Cedric Alaux
Yves Le Conte
Axel Decourtye- 1INRA, UR406 Abeilles et Environnement, Avignon, France
- 2UMT PrADE, Avignon, France
- 3ITSAP-Institut de l'abeille, Avignon, France
- 4ACTA, Avignon, France
Significant losses of managed honey bee colonies (Apis mellifera L.) have been reported annually around the world (Neumann and Carreck, 2010; Potts et al., 2010). It is also well-established that wild bees face localized and broad-scale threats as a result of human activities, including land-use intensification (pesticide use and lack of food resources) and the spread of invasive species and diseases (Potts et al., 2016). Consequently, in recent decades, the species richness of most groups of pollinating bees has declined across Europe and North America (Biesmeijer et al., 2006; Cameron et al., 2011; Burkle et al., 2013; Ollerton et al., 2014).
However, managed honey bees themselves may exacerbate these pressures on wild bee populations, thereby decreasing wild bee abundance and diversity (Russo, 2016; Geslin et al., 2017). For instance, increased densities of managed honey bees in their native and non-native ranges could affect wild bees via resource competition and changes in plant communities (see for a review Mallinger et al., 2017, or disease transmission Fürst et al., 2014; Vanbergen et al., 2018). Indeed, despite some inconsistency of effects, studies mostly reported negative influences of managed honeybees on wild bees (Mallinger et al., 2017). Moreover, honey bees (whether managed or wild) could pose broader risks to non-native ecosystems (e.g., North and South America, Eastern Asia and Australia) by interfering with local pollinators for the pollination of local flora, increasing seed sets of exotic weeds, and competing with other organisms (e.g., bees, birds, mammals) for nesting cavities (Goulson, 2003; Russo, 2016; Ollerton, 2017). Finally, another consequence of the spread of the European honey bee around the world is the progressive replacement of beekeeping with native bees [e.g., A. cerana F. in Asia (Theisen-Jones and Bienefeld, 2016) and stingless bees in Mexico (Quezada-Euán, 2018)] by A. mellifera L., which is more productive but might threaten local biodiversity.
As a consequence, the pressure of managed honey bees on wild bees has led to a growing debate between the need for the conservation of native and wild bees and the use of managed honey bees in natural and protected areas (Geldmann and González-Varo, 2018; González-Varo and Geldmann, 2018; Kleijn et al., 2018; Saunders et al., 2018).
It was notably advised that managed honey bees should not be placed in protected areas, but only in agricultural areas, to conserve and avoid damage to wild pollinators (Colla and MacIvor, 2017; Geldmann and González-Varo, 2018). This claim was first made without discriminating the native and non-native ranges of managed honey bees (Geldmann and González-Varo, 2018) and later, the authors advocated that within their native range, a limited number of honey bee hives could be placed in protected areas (González-Varo and Geldmann, 2018). While we agree that extensive use of managed honey bees may be problematic for wildlife conservation and we should control the number of hives in native, protected areas, we believe that, contrary to the situation in non-native regions, pitting wild bees against managed honey bees in their native range is counterproductive with regards to the conservation of honey bee biodiversity. Indeed, the western honey bee Apis mellifera L. is also a component of biodiversity in its native range (Africa, Europe, Western, and Central Asia), where it has adapted to diverse environmental conditions and natural habitats (De la Rua et al., 2009). The conservation of honey bee biodiversity would therefore benefit from the maintenance of small-scale beekeeping management and conservation areas in natural and protected lands.
Honey Bee Biodiversity in Its Native Range
Despite a long-standing exploitation of honey bees by humans, which dates back nearly 9,000 years (Roffet-Salque et al., 2015), endemic subspecies-specific phenotypes and genetic footprints can still be identified in the honey bee native range (De la Rua et al., 2009; De la Rúa et al., 2013; Meixner et al., 2010). In addition, the number of subspecies, originally estimated at 26 (10 in Europe), has recently increased with the description of two new subspecies in Africa [A. m. simensis, (Meixner et al., 2011)], and Asia [A. m. sinisxinyuan, (Chen et al., 2016)]. The presence of previously unidentified subspecies would also suggest that the actual native range of A. mellifera is not completely defined. Indeed, the discovery of A. m. pomonella in 2003 further extended the endemic range of A. mellifera by about 2,000 km eastward (Sheppard and Meixner, 2003).
