Abstract
Plastic pollution in terrestrial and freshwater environments and its accumulation along food chains has been poorly studied in birds. The Barn owl (Tyto alba) is an opportunistic and nocturnal apex predator feeding mostly on small mammals. In this note, we reported evidence of microplastics (MPs) contamination in Barn owl pellets collected, for the first time, in two sites with different levels of anthropization (low: natural landscape mosaic vs. high extensive croplands). The following polymers have been recorded: polyvinylchloride (PVC), polyethylene (PE), expanded polyester (EPS), polyethylene terephthalate (PET), polybutylene terephthalate (PBT), polyester (PL), viscose, and starch-based biopolymer. We found significant higher MPs frequency in the most anthropized site. Our results suggest that pellet’ analysis may represent a cost-effective method for monitoring MP contamination along food chains in terrestrial ecosystems.
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The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Acampora H, Berrow S, Newton S, O’Connor I (2017a) Presence of plastic litter in pellets from Great Cormorant (Phalacrocorax carbo) in Ireland. Mar Pollut Bull 117(1–2):512–514
Acampora H, Newton S, O’Connor I (2017b) Opportunistic sampling to quantify plastics in the diet of unfledged Black Legged Kittiwakes (Rissa tridactyla), Northern Fulmars (Fulmarus glacialis) and Great Cormorants (Phalacrocorax carbo). Mar Pollut Bull 119(2):171–174
Amori G, Contoli L, Nappi A (eds.) (2008) Mammalia II. Erinaceomorpha, Soricomorpha, Lagomorpha, Rodentia. Fauna d’Italia. Edizioni Calderini - Il Sole 24 ORE Business Media, Milano, XLIV
Avenant NL (2005) Barn Owl pellets: a useful tool for monitoring small mammal communities? Belg J Zool 135(supplement):39–43
Barreto S, Càceres-Medina S, Lambertucci SA (2023) High incidence of plastic debris in Andean condors from remote areas: evidence for marine-terrestrial trophic transfer. Envir Poll 317:120742
Battisti C (2020) Heterogeneous composition of anthropogenic litter recorded in nests of Yellow-legged gull (Larus michahellis) from a small Mediterranean island. Mar Pollut Bull 150:110682
Battisti C, Cignini B, Contoli L (1997) Geographical peninsular effects on the trophic system “Tyto alba – micromammals” in Salento (Italy). Hystrix 9(1–2):13–22
Battisti C, Dodaro G, Franco D (2014) The data reliability in ecological research: a proposal for a quick self-assessment tool. Natural History Sciences 1(2):75–79
Battisti C, Staffieri E, Poeta G, Sorace A, Luiselli L, Amori G (2019) Interactions between anthropogenic litter and birds: a global review with a ‘black-list’of species. Mar Poll Bull 138:93–114
Battisti C, Dodaro G, Di Bagno E, Amori G (2020) Small mammal assemblages in land-reclaimed areas: do historical soil use changes and recent anthropisation affect their dominance structure? Ethol Ecol Evol 32:282–288
Battisti C, Gallitelli L, Vanadia S, Scalici M (2023) General macro-litter as a proxy for fishing lines, hooks and nets entrapping beach-nesting birds: implications for clean-ups. Mar Poll Bull 186:114502
Bhatt V, Chauhan JS (2023) Microplastic in freshwater ecosystem: bioaccumulation, trophic transfer, and biomagnification. Environ Sc Poll Res 30:9389–9400
Binelli A, Pietrelli L, Di Vito S, Coscia L, Sighicelli M, Della Torre C, Parenti C, Magni S (2020) Hazard evaluation of plastic mixtures from four Italian subalpine great lakes on the basis of laboratory exposures of zebra mussels. Sci Total Environ 699:134366
Bontzorlos VA, Peris SJ, Vlachos CG, Bakaloudis DE (2005) The diet of barn owl in the agricultural landscapes of central Greece. Folia Zool 54:99–110
