Colonizing the east and the west: distribution and niche properties of a dwarf Asian honey bee invading Africa, the Middle East, the Malay Peninsula, and Taiwan
Abstract
Species invasions are expected to increase continuously with undeniable impact upon native biodiversity, being an important process in relation to the decline of native pollinators. We used species distribution models and multivariate analyses to assess the climatic niche properties of the red dwarf honey bee, Apis florea Fabricius (Apidae: Apini), an open-nesting species native to southern Asia and parts of the Middle East, currently invading East Africa, Sundaic tropical Southeast Asia (Peninsular Malaysia and Singapore), and East Asia (Taiwan). The species’ niche was relatively conserved, with the climatic conditions in all its invaded range overlapped by those from its native one. Its potential distribution in Africa and the Indomalayan region is broad, with anthropogenic areas likely providing new habitats and dispersal corridors in areas that were formerly too arid or too heavily forested to allow its dispersal. Future studies to evaluate the potential impacts of A. florea in invaded ranges are encouraged.
Keywords
species distribution models macroecology invasion process Asia AfricaNotes
Acknowledgments
The authors thank three independent reviewers who provided significant suggestions that considerably improved a previous version of this study.
Author contribution
DPS and MSE conceived this research and designed the experiments; MSE, JSA, JCT, ASA, and MSE provided the data; DPS, ACFC, and BV analyzed the data; and DPS, ACFC, BV, JSA, JCT, ASA, XRO, and MSE wrote the paper.
Funding information
The International Scientific Partnership Program (ISPP) at King Saud University through ISPP #0083 supported parts of this project. Also, this study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES), while the compilation of distributional records was supported in part by the National Research Foundation Singapore grant R-154-000-673-651.
Supplementary material
References
- Allouche, O., Tsoar, A., Kadmon, R. (2006) Assessing the accuracy of species distribution models: Prevalence, Kappa and the True Skill Statistic (TSS). J. Appl. Ecol. 43,1223–1232.CrossRefGoogle Scholar
- Araújo, M., New, M. (2007) Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47.PubMedCrossRefGoogle Scholar
- Ascher, J.S., Soh, Z.W.W., Ho, B.M., Lee, R.Y.Y., Leong, A.Q.E., Chui, S.X., Lai., J.J.L., Lee, J.X.Q., Foo, M.S. (2019) Bees of the Bukit Timah Nature Reserve and vicinity. Gard Bull Singapore 71, 245–271.CrossRefGoogle Scholar
- Bezabih, G., Adgaba, N., Hepburn, H.R., Pirk, C.W.W. (2014) The territorial invasion of Apis florea in Africa. Afr. Entomol. 22, 888–890.CrossRefGoogle Scholar
- Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J. T., Duncan, R. P., et al (2011) A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339.PubMedCrossRefGoogle Scholar
- Bortolotti, L., Luthi, F., Flaminio, S., Bogo, G., Sgolastra, F. (2018). First record of the Asiatic bee Megachile disjunctiformis in Europe. Bull. Insectology 71, 143–149.Google Scholar
- Braaker, S., Ghazoul, J., Obrist, M.K., Moretti, M. (2014) Habitat connectivity shapes urban arthropod communities: the key role of green roofs. Ecology 95, 1010–1021.PubMedCrossRefGoogle Scholar
- Breiman, L. (2001) Random forests. Mach. Learn. 45, 5–32.CrossRefGoogle Scholar
- Broennimann, O., Fitzpatrick, M.C., Pearman, P.B., Petitpierre, B., Pellissier, L., et al. (2012) Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr. 21, 481–497.CrossRefGoogle Scholar
- Butz-Huryn, V.M. (1997) Ecological impacts of introduced honey bees. Q. Rev. Biol. 72, 275–297.CrossRefGoogle Scholar
- Cane, J.H., Tepedino, V.J. (2017) Gauging the effect of honey bee pollen collection on native bee communities. Conserv. Lett. 10, 205–210.CrossRefGoogle Scholar
- Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F. T., D’Amen, M., et al (2017) ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography 40, 774–787.CrossRefGoogle Scholar
- Google Inc. (2018) Google Earth, version 7.0.3.8542Google Scholar
- Goulson, D. (2003) Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 34, 1–26.CrossRefGoogle Scholar
- Guisan, A., Edwards, T.C., Hastie, T. (2002) Generalized linear and generalized additive models in studies of species distributions: Setting the scene. Ecol. Modell. 157, 89–100.CrossRefGoogle Scholar
- Guisan, A., Petitpierre, B., Broennimann, O., Daehler, C., Kueffer, C. (2014) Unifying niche shift studies: Insights from biological invasions. Trends Ecol. Evol. 29, 260–269.PubMedCrossRefGoogle Scholar
