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Quali-quantitative analysis of plastics and synthetic microfibers found in demersal species from Southern Tyrrhenian Sea (Central Mediterranean)
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Quali-quantitative analysis of plastics and synthetic microfibers found in demersal species from Southern Tyrrhenian Sea (Central Mediterranean) Gioele Capilloa,1, Serena Savocaa,1, Giuseppe Panarelloa, Monique Mancusob,c, Caterina Brancad, Valentino Romanod, Giovanna D'Angelod,e,∗, Teresa Bottarib,c, Nunziacarla Spanòf,∗∗ a
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy Institute for Marine Biological Resources and Biotechnology (IRBIM), National Research Council (CNR), Section of Messina, Spianata S. Raineri, 86, 98122, Messina, Italy c StazioneZoologica Anton Dohrn, Centro Interdipartimentale della Sicilia, Italy d Department of Mathematical and Computational Sciences, Physical Science and Earth Science, Messina University, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy e CNR-IPCF, Viale Ferdinando Stagno d’Alcontres 37, 98158, Messina, Italy f Department of Biomedical, Dental and Morphological and Functional Imaging University of Messina, Via Consolare Valeria, Messina, Italy b
A R T I C LE I N FO
A B S T R A C T
Keywords: Microfiber Marine pollution Demersal species Mediterranean sea Micro-Raman FT-IR
This study highlights plastics occurrence in five demersal fish species from the Southern Tyrrhenian Sea: the Red mullet Mullus barbatus barbatus, the Piper gurnard Trigla lyra, the Blackmouth catshark Galeus melastomus, the Lesser spotted dogfish Scyliorhinus canicula and the Brown ray Raja miraletus. Overall, 125 fish were examined: 21 Red mullets, 16 Piper gurnards, 75 Blackmouth catsharks, 72 Dogfish and 1 Brown ray. The percentage of fish with ingested plastics was 14.4% with 0.24 items per specimen. The majority of the debris were fibers and the application of infrared and Raman spectroscopy allowed the identification and discrimination of plastic and nonplastic fibers. The plastic debris isolated were mainly microplastics (94.1%), while macroplastics occurrence was very low (5.9%). The plastics were identified as polypropylene, Teflon, nylon, kraton G (triblock copolymer) and polyethylene. Also cellulose was detected. S. canicula was the species with the highest number of plastic pollutants.
1. Introduction Each year over 320 million tons of plastics are produced at the global level with an increasing trend and an expected production double in the next 20 years (Andrady, 2011; Wright and Kelly, 2017). Unfortunately, only a small part of this material is actually recycled (6–26%), while the remaining part ends up in landfills or is released directly into the environment (Barnes et al., 2009; Dris et al., 2015). Plastic debris are ubiquitous in the oceans, around the world, from the surface to deep waters (Thompson et al., 2004). Plastic debris are transformed into tiny fragments, classified as microplastics (MPs) (< 5 mm), mesoplastics (5–25 mm) and macroplastics (> 25 mm) (Cole et al., 2011; Faure et al., 2015; Galgani et al., 2013; Pellini et al., 2018). Primary MPs are particles originally manufactured at those sizes,
while secondary MPs are fragments generated by the breakdown of larger pieces (Costa et al., 2010; Mathalon and Hill, 2014). The fragmentation of plastics at the sea occurs through several processes (photodegradation, physical impacts, etc.) and results in the production of a larger number of smaller particles. Most MPs in the marine environment are secondary (Duis and Coors, 2016). The MPs vary in size, shape, colour, specific density and chemical composition. Generally, the most detected MPs in the marine environment are polyethylene (PE), polyvinyl chloride (PVC), polypropylene (PP), polyethylene terephthalate (PET) and polystyrene (PS) (Rochman et al., 2013). A growing concern linked to the presence of MPs in sea water is related to the potential impact of these particles in the marine trophic food web, through the ingestion by marine organisms, ranging from zooplankton to top predators (Collignon et al., 2014; Fossi et al., 2014;
∗ Corresponding author. Department of Mathematical and Computational Sciences, Physical Science and Earth Science, Messina University, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy. ∗∗ Corresponding author. E-mail addresses: [email protected] (G. D'Angelo), [email protected] (N. Spanò). 1 These authors contributed equally to this work.
https://doi.org/10.1016/j.marpolbul.2019.110596 Received 11 June 2019; Received in revised form 10 September 2019; Accepted 11 September 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Gioele Capillo, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110596
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Isolated particles were recorded and categorized in relation to their size and colour. After that, 16 fibers and two macro-items were cleaned in distilled water, centrifuged twice for 30 s removing organic residues and placed in between two microscope slides for subsequent characterization analysis.
Ivar Do Sul and Costa, 2014). The ingestion of MPs may also represent a vehicle of chemical pollutants (additives of these particles or persistent organic pollutants adsorbed on them (Koelmans et al., 2016) towards the organisms and the food chain, constituting a risk for biological functions of marine species; moreover could have implications for their consumers as humans as well (Hanke et al., 2013; Seltenrich, 2015). In the Mediterranean Sea the ingestion of MPs was reported both for pelagic and demersal fish species (Giani et al., 2019; Mancuso et al., 2019; Romeo et al., 2015; S. Savoca et al., 2019). The monitoring of this phenomenon in European waters is one of the objectives of the European Marine Strategy Framework Directive (MFSD) (Galgani et al., 2013; Hanke et al., 2013). Recently, in this context, new emerging debris have been considered, represented by semi-synthetic or natural fibers, coming from the textile industry or urban centres wastewaters. These fibers can be found in the gastrointestinal tract (GIT) of marine organisms and can often be confused with synthetic plastic fibers, since they are morphologically very similar (Serena Savoca et al., 2019). Actually, it is possible that artificial fibers are represented by manufacturing of natural origin (for example cellulose) or completely produced in the industry (cellulose and/or derivatives) (Comnea-Stancu et al., 2017; Remy et al., 2015; Wu et al., 2019). The aims of this study were to document the ingestion and the uptake of microplastics and microfibers in five demersal fish species in the Southern Tyrrhenian area (Central Mediterranean), and to identify the composition of the microfibers for distinguishing plastic fibers from the non-plastic ones. These investigations provide much-needed insight into level of microplastics pollution in the Mediterranean Sea and underline the necessity to use specific analytical techniques to explore and to confirm the microfiber composition in order to avoid overestimation when assessing the level of microplastics occurrence in fish.
