The Signature of Environmental and Parasite Stresses on the Wings of Apis mellifera
DOI:
https://doi.org/10.13102/sociobiology.v72i3.11389Keywords:
Bees, Bioindicator, Environmental stress, Fluctuating asymmetry, Heat stress, Varroa destructorAbstract
The decline of pollinators, particularly Apis mellifera, seriously threatens global ecosystems and agricultural productivity. This study investigated the effects of environmental stress (low vegetation cover, high internal hive temperatures, high internal hive humidity, and high parasitism rate by the mite Varroa destructor) on the fluctuating asymmetry (FA) of honey bee wings in seven apiaries in Dom Joaquim, a reference city for wild honey production in the state of Minas Gerais, Brazil. We evaluated the FA of 18 wing venations of 30 bees from five beehive boxes in seven apiaries, totaling 1050 bees. Our results showed that fluctuating asymmetry (FA) in wing venation traits M4 (P = 0.013), M12 (P = 0.014), M13 (P = 0.020), M14 (P = 0.014), and M18 (P < 0.001) differed significantly among apiaries, likely reflecting variation in local environmental stressors. These differences suggest that site-specific conditions may differentially impact colony stress levels, influencing developmental stability in honey bees. We also noted that the apiaries with lower native forest cover (<50%) and lower floral diversity showed higher FA in the M17 venation. Furthermore, internal hive conditions, such as elevated temperature and mite infestation, were associated with increased FA in venation traits M2 and M18. In contrast, higher humidity levels were linked to increased FA in traits M4 and M17. In general, the results highlight that the FAs of the M2, M17, and M18 wing venations are associated with multiple stress factors, suggesting that the FAs of these venations are the most recommended for use. This research also emphasizes the importance of preserving native vegetation and managing hive conditions to maintain the health and stability of honey bee populations. These results also demonstrate the potential of FA as a bioindicator of environmental stress in A. mellifera, which may help improve beekeeping management practices.
Downloads
References
Abou-Shaara, H.F., Al-Ghamdi, A.A. & Mohamed, A.A. (2012). Tolerance of two honey bee races to various temperature and relative humidity gradients. Environmental and Experimental Biology, 10: 133–138.
Alger, S.A., Burnham, P.A., Lamas, Z.S., Brody, A.K. & Richardson, L.L. (2018). Home sick: Impacts of migratory beekeeping on honey bee (Apis mellifera) pests, pathogens, and colony size. PeerJ, 6: e5812.
Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.D.M. & Sparovek, G. (2013). Köppen's climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711-728.
Amdam, G.V., Hartfelder, K., Norberg, K., Hagen, A. & Omholt, S.W. (2004). Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering? Journal of Economic Entomology, 97: 741-747.
Ashworth, L., Quesada, M., Casas, A., Aguilar, R. & Oyama, K. (2009). Pollinator-dependent food production in Mexico. Biological Conservation, 142: 1050-1057.
Avni, D., Hendriksma, H.P., Dag, A., Uni, Z. & Shafir, S. (2014). Nutritional aspects of honey bee-collected pollen and constraints on colony development in the eastern Mediterranean. Journal of Insect Physiology, 69: 65-73.
Banaji, S. (2022). Colony collapse disorder, neonicotinoids, CO2, climate change, and the four spheres. Open Journal of Ecology, 12: 711-717.
Barour, C. & Baylac, M. (2016). Geometric morphometric discrimination of the three African honeybee subspecies Apis mellifera intermissa, A. m. sahariensis and A. m. capensis (Hymenoptera, Apidae): Fore wing and hind wing landmark configurations. Journal of Hymenoptera Research, 52:61-70.
Becher, M.A., Scharpenberg, H. & Moritz, R.F. (2009). Pupal developmental temperature and behavioral specialization of honeybee workers (Apis mellifera L.). Journal of Comparative Physiology A, 195: 673-679.
Bowen-Walker, P.L. & Gunn, A. (2001). The effect of the ectoparasitic mite, Varroa destructor, on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomologia Experimentalis et Applicata, 101: 207–217.
