Functional Trait-Based Evidence of Microplastic Effects on Aquatic Species
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. The Literature Search and Data Collection
2.2. Calculation and Analysis of Effects
3. Results
3.1. Overall Analysis
3.2. Subgroup Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Duis, K.; Coors, A. Microplastics in the Aquatic and Terrestrial Environment: Sources (with a Specific Focus on Personal Care Products), Fate and Effects. Environ. Sci. Eur. 2016, 28, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salerno, M.; Berlino, M.; Mangano, M.C.; Sarà, G. Microplastics and the Functional Traits of Fishes: A Global Meta-Analysis. Glob. Chang. Biol. 2021, 27, 2645–2655. [Google Scholar] [CrossRef] [PubMed]
- Berlino, M.; Mangano, M.C.; De Vittor, C.; Sarà, G. Effects of Microplastics on the Functional Traits of Aquatic Benthic Organisms: A Global-Scale Meta-Analysis. Environ. Pollut. 2021, 285, 117174. [Google Scholar] [CrossRef] [PubMed]
- Galgani, F.; Souplet, A.; Cadiou, Y. Accumulation of Debris on the Deep Sea Floor off the French Mediterranean Coast. Mar. Ecol. Prog. Ser. 1996, 142, 225–234. [Google Scholar] [CrossRef] [Green Version]
- Jambeck, J.R.; Geyer, R.; Wilcox, C.; Siegler, T.R.; Perryman, M.; Andrady, A.; Narayan, R.; Law, K.L. Plastic Waste Inputs from Land into the Ocean. Science 2015, 347, 768–771. [Google Scholar] [CrossRef]
- Kane, I.A.; Clare, M.A.; Miramontes, E.; Wogelius, R.; Rothwell, J.J.; Garreau, P.; Pohl, F. Seafloor Microplastic Hotspots Controlled by Deep-Sea Circulation. Science 2020, 368, 1140–1145. [Google Scholar] [CrossRef]
- Andrady, A.L. Persistence of Plastic Litter in the Oceans. In Marine Anthropogenic Litter; Springer: Berlin/Heidelberg, Germany, 2015. [Google Scholar]
- Barnes, D.K.A.; Galgani, F.; Thompson, R.C.; Barlaz, M. Accumulation and Fragmentation of Plastic Debris in Global Environments. Philos. Trans. R. Soc. B Biol. Sci. 2009, 364, 1985–1998. [Google Scholar] [CrossRef] [Green Version]
- Browne, M.A.; Crump, P.; Niven, S.J.; Teuten, E.; Tonkin, A.; Galloway, T.; Thompson, R. Accumulation of Microplastic on Shorelines Woldwide: Sources and Sinks. Environ. Sci. Technol. 2011, 45, 9175–9179. [Google Scholar] [CrossRef]
- Claessens, M.; De Meester, S.; Van Landuyt, L.; De Clerck, K.; Janssen, C.R. Occurrence and Distribution of Microplastics in Marine Sediments along the Belgian Coast. Mar. Pollut. Bull. 2011, 62, 2199–2204. [Google Scholar] [CrossRef]
- Eriksen, M.; Mason, S.; Wilson, S.; Box, C.; Zellers, A.; Edwards, W.; Farley, H.; Amato, S. Microplastic Pollution in the Surface Waters of the Laurentian Great Lakes. Mar. Pollut. Bull. 2013, 77, 177–182. [Google Scholar] [CrossRef]
- European Commission. Communication from the Commission to the European Economic and Social Committee and the Committee of the Regions. Pathway to a Healthy Planet for All. EU Action Plan: “Towards Zero Pollution for Air, Water and Soil.” European Union Commission. 2021, COM(2021), 400final. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:52021DC0400&from=EN (accessed on 20 July 2022).
- Bujnicki, J.; Dykstra, P.; Fortunato, E.; Grobert, N.; Heuer, R.D.; Keskitalo, C.; Nurse, P. Environmental and Health Risks of Microplastic Pollution; European Union Commission: Brussels, Belgium, 2019; p. 64. [Google Scholar]
- Hein, L.; Remme, R.P.; Schenau, S.; Bogaart, P.W.; Lof, M.E.; Horlings, E. Ecosystem Accounting in the Netherlands. Ecosyst. Serv. 2020, 44, 101118. [Google Scholar] [CrossRef]
- Bucci, K.; Tulio, M.; Rochman, C.M. What Is Known and Unknown about the Effects of Plastic Pollution: A Meta-Analysis and Systematic Review. Ecol. Appl. 2020, 30, e02044. [Google Scholar] [CrossRef]
- Lusher, A.L.; Welden, N.A.; Sobral, P.; Cole, M. Sampling, Isolating and Identifying Microplastics Ingested by Fish and Invertebrates. In Analysis of Nanoplastics and Microplastics in Food; CRC Press: Boca Raton, FL, USA, 2020; pp. 119–148. [Google Scholar]
- Cole, M.; Lindeque, P.; Halsband, C.; Galloway, T.S. Microplastics as Contaminants in the Marine Environment: A Review. Mar. Pollut. Bull. 2011, 62, 2588–2597. [Google Scholar] [CrossRef]
- Foekema, E.M.; De Gruijter, C.; Mergia, M.T.; van Franeker, J.A.; Murk, A.J.; Koelmans, A.A. Plastic in North Sea Fish. Environ. Sci. Technol. 2013, 47, 8818–8824. [Google Scholar] [CrossRef]
- Ma, J.; Niu, X.; Zhang, D.; Lu, L.; Ye, X.; Deng, W.; Li, Y.; Lin, Z. High Levels of Microplastic Pollution in Aquaculture Water of Fish Ponds in the Pearl River Estuary of Guangzhou, China. Sci. Total Environ. 2020, 744, 140679. [Google Scholar] [CrossRef]
