Honey bee exposure scenarios to selected residues through contaminated beeswax
Graphical abstract
Introduction
Within the colony, wax is secreted by worker honey bees (Apis mellifera) and its production reaches a maximum when they are 10–18 days old (Hepburn et al., 2014). Beeswax is essential to the colony. Within the hive, beeswax is used by worker honey bees to build combs consisting of hexagonal cells that will serve to store food resources, beebread (pollen added with honey, nectar and honey bee secretions) and honey, and to shelter brood (eggs, larvae and pupae of honey bees) during its development.
Beeswax can be contaminated by residues of veterinary drugs applied by beekeepers to treat beehives, notably to control the parasite Varroa destructor (e.g. Bogdanov et al., 1998; Boi et al., 2016; Calatayud-Vernich et al., 2017; Kast et al., 2020; Lozano et al., 2019; Martel et al., 2007; Rosenkranz et al., 2010). Over time, repeated application of varroacides can result in accumulation of residues in beeswax given that they are mostly fat-soluble and non-volatile (Johnson et al., 2010; Lozano et al., 2019; Thompson, 2012; Wallner, 1999). From their environment, honey bees themselves are likely to bring pesticide residues, in particular of plant protection products used in agriculture, back to hives through pollen, nectar, water, honeydew and/or propolis they collect (e.g. Böhme et al., 2018; Calatayud-Vernich et al., 2018; Daniele et al., 2018; Mullin et al., 2010; Piechowicz et al., 2018; Simon-Delso et al., 2014; Tong et al., 2018; Traynor et al., 2016). Within the hive, both types of residues can end up in beeswax of the existing combs (e.g. Chauzat and Faucon, 2007; Herrera López et al., 2016; Ostiguy et al., 2019; Perugini et al., 2018; Ravoet et al., 2015).
Throughout their lives, honey bees can be affected by many stressors, different in nature and origin (ANSES, 2015; Rortais et al., 2017). Next to biotic stressors, and in particular the ectoparasitic V. destructor mite (Boecking and Genersch, 2008), but also Nosema ceranae (Microsporidia) (Higes et al., 2009), viruses (e.g. Black queen cell virus (BQCV) or Deformed wing virus (DWV) (Cornman et al., 2012)), and/or predators (e.g. Asian hornet Vespa velutina (Rortais et al., 2010)), honey bees can also be exposed to abiotic stressors like the residues of a broad range of chemicals that affect the honey bee (colony) health (Johnson et al., 2010; Sánchez-Bayo and Goka, 2014).
This study focuses on the assessment of honey bee health risk posed by the presence of pesticide and veterinary drug residues in beeswax and, to prevent and/or control this potential health risk, aimed to calculate maximum concentrations for several residues following a three-scenario analysis. Beeswax exceeding the provisional action limits based on these maximum concentrations should not be put on the market.
Section snippets
Materials and methods
Wilmart et al. (2016) listed pesticides and veterinary drugs of which residues were detected in beeswax in Europe. This list was then completed with results of more recent studies (Herrera López et al., 2016; Calatayud-Vernich et al., 2017; Daniele et al., 2018; Perugini et al., 2018; Lozano et al., 2019; Shimshoni et al., 2019; El Agrebi et al., 2019, El Agrebi et al., 2020a, El Agrebi et al., 2020b). Table 1 summarizes, for each of these chemical substances, (contact/oral) acute median lethal
Calculation
Honey bee's exposure to each of these twenty-two selected residues through beeswax was then assessed following a three-scenario analysis:
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Scenario 1 corresponds to the exposure of worker larvae following their close contact with wax constituting the cells in which they develop;
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Scenario 2 corresponds to the exposure of worker larvae following consumption of the larval food that was contaminated from contact with contaminated wax;
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Scenario 3 corresponds to the exposure of adult worker honey bees
Results
The maximum concentrations calculated following the three scenarios considered above for the 22 selected active substances are shown in Table 2, Table 3, Table 4 respectively. The maximum concentrations calculated following scenario 1 range from 0.056 mg/kg wax for cyfluthrin to 19218 mg/kg wax for piperonyl butoxide. The maximum concentrations calculated following scenario 2 range from 0.122 mg/kg wax for fipronil to 7534 mg/kg wax for piperonyl butoxide. The maximum concentrations calculated
Discussion
When we compare the proposed provisional action limits (Table 5) to actual residue levels found by El Agrebi et al., 2019, El Agrebi et al., 2020b in beeswax samples from Belgian apiaries (Table 6), we see that most of these limits are met on average. Only for cypermethrin, the mean concentration of 2.34 mg/kg determined in brood comb wax samples (El Agrebi et al., 2020b) exceeds the provisional action limit of 0.150 mg/kg. Compared to other recent European studies (Table 6), the proposed
Conclusions
Twenty-two pesticides and veterinary drugs of which residues were detected in beeswax in Europe have been selected according to different criteria. The risk to honey bee health posed by the presence of these substances in wax was assessed based on three exposure scenarios. Following these scenarios, maximum concentrations which should not be exceeded in beeswax in order to protect honey bee health were calculated for each selected substance. Based on these values, provisional action limits were
Abbreviations
- FASFC
Federal Agency for the Safety of the Food Chain
- Oral/contact LD50 (median lethal dose)
is a statistically derived single dose of a substance that can cause death in 50 per cent (50%) of animals when administered by the oral route (OECD, 1998a)/per contact (OECD, 1998b). The LD50 value is expressed in mg of test substance per bee
- PPDB
Pesticide Properties DataBase (http://sitem.herts.ac.uk/aeru/ppdb/en/index.htm)
- VSDB
Veterinary Substances DataBase (http://sitem.herts.ac.uk/aeru/vsdb/index.htm)
CRediT authorship contribution statement
Olivier Wilmart: Data curation, Writing – original draft, Writing – review & editing. Anne Legrève: Conceptualization, Methodology, Validation. Marie-Louise Scippo: Conceptualization, Methodology, Validation. Wim Reybroeck: Conceptualization, Methodology, Validation. Bruno Urbain: Conceptualization, Methodology, Validation. Dirk C. de Graaf: Conceptualization, Methodology, Validation. Pieter Spanoghe: Conceptualization, Methodology, Validation. Philippe Delahaut: Conceptualization, Methodology,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment
The authors acknowledge the members of the working group (SciCom, 2018) for their collaboration and of the Scientific Committee of the FASFC for their supervision and validation of the approach on which this study is based.
Funding sources
None.
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