2.3. Micro-Raman and ATR-FTIR analysis Plastic particles and fibers were analysed by attenuated total reflectance Fourier transform infrared (ATR–FTIR) and micro-Raman (μR) spectroscopies. Both techniques are routinely used for non-destructive and fast identification of MPs by the vibrational recognition of their molecular structures (Araujo et al., 2018; Güven et al., 2017). But, compared with FTIR techniques, micro-Raman spectroscopy has an higher spatial resolution (about 1 μm as against 10–20 μm of FTIR) which makes this technique better suitable for studying and identifying very small MPs (< 20 μm). Furthermore, the presence of confocal microscope makes very easy focusing the laser beam on the sample placed on the slide, without removing the cover-slip and thus avoiding undesired sample contamination. For these reasons, the use of μR spectrometer was always preferred for the analysis of all the microfibers, except for the samples that showed strong fluorescence signal, hindering the acquisition of a clear Raman spectrum. For these cases, infrared spectra were acquired in ATR mode, and special attention was payed to avoid contamination during the measurements. A micro-Raman system (LabRam HR 800 spectrometer, JobinYvon) equipped with a1800 gr/mm grating and a 77 K–cooled charged couple device detector was used for the Raman measurements. Spectra in the range 100 and 3000 cm-1 were collected in VV backscattering geometry with excitation wavelengths of 532 nm operating at 10–100 mW and with a 50x objective. Integration times were varied from 10 to 50 s, depending on the sample. ATR FTIR spectra were recorded in the mid IR range (400–4000 cm−1) on a Bruker Vertex 80 V FTIR spectrometer equipped with a DLaTGS detector and Platinum ATR accessory (Bruker) with a single reflection diamond crystal as ATR element. For each spectrum, 124 scans were collected at a resolution of 4 cm −1. When necessary, a baseline correction was applied to the recorded Raman or IR spectra using a polynomial regression model. For each sample, repeated measurements were performed for testing the reproducibility of data acquired. Furthermore, Raman spectra were taken from three different points of the same sample for eliminating influence of local impurities such as persistent organic pollutants. No difference was observed between the different spectra of the same sample in all cases. All vibrational spectra (Raman and IR) were analysed by BioRadKnownItAll software. Simple or multiple components were used for comparing sample spectra to reference library spectra. Fibers were identified with a level of certainty higher than 85%, by selecting the most appropriate match based on the correspondence of peak wavenumber positions.
2. Materials and methods 2.1. Fish sampling This study was conducted during a trawl survey in June 2017 in the southernmost part of the Tyrrhenian Sea (northern coasts of Sicily, Gulf of Patti; Fig. 1). Gulf of Patti is a Fishery Exclusion Zone (Regional Law N. 25/90). Four hauls of about 60 min were performed between 50 and 250 m depth. Two teleosts (Mullus barbatus barbatus and Trigla lyra) and three elasmobranch species (Galeus melastomus, Scyliorhinus canicula and Raja miraletus) were sorted on board. Each specimen was individually packaged and frozen (-20C°). Samples remained frozen until further analysis in laboratory. 2.2. Preventing contamination and particles isolation The handling and analysis of samples were performed in a room with restricted access during processing. Workspaces and all instruments and equipment (petri dishes, microscope slides, tweezer, etc.) were washed and rinsed with ultrapure Milli-Q water filtered (0.22 μm) and ethanol according to Bessa (2019). Equipment was checked under a microscope for contamination with airborne fibers before use. All clothing worn during laboratory work were of non-polymer nature and no artificial textiles too. A 100% cotton, white laboratory coat and nitrile gloves were always worn to reduce contamination. For each specimen, morpho-metrical measurements including total body length (TL, cm) and body weight (W, g) were determined (Table 1). The GIT and gills of samples were exposed to air for the minimum time possible and rinsed with pre-filtered deionized water. Subsequently, the gastrointestinal tract and the gills were inspected with the aid of a dissecting stereomicroscope. Filter papers in Petri dishes exposed to the laboratory air were used as control blanks during analysis of each sample (Bessa, 2019; Hanke et al., 2013).
3. Results A total of 125 specimens were examined, 21 of which presented plastic debris (16.8%) in the GIT (18) and in the gills (3). Eighteen specimens (14.4%) had ingested potentially plastic items for a total of 31 particles (0.24 items/specimen; Table 1). Plastic isolation was done by visual inspection under a stereo-microscope and was based on features such as uniformity in thickness and colour. Ingested plastic particles were portioned as follows: 6 in Mullus barbatus barbatus (14.3%), 4 in Trigla lyra (18.7%), 6 in Galeus melastomus (8.0%), 13 in Scyliorhinus canicula (33.3%), 2 in Raja miraletus (100%; see Table 1). Fibers between gill lamellae (0.19 items/specimen) were also isolated from three T. lyra specimens (18.7%). The shape of plastics was the same in most samples (fibers: 97.1%) 2
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Fig. 1. Location map showing the study area, relative to the Southern Tyrrhenian sea (Central Mediterranean). The area analysed in this work is highlighted by the white box.
