Elsevier

Chemosphere

Volume 234, November 2019, Pages 123-131
Chemosphere

The uptake and elimination of polystyrene microplastics by the brine shrimp, Artemia parthenogenetica, and its impact on its feeding behavior and intestinal histology

https://doi.org/10.1016/j.chemosphere.2019.05.267Get rights and content

Highlights

  • Brine shrimp larvae have a large capacity to consume 10 μm polystyrene microspheres.

  • Brine shrimp larvae egested 97% of microplastics within 3 h of ingestion.

  • Microplastics persisted in individuals (1.23 particles/individual) for up to 14 days.

  • Microalgal feeding was significantly reduced in the presence of microplastics.

  • Several histological changes were observed in intestines of exposed individuals.

Abstract

Microplastics are a ubiquitous contaminant of marine ecosystems that have received considerable global attention. The effects of microplastic ingestion on some marine biota have been evaluated, but the uptake, elimination, and histopathological impacts of microplastics remain under-investigated especially for zooplankton larvae. Here, we show that 10 μm polystyrene microspheres can be ingested and egested by Artemia parthenogenetica larvae, which impact their health. The results indicate that A. parthenogenetica larvae have a varying capacity to consume 10 μm polystyrene microspheres that is dependent on microplastic exposure concentrations, exposure times, and the availability of food. The lowest level of microplastics that was ingested by A. parthenogenetica was 0.15 particles/individual when exposed to 10 particles/mL and 0.05 particles/individual when exposed to 1 particle/mL over 24 h and 14 d, respectively. A. parthenogenetica larvae were able to egest feces with microplastics within 3 h of ingestion. However, ingested microplastics persisted in individuals for up to 14 days. Furthermore, microalgal feeding was significantly reduced by 27.2% in the presence of 102 particles/mL microplastics over 24 h. Histological analyses indicated that a greater abundance of lipid droplets was present among epithelia after 24 h of exposure at a concentration of 10 particles/mL. Moreover, intestinal epithelia were deformed and disorderedly arranged after 14 d of exposure. Overall, these results indicate that marine microplastic pollution could pose a threat to A. parthenogenetica health, especially that of larvae. Consequently, further research is required to evaluate the potential physiological and histopathological effects of microplastics for other marine invertebrate species.

Introduction

Microplastics, which are plastic particles <5 mm in size, are an emerging and ubiquitous environmental threat for marine ecosystems due to their adverse impacts on marine animals (Della Torre et al., 2014; Reisser et al., 2015; Galloway and Lewis, 2016; Brach et al., 2018). Microplastics are manufactured for use in numerous applications including personal care products, and also originate during the breakdown of larger plastic materials (Cheung and Fok, 2017; Ivleva et al., 2017). Recent studies have shown that a wide range of marine biota at various trophic levels, including fish, bivalves, and crustaceans, can readily ingest microplastics via feeding and through trophic transfers. Such activities result in physical harm to digestive systems including reduced food uptake and disruption of reproductive behavior, among other impacts (Wright et al., 2013; Lu et al., 2016; Sussarellu et al., 2016; Jovanovic, 2017; Ziajahromi et al., 2017).

Zooplankton encompass a range of aquatic animals that form a key trophic link between primary producers and the rest of marine food webs. Zooplankton play important roles not only in the energy transfer but also in the transport of pollutants across marine food chains (Cole et al., 2015; Batel et al., 2016). Indeed, the trophic transfer of microplastics across aquatic food webs has been observed in animals (Batel et al., 2016). Moreover, the ingestion of microplastics has been observed by zooplankton in the northern South China Sea, the Yellow Sea and in the Northeast Pacific Ocean, thus highlighting the urgent need to investigate the uptake, elimination, and toxicity of microplastics in marine animals (Cole et al., 2013; Sun et al., 2017, 2018).

Ingested microplastics are known to impact the feeding, growth, and fecundity of some zooplankton (Cole et al., 2015; Ogonowski et al., 2016; Jeong et al., 2017). For example, the ingestion of 20 μm polystyrene beads can significantly alter the feeding capacity of the pelagic copepod Calanus helgolandicus, and prolonged exposure to microplastics significantly decreases the reproductive output (Cole et al., 2015). Furthermore, size-dependent oxidative stress responses and associated cellular damage that reduces growth rate and reproduction have been observed for the marine copepod Paracyclopina nana after exposure to 0.5 and 6 μm polystyrene microbeads (Jeong et al., 2017). However, the kinetics of microplastic uptake and elimination by zooplankton larvae and their associated impacts on digestive tracts have rarely been investigated. The lack of analytical methods and difficulty in investigating these processes in larvae owing to their small sizes is one of the hindrances for such studies, as compared to more developed techniques for fish and mussels (Von Moos et al., 2012; Jemec et al., 2016; Lu et al., 2016).

Previously, we found that ingestion of 10 μm polystyrene microspheres by A. parthenogenetica were visualized when exposed to 12 ± 0.57 particles/mL and 1.1 ± 0.16 particles/mL over 24 h and 14 d exposures, respectively (Wang et al., 2019). Ultrastructural changes of epithelial cells lining the intestine occurred following 24 h of exposure, although no major acute or chronic toxicity effects were observed on the survival, growth, or development of individuals (Wang et al., 2019). However, the factors influencing microplastic uptake, and elimination in A. parthenogenetica, are not well understood, nor is the impact of microplastics on their feeding and damage to their intestinal cells due to long-term microplastic exposure.

To evaluate A. parthenogenetica uptake, elimination, and impacts of microplastics, 10 μm polystyrene microspheres were exposed to individuals. First, experiments were conducted to evaluate microplastic uptake and ingestion capacity for A. parthenogenetica over varying exposure concentrations, exposure times and in the presence of food during early-stage (larval) exposure. Second, a 14-d elimination recovery experiment was conducted in clean seawater to investigate the abundance of microplastics remaining in A. parthenogenetica post-ingestion. Third, the impacts of microplastics on shrimp feeding were explored. Finally, histological analyses of intestinal tissues were performed over short-term (24 h) and long-term (14 d) exposure experiments.

Section snippets

Characterization of experimental microplastics

Fluorescently labelled and unlabelled 10 μm polystyrene microspheres (Thermo Fisher Scientific Corporation, USA) were used for experimentation. Specifically, green fluorescently labelled and unlabelled polystyrene microsphere solutions were used for evaluating uptake/elimination and their associated effects, respectively. Labelled and unlabelled microplastics were used at concentrations of 1.76 ± 0.02 × 107 particles/mL and 3.96 ± 0.02 × 106 particles/mL, respectively, as determined by a

Digestion efficiencies and microplastic recovery r ates

The digestion efficiencies of the four HNO3 treatments ranged from 74.1% to 98.5% (Table 1). The methods utilizing 65% HNO3 exhibited efficiencies that were relatively high (i.e., 90%). Among these, the most effective digestion treatment was Method B (65% HNO3, sonication, 40 °C incubation for 40 min) which yielded an efficiency of 98.5 ± 11%. In addition, high digestion efficiencies were also achieved with Method A (65% HNO3, 70 °C incubation for 2 h) and Method C (65% HNO3, room temperature

Acknowledgments

The research was financially supported by the National Key Research and Development Program of China (2016YFC1402201), the Scientific Research Special Fund of Marine Public Welfare Industry (201505034), and the National Natural Science Foundation of China (51479016).

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