The ubiquity of neonicotinoid contamination: Residues in seabirds with different trophic habits

doi:10.1016/j.envres.2021.112637

Environmental Research

Volume 206, 15 April 2022, 112637

https://doi.org/10.1016/j.envres.2021.112637 Get rights and content

Highlights

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Neonicotinoid's occurrence in bird feathers confirms their widespread diffusion.
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Neonicotinoids were detected in mixotrophic and piscivorous birds.
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Neonicotinoids released in the environment may pose a risk for aquatic birds.
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Imidacloprid, clothianidin and thiametoxam are the pesticides most often detected.

Abstract

Neonicotinoids are one of the most diffusely used classes of pesticides whose level of danger toward non-target invertebrate and vertebrate species has raised increasing concern in the last decades. Among vertebrates, birds are particularly susceptible to unintentional neonicotinoid poisoning since they can be exposed through different pathways, including ingestion of dressed seeds, sucking of contaminated pollen, ingestion of sprayed insects, predation on contaminated aquatic and terrestrial preys. In the present study, we investigated the possible exposure of seabirds by measuring the residues of five neonicotinoids (acetamiprid, clothianidin, imidacloprid, thiacloprid and thiamethoxam) in samples of pooled feathers collected from fledglings of the strictly piscivorous Sandwich tern (Thalasseus sandvicensis) and the mixotrophic species Mediterranean gull (Ichthyaetus melanocephalus). At least one neonicotinoid was quantified in all the Mediterranean gull samples (n = 11) and 89% of the analysed Sandwich tern samples (n = 36). The active principles with the highest quantification rates were imidacloprid (100% in Mediterranean gulls and 58% in Sandwich terns) and clothianidin (100% in Mediterranean gulls and 61% in Sandwich terns), while thiacloprid was the less frequently detected pesticide (<20% of samples in both species). Mean concentrations ± standard error for imidacloprid, clothianidin and thiamethoxam were 8.8 ± 1.4, 4.5 ± 0.19 and 0.16 ± 0.02 ng g⁻¹ for the Mediterranean gull, and 5.8 ± 0.55, 0.60 ± 0.08 and 0.36 ± 0.03 ng g⁻¹for the Sandwich tern, respectively. Our data evidenced the exposure of seabirds to neonicotinoids and the further need to investigate the extent of neonicotinoid contamination in non-agricultural ecosystems.

Introduction

Neonicotinoids are neurotoxic pesticides binding to the nicotinic acetylcholine receptors and causing membrane depolarisation, ion channel activation, and propagation of the action potential (Tomizawa and Casida, 2005). Their high effectiveness against pest insects, combined with high water solubility and low mammalian toxicity, favoured their widespread use in agriculture and made them the most popular class of pesticide in the past decades (Jeschke et al., 2011; Simon-Delso et al., 2015). Nonetheless, several studies evidenced that the ingestion of neonicotinoid-coated seeds by granivorous birds may cause mortality and detrimental effects on body condition, behaviour, orientation, the immune system, and reproduction. (Eng et al., 2017; Lopez-Antia et al., 2012; Mineau and Palmer, 2013). Furthermore, the consumption of coated seeds by granivorous birds has been proven to be just one of the multiple pathways of exposure to neonicotinoids for avian species in farmlands, which also include consuming contaminated nectar (Graves et al., 2019), wild bees (Byholm et al., 2018), or other sprayed insects (Humann-Guilleminot et al., 2019b, 2021). Recent studies also demonstrated that the extent of neonicotinoid contamination was underestimated over the past decades and that other bird species not suspected to be in direct contact with pesticides, such as birds of prey, accumulated neonicotinoid residues in their tissues, plasma, and feathers (Badry et al., 2021; Humann-Guilleminot et al., 2021; Taliansky-Chamudis et al., 2017). Seabirds have not previously been considered a possible target of neonicotinoid contamination, although runoff from agricultural land into waterways is a known fate for these chemicals (Anderson et al., 2015; Goulson, 2013, 2014), and their occurrence at quantifiable concentrations has been reported in several estuaries and coastal areas worldwide (Gallen et al., 2014; Hano et al., 2019; Li et al., 2019; Miller et al., 2021). Once in estuaries and coastal areas, neonicotinoids may be taken up by aquatic insects, crustaceans, and other invertebrates that serve as an essential food supply for fishes and birds (Goulson, 2014).