3.1. Plastic composition
with the exception of a fragment found in the stomach of G. melastomus (2.9% Fig. 2; Fig. 4a). The black was the dominant colour (M. barbatus barbatus and R. miraletus 100%). Scyliorhinus canicula and T. lyra also ingested red plastics (15.38% and 14.28%, respectively) and, G. melastomus a white fragment (16.66%; Fig. 4 a). The plastics debris isolated were mainly microplastics (94.1%), while macroplastics occurrence was very low (5.9%; Fig. 4b). Selected images of fibers, taken by a digital camera interfaced to a microscope (Olympus CKX41), are reported in Fig. 5.
A total of 16 particles (47.05% total) were selected and subsequently analysed using micro-Raman or ATR-FTIR spectroscopy and BioRadKnowItAll software to determine their chemical composition and identification. This confirmed the occurrence of three non-plastic fibers identified as cellulose and many synthetic fibers. Specifically the plastic particles were identified as polypropylene (PP), Teflon (PTFE), nylon (PA), Kraton G (triblock copolymer), polyethylene (PE) (Fig. 6). In general, among the plastic fibers isolated, PP was predominant and Kraton G and PE were those present to a lesser extent (Fig. 6). The analysed fibres and debris were distributed in different ways 3
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Table 1 Morphometric measurements of analysed fish species collected from the southern coasts of Sicily (Gulf of Patti) and their corresponding contamination levels of particles. N: number of specimens examined; Np: Number of specimens with particles detected; (standard deviation). Species
Mullus barbatus barbatus Trigla lyra Galeus melastomus Scyliorhinus canicula Raya miraletus Total
Length (cm)
Weight (g)
Range
Mean
Range
Mean
11.0–22.5 10.0–16.0 32.0–52.5 19.8–51.5 45
17.2 (4.1) 13.9 (2.4) 43 (4.3) 40.7 (9) –
15–134 13–36 104–483 100–497 41
66.8 (40.7) 27 (9.48) 248.6 (74.8) 275.3 (140) –
N
Np
Particles detected %
Items/specimen
21 16 75 12 1 125
3 4 6 4 1 18
14.3 18.7 8 33.3 100 14.4
0.3 0.4 0.1 1.1 2.0 0.24
strong fluorescence background were investigated by ATR FTIR. Fluorescence is probably induced by dyes or additives that, however, did not hamper the acquisition of a recognizable infrared spectrum, allowing the identification of the microplastics. The Infrared spectra of some investigated samples are reported in Fig. 8. Anyway, two of the analysed fibers could not be identified unequivocally due to the poor quality of spectra showing very few or no identifiable peaks. Finally, the two macroplastics that were isolated from the stomachs of Galeus melastomus and Scyliorhinus canicula (the large fragment and the macrofilament shown in Figs. 2 and 3) were identified by Raman spectroscopy as polyethylene and polypropylene, respectively.
4. Discussion Fig. 2. Macroplastic fragment (polyethylene) found in the stomach of Galeus melastomus. Scale bar: 1 cm.
In this study, for the first time, is reported the chemical composition of plastic debris and synthetic fibers isolated from the GITs and gills of some demersal fishes coming from the Southern Tyrrhenian Sea. The specimens examined showed 14.4% of plastic polymers contamination. Mullus barbatus barbatus is widely regarded as a bio-indicator species for its benthic behaviour, habitat and feeding modalities and its reduced mobility (Bottari et al., 2016; Carreras-Aubets et al., 2012; Mangano et al., 2017). In our study the percentage of M. barbatus barbatus that ingested microplastics (14.28%) was lower than those reported for the Turkish (42%), Greek (32%) and Spanish (19%) Mediterranean coasts and for Adriatic Sea (64%) and other Italian coasts (Avio et al., 2015; Bellas et al., 2016; Digka et al., 2018; Giani et al., 2019; Güven et al., 2017). The major contaminant that affected examined individuals was represented by polytetrafluoroethylene (PTFE, 75%). Different results for this species have been obtained in the Western Mediterranean, where the specimens showed greater polyethylene terephthalate contamination (PET, 36.36%, Alomar and Deudero, 2017). The risk of ingestion is related to the feeding behaviour of M. barbatus barbatus, that swallows sediment (together with the prey) and expels it then through their gills. As well-known this feeding modality is typical also of T. lyra, and it could explain the presence of cellulose fibers on its gill rakers. Furthermore the ventilation mechanism could be involved in microfibers uptake/occurrences as stated by Watts et al. (2016) in Carcinus maenas. The results underline the presence of microfibers in gills and GIT of T. lyra. The identified fibers in T. lyra specimens were all composed by cellulose (100%). The effect that these fibers can have on the gill tissue is not yet known, but it is easy to hypothesize mechanical damage and therefore alteration of the respiratory function of the organ. Concerning the elasmobranchs, G. melastomus is a benthopelagic predator that feeds mainly of demersal invertebrates (shrimps and cephalopods) and mesopelagic fish (Bottari et al., 2017; Fischer et al., 1987; Giacopello et al., 2013; Rinelli et al., 2005). Recently, Romeo et al. (2016) demonstrated the presence of MPs in the stomach of mesopelagic species (Myctophidae, lanternfish) important food items of G. melastomus. Plastic particles could be ingested during the predation
Fig. 3. Macrofilament (polypropylene) found in the stomach of Scyliorhinus canicula. Scale bar: 1 cm.
