Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T22:46:44.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Interactions of warming and exposure affect susceptibility to parasite infection in a temperate fish species

Published online by Cambridge University Press:  26 May 2016

DANNY J. SHEATH ,
DEMETRA ANDREOU  and
J. ROBERT BRITTON
DANNY J. SHEATH*
Affiliation:
Department of Life and Environmental Sciences, Bournemouth University, BH12 5BB, UK
DEMETRA ANDREOU
Affiliation:
Department of Life and Environmental Sciences, Bournemouth University, BH12 5BB, UK
J. ROBERT BRITTON
Affiliation:
Department of Life and Environmental Sciences, Bournemouth University, BH12 5BB, UK
*
*Corresponding author: Department of Life and Environmental Sciences, Bournemouth University, Bournemouth BH12 5BB, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Predicting how elevated temperatures from climate change alter host–parasite interactions requires understandings of how warming affects host susceptibility and parasite virulence. Here, the effect of elevated water temperature and parasite exposure level was tested on parasite prevalence, abundance and burden, and on fish growth, using Pomphorhynchus laevis and its fish host Squalius cephalus. At 60 days post-exposure, prevalence was higher at the elevated temperature (22 °C) than ambient temperature (18 °C), with infections achieved at considerably lower levels of exposure. Whilst parasite number was significantly higher in infected fish at 22 °C, both mean parasite weight and parasite burden was significantly higher at 18 °C. There were, however, no significant relationships between fish growth rate and temperature, parasite exposure, and the infection parameters. Thus, whilst elevated temperature significantly influenced parasite infection rates, it also impacted parasite development rates, suggesting warming could have complex implications for parasite dynamics and host resistance.

