Assessing the exposure to human and veterinary pharmaceuticals in waterbirds: The use of feathers for monitoring antidepressants and nonsteroidal anti-inflammatory drugs

https://doi.org/10.1016/j.scitotenv.2022.153473Get rights and content

Highlights

  • Pharmaceuticals released into the environment may pose a risk for aquatic birds.

  • Feather analysis can shed light on environmental exposure during feather growth.

  • Antidepressants and non-steroidal anti-inflammatory drugs were detected.

  • The most detected active ingredient in young gulls and terns is diclofenac.

  • Diclofenac was detected at levels between 3.6–56.0 ng g−1 in both species.

Abstract

Exposure to active pharmaceutical ingredients (APIs) from both human and veterinary sources is an increasing threat to wildlife welfare and conservation. Notwithstanding, tracking the exposure to pharmaceuticals in non-target and sensitive vertebrates, including birds, is seldom performed and relies almost exclusively on analysing internal organs retrieved from carcasses or from experimentally exposed and sacrificed birds. Clearly, this excludes the possibility of performing large-scale monitoring. Analysing feathers collected from healthy birds may permit this, by detecting APIs in wild birds, including protected and declining species of waterbirds, without affecting their welfare. To this end, we set up a non-destructive method for analysing the presence of non-steroidal anti-inflammatory drugs (NSAIDs), selective serotonin reuptake inhibitors (SSRIs) and noradrenaline reuptake inhibitors (SNRIs) in the feathers of fledglings of both the Mediterranean gull (Ichtyaetus melanocephalus) and the Sandwich tern (Thalasseus sandvicensis). The presence of several NSAIDs and SSRIs above the method quantification limits have confirmed that feathers might be a suitable means of evaluating the exposure of birds to APIs. Moreover, the concentrations indicated that waterbirds are exposed to NSAIDs, such as diclofenac, ibuprofen and naproxen, and SSRIs, such as citalopram, desmethylcitalopram, fluvoxamine and sertraline, possibly due to their widespread use and incomplete removal in wastewater treatment plants (WWTPs). The active ingredient diclofenac raises a the primary concern for the ecosystem and the welfare of the waterbirds, due to its high prevalence (100% and 83.3% in Mediterranean gull and Sandwich tern, respectively), its concentrations detected in feathers (11.9 ng g−1 and 6.7 ng g−1 in Mediterranean gull and Sandwich tern, respectively), and its documented toxicity toward certain birds.

Introduction

Exposure of wildlife to Active Pharmaceuticals Ingredients (APIs) and their active metabolites is becoming an increasing concern for environmental scientists (Branchet et al., 2021; Madikizela et al., 2020; Puckowski et al., 2016). APIs have been selected to be specific and potent in their therapeutic effects. As such, they may be biologically active and toxic for non-target organisms at low concentrations (Bean et al., 2017, Bean et al., 2018; Shore et al., 2014). Furthermore, they can accumulate in the tissues of both aquatic and terrestrial species (Boström et al., 2017; Du et al., 2016; Zhang et al., 2021).

Current understanding of the sources and the presence of pharmaceuticals within the environment is relatively well described (Taggart et al., 2016). However, many gaps remain in the comprehension of the behaviour and risks posed by APIs occurring in natural environments (Taggart et al., 2016). Wastewater treatment plants, effluents from hospitals, spills from pharmaceutical industries, and waste disposal are all widely accepted as primary sources of APIs (Caldwell, 2015; Gros et al., 2010; Scott et al., 2018; Zhang et al., 2021). In aquatic ecosystems, biota may be exposed to APIs discharge in surface waters and may then bioaccumulate at different trophic levels, which include plankton, invertebrates and fish (Du et al., 2016; Metcalfe et al., 2010; Xie et al., 2017). Similarly, plant and insect communities in terrestrial ecosystems may be exposed to APIs from spills and waste products deposited in the soil, favouring the transfer of pharmaceuticals to herbivorous and insectivorous organisms through the trophic web (Carter et al., 2014; Taggart et al., 2016). Another route of exposure to wildlife in terrestrial ecosystems is via the consumption of carcasses from domestic animals treated with APIs throughout their life (Oaks et al., 2004).

