In the Shadow of Horse

In the Shadow of Horse
In the Shadow of Horse

Thursday, September 1, 2016

Yellowstone River Whitefish PKD Tetracapsuloides bryosalmonae Epidemic

Montana Standard Article: Spread of pathogen in Montana Rivers requires a thoughtful and scientific response.

Preservation Medicine

Sid Gustafson DVM

Aquatic infectious disease is caused by a pathogen present in a river environment that achieves successful reproduction in a vulnerable host, often at the host’s expense.

An appreciation of the Yellowstone River whitefish epidemic requires consideration of three factors; 1) the host(s), 2) the warming river environment, and 3) the pathogen(s).
Epidemics—including the Yellowstone River whitefish Tetra epidemic—are preceded by essential predisposing conditions in all three.
The Yellowstone River and watershed activities compose the environment. Warming temperatures, low flows, silting, proliferation of the pathogen Tetracapsuloides bryosalmonae, diminished oxygenation, salinity, septic seepage, chemical runoff, altered riverbanks, recurrent contamination with pathogens and invasive species, river sporting, boating, and flyfishing, water diversion and irrigation, riparian residential, business, and agricultural practices are the primary environmental factors that facilitated this epidemic.
While all of the aforementioned factors play a role, the warming of the river was the critical factor in this epidemic. Had the river not warmed to the critical temperature, thought to be around 15 degrees centigrade, the epidemic would not have happened despite the presence of the pathogen and the vulnerable whitefish.
Tetracapsuloides bryosalmonae is a native North American pathogen that has resided in American rivers for centuries. The pathogen has spread to European rivers, as well as to the Yellowstone River. In the Yellowstone, this infectious agent has adapted to infect whitefish, finding them more vulnerable than trout. The native Yellowstone mountain whitefish, the salmonid Prosopium williamsoni is our host of concern. The fish is called the mountain whitefish because in cold mountain rivers this fish thrives.
The infective aquatic pathogen T. bryosalmonae is unusual among the myxosporea (of which the whirling disease pathogen is a relative) in that it requires a bryozoan as an intermediate host. The bryozoan in this case may be Plumatella fungosa. In this freshwater jellyfish, the Tetracapsula completes its life cycle. This jellyfish releases fish-infective spores into the river. When waters warm high enough to manifest disease, around 60 degrees F, these floating spores attach to the whitefish’s gills before proceeding to cause proliferative kidney disease
Depending on the fish’s health, resistance, environmental conditions, adaptability, infective dose, and immune status, the fish survives to perhaps be resistant to future infections, or she dies. As the fish dies, the pathogen enters the water. At this stage of this complex life-cycle, rather than finding another fish, the Tetra pathogen finds a fungosa to complete its lifecycle. In this process, the infectious organism begins to flourish in the river and gains momentum to create an epidemic.
Multiple measurable factors preceded the whitefish epidemic, an epidemic a long-time coming, an epidemic that veterinary medical technology had the ability to predict had aquatic veterinary medicine been employed to keep Montana rivers and their fish populations prosperous and healthy.
The hosts of this disease have historically been salmonids, whitefish among them. As any Yellowstone guide knows, a whitefish is no salmon. While considered undesirable by some, the whitefish is an indicator species reflective of river health. Like trout, whitefish and grayling are salmonids. Whitefish require pristine rivers. Grayling, the previous indicator species, were extirpated by sullied river systems. Historically, whitefish often come next.
To monitor and predict future epidemics, competent aquatic veterinarians sample, test, analyze and interpret the host health, river health, intermediate host presence, along with the pathogen load in the river system. With this information, aquatic veterinarians can manage the health of the watershed, river, and fish to minimize the impact of infectious disease. All of this ahead of time. The aquatic veterinary goal is to prevent epidemics, or at least predict them, something beyond biologists’ ability at this time. Veterinarians have a long and effective history of successfully managing the health of animal populations threatened by infectious disease, be they wild or domestic. Veterinarians have the appropriate knowledge and experience to sustain fish and river health. The time has come to look to veterinarians to manage river health in Montana as rivers are managed in progressive fisheries throughout the world where the economy depends on fish health and prosperity. There is a lot to learn about this epidemic, and veterinarians are the best learners regarding management and prevention of infectious disease.

