BEE MORTALITY CAUSED BY THE USE OF PLANT PROTECTION PRODUCTS

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    Update date
    Authors

    Valter Bellucci, Franco Mutinelli (Istituto Zooprofilattico Sperimentale delle Venezie – IZSVe), Valerio Silli

    Abstract
    Graph
    Abstract

    Bees, pollen, and other beekeeping matrices provide important information about the state of the environment and on contamination, particularly chemical contamination from plant protection products (pesticides) that may be present in the environment. Laboratory analyses allow for the detection of active substances contained in the plant protection products used in areas where the insects fly and forage, identifying these traces on the bees' bodies and in the pollen.
    ISPRA has long been involved in research and monitoring activities aimed at identifying the possible factors and causes responsible for honey bee colony mortality, including those related to various agricultural practices involving the use of pesticides in both natural and intensive agricultural areas. The data collected show a fluctuating trend around an annual average of several dozen bee mortality cases, where active pesticide ingredients were detected on the bees' bodies or in other beekeeping matrices.

    Description

    The indicator describes bee mortality events recorded across the national territory by correlating them with the detection of active substances from plant protection products in beekeeping matrices or on the bees themselves; these cases are confirmed by analyses conducted in officially recognized and authorized laboratories, such as IIZZSS, ARPA, ICQRF, and others. Data are collected through the monitoring of bees and hive products based on voluntary reports from beekeepers, a system established in 2014 by the Ministry of Health with the support of the National Health Service (SSN).
    These controls involve the public Veterinary Services, the Phytosanitary Services, and the laboratories of the Experimental Zooprophylactic Institutes (II.ZZ.SS.), which operate in an integrated and coordinated manner with other institutions through the application of specific protocols and guidelines (Ministry of Health Guidelines, 2014). Furthermore, this indicator can be informed by reports from beekeepers and the findings of research projects on the health status of bees and hives, such as the SPIA-BEENET project coordinated by the Ministry of Agriculture, Food Sovereignty and Forests

    Purpose

    Identify the national relationships and the extent to which active substances in plant protection products are associated with mortality events in managed honey bees (Apis mellifera subsp.). Furthermore, it is possible to highlight the most widespread and commonly used active substances, describing the monthly and seasonal trends of mortality. Such data also provide essential information regarding the distribution and environmental contamination of pesticides.

    Policy relevance and utility for users
    It is of national scope or applicable to environmental issues at the regional level but of national significance.
    It is able to describe the trend without necessarily providing an evaluation of it.
    It is simple and easy to interpret.
    It is sensitive to changes occurring in the environment and/or human activities
    Analytical soundness
    Be theoretically well founded in technical and scientific terms
    Measurability (data)
    Readily available or made available at a reasonable cost/benefit ratio
    An “adequate” spatial coverage
    An “appropriate” temporal coverage
    Main regulatory references and objectives

     Beekeeping framework legislation: Law No. 313 of 24 December 2004 – "Beekeeping Regulations".

    • Amendments to Law No. 313 of 24 December 2004, and other provisions concerning beekeeping, as well as the delegation to the Government for regulatory simplification and the protection of the national beekeeping sector.
    • Dossier No. 78 – Elements for evaluating aspects of constitutional legitimacy, 18 December 2023. Information on reference documents A.C. 706.
    • Interministerial Decree of 15 July 2015 – Indicators for the National Action Plan (NAP) on the sustainable use of plant protection products (Official Gazette, 27 July 2015, General Series No. 172).
    • 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].
    • Legislative Decree No. 150 of 14 August 2012 – "Implementation of Directive 2009/128/EC establishing a framework for Community action for the sustainable use of pesticides".
    • Interministerial Decree of 22 January 2014 – "National Action Plan (NAP) for the sustainable use of plant protection products, adopted pursuant to Article 6 of the aforementioned Legislative Decree No. 150 of 14 August 2012".
    • Interministerial Decree of 10 March 2015 – "Guidelines for the protection of the aquatic environment and drinking water and for the reduction of the use of plant protection products and related risks in Natura 2000 sites and protected natural areas," as provided for by the National Action Plan.
    • Decree No. 33 of 22 January 2018 – Regulation on measures and requirements for plant protection products for safe use by non-professional users.
    • Presidential Decree No. 320/1954 – Veterinary Police Regulations.
    • Control and surveillance activities for food products of animal origin, as reiterated by Regulation (EC) No. 852/2004 and the Ministry of Agriculture (SPIA-BEENET project).
    • Ministry of Health Decree of 27 January 2025 – Amendments to the Decree of 7 March 2023, concerning the operating manual for the management and operation of the identification and registration system for operators, establishments, and animals (I&R system). (25A01598) Official Gazette, General Series No. 63 of 17 March 2025.
    DPSIR
    Impact
    Indicator type
    Descriptive (A)
    References

