The Ecotoxicological Effects of Microplastics on Primary Producers in the Marine Environment

Authors

  • Mahibul Islam Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden
  • Mahmudul Hasan Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden
  • Bhaskar Chandra Majudmar Department of Fisheries Technology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur-1706, Bangladesh
  • Sulav Indra Paul Institute of Biotechnology and Genetic Engineering, Bangabandhu Sheikh Mujibur Rahman Agricultural University,Gazipur-1706, Bangladesh

DOI:

https://doi.org/10.30564/jfsr.v2i2.1906

Abstract

Plastic debris is an emerging environmental threat all over the world. But its effect and distribution in the marine ecosystem is barely known. Microplastics abundance in the marine vegetated area is about 2 to 3 times higher than the bare site in the ocean. Although seagrass meadows trap huge amount of microplastics over the ocean floor, a considerable amount of microplastics are also sink incorporating with the marine aggregates from the epipelagic zone of the ocean. Scavenging of microplastics by diatom aggregation decreases the sinking rate of them rather than cryptophyte. As we know, marine snow is the leading carbon source for zoobenthos, but the ubiquitous presence of microplastics damages cell of different microalgae which may alter the food webs of marine ecosystems. Additionally, microplastics releases immense amount of dissolved organic carbons (DOC) in the surrounding seawater that stimulates the growth of heterotrophic microorganisms as well as their functional activity. Plastic debris result in outbreaks of disease in the marine environment and coral reefs are highly affected by it. When coral reef comes in contact with microplastics, the disease infestation rate of the reef increases massively. Three major disease viz., skeletal eroding band, white syndrome and black band of coral reef causes approximately 46% of reef mortality due to microplastics consumption. Due to complex structure and size, the corals accumulates huge amount of microplastics that increases growth of pathogens by hampering the coral immune system. Existing scientific evidence presents that exposure of microplastics in aquatic environments triggers a wide variety of toxic insult from feeding disruption to reproductive performance, disturbances in energy metabolism throughout the ocean. The present review focused on the ecotoxicological effect of microplastics on primary producers of ocean, its uptake, accumulation, and excretion, and its probable toxicity with risk assessment approaches.

Keywords:

Microplastics, Marine, DOC, Microorganisms, Ecological impact, Ecotoxicology

References

[1] Barnes DKA, Galgani F, Thompson RC, Barlaz M. Accumulation and fragmentation of plastic debris in global environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 2009, 364(1526): 1985-1998.

[2] Derraik JGB. The pollution of the marine environment by plastic debris: a review. Marine Pollution Bulletin, 2002, 44(9): 842-852.

[3] Europe P. Plastics-The Facts 2013: An analysis of European latest plastics production, demand and waste data. In: Plastic Europe, 2013: 40.

[4] Andrady AL, Neal MA. Applications and societal benefits of plastics. Philosophical Transactions of the Royal Society B: Biological Sciences 2009, 364(1526): 1977-1984.

[5] Browne MA, Crump P, Niven SJ, Teuten E, Tonkin A, Galloway T, et al. Accumulation of microplastic on shorelines woldwide: sources and sinks. Environmental Science & Technology, 2011, 45(21): 9175-9179.

[6] Zitko V, Hanlon M. Another source of pollution by plastics: skin cleaners with plastic scrubbers. Marine Pollution Bulletin, 1991, 22(1): 41-42.

[7] Sivan A. New perspectives in plastic biodegradation. Current Opinion in Biotechnology, 2011, 22(3): 422- 426.

[8] Wright SL, Thompson RC, Galloway TS. The physical impacts of microplastics on marine organisms: a review. Environmental Pollution, 2013, 178: 483- 492.

[9] Andrady AL. Microplastics in the marine environment. Marine Pollution Bulletin, 2011, 62(8): 1596- 1605.

[10] Thompson RC, Olsen Y, Mitchell RP, Davis A, Rowland SJ, John AWG, et al. Lost at sea: where is all the plastic? Science, 2004, 304(5672): 838-838.

[11] Claessens M, Meester SD, Landuyt LV, Clerck KD, Janssen CR. Occurrence and distribution of microplastics in marine sediments along the Belgian coast. Marine Pollution Bulletin, 2011, 62(10): 2199-2204.

