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What is PKD?

Proliferative kidney disease (PKD) is a disease of salmonid fish caused by the endoparasitic myxozoan,(Okamura et al. 2011).

Clinical PKD is characterized by a massive inflammatory response caused by cells proliferating in the kidney and spleen in salmonid fish infected with T. bryosalmonae. However many salmonid fish infected with T. bryosalmonae do not develop clinical PKD, especially when water temperatures are below 9° C. Thus, occurrence of T. bryosalmonae in fish or in the water does not mean that a fish will develop clinical PKD and die. Fish with subclinical infections may also be able to carry the parasite indefinitely, allowing the continuous production of spores (Okamura et al. 2011).  

 

What is Tetracapsuloides bryosalmonae?

T. bryosalmonae is a eukaryotic myxozoan parasite in the phylum cnidaria (the same phylum that contains coral and jellyfish). It has a complex life cycle, infecting fish and bryozoans and having both endoparasitic and spore-like planktonic life stages associated with both fish and bryozoan hosts.

 

What is PKX?

PKD has been recognized since the early 20th century, but the disease source of PKD was a mystery until 1999 when was identified as the causative agent. Prior to its identification in 1999, the organism that caused the disease was simply referred to as the proliferative kidney organism “X”, hence PKX. However, the disease-causing agent is now referred to by its scientific name, .

 

What is a bryozoan?

Bryozoans are sessile, colonial, aquatic invertebrates that are found throughout the world in both marine and freshwater systems. Freshwater bryozoans (Phylactolaemates) generally experience optimal growth at temperatures between 15-28 °C (59-83 °F; Wood 2009). Phylactolaemate populations are often subject to seasonal dynamics:  a spore-like statoblast (a reproductive body comparable to a seed) affixes to a hard substrate and establishes a colony, the colony grows throughout the warm season and produces new statoblasts. The colony then dies in the cold months and the population is perpetuated with new statoblasts. However, some species are capable of overwintering as a mature colony.

 

Is Tetracapsuloides bryosalmonae an invasive species?

We do not know and likely will never know if . By definition, an invasive species is one that has been introduced to an environment where it is non-native, or alien, and whose introduction causes environmental or economic damage or harm to human health (Pagad et al. 2015). Prior to August 2016, PKD or T. bryosalmonae had not been documented in the Yellowstone River subbasin.   

 

To learn about PKD, the US Geological Survey’s Northern Rocky Mountain Science Center has partnered with the USFWS Bozeman Fish Health Center and Montana FWP to develop molecular tools for surveillance and to use these tools to describe the occurrence and distribution of in regional rivers.

 

Using these molecular tools, we have detected DNA in seemingly healthy salmonids in most major rivers and tributaries in western Montana (see answer to next question). We have also detected DNA in archived fish samples collected in 2012 in the Yellowstone River near Big Timber, MT. PKD was also documented in Middle Creek Reservoir (Smith River drainage) in 1990 and 1991 and in Cherry Creek (Madison River) in the 1990s(Macconnell & Peterson 1992).

 

These data indicate that is broadly distributed and has been in the region for decades. We do not have data to determine when first inhabited the region so cannot definitively label as a native or invasive species.

 

Regardless of ’s status as a native or invasive species, it critical to clean, drain and dry all gear and equipment since unintentional movement of the parasite could extend the geographical range of the disease and facilitate novel and potentially deadly combinations of fish, bryozoan, and parasite strains.

 

 

Where in Montana, other than the Yellowstone River, has PKD and/or Tetracapsuloides bryosalmonae been documented?

In Montana, PKD was first documented in cutthroat trout in Middle Creek Reservoir (Smith River drainage) in 1990 and 1991 (Macconnell & Peterson 1992) and in Cherry Creek (Madison River) in the 1996 (FWP Fish Health Lab, pers. comm.).

