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Anthropogenically altered trophic webs: alien catfish and microplastics in the diet of Eurasian otters

  • Giorgio SmiroldoEmail author
  • Alessandro Balestrieri
  • Elena Pini
  • Paolo Tremolada
Original Paper
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Abstract

With the aim of examining how Eurasian otters (Lutra lutra) face human-mediated environmental alterations, we assessed their diet by spraint analysis on the River Ticino (NW Italy), where this mustelid has been reintroduced in 1997. From March 2016 to March 2017, a total of 101 spraints was found in 50% of 32 sampling stations (mean length ± SD = 567 ± 263 m). Fish formed the bulk of otter diet (95% of the estimated mean percent volume, mV%). Cyprinids were the most preyed fish (mV% = 44.9), followed by European catfish Silurus glanis (mV% = 24.9%) and eel Anguilla anguilla (mV% = 8.5). Introduced European catfish is an invasive species, which can deeply alter the composition and structure of local fish communities and accumulate large amounts of metals and pollutants through the trophic chain. We also recorded for the first time microplastic particles (< 5 mm) in otter spraints. Suspected particles were analysed by Fourier transform infrared (FTIR) spectroscopy and two polymer types were identified: polyethylene terephthalate (PET) and polyamide (PA). Although otters showed to be able to adapt to anthropogenic changes, these results point out new potential threats to otter conservation and ask for further studies.

Keywords

Lutra lutra Marking activity Reintroduction Silurus glanis Endangered species 

Notes

Acknowledgements

We are very grateful to Fondazione Fratelli Confalonieri for having granted the Ph.D. fellowship of GS. We thank V. Parco, A. Bellani, C. Poma (Park of the Ticino Valley) and P. Trovò (Natural Park of the Ticino Valley). A. Nessi and M. Cavenago (University of Milan) helped with field work and FTIR analyses, respectively, for their degree theses. Thanks also to S.J. Lovejoy for language editing.

