The Signature of Environmental and Parasite Stresses on the Wings of Apis mellifera

Authors

  • Benoni de Assis Santos Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
  • Yumi Oki Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil https://orcid.org/0000-0003-1268-9151
  • Israel Munck Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
  • Bruce Dickinson Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil https://orcid.org/0009-0002-4762-3531
  • Marcos Paulo dos Santos Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil https://orcid.org/0009-0009-1499-4177
  • Walisson Kenedy Siqueira Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil https://orcid.org/0000-0001-7766-9077
  • Fernando Figueiredo Goulart Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
  • Mauricio Quesada Laboratorio Nacional de Análisis y Síntesis Ecológica, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico https://orcid.org/0000-0002-7776-9286
  • Geraldo Wilson Fernandes Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais & Knowledge Center for Biodiversity, Belo Horizonte, Minas Gerais, Brazil

DOI:

https://doi.org/10.13102/sociobiology.v72i3.11389

Keywords:

Bees, Bioindicator, Environmental stress, Fluctuating asymmetry, Heat stress, Varroa destructor

Abstract

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

Download data is not yet available.

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. DOI: https://doi.org/10.7717/peerj.5812

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. DOI: https://doi.org/10.1127/0941-2948/2013/0507

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. DOI: https://doi.org/10.1093/jee/97.3.741

Ashworth, L., Quesada, M., Casas, A., Aguilar, R. & Oyama, K. (2009). Pollinator-dependent food production in Mexico. Biological Conservation, 142: 1050-1057. DOI: https://doi.org/10.1016/j.biocon.2009.01.016

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. DOI: https://doi.org/10.1016/j.jinsphys.2014.07.001

Banaji, S. (2022). Colony collapse disorder, neonicotinoids, CO2, climate change, and the four spheres. Open Journal of Ecology, 12: 711-717. DOI: https://doi.org/10.4236/oje.2022.1211040

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. DOI: https://doi.org/10.3897/jhr.52.8787

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. DOI: https://doi.org/10.1007/s00359-009-0442-7

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. DOI: https://doi.org/10.1046/j.1570-7458.2001.00905.x

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. DOI: https://doi.org/10.1016/j.agee.2011.03.020

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. DOI: https://doi.org/10.13102/sociobiology.v64i1.1183

Brunet, J. & Fragoso, F.P. (2024). What are the main reasons for the worldwide decline in pollinator populations? CABI Reviews, 19: 1-11. DOI: https://doi.org/10.1079/cabireviews.2024.0016

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. DOI: https://doi.org/10.1111/rec.12950

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. DOI: https://doi.org/10.1007/BF00054628

Cornelissen, T. & Stiling, P. (2005). Perfect is best: Low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia, 142: 46-56. DOI: https://doi.org/10.1007/s00442-004-1724-y

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. DOI: https://doi.org/10.1016/j.rbe.2015.09.004

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. DOI: https://doi.org/10.1016/j.ecolind.2018.03.009

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. DOI: https://doi.org/10.1016/j.jip.2018.12.005

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. DOI: https://doi.org/10.1371/journal.pone.0162818

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. DOI: https://doi.org/10.1371/journal.pone.0072016

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. DOI: https://doi.org/10.1051/apido:2002052

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. DOI: https://doi.org/10.1016/j.jinsphys.2008.08.011

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. DOI: https://doi.org/10.1111/joac.12360

Eskov, E.K. (2018). Exo-and endogenous water in the honeybee Body (Apis mellifera, Hymenoptera, Apidae). Entomological Review, 98: 129-137. DOI: https://doi.org/10.1134/S001387381802001X

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. DOI: https://doi.org/10.1002/9781119583417.ch19

Feuerbacher, A. (2025). Pollinator declines, international trade and global food security: Reassessing the global economic and nutritional impacts. Ecological Economics, 232: 1–14. DOI: https://doi.org/10.1016/j.ecolecon.2025.108565

Finkel, T. & Holbrook, N.J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408: 239-247. DOI: https://doi.org/10.1038/35041687

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. DOI: https://doi.org/10.1016/j.rvsc.2021.01.001

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. DOI: https://doi.org/10.1051/apido:19960401

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. DOI: https://doi.org/10.1080/00218839.2022.2099188

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. DOI: https://doi.org/10.1093/jisesa/iey073

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. DOI: https://doi.org/10.1016/j.ecolecon.2008.06.014

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. DOI: https://doi.org/10.1051/apido:2004032

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. DOI: https://doi.org/10.3390/foods9040389

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. DOI: https://doi.org/10.1093/jee/tov093

Gilliam, M. (1979). Microbiology of pollen and bee bread: The yeasts. Apidologie, 10: 43-53. DOI: https://doi.org/10.1051/apido:19790106

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. DOI: https://doi.org/10.1126/science.1255957

Graham, J.H., Raz, S., Hel-Or, H. & Nevo, E. (2010). Fluctuating asymmetry: Methods, theory, and applications. Symmetry, 2: 466-540. DOI: https://doi.org/10.3390/sym2020466

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. DOI: https://doi.org/10.1073/pnas.0600929103

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. DOI: https://doi.org/10.3390/d11120243

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. DOI: https://doi.org/10.3390/d12010007

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. DOI: https://doi.org/10.1080/00218839.1980.11100008

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. DOI: https://doi.org/10.1590/1676-0611201600010001

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. DOI: https://doi.org/10.1093/jisesa/ieab058

