Ingestion of microplastics by freshwater Tubifex worms

Department of Geography, The University of Manchester, Manchester, M13 ... Tubifex worms are one of the most abundant invertebrates in freshwater syst...
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Ingestion of microplastics by freshwater Tubifex worms Rachel R Hurley, Jamie C Woodward, and James J. Rothwell Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03567 • Publication Date (Web): 11 Oct 2017 Downloaded from http://pubs.acs.org on October 13, 2017

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Ingestion of microplastics by freshwater Tubifex

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worms

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Rachel R. Hurley*, Jamie C. Woodward, James J. Rothwell

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Department of Geography, The University of Manchester, Manchester, M13 9PL, United

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Kingdom

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ABSTRACT: Microplastic contamination of the aquatic environment is a global issue.

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Microplastics can be ingested by organisms leading to negative physiological impacts. The

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ingestion of microplastics by freshwater invertebrates has not been reported outside the

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laboratory. Here we demonstrate the ingestion of microplastic particles from bottom sediments

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by Tubifex tubifex in a major urban waterbody fed by the River Irwell, Manchester, UK. The host

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sediments had microplastic concentrations ranging from 56 to 2544 particles kg-1. 87% of the

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Tubifex-ingested microplastic particles were microfibres (55 - 4100 µm in length), whilst the

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remaining 13% were microplastic fragments (50 - 4500 µm in length). FT-IR analysis revealed

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ingestion of a range of polymers, including polyethylene terephthalate (polyester) and acrylic

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fibres. Whilst microbeads were present in the host sediment matrix, they were not detected in

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Tubifex worm tissue. The mean concentration of ingested microplastics was 129 ± 65.4 particles

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g-1 tissue. We also show that Tubifex worms retain microplastics longer than other components

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of the ingested sediment matrix. Microplastic ingestion by Tubifex worms poses a significant risk

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for trophic transfer and biomagnification of microplastics up the aquatic food chain.

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TEXT:

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Introduction

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Microplastics represent a global environmental problem1. Defined as small ( 0.34). This was the case within and across sites. There was no significant

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correlation between the size (length or mass) of worms and the number or size of microplastics

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ingested (Pearson’s: p > 0.20). This indicates that there is limited selectivity in the ingestion of

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microplastic particles within fragments or fibres.

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No microbeads were identified in the Tubifex worm tissue (302 worms in total). This strongly

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suggests that microbeads are not ingested by Tubifex worms in the Salford Quays. Selective

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feeding by T. tubifex has been reported by Rodriguez et al.33. A size selectivity of sediments 100 µm) are translocated to organs of the tropical fiddler crab

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Uca rapax. Mar. Pollut. Bull. 2015, 96 (1–2), 491–495.

417 418 419 420 421 422

(11) Farrell, P.; Nelson, K. Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environ. Pollut. 2013, 177, 1–3. (12) Van Cauwenberghe, L.; Janssen, C. R. Microplastics in bivalves cultured for human consumption. Environ. Pollut. 2014, 193, 65–70. (13) Li, J.; Yang, D.; Li, L.; Jabeen, K.; Shi, H. Microplastics in commercial bivalves from China. Environ. Pollut. 2015, 207, 190–195.

423

(14) Galloway, T. S. Micro- and Nano-plastics and Human Health. In Marine Anthropogenic

424

Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer International Publishing,

425

2015; pp 343–366.

426

(15) Sanchez, W.; Bender, C.; Porcher, J.-M. Wild gudgeons (Gobio gobio) from French rivers

427

are contaminated by microplastics: Preliminary study and first evidence. Environ. Res.

428

2014, 128, 98–100.

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Environmental Science & Technology

Page 26 of 38

429

(16) Peters, C. A.; Bratton, S. P. Urbanization is a major influence on microplastic ingestion by

430

sunfish in the Brazos River Basin, Central Texas, USA. Environ. Pollut. 2016, 210, 380–

431

387.

432 433

(17) Phillips, M. B.; Bonner, T. H. Occurrence and amount of microplastic ingested by fishes in watersheds of the Gulf of Mexico. Mar. Pollut. Bull. 2015, 100 (1), 264–269.