[12] Graham ER, Thompson JT. Deposit-and suspension-feeding sea cucumbers (Echinodermata) ingest plastic fragments. Journal of Experimental Marine Biology and Ecology, 2009, 368(1): 22-29.

[13] Nor NHM, Obbard JP. Microplastics in Singapore’s coastal mangrove ecosystems. Marine Pollution Bulletin, 2014, 79(1-2): 278-283.

[14] Dantas DV, Barletta M, Costa MFD. The seasonal and spatial patterns of ingestion of polyfilament nylon fragments by estuarine drums (Sciaenidae). Environmental Science and Pollution Research, 2012, 19(2): 600-606.

[15] Eriksson C, Burton H. Origins and biological accumulation of small plastic particles in fur seals from Macquarie Island. A Journal of the Human Environment,2003, 32(6): 380-384.

[16] Jantz LA, Morishige CL, Bruland GL, Lepczyk CA. Ingestion of plastic marine debris by longnose lancetfish (Alepisaurus ferox) in the North Pacific Ocean. Marine pollution bulletin, 2013, 69(1-2): 97-104.

[17] Browne MA, Galloway TS, Thompson RC. Spatial patterns of plastic debris along estuarine shorelines. Environmental Science & Technology, 2010, 44(9): 3404-3409.

[18] Lattin GL, Moore CJ, Zellers AF, Moore SL, Weisberg SB. A comparison of neustonic plastic and zooplankton at different depths near the southern California shore. Marine Pollution Bulletin, 2004, 49(4): 291-294.

[19] Doyle MJ, Watson W, Bowlin NM, Sheavly SB. Plastic particles in coastal pelagic ecosystems of the Northeast Pacific ocean. Marine Environmental Research, 2011, 71(1): 41-52.

[20] Goldstein MC, Titmus AJ, Ford M. Scales of spatial heterogeneity of plastic marine debris in the northeast Pacific Ocean. PloS One, 2013, 8(11): e80020.

[21] Law KL, Morét-Ferguson S, Maximenko NA, Proskurowski G, Peacock EE, Hafner J, et al. Plastic accumulation in the North Atlantic subtropical gyre. Science, 2010, 329(5996): 1185-1188.

[22] Morét-Ferguson S, Law KL, Proskurowski G, Murphy EK, Peacock EE, Reddy CM. The size, mass, and composition of plastic debris in the western North Atlantic Ocean. Marine Pollution Bulletin, 2010, 60(10): 1873-1878.

[23] Van-Cauwenberghe L, Claessens M, Vandegehuchte MB, Mees J, Janssen CR. Assessment of marine debris on the Belgian continental shelf. Marine Pollution Bulletin, 2013, 73(1): 161-169.

[24] Norén F. Small plastic particles in coastal Swedish waters. In: N-Research Report. commissioned by KIMO Sweden (Submitted to BDC), 2007.

[25] Moore CJ, Moore SL, Leecaster MK, Weisberg SB. A comparison of plastic and plankton in the North Pacific central gyre. Marine pollution bulletin, 2001, 42(12): 1297-1300.

[26] Shim WJ, Hong SH, Eo S. Marine microplastics: abundance, distribution, and composition. In: Microplastic Contamination in Aquatic Environments: Elsevier, 2018: 1-26.

[27] Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger J, et al. Microplastic ingestion by zooplankton. Environmental Science & Technology, 2013, 47(12): 6646-6655.

[28] Lee H, Shim WJ, Kwon JH. Sorption capacity of plastic debris for hydrophobic organic chemicals. Science of the Total Environment, 2014, 470-471: 1545-1552.

[29] Wang F, Wong CS, Chen D, Lu X, Wang F, Zeng EY. Interaction of toxic chemicals with microplastics: a critical review. Water Research, 2018, 139: 208-219.

[30] Zhang H, Zhou Q, Xie Z, Zhou Y, Tu C, Fu C, et al. Occurrences of organophosphorus esters and phthalates in the microplastics from the coastal beaches in north China. Science of the Total Environment, 2018, 616-617: 1505-1512.

[31] Brennecke D, Duarte B, Paiva F, Caçador I, Canning-Clode J. Microplastics as vector for heavy metal contamination from the marine environment. Estuarine, Coastal and Shelf Science, 2016, 178: 189-195.

[32] Vedolin MC, Teophilo CYS, Turra A, Figueira RCL. Spatial variability in the concentrations of metals in beached microplastics. Marine Pollution Bulletin,2018, 129(2): 487-493.

