Oyster reproduction is affected by exposure to polystyrene microplastics

Abstract

Plastics are persistent synthetic polymers that accumulate as waste in the marine environment. Microplastic (MP) particles are derived from the breakdown of larger debris or can enter the environment as microscopic fragments. Because filter-feeder organisms ingest MP while feeding, they are likely to be impacted by MP pollution. To assess the impact of polystyrene microspheres (micro-PS) on the physiology of the Pacific oyster, adult oysters were experimentally exposed to virgin micro-PS (2 and 6 µm in diameter; 0.023 mg·L(-1)) for 2 mo during a reproductive cycle. Effects were investigated on ecophysiological parameters; cellular, transcriptomic, and proteomic responses; fecundity; and offspring development. Oysters preferentially ingested the 6-µm micro-PS over the 2-µm-diameter particles. Consumption of microalgae and absorption efficiency were significantly higher in exposed oysters, suggesting compensatory and physical effects on both digestive parameters. After 2 mo, exposed oysters had significant decreases in oocyte number (-38%), diameter (-5%), and sperm velocity (-23%). The D-larval yield and larval development of offspring derived from exposed parents decreased by 41% and 18%, respectively, compared with control offspring. Dynamic energy budget modeling, supported by transcriptomic profiles, suggested a significant shift of energy allocation from reproduction to structural growth, and elevated maintenance costs in exposed oysters, which is thought to be caused by interference with energy uptake. Molecular signatures of endocrine disruption were also revealed, but no endocrine disruptors were found in the biological samples. This study provides evidence that micro-PS cause feeding modifications and reproductive disruption in oysters, with significant impacts on offspring.

Keywords: energy allocation; microplastic; oyster; reproduction.

Fig. 1.

Histology panels. Micropolystyrene beads of 2 and 6 µm were observed in the stomach lumen (A and B) and intestine (C and D) of exposed oysters but not in the digestive tubules (E). No beads were observed in control oysters. ct: conjunctive tissue; ce: ciliated epithelium; cs: crystalline style; dt: digestive tubule; lu: lumen; 6 µm: 6-µm polystyrene beads, 2 µm: 2-µm polystyrene beads.

Fig. S1.

Boxplots of oyster hemocyte parameters showing significant condition effect or condition–time interaction in the two-way ANOVA. T1, sampling time 1 (2 wk of micro-PS exposure); T2, sampling time 2 (5 wk); T3, sampling time 3 (8 wk); MP, micropolystyrene exposed oysters; C, control oysters (n = 24). Letters represent statistically different groups calculated by the least significant difference post hoc test.

Fig. 2.

Larval growth. Larval size up to metamorphosis. Larval groups were obtained by crossing gametes collected from control genitors (control progeny) and from oysters exposed to micropolystyrene beads (MP progeny). A settlement delay of 6 d was observed in MP progeny compared with controls. For each group, mean and confidence intervals were obtained from triplicate larval rearing (n > 30).

Fig. S2.

Heatmaps of differentially expressed transcripts in female oyster digestive glands (A), gonads (B), and oocytes (C). For A and B, columns represent the averaged mRNA levels for each group (n = 5–8; T1 = sampling time 1, 2 wk of exposure; T3 = sampling time 3, 8 wk of exposure; MP = oysters exposed to polystyrene microbeads, T = control oysters). For C, individual samples are presented corresponding to oocytes collected in three exposed and five control females. Expression levels are shown with a color scale in which shades of red represent higher expression and shades of green represent lower expression.

Fig. 3.

DEB modeling. DEB model simulations for the DFM and oocyte number. Simulations named “control” represent simulations with standard parameters (i.e., fraction of energy allocated to soma, κ = 0.45, and volume-specific cost for maintenance, [ṗ_M] = 44 J⋅cm⁻³⋅d⁻¹) and with absorption efficiency measured in controls. Simulations named “micro-PS.std” represent simulations with standard parameters and with absorption efficiency measured for oysters exposed to micropolystyrene. Simulations named “micro-PS.cal” represent simulations with calibrated parameters (i.e., κ = 0.77 and [ṗ_M] = 84 J⋅cm⁻³⋅d⁻¹) and with absorption efficiency measured for exposed oysters. Initial and final dry flesh mass and oocyte production observed are plotted.

Fig. S3.

Micro-PS chemical analysis. Scan chromatogram of micro-PS extracted with dichloromethane (A). Superimposed scan chromatograms of control digestive styles (black) and digestive styles with micro-PS particles (red) (B).