Breeze, T.D., Bailey, A.P., Balcombe, K.G. & Potts, S.G. (2011). Pollination services in the UK: How important are honeybees? Agriculture, Ecosystems & Environment, 142: 137-143.
Cestaro, L.G., Alves, M.L.T.M.F., Silva, M.V.G.B. & Teixeira, É.W. (2017). Honey bee (Apis mellifera) health in stationary and migratory apiaries. Sociobiology, 64: 42-49.
Brunet, J. & Fragoso, F.P. (2024). What are the main reasons for the worldwide decline in pollinator populations? CABI Reviews, 19: 1-11.
Christmann, S. (2019). Do we realize the full impact of pollinator loss on other ecosystem services and the challenges for any restoration in terrestrial areas? Restoration Ecology, 27: 720-725.
Clarke, G.M. & Oldroyd, B.P. (1996). The genetic basis of developmental stability in Apis mellifera II. Relationships between character size, asymmetry and single-locus heterozygosity. Genetica, 97: 211-224.
Cornelissen, T. & Stiling, P. (2005). Perfect is best: Low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia, 142: 46-56.
Costa, M., Mateus, R.P. & Moura, M.O. (2015). Constant fluctuating asymmetry but not directional asymmetry along the geographic distribution of Drosophila antonietae (Diptera, Drosophilidae). Revista Brasileira de Entomologia, 59: 337-342.
Cuevas-Reyes, P., Canché-Delgado, A., Maldonado-López, Y., Fernandes, G.W., Oyama, K. & González-Rodríguez, A. (2018). Patterns of herbivory and leaf morphology in two Mexican hybrid oak complexes: Importance of fluctuating asymmetry as indicator of environmental stress in hybrid plants. Ecological Indicators, 90: 164-170.
Dalmon, A., Peruzzi, M., Le Conte, Y., Alaux, C. & Pioz, M. (2019). Temperature-driven changes in viral loads in the honey bee Apis mellifera. Journal of Invertebrate Pathology, 160: 87-94.
Di Pasquale, G., Alaux, C., Le Conte, Y., Odoux, J.F., Pioz, M., Vaissière, B.E. & Decourtye, A. (2016). Variations in the availability of pollen resources affect honey bee health. PLoS One, 11: e0162818.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A. & Alaux, C. (2013). Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter? PLoS One, 8: e72016.
Duay, P., De Jong, D. & Engels, W. (2003). Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie, 34:61–65.
Ellis, M.B., Nicolson, S.W., Crewe, R.M. & Dietemann, V. (2008). Hygropreference and brood care in the honeybee (Apis mellifera). Journal of Insect Physiology, 54: 1516-1521.
Ellis, R.A., Weis, T., Suryanarayanan, S. & Beilin, K. (2020). From a free gift of nature to a precarious commodity: Bees, pollination services, and industrial agriculture. Journal of Agrarian Change, 20: 437-459.
Eskov, E.K. (2018). Exo-and endogenous water in the honeybee Body (Apis mellifera, Hymenoptera, Apidae). Entomological Review, 98: 129-137.
Evans, J.D. & Chen, Y. (2021). Colony collapse disorder and honey bee health. In: J.D. Evans & Y. Chen (Eds.), Honey bee medicine for the veterinary practitioner (pp. 229–234). Hoboken: Wiley.
Feuerbacher, A. (2025). Pollinator declines, international trade and global food security: Reassessing the global economic and nutritional impacts. Ecological Economics, 232: 1–14.
Finkel, T. & Holbrook, N.J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408: 239-247.
Flores, J.M., Gámiz, V., Jiménez-Marín, Á., Flores-Cortés, A., Gil-Lebrero, S., Garrido, J.J. & Hernando, M.D. (2021). Impact of Varroa destructor and associated pathologies on the colony collapse disorder affecting honey bees. Research in Veterinary Science, 135: 85-95.
Flores, J.M., Ruiz, J.A., Ruz, J.M., Puerta, F., Bustos, M., Padilla, F. & Campano, F. (1996). Effect of temperature and humidity of sealed brood on chalkbrood development under controlled conditions. Apidologie, 27: 185-192.