- 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, 264–269. [Google Scholar] [CrossRef]
- Engler, R.E. The Complex Interaction between Marine Debris and Toxic Chemicals in the Ocean. Environ. Sci. Technol. 2012, 46, 12302–12315. [Google Scholar] [CrossRef]
- Wu, N.C.; Seebacher, F. Effect of the Plastic Pollutant Bisphenol A on the Biology of Aquatic Organisms: A Meta-analysis. Glob. Chang. Biol. 2020, 26, 3821–3833. [Google Scholar] [CrossRef]
- Rozman, U.; Kalčíková, G. Seeking for a Perfect (Non-Spherical) Microplastic Particle—The Most Comprehensive Review on Microplastic Laboratory Research. J. Hazard. Mater. 2022, 424, 127529. [Google Scholar] [CrossRef]
- Fu, Z.; Chen, G.; Wang, W.; Wang, J. Microplastic Pollution Research Methodologies, Abundance, Characteristics and Risk Assessments for Aquatic Biota in China. Environ. Pollut. 2020, 266, 115098. [Google Scholar] [CrossRef]
- Cernansky, R. The Biodiversity Revolution. Nature 2017, 546, 22–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sibly, R.M.; Brown, J.H.; Kodric-Brown, A. Metabolic Ecology: A Scaling Approach; John Wiley Sons: Hoboken, NJ, USA, 2012; pp. 1–375. [Google Scholar]
- Arnold, S.J. Morphology, Performance and Fitness. Am. Zool. 1983, 23, 347–361. [Google Scholar] [CrossRef]
- Violle, C.; Navas, M.-L.; Vile, D.; Kazakou, E.; Fortunel, C.; Hummel, I.; Garnier, E. Let the Concept of Trait Be Functional! Oikos 2007, 116, 882–892. [Google Scholar] [CrossRef]
- Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G.; PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009, 6, e1000097. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pullin, A.S.; Stewart, G.B. Guidelines for Systematic Review in Conservation and Environmental Management. Conserv. Biol. 2006, 20, 1647–1656. [Google Scholar] [CrossRef]
- Hedges, L.V.; Olkin, I. Statistical Methods for Meta-Analysis; Academic Press: New York, NY, USA, 2014; ISBN 0080570658. [Google Scholar]
- Sarà, G. A Meta-Analysis on the Ecological Effects of Aquaculture on the Water Column: Dissolved Nutrients. Mar. Environ. Res. 2007, 63, 390–408. [Google Scholar] [CrossRef] [Green Version]
- Borenstein, M.; Hedges, L.V.; Higgins, J.P.T.; Rothstein, H.R. Introduction to Meta-Analysis; John Wiley & Sons: Hoboken, NJ, USA, 2011; ISBN 1119558387. [Google Scholar]
- Koricheva, J.; Gurevitch, J.; Mengersen, K. Handbook of Meta-Analysis in Ecology and Evolution; Princeton University: Princeton, NJ, USA, 2013; p. 498. [Google Scholar]
- Anton, A.; Geraldi, N.R.; Lovelock, C.E.; Apostolaki, E.T.; Bennett, S.; Cebrian, J.; Krause-Jensen, D.; Marbà, N.; Martinetto, P.; Pandolfi, J.M.; et al. Global Ecological Impacts of Marine Exotic Species. Nat. Ecol. Evol. 2019, 3, 787–800. [Google Scholar] [CrossRef] [Green Version]
- Viechtbauer, W. Conducting Meta-Analyses in R with the Metafor. J. Stat. Softw. 2010, 36, 1–48. [Google Scholar] [CrossRef] [Green Version]
- Viechtbauer, W. Accounting for Heterogeneity via Random-Effects Models and Moderator Analyses in Meta-Analysis. J. Psychol. 2007, 215, 104–121. [Google Scholar] [CrossRef]
- Konstantopoulos, S. Fixed Effects and Variance Components Estimation in Three-level Meta-analysis. Res. Synth. Methods 2011, 2, 61–76. [Google Scholar] [CrossRef] [Green Version]
- Viechtbauer, W.; Cheung, M.W.-L. Outlier and Influence Diagnostics for Meta-Analysis. Res. Synth. Methods 2010, 1, 112–125. [Google Scholar] [CrossRef]
- Farrell, P.; Nelson, K. Trophic Level Transfer of Microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environ. Pollut. 2013, 177, 1–3. [Google Scholar] [CrossRef]
- Schessl, M.; Johns, C.; Ashpole, S.L. Microbeads in Sediment, Dreissenid Mussels, and Anurans in the Littoral Zone of the Upper St. Lawrence River, New York. Pollution 2019, 5, 41–52. [Google Scholar] [CrossRef]
- Schmid, K.; Winemiller, K.O.; Chelazzi, D.; Cincinelli, A.; Dei, L.; Giarrizzo, T. First Evidence of Microplastic Ingestion by Fishes from the Amazon River Estuary. Mar. Pollut. Bull. 2018, 133, 814–821. [Google Scholar]
- Van Cauwenberghe, L.; Janssen, C.R. Microplastics in Bivalves Cultured for Human Consumption. Environ. Pollut. 2014, 193, 65–70. [Google Scholar] [CrossRef]
- Auta, H.S.; Emenike, C.; Fauziah, S. Distribution and Importance of Microplastics in the Marine Environment: A Review of the Sources, Fate, Effects, and Potential Solutions. Environ. Int. 2017, 102, 165–176. [Google Scholar] [CrossRef]
