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Delayed transmission of a parasite is compensated by accelerated growth

Published online by Cambridge University Press:  28 June 2005

T. HAKALAHTI
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014 University of Jyväskylä, Finland
M. BANDILLA
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014 University of Jyväskylä, Finland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35 (ya), FIN-40014 University of Jyväskylä, Finland

Abstract

Compensatory or ‘catch-up’ growth following prolonged periods of food shortages is known to exist in many free-living animals. It is generally assumed that growth rates under normal circumstances are below maximum because elevated rates of growth are costly. The present paper gives experimental evidence that such compensatory growth mechanisms also exist in parasitic species. We explored the effect of periodic host unavailability on survival, infectivity and growth of the fish ectoparasite Argulus coregoni. Survival and infectivity of A. coregoni metanauplii deprived of a host for selected time periods were age dependent, which indicates that all metanauplii carry similar energy resources for host seeking. Following the periods off-host, metanauplii were allowed to settle on rainbow trout and were length measured until they reached gravidity. During early development on fish, body length of attached A. coregoni was negatively correlated with off-host period indicating a mechanism that creates size variance in an attached parasite cohort originally containing equal amounts of resources. However, over time the size differences between parasites became less pronounced and eventually parasites that were kept off-host for longest periods of time reached the length of those individuals that had been allowed to infect a host sooner. A. coregoni thus appears to compensate for delayed growth resulting from an extended host searching period by elevated growth rates, although we show that such accelerated growth incurred a cost, through decreased life-expectancy.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Ali, M., Nicieza, A. and Wootton, R. J. ( 2003). Compensatory growth in fishes: a response to growth depression. Fish and Fisheries 4, 147190.CrossRefGoogle Scholar
Anderson, R. M. and Whitfield, P. J. ( 1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparker, 1924). Parasitology 70, 295310.CrossRefGoogle Scholar
Andersson, M. ( 1994). Sexual Selection. Princeton University Press, Princeton, USA.
Anscombe, B. ( 1948). The transformation of Poisson, binomial and negative binomial data. Biometrika 35, 246254.CrossRefGoogle Scholar
Arendt, J. D. ( 1997). Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 2, 149177.CrossRefGoogle Scholar
Blum, W. F. ( 1997). Leptin: the voice of the adipose tissue. Hormone Research 48, 28.CrossRefGoogle Scholar
Broekhuizen, N., Gurney, W. S. C., Jones, A. and Bryant, A. D. ( 1994). Modelling compensatory growth. Functional Ecology 8, 770782.CrossRefGoogle Scholar
Cable, J., Tinsley, R. C. and Harris, P. D. ( 2002). Survival, feeding and embryo development of Gyrodactylus gasterostei (Monogenea: Gyrodactylidae). Parasitology 124, 5368. DOI: 10.1017/S0031182001008861.CrossRefGoogle Scholar
De Roos, A. M., Diekmann, O. and Metz, J. A. J. ( 1992). Studying the dynamics of structured population models: a versatile technique and its application to Daphnia. The American Naturalist 139, 123147.CrossRefGoogle Scholar
Dybdahl, M. F. and Storfer, A. ( 2003). Parasite local adaptation: red queen versus suicide king. Trends in Ecology and Evolution 18, 523530. DOI: 10.1016/S0169-5347(03)00223-4.CrossRefGoogle Scholar
Fenton, A. and Rands, S. A. ( 2004). Optimal parasite infection strategies: a state-dependent approach. International Journal for Parasitology 34, 813821. DOI: 10.1016/j.ijpara.2004.02.003.CrossRefGoogle Scholar
Fenton, A. and Hudson, P. J. ( 2002). Optimal infection strategies: should macroparasites hedge their bets? Oikos 96, 92101.Google Scholar
Finch, C. E. and Kirkwood, T. B. L. ( 2000). Chance, Development, and Aging. Oxford University Press, Oxford, UK.
