# Evaluation of the Health Status of Apis mellifera in Relation to the Use of Plant Protection Products in Viticulture Through a Multi-Biomarker Approach

**Authors:** Tommaso Campani, Agata Di Noi, Ginevra Manieri, Ilaria Caliani, Silvia Casini

PMC · DOI: 10.3390/toxics14020176 · Toxics · 2026-02-17

## TL;DR

This study examines how viticulture practices, including plant protection products, affect honey bee health using multiple biomarkers.

## Contribution

The study introduces a multi-biomarker approach to assess the impact of viticulture practices on honey bee health.

## Key findings

- Neurotoxic effects were observed in transitioning farms with decreased AChE activity during PPP treatments.
- Bee health deteriorated most at transitioning farms post-treatment, while biodynamic sites remained stable.
- Immune markers showed inefficient activation, potentially weakening bee immune competence.

## Abstract

The global pollinator decline is linked to intensive farming and the high use of plant protection products (PPPs), necessitating risk assessment and mitigation. This study investigates the potential negative impacts of agricultural practices on pollinator health, specifically focusing on the effects of PPPs used in viticulture on the honey bee, Apis mellifera, despite grapevines’ lack of reliance on bee pollination. The beehives sampled were from two farms with vineyards under different management regimes: one transitioning from conventional to organic practices and an organic–biodynamic site with pollinator mitigation measures. Sampling was conducted during three phases, pre-, during, and post-PPP application, to evaluate biomarkers of neurotoxicity (AChE), detoxification enzymes (CaE, GST), metabolic stress (ALP), and immune markers (Lys, PO, proPO). Comparison between the organic–biodynamic farm and the transitioning one revealed a pattern suggesting significant neurotoxic effects in the transitioning farm characterised by a trend of decreased AChE activity during treatments and the subsequent induction of GST post exposure. Crucially, both PO and proPO were induced post treatment, but with a lower PO/proPO ratio compared to previous seasons, suggesting inefficient proPO activation and potentially weakened immune competence that could favour pathogen proliferation. Bee health appeared to deteriorate most at the transitioning farm post treatment, while the biodynamic site remained relatively stable; these differences are likely associated with legacy residues and drift, exacerbated by overwintering stress and summer heat. Given the specific environmental and management characteristics of these two farms, the results provide an indicative comparison of how different agronomic approaches may influence bee health. Moreover, these results support the multi-biomarker approach for detecting potential PPP impacts, suggesting that organic transitions and mitigation strategies could play a role in pollinator conservation.

## Linked entities

- **Proteins:** ACHE (acetylcholinesterase (Yt blood group)), GJA8 (gap junction protein alpha 8), SLCO6A1 (solute carrier organic anion transporter family member 6A1), ALPP (alkaline phosphatase, placental), lys (endolysin), PRB4 (proline rich protein BstNI subfamily 4), PPO1 (Prophenoloxidase 1)
- **Chemicals:** PPP (PubChem CID 72435)
- **Species:** Apis mellifera (taxon 7460)

## Full-text entities

- **Genes:** AChE-2 (acetylcholinesterase 2) [NCBI Gene 406104] {aka ACE2, Ache, GB14873, GB41856}, Carboxylesterase [NCBI Gene 726134], Prophenoloxidase [NCBI Gene 406155], Lysozyme [NCBI Gene 409663], Glutathione S-Transferase [NCBI Gene 552283], Acetylcholinesterase [NCBI Gene 410270]
- **Diseases:** bacterial infection (MESH:D001424), Deformed Wing Virus (MESH:D008579), CaE (MESH:C566173), infection (MESH:D007239), injury to (MESH:D014947), Neurotoxic damage (MESH:D020258)
- **Chemicals:** melanin (MESH:D008543), LPS (MESH:D008070), GSH (MESH:D005978), ice (MESH:D007053), 1-Chloro-2,4-dinitrobenzene (MESH:D004137), coumaphos oxon (MESH:C007130), p-NPB (MESH:C033592), sulphur dioxide (MESH:D013458), cadmium (MESH:D002104), Lys (MESH:D008239), EMS (MESH:D005020), p-nitrophenyl acetate (MESH:C008642), Coumaphos (MESH:D003372), L-DOPA (MESH:D007980), OP/carbamates (-), organophosphate (MESH:D010755), carbamate (MESH:D002219), glyphosate (MESH:C010974), p-nitrophenol (MESH:C024836), thiamethoxam (MESH:D000077922), ALP (MESH:C001864), copper oxychloride (MESH:C007120), acetamiprid (MESH:C464485), tebuconazole (MESH:C087114), PO (MESH:D011059), CuCl2 (MESH:C029892), PbCl2 (MESH:C029891), CdCl2 (MESH:D019256), aldicarb sulfoxide (MESH:C030579), Cu (MESH:D003300), phosphate (MESH:D010710), metal (MESH:D008670), copper hydroxide (MESH:C508959), fipronil (MESH:C082360), acetylthiocholine (MESH:D000122), chlorpyrifos oxon (MESH:C009618), nitrogen (MESH:D009584)
- **Species:** Micrococcus luteus (species) [taxon 1270], Apis mellifera (bee, species) [taxon 7460], Homo sapiens (human, species) [taxon 9606], Vespidae (wasps, family) [taxon 7438]
- **Cell lines:** C — Mus musculus (Mouse), Finite cell line (CVCL_S361), 23 — Cricetulus griseus (Chinese hamster), Spontaneously immortalized cell line (CVCL_K265), SUM — Homo sapiens (Human), Medulloblastoma, non-WNT/non-SHH, group 3, Cancer cell line (CVCL_VU79)

## Full text

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## Figures

9 figures with captions in the complete paper: https://tomesphere.com/paper/PMC12944965/full.md

## References

65 references — full list in the complete paper: https://tomesphere.com/paper/PMC12944965/full.md

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Source: https://tomesphere.com/paper/PMC12944965