Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-25T12:34:28.525Z Has data issue: false hasContentIssue false

Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata)

Published online by Cambridge University Press:  03 October 2005

C. GHEORGIU
Affiliation:
Institute of Parasitology, Macdonald Campus of McGill University, 21 111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, Canada H9X 3V9
D. J. MARCOGLIESE
Affiliation:
St Lawrence Centre, Environment Canada, 105 McGill, 7th Floor, Montreal, Quebec, Canada H2Y 2E7
M. SCOTT
Affiliation:
Institute of Parasitology, Macdonald Campus of McGill University, 21 111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, Canada H9X 3V9

Abstract

The effect of waterborne zinc (Zn) on Gyrodactylus population dynamics was studied on isolated guppies maintained at concentrations ranging from 0 to 240 μg Zn/l. After 1 week pre-exposure to Zn, each fish was experimentally infected with 3 gyrodactylids and parasite numbers were recorded daily on each fish until the fish either died or recovered from infection. Parasite establishment was most successful at 0 and 240 μg Zn/l (97%) compared with the intermediate Zn concentrations. Low to moderate concentrations of Zn were beneficial to the parasite, as evidenced by the concentration-dependent increase in peak parasite burden on recovered fish up to 120 μg Zn/l. In contrast, 240 μg Zn/l may have been toxic to the parasite, as both peak parasite burden (in fish that recovered from infection), and maximum rate of increase of the parasite population (in fish that died) declined at this concentration. The combined effect of infection and Zn is harmful to the fish, because mortality of infected fish (but not uninfected fish) increased with increasing Zn concentrations. We suggest that the observed mortality occurs because of the inability of fish to continuously produce mucous that is a key factor for protecting fish from both waterborne Zn and ectoparasites.

