Sex-specific element accumulation in honey bees (Apis mellifera).

Drones Element composition Food filtration ICPMS Sexual dimorphism Workers

Journal

Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769

Informations de publication

Date de publication:
13 Mar 2024
Historique:
received: 10 11 2023
accepted: 04 03 2024
pubmed: 13 3 2024
medline: 13 3 2024
entrez: 13 3 2024
Statut: aheadofprint

Résumé

Honey bees are social insects that show division of labor and sexual dimorphism. Female honey bees differentiate in two different castes, queens or worker bees, while males are called drones. Worker bees have different tasks in the hive including collection of food, its processing, caring for brood, protecting the hive, or producing wax. The drones' only role is to mate with a virgin queen. Many studies have dealt with differences in physiology, behavior, and morphology of workers and drones. This is the first study that demonstrates differences in element accumulation and composition between workers and drones honey bees. Using inductively coupled plasma mass spectrometry, we found that worker honey bees have higher concentrations of most elements analyzed. Drones had higher concentrations of elements essential to bees, Na, P, S, Zn, Cu, and especially Se (2.2 × higher), which is known to be important for sperm quality and fertility in many animals. Until now higher Se content was not observed in male insects. These differences can be attributed to different environmental exposure, reproductive role of drones, but mostly to the food workers and drones consume. Worker bees feed on bee bread, which is rich in minerals. Drones are fed food pre-processed by worker bees.

Identifiants

pubmed: 38472584
doi: 10.1007/s11356-024-32822-z
pii: 10.1007/s11356-024-32822-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : 337-00-577/2021-09/19
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : 451-03-47/2023-01/200178
Organisme : Österreichische Agentur für Internationale Mobilität und Kooperation in Bildung, Wissenschaft und Forschung
ID : RS 17/2022

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2024. The Author(s).

