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Article

Occurrence of Novel and Legacy Per/Polyfluoroalkyl Substances (PFASs) in Scopoli’s Shearwater (Calonectris diomedea) Feathers

by
Eirini Trypidaki
1,
Silje Marie Bøe Gudmundsen
1,
Georgios Karris
2,*,
Stavros Xirouchakis
3,
Susana V. Gonzalez
1,
Junjie Zhang
1,
Veerle L. B. Jaspers
4,
Tomasz Maciej Ciesielski
4,5,
Catherine Tsangaris
6 and
Alexandros G. Asimakopoulos
1
1
Department of Chemistry, Norwegian University of Science and Technology (NTNU), 7491 Trondheim, Norway
2
Department of Environment, School of Environment, Ionian University, M. Minotou-Giannopoulou Str., 29100 Panagoula, Greece
3
School of Science & Engineering, Natural History Museum of Crete, University of Crete, University Campus (Knossos), 71409 Heraklion, Greece
4
Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, 7491 Trondheim, Norway
5
Department of Arctic Technology, The University Center in Svalbard, 9171 Longyearbyen, Norway
6
Institute of Oceanography, Hellenic Centre for Marine Research (HCMR), 46.7 Athens Sounio Ave, 19013 Anavyssos, Greece
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(9), 541; https://doi.org/10.3390/d16090541
Submission received: 3 August 2024 / Revised: 30 August 2024 / Accepted: 30 August 2024 / Published: 3 September 2024
(This article belongs to the Special Issue Ecology, Diversity and Conservation of Seabirds—2nd Edition)
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Versions Notes

Abstract

:
Per- and polyfluoroalkyl substances (PFASs) are contaminants of great concern due to their ubiquitous environmental occurrence in the environment and their potential adverse effects on organisms. There is currently limited information regarding the occurrence of PFASs in Scopoli’s Shearwater (Calonectris diomedea). In this study, two feather samples per bird were obtained from 26 adults on Strofades colony (Ionian Sea/Greece) during the early phase of the chick-rearing period (late July 2019). The samples consisted of barbs and barbules of the primary feathers, P1 and P10, reflecting pollution pressures at the time and the place of feather growth, i.e., at the species’ breeding and wintering grounds for P1 and P10, respectively. There were 25 PFAS detected in the feathers, with detection rates ranging from 2% (perfluorododecanoic acid—PFDoDA; perfluorohexane sulfonate—PFHxS; 9-chlorohexadecafluoro-3-oxanonane-1-sulfonate—9Cl-PF3ONS; 2,3,3,3-tetrafluoro-2-(1,1,2,2,3,3,3-heptafluoropropoxy)propanoate—Gen-X) to 98% (sodium 1H,1H,2H,2H-perfluorooctane sulfonate; 6:2 FTSA). ∑PFAS ranged from 25.93 ng/g to 426.86 ng/g of feather sample. The highest mean concentration (109.10 ng/g feather) was reported for perfluorononanoic acid (PFNA). No significant differences in PFAS concentrations with high detection rate (>20%) were found according to the sex of the birds. PFAS concentrations with a detection rate > 20% in the P1 vs. P10 feathers of Scopoli’s Shearwater adults were not significantly different, reflecting the fact that breeding grounds in the Mediterranean and wintering grounds in the Atlantic seem to be contaminated with similar PFASs levels, even though some compounds showed regional trends.

