ORIGINAL ARTICLE
A case study on the occurrence of pyrimethanil, cyprodinil and cyflufenamid residues in soil and on apple leaves, blossoms and pollen, and their transfer by worker bees to the hive
1
Institute of Biology and Biotechnology, College of Natural Sciences, University of Rzeszów, Poland
2
Interdisciplinary Center for Preclinical and Clinical Research, University of Rzeszów, Poland
3
Institute of Material Engineering, College of Natural Sciences, University of Rzeszów, Poland
4
Interdisciplinary Centre for Computational Modelling, College of Natural Sciences, University of Rzeszów, Poland
5
Independent researcher, Institute of Biology and Biotechnology, College of Natural Sciences, University of Rzeszów, Poland
6
Professor retired, Institute of Biology and Biotechnology, College of Natural Sciences, University of Rzeszów, Poland
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2022-01-10
Acceptance date: 2022-02-25
Online publication date: 2022-05-03
Corresponding author
Anna Koziorowska
Institute of Material Engineering, College of Natural Sciences, University of Rzeszow, Poland
Institute of Material Engineering, College of Natural Sciences, University of Rzeszow, Poland
Journal of Plant Protection Research 2022;62(2):176-188
HIGHLIGHTS
- Pesticides are transferred by the bees from the crops to the hives
- Pesticide residues are transferred to the hive immediately after use.
- The residues of pesticides in worker bees have not exceeded 0.3% of the LD50.
- Pyrimethanil and Cyprodinil have exceeded the Maximum Residue Levels in honey.
KEYWORDS
TOPICS
ABSTRACT
A field trial on the transfer of pyrimethanil, cyprodinil and cyflufenamid residues from
apple trees of Idared cultivar to hives by honeybees Apis mellifera was carried out. Two
days after spraying (Faban 500 SC and Kendo 50 EW), and on the day of spraying (Chorus
50 WG), the quantities of residues on leaves and flowers of apple trees and pollen were as
follows: pyrimethanil: 1.45 μg per cm2 of leaves, 11.51 μg per single flower and 7.18 μg · g−1
of pollen, cyprodinil:1.35, 8.64 and 7.94 μg, and cyflufenamid: 0.064, 0.266 and 0.11 μg,
respectively. All of them subsequently disappeared exponentially. Two days after, and on
the day of spraying, pyrimethanil (1.81 μg · g−1), cyprodinil (up to 0.55 μg · g−1) and cyflufenamid
(0.04 μg · g−1) were found in worker bees. Residues of all used chemicals were
found in the brood, honey and wax samples. The residues of pyrimethanil, cyprodinil and
cyflufenamid in worker bees exceeded the level of 0.2% of the LD50, which indicates that
their application rates (doses) are safe for the honey bee.
ACKNOWLEDGEMENTS
We would like to thank Mr. Kazimierz Czepiela for his
help in carrying out this research. The study was supported
by funds from the University of Rzeszów, College
of Natural Sciences.
FUNDING
The part of the research was supported by the
project Interdisciplinary Center for Preclinical and
Clinical Research (the project number RPPK.01.01.00-
18-0001/18).
RESPONSIBLE EDITOR
Piotr Kaczyński
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (53)
1.
Aleksić M., Stanisavljević D., Smiljković M., Vasiljević P., Stevanović M., Soković M., Stojković D. 2019. Pyrimethanil: Between efficient fungicide against Aspergillus rot on cherry tomato and cytotoxic agent on human cell lines. Annals of Applied Biology 175 (2): 228–235. DOI: 10.1111/aab.12532.
2.
Almasri H., Tavares D.A., Pioz M., Sené D., Tchamitchian S., Cousin M., Brunet J.L., Belzunces L.P. 2020. Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicology and Environmental Safety 203: 111013. DOI: 10.1016/j.ecoenv.2020.111013.
3.
Bakour M., Fernandes Â., Barros L., Soković M., Ferreira I.C.F.R., Iyoussi B. 2019. Bee bread as a functional product: Chemical composition and bioactive properties. Lebensmittel-Wissenschaft and Technologie 109: 276–282. DOI: 10.1016/j.lwt.2019.02.008.
4.
Batista A.C., Domingues C.E., Costa M.J., Silva-Zacarin E.C. 2020. Is a strobilurin fungicide capable of inducing histopathological effects on the midgut and Malpighian tubules of honey bees? Journal of Apicultural Research 59: 834–843. DOI: 10.1080/00218839.2020.1724678.
5.
