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Density of invasive western honey bee (Apis mellifera) colonies in fragmented woodlands indicates potential for large impacts on native species

  • Geslin, B. et al. Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57, 147–199 (2017).

    Google Scholar 

  • Huryn, V. M. B. Ecological impacts of introduced honey bees. Q. R. Biol. 72, 275–297 (1997).

    Google Scholar 

  • Stout, J. C. & Morales, C. L. Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409 (2009).

    Google Scholar 

  • Hung, K.-L.J., Kingston, J. M., Albrecht, M., Holway, D. A. & Kohn, J. R. The worldwide importance of honey bees as pollinators in natural habitats. Proc. R. Soc. Ser. B 285, 20172140 (2018).

    Google Scholar 

  • Paini, D. R. Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review. Austral Ecol. 29, 399–407 (2004).

    Google Scholar 

  • Moritz, R. F. A., Hartel, S. & Neumann, P. Global invasions of the western honey bee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12, 289–301 (2005).

    Google Scholar 

  • Paini, D. R. & Roberts, J. D. Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biol. Cons. 123, 103–112 (2005).

    Google Scholar 

  • Munoz, I. & De la Rua, P. Wide genetic diversity in old world honey bees threatened by introgression. Apidologie 52, 200–217 (2021).

    Google Scholar 

  • Williams, I. H. The dependences of crop production within the European Union on pollination by honey bees. Agric. Zool. Rev. 6, 229–257 (1994).

    Google Scholar 

  • Thompson, C. E., Biesmeijer, J. C., Allnutt, T. R., Pietravalle, S. & Budge, G. E. Parasite pressures on feral honey bees (Apis mellifera sp.). PLoS One 9, e105164 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Belsky, J. & Joshi, N. K. Impact of biotic and abiotic stressors on managed and feral bees. Insects 10, 233 (2019).

    PubMed Central 

    Google Scholar 

  • Medina-Flores, C. A., Guzman-Novoa, E., Hamiduzzaman, M. M., Arechiga-Flores, C. F. & Lopez-Carlos, M. A. Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological regions in Mexico. Genet. Mol. Res. 13, 7282–7293 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Portman, Z. M., Tepedino, V. J., Tripodi, A. D., Szalanski, A. L. & Durham, S. L. Local extinction of a rare plant pollinator in Southern Utah (USA) associated with invasion by Africanized honey bees. Biol. Invasions 20, 593–606 (2018).

    Google Scholar 

  • Santos, G. M. D. et al. Invasive Africanized honeybees change the structure of native pollination networks in Brazil. Biol. Invasions 14, 2369–2378 (2012).

    Google Scholar 

  • Chapman, R. E. & Bourke, A. F. G. The influence of sociality on the conservation biology of social insects. Ecol. Lett. 4, 650–662 (2001).

    Google Scholar 

  • Aizen, M. A. et al. When mutualism goes bad: Density-dependent impacts of introduced bees on plant reproduction. New Phytol. 204, 322–324 (2014).

    Google Scholar 

  • Breeze, T. D. et al. Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS One 9, e82996 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baum, K. A. et al. Spatial distribution of Africanized honey bees in an urban landscape. Landsc. Urban Plan. 100, 153–163 (2011).

    Google Scholar 

  • Ratnieks, F. L. W., Piery, M. A. & Cuadriello, I. The natural nest and nest density of the africanized honey-bee (Hymenoptera, Apidae) near Tapachula, Chiapas, Mexico. Can. Entomol. 123, 353–359 (1991).

    Google Scholar 

  • Baum, K. A., Rubink, W. L., Pinto, M. A. & Coulson, R. N. Spatial and temporal distribution and nest site characteristics of feral honey bee (Hymenoptera: Apidae) colonies in a coastal prairie landscape. Environ. Entomol. 33, 727–739 (2004).

    Google Scholar 

  • Rangel, J. et al. Africanization of a feral honey bee (Apis mellifera) population in South Texas: Does a decade make a difference?. Ecol. Evol. 6, 2158–2169 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Oldroyd, B. P., Thexton, E. G., Lawler, S. H. & Crozier, R. H. Population demography of Australian feral bees (Apis mellifera). Oecologia 111, 381–387 (1997).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Arundel, J. et al. Remarkable uniformity in the densities of feral honey bee Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) colonies in South Eastern Australia. Austral Entomol. 53, 328–336 (2014).

