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Temporal changes in growth, condition and trophic niche in juvenile Cyprinus carpio infected with a non-native parasite

Published online by Cambridge University Press:  23 September 2015

J. PEGG Open the ORCID record for J. PEGG [Opens in a new window] ,
D. ANDREOU ,
C. F. WILLIAMS  and
J. R. BRITTON
J. PEGG*
Affiliation:
Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Poole BH12 5BB, UK
D. ANDREOU
Affiliation:
Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Poole BH12 5BB, UK
C. F. WILLIAMS
Affiliation:
Fisheries Technical Services, Environment Agency, Bromholme Lane, Brampton, Huntingdon, Cambridgeshire PE28 4NE, UK
J. R. BRITTON
Affiliation:
Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Poole BH12 5BB, UK
*
*Corresponding author. Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Poole BH12 5BB, UK. E-mail: jpegg@bournemouth.ac.uk
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Summary

In host–parasite relationships, parasite prevalence and abundance can vary over time, potentially impacting how hosts are affected by infection. Here, the pathology, growth, condition and diet of a juvenile Cyprinus carpio cohort infected with the non-native cestode Bothriocephalus acheilognathi was measured in October 2012 (end of their first summer of life), April 2013 (end of first winter) and October 2013 (end of second summer). Pathology revealed consistent impacts, including severe compression and architectural modification of the intestine. At the end of the first summer, there was no difference in lengths and condition of the infected and uninfected fish. However, at the end of the winter period, the condition of infected fish was significantly reduced and by the end of their second summer, the infected fish were significantly smaller and remained in significantly reduced condition. Their diets were significantly different over time; infected fish consumed significantly higher proportions of food items <53 µm than uninfected individuals, a likely consequence of impaired functional traits due to infection. Thus, the sub-lethal impacts of this parasite, namely changes in histopathology, growth and trophic niche were dependent on time and/or age of the fish.