References

  1. Anderson JC, Park BJ, Palace VP (2016) Microplastics in aquatic environments: implications for Canadian ecosystems. Environ Pollut 218:269e280CrossRefGoogle Scholar
  2. Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62:1596e1605CrossRefGoogle Scholar
  3. Arthur C, Baker J, Bamford H (2009) Proceedings of the international research workshop on the occurrence, effects and fate of microplastic marine debris. NOAA Technical Memorandum NOS- OR & R-30.NOAA, Silver Spring, U.S., September 9-11, 2008Google Scholar
  4. Bakir A, Rowland SJ, Thompson RC (2012) Competitive sorption of persistent organic pollutants onto microplastics in the marine environment. Mar Pollut Bull 64:2782–2789CrossRefGoogle Scholar
  5. Balestrieri A, Remonti L, Vezza P, Prigioni C, Copp GH (2013) Do non-native fish as prey favour the conservation of the threatened indigenous Eurasian otter? Freshw Biol 58:995–1007CrossRefGoogle Scholar
  6. Balestrieri A, Remonti L, Prigioni C (2016) Towards extinction and back: decline and recovery of otter populations in Italy. In: Angelici FM (ed) Problematic wildlife Springer International Publishing, Switzerland, pp 91–105Google Scholar
  7. Barbar F, Hiraldo F, Lambertucci SA (2016) Medium-sized exotic prey create novel food webs: the case of predators and scavengers consuming lagomorphs. PeerJ 4:e2273.  https://doi.org/10.7717/peerj.2273 CrossRefGoogle Scholar
  8. Barnes DK, 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 364:1985–1998CrossRefGoogle Scholar
  9. Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23CrossRefGoogle Scholar
  10. Beja R (1996) An analysis of otter Lutra lutra predation on introduced American crayfish Procambarus clarkii in Iberian streams. J Appl Ecol 33:1156–1170CrossRefGoogle Scholar
  11. Birks J (2015) Polecats. The British Natural History Collection Vol. 5, Whittet Books Ltd, Stansted, EssexGoogle Scholar
  12. Brooks TM, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Rylands AB, Konstant WR, Flick P, Pilgrim J (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16:909–923CrossRefGoogle Scholar
  13. Browne MA, Crump P, Niven SJ, Teuten EL, Tonkin A, Galloway T, Thompson RC (2011) Accumulations of microplastic on shorelines worldwide: sources and sinks. Environ Sci Technol 45:9175–9179CrossRefGoogle Scholar
  14. C.N.R.-I.S.E (2016) Ricerche sull'evoluzione del Lago Maggiore. Aspetti limnologici. Programma triennale 2013-2015. Campagna 2015 e Rapporto triennale 2013-2015. Commissione Internazionale per la protezione delle acque italo-svizzereGoogle Scholar
  15. Camby A, Le Gall O, Maizeret C (1984) Atlas d'identification des restes alimentaires de la Loutre (premiers elements). Groupe Loutres, Bulletin de Liaison, n 16Google Scholar
  16. Castañeda RA, Avlijas S, Simard MA, Ricciardi A (2014) Microplastic pollution in St. Lawrence river sediments. Can J Fish Aquat Sci 71:1767e1771CrossRefGoogle Scholar
  17. Clavero M, Prenda J, Delibes M (2003) Trophic diversity of the otter (Lutra lutra L.) in temperate and Mediterranean freshwater habitats. J Biogeogr 30(5):761–769CrossRefGoogle Scholar
  18. Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bull 62:2588e2597CrossRefGoogle Scholar
  19. Contesse P, Hegglin D, Gloor S, Bontadina F, Deplazes P (2004) The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich, Switzerland. Mamm Biol 69:81–95CrossRefGoogle Scholar
  20. Crooks JA, Chang AL, Ruiz GM (2011) Aquatic pollution increases the relative success of invasive species. Biol Invasions 13:165–176CrossRefGoogle Scholar
  21. De Rivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376CrossRefGoogle Scholar
  22. Consorzio del Ticino, Parco Ticino (2016) Ente di gestione delle aree protette del Ticino e del Lago Maggiore. Il Fiume Ticino riqualificazione e valorizzazione del corridoio ecologico. Italgrafica NovaraGoogle Scholar
  23. Derraik JGB (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44:842–852CrossRefGoogle Scholar
  24. Di Palma MG, Massa B (1981) Contributo metodologico per lo studio dell'alimentazione dei rapaci. Atti I Conv ital Orn, Aulla, pp 69–76Google Scholar
  25. Dorresteijn I, Schultner J, Nimmo DG, Fischer J, Hanspach J, Kuemmerle T, Kehoe L, Ritchie EG (2015) Incorporating anthropogenic effects into trophic ecology: predator–prey interactions in a human-dominated landscape. Proc R Soc B 282:20151602CrossRefGoogle Scholar