This natural diversity of honey bee populations (each generally composed of both managed and feral colonies) reflects a large range of local and regional adaptations to various ecological conditions. Indeed, subspecies, which have been estimated to diverge 0.7–1.3 million years ago (Garnery et al., 1992; Arias and Sheppard, 1996), and ecotypes have developed behavioral and phenological adaptations to local environments, characterized by specific climatic conditions and patterns of resource availability (Ruttner, 1988; De la Rua et al., 2009). For instance, the Landes ecotype of A. m. mellifera (southwest France), described in managed honey bee populations, has tightly linked its annual brood cycle to the local floral phenology of ling heather (Calluna vulgaris L.) (Louveaux et al., 1966). This ecotype is quite persistent, because 40 years later, half of the local managed colonies (Landes) that were tested were found to have a brood cycle similar to the one described in 1966 (Strange et al., 2007). Another example is the climate-driven separation of the two subspecies A. m. carnica and A. m. macedonica at an average threshold temperature of 9°C (Coroian et al., 2014): A. m. carnica being more abundant in areas with an average temperature below 9°C and inversely for A. m. macedonica.
Genetic Conservation of Honey Bees in Their Native Range
The conservation of these honey bee populations (feral and managed colonies) is a pressing priority, given that their survival in natural habitats is endangered by the same factors that affect wild pollinators (De la Rua et al., 2009; Jaffé et al., 2010; Meixner et al., 2010; Goulson et al., 2015). Furthermore, endemic populations are highly adapted to their local environment through a range of unique behavioral and morphological traits, such that removal from their native range is associated with lower survival and productivity (Buchler et al., 2014). For instance, some managed populations have been found to naturally survive Varroa mite infestation, a major pest of honey bee colonies (Locke, 2016). However, when removed from their native environment, these populations became as sensitive to Varroa as non-resistant local populations, suggesting that the mechanism of mite resistance is dependent on genotype-environment interactions (Buchler et al., 2014; Meixner et al., 2014, 2015). Therefore, the diversity of honey bee populations constitutes a great natural heritage that needs to be preserved, notably for preventing colony losses. This is further supported by the European regulation on organic beekeeping, which recommends “the use of European breeds of Apis mellifera L. and local genotypes” (Council Regulation ECN°889/2008)1.
For that purpose, we concur that beekeeping in protected areas should be done in a way that is not detrimental to wildlife (e.g., restricted number of colonies). While it is not yet known what would constitute a safe level of managed honey bee colonies, small-scale beekeeping management could be a win-win situation for both the conservation of wild bees and honey bee biodiversity. The number of managed honey bee colonies in protected areas needs to be small enough that it would limit the impact of resource competition and disease transmission to wild bees but still allow the implementation of conservation areas for managed honey bee colonies. These conservations areas managed by technical institutes or beekeeper associations (non-profit organization) would then facilitate the development of conservation genetics programs. For instance, four conservation areas have been created in nature reserves of Switzerland for preserving the local honey bee subspecies A. m. mellifera (Parejo et al., 2016). Downsizing beekeeping management of local honey bees in such conservation areas would also reduce potential disease transmission and protect feral colonies in the vicinity. Feral colonies, which represent a reservoir of genetic diversity (Oleksa et al., 2013), can be important for the maintenance of endemic populations by beekeepers and conservation programs (management of wild-caught swarms). However, the use or protection of feral colonies should be considered as a complementary management measure to conserve honey bee genetic diversity rather than an exclusive solution since their nests are hard to detect, and therefore their number, densities, survival, and genetic background are very difficult to assess (Jaffé et al., 2010; Kohl and Rutschmann, 2018) as compared to managed honey bee colonies.
As for the extreme scenario in which managed honey bees should be limited to agricultural areas, beekeepers would need to intensify their practices to compensate for colony losses due to resource scarcity and pollution, resulting in revenue loss due to the low price of honey from mass-flowering crops. As a result, intensive beekeeping would threaten the extinction of local honey bee populations by favoring the expansion of only the most productive (high honey yields) and adaptive subspecies or ecotypes that thrive in agricultural areas. The use of non-local honey bees would also reinforce the development of admixed populations, which may have a higher genetic diversity (Harpur et al., 2012) but which would contribute to the loss of important naturally–selected traits (De la Rúa et al., 2013). This would be counterproductive given that the current challenge of livestock production is to limit overbreeding and the loss of valuable local adaptations in order to adapt to rapidly changing environments (e.g., climate change, spread of new diseases) (Notter, 1999).