Freitas, C.D., Oki, Y., Resende, F.M., Zamudio, F., Freitas, G.S., Rezende, K.M., Souza, F.A., De Jong, D., Quesada, M., Carvalho, A.S., Pires, C.S.S. & Fernandes, G.W. (2022). Impacts of pests and diseases on the decline of managed bees in Brazil: A beekeeper perspective. Journal of Apicultural Research, 62: 969-982.
Gage, S.L., Ahumada, F., Rivera, A., Graham, H. & DeGrandi-Hoffman, G. (2018). Smoke conditions affect the release of the venom droplet accompanying sting extension in honey bees (Hymenoptera: Apidae). Journal of Insect Science, 18: Article 7.
Gallai, N., Salles, J.M., Settele, J. & Vaissière, B.E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68: 810-821.
Garedew, A., Schmolz, E. & Lamprecht, I. (2004). The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie, 35: 419-430.
Ghosh, S., Sohn, H.Y., Pyo, S.J., Jensen, A.B., Meyer-Rochow, V.B. & Jung, C. (2020). Nutritional composition of Apis mellifera drones from Korea and Denmark as a potential sustainable alternative food source: Comparison between developmental stages. Foods, 9: 389.
Giannini, T.C., Cordeiro, G.D., Freitas, B.M., Saraiva, A.M. & Imperatriz-Fonseca, V.L. (2015). The dependence of crops for pollinators and the economic value of pollination in Brazil. Journal of Economic Entomology, 108: 849-857.
Gilliam, M. (1979). Microbiology of pollen and bee bread: The yeasts. Apidologie, 10: 43-53.
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347: 1435.
Graham, J.H., Raz, S., Hel-Or, H. & Nevo, E. (2010). Fluctuating asymmetry: Methods, theory, and applications. Symmetry, 2: 466-540.
Greenleaf, S.S. & Kremen, C. (2006). Wild bees enhance honey bees’ pollination of hybrid sunflower. Proceedings of the National Academy of Sciences of the United States of America, 103: 13890–13895.
Gregorc, A. & Sampson, B. (2019). Diagnosis of Varroa mite (Varroa destructor) and sustainable control in honey bee (Apis mellifera) colonies—A review. Diversity, 11: 243.
Havard, T., Laurent, M. & Chauzat, M.P. (2020). Impact of stressors on honey bees (Apis mellifera; Hymenoptera: Apidae): Some guidance for research emerge from a meta-analysis. Diversity, 12: 7.
Herbert Jr, E.W., Shimanuki, H. & Shasha, B.S. (1980). Brood rearing and food consumption by honeybee colonies fed pollen substitutes supplemented with starch-encapsulated pollen extracts. Journal of Apicultural Research, 19: 115-118.
Instituto Brasileiro de Geografia e Estatística (IBGE). (2023). Produção agropecuária: Mel de abelha em Minas Gerais. Instituto Brasileiro de Geografia e Estatística. Available at: https://www.ibge.gov.br/explica/producao-agropecuaria/mel-de-abelha/mg (accessed 28 September 2024).
Instituto Nacional de Meteorologia (INMET). (2022). Dados meteorológicos. Available at: https://tempo.inmet.gov.br/TabelaEstacoes (accessed 28 September 2024).
Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES). (2016). Summary for policymakers of the thematic assessment on pollinators, pollination and food production. Biota Neotropica, 16: e20160101.
Jack, C.J. & Ellis, J.D. (2021). Integrated pest management control of Varroa destructor (Acari: Varroidae), the most damaging pest of Apis mellifera L. (Hymenoptera: Apidae) colonies. Journal of Insect Science, 21: Article 6.
Jones, J.C., Myerscough, M.R., Graham, S. & Oldroyd, B.P. (2004). Honey bee nest thermoregulation: Diversity promotes stability. Science, 305: 402-404.
Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274: 303-313.
