Ecotoxicity of polystyrene microplastics to submerged carnivorous Utricularia vulgaris plants in freshwater ecosystems

Highlights

• We explored effects of microplastics for submerged carnivorous aquatic plants.

• Polystyrene microplastics have been ingested by the bladders.

• Growth performance of U.vulgaris was reduced with increasing microplastic concentration.

• U. vulgaris can be potential eco-friendly purifiers for microplastics biodegradation.

Abstract

Much attention is currently paid to microplastic (MP) pollution, particularly in marine systems. There is increasing concern regarding the potential toxicity of MPs to organisms at the physiological and morphological levels. However, little is known about the impact of MPs on aquatic life, despite their ubiquitous presence in freshwater ecosystems. In this study, the aquatic plant Utricularia vulgaris was exposed to 1, 2 and 5 μm polystyrene fluorescent MP particles at concentrations of 15, 70 and 140 mg/L for 7 days. The toxic effects of MPs on the growth rate and morphological and physiological characteristics of U. vulgaris were assessed. The results showed that the relative growth rates and the functional traits of leaves (morphological and photosynthetic) were significantly inhibited at a high concentration of MP particles (140 mg/L) when compared to the control group. The impacts on growth performance were likely due to bioaccumulation of MPs in the bladders, as shown by confocal microscopy. Furthermore, the antioxidative enzyme activities showed that high concentrations of MPs induce high ecotoxicity and oxidative damage to U. vulgaris. Thus, U. vulgaris has the potential to be an excellent bioindicator of MP pollution in freshwater ecosystems and should further be applied in ecological risk assessments of the effects of MPs on higher aquatic plants.

Introduction

Pollution caused by microplastics (MPs, 1 to <1000 μm in size) is persistent, variable, and ubiquitous in marine, terrestrial, and freshwater ecosystems across the globe (Hartmann et al., 2019). These submicron-sized particles are directly manufactured (primary MPs, e.g., cosmetics and bath products) or derived from the fragmentation of larger items (secondary MPs) (Koelmans et al., 2015; Cong et al., 2019). Due to their stability and high durability, plastics generally take a long time to completely degrade in natural habitats, ranging from decades to centuries (Gewert et al., 2015; Weinstein et al., 2016). As one of the fastest-growing sources of pollution, plastic fragments have become a matter of great environmental concern. Nonetheless, despite the size of plastic fragments ranging from microscopic to several meters, microplastics are currently attracting widespread public attention.

MPs can be discharged into freshwater in various ways, including through liquid emissions, town sewage, soil erosion, precipitation, and runoff (Wagner et al., 2014). Recent studies have reported that MPs represent a growing contaminant of concern in the Great Lakes (Baldwin et al., 2016). Lakes may serve as important sites of MP enrichment among freshwater ecosystems since plastic items can continuously accumulate and be preserved over a prolonged period of time in such environments, causing them to become available to aquatic organisms (Franzellitti et al., 2019; Yuan et al., 2019). For instance, large amounts of small, fibrous, transparent MPs (with abundances ranging from 483 to 967 items/m³ in surface waters and from 50 to 195 items/kg in sediment) have been found on the Tibetan Plateau (Jiang et al., 2019a). Fibrous and colored MPs from domestic sewage and fishing activities have also been found in Poyang Lake, the largest freshwater lake in China (Yuan et al., 2019). Over time, an increasing amount of plastic waste enters the freshwater environment, which may have a significant impact on the freshwater ecosystem.

Owing to their small size, MPs can be ingested by and accumulate in a range of organisms, including fishes (Foekema et al., 2013), mammals (Lusher et al., 2015), zooplankton (Cole et al., 2013), oligochaetes (Huerta Lwanga et al., 2016), and vascular plants (Kalčíková et al., 2017; van Weert et al., 2019). Substantial research and experimentation have revealed that the adverse effects of MPs on aquatic organisms include reductions in growth rates, physical damage, and induction of oxidative stress (Foekema et al., 2013; Bouwmeester et al., 2015; Mattsson et al., 2015; Qu et al., 2020). Environmental pollution can cause oxidative stress on the biological system, resulting in the accumulation of reactive oxygen species (ROS). For example, MPs can cause oxidative stress in freshwater algae (Chlorella pyrenoidosa) and snails (Cipangopaludina cathayensis) (Qu et al., 2020). Plants can cope with oxidative stress by increasing antioxidant enzymes (e.g., superoxide dismutase and catalase) and antioxidants to eliminate excess ROS (Singh et al., 2006; Zhong et al., 2018). However, only a few studies have focused on the effects of MPs on vascular plants in freshwater ecosystems. For instance, MPs reduced the main shoot length of sediment-rooted macrophytes (Myriophyllum spicatum) (van Weert et al., 2019). Additionally, MPs inhibited root growth, photosynthetic activity and cell viability in freshwater floating plants (Lemna minor and Spirodela polyrhiza) (Kalčíková et al., 2017; Dovidat et al., 2020). While data on the antioxidant reaction of aquatic plants to MPs are scarce, especially for submerged plants, there is no reason to suppose that they remain unaffected. Aquatic plants play an important role in the functioning of freshwater ecosystems, for example, by providing energy to the food chain as primary producers (Gross et al., 2001), offering habitat and refuge for other species (Cremona et al., 2008), and functioning in biochemical cycling (Madsen and Cedergreen, 2010) and the reduction in suspended solids (Gurnell et al., 2010). Thus, concerns about the impact of MPs on aquatic plants should receive more scientific attention.

Based on recent research, MPs are strongly attracted to plant tissue surfaces by electrostatic forces and the presence of periphyton (Kalčíková, 2020). To further study the effects of MPs on plant internal organs, we investigated the impact of polystyrene plastic particle exposure on the growth rate and morphological and physiological characteristics of the submerged plant Utricularia vulgaris, a perennial, carnivorous, herbaceous plant in the Lentibulariaceae family that is widely distributed in lakes, pools and ditches. This plant has traps, called bladders, on finely dissected leaves (Adamec, 2006). Individuals of this plant species are rootless, and the main way in which they obtain nutrition is through the capture and digestion of prey (detritus and small aquatic animals) in traps (Kibriya and Iwan Jones, 2007). We hypothesized that exposure to increasing MP concentrations would (i) cause decreased growth rates and chlorophyll in U. vulgaris and (ii) activate the antioxidant defense system. We also predicted that a large number of MPs would accumulate in the foraging organs of U. vulgaris and, hence, more particles would cause negative impacts.