Sequestration of microfibers and other microplastics by green algae, Cladophora, in the US Great Lakes

https://doi.org/10.1016/j.envpol.2021.116695Get rights and content

Highlights

  • Cladophora beds in the Great Lakes contain significant amounts of microfibers.

  • Synthetic microfibers, such as PET, likely distribute lower in the water column.

  • Cladophora cell walls successfully bio-adsorb microplastics.

  • Submerged aquatic vegetation influence the distribution of microplastics in water.

Abstract

Daunting amounts of microplastics are present in surface waters worldwide. A main category of microplastics is synthetic microfibers, which originate from textiles. These microplastics are generated and released in laundering and are discharged by wastewater treatment plants or enter surface waters from other sources. The polymers that constitute many common synthetic microfibers are mostly denser than water, and eventually settle out in aquatic environments. The interaction of these microfibers with submerged aquatic vegetation has not been thoroughly investigated but is potentially an important aquatic sink in surface waters. In the Laurentian Great Lakes, prolific growth of macrophytic Cladophora creates submerged biomass with a large amount of surface area and the potential to collect and concentrate microplastics. To determine the number of synthetic microfibers in Great Lakes Cladophora, samples were collected from Lakes Erie and Michigan at multiple depths in the spring and summer of 2018. After rinsing and processing the algae, associated synthetic microfibers were quantified. The average loads of synthetic microfibers determined from the Lake Erie and Lake Michigan samples were 32,000 per kg (dry weight (dw)) and 34,000 per kg (dw), respectively, 2–4 orders of magnitude greater than loads previously reported in water and sediment. To further explore this sequestration of microplastics, fresh and aged Cladophora were mixed with aqueous mixtures of microfibers or microplastic in the laboratory to simulate pollution events. Microscopic analyses indicated that fresh Cladophora algae readily interacted with microplastics via adsorptive forces and physical entanglement. These interactions mostly cease upon algal senescence, with an expected release of microplastics in benthic sediments. Collectively, these findings suggest that synthetic microfibers are widespread in Cladophora algae and the affinity between microplastics and Cladophora may offer insights for removing microplastic pollution.

Macroalgae in the Laurentian Great Lakes contain high loads of synthetic microfibers, both entangled and adsorbed, which likely account for an important fraction of microplastics in these surface waters.

Introduction

In the Laurentian Great Lakes of North America, accumulation of persistent microplastic pollution is a present and growing concern. Microplastics have been identified in surface lake and tributary waters, sediment and shoreline sand, and they continue to enter the lakes at a rapid pace (Baldwin et al., 2016; Eriksen et al., 2013; Peller et al., 2020). All common classes of microplastics, including films, fragments and fibers, have been identified in the Great Lakes and typically reflect nearby sources, such as urban or agricultural run-off or wastewater treatment plants (Peller et al., 2020). The fates of these plastic pollutants are not well understood (Grbic et al., 2020; Lenaker et al., 2019). Researchers have modeled plastic input and microplastic debris in the Great Lakes; estimates indicate that as much as 10,000 metric tons enter the Great Lakes annually, with Lake Michigan receiving the largest amount (Hoffman and Hittinger, 2017); however, this value is higher than the actual microplastic pollution inventory by 2–3 orders of magnitude (Hoffman and Hittinger, 2017). The discrepancy in modeled input versus estimates based on recovery is attributed, in part, to the use of trawl nets for water sampling, which are often inadequate for collecting smaller microplastic pollution (Lindeque et al., 2020). While consistency in field and laboratory procedures will improve comparability between studies and estimates of load and recovery (Zhu and Wang, 2020), a gap in accounting for these plastic pollutants remains, and defining properties of microplastic distribution may help in these efforts.

Synthetic microfibers constitute a category of microplastics often most commonly recovered from surface water, especially near wastewater treatment plants and when grab sampling is the field collection method (Peller et al., 2020). The densities of common microfibers, such as polyester, are greater than 1.0 (Table 1) and therefore are inclined to sink and settle, in comparison to the lower density microplastics, such as polypropylene and polyethylene. Due to the expected downward movement of most synthetic microfibers, reported amounts of microplastics in surface water may constitute only a fraction of the total loadings (Barrows et al., 2017). Moreover, microplastics may associate with suspended mineral particles in surface water, which can affect buoyancy, movement and fate (Naqash et al., 2020; Kooi et al., 2017). The persistent microplastic pollutants in surface water also interact with natural organic particulates (Tekman et al., 2020), aquatic organisms through ingestion or surface interactions (de Sa et al., 2018), and floating aquatic vegetation (Kalcikova, 2020; Goss et al., 2018), all of which can affect vertical movement and distribution (Long et al., 2015).