among the various demersal species under study. In M. barbatus barbatus were predominant PTFE and PA, 75% and 25% respectively. All the microfibers analysed in T. lyra specimens were extracted from the gills lamellae. The fibers were analysed by Raman spectroscopy and identical spectra were obtained. The typical bands of cellulose (CL) (a large peak at 1400 cm-1, a strong double peak at 1100 cm-1, a weak band at 900 cm-1) were clearly observed (Kavkler and Demšar, 2011) and confirmed by library matching (see Fig. 7). The elasmobranchs showed a higher incidence of plastic polymers compared to the teleost and all were extracted from gastrointestinal tracts. G. melastomus specimens showed a contamination represented by PA and PE (50% for both), while the polymeric composition of particles, extracted by GIT of S. canicula specimens, consisted of PP, PTFE and CL. Finally, it was isolated a single fiber from R. miraletus GIT, which has been identified by library spectra matching of 85% as Kraton G. The Raman spectra of selected fibers are shown and compared with the reference spectra from libraries in Fig. 7. All the fibers exhibiting a 4
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Fig. 4. Percentage (%) of macro and micro plastics and cellulose categorized by shape and colour (a) and by size (b) extracted from the gastrointestinal tract and gills of demersal species along the northern Sicilian coasts (central Mediterranean Sea). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 5. Images of microfibers found in demersal fish species: a) Teflon (Mullus barbatus barbatus); b) cellulose (Trigla lyra); c) nylon (Galeus melasomus); d) p-propylene (Scyliorhinus canicula); e) Kraton G (Raja miraletus). Ruler in mm. 5
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In our study, the proportion of S. canicula ingesting microplastics was higher than the percentage of G. melastomus (33% and 8% respectively) and the most frequent plastic polymer found in this species was polypropylene (71.4%). This is in contrast with the hypothesis (Alomar and Deudero, 2017) that G. melastomus may be more vulnerable to microplastics ingestion than other elasmobranchs. An interesting result is given by the occurrence of Kraton G in Raja miraletus. Kraton G is the trade name given to a number of high performance elastomers manufactured by Kraton G Polymers, which are styrenic block copolymer (SBC) consisting of polystyrene and rubber blocks. These are widely used for many personal care products (i.e. grips on toothbrushes, elastic component together polyethylene baby diapers). To our knowledge, this is the first documented finding of this polymer in marine wildlife. Plastic contamination in Raja GIT could be linked to the food habits of the species (Capapé and Azouz, 1976) as well as to the presence of high quantities of plastic debris and fibers present on the sediment (Fastelli et al., 2016; Sanchez-Vidal et al., 2018; Woodall et al., 2014). The density of polymers may play a role on fibers ingested by demersal fishes. In fact, except for Kraton G (density 0.91 g/cm3) and polypropylene (density 0.95 g/cm3), the fibers identified in the present study were denser than water (range 1.15–2.2 g/cm3) and are expected to sink, becoming available in benthopelagic environments. The presence of low-density polymers in the GIT of demersal species demonstrate the spread of these pollutants along different trophic compartments. It has been already reported, in fact, the presence of these polymers in different marine species from pelagic, demersal and benthic environments (Bottari et al., 2019; Valente et al., 2019) highlighting the ubiquitous distribution debris throughout the entire water column (Choy et al., 2019). For the purposes of the research reported in this paper, it is worth noting that most of plastic microparticles were synthetic fibers. This result is in agreement with previous findings (Wright et al., 2013; Claessens et al., 2013; Lusher et al., 2013; Rochman et al., 2015; Barrows et al., 2018). Synthetic fibres tangle easily; this characteristic can originate bundles of fibers that can cause obstruction in the organs and hinder or prevent feeding (Lusher et al., 2013). The same consideration applies to cellulosic fibers. Cellulosic fibers do not indeed constitute an environmental problem in itself, but any additive or dye within them could be potentially carcinogenic and harmful for marine organisms and humans (Oehlmann et al., 2009; Talsness et al., 2009; Wright et al., 2013). In addition, the faster degradation of natural fiber compared to the synthetic one make it easier to release toxic compounds and organic pollutant adsorbed to the large surface area of fibers (Ladewig et al., 2015). Whether and to what extent these substances are a threat to marine biota is an issue in need of further and urgent investigation. It is also useful to observe that most of the types of identified synthetic and non-synthetic microfibers are used in clothes and textile manufacturing. Due to the extreme proximity of the Southern Tyrrhenian Sea to populated areas, there is a good reason to consider synthetic textiles a major cause of the found microplastic fibers. Consequently, it can be reasonably supposed that the main source of microfibers in sediments might be wastewater from washing machines (in accordance with Henry et al., 2019). Further studies are needed to determine the implications of microplastic ingestion on fish health and the hygienic sanitary implications for the humans (Thompson et al., 2009; Wright and Kelly, 2017).
Fig. 6. Percentage of ingested particles composition extracted from demersal species along the northern Sicilian coasts (central Mediterranean Sea).
Fig. 7. Raman spectra of selected fibers found in fishes (red) compared with related reference spectra (grey). . (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
action (primary ingestion) or more probably by preys of G. melastomus (secondary ingestion). In the same way our estimation of the microplastics ingestion percentage (8%) in G. melastomus is different from those reported in other areas of the Mediterranean Sea. In the Eastern Ionian Sea were reported percentages varying from 3.2% to 12.5% (Madurell and Cartes, 2003 and Anastasopoulou et al., 2013; respectively) and in the western Mediterranean Sea from 3.24.8% to 16–18% (Cartes et al., 2016 and Alomar and Deudero, 2017, respectively). The results indicate that G. melastomus ingested both synthetic microfibres (nylon) and macroplastic fragment (polyethylene). For what concerns the ingestion of plastics in the western Mediterranean Sea, Alomar and Deudero (2017) reported the presence of cellophane (33.3%) and polyethylene terephthalate (27.3%). The differences found are related to the different location of the study area and the local contamination level. Scyliorhinus canicula lives in direct contact with the seafloor where preys benthic and demersal species including fish, crustaceans, cephalopod and polychaetes (Bottari et al., 2014; Busalacchi et al., 2010; Lauriano et al., 2019). The MPs have already been recorded in S. canicula from Spanish Atlantic and Mediterranean coasts with a lower percentage (15.3%) than our samples (33%), but no comparison on the type of polymer can be done as the MPs were not characterized (Bellas et al., 2016).
Declaration of competing interest None. Acknowledgments The authors are grateful to the Captains and the crews of the CNR 6
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Fig. 8. Infrared spectra of selected fibers found in fishes (red) compared with related reference spectra (grey). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
scientific vessel ‘DALLAPORTA’. The authors thank all those participants who helped with fieldwork.
