Rapid effects of plastic pollution on coastal sediment metabolism in nature.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
02 Aug 2024
Historique:
received: 14 01 2024
accepted: 29 07 2024
medline: 3 8 2024
pubmed: 3 8 2024
entrez: 2 8 2024
Statut: epublish

Résumé

While extensive research has explored the effects of plastic pollution, ecosystem responses remain poorly quantified, especially in field experiments. In this study, we investigated the impact of polyester pollution, a prevalent plastic type, on coastal sediment ecosystem function. Strips of polyester netting were buried into intertidal sediments, and effects on sediment oxygen consumption and polyester additive concentrations were monitored over 72-days. Our results revealed a rapid reduction in the magnitude and variability of sediment oxygen consumption, a crucial ecosystem process, potentially attributed to the loss of the additive di(2-ethylhexyl) phthalate (DEHP) from the polyester material. DEHP concentrations declined by 89% within the first seven days of deployment. However, effects on SOC dissipated after 22 days, indicating a short-term impact and a quick recovery by the ecosystem. Our study provides critical insights into the immediate consequences of plastic pollution on ecosystem metabolism in coastal sediments, contributing to a nuanced understanding of the temporal variation of plastic pollution's multifaceted impacts. Additionally, our research sheds light on the urgent need for comprehensive mitigation strategies to preserve marine ecosystem functionality from plastic pollution impacts.

Identifiants

pubmed: 39095589
doi: 10.1038/s41598-024-68766-0
pii: 10.1038/s41598-024-68766-0
doi:

Substances chimiques

Plastics 0
Water Pollutants, Chemical 0
Polyesters 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

17963

Informations de copyright

© 2024. The Author(s).

