Skip to main content

Marine litter in stomach content of small pelagic fishes from the Adriatic Sea: sardines (Sardina pilchardus) and anchovies (Engraulis encrasicolus)

Abstract

Marine litter impacts oceans and affects marine organisms, representing a potential threat for natural stocks of pelagic fish species located at the first levels of the marine food webs. In 2013–2014, on a seasonal basis, marine litter and microplastics in stomach contents from Sardinia pilchardus and Engraulis encrasicolus were evaluated. Selected species are plankitivores of great ecological and commercial importance in the Adriatic Sea. Collected data were correlated to possible factors able to affect ingested levels as well as species, season of sampling, biometry and sex of animals. Almost all tested samples (80 organisms for each species) contained marine litter (over 90% of samples from both species) and also microplastics; while any meso- or macroplastics were recorded. On average, recorded items were as follows: 4.63 (S. plichardus) and 1.25 (E. encrasicolus) per individual. Sardines evidenced a higher number of microplastics characterised by a smaller size than those recorded in anchovies. For sardines, sex, Gastro Somatic Index and sampling season showed negligible effects on the number of ingested litter; conversely, anchovies showed differences related with both sex of animals and dominant colour of ingested materials with prevalence for black and blue colours.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alomar C, Estarellas F, Deudero S (2016) Microplastics in the Mediterranean Sea: deposition in coastal shallow sediments, spatial variation and preferential grain size. Mar Environ Res 115:1–10

    Article  CAS  Google Scholar 

  • Avio CG, Gorbi S, Regoli F (2015) Experimental development of a new protocol for extraction and characterization of microplastics in fish tissue: first observation in commercial species from Adriatic Sea. Mar Environ Res 111:18–26

    Article  CAS  Google Scholar 

  • Barboza LGA, Vethaak AD, Lavorante BRBO, Lundebye AK, Guilhermino L (2018) Marine microplastic debris: an emerging issue for food security, food safety and human health. Mar Pollut Bull 133:336–348

    Article  CAS  Google Scholar 

  • Barnes DKA, Galgani F, Thompson RC, Barlaz M (2009) Accumulation and fragmentation of plastic debris in global environments. Philos Trans R Soc Lond Ser B Biol Sci 364:1985–1998

    Article  CAS  Google Scholar 

  • Blašković A, Fastelli P, Čižmek H, Guerranti C, Renzi M (2017) Plastic litter in sediments from the Croatian marine protected area of the natural park of Telaščica Bay (Adriatic Sea). Mar Pollut Bull 114:583–586

    Article  CAS  Google Scholar 

  • Borme D, Tirelli V, Brandt SB, Fonda Umani S, Arneri E (2009) Diet of Engraulis encrasicolus in the northern Adriatic Sea (Mediterranean): ontogenetic changes and feeding selectivity. Mar Ecol Prog Ser 392:193–209

    Article  Google Scholar 

  • Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.). Environ Sci Technol 42:5026–5031

    Article  CAS  Google Scholar 

  • Browne MA, Niven SJ, Galloway TS, Rowland SJ, Thompson RC (2013) Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr Biol 23:2388–2392

    Article  CAS  Google Scholar 

  • Carpi P, Martinelli M, Belardinelli A, Russo A, Arneri E, Coluccelli A, Santojanni A (2015) Coupling an oceanographic model to a Fishery Observing System through mixed models: the importance of fronts for anchovy in the Adriatic Sea. Fish Oceanogr 24(6):521–532

    Article  Google Scholar 

  • Choy CA, Drazen JC (2013) Plastic for dinner? Observation of frequent debris ingestion by pelagic predatory fishes from the central North Pacific. Mar Ecol Prog Ser 485:155–163

    Article  Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, Plymouth

    Google Scholar 

  • Cole M, Webb H, Lindeque PK, Fileman SE, Halsband C, Galloway TS (2014) Isolation of microplastics in biota-rich seawater samples and marine organisms. Sci Rep 4:4528

    Article  CAS  Google Scholar 

  • Collard F, Gilbert B, Compère P, Eppe G, Das K, Jauniaux T, Parmentier E (2017a) Microplastics in livers of European anchovies (Engraulis encrasicolus, L.). EnvironPollut 229:1000–1005

    CAS  Google Scholar 

  • Collard F, Gilbert B, Eppe G, Roos L, Compère P, Das K, Parmentier E (2017b) Morphology of the filtration apparatus of three planktivorous fishes and relation with ingested anthropogenic particles. Mar Pollut Bull 116:182–191

    Article  CAS  Google Scholar 

  • Crawford CB, Quinn B (2016) Plastic production, waste and legislation, Microplastic pollutants. Elsevier Inc., pp 39–56

