Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-19T11:42:07.642Z Has data issue: false hasContentIssue false
  • English
  • Français

Consistent patterns of trophic niche specialization in host populations infected with a non-native copepod parasite

Published online by Cambridge University Press:  08 March 2017

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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Populations of generalist species often comprise of smaller sub-sets of relatively specialized individuals whose niches comprise small sub-sets of the overall population niche. Here, the role of parasite infections in trophic niche specialization was tested using five wild fish populations infected with the non-native parasite Ergasilus briani, a copepod parasite with a direct lifecycle that infects the gill tissues of fish hosts. Infected and uninfected fishes were sampled from the same habitats during sampling events. Prevalence in the host populations ranged between 16 and 67%, with parasite abundances of up to 66 parasites per fish. Although pathological impacts included hyperplasia and localized haemorrhaging of gill tissues, there were no significant differences in the length, weight and condition of infected and uninfected fishes. Stable isotope analyses (δ13C, δ15N) revealed that the trophic niche of infected fishes, measured as standard ellipse area (i.e. the isotopic niche), was consistently and significantly smaller compared with uninfected conspecifics. These niches of infected fishes always sat within that of uninfected fish, suggesting trophic specialization in hosts. These results suggested trophic specialization is a potentially important non-lethal consequence of parasite infection that results from impaired functional traits of the host.