Références

AL Naggar Y, Dabour K, Masry S, Sadek A, Naiem E, Giesy JP (2020) Sublethal effects of chronic exposure to CdO or PbO nanoparticles or their binary mixture on the honey bee (Apis millefera L.). Environ Sci Pollut Res 27:19004–19015. https://doi.org/10.1007/s11356-018-3314-2
doi: 10.1007/s11356-018-3314-2
Alavi MH, Allymehr M, Talebi A, Najafi G (2020) Comparative effects of nano-selenium and sodium selenite supplementations on fertility in aged broiler breeder males. Vet Res Forum 11:135–141. https://doi.org/10.30466/vrf.2018.83172.2093
doi: 10.30466/vrf.2018.83172.2093 pubmed: 32782742 pmcid: 7413000
Alburaki M, Smith KD, Adamczyk J, Karim S (2019) Interplay between Selenium, selenoprotein genes, and oxidative stress in honey bee Apis mellifera L. J Insect Physiol 117:103891. https://doi.org/10.1016/j.jinsphys.2019.103891
doi: 10.1016/j.jinsphys.2019.103891 pubmed: 31176625 pmcid: 7298915
Behmer ST (2008) Nutrition in insects BT - encyclopedia of entomology. In: Capinera JL (ed) Springer Netherlands, Dordrecht, pp 2646–2654. https://doi.org/10.1007/978-1-4020-6359-6_2277
Bilalov F, Skrebneva L, Nikitin O, Shuralev EA, Mukminov M (2015) Seasonal variation in heavy-metal accumulation in honey bees as an indicator of environmental pollution. Res J Pharm Biol Chem Sci 6:215–221
Bowen-Walker PL, 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. Entomol Exp Appl 101:207–217. https://doi.org/10.1046/j.1570-7458.2001.00905.x
doi: 10.1046/j.1570-7458.2001.00905.x
Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41:278–294. https://doi.org/10.1051/apido/2010012
doi: 10.1051/apido/2010012
Brodschneider R, Riessberger-Gallé U, Crailsheim K (2009) Flight performance of artificially reared honeybees (Apis mellifera). Apidologie 40:441–449. https://doi.org/10.1051/apido/2009006
doi: 10.1051/apido/2009006
Burden CM, Elmore C, Hladun KR, Trumble JT, Smith BH (2016) Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera). Ecotoxicol Environ Saf 127:71–79. https://doi.org/10.1016/j.ecoenv.2015.12.034
doi: 10.1016/j.ecoenv.2015.12.034 pubmed: 26802564
Chicas-Mosier AM, Cooper BA, Melendez AM, Pérez M, Oskay D, Abramson CI (2017) The effects of ingested aqueous aluminum on floral fidelity and foraging strategy in honey bees (Apis mellifera). Ecotoxicol Environ Saf 143:80–86. https://doi.org/10.1016/j.ecoenv.2017.05.008
doi: 10.1016/j.ecoenv.2017.05.008 pubmed: 28505483
Ćirić J, Spirić D, Baltić T, Lazić IB, Trbović D, Parunović N, Petronijević R, Đorđević V (2021) Honey bees and their products as indicators of environmental element deposition. Biol Trace Elem Res 199:2312–2319. https://doi.org/10.1007/s12011-020-02321-6
doi: 10.1007/s12011-020-02321-6 pubmed: 32757175
Conti ME, Astolfi ML, Finoia MG, Massimi L, Canepari S (2022) Biomonitoring of element contamination in bees and beehive products in the Rome province (Italy). Environ Sci Pollut Res 29:36057–36074. https://doi.org/10.1007/s11356-021-18072-3
doi: 10.1007/s11356-021-18072-3
Crailsheim K (1992) The flow of jelly within a honeybee colony. J Comp Physiol B 162:681–689
doi: 10.1007/BF00301617
de Barbosa MM, Fernandes ACC, Alves RSC, Alves DA, Barbosa Junior F, Batista BL, Ribeiro MC, Hornos Carneiro MF (2021) Effects of native forest and human-modified land covers on the accumulation of toxic metals and metalloids in the tropical bee Tetragonisca angustula. Ecotoxicol Environ Saf 215:112147. https://doi.org/10.1016/j.ecoenv.2021.112147
doi: 10.1016/j.ecoenv.2021.112147 pubmed: 33756294
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. https://doi.org/10.1051/apido:2002052
doi: 10.1051/apido:2002052
Es’kov EK, Es’kova MD (2013) Factors influencing wing size and body weight variation in the western honeybee. Russ J Ecol 44:433–438. https://doi.org/10.1134/S1067413613050056
doi: 10.1134/S1067413613050056
Farias RA, Nunes CN, Quináia SP (2023) Bees reflect better on their ecosystem health than their products. Environ Sci Pollut Res 30:79617–79626. https://doi.org/10.1007/s11356-023-28141-4