- Windsor, F.M.; Durance, I.; Horton, A.A.; Thompson, R.C.; Tyler, C.R.; Ormerod, S.J. A Catchment-Scale Perspective of Plastic Pollution. Glob. Chang. Biol. 2019, 25, 1207–1221. [Google Scholar] [CrossRef] [Green Version]
- Enquist, B.J.; Norberg, J.; Bonser, S.P.; Violle, C.; Webb, C.T.; Henderson, A.; Sloat, L.L.; Savage, V.M. Scaling from Traits to Ecosystems: Developing a General Trait Driver Theory via Integrating Trait-Based and Metabolic Scaling Theories. Adv. Ecol. Res. 2015, 52, 249–318. [Google Scholar] [CrossRef]
- Sarà, G.; Giommi, C.; Giacoletti, A.; Conti, E.; Mulder, C.; Mangano, M.C. Multiple Climate-Driven Cascading Ecosystem Effects after the Loss of a Foundation Species. Sci. Total Environ. 2021, 770, 144749. [Google Scholar] [CrossRef]
- Wang, S.; Isbell, F.; Deng, W.; Hong, P.; Dee, L.E.; Thompson, P.; Loreau, M. How Complementarity and Selection Affect the Relationship between Ecosystem Functioning and Stability. Ecology 2021, 102, e03347. [Google Scholar] [CrossRef]
- Green, D.S. Effects of Microplastics on European Flat Oysters, Ostrea edulis and Their Associated Benthic Communities. Environ. Pollut. 2016, 216, 95–103. [Google Scholar] [CrossRef] [PubMed]
- 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. 2015, 199, 10–17. [Google Scholar] [CrossRef] [PubMed]
- Marn, N.; Jusup, M.; Kooijman, S.A.L.M.; Klanjscek, T. Quantifying Impacts of Plastic Debris on Marine Wildlife Identifies Ecological Breakpoints. Ecol. Lett. 2020, 23, 1479–1487. [Google Scholar] [CrossRef] [PubMed]
- Bayne, B.L.; Hawkins, A.J.S.; Navarro, E. Feeding and Digestion by the Mussel Mytilus edulis L.(Bivalvia: Mollusca) in Mixtures of Silt and Algal Cells at Low Concentrations. J. Exp. Mar. Bio. Ecol. 1987, 111, 1–22. [Google Scholar] [CrossRef]
- McCauley, S.J.; Bjorndal, K.A. Conservation Implications of Dietary Dilution from Debris Ingestion: Sublethal Effects in Post-hatchling Loggerhead Sea Turtles. Conserv. Biol. 1999, 13, 925–929. [Google Scholar] [CrossRef]
- Charnov, E.L. Optimal Foraging, the Marginal Value Theorem. Theor. Popul. Biol. 1976, 9, 129–136. [Google Scholar] [CrossRef] [Green Version]
- Holling, C.S. Some Characteristics of Simple Types of Predation and Parasitism1. Can. Entomol. 1959, 91, 385–398. [Google Scholar] [CrossRef]
- Kooijman, S.A.L.M. Dynamic Energy Budget Theory for Metabolic Organisation; Cambridge University Press: Cambridge, UK, 2010; ISBN 052113191X. [Google Scholar]
- Abdel-Tawwab, M.; Monier, M.N.; Hoseinifar, S.H.; Faggio, C. Fish Response to Hypoxia Stress: Growth, Physiological, and Immunological Biomarkers. Fish Physiol. Biochem. 2019, 45, 997–1013. [Google Scholar] [CrossRef]
- Watts, A.J.R.; Urbina, M.A.; Goodhead, R.; Moger, J.; Lewis, C.; Galloway, T.S. Effect of Microplastic on the Gills of the Shore Crab Carcinus maenas. Environ. Sci. Technol. 2016, 50, 5364–5369. [Google Scholar] [CrossRef] [Green Version]
- 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. 2015, 196, 359–362. [Google Scholar] [CrossRef]
- Avery-Gomm, S.; O’Hara, P.D.; Kleine, L.; Bowes, V.; Wilson, L.K.; Barry, K.L. Northern Fulmars as Biological Monitors of Trends of Plastic Pollution in the Eastern North Pacific. Mar. Pollut. Bull. 2012, 64, 1776–1781. [Google Scholar] [CrossRef]
- Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Galloway, T.S. The Impact of Polystyrene Microplastics on Feeding, Function and Fecundity in the Marine Copepod Calanus helgolandicus. Environ. Sci. Technol. 2015, 49, 1130–1137. [Google Scholar] [CrossRef]
- Boerger, C.M.; Lattin, G.L.; Moore, S.L.; Moore, C.J. Plastic Ingestion by Planktivorous Fishes in the North Pacific Central Gyre. Mar. Pollut. Bull. 2010, 60, 2275–2278. [Google Scholar] [CrossRef]
- Yin, L.; Liu, H.; Cui, H.; Chen, B.; Li, L.; Wu, F. Impacts of Polystyrene Microplastics on the Behavior and Metabolism in a Marine Demersal Teleost, Black Rockfish (Sebastes schlegelii). J. Hazard. Mater. 2019, 380, 120861. [Google Scholar] [CrossRef]
- Little, E.E.; Finger, S.E. Swimming Behavior as an Indicator of Sublethal Toxicity in Fish. Environ. Toxicol. Chem. Int. J. 1990, 9, 13–19. [Google Scholar] [CrossRef]
- Duffy, J.E.; Cardinale, B.J.; France, K.E.; McIntyre, P.B.; Thébault, E.; Loreau, M. The Functional Role of Biodiversity in Ecosystems: Incorporating Trophic Complexity. Ecol. Lett. 2007, 10, 522–538. [Google Scholar] [CrossRef] [Green Version]
- Setälä, O.; Lehtiniemi, M.; Coppock, R.; Cole, M. Microplastics in Marine Food Webs. In Microplastic Contamination in Aquatic Environments An Emerging Matter of Environmental Urgency; Elsevier: Amsterdam, The Netherlands, 2018; pp. 339–363. [Google Scholar] [CrossRef]
