Keeping an Eye on Wild Brown Trout (Salmo trutta) Populations: Correlation Between Temperature, Environmental Parameters, and Proliferative Kidney Disease

Abstract

Proliferative kidney disease (PKD) is an emerging disease of salmonids caused by the myxozoan parasite Tetracapsuloides bryosalmonae , which plays a major role in the decrease of wild brown trout ( Salmo trutta ) populations in Switzerland. Strong evidence demonstrated that water temperature modulates parasite infection. However, less knowledge exists on how seasonal water temperature fluctuations influence PKD manifestation under field conditions, how further environmental factors such as water quality may modulate the disease, and whether these factors coalesce with temperatures role possibly giving rise to cumulative effects on PKD. The aims of this study were to (1) determine the correlation between seasonal course of water temperature and PKD prevalence and intensity in wild brown trout populations, (2) assess if other factors such as water quality or ecomorphology correlate with the infection, and (3) quantitatively predict the implication of these factors on PKD prevalence with a statistical model. Young-of-the-year brown trout were sampled in 45 sites through the Canton of Vaud (Switzerland). For each site, longitudinal time series of water temperature, water quality (macroinvertebrate community index, presence of wastewater treatment plant effluent) and ecomorphological data were collected and correlated with PKD prevalence and intensity. 251 T. bryosalmonae -infected trout of 1,118 were found (overall prevalence 22.5%) at 19 of 45 study sites (42.2%). Relation between PKD infection and seasonal water temperature underlined that the mean water temperature for June and the number of days with mean temperature ≥15°C were the most significantly correlated parameters with parasite prevalence and intensity. The presence of a wastewater treatment plant effluent was significantly correlated with the prevalence and infection intensity. In contrast, macroinvertebrate diversity and river ecomorphology were shown to have little impact on disease parameters. Linear and logistic regressions highlighted quantitatively the prediction of PKD prevalence depending on environmental parameters at a given site and its possible increase due to rising temperatures. The model developed within this study could serve as a useful tool for identifying and predicting disease hot spots. These results support the importance of temperature for PKD in salmonids and provides evidence for a modulating influence of additional environmental stress factors.

Health Surveillance of Wild Brown Trout (Salmo trutta fario) in the Czech Republic Revealed a Coexistence of Proliferative Kidney Disease and Piscine Orthoreovirus-3 Infection

“…In this study, the only two repeatedly sampled locations showed higher percentages of the examined fish displaying pathomorphological signs of PKD, along with greater numbers of samples tested positive for the presence of T. bryosalmonae using both IHC and qPCR in November, compared with the situation in April. Although the temperature in every sampling campaign presented was not optimal for the propagation of the parasite [ 43 ], the data confirmed the observed cycle of the infection in brown trout, with infection rates and pathoanatomical changes peaking in late summer [ 24 ], and a significant decline during cold temperature periods [ 25 , 27 ] when a partial or complete regeneration of renal tissue occurs [ 38 ]. To establish whether the reoccurring PKD symptoms in specific rivers are caused by reinfection of susceptible animals [ 38 ] or by a persistence of the parasite in clinically healthy fish [ 46 , 47 ] was beyond the scope of this study and would require additional repeated testing of selected locations.…”

“…Using histopathology and IHC, the PKD situation was best mapped in Switzerland, where T. bryosalmonae was found in 40–50% of the sampled rivers [ 41 , 42 , 43 ]. Studies on brown trout were also conducted in England (86% of rivers [ 44 ]) and Estonia (around 50% of rivers [ 45 ]).…”

Current and projected impacts of the parasite Tetracapsuloides bryosalmonae (causative to proliferative kidney disease) on Central European salmonid populations under predicted climate change

“…Temperature driven PKD induced population decline is multifaceted, involving many indirect effects on survival (Burkhardt‐Holm & Zehnder, 2018). For example, PKD may make fish more susceptible to existing environmental stressors (Bruneaux et al., 2017) such as warmer than average summers (Borsuk et al., 2006; Hari set al., 2006; Rubin et al., 2019), pollution (Bailey et al., 2018), or secondary infection with other pathogens (Arndt et al., 2019; Chilmonczyk et al., 2002; Hedrick et al., 1993). PKD compromised condition (Bruneaux et al., 2017) could potentially decrease survival through subsequent metabolic challenging periods like winter (recruitment) or migration (Kent et al., 1995).…”

“…The current 51.9% decrease in brown trout density in the Wutach in the last decade is suggestive of a recent upstream spread of T. bryosalmonae . The pending increase in temperatures due to climate change make it increasingly essential for surviving salmonid populations in rivers such as the Wutach to have secure access to head waters, small tributaries or other areas with relatively cool and well oxygenated water, where the effects of T. bryosalmonae infection tend to be mild (Rubin et al., 2019; Strepparava et al., 2018; Wahli et al., 2008).…”

“…Moreover, it has been suggested that conditional effects inflicted by PKD (see Bruneaux et al., 2017) might affect the return rates of anadromous salmonid species (Kent et al., 1995). The pathogenicity of PKD is temperature dependent (Clifton‐Hadley et al., 1986; Okamura et al., 2011; Rubin et al., 2019; Strepparava et al., 2018). Therefore, it was suggested that recent declines in salmonid stocks were the result of elevated mortality caused by PKD under climate change (Burkhardt‐Holm et al., 2002; Burkhardt‐Holm & Zehnder, 2018; Carraro et al., 2017; Lewisch et al., 2018; Waldner et al., 2020).…”