Kleinhenz, M., Bujok, B., Fuchs, S. & Tautz, J. (2003). Hot bees in empty broodnest cells: Heating from within. Journal of Experimental Biology, 206: 4217-4231.
Kluser, S., Neumann, P., Chauzat, M.P., Pettis, J.S., Peduzzi, P., Witt, R. & Theuri, M. (2010). Global honey bee colony disorders and other threats to insect pollinators. United Nations Environment Programme (UNEP), 16 p.
Knierim, U., Van Dongen, S., Forkman, B., Tuyttens, F.A.M., Špinka, M., Campo, J.L. & Weissengruber, G.E. (2007). Fluctuating asymmetry as an animal welfare indicator—A review of methodology and validity. Physiology & Behavior, 92: 398-421.
Köppen, W. (1936). Das geographische System der Klimate. In: W. Köppen & R. Geiger (Eds.), Handbuch der Klimatologie (pp. 1–44). Berlin: Gebrüder Borntraeger.
Kronenberg, F. & Heller, H.C. (1982). Colonial thermoregulation in honey bees (Apis mellifera). Journal of Comparative Physiology A, 148: 65-76.
Kühnholz, S. & Seeley, T.D. (1997). The control of water collection in honey bee colonies. Behavioral Ecology and Sociobiology, 41: 407–422.
Lau, P.W., & Nieh, J.C. (2016). Salt preferences of honey bee water foragers. Journal of Experimental Biology, 219: 790-796.
Le Conte, Y., Ellis, M. & Ritter, W. (2010). Varroa mites and honey bee health: Can Varroa explain part of the colony losses? Apidologie, 41: 353–363.
Lee, K.V., Steinhauer, N., Rennich, K., Wilson, M.E., Tarpy, D.R., Caron, D.M., Rose, R., Delaplane, K.S., Baylis, K., Lengerich, E.J., Pettis, J., Skinner, J.A., Wilkes, J.T., Sagili, R. & vanEngelsdorp, D. (2015). A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie, 46: 292–305.
Leonard, R.J., Wat, K.K.Y., McArthur, C. & Hochuli, D.F. (2018). Urbanisation and wing asymmetry in the western honey bee (Apis mellifera, Linnaeus 1758) at multiple scales. PeerJ, 6: e5940.
Levin, S., Sela, N. & Chejanovsky, N. (2016). Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Scientific Reports, 6: Article 37710.
Li, X., Ma, W., Shen, J., Long, D., Feng, Y., Su, W., Xu, K., Du, Y. & Jiang, Y. (2019). Tolerance and response of two honeybee species Apis cerana and Apis mellifera to high temperature and relative humidity. PLoS One, 14: e0217921.
MapBiomas. (2024). Projeto MapBiomas – Coleção 9 da Série Anual de Mapas de Cobertura e Uso da Terra do Brasil. Available at: https://brasil.mapbiomas.org/estatisticas/ (accessed 28 September 2024).
Marshman, J., Blay-Palmer, A. & Landman, K. (2019). Anthropocene crisis: Climate change, pollinators, and food security. Environments, 6: 22.
Martínez-López, V., Ruiz, C. & De la Rúa, P. (2022). Migratory beekeeping and its influence on the prevalence and dispersal of pathogens to managed and wild bees. International Journal for Parasitology: Parasites and Wildlife, 18: 184–193.
Medina, R.G., Paxton, R.J., De Luna, E., Fleites-Ayil, F.A., Medina, L.A.M. & Quezada-Euan, J.J.G. (2018). Developmental stability, age at onset of foraging and longevity of Africanized honey bees (Apis mellifera L.) under heat stress (Hymenoptera: Apidae). Journal of Thermal Biology, 74: 214-225.
Miranda, J.R. & Fries, I. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of Invertebrate Pathology, 98: 184-189.
Moore, J., Jironkin, A., Chandler, D., Burroughs, N., Evans, D.J. & Ryabov, E.V. (2011). Recombinants between deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. Journal of General Virology, 92: 156-161.
