Interactions of microplastic debris throughout the marine ecosystem

Abstract

Marine microscopic plastic (microplastic) debris is a modern societal issue, illustrating the challenge of balancing the convenience of plastic in daily life with the prospect of causing ecological harm by careless disposal. Here we develop the concept of microplastic as a complex, dynamic mixture of polymers and additives, to which organic material and contaminants can successively bind to form an ‘ecocorona’, increasing the density and surface charge of particles and changing their bioavailability and toxicity. Chronic exposure to microplastic is rarely lethal, but can adversely affect individual animals, reducing feeding and depleting energy stores, with knock-on effects for fecundity and growth. We explore the extent to which ecological processes could be impacted, including altered behaviours, bioturbation and impacts on carbon flux to the deep ocean. We discuss how microplastic compares with other anthropogenic pollutants in terms of ecological risk, and consider the role of science and society in tackling this global issue in the future.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Schematic illustration of the dynamic changes experienced by microplastic in the water column.
Figure 2: Scanning electron microscopy images of microplastics.
Figure 3
Figure 4: Mechanisms by which benthic organisms could influence the partitioning of microplastics between the water column and sediments.
Figure 5: Graph showing global statistics for the amount of crude oil spilled at sea compared with the increase in terrestrial plastics export into the oceans, as a function of time.

References

  1. 1

    Carpenter, E. J. & Smith, K. L. Plastics on the Sargasso Sea surface. Science 175, 1240–1241 (1972).

    Article  CAS  Google Scholar 

  2. 2

    Plastics — The Facts 2014/2015 (PlasticsEurope, 2015).

  3. 3

    Waters, C. N. et al. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351, aad2622 (2016).

    Article  CAS  Google Scholar 

  4. 4

    Jambeck, J. R. et al. Plastic waste inputs from land into the ocean. Science 347, 768–771 (2015). Combines data on waste production with a model that uses population density and economic status to estimate the amount of land-based plastic waste entering the ocean.

    Article  CAS  Google Scholar 

  5. 5

    Eriksen, M. et al. Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS ONE 9, e111913 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Thompson, R. C. et al. Lost at sea: where is all the plastic?. Science 304, 838 (2004).

    Article  CAS  Google Scholar 

  7. 7

    Cole, M., Lindeque, P., Halsband, C. & Galloway, T. S. Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. 62, 2588–2597 (2011).

    Article  CAS  Google Scholar 

  8. 8

    Andrady, A. L. in Marine Anthropogenic Litter (eds Bergmann, M., Gutow, L. & Klages, M. ) 57–72 (Springer, 2015).

    Google Scholar 

  9. 9

    Gewert, B., Plassmann, M. M. & MacLeod, M. Pathways for degradation of plastic polymers floating in the marine environment. Environ. Sci. Processes Impacts 17, 1513–1521 (2015).

    Article  CAS  Google Scholar 

  10. 10

    Harshvardhan, K. & Jha, B. Biodegradation of low-density polyethylene by marine bacteria from pelagic waters, Arabian Sea, India. Mar. Pollut. Bull. 77, 100–106 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Wright, S. L., Thompson, R. C. & Galloway, T. S. The physical impacts of microplastics on marine organisms: a review. Environ. Pollut. 178, 483–492 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Lusher, A. in Marine Anthropogenic Litter (eds Bergmann, M., Gutow, L. & Klages, M. ) 245–307 (Springer, 2015).

    Google Scholar 

  13. 13

    Lynch, I. et al. in Nanoscience and the Environment (eds Lead, J. R. & Valsami-Jones, E. ) Ch. 4, 127–156 (Frontiers of Nanoscience Vol. 7, 2014). Introduces the ecocorona as an important concept that helps to explain how nanoparticles behave in the environment.

    Google Scholar 

  14. 14

    Zettler, E. R., Mincer, T. J. & Amaral-Zettler, L. A. Life in the ‘plastisphere’: microbial communities on plastic marine debris. Environ. Sci. Technol. 47, 7137–7146 (2013).

    Article  CAS  Google Scholar 

  15. 15

    Koelmans, A. A., Bakir, A., Burton, G. A. & Janssen, C. R. 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 (2016).