The green macroalga Cladophora, the most widespread of global freshwater macroalga (Higgins et al., 2008), has a prominent role in the Great Lakes ecosystem, providing habitat for epiphytic algae and safe haven for larval fishes (Dodds and Gudder, 1992). It colonizes hard substrates such as boulders and cobbles, as well as mussel mounds. However, Cladophora has been identified as one of the 50 stressors affecting the Great Lakes (Smith et al., 2015). According to the estimation of dry mass from remote sensing, the amount of Cladophora growth in the Great Lakes can reach 129 kilotons (dry weight (dw)) (Brooks et al., 2015). Light and temperature requirements for Cladophora growth are minimal, especially in the first phase of early spring growth, and high levels of nutrients, especially nitrogen and phosphorus, enable the development of dense algal beds (Pikosz et al., 2017). According to studies of Lake Huron Cladophora, it can increase in biomass by 60% over 24 h at optimum irradiance and temperature and without phosphorus limitations (Auer and Canale, 1982). This filamentous alga grows throughout the warm weather months (∼May–September), followed by a cycle of senescence in the late summer and fall, reemerging the following spring (Verhougstraete et al., 2010; Zulkifly et al., 2013). The alga is sloughed during high wind and wave conditions or at senescence, and floating filaments disperse and accumulate along shorelines (Higgins et al., 2008).

Functions of green macroalgae include its role as a primary producer, a sink for CO2, and the removal of excess nutrients from the water, where it is critical in overall nutrient cycling. (Michalak and Messyasz, 2020) In some cultures, green algae and seaweed are harvested for food and/or medicinal purposes since they contain a range of nutrients and bioactive compounds, including proteins, pigments and polysaccharides (Messyasz et al., 2015; Boonchum et al., 2011). Due to the high protein content, Cladophora can be used as a nutritional supplement for human food and animal feed (Messyasz et al., 2015). Recent studies have shown that nitrogen-fixing microbes representing bacteria and archaea are common in fresh Cladophora potentially contributing to the algal nitrogen needs (Byappanahalli et al., 2019).

In many areas of the Great Lakes and other fresh surface waters worldwide, intense overgrowth of Cladophora and subsequent massive shoreline accumulations of the decaying mats have been widely reported and studied. (Watson et al., 2016, Dodds and Gudder, 1992, Van den Hoek et al., 1995) A resurgence of Cladophora, associated with the proliferation of invasive mussels (Dreissena polymorpha, Dreissena bugensis) and subsequent increase in water clarity, was documented in the Great Lakes starting in the 1990s, and by 2004, Cladophora negatively impacted 80% of the western Lake Michigan shoreline with massive washed up mats (Higgins et al., 2008). While Cladophora beds provide habitat for a diverse group of microbes, epiphytic algae, and invertebrates, the washed up algal mats accumulating along the shoreline create a nuisance, as these mats harbor a variety of bacterial communities (e.g., E. coli, Salmonella, enterococci, C. botulinum) affecting human and wildlife health (Verhougstraete et al., 2010; Chun et al., 2015; Chun et al., 2017). Overgrowth of algae leads to unsightly, odorous shoreline accumulations, which compromise environmental and public health, diminish property value and threaten water quality, among other consequences (Depew et al., 2011; Whitman et al., 2003).

The purpose of this study was to report on the load of pollutant microfibers present in samples of Cladophora and the accompanying submerged aquatic vegetation from Lakes Michigan and Erie. The experiments include an examination of the physical interactions by Cladophora that lead to sequestration of microfibers from the lake waters. Given the abundance in the Great Lakes in warmer weather months, the macroalgae might play a significant role in the distribution and deposition of microplastics, especially microfibers, in the lakes and surrounding shorelines (Riley et al., 2015). An additional concern is the potential for adsorption of microplastics by these primary producers in the food chain, which may translate to consequences for other aquatic life or for humans or other animals when the macroalgae is consumed. The ability of Cladophora to remove microplastics from water may also provide insight into effective methods for removing microfiber pollutants from fresh and marine waters. To the best of our knowledge, this is the first study to report on the natural accumulation of microplastics and microfibers by macroalgae or other submerged aquatic vegetation in the Great Lakes.

Section snippets

Study sites

Cladophora is a macroalga and part of submerged aquatic vegetation (SAV) that typically lives in diverse community with many other macroalgae, microalgae, and microbes (Dodds and Gudder, 1992). Rarely does Cladophora form a monoculture on the lake bottom; use of the term Cladophora in this study is inclusive of the species Cladophora and associated submerged vegetation.

Cladophora samples were collected from shoreline and offshore areas of Lakes Michigan and Erie in the Laurentian Great Lakes.