    Bellucci V., Bianco P., Formato G., Mutinelli F., Porrini C., Lodesani M. (2016). Deaths of bees and plant protection products. 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). Results of the first semester of activity of the investigation into the phenomenon of bee deaths within protected natural areas. APOidea Year VII, 23-27; 

    Bellucci V., Bianco P. M., Iorio M. (2018). The complex world of bees. Science and Research 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) Apoidea and sustainable agriculture Edition: Quaderni NATURA e Biodiversità 16/21Publisher: ISPRA Publisher: 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), ISPRA Report 330/2020 "Testing the effectiveness of the Measures of the National Action Plan for the sustainable use of plant protection products (PAN) for the protection of biodiversity" https://www. isprambiente. gov. it/it/pubblicazioni/rapporti/la-sperimentazione-delleconomia-delle-misure-del-pan-per-la-tutela-della-biodiversita

    ISPRA (2015), Report 216/2015. Assessment of the potential risk of plant protection products in Natura 2000 areas; 

    ISPRA (2011). Technical survey on the phenomenon of bee deaths within protected natural areas. Final Report, pp. 185. 

    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); 

    Ministry of Health (2014). Guidelines for the management of reports of die-off or depopulation of beehives connected to the use of agropharmaceuticals, (https://www. izsvenezie. it/linee-guida-per-la-gestion-delle-segnalazioni-di-moria-o-spopolamento-degli-alveari-connesse-alluso-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 loss s. J. Apic. Res. 49 (1): 1-6. (http://www. ask-force. org/web/Bees/Neumann-Honey-Bee-Colony-Losses-2010. pdf (accessed 02/20/2013)); 

    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/associazione/centri-di-reformazione-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/

    Limitations

    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 (e.g., neonicotinoids, pyrethroids) degrade rapidly in the environment due to atmospheric agents such as temperature, UV radiation, and precipitation,. To prevent this, it is necessary that beekeeping matrices—particularly dead bees—be sampled promptly after the reported event and stored at freezing temperatures until laboratory analysis.

    Further actions

    In order to encourage beekeepers to report mortality events and thus improve data accuracy, it may be appropriate to introduce protection measures for beekeeping activities. Such measures should incentivize reporting and collaboration with regulatory bodies, while simultaneously ensuring the timely conduct of investigations and the continuation of the holding's production activities.

    Data source

    ASL: Local Health Authorities (AA.SS.LL).
    CREA: Council for Research and Economics in Agriculture.
    II. ZZ. SS.: Experimental Zooprophylactic Institutes (II.ZZ.SS.).
    MASAF: Ministry of Agriculture, Food Sovereignty and Forests (formerly MiPAAF - Ministry of Agricultural, Food and Forestry Policies)

    Data collection frequency
    Yearly
    Data availabilty

    http://www. iizzss. it/

    Spatial coverage

    National; Regional

    Time coverage

    2015-2024

    Core SET
    7° Programma di azione per l’Ambiente Europeo (7° EAP) - Dati sull’ambiente
    Processing methodology

    ISPRA analyzes the data provided by the II.ZZ.SS., validates it, processes it, and aggregates it based on spatial and temporal parameters

    Update frequency
    Year
    Data quality

    The indicator is relevant as it provides information on the spread and environmental contamination caused by plant protection products; however, data collection has limitations, as toxic active ingredients degrade rapidly in the environment due to atmospheric factors (e.g., neonicotinoids and pyrethroids).
    Data is voluntarily reported by beekeepers to the veterinary services of the territorially competent Local Health Authorities (AA.SS.LL). Nevertheless, beekeepers do not always report mortality cases to avoid potential restrictive or sanctioning measures, particularly if they are not compliant with the National Beekeeping Registry. In light of these factors, the indicator may underestimate the actual mortality and depopulation events occurring in the area.

    Status
    Poor
    Trend
    Undefinable
    State assessment/description

    In 2024, 51 suspected cases of apiary poisoning linked to the use of plant protection products were reported; in 26 of these cases, the presence of one or more active substances was detected (Table 1) . It should be highlighted that these data may not represent the total number of bee mortality events, as beekeepers often choose not to report such incidents to avoid being subjected to inspections by control bodies . During 2024, following the trend of the previous ten years, the months with the highest number of reported mortalities included April and May, coinciding with spring blooms (Figure 1) . During these periods, phytosanitary treatments are prohibited because bees engage in intense foraging activity, which makes them more vulnerable to widespread environmental pollutants and specifically to the plant protection products used in agricultural areas .

