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Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure?

Published online by Cambridge University Press:  21 September 2004

M. BANDILLA
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014, University of Jyväskylä, Finland
T. HAKALAHTI
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014, University of Jyväskylä, Finland
P. J. HUDSON
Affiliation:
Department of Biology, Pennsylvania State University, University Park, PA 16902, USA
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014, University of Jyväskylä, Finland

Abstract

By sampling individual rainbow trout, Oncorhynchus mykiss, at a fish farm we showed that Argulus coregoni were aggregated within their host population. The relative significance of susceptibility and exposure generating the observed pattern was tested using experimental infections. We examined, whether rainbow trout developed protective resistance mechanisms against the louse following a challenge infection and if there was variation between individual trout in their susceptibility to A. coregoni metanauplii. Fish were exposed to 20 A. coregoni for 5, 25, 50, 85 or 120 min and the numbers attaching recorded. Three weeks later, developing argulids were removed and the experiment repeated with a standardized exposure of 20 metanauplii. Prior exposure of fish with A. coregoni did not reduce the total infection intensity compared to naïve fish, but fish gained infection more rapidly. We suggest that there is no protective acquired resistance of pre-exposed rainbow trout to subsequent Argulus exposure. The possibility that an immunosuppressive mechanism by argulids was acting enabling the higher attachment rate could be refuted since control individuals, not previously exposed to lice, gained the infection at a similar rate as the fish challenged twice. Our results do not indicate clear differences in susceptibility among individual fish but the transmission of metanauplii on fish seemed to be opportunistic and non-selective. Our results support the view that variation in exposure time, rather than differences in susceptibility of individual hosts, might be the key factor in generating the aggregated distribution of Argulus on their hosts.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

