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Fish population size, and not density, as the determining factor of parasite infection: a case study

Published online by Cambridge University Press:  03 March 2004

A. M. BAGGE ,
R. POULIN  and
E. T. VALTONEN
A. M. BAGGE
Affiliation:
Department of Bio- and Environmental Science, University of Jyväskylä, P.O. Box 35, 40351 Jyväskylä, Finland
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
E. T. VALTONEN
Affiliation:
Department of Bio- and Environmental Science, University of Jyväskylä, P.O. Box 35, 40351 Jyväskylä, Finland
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Abstract

The diversity and abundance of parasites vary widely among populations of the same host species. These infection parameters are, to some extent, determined by characteristics of the host population or of its habitat. Recent studies have supported predictions derived from epidemiological models regarding the influence of host population density: parasite abundance and parasite species richness are expected to increase with increasing host population density, at least for directly transmitted parasites. Here, we test this prediction using a natural system in which populations of the crucian carp, Carassius carassius (L.), occur alone, with no other fish species, in a series of 9 isolated ponds in Finland. The ectoparasite communities in these fish populations consist of only 4 species of monogeneans (Dactylogyrus formosus, D. wegeneri, D. intermedius and Gyrodactylus carassii); the total and relative abundance of these 4 species varies among ponds, with one or two of the species missing from certain ponds. Across ponds, only one factor, total fish population size, explained a significant portion of the variance in both the mean number of monogenean species per fish and the mean total abundance of monogenean individual per fish. In contrast, fish population density did not influence either monogenean abundance or species richness, and neither did any of the other variables investigated (mean fish length per pond, number of fish examined per pond, distance to the nearest lake, and several water quality measures). In our system, proximity among fish individuals (i.e. host population density) may not be relevant to the proliferation of monogeneans; instead, the overall availability of host individuals in the host population appeared to be the main constraint limiting parasite population growth.

Keywords

Monogeneapopulation sizepopulation densityepidemiologycrucian carpCarassius carassius
Type
Research Article
Information
Parasitology , Volume 128 , Issue 3 , March 2004 , pp. 305 - 313
Copyright
2004 Cambridge University Press

