A class of their own? Water-soluble polymer pollution impacting a freshwater host-pathogen system.

While the inclusion of synthetic polymers such as primary microplastics within personal care products have been widely restricted under EU/UK Law, water-soluble polymers (WSPs) have so far slipped the net of global chemical regulation despite evidence that these could be polluting wastewater effluents at concentrations greatly exceeding those of microplastics. Polyvinyl alcohol (PVA) and polyvinylpyrrolidone (PVP) represent WSPs with common industry and household uses, down-the-drain disposal and a direct route to wastewater treatment plants, conveying high risk of environmental leaching into freshwater ecosystems. The current study is the first investigating the impacts of predicted environmental concentrations of these WSPs on life-history traits of two freshwater species also constituting a disease model (fish - Poecilia reticulata and parasite - Gyrodactylus turnbulli). Single effects of WSPs on fish as well as their interactive effects with infection of the ectoparasite were determined over a 45-day exposure. Generally, WSPs reduced fish growth and increased routine metabolic rate of fish implying a depleted energetic budget, however these effects were dose, exposure time and polymer dependent. Parasitic infection alone caused a significant reduction in fish growth and enhanced fish routine metabolic rate. In contrast, a non-additive effect on metabolic rate was evident in fish experiencing simultaneous infection and WSP exposure, suggesting a protective effect of the two WSPs for fish also exposed to a metazoan ectoparasite. Off-host parasite survival was significantly lowered by both WSPs; however, parasite counts of infected fish also exposed to WSP were not significantly different from the control, implying more complex mechanisms may underpin this stressor interaction. Distinct detrimental impacts were inflicted on both organisms implying environmental leaching of WSPs may be causing significant disruption to interspecies interactions within freshwater ecosystems. Additionally, these results could contribute to sustainable development in industry, as we conclude PVA represents a less harmful alternative to PVP.

The impacts of synthetic and cellulose-based fibres and their associated dyes on fish hosts and parasite health.

Plastic pollution is now a ubiquitous feature of freshwater systems and the majority of this is fibrous. Here, we test the effects of plastic and cellulose-based fibres (polyester, cotton, and bamboo from commercial clothing) on fish host-parasite interactions using a freshwater fish host-parasite model system (guppy Poecilia reticulata-Gyrodactylus turnbulli). For uninfected fish, polyester exposure was associated with significantly higher mortality rates compared with the other two fibre types. For infected fish, whilst polyester and cotton exposure were not associated with any significant changes to parasite burdens, fish exposed to bamboo fibres had significantly reduced maximum parasite burdens compared with fish not exposed to any fibres, indicating that the bamboo fibres and/or associated dyes conferred some degree of resistance or tolerance. Whilst unable to determine the exact nature of the chemical dyes, when testing off-host parasite survival on exposure to the fibre dyes, cotton and particularly polyester dyes were associated with higher parasite mortality compared to bamboo. Overall, we add to the growing body of evidence which shows that polyester microplastic fibres and their associated dyes can be detrimental for both fish and parasite survival, and we highlight the need for increased transparency from textile industries on the chemical identity of fabric dyes.

Microplastic exposure and consumption increases susceptibility to gyrodactylosis and host mortality for a freshwater fish.

Microplastics have been found in all surveyed ecosystems and in the diet of multiple species. Detrimental health impacts of microplastic consumption include reduced growth and fecundity, metabolic stress and immune alterations for both invertebrates and vertebrates. Limited information exists, however, on how disease resistance may be affected by microplastic exposure and consumption. Here, the impact of microplastic (0.01 and 0.05 mg l-1 of polypropylene) on fish host susceptibility to disease and mortality was assessed using the guppy Poecilia reticulata-gyrodactylid Gyrodactylus turnbulli system. Fish exposed to and/or consuming microplastic at both concentrations demonstrated significantly higher pathogen burdens over time compared with fish fed a plastic-free diet. Furthermore, microplastic (at both tested concentrations) was associated with increased mortality events for fish within all treatments, regardless of host infection status. This study adds to the growing body of evidence showing that microplastic pollution can be detrimental to fish welfare by reducing disease resistance.

Differential effects of two prevalent environmental pollutants on host-pathogen dynamics.

Chemical pollutants are a major factor implicated in freshwater habitat degradation and species loss. Microplastics and glyphosate-based herbicides are prevalent pollutants with known detrimental effects on animal welfare but our understanding of their impacts on infection dynamics are limited. Within freshwater vertebrates, glyphosate formulations reduce fish tolerance to infections, but the effects of microplastic consumption on disease tolerance have thus far not been assessed. Here, we investigated how microplastic (polypropylene) and the commercial glyphosate-based herbicide, Roundup®, impact fish tolerance to infectious disease and mortality utilising a model fish host-pathogen system. For uninfected fish, microplastic and Roundup had contrasting impacts on mortality as individual stressors, with microplastic increasing and Roundup decreasing mortality compared with control fish not exposed to pollutants. Concerningly, microplastic and Roundup combined had a strong interactive reversal effect by significantly increasing host mortality for uninfected fish (73% mortality). For infected fish, the individual stressors also had contrasting effects on mortality, with microplastic consumption not significantly affecting mortality and Roundup increasing mortality to 55%. When combined, these two pollutants had a moderate interactive synergistic effect on mortality levels of infected fish (53% mortality). Both microplastic and Roundup individually had significant and contrasting impacts on pathogen metrics with microplastic consumption resulting in fish maintaining infections for significantly longer and Roundup significantly reducing pathogen burdens. When combined, the two pollutants had a largely additive effect in reducing pathogen burdens. This study is the first to reveal that microplastic and Roundup individually and interactively impact host-pathogen dynamics and can prove fatal to fish.

