Descrizione 1
Valter Bellucci, Franco Mutinelli (Istituto Zooprofilattico Sperimentale delle Venezie – IZSVe), Valerio Silli
Bees, pollen, and other beekeeping matrices provide important information about the state of the environment, particularly in relation to chemical contamination from plant protection products (pesticides). Laboratory analyses can detect active substances from these products on the bees' bodies and in the pollen they collect during their flights in treated areas.
ISPRA has long been involved in research and monitoring activities aimed at identifying the possible factors and causes of honey bee colony mortality, including those related to agricultural practices involving the use of pesticides, especially in natural and agriculturally intensive areas.
The data collected suggest a fluctuating trend around an annual average of several dozen bee mortality cases, often with the detection of active pesticide ingredients on the bees or in other beekeeping matrices.
The indicator describes bee mortality events recorded across the national territory, correlating them with the detection of active substances from plant protection products (pesticides) in beekeeping matrices or on the bees themselves. These cases are confirmed by officially recognized and authorized laboratories (such as IIZZSS, ARPA, ICQRF, and others).
Data are collected through monitoring of bees and hive products, based on voluntary reports from pollinators. This monitoring system was established in 2014 by the Ministry of Health with support from the National Health Service (SSN). The monitoring involves public veterinary services, plant health services, and laboratories of the Experimental Zooprophylactic Institutes (II.ZZ.SS.), which operate in an integrated and coordinated manner with other institutions by following dedicated protocols and guidelines (Ministry of Health Guidelines, 2014).
Additionally, this indicator can also be informed by reports from beekeepers and findings from research projects on the health of bees and hives, such as the SPIA-BEENET project coordinated by the Ministry of Agriculture, Food Sovereignty and Forests.
To identify, at the national level, the relationships and magnitude by which active substances in plant protection products are associated with mortality events in managed honeybee populations (Apis mellifera subsp.). These data also provide insights into the spatial distribution and environmental contamination by pesticides.
Regulatory framework for beekeeping and sustainable pesticide use
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Law No. 313 of 24 December 2004 – “Regulations on beekeeping”: establishes the legal basis for the protection, promotion, and sustainable development of apiculture in Italy.
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Amendments to Law No. 313/2004 and additional provisions on beekeeping, including a delegation to the Government for regulatory simplification and the protection of the national beekeeping sector (Dossier No. 78, 18 December 2023 – Reference Act A.C. 706).
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Interministerial Decree of 15 July 2015 – Indicators for the National Action Plan (NAP) on the sustainable use of plant protection products (G.U. 27 July 2015, General Series No. 172).
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Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides.
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Legislative Decree No. 150 of 14 August 2012 – Transposition of Directive 2009/128/EC into national law.
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Interministerial Decree of 22 January 2014 – National Action Plan (NAP) for the sustainable use of plant protection products, adopted pursuant to Article 6 of Legislative Decree No. 150/2012.
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Interministerial Decree of 10 March 2015 – Guidelines for the protection of aquatic environments and drinking water, and for reducing the use and risks of plant protection products in Natura 2000 sites and protected natural areas, in accordance with the NAP.
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Decree of 22 January 2018, No. 33 – Regulation on measures and requirements for the safe use of plant protection products by non-professional users.
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Presidential Decree No. 320/1954 – Veterinary Police Regulations.
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Regulation (EC) No. 852/2004 – Lays down general hygiene rules for foodstuffs, including controls and surveillance activities for food of animal origin, reaffirmed under the remit of the Ministry of Agriculture (Project SPIA-BEENET).
