IMPACT OF SOME ENVIRONMENTAL FACTORS OVER APIS MELLIFERA L. (REVIEW)

Zheko Radev

Abstract


A number of factors and reasons from different directions, accumulated over the

last two-three decades, led to a negative impact on the environment and threaten the existence of

number of living organisms from the plant and animal world. Ones of the main problems are the

increased urbanization and agriculture. Honey bee Apis mellifera L. are one of the most affected

and concerned living organisms. They are under the direct influence and impact of the pesticides

used in agriculture during plant protection measures. Heavy metals in the environment and

acaricides used to control the mite Varroa destructor Anderson & Trueman also have a negative

effect over honey bees. A number of scientific reports prove honey bees as a bioindicator of the

environment. This study examines the status of A. mellifera and the impact of the environment over

honey bees in modern conditions, as well as the understanding of the ecological role of A. mellifera.


Keywords


honey bees, Apis mellifera, environment, pollution, ecology.

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References


Abd Wahid, D. N., Wan Mohamad Nazarie, W. F., Jawan, R., Abdulla, R., Gansau, J. A.

& Sabullah, M. K. (2021). Potential existence of heavy metal pollution and pesticide in honey-

based products. Preprints, 2021120379. https://doi.org/10.20944/preprints202112.0379.v1

Alburaki, M., Smith, K. D., Adamczyk, J. & Karim, S. (2019). Interplay between

Selenium, selenoprotein genes, and oxidative stress in honey bee Apis mellifera L. Journal of

Insect Physiology, 117, 103891. https://doi.org/10.1016/j.jinsphys.2019.103891

Alister, C., Araya, M., Becerra, K., Saavedra, J. & Kogan, M. (2017). Preharvest

Interval Periods and their relation to fruit growth stages and pesticide formulations. Food

Chemistry, 221, 548–554. https://doi.org/10.1016/j.foodchem.2016.11.140

Archer, C. R., Pirk, C. W., Wright, G. A. & Nicolson, S. W. (2013). Nutrition affects

survival in African honeybees exposed to interacting stressors. Functional Ecology, 28(4),

-923. https://doi.org/10.1111/1365-2435.12226

Arena, M. & Sgolastra, F. (2014). A meta-analysis comparing the sensitivity of bees to

pesticides. Ecotoxicology, 23(3), 324–334. https://doi.org/10.1007/s10646-014-1190-1

Behmer, S. T. (2008). Nutrition in insects. In: Encyclopedia of Entomology (Capinera, J.

L.). Springer Dordrecht, Netherlands, 2646–2654.

Bogdanov, S. (2006). Contaminants of bee products. Apidologie, 37(1), 1–18. https://

doi.org/10.1051/apido:2005043

Briffa, J., Sinagra, E. & Blundell, R. (2020). Heavy metal pollution in the environment

and their toxicological effects on humans. Heliyon, 6(9), e04691. https://doi.org/10.1016/

j.heliyon.2020.e04691

Brown, M. J. F. & Paxton, R. J. (2009). The conservation of bees: A global perspective.

Apidologie, 40(3), 410–416. https://doi.org/10.1051/apido/2009019

Celli, G. & Maccagnani, B. (2003). Honeybees as bioindicators of environmental

pollution. Bulletin of Insectology, 56(1), 137–139.

Ciric, J., Spiric, D., Baltic, T., Lazic, I. B., Trbovic, D., Parunovic, N., Petronijevic, R.

& Dordevic, V. (2021). Honey bees and their products as indicators of environmental element

deposition. Biological Trace Element Research, 199(8-9), 2312–2319. https://doi.org/10.1007/

s12011-020-02321-6

Craddock, H. A., Huang, D., Turner, P. C., Quiros-Alcala, L. & Payne-Sturges, D. C.

(2019). Trends in neonicotinoid pesticide residues in food and water in the United States, 1999–

Environmental Health, 18(1), 7. https://doi.org/10.1186/s12940-018-0441-7

Crane, E. (1984). Bees, honey and pollen as indicators of metals in the environment.

Bee World, 65(1), 47-49. https://doi.org/10.1080/0005772X.1984.11098770

Cunningham, M. M., Tran, L., McKee, C. G., Polo, R. O., Newman, T., Lansing, L.,

Griffiths, J. S, Bilodeau, G. J., Rott, M. & Guarna, M. M. (2022). Honey bees as biomonitors of

environmental contaminants, pathogens, and climate change. Ecological Indicators, 134(9SE),

https://doi.org/10.1016/j.ecolind.2021.108457

Dudka, S., & Miller, W. P. (1999). Accumulation of potentially toxic elements in plants

and their transfer to human food chain. Journal of Environmental Science and Health, Part B,

(4), 681–708. https://doi.org/10.1080/03601239909373221

European Commisison 2023/915 on maximum levels for certain contaminants in food

and repealing Regulation (EC). 2023, No 1881/2006 (Text with EEA relevance). https:// eur-

lex. europa. eu/legal- conte nt/ EN/ TXT/? uri= CELEX% 3A320 23R09 15

Filipiak, M., Kuszewska, K., Asselman, M., Denisow, B., Stawiarz, E., Woyciechowski,

M. & Weiner, J. (2017). Ecological stoichiometry of the honeybee: pollen diversity and

adequate species composition are needed to mitigate limitations imposed on the growth and

development of bees by pollen quality. PLoS One, 12(8), e0183236. https://doi.org/10.1371/

journal.pone.0183236

Fry, K. L., McPherson, V. J., Gillings, M. R. & Taylor, M. P. (2023). Tracing the sources

and prevalence of class 1 integrons, antimicrobial resistance, and trace elements using european

honey bees. Environmental Science and Technology, 57(29), 10582–10590. https://doi.org/

1021/acs.est.3c03775

Gekiere, A., Vanderplanck, M. & Michez, D. (2023). Trace metals with heavy

consequences on bees: a comprehensive review. The Science of The Total Environment, 895(7),

https://doi.org/10.1016/j.scitotenv.2023.165084

Gordon, H. T. (1959). Minimal nutritional requirements of the German roach, Blattella

germanica L. Annals of the New York Academy of Sciences, 77(20), 290. https://doi.org/

1111/j.1749-6632.1959.tb36910.x

Goulson, D. (2013). Review: An overview of the environmental risks posed by

neonicotinoid insecticides. Journal of Applied Ecology, 50(4), 977-987. https://doi.org/

1111/1365-2664.12111

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(6229), 1255957.

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

Graham, K. K., Milbrath, M. O., Zhang, Y., Baert, N., McArt, S. & Isaacs, R. (2022).

Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm

exposures. Scientific Reports, 12(1), 7189. https://doi.org/10.1038/s41598-022-11156-1

Henry, M., Béguin, М., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J.,

Tchamitchian, S. & Decourtyeet, A. (2012). A Common Pesticide Decreases Foraging Success

and Survival in Honey Bees. Science, 336(6079), 348-350. https://doi.org/10.1126/

science.1215039

Hladun, K. R., Smith, B. H., Mustard, J. A., Morton, R. R. & Trumble, J. T. (2012).

Selenium toxicity to honey bee (Apis mellifera L.) pollinators: effects on behaviors and

survival. PLoS One, 7(4), e34137. https://doi.org/10.1371/journal.pone.0034137

Huang, Z. (2012). Pollen nutrition affects honey bee stress resistance. Terrestrial

Arthropod Reviews, 5(5), 175–189. https://doi.org/10.1163/187498312X639568

Ilijevic, K., Vujanovic, D., Orcic, S., Purac, J., Kojic, D.; Zaric, N.; Grzetic, I.;

Blagojevic, D. P. & Celic, T. V. (2021). Anthropogenic influence on seasonal and spatial

variation in bioelements and non-essential elements in honeybees and their hemolymph.

Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 239(3),

https://doi.org/10.1016/j.cbpc.2020.108852

Jovetic, M. S., Redzepovic, A. S., Nedic, N. M., Vojt, D., Durdic, S. Z., Brceski, I. D. &

Milojkovic-Opsenica, D. M. (2018). Urban honey—The aspects of its safety. Archives of

Industrial Hygiene and Toxicology, 69(3), 264–274. https://doi.org/10.2478/aiht-2018-69-3126

Kiljanek, T., Niewiadowska, A., Malysiak, M. & Posyniak, A. (2021). Miniaturized

multiresidue method for determination of 267 pesticides, their metabolites and polychlorinated

biphenyls in low mass beebread samples by liquid and gas chromatography coupled with

tandem mass spectrometry. Talanta, 235, 122721. https://doi.org/10.1016/j.talanta.2021.122721

Knapp, J. L., Nicholson, C. C., Jonsson, O., de Miranda, J. R. & Rundlof, M. (2023).

Ecological traits interact with landscape context to determine bees’ pesticide risk. Nature

Ecology & Evolution, 7(4), 547–556. https://doi.org/10.1038/s41559-023-01990-5

Kulhanek, K., Steinhauer, N., Rennich, K., Caron, D. M., Sagili, R. R., Pettis, J. S.;

Ellis, J. D., Wilson, M. E., Wilkes, J. T. & Tarpy, D. R. (2017). A national survey of managed

honey bee 2015–2016 annual colony losses in the USA. Journal of Apicultural Research, 56(4),

–340. https://doi.org/10.1080/00218839.2017.1344496

Kumari, S., Jain, M. K. & Elumalai, S. P. (2021). Assessment of pollution and health

risks of heavy metals in particulate matter and road dust along the road network of Dhanbad,

India. Journal of Health and Pollution, 11(29), 210305. https://doi.org/

5696/2156-9614-11.29.210305

Laurent, M., Bougeard, S., Caradec, L., Ghestem, F., Albrecht, M., Brown, M. J. F., De

Miranda, J., Karise, R., Knapp, J., Serrano, J., Potts, S. G., Rundlof, M., Schwarz, J., Attridge,

E., Babin, A., Bottero, I., Cini, E., De Larua, P., Di Prisco, G., Dominik, C., Dzul, D., Garcia-

Reina, A., Hodge, S., Klein, A. M., Knauer, A., Mand, M., Martinez Lopez, V., Sarra, G.,

Pereira-Peixoto, H., Raimets, R., Schweiger, O., Senapathi, D., Stout, J. C., Tamburini, G.,

Costa, C., Kiljanek, T., Martel, A. C.; Le, S. & Chauzat, M. P. (2024). Novel indices reveal that

pollinator exposure to pesticides varies across biological compartments and crop surroundings.

The Science of The Total Environment, 927, 172118. https://doi.org/10.1016/

j.scitotenv.2024.172118

McCune, F., Samson-Robert, O., Rondeau, S., Chagnon, M. & Fournier, V. (2021).

Supplying honey bees with waterers: a precautionary measure to reduce exposure to pesticides.

Environmental Science and Pollution Research, 28(364-365), 17573–17586. https://doi.org/

1007/s11356-020-12147-3

Mitra, S., Chakraborty, A. J., Tareq, A. M., Emran, T. B., Nainu, F., Khusro, A., Idris, A.

M., Khandaker, M. U., Osman, H., Alhumaydhi, F. A. & Simal-Gandara, J. (2022). Impact of

heavy metals on the environment and human health: Novel therapeutic insights to counter the

toxicity. Journal of King Saud University – Science, 34(3), 101865. https://doi.org/10.1016/

j.jksus.2022.101865

Nation, J. L. (2015). Insect Physiology and Biochemistry., 3rd ed.; Publisher: CRC

Press, Boca Raton.

Negri, I., Mavris, C., Di Prisco, G., Caprio, E. & Pellecchia, M. (2015). Honey bees

(Apis mellifera L.) as active samplers of airborne particulate matter. PloS One, 10(7),

e0132491. https://doi.org/10.1371/journal.pone.0132491

Panseri, S., Bonerba, E., Nobile, M., Di Cesare, F., Mosconi, G., Cecati, F., Arioli, F.,

Tantillo, G. & Chiesa, L. (2020). Pesticides and environmental contaminants in organic honeys

according to their different productive areas toward food safety protection. Foods, 9(12), 1863.

https://doi.org/10.3390/foods9121863

Papa, G., Capitani, G., Capri, E., Pellecchia, M. & Negri, I. (2021). Vehiclederived

ultrafine particulate contaminating bees and bee products. Science of The Total Environment,

, 141700. https://doi.org/10.1016/j.scitotenv.2020.141700

Perugini, M., Manera, M., Grotta, L., Abete, M. C., Tarasco, R. & Amorena, M. (2011).

Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves:

Honeybees as bioindicators. Biological Trace Element Research, 140(2), 170–176. https://

doi.org/10.1007/s12011-010-8688-z

Porrini, C., Sabatini, A. G., Girotti, S., Fini, F., Monaco, L., Celli, G., Bortolotti, L. &

Ghini, S. (2003). The death of honey bees and environmental pollution by pesticides: The

honey bees as biological indicators. Bulletin of Insectology, 56(1), 147–152.

Potts, S. G., Imperatriz-Fonseca, V. L., Ngo, H. T., Biesmeijer, J. C., Breeze, T. D.,

Dicks, L. V., Garibaldi, L. A., Hill, R., Settele, J., Vanbergen, A. J., Aizen, M. A., Cunningham,

S. A., Eardley, C., Freitas, B. M., Gallai, N., Kevan, P. G.; Kovacs-Hostyanszki, A., Kwapong,

P. K., Li, J., Li, X., Martins, D. J., Nates-Parra, G., Pettis, J. S., Rader, R. & Viana, B. F. (2016).

Summary for Policymakers of the Assessment Report of the Intergovernmental Science-policy

Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food

Production. Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and

Ecosystem Services, Bonn, Germany.

Radev, Z., Liolios, V., Tananaki, C. & Thrasyvoulou, A. (2014). The impact of the

nutritive value of pollen on the development, reproduction and productivity of honey bees (Apis

mellifera L.). Bulgarian Journal of Agricultural Science, 20(3), 685–689.

Radev, Z. & Raycheva, Ts. (2022). Study on toxic tolerance of beneficial entomofauna

(Apis mellifera L.) through usage of pollen from a forestry area. Forestry ideas, 28(1), 84-87.

Raes, H., Cornelis, R. & Rzeznik, U. (1992). Distribution, accumulation and depuration

of administered lead in adult honeybees. The Science of The Total Environment, 113(3), 269–

https://doi.org/10.1016/0048-9697(92)90005-D

Ryalls, J. M. V., Langford, B., Mullinger, N. J., Bromfield, L. M., Nemitz, E., Pfrang, C.

& Girling, R. D. (2022). Anthropogenic air pollutants reduce insect-mediated pollination

services. Environmental Pollution, 297, 118847. https://doi.org/10.1016/j.envpol.2022.118847

Satta, A., Verdinelli, M., Ruiu, L., Buffa, F., Salis, S., Sassu, A. & Floris, I. (2012).

Combination of beehive matrices analysis and ant biodiversity to study heavy metal pollution

impact in a post-mining area (Sardinia, Italy). Environmental Science and Pollution Research,

(9), 3977–3988. https://doi.org/10.1007/s11356-012-0921-1

Scarfone, A., Cammerata, A., Romano, E., Vinciguerra, V., Marabottini, R., Gallucci, F.,

Paris, E., Carnevale, M., Vincenti, B., Palma, A. & Bergonzoli, S. (2024). Effects of ground

transport on the presence of heavy metals in selected honeybee products. Environmental

Science and Pollution Research, 31(30), 43037–43048. https://doi.org/10.1007/

s11356-024-33982-8

Schmarsow, R., de la Moline, M. P., Damiani, N., Domínguez, E., Medici, S. K.,

Churio, M. S. & Gende, L. B. (2023). Toxicity and sublethal effects of lead (Pb) intake on

honey bees (Apis mellifera). Chemosphere, 344(4), 140345. https://doi.org/10.1016/

j.chemosphere.2023.140345

Schmehl, D. R., Teal, P. E., Frazier, J. L. & Grotzinger, C. M. (2014). Genomic analysis

of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera).