1. Introduction

Per- and polyfluoroalkyl substances (PFASs) are a large group of anthropogenic organic contaminants that have been used since the 1950s [1] in various applications such as textile products, food packaging, firefighting foams, floor polishes, coatings, and hydraulic fluids [2]. PFASs have gained scientific attention due to their global distribution, environmental persistence, and associations with adverse health effects in organisms [3,4,5,6,7,8,9,10,11]. Legacy PFASs (e.g., perfluorooctanesulfonic acid (PFOS)) have been classified by the European Union as hazardous chemicals subject to REACH regulation [12], while emerging novel PFASs (e.g., GenX) are being considered for further regulatory restriction [13].
Several studies have examined PFAS contamination in various bird species, with focus on seabirds including white-tailed eagle (Haliaeetus albicilla) [14,15,16,17]. PFAS concentrations are found at high levels in the liver, blood, plasma, and eggs of seabirds [14,17,18,19,20]. Seabirds are ideal environmental sentinels for PFAS monitoring since they occupy higher trophic levels in a marine food web [21,22,23], and they can allow us to monitor contamination loads through longer time periods [24,25,26,27].
Feathers are increasingly being used as a matrix of choice for biomonitoring purposes; primarily due to the simplicity of gathering and storage as a non-invasive sampling method. According to species-specific molting strategies, feathers mainly reflect a bird’s diet from when and where each feather was grown; as a consequence, they can provide an overview of the concentrations of inorganic and organic pollutants in a specific environment. In general, feathers are used for the biomonitoring of metals [24] and organic contaminants [28,29]. PFASs in particular can be found in feathers due to their great affinity towards proteins [30,31]. Associations between perfluorooctane sulfonic acid (PFOS) concentrations in the feathers and livers of birds have been documented [32]. However, the relationship between PFASs concentrations in feathers and internal tissue concentrations is not always clear [33]. To our knowledge, fewer studies were performed on PFAS in seabird feathers compared to those of raptors from terrestrial ecosystems [23,25,26,27,34].
In the literature, the occurrence of contaminants, such as mercury [35,36], plastics [37], and persistent organic contaminants [38] in Scopoli’s Shearwater (Calonectris diomedea) is well documented. However, there is currently limited information regarding PFAS exposure and accumulation in Scopoli’s Shearwaters, with only one report of PFAS concentrations in blood samples of populations from Spain, Tunisia, and Greece [39]. The findings suggest that this top marine predator can be used as a sentinel species that can provide guidelines for marine ecosystem science and specific conservation efforts [40].
With this background, the present study aimed to establish feather concentrations of PFAS in a Scopoli’s Shearwater population that was sampled along the coastal waters of Greece. The objectives were as follows: (a) to investigate the occurrence of PFASs; (b) to identify potential differences among primary feathers (innermost, P1–outermost, P10) that reflect differences in the breeding and wintering settings of the target species; (c) establish baseline concentrations needed for determining future trends in exposures. The effect of sex differences on feather concentrations was also investigated. To our knowledge, this is the first study on the occurrence of 32 PFASs in the feathers of Scopoli’s Shearwaters.