Bernabò I., Guardia A., Macirella R., Sesti S., Crescente A., Brunelli E. 2016. Effects of long-term exposure to two fungicides, pyrimethanil and tebuconazole, on survival and life history traits of Italian tree frog (Hyla intermedia). Aquatic Toxicology 172: 56–66. DOI: 10.1016/j.aquatox.2015.12.017.
6.
Bogdanov S. 2006. Contaminants of bee products. Apidologie 37 (1): 1–18. DOI: 10.1051/apido:2005043.
7.
Böhme F., Bischoff G., Zebitz C.P., Rosenkranz P., Wallner K. 2017. From field to food—will pesticide-contaminated pollen diet lead to a contamination of royal jelly? Apidologie 49: 112–119. DOI: 10.1007/s13592-017-0533-3.
8.
Calatayud-Vernich P., Calatayud F., Simó E., Picó Y. 2018. Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environmental Pollution 241: 106–114. DOI: 10.1016/j.envpol.2018.05.062.
9.
Costa Domingues da C.E., Tadei R., Inoue L.V.B., Silva-Zacarin da E.C.M., Malaspina O. 2021. Effects of larval exposure to the fungicide pyraclostrobin on the post-embryonic development of Africanized Apis mellifera workers. Environmental Advances 4: 100069. DOI: 10.1016/j.envadv.2021.100069.
10.
Doublet V., Labarussias M., de Miranda J.R., Moritz R.F., Paxton R.J. 2015. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology 17 (4): 969–983. DOI: 10.1111/1462-2920.12426.
11.
Eeraerts M., Vanderhaegen R., Smagghe G., Meeus I. 2019. Pollination efficiency and foraging behaviour of honey bees and non-Apis bees to sweet cherry. Agricultural and Forest Entomology 22 (1): 75–82. DOI: 10.1111/afe.12363.
12.
EU Pesticides Database (2022). Available on: https://ec.europa.eu/food/plan.... [Accessed: 18 January 2022].
13.
Everich R., Schiller C., Whitehead J., Beavers M., Barrett K. 2009. Effects of captan on Apis mellifera brood development under field conditions in California almond orchards. Journal of Economic Entomology 102 (1): 20–29. DOI: 10.1603/029.102.0104.
14.
Evrenosoğlu Y., Mısırlı A. 2009. Investigations on the pollen morphology of some fruit species. Turkish Journal of Agriculture and Forestry 33 (2): 181–190. DOI: 10.3906/tar-0801-47.
15.
Ferreira E.S., Cordeiro L.V., Silva D.F., Souza H.D.S., Athayde-Filho P.F., Barbosa-Filho J.M., Scotti L., Lima E.O., Castro R.D. 2021. Antifungal activity and mechanism of action of 2-chloro-N -phenylacetamide: a new molecule with activity against strains of Aspergillus flavus. Anais da Academia Brasileira de Ciencias 93 (3): e20200997. DOI: 10.1590/0001-3765202120200997.
16.
Fritz R., Lanen C., Chapeland-Leclerc F., Leroux P. 2003. Effect of the anilinopyrimidine fungicide pyrimethanil on the cystathionine β-lyase of Botrytis cinerea. Pesticide Biochemistry and Physiology 77 (2): 54–65. DOI: 10.1016/S0048-3575(03)00094-4.
17.
Gallai N., Salles J.-M., Settele J., Vaissiere B.E. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68 (3): 810–821. DOI:10.1016/j.ecolecon.2008.06.014.
18.
Grassl J., Holt S., Cremen N., Peso M., Hahne D., Baer B. 2018. Synergistic effects of pathogen and pesticide exposure on honey bee (Apis mellifera) survival and immunity. Journal of Invertebrate Pathology 159: 78–86. DOI: 10.1016/j.jip.2018.10.005.
19.
GUS. 2020. Produkcja i handel zagraniczny produktami rolnymi w 2019 r. Available on: https://stat.gov.pl/files/gfx/... [Accessed: 18 January 2022].
20.
GUS. 2021a. Stan i struktura ludności według wieku w latach 1989–2019. Available on: https://stat.gov.pl/obszarytem... [Accessed: 18 January 2022].
21.
GUS. 2021b. Wynikowy szacunek głównych ziemiopłodów rolnych i ogrodniczych w 2021 roku. Available on: https://stat.gov.pl/download/g... [Accessed: 18 January 2022].
22.
Hrynko I., Łozowicka B., Kaczyński P. 2021. Development of precise micro analytical tool to identify potential insecticide hazards to bees in guttation fluid using LC-ESI-MS/MS. Chemosphere 263: 128143. DOI: 10.1016/j.chemosphere.2020.128143.
23.
Jankowska M., Łozowicka B., Kaczyński P. 2019. Comprehensive toxicological study over 160 processing factors of pesticides in selected fruit and vegetables after water, mechanical and thermal processing treatments and their application to human health risk assessment. Science of the Total Environment 652: 1156–1167. DOI: 10.1016/j.scitotenv.2018.10.324.
24.
Johnson R.M., Dahlgren L., Siegfried B.D., Ellis M.D. 2013. Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS One 8 (1): e54092. DOI: 10.1371/journal.pone.0054092.
25.
Kapsi M., Tsoutsi C., Paschalidou A., Albanis T. 2019. Environmental monitoring and risk assessment of pesticide residues in surface waters of the Louros River (N.W. Greece). Science of The Total Environment 650 (2): 2188–2198. DOI: 10.1016/j.scitotenv.2018.09.185.
26.
Kobylińska M. 2021. Regionalne zróżnicowanie pszczelarstwa w Polsce. In: The Polish Statistician, Statistics Poland 66 (2). Available on: https://ws.stat.gov.pl/WS/2021... [Accessed: 18 January 2022] DOI: 10.5604/01.3001.0014.7388.
27.
Majewski J. 2011. The value of crops pollination in Poland. Prace Naukowe Uniwersytetu Ekonomicznego we Wrocławiu 166: 426–435.
28.
Mayer D.F., Lunden J.D. 1986. Toxicity of fungicides and an acaricide to honey bees (Hymenoptera: Apidae) and their effects on bee foraging behavior and pollen viability on blooming apples and pears. Environmental Entomology 15 (5): 1047–1049. DOI: 10.1093/ee/15.5.1047.
29.
McKerchar M., Potts S.G., Fountain M.T., Garratt M.P.D., Westbury D.B. 2020. The potential for wildflower interventions to enhance natural enemies and pollinators in commercial apple orchards is limited by other management practices. Agriculture, Ecosystems and Environment 301: 107034. DOI: 10.1016/j.agee.2020.107034.
30.
Meng Y., Zhong K., Xiao J., Huang Y., Wei Y., Tang L., Chen S., Wu J., Ma J., Cao Z., Liao X., Lu H. 2020. Exposure to pyrimethanil induces developmental toxicity and cardiotoxicity in zebrafish. Chemosphere 255: 126889. DOI: 10.1016/j.chemosphere.2020.126889.
31.
Meo S.A., Al-Asiri S.A., Mahesar A.L., Ansari M.J. 2017. Role of honey in modern medicine. Saudi Journal of Biological Sciences 24 (5): 975–978. DOI: 10.1016/j.sjbs.2016.12.010.
32.
Milling R., Richardson C.J. 1995. Mode of action of the anilinopyrimidine fungicide pyrimethanil. 2. Effects on enzyme secretion in Botrytis cinerea. Pesticide Science 45 (1): 43–48. DOI: 10.1002/ps.2780450107.
33.
Mussen E.C., Lopez J.E., Peng C.Y.S. 2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environmental Entomology 33 (5): 1151–1154. DOI: 10.1603/0046-225X-33.5.1151.
34.
NIK. 2017. NIK o wsparciu pszczelarstwa. Available on: https://www.nik.gov.pl/aktualn... [Accessed: 18 January 2022].
35.
Piechowicz B., Kobielska M., Koziorowska A., Podbielska M., Szpyrka E., Pieniążek M., Potocki L. 2021a. Dynamics of λ-cyhalothrin disappearance and expression of selected P450 genes in bees depending on the ambient temperature. Open Chemistry 19 (1): 1242–1249. DOI: 10.1515/chem-2021-0104.
36.
Piechowicz B., Sadło S., Piechowicz I., Czawa M. 2019. Formal and legal aspects of obtaining honey from beehives located in apple orchard during blossoming and intensive chemical protection (in Polish). Research Papers of the University of Work Protection Management in Katowice 1 (15): 125–134. DOI: 10.32039/WSZOP/1895-3794-2019-09.
37.
Piechowicz B., Sieńko J., Mytych J., Grodzicki P., Podbielska M., Szpyrka E., Zaręba L., Piechowicz I., Sadło S. 2021b. Assessment of risk to honey bees and honey consumers resulting from the insect exposure to captan, thiacloprid, penthiopyrad, and λ-cyhalothrin used in a commercial apple orchard. Environmental Monitoring and Assessment 193 (3): 129. DOI: 10.1007/s10661-021-08913-6.