The presence of APIs in the environment may lead to multiple adverse effects in wildlife, both in aquatic (Corcoran et al., 2010; Shore et al., 2014) and terrestrial habitats (Oaks et al., 2004; Pain et al., 2008). Despite this, the research in this field has focused mainly on fish and a few freshwater invertebrate species (Brausch et al., 2012; Brodin et al., 2014; Corcoran et al., 2010). In particular, pharmaceuticals have been shown to potentially alter the feeding rate of fish and to affect behavioural traits such as activity, aggression, boldness, exploration and sociality (see review in Brodin et al., 2014). Conversely, very little field-based information for higher vertebrates such as birds and mammals is currently available (Taggart et al., 2016). More specifically, in marine ecosystems the fate, behaviour, and routes of exposure of APIs remain poorly understood (Bean et al., 2018; Branchet et al., 2021; Fabbri and Franzellitti, 2016).

Exposure to APIs in aquatic top predators following dermal and oral (water-piscivorous) pathways has been recently reported. These studies have highlighted both digestive and dermal exposure to diclofenac and ibuprofen in otters (Lutra lutra) (Richards et al., 2011), the presence of acetaminophen, diclofenac and diltiazem in osprey (Pandion haliaetus) plasma (Bean et al., 2018; Lazarus et al., 2015), as well as the aquatic food web transference of ibuprofen residues in the white-tailed eagle (Haliaeetus albicilla) (Badry et al., 2021).

Despite recent advances, API accumulation in aquatic birds has been studied exclusively on birds of prey (Badry et al., 2021; Bean et al., 2018; Lazarus et al., 2015), while there is no available data on other waterbirds. Antidepressants and non-steroidal anti-inflammatory drugs (NSAIDs) are among the most frequently detected drugs in marine surface waters, including estuaries, lagoons and coastal areas (Arpin-Pont et al., 2016; Bayen et al., 2013; Moreno-González et al., 2015). Antidepressants such as fluoxetine and citalopram and NSAIDs such as diclofenac, ibuprofen, nimesulide and naproxen were also frequently detected in aquatic invertebrates and fishes suggesting potential transfer to ichthyophagous and invertivorous vertebrates (Álvarez-Muñoz et al., 2015; Moreno-González et al., 2016; Świacka et al., 2022). Therefore, with the aim of extending current knowledge concerning the potential exposure of wild birds to APIs in estuarine areas, we investigated the possibility of detecting NSAIDs and the antidepressants selective serotonin reuptake inhibitors (SSRIs) and noradrenaline reuptake inhibitors (SNRIs) on wild birds using non-destructive sample collection methods.

The Sandwich tern (Thalasseus sandvicensis) and the Mediterranean gull (Ichthyaetus melanocephalus) were the two species chosen for the study as they are top predators in the aquatic food web and the adults generally hunt their prey within a range of a few kilometres from the colony (Fasola et al., 1989; Fijn et al., 2017; Perrow et al., 2011). Consequently, contaminant exposure could be ascribed almost exclusively to local uptake. Furthermore, both species are listed in Directive 2009/147/EC and are included in the IUCN Italian Red List as vulnerable (VU) species due to their small distribution (the Sandwich tern) and least concern (LC) species (the Mediterranean gull) (Rondinini et al., 2013). As such, results obtained may have major conservation implications.

We collected feathers from Sandwich tern and Mediterranean gull fledglings. Fledglings were selected as they are much easier to sample and they obtain all their nutrients and body burdens through food and the egg directly from their parents. Given the rapid growth of young birds, maternal transfer via the egg is usually a negligible part of the total biomass of fledging birds (Ackerman et al., 2011). Therefore, sampling fledgling feathers can provide local information on contaminant exposure for these species (Burger and Gochfeld, 1997; Picone et al., 2021).

Feathers were used to measure exposure to APIs because feather collection is a non-destructive procedure that allows biomonitoring without affecting bird welfare or survival (Jaspers et al., 2011; Picone et al., 2019, Picone et al., 2021). Feathers are connected to blood circulation only during the growth period, then contaminants taken up after food ingestion and assimilated into the blood may be incorporated into the keratinous matrix of the developing feather, where they are stored (Burger, 1993). The vascular connection wanes when the feather is fully grown, and contaminants cannot be further allocated into the keratin (García-Fernández et al., 2013). Consequently, feathers can serve as an archive of contaminant exposure for a bird during their growth period. Previous studies have confirmed that feathers are a suitable matrix for assessing exposure to pharmaceuticals, such as starlings exposed to fluoxetine (Whitlock et al., 2019) and chicken broilers to antibiotics (Církva et al., 2019; Cornejo et al., 2011). In the present paper, we have therefore assessed the use of feathers as a potential tool for monitoring wild birds exposure to pharmaceuticals in marine ecosystems.