AALTONEN, T. M., JOKINEN, E. I. & VALTONEN, E. T. ( 1994). Antibody synthesis in roach (Rutilus rutilus); analysis of antibody secreting cells in lymphoid organs with ELISPOT-assay. Fish and Shellfish Immunology 4, 129140.CrossRefGoogle Scholar
AHNE, W. ( 1985). Argulus foliaceus L. and Piscicola geometra L. as mechanical vectors of spring viraemia of carp virus (SVCV). Journal of Fish Diseases 8, 241242.Google Scholar
ANDERSON, R. M., WHITFIELD, P. J. & DOBSON, A. P. ( 1978). Experimental studies of infection dynamics: infection of the definitive host by the cercariae of Transversotrema patialense. Parasitology 77, 189200.CrossRefGoogle Scholar
ANDERSON, R. M. & MAY, R. M. ( 1991). Infectious Disease of Humans: Dynamics and Control. Oxford University Press, Oxford.
BOWER-SHORE, C. ( 1940). An investigation of the common fish louse, Argulus foliaceus (Linn.). Parasitology 32, 361371.CrossRefGoogle Scholar
BOXSHALL, G. A. ( 1974). The population dynamics of Lepeoptheirus pectoralis (Müller): dispersion pattern. Parasitology 69, 373390.CrossRefGoogle Scholar
CROSS, D. G. & STOTT, B. ( 1974). The effect of Argulus foliaceus L. on the growth and mortality of a grass carp population. Journal of Institutional Fisheries Management 5, 3942.Google Scholar
DALGAARD, M. B., NIELSEN, C. V. & BUCHMANN, K. ( 2003). Comparative susceptibility of two races of Salmo salar (Baltic Lule river and Atlantic Conon river strains) to infection with Gyrodactylus salaris. Diseases of Aquatic Organisms 53, 173176.CrossRefGoogle Scholar
ELLIOT, J. M. ( 1977). Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Ambleside.
FRY, F. E. J. ( 1971). The effect of environmental factors on the physiology of fish. In Fish Physiology, 6 (ed. Hoar, W. S. & Randall, D. J.), pp. 198. Academic Press, London, New York.CrossRef
FRYER, G. ( 1965). Habitat selection and gregarious behaviour in parasitic crustaceans. Crustaceana 10, 199209.Google Scholar
GALAROWICZ, T. & COCHRAN, P. A. ( 1991). Responses by the parasitic Crustacean Argulus japonicus to host chemical cues. Journal of Freshwater Ecology 6, 455456.CrossRefGoogle Scholar
GRAYSON, T. H., JENKINS, P. G., WRATHMELL, A. B. & HARRIS, J. E. ( 1991). Serum responses to the salmon louse Lepeoptheirus salmonis (Krøyer, 1838), in naturally infected salmonids and immunised rainbow trout, Oncorhynchus mykiss (Walbaum), and rabbits. Fish and Shellfish Immunology 1, 141155.CrossRefGoogle Scholar
GRENFELL, B. T., WILSON, K., ISHAM, V. S., BOYD, H. E. G. & DIETZ, K. ( 1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology 111 (Suppl.), S135S151.CrossRefGoogle Scholar
HAKALAHTI, T. & VALTONEN, E. T. ( 2003). Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitology 127, 7985.CrossRefGoogle Scholar
HAKALAHTI, T., PASTERNAK, A. F. & VALTONEN, E. T. ( 2004). Seasonal dynamics of egg laying and egg-laying strategy of the ectoparasite Argulus coregoni (Crustacea: Branchiura). Parasitology 128, 655660.CrossRefGoogle Scholar
HERTER, K. ( 1927). Reizphysiologische Untersuchungen an der Karpfenlaus (Argulus foliaceus L.). Zeitschrift für vergleichende Physiologie 5, 283370.Google Scholar
JOHNSON, S. C. & ALBRIGHT, L. J. ( 1992). Comparative susceptibility and histopathology of the response of naïve Atlantic, chinook and coho salmon to experimental infection with Lepeoptheirus salmonis (Copepoda: Caligidae). Diseases of Aquatic Organisms 14, 179193.CrossRefGoogle Scholar
JONES, S. R. M. ( 2001). The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25, 841852.CrossRefGoogle Scholar
KARVONEN, A., HUDSON, P. J., SEPPÄLÄ, O. & VALTONEN, E. T. ( 2004). Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92, 183188.CrossRefGoogle Scholar
LAMARRE, E. & COCHRAN, P. A. ( 1992). Lack of host species selection by the exotic parasitic crustacean, Argulus japonicus. Journal of Freshwater Ecology 7, 7780.CrossRefGoogle Scholar
LESTER, R. J. G. & ROUBAL, F. R. ( 1995). Phylum Arthropoda. In Fish Diseases and Disorders (ed. Woo, P. T. K.), pp. 475599. Cab International, Wallingford, UK.
MacKINNON, B. M. ( 1993). Host response of Atlantic salmon (Salmo salar) to infection by sea lice (Caligus elongatus). Canadian Journal of Fisheries and Aquatic Sciences 50, 789792.CrossRefGoogle Scholar
MacKINNON, B. M. ( 1998). Host factors important in sea lice infestations. Journal of Marine Science 55, 188192.CrossRefGoogle Scholar
MALYUSHINA, G. A., KASUMYAN, A. O. & MARUSOV, E. A. ( 1991). Ecological aspects of chemical signals in fish. Journal of Ichthyology 31, 17.Google Scholar
MENEZES, J., RAMOS, M. A., PEREIRA, T. G. & DA SILVA, A. M. ( 1990). Rainbow trout culture failure in a small lake as a result of massive parasitosis related to careless fish introductions. Aquaculture 89, 123126.CrossRefGoogle Scholar