Descrizione 2
Bellucci V., Bianco P., Formato G., Mutinelli F., Porrini C., Lodesani M. (2016). Morie dì api e prodotti fitosanitari. Apitalia Ricerca, 12/2016, 46-52, (https://www.researchgate.net/profile/Pietro_Bianco/publication/312295130_Morie_di_api_e_prodotti_fitosanitari/links/5878bf1b08ae329d622a8ac6/Morie-di-api-e-prodotti-fitosanitari.pdf);
Bellucci, V., Lucci, S., Campanelli, F., Sannino R., Formato, G., Giacomelli, A., Scaramozzino, Baggio A. (2010). Risultati del primo semestre di attività dell’indagine sul fenomeno della moria delle api all’interno delle aree naturali protette. APOidea Anno VII, 23-27;
Bellucci V., Bianco P. M., Iorio M. (2018). Il mondo complesso delle api. Scienze e Ricerche 56, 5-10;
Bellucci V., Lucci S., Bianco P., Ubaldi A., Felicioli A., Porrini C., Mutinelli F., Battisti S., Spallucci V., Cersini A., Pietropaoli M. and Formato G. (2019). Monitoring honey bee health in five natural protected areas in Italy. Veterinaria Italiana, 55 (1), pp. 15-25. doi: 0.12834/VetIt.1209.6739.4;
Celli G., Maccagnani B. (2003). Honey bees as bioindicators of environmental pollution. Bulletin of Insectology 56 (1): 137-139, 2003 ISSN 1721-8861;
ISPRA (2021) Gli apoidei e l'agricoltura sostenibile Edizione: Quaderni NATURA e Biodiversità 16/21Editore: ISPRA Editore: ISPRAISBN: 978-88-448-1050-4 https://www.isprambiente.gov.it/it/pubblicazioni/quaderni/natura-e-biodiversita/quaderno-nat-bio-gli-apoidei-e-agricoltura-sostenibile
ISPRA (2020), Rapporto ISPRA 330/2020 “La sperimentazione dell'efficacia delle Misure del Piano d'Azione Nazionale per l'uso sostenibile dei prodotti fitosanitari (PAN) per la tutela della biodiversità” https://www.isprambiente.gov.it/it/pubblicazioni/rapporti/la-sperimentazione-dellefficacia-delle-misure-del-pan-per-la-tutela-della-biodiversita
ISPRA (2015), Rapporto 216/2015. Valutazione del rischio potenziale dei prodotti fitosanitari nelle Aree Natura 2000;
ISPRA (2011). Indagine tecnico conoscitiva sul fenomeno della moria delle api all’interno delle aree naturali protette Relazione Finale, pp. 185 (https://www.minambiente.it/sites/default/files/archivio/allegati/vari/indagine_tecnico_conoscitiva_moria_api_rapporto_finale.pdf) ;
Girotti S.,Ghini E., Maiolini L., Bolelli E., Ferri N. (2013). Trace analysis of pollutants by use of honeybees, immunoassays, and chemiluminescence detection. Anal Bioanal Chem 405: 555 (https://doi.org/10.1007/s00216-012-6443-3);
Ministero della salute (2014). Linee guida per la gestione delle segnalazioni di moria o spopolamento degli alveari connesse all’utilizzo di agro farmaci, (https://www.izsvenezie.it/linee-guida-per-la-gestione-delle-segnalazioni-di-moria-o-spopolamento-degli-alveari-connesse-allutilizzo-di-fitofarmaci/) ;
Mitchell E. A. D, Mulhauser B., Mulot M., Mutabazi A., Glauser G., Aebi1 A. (2017). A worldwide survey of neonicotinoids in honey. Science 358, (6359): 109-111;
Neumann., P., Carreck N. (2010). Honey bee colony losses. J. Apic. Res. 49 (1): 1-6. (http://www.ask-force.org/web/Bees/Neumann-Honey-Bee-Colony-Losses-2010.pdf (accessed 20/02/2013));
Porrini, C., Sabatini, A., Girotti, S., Ghini, S., Medrzycki, P., Grillenzoni, F., Bortolotti, … Celli G. (2003). Honey bees and bee products as monitors of the environmental contamination APIACTA 38, 63-70;
Porrini C., Mutinelli F., Bortolotti L., Granato A., Laurenson L., Roberts K., et al. (2016). The Status of Honey Bee Health in Italy: Results from the Nationwide Bee Monitoring Network. PLoS ONE 11(5): e0155411. doi.org/10.1371/journal.pone.0155411;
Rişcu A., Bura M. (2013). The impact of pesticides on honey bees and hence on humans. Animal Science and Biotechnologies, 46 (2), 272;
Sánchez-Bayo F., Goulson D., Pennacchio F, Nazzi F., Goka K., Desneux N. (2016). Are bee diseases linked to pesticides? — A brief review. Environment International 89–90, 7–11;
Whitehorn P.R., Connor S.O. Wackers F.L., Goulson D., (2012). Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production. Science 336 (6079): 351-352. (https://www.sussex.ac.uk/webteam/gateway/file.php?name=whitehorn-2012.pdf&site=411);
http://www.izslt.it/apicoltura
http://www.isprambiente.gov.it/it
http://www.reterurale.it/api
https://www.izsvenezie.it/istituto/centri-di-referenza-nazionale/apicoltura/
http://api.entecra.it/index.php?c=8
http://www.informamiele.it/
http://www.federapi.biz/index.php?option=com_content&task=view&id=669&Itemid=0
http://www.mieliditalia.it/
https://www.anaiapi.it/
Data on bee mortality may be underestimated, as reporting and data collection are voluntary, with no measures in place to encourage affected beekeepers or to protect their productive activities.