 

We used molecular DNA tools to screen fish tissue samples collected in 2016 and 2017 for presence of DNA. It is important to underscore that presence of the parasite’s DNA in fish tissue is not indicative of presence of the clinical PKD disease or fish mortality and that our findings likely do not represent the full extent of ’s distribution. Major tributaries where we have detected DNA include:

 

• Big Hole R.

• Bighorn R.

• Blackfoot R.

• Boulder R.

• Clark Fork R.

• East Gallatin R.

• Flathead R.

• Gallatin R.

• Jefferson R.

• Madison R.

• Middle Fork of Flathead R.

• North Fork of Flathead R.

• Missouri R.

• Ruby R.

• Shields R.

• Smith R.

• Stillwater R.

• Sun R.

 

How long has Tetracapsuloides bryosalmonae been in the area?

PKD-like disease signs in North America were first documented in the 1960s in the American River Hatchery (CA; Hedrick et al. 1985). The first verified outbreak of PKD in North America was in 1981, at an Idaho fish hatchery (Smith et al. 1984), and was subsequently detected in salmonids in California, Washington and British Columbia.  In Montana, PKD was first documented in cutthroat trout in Middle Creek Reservoir (Smith River drainage) in 1990 and 1991 (MacConnell and Peterson 1992). T.bryosalmonae was detected in Cherry Creek (tributary to the lower Madison) in 1996 (FWP Fish Health Lab, pers. comm.).

 

Where else has PKD resulted in fish kills and how do they compare to the Yellowstone fish kill?

The magnitude of the Yellowstone River fish kill appears to be unprecedented, as no other published report or study describes events were > 1000 fish died. Because the population size of Mountain whitefish in the Yellowstone River is not known, it is unclear what percent of this population died. Reports from fish farms and hatcheries do indicate instances with 85% - 100% mortality. In North America, PKD fish kills have been infrequently reported in technical or peer-reviewed literature. Specific examples include:

 

European examples:

• 85% reduction in Atlantic salmon parr densities in the River Aelva in central Norway (Sterud et al. 2007). The number of dead fish sampled each day varied from 3 – 120.

• Swiss lowland rivers, models indicate PKD can cause brown trout mortality of >25% (Borsuk et al. 2006)

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North American examples:

• Cutthroat trout in Middle Creek Reservoir, MT (MacConnell and Peterson 1992)

• Rainbow trout in Hagerman Fish Hatchery, ID (Smith et al. 1984)

• Mountain whitefish in South Fork of Snake River, ID

• Trout in Silver Creek, ID

• Chinook salmon in Merced & Tuolumne  rivers, CA (Foott, Stone & Nichols 2007)

  • First detected in the 1980s

  • In hatchery, 27% cumulative mortality of juvenile chinook salmon

• Wild sockeye salmon in Vancouver Island, British Columbia (Kent et al. 1995)

• Pink salmon in the Quinsam River, British Columbia (Braden et al. 2010)

 

Since Tetracapsuloides bryosalmonae occurs in other rivers in the region, why did a PKD fish die-off only occur in the Yellowstone River?

We do not know. Many regional rivers had stressful (e.g., high water temperature and low discharge) conditions similar or worse than the Yellowstone River in 2016, yet there were no documented PKD fish kills. Despite higher flows and cooler water temperatures in July, another documented PKD fish kill occurred in the Yellowstone River in 2017, though mortality was much lower. This unanticipated die-off further underscores how little we understand about PKD disease dynamics. Taken together, these results indicate that T. bryosalmonae is widely distributed and suggest that warm temperatures and low flow conditions cannot alone explain PKD-caused fish kills though these stressful conditions are clearly important to PKD.

 

Currently, we are collecting data to test two hypotheses that may explain why the Yellowstone River was more vulnerable to PKD. First, we are testing if variations in infection patterns across rivers are a result of different genetic types of and that genetic types in the Yellowstone River are distinct and potentially more virulent. Second, we are testing if bryozoan hosts for are more abundant in the Yellowstone River, though we do not know what past densities of bryozoans were like. We anticipate that there will not be a single answer that explains PKD fish die-offs in all places across all times.