Borges-Ramírez MM, Escalona-Segura G, Huerta-Lwanga E, Iñigo-Elias E, Rendón-von Osten J (2021) Organochlorine pesticides, polycyclic aromatic hydrocarbons, metals and metalloids in microplastics found in regurgitated pellets of black vulture from Campeche. Mexico Sci Total Environ 801:149674
Bourdages MP, Provencher JF, Baak JE, Mallory ML, Vermaire JC (2021) Breeding seabirds as vectors of microplastics from sea to land: evidence from colonies in Arctic Canada. Sc Total Environ 764:142808
Brebu M, Vasile C, Antonie SR, Chiriac M, Precup M, Yang J, Roy C (2000) Study of the natural ageing of PVC insulation for electrical cables. Polymer Degr Stabil 67(2):209–221
Campanale C, Galafassi S, Savino I, Massarelli C, Ancona V, Volta P, Uricchio VF (2022) Microplastics pollution in the terrestrial environments: poorly known diffuse sources and implications for plants. Sci Total Environ 805:150431
Carlin J, Craig C, Little S, Donnelly M, Fox D, Zhai L, Walters L (2020) Microplastic accumulation in the gastrointestinal tracts in birds of prey in central Florida, USA. Environ Poll 264:114633. https://doi.org/10.1016/j.envpol.2020.114633
Celauro D, Battisti C (2006) Small mammal communities in a suburban agroforest landscape (Rome, Central Italy): faunal and ecological considerations using Tyto alba pellets. Aldrovandia 2:55–60
Cerasa M, Teodori S, Pietrelli L (2021) Searching nanoplastics: from sampling to sample processing. Polymers 13:3658. https://doi.org/10.3390/polym13213658
Chaline J, Baudvin H, Jammot D, Saint Girons MC (1974) Les proies des rapaces. Petits mammifères et leur environment. Doin, Paris
Contoli L (1975) Micro-mammals and environment in Central Italy: data from Tyto alba (Scop.) pellets. Ital J Zool 42(2–3):223–229
D’Souza JM, Windsor FM, Santillo D, Ormerod SJ (2020) Food web transfer of plastics to an apex riverine predator. Glob Change Biol 26(7):3846–3857
De la Peña NM, Butet A, Delettre Y, Paillat G, Morant P, Le Du L, Burel F (2003) Response of the small mammal community to changes in western French agricultural landscapes. Landsc Ecol 18:265–278
de Souza SS, Freitas ÍN, de Oliveira GS, da Luz TM, da Costa Araújo AP, Rajagopal R, Balasubramani G, Rahman MM, Malafaia G (2022) Toxicity induced via ingestion of naturally-aged polystyrene microplastics by a small-sized terrestrial bird and its potential role as vectors for the dispersion of these pollutants. J Hazard Mater 434:128814. https://doi.org/10.1016/j.jhazmat.2022.128814
Dell’Agnello F, Martini M, Mori E, Mazza G, Mazza V, Zaccaroni M (2020) Winter activity rhythms of a rodent pest species in agricultural habitats. Mamm Res 65:69–74
Denneman WD, Douben PE (1993) Trace metals in primary feathers of the barn owl (Tyto alba guttatus) in the Netherlands. Environm Poll 82(3):301–310
di Bagno E, Battisti C, Zullo F, Amori G (2020) Applying abundance/biomass comparison curves to small mammals: a weak tool for detect urbanization-related stress in the assemblages? Folia Oecol 47(1):10–15
Dytham C (2011) Choosing and using statistics: a biologist’s guide. John Wiley and Sons
English MD, Robertson GJ, Avery-Gomm S, Pirie-Hay D, Roul S, Ryan PC, Wilhelm SI, Mallory ML (2015) Plastic and metal ingestion in three species of coastal waterfowl wintering in Atlantic Canada. Mar Pollut Bull 98(1–2):349–353
Ferri V, Crescia P, Battisti C (2023) Discarded bottles entrap endemic small mammal species in a large Mediterranean island. Environ Sc Poll Res 30(19):57164–57173
Fisher DD (1984) House mouse populations and their damage to common building insulations. Dissertations & theses in natural resources, 218. University of Nebraska, Lincoln. https://digitalcommons.unl.edu/natresdiss/218