  26. Dotti N, Genoni P, Paleari M, Tremolada L (2014) Stato delle acque superficiali bacino del fiume Ticino e lago maggiore. ARPA Lombardia, MilanoGoogle Scholar
  27. Eerkes-Medranoa D, Thompson RC, Aldridgea DC (2015) Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res 75:63–82CrossRefGoogle Scholar
  28. Elvira B (2001) Identification of non-native freshwater fishes established in Europe and assessment of their potential threats to the biological diversity. Convention on the conservation of European wildlife and natural habitats, Strasbourg, 11 December 2000 T-PVS: 6Google Scholar
  29. Engler RE (2012) The complex interaction between marine debris and toxic chemicals in the ocean. Environ Sci Technol 46:12302e12315CrossRefGoogle Scholar
  30. Eriksen M, Mason S, Wilson S, Box C, Zellers A, Edwards W, Farley H, Amato S (2013) Microplastic pollution in the surface waters of the Laurentian Great Lakes. Mar Pollut Bull 77:177e182CrossRefGoogle Scholar
  31. Eriksson C, Burton H (2003) Origins and biological accumulation of small plastic particles in fur seals from Macquarie Island Ambio 32:380e384Google Scholar
  32. Feinsinger P, Spers EE, Poole RW (1981) A simple measure of niche breadth. Ecology 62:27–32CrossRefGoogle Scholar
  33. Foekema EM, De Gruijter C, Mergia MT, van Franeker JA, Murk AJ, Koelmans AA (2013) Plastic in north sea fish. Environ Sci Technol 47:8818–8824CrossRefGoogle Scholar
  34. Foley JA, DeFries R, Asner GP, Barford C et al (2005) Global consequences of land use. Science 309:570–574CrossRefGoogle Scholar
  35. Fossi MC, Coppola D, Baini M, Giannetti M, Guerranti C, Marsili L, Panti C, De Sabata E, Clò S (2014) Large filter feeding marine organisms as indicators of microplastic in the pelagic environment: the case studies of the Mediterranean basking shark (Cetorhinus maximus) and fin whale (Balaenoptera physalus). Mar Environ Res.  https://doi.org/10.1016/j.marenvres.2014.02.002
  36. Gobas FAPC, Zhang X, Wells R (1993) Gastrointestinal magnification: the mechanism of biomagnification and food chain accumulation of organic chemicals. Environ Sci Technol 27:2855–2863CrossRefGoogle Scholar
  37. GRAIA (1999) Ricerca sulla fauna ittica del fiume Ticino. Parco Ticino e Castalia, pp 108Google Scholar
  38. GRAIA (2007) Il siluro Silurus glanis. Ecologia della specie nel Fiume Ticino e risultati dell’azione di contrasto alla sua espansione svolta dal Parco negli anni 2001 – 2006. Consorzio Parco Lombardo della Valle del Ticino Pontevecchio di Magenta (MI)Google Scholar
  39. Haberl H, Erb KH, Krausmann F, Gaube V, Bondeau A, Plutzar C, Gingrich S, Lucht W, Fischer-Kowalski M (2007) Quantifying and mapping the human appropriation of net primary production in earth’s terrestrial ecosystems. Proc Natl Acad Sci U S A 104:12942–12947CrossRefGoogle Scholar
  40. Hanski I (2011) Habitat loss, the dynamics of biodiversity, and a perspective on conservation. AMBIO 40:248–255CrossRefGoogle Scholar
  41. Holmes LA, Turner A, Thompson RC (2014) Interactions between trace metals and plastic production pellets under estuarine conditions. Mar Chem 167:25e32CrossRefGoogle Scholar
  42. Ivar do Sul JA, Costa MF (2014) The present and future of microplastic pollution in the marine environment. Environ Pollut 185:352–364CrossRefGoogle Scholar
  43. Kloskowski J, Rechulicz J, Jarzynowa B (2013) Resource availability and use by Eurasian otters Lutra lutra in a heavily modified river-canal system. Wildl Biol 19:439–451CrossRefGoogle Scholar
  44. Kranz A, Toman A (2000) Otters recovering in man-made habitats in central Europe. In: Griffiths HI (ed) Mustelids in a modern world. Bachhuys Publishers, Leiden, pp 163–184Google Scholar
  45. Kruuk H (2006) Wild otters. Ecology, behaviour and conservation. Oxford University Press, OxfordGoogle Scholar
  46. Kruuk H, Parish T (1981) Feeding specialization of the European badger (Meles meles) in Scotland. J Anim Ecol 50:773–788CrossRefGoogle Scholar
  47. Kruuk H, Conroy WH, Glimmerveenl U, Ouwerkerk EJ (1986) The use of spraints to survey populations of otters Lutra lutra. Biol Conserv 35:187–194CrossRefGoogle Scholar
  48. Lambertucci SA, Trejo A, Di Martino S, Sánchez-Zapata JA, Donázar JA, Hiraldo F (2009) Spatial and temporal patterns in the diet of the Andean condor: ecological replacement of native fauna by exotic species. Anim Conserv 12:338–345CrossRefGoogle Scholar
  49. Leprieur F, Brosse S, Garcıa-Berthou E, Oberdorff T, Olden JD, Townsend CR (2009) Scientific uncertainty and the assessment of risks posed by non-native freshwater fishes. Fish 10:88–97Google Scholar