Références

Borrelle, S. B. et al. Predicted growth in plastic waste exceeds efforts to mitigate plastic pollution. Science 369(6509), 1515–1518. https://doi.org/10.1126/science.aba3656 (2020).
doi: 10.1126/science.aba3656 pubmed: 32943526
Kumar, R. et al. Impacts of plastic pollution on ecosystem services, sustainable development goals, and need to focus on circular economy and policy interventions. Sustainability (Switzerland) 13, 9963. https://doi.org/10.3390/SU13179963 (2021).
doi: 10.3390/SU13179963
MacLeod, M., Arp, H. P. H., Tekman, M. B. & Jahnke, A. The global threat from plastic pollution. Science 373(6550), 61–65. https://doi.org/10.1126/SCIENCE.ABG5433 (2021).
doi: 10.1126/SCIENCE.ABG5433 pubmed: 34210878
Barbier, E. B. Marine ecosystem services. Curr. Biol. 27(11), R507–R510. https://doi.org/10.1016/J.CUB.2017.03.020 (2017).
doi: 10.1016/J.CUB.2017.03.020 pubmed: 28586688
Barnes, D. K. A., Galgani, F., Thompson, R. C. & Barlaz, M. Accumulation and fragmentation of plastic debris in global environments. Philos. Transa. Biol. Sci. 364(1526), 1985–1998. https://doi.org/10.1098/rstb.2008.0205 (2009).
doi: 10.1098/rstb.2008.0205
Lebreton, L. C. M. et al. River plastic emissions to the world’s oceans. Nat. Commun. 8, 15611. https://doi.org/10.1038/ncomms15611 (2017).
doi: 10.1038/ncomms15611 pubmed: 28589961 pmcid: 5467230
Harris, P. T. The fate of microplastic in marine sedimentary environments: A review and synthesis. Marine Pollut. Bull. 158, 111398. https://doi.org/10.1016/j.marpolbul.2020.111398 (2020).
doi: 10.1016/j.marpolbul.2020.111398
Hope, J. A., Coco, G. & Thrush, S. F. Effects of polyester microfibers on microphytobenthos and sediment-dwelling infauna. Environ. Sci. Technol. 54(13), 7970–7982. https://doi.org/10.1021/acs.est.0c00514 (2020).
doi: 10.1021/acs.est.0c00514 pubmed: 32463225
Coppock, R. L. et al. Benthic fauna contribute to microplastic sequestration in coastal sediments. J. Hazard. Mater. 415, 125583. https://doi.org/10.1016/j.jhazmat.2021.125583 (2021).
doi: 10.1016/j.jhazmat.2021.125583 pubmed: 33773248
Urban-Malinga, B., Jakubowska, M. & Białowąs, M. Response of sediment-dwelling bivalves to microplastics and its potential implications for benthic processes. Sci. Total Environ. 769, 144302. https://doi.org/10.1016/j.scitotenv.2020.144302 (2021).
doi: 10.1016/j.scitotenv.2020.144302 pubmed: 33736255
Wright, R. J., Langille, M. G. I. & Walker, T. R. Food or just a free ride? A meta-analysis reveals the global diversity of the Plastisphere. ISME J. 15(3), 789–806. https://doi.org/10.1038/s41396-020-00814-9 (2021).
doi: 10.1038/s41396-020-00814-9 pubmed: 33139870
Zhao, S., Zettler, E. R., Amaral-Zettler, L. A. & Mincer, T. J. Microbial carrying capacity and carbon biomass of plastic marine debris. ISME J. 15(1), 67–77. https://doi.org/10.1038/s41396-020-00756-2 (2021).
doi: 10.1038/s41396-020-00756-2 pubmed: 32879460
Zhai, X., Zhang, X. H. & Yu, M. Microbial colonization and degradation of marine microplastics in the plastisphere: A review. Front. Microbiol. 14, 1127308. https://doi.org/10.3389/fmicb.2023.1127308 (2023).
doi: 10.3389/fmicb.2023.1127308 pubmed: 36876073 pmcid: 9981674
Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M. B. & Janssen, C. R. Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina) living in natural habitats. Environ. Pollut. 199, 10–17. https://doi.org/10.1016/j.envpol.2015.01.008 (2015).
doi: 10.1016/j.envpol.2015.01.008 pubmed: 25617854
Romera-Castillo, C., Pinto, M., Langer, T. M., Alvarez-Salgado, X. A. & Herndl, G. J. Dissolved organic carbon leaching from plastics stimulates microbial activity in the ocean. Nat. Commun. 9, 1430. https://doi.org/10.1038/s41467-018-03798-5 (2018).
doi: 10.1038/s41467-018-03798-5 pubmed: 29651045 pmcid: 5897397