434

(18) Jabeen, K.; Su, L.; Li, J.; Yang, D.; Tong, C.; Mu, J.; Shi, H. Microplastics and

435

mesoplastics in fish from coastal and fresh waters of China. Environ. Pollut. 2017, 221,

436

141–149.

437

(19) Biginagwa, F. J.; Mayoma, B. S.; Shashoua, Y.; Syberg, K.; Khan, F. R. First evidence of

438

microplastics in the African Great Lakes: Recovery from Lake Victoria Nile perch and

439

Nile tilapia. J. Gt. Lakes Res. 2016, 42 (1), 146–149.

440

(20) Van Cauwenberghe, L.; Claessens, M.; Vandegehuchte, M. B.; Janssen, C. R.

441

Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina)

442

living in natural habitats. Environ. Pollut. 2015, 199, 10–17.

443

(21) Besseling, E.; Wegner, A.; Foekema, E. M.; van den Heuvel-Greve, M. J.; Koelmans, A.

444

A. Effects of Microplastic on Fitness and PCB Bioaccumulation by the Lugworm

445

Arenicola marina (L.). Environ. Sci. Technol. 2013, 47 (1), 593–600.

446 447

(22) Wright, S. L.; Rowe, D.; Thompson, R. C.; Galloway, T. S. Microplastic ingestion decreases energy reserves in marine worms. Curr. Biol. 2013, 23 (23), R1031–R1033.

448

(23) Huerta Lwanga, E.; Gertsen, H.; Gooren, H.; Peters, P.; Salánki, T.; van der Ploeg, M.;

449

Besseling, E.; Koelmans, A. A.; Geissen, V. Microplastics in the Terrestrial Ecosystem:

450

Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environ. Sci. Technol.

451

2016, 50 (5), 2685–2691.

ACS Paragon Plus Environment

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Page 27 of 38

Environmental Science & Technology

452

(24) Rodriguez-Seijo, A.; Lourenço, J.; Rocha-Santos, T. A. P.; da Costa, J.; Duarte, A. C.;

453

Vala, H.; Pereira, R. Histopathological and molecular effects of microplastics in Eisenia

454

andrei Bouché. Environ. Pollut. 2017, 220, Part A, 495–503.

455

(25) Hodson, M. E.; Duffus-Hodson, C. A.; Clark, A.; Prendergast-Miller, M. T.; Thorpe, K. L.

456

Plastic Bag Derived-Microplastics as a Vector for Metal Exposure in Terrestrial

457

Invertebrates. Environ. Sci. Technol. 2017, 51 (8), 4714–4721.

458

(26) Lagauzère; Terrail, R.; Bonzom, J.-M. Ecotoxicity of uranium to Tubifex tubifex worms

459

(Annelida, Clitellata, Tubificidae) exposed to contaminated sediment. Ecotoxicol.

460

Environ. Saf. 2009, 72 (2), 527–537.

461

(27) Lagauzère; Boyer, P.; Stora, G.; Bonzom, J.-M. Effects of uranium-contaminated

462

sediments on the bioturbation activity of Chironomus riparius larvae (Insecta, Diptera) and

463

Tubifex tubifex worms (Annelida, Tubificidae). Chemosphere 2009, 76 (3), 324–334.

464

(28) Bouché, M.-L.; Habets, F.; Biagianti-Risbourg, S.; Vernet, G. Toxic Effects and

465

Bioaccumulation of Cadmium in the Aquatic Oligochaete Tubifex tubifex. Ecotoxicol.

466

Environ. Saf. 2000, 46 (3), 246–251.

467 468

(29) Hare, L.; Tessier, A.; Warren, L. Cadmium accumulation by invertebrates living at the sediment–water interface. Environ. Toxicol. Chem. 2001, 20 (4), 880–889.

469

(30) Méndez-Fernández, L.; Martínez-Madrid, M.; Rodriguez, P. Toxicity and critical body

470

residues of Cd, Cu and Cr in the aquatic oligochaete Tubifextubifex (Müller) based on

471

lethal and sublethal effects. Ecotoxicology 2013, 22 (10), 1445–1460.

472 473

(31) Karickhoff, S. W.; Morris, K. R. Impact of tubificid oligochaetes on pollutant transport in bottom sediments. Environ. Sci. Technol. 1985, 19 (1), 51–56.