The resolution of the Tetra epidemic could be similar to the resolution of the whirling disease epidemic. The whitefish and trout survivors will perpetuate offspring that are more resistant than their immunologically naïve predecessors. Disease resistance will develop. The fish will adapt to and/or find a balance with their pathogen and intermediate host. An equilibrium between pathogens and hosts emerges over time if the river system is kept healthy and cool. The trout may have previously acquired a resistance from their experience with the whirling disease organism, and now with this Tetra experience, the trout appear to be developing resistance to infective pathogens of various sorts.

An antimicrobial agent to kill the aquatic pathogen is not an available method of control or prevention, as the river environment would be further deteriorated by the drug’s side-effects and unintended victims.
The jellyfish host, Plumatella fungosa, could be medically manipulated, sterilized, or genetically altered to block the two-host disease transmission cycle, and that is a consideration.
The environment (the river et al) can be made healthier; water cooled, flow quickened, and oxygenation enhanced using progressive river management techniques (limiting water drawouts, averting septic and manure seepage, and halting chemically contaminated runoffs). The fish populations could be treated more kindly and carefully by educating guides and anglers on the principles of animal welfare (fish are sentient beings) and the principles of disease transmission. Fishing hooks, boats, gear, and fishermen transmit fish diseases near and far. This needs to be evaluated and addressed.
Fishing stress and disease vulnerability can be significantly reduced by regulating fishing and/or floating in consideration of the fish, rather than the fisherman, accountants, and irrigators. Catch-and-release practices and their relationship to perpetuating and spreading fish diseases require investigation. Harvesting can be considered a possible disease management measure. Stressed or injured fish should not be released back into the river.

Rest is the oldest remedy to manage disease. While naïve to the vagaries of infectious animal disease, the Montana FWP is to be commended for closing the river and giving her a long-needed rest. Periodic rest during critical times appears to be one solution of many. Whitefish populations can balance trout populations, and overpopulations, keeping fish numbers balanced and healthy. Pathogens often find imbalanced populations vulnerable. The microbe often has the last word (when the humans don’t pay attention). Aquatic veterinarians pay attention.

Recommended reading:

^ Hedrick R.; McConnell E.; de Kinkelin P (1993). "Proliferative kidney disease of salmonid fish". Annual Review of Fish Diseases. 3: 277–290. doi:10.1016/0959-8030(93)90039-E.
^ Kent, M.L. & R.P. Hedrick (1985). "PKX the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa". Journal of Protozoology. 32 (2): 254 260. doi:10.1111/j.1550-7408.1985.tb03047.x. PMID 4009511.
^ Korotneff, A. (1892). "Myxosporidium bryozoides". Z. Wiss. Zool. 53: 591–596.
^ Anderson, C.L., Canning, E.U. & Okamura, B. (1999). "18S rDNA sequences indicate that PKX organism parasitizes Bryozoa". Bulletin of the European Association of Fish Pathologists. 19: 94–97.
^ Canning, E.U., Curry, A., Feist, S.W., Longshaw, M., & Okamura, B. (1999). "Tetracapsula bryosalmonae n.sp. for PKX organism the cause of PKD in salmonid fish". Bulletin of the European Association of Fish Pathologists. 19 (2): 203–206.
^ Canning, E.U., Curry, A., Feist, S.W., Longshaw, M., & Okamura, B. (2000). "A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism)". Journal of Eukaryotic Microbiology. 47 (5): 456–468. doi:10.1111/j.1550-7408.2000.tb00075.x. PMID 11001143.
^ Kent, M.L. J. Khattra, R.P. Hedrick, and R.H. Devlin (2000). "Tetracapsula renicola (Myxozoa: Saccosporidae); the PKX myxozoan – the cause of proliferative kidney disease of salmonid fishes". Journal of Parasitology. 86 (1): 103–111. doi:10.1645/0022-3395(2000)086[0103:TRNSMS]2.0.CO;2. PMID 10701572.
^ Anderson, C.L., Canning, E.U. & Okamura, B. (1999). "18S rDNA sequences indicate that PKX organism parasitizes Bryozoa". Bulletin of the European Association of Fish Pathologists. 19: 94–97.
^ Henderson, M. & Okamura, B. (2004). "The phylogeography of salmonid proliferative kidney disease in Europe and North America". Proceedings of the Royal Society B. 271 (1549): 1729–1736. doi:10.1098/rspb.2004.2677. PMC 1691782. PMID 15306294.