Nauendorf, A. et al. Microbial colonization and degradation of polyethylene and biodegradable plastic bags in temperate fine-grained organic-rich marine sediments. Marine Pollut. Bull. 103, 168–178. https://doi.org/10.1016/j.marpolbul.2015.12.024 (2016).
doi: 10.1016/j.marpolbul.2015.12.024
Seeley, M. E., Song, B., Passie, R. & Hale, R. C. Microplastics affect sedimentary microbial communities and nitrogen cycling. Nat. Commun. 11, 2372. https://doi.org/10.1038/s41467-020-16235-3 (2020).
doi: 10.1038/s41467-020-16235-3 pubmed: 32398678 pmcid: 7217880
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. https://doi.org/10.1016/j.envpol.2015.10.010 (2016).
doi: 10.1016/j.envpol.2015.10.010 pubmed: 26552519
Ladewig, S. M., Coco, G., Hope, J. A., Vieillard, A. M. & Thrush, S. F. Real-world impacts of microplastic pollution on seafloor ecosystem function. Sci. Total Environ. 858, 160114. https://doi.org/10.1016/J.SCITOTENV.2022.160114 (2023).
doi: 10.1016/J.SCITOTENV.2022.160114 pubmed: 36370782
Glud, R. N. Oxygen dynamics of marine sediments. Marine Biol. Res. 4(4), 243–289. https://doi.org/10.1080/17451000801888726 (2008).
doi: 10.1080/17451000801888726
Ladewig, S. M., Bianchi, T. S., Coco, G., Hope, J. A. & Thrush, S. F. A call to evaluate plastic’s impacts on marine, benthic ecosystem interaction networks. Environ. Pollut. 273, 116423. https://doi.org/10.1016/j.envpol.2021.116423 (2021).
doi: 10.1016/j.envpol.2021.116423 pubmed: 33477066
Thrush, S. F. et al. Cumulative stressors reduce the self-regulating capacity of coastal ecosystems. Ecol. Appl. 31(1), e02223. https://doi.org/10.1002/eap.2223 (2021).
doi: 10.1002/eap.2223 pubmed: 32869444
You, Y., Della Penna, A. & Thrush, S. F. Modelled broad-scale shifts on seafloor ecosystem functioning due to microplastic impacts on bioturbation. Sci. Rep. 13, 17121. https://doi.org/10.1038/s41598-023-44425-8 (2023).
doi: 10.1038/s41598-023-44425-8 pubmed: 37816828 pmcid: 10564913
Chen, Y., Chen, Q., Zhang, Q., Zuo, C. & Shi, H. An overview of chemical additives on (micro)plastic fibers: Occurrence, release, and health risks. Rev. Environ. Contam. Toxicol. 260, 22. https://doi.org/10.1007/s44169-022-00023-9 (2022).
doi: 10.1007/s44169-022-00023-9 pmcid: 9748405
Hermabessiere, L. et al. Occurrence and effects of plastic additives on marine environments and organisms: A review. Chemosphere 182, 781–793. https://doi.org/10.1016/j.chemosphere.2017.05.096 (2017).
doi: 10.1016/j.chemosphere.2017.05.096 pubmed: 28545000
Hahladakis, J. N., Velis, C. A., Weber, R., Iacovidou, E. & Purnell, P. An overview of chemical additives present in plastics: Migration, release, fate and environmental impact during their use, disposal and recycling. J. Hazard. Mater. 344, 179–199. https://doi.org/10.1016/j.jhazmat.2017.10.014 (2018).
doi: 10.1016/j.jhazmat.2017.10.014 pubmed: 29035713
Paluselli, A., Fauvelle, V., Ois Galgani, F., Sempéré, R. & Sempéré, S. Phthalate release from plastic fragments and degradation in seawater. Environ. Sci. Technol. 53, 166–175. https://doi.org/10.1021/acs.est.8b05083 (2019).
doi: 10.1021/acs.est.8b05083 pubmed: 30479129
Kohli, J., Ryan, J. F. & Afghan, B. K. Phthalate esters in the aquatic environment. Anal. Trace Org. Aquat. Environ. https://doi.org/10.1201/9781315149882-7 (2018).
doi: 10.1201/9781315149882-7
Hidalgo-Serrano, M., Borrull, F., Marc, R. M. & Pocurull, E. Phthalate esters in marine ecosystems: Analytical methods, occurrence and distribution. Trends Anal. Chem. 151, 116598. https://doi.org/10.1016/j.trac.2022.116598 (2022).
doi: 10.1016/j.trac.2022.116598
Gunaalan, K., Fabbri, E. & Capolupo, M. The hidden threat of plastic leachates: A critical review on their impacts on aquatic organisms. Water Res. 184, 116170. https://doi.org/10.1016/j.watres.2020.116170 (2020).
doi: 10.1016/j.watres.2020.116170 pubmed: 32698093
