plowright, S. (2004). Blue-gums Eucalyptus globulus in north-west Tasmania: an important food resource for the endangered swift parrot Lathamus discolor. Victorian Naturalist 121, 36–46.
Manley, R., Boots, M., and Wilfert, L. (2015). Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. Journal of Applied Ecology 52, 331–340.
| Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpvFahtLc%3D&md5=b52ca64232306cd7702c767839f6087fCAS | 25954053PubMed |
McMahon, D. P., Fürst, M. A., Caspar, J., Theodorou, P., Brown, M. J. F., and Paxton, R. J. (2015). A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. Journal of Animal Ecology 84, 615–624.
| A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees.Crossref | GoogleScholarGoogle Scholar | 25646973PubMed |
Monceau, K., Bonnard, O., and Thiéry, D. (2014). Vespa velutina: a new invasive predator of honeybees in Europe. Journal of Pest Science 87, 1–16.
| Vespa velutina: a new invasive predator of honeybees in Europe.Crossref | GoogleScholarGoogle Scholar |
Moreira, A. S., Horgan, F. G., Murray, T. E., and Kakouli-Duarte, T. (2015). Population genetic structure of Bombus terrestris in Europe: isolation and genetic differentiation of Irish and British populations. Molecular Ecology 24, 3257–3268.
| Population genetic structure of Bombus terrestris in Europe: isolation and genetic differentiation of Irish and British populations.Crossref | GoogleScholarGoogle Scholar | 25958977PubMed |
Paini, D. R., and Roberts, J. D. (2005). Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biological Conservation 123, 103–112.
| Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus).Crossref | GoogleScholarGoogle Scholar |
Paton, D. C. (1993). Honeybees in the Australian environmnent. Does Apis mellifera disrupt or benefit the native biota? Bioscience 43, 95–103.
| Honeybees in the Australian environmnent. Does Apis mellifera disrupt or benefit the native biota?Crossref | GoogleScholarGoogle Scholar |
Peat, J., and Goulson, D. (2005). Effects of experience and weather on foraging efficiency and pollen versus nectar collection in the bumblebee, Bombus terrestris. Behavioral Ecology and Sociobiology 58, 152–156.
| Effects of experience and weather on foraging efficiency and pollen versus nectar collection in the bumblebee, Bombus terrestris.Crossref | GoogleScholarGoogle Scholar |
Porfirio, L. L., Harris, R. M. B., Stojanovic, D., Webb, M. H., and Mackey, B. (2016). Projected direct and indirect effects of climate change on the swift parrot, an endangered migratory species. Emu 116, 273–283.
| Projected direct and indirect effects of climate change on the swift parrot, an endangered migratory species.Crossref | GoogleScholarGoogle Scholar |
Potts, S. G., Dafni, A., and Ne’eman, G. (2001). Pollination of a core flowering shrub species in a Mediterranean phrygana: variation in pollinator diversity, abundance and effectiveness in response to fire. Oikos 92, 71–80.
| Pollination of a core flowering shrub species in a Mediterranean phrygana: variation in pollinator diversity, abundance and effectiveness in response to fire.Crossref | GoogleScholarGoogle Scholar |
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., and Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25, 345–353.
| Global pollinator declines: trends, impacts and drivers.Crossref | GoogleScholarGoogle Scholar |
Pryor, L. D. (1976). ‘The Biology of Eucalypts.’ (Edward Arnold Publishers Limited: London.)
Pullinger, P. (2015). Pulling a swiftie: systematic Tasmanian Government approval of logging known to damage swift parrot habitat. Environment Tasmania, Hobart.
R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/
Rippon, R. J., Alley, M. R., and Castro, I. (2013). Traumatic ventriculitis following consumption of introduced insect prey (Hymenoptera) in nestling hihi (Notiomystis cincta). Journal of Wildlife Diseases 49, 80–90.
| Traumatic ventriculitis following consumption of introduced insect prey (Hymenoptera) in nestling hihi (Notiomystis cincta).Crossref | GoogleScholarGoogle Scholar | 23307374PubMed |
Rogers, H. J. (2006). Programmed cell death in floral organs: how and why do flowers die? Annals of Botany 97, 309–315.
| Programmed cell death in floral organs: how and why do flowers die?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislCksbk%3D&md5=581a8f9c2a26ade5d640949d6c3e4f87CAS | 16394024PubMed |
Saunders, D. L., and Tzaros, C. L. (2011). National recovery plan for the swift parrot Lathamus discolor. Birds Australia, Melbourne.
Saunders, D., Brereton, R., Tzaros, C., Holdsworth, M., and Price, R. (2007). Conservation of the swift parrot Lathamus discolor – management lessons for a threatened migratory species. Pacific Conservation Biology 13, 111–119.
| Conservation of the swift parrot Lathamus discolor – management lessons for a threatened migratory species.Crossref | GoogleScholarGoogle Scholar |
Schmid-Hempel, R., Eckhardt, M., Goulson, D., Heinzmann, D., Lange, C., Plischuk, S., Escudero, L. R., Salathé, R., Scriven, J. J., and Schmid-Hempel, P. (2014). The invasion of southern South America by imported bumblebees and associated parasites. Journal of Animal Ecology 83, 823–837.
| The invasion of southern South America by imported bumblebees and associated parasites.Crossref | GoogleScholarGoogle Scholar | 24256429PubMed |
Stojanovic, D., Webb, M. H., Alderman, R., Porfirio, L. L., and Heinsohn, R. (2014). Discovery of a novel predator reveals extreme but highly variable mortality for an endangered migratory bird. Diversity & Distributions 20, 1200–1207.
| Discovery of a novel predator reveals extreme but highly variable mortality for an endangered migratory bird.Crossref | GoogleScholarGoogle Scholar |
Stojanovic, D., Terauds, A., Westgate, M. J., Webb, M. H., Roshier, D. A., and Heinsohn, R. (2015). Exploiting the richest patch has a fitness pay-off for the migratory swift parrot. Journal of Animal Ecology 84, 1194–1201.
| Exploiting the richest patch has a fitness pay-off for the migratory swift parrot.Crossref | GoogleScholarGoogle Scholar | 25973857PubMed |
Stout, J. C., and Morales, C. L. (2009). Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409.
| Ecological impacts of invasive alien species on bees.Crossref | GoogleScholarGoogle Scholar |
Thomson, D. (2004). Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85, 458–470.
| Competitive interactions between the invasive European honey bee and native bumble bees.Crossref | GoogleScholarGoogle Scholar |
Tripathi, S. K., and Tuteja, N. (2007). Integrated signaling in flower senescence. Plant Signaling & Behavior 2, 437–445.
| Integrated signaling in flower senescence.Crossref | GoogleScholarGoogle Scholar |
Webb, M. H., Holdsworth, M. C., and Webb, J. (2012). Nesting requirements of the endangered swift parrot (Lathamus discolor). Emu 112, 181–188.
| Nesting requirements of the endangered swift parrot (Lathamus discolor).Crossref | GoogleScholarGoogle Scholar |
Williams, K. J., and Potts, B. M. (1996). The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39–165.
Wyatt, R., Broyles, S. B., and Derda, G. S. (1992). Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata). American Journal of Botany 79, 636–642.
| Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata).Crossref | GoogleScholarGoogle Scholar |
Ziegler, K. I. (1993). Leatherwood nectar resource management report. Forests and Forest Industry Council, Tasmania.