2. Materials and Methods

2.1. Study Area and Sampling

The Scopoli’s Shearwater is a long-lived migratory and colonial pelagic seabird with a high degree of site tenacity [41,42]. Its diet consists primarily of pelagic and mesopelagic fish, crabs, squids, and zooplankton found in shallow seas and reefs [43,44,45,46], and trawl fishery discards that are mainly benthopelagic [47].
Sampling was carried out in the Strofades Island complex (37°15′ N, 21°00′ E), a remote group of two small low-altitude islets (22 m above sea level; m. a.s.l.) and several rocks, located in the southern Ionian Sea, 32 nautical miles (nm) south of Zakynthos Island and 26 nm west of the Peloponnese (Figure 1). Roughly 5550 pairs of the species [48] breed on the two main islets (Stamfani and Arpyia), that span over 4 km2 and constitute part of the National Marine Park of Zakynthos. It is worth mentioning that the current study will provide baseline data for PFAS contamination on Shearwaters that are located in the pristine environment of the Strofades Island group before the initiation of the forthcoming local developments from the offshore wind and oil energy industry. This is also very important for the conservation of the species on a global scale, considering the fact that the Strofades Islands presently constitute one of the three European strongholds, with colonies comprising more than 1000 breeding pairs each [49].
Two feather samples per bird (n = 52) were obtained from 26 adult birds during the early phase of chick-rearing (end of July 2019). The sampled birds belonged to both sexes with most of them being breeders (19 inds; 73%) and a few of them being prospectors (7 inds; 27%). Due to the ethical restrictions of removing an entire feather, the samples consisted of barbs and barbules close to the tip of the primary feathers, P1 (innermost feather) and P10 (outermost feather) (Figure 2). The samples had a mean weight of 10.6 ± 3.67 mg and were stored in separate sealed plastic bags (LDPE) to avoid contamination. According to the molting pattern of the species, these feathers are mostly suitable for examining the ecological regimes in the species distribution range; P1 and P10 grow then the birds are at their breeding grounds and their wintering grounds, respectively [50]. In Scopoli’s Shearwater, specific secondary feathers and rectrices can be also considered to grow around the breeding or wintering sites according to the molting pattern of the species [50]. In our case, we decided to focus on the primary feathers since it is more convenient to collect adequate samples from the outermost feathers; consequently, this is a less stressful process, as it minimizes the amount of time the birds are handled. More details about the samples are available in Table S1.
Notable sexual dimorphism in voice (males are high-pitched, and females are low-pitched) was used for the sex determination of the sampled individuals [51,52]. The discriminant function developed for the sex classification of Scopoli’s Shearwater on the Strofades colony, based on morphometric variables and weight, was not used here, since the previous sampling included fledglings and not adults [53].