In this study the concentrations of five active principles in feathers collected from two seabird species breeding in Venice's Lagoon, Italy, were measured in order to verify whether also seabirds could be exposed to neonicotinoids. The focus was on feathers collected from chicks of Sandwich terns (Thalasseus sandvicensis) and Mediterranean gulls (Ichthyaetus melanocephalus). Feathers were chosen as the target tissue because their collection is a non-destructive, harmless procedure allowing the study of a chemical's bioaccumulation without affecting the welfare or survival of birds (Picone et al., 2019, 2021). Both species are listed in the Directive 2009/147/EC and are included in the IUCN Italian Red List of endangered species as vulnerable species due to their small distribution (Sandwich tern) and least concern species (Mediterranean gull) (Rondinini et al., 2013). To the best of our knowledge, the present study is the first research to address the possible occurrence of neonicotinoid residues in seabirds.

Section snippets

Study area

Located in North-East Italy, the Lagoon of Venice is one of the largest coastal-transitional ecosystems of the Mediterranean sea with its 540 km² surface (Tagliapietra et al., 2009). The drainage basin of the lagoon has a surface area of 2038 km² (Soccio et al., 2018); the inflow from the catchment area averages 3.7 million m³ of water and includes riverine and subsoil inputs (Bernstein and Montobbio, 2011). In particular, the lagoon receives water through a network of approximately 30 streams

Results and discussion

Overall, neonicotinoids were quantified at concentrations above MQL in 43 out of 47 analysed samples (91%). The neonicotinoids with the highest prevalence were CLO (70%), IMI (68%), and TMX (49%), all active principles whose outdoor use in agriculture was severely restricted by the European Union (EU) in 2013 (Regulation 485/2013/EU) and then finally banned in 2018 (Regulations 783/2018/EU, 784/2018/EU and 785/2018/EU). Conversely, the lowest prevalence was observed for ACE (32%) and THI (15%),

Conclusions

This research evidenced that seabirds at the top of the aquatic food webs in estuaries and coastal areas are exposed to neonicotinoids. In particular, residues of neonicotinoids were reported in omnivorous (MG) and piscivorous (ST) birds, confirming that seabirds with different trophic habits may be affected by the ubiquitous presence of neonicotinoids. Despite the ban on the outdoor uses of IMI, CLO, and TMX, residues of these pesticides can still be measured in the feathers of young ST

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Author contribution

Gabriele Giuseppe Distefano: Investigation. Resources. Formal analysis. Data curation. Writing-Original draft preparation. Roberta Zangrando: Investigation. Resources. Formal analysis. Data curation. Writing-Original draft preparation. Marco Basso: Investigation. Resources. Lucio Panzarin: Investigation. Resources. Andrea Gambaro: Supervision. Writing - Review & Editing. Annamaria Volpi Ghirardini: Supervision. Writing - Review & Editing. Marco Picone: Conceptualization, Methodology.

Funding sources

This work was supported by the Ca'Foscari University of Venice, Italy, through the 2018 SPIN Initiative (Supporting Principal INvestigators), Measure 2, 1st call of proposals (Rectoral Decree 1065/2018 prot. 67,416/2018).

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.

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Neonicotinoid insecticides in waters of the northern Jiangsu segment of the Beijing-Hangzhou Grand Canal: Environmental and health implications
2024, Science of the Total Environment
Neonicotinoid (NEO) insecticides have been frequently detected in natural aquatic environments. Nevertheless, the distribution of NEOs in artificial environments is not clear. The Beijing-Hangzhou Grand Canal is the longest canal in the world. The northern Jiangsu segment of the Grand Canal was selected to study the spatiotemporal variation and source of eight NEOs in the canal water and assess their ecological and health risks. The total NEO concentration in the canal water was 12–289 ng L⁻¹ in the dry season and 18–373 ng L⁻¹ in the wet season, which were within the concentration range in other 11 natural rivers worldwide. The average total NEO concentrations were not statistically different between the seasons; only the concentrations of imidaclothiz, thiacloprid (THI), acetamiprid, and dinotefuran were different. At city scale, the total NEO concentration in the dry season showed a decreasing trend along the water flow from Xuzhou City to Yangzhou City. The total NEO concentrations were found to be positively correlated with the sown area of farm crops and the rural labour force, indicating the agricultural influence on the spatial distribution of NEO concentrations. In the wet season, relatively high NEO concentrations were distributed in downstream sites under the influence of artificial regulation. The primary contributor to the NEO inputs into the canal was the nonpoint source in the dry and wet seasons, with a relative contribution of 68 %. THI, imidacloprid, clothianidin and thiamethoxan would produce chronic ecological risks in both seasons. Further consideration needs to be given to the above four NEOs and NEO mixtures. The human health risks that NEOs posed by drinking water were assessed based on the chronic daily intake (CDI). The maximum CDI for adults and children was lower than the reference doses. This suggested public health would not be at risk from canal water consumption.
Neonicotinoids in tea leaves and infusions from China: Implications for human exposure
2023, Science of the Total Environment
The ingestion of contaminated tea involves the risk of human exposure to residues of neonicotinoids (NEOs). Nevertheless, there is little empirical research about this topic; to bridge the current knowledge gap, we collected 220 samples of various tea products from four geographical areas in China, including unfermented green tea, semi-fermented white tea and oolong tea, completely fermented black tea, and post-fermented dark tea. A total of six NEOs were detected from the tea leaves and infusions, namely, dinotefuran (DIN), thiamethoxam (THM), clothianidin (CLO), imidacloprid (IMI), acetamiprid (ACE), and thiacloprid (THI). The detection frequencies (DFs) and concentrations of all target NEOs were relatively high across the investigated tea samples, and the DIN, IMI and ACE residues measured in some samples exceeded the maximum residue level (MRL) standards for the European Union. Samples representing the Jiangnan area exhibited greater levels of total target NEOs (∑₆NEOs) than samples representing the Jiangbei area (p < 0.001). Moreover, dark tea samples were found to have far higher levels of NEO residues than green (p < 0.001), white (p < 0.05), or oolong (p < 0.001) samples. The health risks associated with exposure to NEO residues via tea were small for both children and adults in terms of acute, chronic, and cumulative dietary exposure risk assessments. The transfer rates (TRs) of NEOs observed in white, black, and dark tea infusions gradually decreased after the third brewing time. As such, it is recommended to only consume tea that has been brewed at least three times. The presented results not only describe the extent of NEO contamination in Chinese tea leaves and infusions, but also provide tea drinking guidelines for consumers.
Neonicotinoids and pharmaceuticals in hair of the Red fox (Vulpes vulpes) from the Cavallino-Treporti peninsula, Italy
2023, Environmental Research
Neonicotinoids (NEOs) and active pharmaceuticals ingredients (API) are contaminants widely diffused worldwide, causing increasing concern for potential adverse effects on wildlife. However, research on these contaminants have focused on target and non-target invertebrates, while information on potential effects in terrestrial mammals is lacking. We performed preliminary non-invasive monitoring of NEOs and API in a suburban and agricultural area using hair of the Red fox. The Red fox is a widely diffused mesopredator in Europe, and its plasticity in feeding habits makes it an excellent indicator for assessing exposure to environmental contamination. We observed the presence of NEOs in many Red fox hair samples (n = 11), including imidacloprid (IMI), acetamiprid (ACE), and clothianidin (CLO). The highest quantified concentrations were 6.4 ng g⁻¹ dry weight (dw), 6.7 ng g⁻¹ dw, and 0.9 ng g⁻¹ dw for IMI, ACE, and CLO, respectively. The targeted APIs included non-steroidal anti-inflammatory drugs (NSAIDs) and antidepressants. APIs were less frequently detected than NEOs, and the compounds with the highest prevalence were the NSAID ketoprofen (36%), the antidepressant sertraline (36%), and its active metabolite norsertraline (27%). The presence of human pharmaceuticals such as the NSAID ibuprofen and the antidepressants sertraline, fluoxetine, and their active metabolites norsertraline and norfluoxetine suggest environmental contamination due to untreated and partially treated wastewater discharged in surface waters and soils of the study area. The detection and quantification of ketoprofen and flunixin also suggest the possible use of contaminated manure on farmland. Findings indicate that hair may be used for monitoring environmental exposure to NEOs and provide evidence that hair is a good marker of exposure for antidepressants and certain NSAIDs, including ibuprofen, ketoprofen, and flunixin.
Experimental evidence for clothianidin deposition in feathers of house sparrows after ingestion of sublethal doses treated seeds.
2023, Chemosphere
Citation Excerpt :