    Article  CAS  Google Scholar 

  16. 16

    Galloway, T. S. in Marine Anthropogenic Litter (eds Bergmann, M., Gutow, L. & Klages, M. ) 343–366 (Springer, 2015).

    Google Scholar 

  17. 17

    Rochman, C. M. et al. Policy: classify plastic waste as hazardous. Nature 494, 169–171 (2013).

    Article  CAS  Google Scholar 

  18. 18

    Rochman, C. M. et al. The ecological impacts of marine debris: unraveling the demonstrated evidence from what is perceived. Ecology 97, 302–312 (2016).

    Article  Google Scholar 

  19. 19

    Cózar, A. et al. Plastic debris in the open ocean. Proc. Natl Acad. Sci. USA 111, 10239–10244 (2014). Provides a first-order approximation of how much plastic pollution there is in surface waters resulting in a global map of high-density areas.

    Article  CAS  Google Scholar 

  20. 20

    Gigault, J., Pedrono, B., Maxit, B. & Ter Halle, A. Marine plastic litter: the unanalyzed nano-fraction. Environ. Sci. Nano 3, 346–350 (2016).

    Article  CAS  Google Scholar 

  21. 21

    Nel, A. E. et al. Understanding biophysicochemical interactions at the nano–bio interface. Nat. Mater. 8, 543–557 (2009).

    Article  CAS  PubMed  Google Scholar 

  22. 22

    Koelmans, A. A., Besseling, E. & Shim, W. J. in Marine Anthropogene Litter (eds Bergmann, M., Gutow, L. & Klages, M. ) 325–340 (Springer, 2015).

    Google Scholar 

  23. 23

    Wegner, A., Besseling, E., Foekema, E., Kamermans, P. & Koelmans, A. Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environ. Toxicol. Chem. 31, 2490–2497 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 24

    Turner, J. T. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130, 205–248 (2015).

    Article  Google Scholar 

  25. 25

    Clark, J. R. et al. Marine microplastic debris: a targeted plan for understanding and quantifying interactions with marine life. Front. Ecol. Environ. 14, 317–324 (2016).

    Article  Google Scholar 

  26. 26

    Monopoli, M. P., Åberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotech. 7, 779–786 (2012).

    Article  CAS  Google Scholar 

  27. 27

    Tenzer, S. et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat. Nanotech. 8, 772–781 (2013).

    Article  CAS  Google Scholar 

  28. 28

    Smita, S. et al. Nanoparticles in the environment: assessment using the causal diagram approach. Environ. Health 11, 1 (2012).

    Article  Google Scholar 

  29. 29

    Walczyk, D., Bombelli, F. B., Monopoli, M. P., Lynch, I. & Dawson, K. A. What the cell “sees” in bionanoscience. J. Am. Chem. Soc. 132, 5761–5768 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Walkey, C. D. & Chan, W. C. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem. Soc. Rev. 41, 2780–2799 (2012).

    Article  CAS  Google Scholar 

  31. 31

    Lundquist, J. J. & Toone, E. J. The cluster glycoside effect. Chem. Rev. 102, 555–578 (2002).

    Article  CAS  Google Scholar 

  32. 32

    Gibson, C., Turner, I. J., Roberts, C. J. & Lead, J. Quantifying the dimensions of nanoscale organic surface layers in natural waters. Environ. Sci. Technol. 41, 1339–1344 (2007).

    Article  CAS  Google Scholar 

  33. 33

    Cole, M. et al. Microplastics alter the properties and sinking rates of zooplankton faecal pellets. Environ. Sci. Technol. 50, 3239–3246 (2016). Introduces the hypothesis that faecal pellets provide a route for the sinking of microplastics from surface waters to the ocean floor.

    Article  CAS  Google Scholar 

  34. 34

    Wright, S. L., Rowe, D., Thompson, R. C. & Galloway, T. S. Microplastic ingestion decreases energy reserves in marine worms. Curr. Biol. 23, 1031–1033 (2013).

    Article  CAS  Google Scholar 

  35. 35

    Park, E.-J., Yi, J., Kim, Y., Choi, K. & Park, K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol. In Vitro 24, 872–878 (2010).

    Article  CAS  Google Scholar 

  36. 36

    Khan, F. R., Syberg, K., Shashoua, Y. & Bury, N. R. Influence of polyethylene microplastic beads on the uptake and localization of silver in zebrafish (Danio rerio). Environ. Pollut. 206, 73–79 (2015).

