Environmental Pollution

Volume 385, 15 November 2025, 127132
Environmental Pollution

Weak recovery of insectivorous bird populations after ban of neonicotinoids in France, hinting at lasting impacts☆

https://doi.org/10.1016/j.envpol.2025.127132Get rights and content

Highlights

  • •
    Imidacloprid is expected to play a role in the decline of bird populations.
  • •
    Recent ban on neonicotinoids in Europe may have allowed populations to recover.
  • •
    This relationship was investigated in France for 57 species over 1900 plots.
  • •
    Imidacloprid reduced bird population between 12.7 and 9% before and after the ban.
  • •
    Pesticide ban does not ensure immediate biodiversity recovery after ban.

Abstract

Neonicotinoids are expected to play a significant role in the decline of bird populations through their adverse effects on food resources (primarily insects) and their lethal and sub-lethal toxicity. Previous studies in the US and the Netherlands have shown links between neonicotinoid use and bird abundance, but the potential for population recovery after ban has not been investigated. Here, we investigated this relationship in France over the 2013–2022 period, focusing on 57 bird species from insectivorous, granivorous and generalist guilds, surveyed across a large number of plots (n = 1983). We specifically examined imidacloprid, the most widely sold neonicotinoid in France before its ban in 2018, which is still found in surface waters and soils. Additionally, we accounted for potential effects of other pesticides by calculating the Total Applied Toxicity (TAT) for different species groups, as well as landscape and climate factors. We found that population abundance of insectivorous birds was negatively associated with imidacloprid use. We also found that the difference in insectivorous bird abundance between sites with high versus no imidacloprid use was slightly higher before the ban (12.7 % more birds in sites with no imidacloprid) than after (9 %), suggesting only weak recovery of their populations. In contrast, granivorous and generalist species showed neutral or non-linear associations with other pesticide use and no response to imidacloprid. Our study confirms the detrimental impact of imidacloprid on insectivorous birds and highlights that pesticide bans alone do not ensure immediate biodiversity recovery. This calls for additional conservation actions in landscapes contaminated with neonicotinoids to restore insect and bird populations.

