The Effects of Combined Ocean Acidification and Nanoplastic Exposures on the Embryonic Development of Antarctic Krill

In aquatic environments, plastic pollution occurs concomitantly with anthropogenic climate stressors such as ocean acidification. Within the Southern Ocean, Antarctic krill (Euphausia Superba) support many marine predators and play a key role in the biogeochemical cycle. Ocean acidification and plastic pollution have been acknowledged to hinder Antarctic krill development and physiology in singularity, however potential multi-stressor effects of plastic particulates coupled with ocean acidification are unexplored. Furthermore, Antarctic krill may be especially vulnerable to plastic pollution due to their close association with sea-ice, a known plastic sink. Here, we investigate the behaviour of nanoplastic [spherical, aminated (NH2), and yellow-green fluorescent polystyrene nanoparticles] in Antarctic seawater and explore the single and combined effects of nanoplastic (160 nm radius, at a concentration of 2.5 μg ml–1) and ocean acidification (pCO2 ∼900, pHT 7.7) on the embryonic development of Antarctic krill. Gravid female krill were collected in the Atlantic sector of the Southern Ocean (North Scotia Sea). Produced eggs were incubated at 0.5 °C in four treatments (control, nanoplastic, ocean acidification and the multi-stressor scenario of nanoplastic presence, and ocean acidification) and their embryonic development after 6 days, at the incubation endpoint, was determined. We observed that negatively charged nanoplastic particles suspended in seawater from the Scotia Sea aggregated to sizes exceeding the nanoscale after 24 h (1054.13 ± 53.49 nm). Further, we found that the proportion of embryos developing through the early stages to reach at least the limb bud stage was highest in the control treatment (21.84%) and lowest in the multi-stressor treatment (13.17%). Since the biological thresholds to any stressors can be altered by the presence of additional stressors, we propose that future nanoplastic ecotoxicology studies should consider the changing global ocean under future climate scenarios for assessments of their impact and highlight that determining the behaviour of nanoplastic particles used in incubation studies is critical to determining their toxicity.

[1]  T. Galloway,et al.  A Polar outlook: Potential interactions of micro- and nano-plastic with other anthropogenic stressors. , 2021, The Science of the total environment.

[2]  E. Murphy,et al.  Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean , 2020, Nature Communications.

[3]  E. Bergami,et al.  Nanoplastics affect moulting and faecal pellet sinking in Antarctic krill (Euphausia superba) juveniles. , 2020, Environment international.

[4]  Kathryn E. L. Smith,et al.  Fluctuating seawater pCO2/pH induces opposing interactions with copper toxicity for two intertidal invertebrates. , 2020, The Science of the total environment.

[5]  S. Kawaguchi,et al.  Temperature–Induced Hatch Failure and Nauplii Malformation in Antarctic Krill , 2020, Frontiers in Marine Science.

[6]  G. Grassi,et al.  Behavior and Bio-Interactions of Anthropogenic Particles in Marine Environment for a More Realistic Ecological Risk Assessment , 2020, Frontiers in Environmental Science.

[7]  T. Galloway,et al.  Close encounters - microplastic availability to pelagic amphipods in sub-antarctic and antarctic surface waters. , 2020, Environment international.

[8]  A. Kelly,et al.  Microplastic contamination in east Antarctic sea ice. , 2020, Marine pollution bulletin.

[9]  A. Sfriso,et al.  Microplastic accumulation in benthic invertebrates in Terra Nova Bay (Ross Sea, Antarctica). , 2020, Environment international.

[10]  P. Ryan,et al.  Floating macro- and microplastics around the Southern Ocean: Results from the Antarctic Circumnavigation Expedition. , 2020, Environment international.

[11]  M. Renzi,et al.  PET microplastics toxicity on marine key species is influenced by pH, particle size and food variations. , 2020, The Science of the total environment.

[12]  P. Kukliński,et al.  Offshore surface waters of Antarctica are free of microplastics, as revealed by a circum-Antarctic study. , 2019, Marine pollution bulletin.

[13]  Youji Wang,et al.  Microplastics impair digestive performance but show little effects on antioxidant activity in mussels under low pH conditions. , 2019, Environmental pollution.

[14]  A. Catarino,et al.  Use of fluorescent-labelled nanoplastics (NPs) to demonstrate NP absorption is inconclusive without adequate controls. , 2019, The Science of the total environment.

[15]  M. Oliviero,et al.  Leachates of micronized plastic toys provoke embryotoxic effects upon sea urchin Paracentrotus lividus. , 2019, Environmental pollution.

[16]  C. Cárdenas,et al.  Polystyrene nanoparticles affect the innate immune system of the Antarctic sea urchin Sterechinus neumayeri , 2019, Polar Biology.

[17]  A. Huvet,et al.  Surface functionalization determines behavior of nanoplastic solutions in model aquatic environments. , 2019, Chemosphere.

[18]  F. Kessler,et al.  Plastics in sea surface waters around the Antarctic Peninsula , 2019, Scientific Reports.

[19]  S. Henson,et al.  Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone , 2019, Nature Communications.