    Article  CAS  Google Scholar 

  37. 37

    Fotopoulou, K. N. & Karapanagioti, H. K. Surface properties of beached plastic pellets. Mar. Environ. Res. 81, 70–77 (2012).

    Article  CAS  Google Scholar 

  38. 38

    Wotton, R. S. The essential role of exopolymers (EPS) in aquatic systems. Oceanogr. Mar. Biol. Annu. Rev. 42, 57–94 (2004).

    Google Scholar 

  39. 39

    Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655–661 (1987).

    Article  CAS  Google Scholar 

  40. 40

    Savoca, M. S., Wohlfeil, M. E., Ebeler, S. E. & Nevitt, G. A. Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds. Sci. Adv. 2 e1600395 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Nasser, F. & Lynch, I. Secreted protein eco-corona mediates uptake and impacts of polystyrene nanoparticles on Daphnia magna. J. Proteomics 137, 45–51 (2016).

    Article  CAS  Google Scholar 

  42. 42

    Oberbeckmann, S., Löder, M. G. & Labrenz, M. Marine microplastic-associated biofilms–a review. Environ. Chem. 12, 551–562 (2015).

    Article  CAS  Google Scholar 

  43. 43

    De Tender, C. A. et al. Bacterial community profiling of plastic litter in the Belgian part of the North Sea. Environ. Sci. Technol. 49, 9629–9638 (2015).

    Article  CAS  Google Scholar 

  44. 44

    Foulon, V. et al. Colonization of polystyrene microparticles by Vibrio crassostreae: light and electron microscopic investigation. Environ. Sci. Technol. 50, 10988–10996 (2016).

    Article  CAS  Google Scholar 

  45. 45

    Long, M. et al. Interactions between microplastics and phytoplankton aggregates: Impact on their respective fates. Mar. Chem. 175, 39–46 (2015).

    Article  CAS  Google Scholar 

  46. 46

    Thiele, S., Fuchs, B. M., Amann, R. & Iversen, M. H. Colonization in the photic zone and subsequent changes during sinking determine bacterial community composition in marine snow. Appl. Environ. Microbiol. 81, 1463–1471 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    Jatt, A. N., Tang, K., Liu, J., Zhang, Z. & Zhang, X.-H. Quorum sensing in marine snow and its possible influence on production of extracellular hydrolytic enzymes in marine snow bacterium Pantoea ananatis B9. FEMS Microbiol. Ecol. 91, 1–13 (2015).

    Article  CAS  Google Scholar 

  48. 48

    Lusher, A., Welden, N., Sobral, P. & Cole, M. Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal. Methods (2016).

  49. 49

    Adverse Outcome Pathways, Molecular Screening and Toxicogenomics (OECD, 2016).

  50. 50

    Jeong, C.-B. et al. Microplastic size-dependent toxicity, oxidative stress induction, and p-jnk and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ. Sci. Technol. 50, 8849–8857 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Paul-Pont, I. et al. Exposure of marine mussels Mytilus spp. to polystyrene microplastics: Toxicity and influence on fluoranthene bioaccumulation. Environ. Pollut. 216, 724–737 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Oliveira, M., Ribeiro, A., Hylland, K. & Guilhermino, L. Single and combined effects of microplastics and pyrene on juveniles (0+ group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol. Indic. 34, 641–647 (2013).

    Article  CAS  Google Scholar 

  53. 53

    Rist, S. E. et al. Suspended micro-sized PVC particles impair the performance and decrease survival in the Asian green mussel Perna viridis. Mar. Pollut. Bull. 111, 213–220 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Ogonowski, M., Schür, C., Jarsén, Å. & Gorokhova, E. The effects of natural and anthropogenic microparticles on individual fitness in Daphnia magna. PLoS ONE 11, e0155063 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Galloway, T. S. & Lewis, C. N. Marine microplastics spell big problems for future generations. Proc. Natl Acad. Sci. USA 113, 2331–2333 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 56

    Cole, M., Lindeque, P., Fileman, E., Halsband, C. & Galloway, T. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 49, 1130–1137 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 57

    Welden, N. A. C. & Cowie, P. R. Environment and gut morphology influence microplastic retention in langoustine, Nephrops norvegicus. Environ. Pollut. 214, 859–865 (2016).