[33] Liu H, Tang L, Liu Y, Zeng G, Lu Y, Wang J, et al. Wetland-a hub for microplastic transmission in the global ecosystem. Resources, Conservation & Recycling, 2019, 142: 153-154.

[34] Zedler JB. Progress in wetland restoration ecology. Trends in Ecology & Evolution, 2000, 15(10): 402- 407.

[35] Herr D, Landis E. Coastal blue carbon ecosystems. In: Opportunities for Nationally Determined Contributions Policy Brief. Gland, Switzerland: IUCN. Washington, DC: TNC, 2016.

[36] Gullström M, Lyimo LD, Dahl M, Samuelsson GS, Eggertsen M, Anderberg E, et al. Blue carbon storage in tropical seagrass meadows relates to carbonate stock dynamics, plant–sediment processes, and landscape context: insights from the western Indian Ocean. Ecosystems, 2018, 21(3): 551-566.

[37] Boström C, Törnroos A, Bonsdorff E. Invertebrate dispersal and habitat heterogeneity: expression of biological traits in a seagrass landscape. Journal of Experimental Marine Biology and Ecology, 2010, 390(2): 106-117.

[38] Butman CA, Grassle JP, Webb CM. Substrate choices made by marine larvae settling in still water and in a flume flow. Nature, 1988, 333(6175): 771-773.

[39] Gacia E, Granata TC, Duarte CM. An approach to measurement of particle flux and sediment retention within seagrass (Posidonia oceanica) meadows. Aquatic Botany, 1999, 65(1-4): 255-268.

[40] Huang Y, Xiao X, Xu C, Perianen YD, Hu J, Holmer M. Seagrass beds acting as a trap of microplastics-Emerging hotspot in the coastal region? Environmental Pollution, 2020, 257: 113450.

[41] Barber RT. Dissolved organic carbon from deep waters resists microbial oxidation. Nature, 1968, 220(5164): 274-275.

[42] Hansell DA. Recalcitrant dissolved organic carbon fractions. Annual Review of Marine Science, 2013, 5: 421-445.

[43] Williams PM, Druffel ERM. Radiocarbon in dissolved organic matter in the central North Pacific Ocean. Nature, 1987, 330(6145): 246-248.

[44] Benner R, Amon RMW. The size-reactivity continuum of major bioelements in the ocean. Annual Review of Marine Science, 2015, 7: 185-205.

[45] Hansell DA, Carlson CA, Repeta DJ, Schlitzer R. Dissolved organic matter in the ocean: A controversy stimulates new insights. Oceanography, 2009, 22(4): 202-211.

[46] Prather MJ, Holmes CD, Hsu J. Reactive greenhouse gas scenarios: Systematic exploration of uncertainties and the role of atmospheric chemistry. Geophysical Research Letters, 2012, 39(9): L09803.

[47] Romera-Castillo C, Letscher RT, Hansell DA. New nutrients exert fundamental control on dissolved organic carbon accumulation in the surface Atlantic Ocean. Proceedings of the National Academy of Sciences, 2016, 113(38): 10497-10502.

[48] Romera-Castillo C, Pinto M, Langer TM, Álvarez-Salgado XA, Herndl GJ. Dissolved organic carbon leaching from plastics stimulates microbial activity in the ocean. Nature Communications, 2018; 9(1): 1430.

[49] Cózar A, Echevarría F, González-Gordillo JI, Irigoien X, Úbeda B, Hernández-León S, et al. Plastic debris in the open ocean. Proceedings of the National Academy of Sciences, 2014, 111(28): 10239-10244.

[50] Eriksen M, Lebreton LCM, Carson HS, Thiel M, Moore CJ, Borerro JC, 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, 2014, 9(12): e111913.

[51] Woodall LC, Sanchez-Vidal A, Canals M, Paterson GLJ, Coppock R, Sleight V, et al. The deep sea is a major sink for microplastic debris. Royal Society Open Science, 2014, 1(4): 140317.

[52] Collignon A, Hecq JH, Glagani F, Voisin P, Collard F, Goffart A. Neustonic microplastic and zooplankton in the North Western Mediterranean Sea. Marine Pollution Bulletin, 2012, 64(4): 861-864.

[53] Barnes DKA, Milner P. Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean. Marine Biology, 2005, 146(4): 815-825.