doi: 10.1007/s11356-023-28141-4
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. https://doi.org/10.1371/journal.pone.0183236
Fry KL, McPherson VJ, Gillings MR, Taylor MP (2023) Tracing the sources and prevalence of class 1 integrons, antimicrobial resistance, and trace elements using european honey bees. Environ Sci Technol 57:10582–10590. https://doi.org/10.1021/acs.est.3c03775
doi: 10.1021/acs.est.3c03775 pubmed: 37417314
Gekière A, Vanderplanck M, Michez D (2023) Trace metals with heavy consequences on bees: a comprehensive review. Sci Total Environ 895:165084. https://doi.org/10.1016/j.scitotenv.2023.165084
doi: 10.1016/j.scitotenv.2023.165084 pubmed: 37379929
Gordon HT (1959) Minimal nutritional requirements of the German roach, Blattella germanica L. Ann N Y Acad Sci. https://doi.org/10.1111/j.1749-6632.1959.tb36910.x
doi: 10.1111/j.1749-6632.1959.tb36910.x pubmed: 13851180
Hansen JC, Deguchi Y (1996) Selenium and fertility in animals and man–a review. Acta Vet Scand 37:19–30. https://doi.org/10.1186/BF03548116
doi: 10.1186/BF03548116 pubmed: 8659343 pmcid: 8064001
Haydak MH (1957) The Food of the Drone Larvae1. Ann Entomol Soc Am 50:73–75. https://doi.org/10.1093/aesa/50.1.73
doi: 10.1093/aesa/50.1.73
Haydak MH (1970) Honey Bee Nutrition. Annu Rev Entomol 15:143–156. https://doi.org/10.1146/annurev.en.15.010170.001043
doi: 10.1146/annurev.en.15.010170.001043
Helm BR, Slater GP, Rajamohan A, Yocum GD, Greenlee KJ, Bowsher JH (2017) The geometric framework for nutrition reveals interactions between protein and carbohydrate during larval growth in honey bees. Biol Open 6:872–880. https://doi.org/10.1242/bio.022582
doi: 10.1242/bio.022582 pubmed: 28396492 pmcid: 5483014
Henderson CE (1992) Variability in the size of emerging drones and of drone and worker eggs in honey bee (Apis mellifera L.) colonies. J Apic Res 31:114–118. https://doi.org/10.1080/00218839.1992.11101271
doi: 10.1080/00218839.1992.11101271
Hladun KR, Parker DR, Trumble JT (2015) Cadmium, copper, and lead accumulation and bioconcentration in the vegetative and reproductive organs of Raphanus sativus: implications for plant performance and pollination. J Chem Ecol 41:386–395. https://doi.org/10.1007/s10886-015-0569-7
doi: 10.1007/s10886-015-0569-7 pubmed: 25845355
Hladun KR, Di N, Liu TX, Trumble JT (2016) Metal contaminant accumulation in the hive: consequences for whole-colony health and brood production in the honey bee (Apis mellifera L.). Environ Toxicol Chem 35:322–329. https://doi.org/10.1002/etc.3273
doi: 10.1002/etc.3273 pubmed: 26448590
Hrassnigg N, Crailsheim K (2005) Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie 36:255–277
doi: 10.1051/apido:2005015
Hrassnigg N, Brodschneider R, Fleischmann PH, Crailsheim K (2005) Unlike nectar foragers, honeybee drones (Apis mellifera) are not able to utilize starch as fuel for flight. Apidologie 36:547–557. https://doi.org/10.1051/apido:2005042
doi: 10.1051/apido:2005042
Ilijević K, Vujanović D, Orčić S, Purać J, Kojić D, Zarić N, Gržetić I, Blagojević DP, Čelić TV (2021) Anthropogenic influence on seasonal and spatial variation in bioelements and non-essential elements in honeybees and their hemolymph. Comp Biochem Physiol Part - C: Toxicol Pharmacol 239. https://doi.org/10.1016/j.cbpc.2020.108852
Kunert K, Crailsheim K (1988) Seasonal changes in carbohydrate, Lipid and Protein Content in Emerging Worker Honeybees and their Mortality. J Apic Res 27:13–21. https://doi.org/10.1080/00218839.1988.11100775
doi: 10.1080/00218839.1988.11100775
Lucchetti MA, Kilchenmann V, Glauser G, Praz C, Kast C (2018) Nursing protects honeybee larvae from secondary metabolites of pollen. Proc R Soc B: Biol Sci 285:20172849. https://doi.org/10.1098/rspb.2017.2849
doi: 10.1098/rspb.2017.2849
Mao W, Schuler MA, Berenbaum MR (2024) A dietary phytochemical alters caste-associated gene expression in honey bees. Sci Adv 1:e1500795. https://doi.org/10.1126/sciadv.1500795
doi: 10.1126/sciadv.1500795
