Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae (Myxozoa)

Abstract

Extensive mortality in Atlantic salmon fry was reported in the River Åelva from 2002 to 2004. Dead fish were collected in late summer 2006, and live fish were sampled by electrofishing in September the same year. At autopsy and in histological sections, the fish kidneys were found to be pale and considerably enlarged. Proliferative lesions with characteristic PKX cells were seen in a majority of the fish. DNA from kidney samples of diseased fish was subjected to PCR and sequencing, and the amplified sequences matched those of Tetracapsuloides bryosalmonae. We concluded that this myxozoan transmitted from bryozoans was the main cause of the observed mortality in salmon fry in 2006. Results from quantitative electrofishing in 2005 and 2006, combined with the observed fry mortality from 2002 to 2004, show that the smolt production in the river is severely reduced and that T. bryosalmonae is the most likely explanation for this decline. The present study is the first to report a considerable negative population effect in wild Atlantic salmon due to proliferative kidney disease (PKD). It also represents the northernmost PKD outbreak in wild fish. The river is regulated for hydroelectric power purposes, causing reduced water flow and elevated summer temperatures, and the present PKD outbreak may serve as an example of increased disease vulnerability of northern fish populations in a warmer climate.

Tetracapsuloides bryosalmonae and PKD in juvenile wild salmonids in Denmark

“…In Switzerland, it has been suggested that recent decreases in brown trout populations were caused by PKD (Wahli et al 2002(Wahli et al , 2007. A similar scenario is thought to be the case for Atlantic salmon in Norway (Sterud et al 2007), and (Kristmundsson et al 2010) hypothesize that PKD may play a significant role in the recent decline in Arctic charr populations in Iceland. Indeed, there is justification for concluding that PKD is an important factor for these declines in trout populations, and it is to be expected that the consequences of PKD will become more severe if water temperatures are to increase in the future (Burkhardt-Holm & Scheurer 2007, Okamura et al 2011.…”

“…Yet, the impact of PKD on wild fish is a matter of some uncertainty because the effect of PKD on wild fish populations has not been adequately documented. At some European localities, it has been concluded that PKD is responsible for high mortality in wild brown trout Salmo trutta (Wahli et al 2002(Wahli et al , 2007 and Atlantic salmon S. salar (Sterud et al 2007). Even though this is probable, it is difficult, however, to prove with certainty that PKD is the only cause of the observed mortalities.…”

“…Investigations have confirmed infections with T. bryosalmonae in wild populations of salmonid fishes both in North America and in Europe. The presence of T. bryosalmonae has been demonstrated in wild fish through histological observations of parasite cells (Hedrick et al 1993, Braden et al 2010, by PCR and sequencing (Sterud et al 2007), and in addition, wild fish with pathological signs corresponding to PKD have been reported (Wootten & McVicar 1982, Bucke et al 1991, Feist & Bucke 1993, Sterud et al 2007). Yet, the impact of PKD on wild fish is a matter of some uncertainty because the effect of PKD on wild fish populations has not been adequately documented.…”

“…Intuitively, T. bryosalmonae is most probably common in natural freshwater habitats, since its bryozoan hosts are widespread in nature (Wiebach 1960, Wood 2002, and PKD is being found in more and more fish populations of salmonids, but so far only in freshwater (Sterud et al 2007, Kristmundsson et al 2010. Furthermore, infections in farmed fish are thought to originate from the environment, i.e.…”

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

“…There is a growing body of evidence indicating that some pathogens become more prevalent (Chiaramonte, Munson, & Trushenski, 2016; Sterud et al., 2007) and more virulent at warmer temperatures (Smith et al., 2014). For example, it has been shown that increased expression of virulence factors is correlated with increased temperature in Vibrio species (Mahoney, Gerding, Jones, & Whistler, 2010; Oh, Lee, Lee, & Choi, 2009).…”