The target chemicals—namely PFBA, PFHxA, 7H-PFHpA, PFPeA, PFHpA, PFOA, P37DMOA, PFNA, PFDA, PFUnDA, PFDoDA, PFTrDA, PFTeDeA, PFHxDA, PFBS, PFHxS, PFHpS, PFOS, 4:2 FTSA, 6:2 FTSA, 8:2 FTSA, 10:2 FTSA, FOSA, MeFOSA, EtFOSA, MeFOSE, EtFOSE, FOSAA, MeFOSAA, EtFOSAA, diSAMPAP, ADONA, GenX, 9Cl-PF3ONS, as well as materials used herein—are the same as those described in [53] and their full names are included in the Supplementary Materials. Data on the target analytes (TAs) are available in the Supplementary Materials, Tables S2–S6.

2.2. Pre-Treatment of the Feathers, Sample Extraction, and Analysis

To remove external contamination from the feathers, sample treatment was performed according to the methods described in the existing literature [28,29]. Briefly, the feathers were washed with water (Milli-Q, ultra-pure) in a large Petri dish and each barb was properly cleaned with distilled water (Milli-Q ultra-pure) by separating the barbs. It is noteworthy that, for a thorough wash, two pairs of tweezers were used to separate the barbs by pulling them downwards and away from each other. The washed feathers were then placed in aluminum foil trays to dry for at least 24 h. The dried feathers were weighed and cut into small pieces (1–3 mm). Between each sample, all equipment used for washing and cutting was cleaned consecutively with distilled water (Milli-Q ultra-pure) and methanol (MeOH). Samples were transferred into 15 mL PP-tubes, weighed, and then 2 mL hexane was added to each, followed by 10 min of ultrasonication. Thereafter, the samples were wrapped in aluminum foil that was pre-punctured and allowed to dry. According to the previous literature, n-hexane does not remove any internal PFASs from feathers [15].
The extraction and analysis were performed as previously described [54]. In brief, the cut barbs were transferred to 15 mL PP-tubes and weighed. After the samples were transferred to PP-tubes, 10 mL of hexane was added. The samples were then placed in an ultrasonic bath for 10 min before the hexane was decanted, and the samples were capped with aluminum foil and dried for 48 h. The isotopically labeled internal standard (IS) was added when the samples were dry. The IS consisted of a mix of 0.03 mL 13C8-PFOA (50 ppm) and 0.03 mL 13C8-PFOS (50 ppm) diluted with 1.44 mL MeOH. A measure of 0.03 mL of IS was added to each sample. Exactly 2 mL of 200 mM solution of NaOH in MeOH was also added to each sample. The samples were thoroughly mixed using a vortex mixer and left to soak for 1 h. After that step, a total of 10 mL MeOH was added to the samples. Samples were mixed for 20 s using a vortex mixer and left in an ultrasonic bath for 10 min. This procedure was repeated three times; after the third time, the samples were left to soak overnight. MeOH was chosen as the extraction solution to resolve the PFASs bound to proteins in the feathers. A measure of 2 mL of a 2M solution of HCl in MeOH was added, and the samples were mixed using a vortex mixer and put in an ultrasonic bath for 10 min. Then, the samples were centrifuged at 3500 rpm for 10 min, and the extract was transferred to clean 15 mL PP-tubes. The remaining samples were rinsed with 2 mL of MeOH and the extract was transferred to the clean PP-tubes. The extracted samples were evaporated to approximately 1 mL under a gentle stream of nitrogen at 35 °C using a TurboVap®LV automated evaporation system.