Friedman, J. M. ( 1998). Leptin, leptin receptors and the control of body weight. Nutrition Reviews 56, 3846.CrossRefGoogle Scholar
Gannicott, A. M. and Tinsley, R. C. ( 1998). Larval survival characteristics and behaviour of the gill monogenean Discocotyle sagittata. Parasitology 117, 491498.CrossRefGoogle Scholar
Gotthard, K., Nylin, S. and Wiklund, C. ( 1994). Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281289.CrossRefGoogle Scholar
Hakalahti, T. and Valtonen, E. T. ( 2003). Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitology 127, 7985. DOI: 10.1017/S0031182003003196.CrossRefGoogle Scholar
Hakalahti, T., Häkkinen, H. and Valtonen, E. T. ( 2004). Ectoparasitic Argulus coregoni (Crustacea: Branchiura) hedge their bets – studies on egg hatching dynamics. Oikos 107, 295302. DOI: 10.1111/j.0030-1299.2004.13213.x.CrossRefGoogle Scholar
Heins, D. C., Baker, J. A. and Martin, H. C. ( 2002). The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302307.Google Scholar
Heuch, P. A. and Schram, T. A. ( 1996). Male mate choice in a natural population of the parasitic copepod Lernaeocera branchialis. Behaviour 133, 221239.CrossRefGoogle Scholar
Hopper, K. R. ( 1999). Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535560.CrossRefGoogle Scholar
Hoskonen, P. and Pirhonen, J. ( 2004). Temperature effects on anaesthesia with clove oil in six temperate zone fishes. Journal of Fish Biology 64, 11361142. DOI: 10.1111/j.1095-8649.2004.00359.x.CrossRefGoogle Scholar
Jespersen, L. B. and Toft, S. ( 2003). Compensatory growth following early nutritional stress in the Wolf Spider Pardosa Prativaga. Functional Ecology 17, 737746.CrossRefGoogle Scholar
Jobling, M. and Johansen, S. J. S. ( 1999). The lipostat, hyperphagia and catch-up growth. Aquaculture Research 30, 473478.CrossRefGoogle Scholar
Kabata, Z. ( 1970). Diseases of Fishes: Book I. Crustacean as Enemy of Fishes. T.F.H. Publications, New Jersey, USA.
Karvonen, A., Paukku, S., Valtonen, E. T. and Hudson, P. J. ( 2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224. DOI: 10.1017/S0031182003003561.CrossRefGoogle Scholar
Keeley, E. R. and Grant, J. W. A. ( 1997). Allometry of diet selectivity in juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Science 54, 18941902.CrossRefGoogle Scholar
Keeley, E. R. and Grant, J. W. A. ( 2001). Prey size of salmonid fishes in streams, lakes and oceans. Canadian Journal of Fisheries and Aquatic Science 58, 11221132.CrossRefGoogle Scholar
Kollatsch, D. ( 1959). Untersuchungen über die Biologie und Ökologie der Karpfenlaus (Argulus foliaceus L.). Zoologische Beiträge 5, 136.Google Scholar
Lee, E. T. ( 1992). Statistical Methods for Survival Data Analysis. John Wiley & Sons, New York, USA.