    Google Scholar 

  • Remm, J. & Lõhmus, A. Tree cavities in forests—The broad distribution pattern of a keystone structure for biodiversity. For. Ecol. Manag. 262, 579–585 (2006).

    Google Scholar 

  • Lindenmayer, D., Crane, M., Blanchard, W., Okada, S. & Montague-Drake, R. Do nest boxes in restored woodlands promote the conservation of hollow-dependent fauna?. Restor. Ecol. 24, 244–251 (2016).

    Google Scholar 

  • New South Wales Department of Planning, Industry and Environment 2003. https://www.environment.nsw.gov.au/topics/animals-and-plants/threatened-species/nsw-threatened-species-scientific-committee/determinations/final-determinations/2000-2003/competition-from-feral-honeybees-key-threatening-process-listing (accessed 22 Feb 2021).

  • Goldingay, R. L., Rohweder, D. & Taylor, B. D. Nest box contentions: Are nest boxes used by the species they target?. Ecol. Manag. Restor. 21, 115–122 (2020).

    Google Scholar 

  • Lindenmayer, D. B. et al. Are nest boxes a viable alternative source of cavities for hollow-dependent animals? Long-term monitoring of nest box occupancy, pest use and attrition. Biol. Cons. 142, 33–42 (2009).

    Google Scholar 

  • Lindenmayer, D. B. et al. The anatomy of a failed offset. Biol. Conserv. 210, 286–292 (2017).

    Google Scholar 

  • Macak, P. V. Nest boxes for wildlife in Victoria: An overview of nest box distribution and use. Vic. Nat. 137, 4–14 (2020).

    Google Scholar 

  • Le Roux, D. S. et al. Effects of entrance size, tree size and landscape context on nest box occupancy: Considerations for management and biodiversity offsets. For. Ecol. Manag. 366, 135–142 (2016).

    Google Scholar 

  • Berris, K. K. & Barth, M. PVC nest boxes are less at risk of occupancy by feral honey bees than timber nest boxes and natural hollows. Ecol. Manag. Restor. 21, 155–157 (2020).

    Google Scholar 

  • Jaffe, R. et al. Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 24, 583–593 (2010).

    PubMed 

    Google Scholar 

  • Utaipanon, P., Schaerf, T. M. & Oldroyd, B. P. Assessing the density of honey bee colonies at ecosystem scales. Ecol. Entomol. 44, 291–304 (2019).

    Google Scholar 

  • Utaipanon, P., Holmes, M. J., Chapman, N. C. & Oldroyd, B. P. Estimating the density of honey bee (Apis mellifera) colonies using trapped drones: Area sampled and drone mating flight distance. Apidologie 50, 578–592 (2019).

    CAS 

    Google Scholar 

  • Williamson, E. M. Reliability of honey bee hive density estimates using drone sampling: does relative hive size or distance affect a colony’s drone contribution? Honours Thesis, The University of Adelaide (2020).

  • Benson, J. S. The effect of 200 years of European settlement on the vegetation and flora of New South Wales. Cunninghamia 2, 343–370 (1991).

    Google Scholar 

  • New South Wales Office of Environment and Heritage 2015. Upgraded NSW woody vegetation extent for 2011. http://data.auscover.org.au/xwiki/bin/view/Product+pages/nsw+5m+woody+extent+and+fpc (accessed 13 May 2020).

  • R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020). www.R-project.org (accessed 12 January 2021).

  • Burnham, K. P. & Anderson, D. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).

    MATH 

    Google Scholar 

  • Albert, A. & Anderson, J. A. On the existence of maximum likelihood estimates in logistic regression models. Biometrika 71, 1–10 (1984).

    MathSciNet 
    MATH 

    Google Scholar 

  • Firth, D. Bias reduction of maximum likelihood estimates. Biometrika 80, 27–38 (1993).

    MathSciNet 
    MATH 

    Google Scholar 

  • Kosmidis, I., Pagui, E. C. K. & Sartori, N. Mean and median bias reduction in generalized linear models. Stat. Comput. 30, 43–59 (2020).

    MathSciNet 
    MATH 

    Google Scholar 

  • Anderson, D. R. Model Based Inference in the Life Sciences: A Primer on Evidence (Springer Science & Business Media, 2007).

    Google Scholar 

  • Barton, K. MuMIn: Multi-model inference. R package version 1.43.17 (2016).

  • Hijmans, R. J. Raster: Geographic Data Analysis and Modeling. R package version 3.4-5 (2020).

  • Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.3.0 (2018).