2.3. Data Generation and Treatment

The method used in this study for assessing the performance characteristics, including quality control, is reported in [54]. The method limits of detection (mLODs) and quantification (mLOQs) for all targeted PFASs ranged from 0.06 to 6 ng/g and from 0.2 to 18 ng/g, respectively (Table S7). MassLynx v4.1 (Waters, Milford, MA, USA) was used to acquire UHPLC-MS/MS data and Targetlynx was used for the data integration. Data below mLOD for a target analyte were not included in the data analysis. An independent-samples t-test or a non-parametric Mann–Whitney U test were applied to determine differences in PFAS concentrations between P1 and P10 feather samples or between sexes according to Levene’s test for the homogeneity of variance (p < 0.05). All tests were performed at the 0.05 level of significance, whereas all concentrations are reported as ng/g feather (air-dried but not freeze-dried). Data handling was performed using Microsoft Excel 2019 (Washington, DC, USA), while statistical analysis was performed using R (v. 4.1.2, Development Core Team, November 2021) and SPSS 22 (IBM, Armonk, NY, USA). Mapping was implemented using ESRI’s integrated GIS system ArcGIS v 10.1.

3. Results and Discussion

3.1. Occurrence of PFASs in Feathers

The concentrations of PFASs determined in the feathers of Scopoli’s Shearwater are shown in Table 1. Among the 32 compounds studied, 25 were detected in the samples with a detection rate ranging from 2 to 98%. On an individual level, the ∑PFAS concentrations ranged from 25.93 ng/g to 426.86 ng/g, whereas the number of detected and/or quantified PFASs ranged from 4 to 14 different compounds. The highest detection rate was determined in 6:2 FTSA (98%), followed by FOSAA, which was detected in less than half of the samples (42%), while the lowest detection rates were found for PFDoA, PFHxS, GenX, and 9Cl-PF3ONS (2%). Seven compounds, namely PFOA, PFHxDA, 4:2 FTSA, 10:2 FTSA, FOSA, MeFOSE, and EtFOSE, were not detected in any sample. The highest mean concentration was reported for PFNA (109.10 ng/g).
A previous study identified PFASs in blood samples of Scopoli’s Shearwaters from Greece, Tunisia, and Spain (Menorca and Murcia) [39]. The mean concentrations determined ranged from 0.20 to 41.9 ng/mL, with PFOS being the most dominant compound. The concentrations of PFOS, PFUnA, and PFDoA determined in Shearwaters blood samples from different colonies, including a satellite islet of Crete (Eastern Mediterranean) [39], were higher than those determined (at a low rate) in the feathers used in the present study. Only PFTrDA was detected in higher concentrations in Scopoli’s Shearwater feather samples (17.15–72.8 ng/g) than in blood samples (0.1–3.4 ng/mL). This finding about PFASs concentrations is in accordance with PFASs detected in white-tailed eagle feathers and plasma from Norway [15]. PFOS was found to be the most common target analyte in plasma in other marine species such as the Black-Legged Kittiwake (Rissa tridactyla) studied in Norway in 2012 [55], where many PFAS were detected in higher concentrations than the present study; this may be the result of the different use pattern of PFASs today compared to the recent past, but it may also be explained by the use of a different biological matrices for analysis. It is noteworthy that a critical factor for the differences in PFAS concentrations and analogue abundances between studies is the actual year of sampling, due to the recently imposed, ongoing restrictions [4]. In addition, feathers have occasionally demonstrated their ability to reflect regional differences in contamination [56]. However, spatial and interspecies heterogeneity of contaminant concentrations in seabirds suggested that factors such as metabolic capabilities and spatial movements may obscure expected differences [57]. Similarly, a recent study found no significant regional or yearly differences in Tawny Owl (Strix aluco) feathers, although a slight increase was indicated throughout the years of study [54]. In general, even if diet constitutes the main origin of PFASs for predators, due to their accumulation process, additional environmental factors other than trophic level (e.g., trans-equatorial migration pattern; core foraging areas during breeding and non-breeding seasons; species-specific accumulation process depending on metabolic capabilities, sex, and breeding status) have been implied to manage accumulation patterns in wildlife [57,58,59]. This is of crucial importance for the current target species which is a long-lived migrant Procellariid species that is well known for delayed maturity.
In contrast to terrestrial environments where several relevant studies have been conducted in feathers, e.g., raptors in Norway [23,60,61,62], there is a certain knowledge gap from marine habitats, especially from the Mediterranean region. In both Black Guillemot (Cepphus grylle) and Thick-Billed Murre (Uria lomvia) eggs sampled from Prince Leopold Island in the Canadian Arctic, PFOS was the most prevalent PFAS [63]. PFASs have also been identified in bottlenose dolphins (Tursiops truncatus) along the northern Adriatic Sea coast [64], and in shark and ray species from the Ionian and Aegean Seas [65]. Nonetheless, a few studies have been carried out in the Adriatic and the Ionian archipelagos, where Scopoli’s Shearwaters originating from the Strofades colony feed during the breeding season. The occurrence of PFASs in a remote island complex like Strofades can also be attributed to the long-range transport of PFASs by ocean currents [66,67,68] and to the atmospheric oxidative transformations and subsequent wet and dry deposition of airborne PFAS precursors [69,70]. This scenario is also enhanced by the wide foraging dispersal of the highly mobile seabird species, which may cover distances up to 250 km from the colony of Strofades in visiting foraging areas [71].
No significant differences were found herein between the sexes and PFAS concentrations with a detection rate >20% (Table S8). Prior studies on the liver in other avian species have indicated that female individuals had lower concentrations of PFOSs than males due to PFOS elimination through eggs [72]. At low exposure concentrations, PFOSs are likely to be eliminated in the feathers rather than the liver; when a certain threshold value is achieved, accumulation might then occur in the liver [73].