  • Cury P, Bakun A, Crawford R, Jarre A, Quiñones R, Shannon L, Verheye H (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci 57(3):603–618

    Article  Google Scholar 

  • Davision P, Asch R (2011) Plastic ingestion by mesopelagic fishes in the North Pacific Subtropical Gyre. Mar Ecol Prog Ser 432:173–180

    Article  Google Scholar 

  • Dehaut A, Cassone AL, Frere L, Hermabessiere L, Himber C, Rinnert E, Riviere G, Lambert C, Soudant P, Huvert A, Deflos G, Paul-Pont I (2016) Microplastic in seafood: benchmark protocol for their extraction and characterization. Environ Pollut 215:223–233

    Article  CAS  Google Scholar 

  • Desai VR (1970) Studies on the fishery and biology of tortor (Hamilton) from river Narmada. J Inland Fish Soc India 2:101–112

    Google Scholar 

  • Desforges JPW, Galbraith M, Dangerfield N, Ross PS (2014) Widespread distribution of microplastics in subsurface seawater in the NE Pacific Ocean. Mar Pollut Bull 79:94–99

    Article  CAS  Google Scholar 

  • Enders K, Lenz R, Beer S, Stademan CA (2017) Extraction of microplastic from biota: recommended acidic digestion destroys common plastic polymers. ICES J Mar Sci 74(1):326–331

    Article  Google Scholar 

  • Fastelli P, Blăsković A, Bernardi G, Romeo T, Čižmek H, Andaloro F, Russo GF, Guerranti C, Renzi M (2016) Plastic litter in sediments from a marine area likely to become protected (Aeolian Archipelago’s islands, Tyrrhenian Sea). Mar Pollut Bull 113:526–529

    Article  CAS  Google Scholar 

  • Fossi MC, Marsili L, Baini M, Giannetti M, Coppola D, Guerranti C, Caliani I, Minutoli R, Lauriano G, Finoia MG, Rubegni F (2016) Fin whales and microplastics: the Mediterranean Sea and the Sea of Cortez scenarios. EnvironPollut 209:68–78

    CAS  Google Scholar 

  • Fossi MC, Pedà C, Compa M, Tsangaris C, Alomar C, Claro F, Ioakeimidis C, Galgani F, Hema T, Deudero S, Romeo T, Battaglia P, Andaloro F, Caliani I, Casini S, Panti C, Baini M (2017) Bioindicators for monitoring marine litter ingestion and its impacts on Mediterranean biodiversity. Environ Pollut 237:1023–1040

    Article  CAS  Google Scholar 

  • Galgani F, Hanke G, Werner S, De Vrees L (2013) Marine litter within the European Marine Strategy Framework Directive. ICES J Mar Sci 70:1055–1064

    Article  Google Scholar 

  • Ivar do Sul JA, Costa MF (2014) The present and future of microplastic pollution in the marine environment. Environ Pollut 185:352–364

    Article  CAS  Google Scholar 

  • Karami A, Golieskardi A, Ho YB, Larat V, Salamatinia B (2017) Microplastics in eviscerated flesh and excised organs of dried fish. Sci Rep 7:5473

    Article  CAS  Google Scholar 

  • Karlsson TM, Vethaak AD, Almorth BC, Ariese F, van Velzen M, Hassellov M, Leslie HA (2017) Screening for microplastic in sediment, water, marine invertebrates and fish: method development and microplastic accumulation. Mar Pollut Bull 122:403–408

    Article  CAS  Google Scholar 

  • Koelmans AA, Bakir A, Burton GA, Janssen CR (2016) Microplastic as a vector for chemicals in the aquatic environment: critical review and model-supported reinterpretation of empirical studies. Environ Sci Technol 50:3315–3326. https://doi.org/10.1021/acs.est.5b06069

    Article  CAS  Google Scholar 

  • Kraus R, Supić N, Lučić D, Njire J (2015) Impact of winter oceanographic conditions on zooplankton abundance in northern Adriatic with implications on Adriatic anchovy stock prognosis. Estuar Coast Shelf Sci 167:56–66

    Article  Google Scholar 

  • Lakshmanan R, Venugopal V, Rao BYK, Bongirwar DR (1999) Stability of lipids of Indian mackerel to gamma irradiation. J Food Lipids 6:277–285

    Article  CAS  Google Scholar 

  • Law KL, Moret-Ferguson S, Maximenko NA, Proskurowsk G, Peacock EE, Hafner J, Reddy CM (2010) Plastic accumulation in the North Atlantic Subtropical Gyre. Science 329:1185–1188

    Article  CAS  Google Scholar 

  • Lee H, Byun DE, Kim JM, Kwon JH (2018) Desorption modeling of hydrophobic organic chemicals from plastic sheets using experimentally determined diffusion coefficients in plastics. Mar Pollut Bull 126:312–317