Quantification of synthetic microfibers in field collected Cladophora

The Cladophora and submerged aquatic vegetation (SAV) as measured in g/m2 (dw) collected from Lakes Erie and Michigan in 2018, are highlighted in Fig. 1, Fig. 2. These maps also show the lake locations where samples were collected. The experimentally determined synthetic microfiber loads from Cladophora/SAV samples from Lake Erie (N = 5, 30 replicates) and Lake Michigan (N = 14, 113 replicates) are summarized in Fig. 3, Fig. 4. The average number of synthetic microfibers (MFs) in Lake Erie was

Conclusions

The data from this study have shown that synthetic microfibers, a key class of microplastics, are highly sequestered by Great Lakes algae. This constitutes a critical finding concerning the distribution and fate of these pollutants in freshwater environments. The data further suggest that common synthetic microfibers, due to their densities, distribute in the lower levels of the lake, and have likely been under-reported. Once in contact with Cladophora, and other SAV, the microplastics readily

Author contributions

Julie Peller: Conceptualization, Methodology, Formal analysis, Investigation, Supervision, Validation, Writing – original draft and editing; Meredith Nevers: Conceptualization, Methodology, Formal analysis, Supervision, Validation, Writing –original draft and editing; Muruleedhara Byappanahalli: Conceptualization, Methodology, Formal analysis, Supervision, Validation, Writing – original draft and editing; Cassie Nelson: Formal analysis, Validation, Writing-review and editing; Bharath Ganesh

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank Kasia Przybyla-Kelly and Danielle Szymkowski, USGS, for assistance with preparing and processing Cladophora samples. Offshore samples were collected as part of the Great Lakes Cladophora Assessment study funded by the Great Lakes Restoration Initiative (US EPA). Additional funding for time was provided by the USGS Ecosystems Mission Area. The authors also acknowledge Valparaiso University professor Michael Watters for guidance and assistance with the compound microscope images.

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References (63)

  • H. Goss et al.

    Thalassia testudinum as a potential vector for incorporating microplastics into benthic marine food webs

    Mar. Pollut. Bull.

    (2018)
  • M.J. Hoffman et al.

    Inventory and transport of plastic debris in the laurentian Great lakes

    Mar. Pollut. Bull.

    (2017)
  • P.K. Lindeque et al.

    Are we underestimating microplastic abundance in the marine environment? A comparison of microplastic capture with nets of different mesh-size

    Environ. Pollut.

    (2020)
  • M. Long et al.

    Interactions between microplastics and phytoplankton aggregates: impact on their respective fates

    Mar. Chem.

    (2015)
  • P.M. Lourenco et al.

    Plastic and other microfibers in sediments, macroinvertebrates and shorebirds from three intertidal wetlands of southern Europe and west Africa

    Environ. Pollut.

    (2017)
  • J.R. Peller et al.

    Notable decomposition products of senescing Lake Michigan Cladophora glomerata

    J. Gt. Lakes Res.

    (2014)
  • M. Pikosz et al.

    Functional structure of algal mat (Cladophora glomerata) in a freshwater in western Poland

    Ecol. Indicat.

    (2017)
  • S.C. Riley et al.

    Factors associated with the deposition of Cladophora on Lake Michigan beaches in 2012

    J. Gt. Lakes Res.

    (2015)
  • V. Thiagarajan et al.

    Influence of differently functionalized polystyrene microplastics on the toxic effects of P25 TiO2 NPs towards marine algae Chlorella sp

    Aquat. Toxicol.

    (2019)
  • L.A. Tziveleka et al.

    Ulvan, a bioactive marine sulphated polysaccharide as a key constituent of hybrid biomaterials: a review

    Carbohydr. Polym.

    (2019)
  • W.F. Wang et al.

    The ecotoxicological effects of microplastics on aquatic food web, from primary producer to human: a review

    Ecotoxicol. Environ. Saf.

    (2019)
  • S.B. Watson et al.

    The re-eutrophication of Lake Erie: harmful algal blooms and hypoxia

    Harmful Algae

    (2016)
  • A.K. Baldwin et al.

    Plastic debris in 29 Great lakes tributaries: relations to watershed attributes and hydrology

    Environ. Sci. Technol.

    (2016)
  • A.P.W. Barrows et al.

    Grab vs. neuston tow net: a microplastic sampling performance comparison and possible advances in the field

    Anal. Methods

    (2017)
  • P. Bhattacharya et al.

    Physical adsorption of charged plastic nanoparticles affects algal photosynthesis

    J. Phys. Chem. C

    (2010)
  • W. Boonchum et al.

    Antioxidant activity of some seaweed from the gulf of Thailand

    Int. J. Agric. Biol.

    (2011)
  • M.N. Byappanahalli et al.

    Clostridium botulinum type E occurs and grows in the alga Cladophora glomerata

    Can. J. Fish. Aquat. Sci.

    (2009)
  • M.N. Byappanahalli et al.

    Great Lakes Cladophora harbors phylogenetically diverse nitrogen-fixing microorganisms

    Environ. DNA

    (2019)
  • C.L. Chun et al.

    Association of toxin-producing Clostridium botulinum with the macroalga Cladophora in the Great lakes

    Environ. Sci. Technol.

    (2013)
  • C.L. Chun et al.

    Prevalence of toxin-producing Clostridium botulinum associated with the macroalga Cladophora in three Great Lakes: growth and management

    Sci. Total Environ.

    (2015)
  • W.K. Dodds et al.

    The ecology of Cladophora

    J. Phycol.

    (1992)
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