- Wang, W.; Gao, H.; Jin, S.; Li, R.; Na, G. The Ecotoxicological Effects of Microplastics on Aquatic Food Web, from Primary Producer to Human: A Review. Ecotoxicol. Environ. Saf. 2019, 173, 110–117. [Google Scholar] [CrossRef]
- Burns, E.E.; Boxall, A.B.A. Microplastics in the Aquatic Environment: Evidence for or against Adverse Impacts and Major Knowledge Gaps. Environ. Toxicol. Chem. 2018, 37, 2776–2796. [Google Scholar] [CrossRef] [Green Version]
- Pirsaheb, M.; Hossini, H.; Makhdoumi, P. Review of Microplastic Occurrence and Toxicological Effects in Marine Environment: Experimental Evidence of Inflammation. Process Saf. Environ. Prot. 2020, 142, 1–14. [Google Scholar] [CrossRef]
- Lehtiniemi, M.; Hartikainen, S.; Näkki, P.; Engström-Öst, J.; Koistinen, A.; Setälä, O. Size Matters More than Shape: Ingestion of Primary and Secondary Microplastics by Small Predators. Food Webs 2018, 17, e00096. [Google Scholar] [CrossRef]
- Ismail, M.A.; Kamarudin, M.S.; Syukri, F.; Ain, S.N.; Latif, K. Changes in the Mouth Morpho-Histology of Hybrid Malaysian Mahseer (Barbonymus gonionotus♀× Tor tambroides♂) during the Larval Development. Aquac. Rep. 2019, 15, 100210. [Google Scholar] [CrossRef]
- Kohno, H.; Ordonio-Aguilar, R.S.; Ohno, A.; Taki, Y. Why Is Grouper Larval Rearing Difficult?: An Approach from the Development of the Feeding Apparatus in Early Stage Larvae of the Grouper, Epinephelus coioides. Ichthyol. Res. 1997, 44, 267–274. [Google Scholar] [CrossRef]
- Malinich, T.D.; Chou, N.; Sepúlveda, M.S.; Höök, T.O. No Evidence of Microplastic Impacts on Consumption or Growth of Larval Pimephales promelas. Environ. Toxicol. Chem. 2018, 37, 2912–2918. [Google Scholar] [CrossRef] [PubMed]
- Alava, J.J. Modeling the Bioaccumulation and Biomagnification Potential of Microplastics in a Cetacean Foodweb of the Northeastern Pacific: A Prospective Tool to Assess the Risk Exposure to Plastic Particles. Front. Mar. Sci. 2020, 7, 793. [Google Scholar] [CrossRef]
- Beauchard, O.; Veríssimo, H.; Queirós, A.M.; Herman, P.M.J. The Use of Multiple Biological Traits in Marine Community Ecology and Its Potential in Ecological Indicator Development. Ecol. Indic. 2017, 76, 81–96. [Google Scholar] [CrossRef]
- Critchell, K.; Hoogenboom, M.O. Effects of microplastic exposure on the body condition and behaviour of planktivorous reef fish (Acanthochromis polyacanthus). PLoS ONE 2018, 13, e0193308. [Google Scholar] [CrossRef] [Green Version]
- Rochman, C.M.; Parnis, J.M.; Browne, M.A.; Serrato, S.; Reiner, E.J.; Robson, M.; Young, T.; Diamond, M.L.; Teh, S.J. Direct and indirect effects of different types of microplastics on freshwater prey (Corbicula fluminea) and their predator (Acipenser transmontanus). PLoS ONE 2017, 12, e0187664. [Google Scholar] [CrossRef]
- Naidoo, T.; Glassom, D. Decreased growth and survival in small juvenile fish, after chronic exposure to environmentally relevant concentrations of microplastic. Mar. Pollut. Bull. 2019, 145, 254–259. [Google Scholar] [CrossRef]
- Jabeen, K.; Li, B.; Chen, Q.; Su, L.; Wu, C.; Hollert, H.; Shi, H. Effects of virgin microplastics on goldfish (Carassius auratus). Chemosphere 2018, 213, 323–332. [Google Scholar] [CrossRef]
- Choi, J.S.; Jung, Y.-J.; Hong, N.-H.; Hong, S.H.; Park, J.-W. Toxicological effects of irregularly shaped and spherical microplastics in a marine teleost, the sheepshead minnow (Cyprinodon variegatus). Mar. Pollut. Bull. 2018, 129, 231–240. [Google Scholar] [CrossRef]
- Xia, X.; Sun, M.; Zhou, M.; Chang, Z.; Li, L. Polyvinyl chloride microplastics induce growth inhibition and oxidative stress in Cyprinus carpio var. larvae. Sci. Total. Environ. 2020, 716, 136479. [Google Scholar] [CrossRef]
- Chen, Q.; Gundlach, M.; Yang, S.; Jiang, J.; Velki, M.; Yin, D.; Hollert, H. Quantitative investigation of the mechanisms of microplastics and nanoplastics toward zebrafish larvae locomotor activity. Sci. Total. Environ. 2017, 584–585, 1022–1031. [Google Scholar] [CrossRef]
- Malafaia, G.; de Souza, A.M.; Pereira, A.C.; Goncalves, S.; da Costa Araujo, A.P.; Ribeiro, R.X.; Rocha, T.L. Barrier function of zebrafish embryonic chorions against microplastics and nanoplastics and its impact on embryo development. J. Hazard. Mater. 2020, 395, 122621. [Google Scholar]
- Karami, A.; Groman, D.B.; Wilson, S.P.; Ismail, P.; Neela, V.K. Biomarker responses in zebrafish (Danio rerio) larvae exposed to pristine low-density polyethylene fragments. Environ. Pollut. 2017, 223, 466–475. [Google Scholar] [CrossRef]
