Bioavailability of Microplastics to Marine Zooplankton: Effect of Shape and Infochemicals.

The underlying mechanisms that influence microplastic ingestion in marine zooplankton remain poorly understood. Here, we investigate how microplastics of a variety of shapes (bead, fiber, and fragment), in combination with the algal-derived infochemicals dimethyl sulfide (DMS) and dimethylsulfoniopropionate (DMSP), affect the ingestion rate of microplastics in three species of zooplankton, the copepods Calanus helgolandicus and Acartia tonsa and larvae of the European lobster Homarus gammarus. We show that shape affects microplastic bioavailability to different species of zooplankton, with each species ingesting significantly more of a certain shape: C. helgolandicus-fragments (P < 0.05); A. tonsa-fibers (P < 0.01); H. gammarus larvae-beads (P < 0.05). Thus, different feeding strategies between species may affect shape selectivity. Our results also showed significantly increased ingestion rates by C. helgolandicus on all microplastics that were infused with DMS (P < 0.01) and by H. gammarus larvae and A. tonsa on DMS-infused fibers and fragments (P < 0.05). By using a range of more environmentally relevant microplastics, our findings highlight how the feeding strategies of different zooplankton species may influence their susceptibility to microplastic ingestion. Furthermore, our novel study suggests that species reliant on chemosensory cues to locate their prey may be at an increased risk of ingesting aged microplastics in the marine environment.

[1]  M. Renzi,et al.  Marine Litter , 2021, Journal of Marine Science and Engineering.

[2]  C. Lewis,et al.  Are we underestimating microplastic abundance in the marine environment? A comparison of microplastic capture with nets of different mesh-size. , 2020, Environmental pollution.

[3]  L. Amaral-Zettler,et al.  Ecology of the plastisphere , 2020, Nature Reviews Microbiology.

[4]  Elaine S. Fileman,et al.  Microplastics alter feeding selectivity and faecal density in the copepod, Calanus helgolandicus. , 2019, The Science of the total environment.

[5]  T. Hofmann,et al.  The composition of bacterial communities associated with plastic biofilms differs between different polymers and stages of biofilm succession , 2019, PloS one.

[6]  T. Galloway,et al.  Effects of Nylon Microplastic on Feeding, Lipid Accumulation, and Moulting in a Coldwater Copepod , 2019, Environmental science & technology.

[7]  Richard C. Thompson,et al.  Bioavailability and effects of microplastics on marine zooplankton: A review. , 2019, Environmental Pollution.

[8]  Elaine S. Fileman,et al.  Smells good enough to eat: Dimethyl sulfide (DMS) enhances copepod ingestion of microplastics. , 2019, Marine pollution bulletin.

[9]  June-Woo Park,et al.  Toxicological effects of irregularly shaped and spherical microplastics in a marine teleost, the sheepshead minnow (Cyprinodon variegatus). , 2018, Marine pollution bulletin.

[10]  Kit Yu Karen Chan,et al.  Negative effects of microplastic exposure on growth and development of Crepidula onyx. , 2018, Environmental pollution.

[11]  B. Godley,et al.  A global review of marine turtle entanglement in anthropogenic debris: A baseline for further action , 2017 .

[12]  A. Koelmans,et al.  Aging of microplastics promotes their ingestion by marine zooplankton. , 2017, Environmental pollution.

[13]  D. Rittschof,et al.  Chemoreception drives plastic consumption in a hard coral. , 2017, Marine pollution bulletin.

[14]  K. Syberg,et al.  Microplastic potentiates triclosan toxicity to the marine copepod Acartia tonsa (Dana) , 2017, Journal of toxicology and environmental health. Part A.

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

[16]  Richard C. Thompson,et al.  Microplastic ingestion in fish larvae in the western English Channel. , 2017, Environmental pollution.

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

[18]  Yongfang Zhao,et al.  Ingestion of microplastics by natural zooplankton groups in the northern South China Sea. , 2017, Marine pollution bulletin.

[19]  A. Harding,et al.  Microplastic pollution in the Greenland Sea: Background levels and selective contamination of planktivorous diving seabirds. , 2016, Environmental pollution.

[20]  Richard C. Thompson,et al.  Release of synthetic microplastic plastic fibres from domestic washing machines: Effects of fabric type and washing conditions. , 2016, Marine pollution bulletin.

[21]  S. Ebeler,et al.  Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds , 2016, Science Advances.

[22]  M. Cole A novel method for preparing microplastic fibers , 2016, Scientific Reports.

[23]  F. Lagarde,et al.  Is there any consistency between the microplastics found in the field and those used in laboratory experiments? , 2016, Environmental pollution.

[24]  Richard C. Thompson,et al.  Sources, Distribution, and Fate of Microscopic Plastics in Marine Environments , 2016 .

[25]  T. Galloway,et al.  Ingestion of Nanoplastics and Microplastics by Pacific Oyster Larvae. , 2015, Environmental science & technology.

[26]  C. Stedmon,et al.  Abundance, size and polymer composition of marine microplastics ≥10μm in the Atlantic Ocean and their modelled vertical distribution. , 2015, Marine pollution bulletin.

[27]  M. Leopold,et al.  Microplastic in a macro filter feeder: Humpback whale Megaptera novaeangliae. , 2015, Marine pollution bulletin.

[28]  P. Ross,et al.  Ingestion of Microplastics by Zooplankton in the Northeast Pacific Ocean , 2015, Archives of Environmental Contamination and Toxicology.

[29]  I. O’Connor,et al.  Microplastic and macroplastic ingestion by a deep diving, oceanic cetacean: the True's beaked whale Mesoplodon mirus. , 2015, Environmental pollution.

[30]  Elaine S. Fileman,et al.  The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. , 2015, Environmental science & technology.

[31]  A. Bond,et al.  Plastic ingestion by Flesh-footed Shearwaters (Puffinus carneipes): Implications for fledgling body condition and the accumulation of plastic-derived chemicals. , 2014, Environmental pollution.

[32]  S. Baulch,et al.  Evaluating the impacts of marine debris on cetaceans. , 2014, Marine pollution bulletin.

[33]  Vivi Fleming-Lehtinen,et al.  Ingestion and transfer of microplastics in the planktonic food web. , 2014, Environmental pollution.

[34]  Kyun-Woo Lee,et al.  Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. , 2013, Environmental science & technology.

[35]  Richard C. Thompson,et al.  The physical impacts of microplastics on marine organisms: a review. , 2013, Environmental pollution.

[36]  L. Amaral-Zettler,et al.  Life in the "plastisphere": microbial communities on plastic marine debris. , 2013, Environmental science & technology.

[37]  Julian Moger,et al.  Microplastic ingestion by zooplankton. , 2013, Environmental science & technology.

[38]  K. Lohmann,et al.  Perception of dimethyl sulfide (DMS) by loggerhead sea turtles: a possible mechanism for locating high-productivity oceanic regions for foraging , 2012, Journal of Experimental Biology.

[39]  T. Kiørboe How zooplankton feed: mechanisms, traits and trade‐offs , 2011, Biological reviews of the Cambridge Philosophical Society.

[40]  M. Steinke,et al.  The role of dissolved infochemicals in mediating predator–prey interactions in the heterotrophic dinoflagellate Oxyrrhis marina , 2011 .

[41]  A. J. Kettle,et al.  An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean , 2011 .

[42]  Werner Stefanie,et al.  Marine Litter : Technical Recommendations for the Implementation of MSFD Requirements , 2011 .

[43]  Michael Cunliffe,et al.  Early microbial biofilm formation on marine plastic debris. , 2011, Marine pollution bulletin.

[44]  G. Nevitt,et al.  Rapid Communication: Experimental Evidence that Juvenile Pelagic Jacks (Carangidae) Respond Behaviorally to DMSP , 2010, Journal of Chemical Ecology.

[45]  S. Archer,et al.  Phytoplankton taxa, irradiance and nutrient availability determine the seasonal cycle of DMSP in temperate shelf seas , 2009 .

[46]  Richard C. Thompson,et al.  Accumulation and fragmentation of plastic debris in global environments , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[48]  P. Evans,et al.  True’s beaked whale Mesoplodon mirus , 2008 .

[49]  G. Nevitt,et al.  Dimethylsulfoniopropionate as a Foraging Cue for Reef Fishes , 2008, Science.

[50]  R. Tollrian,et al.  Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. , 2007, Trends in ecology & evolution.

[51]  E. Barbier,et al.  Impacts of Biodiversity Loss on Ocean Ecosystem Services , 2006, Science.

[52]  E. Stamhuis,et al.  Dimethyl sulfide triggers search behavior in copepods , 2006 .

[53]  S. Finch,et al.  Lost at Sea , 2004, math/0411518.

[54]  Richard C. Thompson,et al.  Lost at Sea: Where Is All the Plastic? , 2004, Science.

[55]  V. Meyer-Rochow,et al.  Larval and adult eye of the Western Rock Lobster (Panulirus longipes) , 1975, Cell and Tissue Research.

[56]  D. C. Yoch Dimethylsulfoniopropionate: Its Sources, Role in the Marine Food Web, and Biological Degradation to Dimethylsulfide , 2002, Applied and Environmental Microbiology.

[57]  D. Barnes,et al.  Biodiversity: Invasions by marine life on plastic debris , 2002, Nature.

[58]  D. W. Laist Impacts of Marine Debris: Entanglement of Marine Life in Marine Debris Including a Comprehensive List of Species with Entanglement and Ingestion Records , 1997 .

[59]  Thomas Kiørboe,et al.  Predatory and suspension feeding of the copepod Acartia tonsa in turbulent environments , 1995 .

[60]  J. Cobb,et al.  Natural diet and feeding habits of the postlarval lobster Homarus americanus , 1992 .

[61]  R. Forward,et al.  Photosensitivity of the calanoid copepod Acartia tonsa , 1984 .

[62]  M. Huntley,et al.  Particle rejection by Calanus pacificus: discrimination between similarly sized particles , 1983 .

[63]  守安 実己郎 カナダのオマ-ルHomarus americanus漁業 , 1983 .

[64]  J. Strickler,et al.  Suspension-feeding by herbivorous calanoid copepods: A cinematographic study , 1982 .

[65]  P. Donaghay,et al.  Food selection capabilities of the estuarine copepod Acartia clausi , 1979 .

[66]  B. Frost EFFECTS OF SIZE AND CONCENTRATION OF FOOD PARTICLES ON THE FEEDING BEHAVIOR OF THE MARINE PLANKTONIC COPEPOD CALANUS PACIFICUS1 , 1972 .

[67]  B. Mr EFFECTS OF SIZE AND CONCENTRATION OF FOOD PARTICLES ON THE FEEDING BEHAVIOR OF THE MARINE PLANKTONIC COPEPOD CALANUS PACIFICUS , 1972 .

[68]  H. G. Cannon On the Feeding Mechanism of the Copepods, Calanus Finmarchicus and Diaptomus Gracilis , 1928 .