    Article  CAS  Google Scholar 

  • Lenz R, Enders K, Stedmon CA, Mackenzie DMA, Nielsen TG (2015) A critical assessment of visual identification of marine microplastic using Raman spectroscopy for analysis improvement. Mar Pollut Bull 100(1):82–91

    Article  CAS  Google Scholar 

  • de Lucia GA, Caliani I, Marra S, Camedda A, Coppa S, Alcaro L, Campani T, Giannetti M, Coppola D, Cicero AM, Panti C, Baini M, Guerranti C, Marsili L, Massaro G, Fossi MC, Matiddi M (2014) Amount and distribution of neustonic micro-plastic off the western Sardinian coast (Central-Western Mediterranean Sea). Mar Environ Res 100:10–16

    Article  CAS  Google Scholar 

  • Lusher AL, Hollman PCH, Mendoza-Hill JJ (2017) Microplastics in fisheries and aquaculture: status of knowledge on their occurrence and implications for aquatic organisms and food safety. FAO Fisheries and Aquaculture Technical Paper. No. 615, Rome 147p

  • Mohammadizadeh F, Valinassab T, Jamili S, Marinfar A, Bahri-Shabanipour AH, Mohammadizadeh M (2010) A study on diet composition and feeding habitats of sawtooth barracuda (Sphyraenaputnamae) in Bandar-Abbas (north of Persian Gulf). J Fish Aquat Sci 5(3):179–190

    Article  Google Scholar 

  • Murua H, Saborido-Rey F (2003) Female reproductive strategies of marine fish species of the North Atlantic. J Northwest At Fis Sc 33:23–31

    Article  Google Scholar 

  • Muus BJ, Nielsen JG (1999) Sea fish. Scandinavian fishing year book, Hedehusene 340 pp

    Google Scholar 

  • Neves D, Sobral P, Ferreira JL, Pereira T (2015) Ingestion of microplastics by commercial fish off the Portuguese coast. Mar Pollut Bull 101:119–126

    Article  CAS  Google Scholar 

  • Nikolioudakis N, Palomera I, Machias A, Somarakis S (2011) Diel feeding intensity and daily ration of the sardine Sardina plchardus. Mar Ecol Prog Ser 437:215–228

    Article  Google Scholar 

  • Nuelle MT, Dekiff JH, Remy D, Friies E (2014) A new analytical approach for monitoring microplastics in marine sediments. Environ Pollut 184:161–169

    Article  CAS  Google Scholar 

  • Pellini G, Gomiero A, Fortibuoni T, Ferrà C, Grati F, Tassetti N, Polidori P, Fabi G, Scarcella G (2018) Characterization of microplastic litter in the gastrointestinal tract of Solea solea from the Adriatic Sea. Environ Pollut 234:943–952

    Article  CAS  Google Scholar 

  • Plastic Europe (2014). Plastics—the fact 2014/2015. https://www.plasticseurope.org/application/files/5515/1689/9220/2014plastics_the_facts_PubFeb2015.pdf

  • Plounevez S, Champalbert G (1999) Feeding behaviour and trophic environment of Engraulis encrasicolus (L.) in the bay of Biscay. Estuar Coast Shelf Sci 49:177–191

    Article  Google Scholar 

  • Qu X, Su L, Li H, Liang M, Shi H (2018) Assessing the relationship between the abundance and properties of microplastics in water and in mussels. Sci Total Environ 621:679–686

    Article  CAS  Google Scholar 

  • Renzi M, Blašković A, Bernardi G, Russo GF (2018) Plastic litter transfer from sediments towards marine trophic webs: a case study on holothurians. Mar Pollut Bull 135:376–385

    Article  CAS  Google Scholar 

  • Riede K (2004) Global register of migratory species—from global to regional scales. Final report of the R&D-Projekt 808 05 081. Federal Agency for Nature Conservation, Bonn 329 pp

    Google Scholar 

  • Rist S, Almroth BC, Hartmann NB, Karlsson TM (2018) A critical perspective on early communications concerning human health aspects of microplastics. Sci Total Environ 626:720–726

    Article  CAS  Google Scholar 

  • Romeo T, Battaglia P, Pedà C, Consoli P, Andaloro F, Fossi MC (2015) First evidence of presence of plastic debris in stomach of large pelagic fish in the Mediterranean Sea. Mar Pollut Bull 95(1):358–361

    Article  CAS  Google Scholar 

  • Rummel CD, Loder MG, Fricke NF, Lang T, Griebeler EM, Janke M, Gerdts G (2016) Plastic ingestion by pelagic and demersal fish from the North Sea and Balthic Sea. Mar Pollut Bull 102(1):134–141