3.2. Comparison of PFAS Concentrations between P1 and P10 Feathers

The molting pattern of Shearwaters follows a simple and descendant sequence from the innermost (P1) to the outermost primary feathers (P10) [50], which temporally coincides with the foraging range of Strofades breeders constrained to the Ionian and Adriatic Seas in the Central Mediterranean and the overwintering in the upwelling systems of the tropical Atlantic Ocean, respectively [74,75,76] (Figure 3). The comparison of the means of the concentrations of PFASs with detection rates > 20% in P1 vs. P10 feathers of Scopoli’s Shearwater adults originating from the Strofades colony revealed no significant differences (Table 2). Nevertheless, our findings with the (non-significant) higher concentrations of 6:2 FTSA and FOSAA determined in P1 denote some regional differences that reflect the different contaminant loads that can be found between the marine ecosystems of the breeding and the wintering areas; the Mediterranean basin has higher contamination pressures of in comparison with the Atlantic. Similar results were found in Shearwater feathers for inorganic elements (such as Hg, Se, and Pb), with feathers molted during winter demonstrating lower concentrations compared to those growing during the breeding period [34]. However, longer breeding seasons and shorter wintering periods in procellariform species such as Scopoli’s Shearwater—as well as their possibly higher daily food intake while breeding—may explain the differences in PFAS concentrations found herein. For instance, Shearwaters spend 243 days in their breeding areas, 80 days at their wintering grounds, and 42 days in migration between the two regions [76]. Individual dietary specialization in feeding strategies—as an adaptation strategy to environmental conditions—could also explain the variation in PFAS contaminant concentrations in breeding and wintering grounds; this has already been documented in a relative species, the Cory’s Shearwater (Calonectris borealis) [77]. Consequently, further research on the year-round dietary habits of the species should be carried out.
The overall impact of PFASs on Shearwaters remains uncertain. PFAS contaminants in various organisms can reach concentrations that are comparable to those of organochlorine chemicals [78], with documented effects. For instance, gulls with high concentrations of organochlorine pesticides have lower breeding success, higher adult mortality [79], higher parasite loads [80], and more asymmetric wing feathers [81]. Laboratory studies have shown that PFOSs are harmful to birds, with effects ranging from lower weight gain and increased liver mass [72,82] to increased mortality, reduced hatchability, and histological alterations in the liver [83]. Furthermore, a study examining the avian developmental toxicity of F-53B and PFOS using eggs from domesticated chickens (Gallus gallus domesticus) found that environmentally relevant concentrations have a significant impact on the heart rate of avian embryos; F-53B significantly increased the liver mass of the hatchlings [60]. Additionally, toxicological data on an avian predator suggested the occurrence of the immunomodulatory effects of some organohalogenated contaminants (OHCs), such as organochlorines (OCs) and PFAS, in avian wildlife [84]. PFAS concentrations as low as 50 ng/g in liver tissues have also been shown to cause sublethal effects, such as reduced hatching success, in the Northern Bobwhite (Colinus virginianus) [85]. In general, the PFAS concentrations found herein are low, although factors such as PFAS mixture, age, sex, and species influence toxicity effects [57]. However, PFAS can be biomagnified and bioaccumulated in Shearwaters and we must consider the fact that little information is available concerning the effects of low-level concentrations of these contaminants in multiple-contaminant-exposure and multiple-stressor scenarios; we must also consider their potential chronic effect on Shearwater populations.

4. Conclusions

To the best of our knowledge, this is the first study on the occurrence of 32 PFASs in Scopoli’s Shearwater feathers. Given the ongoing use of PFASs in industry and the remoteness of the research location, this is an important discovery. More research is needed to evaluate connections between concentrations in different feather types and internal tissues for various contaminants including PFASs. It is noteworthy that GenX-related chemicals were recently identified as substances of very high concern by ECHA, raising concerns about the need for further investigation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16090541/s1, Table S1: Sample information including the sample ID, the Ring ID, the date of sampling, and the sex of the Shearwaters from the Strofades Island complex (Ionian Sea, Greece); Table S2: Per- and polyfluoroalkyl carboxylates (PFCAs); Table S3: Perfluoroalkane sulfonates (PFSAs); Table S4: Fluorotelomer sulfonates (FTSAs); Table S5: Polyfluoroalkane sulfonamido substances (FASA/Es); Table S6: Perfluoroalkyl sulfonamino phosphate and, per- and polyfluoroalkyl ether acids; Table S7: The method limits (in ng/g feather) of detection (LODs) and quantification (LOQs) for all targeted PFASs; Table S8: Comparison of mean concentrations in ng/g feather of PFAS with a detection rate > 20% in males (M) and females (F) of Scopoli’s Shearwater adults originating from Strofades island group (July 2019).