    Article  CAS  Google Scholar 

  58. 58

    Watts, A. J. R., Urbina, M. A., Corr, S., Lewis, C. & Galloway, T. S. Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environ. Sci. Technol. 49, 14597–14604 (2015).

    Article  CAS  Google Scholar 

  59. 59

    Wright, S., Rowe, D., Thompson, R. C. & Galloway, T. S. Microplastic ingestion decreases energy reserves in marine worms. Curr. Biol. 23, 1031–1033 (2013).

    Article  CAS  Google Scholar 

  60. 60

    Green, D. S. Effects of microplastics on European flat oysters, Ostrea edulis and their associated benthic communities. Environ. Pollut. 216, 95–103 (2016).

    Article  CAS  PubMed  Google Scholar 

  61. 61

    Cole, M. & Galloway, T. Ingestion of nanoplastics and microplastics by Pacific oyster larvae. Environ. Sci. Technol. 49, 14625–14632 (2015).

    Article  CAS  PubMed  Google Scholar 

  62. 62

    Kaposi, K. L., Mos, B., Kelaher, B. & Dworjanyn, S. A. Ingestion of microplastic has limited impact on a marine larva. Environ. Sci. Technol. 48, 1638–1645 (2013).

    Article  CAS  Google Scholar 

  63. 63

    Sussarellu, R. et al. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl Acad. Sci. USA 113, 2430–2435 (2016). Provides data to illustrate multigenerational effects of microplastic in an invertebrate model illustrating potential ecological impact in marine ecosystems.

    Article  CAS  PubMed  Google Scholar 

  64. 64

    Ha¨mer, J., Gutow, L., Ko¨hler, A. & Saborowski, R. Fate of microplastics in the marine isopod Idotea emarginata. Environ. Sci. Technol. 48, 13451–13458 (2014).

    Article  CAS  Google Scholar 

  65. 65

    Blarer, P. & Burkhardt-Holm, P. Microplastics affect assimilation efficiency in the freshwater amphipod Gammarus fossarum. Environ. Sci. Pollut. Res. 23, 23522–23532 (2016).

    Article  CAS  Google Scholar 

  66. 66

    Lee, K.-W., Shim, W. J., Kwon, O. Y. & Kang, J.-H. Size-Dependent Effects of Micro Polystyrene Particles in the Marine Copepod Tigriopus japonicus. Environ. Sci. Technol. 47, 11278–11283 (2013).

    Article  CAS  PubMed  Google Scholar 

  67. 67

    Weis, J. S. Developmental and Behavioural Effects of Marine Pollution (Springer, 2014).

    Google Scholar 

  68. 68

    Wong, B. B. & Candolin, U. Behavioral responses to changing environments. Behav. Ecol. 26, 665–673 (2015).

    Article  Google Scholar 

  69. 69

    de Sá, L. C., Luís, L. G. & Guilhermino, L. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environ. Pollut. 196, 359–362 (2015).

    Article  CAS  Google Scholar 

  70. 70

    Waloff, N. The mechanisms of humidity reactions of terrestrial isopods. J. Exp. Biol. 18, 8–135 (1941).

    Google Scholar 

  71. 71

    Tosetto, L., Brown, C. & Williamson, J. E. Microplastics on beaches: ingestion and behavioural consequences for beachhoppers. Mar. Biol. 163, 199 (2016).

    Article  Google Scholar 

  72. 72

    Rehse, S., Kloas, W. & Zarfl, C. Short-term exposure with high concentrations of pristine microplastic particles leads to immobilisation of Daphnia magna. Chemosphere 153, 91–99 (2016).

    Article  CAS  Google Scholar 

  73. 73

    Godin, J.-G. J. & Crossman, S. L. Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk. Behav. Ecol. Sociobiol. 34, 359–366 (1994).

    Article  Google Scholar 

  74. 74

    Dill, L. M. & Fraser, A. H. Risk of predation and the feeding behavior of juvenile coho salmon (Oncorhynchus kisutch). Behav. Ecol. Sociobiol. 16, 65–71 (1984).