    Article  CAS  Google Scholar 

  • Sanchez W, Bender C, Porcher JM (2014) Wild gudgeons (Gobio gobio) from French rivers are contaminated by microplastic: preliminary study and first evidence. Environ Res 128:98–100

    Article  CAS  Google Scholar 

  • Santillo D, Miller K, Johnston P (2017) Microplastics as contaminants in commercially important seafood species. Integr Environ Assess Manag 13:516–521. https://doi.org/10.1002/ieam.1909

    Article  Google Scholar 

  • Schneider W (1990) FAO species identification sheets for fishery purposes. Field guide to the commercial marine resources of the Gulf of Guinea. Prepared and published with the support of the FAO Regional Office for Africa. FAO, Rome 268 pp

    Google Scholar 

  • Setala O, Flemig-Lehtinen V, Lehtinen M (2014) Ingestion and transfer of microplastic in the planktonik food web. Environ Pollut 185:77–83

    Article  CAS  Google Scholar 

  • Teuten EL, Saquing JM, Knappe DRU, Barlaz MA, Jonsson S, Björn A, Rowland SJ et al (2009) Transport and release of chemicals from plastics to the environment and to wildlife. Philos Trans R Soc B 364:2027–2045

    Article  CAS  Google Scholar 

  • Thevenon F, Carroll C, Sousa J (2014) Plastic debris in the ocean: the characterization of marine plastics and their environmental impacts. In: Situation analysis report. 52 IUCN, Gland. https://doi.org/10.2305/IUCN.CH.2014.03.en

  • Thompson RC, Moore C, vom Saal FS, Swan SH (2009) Plastics, the environment and human health: current consensus and future trends. Philos Trans R SocLond B 364:2153–2166

    Article  CAS  Google Scholar 

  • Tonay AM, Dede A, Oztürk AA, Oztürk B (2007) Stomach content of harbour porpoises (Phocoena phocoena) from the Turkish western Black Sea in spring and early summer. Rapp Commint Mer Mdit 38:616

    Google Scholar 

  • Tudela S, Palomera I (1997) Trophic ecology of the European anchovy Engraulis encrasicolus in the Catalan Sea (northwest Mediterranean). Mar Ecol Prog Ser 160:121–134

    Article  Google Scholar 

  • UNEP (2014) UNEP year book 2014. Emerging issues update. Chapter 8: plastic debris in the ocean. http://www.unep.org/yearbook/2014/PDF/chapt8.pdf. Accessed May 2018

  • Wegner A, Besseling E, Foekema EM, Kamermans P, Koelmans AA (2012) Effects of nanopolystyrene on the feeding behaviour of the blue mussel (Mytylus edulis L.). Environ Toxicol Chem 31:2490–3297

    Article  CAS  Google Scholar 

  • Whitehead PJP (1990) Clupeidae. In: Quero JC, Hureau JC, Karrer C, Post A, Saldanha L (eds) Check-list of the fishes of the eastern tropical Atlantic (CLOFETA), vol Vol. 1. JNICT, Lisbon; SEI, Paris; and UNESCO, Paris, pp 208–227

    Google Scholar 

  • Wieczorek AM, Morrison L, Croot PL, Allock AL, MacLoughlin E, Savard O, Brownlow H, Doyle TK (2018) Frequency of microplastics in mesopelagic fishes from the Northwest Atlantic. Front Mar Sci 5 article 39. https://doi.org/10.3389/fmars.2018.00039

  • Wright SL, Kelly FJ (2017) Plastic and human health: a micro issue? Environ Sci Technol 51(12):6634–6647

    Article  CAS  Google Scholar 

  • Wright SL, Thompson RC, Galloway TS (2013) The physical impacts of microplastics on marine organisms: a review. Environ Pollut 178:483–492

    Article  CAS  Google Scholar 

  • Zettler ER, Mincer TJ, Amaral-Zettler LA (2013) Life in the “Plastisphere”: microbial communities on plastic marine debris. Environ Sci Tecnol 47:7137–7146

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Sergio Pelosi and Gianfranco Pazienza for field assistance and support to the laboratory biometric measurements.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monia Renzi.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Renzi, M., Specchiulli, A., Blašković, A. et al. Marine litter in stomach content of small pelagic fishes from the Adriatic Sea: sardines (Sardina pilchardus) and anchovies (Engraulis encrasicolus). Environ Sci Pollut Res 26, 2771–2781 (2019). https://doi.org/10.1007/s11356-018-3762-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3762-8

Keywords

  • Marine litter
  • Microplastic
  • Plastic ingestion
  • Stomach content
  • Edible fish species
  • Human consumption