Journal of Insect Physiology, 71, 177-190. https://doi.org/10.1016/j.jinsphys.2014.10.002

Sereviciene, V., Zigmontiene, A. & Paliulis, D. (2022). Heavy Metals in Honey

Collected from Contaminated Locations: A Case of Lithuania. Sustainability, 14(15), 9196.

https://doi.org/10.3390/su14159196

Siviter, H., Richman, S. K. & Muth, F. (2021). Field-realistic neonicotinoid exposure

has sub-lethal effects on non-Apis bees: a meta-analysis. Ecology Letters, 24(12), 2586–2597.

https://doi.org/10.1111/ele.13873

Straw, E. A. & Brown, M. J. F. (2021). Co-formulant in a commercial fungicide product

causes lethal and sub-lethal effects in bumble bees. Scientific Reports, 11(1), 21653. https://

doi.org/10.1038/s41598-021-00919-x

Taylor, M. P., Gillings, M. M., Fry, K. L. Barlow, C. F., Gunkel-Grillion, P., Gueyte, R.

& Camoin, M. (2023). Tracing nickel smelter emissions using European honey bees.

Environmental Pollution, 335(1), 122257. https://doi.org/10.1016/j.envpol.2023.122257

Tosi, S., Nieh, J. C. & Sgolastra, F. (2017). Neonicotinoid pesticides and nutritional

stress synergistically reduce survival in honey bees. Proceedings of the Royal Society B,

(1869), 20171711. https://doi.org/10.1098/rspb.2017.1711

Vidau, C., Diogon, М., Aufauvre, J., Fontbonne, R., Vigues, B., Brunet, J. L., Texier, C.,

Biron, D. G., Blot, N., El Alaoui, H., Belzunces, L. P. & Delbac, F. (2011). Exposure to

Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees

Previously Infected by Nosema ceranae. PLoS One, 6(6), e21550. https://doi.org/10.1371/

journal.pone.0021550

Vodovnik, C., Borshagovski, A. M., Hakala, S. M., Leponiemi, M. & Freitak, D. (2021).

Coeffects of diet and neonicotinoid exposure on honeybee mobility and food choice.

Apidologie, 52(4), 658–667. https://doi.org/10.1007/s13592-021-00853-x

Wisk, J. D., Pistorius, J., Beevers, M., Bireley, R., Browning, Z., Chauzat, M. P.,

Nikolakis, A., Overmyer, J. P., Rose, R., Sebastien, R., Vaissière, B. E., Maynard, G., Kasina,

M., Nocelli, R. C. F. Scott-Dupree, C., Johansen, E., Brittain, C., Coulson, M., Dinter, A. &

Vaughanet, M. (2014). Assessing the exposure of pesticides to bees. In: Pesticide Risk

Assessment for Pollinators (ed. eds. D. Fischer, T. Moriarty). Wiley Blackwell, 45–74.

Yang, E., Chuang, Y., Chen, Y. & Chang, L. (2008). Abnormal Foraging Behavior

Induced by Sublethal Dosage of Imidacloprid in the Honey Bee (Hymenoptera: Apidae).

Journal of Economic Entomology, 101(6), 1743- 1748. https://doi.org/

1603/0022-0493-101.6.1743

Yu, X., Jiang, N., Yang, Y., Liu, H., Gao, X. & Cheng, L. (2023). Heavy metals

remediation through bio-solidification: potential application in environmental geotechnics.

Ecotoxicology and Environmental Safety, 263(38), 115305. https://doi.org/10.1016/

j.ecoenv.2023.115305

Zaric, N. M., Ilijevic, K., Stanisavljevic, L. & Grzetic, I. (2017). Use of honeybees

(Apis mellifera L.) as bioindicators for assessment and source appointment of metal pollution.

Environmental Science and Pollution Research, 24(3), 25828–25838. https://doi.org/10.1007/

s11356-017-0196-7

Zaric, N. M., Brodschneider, R. & Goessler, W. (2024). Sex-specific element

accumulation in honey bees (Apis mellifera). Environmental Science and Pollution Research,

(16), 10348-10355. https://doi.org/10.1007/s11356-024-32822-z

Zavrtnik, S. & Cvitkovic, D. (2023). Impact of contaminated environment with heavy

metals and pesticides on bees. In: Safe and Sustainable Food Production in Croatia; Croatian

Biophil Association, Faculty of Veterinary Medicine University of Zagreb: Zagreb, Croatia.


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