National Research Council, Division on Earth and Life Studies, Board on Agriculture and Natural Resources, Board on Life Sciences & Committee on the Status of Pollinators in North America. (2007). Status of pollinators in North America. Washington, DC: National Academies Press, 326 p.
Nazzi, F. & Le Conte, Y. (2016). Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annual Review of Entomology, 61: 417-432.
Nearman, A., & VanEngelsdorp, D. (2022). Water provisioning increases caged worker bee lifespan and caged worker bees are living half as long as observed 50 years ago. Scientific Reports, 12: 18660.
Noël, A., Le Conte, Y. & Mondet, F. (2020). Varroa destructor: How does it harm Apis mellifera honey bees and what can be done about it? Emerging Topics in Life Sciences, 4: 45-57.
Novais, S.M., Nunes, C.A., Santos, N.B., D'Amico, A.R., Fernandes, G.W., Quesada, M. & Neves, A.C.O. (2016). Effects of a possible pollinator crisis on food crop production in Brazil. PLoS One, 11: e0167292.
Nunes, L.A., Araújo, E.D.D. & Marchini, L.C. (2015). Fluctuating asymmetry in Apis mellifera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments. Revista de Biología Tropical, 63: 673-682.
Ollerton, J., Winfree, R. & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120: 321-326.
Palmer, A.R. & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology, Evolution, and Systematics, 17: 391-421.
Palmer, A.R. & Strobeck, C. (1992). Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zoologica Fennica, 191: 57-72.
Palmer, A.R. (1994). Fluctuating asymmetry analyses: A primer. In: Markow, T.A. (Ed.), Developmental Instability: Its Origins and Evolutionary Implications. Contemporary Issues in Genetics and Evolution, vol. 2, Springer, Dordrecht, pp. 335-364.
Papa, G., Maier, R., Durazzo, A., Lucarini, M., Karabagias, I.K., Plutino, M., Bianchetto, E., Aromolo, R., Pignatti, G., Ambrogio, A., Pellecchia, M. & Negri, I. (2022). The honey bee Apis mellifera: An insect at the interface between human and ecosystem health. Biology, 11: 233.
Parsons, P.A. (1990). Fluctuating asymmetry: An epigenetic measure of stress. Biological Reviews of the Cambridge Philosophical Society, 65: 131-145.
Patel, V., Pauli, N., Biggs, E., Barbour, L. & Boruff, B. (2021). Why bees are critical for achieving sustainable development. Ambio, 50: 49-59.
Peixoto, M.C., Correia-Oliveira, M.E., Silva, F.L., Ramos, C.E.C.O. & Carvalho, C.A.L. (2021). Varroa destructor in Apis mellifera colonies in Brazil. Journal of Apicultural Research, 63: 480-486.
Pinto, F.A., Teixeira, E.W., Cestaro, L.G., Martins, M.F., Alves, M.L.T.M.F. & Message, D. (2022). Varroa destructor in Africanized honey bees in Brazil: Genetic and reproductive profile. Sociobiology, 69: e7340.
Piou, V., Schurr, F., Dubois, E. & Vétillard, A. (2022). Transmission of deformed wing virus between Varroa destructor foundresses, mite offspring, and infested honey bees. Parasites & Vectors, 15: Article 333.
Pires, C.S.S., Pereira, F.D.M., Lopes, M.T.D.R., Nocelli, R.C.F., Malaspina, O., Pettis, J.S. & Teixeira, É.W. (2016). Enfraquecimento e perda de colônias de abelhas no Brasil: há casos de CD? Pesquisa Agropecuária Brasileira, 51: 422-442.
Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Aizen, M.A., Biesmeijer, J.C., Breeze, T.D. & Vanbergen, A.J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540: 220-229.
Potts, S.G., Roberts, S.P., Dean, R., Marris, G., Brown, M.A., Jones, R. & Settele, J. (2010). Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research, 49: 15-22.