Finally, preserving the management of endemic honey bee subspecies in their natural habitats would not only benefit the conservation of honey bee biodiversity but would also help to adapt beekeeping activity and crop pollination to climate change (Le Conte and Navajas, 2008). Indeed, maintaining a reservoir of adaptive traits to different climatic regions in the native ecosystem will be extremely useful for selecting honey bee populations that are best suited for providing pollination services of crops under new climatic conditions, whether it is in their native or non-native range.
Conclusion
We do not dispute that a high density of managed honey bees may introduce resource competition with wild pollinators and favor the spread of diseases. Indeed, it seems unavoidable to prevent (non-native range) or limit (native range) the access of managed honey bees to areas where wild pollinator species are threatened (Henry and Rodet, 2018). However, in the current context of a fast-evolving biodiversity crisis at global and local scales, there is a need for implementing adequate policies to protect native and locally adapted honey bees since they provide an important reservoir of adaptation for beekeeping activity and crop pollination services. For that purpose, rather than creating opposition between managed honey bees and wild pollinators, and creating conflicts between stakeholders, we need to find ways to reconcile wild pollinator conservation with responsible and sustainable beekeeping practices in natural and/or protected areas of the honey bee native range (e.g., conservation areas for local honey bees). Therefore, before considering any exclusion of managed honey bees from their native and natural habitats, we should start with conservation policies that place priority on the restoration of native habitats to support all bees, managed and wild.
Author Contributions
CA and AD conceived and wrote the paper. YLC provided new ideas and participated in writing.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Footnotes
1. ^Commission Regulation (EC) (2008). Laying Down Detailed Rules for the Implementation of Council Regulation (EC) No 834/2007 on Organic Production and Labeling of Organic Products With Regard to Organic Production, Labeling and Control. No 889/2008.
References
Arias, M. C., and Sheppard, W. S. (1996). Molecular phylogenetics of honey bee subspecies (Apis mellifera L) inferred from mitochondrial DNA sequence. Mol. Phylogenet. Evol. 5, 557–566. doi: 10.1006/mpev.1996.0050
Biesmeijer, J. C., Roberts, S. P., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., et al. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354. doi: 10.1126/science.1127863
Buchler, R., Costa, C., Hatjina, F., Andonov, S., Meixner, M. D., Le Conte, Y., et al. (2014). The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. J. Apicult. Res. 53, 205–214. doi: 10.3896/IBRA.1.53.2.03
Burkle, L. A., Marlin, J. C., and Knight, T. M. (2013). Plant-pollinator interactions over 120 Years: loss of species, Co-occurrence, and function. Science 339, 1611–1615. doi: 10.1126/science.1232728
Cameron, S. A., Lozier, J. D., Strange, J. P., Koch, J. B., Cordes, N., Solter, L. F., et al. (2011). Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U.S.A. 108, 662–667. doi: 10.1073/pnas.1014743108
Chen, C., Liu, Z., Pan, Q., Chen, X., Wang, H., Guo, H., et al. (2016). Genomic analyses reveal demographic history and temperate adaptation of the newly discovered honey bee subspecies Apis mellifera sinisxinyuan n. ssp. Mol. Biol. Evol. 33, 1337–1348. doi: 10.1093/molbev/msw017