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Quali-quantitative analysis of plastics and synthetic microfibers found in demersal species from Southern Tyrrhenian Sea (Central Mediterranean) Gioele Capilloa,1, Serena Savocaa,1, Giuseppe Panarelloa, Monique Mancusob,c, Caterina Brancad, Valentino Romanod, Giovanna D'Angelod,e,∗, Teresa Bottarib,c, Nunziacarla Spanòf,∗∗ a
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy Institute for Marine Biological Resources and Biotechnology (IRBIM), National Research Council (CNR), Section of Messina, Spianata S. Raineri, 86, 98122, Messina, Italy c StazioneZoologica Anton Dohrn, Centro Interdipartimentale della Sicilia, Italy d Department of Mathematical and Computational Sciences, Physical Science and Earth Science, Messina University, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy e CNR-IPCF, Viale Ferdinando Stagno d’Alcontres 37, 98158, Messina, Italy f Department of Biomedical, Dental and Morphological and Functional Imaging University of Messina, Via Consolare Valeria, Messina, Italy b
A R T I C LE I N FO
A B S T R A C T
Keywords: Microfiber Marine pollution Demersal species Mediterranean sea Micro-Raman FT-IR
This study highlights plastics occurrence in five demersal fish species from the Southern Tyrrhenian Sea: the Red mullet Mullus barbatus barbatus, the Piper gurnard Trigla lyra, the Blackmouth catshark Galeus melastomus, the Lesser spotted dogfish Scyliorhinus canicula and the Brown ray Raja miraletus. Overall, 125 fish were examined: 21 Red mullets, 16 Piper gurnards, 75 Blackmouth catsharks, 72 Dogfish and 1 Brown ray. The percentage of fish with ingested plastics was 14.4% with 0.24 items per specimen. The majority of the debris were fibers and the application of infrared and Raman spectroscopy allowed the identification and discrimination of plastic and nonplastic fibers. The plastic debris isolated were mainly microplastics (94.1%), while macroplastics occurrence was very low (5.9%). The plastics were identified as polypropylene, Teflon, nylon, kraton G (triblock copolymer) and polyethylene. Also cellulose was detected. S. canicula was the species with the highest number of plastic pollutants.
1. Introduction Each year over 320 million tons of plastics are produced at the global level with an increasing trend and an expected production double in the next 20 years (Andrady, 2011; Wright and Kelly, 2017). Unfortunately, only a small part of this material is actually recycled (6–26%), while the remaining part ends up in landfills or is released directly into the environment (Barnes et al., 2009; Dris et al., 2015). Plastic debris are ubiquitous in the oceans, around the world, from the surface to deep waters (Thompson et al., 2004). Plastic debris are transformed into tiny fragments, classified as microplastics (MPs) (< 5 mm), mesoplastics (5–25 mm) and macroplastics (> 25 mm) (Cole et al., 2011; Faure et al., 2015; Galgani et al., 2013; Pellini et al., 2018). Primary MPs are particles originally manufactured at those sizes,
while secondary MPs are fragments generated by the breakdown of larger pieces (Costa et al., 2010; Mathalon and Hill, 2014). The fragmentation of plastics at the sea occurs through several processes (photodegradation, physical impacts, etc.) and results in the production of a larger number of smaller particles. Most MPs in the marine environment are secondary (Duis and Coors, 2016). The MPs vary in size, shape, colour, specific density and chemical composition. Generally, the most detected MPs in the marine environment are polyethylene (PE), polyvinyl chloride (PVC), polypropylene (PP), polyethylene terephthalate (PET) and polystyrene (PS) (Rochman et al., 2013). A growing concern linked to the presence of MPs in sea water is related to the potential impact of these particles in the marine trophic food web, through the ingestion by marine organisms, ranging from zooplankton to top predators (Collignon et al., 2014; Fossi et al., 2014;
∗ Corresponding author. Department of Mathematical and Computational Sciences, Physical Science and Earth Science, Messina University, Viale Ferdinando Stagno D'Alcontres 31, 98166, Messina, Italy. ∗∗ Corresponding author. E-mail addresses: [email protected] (G. D'Angelo), [email protected] (N. Spanò). 1 These authors contributed equally to this work.
https://doi.org/10.1016/j.marpolbul.2019.110596 Received 11 June 2019; Received in revised form 10 September 2019; Accepted 11 September 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Gioele Capillo, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110596
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Isolated particles were recorded and categorized in relation to their size and colour. After that, 16 fibers and two macro-items were cleaned in distilled water, centrifuged twice for 30 s removing organic residues and placed in between two microscope slides for subsequent characterization analysis.
Ivar Do Sul and Costa, 2014). The ingestion of MPs may also represent a vehicle of chemical pollutants (additives of these particles or persistent organic pollutants adsorbed on them (Koelmans et al., 2016) towards the organisms and the food chain, constituting a risk for biological functions of marine species; moreover could have implications for their consumers as humans as well (Hanke et al., 2013; Seltenrich, 2015). In the Mediterranean Sea the ingestion of MPs was reported both for pelagic and demersal fish species (Giani et al., 2019; Mancuso et al., 2019; Romeo et al., 2015; S. Savoca et al., 2019). The monitoring of this phenomenon in European waters is one of the objectives of the European Marine Strategy Framework Directive (MFSD) (Galgani et al., 2013; Hanke et al., 2013). Recently, in this context, new emerging debris have been considered, represented by semi-synthetic or natural fibers, coming from the textile industry or urban centres wastewaters. These fibers can be found in the gastrointestinal tract (GIT) of marine organisms and can often be confused with synthetic plastic fibers, since they are morphologically very similar (Serena Savoca et al., 2019). Actually, it is possible that artificial fibers are represented by manufacturing of natural origin (for example cellulose) or completely produced in the industry (cellulose and/or derivatives) (Comnea-Stancu et al., 2017; Remy et al., 2015; Wu et al., 2019). The aims of this study were to document the ingestion and the uptake of microplastics and microfibers in five demersal fish species in the Southern Tyrrhenian area (Central Mediterranean), and to identify the composition of the microfibers for distinguishing plastic fibers from the non-plastic ones. These investigations provide much-needed insight into level of microplastics pollution in the Mediterranean Sea and underline the necessity to use specific analytical techniques to explore and to confirm the microfiber composition in order to avoid overestimation when assessing the level of microplastics occurrence in fish.