Metcalfe, N. B. and Monaghan, P. ( 2001). Compensation for a bad start: grow now, pay later? Trends in Ecology Evolution 16, 254260. DOI: 10.1016/S0531-5565(03)00159-1.CrossRefGoogle Scholar
Metcalfe, N. B. and Monaghan, P. ( 2003). Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology 38, 935940.CrossRefGoogle Scholar
Meyer-Rochow, V. B., Au, D. and 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., Mikheev, A. V., Pasternak, A. F. and 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. and Lankinen, Y. ( 2001). Spatial distribution and hatching of overwintered eggs in a fish ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura). Diseases of Aquatic Organisms 46, 123128.CrossRefGoogle Scholar
Mikheev, V. N., Pasternak, A. F. and Valtonen, E. T. ( 2004). Tuning host specificity during the ontogeny of a fish ectoparasite: behavioural responses to host-induced cues. Parasitology Research 92, 220224. DOI: 10.1007/S00436-003-1044-x.CrossRefGoogle Scholar
Mikheev, V. N., Valtonen, E. T. and Rintamäki-Kinnunen, P. ( 1998). Host searching in Argulus foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity. Parasitology 116, 425430.Google Scholar
Morgan, I. J. and Metcalfe, N. B. ( 2001). Deferred costs of compensatory growth after autumnal food shortage in juvenile salmon. Proceedings Royal Society of London, B 268, 295301. DOI: 10.1098/rspb.2000.1365.CrossRefGoogle Scholar
O'Connor, K. I., Taylor, A. C. and Metcalfe, N. B. ( 2000). The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon. Journal of Fish Biology 57, 4151.CrossRefGoogle Scholar
Pasternak, A. F., Mikheev, V. N. and Valtonen, E. T. ( 2000). Life history characteristics of Argulus foliaceus L. (Crustacea: Branchiura) populations in Central Finland. Annales Zoologici Fennici 37, 2535.Google Scholar
Pasternak, A., Mikheev, V. and Valtonen, E. T. ( 2004). Growth and development of Argulus coregoni (Crustacea: Branchiura) on salmonid and cyprinid hosts. Diseases of Aquatic Organisms 58, 203207.CrossRefGoogle Scholar
Patel, M. N., Stolinski, M. and Wright, D. J. ( 1997). Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations of four Steinernema species. Parasitology 114, 489496.CrossRefGoogle Scholar
Philippi, T. and Seger, J. ( 1989). Hedging one's evolutionary bets, revisited. Trends in Ecology and Evolution 2, 4144.CrossRefGoogle Scholar
Ricklefs, R. E. ( 1969). Preliminary models for growth rates in altricial birds. Ecology 50, 10311039.CrossRefGoogle Scholar
Seger, J. and Brockmann, H. J. ( 1987). What is bet-hedging? In Oxford Surveys in Evolutionary Biology, Vol. 4. ( ed. Harvey, P. H. and Partridge, L.), pp. 182211. Oxford University Press, Oxford, UK.
Shimura, S. ( 1981). The larval development of Argulus coregoni Thorell (Crustacea: Branchiura). Journal of Natural History 15, 331348.CrossRefGoogle Scholar
Shimura, S. ( 1983). Seasonal occurrence, sex ratio and site preference of Argulus coregoni Thorell (Crustacea: Brachiura) parasitic on cultured freshwater salmonids in Japan. Parasitology 86, 537552.CrossRefGoogle Scholar
Shotts Jr., E. B. and Starliper, C. E. ( 1999). Flavobacterial diseases: columnaris disease, cold-water disease and bacterial gill disease. In Fish Diseases and Disorders, Vol. 3: Viral, Bacterial and Fungal Infections. ( ed. Woo, P. T. K. and Bruno, D. W.), pp. 559659. CABI Publishing, Wallingford, UK.
Sibly, R. M. and Calow, P. ( 1986). Physiological Ecology of Animals. Blackwell Scientific, Oxford, UK.
Stearns, S. C. ( 1992). The Evolution of Life Histories. Oxford University Press, New York.
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. ( 2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.Google Scholar
Thomas, K. and Ollevier, F. ( 1993). Hatching, survival, activity and penetration efficiency of second-stage larvae of Anguillicola crassus (Nematoda). Parasitology 107, 211217.CrossRefGoogle Scholar
Timi, J. T., Lanfranchi, A. L. and Poulin, R. ( 2005). Is there a trade-off between fecundity and egg volume in parasitic copepod Lernanthropus cynoscicola? Parasitology Research 95, 14.Google Scholar
Whitfield, P. J., Bartlett, A., Khammo, N. and Clothier, R. H. ( 2003). Age-dependent survival and infectivity of Schistosoma mansoni cercariae. Parasitology 127, 2935. DOI: 10.1017/S0031182003003263.CrossRefGoogle Scholar
Wu, L. and Dong, S. ( 2002). Compensatory growth responses in juvenile Chinese shrimp, Fenneropenaeus chinensis, at different temperatures. Journal of Crustacean Biology 22, 511520. DOI: 10.1043/0278-0372.2002)022<0511:CGRIJC>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Zar, J. H. ( 1999). Biostatistical Analysis. Prentice-Hall, New Jersey, USA.