Assessing the exposure to human and veterinary pharmaceuticals in waterbirds: The use of feathers for monitoring antidepressants and nonsteroidal anti-inflammatory drugs
Graphical abstract
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.
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2023, ChemosphereCitation Excerpt :Feathers are commonly used to biomonitor diverse pollutants such as persistent organic pollutants (POPs) or trace elements (Borghesi et al., 2016; Espín et al., 2014; García-Fernández et al., 2013; Jaspers et al., 2011). Biomonitoring, i.e. the use of organisms or tissues to assess environmental contamination of a chemical with the purpose of assessing its potential hazardous exposure, requires differentiating between external and internal deposition of a pollutant (Distefano et al., 2022a; Jaspers et al., 2019). Feather analysis has been reported to be a valuable low-invasive method for the detection of environmental exposure to NNIs, but we still lack information regarding the suitability of feathers to biomonitor the contamination by NNIs.
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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.