Tuuri, E. M. & Leterme, S. C. How plastic debris and associated chemicals impact the marine food web: A review. Environ. Pollut. 321, 121156. https://doi.org/10.1016/J.ENVPOL.2023.121156 (2023).
doi: 10.1016/J.ENVPOL.2023.121156 pubmed: 36709917
Xu, H. et al. Dose-dependent effects of Di-(2-Ethylhexyl) phthalate (DEHP) in mussel Mytilus galloprovincialis. Front. Marine Sci. 8, 658361. https://doi.org/10.3389/FMARS.2021.658361 (2021).
doi: 10.3389/FMARS.2021.658361
Zhou, Y., Li, Y., Lan, W., Jiang, H. & Pan, K. Short-term exposure to MPs and DEHP disrupted gill functions in marine bivalves. Nanomaterials 12(22), 4077. https://doi.org/10.3390/NANO12224077 (2022).
doi: 10.3390/NANO12224077 pubmed: 36432362 pmcid: 9699028
Andreyeva, A. Y. et al. Accumulation, functional and antioxidant responses to acute exposure to Di (2-ethylhexyl)phthalate (DEHP) in Mytilus galloprovincialis. Marine Pollut. Bull. 191, 114923. https://doi.org/10.1016/j.marpolbul.2023.114923 (2023).
doi: 10.1016/j.marpolbul.2023.114923
Ningthoujam, R. et al. Bacterial community shifts in a di-(2-ethylhexyl) phthalate-degrading enriched consortium and the isolation and characterization of degraders predicted through network analyses. Chemosphere 310, 136730. https://doi.org/10.1016/j.chemosphere.2022.136730 (2023).
doi: 10.1016/j.chemosphere.2022.136730 pubmed: 36209845
Yu, Q. et al. Photolysis of bis(2-ethylhexyl) phthalate in aqueous solutions at the presence of natural water photoreactive constituents under simulated sunlight irradiation. Environ. Sci. Pollut. Res. 26, 26797–26806. https://doi.org/10.1007/s11356-019-05913-5 (2019).
doi: 10.1007/s11356-019-05913-5
Hansen, R., Forbes, T. L. & Westermann, P. Importance of bioturbation and feeding by the polychaete Capitella sp. I in the degradation of di(2-ethylhexy1)phthalate (DEHP). Marine Ecol. Prog. Ser. 182, 187–199 (1999).
doi: 10.3354/meps182187
Sandnes, J., Hansen, R. & Sandnes, B. Influence of particle type and faunal activity on mixing of di(2-ethylhexy1)phthalate (DEHP) in natural sediments. Marine Ecol. Prog. Ser. 197, 151–167 (2000).
doi: 10.3354/meps197151
Yang, T. et al. Biodegradation of Di-(2-ethylhexyl) phthalate by Rhodococcus ruber YC-YT1 in contaminated water and soil. Int. J. Environ. Res. Public Health 15, 964. https://doi.org/10.3390/ijerph15050964 (2018).
doi: 10.3390/ijerph15050964 pubmed: 29751654 pmcid: 5982003
Schutte, C. A. et al. Biogeochemical dynamics of coastal tidal flats. Coast. Wetl. Integr. Ecosyst. Approach https://doi.org/10.1016/B978-0-444-63893-9.00012-5 (2019).
doi: 10.1016/B978-0-444-63893-9.00012-5
Hillman, J. R., Stephenson, F., Thrush, S. F. & Lundquist, C. J. Investigating changes in estuarine ecosystem functioning under future scenarios. Ecol. Appl. 30(4), e02090. https://doi.org/10.1002/EAP.2090 (2020).
doi: 10.1002/EAP.2090 pubmed: 32022961
Thrush, S. F., Gray, J. S., Hewitt, J. E. & Ugland, K. I. Predicting the effects of habitat homogenization on marine biodiversity. Ecol. Appl. 16(5), 1636–1642 (2006).
doi: 10.1890/1051-0761(2006)016[1636:PTEOHH]2.0.CO;2 pubmed: 17069359
Thrush, S. F., Halliday, J., Hewitt, J. E. & Lohrer, A. M. The effects of habitat loss, fragmentation, and community homogenization on resilience in estuaries. Ecol. Appl. 18(1), 12–21 (2008).
doi: 10.1890/07-0436.1 pubmed: 18372552
Drylie. Marine ecology state and trends in Tamaki Makaurau/Auckland to 2019. Auckland Council Research and Evaluation Unit (RIMU) (2021).
Rochman, C. M., Hoh, E., Hentschel, B. T. & Kaye, S. Long-term field measurement of sorption of organic contaminants to five types of plastic pellets: Implications for plastic marine debris. Environ. Sci. Technol. 47(3), 1646–1654. https://doi.org/10.1021/es303700s (2013).
doi: 10.1021/es303700s pubmed: 23270427
Tang, Z., Chai, M., Wang, Y. & Cheng, J. Phthalates in preschool children’s clothing manufactured in seven Asian countries: Occurrence, profiles and potential health risks. J. Hazard. Mater. 387, 121681. https://doi.org/10.1016/j.jhazmat.2019.121681 (2020).