- Guo, Q.H., Kelly, M., Graham, C.H. (2005) Support vector machines for predicting distribution of sudden oak death in California. Ecol. Modell. 182, 75–90.CrossRefGoogle Scholar
- Hastie, T., Tibshirani, R. (1986) Generalized Additive Models. Stat. Sci. 1, 297–310.CrossRefGoogle Scholar
- Hennig, E.I., Ghazoul, J. (2012) Pollinating animals in the urban environment. Urban Ecosyst 15, 149–166.CrossRefGoogle Scholar
- Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P. G., Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978.CrossRefGoogle Scholar
- Hill, M.P., Gallardo, B., Terblanche, J.S. (2017) A global assessment of climatic niche shifts and human influence in insect invasions. Glob. Ecol. Biogeogr. 26, 679-689 .CrossRefGoogle Scholar
- Hinojosa-Díaz, I.A., Yáñez-Ordóñez, O., Chen, G., Peterson, A. T., Engel, M. S. (2005) The North American invasion of the giant resin bee (Hymenoptera: Megachilidae). J. Hymenopt. Res. 14, 69–77.Google Scholar
- Jarnevich, C.S., Esaias, W.E., Ma, P.L.A., Morisette, J. T., Nickeson, J. E. et al. (2014) Regional distribution models with lack of proximate predictors: Africanized honeybees expanding north. Divers. Distrib. 20, 193–201. doi: https://doi.org/10.1111/ddi.12143 CrossRefGoogle Scholar
- Jiménez-Valverde, A., Lobo, J.M. (2006) The ghost of unbalanced species distribution data in geographical model predictions. Divers. Distrib. 12, 521–524.CrossRefGoogle Scholar
- Jiménez-Valverde, A., Lobo, J.M. (2007) Threshold criteria for conversion of probability of species presence to either-or presence–absence. Acta Oecologica, 31, 361–369.CrossRefGoogle Scholar
- Jiménez-Valverde, A., Peterson, A.T., Soberón, J., Overton, J. M., Aragón, P., et al. (2011) Use of niche models in invasive species risk assessments. Biol. Invasions 13, 2785–2797.CrossRefGoogle Scholar
- Keane, R.M., Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170.CrossRefGoogle Scholar
- Koetz, A. (2013) Ecology, behaviour and control of Apis cerana with a focus on relevance to the Australian incursion. Insects 4, 558–592.PubMedPubMedCentralCrossRefGoogle Scholar
- Le Feón, V., Aubert, M., Genoud, D., Andrieu-Ponel, V., Westrich, P., et al (2018) Range expansion of the Asian native giant resin bee Megachile sculpturalis (Hymenoptera, Apoidea, Megachilidae) in France. Ecol. Evol. 8, 1534–1542.PubMedPubMedCentralCrossRefGoogle Scholar
- Liow, L.H., Sodhi, N.S., Elmqvist, T. (2001) Bee diversity along a disturbance gradient in tropical lowland forests of south-east Asia. J Appl Ecol 38, 180–192.CrossRefGoogle Scholar
- Lobo, J.M., Tognelli, M.F. (2011) Exploring the effects of quantity and location of pseudo-absences and sampling biases on the performance of distribution models with limited point occurrence data. J. Nat. Conserv. 19, 1–7.CrossRefGoogle Scholar
- Mossagegh, M.S. (1993) New geographical distribution line of Apis florea in Iran. In: Conner LJ, Rinderer T, Sylvester HA, Wongsiri S (eds) Asian Apiculture, 1st edn. Wicwas Press, Cheshire, pp 64–66Google Scholar
- Müller-Schärer, H., Schaffner, U. (2008) Classical biological control: Exploiting enemy escape to manage plant invasions. Biol. Invasions 10, 859–874.CrossRefGoogle Scholar
- Muscarella, R., Galante, P.J., Soley-Guardia, M., Boria, R. A., Kass, J. M., et al (2014) ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol. Evol. 5, 1198–1205.CrossRefGoogle Scholar
- Oldroyd, B., Nanork, P. (2009) Conservation of Asian honey bees. Apidologie 40, 296–312CrossRefGoogle Scholar
- Paini, D.R. (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review. Austral Ecol. 29, 399–407.CrossRefGoogle Scholar
- Paini, D.R., Sheppard, A.W., Cook, D.C., De Barro, P.J., Worner, S. P., et al. (2016) Global threat to agriculture from invasive species. Proc Natl Acad Sci USA 113, 7575–7579.PubMedCrossRefGoogle Scholar
- Pejchar, L., Mooney, H.A. (2009) Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 24, 497–504.PubMedCrossRefGoogle Scholar
- Petitpierre, B., Kueffer, C., Broennimann, O., Randin, C., Daehler, C., et al. (2012) Climatic niche shifts are rare among terrestrial plant invaders. Science 335, 1344–1348.PubMedCrossRefGoogle Scholar
- Phillips, S.J., Anderson, R.P., Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecol. Modell. 190, 231–259.CrossRefGoogle Scholar
- Phillips, S.J., Dudík, M. (2008) Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography 31, 161–175.CrossRefGoogle Scholar