Type
Research Article
Copyright
2005 Cambridge University Press

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

Asch, H. L. and Dresden, M. H. ( 1977). Schistosoma mansoni: effects of zinc on cercarial and schistosomule viability. Journal of Parasitology 63, 8086.CrossRefGoogle Scholar
Bakke, T. A., Harris, P. D., Hansen, L. P. and Jansen, P. A. ( 1992). Host specificity and dispersal strategy in gyrodactylid monogeneans with particular reference to Gyrodactylus salaris (Plathyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 4557.Google Scholar
Buchmann, K. ( 1998). Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195200.CrossRefGoogle Scholar
Buchmann, K. ( 1999). Immune mechanisms in fish skin against monogeneans – a model. Folia Parasitologica 46, 19.Google Scholar
Buchmann, K. and Bresciani, J. ( 1998). Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitology Research 84, 1724.Google Scholar
Buchmann, K. and Bresciani, J. ( 1999). Rainbow trout leukocyte activity: influence on the ectoparasitic monogenean Gyrodactylus derjavini. Diseases of Aquatic Organisms 35, 1322.CrossRefGoogle Scholar
Cable, J., Harris, P. D. and Tinsley, R. C. ( 1996). Ultrastructural adaptations for viviparity in the female reproductive system of gyrodactylid monogeneans. Tissue and Cell 28, 515526.CrossRefGoogle Scholar
Cable, J., Scott, E. C. G., Tinsley, R. C. and Harris, P. D. ( 2002 a). Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. Journal of Parasitology 88, 183184.Google Scholar
Cable, J., Tinsley, R. C. and Harris, P. D. ( 2002 b). Survival, feeding and embryo development of Gyrodactylus gasterostei (Monogenea: Gyrodactylidae). Parasitology 124, 5368.Google Scholar
CANADIAN COUNCIL OF MINISTERS OF THE ENVIRONMENT ( 2001). Canadian Water Quality Guidelines (CWQG) for the Protection of Aquatic Life. http://www.ccme.ca/assets/pdf/e1_062.pdf
CANADIAN COUNCIL ON ANIMAL CARE ( 1993). Guide to the Care and Use of Experimental Animals, Vol. 1, 2nd Edn. ( ed. Olfert, E. D., Cross, B. M. and McWilliam, A. A.).
Cone, D. K. ( 1999). Monogenea. In Fish Diseases and Disorders. Vol. I. Protozoan and Metazoan Infections ( ed. Woo, P. T. K.), pp. 289327. CABI Publishing, Wallingford, UK.
Evans, N. A. ( 1982 a). Effect of copper and zinc upon the survival and infectivity of Echinoparyphium recurvatum cercariae. Parasitology 85, 295303.Google Scholar
Evans, N. A. ( 1982 b). Effect of copper and zinc on the life cycle of Notocotyllus attenuatus (Digenea: Notocotylidae). International Journal for Parasitology 12, 363369.Google Scholar
Florence, T. M., Morrison, G. M. and Stauber, J. L. ( 1992). Determination of trace element speciation and the role of speciation in aquatic toxicity. The Science of the Total Environment 125, 113.CrossRefGoogle Scholar
Gagnon, C. and Saulnier, I. ( 2003). Distribution and fate of metals in the dispersion plume of a major municipal effluent. Environmental Pollution 124, 4755.CrossRefGoogle Scholar
Glover, C. N. and Hogstrand, C. ( 2002). In vivo characterization of intestinal zinc uptake in freshwater rainbow trout. Journal of Experimental Biology 205, 141150.Google Scholar
Handy, R. D. ( 1996). Dietary exposure to toxic metals in fish. In Toxicology of Aquatic Pollution. Physiological, Cellular and Molecular Approaches ( ed. Taylor, E. W.), pp. 2960. Cambridge University Press, Cambridge.CrossRef
Handy, R. D., Eddy, F. B. and Romain, G. ( 1989). In vitro evidence for the ionoregulatory role of rainbow trout mucous in acid, acid/aluminium and zinc toxicity. Journal of Fish Biology 35, 737747.CrossRefGoogle Scholar
Harris, P. D., Soleng, A. and Bakke, T. A. ( 1998). Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology 117, 137143.CrossRefGoogle Scholar
Hogstrand, C. and Wood, C. M. ( 1996). The physiology and toxicology of zinc in fish. In Toxicology of Aquatic Pollution. Physiological, Cellular and Molecular Approaches ( ed. Taylor, E. W.), pp. 6184. Cambridge University Press, Cambridge.CrossRef
Iger, Y., Jenner, H. and Wendelaar Bonga, S. E. ( 1994). Cellular responses in the skin of rainbow trout (Oncorhynchus mykiss) exposed to Rhine water. Journal of Fish Biology 45, 11191132.CrossRefGoogle Scholar
Johnsen, B. O. and Jensen, A. J. ( 1991). The Gyrodactylus story in Norway. Aquaculture 98, 289302.CrossRefGoogle Scholar
Kearn, G. C. ( 1998). Parasitism and the Platyhelminths. Chapman and Hall, London.
Khan, R. A. and Thulin, J. ( 1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.CrossRefGoogle Scholar
Khunyakari, R. P., Tare, V. and Sharma, R. N. ( 2001). Effects of some trace heavy metals on Poecilia reticulata (Peters). Journal of Environmental Biology 22, 141144.Google Scholar
Lindenstrom, T. and Buchmann, K. ( 2000). Acquired resistance in rainbow trout against Gyrodactylus derjavini. Journal of Helminthology 74, 155160.Google Scholar