  50. Lima SL (2002) Putting predators back into behavioural predator-prey interactions. Trends Ecol Evol 7:70–75CrossRefGoogle Scholar
  51. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  52. Lusher AL, McHugh M, Thompson RC (2013) Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar Pollut Bull 67:94–99CrossRefGoogle Scholar
  53. Macdonald SM, Mason CF (1983) The otter Lutra lutra in Southern Italy. Biol Conserv 25:95–101CrossRefGoogle Scholar
  54. Mahon AM, Officer RA, Nash R, O’Connor I (2017) Scope, fate, risks and impacts of microplastic pollution in Irish freshwater systems. Epa Research Programme 2014–2020Google Scholar
  55. Marr SM, Marchetti MP, Olden JD, García-Berthou E, Morgan DL, Arismendi I, Day JA, Griffiths CL, Skelton PH (2010) Freshwater fish introductions in Mediterranean-climate regions: are there commonalities in the conservation problem? Divers Distrib 16:606–619CrossRefGoogle Scholar
  56. McCormick A, Hoellein TJ, Mason S, Schluep J, Kelly JJ (2014) Microplastic is an abundant and distinct microbial habitat in an urban river. Environ Sci Technol 48:11863–11871CrossRefGoogle Scholar
  57. McMahon CR, Holley D, Robinson S (1999) The diet of itinerant male Hooker’s sea lions, Phocarctos hookeri, at sub-Antarctic Macquarie Island. Wildl Res 26:839e846CrossRefGoogle Scholar
  58. Mintenig SM, Int-Veen I, Loder MGJ, Primpke S, Gerdts G (2017) Identification of microplastic in effluents of waste water treatment plants using focal plane array-based micro-Fourier-transform infrared imaging. Water Res 108:365–372CrossRefGoogle Scholar
  59. Montanari M, Boffino G (2000) Il ritorno della Lontra. 1990–2000, il progetto di reintroduzione nel Parco Naturale della Valle del Ticino Piemontese. Parco Ticino Piemontese e Regione PiemonteGoogle Scholar
  60. Moyle PB (1986) Fish introductions into North America: patterns and ecological impact. In: Mooney HA, Drake JA (eds) Ecology of biological invasion of North America and Hawaii. Springer-Verlag, New York, pp 27–43CrossRefGoogle Scholar
  61. Muhly TB, Hebblewhite M, Paton D, Pitt JA, Boyce MS, Musiani M (2013) Humans strengthen bottom-up effects and weaken trophic cascades in a terrestrial food web. PLoS One 8:e64311CrossRefGoogle Scholar
  62. Newsome TM, Dellinger JA, Pavey CR, Ripple WJ, Shores CR, Wirsing AJ, Dickman CR (2014) The ecological effects of providing resource subsidies to predators. Glob Ecol Biogeogr 24:1–11CrossRefGoogle Scholar
  63. Pintor LM, Byers JE (2015) Do native predators benefit from non-native prey. Ecol Lett 18:1174–1180CrossRefGoogle Scholar
  64. Prigioni C (1986) La lontra in Lombardia e nelle province di Asti, Alessandria, Parma e Piacenza. In: Cassola F (ed), La Lontra in Italia. Serie Atti e Studi no 5, WWF-Italia, Roma, pp 25–28Google Scholar
  65. Prigioni C (1997) La lontra. Una vita silenziosa negli ambienti acquatici. Edagricole, BolognaGoogle Scholar
  66. Prigioni C, Balestrieri A (2011) Piano di monitoraggio dei Vertebrati terrestri di interesse comunitario (Direttive 79/409/CEE e 92/43/CEE) in Lombardia – Lontra Lutra lutra. Technical report, University of Pavia, ItalyGoogle Scholar
  67. Prigioni C, Pandolfi M, Grimod I, Fumagalli R, Santolini R, Arcá G, Montemurro F, Bonacoscia M, Racana A (1991) The otter in five Italian rivers - first report. Habitat 6:143–145Google Scholar
  68. Prigioni C, Remonti L, Balestrieri A, Sgrosso S, Priore G, Misin CE, Viapiana M, Spada S, Anania R (2005) Distribution and sprainting activity of the otter (Lutra lutra) in the Pollino National Park (Southern Italy). Ethol Ecol Evol 17:171–180CrossRefGoogle Scholar
  69. Prigioni C, Balestrieri A, Remonti L, Gargaro A, Priore G (2006a) Diet of the Eurasian otter (Lutra lutra) in relation to freshwater habitats and alien fish species in southern Italy. Ethol Ecol Evol 18:307–320CrossRefGoogle Scholar
  70. Prigioni C, Balestrieri A, Remonti L, Sgrosso S, Priore G (2006b) How many otters are there in Italy? Hystrix 17:29–36Google Scholar
  71. Prigioni C, Balestrieri A, Remonti L (2007) Decline and recovery in otter Lutra lutra populations in Italy. Mammal Rev 37:71–79CrossRefGoogle Scholar
  72. Prigioni C, Smiroldo G, Remonti L, Balestrieri A (2009) Distribution and diet of reintroduced otters (Lutra lutra) on the River Ticino (NW Italy). Hystrix 20:45–53Google Scholar
