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

Abstract

Proliferative kidney disease (PKD) caused by the myxozoan parasite Tetracapsuloides bryosalmonae is an emerging salmonid disease implicated in recent declines in salmonid populations. Laboratory experiments have shown that the clinical symptoms of PKD exacerbate with increasing temperature. However, empirical evidence for a relationship between climate change and PKD driven declines in wild salmonid stocks is scarce. The current study uses both empirical data and ecological niche modelling to extrapolate future changes in temperature and precipitation on the spread of PKD in relation to changes in suitability of rivers for its primary bryozoan and secondary salmonid hosts. A 20‐year dataset on brown trout density using standardised method shows a decline of more than 50% in the population of the river Wutach, south‐western Germany at 536–755 m elevation. The decline coincides with higher prevalence of PKD. This decline was temperature related and driven by reduced local survival of parr to yearlings. Kidney hyperplasia was highest at low elevations and correlated negatively with trout density. Niche models based on state‐wide data show strong overlap in the areas suitable for T. bryosalmonae and its primary bryozoan hosts, and a strong link with temperature. Projections based on moderate to high emission‐case climate change scenarios predict a 50%–82% decrease in the area suitable for salmonids within this century, linked to PKD. The empirical data identify temperature‐mediated PKD as the underlying cause of the population decline. This relationship was corroborated by the niche modelling results. The highest losses are expected in projected salmonid suitable areas where salmonid habitats currently overlap with areas suitable for T. bryosalmonae. With ongoing climate change, both current and future populations are at severe risk to T. bryosalmonae and its associated disease PKD. Conservation efforts of salmonid stocks are dependent on climate mitigation and measures to help salmonids adapt to the disease.

Patterns of Tetracapsuloides bryosalmonae infection of three salmonid species in large, deep Norwegian lakes

“…Several factors have been suggested to influence the risk of infection and spread of T. bryosalmonae in lakes and rivers, often linked with increased water temperatures (Hendrick et al, 1986;Rubin et al, 2019;Tops et al, 2006Tops et al, , 2009Waldner et al, 2021), manipulations of watercourses, fish stocking, increased water pollution, differences in susceptibility and immune responses to the parasite (Bailey et al, 2019;Grabner & El-Matbouli, 2009;Kumar et al, 2013;Ros et al, 2021;Schmidt-Posthaus et al, 2017). Outbreak of PKD is observed when the water temperature exceeds 12-15°C for more than 14 days Brown et al, 1991;Ferguson, 1981;Hedrick et al, 1993;Wahli et al, 2002), and high morbidity and mortality of wild salmonids associated with PKD are mainly observed during summer and early autumn in the Northern Hemisphere (Mo & Jørgensen, 2017;Sterud et al, 2007;Wahli et al, 2008).…”

“…Outbreak of PKD is observed when the water temperature exceeds 12-15°C for more than 14 days Brown et al, 1991;Ferguson, 1981;Hedrick et al, 1993;Wahli et al, 2002), and high morbidity and mortality of wild salmonids associated with PKD are mainly observed during summer and early autumn in the Northern Hemisphere (Mo & Jørgensen, 2017;Sterud et al, 2007;Wahli et al, 2008). It is expected that the spread of the parasite T. bryosalmonae and outbreaks of PKD will constitute an increased threat to salmonids in the future, due to climate change with expected increasing water temperatures, as well as human activities and water pollution (Mo & Jørgensen, 2017;Ros et al, 2021;Strepparava et al, 2017;Sudhagar et al, 2019;Tops et al, 2006).…”

“…Several bryozoan species belonging to the Class Phylactolaemata are shown to host T. bryosalmonae, including Fredericella sultana, Plumatella rugosa, P. fruticosa, P. emerginata, Plumatella sp., Cristatella mucedo, and Pectinatella magnifica (Anderson et al, 1999;Longshaw et al, 1999;Okamura et al, 2001;Ros et al, 2021;Sudhagar et al, 2019); F. sultana considered to be the main primary host (Abd-Elfattah, Fontes, et al, 2014;Ros et al, 2021). In Norway, bryozoan species belonging to the Class Phylactolaemata are widespread throughout the country (Økland and Økland, 2000, 2001, 2002; 2005; Økland et al, 2003).…”

“…In Switzerland, outbreaks of PKD in wild and farmed rainbow trout, brown trout and grayling have been documented almost every year since the first diagnosis in 1979 (Wahli et al, 2002). T. bryosalmonae is now considered to be one of the major factors for decline in wild populations of brown trout and rainbow trout in the alpine rivers (Burkhardt-Holm et al, 2005;Gorgoglione et al, 2016;Lewisch et al, 2018;Ros et al, 2021;Sudhagar et al, 2019). Also in other countries in Europe and North America, the parasite and mortality due to PKD are observed in Atlantic salmon, Arctic charr, European whitefish (Coregonus lavaretus) and mountain whitefish (Prosopium williamsoni) (Feist et al, 2002;Forseth, Jørgensen, et al, 2017;Gorgoglione et al, 2016;Hutchins et al, 2021;Kristmundsson et al, 2010;Mo, 2007;Mo & Jørgensen, 2017;Mo et al, 2011;Naldoni et al, 2019;Opitz & Rhoten, 2016;Skovgaard & Buchmann, 2012;Sterud et al, 2007;Sudhagar et al, 2019;Svavarsdottir, 2016;Vasemagi et al, 2017;Wahli et al, 2002).…”

Kinetics of Parasite-Specific Antibody and B-Cell-Associated Gene Expression in Brown Trout, Salmo trutta during Proliferative Kidney Disease

“…The major clinical manifestations of this disease in infected fish include renal hyperplasia (kidney swelling) and splenomegaly (spleen enlargement) resulting from intense inflammatory response in these tissues. During advanced pathogenesis, pale gills, indicative of anaemia, are frequently observed [ 9 ].…”