[54] Zettler ER, Mincer TJ, Amaral-Zettler LA. Life in the “plastisphere”: microbial communities on plastic marine debris. Environmental Science & Technology, 2013, 47(13): 7137-7146.

[55] Staats N, Stal LJ, Mur LR. Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions. Journal of Experimental Marine Biology and Ecology, 2000, 249(1): 13-27.

[56] Passow U. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography, 2002, 55(3-4): 287-333.

[57] Underwood GJC, Boulcott M, Raines CA, Waldron K. Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. Journal of Phycology, 2004, 40(2): 293-304.

[58] Engel A. The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (α) during the decline of a diatom bloom. Journal of Plankton Research, 2000, 22(3): 485-497.

[59] Wright SL, Rowe D, Thompson RC, Galloway TS. Microplastic ingestion decreases energy reserves in marine worms. Current Biology, 2013, 23(23): R1031-R1033.

[60] Long M, Moriceau B, Gallinari M, Lambert C, Huvet A, Raffray J, et al. Interactions between microplastics and phytoplankton aggregates: Impact on their respective fates. Marine Chemistry, 2015, 175: 39- 46.

[61] Boerger CM, Lattin GL, Moore SL, Moore CJ. Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin, 2010, 60(12): 2275-2278.

[62] Carson HS. The incidence of plastic ingestion by fishes: From the prey’s perspective. Marine Pollution Bulletin, 2013, 74(1): 170-174.

[63] Farrell P, Nelson K. Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environmental Pollution, 2013, 177: 1-3.

[64] Fossi MC, Panti C, Guerranti C, Coppola D, Giannetti M, Marsili L, et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Marine Pollution Bulletin, 2012, 64(11): 2374-2379.

[65] McCormick A, Hoellein TJ, Mason SA, Schluep J, Kelly JJ. Microplastic is an abundant and distinct microbial habitat in an urban river. Environmental Science & Technology, 2014, 48(20): 11863-11871.

[66] Welden NAC, Cowie PR. Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environmental Pollution, 2016, 218: 895-900.

[67] Isobe A, Uchiyama-Matsumoto K, Uchida K, Tokai T. Microplastics in the Southern Ocean. Marine Pollution Bulletin, 2017, 114(1): 623-626.

[68] Veerasingam S, Mugilarasan M, Venkatachalapathy R, Vethamony P. Influence of 2015 flood on the distribution and occurrence of microplastic pellets along the Chennai coast, India. Marine Pollution Bulletin, 2016, 109(1): 196-204.

[69] Zhang C, Chen X, Wang J, Tan L. Toxic effects of microplastic on marine microalgae Skeletonema costatum: interactions between microplastic and algae. Environmental Pollution, 2017, 220: 1282-1288.

[70] Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, et al. Climate warming and disease risks for terrestrial and marine biota. Science, 2002, 296(5576): 2158-2162.

[71] Kirstein IV, Kirmizi S, Wichels A, Garin-Fernandez A, Erler R, Martin L, et al. Dangerous hitchhikers? Evidence for potentially pathogenic Vibrio spp. on microplastic particles. Marine Environmental Research, 2016, 120: 1-8.

[72] Bourne DG, Ainsworth TD, Pollock FJ, Willis BL. Towards a better understanding of white syndromes and their causes on Indo-Pacific coral reefs. Coral Reefs, 2015, 34(1): 233-242.

[73] Fazey FMC, Ryan PG. Biofouling on buoyant marine plastics: An experimental study into the effect of size on surface longevity. Environmental Pollution, 2016, 210: 354-360.

[74] Linders T, Infantes E, Joyce A, Karlsson T, Ploug H, Hassellöv M, et al. Particle sources and transport in stratified Nordic coastal seas in the Anthropocene. Elementa Science of the Anthropocene, 2018, 6(1).

[75] Abdelrhman MA. Effect of eelgrass Zostera marina canopies on flow and transport. Marine Ecology Progress Series, 2003, 248: 67-83.

[76] Duarte CM, Kennedy H, Marbà N, Hendriks I. Assessing the capacity of seagrass meadows for carbon burial: current limitations and future strategies. Ocean and Coastal Management, 2013, 83: 32-38.

[77] Fonseca MS, Koehl MAR, Fourqurean JW. Effect of Seagrass on current speed: importance of flexibility versus shoot density. Frontiers in Marine Science, 2019, 6: 376.

[78] Miyajima T, Hori M, Hamaguchi M, Shimabukuro H, Adachi H, Yamano H, et al. Geographic variability in organic carbon stock and accumulation rate in sediments of East and Southeast Asian seagrass meadows. Global Biogeochemical Cycles, 2015, 29(4): 397-415.

[79] Röhr ME, Holmer M, Baum JK, Björk M, Boyer K, Chin D, et al. Blue carbon storage capacity of temperate eelgrass (Zostera marina) meadows. Global Biogeochemical Cycles, 2018, 32(10): 1457-1475.

[80] A’an JW, Rahmawati S, Prayudha B, Iskandar MR, Arfianti T. Vertical carbon flux of marine snow in Enhalus acoroides-dominated seagrass meadows. Regional Studies in Marine Science, 2016, 5: 27-34.

[81] Hendriks IE, Sintes T, Bouma TJ, Duarte CM. Experimental assessment and modeling evaluation of the effects of the seagrass Posidonia oceanica on flow and particle trapping. Marine Ecology Progress Series, 2008, 356: 163-173.

[82] Lo H-S, Xu X, Wong CY, Cheung SG. Comparisons of microplastic pollution between mudflats and sandy beaches in Hong Kong. Environmental Pollution, 2018, 236: 208-217.

[83] Martin C, Almahasheer H, Duarte CM. Mangrove forests as traps for marine litter. Environmental Pollution, 2019, 247: 499-508.

[84] Karapanagioti HK, Klontza I. Testing phenanthrene distribution properties of virgin plastic pellets and plastic eroded pellets found on Lesvos island beaches (Greece). Marine Environmental Research, 2008, 65(4): 283-290.

[85] Bakir A, Rowland SJ, Thompson RC. Transport of persistent organic pollutants by microplastics in estuarine conditions. Estuarine, Coastal Shelf Science, 2014, 140: 14-21.

[86] Gewert B, Plassmann MM, MacLeod M. Pathways for degradation of plastic polymers floating in the marine environment. Environmental Science: Processes Impacts, 2015, 17(9): 1513-1521.

[87] Anesio AM, Granéli W, Aiken GR, Kieber DJ, Mopper K. Effect of humic substance photodegradation on bacterial growth and respiration in lake water. Applied and Environmental Microbiology, 2005, 71(10): 6267-6275.

[88] Xiao F, Li X, Lam K, Wang D. Investigation of the hydrodynamic behavior of diatom aggregates using particle image velocimetry. Journal of Environmental Sciences, 2012, 24(7): 1157-1164.

[89] Chen P, Powell BA, Mortimer M, Ke PC. Adaptive interactions between zinc oxide nanoparticles and Chlorella sp. Environmental Science & Technology, 2012, 46(21): 12178-12185.

[90] Quigg A, Chin WC, Chen CS, Zhang S, Jiang Y, Miao AJ, et al. Direct and indirect toxic effects of engineered nanoparticles on algae: role of natural organic matter. ACS Sustainable Chemistry & Engineering, 2013, 1(7): 686-702.

[91] Mao Y, Ai H, Chen Y, Zhang Z, Zeng P, Kang L, et al. Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere, 2018, 208: 59-68.

[92] Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryman M, Andrady A, et al. Plastic waste inputs from land into the ocean. Science, 2015, 347(6223): 768- 771.

[93] Ward JE, Kach DJ. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Marine Environmental Research, 2009, 68(3): 137-142.

[94] Davarpanah E, Guilhermino L. Single and combined effects of microplastics and copper on the population growth of the marine microalgae Tetraselmis chuii. Estuarine, Coastal and Shelf Science, 2015, 167: 269-275.

[95] Lyakurwa DJ. Uptake and effects of microplastic particles in selected marine microalgae species; Oxyrrhis marina and Rhodomonas baltica [MSc Thesis]: Norwegian University of Science and Technology (NTNU). 2017.

[96] Lamb JB, Willis BL, Fiorenza EA, Couch CS, Howard R, Rader DN, et al. Plastic waste associated with disease on coral reefs. Science, 2018, 359(6374): 460-462.

[97] Altizer S, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD. Climate change and infectious diseases: from evidence to a predictive framework. Science, 2013, 341(6145): 514-519.

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