Author Contributions

Conceptualization, G.K. and S.X.; methodology, A.G.A., G.K. and S.X.; software, A.G.A.; validation, A.G.A., S.M.B.G., S.V.G., J.Z., T.M.C. and V.L.B.J.; formal analysis, E.T., S.M.B.G., A.G.A. and G.K.; investigation, E.T., G.K., S.X., A.G.A. and C.T.; resources, C.T. and A.G.A.; data curation, A.G.A., G.K., S.X. and C.T.; writing—original draft preparation, E.T. and S.M.B.G.; writing—review and editing, A.G.A., G.K., S.X., V.L.B.J., J.Z. and C.T.; visualization, G.K.; supervision, A.G.A. and G.K.; project administration, C.T. and A.G.A.; funding acquisition, C.T. and A.G.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded as part of the Interreg Med project Plastic Busters MPAs, co-financed by the European Regional Development Fund (grant agreement No 4MED17_3.2_M123_027).

Institutional Review Board Statement

Research expedition of the current study had specific permit from the Management Agency of the National Marine Park of Zakynthos (NMPZ), which is a public service of the Greek Ministry of Environment and Energy (e.g., ref. no. 579/12-3-2019 NMPZ; 180468/657/20-3-2019 Ministry of Environment and Energy). Additionally, the Natural History Museum of Crete (scientific institution code GR002), the partner of the current research study, has a CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) sampling permit for wildlife (ref. no. 096860/2199/23-8-2005). All sampling procedures were carried out with the maximum safety of Scopoli’s Shearwater adults, as well as the least possible disturbance to the adults and chicks of the target species and its breeding habitats.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Materials, further inquiries can be directed to the corresponding author.

Acknowledgments

We would like to thank the local authorities, e.g., the Management Agency of National Marine Park of Zakynthos, the National Coastguard Authorities, and the Metropolis of Zakynthos for permitting us to carry out the fieldwork in the study area. Also, we would like to thank the Hellenic Bird Ringing Centre for providing us with Rings and Nikolaos Manolas for preparing the drawings.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location of the remote insular study area in the Ionian Sea, Western Greece.
Figure 1. Location of the remote insular study area in the Ionian Sea, Western Greece.
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Figure 2. Feather sampling on P1 and P10 feathers of Scopoli’s Shearwater.
Figure 2. Feather sampling on P1 and P10 feathers of Scopoli’s Shearwater.
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Figure 3. Distribution of Scopoli’s Shearwater adults from Strofades during the breeding and the wintering season in Mediterranean Sea and Atlantic Ocean, respectively. The distribution pattern was based on geolocators deployed on Shearwaters during the period 2009–2014 [71,72].
Figure 3. Distribution of Scopoli’s Shearwater adults from Strofades during the breeding and the wintering season in Mediterranean Sea and Atlantic Ocean, respectively. The distribution pattern was based on geolocators deployed on Shearwaters during the period 2009–2014 [71,72].
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Table 1. Occurrence of PFAS in Scopoli’s Shearwater feather samples (n = 52) collected on Stamfani Island/Strofades during breeding season of 2019. Values are given in ng/g feather (n.q.: not quantified).
Table 1. Occurrence of PFAS in Scopoli’s Shearwater feather samples (n = 52) collected on Stamfani Island/Strofades during breeding season of 2019. Values are given in ng/g feather (n.q.: not quantified).
Chemical TypenDetection Rate (%)Mean ± StdvMedianMinMax
6:2 FTSA519814.08 ± 10.0112.161.7436.96
FOSA22428.03 ± 9.625.000.7637.56
PFTeDeA142726.85 ± 12.1725.6513.0754.19
7H-PFHpA12233.29 ± 3.122.621.1813.23
PFNA1019109.10 ± 80.0077.5613.71248.43
PFHpA91715.12 ± 8.3915.295.1428.08
PFTrDA71329.60 ± 18.0625.3417.1572.83
EtFOSA51010.24 ± 6.837.363.0322.60
PFHxA5107.69 ± 2.286.894.5210.84
PFHpS51010.32 ± 3.7710.385.2614.83
PFUnDA51016.63 ± 6.7813.5111.3929.88
ADONA51010.63 ± 9.825.593.4129.95
diSAMPAP51014.77 ± 3.3313.4011.8020.98
PFPeA4832.13 ± 6.4531.2423.9742.05
PFOS3620.53 ± 6.1823.6911.9026.01
P37DMOA363.03 ± 0.213.082.763.26
MeFOSAA3614.81 ± 5.2217.297.5419.59
PFBS362.35 ± 1.132.151.083.82
PFDA3611.44 ± 1.6011.729.3613.25
PFDoDA1215.3715.3715.3715.37
PFHxS127.797.797.797.79
GenX1261.9461.9461.9461.94
MeFOSA815n.q.n.q.n.q.n.q.
8:2 FTSA24n.q.n.q.n.q.n.q.
9Cl-PF3ONS12n.q.n.q.n.q.n.q.
Table 2. Comparison of mean concentrations in ng/g feather of PFAS with a detection rate > 20% in P1 vs. P10 feathers of Scopoli’s shearwater adults originating from the Strofades island group (July 2019).
Table 2. Comparison of mean concentrations in ng/g feather of PFAS with a detection rate > 20% in P1 vs. P10 feathers of Scopoli’s shearwater adults originating from the Strofades island group (July 2019).
PFASnMeanStdvSt. Error MeanMann–Whitney U Test Asymp. Sig. (2-Tailed)Independent Samples t-Test Sig. (2-Tailed)
6:2 FTS–P12616.0311.662.290.356-
6:2 FTS–P102512.067.941.59
FOSAA–P11410.1510.422.780.306-
FOSAA–P1084.322.660.94
7H-PFHpA–P172.501.120.421.000-
7H-PFHpA–P1054.384.982.23
PFTeDA–P1526.2713.406.00-0.904
PFTeDA–P10927.1713.004.33
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MDPI and ACS Style