Introduction

Recent studies pointed out alarming declines in bird abundance across different regions of the world (Rigal et al., 2023; Rosenberg et al., 2019). Pesticides have been identified numerous times as one of the potential causes of these declines (Eng et al., 2019; Hallmann et al., 2014; Li et al., 2020; Moreau et al., 2022; Rigal et al., 2023; Stanton et al., 2018), along with changes in land use (Butler et al., 2010; Wade et al., 2013) or climate (Devictor et al., 2012; Stephens et al., 2016).
Pesticides are known to affect birds through different pathways. Direct contamination, with lethal or sublethal effects (Moreau et al., 2022), affects demographic parameters as well as bird behavior, such as predator avoidance or migration timing (Eng et al., 2019; Moreau et al., 2022), with negative consequences on individual fitness and population dynamics. Pesticides also impact birds indirectly by decreasing the amount and diversity of food sources (Hallmann et al., 2014) namely insects for most bird species, but also seeds. Major losses have been documented both in insects (Hallmann et al., 2017; Van Klink et al., 2023) and seed plants (Chamorro et al., 2016; Fried et al., 2009) and some of them were linked to high pesticides use (Brittain et al., 2010).
Among pesticides, neonicotinoid insecticides are particularly suspected of contributing to bird declines (Hallmann et al., 2014; Li et al., 2020; Pisa et al., 2017). Until recently, neonicotinoids were the most widely sold insecticides in the world (Simon-Delso et al., 2015). Imidacloprid, in particular, has widely contaminated the environment worldwide and is commonly found in both aquatic and terrestrial ecosystems (Pelosi et al., 2021; Stehle et al., 2023; Van Dijk et al., 2013), as well as in birds (Anderson et al., 2023; Fuentes et al., 2023). Neonicotinoids are thought to lower bird populations indirectly, due to their high toxicity for insects and the resulting declines in insect populations (Forister et al., 2016; Pisa et al., 2017). However, birds can also feed on neonicotinoid-coated seeds in sufficient amounts to experience sub-lethal and lethal effects, especially for small birds (Poliserpi et al., 2021). While neonicotinoids are expected to be a strong driver of bird decline, studies linking bird decline to neonicotinoid use remain scarce (but see Hallmann et al., 2014; Li et al., 2020).
In France, imidacloprid was the primary neonicotinoid used, as well as the most frequently detected in surface waters (Mamy et al., 2023; Perrot et al., 2024) and arable soils (Froger et al., 2023; Pelosi et al., 2021). It was also the main insecticide found in earthworms in France (Pelosi et al., 2021), and was commonly detected in rodents (Fritsch et al., 2022) or honeybees (Daniele et al., 2018). Despite the ban of neonicotinoid for flowering crops in 2013 and for all crops in 2018 (https://eur-ex.europa.eu/eli/reg_impl/2018/783/oj), annual exemptions were granted in France for sugar beet in 2021 and 2022. Imidacloprid continues to be detected in the environment (Froger et al., 2023; Perrot et al., 2024) and others neonicotinoids have been found in birds (Fuentes et al., 2023, 2024), suggesting the persistence of these active substances in the environment and their potential adverse effects on birds.
In this study, we focused on the effects of imidacloprid and its 2018 ban on bird abundance in France. For this purpose, we combined publicly available data on pesticide sales, land use, and climate metrics in France, with common bird monitoring data at the national scale. We first compared the effects of imidacloprid with those of other pesticides, estimated by calculating the Total Applied Toxicity (hereafter TAT; Bub et al., 2023; Schulz et al., 2021) over the 2013–2022 period. The TAT is calculated from toxicity towards specific taxonomic groups (e.g. birds, non-target arthropods), and may be indicative of direct effects of pesticides on birds, but also of indirect effects through bird food sources, such as insects or plants. For this reason, the investigation of the effects of imidacloprid and other pesticides on birds was carried out considering their trophic guild (insectivorous, granivorous and generalist) under the assumption that imidacloprid primarily impacts insectivorous birds, as previously found (Hallmann et al., 2014; Li et al., 2020). We also assessed whether the 2018 neonicotinoid ban was sufficient to trigger recovery in bird populations.

Access through your organization

Check access to the full text by signing in through your organization.

Access through your organization

Section snippets

Bird survey data

To estimate bird abundance, we used data from the French Breeding Bird Survey (FBBS; Jiguet et al., 2012) from 2013 to 2022. FBBS is a citizen-science monitoring program that provides standardized annual counts of breeding birds since 2001, collected by volunteer skilled ornithologists. For each participant, a 2 × 2 km monitoring plot has been provided that was randomly selected within a 10 km radius of their home locality (i.e. among 80 possible plots, Fig. S1). Within this plot, the observer

Spatial patterns in bird abundance and pesticide

Both bird abundances and pesticide use exhibited strong spatial patterns (Fig. 1). The spatial distribution of common birds differed across diets, with higher abundance of insectivorous birds in central, north-western and eastern France, while granivorous birds were more abundant in southern France, and generalists were more abundant in northern France (Fig. 1A–C).
The mean annual amount of imidacloprid sold around a monitoring plot was 36.6 kg around the zip codes surrounding the monitoring

Discussion

Our study shows that imidacloprid is a major covariate of the abundance of birds, in addition to other pesticides that are also negatively related to bird populations, and that these effects are not uniform across species. The relationship varied across bird diets: while the abundance of insectivorous birds was consistently lower under increasing pesticide use, in particular imidacloprid, the abundance of granivorous birds exhibited non-linear response, being highest at intermediate pesticide

CRediT authorship contribution statement

Thomas Perrot: Writing – original draft, Visualization, Validation, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Karine Princé: Writing – original draft, Validation, Investigation, Formal analysis. Emmanuelle Porcher: Writing – original draft, Validation, Investigation, Formal analysis. Jakob Wolfram: Writing – original draft, Validation, Investigation, Formal analysis. Ralf Schulz: Writing – original draft, Supervision, Investigation, Formal analysis. Colin