Fraticelli F, Burresi V, Damiano A, Giardina G, Maggi N, Manzia F, Tartari D, Gustin M (2021) Barn Owl Tyto alba in Italy: data from fauna recovery centers show a patchy decline. Avocetta 45(1):89–94
French SK, Giacinti JA, Robinson SJ, Pearl DL, Jardine CM (2022) The urban myth: A lack of agreement between definitions of urban environments used in wildlife health research may contribute to inconsistent epidemiological findings. Urban Ecosyst 25(3):999–1005
Gallitelli L, Battisti C, Pietrelli L, Scalici M (2022) Anthropogenic particles in coypu (Myocastor coypus; Mammalia, Rodentia)’faeces: first evidence and considerations about their use as track for detecting microplastic pollution. Environm Sc Poll Res 29(36):55293–55301
Gallitelli L, Battisti C, Scalici M (2023) Using social media to determine the global distribution of plastics in birds’ nests: the role of riverine habitats. Land 12(3):670
Gamarra-Toledo V, Plaza PI, Pen ̃YA, Bermejo PA, Lopez J, Cano GL, Borges-Ramírez MM, Escalona-Segura G, Huerta-Lwanga E, Iñigo-Elias E, Rendón-von Osten J (2021) Organochlorine pesticides, polycyclic aromatic hydrocarbons, metals and metalloids in microplastics found in regurgitated pellets of black vulture from Campeche, Mexico. Sc Total Environ 801:149674
Gil-Delgado JA, Guijarro D, Gosálvez RU, López-Iborra GM, Ponz A, Velasco A (2017) Presence of plastic particles in waterbirds faeces collected in Spanish lakes. Environ Poll 220:732–736
Hammer S, Nager RG, Johnson PCD, Furness RW, Provencher JF (2016) Plastic debris in great skua (Stercorarius skua) pellets corresponds to seabird prey species. Mar Poll Bull 103(1–2):206–210
Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electr 4(1):4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed Sept 2023
Heink U, Kowarik I (2010) What are indicators? On the definition of indicators in ecology and environmental planning. Ecol Indic 10:584–593
Herzke D, Anker-Nilssen T, Nøst TH, Götsch A, Christensen-Dalsgaard S, Langset M, Fangel K, Koelmans AA (2016) Negligible impact of ingested microplastics on tissue concentrations of persistent organic pollutants in northern fulmars off coastal Norway. Environ Sci Technol 50:1924–1933
Holland ER, Mallory ML, Shutler D (2016) Plastics and other anthropogenic debris in freshwater birds from Canada. Sc Total Environ 571:251–258
Horváth A, Morvai A, Horváth GF (2022) Difference in small mammal assemblages in the diet of the common barn-owl Tyto alba between two landscapes. Acta Zool Academ Scient Hung 68(2):189–216
Huang AC, Elliott JE, Hindmarch S, Lee SL, Maisonneuve F, Bowes V, Cheng KM, Martin K (2016) Increased rodenticide exposure rate and risk of toxicosis in barn owls (Tyto alba) from southwestern Canada and linkage with demographic but not genetic factors. Ecotoxicology 25:1061–1071
Hussain M, Imitiyaz I (2018) Urbanization concepts, dimensions and factors. Intern J Recent Scient Res 9(1):23513–23523
Janžekovič F, Klenovšek T (2020) The biogeography of diet diversity of barn owls on Mediterranean islands. J Biogeogr 47:2353–2361
Jin T, Tang J, Lyu H, Wang L, Gilmore AB, Schaeffer SM (2022) Activities of microplastics (MPs) in agricultural soil: a review of MPs pollution from the perspective of agricultural ecosystems. J Agric Food Chem 70:4182–4201
Jordan MJR (2005) Dietary analysis for mammals and birds: a review of field techniques and animal-management applications. Internat Zoo Yearb 39(1):108–116
Ksibi M (2006) Chemical oxidation with hydrogen peroxide for domestic wastewater treatment. Chem Eng J 119:161–165
