Parasite infection and decreased thermal tolerance: impact of proliferative kidney disease on a wild salmonid fish in the context of climate change

Abstract

Summary Parasites and pathogens can have an important effect on their host's thermal resistance. The impact of parasite infection on host physiological performances has traditionally been studied in controlled laboratory conditions, and much less is known about its actual effects in wild populations. Nonetheless, such knowledge is critical when assessing the effect of climate change on the future survival of the host. Tetracapsuloides bryosalmonae is a myxozoan endoparasite causing proliferative kidney disease (PKD) in salmonids. Infection and clinical symptoms of PKD are dependent on environmental temperature and PKD has become an emerging disease of primary importance for farmed and wild salmonids in the last decades. Despite important achievements in understanding PKD pathology in recent years, there are still crucial gaps in the knowledge of the disease ecology, notably in how the parasite affects host performance in the wild. We sampled juvenile (0+) brown trout (Salmo trutta) from the wild during early and late summer and assessed relative parasite load (DNA quantification with qPCR) and disease severity (kidney hyperplasia). We also measured haematocrit, leucocyte formula, aerobic scope and upper thermal tolerance in a field‐physiology approach in order to better understand the relationships between PKD severity and host performance. By using wild‐caught individuals and performing measurements directly on location, we aimed to gain insights into host physiology in a natural environment while avoiding biases caused by laboratory acclimation. We found that most physiopathological symptoms in the wild were strongly correlated with kidney hyperplasia, but more weakly linked to parasite load. Disease severity was positively correlated with anaemia and abundance of circulating thrombocytes, and negatively correlated with aerobic scope and thermal tolerance. Our results suggest that impaired aerobic performances and thermal tolerance in infected fish may potentially result in decreased host survival in the wild, especially in relation with predicted higher average summer temperatures and increased frequency of extreme events (summer heatwaves) in the context of global climate change. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12701/suppinfo is available for this article.

First record of proliferative kidney disease agent Tetracapsuloides bryosalmonae in wild brown trout and European grayling in Finland

“…Comparison of the renal swelling of the 6 samples with the earlier data from anadromous brown trout collected from Estonia (River Vainupea, Bruneaux et al 2017) indicated that some individuals from the River Siuntionjoki exhibited severe signs of PKDinduced kidney hyperplasia (K:B ratio > 0.3; Fig. 2).…”

“…Before storing the sample in 96% ethanol, the body section was photo graphed with a digital camera for measurement of the kidney-to-body thickness ratio (K:B ratio, as in Fig. 1a in Bruneaux et al 2017) the PKD-induced hyperplasia of the kidney. We compared the estimated kidney hyperplasia measurements (K:B ratio) to published data on T. bryo sal monae-infected 0+ brown trout (n = 77) collected from the River Vainupea, Estonia (Bruneaux et al 2017).…”

“…The clinical symptoms of PKD in fish include renal swelling, exophthalmia, and anemia (Hedrick et al 1993). Anemia decreases individual performance of fish by lowering metabolic rate and aerobic scope, also causing a reduction in upper thermal tolerance (Bruneaux et al 2017). As a result, PKD can lead to high mortalities at elevated water temperatures, while fish show less severe clinical signs of disease and are able to survive the infection when water temperature is low (Bettge et al 2009, Okamura et al 2011, Schmidt-Posthaus & Wahli 2015.…”

“…1a the PKD-induced hyperplasia of the kidney. We compared the estimated kidney hyperplasia measurements (K:B ratio) to published data on T. bryo sal monae-infected 0+ brown trout (n = 77) collected from the River Vainupea, Estonia (Bruneaux et al 2017). When testing the multiplex PCR method for T. bryosalmonae screening in grayling, we noted that the amplification product of the Salmo sp.-specific fragment was very weak or absent.…”

“…Therefore, future efforts to understand the impact of T. bryosalmonae in salmonid fish should focus on parasite abundance and prevalence as well as the physiological impact of infection by quantifying disease symptoms, such as kidney hyperplasia and hematocrit levels (e.g. Bruneaux et al 2017, Debes et al 2017. In view of the endangered status of brown trout in Finland (Finnish Red Data Book;Rassi et al 2010), more information about the occurrence of T. bryosalmonae, its bryozoan host, host condition-dependent developmental cycling (Okamura 2016), and the physiological and ecological effects of PKD on wild trout populations is urgently needed.…”