    Trend assessment/description

    Data collected from 2015 to 2024 highlight a fluctuating trend oscillating around an annual average of approximately 37 bee mortality cases, where active substances were detected on the bees' bodies or in other beekeeping matrices. In 2016, 2017, and 2019, mortality cases averaged around 50 units, while in 2015, 2018, 2020, 2021, 2023, and 2024, the recorded figures were 31, 32, 38, 32, 39, and 26, respectively. Only in 2022 was there a halving of cases, with just 16 detections of active substances from plant protection products (PPPs) following a report. Nevertheless, the observed trend indicates the continuous presence of plant protection products, particularly in certain areas of the country (Figure 2).
    It is not possible to establish a clear trend as the reported cases may not be exhaustive due to unreported or delayed mortality events. Beekeepers may be deterred from reporting mortality to avoid official inspections by regulatory bodies or due to concerns regarding the compliance of their inventory records for beekeeping materials, products, and performed treatments. The excessively long timeframes required to confirm a probable or certain mortality event linked to plant protection products are also a significant factor. All these factors contribute to the underestimation of reported mortalities compared to actual occurrences. Starting from March 2025, pursuant to the Decree of 27 January 2025, registration will only be mandatory for mortality events that exceed 50% of the apiary's size.


    Comments

    According to the information provided, the causes of abnormal mortality can be attributed both to poisoning by plant protection products and to the impact of various pathogens on bees. When laboratory analyses for active substances contained in plant protection products return a positive result, it confirms the presence of one or more active ingredients, indicating that a combination of several factors can lead to abnormal mortality and the depopulation of hives.
    The data on bee mortality from 2015 to 2024 suggests a possible improper use of plant protection products, as the bees themselves or beekeeping matrices consistently reveal the presence of one or more active ingredients.
    Based on the analysis of available data for the ten-year period examined (Table 2), the active substances most toxic to bees and most frequently detected in samples were as follows:
    • In 2024, as in previous survey years, pyrethroids were among the most common active substances widely used in agriculture and for pest control against mosquitoes and other nuisance insects. Specifically, etofenprox, cypermethrin, and permethrin were detected multiple times on bee bodies. On average, this chemical family is highly toxic to pollinators, including honey bees, affecting them at very low concentrations with both acute and long-term effects.
    Piperonyl-Butoxide has shown a consistent presence over the years. It is widely used as a synergist in many plant protection products, which explains its frequent detection on the bodies of the bees themselves.
    • Among the systemic insecticidal active substances found in 2024 were Sulfoxaflor and Chlorfenviphos, detected on bee bodies in numerous samples, as well as the acaricides Amitraz and Fluvalinate; the latter is often used by beekeepers themselves to control the bee parasite Varroa destructor.
    • Among the neonicotinoid insecticides that are particularly harmful to all pollinating insects, thiamethoxam and clothianidin were detected in 2024; in previous years, records showed the presence of the extremely toxic imidacloprid and the less toxic acetamiprid.
    Tetraconazole, Penconazole, and Trifloxystrobin: These are first-generation systemic fungicides often used preventively in vineyards and horticultural crops. In 2024, they were found on the bodies of bees in 6, 5, and 4 poisoning cases, respectively.

    Analyzing regional data on bee mortality associated with plant protection product (PPP) residues in beekeeping matrices, it is noted that in 2024—following the trend of previous years—the Autonomous Province of Bolzano, Veneto, and Emilia-Romagna recorded the highest number of positive findings, with 7, 6, and 6 cases respectively. Other regions, including Basilicata, Calabria, Campania, Piedmont, and Friuli-Venezia Giulia, recorded only one case each, with the exception of Puglia, which recorded 2 cases.
    An uneven distribution of bee mortality cases across the national territory is confirmed for 2024, occurring simultaneously with the identification of positive samples containing active substances that are toxic or highly toxic to bees. While certain areas show notable pesticide use linked to confirmed mortality, other regions with similarly high usage do not report the expected volume of cases; this discrepancy may be attributed to the varying diligence of the regulatory and control bodies responsible for oversight.
    Beginning in March 2025, pursuant to the Decree of 27 January 2025 (Official Journal, General Series No. 63, 17 March 2025), which introduced improvements and simplifications to the Decree of 7 March 2023, registration is only mandatory for mortality events exceeding 50% of the apiary's size. This registration obligation must be fulfilled within 7 days of the occurrence. Consequently, beekeepers are no longer required to report "minor" bee losses, a policy change designed to reduce administrative workloads and costs, allowing for a concentrated focus on the most significant die-off events


    Data
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    Figure 1: Bee mortality cases associated with the presence of active substances, by month.

    Data source

    ISPRA processing of II.ZZ.SS data

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    Headline

    Figure 2: Cases of bee mortality associated with the presence of active substances, by region

    Data source

    ISPRA processing of II.ZZ.SS data

    Headline

    Table 1: Cases of bee mortality associated with the presence of active substances, by region

    Data source

    ISPRA processing of II.ZZ.SS data

    Headline

    Table 2: Active substances detected in samples of dead bees

    Data source

    ISPRA processing of II.ZZ.SS data

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