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Between-individual variation in nematode burden among juveniles in a wild host

Published online by Cambridge University Press:  22 November 2016

H. M. V. GRANROTH-WILDING Open the ORCID record for H. M. V. GRANROTH-WILDING [Opens in a new window] ,
F. DAUNT ,
E. J. A. CUNNINGHAM  and
S. J. BURTHE
H. M. V. GRANROTH-WILDING*
Affiliation:
Ashworth Laboratories, Wellcome Centre for Infection, Immunity and Evolution/Institute of Evolutionary Biology, University of Edinburgh, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK
F. DAUNT
Affiliation:
NERC Centre for Ecology & Hydrology, Bush Estate, Penicuik EH26 0QB, UK
E. J. A. CUNNINGHAM
Affiliation:
Ashworth Laboratories, Wellcome Centre for Infection, Immunity and Evolution/Institute of Evolutionary Biology, University of Edinburgh, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK
S. J. BURTHE
Affiliation:
NERC Centre for Ecology & Hydrology, Bush Estate, Penicuik EH26 0QB, UK
*
*Corresponding author. P.O. Box 65, 00014 Helsinki. E-mail: [email protected]
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Summary

Parasite infection in young animals can affect host traits related to demographic processes such as survival and reproduction, and is therefore crucial to population viability. However, variation in infection among juvenile hosts is poorly understood. Experimental studies have indicated that effects of parasitism can vary with host sex, hatching order and hatch date, yet it remains unclear whether this is linked to differences in parasite burdens. We quantified gastrointestinal nematode burdens of wild juvenile European shags (Phalacrocorax aristotelis) using two in situ measures (endoscopy of live birds and necropsy of birds that died naturally) and one non-invasive proxy measure (fecal egg counts (FECs)). In situ methods revealed that almost all chicks were infected (98%), that infections established at an early age and that older chicks hosted more worms, but FECs underestimated prevalence. We found no strong evidence that burdens differed with host sex, rank or hatch date. Heavier chicks had higher burdens, demonstrating that the relationship between burdens and their costs is not straightforward. In situ measures of infection are therefore a valuable tool in building our understanding of the role that parasites play in the dynamics of structured natural populations.