Keywords

non-native parasitestable isotope analysisRutilus rutilusAbramis bramaniche constrictionErgasilus briani
Type
Research Article
Information
Parasitology , Volume 144 , Issue 7 , June 2017 , pp. 945 - 953
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Abdelhalim, A. I., Lewis, J. W. and Boxshall, G. A. (1991). The life-cycle of Ergasilus sieboldi Nordmann (Copepoda, Poecilostomatoida), parasitic on British freshwater fish. Journal of Natural History 25, 559–582.CrossRefGoogle Scholar
Alston, S. and Lewis, J. W. (1994). The ergasilid parasites (Copepoda:Poecilostomatoida) of British freshwater fish. In Parasitic Diseases of Fish (ed. Pike, A. W. and Lewis, J. W.), p. 251. Samara Publishing Ltd, Dyfed, Wales.Google Scholar
Andreou, D., Arkush, K. D., Guegan, J.-F. and Gozlan, R. E. (2012). Introduced pathogens and native freshwater biodiversity: a case study of Sphaerothecum destruens . PLoS ONE 7, e36998.CrossRefGoogle ScholarPubMed
Araujo, M. S., Bolnick, D. I. and Layman, C. A. (2011). The ecological causes of individual specialisation. Ecology Letters 14, 948–958.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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
Bolnick, D. I., Svanback, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D. and Forister, M. L. (2003). The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161, 1–28.CrossRefGoogle ScholarPubMed
Bolnick, D. I., Svanback, R., Araujo, M. S. and Persson, L. (2007). Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences of the United States of America 104, 10075–10079.CrossRefGoogle ScholarPubMed
Britton, J. R. (2013). Introduced parasites in food webs: new spades, shifting structures? Trends in Ecology & Evolution 28, 93–99.CrossRefGoogle Scholar
Britton, J. R. and Andreou, D. (2016). Parasitism as a driver of trophic niche specialisation. Trends in Parasitology 32, 437–445.CrossRefGoogle ScholarPubMed
Clerc, M., Ebert, D. and Hall, M. D. (2015). Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence. Proceedings of the Royal Society of London B: Biological Sciences 282, 20142820.Google ScholarPubMed
Cornell University Stable Isotope laboratory (2015). Preparation guidelines. http://www.cobsil.com/iso_main_preparation_guidlines.php.Google Scholar
Crowden, A. E. and Broom, D. M. (1980). Effects of the eye fluke Diplostomum spathaceum on the behaviour of Dace Leuciscus leuciscus . Animal Behaviour 28, 286–294.CrossRefGoogle Scholar
Cunningham, E. J., Tierney, J. F. and Huntingford, F. A. (1994). Effects of the cestode Schistocephalus solidus on food intake and foraging decisions in the 3 spined stickleback Gasterosteus aculeatus . Ethology 97, 65–75.CrossRefGoogle Scholar
Dezfuli, B. S., Giari, L., Konecny, R., Jaeger, P. and Manera, M. (2003). Immunohistochemistry, ultrastructure and pathology of gills of Abramis brama from lake Mondsee, Austria, infected with Ergasilus sieboldi (Copepoda). Diseases of Aquatic Organisms 53, 257–262.CrossRefGoogle ScholarPubMed
Durell, S. (2000). Individual feeding specialisation in shorebirds: population consequences and conservation implications. Biological Reviews 75, 503–518.CrossRefGoogle Scholar
Duthie, G. G. and Hughes, G. M. (1987). The effects of reduced gill area and hyperoxia on the oxygen consumption and swimming speed of Rainbow trout. Journal of Experimental Biology 127, 349–354.CrossRefGoogle Scholar
Fryer, A. G. and Andrews, A. C. (1983). The parasitic copepod Ergasilus briani Markewitsch in Yorkshire: an addition to the British fauna. Naturalist 108, 7–10.Google Scholar
Giles, N. (1983). Behavioral effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the 3 spined stickleback, Gasterosteus aculeatus L. Animal Behaviour 31, 1192–1194.CrossRefGoogle Scholar
Giles, N. (1987). Predation risk and reduced foraging activity in fish – experiments with parasitized and non-parasitized 3-spined sticklebacks, Gasterosteus aculeatus L. Journal of Fish Biology 31, 37–44.CrossRefGoogle Scholar
Hansen, H., Bachmann, L. and Bakke, T. A. (2003). Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling, and rainbow trout in Norway and Sweden. International Journal for Parasitology 33, 1471–1478.CrossRefGoogle ScholarPubMed
Hernandez, A. D. and Sukhdeo, M. V. K. (2008). Parasites alter the topology of a stream food web across seasons. Oecologia 156, 613–624.CrossRefGoogle ScholarPubMed
Hoole, D., Bucke, D., Burgess, P. and Wellby, I. (2001). Diseases of Carp and Other Cyprinid Fishes. Fishing News Books, Oxford.CrossRefGoogle Scholar
Huss, M., Bystrom, P. and Persson, L. (2008). Resource heterogeneity, diet shifts and intra-cohort competition: effects on size divergence in YOY fish. Oecologia 158, 249–257.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 CrossRefGoogle ScholarPubMed
Jakobsen, P. J., Johnsen, G. H. and Larsson, P. (1988). Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine threespine stickleback (Gasterosteus aculeatus). Canadian Journal of Fisheries and Aquatic Sciences 45, 426–431.CrossRefGoogle Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 11211–11216.CrossRefGoogle ScholarPubMed
Lefevre, T., Lebarbenchon, C., Gauthier-Clerc, M., Misse, D., Poulin, R. and Thomas, F. (2009). The ecological significance of manipulative parasites. Trends in Ecology & Evolution 24, 41–48.CrossRefGoogle ScholarPubMed
Lomnicki, A. (1988). Population ecology of individuals. Monographs in Population Biology 25, 1–216.Google ScholarPubMed
Milinski, M. (1984). Parasites determine a predators optimal feeding strategy. Behavioral Ecology and Sociobiology 15, 35–37.CrossRefGoogle Scholar
Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour 93, 203–216.CrossRefGoogle Scholar
Montero, F. E., Crespo, S., Padros, F., De la Gandara, F., Garcia, A. and Raga, J. A. (2004). Effects of the gill parasite Zeuxapta seriolae (Monogenea: Heteraxinidae) on the amberjack Seriola dumerili Risso (Teleostei: Carangidae). Aquaculture 232, 153–163.CrossRefGoogle Scholar
Peeler, E. J. and Thrush, M. A. (2004). Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom. Diseases of Aquatic Organisms 62, 103–113.CrossRefGoogle ScholarPubMed
Pegg, J., Andreou, D., Williams, C. F. and Britton, J. R. (2015). Head morphology and piscivory of European eels, Anguilla anguilla, predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus . Freshwater Biology 60, 1977–1987.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J. and Montana, C. G. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.CrossRefGoogle Scholar
Poulin, R., Rau, M. E. and 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, 467–476.CrossRefGoogle Scholar
Quevedo, M., Svanback, R. and Eklov, P. (2009). Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90, 2263–2274.CrossRefGoogle Scholar
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Schuwerack, P. M. M., Lewis, J. W. and Jones, P. W. (2001). Pathological and physiological changes in the South African freshwater crab Potamonautes warreni calman induced by microbial gill infestations. Journal of Invertebrate Pathology 77, 269–279.CrossRefGoogle ScholarPubMed
Sheath, D., Reading, A., Williams, C. and Britton, J. (2015). Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biological Invasions 17, 2235–2246.CrossRefGoogle Scholar
Stephens, D. W. and Krebs, J. R. (1986). Monographs in Behavior and Ecology: Foraging Theory. Xiv+247p. Princeton University Press, Princeton, New Jersey, USA.Google Scholar
Svanback, R. and Bolnick, D. I. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B: Biological Sciences 274, 839–844.CrossRefGoogle ScholarPubMed
Svanback, R. and Persson, L. (2004). Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. Journal of Animal Ecology 73, 973–982.CrossRefGoogle Scholar
Thorarensen, H., Gallaugher, P. E., Kiessling, A. K. and Farrell, A. P. (1993). Intestinal blood-flow in swimming Chinook salmon Oncorhynchus tshawytscha and the effects of hematocrit on blood flow distribution. Journal of Experimental Biology 179, 115–129.CrossRefGoogle Scholar
Tran, T. N. Q., Jackson, M. C., Sheath, D., Verreycken, H. and Britton, J. R. (2015). Patterns of trophic niche divergence between invasive and native fishes in wild communities are predictable from mesocosm studies. Journal of Animal Ecology 84, 1071–1080.CrossRefGoogle ScholarPubMed
Van Valen, L. (1965). Morphological variation and width of ecological niche. American Naturalist 377–390.CrossRefGoogle Scholar
Ward, A. J. W., Hoare, D. J., Couzin, I. D., Broom, M. and Krause, J. (2002). The effects of parasitism and body length on positioning within wild fish shoals. Journal of Animal Ecology 71, 10–14.CrossRefGoogle Scholar
Wood, C. L., Byers, J. E., Cottingham, K. L., Altman, I., Donahue, M. J. and Blakeslee, A. M. H. (2007). Parasites alter community structure. Proceedings of the National Academy of Sciences of the United States of America 104, 9335–9339.CrossRefGoogle ScholarPubMed