  • Kosmidis, I. brglm2: Bias Reduction in Generalized Linear Models. R package version 0.6.2 (2020).

  • Kosmidis, I., Schumacher, D. detectseparation: Detect and Check for Separation and Infinite Maximum Likelihood Estimates. R package version 0.1 (2020).

  • Pebesma, E. Simple features for R: Standardized support for spatial vector data. R J. 10, 439–446 (2018).

    Google Scholar 

  • Pateiro-Lopez, B., Rodriguez-Casal, A. Alphahull: Generalization of the Convex Hull of a Sample of Points in the Plane. R package version 2.2 (2019).

  • Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).

    MATH 

    Google Scholar 

  • Wickham, H. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40, 1–29 (2011).

    Google Scholar 

  • Wickham, H. Forcats: Tools for working with categorical variables (factors). R package version 0.5.0 (2018).

  • Wickham, H., François, R., Henry, L., Müller, K. dplyr: A Grammar of Data Manipulation. R package version 1.0.0 (2021).

  • Birtchnell, M. J. & Gibson, M. Long-term flowering patterns of melliferous Eucalyptus (Myrtaceae) species. Aust. J. Bot. 54, 745–754 (2006).

    Google Scholar 

  • Steinhauer, N. et al. Drivers of colony losses. Curr. Opin. Insect Sci. 26, 142–148 (2018).

    PubMed 

    Google Scholar 

  • Cunningham, S. A., Heard, T. & FitzGibbon, F. The future of pollinators for Australian Agriculture. Aust. J. Agric. Res. 53, 893–900 (2002).

    Google Scholar 

  • Hinson, E. M., Duncan, M., Lim, J., Arundel, J. & Oldroyd, B. P. The density of feral honey bee (Apis mellifera) colonies in South East Australia is greater in undisturbed than in disturbed habitats. Apidologie 46, 403–413 (2015).

    Google Scholar 

  • McIntyre, S. Ecological and anthropomorphic factors permitting low-risk assisted colonization in temperate grassy woodlands. Biol. Conserv. 144, 1781–1789 (2011).

    Google Scholar 

  • Steffan-Dewenter, I. & Kuhn, A. Honeybee foraging in differentially structured landscapes. Proc. R. Soc. B Biol. Sci. 270, 569–575 (2003).

    Google Scholar 

  • Wintle, B. A. et al. Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proc. Natl. Acad. Sci. U.S.A. 116, 909–914 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Arthur, A. D., Li, J., Henry, S. & Cunningham, S. A. Influence of woody vegetation on pollinator densities in oilseed Brassica fields in an Australian temperate landscape. Basic Appl. Ecol. 11, 406–414 (2010).

    Google Scholar 

  • Lindenmayer, D. B. et al. New policies for old trees: Averting a global crisis in a keystone ecological structure. Conserv. Lett. 7, 61–69 (2014).

    Google Scholar 

  • Crane, M. J., Lindenmayer, D. B. & Cunningham, R. B. The value of countryside elements in the conservation of a threatened arboreal marsupial Petaurus norfolcensis in agricultural landscapes of south-eastern Australia—the disproportional value of scattered trees. PLoS One 9, e107178 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gibbons, P., Lindenmayer, D. B., Barry, S. C. & Tanton, M. T. Hollow selection by vertebrate fauna in forests of southeastern Australia and implications for forest management. Biol. Conserv. 103, 1–12 (2002).

    Google Scholar 

  • Seeley, T. D. & Morse, R. A. The nest of the honey bee (Apis mellifera L.). Insectes Soc. 23, 495–512 (1976).

    Google Scholar 

  • Hung, K. L. J., Ascher, J. S., Davids, J. A. & Holway, D. A. Ecological filtering in scrub fragments restructures the taxonomic and functional composition of native bee assemblages. Ecology 100, e02654 (2019).

    PubMed 

    Google Scholar 

  • Cockle, K. L., Martin, K. & Drever, M. C. Supply of tree-holes limits nest density of cavity-nesting birds in primary and logged subtropical Atlantic forest. Biol. Conserv. 143, 2851–2857 (2010).

    Google Scholar 

  • Heard, T. Stingless bees. In Australian Native Bees: A Practical Hand Book 106–139 (NSW Department of Primary Industries, 2016).

  • Geoscience Australia 2006. GEODATA TOPO 250K. Commonwealth of Australia. http://pid.geoscience.gov.au/dataset/ga/63999 (accessed 11 December 2020).


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