Keywords

climate changePomphorhynchus laevisSqualius cephalusparasite prevalenceparasite abundance
Type
Research Article
Information
Parasitology , Volume 143 , Issue 10 , September 2016 , pp. 1340 - 1346
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Altizer, S., Ostfield, R. S., Johnson, P. T. J., Kutz, S. and Harvell, C. D. (2013). Climate change, infectious diseases: from evidence to a predictive framework. Science 341, 514–519.Google Scholar
Bakker, T. C., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle Scholar
Bauer, A. and Rigaud, T. (2015). Identifying a key host in an acanthocephalan-amphipod system. Parasitology 142, 1588–1594.CrossRefGoogle Scholar
Bentley, K. T. and Burgner, R. L. (2011). An assessment of parasite infestation rates of juvenile sockeye salmon after 50 years of climate warming in southwest Alaska. Environmental Biology of Fishes 92, 267–273.Google Scholar
Britton, J. R. (2007). Reference data for evaluating the growth of common riverine fishes in the UK. Journal of Applied Ichthyology 23, 555–560.CrossRefGoogle Scholar
Callaway, R., Shinn, A. P., Grenfell, S. E., Bron, J. E., Burnell, G., Cook, E. J. and Shields, R. J. (2012). Review of climate change impacts on marine aquaculture in the UK and Ireland. Aquatic Conservation Marine and Freshwater Ecosystems 22, 389–421.CrossRefGoogle Scholar
Cramp, R. L., Reid, S., Seebacher, F. and Franklin, C. E. (2014). Synergistic interaction between UVB radiation, temperature increases susceptibility to parasitic infection in a fish. Biology Letters 10, 20140449.CrossRefGoogle ScholarPubMed
Dianne, L., Perrot-Minnot, M. J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698.CrossRefGoogle ScholarPubMed
Dittmar, J., Janssen, H., Kuske, A., Kurtz, J., Scharsack, J. P. and Ardia, D. (2014). Heat, immunity: an experimental heat wave alters immune functions in three-spined sticklebacks (Gasterosteus aculeatus). Journal of Animal Ecology 83, 744–757.Google Scholar
Franceschi, N., Bauer, A., Bollache, L. and Rigaud, T. (2008). The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 1161–1170.Google Scholar
Hakalahti, T., Karvonen, A. and Valtonen, E. T. (2006). Climate warming, disease risks in temperate regions – Argulus coregoni, Diplostomum spathaceum as case studies. Journal of Helminthology 80, 93–98.CrossRefGoogle ScholarPubMed
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Climate warming, disease risks for terrestrial, marine biota. Science 296, 2158–2162.CrossRefGoogle ScholarPubMed
Hine, P. M. and Kennedy, C. R. (1974). The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon. Journal of Fish Biology 6, 665–679.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
Karvonen, A., Rintamaki, P., Jokela, J. and Valtonen, E. T. (2010). Increasing water temperature, disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. International Journal of Parasitology 40, 1483–1488.Google Scholar
Labaude, S., Rigaud, T. and Cézilly, F. (2015). Host manipulation in the face of environmental changes: ecological consequences. International Journal for Parasitology: Parasites and Wildlife 4, 442–451.Google Scholar
Lafferty, K. D. (2009). Calling for an ecological approach to studying climate change, infectious diseases. Ecology 90, 932–933.Google Scholar
Latham, A. and Poulin, R. (2002). Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zeal, shore crabs (Brachyura). Marine Biology 141, 1131–1139.Google Scholar
Lõhmus, M. and Björklund, M. (2015). Climate change: what will it do to fish–parasite interactions? Biological Journal of the Linnean Society 116, 397–411.CrossRefGoogle Scholar
Luong, L. T., Vigliotti, B. A. and Hudson, P. J. (2011). Strong density-dependent competition, acquired immunity constrain parasite establishment: Implications for parasite aggregation. International Journal of Parasitology 41, 505–511.Google Scholar
Macnab, V. and Barber, I. (2012). Some (worms) like it hot: fish parasites grow faster in warmer water and alter host thermal preferences. Global Change Biology 18, 1540–1548.Google Scholar
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.CrossRefGoogle Scholar
Marcogliese, D. J. (2008). The impact of climate change on the parasites, infectious diseases of aquatic animals. Revue Scientifique et Technique 27, 467–484.CrossRefGoogle ScholarPubMed
Nedeva, I., Atanassov, G., Karaivanova, E., Cakic, P. and Lenghardt, M. (2003). Pomphorhynchus laevis (Müller, 1776) from the river Danube. Experimental Pathology and Parasitology 6, 14–16.Google Scholar
Nikoskelainen, S., Bylund, G. and Lilius, E. M. (2004). Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Developmental and Comparative Immunology 28, 581–592.Google Scholar
Paull, S. H. and Johnson, P. T. (2011). High temperature enhances host pathology in a snail–trematode system: possible consequences of climate change for the emergence of disease. Freshwater Biology 56, 767–778.Google Scholar
Paull, S. H., LaFonte, B. E. and Johnson, P. T. (2012). Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk. Global Change Biology 18, 3558–3567.Google Scholar
Pegg, J., Andreou, D., Williams, C. F. and Britton, J. R. (2015). Temporal changes in growth, condition and trophic niche in juvenile Cyprinus carpio infected with a non-native parasite. Parasitology 142, 1579–1587.Google Scholar
Poisot, T., Šimková, A., Hyršl, P. and Mor, S. (2009). Interactions between immuno-competence, somatic condition, parasitism in the chub Leuciscus cephalus in early spring. Journal of Fish Biology 75, 1667–1682.Google Scholar
Raffel, T. R., Rohr, J. R., Kiesecker, J. M. and Hudson, P. J. (2006). Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20, 819–828.CrossRefGoogle Scholar
Rohr, J. R., Dobson, A. P., Johnson, P. T., Kilpatrick, A. M., Paull, S. H., Raffel, T. R., Ruiz-Moreno, D. and Thomas, M. B. (2011). Frontiers in climate change-disease research. Trends in Ecology & Evolution 26, 270–277.Google Scholar
Tinsley, R. C., York, J. E., Stott, L. C., Averard, A. L. E., Chapple, S. J. and Tinsley, M. C. (2011). Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on development within the host. Parasitology 138, 1039–1052.CrossRefGoogle Scholar
Toscano, B. J., Newsome, B. and Griffen, B. D. (2014). Parasite modification of predator functional response. Oecologia 175, 345–352.CrossRefGoogle ScholarPubMed
Weyts, F. A. A., Cohen, N., Flik, G. and Verburg-Van Kemenade, B. M. L. (1999). Interactions between the immune system, the hypothalamo–pituitary–interrenal axis in fish. Fish and Shellfish Immunology 9, 1–20.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236–244.Google Scholar