ACS Paragon Plus Environment

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Environmental Science & Technology

474 475

Page 28 of 38

(32) Coler, R. A.; Gunner, H. B.; Zuckerman, B. M. Selective feeding of tubificids on bacteria. Nature 1967, 216 (5120), 1143–1144.

476

(33) Rodriguez, P.; Martinez-Madrid, M.; Arrate, J. A.; Navarro, E. Selective feeding by the

477

aquatic oligochaete Tubifex tubifex (Tubificidae, Clitellata). Hydrobiologia 2001, 463 (1–

478

3), 133–140.

479

(34) Reynoldson, T. B.; Thompson, S. P.; Bamsey, J. L. A sediment bioassay using the

480

tubificid oligochaete worm Tubifex tubifex. Environ. Toxicol. Chem. 1991, 10 (8), 1061–

481

1072.

482 483 484 485

(35) Wiederholm, T.; Dave, G. Toxicity of metal polluted sediments to Daphnia magna and Tubifex tubifex. Hydrobiologia 1989, 176–177 (1), 411–417. (36) Milbrink, G. Biological characterization of sediments by standardized tubificid bioassays. Hydrobiologia 1987, 155 (1), 267–275.

486

(37) Kaonga, C. C.; Kumwenda, J.; Mapoma, H. T. Accumulation of lead, cadmium,

487

manganese, copper and zinc by sludge worms; Tubifex tubifex in sewage sludge. Int. J.

488

Environ. Sci. Technol. 2010, 7 (1), 119–126.

489

(38) Mosleh, Y. Y.; Paris-Palacios, S.; Biagianti-Risbourg, S. Metallothioneins induction and

490

antioxidative response in aquatic worms Tubifex tubifex (Oligochaeta, Tubificidae)

491

exposed to copper. Chemosphere 2006, 64 (1), 121–128.

492 493

(39) Chapman, P. M. Utility and relevance of aquatic oligochaetes in ecological risk assessment. In Aquatic Oligochaete Biology VIII; Springer, 2001; pp 149–169.

494

(40) Chapman, K. K.; Benton, M. J.; Brinkhurst, R. O.; Scheuerman, P. R. Use of the aquatic

495

oligochaetes Lumbriculus variegatus and Tubifex tubifex for assessing the toxicity of

ACS Paragon Plus Environment

28

Page 29 of 38

Environmental Science & Technology

496

copper and cadmium in a spiked-artificial-sediment toxicity test. Environ. Toxicol. 1999,

497

14 (2), 271–278.

498 499 500 501

(41) Brinkhurst, R. O. A guide for the identification of British aquatic Oligochaeta; Freshwater Biological Association Kendal, Wilson, 1971. (42) Brinkhurst, R. O. Guide to the freshwater aquatic microdrile oligochaetes of North America. Canada. Spec Publ Fish Aquat Sci 1986, 84.

502

(43) Brinkhurst, R. O.; Jamieson, B. G. M. Aquatic Oligochaeta of the world. 1971.

503

(44) Klemm, D. J. A guide to the freshwater Annelida (Polychaeta, Naidid and tubificid

504

Oligochaeta, and Hirudinea) of North America; Kendall Hunt Publishing Company, 1985.

505

(45) Williams, A. E.; Waterfall, R. J.; White, K. N.; Hendry, K.; others. Manchester Ship Canal

506

and Salford Quays: industrial legacy and ecological restoration. Ecol. Ind. Pollution–

507

Cambridge Univ. Press Camb. 2010, 276.

508

(46) Gillis, P. L.; Dixon, D. G.; Borgmann, U.; Reynoldson, T. B. Uptake and depuration of

509

cadmium, nickel, and lead in laboratory-exposed Tubifex tubifex and corresponding

510

changes in the concentration of a metallothionein-like protein. Environ. Toxicol. Chem.

511

2004, 23 (1), 76–85.

512

(47) Rochman, C. M.; Tahir, A.; Williams, S. L.; Baxa, D. V.; Lam, R.; Miller, J. T.; Teh, F.-

513

C.; Werorilangi, S.; Teh, S. J. Anthropogenic debris in seafood: Plastic debris and fibers

514

from textiles in fish and bivalves sold for human consumption. Sci. Rep. 2015, 5.