- Qiang, L.; Cheng, J. Exposure to microplastics decreases swimming competence in larval zebrafish (Danio rerio). Ecotoxicol. Environ. Saf. 2019, 176, 226–233. [Google Scholar] [CrossRef]
- Malafaia, G.; de Souza, A.M.; Pereira, A.C.; Gonçalves, S.; Araújo, A.P.D.C.; Ribeiro, R.X.; Rocha, T.L. Developmental toxicity in zebrafish exposed to polyethylene microplastics under static and semi-static aquatic systems. Sci. Total. Environ. 2019, 700, 134867. [Google Scholar] [CrossRef]
- LeMoine, C.M.; Kelleher, B.M.; Lagarde, R.; Northam, C.; Elebute, O.O.; Cassone, B.J. Transcriptional effects of polyethylene microplastics ingestion in developing zebrafish (Danio rerio). Environ. Pollut. 2018, 243, 591–600. [Google Scholar] [CrossRef]
- Qiao, R.; Deng, Y.; Zhang, S.; Wolosker, M.B.; Zhu, Q.; Ren, H.; Zhang, Y. Accumulation of different shapes of microplastics initiates intestinal injury and gut microbiota dysbiosis in the gut of zebrafish. Chemosphere 2019, 236, 124334. [Google Scholar] [CrossRef]
- Kim, S.W.; Chae, Y.; Kim, D.; An, Y.-J. Zebrafish can recognize microplastics as inedible materials: Quantitative evidence of ingestion behavior. Sci. Total. Environ. 2018, 649, 156–162. [Google Scholar] [CrossRef]
- Jin, Y.; Xia, J.; Pan, Z.; Yang, J.; Wang, W.; Fu, Z. Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ. Pollut. 2018, 235, 322–329. [Google Scholar] [CrossRef]
- Limonta, G.; Mancia, A.; Benkhalqui, A.; Bertolucci, C.; Abelli, L.; Fossi, M.C.; Panti, C. Microplastics induce transcriptional changes, immune response and behavioral alterations in adult zebrafish. Sci. Rep. 2019, 9, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, Y.; Bao, Z.; Wan, Z.; Fu, Z.; Jin, Y. Polystyrene microplastic exposure disturbs hepatic glycolipid metabolism at the physiological, biochemical, and transcriptomic levels in adult zebrafish. Sci. Total. Environ. 2019, 710, 136279. [Google Scholar] [CrossRef] [PubMed]
- Mazurais, D.; Ernande, B.; Quazuguel, P.; Severe, A.; Huelvan, C.; Madec, L.; Mouchel, O.; Soudant, P.; Robbens, J.; Huvet, A.; et al. Evaluation of the impact of polyethylene microbeads ingestion in European sea bass (Dicentrarchus labrax) larvae. Mar. Environ. Res. 2015, 112, 78–85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barboza, L.G.A.; Vieira, L.R.; Guilhermino, L. Single and combined effects of microplastics and mercury on juveniles of the European seabass (Dicentrarchus labrax): Changes in behavioural responses and reduction of swimming velocity and resistance time. Environ. Pollut. 2018, 236, 1014–1019. [Google Scholar] [CrossRef]
- Pedà, C.; Caccamo, L.; Fossi, M.C.; Gai, F.; Andaloro, F.; Genovese, L.; Perdichizzi, A.; Romeo, T.; Maricchiolo, G. Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: Preliminary results. Environ. Pollut. 2016, 212, 251–256. [Google Scholar] [CrossRef]
- Jinhui, S.; Sudong, X.; Yan, N.; Xia, P.; Jiahao, Q.; Yongjian, X. Effects of microplastics and attached heavy metals on growth, immunity, and heavy metal accumulation in the yellow seahorse, Hippocampus kuda Bleeker. Mar. Pollut. Bull. 2019, 149, 110510. [Google Scholar] [CrossRef]
- Guven, O.; Bach, L.; Munk, P.; Dinh, K.V.; Mariani, P.; Nielsen, T.G. Microplastic does not magnify the acute effect of PAH pyrene on predatory performance of a tropical fish (Lates calcarifer). Aquat. Toxicol. 2018, 198, 287–293. [Google Scholar] [CrossRef]
- Zhu, M.; Chernick, M.; Rittschof, D.; Hinton, D.E. Chronic dietary exposure to polystyrene microplastics in maturing Japanese medaka (Oryzias latipes). Aquat. Toxicol. 2019, 220, 105396. [Google Scholar] [CrossRef]
- Chisada, S.; Yoshida, M.; Karita, K. Ingestion of polyethylene microbeads affects the growth and reproduction of medaka, Oryzias latipes. Environ. Pollut. 2019, 254, 113094. [Google Scholar] [CrossRef]
- Hu, L.; Chernick, M.; Lewis, A.M.; Ferguson, P.L.; Hinton, D.E. Chronic microfiber exposure in adult Japanese medaka (Oryzias latipes). PLoS ONE 2020, 15, e0229962. [Google Scholar] [CrossRef] [Green Version]
- Pannetier, P.; Morin, B.; Clérandeau, C.; Laurent, J.; Chapelle, C.; Cachot, J. Toxicity assessment of pollutants sorbed on environmental microplastics collected on beaches: Part II-adverse effects on Japanese medaka early life stages. Environ. Pollut. 2019, 248, 1098–1107. [Google Scholar] [CrossRef]
- Cong, Y.; Jin, F.; Tian, M.; Wang, J.; Shi, H.; Wang, Y.; Mu, J. Ingestion, egestion and post-exposure effects of polystyrene microspheres on marine medaka (Oryzias melastigma). Chemosphere 2019, 228, 93–100. [Google Scholar] [CrossRef]