Colla, S. R., and MacIvor, J. S. (2017). Questioning public perception, conservation policy, and recovery actions for honeybees in North America. Conserv. Biol. 31, 1202–1204. doi: 10.1111/cobi.12839
Coroian, C. O., Muñoz, I., Schlüns, E. A., Paniti-Teleky, O. R., Erler, S., Furdui, E. M., et al. (2014). Climate rather than geography separates two European honeybee subspecies. Mol. Ecol. 23, 2353–2361. doi: 10.1111/mec.12731
De la Rua, P., Jaffe, R., Dall'Olio, R., Munoz, I., and Serrano, J. (2009). Biodiversity, conservation and current threats to European honeybees. Apidologie 40, 263–284. doi: 10.1051/apido/2009027
De la Rúa, P., Jaffé, R., Muñoz, I., Serrano, J., Moritz, R. F., and Kraus, F. B. (2013). Conserving genetic diversity in the honeybee: comments on harpur et al. (2012). Mol. Ecol. 22, 3208–3210. doi: 10.1111/mec.12333
Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J., and Brown, M. J. F. (2014). Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366. doi: 10.1038/nature12977
Garnery, L., Cornuet, J. M., and Solignac, M. (1992). Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1, 145–154. doi: 10.1111/j.1365-294X.1992.tb00170.x
Geldmann, J., and González-Varo, J. P. (2018). Conserving honey bees does not help wildlife. Science 359, 392–393. doi: 10.1126/science.aar2269
Geslin, B., Gauzens, B., Baude, M., Dajoz, I., Fontaine, C., Henry, M., et al. (2017). Massively introduced managed species and their consequences for plant-pollinator interactions. Networks of invasion: empirical evidence and case studies. Adv. Ecol. Res. 57, 147–199. doi: 10.1016/bs.aecr.2016.10.007
González-Varo, J. P., and Geldmann, J. (2018). Bee conservation: inclusive solutions response. Science 360, 390–390. doi: 10.1126/science.aat3746
Goulson, D. (2003). Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 34, 1–26. doi: 10.1146/annurev.ecolsys.34.011802.132355
Goulson, D., Nicholls, E., Botías, C., and Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. doi: 10.1126/science.1255957
Harpur, B. A., Minaei, S., Kent, C. F., and Zayed, A. (2012). Management increases genetic diversity of honey bees via admixture. Mol. Ecol. 21, 4414–4421. doi: 10.1111/j.1365-294X.2012.05614.x
Henry, M., and Rodet, G. (2018). Controlling the impact of the managed honeybee on wild bees in protected areas. Sci. Rep. 8:9308. doi: 10.1038/s41598-018-27591-y
Jaffé, R., Dietemann, V., Allsopp, M. H., Costa, C., Crewe, R. M., Dall'olio, R., et al. (2010). Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 24, 583–593. doi: 10.1111/j.1523-1739.2009.01331.x
Kleijn, D., Biesmeijer, K., Dupont, Y. L., Nielsen, A., Potts, S. G., and Settele, J. (2018). Bee conservation: inclusive solutions. Science 360, 389–390. doi: 10.1126/science.aat2054
Kohl, P. L., and Rutschmann, B. (2018). The neglected bee trees: european beech forests as a home for feral honey bee colonies. Peer J. 6:e4602. doi: 10.7717/peerj.4602
Le Conte, Y., and Navajas, M. (2008). Climate change: impact on honey bee populations and diseases. Rev. Sci. Tech. Off. Int. Epiz. 27, 499–510.
Locke, B. (2016). Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47, 467–482. doi: 10.1007/s13592-015-0412-8
Louveaux, J., lbisetti, M., Delangue, M., and Theurkauff, D. (1966). Les modalités de l'adaptation des abeilles (Apis mellifica L.) au milieu naturel. Ann. Abeille 9, 323–350.