Section snippets

Study site

The Venice Lagoon is located in northeastern Italy and has a surface of about 540 km2. The basin is connected to the Adriatic Sea by three inlets (Lido, Malamocco and Chioggia) which allow tidal flushing twice a day (microtidal and predominantly semidiurnal tides) (Tagliapietra and Volpi Ghirardini, 2006). The Lagoon is also one of the primary breeding areas for marine birds in the Mediterranean and hosts significant fractions of the Italian population of several species. Inputs of

Results

Feathers from both species contained NSAIDs and antidepressants at concentrations above the MQLs, although to a different extent. One or more APIs were quantified in 44 of the analysed composite samples (11 MG and 33 ST); the prevalence was higher in MG (100%) as compared to ST (92%). The most frequently occurring API was DICLO, with an overall prevalence of 87.2%, followed by NAP (27.7%), CITA (23.4%), DCITA (21.3%), FLUV (19.1%), IBU (17.0%) and SER (12.8%). VEN, NIM and FLUO were quantified

Feathers as biomonitors for APIs

Concentrations detected in the feathers indicated that waterbirds are exposed to NSAIDs and SSRIs, possibly due to the widespread use of these APIs and their incomplete removal in WWTPs (Carballa et al., 2004; Loos et al., 2013; Mole and Brooks, 2019). However, although dietary intake has been considered as the primary source of pharmaceuticals for fish-eating birds (Bean et al., 2018; Lazarus et al., 2015), our data cannot discriminate between internal deposition due to dietary intake and

Conclusions

This study is the first to consider the potential suitability of the use of feathers in assessing the exposure of waterbirds to human and veterinary pharmaceuticals. The focus of the study is on NSAIDs, SSRIs and SNRIs as well as some of their active metabolites.

Our research provides the first evidence of the presence of pharmaceutical residues in the fledglings of waterbirds. The detection of several active ingredients above method quantification limits suggests that feathers can be used as a

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.

Funding

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. 67416/2018).

CRediT authorship contribution statement

Gabriele Giuseppe Distefano: Investigation, Resources, Formal analysis, Data curation, Validation, Writing – original draft. Roberta Zangrando: Investigation, Resources, Formal analysis, Data curation, Validation, Writing – original draft. 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,

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.

Acknowledgements

The authors gratefully acknowledge the help of ELGA LabWater in providing the Chorus I and Chorus II that produced the ultrapure water used in these experiments.

References (109)

  • K. Fent et al.

    Ecotoxicology of human pharmaceuticals

    Aquat. Toxicol.

    (2006)
  • R.C. Fijn et al.

    GPS-tracking and colony observations reveal variation in offshore habitat use and foraging ecology of breeding Sandwich terns

    J. Sea Res.

    (2017)
  • K. Grabicova et al.

    Bioaccumulation of psychoactive pharmaceuticals in fish in an effluent dominated stream

    Water Res.

    (2017)
  • M. Gros et al.

    Removal of pharmaceuticals during wastewater treatment and environmental risk assessment using hazard indexes

    Environ. Int.

    (2010)
  • M. Herrero-Villar et al.

    NSAIDs detected in iberian avian scavengers and carrion after diclofenac registration for veterinary use in Spain

    Environ. Pollut.

    (2020)
  • M. Herrero-Villar et al.

    First diclofenac intoxication in a wild avian scavenger in Europe

    Sci. Total Environ.

    (2021)
  • V.L.B. Jaspers et al.

    Preen oil as the main source of external contamination with organic pollutants onto feathers of the common magpie (Pica pica)

    Environ. Int.

    (2008)
  • V.L.B. Jaspers et al.

    Body feathers as a potential new biomonitoring tool in raptors: a study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla)

    Environ. Int.

    (2011)
  • V.L.B. Jaspers et al.

    Bird feathers as a biomonitor for environmental pollutants: prospects and pitfalls

    TrAC Trends Anal. Chem.

    (2019)
  • A. Lajeunesse et al.

    Distribution of antidepressant residues in wastewater and biosolids following different treatment processes by municipal wastewater treatment plants in Canada

    Water Res.

    (2012)
  • M. Lierz

    Avian renal disease: pathogenesis, diagnosis, and therapy

    Vet. Clin. Exot. Anim. Pract.

    (2003)
  • R. Loos et al.

    EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents

    Water Res.

    (2013)
  • M.E. Løseth et al.

    White-tailed eagle (Haliaeetus albicilla) feathers from Norway are suitable for monitoring of legacy, but not emerging contaminants

    Sci. Total Environ.

    (2019)
  • L.M. Madikizela et al.

    Pharmaceuticals and their metabolites in the marine environment: sources, analytical methods and occurrence

    Trends Environ. Anal. Chem.

    (2020)
  • A. Mechlińska et al.