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Will a PKD fish die-off happen again in the Yellowstone River or other rivers?

We don’t know, but suspect that future die-offs are possible. 

 

Why did PKD primarily kill Mountain whitefish in the Yellowstone River? Why not trout?

We don’t know why PKD primarily killed Mountain whitefish in the Yellowstone River and also in the South Fork of the Snake River (ID). No previous research has assessed Mountain whitefish vulnerability to PKD.

 

What research is being done to prevent, predict, or control PKD?

• Our collaborative team is currently doing research on the following topics related to PKD:

• Testing if variations in infection and disease are a result of different genetic types of T. bryosalmonae and that the 2016 outbreak was the result of a host-specific type.

• Validating environmental DNA (eDNA) tools for T. bryosalmonae surveillance and associate eDNA measurements with infection prevalence based on lethal fish sampling.

• Developing and validating quantitative PCR (qPCR) methods to characterize infection status and benchmark method against histological measures of disease state.

• Identify bryozoan species that act as hosts for T. bryosalmonae at sentinel sites in the Yellowstone River.

• Collect temporal data at sentinel sites on the target bryozoan hosts, fish hosts, parasite eDNA and environmental parameters that will eventually feed into epidemiological models to predict PKD outbreaks.

 

We are also collaborating with European PKD experts (B. Okamara and H. Hartikainen) to better describe T. bryosalmonae genomics and the factors that influence the contemporary distribution and potential virulence of different T. bryosalmonae genetic types.

 

How can private citizens and businesses help?

• Communicate the need for PKD research to local, state and federal lawmakers and legislative staff.

• If you see something suspicious like dead fish, disease signs or fish behavioral changes, please contact Montana FWP.

• Conserve water, low water causes stress to aquatic communities

• Minimize stress to fish during any fish kills.

• Follow aquatic invasive species prevention and containment best practices and clean, drain, and dry all gear and equipment.

 

​References

• Borsuk, M.E., Reichert, P., Peter, A., Schager, E. & Burkhardt-Holm, P. (2006) Assessing the decline of brown trout (Salmo trutta) in Swiss rivers using a Bayesian probability network. 224-244.

• Braden, L., Prosperi‐Porta, G., Kim, E. & Jones, S. (2010) Tetracapsuloides bryosalmonae in spawning pink salmon, Oncorhynchus gorbuscha (Walbaum), in the Quinsam River, British Columbia, Canada. Journal of Fish Diseases, 33, 617-621.

• Foott, J.S., Stone, R. & Nichols, K. (2007) Proliferative kidney disease (Tetracapsuloides bryosalmonae) in Merced River Hatchery juvenile Chinook salmon: Mortality and performance impairment in 2005 smolts. 57.

• Kent, M., Higgins, M., Whitaker, D. & Yokoyama, H. (1995) Proliferative kidney disease and in wild-caught salmonids from the Puntledge River system, Vancouver Island, British Columbia. 13-17.

• Macconnell, E. & Peterson, J.E. (1992) Proliferative kidney disease in feral cutthroat trout from a remote Montana reservoir: a first case. 182-187.

• Okamura, B., Hartikainen, H., SCHMIDT‐POSTHAUS, H. & Wahli, T. (2011) Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshwater Biology, 56, 735-753.

• Pagad, S., Genovesi, P., Carnevali, L., Scalera, R. & Clout, M. (2015) IUCN SSC Invasive Species Specialist Group: invasive alien species information management supporting practitioners, policy makers and decision takers.

• Smith, C., Morrison, J., Ramsey, H. & Ferguson, H. (1984) Proliferative kidney disease: first reported outbreak in North America. 207-216.

• Sterud, E., Forseth, T., Ugedal, O., Poppe, T.T., Jørgensen, A., Bruheim, T., Fjeldstad, H.-P. & Mo, T.A. (2007) Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by (Myxozoa). 191-198.

• Wood, T.S. (2009) Bryozoans. , pp. 437-454. Elsevier.

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