Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-17T16:52:11.517Z Has data issue: false hasContentIssue false

Estimation of transmission dynamics of the Ceratomyxa shasta actinospore to the salmonid host

Published online by Cambridge University Press:  18 March 2013

R. A. RAY
Affiliation:
Department of Fisheries and Wildlife, Oregon State University, 220 Nash Hall, Corvallis 97331, USA
J. L. BARTHOLOMEW*
Affiliation:
Department of Microbiology, Oregon State University, 220 Nash Hall, Corvallis 97331, USA
*
*Corresponding author: Oregon State University, 220 Nash Hall, Corvallis, OR, 97331, USA. Tel: +541 737 1856. Fax: +541 737 0496. E-mail: [email protected]

Summary

Transmission dynamics of the actinospore stage of Ceratomyxa shasta to the salmonid host were investigated under field and laboratory conditions. The number of parasites transmitted and the transmission rate were compared between 2 different exposure durations and also among different water velocities, by means of field exposures. Under laboratory conditions, the number of parasites transmitted and the transmission rates were compared across a broader range of water velocities and also at different water temperatures. Transmission rate was not constant over time as the number of parasites transmitted increased non-linearly between the 2 exposure durations. Transmission was also inversely related to water velocity and there was a threshold to transmission between 0·2–0·3 m s−1. Lastly, transmission rate increased with water temperature up to 18 °C then decreased at 23 °C. These experiments provide a range of values of transmission that will be incorporated into an epidemiological model to simulate the effectiveness of different management strategies. Additionally, these experiments provided novel information on the effects of environmental conditions (i.e. water velocity and water temperature) on the transmission dynamics between the salmonid host and the actinospore stage.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In International Symposium on Information Theory, 2nd, Tsahkadsor, Armenian SSR, pp. 267281.Google Scholar
Anderson, R. M., Jackson, H. C., May, R. M. and Smith, A. M. (1981). Population dynamics of fox rabies in Europe. Nature 289, 765771.CrossRefGoogle ScholarPubMed
Anderson, R. M., Mercer, J. G., Wilson, R. A. and Carter, N. P. (1982). Transmission of Schistosoma mansoni from man to snail: experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age. Parasitology 85, 339360.CrossRefGoogle Scholar
Barker, D. E. and Cone, D. K. (2000). Occurrence of Ergasilus celestis (Copepoda) and Pseudodactylogryrus anguillae (Monogenea) among wild eels (Anguilla rostrata) in relation to stream flow, pH and temperature and recommendations for controlling their transmission among captive eels. Aquaculture 187, 261274.CrossRefGoogle Scholar
Bartholomew, J. L. (1998). Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. Journal of Aquatic Animal Health 10, 112120.2.0.CO;2>CrossRefGoogle Scholar
Bartholomew, J. L., Whipple, M. J., Stevens, D. G. and Fryer, J. L. (1997). The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology 83, 859868.CrossRefGoogle ScholarPubMed
Begon, M., Hazel, S. M., Baxby, D., Bown, K., Cavanagh, R., Chantrey, J., Jones, T. and Bennett, M. (1999). Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society of London, B 266, 19391945.CrossRefGoogle ScholarPubMed
Bjork, S. J. and Bartholomew, J. L. (2010). Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. International Journal for Parasitology 40, 10871095.CrossRefGoogle Scholar
Bodensteiner, L. R., Sheehan, R. J., Wills, P. S., Brandenburg, A. M. and Lewis, W. M. (2000). Flowing water: an effective treatment for ichthyophthiriasis. Journal of Aquatic Animal Health 12, 209219.2.0.CO;2>CrossRefGoogle Scholar
Bouma, A., De Jong, M. C. M. and Kimman, T. G. (1995). Transmission of pseudorabies virus within pig populations is independent of the size of the population. Preventive Veterinary Medicine 23, 163172.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York, USA.Google Scholar
Dwyer, G. (1991). The roles of density, stage, and patchiness in the transmission of an insect virus. Ecology 72, 559574.CrossRefGoogle Scholar
Earn, D. J. D., Rohani, P., Bolker, B. M. and Grenfell, B. T. (2000). A simple model for complex dynamical transitions in epidemics. Science 287, 667670.CrossRefGoogle ScholarPubMed
El-Matbouli, M., Hoffmann, R. W. and Mandok, C. (1995). Light and electron microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. Journal of Fish Biology 46, 919935.Google Scholar