doi: 10.1016/j.jhazmat.2019.121681 pubmed: 31757725
Erythropel, H. C. et al. Designing greener plasticizers: Effects of alkyl chain length and branching on the biodegradation of maleate based plasticizers. Chemosphere 134, 106–112. https://doi.org/10.1016/j.chemosphere.2015.04.014 (2015).
doi: 10.1016/j.chemosphere.2015.04.014 pubmed: 25917507
Payne, J. & Jones, M. D. The chemical recycling of polyesters for a circular plastics economy: Challenges and emerging opportunities. ChemSusChem 14(19), 4041–4070. https://doi.org/10.1002/CSSC.202100400 (2021).
doi: 10.1002/CSSC.202100400 pubmed: 33826253 pmcid: 8518041
Hewitt, J. E., Thrush, S. F., Legendre, P., Cummings, V. J. & Norkko, A. Integrating heterogeneity across spatial scales: Interactions between Atrina zelandica and benthic macrofauna. Marine Ecol. Prog. Ser. 239, 115–128 (2002).
doi: 10.3354/meps239115
Hillman, J. R., Lundquist, C. J., Pilditch, C. A. & Thrush, S. F. The role of large macrofauna in mediating sediment erodibility across sedimentary habitats. Limnol. Oceanogr. 65, 683–693. https://doi.org/10.1002/lno.11337 (2020).
doi: 10.1002/lno.11337
Primpke, S., Wirth, M., Lorenz, C. & Gerdts, G. Reference database design for the automated analysis of microplastic samples based on Fourier transform infrared (FTIR) spectroscopy. Anal. Bioanal. Chem. 410, 5131–5141. https://doi.org/10.1007/s00216-018-1156-x (2018).
doi: 10.1007/s00216-018-1156-x pubmed: 29978249 pmcid: 6113679
Bridson, J. H., Patel, M., Lewis, A., Gaw, S. & Parker, K. Microplastic contamination in Auckland (New Zealand) beach sediments. Marine Pollut. Bull. 151, 110867. https://doi.org/10.1016/j.marpolbul.2019.110867 (2020).
doi: 10.1016/j.marpolbul.2019.110867
Hope, J. A., Coco, G., Ladewig, S. M. & Thrush, S. F. The distribution and ecological effects of microplastics in an estuarine ecosystem. Environ. Pollut. 288, 117731. https://doi.org/10.1016/J.ENVPOL.2021.117731 (2021).
doi: 10.1016/J.ENVPOL.2021.117731 pubmed: 34273763
Wang, J., Peng, C., Li, H., Zhang, P. & Liu, X. The impact of microplastic-microbe interactions on animal health and biogeochemical cycles: A mini-review. Sci. Total Environ. 773, 145697. https://doi.org/10.1016/j.scitotenv.2021.145697 (2021).
doi: 10.1016/j.scitotenv.2021.145697 pubmed: 33940764
Kunz, A., Löwemark, L. & Yang, J. Dataset on mesoplastics and microplastics abundances and characteristics from sandy beaches before and after typhoon events in northern Taiwan. Data Brief 49, 109317. https://doi.org/10.1016/J.DIB.2023.109317 (2023).
doi: 10.1016/J.DIB.2023.109317 pubmed: 37600133 pmcid: 10439264
Zahari, N. Z., Tuah, P. M., Junaidi, M. R. & Ali, S. A. M. Identification, abundance, and chemical characterization of macro-, meso-, and microplastics in the intertidal zone sediments of two selected beaches in Sabah, Malaysia. Water 14(10), 1600. https://doi.org/10.3390/W14101600 (2022).
doi: 10.3390/W14101600
Rindelaub, J. D., Baird, Z., Lindner, B. A. & Strantz, A. A. Identifying extractable profiles from 3D printed medical devices. PLoS One 14(5), e0217137. https://doi.org/10.1371/journal.pone.0217137 (2019).
doi: 10.1371/journal.pone.0217137 pubmed: 31116763 pmcid: 6530847

Auteurs

Samantha M Ladewig (SM)

Institute of Marine Science, The University of Auckland, Auckland, 1142, New Zealand. slad852@aucklanduni.ac.nz.

Ines Bartl (I)

Institute of Marine Science, The University of Auckland, Auckland, 1142, New Zealand. ines.bartl@auckland.ac.nz.

Joel D Rindelaub (JD)

School of Chemical Sciences, The University of Auckland, Auckland, 1142, New Zealand.

Simon F Thrush (SF)

Institute of Marine Science, The University of Auckland, Auckland, 1142, New Zealand.

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