Mallinger, R. E., Gaines-Day, H. R., and Gratton, C. (2017). Do managed bees have negative effects on wild bees?: a systematic review of the literature. PLos ONE 12:e0189268. doi: 10.1371/journal.pone.0189268
Meixner, M. D., Costa, C., Kryger, P., Hatjina, F., Bouga, M., Ivanova, E., et al. (2010). Conserving diversity and vitality for honey bee breeding. J. Apicult. Res. 49, 85–92. doi: 10.3896/IBRA.1.49.1.12
Meixner, M. D., Francis, R. M., Gajda, A., Kryger, P., Andonov, S., Uzunov, A., et al. (2014). Occurrence of parasites and pathogens in honey bee colonies used in a European genotype-environment interactions experiment. J. Apicult. Res. 53, 215–229. doi: 10.3896/IBRA.1.53.2.04
Meixner, M. D., Kryger, P., and Costa, C. (2015). Effects of genotype, environment, and their interactions on honey bee health in Europe. Curr. Opin. Insect Sci. 10, 177–184. doi: 10.1016/j.cois.2015.05.010
Meixner, M. D., Leta, M. A., Koeniger, N., and Fuchs, S. (2011). The honey bees of Ethiopia represent a new subspecies of Apis mellifera-Apis mellifera simensis n. ssp. Apidologie 42, 425–437. doi: 10.1007/s13592-011-0007-y
Neumann, P., and Carreck, N. L. (2010). Honey bee colony losses. J. Apicult. Res. 49, 1–6. doi: 10.3896/IBRA.1.49.1.01
Notter, D. R. (1999). The importance of genetic populations diversity in livestock populations of the future. J. Anim. Sci. 77, 61–69. doi: 10.2527/1999.77161x
Oleksa, A., Gawronski, R., and Tofilski, A. (2013). Rural avenues as a refuge for feral honey bee population. J. Insect Conserv. 17, 465–472. doi: 10.1007/s10841-012-9528-6
Ollerton, J. (2017). Pollinator diversity: distribution, ecological function, and conservation. Annu. Rev. Ecol. Evol. Syst. 48, 353–376. doi: 10.1146/annurev-ecolsys-110316-022919
Ollerton, J., Erenler, H., Edwards, M., and Crockett, R. (2014). Pollinator declines. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346, 1360–1362. doi: 10.1126/science.1257259
Parejo, M., Wragg, D., Gauthier, L., Vignal, A., Neumann, P., and Neuditschko, M. (2016). Using whole-genome sequence information to foster conservation efforts for the european dark honey bee, Apis mellifera mellifera. Front. Ecol. Evol. 4:140. doi: 10.3389/fevo.2016.00140
Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., et al. (2016). Safeguarding pollinators and their values to human well-being. Nature 540, 220–229. doi: 10.1038/nature20588
Potts, S. G., Roberts, S. P. M., Dean, R., Marris, G., Brown, M. A., Jones, H. R., et al. (2010). Declines of managed honey bees and beekeepers in Europe. J. Apicult. Res. 49, 15–22. doi: 10.3896/IBRA.1.49.1.02
Quezada-Euán, J. J. G. (2018). Stingless Bees of Mexico: The Biology, Management and Conservation of An Ancient Heritage. New York, NY: Springer, 294.
Roffet-Salque, M., Regert, M., Evershed, R. P., Outram, A. K., Cramp, L. J., Decavallas, O., et al. (2015). Widespread exploitation of the honeybee by early Neolithic farmers. Nature 527, 226–231. doi: 10.1038/nature15757
Russo, L. (2016). Positive and negative impacts of non-native bee species around the world. Insects 7:E69. doi: 10.3390/insects7040069
Saunders, M. E., Smith, T. J., and Rader, R. (2018). Bee conservation: key role of managed bees. Science 360, 389–389. doi: 10.1126/science.aat1535
Sheppard, W. S., and Meixner, M. D. (2003). Apis mellifera pomonella, a new honey bee subspecies from Central Asia. Apidologie 34, 367–375. doi: 10.1051/apido:2003037
Strange, J. P., Garnery, L., and Sheppard, W. S. (2007). Persistence of the Landes ecotype of Apis mellifera mellifera in southwest France: confirmation of a locally adaptive annual brood cycle trait. Apidologie 38, 259–267. doi: 10.1051/apido:2007012
Theisen-Jones, H., and Bienefeld, K. (2016). The Asian Honey Bee (Apis cerana) is Significantly in Decline. Bee World 93, 90–97. doi: 10.1080/0005772X.2017.1284973
Keywords: biodiversity, local adaptation, pollinator, subspecies, ecotype, natural habitats, native range
Citation: Alaux C, Le Conte Y and Decourtye A (2019) Pitting Wild Bees Against Managed Honey Bees in Their Native Range, a Losing Strategy for the Conservation of Honey Bee Biodiversity. Front. Ecol. Evol. 7:60. doi: 10.3389/fevo.2019.00060
Received: 14 September 2018; Accepted: 18 February 2019;
Published: 13 March 2019.
Edited by:
Rachel Mallinger, University of Florida, United StatesReviewed by:
Margarita M. Lopez-Uribe, Pennsylvania State University, United StatesCopyright © 2019 Alaux, Le Conte and Decourtye. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Cedric Alaux, Y2VkcmljLmFsYXV4QGlucmEuZnI=