    Article  Google Scholar 

  75. 75

    Gotceitas, V. & Godin, J.-G. J. Foraging under the risk of predation in juvenile Atlantic salmon (Salmo salar L.): effects of social status and hunger. Behav. Ecol. Sociobiol. 29, 255–261 (1991).

    Article  Google Scholar 

  76. 76

    Houston, A. I. & McNamara, J. M. Models of Adaptive Behaviour: an Approach Based on State. (Cambridge Univ. Press, 1999).

    Google Scholar 

  77. 77

    Meadows, P. S., Meadows, A. & Murray, J. M. Biological modifiers of marine benthic seascapes: Their role as ecosystem engineers. Geomorphology 157, 31–48 (2012).

    Article  Google Scholar 

  78. 78

    Green, D. S., Boots, B., Sigwart, J., Jiang, S. & Rocha, C. Effects of conventional and biodegradable microplastics on a marine ecosystem engineer (Arenicola marina) and sediment nutrient cycling. Environ. Pollut. 208, 426–434 (2016).

    Article  CAS  Google Scholar 

  79. 79

    Sailley, S. F., Polimene, L., Mitra, A., Atkinson, A. & Allen, J. I. Impact of zooplankton food selectivity on plankton dynamics and nutrient cycling. J. Plankton Res. 37, 519–529 (2015).

    Article  CAS  Google Scholar 

  80. 80

    Desforges, J.-P. W., Galbraith, M. & Ross, P. S. Ingestion of microplastics by zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contam. Toxicol. 69, 320–330 (2015). First report of ingestion of microplastics in situ by zooplankton indicating that species at lower trophic levels can mistake plastic for food. This highlights the potential risks to higher trophic level species.

    Article  CAS  Google Scholar 

  81. 81

    Buesseler, K. O. et al. Revisiting carbon flux through the ocean's twilight zone. Science 316, 567–570 (2007).

    Article  CAS  Google Scholar 

  82. 82

    Small, L., Fowler, S. & Ünlü, M. Sinking rates of natural copepod fecal pellets. Mar. Biol. 51, 233–241 (1979).

    Article  Google Scholar 

  83. 83

    Giering, S. L. et al. Reconciliation of the carbon budget in the ocean/'s twilight zone. Nature 507, 480–483 (2014).

    Article  CAS  Google Scholar 

  84. 84

    Report of the First Session of the INC for an International Legally Binding Instrument for Implementing International Action on certain Persistent Organic Pollutants (POPs) (UNEP, 1998).

  85. 85

    Diamond, M. L. et al. Exploring the planetary boundary for chemical pollution. Environ. Int. 78, 8–15 (2015).

    Article  CAS  Google Scholar 

  86. 86

    Rockström, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009).

    Article  CAS  Google Scholar 

  87. 87

    Oil Tanker Spill Statistics (ITOPF, 2016).

  88. 88

    Sanderson, K. It's not easy being green. Nature 469, 18–20 (2011).

    Article  CAS  Google Scholar 

  89. 89

    Guide to the Business of Chemistry, American Chemical Council Facts and Figs 2011 (CEFIC, 2011).

  90. 90

    Global Plastic Production from 1950 to 2015 (STATISTA, 2016).

  91. 91

    Scheringer, M. Characterization of the environmental distribution behavior of organic chemicals by means of persistence and spatial range. Environ. Sci. Technol. 31, 2891–2897 (1997).

    Article  CAS  Google Scholar 

  92. 92

    Scheringer, M. Persistence and spatial range as endpoints of an exposure-based assessment of organic chemicals. Environ. Sci. Technol. 30, 1652–1659 (1996).

    Article  CAS  Google Scholar 

  93. 93

    Persson, L. M. et al. Confronting unknown planetary boundary threats from chemical pollution. Environ. Sci. Technol. 47, 12619–12622 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Funding was provided by the Natural Environment Research Council (grants NE/L007010 and NE/N006178) and European Union FP7 (grant 308370). We gratefully acknowledge helpful discussions with colleagues, including R. Lohmann (University of Rhode Island) for discussions on persistent organic pollutants.

Author information

Affiliations

Authors

Contributions

All authors contributed to writing and revising the manuscript.

Corresponding author

Correspondence to Tamara S. Galloway.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Galloway, T., Cole, M. & Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nat Ecol Evol 1, 0116 (2017). https://doi.org/10.1038/s41559-017-0116

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing