Do fish get wasted? Assessing the influence of effluents on parasitic infection of wild fish

Abstract

Many ecosystems are influenced simultaneously by multiple stressors. One important environmental stressor is aquatic pollution via wastewater treatment plant (WWTP) effluents. WWTP effluents may contribute to eutrophication or contain anthropogenic contaminants that directly and/or indirectly influence aquatic wildlife. Both eutrophication and exposure to anthropogenic contaminants may affect the dynamics of fish-parasite systems. With this in mind, we studied the impact of WWTP effluents on infection of brown trout by the parasite Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD). PKD is associated with the long-term decline of wild brown trout (Salmo trutta) populations in Switzerland. We investigated PKD infection of brown trout at two adjacent sites (≈400 m apart) of a Swiss river. The sites are similar in terms of ecology except that one site receives WWTP effluents. We evaluated the hypothesis that fish inhabiting the effluent site will show greater susceptibility to PKD in terms of prevalence and disease outcome. We assessed susceptibility by (i) infection prevalence, (ii) parasite intensity, (iii) host health in terms of pathology, and (iv) estimated apparent survival rate. At different time points during the study, significant differences between sites concerning all measured parameters were found, thus providing evidence of the influence of effluents on parasitic infection of fish in our study system. However, from these findings we cannot determine if the effluent has a direct influence on the fish host via altering its ability to manage the parasite, or indirectly on the parasite or the invertebrate host via increasing bryozoa (the invertebrate host) reproduction. On a final note, the WWTP adhered to all national guidelines and the effluent only resulted in a minor water quality reduction assessed via standardized methods in this study. Thus, we provide evidence that even a subtle decrease in water quality, resulting in small-scale pollution can have consequences for wildlife.

Keywords: Aquatic pollution; Host-parasite interactions; Multiple stressors; PKD; Tetracapsuloides bryosalmonae; Wastewater; Wild fish.

Figure 1. Location of sampling sites along the Boiron in the canton of Vaud, Switzerland.

Two sites, a short distance apart (∼400 m) were sampled: the Amont step (46°29′56.171″N 6°28′01.204″E) and the Aval step (46°29′47.961″N 6°28′13.301″E). Also included is the location of the wastewater treatment plant (WWTP) (46°29′52.513″N 6°28′05.500″E) and the effluent (just below the highway).

Figure 2. Daily mean temperature of sampling sites.

Water temperature curves measured throughout the year at the sampling sites the Amont step (blue line) and the Aval step (red line). Black dotted line indicates 15 °C, the critical water temperature for proliferative kidney disease-related clinical signs and mortality in trout.

Figure 3. Proliferative kidney disease dynamics observed in infected fish sampled at the Amont and Aval step.

(A) Infection prevalence and (B) Parasite intensity (black lines indicate mean ± SE) at sampling point of the Amont (blue bars (A) or blue squares (B)) and the Aval (red bars (A) or red circles (B)) sites. Parasite intensity was determined using copy numbers of parasite DNA as a proxy. Asterisks indicate levels of significance (t-Test), *P < 0.05, **P < 0.01, and ***P < 0.001. N = 25 per site, per monthly sampling per site.

Figure 4. Fish body weight at the Amont and Aval.

Amont (blue squares) and Aval (red circles) (black lines indicate mean ± SE) at different sampling points. Asterisks indicate levels of significance (t-Test), *P < 0.05, **P < 0.01, and ***P < 0.001. N = 25 per site, per monthly sampling per site.

Figure 5. Histologicalimages of the posterior kidney.

(A) Demonstrates a zero in all categories according to the histological assessment and (B–D) the highest scores in each category. (A) Is from a fish sampled at the Amont in June. (B) Is from a fish sampled at the Aval in August showing a score of six for infection degree (presence and distribution of parasites). (C) Is also from a fish sampled at the Aval in August showing a score of five (moderate to severe) for tissue proliferation. (D) Is from a fish sampled at the Amont in September showing a score of five for fibrous tissue. Scale bar = 50 μm. All pictures are taken from slides stained with H&E.

Figure 6. Correlation of copy number of T. bryosalmonae DNA per gram of kidney tissue and host health at each sampling site.

(A) Amont step (blue squares) and (B) Aval step (red circles). Pearson correlation coefficients r as well as confidence intervals are given (black lines). Tissue proliferation score determined via histology and used as a proxy for host health. Y-axis is inverted to indicate that an increase in tissue proliferation is associated with a decrease in host health. There were no significant correlations between the variables at either sampling site. For the Amont step N = 63 and for the Aval step N = 82.

Figure 7. Estimates generated from the capture-mark-recapture method using PIT tags of fish at the Amont and Aval step.

Estimations include apparent (AP) survival rate, mortality and possible emigration at Amont step (blue) and Aval step (red). While could be assumed that emigrated fish may have died post dispersal, though this is impossible to confirm, thus, for the sake of the study, these fish were defined as emigrated. N is indicated above the respective bar.