    Isotope-labeled substances in analysis of persistent organic pollutants in environmental samples

    TrAC Trends Anal. Chem.

    (2010)
  • M. Melnes et al.

    Dissimilar effects of organohalogenated compounds on thyroid hormones in glaucous gulls

    Environ. Res.

    (2017)
  • R.A. Mole et al.

    Global scanning of selective serotonin reuptake inhibitors: occurrence, wastewater treatment and hazards in aquatic systems

    Environ. Pollut.

    (2019)
  • R. Moreno-González et al.

    Seasonal distribution of pharmaceuticals in marine water and sediment from a mediterranean coastal lagoon (SE Spain)

    Environ. Res.

    (2015)
  • R. Moreno-González et al.

    Do pharmaceuticals bioaccumulate in marine molluscs and fish from a coastal lagoon?

    Environ. Res.

    (2016)
  • V. Naidoo et al.

    The use of toxicokinetics and exposure studies to show that carprofen in cattle tissue could lead to secondary toxicity and death in wild vultures

    Chemosphere

    (2018)
  • T.H. Nøst et al.

    Halogenated organic contaminants and their correlations with circulating thyroid hormones in developing Arctic seabirds

    Sci. Total Environ.

    (2012)
  • M. Picone et al.

    Accumulation of trace elements in feathers of the kentish plover Charadrius alexandrinus

    Ecotoxicol. Environ. Saf.

    (2019)
  • A. Puckowski et al.

    Bioaccumulation and analytics of pharmaceutical residues in the environment: a review

    J. Pharm. Biomed. Anal.

    (2016)
  • R. Rodil et al.

    Emerging pollutants in sewage, surface and drinking water in Galicia (NW Spain)

    Chemosphere

    (2012)
  • A. Ruhí et al.

    Bioaccumulation and trophic magnification of pharmaceuticals and endocrine disruptors in a Mediterranean river food web

    Sci. Total Environ.

    (2016)
  • T.M. Scott et al.

    Pharmaceutical manufacturing facility discharges can substantially increase the pharmaceutical load to U.S. Wastewaters

    Sci. Total Environ.

    (2018)
  • M. Sebastiano et al.

    High levels of fluoroalkyl substances and potential disruption of thyroid hormones in three gull species from South Western France

    Sci. Total Environ.

    (2021)
  • K. Świacka et al.

    Presence of pharmaceuticals and their metabolites in wild-living aquatic organisms – current state of knowledge

    J. Hazard. Mater.

    (2022)
  • J.T. Ackerman et al.

    Bird mercury concentrations change rapidly as chicks age: toxicological risk is highest at hatching and fledging

    Environ. Sci. Technol.

    (2011)
  • AIFA

    National Report on Medicines Use in Italy. Year 2019. Rome

    (2020)
  • H.F.D. Almeida et al.

    Removal of nonsteroidal anti-inflammatory drugs from aqueous environments with reusable ionic-liquid-based systems

    ACS Sustain. Chem. Eng.

    (2017)
  • P. Arnnok et al.

    Selective uptake and bioaccumulation of antidepressants in fish from effluent-impacted Niagara River

    Environ. Sci. Technol.

    (2017)
  • L. Arpin-Pont et al.

    Occurrence of PPCPs in the marine environment: a review

    Environ. Sci. Pollut. Res.

    (2016)
  • T.G. Bean et al.

    Behavioural and physiological responses of birds to environmentally relevant concentrations of an antidepressant

    Philos. Trans. R. Soc. B Biol. Sci.

    (2014)
  • T.G. Bean et al.

    Predictive framework for estimating exposure of birds to pharmaceuticals

    Environ. Toxicol. Chem.

    (2017)
  • M.L. Boström et al.

    Bioaccumulation and trophodynamics of the antidepressants sertraline and fluoxetine in laboratory-constructed, 3-level aquatic food chains

    Environ. Toxicol. Chem.

    (2017)
  • R.K. Boyd et al.

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

    (2008)
  • J.M. Brausch et al.

    Human pharmaceuticals in the aquatic environment: a review of recent toxicological studies and considerations for toxicity testing

    Rev. Environ. Contam. Toxicol.

    (2012)
  • T. Brodin et al.

    Ecological effects of pharmaceuticals in aquatic systems–impacts through behavioural alterations

    Philos. Trans. R. Soc. B Biol. Sci.

    (2014)
  • B.W. Brooks et al.

    Determination of select antidepressants in fish from an effluent-dominated stream

    Environ. Toxicol. Chem.

    (2005)
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    Gabriele Giuseppe Distefano and Roberta Zangrando worked together and contributed equally to this paper, and thus declare they share co-first authorship.

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