Quesada, M., Rosas, F., Aguilar, R., Ashworth, L., Rosas-Guerrero, V.M., Sayago, R., Lobo, J.A., Herrerías-Diego, Y. & Sánchez-Montoya, G. (2011). Human impacts on pollination, reproduction, and breeding systems in tropical forest plants. In: R. Dirzo, H.S. Young, H.A. Mooney & G. Ceballos (Eds.), Seasonally dry tropical forests (pp. 173–194). Washington, DC: Island Press.
Quinn, G.P. & Keough, M.J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, 537 p.
Reams, T. & Rangel, J. (2022). Understanding the enemy: A review of the genetics, behavior, and chemical ecology of Varroa destructor, the parasitic mite of Apis mellifera. Journal of Insect Science, 22: 18.
Silva, A.F., Pereira, D.S., Paiva, C.S., Souza, R.M. & Maracajá, P.B. (2012). Comportamento defensivo de abelhas africanizadas na Fazenda Experimental-UFERSA, Mossoró-RN, Brasil. Revista Verde de Agroecologia e Desenvolvimento Sustentável, 7: 63-72.
Smith, D.R., Crespi, B.J. & Bookstein, F.L. (1997). Fluctuating asymmetry in the honey bee, Apis mellifera: Effects of ploidy and hybridization. Journal of Evolutionary Biology, 10: 551-574.
Spivak, M. & Reuter, G.S. (2001). Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. Journal of Economic Entomology, 94: 326-331.
Steffan-Dewenter, I. & Tscharntke, T. (1999). Effects of habitat isolation on pollinator communities and seed set. Oecologia, 121: 432-440.
Strauss, U., Dietemann, V., Human, H., Crewe, R.M. & Pirk, C.W.W. (2016). Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor. Parasitology, 143: 374–387.
Vaca-Sánchez, M.S., Cuevas-Reyes, P., Munck, I., Oki, Y., Moia, N., Freitas, T., Almeida, A., Castelan, K. & Fernandes, G.W. (2023). Patterns in wing morphology and fluctuating asymmetry in Eulaema nigrita along an altitudinal gradient in the Brazilian rupestrian grassland. Neotropical Entomology, 52: 837–847.
Vasiliev, D. & Greenwood, S. (2020). Pollinator biodiversity and crop pollination in temperate ecosystems, implications for national pollinator conservation strategies: Mini review. Science of the Total Environment, 744: 140880.
Vaudo, A.D., Tooker, J.F., Grozinger, C.M. & Patch, H.M. (2015). Bee nutrition and floral resource restoration. Current Opinion in Insect Science, 10: 133-141.
Williams, G.R., Tarpy, D.R., vanEngelsdorp, D., Chauzat, M.P., Cox-Foster, D.L., Delaplane, K.S., Neumann, P., Pettis, J.S., Rogers, R.E.L. & Shutler, D. (2010). Colony collapse disorder in context. BioEssays, 32: 837-847.
Williams, I.H. (1994). The dependence of crop production within the European Union on pollination by honey bees. Agricultural Zoology Reviews, 6: 229-257.
Willmer, P. (2011). Pollination and floral ecology. Princeton, NJ: Princeton University Press, 792 p.
Winfree, R. (2010). The conservation and restoration of wild bees. Annals of the New York Academy of Sciences, 1195: 169-197.
Woods, R.E., Hercus, M.J. & Hoffmann, A.A. (1998). Estimating the heritability of fluctuating asymmetry in field Drosophila. Evolution, 52: 816-824.
Zakharov, V.M., Shadrina, E.G. & Trofimov, I.E. (2020). Fluctuating asymmetry, developmental noise, and developmental stability: Future prospects for the population developmental biology approach. Symmetry, 12: 1-24.
Zhao, H., Li, G., Guo, D., Li, H., Liu, Q., Xu, B. & Guo, X. (2021). Response mechanisms to heat stress in bees. Apidologie, 52: 388-399.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Benoni de Assis Santos, Yumi Oki, Israel Munck, Bruce Dickinson, Marcos Paulo dos Santos, Walisson Kenedy Siqueira, Fernando Figueiredo Goulart, Mauricio Quesada, Geraldo Wilson Fernandes
This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
eISSN 2447-8067