Keywords

Parasite burdenendoscopedissectionContracaecumanisakidseabirdmacroparasiteprevalenceFECdemographic traitgrowthhost–parasite interaction
Type
Research Article
Information
Parasitology , Volume 144 , Issue 2 , February 2017 , pp. 248 - 258
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Abollo, E., Gestal, C. and Pascual, S. (2001). Anisakid infection in the European shag Phalacrocorax aristotelis aristotelis . Journal of Helminthology 75, 209–214.Google Scholar
Adamo, S. A., Jensen, M. and Younger, M. (2001). Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Animal Behaviour 62, 417–425.Google Scholar
Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorsen, O. (2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society B: Biological Sciences 269, 1625–1632.Google Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission. CABI, Wallingford, UK.CrossRefGoogle Scholar
Bates, D., Maechlar, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bowman, D. D. and Georgi, J. R. (2009). Georgis’ Parasitology for Veterinarians. Elsevier Health Sciences, St Louis, Missouri, USA.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach. Springer, New York.Google Scholar
Burthe, S., Newell, M. A., Goodman, G., Butler, A., Bregnballe, T., Harris, E., Wanless, S., Cunningham, E. J. A. and Daunt, F. (2013). Endoscopy as a novel method for assessing endoparasite burdens in free-ranging European shags (Phalacrocorax aristotelis). Methods in Ecology and Evolution 4, 207–216.Google Scholar
Colditz, I. G. (2008). Six costs of immunity to gastrointestinal nematode infections. Parasite Immunology 30, 63–70.Google Scholar
Craig, B. H., Pilkington, J. G. and Pemberton, J. M. (2006). Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496.Google Scholar
Daunt, F., Wanless, S., Harris, M. P. and Monaghan, P. (1999). Experimental evidence that age-specific reproductive success is independent of environmental effects. Proceedings of the Royal Society B: Biological Sciences 266, 1489–1493.Google Scholar
Daunt, F., Monaghan, P., Wanless, S., Harris, M. P. and Griffiths, R. (2001). Sons and daughters: age-specific differences in parental rearing capacities. Functional Ecology 15, 211–216.CrossRefGoogle Scholar
Dubinin, V. B. (1949). Experimental study of the life cycles of some parasitic worms of animals in the delta of the Volga river (in Russian). Parasit Sb Zool Inst SSSR Parasitology Digest Zoological Institute Institute of Science USSR [Parasitology Digest, Zoological Institute, Insititute of Science, USSR] 11, 126–160.Google Scholar
Fagerholm, H. P. and Overstreet, R. M. (2008). Ascaridoid Nematodes: Contracaecum, Porrocaecum, and Baylisascaris . In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 413–433. Wiley-Blackwell, New Jersey, USA.Google Scholar
Fitze, P. S., Clobert, J. and Richner, H. (2004). Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology 85, 2018–2026.Google Scholar
Granroth-Wilding, H. M. V., Burthe, S. J., Lewis, S., Reed, T. E., Herborn, K. A., Newell, M. A., Takahashi, E. A., Daunt, F. and Cunningham, E. J. A. (2014). Parasitism in early life: environmental conditions shape within-brood variation in responses to infection. Ecology and Evolution 4, 3408–3419.Google Scholar
Granroth-Wilding, H. M. V., Burthe, S. J., Lewis, S., Herborn, K. A., Takahashi, E. A., Daunt, F. and Cunningham, E. J. A. (2015). Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host. Proceedings of the Royal Society B: Biological Sciences 282, art. 20150602.Google Scholar
Griffiths, R., Daan, S. and Dijkstra, C. (1996). Sex identification in birds using two CHD genes. Proceedings of the Royal Society B: Biological Sciences 263, 1251–1256.Google ScholarPubMed
Harris, M. P., Buckland, S. T., Russell, S. M. and Wanless, S. (1994). Post fledging survival to breeding age of Shags Phalacrocorax aristotelis in relation to year, date of fledging and brood size. Journal of Avian Biology 25, 268–274.Google Scholar
Hasselquist, D. and Nilsson, J.-A. (2012). Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Animal Behaviour 83, 1303–1312.CrossRefGoogle Scholar
Hoberg, E. P. (2005). Marine birds and their helminth parasites. In Marine Parasitology (ed. Rohde, K.), pp. 414–420. CSIRO, Australia.Google Scholar
Huizinga, H. W. (1971). Contracaeciasis in pelicaniform Birds. Journal of Wildlife Diseases 7, 198–204.Google Scholar
Kuiken, T. (1999). Review of Newcastle Disease in Cormorants. Waterbirds 22, 333–347.Google Scholar
Levecke, B., De Wilde, N., Vandenhoute, E. and Vercruysse, J. (2009). Field validity and feasibility of four techniques for the detection of Trichuris in simians: a model for monitoring drug efficacy in public health? PLoS Neglected Tropical Diseases 3, e366.Google Scholar
Lindström, J. (1999). Early development and fitness in birds and mammals. Trends in Ecology and Evolution 14, 343–348.Google Scholar
Magrath, R. (1991). Nestling weight and juvenile survival in the blackbird, Turdus merula . Journal of Animal Ecology 60, 335–351.Google Scholar
McClelland, G. (2005). Nematoda (roundworms). In Marine Parasitology (ed. Rohde, K.), pp. 104–116. CSIRO, Australia.Google Scholar
Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends in Ecology and Evolution 16, 254–260.Google Scholar
Monaghan, P. (2008). Review. Early growth conditions, phenotypic development and environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 1635–1645.Google Scholar
Moravec, F. (2009). Experimental studies on the development of Contracaecum rudolphii (Nematoda: Anisakidae) in copepod and fish paratenic hosts. Folia Parasitologica 56, 185–193.Google Scholar
Mougeot, F., Martínez-Padilla, J., Webster, L. M. I., Blount, J. D., Pérez-Rodríguez, L. and Piertney, S. B. (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proceedings of the Royal Society B: Biological Sciences 276, 1093–1100.Google Scholar
Newey, S., Shaw, D. J., Kirby, A., Montieth, P., Hudson, P. J. and Thirgood, S. J. (2005). Prevalence, intensity and aggregation of intestinal parasites in mountain hares and their potential impact on population dynamics. International Journal for Parasitology 35, 367–373.Google Scholar
Pihlaja, M., Siitari, H. and Alatalo, R. V. (2006). Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. Journal of Animal Ecology 75, 1154–1164.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and Team, R. D. C. (2012). nlme: Linear and nonlinear mixed effects models. R package version 3.1-126.Google Scholar
Randolph, S. E., Miklisova, D., Lysy, J., Rogers, D. J. and Labuda, M. (1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186.CrossRefGoogle ScholarPubMed
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Redpath, S. M., Mougeot, F., Leckie, F. M., Elston, D. A. and Hudson, P. J. (2006). Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters 9, 410–418.CrossRefGoogle ScholarPubMed
Reed, T. E., Daunt, F., Hall, M. E., Phillips, R. A., Wanless, S. and Cunningham, E. J. A. (2008). Parasite treatment affects maternal investment in sons. Science 321, 1681–1682.Google Scholar
Reed, T. E., Daunt, F., Kiploks, A. J., Burthe, S. J., Granroth-Wilding, H. M. V., Takahashi, E. A., Newell, M., Wanless, S. and Cunningham, E. J. A. (2012). Impacts of parasites in early life: contrasting effects on juvenile growth for different family members. PLoS ONE 7, e32236.Google Scholar
Romano, A., Rubolini, D., Caprioli, M., Boncoraglio, G., Ambrosini, R. and Saino, N. (2011). Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings. PLoS ONE 6, e22805.Google Scholar
Schwagmeyer, P. L. and Mock, D. W. (2008). Parental provisioning and offspring fitness: size matters. Animal Behaviour 75, 291–298.CrossRefGoogle Scholar
Seivwright, L. J., Redpath, S. M., Mougeot, F., Watt, L. and Hudson, P. J. (2004). Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus . Journal of Helminthology 78, 69–76.Google Scholar
Shaw, D. and Dobson, A. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.Google Scholar
Shaw, J. L. and Moss, R. (1989). The role of parasite fecundity and longevity in the success of Trichostrongylus tenuis in low density red grouse populations. Parasitology 99, 253–258.Google Scholar
Stokland, J. N. and Amundsen, T. (1988). Initial size hierarchy in broods of the shag: relative significance of egg size and hatching asynchrony. Auk 105, 308–315.CrossRefGoogle Scholar
Tompkins, D. M. and Hudson, P. J. (1999). Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence. Parasitology 118, 417–423.Google Scholar
Tompkins, D. M., Dunn, A. M., Smith, M. J. and Telfer, S. (2011). Wildlife disease: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38.Google Scholar
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