- Le Bihanic, F.; Clérandeau, C.; Cormier, B.; Crebassa, J.-C.; Keiter, S.H.; Beiras, R.; Morin, B.; Bégout, M.-L.; Cousin, X.; Cachot, J. Organic contaminants sorbed to microplastics affect marine medaka fish early life stages development. Mar. Pollut. Bull. 2020, 154, 111059. [Google Scholar] [CrossRef]
- Li, Y.; Wang, J.; Yang, G.; Lu, L.; Zheng, Y.; Zhang, Q.; Zhang, X.; Tian, H.; Wang, W.; Ru, S. Low level of polystyrene microplastics decreases early developmental toxicity of phenanthrene on marine medaka (Oryzias melastigma). J. Hazard. Mater. 2020, 385, 121586. [Google Scholar] [CrossRef]
- Wang, J.; Li, Y.; Lu, L.; Zheng, M.; Zhang, X.; Tian, H.; Wang, W.; Ru, S. Polystyrene microplastics cause tissue damages, sex-specific reproductive disruption and transgenerational effects in marine medaka (Oryzias melastigma). Environ. Pollut. 2019, 254, 113024. [Google Scholar] [CrossRef]
- Lönnstedt, O.M.; Eklöv, P. Environmentally relevant concentrations of microplastic particles influence larval fish ecology. Science 2016, 352, 1213–1216. [Google Scholar] [CrossRef]
- Ferreira, P.; Fonte, E.; Soares, M.E.; Carvalho, F.; Guilhermino, L. Effects of multi-stressors on juveniles of the marine fish Pomatoschistus microps: Gold nanoparticles, microplastics and temperature. Aquat. Toxicol. 2016, 170, 89–103. [Google Scholar] [CrossRef]
- Fonte, E.; Ferreira, P.; Guilhermino, L. Temperature rise and microplastics interact with the toxicity of the antibiotic cefalexin to juveniles of the common goby (Pomatoschistus microps): Post-exposure predatory behaviour, acetylcholinesterase activity and lipid peroxidation. Aquat. Toxicol. 2016, 180, 173–185. [Google Scholar] [CrossRef]
- Luís, L.G.; Ferreira, P.; Fonte, E.; Oliveira, M.; Guilhermino, L. Does the presence of microplastics influence the acute toxicity of chromium(VI) to early juveniles of the common goby (Pomatoschistus microps)? A study with juveniles from two wild estuarine populations. Aquat. Toxicol. 2015, 164, 163–174. [Google Scholar] [CrossRef]
- Miranda, T.; Vieira, L.R.; Guilhermino, L. Neurotoxicity, behavior, and lethal effects of cadmium, microplastics, and their mixtures on Pomatoschistus microps juveniles from two wild populations exposed under laboratory conditions―implications to environmental and human risk assessment. Int. J. Environ. Res. Public Health 2019, 16, 2857. [Google Scholar] [CrossRef] [Green Version]
- Schmieg, H.; Huppertsberg, S.; Knepper, T.P.; Krais, S.; Reitter, K.; Rezbach, F.; Ruhl, A.S.; Köhler, H.-R.; Triebskorn, R. Polystyrene microplastics do not affect juvenile brown trout (Salmo trutta f. fario) or modulate effects of the pesticide methiocarb. Environ. Sci. Eur. 2020, 32, 1–15. [Google Scholar] [CrossRef]
- Yin, L.; Chen, B.; Xia, B.; Shi, X.; Qu, K. Polystyrene microplastics alter the behavior, energy reserve and nutritional composition of marine jacopever (Sebastes schlegelii). J. Hazard. Mater. 2018, 360, 97–105. [Google Scholar] [CrossRef] [PubMed]
- Espinosa, C.; Cuesta, A.; Esteban, M. Effects of dietary polyvinylchloride microparticles on general health, immune status and expression of several genes related to stress in gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol. 2017, 68, 251–259. [Google Scholar] [CrossRef] [PubMed]
- Wen, B.; Jin, S.-R.; Chen, Z.-Z.; Gao, J.-Z.; Liu, Y.-N.; Liu, J.-H.; Feng, X.-S. Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defence and innate immunity of the discus fish (Symphysodon aequifasciatus). Environ. Pollut. 2018, 243, 462–471. [Google Scholar] [CrossRef]
- 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. 2016, 208, 426–434. [Google Scholar] [CrossRef]
- Bour, A.; Haarr, A.; Keiter, S.; Hylland, K. Environmentally relevant microplastic exposure affects sediment-dwelling bivalves. Environ. Pollut. 2018, 236, 652–660. [Google Scholar] [CrossRef]
- Redondo-Hasselerharm, P.E.; Falahudin, D.; Peeters, E.T.H.M.; Koelmans, A.A. Microplastic Effect Thresholds for Freshwater Benthic Macroinvertebrates. Environ. Sci. Technol. 2018, 52, 2278–2286. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.-Y.; Lee, W.; Chan, A.; Lo, H.; Shin, P.; Cheung, S. Microplastic ingestion reduces energy intake in the clam Atactodea striata. Mar. Pollut. Bull. 2017, 124, 798–802. [Google Scholar] [CrossRef]
- Lei, L.; Wu, S.; Lu, S.; Liu, M.; Song, Y.; Fu, Z.; Shi, H.; Raley-Susman, K.M.; He, D. Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci. Total. Environ. 2017, 619-620, 1–8. [Google Scholar] [CrossRef]
- 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. 2015, 49, 14597–14604. [Google Scholar] [CrossRef]