Martin-Romero FJ, Kryukov GV, Lobanov AV, Carlson BA, Lee BJ, Gladyshev VN, Hatfield DL (2001) Selenium metabolism in <em>Drosophila</em>: selenoproteins, selenoprotein mRNA expression, fertility, and mortality *. J Biol Chem 276:29798–29804. https://doi.org/10.1074/jbc.M100422200
doi: 10.1074/jbc.M100422200 pubmed: 11389138
Matsuka M, Watabe N, Takeuchi K (1973) Analysis of the food of larval drone honeybees. J Apic Res 12:3–7. https://doi.org/10.1080/00218839.1973.11099724
doi: 10.1080/00218839.1973.11099724
Monchanin C, Blanc-Brude A, Drujont E, Negahi MM, Pasquaretta C, Silvestre J, Baqué D, Elger A, Barron AB, Devaud J-M, Lihoreau M (2021) Chronic exposure to trace lead impairs honey bee learning. Ecotoxicol Environ Saf 212:112008. https://doi.org/10.1016/j.ecoenv.2021.112008
doi: 10.1016/j.ecoenv.2021.112008 pubmed: 33578129
Nation JL (2015) Insect Physiology and Biochemistry, 3rd ed. CRC Press. https://doi.org/10.1201/9780429277658
Pankiw T, Huang Z-Y, Winston ML, Robinson GE (1998) Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. J Insect Physiol 44:685–692. https://doi.org/10.1016/S0022-1910(98)00040-7
doi: 10.1016/S0022-1910(98)00040-7 pubmed: 12769952
Perugini M, Manera M, Grotta L, Abete MC, Tarasco R, Amorena M (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: Honeybees as bioindicators. Biol Trace Elem Res 140:170–176. https://doi.org/10.1007/s12011-010-8688-z
doi: 10.1007/s12011-010-8688-z pubmed: 20393811
Raes H, Cornelis R, Rzeznik U (1992) Distribution, accumulation and depuration of administered lead in adult honeybees. Sci Total Environ 113:269–279. https://doi.org/10.1016/0048-9697(92)90005-D
doi: 10.1016/0048-9697(92)90005-D pubmed: 1519047
Retschnig G, Williams GR, Mehmann MM, Yañez O, de Miranda JR, Neumann P (2014) Sex-Specific Differences in Pathogen Susceptibility in Honey Bees (Apis mellifera). PLoS One 9:e85261
doi: 10.1371/journal.pone.0085261 pubmed: 24465518 pmcid: 3894969
Roessink I, van der Steen JJM (2021) Beebread consumption by honey bees is fast: results of a six-week field study. J Apic Res 60:659–664. https://doi.org/10.1080/00218839.2021.1915612
doi: 10.1080/00218839.2021.1915612
Sadeghi A, Mozafari A-A, Bahmani R, Shokri K (2012) Use of honeybees as bio-indicators of environmental pollution in the Kurdistan Province of Iran. J Apic Sci 56:83–88. https://doi.org/10.2478/v10289-012-0026-6
doi: 10.2478/v10289-012-0026-6
Sagili RR, Metz BN, Lucas HM, Chakrabarti P, Breece CR (2018) Honey bees consider larval nutritional status rather than genetic relatedness when selecting larvae for emergency queen rearing. Sci Rep 8. https://doi.org/10.1038/s41598-018-25976-7
Schmarsow R, de la Moliné MP, Damiani N, Domínguez E, Medici SK, Churio MS, Gende LB (2023) Toxicity and sublethal effects of lead (Pb) intake on honey bees (Apis mellifera). Chemosphere 140345. https://doi.org/10.1016/j.chemosphere.2023.140345
Schmickl T, Crailsheim K (2002) How honeybees (Apis mellifera L.) change their broodcare behaviour in response to non-foraging conditions and poor pollen conditions. Behav Ecol Sociobiol 51:415–425. https://doi.org/10.1007/s00265-002-0457-3
doi: 10.1007/s00265-002-0457-3
Schmickl T, Crailsheim K (2004) Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie 35:249–263
doi: 10.1051/apido:2004019
Slater GP, Yocum GD, Bowsher JH (2020) Diet quantity influences caste determination in honeybees (Apis mellifera): caste determination in honey bees. Proc R Soc B: Biol Sci 287. https://doi.org/10.1098/rspb.2020.0614
Smith KE, Weis D (2022) Metal and Pb isotope characterization of particulates encountered by foraging honeybees in Metro Vancouver. Sci Total Environ 826:154181. https://doi.org/10.1016/j.scitotenv.2022.154181
doi: 10.1016/j.scitotenv.2022.154181 pubmed: 35231520
Snodgrass RE (1956) Anatomy of the honey bee, Comstock Series. Comstock Pub. Associates, Cornell University Press, Ithaca, NY
Szolderits MJ, Crailsheim K (1993) A comparison of pollen consumption and digestion in honeybee (Apis mellifera carnica) drones and workers. J Insect Physiol 39:877–881. https://doi.org/10.1016/0022-1910(93)90120-G