MEYER-ROCHOW, V. B., AU, D. & KESKINEN, E. ( 2001). Photoreception in fish lice (Branchiura): the eyes of Argulus foliaceus Linné, 1758 and A. coregoni Thorell, 1865. Acta Parasitologica 46, 321331.Google Scholar
MIKHEEV, V. N., VALTONEN, E. T. & RINTAMÄKI-KINNUNEN, P. ( 1998). Host searching in Argulus foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity. Parasitology 116, 425430.Google Scholar
MIKHEEV, V. N., MIKHEEV, A. V., PASTERNAK, A. F. & VALTONEN, E. T. ( 2000). Light-mediated host searching strategies in a fish ectoparasite, Argulus foliaceus L. (Crustacea: Branchiura). Parasitology 120, 409416.Google Scholar
MIKHEEV, V. N., PASTERNAK, A. F., VALTONEN, E. T. & LANKINEN, Y. ( 2001). Spatial distribution and hatching of overwintered eggs of a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura). Diseases of Aquatic Organisms 46, 123128.CrossRefGoogle Scholar
MIKHEEV, V. N., PASTERNAK, A. F. & VALTONEN, E. T. ( 2004). Tuning host specificity during the ontogeny of a fish ectoparasite: behavioural responses to host-induced cues. Parasitology Research 92, 220224.CrossRefGoogle Scholar
NORTHCOTT, S. J., LYNDON, A. R. & CAMPBELL, A. D. ( 1997). An outbreak of freshwater fish lice, Argulus foliaceus L., seriously affecting Scottish stillwater fishery. Fisheries Management and Ecology 4, 7375.CrossRefGoogle Scholar
PASTERNAK, A. F., MIKHEEV, V. N. & VALTONEN, E. T. ( 2000). Life history characteristics of Argulus foliaceus L. (Crustacea: Branchiura) populations in Central Finland. Annales Zoologici Fennici 37, 2535.Google Scholar
PFEIL-PUTZIEN, C. ( 1977). Experimentelle Übertragung der Frühjahrsvirämie (spring viraemia) der Karpfen durch Karpfenläuse (Argulus foliaceus). Zentralblatt für Veterinärmedizin, Reihe B 25, 319323.Google Scholar
PINHEIRO, J. C. & DOUGLAS, M. B. ( 2000). Statistics and Computing: Mixed-effects Models in S and S-Plus. Springer, New York.
POULIN, R. & FITZGERALD, G. J. ( 1989 a). Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.). Behavioural Ecology and Sociobiology 24, 251255.Google Scholar
POULIN, R. & FITZGERALD, G. J. ( 1989 b). A possible explanation for the aggregated distribution of Argulus canadensis Wilson, 1916 (Crustacea: Branchiura) on juvenile sticklebacks (Gasterosteidae). Journal of Parasitology 75, 5860.Google Scholar
POULIN, R., RAU, M. E. & CURTIS, M. A. ( 1991). Infection of brook trout fry, Salvelinus fontinalis, by ectoparasitic copepods: the role of host behaviour and initial parasite load. Animal Behaviour 41, 467476.CrossRefGoogle Scholar
SAKUMA, K. M., RALSTON, S., LANARZ, W. H. & EMBURY, M. ( 1999). Effects of the parasitic copepod Cardiodectes medusaeus on the lanternfishes Diaphus theta and Tarletonbeania crenularis off central California. Environmental Biology of Fishes 55, 423430.CrossRefGoogle Scholar
SALONIUS, K. & IWAMA, G. K. ( 1993). Effects of early rearing environment on stress response, immune function, and disease resistance in juvenile coho (Oncorhynchus kisutsch) and chinook salmon (O. tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 50, 759766.CrossRefGoogle Scholar
SHAW, D. J. & DOBSON, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111 (Suppl.), S111S133.CrossRefGoogle Scholar
SHIMURA, S. ( 1983). Seasonal occurrence, sex ratio and site preference of Argulus coregoni Thorell (Crustacea: Branchiura) parasitic on cultured freshwater salmonids in Japan. Parasitology 86, 537552.CrossRefGoogle Scholar
STAMMER, H. J. ( 1959). Beiträge zur Morphologie, Biologie und Bekämpfung der Karpfenläuse. Zeitschrift für Parasitenkunde 19, 135208.Google Scholar
THONEY, D. A. & BURRESON, E. M. ( 1988). Lack of a specific humoral response in Leiostomus xanthurus (Pisces: Scianidae) to parasitic copepods and monogeneans. Journal of Parasitology 74, 191194.CrossRefGoogle Scholar
TULLY, O. & NOLAN, D. T. ( 2002). A review of the population biology and host-parasite interactions of the sea louse Lepeoptheirus salmonis (Copepoda: Caligidae). Parasitology 124 (Suppl.), S165S182.Google Scholar
WILSON, K., BJØRNSTAD, O. N., DOBSON, A. P., MERLER, S., POGLAYEN, G., RANDOLPH, S. E., READ, A. F. & SKORPING, A. ( 2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P.), pp. 644. Oxford University Press, Oxford.
WOO, P. T. K. ( 1992). Immunological responses of fish to parasitic organisms. Annual Review of Fish Diseases, pp. 339366.CrossRefGoogle Scholar
WOO, P. T. K. & SHARIFF, M. ( 1990). Lernaea cyprinacea L. (Copepoda: Caligidae) in Helostoma temminicki Cuvier & Valenciennes: the dynamics of resistance in recovered and naïve fish. Journal of Fish Diseases 13, 485493.Google Scholar
ZELMER, D. A. & ARAI, H. P. ( 1998). The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. Journal of Parasitology 84, 2428.CrossRefGoogle Scholar