515

(48) Dehaut, A.; Cassone, A.-L.; Frère, L.; Hermabessiere, L.; Himber, C.; Rinnert, E.; Rivière,

516

G.; Lambert, C.; Soudant, P.; Huvet, A.; et al. Microplastics in seafood: Benchmark

517

protocol for their extraction and characterization. Environ. Pollut. 2016, 215, 223–233.

ACS Paragon Plus Environment

29

Environmental Science & Technology

Page 30 of 38

518

(49) Karami, A.; Golieskardi, A.; Choo, C. K.; Romano, N.; Ho, Y. B.; Salamatinia, B. A high-

519

performance protocol for extraction of microplastics in fish. Sci. Total Environ. 2017, 578,

520

485–494.

521

(50) De Witte, B.; Devriese, L.; Bekaert, K.; Hoffman, S.; Vandermeersch, G.; Cooreman, K.;

522

Robbens, J. Quality assessment of the blue mussel (Mytilus edulis): Comparison between

523

commercial and wild types. Mar. Pollut. Bull. 2014, 85 (1), 146–155.

524

(51) Faure, F.; Demars, C.; Wieser, O.; Kunz, M.; Alencastro, L. F. de. Plastic pollution in

525

Swiss surface waters: nature and concentrations, interaction with pollutants. Environ.

526

Chem. 2015, 12 (5), 582–591.

527

(52) Fischer, E. K.; Paglialonga, L.; Czech, E.; Tamminga, M. Microplastic pollution in lakes

528

and lake shoreline sediments – A case study on Lake Bolsena and Lake Chiusi (central

529

Italy). Environ. Pollut. 2016, 213, 648–657.

530

(53) Ballent, A.; Corcoran, P. L.; Madden, O.; Helm, P. A.; Longstaffe, F. J. Sources and sinks

531

of microplastics in Canadian Lake Ontario nearshore, tributary and beach sediments. Mar.

532

Pollut. Bull. 2016, 110 (1), 383–395.

533 534

(54) Su, L.; Xue, Y.; Li, L.; Yang, D.; Kolandhasamy, P.; Li, D.; Shi, H. Microplastics in Taihu Lake, China. Environ. Pollut. 2016, 216, 711–719.

535

(55) Zhang, K.; Su, J.; Xiong, X.; Wu, X.; Wu, C.; Liu, J. Microplastic pollution of lakeshore

536

sediments from remote lakes in Tibet plateau, China. Environ. Pollut. 2016, 219, 450–455.

537

(56) Lazim, M. N.; Learner, M. A. The life-cycle and productivity of Tibifex tubifex

538

(Oligochaeta; Tibificidae) in the Moat-Feeder Stream, Cardiff, South Wales. Ecography

539

1986, 9 (3), 185–192.

ACS Paragon Plus Environment

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Page 31 of 38

540 541 542 543 544 545

Environmental Science & Technology

(57) Palmer, M. F. Aspects of the respiratory physiology of Tubifex tubifex in relation to its ecology. J. Zool. 1968, 154 (4), 463–473. (58) Anlauf, A. Some characteristics of genetic variants of Tubifex tubifex (Müller, 1774)(Oligochaeta: Tubificidae) in laboratory cultures. Hydrobiologia 1994, 278 (1), 1–6. (59) Hämer, J.; Gutow, L.; Köhler, A.; Saborowski, R. Fate of Microplastics in the Marine Isopod Idotea emarginata. Environ. Sci. Technol. 2014, 48 (22), 13451–13458.

546

(60) Li, J.; Qu, X.; Su, L.; Zhang, W.; Yang, D.; Kolandhasamy, P.; Li, D.; Shi, H.

547

Microplastics in mussels along the coastal waters of China. Environ. Pollut. 2016, 214,

548

177–184.

549 550 551 552

(61) Brinkhurst, R. O.; Chua, K. E.; Kaushik, N. K. Interspecific Interactions and Selective Feeding by Tubificid Oligochaetes1. Limnol. Oceanogr. 1972, 17 (1), 122–133. (62) Brinkhurst, R. O.; Austin, M. J. Assimilation by Aquatic Oligochaeta. Int. Rev. Gesamten Hydrobiol. Hydrogr. 1979, 64 (2), 245–250.