El-Matbouli, M., McDowell, T. S., Antonio, D. B., Andree, K. B. and Hedrick, R. P. (1999). Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. International Journal for Parasitology 29, 627641.CrossRefGoogle ScholarPubMed
Evans, N. A. (1985). The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269275.CrossRefGoogle Scholar
Fujiwara, M., Mohr, M. S., Greenberg, A., Foott, J. S. and Bartholomew, J. L. (2011). Effects of ceratomyxosis on population dynamics of Klamath fall-run Chinook salmon. Transactions of the American Fisheries Society 140, 13801391.CrossRefGoogle Scholar
Getz, W. M. and Pickering, J. (1983). Epidemic models: thresholds and population regulation. American Naturalist 121, 892898.CrossRefGoogle Scholar
Hallett, S. L. and Bartholomew, J. L. (2006). Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Diseases of Aquatic Organisms 71, 109.CrossRefGoogle ScholarPubMed
Hallett, S. L. and Bartholomew, J. L. (2008). Effects of water flow on the infection dynamics of Myxobolus cerebralis. Parasitology 135, 371384.CrossRefGoogle ScholarPubMed
Hallett, S. L., Ray, R. A., Hurst, C. N., Holt, R. A., Buckles, G. R., Atkinson, S. D. and Bartholomew, J. L. (2012). Density of the waterborne parasite, Ceratomyxa shasta, and its biological effects on salmon. Applied and Environmental Microbiology 78, 37243731.CrossRefGoogle ScholarPubMed
Karvonen, A., Paukku, S., Valtonen, E. T. and Hudson, P. J. (2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224.CrossRefGoogle ScholarPubMed
Lloyd-Smith, J. O., Getz, W. M. and Westerhoff, H. V. (2004). Frequency-dependent incidence in models of sexually transmitted diseases: portrayal of pair-based transmission and effects of illness on contact behaviour. Proceedings of the Royal Society of London, B 271, 625634.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352.CrossRefGoogle Scholar
Markiw, M. E. (1989). Salmonid whirling disease: myxosporean and actinosporean stages cross-react in direct fluorescent antibody test. Journal of Fish Diseases 12, 137141.CrossRefGoogle Scholar
Markiw, M. E. (1992). Experimentally induced whirling disease II. Determination of longevity of the infective triactinomyxon stage of Myxobolus cerebralis by vital staining. Journal of Aquatic Animal Health 4, 4447.2.3.CO;2>CrossRefGoogle Scholar
McCallum, H., Barlow, N. and Hone, J. (2001). How should pathogen transmission be modelled? Trends in Ecology and Evolution 16, 295300.CrossRefGoogle ScholarPubMed
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.CrossRefGoogle ScholarPubMed
R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.orgGoogle Scholar
Radke, M. G., Ritchie, L. S. and Rowan, W. B. (1961). Effects of water velocities on worm burdens of animals exposed to Schistosoma mansoni cercariae released under laboratory and field conditions. Experimental Parasitology 11, 323331.CrossRefGoogle ScholarPubMed
Ray, R. A., Rossignol, P. A. and Bartholomew, J. L. (2010). Mortality threshold for juvenile Chinook salmon Oncorhynchus tshawytscha in an epidemiological model of Ceratomyxa shasta. Diseases of Aquatic Organisms 93, 6370.CrossRefGoogle Scholar
Ray, R. A., Holt, R. A. and Bartholomew, J. L. (2012). Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. Journal of Parasitology 98, 520526.CrossRefGoogle ScholarPubMed
Richter, A. and Kolmes, S. A. (2005). Maximum temperature limits for Chinook, coho, and chum salmon, and steelhead trout in the Pacific Northwest. Reviews in Fisheries Science 13, 2349.CrossRefGoogle Scholar
Rowan, W. B. and Gram, A. L. (1959). Relation of water velocity to Schistosoma mansoni infection in mice. American Journal of Tropical Medicine and Hygiene 8, 630634.CrossRefGoogle ScholarPubMed
Smith, D. L., McKenzie, F. E., Snow, R. W. and Hay, S. I. (2007). Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biology 5, e42. doi:10.1371/journal.pbio.0050042CrossRefGoogle ScholarPubMed
Stocking, R. W., Holt, R. A., Foott, J. S. and Bartholomew, J. L. (2006). Spatial and temporal occurrence of the salmonid parasite Ceratomyxa shasta in the Oregon–California Klamath River Basin. Journal of Aquatic Animal Health 18, 194202.CrossRefGoogle Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407426.CrossRefGoogle ScholarPubMed
Thrall, P. H., Biere, A. and Uyenoyama, M. K. (1995). Frequency-dependent disease transmission and the dynamics of the Silene-Ustilago host–pathogen system. American Naturalist 145, 4362.CrossRefGoogle Scholar