Lampard E (1966) Historical aspects of urbanization. In: Hauser P, Schnore L (eds) The study of urbanization. John Wiley & Sons Inc, London, pp 519–554
Lechthaler S, Waldschläger K, Sandhani CG, Sannasiraj SA, Sundar V, Schwarzbauer J, Schüttrumpf H (2021) Baseline study on microplastics in Indian rivers under different anthropogenic influences. Water 13(12):1648
Leviner A, Perrine J (2023) Documentation of microplastics in the gastrointestinal tracts of terrestrial raptors in central California, USA. Calif Fish Wildl J 109(2):e06. https://doi.org/10.51492/cfwj.109.6
Lovari S, Renzoni A, Fondi R (1976) The predatory habits of the barn owl (Tyto alba, Scopoli) in an area of central Italy. Le Gerfaut 67:25–234
Love AR, Webon C, Glue DE, Harris S, Harris S (2000) Changes in the food of British Barn owls (Tyto alba) between 1974 and 1997. Mammal Rev 30:107–129
Lusher AL, Provencher JF, Baak JE, Hamilton BM, Vorkamp K, Hallanger IG, Pijogge L, Liboiron M, Bourdages MPT, Hammer S, Gavrilo M, Vermaire JC, Linnebjerg JF, Mallory ML, Gabrielsen GW (2022) Monitoring litter and microplastics in Arctic mammals and birds. Arctic Science 8(4):1217–1235
Malizia A, Monmany-Garzia AC (2019) Terrestrial ecologists should stop ignoring plastic pollution in the Anthropocene time. Sc Tot Environ 668:1025–1029
Meek WR, Burman PJ, Sparks TH, Nowakowski M, Burman NJ (2012) The use of Barn Owl Tyto alba pellets to assess population change in small mammals. Bird Study 59(2):166–174
Merlino S, Abbate M, Pietrelli L, Canepa P, Varella P (2018) Marine litter detection and correlation with the seabird nest content. Rendiconti Lincei 29(4):867–875
Mikkola H (1983) Owls of Europe. T & AD Poyser, Calton
Milana G, Battisti C, Luiselli L, Amori G (2019) Altitudinal variation of community metrics in Italian small mammal assemblages as revealed by Barn Owl (Tyto alba) pellets. Zoolog Anzeiger 281:11–15
Nessi A, Winkler A, Tremolada P, Saliu F, Lasagni M, Ghezzi LLM, Balestrieri A (2022) Microplastic contamination in terrestrial ecosystems: a study using barn owl (Tyto alba) pellets. Chemosphere 308:136281
Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conserv Biol 4:355–364
Pietrelli L (2022) Polypropylene recovery and recycling from mussel nets. Polymers 14:3469
Prata JC, da Costa JP, Lopes I, Andrady AL, Duarte AC, Rocha-Santos T (2021) A One Health perspective of the impacts of microplastics on animal, human and environmental health. Sc Total Environ 777:146094. https://doi.org/10.1016/j.scitotenv.2021.146094
Prete S, Battisti C, Marini F, Ciucci P (2012) Applying abundance/biomass comparisons on a small mammal assemblage from Barn owl (Tyto alba) pellets (Mount Soratte, central Italy): a cautionary note. Rendiconti Lincei 23:349–354
Provencher JF, Borrelle SB, Bond AL, Lavers JL, Van Franeker JA, Kühn S, Hammer S, Avery-Gomm S, Mallory ML (2019) Recommended best practices for plastic and litter ingestion studies in marine birds: collection, processing, and reporting. Facets 4(1):111–130
Provencher JF, Covernton GA, Moore RC, Horn DA, Conkle JL, Lusher AL (2020) Proceed with caution: the need to raise the publication bar for microplastics research. Sc Total Environm 748:141426
Reynolds C, Ryan PG (2018) Micro-plastic ingestion by waterbirds from contaminated wetlands in South Africa. Mar Pollut Bull 126:330–333
Richard FJ, Gigauri M, Bellini G, Rojas O, Runde A (2021) Warning on nine pollutants and their effects on avian communities. Glob Ecol Conserv 32:e01898
Romano B, Zullo F (2014) Land urbanization in Central Italy: 50 years of evolution. J Land Use Sc 2:143–164