553

(63) Matisoff, G.; Wang, X.; McCall, P. L. Biological Redistribution of Lake Sediments by

554

Tubificid Oligochaetes: Branchiura sowerbyi and Limnodrilus hoffmeisteri/Tubifex

555

tubifex. J. Gt. Lakes Res. 1999, 25 (1), 205–219.

556

(64) McCormick, A.; Hoellein, T. J.; Mason, S. A.; Schluep, J.; Kelly, J. J. Microplastic is an

557

Abundant and Distinct Microbial Habitat in an Urban River. Environ. Sci. Technol. 2014,

558

48 (20), 11863–11871.

559

(65) Lagarde, F.; Olivier, O.; Zanella, M.; Daniel, P.; Hiard, S.; Caruso, A. Microplastic

560

interactions with freshwater microalgae: Hetero-aggregation and changes in plastic density

561

appear strongly dependent on polymer type. Environ. Pollut. 2016, 215, 331–339.

ACS Paragon Plus Environment

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Environmental Science & Technology

562 563 564 565 566 567

Page 32 of 38

(66) Oberbeckmann, S.; Löder, M. G. J.; Labrenz, M. Marine microplastic-associated biofilms – a review. Environ. Chem. 2015, 12 (5), 551–562. (67) Carpenter, E. J.; Anderson, S. J.; Harvey, G. R.; Miklas, H. P.; Peck, B. B. Polystyrene spherules in coastal waters. Science 1972, 178 (4062), 749–750. (68) Wright, S. L.; Thompson, R. C.; Galloway, T. S. The physical impacts of microplastics on marine organisms: A review. Environ. Pollut. 2013, 178, 483–492.

568

(69) Rochman, C. M. The Role of Plastic Debris as Another Source of Hazardous Chemicals in

569

Lower-Trophic Level Organisms; The Handbook of Environmental Chemistry; Springer

570

Berlin Heidelberg, 2016; pp 1–15.

571 572 573 574

(70) Reisser, J.; Proietti, M.; Shaw, J.; Pattiaratchi, C. Ingestion of plastics at sea: does debris size really matter? Front. Mar. Sci. 2014, 70, 1-2. (71) Young, J. O.; Ironmonger, J. W. A laboratory study of the food of three species of leeches occurring in British lakes. Hydrobiologia 1980, 68 (3), 209–215.

575

(72) Egeler, P.; Meller, M.; Roembke, J.; Spoerlein, P.; Streit, B.; Nagel, R. Tubifex tubifex as

576

a link in food chain transfer of hexachlorobenzene from contaminated sediment to fish.

577

Hydrobiologia 2001, 463 (1–3), 171–184.

578

(73) Dunbrack, R. L. Feeding of Juvenile Coho Salmon (Oncorhynchus kisutch): Maximum

579

Appetite, Sustained Feeding Rate, Appetite Return, and Body Size. Can. J. Fish. Aquat.

580

Sci. 1988, 45 (7), 1191–1196.type

581 582

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TOC Art 47x26mm (300 x 300 DPI)

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The location of the study site in relation to the UK (A) and River Irwell catchment (B) and the spatial distribution of sampling sites across Salford Quays (C).The basin receives waters from the River Irwell (right) and drains into the Manchester Ship Canal through a series of locks (top left). An aerial photograph of the area is also provided (D), showing the Salford Quays basin in relation to the cities of Manchester (top centre) and Salford (middle left). Aerial photograph by M J Richardson (2010) licensed under CC BY-SA 2.0. 170x152mm (300 x 300 DPI)

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Concentrations of microplastics in the bottom sediments of Salford Quays. These are provided as total concentrations in particles kg-1 (A), in addition to the relative proportions of each density extract (B), microplastic type (C) and polymer composition (D). 260x554mm (300 x 300 DPI)

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Density of Tubifex worm populations (A) and concentrations of ingested microplastics (B) in Salford Quays. Concentrations are also broken down by microplastic type (C) and polymer composition (D). *Polymer composition refers to the microplastic ingested by the 75 worms analysed individually 248x532mm (300 x 300 DPI)

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Greyscale version of Figure 2 260x554mm (300 x 300 DPI)

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Greyscale version of Figure 3 248x532mm (300 x 300 DPI)

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