Our data does not allow us to address such relationship in more detail and further experiments that would expose groups of birds to varying amounts of neonicotinoids in their food, would monitor neonicotinoid concentrations in the blood at several time points and would concomitantly monitor the deposition of these compounds into the growing feathers are needed to examine whether increasing exposure to neonicotinoids translates into increasing concentrations in bird plasma and feathers, whether such relationship is linear or not (e.g. saturation effect) and whether such relationship depends on, e.g. sex, age, position in the social hierarchy. To conclude, recent studies have reported the presence, at varying concentrations, of neonicotinoids in the feathers of some bird species (e.g. Humann-Guilleminot et al., 2021; Distefano et al., 2022b). It remains unclear, however, whether the reported concentrations resulted from the ingestion of neonicotinoids and subsequent deposition in the feathers or whether it reflected an external deposition on the surface of the feathers.
Bird feathers are commonly used to assess environmental contamination by chemical pollutants. However, although neonicotinoid insecticides are widely applied worldwide, feathers have rarely been used to survey the contamination by neonicotinoids in birds. To investigate whether clothianidin, one compound of the neonicotinoid class, is deposited into birds’ feathers, we conducted an experiment with 56 wild male and female house sparrows dispatched in 7 aviaries. During this experiment, house sparrows were fed with certified organic seeds treated with clothianidin at an estimated concentration of 0.25 μg/g BW per day and per individual. We collected blood samples and plucked four tail feathers at the onset of the experiment to confirm that no birds were previously exposed to clothianidin. 35 days later, we collected blood samples and the newly grown feathers. Before exposure, a small number of birds showed very low clothianidin concentrations in plasma and feathers. After exposure, the plasma and the newly grown feathers of all birds contained clothianidin. Clothianidin concentrations in feathers were similar in both sexes, but the plasma of males contained clothianidin at higher concentrations than that of females. Our results confirm that ingested clothianidin transits in the plasma and is deposited in feathers during their growth. They also suggest substantial individual variation in the amounts of clothianidin transiting in the plasma and being deposited in feathers that may reflect variation in metabolism and/or access to food in relation to sex, social hierarchy and group dynamics. Whether increasing levels of exposure translate linearly or non-linearly (e.g. saturation process) into increasing clothianidin concentrations in bird plasma and feathers remains to be investigated. To conclude, these results confirm the relevance of using feathers to biomonitor the presence of neonicotinoids, but the relationship between the level of exposure and the concentrations found in feathers remains to be established.
High population prevalence of neonicotinoids in sharp-tailed grouse and greater prairie-chickens across an agricultural gradient during spring and fall
2023, Science of the Total Environment
Neonicotinoids have been detected in many species of wild birds; however, few studies have quantified population-level exposure. We examined population-level exposure to 7 neonicotinoids in 2 species that use agricultural areas, sharp-tailed grouse (Tympanuchus phasianellus) and greater prairie-chickens (T. cupido). We sampled fecal pellets at leks in spring and collected livers from hunter-harvested birds in fall along an agricultural gradient throughout their respective ranges in Minnesota, USA. Most sharp-tailed grouse (93 %) and prairie-chicken (80 %) fecal pellets and livers (90 % and 76 %, respectively) had detectable concentrations of ≥1 neonicotinoid, with imidacloprid (IMI) and clothianidin (CLO) most commonly detected. Spring detections of IMI in both species increased with the proportion of a 2-km buffer in cultivation surrounding sampling locations and varied by year. A similar relationship with cultivation was not supported for CLO, which may reflect differences in the availability of seed types treated with IMI and CLO on the soil surface after planting. However, we also detected IMI and CLO from birds sampled in areas of low cultivation. Sharp-tailed grouse and prairie-chickens may select crop fields preferentially to forage, and thus have a higher risk of exposure than would be expected based only on the amount of cultivation. Year was important in models of IMI and CLO in both species and seasons, which likely reflects differences in planting and in the availability of natural foods among years. In contrast, the proportion of surrounding area in cultivation was not supported in models of fall neonicotinoid detections. Fewer crops are planted in the fall in Minnesota and grouse may be exposed through routes other than treated seeds. High detections, even in areas with little cultivation and during seasons with little planting, likely reflect prairie grouse selection of cultivated fields for food, but may also indicate that exposure risk extends beyond sites of application.
Oxidation of solid thin films of neonicotinoid pesticides by gas phase hydroxyl radicals
2022, Environmental Science: Atmospheres
Neonicotinoids (NNs) are commonly found throughout the environment on surfaces such as seeds, soil, vegetation, and blowing dust particles. However, there is a paucity of data on the kinetics and oxidation products formed on contact with the atmosphere which limits understanding of their potentially far-reaching impacts. In this study, in situ attenuated total reflectance (ATR) FTIR spectroscopy was used to investigate the OH oxidation of thin films of three solid NNs, imidacloprid (IMD), dinotefuran (DNF) and clothianidin (CLD) at 295 ± 3 K. The experimentally measured reaction probabilities based on initial rates of NN loss are (1.6 ± 0.8) × 10⁻² for IMD, (1.5 ± 0.6) × 10⁻² for DNF and (0.9 ± 0.2) × 10⁻² for CLD (±1σ), suggesting initial NN lifetimes with respect to OH of 10–17 days. The kinetics were interpreted using a multiphase kinetics model, KM-SUB, which showed that the OH uptake and reaction occurred primarily in the surface layer. Products identified by mass spectrometry included carbonyl-, alcohol- and olefin-containing species formed via hydrogen abstraction from aliphatic C–H groups. Additionally, carbonyl-containing desnitro and urea derivative products were observed from secondary reactions of the initially formed photodegradation products. Reaction with OH will contribute to NN loss both during the day as well as at night when there are non-photolytic sources of this radical. Thus, OH reactions with both the parent neonicotinoid and its photodegradation products should be considered in assessing their environmental impacts.