Noise pollution: acute noise exposure increases susceptibility to disease and chronic exposure reduces host survival.

Anthropogenic noise is a pervasive global pollutant that has been detected in every major habitat on the planet. Detrimental impacts of noise pollution on physiology, immunology and behaviour have been shown in terrestrial vertebrates and invertebrates. Equivalent research on aquatic organisms has until recently been stunted by the misnomer of a silent underwater world. In fish, however, noise pollution can lead to stress, hearing loss, behavioural changes and impacted immunity. But, the functional effects of this impacted immunity on disease resistance due to noise exposure have remained neglected. Parasites that cause transmissible disease are key drivers of ecosystem biodiversity and a significant factor limiting the sustainable expansion of the animal trade. Therefore, understanding how a pervasive stressor is impacting host-parasite interactions will have far-reaching implications for global animal health. Here, we investigated the impact of acute and chronic noise on vertebrate susceptibility to parasitic infections, using a model host-parasite system (guppy-Gyrodactylus turnbulli). Hosts experiencing acute noise suffered significantly increased parasite burden compared with those in no noise treatments. By contrast, fish experiencing chronic noise had the lowest parasite burden. However, these hosts died significantly earlier compared with those exposed to acute and no noise treatments. By revealing the detrimental impacts of acute and chronic noise on host-parasite interactions, we add to the growing body of evidence demonstrating a link between noise pollution and reduced animal health.

Cost of a deprived environment - increased intraspecific aggression and susceptibility to pathogen infections.

A lack of environmental enrichment can be severely detrimental to animal welfare. For terrestrial species, including humans, barren environments are associated with reduced cognitive function and increased stress responses and pathology. Despite a clear link between increased stress and reduced immune function, uncertainty remains on how enrichment might influence susceptibility to disease. For aquatic vertebrates, we are only now beginning to assess enrichment needs. Enrichment deprivation in fish has been linked to increased stress responses, agonistic behaviour, physiological changes and reduced survival. Limited data exist, however, on the impact of enrichment on disease resistance in fish, despite infectious diseases being a major challenge for global aquaculture. Here, using a model vertebrate host-parasite system, we investigated the impact of enrichment deprivation on susceptibility to disease, behaviour and physiology. Fish in barren tanks showed significantly higher infection burdens compared with those in enriched enclosures and they also displayed increased intraspecific aggression behaviour. Infections caused hosts to have significantly increased standard metabolic rates compared with uninfected conspecifics, but this did not differ between enriched and barren tanks. This study highlights the universal physiological cost of parasite infection and the biological cost (increased susceptibility to infection and increased aggression) of depriving captive animals of environmental enrichment.

Partitioning the environmental drivers of immunocompetence.

By determining susceptibility to disease, environment-driven variation in immune responses can affect the health, productivity and fitness of vertebrates. Yet how the different components of the total environment control this immune variation is remarkably poorly understood. Here, through combining field observation, experimentation and modelling, we are able to quantitatively partition the key environmental drivers of constitutive immune allocation in a model wild vertebrate (three-spined stickleback, Gasterosteus aculeatus). We demonstrate that, in natural populations, thermal conditions and diet alone are sufficient (and necessary) to explain a dominant (seasonal) axis of variation in immune allocation. This dominant axis contributes to both infection resistance and tolerance and, in turn, to the vital rates of infectious agents and the progression of the disease they cause. Our results illuminate the environmental regulation of vertebrate immunity (given the evolutionary conservation of the molecular pathways involved) and they identify mechanisms through which immunocompetence and host-parasite dynamics might be impacted by changing environments. In particular, we predict a dominant sensitivity of immunocompetence and immunocompetence-driven host-pathogen dynamics to host diet shifts.

Not going with the flow: Locomotor activity does not constrain immunity in a wild fish.

Immunity is a central component of fitness in wild animals, but its determinants are poorly understood. In particular, the importance of locomotory activity as a constraint on immunity is unresolved. Using a piscine model (Gasterosteus aculeatus), we combined a 25-month observational time series for a wild lotic habitat with an open flume experiment to determine the influence of locomotor activity (countercurrent swimming) on natural variation in immune function. To maximize the detectability of effects in our flume experiment, we set flow velocity and duration (10 cm/s for 48 hr) just below the point at which exhaustion would ensue. Following this treatment, we measured expression in a set of immune-associated genes and infectious disease resistance through a standard challenge with an ecologically relevant monogenean infection (Gyrodactylus gasterostei). In the wild, there was a strong association of water flow with the expression of immune-associated genes, but this association became modest and more complex when adjusted for thermal effects. Our flume experiment, although statistically well-powered and based on a scenario near the limits of swimming performance in stickleback, detected no countercurrent swimming effect on immune-associated gene expression or infection resistance. The field association between flow rate and immune expression could thus be due to an indirect effect, and we tentatively advance hypotheses to explain this. This study clarifies the drivers of immune investment in wild vertebrates; although locomotor activity, within the normal natural range, may not directly influence immunocompetence, it may still correlate with other variables that do.