Jones, J.C., Myerscough, M.R., Graham, S. & Oldroyd, B.P. (2004). Honey bee nest thermoregulation: Diversity promotes stability. Science, 305: 402-404. DOI: https://doi.org/10.1126/science.1096340

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. DOI: https://doi.org/10.1098/rspb.2006.3721

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. DOI: https://doi.org/10.1242/jeb.00680

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. DOI: https://doi.org/10.1016/j.physbeh.2007.02.014

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. DOI: https://doi.org/10.1007/BF00688889

Kühnholz, S. & Seeley, T.D. (1997). The control of water collection in honey bee colonies. Behavioral Ecology and Sociobiology, 41: 407–422. DOI: https://doi.org/10.1007/s002650050402

Lau, P.W., & Nieh, J.C. (2016). Salt preferences of honey bee water foragers. Journal of Experimental Biology, 219: 790-796. DOI: https://doi.org/10.1242/jeb.132019

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. DOI: https://doi.org/10.1051/apido/2010017

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. DOI: https://doi.org/10.1007/s13592-015-0356-z

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. DOI: https://doi.org/10.7717/peerj.5940

Levin, S., Sela, N. & Chejanovsky, N. (2016). Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Scientific Reports, 6: Article 37710. DOI: https://doi.org/10.1038/srep37710

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. DOI: https://doi.org/10.1371/journal.pone.0217921

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. DOI: https://doi.org/10.3390/environments6020022

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. DOI: https://doi.org/10.1016/j.ijppaw.2022.05.004

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. DOI: https://doi.org/10.1016/j.jtherbio.2018.04.003

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. DOI: https://doi.org/10.1016/j.jip.2008.02.004

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. DOI: https://doi.org/10.1099/vir.0.025965-0

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. DOI: https://doi.org/10.1146/annurev-ento-010715-023731

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. DOI: https://doi.org/10.1038/s41598-022-21401-2

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. DOI: https://doi.org/10.1042/ETLS20190125

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. DOI: https://doi.org/10.1371/journal.pone.0167292

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. DOI: https://doi.org/10.15517/rbt.v63i3.15869

Ollerton, J., Winfree, R. & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120: 321-326. DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x

Palmer, A.R. & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology, Evolution, and Systematics, 17: 391-421. DOI: https://doi.org/10.1146/annurev.es.17.110186.002135

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. DOI: https://doi.org/10.1007/978-94-011-0830-0_26

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. DOI: https://doi.org/10.3390/biology11020233

Parsons, P.A. (1990). Fluctuating asymmetry: An epigenetic measure of stress. Biological Reviews of the Cambridge Philosophical Society, 65: 131-145. DOI: https://doi.org/10.1111/j.1469-185X.1990.tb01186.x

Patel, V., Pauli, N., Biggs, E., Barbour, L. & Boruff, B. (2021). Why bees are critical for achieving sustainable development. Ambio, 50: 49-59. DOI: https://doi.org/10.1007/s13280-020-01333-9

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. DOI: https://doi.org/10.1080/00218839.2021.1960746

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. DOI: https://doi.org/10.13102/sociobiology.v69i1.7340

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. DOI: https://doi.org/10.1186/s13071-022-05463-9

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. DOI: https://doi.org/10.1590/S0100-204X2016000500003

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. DOI: https://doi.org/10.1038/nature20588

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. DOI: https://doi.org/10.3896/IBRA.1.49.1.02

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. DOI: https://doi.org/10.5822/978-1-61091-021-7_11

Quinn, G.P. & Keough, M.J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, 537 p. DOI: https://doi.org/10.1017/CBO9780511806384

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. DOI: https://doi.org/10.1093/jisesa/ieab101

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. DOI: https://doi.org/10.1046/j.1420-9101.1997.10040551.x

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. DOI: https://doi.org/10.1603/0022-0493-94.2.326

Steffan-Dewenter, I. & Tscharntke, T. (1999). Effects of habitat isolation on pollinator communities and seed set. Oecologia, 121: 432-440. DOI: https://doi.org/10.1007/s004420050949

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. DOI: https://doi.org/10.1017/S0031182015001754

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. DOI: https://doi.org/10.1007/s13744-023-01069-7

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. DOI: https://doi.org/10.1016/j.scitotenv.2020.140880

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. DOI: https://doi.org/10.1016/j.cois.2015.05.008

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. DOI: https://doi.org/10.1002/bies.201000075

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. DOI: https://doi.org/10.23943/princeton/9780691128610.001.0001

Winfree, R. (2010). The conservation and restoration of wild bees. Annals of the New York Academy of Sciences, 1195: 169-197. DOI: https://doi.org/10.1111/j.1749-6632.2010.05449.x

Woods, R.E., Hercus, M.J. & Hoffmann, A.A. (1998). Estimating the heritability of fluctuating asymmetry in field Drosophila. Evolution, 52: 816-824. DOI: https://doi.org/10.1111/j.1558-5646.1998.tb03705.x

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. DOI: https://doi.org/10.3390/sym12081376

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. DOI: https://doi.org/10.1007/s13592-020-00830-w

Downloads

Published

2025-08-11

How to Cite

Santos, B. de A., Oki, Y., Munck, I., Dickinson, B., Santos, M. P. dos, Siqueira, W. K., Goulart, F. F., Quesada, M., & Fernandes, G. W. (2025). The Signature of Environmental and Parasite Stresses on the Wings of Apis mellifera. Sociobiology, 72(3), e11389. https://doi.org/10.13102/sociobiology.v72i3.11389

Issue

Section

Research Article - Bees

Most read articles by the same author(s)