[20]  Taejoon Kang,et al.  Bioaccumulation of polystyrene nanoplastics and their effect on the toxicity of Au ions in zebrafish embryos. , 2019, Nanoscale.

[21]  Anja Verschoor,et al.  Are We Speaking the Same Language? Recommendations for a Definition and Categorization Framework for Plastic Debris. , 2019, Environmental science & technology.

[22]  A. Huvet,et al.  Nanoplastics impaired oyster free living stages, gametes and embryos. , 2018, Environmental pollution.

[23]  R. Goto,et al.  Microinjection of Marine Fish Eggs. , 2018, Methods in molecular biology.

[24]  A. Huvet,et al.  Cellular responses of Pacific oyster (Crassostrea gigas) gametes exposed in vitro to polystyrene nanoparticles. , 2018, Chemosphere.

[25]  W. Cheung,et al.  Projected amplification of food web bioaccumulation of MeHg and PCBs under climate change in the Northeastern Pacific , 2018, Scientific Reports.

[26]  Richard C. Thompson,et al.  Microplastics in marine sediments near Rothera Research Station, Antarctica. , 2018, Marine pollution bulletin.

[27]  T. Krumpen,et al.  Arctic sea ice is an important temporal sink and means of transport for microplastic , 2018, Nature Communications.

[28]  R. Obbard Microplastics in Polar Regions: The role of long range transport , 2018 .

[29]  Jeffrey Farner Budarz,et al.  Microplastics and Nanoplastics in Aquatic Environments: Aggregation, Deposition, and Enhanced Contaminant Transport. , 2017, Environmental science & technology.

[30]  A. ter Halle,et al.  Nanoplastic in the North Atlantic Subtropical Gyre. , 2017, Environmental science & technology.

[31]  G. Grassi,et al.  Comparative ecotoxicity of polystyrene nanoparticles in natural seawater and reconstituted seawater using the rotifer Brachionus plicatilis. , 2017, Ecotoxicology and environmental safety.

[32]  H. Lotze,et al.  Plastic as a Persistent Marine Pollutant , 2017 .

[33]  C. Corinaldesi,et al.  Microplastics in the sediments of Terra Nova Bay (Ross Sea, Antarctica). , 2017, Marine pollution bulletin.

[34]  K. Dawson,et al.  Long-term toxicity of surface-charged polystyrene nanoplastics to marine planktonic species Dunaliella tertiolecta and Artemia franciscana. , 2017, Aquatic toxicology.

[35]  R. Geyer,et al.  Production, use, and fate of all plastics ever made , 2017, Science Advances.

[36]  A. D. Vethaak,et al.  The adverse effects of virgin microplastics on the fertilization and larval development of sea urchins. , 2017, Marine environmental research.

[37]  S. Corsolini,et al.  Microplastic in the surface waters of the Ross Sea (Antarctica): Occurrence, distribution and characterization by FTIR. , 2017, Chemosphere.

[38]  C. Lewis,et al.  Interactions of microplastic debris throughout the marine ecosystem , 2017, Nature Ecology &Evolution.

[39]  K. Dawson,et al.  Amino-modified polystyrene nanoparticles affect signalling pathways of the sea urchin (Paracentrotus lividus) embryos , 2017, Nanotoxicology.

[40]  A. Isobe,et al.  Microplastics in the Southern Ocean. , 2017, Marine pollution bulletin.

[41]  M. Di Carlo,et al.  Oxidative responsiveness to multiple stressors in the key Antarctic species, Adamussium colbecki: Interactions between temperature, acidification and cadmium exposure. , 2016, Marine environmental research.

[42]  J. Lavers,et al.  Plastic ingestion by fish in the Southern Hemisphere: A baseline study and review of methods. , 2016, Marine pollution bulletin.

[43]  C. Lewis,et al.  Ocean acidification increases copper toxicity differentially in two key marine invertebrates with distinct acid-base responses , 2016, Scientific Reports.

[44]  Wei Shi,et al.  Ocean acidification increases cadmium accumulation in marine bivalves: a potential threat to seafood safety , 2016, Scientific Reports.

[45]  Camille Mellin,et al.  A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae , 2015, Global change biology.

[46]  K. Hobson,et al.  Changes in food web structure alter trends of mercury uptake at two seabird colonies in the Canadian Arctic. , 2014, Environmental science & technology.

[47]  K. Dawson,et al.  Accumulation and embryotoxicity of polystyrene nanoparticles at early stage of development of sea urchin embryos Paracentrotus lividus. , 2014, Environmental science & technology.

[48]  E. Murphy,et al.  Krill, climate, and contrasting future scenarios for Arctic and Antarctic fisheries , 2014 .

[49]  S. Kawaguchi,et al.  A photographic documentation of the development of Antarctic krill (Euphausia superba) from egg to early juvenile , 2014, Polar Biology.

[50]  A. Ishida,et al.  Risk maps for Antarctic krill under projected Southern Ocean acidification , 2013 .

[51]  M. Collins,et al.  Spatial and Temporal Operation of the Scotia Sea Ecosystem , 2012 .

[52]  A. Ishida,et al.  Will krill fare well under Southern Ocean acidification? , 2011, Biology Letters.

[53]  S. Dupont,et al.  Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification , 2011, Journal of Experimental Biology.

[54]  A. Kiderman,et al.  Are we speaking the same language? , 2011, Journal of evaluation in clinical practice.

[55]  Pierre-Yves Pascal,et al.  The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. , 2010, Marine pollution bulletin.

[56]  Fengchang Wu,et al.  Fate and transport of engineered nanomaterials in the environment. , 2010, Journal of environmental quality.

[57]  H. Pörtner,et al.  Impact of Ocean Acidification on Energy Metabolism of Oyster, Crassostrea gigas—Changes in Metabolic Pathways and Thermal Response , 2010, Marine drugs.

[58]  Charles B. Miller,et al.  Embryo biometry of three broadcast spawning euphausiid species applied to identify cross-shelf and seasonal spawning patterns along the Oregon coast , 2010 .

[59]  V. Fabry,et al.  Ocean Acidification at High Latitudes: The Bellwether , 2009 .

[60]  F. Millero,et al.  Effect of ocean acidification on the speciation of metals in seawater , 2009 .

[61]  R. Quinta-Ferreira,et al.  The influence of pH on the leaching behaviour of inorganic components from municipal solid waste APC residues. , 2009, Waste management.

[62]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[63]  V. Siegel,et al.  A re-appraisal of the total biomass and annual production of Antarctic krill , 2009 .

[64]  H. Kurihara Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates , 2008 .

[65]  Richard J. Matear,et al.  Southern Ocean acidification: A tipping point at 450-ppm atmospheric CO2 , 2008, Proceedings of the National Academy of Sciences.

[66]  Richard C. Thompson,et al.  Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L). , 2008, Environmental science & technology.

[67]  M. Collins,et al.  Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  Richard A. Feely,et al.  Global relationships of total alkalinity with salinity and temperature in surface waters of the world's oceans , 2006 .

[69]  S. Kashiwada,et al.  Distribution of Nanoparticles in the See-through Medaka (Oryzias latipes) , 2006, Environmental health perspectives.

[70]  Peter Rothery,et al.  Natural growth rates in Antarctic krill (Euphausia superba): II. Predictive models based on food, temperature, body length, sex, and maturity stage , 2006 .

[71]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[72]  J. Gómez‐Gutiérrez,et al.  Embryonic, early larval development time, hatching mechanism and interbrood period of the sac-spawning euphausiid Nyctiphanes simplex Hansen , 2005 .

[73]  S. Kawaguchi,et al.  Effect of temperature on embryo development time and hatching success of the Antarctic krill Euphausia superba Dana in the laboratory , 2004 .

[74]  W. Norwood,et al.  Effects of Metal Mixtures on Aquatic Biota: A Review of Observations and Methods , 2003 .

[75]  L. Zane,et al.  Krill: a possible model for investigating the effects of ocean currents on the genetic structure of a pelagic invertebrate , 2000 .

[76]  D. Wallace,et al.  Program developed for CO{sub 2} system calculations , 1998 .

[77]  C. Goyet,et al.  Distribution of carbon dioxide partial pressure in surface waters of the Southwest Indian Ocean , 1991 .

[78]  A. Dickson Standard potential of the reaction: , and and the standard acidity constant of the ion HSO4− in synthetic sea water from 273.15 to 318.15 K , 1990 .

[79]  F. Millero,et al.  A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media , 1987 .

[80]  T. Ikeda,et al.  Laboratory observations on spawning, brood size and egg hatchability of the Antarctic krill Euphausia superba from Prydz Bay, Antarctica , 1986 .

[81]  L. Quetin,et al.  Depth distribution of developing Euphausia superba embryos, predicted from sinking rates , 1984 .

[82]  T. Ikeda Development of the larvae of the Antarctic krill (Euphausia superba Dana) observed in the laboratory , 1984 .

[83]  C. Culberson,et al.  MEASUREMENT OF THE APPARENT DISSOCIATION CONSTANTS OF CARBONIC ACID IN SEAWATER AT ATMOSPHERIC PRESSURE1 , 1973 .

[84]  J. Edmond High precision determination of titration alkalinity and total carbon dioxide content of sea water by potentiometric titration , 1970 .

[85]  V. Tirelli,et al.  Microplastics in Polar Samples , 2020 .

[86]  Isa Doverbratt,et al.  Nanoplastics in the aquatic environment , 2018 .

[87]  Kenneth A Dawson,et al.  Nano-sized polystyrene affects feeding, behavior and physiology of brine shrimp Artemia franciscana larvae. , 2016, Ecotoxicology and environmental safety.

[88]  Ellen Besseling,et al.  Nanoplastics in the Aquatic Environment. Critical Review , 2015 .

[89]  J. Schnoor Ocean acidification. , 2013, Environmental science & technology.

[90]  B. Blaine a review and meta-analysis , 2006 .

[91]  J. Priddle,et al.  An assessment of the merits of length and weight measurements of Antarctic krill Euphausia superba , 1988 .