- Pimentel, D., Zuniga, R., Morrison, D. (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52, 273–288.CrossRefGoogle Scholar
- Pyke, G.H., Ehrlich, P.R. (2010) Biological collections and ecological/environmental research: A review, some observations and a look to the future. Biol. Rev. 85, 247–266.PubMedCrossRefGoogle Scholar
- Quaranta, M., Sommaruga, A., Balzarini, P., Felicioli, A. (2014) A new species for the bee fauna of Italy: Megachile sculpturalis continues its colonization of Europe. Bull. Insectology 67, 287–293.Google Scholar
- Radloff, S.E., Hepburn, H.R., Engel, M.S. (2011) The Asian species of Apis. In: Hepburn HR, Radloff SE (eds) Honeybees of Asia, 1st edn. Springer, Berlin, pp 1–22.Google Scholar
- Richardson, D.M., Pysek, P., Rejmanek, M., Wightman, J., Simmonds, C., et al. (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6, 93–107.CrossRefGoogle Scholar
- Roberts, D.R., Bahn, V., Ciuti, S., Boyce, M. S., Elith, J., et al. (2017) Cross-validation strategies for data with temporal, spatial, hierarchical, or phylogenetic structure. Ecography 40, 913–929.CrossRefGoogle Scholar
- Russo, L. (2016) Positive and negative impacts of non-native bee species around the world. Insects 7, 69.PubMedCentralCrossRefPubMedGoogle Scholar
- Schoener, T.W. (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology, 51, 408–418.CrossRefGoogle Scholar
- Schölkopf, B., Platt, J.C., Shawe-Taylor, J., Smola, A. J., Williamson, R. C. (2001) Estimating the support of a high-dimensional distribution. Neural Comput. 13, 1443–71.PubMedCrossRefGoogle Scholar
- Shebl, M.A. (2017) Discovery of Apis florea colonies in northeastern Egypt. African Entomol. 25, 248–248.CrossRefGoogle Scholar
- Shield, J. (2007) The Asian Honey Bee: Report of an incursion in Cairns 2007 - Technical aspects of the response. Department of Primary Industries and Fisheries (Ed.). Brisbane: pp: 1-106.Google Scholar
- Silva, D.P., Gonzalez, V.H., Melo, G.A.R., Lucia, M., Alvarez, L. J., et al. (2014) Seeking the flowers for the bees: Integrating biotic interactions into niche models to assess the distribution of the exotic bee species Lithurgus huberi in South America. Ecol. Modell. 273, 200–209.CrossRefGoogle Scholar
- Silva, D.P., Vilela, B., Buzatto, B.A., Moczek, A. P., Hortal, J. (2016) Contextualized niche shifts upon independent invasions by the dung beetle Onthophagus taurus. Biol. Invasions 18, 3137–3148.CrossRefGoogle Scholar
- Soberón, J., 2007. Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10, 1115–1123.PubMedCrossRefGoogle Scholar
- Strange, J.P., Koch, J.B., Gonzalez, V.H., Nemelka, L., Griswold, T. (2011) Global invasion by Anthidium manicatum (Linnaeus) (Hymenoptera: Megachilidae): assessing potential distribution in North America and beyond. Biol. Invasions 13, 2115–2133.CrossRefGoogle Scholar
- Strubbe, D., Broennimann, O., Chiron, F., Matthysen, E. (2013) Niche conservatism in non-native birds in Europe: Niche unfilling rather than niche expansion. Glob. Ecol. Biogeogr. 22, 962–970.CrossRefGoogle Scholar
- Tax, D.M.J., Duin, R.P.W. (2004) Support vector data description. Mach. Learn. 54, 45–66.CrossRefGoogle Scholar
- Threlfall, C.G., Mata, L., Mackie, J.A., Hahs, A. K., Stork, N. E., Williams, N. S.G., Livesley, S. J. (2017) Increasing biodiversity in urban green spaces through simple vegetation interventions. J Appl Ecol 54, 1874–1883.CrossRefGoogle Scholar
- Tylianakis, J.M., Didham, R.K., Bascompte, J., Wardle, D.A. (2008) Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363.PubMedCrossRefGoogle Scholar
- VanDerWal, J., Shoo, L.P., Johnson, C.N., Williams, S.E. (2009) Abundance and the environmental niche: Environmental suitability estimated from niche models predicts the upper limit of local abundance. Am. Nat. 174, 282–291.PubMedCrossRefGoogle Scholar
- Vanhatalo, J., Veneranta, L., Hudd, R. (2012) Species distribution modeling with Gaussian processes: A case study with the youngest stages of sea spawning whitefish (Coregonus lavaretus L. s.l.) larvae. Ecol. Modell. 228, 49–58.CrossRefGoogle Scholar
- Vital, M.V.C., Hepburn, R., Radloff, S., Fuchs, S. (2012) Geographic distribution of africanized honeybees (Apis mellifera) reflects niche characteristics of ancestral african subspecies. Nat. Conserv. 10, 184–190.CrossRefGoogle Scholar
- Warren, D.L., Glor, R.E., Turelli, M. (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62, 2868–2883.PubMedCrossRefGoogle Scholar
- Westrich, P., Knapp, A., Berney, I. (2015) Megachile sculpturalis Smith 1853 (Hymenoptera, Apidae), a new species for the bee fauna of Germany, now north of the Alps. Eucera 9, 3–10.Google Scholar