McGeer, J. C., Szebedinszky, C., McDonald, D. G. and Wood, C. M. ( 2000). Effects of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout. 1. Iono-regulatory disturbance and metabolic costs. Aquatic Toxicology 50, 231234.Google Scholar
Möller, H. ( 1987). Pollution and parasitism in the aquatic environment. International Journal for Parasitology 17, 353361.CrossRefGoogle Scholar
Morley, N. J., Crane, M. and Lewis, J. W. ( 2001 a). Toxicity of cadmium and zinc to miracidia of Schistosoma mansoni. Parasitology 122, 8185.Google Scholar
Morley, N. J., Crane, M. and Lewis, J. W. ( 2001 b). Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. International Journal for Parasitology 31, 12111217.Google Scholar
Morley, N. J., Crane, M. and Lewis, J. W. ( 2002). Toxicity of cadmium and zinc mixtures to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. Archives of Environmental Contamination and Toxicology 43, 2833.CrossRefGoogle Scholar
Nursita, A. I., Singh, B. and Lees, E. ( 2005). The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola). Ecotoxicology and Environmental Safety 60, 306314.CrossRefGoogle Scholar
Overstreet, R. M. ( 1993). Parasitic diseases of fishes and their relationship with toxicants and other environmental factors. In Pathobiology of Marine and Estuarine Organisms ( ed. Couch, J. A. and Fournie, W.), pp. 111156. CRC Press, Boca Raton, Florida.
Overstreet, R. M. ( 1997). Parasitological data as monitors of environmental health. Parassitologia 39, 169175.Google Scholar
Poléo, A. B. S., Schjolden, J., Hansen, H., Bakke, T. A., Mo, T. A., Rosseland, B. O. and Lydersen, E. ( 2003). The effect of various metals on Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon (Salmo salar). Parasitology 128, 169177.Google Scholar
Poulin, R. ( 1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 5861.CrossRefGoogle Scholar
Richards, G. R. and Chubb, J. C. ( 1996). Host response to initial and challenge infections, following treatment of Gyrodactylus bullatarudis and Gyrodactylus turnbulli (Monogenea) on the guppy (Poecilia reticualta). Parasitology Research 82, 242247.CrossRefGoogle Scholar
Richards, G. R. and Chubb, J. C. ( 1998). Long-term population dynamics of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on adult guppies (Poecilia reticulata) in 50-l experimental arenas. Parasitology Research 84, 753756.Google Scholar
Rohlf, F. J. and Sokal, R. R. ( 1981). Statistical Tables, 2nd Edn. W.H. Freeman and Company, NY.
Rozan, T. F., Lassman, M. E., Ridge, D. P. and Luther, G. W. ( 2000). Evidence for iron, copper and zinc complexation as multinuclear sulphide clusters in oxidic rivers. Nature, London 406, 879882.CrossRefGoogle Scholar
Scott, M. E. ( 1982). Reproductive potential of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 85, 217236.CrossRefGoogle Scholar
Scott, M. E. ( 1985). Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). Journal of Fish Diseases 8, 495503.CrossRefGoogle Scholar
Scott, M. E. and Nokes, D. J. ( 1984). Temperature-dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89, 221227.CrossRefGoogle Scholar
Scott, M. E. and Robinson, M. A. ( 1984). Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies, Poecilia reticulata (Peters), following treatment. Journal of Fish Biology 24, 581586.CrossRefGoogle Scholar
Shephard, K. L. ( 1994). Functions for fish mucous. Reviews in Fish Biology and Fisheries 4, 401429.CrossRefGoogle Scholar
Singh, S. and Srinivastav, A. K. ( 1993). Effects of calcitonin administration on serum calcium and inorganic phosphate levels of the fish, Heteropneustes fossilis, maintained either in artificial freshwater, calcium-rich freshwater, or calcium-deficient freshwater. The Journal of Experimental Zoology 265, 3539.CrossRefGoogle Scholar
Soleng, A., Poléo, A. B. S., Alstand, N. E. W. and Bakke, T. A. ( 1999). Aqueous aluminium eliminates Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon. Parasitology 119, 1925.CrossRefGoogle Scholar
Spurgeon, D. J. and Hopkin, S. P. ( 1996). Effects of metal-contaminated soils on the growth, sexual development, and early cocoon production of the earthworm Eisenia fetida, with particular reference to zinc. Ecotoxicology and Environmental Safety 35, 8695.CrossRefGoogle Scholar
Wells, P. R. and Cone, D. K. ( 1990). Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on density of mucous cells in the epidermis of fry of Oncorhynchus mykiss. Journal of Fish Biology 37, 599603.Google Scholar
Widianarko, B., Kuntoro, F. X. S., van Gestel, C. A. M., Verweij, R. A. and van Straalen, N. M. ( 2001). Toxicokinetics and toxicity of zinc under time-varying exposure in the guppy (Poecilia reticulata). Environmental Toxicology and Chemistry 20, 763768.CrossRefGoogle Scholar
Widianarko, B., van Gestel, C. A. M., Verweij, R. A. and van Straalen, N. M. ( 2000). Associations between trace metals in sediment, water, and guppy, Poecilia reticulata (Peters), from urban streams of Semarag, Indonesia. Ecotoxicology and Environmental Safety 46B, 101107.CrossRefGoogle Scholar