There are limitations in data collection, as toxic active ingredients degrade rapidly in the environment due to atmospheric agents (e.g., neonicotinoids, pyrethroids). Therefore, it is necessary that beekeeping matrices—particularly dead bees—be sampled promptly after the reported event and stored at freezing temperatures until laboratory analysis.
To enhance the reporting of bee mortality cases by beekeepers and improve data accuracy, it would be advisable to introduce protective measures that encourage beekeepers to report incidents and collaborate with regulatory bodies. This would facilitate swift investigations while ensuring the continuation of the productive activities of their enterprises.
Qualificazione dati
http://www.iizzss.it/
National; Regional
2015-2023
Qualificazione indicatore
ISPRA analyzes the data provided by the II.ZZ.SS., validates it, processes it, and aggregates it based on spatial and temporal parameters.
In 2023, 51 suspected cases of apiary poisoning linked to the use of plant protection products were reported, 39 of which showed the presence of at least one or more active ingredients—more than double the cases reported in the previous year (16 cases, Table 1).
It is important to note that these data may not fully represent the totality of bee mortality events, as beekeepers often choose not to report these incidents to avoid inspections by regulatory bodies.
As in previous years, the highest number of reported bee mortality cases in 2023 occurred in May and April, coinciding with spring bloom periods (Figure 1). During these months, the application of plant protection treatments is prohibited, as bees engage in intense foraging activity, making them more vulnerable to environmental contaminants, particularly the pesticides used in agricultural areas.
Data recorded from 2015 to 2023 highlights a fluctuating trend, with several dozen cases of honey bee mortality per year, where active ingredients were detected on the bees' bodies or in other beekeeping matrices. In 2016, 2017, and 2019, bee mortality cases were approximately 50, while in 2015, 2018, 2020, 2021, and 2023, the numbers were 31, 32, 38, 32, and 39, respectively (Table 1). Only in 2022, there was a halving of beekeeping matrix samples, where active substances from plant protection products were detected following reports, with 16 recorded cases. The observed trend indicates continuous exposure to plant protection products, especially in certain areas of the country (Figure 2).
It is not possible to establish a clear trend, as these figures may be underestimated due to unreported or delayed reports of bee mortality events. Beekeepers often choose not to report such cases to avoid official inspections by regulatory bodies, either due to concerns about compliance with beekeeping product inventory records or with the documentation of applied treatments. Additionally, the time required to confirm a probable or definitive bee mortality event due to pesticides is often excessively long. All these factors contribute to the underestimation of reported cases compared to actual occurrences.
Dati
Figure 1: Cases of bee mortality associated with the presence of active substances, categorized by month
ISPRA processing based on data from II.ZZ.SS
Figure 2: Cases of bee mortality associated with the presence of active substances, by region
ISPRA processing based on data from II.ZZ.SS
Table 1: Cases of bee mortality associated with the presence of active substances, by region
ISPRA processing based on data from II.ZZ.SS
Table 2: Active substances detected in samples of dead bees
ISPRA processing based on data from II.ZZ.SS
The causes of abnormal honey bee mortality, according to available information, can be attributed both to pesticide poisoning and to the action of various pathogens affecting bees. In cases where laboratory analysis for active ingredients found in plant protection products tested positive, the presence of one or more active substances was detected, indicating that a combination of multiple factors can lead to abnormal mortality and colony depopulation.
Data on bee mortality from 2015 to 2023 continues to suggest, presumably, frequent misuse of pesticides, as honey bees and beekeeping matrices consistently reveal the presence of one or more active ingredients.
According to data analysis conducted over the nine-year period examined (Table 2), the most toxic active substances detected in samples were:
In 2023, as in previous years, pyrethroids were among the most common active ingredients, widely used in agriculture as well as for mosquito and pest control. In particular, cypermethrin, permethrin, and tetramethrin were frequently found on bee bodies. This class of chemical compounds is highly toxic to pollinating insects, including honey bees.
Piperonyl-Butoxide showed consistent presence over the years, as it is widely used as a synergist in many plant protection products, which explains its detection on bee bodies.
Among neonicotinoids, in 2023, only acetamiprid was detected, whereas in previous years, the much more toxic imidacloprid, clothianidin, and thiamethoxam were recorded.
Dimethoate and its primary metabolite, omethoate, are systemic organophosphate insecticides characterized by high toxicity, including for honey bees.
When analyzing bee mortality data with pesticide residues in beekeeping matrices by region, it was observed that in 2023, as in previous years, Veneto and the Autonomous Province of Bolzano recorded the highest number of positive detections, with 19 and 6 cases, respectively. The trend was also confirmed for Piedmont (3 cases), Calabria (4), Valle d’Aosta and Emilia-Romagna (2 cases each), and finally Friuli-Venezia Giulia and Campania (1 case each) (Table 1 and Figure 2).