Trypidaki, E.; Gudmundsen, S.M.B.; Karris, G.; Xirouchakis, S.; Gonzalez, S.V.; Zhang, J.; Jaspers, V.L.B.; Ciesielski, T.M.; Tsangaris, C.; Asimakopoulos, A.G. Occurrence of Novel and Legacy Per/Polyfluoroalkyl Substances (PFASs) in Scopoli’s Shearwater (Calonectris diomedea) Feathers. Diversity 2024, 16, 541. https://doi.org/10.3390/d16090541

AMA Style

Trypidaki E, Gudmundsen SMB, Karris G, Xirouchakis S, Gonzalez SV, Zhang J, Jaspers VLB, Ciesielski TM, Tsangaris C, Asimakopoulos AG. Occurrence of Novel and Legacy Per/Polyfluoroalkyl Substances (PFASs) in Scopoli’s Shearwater (Calonectris diomedea) Feathers. Diversity. 2024; 16(9):541. https://doi.org/10.3390/d16090541

Chicago/Turabian Style

Trypidaki, Eirini, Silje Marie Bøe Gudmundsen, Georgios Karris, Stavros Xirouchakis, Susana V. Gonzalez, Junjie Zhang, Veerle L. B. Jaspers, Tomasz Maciej Ciesielski, Catherine Tsangaris, and Alexandros G. Asimakopoulos. 2024. "Occurrence of Novel and Legacy Per/Polyfluoroalkyl Substances (PFASs) in Scopoli’s Shearwater (Calonectris diomedea) Feathers" Diversity 16, no. 9: 541. https://doi.org/10.3390/d16090541

APA Style

Trypidaki, E., Gudmundsen, S. M. B., Karris, G., Xirouchakis, S., Gonzalez, S. V., Zhang, J., Jaspers, V. L. B., Ciesielski, T. M., Tsangaris, C., & Asimakopoulos, A. G. (2024). Occurrence of Novel and Legacy Per/Polyfluoroalkyl Substances (PFASs) in Scopoli’s Shearwater (Calonectris diomedea) Feathers. Diversity, 16(9), 541. https://doi.org/10.3390/d16090541

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