  73. Puzzi CM, Trasforini S, Casoni A, Bardazzi MA (2007) Specie Invasive: il siluro Silurus glanis. Consorzio Parco Lombardo della Valle del Ticino, MagentaGoogle Scholar
  74. Puzzi CM, Trasforini S, Sartorelli M, Tamborini D (2014) Ricostituzione e monitoraggio del corridoio ecologico fluviale del Ticino per specie ittiche di importanza conservazionistica. In: Casale F, Sala D, Bellani A (eds), Il patrimonio faunistico del Parco del Ticino negli anni 2000. Parco Lombardo della Valle del Ticino e Fondazione Lombardia per l’Ambiente, pp 119–127Google Scholar
  75. Radeloff VC, Hammer RB, Stewart SI, Fried JS, Holcomb SS, Mckeefry JF (2005) The wildland-urban interface in the United States. Ecol Appl 15:799–805CrossRefGoogle Scholar
  76. Remonti L, Prigioni C, Balestrieri A, Sgrosso S, Priore G (2008) Trophic flexibility of the otter (Lutra lutra) in southern Italy. Mamm Biol 73:293–302CrossRefGoogle Scholar
  77. Reuther C, Dolch D, Green R, Jahrl J, Jefferies D, Krekemeyer A, Kucerova M, Madsen AB, Romanowski J, Roche K, Ruiz-Olmo J, Teubner J, Trindade A (2000) Surveying and monitoring distribution and population trends of the Eurasian otter (Lutra lutra). Habitat 12:1–152Google Scholar
  78. Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939CrossRefGoogle Scholar
  79. Roos A, Loy A, de Silva A, Hajkova P, Zemanová B (2015) Lutra lutra. The IUCN Red List of Threatened Species 2015. e.T12419A21935287.  https://doi.org/10.2305/IUCN.UK.2015- 2.RLTS.T12419A21935287.en. Downloaded on 10 Aug 2018
  80. Schlaepfer MA, Sax DF, Olden JD (2011) The potential conservation value of non-native species. Conserv Biol 25:428–437CrossRefGoogle Scholar
  81. Setälä O, Fleming-Lehtinen V, Lehtiniemi M (2014) Ingestion and transfer of microplastics in the planktonic food web. Environ Pollut 185:77–83CrossRefGoogle Scholar
  82. Smiroldo G, Balestrieri A, Remonti L, Prigioni C (2009) Seasonal and habitat-related variation of otter Lutra lutra diet in a Mediterranean river catchment (Italy). Folia Zool 58:87–97Google Scholar
  83. Squadrone S, Prearo M, Brizio P, Gavinelli S, Pellegrino M, Scanzio T, Guarise S, Benedetto A, Abete MC (2012) Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian Rivers. Chemosphere.  https://doi.org/10.1016/j.chemosphere.2012.07.028
  84. Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174CrossRefGoogle Scholar
  85. Tanaka K, Takada H, Yamashita R, Mizukawa K, Fukuwaka MA, Watanuki Y (2013) Accumulation of plastic derived chemicals in tissues of seabirds ingesting marine plastics. Mar Pollut Bull 69:219e222CrossRefGoogle Scholar
  86. Tetzlaff JC, Roth BM, Weidel BC, Kitchell JF (2010) Predation by native sunfishes (Centrarchidae) on the invasive crayfish Orconectes rusticus in four northern Wisconsin lakes. Ecol Freshw Fish 20:133–143CrossRefGoogle Scholar
  87. Volta P, Tremolada P, Neri MC, Giussani G, Galassi S (2009) Age-dependent bioaccumulation of organochlorine compounds in fish and their selective biotransformation in top predators from Lake Maggiore (Italy). Water Air Soil Pollut 197:193–209CrossRefGoogle Scholar
  88. Webb JB (1976) Otter spraint analysis. The Mammal Society, Reading, UKGoogle Scholar
  89. Wierzbowska IA, Almeida A, Sanches J, Widera E, Gaspar G, Gajda A (2017) Mustelids in the city – case studies of urban adapters. 32nd European Mustelid Colloquium, 15-17 November 2017, Lyon, FranceGoogle Scholar
  90. Wise MH (1980) The use of fish vertebrae in scats for estimating prey size of otters and mink. J Zool (Lond) 195:181–213CrossRefGoogle Scholar
  91. Yirga G, de Iongh HH, Leirs H, Gebrihiwot K, Deckers J, Bauer H (2012) Adaptability of large carnivores to changing anthropogenic food sources: diet change of spotted hyena (Crocuta crocuta) during Christian fasting period in northern Ethiopia. J Anim Ecol 81:1052–1055CrossRefGoogle Scholar
  92. Yonkos LT, Friedel EA, Perez-Reyes AC, Ghosal ACD (2014) Microplastics in four estuarine rivers in the Chesapeake Bay, U.S.A. Environ Sci Technol 48:14195–14202CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2019

Authors and Affiliations

  • Giorgio Smiroldo
    • 1
    Email author
  • Alessandro Balestrieri
    • 1
  • Elena Pini
    • 2
  • Paolo Tremolada
    • 1
  1. 1.Department of Environmental Science and PolicyUniversity of MilanMilanItaly
  2. 2.Department of Pharmaceutical Sciences – Section of General and Organic Chemistry “A.Marchesini”University of MilanMilanItaly

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