Fibre contamination is now recognised as the major constituent of particulate pollution in marine, freshwater, and terrestrial ecosystems (Horton et al., 2017; Vince & Stoett, 2018). In freshwater systems, fibre contaminants are present in multiple fish species (e.g., Silva-Cavalcanti et al., 2017; Su et al., 2019). Despite the prevalence of fibres in freshwater systems, this study is the first to assess the functional impacts of plastic and cellulose-based fibres and associated dye exposure and consumption (polyester, cotton, and bamboo) on fish host-parasite dynamics, specifically host mortality, disease resistance, and off-host parasite survival. For infected fish, while polyester and cotton had no major effects on disease dynamics, bamboo was associated with significantly lower peak parasite burdens. Polyester exposure and/or consumption were also associated with significantly increased mortality of uninfected hosts. Analysis of fibre-based dyes on off-host parasite survival revealed that cotton and polyester associated dyes were linked to significantly reduced parasite survival, with the polyester dyes associated with the highest parasite mortalities.
Polyester, specifically polyethylene terephthalate, is the most common thermoplastic polymer used for clothing (Ji, 2013) and unsurprisingly most prevalent in multiple surveys of fibre types in fish gastrointestinal tracts (Su et al., 2019). The only studies we are aware off that have tested polyester health effects in fish revealed no significant detrimental effects (Spanjer et al., 2020; Hu et al., 2020). Juvenile chinook salmon successfully cleared 94% of their gut polyester fibres over 10 days (following in-feed exposure of 20 fibres per food pellet with guts sampled at days 0,3,5,7 and 10) and polyester exposure had no effect on their mean gastrointestinal mass when compared with fish not exposed to any fibres (Spanjer et al., 2020). This chinook salmon study though was based on short term exposure and the authors commented that longer term studies may reveal detrimental health effects. In contrast, exposure of adult medaka for 21 days to polyester at levels x14 greater than those tested in the current study (10,000 fibres/L versus 700 fibres/L) reported denuded epithelium on gill arches, fusion of primary lamellae, and increased mucus production, but no changes in adult growth, weight or mortality, or embryonic mortality (Hu et al., 2020). In contrast, the current study which exposed fish to polyester fibres for 52 days demonstrated significantly reduced survival for uninfected hosts, but we acknowledge that longer exposure times may have revealed more pronounced effects than those we see in the current study.
When assessing the impacts of fibre associated dyes on parasite mortality, we observed that cotton and polyester dyes were linked to significantly higher off host parasite mortalities compared with bamboo dyes and controls. Off-host survival for this G. turnbulli strain typically ranges from 2 to 31 hours (mean 13.7 hours at 25oC; Schelkle et al., 2013), which was reflected in our control worms (i.e., not exposed to any dyes). Of the three fibre dye types, polyester had the highest number of parasite mortalities and while we were unable to tackle the mechanism underlying this increased parasite or host mortality, polyester was leaching a specific dye component (as identified via LCMS analysis; see Supplementary Material) more than bamboo and cotton, and this might have been a contributing factor. The chromatographic analysis also revealed that comparable amounts of dye were found between bamboo and cotton fibres tested, but the cotton associated dyes were leading to higher parasite mortalities but it is unclear why this is so. Current industry practices mean that the chemical identity of fabric dyes tend to remain confidential (Chen & Burns, 2006), and unfortunately, we were unable to determine the exact nature of the dye. While there are investigations revealing that wastewater effluent which contain textile dyes can be toxic to fish (Zhang et al., 2013; Kaur & Due 2015), targeting specific dyes found within fabrics and their impacts on fish welfare is much harder without actually knowing the specific dyes in question. However, plausible reasons why fibres and their dyes were associated with increased host and off-host parasite mortality include 1) development of biofilms harbouring infectious agents (Di Pippo et al., 2020; Tang et al., 2021); 2) gastrointestinal related pathologies (i.e., gut blockage and lesions, Jovanovic, 2017); 3) toxic effects related to a breakdown product from either the fibres or the associated dyes and/or 4) immune priming associated with microfibres being treated as antigens leading to reduced host survival (Tort, 2011).
Unlike the thermoplastic plastic polymer polyester, cotton and bamboo are cellulose based fibres and with the push to utilise natural alternatives, such as bamboo and hemp (Raj, 2021), the biological impacts of these alternatives must be established. Tropical fish, such as guppies used in this study, would naturally consume cellulose-based foliage (Zandona et al., 2011), and the current study revealed that, compared with controls not exposed to any fibres, cotton consumption did not impact disease burden or mortality. Though bamboo is also composed of cellulose, the bamboo utilised in this study was 95% viscose based and therefore technically synthetic in nature (i.e., chemically treated) using regenerated cellulose (structurally the same as natural cellulose; Kauffman, 1993) and 5% elastane, which is a synthetic polymer. Elastane is known for its extreme flexibility and hence a useful addition to clothing, but it is also recognised as non-recyclable and not easily degraded in natura (Yin et al., 2014). For this study bamboo exposure and consumption was associated with significantly lower peak pathogen burdens compared with fish not exposed to any fibres, while also reaching these peaks much later than the control treatments. It is unclear why bamboo consumption was associated with such low peak burdens but this could be related to the host immune system being primed to a chronic pollutant leading to a heightened disease response (see Tort, 2011) and/or reduced parasite survival and/or reproduction rate in response to the bamboo fibre and associated dye exposure. However, off-host parasite survival was not affected by direct bamboo dye exposure; leaving potential reproductive changes to the parasite and or host immune related effects as the likely explanation behind why bamboo may be conferring some degree of protection to the fish.