2.3. Micro-Raman and ATR-FTIR analysis Plastic particles and fibers were analysed by attenuated total reflectance Fourier transform infrared (ATR–FTIR) and micro-Raman (μR) spectroscopies. Both techniques are routinely used for non-destructive and fast identification of MPs by the vibrational recognition of their molecular structures (Araujo et al., 2018; Güven et al., 2017). But, compared with FTIR techniques, micro-Raman spectroscopy has an higher spatial resolution (about 1 μm as against 10–20 μm of FTIR) which makes this technique better suitable for studying and identifying very small MPs (< 20 μm). Furthermore, the presence of confocal microscope makes very easy focusing the laser beam on the sample placed on the slide, without removing the cover-slip and thus avoiding undesired sample contamination. For these reasons, the use of μR spectrometer was always preferred for the analysis of all the microfibers, except for the samples that showed strong fluorescence signal, hindering the acquisition of a clear Raman spectrum. For these cases, infrared spectra were acquired in ATR mode, and special attention was payed to avoid contamination during the measurements. A micro-Raman system (LabRam HR 800 spectrometer, JobinYvon) equipped with a1800 gr/mm grating and a 77 K–cooled charged couple device detector was used for the Raman measurements. Spectra in the range 100 and 3000 cm-1 were collected in VV backscattering geometry with excitation wavelengths of 532 nm operating at 10–100 mW and with a 50x objective. Integration times were varied from 10 to 50 s, depending on the sample. ATR FTIR spectra were recorded in the mid IR range (400–4000 cm−1) on a Bruker Vertex 80 V FTIR spectrometer equipped with a DLaTGS detector and Platinum ATR accessory (Bruker) with a single reflection diamond crystal as ATR element. For each spectrum, 124 scans were collected at a resolution of 4 cm −1. When necessary, a baseline correction was applied to the recorded Raman or IR spectra using a polynomial regression model. For each sample, repeated measurements were performed for testing the reproducibility of data acquired. Furthermore, Raman spectra were taken from three different points of the same sample for eliminating influence of local impurities such as persistent organic pollutants. No difference was observed between the different spectra of the same sample in all cases. All vibrational spectra (Raman and IR) were analysed by BioRadKnownItAll software. Simple or multiple components were used for comparing sample spectra to reference library spectra. Fibers were identified with a level of certainty higher than 85%, by selecting the most appropriate match based on the correspondence of peak wavenumber positions.
2. Materials and methods 2.1. Fish sampling This study was conducted during a trawl survey in June 2017 in the southernmost part of the Tyrrhenian Sea (northern coasts of Sicily, Gulf of Patti; Fig. 1). Gulf of Patti is a Fishery Exclusion Zone (Regional Law N. 25/90). Four hauls of about 60 min were performed between 50 and 250 m depth. Two teleosts (Mullus barbatus barbatus and Trigla lyra) and three elasmobranch species (Galeus melastomus, Scyliorhinus canicula and Raja miraletus) were sorted on board. Each specimen was individually packaged and frozen (-20C°). Samples remained frozen until further analysis in laboratory. 2.2. Preventing contamination and particles isolation The handling and analysis of samples were performed in a room with restricted access during processing. Workspaces and all instruments and equipment (petri dishes, microscope slides, tweezer, etc.) were washed and rinsed with ultrapure Milli-Q water filtered (0.22 μm) and ethanol according to Bessa (2019). Equipment was checked under a microscope for contamination with airborne fibers before use. All clothing worn during laboratory work were of non-polymer nature and no artificial textiles too. A 100% cotton, white laboratory coat and nitrile gloves were always worn to reduce contamination. For each specimen, morpho-metrical measurements including total body length (TL, cm) and body weight (W, g) were determined (Table 1). The GIT and gills of samples were exposed to air for the minimum time possible and rinsed with pre-filtered deionized water. Subsequently, the gastrointestinal tract and the gills were inspected with the aid of a dissecting stereomicroscope. Filter papers in Petri dishes exposed to the laboratory air were used as control blanks during analysis of each sample (Bessa, 2019; Hanke et al., 2013).
3. Results A total of 125 specimens were examined, 21 of which presented plastic debris (16.8%) in the GIT (18) and in the gills (3). Eighteen specimens (14.4%) had ingested potentially plastic items for a total of 31 particles (0.24 items/specimen; Table 1). Plastic isolation was done by visual inspection under a stereo-microscope and was based on features such as uniformity in thickness and colour. Ingested plastic particles were portioned as follows: 6 in Mullus barbatus barbatus (14.3%), 4 in Trigla lyra (18.7%), 6 in Galeus melastomus (8.0%), 13 in Scyliorhinus canicula (33.3%), 2 in Raja miraletus (100%; see Table 1). Fibers between gill lamellae (0.19 items/specimen) were also isolated from three T. lyra specimens (18.7%). The shape of plastics was the same in most samples (fibers: 97.1%) 2
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Fig. 1. Location map showing the study area, relative to the Southern Tyrrhenian sea (Central Mediterranean). The area analysed in this work is highlighted by the white box.
3.1. Plastic composition
with the exception of a fragment found in the stomach of G. melastomus (2.9% Fig. 2; Fig. 4a). The black was the dominant colour (M. barbatus barbatus and R. miraletus 100%). Scyliorhinus canicula and T. lyra also ingested red plastics (15.38% and 14.28%, respectively) and, G. melastomus a white fragment (16.66%; Fig. 4 a). The plastics debris isolated were mainly microplastics (94.1%), while macroplastics occurrence was very low (5.9%; Fig. 4b). Selected images of fibers, taken by a digital camera interfaced to a microscope (Olympus CKX41), are reported in Fig. 5.