- Cole, M.; Galloway, T.S. Ingestion of Nanoplastics and Microplastics by Pacific Oyster Larvae. Environ. Sci. Technol. 2015, 49, 14625–14632. [Google Scholar] [CrossRef] [Green Version]
- Sussarellu, R.; Suquet, M.; Thomas, Y.; Lambert, C.; Fabioux, C.; Pernet, M.E.J.; Le Goïc, N.; Quillien, V.; Mingant, C.; Epelboin, Y.; et al. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. USA 2016, 113, 2430–2435. [Google Scholar] [CrossRef] [Green Version]
- Ziajahromi, S.; Kumar, A.; Neale, P.A.; Leusch, F.D. Environmentally relevant concentrations of polyethylene microplastics negatively impact the survival, growth and emergence of sediment-dwelling invertebrates. Environ. Pollut. 2018, 236, 425–431. [Google Scholar] [CrossRef]
- Messinetti, S.; Mercurio, S.; Parolini, M.; Sugni, M.; Pennati, R. Effects of polystyrene microplastics on early stages of two marine invertebrates with different feeding strategies. Environ. Pollut. 2018, 237, 1080–1087. [Google Scholar] [CrossRef]
- Guilhermino, L.; Vieira, L.R.; Ribeiro, D.; Tavares, A.S.; Cardoso, V.; Alves, A.; Almeida, J.M. Uptake and effects of the antimicrobial florfenicol, microplastics and their mixtures on freshwater exotic invasive bivalve Corbicula fluminea. Sci. Total. Environ. 2018, 622-623, 1131–1142. [Google Scholar] [CrossRef]
- Oliveira, P.; Barboza, L.G.A.; Branco, V.; Figueiredo, N.; Carvalho, C.; Guilhermino, L. Effects of microplastics and mercury in the freshwater bivalve Corbicula fluminea (Müller, 1774): Filtration rate, biochemical biomarkers and mercury bioconcentration. Ecotoxicol. Environ. Saf. 2018, 164, 155–163. [Google Scholar] [CrossRef]
- Bruck, S.; Ford, A.T. Chronic ingestion of polystyrene microparticles in low doses has no effect on food consumption and growth to the intertidal amphipod Echinogammarus marinus? Environ. Pollut. 2018, 223, 1125–1130. [Google Scholar] [CrossRef] [Green Version]
- Yu, P.; Liu, Z.; Wu, D.; Chen, M.; Lv, W.; Zhao, Y. Accumulation of polystyrene microplastics in juvenile Eriocheir sinensis and oxidative stress effects in the liver. Aquat. Toxicol. 2018, 200, 28–36. [Google Scholar] [CrossRef]
- Blarer, P.; Burkhardt-Holm, P. Microplastics affect assimilation efficiency in the freshwater amphipod Gammarus fossarum. Environ. Sci. Pollut. Res. 2016, 23, 23522–23532. [Google Scholar] [CrossRef]
- Straub, S.; Hirsch, P.E.; Burkhardt-Holm, P. Biodegradable and Petroleum-Based Microplastics Do Not Differ in Their Ingestion and Excretion but in Their Biological Effects in a Freshwater Invertebrate Gammarus fossarum. Int. J. Environ. Res. Public Heal. 2017, 14, 774. [Google Scholar] [CrossRef] [Green Version]
- Weber, A.; Scherer, C.; Brennholt, N.; Reifferscheid, G.; Wagner, M. PET microplastics do not negatively affect the survival, development, metabolism and feeding activity of the freshwater invertebrate Gammarus pulex. Environ. Pollut. 2017, 234, 181–189. [Google Scholar] [CrossRef] [PubMed]
- Au, S.Y.; Bruce, T.F.; Bridges, W.C.; Klaine, S.J. Responses of Hyalella azteca to acute and chronic microplastic exposures. Environ. Toxicol. Chem. 2015, 34, 2564–2572. [Google Scholar] [CrossRef] [PubMed]
- Hämer, J.; Gutow, L.; Köhler, A.; Saborowski, R. Fate of Microplastics in the Marine Isopod Idotea emarginata. Environ. Sci. Technol. 2014, 48, 13451–13458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Browne, M.A.; Dissanayake, A.; Galloway, T.S.; Lowe, D.M.; Thompson, R.C. Ingested Microscopic Plastic Translocates to the Circulatory System of the Mussel, Mytilus edulis (L.). Environ. Sci. Technol. 2008, 42, 5026–5031. [Google Scholar] [CrossRef] [PubMed]
- Green, D.S.; Boots, B.; O’connor, N.E.; Thompson, R. Microplastics Affect the Ecological Functioning of an Important Biogenic Habitat. Environ. Sci. Technol. 2016, 51, 68–77. [Google Scholar] [CrossRef]
- Green, D.S.; Colgan, T.J.; Thompson, R.C.; Carolan, J.C. Exposure to microplastics reduces attachment strength and alters the haemolymph proteome of blue mussels (Mytilus edulis). Environ. Pollut. 2018, 246, 423–434. [Google Scholar] [CrossRef]
- Rist, S.; Baun, A.; Almeda, R.; Hartmann, N.B. Ingestion and effects of micro- and nanoplastics in blue mussel (Mytilus edulis) larvae. Mar. Pollut. Bull. 2019, 140, 423–430. [Google Scholar] [CrossRef]
- Woods, M.N.; Stack, M.E.; Fields, D.M.; Shaw, S.D.; Matrai, P.A. Microplastic fiber uptake, ingestion, and egestion rates in the blue mussel (Mytilus edulis). Mar. Pollut. Bull. 2018, 137, 638–645. [Google Scholar] [CrossRef]