Keywords

Trophically transmitted parasitecestodestable isotope analysisBothriocephalus acheilognathidietfitness
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1579 - 1587
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Agnew, P., Koella, J. C. and Michalakis, Y. (2000). Host life history responses to parasitism. Microbes and Infection 2, 891–896.CrossRefGoogle ScholarPubMed
Ali, M. and Wootton, R. J. (1999). Effect of variable food levels on reproductive performance of breeding female three-spined sticklebacks. Journal of Fish Biology 55, 1040–1053.Google Scholar
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Amundsen, P. A., Knudsen, R., Kuris, A. M. and Kristoffersen, R. (2003). Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102, 285–293.Google Scholar
Arnott, S. A., Barber, I. and Huntingford, F. A. (2000). Parasite-associated growth enhancement in a fish-cestode system. Proceedings of the Royal Society B – Biological Sciences 267, 657–663.Google Scholar
Bagenal, T. B. (1969). Relationship between food supply and fecundity in brown trout Salmo trutta L. Journal of Fish Biology 1, 167.CrossRefGoogle Scholar
Barber, I., Huntingford, F. A. and Crompton, D. W. T. (1995). The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. Journal of Fish Biology 47, 524–536.Google Scholar
Barber, I., Hoare, D. and Krause, J. (2000). Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165.CrossRefGoogle Scholar
Beldade, R., Holbrook, S. J., Schmitt, R. J., Planes, S., Malone, D. and Bernardi, G. (2012). Larger female fish contribute disproportionately more to self-replenishment. Proceedings of the Royal Society B – Biological Sciences 279, 2116–2121.CrossRefGoogle ScholarPubMed
Bowden, T. J., Thompson, K. D., Morgan, A. L., Gratacap, R. M. L. and Nikoskelainen, S. (2007). Seasonal variation and the immune response: a fish perspective. Fish & Shellfish Immunology 22, 695–706.CrossRefGoogle ScholarPubMed
Britton, J. R. (2013). Introduced parasites in food webs: new spades, shifting structures? Trends in Ecology & Evolution 28, 93–99.Google Scholar
Britton, J. R., Pegg, J. and Williams, C. F. (2011). Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS ONE 6, e26365–e26365.Google Scholar
Britton, J. R., Pegg, J., Baker, D. and Williams, C. F. (2012). Do lower feeding rates result in reduced growth of a cyprinid fish infected with the Asian tapeworm? Ecology of Freshwater Fish 21, 172–175.Google Scholar
Bromage, N., Porter, M. and Randall, C. (2001). The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197, 63–98.Google Scholar
Christe, P., Richner, H. and Oppliger, A. (1996). Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behavioral Ecology 7, 127–131.Google Scholar
Costello, M. J. (2006). Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology 22, 475–483.Google Scholar
Dynamite Baits (2015). http://www.dynamitebaits.com/products/p/marine-halibut-pellets Google Scholar
Gozlan, R. E., Britton, J. R., Cowx, I. and Copp, G. H. (2010). Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology 76, 751–786.Google Scholar
Granath, W. O. and Esch, G. W. (1983). Temperature and other factors that regulate the composition and infrapopulation densities of Bothriocephalus acheilognathi (Cestoda) in Gambusia affinis (Pisces). Journal of Parasitology 69, 1116–1124.Google Scholar
Hansen, S. P., Choudhury, A., and Cole, R. A. (2007). Evidence of experimental postcyclic transmission of Bothriocephalus acheilognathi in bonytail chub (Gila elegans). Journal of Parasitology 93, 202–204.Google Scholar
Hislop, J. R. G. (1988). The influence of maternal length and age on the size and weight of the eggs and the relative fecunsity of the haddock, Melanogrammus melanogrammus aeglefinus, in British waters. Journal of Fish Biology 32, 923–930.Google Scholar
Hoole, D., Bucke, D., Burgess, P. and Wellby, I. (2001). Diseases of Carp and other Cyprinid Fishes, Fishing News Books, Oxford.CrossRefGoogle Scholar
Jackson, A. L., Inger, R., Parnell, A. C. and Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595–602.Google Scholar
Jackson, M. C., Donohue, I., Jackson, A. L., Britton, J. R., Harper, D. M. and Grey, J. (2012). Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE 7, e31757.Google Scholar
Jiménez-Garcia, M. I. and Vidal-Martínez, V. M. (2005). Temporal variation in the infection dynamics and maturation cycle of Oligogonotylus manteri (digenea) in the cichlid fish, ‘Cichlasoma’ urophthalmus, from Yucatan, Mexico. Journal of Parasitology 91, 1008–1014.Google Scholar
Lamkova, K., Simkova, A., Palikova, M., Jurajda, P. and Lojek, A. (2007). Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitology Research 101, 775–789.CrossRefGoogle ScholarPubMed
Linder, C. M., Cole, R. A., Hoffnagle, T. L., Persons, B., Choudhury, A., Haro, R. and Sterner, M. (2012). Parasites of fishes in the Colorado River and selected tributaries in Grand Canyon, Arizona. Journal of Parasitology 98, 117–127.Google Scholar
Loot, G., Brosse, S., Lek, S. and Guegan, J. F. (2001). Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 1219–1227.Google Scholar
Medoc, V., Rigaud, T., Motreuil, S., Perrot-Minnot, M.-J. and Bollache, L. (2011). Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98, 825–835.CrossRefGoogle ScholarPubMed
Michalakis, Y. and Hochberg, M. E. (1994). Parasitic effects on host life history traits – a review of recent studies. Parasite 1, 291–294.Google Scholar
Moore, J. W. and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.CrossRefGoogle ScholarPubMed
Öztürk, M. O. and Altunel, F. N. (2006). Occurrence of Dactylogyrus infection linked to seasonal changes and host fish size on four cyprinid fishes in Lake Manyas, Turkey. Acta Zoologica Academiae Scientiarum Hungaricae 52, 407–415.Google Scholar
Pagan, I., Alonso-Blanco, C. and Garcia-arenal, F. (2008). Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathogens 4, e1000124.CrossRefGoogle ScholarPubMed
Parnell, A. C., Inger, R., Bearhop, S. and Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.Google Scholar
Phillips, D. L., Newsome, S. D. and Gregg, J. W. (2005). Combining sources in stable isotope mixing models: alternative methods. Oecologia 144, 520–527.Google Scholar
Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.Google Scholar
Poulin, R. and Thomas, F. (1999). Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15, 28–32.Google Scholar
Power, A. G. and Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. American Naturalist 164, S79–S89.Google Scholar
R Core Development Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org.Google Scholar
Riggs, M. R., Lemly, A. D. and Esch, G. W. (1987). The growth, biomass, and fecundity of Bothriocephalus acheilognathi in a North Carolina cooling reservoir. Journal of Parasitology 73, 893–900.Google Scholar
Salgado-Maldonado, G. and Pineda-López, R. F. (2003). The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions 5, 261–268.Google Scholar
Scholz, T., Kutcha, R. and Williams, C. (2012). Bothriocephalus acheilognathi. In Fish Parasites: Pathobiology and Protection (ed. Woo, P. T. K. and Buchmann, K.), pp. 282–297. CAB International, London.Google Scholar
Scott, A. L. and Grizzle, J. M. (1979). Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis yea, 1955 (Cestoda, Pseudophyllidea). Journal of Fish Diseases 2, 69–73.CrossRefGoogle Scholar
Scott, D. P. (1962). Effect of food quality on fecundity of rainbow trout, Salmo gairdneri . Journal of the Fisheries Research Board of Canada 19, 715.Google Scholar
Sirois, P. and Dodson, J. J. (2000). Influence of turbidity, food density and parasites on the ingestion and growth of larval rainbow smelt Osmerus mordax in an estuarine turbidity maximum. Marine Ecology Progress Series 193, 167–179.Google Scholar
Sorci, G., Morand, S. and Hugot, J. P. (1997). Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites. Proceedings of the Royal Society B – Biological Sciences 264, 285–289.Google Scholar
Stock, B. C. and Semmens, B. X. (2013). MixSIAR GUI User Manual, version 1.0. http://conserver.iugo-cafe.org/user/brice.semmens/MixSIAR Google Scholar
Thompson, S. N. and Kavaliers, M. (1994). Physiological bases for parasite induced alterations of host behavior. Parasitology 109, S119–S138.Google Scholar
Williams, C. F., Poddubnaya, L. G., Scholz, T., Turnbull, J. F. and Ferguson, H. W. (2011). Histopathological and ultrastructural studies of the tapeworm Monobothrium wageneri (Caryophyllidea) in the intestinal tract of tench Tinca tinca . Diseases of Aquatic Organisms 97, 143–154.CrossRefGoogle ScholarPubMed
Xiang-Hua, L. (2007). Diversity of the Asiatic tapeworm Bothriocephalus acheilognathi parasitizing common carp and grass carp in China. Current Zoology 53, 470–480.Google Scholar