38.
Piechowicz B., Woś I., Podbielska M., Grodzicki P. 2018. The transfer of active ingredients of insecticides and fungicides from an orchard to beehives. Journal of Environmental Science and Health B 53 (1): 18–24.
39.
Pohorecka K., Szczęsna T., Witek M., Miszczak A., Sikorski P. 2017. The exposure of honey bees to pesticide residues in the hive environment with regard to winter colony losses. Journal of Apicultural Science 61 (1): 105–125. DOI: 10.1515/jas-2017-0013.
40.
Potts S.G., Biesmeijer J.C., Kremen C., Neumann P., Schweiger O., Kunin W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25 (6): 345–353. DOI: 10.1016/j.tree.2010.01.007.
41.
PPDB. Pesticide Properties Database (2022). Available on: http://sitem.herts.ac.uk/aeru/... [Accessed: 18 January 2022].
42.
Sad Sło. 2002. Disappearance of pyrimethanil residues on tomato plants. Journal of Agricultural and Food Chemistry 50 (5): 1089–1091. DOI: 10.1021/jf010570y.
43.
Sadło S., Grodzicki P., Piechowicz B. 2017. Dissipation of captan, boscalid and trifloxystrobin residues in apples of four varieties within 2 months before their harvest. Journal of Plant Diseases and Protection 124: 177–184. DOI: 10.1007/s41348-016-0069-1.
44.
Sadło S., Piechowicz B., Podbielska M., Szpyrka E. 2018. A study on residue levels of fungicides and insecticides applied according to the program of raspberry protection. Environmental Science and Pollution Research 25 (8): 8057–8068. DOI: 10.1007/s11356-017-1098-4.
45.
Sadło S., Szpyrka E., Stawarczyk M., Piechowicz B. 2014. Behavior of pyrimethanil, pyraclostrobin, boscalid, cypermethrin and chlorpyrifos residues on raspberry fruit and leaves of Laszka variety. Journal of Environmental Science and Health B. 49 (3): 159–168. DOI: 10.1080/03601234.2014.858005.
46.
SANTE 2017. Analytical quality control and method validation procedures for pesticide residues analysis in food and feed. SANTE/2017/11813. Available on: https://www.eurl-pesticides.eu... [Accessed: 18 January 2022].
47.
Silva V., Mol H.G.J., Zomer P., Tienstra M., Ritsema C.J., Geissen V. 2019. Pesticide residues in European agricultural soils – A hidden reality unfolded. Science of the Total Environment 653: 1532–1545. DOI: 10.1016/j.scitotenv.2018.10.441.
48.
Smith D.B., Arce A.N., Ramos R.A., Bischoff P.H., Burris D., Ahmed F., Gill R.J. 2020. Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees. Proceedings of the Royal Society B: Biological Sciences 287: 20192442. DOI: 10.1098/rspb.2019.2442.
49.
Stavnichenko P.V., Antonenko A.M., Korshun M.M., Bardov V.G. 2016. Toxicological and hygienic regulation and assessment of danger of the new fungicide-cyflufenamid. Medical Perspectives 21 (2): 106–111. DOI: 10.26641/2307-0404.2016.2.72279.
50.
Szpyrka E., Sadło S. 2009. Disappearance of azoxystrobin, cyprodinil, and fludioxonil residues on tomato leaves in a greenhouse. Journal of Plant Protection Research 49 (2): 204–208. DOI: 10.2478/v10045-009-0030-4.
51.
Traynor K.S., van Engelsdorp D., Lamas Z.S. 2021. Social disruption: Sublethal pesticides in pollen lead to Apis mellifera queen events and brood loss. Ecotoxicology and Environmental Safety 214: 112105. DOI: 10.1016/j.ecoenv.2021.112105.
52.
Wu J.Y., Anelli C.M., Sheppard W.S. 2011. Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS One 6 (2): e14720. DOI: 10.1371/journal.pone.0014720.
53.
Yele V., Sanapalli B.K.R., Wadhwani A.D., Mohammed A.A. 2021. Benzohydrazide and phenylacetamide scaffolds: New putative ParE inhibitors. Frontiers in Bioengineering and Biotechnology 17(9): 669728. DOI: 10.3389/fbioe.2021.669728.
| eISSN: | 1899-007X |
| ISSN: | 1427-4345 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