Fumagillin (or other effective drug)
Microsporidians (Loma salmonae, proliferative kidney disease, whirling disease, proliferative gill disease)/freshwater-reared finfish

Ray, R.A., R.W. Perry, N.A. Som and J.L. Bartholomew.  2014.  Using cure models for analyzing the influence of pathogens on salmon survival.  Transactions of the American Fisheries Society.  143(2):

Bjork, S.J., Zhang, Y.A., Hurst, C.N., Alonso-Naveiro, M.E., Alexander, J.D., Sunyer, J.O., and Bartholomew, J.L.  2014.  Defenses of susceptible and resistant Chinook salmon (Onchorhynchus tshawytscha) against the myxozoan parasite Ceratomyxa shasta.  Fish Shellfish Immunol. 1:87-95.

Gómez, D., Bartholomew, J., and Sunyer, J.O.  2014.  Biology and mucosal immunity to myxozoans.  Dev. Comp. Immunol. 43(2): 243-56.

Ray, A.R. and J.L. Bartholomew.  2013.  Estimation of transmission dynamics of the Ceratomyxa shasta actinospore to the salmonid host.  Parasitology.  140:907-916.

Bartošová, P., I. Fiala, M. Jirku, M. Cinkova, M. Caffara, M.L. Fioravante, S.D. Atkinson, J.L. Bartholomew and A.S. Holzer.  2013.  Sphaerospora sensu stricto:  Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa).  Molec. Phylogentics and Evolution.  68:93-105.

Ray, A.R., R.A. Holt and J.L. Bartholomew.  2012.  Relationship between temperature and C. shasta-induced mortality in Klamath River salmonids.  Journal of Parasitology.  98:520-526.

Ordás, M.C., R. Castro, B. Dixon, J.O. Sunyer, S. Bjork, J. Bartholomew, T. Korytar, B. Kollner, A. Cuesta and C. Tafalla.  2012.  Identification of a novel CCR7 gene in rainbow trout with differential expression in the context of mucosal or systemic infection.  Developmental and Comparative Immunology.  38:302-311.

Stinson, M.E.T. and J.L. Bartholomew.  2012.  Predicted redistribution of Ceratomyxa shasta genotypes with salmonid passage in the Deschutes River, Oregon.  J. of Aquatic Animal Hlth.  24:274-280.

Hallett, S.L., R.A. Ray, C.N. Hurst, R.A. Holt, G.R. Buckles, S.D. Atkinson and J.L. Bartholomew.  2012.  Density of the waterborne parasite, Ceratomyxa shasta, and its biological effects on salmon.  Applied and Environmental Microbiology 78:3724-3731.

Zielinski, C.M., H.V. Lorz, S.L. Hallett, L. Xue and J.L. Bartholomew.  2011.  Comparative susceptibility of Deschutes River (Oregon, USA) Tubifex tubifex populations to Myxobolus cerebralis.  Journal of Aquatic Animal Health 23:1-8.

Zhang, Y-A., I. Salinas, J. Li, D. Parra, S. Bjork, S. LePatra, J. Bartholomew and J.O. Sunyer.  2010.  IgT, a primitive immunoglobulin class specialized in mucosal immunity.  Nature Immunology 11:827-835.

Bjork, S.J. and J.L. Bartholomew.  2010.  Invasion of Ceratomyxa shasta (Myzozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts.  International Journal for Parasitology, 40:1087-1095.
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