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References

REFERENCES

ANDERSON, J. A., BLAZEK, K. J., PERCIVAL, T. J. & JANOVY, J. jr. (1993). The niche of the gill parasite Dactylogyrus banghami (Monogenea: Dactylogyridae) on Notropis stramineus (Pisces: Cyprinidae). Journal of Parasitology 79, 435–437.CrossRefGoogle Scholar
ARNEBERG, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352–358.CrossRefGoogle Scholar
ARNEBERG, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.CrossRefGoogle Scholar
ARNEBERG, P., SKORPING, A., GRENFELL, B. T. & READ, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B 265, 1283–1289.CrossRefGoogle Scholar
BAGGE, A. M. & VALTONEN, E. T. (1996). Experimental study on the influence of paper and pulp mill effluent on the gillparasite communities of roach (Rutilus rutilus). Parasitology 112, 499–508.CrossRefGoogle Scholar
BAGGE, A. M. & VALTONEN, E. T. (1999). Development of monogenean communities on the gills of roach fry (Rutilus rutilus). Parasitology 118, 479–487.CrossRefGoogle Scholar
BJORNSTAD, O. N., FINKENSTADT, B. F. & GRENFELL, B. T. (2002). Dynamics of measles epidemics: estimating scaling of transmission rates using a time series SIR model. Ecological Monographs 72, 169–184.CrossRefGoogle Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
BYKHOVSKAYA-PAVLOVSKAYA, I. E., GUSEV, A. V., DUBININA, M. N., IZYUMOVA, N. A., SMIRNOVA, T. S., SOKOLOVSKAYA, I. L., SHTEIN, G. A., SHULMAN, S. S. & EPSHTEIN, V. M. (1962). Key to Parasites of Freshwater Fish of the USSR (ed. Pavlovskii, E. N.) Akademy of Sciences of the USSR, Moskva. (In Russian.)
CARO, A., COMBES, C. & EUZET, L. (1997). What makes a fish a suitable host for Monogenea in the Mediterranean? Journal of Helminthology 71, 203–210.Google Scholar
DOGIEL, V. A. (1961). Ecology of the parasites of freshwater fish. In Parasitology of Fishes (ed. Dogiel, V. A., Petrushevski, G. K. & Polyanski, YU. I.), pp. 1–47. Oliver & Boyd, Edinburgh.
DZIDZIUL, A. (1973). The pathogenicity of Lernaea cyprinaceae (L.) in the cases of heavy infestation in Carassius carassius (L.). Acta Parasitologica Polonica XXI, 281–288.Google Scholar
EARN, D. J. D., ROHANI, P., BOLKER, B. M. & GRENFELL, B. T. (2000). A simple model for complex dynamical transitions in epidemics. Science 287, 667–670.CrossRefGoogle Scholar
GEETS, A., COENE, H. & OLLEVIER, F. (1997). Ectoparasites of the whitespotted rabbitfish, Siganus sutor (Valenciennes, 1835) of the Kenyan Coast: Distribution within the host population and site selection on the gills. Parasitology 115, 69–79.CrossRefGoogle Scholar
GUSEV, A. V. (1985). Keys to Parasites of Freshwater Fish of the USSR Vol. 2. Parasitic Metazoa, Leningrad, Nauka. (In Russian.)
GUTIÉRREZ, P. A. (2001). Monogenean community structure on the gills of Pimelodus albicans from Ri'o de la Plata (Argentina): a comparative approach. Parasitology 122, 465–470.Google Scholar
GUTIÉRREZ, P. A. & MARTORELLI, S. R. (1999). The structure of the monogenean community on the gills of Pimelodus maculatus in Ri'o de la Plata (Argentina). Parasitology 119, 177–182.CrossRefGoogle Scholar
HARTVIGSEN, R. & HALVORSEN, O. (1994). Spatial patterns in the abundance and distribution of parasites of freshwater fish. Parasitology Today 10, 28–31.CrossRefGoogle Scholar
HAYWARD, G. J., LAKSHMI PERERA, K. M. & ROHDE, K. (1998). Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia. International Journal for Parasitology 28, 263–273.CrossRefGoogle Scholar
HOLOPAINEN, I. J., HYVÄRINEN, H. & PIIRONEN, A. K. (1986). Anaerobic wintering of Crucian carp (Carassius carassius (L.)). II. Metabolic products. Comparative Biochemistry and Physiology 83A, 239–242.Google Scholar
HOLOPAINEN, I. J. & PITKÄNEN, A. K. (1985). Population size and structure of Crucian carp (Carassius carassius (L.)) in two small natural ponds in Eastern Finland. Annales Zoologi Fennici 22, 397–406.Google Scholar
HOLOPAINEN, I. J., TONN, W. M. & PASZKOWSKI, C. A. (1992). Effects of fish density on planctonic communities and water quality in a manipulated forest pond. Hydrobiologia 243/244, 311–321.CrossRefGoogle Scholar
HOLOPAINEN, I. J., TONN, W. M. & PASZKOWSKI, C. A. (1997). Tales of two fish: the dichotomous biology of crucian carp (Carassius carassius (L.)) in northern Europe. Annales Zoologi Fennici 34, 1–22.Google Scholar
HUDSON, P. J., RIZZOLLI, A., GRENFELL, B. T., HEESTERBEEK, H. & DOBSON, A. P. (2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford.
KARVONEN, A., PAUKKU, S., VALTONEN, E. T. & HUDSON, P. J. (2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217–224.CrossRefGoogle Scholar
KAZUBSKI, S. L. (1982). Morphological variability of Trichodina reticulata Hirschmann et Partsch, 1955 (Ciliata, Peritrichida), a parasite of Carassius carassius (L.) from small pond in Kortowo (Olsztyn). Acta Protozoologica 21, 1–6.Google Scholar
KENNEDY, C. R. (1978). An analysis of the metazoan parasitocoenoses of brown trout Salmo trutta from British lakes. Journal of Fish Biology 13, 255–263.CrossRefGoogle Scholar
KENNEDY, C. R. (1990). Helminth communities in freshwater fish: structured assemblages or stochastic assemblages? In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. & Aho, J. M.), pp. 131–156. London.
KOSKIVAARA, M., VALTONEN, E. T. & PROST, M. (1991). Dactylogyrids on the gills of roach in Central Finland: features of infection and species composition. International Journal for Parasitology 21, 47–55.CrossRefGoogle Scholar
KOSKIVAARA, M., VALTONEN, E. T. & VUORI, K.-M. (1992). Microhabitat distribution and coexistence of Dactylogyrus species (Monogenea) on the gills of roach. Parasitology 104, 273–281.CrossRefGoogle Scholar
MARCOGLIESE, D. J. & CONE, D. K. (1991). Importance of lake characteristics in structuring parasite communities of salmonids from insular Newfoundland. Canadian Journal of Zoology 69, 2962–2967.CrossRefGoogle Scholar
McCALLUM, H., BARLOW, N. & HONE, J. (2001). How should pathogen transmission be modelled? Trends in Ecology and Evolution 16, 295–300.Google Scholar
MORAND, S. & POULIN, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717–727.CrossRefGoogle Scholar
PASZKOWSKI, C. A., TONN, W. M., PIIRONEN, J. & HOLOPAINEN, I. J. (1990). Behavioral and population-level aspects of intraspesific competition in crucian carp. Annales Zoologi Fennici 27, 77–85.Google Scholar
RAATIKAINEN, M. (1987). Niitä on 187888. Suomen Kuvalehti 24B, 20–23. (In Finnish.)Google Scholar
RAIBAUT, A., COMBES, C. & BENOIT, F. (1998). Analysis of the parasitic copepod species richness among Mediterranean fish. Journal of Marine Systems 15, 185–206.CrossRefGoogle Scholar
ROHDE, K., HAYWARD, C., HEAP, M. & GOSPER, D. (1994). A tropical assemblage of ectoparasites: gill and head parasites of Lethrinus miniatus (Teleostei, Lethrinidae). International Journal for Parasitology 24, 1031–1053.CrossRefGoogle Scholar
SASAL, P. & MORAND, S. (1998). Comparative analysis: a tool for studying monogenean ecology and evolution. International Journal for Parasitology 28, 1637–1644.CrossRefGoogle Scholar
SOKAL, R. R. & ROHLF, F. J. (1995). Biometry, 2nd Edn. W. H. Freeman & Co., New York.
TONN, W. M., MAGNUSON, J. J., RASK, M. & TOIVONEN, J. (1990). Intercontinental comparison of small-lake fish assemblages: the balance between local and regional processes. American Naturalist 136, 345–375.CrossRefGoogle Scholar
VALTONEN, E. T., PULKKINEN, K. & JULKUNEN, M. (2003). Getting to the core of the parasite communities: revealing the exchange patterns among sympatric host species. In Taxonomy, Ecology and Evolution of Metazoan Parasites (ed. Combes, C.) (in the Press).