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Variation in fecal egg counts in horses managed for conservation purposes: individual egg shedding consistency, age effects and seasonal variation

Published online by Cambridge University Press:  16 August 2012

E. L. D. WOOD ,
J. B. MATTHEWS ,
S. STEPHENSON ,
M. SLOTE  and
D. H. NUSSEY
E. L. D. WOOD
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh, UK
J. B. MATTHEWS*
Affiliation:
Disease Control, Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian, UK
S. STEPHENSON
Affiliation:
Broads Authority, Dragonfly House, 2 Gilders Way, Norwich NR3 1UB, UK
M. SLOTE
Affiliation:
Norfolk Wildlife Trust, