Biogenic Aggregation of Small Microplastics Alters Their Ingestion by a Common Freshwater Micro-Invertebrate

In recent years, increasing concerns have been raised about the environmental risk of microplastics in freshwater ecosystems. Small microplastics enter the water either directly or accumulate through disintegration of larger plastic particles. These particles might then be ingested by filter-feeding zooplankton, such as rotifers. Particles released into the water may also interact with the biota through the formation of aggregates, which might alter the uptake by zooplankton. In this study, we tested for size-specific aggregation of polystyrene microspheres and their ingestion by a common freshwater rotifer Brachionus calyciflorus. The ingestion of three sizes of polystyrene microspheres (MS) 1-, 3-, and 6-μm was investigated. Each MS size was tested in combination with three different treatments: MS as the sole food intake, MS in association with food algae and MS aggregated with biogenic matter. After 72 h incubation in pre-filtered natural river water, the majority of the 1-μm spheres occurred as aggregates. The larger the particles, the higher the relative number of single particles and the larger the aggregates. All particles were ingested by the rotifer following a Type-II functional response. The presence of algae did not influence the ingestion of the MS for all three sizes. The biogenic aggregation of microspheres led to a significant size-dependent alteration in their ingestion. Rotifers ingested more microspheres (MS) when exposed to aggregated 1- and 3-μm MS as compared to single spheres, whereas fewer aggregated 6-μm spheres were ingested. This indicates that the small particles when aggregated were in an effective size range for Brachionus, while the aggregated larger spheres became too large to be efficiently ingested. These observations provide the first evidence of a size- and aggregation-dependent feeding interaction between microplastics and rotifers. Microplastics when aggregated with biogenic particles in a natural environment can rapidly change their size-dependent availability. The aggregation properties of microplastics should be taken into account when performing experiments mimicking the natural environment.

[1]  Daniel C W Tsang,et al.  A review of microplastics aggregation in aquatic environment: Influence factors, analytical methods, and environmental implications. , 2020, Journal of hazardous materials.

[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]  P. Mayer,et al.  Surface-Related Toxicity of Polystyrene Beads to Nematodes and the Role of Food Availability. , 2020, Environmental science & technology.

[5]  Yongfang Zhao,et al.  Characteristics of microplastics ingested by zooplankton from the Bohai Sea, China. , 2020, The Science of the total environment.

[6]  T. Kögel,et al.  Micro- and nanoplastic toxicity on aquatic life: Determining factors. , 2019, The Science of the total environment.

[7]  A. Wacker,et al.  Fitness response variation within and among consumer species can be co-mediated by food quantity and biochemical quality , 2019, Scientific Reports.

[8]  F. Kelly,et al.  Advances and challenges of microplastic pollution in freshwater ecosystems: A UK perspective. , 2019, Environmental pollution.

[9]  E. Holland,et al.  Validation and application of cost and time effective methods for the detection of 3-500 μm sized microplastics in the urban marine and estuarine environments surrounding Long Beach, California. , 2019, Marine pollution bulletin.

[10]  N. Nogueira,et al.  Marine vs freshwater microalgae exopolymers as biosolutions to microplastics pollution. , 2019, Environmental pollution.

[11]  J. Gantelius,et al.  A 61% lighter cell culture dish to reduce plastic waste , 2019, PloS one.

[12]  Richard C. Thompson,et al.  Response to the Letter to the Editor Regarding Our Feature "Are We Speaking the Same Language? Recommendations for a Definition and Categorization Framework for Plastic Debris". , 2019, Environmental science & technology.

[13]  A. Wichels,et al.  The Plastisphere – Uncovering tightly attached plastic “specific” microorganisms , 2019, PloS one.

[14]  H. Grossart,et al.  The Eukaryotic Life on Microplastics in Brackish Ecosystems , 2019, Front. Microbiol..

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

[16]  C. Faggio,et al.  Micro- (nano) plastics in freshwater ecosystems: Abundance, toxicological impact and quantification methodology , 2019, TrAC Trends in Analytical Chemistry.

[17]  E. Foekema,et al.  Quantifying ecological risks of aquatic micro- and nanoplastic , 2018, Critical Reviews in Environmental Science and Technology.

[18]  Ralph Tiedemann,et al.  Differential response to heat stress among evolutionary lineages of an aquatic invertebrate species complex , 2018, Biology Letters.

[19]  A. Wacker,et al.  One man’s trash is another man’s treasure - the effect of bacteria on phytoplankton-zooplankton interactions in chemostat systems , 2018, bioRxiv.

[20]  Minghua Wang,et al.  Nanoplastic Ingestion Enhances Toxicity of Persistent Organic Pollutants (POPs) in the Monogonont Rotifer Brachionus koreanus via Multixenobiotic Resistance (MXR) Disruption. , 2018, Environmental science & technology.

[21]  T. Neu,et al.  Plastic Alters Biofilm Quality as Food Resource of the Freshwater Gastropod Radix balthica. , 2018, Environmental science & technology.

[22]  T. Mincer,et al.  Field-Based Evidence for Microplastic in Marine Aggregates and Mussels: Implications for Trophic Transfer. , 2018, Environmental science & technology.

[23]  J. Michels,et al.  Rapid aggregation of biofilm-covered microplastics with marine biogenic particles , 2018, Proceedings of the Royal Society B.

[24]  A. Lundebye,et al.  Marine microplastic debris: An emerging issue for food security, food safety and human health. , 2018, Marine pollution bulletin.

[25]  T. Gutierrez,et al.  Agglomeration of nano- and microplastic particles in seawater by autochthonous and de novo-produced sources of exopolymeric substances. , 2018, Marine pollution bulletin.

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

[27]  J. Paul Chen,et al.  Microplastics in freshwater systems: A review on occurrence, environmental effects, and methods for microplastics detection. , 2017, Water research.

[28]  M. Wagner,et al.  Interactions of Microplastics with Freshwater Biota , 2018 .

[29]  G. Reifferscheid,et al.  Feeding type and development drive the ingestion of microplastics by freshwater invertebrates , 2017, Scientific Reports.

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

[31]  Daniel Barrios-O'Neill,et al.  frair: an R package for fitting and comparing consumer functional responses , 2017 .

[32]  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.

[33]  Ellen Besseling,et al.  Fate of nano- and microplastic in freshwater systems: A modeling study. , 2017, Environmental pollution.

[34]  Su-Jae Lee,et al.  Microplastic Size-Dependent Toxicity, Oxidative Stress Induction, and p-JNK and p-p38 Activation in the Monogonont Rotifer (Brachionus koreanus). , 2016, Environmental science & technology.

[35]  Maiju Lehtiniemi,et al.  Feeding type affects microplastic ingestion in a coastal invertebrate community. , 2016, Marine pollution bulletin.

[36]  A. Decho,et al.  When nanoparticles meet biofilms—interactions guiding the environmental fate and accumulation of nanoparticles , 2015, Front. Microbiol..

[37]  C. Wilcox,et al.  Plastic waste inputs from land into the ocean , 2015, Science.

[38]  M. Silver Marine Snow: A Brief Historical Sketch , 2015 .

[39]  U. Gaedke,et al.  Heated Relations: Temperature-Mediated Shifts in Consumption across Trophic Levels , 2014, PloS one.

[40]  Hsin-Hsin Peng,et al.  Of nanobacteria, nanoparticles, biofilms and their role in health and disease: facts, fancy and future. , 2014, Nanomedicine.

[41]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[42]  B. Drake Differential Response , 2013 .

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

[44]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[45]  C. Langdon,et al.  Particle size preference, gut filling and evacuation rates of the rotifer Brachionus “Cayman” using polystyrene latex beads , 2008 .

[46]  Benjamin M. Bolker,et al.  Ecological Models and Data in R , 2008 .

[47]  M. Pagano Feeding of tropical cladocerans (Moina micrura, Diaphanosoma excisum) and rotifer (Brachionus calyciflorus) on natural phytoplankton: effect of phytoplankton size–structure , 2008 .

[48]  P. Dalgaard,et al.  Nonlinear curve fitting , 2008 .

[49]  Takehito Yoshida,et al.  A DIRECT, EXPERIMENTAL TEST OF RESOURCE VS. CONSUMER DEPENDENCE , 2005 .

[50]  T. Snell,et al.  Rotifers in ecotoxicology: a review , 1995, Hydrobiologia.

[51]  O. Vadstein,et al.  Particle size dependent feeding by the rotifer Brachionus plicatilis , 1993, Hydrobiologia.

[52]  W. R. Demott The role of taste in food selection by freshwater zooplankton , 1986, Oecologia.

[53]  H. Müller,et al.  The filtration apparatus of Cladocera: Filter mesh-sizes and their implications on food selectivity , 1981, Oecologia.

[54]  P. Starkweather Aspects of the feeding behavior and trophic ecology of suspension-feeding rotifers , 1980, Hydrobiologia.

[55]  J. J. Gilbert,et al.  Bacterial feeding by the rotifer Brachionus calyciflorus: Clearance and ingestion rates, behavior and population dynamics , 1979, Oecologia.

[56]  U. Passow Transparent exopolymer particles (TEP) in aquatic environments , 2002 .

[57]  R. Adrian,et al.  Functional responses of the rotifers Brachionus calyciflorus and Brachionus rubens feeding on armored and unarmored ciliates , 2000 .

[58]  T. Snell Review paper: Chemical ecology of rotifers , 1998 .

[59]  T. Snell,et al.  Rapid toxicity assessment using rotifer ingestion rate , 1994 .

[60]  Jessica Gurevitch,et al.  Design and Analysis of Ecological Experiments , 1993 .

[61]  H. Grossart,et al.  Limnetic macroscopic organic aggregates (lake snow): Occurrence, characteristics, and microbial dynamics in Lake Constance , 1993 .

[62]  H. Brendelberger Filter mesh size of cladocerans predicts retention efficiency for bacteria , 1991 .

[63]  K. Rothhaupt Population growth rates of two closely related rotifer species: effects of food quantity, particle size, and nutritional quality , 1990 .

[64]  K. Rothhaupt Differences in particle size-dependent feeding efficiencies of closely related rotifer species , 1990 .

[65]  L. Bern Size-related discrimination of nutritive and inert particles by freshwater zooplankton , 1990 .

[66]  K. Porter,et al.  The use of DAPI for identifying and counting aquatic microflora1 , 1980 .

[67]  R. Guillard,et al.  YELLOW‐GREEN ALGAE WITH CHLOROPHYLLIDE C 1, 2 , 1972 .

[68]  C. Burns PARTICLE SIZE AND SEDIMENTATION IN THE FEEDING BEHAVIOR OF TWO SPECIES OF DAPHNIA , 1969 .