- Capolupo, M.; Franzellitti, S.; Valbonesi, P.; Lanzas, C.S.; Fabbri, E. Uptake and transcriptional effects of polystyrene microplastics in larval stages of the Mediterranean mussel Mytilus galloprovincialis. Environ. Pollut. 2018, 241, 1038–1047. [Google Scholar] [CrossRef]
- Beiras, R.; Tato, T.; López-Ibáñez, S. A 2-Tier standard method to test the toxicity of microplastics in marine water using Paracentrotus lividus and Acartia clausi larvae. Environ. Toxicol. Chem. 2018, 38, 630–637. [Google Scholar] [CrossRef]
- Détrée, C.; Gallardo-Escárate, C. Single and repetitive microplastics exposures induce immune system modulation and homeostasis alteration in the edible mussel Mytilus galloprovincialis. Fish Shellfish Immunol. 2018, 83, 52–60. [Google Scholar] [CrossRef]
- Devriese, L.I.; De Witte, B.; Vethaak, A.D.; Hostens, K.; Leslie, H.A. Bioaccumulation of PCBs from microplastics in Norway lobster (Nephrops norvegicus): An experimental study. Chemosphere 2017, 186, 10–16. [Google Scholar] [CrossRef]
- Welden, N.A.; Cowie, P.R. Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ. Pollut. 2016, 218, 895–900. [Google Scholar] [CrossRef] [Green Version]
- Beiras, R.; Bellas, J.; Cachot, J.; Cormier, B.; Cousin, X.; Engwall, M.; Gambardella, C.; Garaventa, F.; Keiter, S.; Le Bihanic, F.; et al. Ingestion and contact with polyethylene microplastics does not cause acute toxicity on marine zooplankton. J. Hazard. Mater. 2018, 360, 452–460. [Google Scholar] [CrossRef] [Green Version]
- Leung, J.; Chan, K.Y.K. Microplastics reduced posterior segment regeneration rate of the polychaete Perinereis aibuhitensis. Mar. Pollut. Bull. 2018, 129, 782–786. [Google Scholar] [CrossRef]
- Santana, M.F.M.; Moreira, F.T.; Pereira, C.D.S.; Abessa, D.M.S.; Turra, A. Continuous Exposure to Microplastics Does Not Cause Physiological Effects in the Cultivated Mussel Perna perna. Arch. Environ. Contam. Toxicol. 2018, 74, 594–604. [Google Scholar] [CrossRef] [Green Version]
- Rist, S.E.; Assidqi, K.; Zamani, N.P.; Appel, D.; Perschke, M.; Huhn, M.; Lenz, M. Suspended micro-sized PVC particles impair the performance and decrease survival in the Asian green mussel Perna viridis. Mar. Pollut. Bull. 2016, 111, 213–220. [Google Scholar] [CrossRef]
- Gardon, T.; Reisser, C.; Soyez, C.; Quillien, V.; Le Moullac, G. Microplastics Affect Energy Balance and Gametogenesis in the Pearl Oyster Pinctada margaritifera. Environ. Sci. Technol. 2018, 52, 5277–5286. [Google Scholar] [CrossRef] [Green Version]
- Tosetto, L.; Brown, C.; Williamson, J.E. Microplastics on beaches: Ingestion and behavioural consequences for beachhoppers. Mar. Biol. 2016, 163. [Google Scholar] [CrossRef]
- Imhof, H.K.; Laforsch, C. Hazardous or not—Are adult and juvenile individuals of Potamopyrgus antipodarum affected by non-buoyant microplastic particles? Environ. Pollut. 2016, 218, 383–391. [Google Scholar] [CrossRef]
- Kaposi, K.L.; Mos, B.; Kelaher, B.P.; Dworjanyn, S.A. Ingestion of Microplastic Has Limited Impact on a Marine Larva. Environ. Sci. Technol. 2014, 48, 1638–1645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Variable | Dataset | Qm | df | p-Value |
---|---|---|---|---|
Trait | Fish vs. Benthos | 0.034 | / | 0.853 |
Habitat | Fish | 1.735 | 2 | 0.420 |
Benthos | 2.579 | 1 | 0.108 | |
Life stage | Fish | 3.303 | 2 | 0.191 |
Benthos | 1.771 | 2 | 0.412 | |
Trophic level | Fish | 0.039 | 1 | 0.843 |
Benthos | 0.310 | 1 | 0.577 |
Variable | Dataset | Qm | df | p-Value |
---|---|---|---|---|
Type | Fish | 6.394 | 8 | 0.603 |
Benthos | 5.990 | 9 | 0.740 | |
Size | Fish | 1.564 | 4 | 0.815 |
Benthos | 18.484 | 4 | 0.001 | |
Duration | Fish | 5.412 | 7 | 0.609 |
Benthos | 45.663 | 7 | <0.001 | |
Shape | Fish | 0.566 | 2 | 0.753 |
Benthos | 20.312 | 2 | <0.001 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Berlino, M.; Sarà, G.; Mangano, M.C. Functional Trait-Based Evidence of Microplastic Effects on Aquatic Species. Biology 2023, 12, 811. https://doi.org/10.3390/biology12060811
Berlino M, Sarà G, Mangano MC. Functional Trait-Based Evidence of Microplastic Effects on Aquatic Species. Biology. 2023; 12(6):811. https://doi.org/10.3390/biology12060811
Chicago/Turabian StyleBerlino, M., G. Sarà, and M. C. Mangano. 2023. "Functional Trait-Based Evidence of Microplastic Effects on Aquatic Species" Biology 12, no. 6: 811. https://doi.org/10.3390/biology12060811
APA StyleBerlino, M., Sarà, G., & Mangano, M. C. (2023). Functional Trait-Based Evidence of Microplastic Effects on Aquatic Species. Biology, 12(6), 811. https://doi.org/10.3390/biology12060811