Ryan PG, Fraser MW (1988) The use of Great Skua pellets as indicators of plastic pollution in seabirds. Emu 88(1):16–19
Sarkar S, Diab H, Thompson J (2023) Microplastic pollution: chemical characterization and impact on wildlife. Int J Environ Res Public Health 20:1745. https://doi.org/10.3390/ijerph20031745
Schutten K, Chandrashekar A, Bourdages M, Bowes V, Elliott J, Lee S, Redford T, Provencher J, Jardine C, Wilson L (2023) Assessing plastic ingestion in birds of prey from British Columbia, Canada. Environ Sc Poll Res 30:76631–76639
Sherlock C, Fernie KJ, Munno K, Provencher J, Rochman C (2022) The potential of aerial insectivores for monitoring microplastics in terrestrial environments. Sc Total Environ 807:150453
Shumake SA, Thompson RD, Caudill CJ (1972) Taste preference behavior of laboratory vs wild Norway rats. J Colorado-Wyoming Acad Sc 7:108–109
Sidorov GN, Putin AV (2010) The house mouse (Mus musculus L.) in Omsk educational institutions: seasonal migration, abundance, reproduction, distribution, foraging, and associated damage. Contemp Probl Ecol 3:601–605
Terepocki AK, Brush AT, Kleine LU, Shugart GW, Hodum P (2017) Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Ardenna grisea). Mar Pollut Bull 116(1–2):143–150
Thrift E, Porter A, Galloway TS, Coomber FG, Mathews F (2022) Ingestion of plastics by terrestrial small mammals. Sc Tot Environ 842:156679
Winkler A, Nessi A, Antonioli D, Laus M, Santo N, Parolini M, Tremolada P (2020) Occurrence of microplastics in pellets from the common kingfisher (Alcedo atthis) along the Ticino River, North Italy. Environ Sc Poll Res 27:41731–41739
Yom-Tov Y, Wool D (1997) Do the contents of barn owl pellets accurately represent the proportion of prey species in the field? The Condor 99(4):972–976
Zhao S, Zhu L, Li D (2016) Microscopic anthropogenic litter in terrestrial birds from Shanghai, China: not only plastics but also natural fibers. Sc Tot Environ 550:1110–1115
Ziccardi LM, Edgington A, Hentz K, Kulacki KJ, Kane Driscoll S (2016) Microplastics as vectors for bioaccumulation of hydrophobic organic chemicals in the marine environment: a state-of-the-science review. Environ Toxicol Chem 35(7):1667–1676
Acknowledgements
The owl’s pellet collection was carried out during the LIFE GREENCHANGE (“Green Infrastructure for increasing biodiversity in Agro Pontino and Maltese rural areas;” LIFE17 NAT/IT/000619) and was included in NBFC, funded by the Italian Ministry of University and Research, PNRR, Missione 4 Componente 2, “Dalla ricerca all’impresa”, Investimento 1.4, Project CN00000033. We thank: the Caetani Foundation and the “Gelasio Caetani” farm for allowing us access to the pellets collection sites; Giovanni Mastrobuoni, Simonetta Dario and Giampaolo Matricaria for helping us in the fieldwork. We would also like to thank two anonymous reviewers and the Editor (Philippe Garrigues): their useful comments and suggestions have largely improved the first and the second draft of the manuscript.
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All authors contributed to the study conception and design. Data collection and pellet analysis were performed by GD, IP, and CB; chemical analysis was performed by LP and PM. CC and MS checked for the last version. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Pietrelli, L., Dodaro, G., Pelosi, I. et al. Microplastic in an apex predator: evidence from Barn owl (Tyto alba) pellets in two sites with different levels of anthropization. Environ Sci Pollut Res 31, 33155–33162 (2024). https://doi.org/10.1007/s11356-024-33637-8
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DOI: https://doi.org/10.1007/s11356-024-33637-8