Funding sources

T.P. was supported by the FRB. The FRB is funded by the French Ministry of Research and its founding members BRGM, CIRAD, CNRS, IFREMER, INERIS, INRAE, IRD, LVMH, MNHN, OFB, and the University of Montpellier to implement its research programs. The FRB received additional funding from the LPO to implement the research program on the impacts of neonicotinoids on biodiversity and ecosystem services. The FRB guarantees that public or private funders will not intervene in the conduct or results of

Declaration of competing interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Thomas Perrot reports financial support was provided by French Bird Protection Society. Karine Prince reports financial support was provided by National Agency for Food Environmental and Occupational Health and Safety. The other authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence

References (59)

  • C. Pelosi et al.

    Residues of currently used pesticides in soils and earthworms: a silent threat?

    Agric. Ecosyst. Environ.

    (2021)
  • T. Perrot et al.

    Temporal and spatial trends of imidacloprid-related hazards in France

    Sci. Total Environ.

    (2024)
  • M.B. Poliserpi et al.

    Imidacloprid seed coating poses a risk of acute toxicity to small farmland birds: a weight-of-evidence analysis using data from the grayish baywing Agelaioides badius

    Sci. Total Environ.

    (2021)
  • D. Russo et al.

    To improve or not to improve? The dilemma of “bat-friendly” farmland potentially becoming an ecological trap

    Agric. Ecosyst. Environ.

    (2024)
  • H. Siviter et al.

    Wild bees are exposed to low levels of pesticides in urban grasslands and community gardens

    Sci. Total Environ.

    (2023)
  • R.L. Stanton et al.

    Analysis of trends and agricultural drivers of farmland bird declines in North America: a review

    Agric. Ecosyst. Environ.

    (2018)
  • S. Stehle et al.

    Neonicotinoid insecticides in global agricultural surface waters – exposure, risks and regulatory challenges

    Sci. Total Environ.

    (2023)
  • C. Vallé et al.

    Farmland biodiversity benefits from small woody features

    Biol. Conserv.

    (2023)
  • S. Bub et al.

    Trends of total applied pesticide toxicity in German agriculture

    Environ. Sci. Technol.

    (2023)
  • K.P. Burnham et al.

    Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach

    (2002)
  • G. Daniele et al.

    Exposure assessment of honeybees through study of hive matrices: analysis of selected pesticide residues in honeybees, beebread, and beeswax from French beehives by LC-MS/MS

    Environ. Sci. Pollut. Control Ser.

    (2018)
  • V. Devictor et al.

    Differences in the climatic debts of birds and butterflies at a continental scale

    Nat. Clim. Change

    (2012)
  • J.L. Dorne et al.

    Editorial: openfoodtox: efsa's open source toxicological database on chemical hazards in food and feed

    EFSA J.

    (2017)
  • S. Ducatez et al.

    Ecological generalism and behavioural innovation in birds: technical intelligence or the simple incorporation of new foods?

    J. Anim. Ecol.

    (2015)
  • P.K. Dunn et al.

    Generalized Linear models with examples in R

  • L. Dvořáková et al.

    Habitat characteristics supporting bird Species richness in mid-field woodlots

    Front. Environ. Sci.

    (2022)
  • M.L. Eng et al.

    A neonicotinoid insecticide reduces fueling and delays migration in songbirds

    Science

    (2019)
  • M.L. Forister et al.

    Increasing neonicotinoid use and the declining butterfly fauna of lowland California

    Biol. Lett.

    (2016)
  • C. Fritsch et al.

    Pervasive exposure of wild small mammals to legacy and currently used pesticide mixtures in arable landscapes

    Sci. Rep.

    (2022)

    • Cited by (0)

    ☆
    This paper has been recommended for acceptance by Philip N. Smith.
    View full text
    © 2025 Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.