A total of 16 particles (47.05% total) were selected and subsequently analysed using micro-Raman or ATR-FTIR spectroscopy and BioRadKnowItAll software to determine their chemical composition and identification. This confirmed the occurrence of three non-plastic fibers identified as cellulose and many synthetic fibers. Specifically the plastic particles were identified as polypropylene (PP), Teflon (PTFE), nylon (PA), Kraton G (triblock copolymer), polyethylene (PE) (Fig. 6). In general, among the plastic fibers isolated, PP was predominant and Kraton G and PE were those present to a lesser extent (Fig. 6). The analysed fibres and debris were distributed in different ways 3
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Table 1 Morphometric measurements of analysed fish species collected from the southern coasts of Sicily (Gulf of Patti) and their corresponding contamination levels of particles. N: number of specimens examined; Np: Number of specimens with particles detected; (standard deviation). Species
Mullus barbatus barbatus Trigla lyra Galeus melastomus Scyliorhinus canicula Raya miraletus Total
Length (cm)
Weight (g)
Range
Mean
Range
Mean
11.0–22.5 10.0–16.0 32.0–52.5 19.8–51.5 45
17.2 (4.1) 13.9 (2.4) 43 (4.3) 40.7 (9) –
15–134 13–36 104–483 100–497 41
66.8 (40.7) 27 (9.48) 248.6 (74.8) 275.3 (140) –
N
Np
Particles detected %
Items/specimen
21 16 75 12 1 125
3 4 6 4 1 18
14.3 18.7 8 33.3 100 14.4
0.3 0.4 0.1 1.1 2.0 0.24
strong fluorescence background were investigated by ATR FTIR. Fluorescence is probably induced by dyes or additives that, however, did not hamper the acquisition of a recognizable infrared spectrum, allowing the identification of the microplastics. The Infrared spectra of some investigated samples are reported in Fig. 8. Anyway, two of the analysed fibers could not be identified unequivocally due to the poor quality of spectra showing very few or no identifiable peaks. Finally, the two macroplastics that were isolated from the stomachs of Galeus melastomus and Scyliorhinus canicula (the large fragment and the macrofilament shown in Figs. 2 and 3) were identified by Raman spectroscopy as polyethylene and polypropylene, respectively.
4. Discussion Fig. 2. Macroplastic fragment (polyethylene) found in the stomach of Galeus melastomus. Scale bar: 1 cm.
In this study, for the first time, is reported the chemical composition of plastic debris and synthetic fibers isolated from the GITs and gills of some demersal fishes coming from the Southern Tyrrhenian Sea. The specimens examined showed 14.4% of plastic polymers contamination. Mullus barbatus barbatus is widely regarded as a bio-indicator species for its benthic behaviour, habitat and feeding modalities and its reduced mobility (Bottari et al., 2016; Carreras-Aubets et al., 2012; Mangano et al., 2017). In our study the percentage of M. barbatus barbatus that ingested microplastics (14.28%) was lower than those reported for the Turkish (42%), Greek (32%) and Spanish (19%) Mediterranean coasts and for Adriatic Sea (64%) and other Italian coasts (Avio et al., 2015; Bellas et al., 2016; Digka et al., 2018; Giani et al., 2019; Güven et al., 2017). The major contaminant that affected examined individuals was represented by polytetrafluoroethylene (PTFE, 75%). Different results for this species have been obtained in the Western Mediterranean, where the specimens showed greater polyethylene terephthalate contamination (PET, 36.36%, Alomar and Deudero, 2017). The risk of ingestion is related to the feeding behaviour of M. barbatus barbatus, that swallows sediment (together with the prey) and expels it then through their gills. As well-known this feeding modality is typical also of T. lyra, and it could explain the presence of cellulose fibers on its gill rakers. Furthermore the ventilation mechanism could be involved in microfibers uptake/occurrences as stated by Watts et al. (2016) in Carcinus maenas. The results underline the presence of microfibers in gills and GIT of T. lyra. The identified fibers in T. lyra specimens were all composed by cellulose (100%). The effect that these fibers can have on the gill tissue is not yet known, but it is easy to hypothesize mechanical damage and therefore alteration of the respiratory function of the organ. Concerning the elasmobranchs, G. melastomus is a benthopelagic predator that feeds mainly of demersal invertebrates (shrimps and cephalopods) and mesopelagic fish (Bottari et al., 2017; Fischer et al., 1987; Giacopello et al., 2013; Rinelli et al., 2005). Recently, Romeo et al. (2016) demonstrated the presence of MPs in the stomach of mesopelagic species (Myctophidae, lanternfish) important food items of G. melastomus. Plastic particles could be ingested during the predation
Fig. 3. Macrofilament (polypropylene) found in the stomach of Scyliorhinus canicula. Scale bar: 1 cm.
