Exploration of the 2016 Yellowstone River fish kill and proliferative kidney disease in wild fish populations

Abstract

Proliferative kidney disease (PKD) is an emerging disease that recently resulted in a large mortality event of salmonids in the Yellowstone River (Montana, USA). Total PKD fish mortalities in the Yellowstone River were estimated in the tens of thousands, which resulted in a multi-week river closure and an estimated economic loss of US$500,000. This event shocked scientists, managers, and the public, as this was the first occurrence of the disease in the Yellowstone River, the only reported occurrence of the disease in Montana in the past 25 yr, and arguably the largest wild PKD fish kill in the world. To understand why the Yellowstone River fish kill occurred, we used molecular and historical data to evaluate evidence for several hypotheses: Was the causative parasite Tetracapsuloides bryosalmonae a novel invader, was the fish kill associated with a unique parasite strain, and/or was the outbreak caused by unprecedented environmental conditions? We found that T. bryosalmonae is widely distributed in Montana and have documented occurrence of this parasite in archived fish collected in the Yellowstone River prior to the fish kill. T. bryosalmonae had minimal phylogeographic population structure, as the DNA of parasites sampled from the Yellowstone River and distant water bodies were very similar. These results suggest that T. bryosalmonae could be endemic in Montana. Due to data limitations, we could not reject the hypothesis that the fish kill was caused by a novel and more virulent genetic strain of the parasite. Finally, we found that single-year environmental conditions are insufficient to explain the cause of the 2016 Yellowstone River PKD outbreak. Other regional rivers where we documented T. bryosalmonae had similar or even more extreme conditions than the Yellowstone River and similar or more extreme conditions have occurred in the Yellowstone River in the recent past, yet mass PKD mortalities have not been documented in either instance. We conclude by placing these results and unresolved hypotheses into the broader context of international research on T. bryosalmonae and PKD, which strongly suggests that a better understanding of bryozoans, the primary host of T. bryosalmonae, is required for better ecosystem understanding.

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

“…Naldoni et al (2019) found indications of parasite spore production in whitefish, but due to co-infection of a sphaerosporid species, they could not confirm that European whitefish is a true host for T. bryosalmonae . The parasite was also detected in mountain whitefish (Prosopium williamsoni) in a severe outbreak with high mortalities in Yellowstone, Montana, USA, in 2016 (Hutchins et al, 2021;Opitz, 2017;Opitz & Rhoten, 2016). Hutchins et al (2021) detected T. bryosalmonae presence in a broad host range in a wide distribution area of Montana, but mountain whitefish have the highest prevalence (50%) among the species.…”

“…The parasite was also detected in mountain whitefish (Prosopium williamsoni) in a severe outbreak with high mortalities in Yellowstone, Montana, USA, in 2016 (Hutchins et al, 2021;Opitz, 2017;Opitz & Rhoten, 2016). Hutchins et al (2021) detected T. bryosalmonae presence in a broad host range in a wide distribution area of Montana, but mountain whitefish have the highest prevalence (50%) among the species.…”

“…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).…”

It's a hard knock life for some: Heterogeneity in infection life history of salmonids influences parasite disease outcomes

“…For example, their size may enable them to stay in areas with higher water flow rates as has been reported for larger fish (Hockley et al, 2014). In this context, it has been suggested that often lower flow regimes are associated with the environmental parameters linked with an increased abundance of T. bryosalmonae malacospore release from the bryozoan host (Hutchins et al, 2021).…”

“…In this context, it has been suggested that often lower flow regimes are associated with the environmental parameters linked with an increased abundance of T . bryosalmonae malacospore release from the bryozoan host (Hutchins et al., 2021 ).…”