doi: 10.1016/0022-1910(93)90120-G
Taylor MP, Gillings MM, Fry KL, Barlow CF, Gunkel-Grillion P, Gueyte R, Camoin M (2023) Tracing nickel smelter emissions using European honey bees. Environmental Pollution 122257. https://doi.org/10.1016/j.envpol.2023.122257
van der Steen J, Cornelissen B, Blacquière T, Pijnenburg JEML, Severijnen M (2016) Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environ Monit Assess 188. https://doi.org/10.1007/s10661-016-5451-8
Van der Steen JJM, De Kraker J, Grotenhuis T (2012) Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environ Monit Assess 184:4119–4126. https://doi.org/10.1007/s10661-011-2248-7
doi: 10.1007/s10661-011-2248-7 pubmed: 21823048
Végh R, Csóka M, Sörös C, Sipos L (2021) Food safety hazards of bee pollen – a review. Trends Food Sci Technol 114:490–509. https://doi.org/10.1016/j.tifs.2021.06.016
doi: 10.1016/j.tifs.2021.06.016
Wang Y, Ma L, Zhang W, Cui X, Wang H, Xu B (2016) Comparison of the nutrient composition of royal jelly and worker jelly of honey bees (Apis mellifera). Apidologie 47:48–56. https://doi.org/10.1007/s13592-015-0374-x
doi: 10.1007/s13592-015-0374-x
Xu S, Wu Y, Chen Y, Lu W, Wang Y-X, Gao B, Zhang J (2022) Environmental metal exposure, seminal plasma metabolome and semen quality: evidence from Chinese reproductive-aged men. Sci Total Environ 838:155860. https://doi.org/10.1016/j.scitotenv.2022.155860
doi: 10.1016/j.scitotenv.2022.155860 pubmed: 35595136
Yu X, Jiang N, Yang Y, Liu H, Gao X, Cheng L (2023) Heavy metals remediation through bio-solidification: potential application in environmental geotechnics. Ecotoxicol Environ Saf 263:115305. https://doi.org/10.1016/j.ecoenv.2023.115305
doi: 10.1016/j.ecoenv.2023.115305 pubmed: 37517309
Zarić NM, Ilijević K, Stanisavljević L, Gržetić I (2017) Use of honeybees (Apis mellifera L.) as bioindicators for assessment and source appointment of metal pollution. Environ Sci Pollut Res 24:25828–25838. https://doi.org/10.1007/s11356-017-0196-7
doi: 10.1007/s11356-017-0196-7
Zarić NM, Deljanin I, Ilijević K, Stanisavljević L, Ristić M, Gržetić I (2018a) Honeybees as sentinels of lead pollution: spatio-temporal variations and source appointment using stable isotopes and Kohonen self-organizing maps. Sci Total Environ 642:56–62. https://doi.org/10.1016/j.scitotenv.2018.06.040
doi: 10.1016/j.scitotenv.2018.06.040 pubmed: 29894882
Zarić NM, Deljanin I, Ilijević K, Stanisavljević L, Ristić M, Gržetić I (2018b) Assessment of spatial and temporal variations in trace element concentrations using honeybees (Apis mellifera) as bioindicators. PeerJ 2018. https://doi.org/10.7717/peerj.5197
Zarić NM, Braeuer S, Goessler W (2022) Arsenic speciation analysis in honey bees for environmental monitoring. J Hazard Mater 432:1–6. https://doi.org/10.1016/j.jhazmat.2022.128614
doi: 10.1016/j.jhazmat.2022.128614
Zarić NM, Brodschneider R, Goessler W (2021) Honey bees as biomonitors – variability in the elemental composition of individual bees. Environ Res 112237. https://doi.org/10.1016/j.envres.2021.112237
Zhou X, Taylor MP, Davies PJ, Prasad S (2018) Identifying sources of environmental contamination in European honey bees (Apis mellifera) using trace elements and lead isotopic compositions. Environ Sci Technol 52:991–1001. https://doi.org/10.1021/acs.est.7b04084
doi: 10.1021/acs.est.7b04084 pubmed: 29249154

Auteurs

Nenad M Zarić (NM)

Faculty of Biology, University of Belgrade, Studentski Trg 16, 11000, Belgrade, Serbia. nenad.zaric@bio.bg.ac.rs.
Analytical Chemistry for Health and Environment, Institute of Chemistry, University of Graz, Universitaetsplatz 1, 8010, Graz, Austria. nenad.zaric@bio.bg.ac.rs.

Robert Brodschneider (R)

Institute of Biology, University of Graz, Universitaetsplatz 2, 8010, Graz, Austria.

Walter Goessler (W)

Analytical Chemistry for Health and Environment, Institute of Chemistry, University of Graz, Universitaetsplatz 1, 8010, Graz, Austria.

Classifications MeSH