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¹: Gabriele Giuseppe Distefano and Roberta Zangrando worked together and contributed equally to the paper, thus they are proposed for shared co-first authorship.

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The ubiquity of neonicotinoid contamination: Residues in seabirds with different trophic habits

Highlights

Abstract

Introduction

Section snippets

Study area

Results and discussion

Conclusions

Compliance with ethical standards

Author contribution

Funding sources

Declaration of competing interest

Sci. Total Environ.

Environ. Res.

Sci. Total Environ.

Environ. Res.

J. Sea Res.

Environ. Pollut.

Sci. Total Environ.

Sci. Total Environ.

Environ. Res.

Sci. Total Environ.

Chemosphere

TrAC Trends Anal. Chem. (Reference Ed.)

Environ. Pollut.

Amandava amandava. Reprod. Toxicol.

Chemosphere

Ecotoxicol. Environ. Saf.

Sci. Total Environ.

Environ. Int.

Environ. Int.

La gestione dei sedimenti in laguna di Venezia. Sintesi dei principali risultati acquisiti da studi e indagini di base

Quad. Trimest. del Consorzio Venezia Nuova

Trace Quantitative Analysis by Mass Spectrometry, Trace Quantitative Analysis by Mass Spectrometry

Evaluation of censored data methods to allow statistical comparisons among very small samples with below detection limit observations

Environ. Sci. Technol.

Floating rafts as breeding habitats for the Common tern, Sterna hirundo. Colonization patterns, abundance and reproductive success in Venice Lagoon

Riv. Ital. di Ornitol. Ornithol.

Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic: 3. Waders to Gulls

A neonicotinoid insecticide reduces fueling and delays migration in songbirds

Science

Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird

Sci. Rep.

Analytical Quality Control and Method Validation Procedures for Pesticide Residues Analysis in Food and Feed