among the various demersal species under study. In M. barbatus barbatus were predominant PTFE and PA, 75% and 25% respectively. All the microfibers analysed in T. lyra specimens were extracted from the gills lamellae. The fibers were analysed by Raman spectroscopy and identical spectra were obtained. The typical bands of cellulose (CL) (a large peak at 1400 cm-1, a strong double peak at 1100 cm-1, a weak band at 900 cm-1) were clearly observed (Kavkler and Demšar, 2011) and confirmed by library matching (see Fig. 7). The elasmobranchs showed a higher incidence of plastic polymers compared to the teleost and all were extracted from gastrointestinal tracts. G. melastomus specimens showed a contamination represented by PA and PE (50% for both), while the polymeric composition of particles, extracted by GIT of S. canicula specimens, consisted of PP, PTFE and CL. Finally, it was isolated a single fiber from R. miraletus GIT, which has been identified by library spectra matching of 85% as Kraton G. The Raman spectra of selected fibers are shown and compared with the reference spectra from libraries in Fig. 7. All the fibers exhibiting a 4
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Fig. 4. Percentage (%) of macro and micro plastics and cellulose categorized by shape and colour (a) and by size (b) extracted from the gastrointestinal tract and gills of demersal species along the northern Sicilian coasts (central Mediterranean Sea). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 5. Images of microfibers found in demersal fish species: a) Teflon (Mullus barbatus barbatus); b) cellulose (Trigla lyra); c) nylon (Galeus melasomus); d) p-propylene (Scyliorhinus canicula); e) Kraton G (Raja miraletus). Ruler in mm. 5
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In our study, the proportion of S. canicula ingesting microplastics was higher than the percentage of G. melastomus (33% and 8% respectively) and the most frequent plastic polymer found in this species was polypropylene (71.4%). This is in contrast with the hypothesis (Alomar and Deudero, 2017) that G. melastomus may be more vulnerable to microplastics ingestion than other elasmobranchs. An interesting result is given by the occurrence of Kraton G in Raja miraletus. Kraton G is the trade name given to a number of high performance elastomers manufactured by Kraton G Polymers, which are styrenic block copolymer (SBC) consisting of polystyrene and rubber blocks. These are widely used for many personal care products (i.e. grips on toothbrushes, elastic component together polyethylene baby diapers). To our knowledge, this is the first documented finding of this polymer in marine wildlife. Plastic contamination in Raja GIT could be linked to the food habits of the species (Capapé and Azouz, 1976) as well as to the presence of high quantities of plastic debris and fibers present on the sediment (Fastelli et al., 2016; Sanchez-Vidal et al., 2018; Woodall et al., 2014). The density of polymers may play a role on fibers ingested by demersal fishes. In fact, except for Kraton G (density 0.91 g/cm3) and polypropylene (density 0.95 g/cm3), the fibers identified in the present study were denser than water (range 1.15–2.2 g/cm3) and are expected to sink, becoming available in benthopelagic environments. The presence of low-density polymers in the GIT of demersal species demonstrate the spread of these pollutants along different trophic compartments. It has been already reported, in fact, the presence of these polymers in different marine species from pelagic, demersal and benthic environments (Bottari et al., 2019; Valente et al., 2019) highlighting the ubiquitous distribution debris throughout the entire water column (Choy et al., 2019). For the purposes of the research reported in this paper, it is worth noting that most of plastic microparticles were synthetic fibers. This result is in agreement with previous findings (Wright et al., 2013; Claessens et al., 2013; Lusher et al., 2013; Rochman et al., 2015; Barrows et al., 2018). Synthetic fibres tangle easily; this characteristic can originate bundles of fibers that can cause obstruction in the organs and hinder or prevent feeding (Lusher et al., 2013). The same consideration applies to cellulosic fibers. Cellulosic fibers do not indeed constitute an environmental problem in itself, but any additive or dye within them could be potentially carcinogenic and harmful for marine organisms and humans (Oehlmann et al., 2009; Talsness et al., 2009; Wright et al., 2013). In addition, the faster degradation of natural fiber compared to the synthetic one make it easier to release toxic compounds and organic pollutant adsorbed to the large surface area of fibers (Ladewig et al., 2015). Whether and to what extent these substances are a threat to marine biota is an issue in need of further and urgent investigation. It is also useful to observe that most of the types of identified synthetic and non-synthetic microfibers are used in clothes and textile manufacturing. Due to the extreme proximity of the Southern Tyrrhenian Sea to populated areas, there is a good reason to consider synthetic textiles a major cause of the found microplastic fibers. Consequently, it can be reasonably supposed that the main source of microfibers in sediments might be wastewater from washing machines (in accordance with Henry et al., 2019). Further studies are needed to determine the implications of microplastic ingestion on fish health and the hygienic sanitary implications for the humans (Thompson et al., 2009; Wright and Kelly, 2017).
Fig. 6. Percentage of ingested particles composition extracted from demersal species along the northern Sicilian coasts (central Mediterranean Sea).
Fig. 7. Raman spectra of selected fibers found in fishes (red) compared with related reference spectra (grey). . (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
action (primary ingestion) or more probably by preys of G. melastomus (secondary ingestion). In the same way our estimation of the microplastics ingestion percentage (8%) in G. melastomus is different from those reported in other areas of the Mediterranean Sea. In the Eastern Ionian Sea were reported percentages varying from 3.2% to 12.5% (Madurell and Cartes, 2003 and Anastasopoulou et al., 2013; respectively) and in the western Mediterranean Sea from 3.24.8% to 16–18% (Cartes et al., 2016 and Alomar and Deudero, 2017, respectively). The results indicate that G. melastomus ingested both synthetic microfibres (nylon) and macroplastic fragment (polyethylene). For what concerns the ingestion of plastics in the western Mediterranean Sea, Alomar and Deudero (2017) reported the presence of cellophane (33.3%) and polyethylene terephthalate (27.3%). The differences found are related to the different location of the study area and the local contamination level. Scyliorhinus canicula lives in direct contact with the seafloor where preys benthic and demersal species including fish, crustaceans, cephalopod and polychaetes (Bottari et al., 2014; Busalacchi et al., 2010; Lauriano et al., 2019). The MPs have already been recorded in S. canicula from Spanish Atlantic and Mediterranean coasts with a lower percentage (15.3%) than our samples (33%), but no comparison on the type of polymer can be done as the MPs were not characterized (Bellas et al., 2016).
Declaration of competing interest None. Acknowledgments The authors are grateful to the Captains and the crews of the CNR 6
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Fig. 8. Infrared spectra of selected fibers found in fishes (red) compared with related reference spectra (grey). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
scientific vessel ‘DALLAPORTA’. The authors thank all those participants who helped with fieldwork.
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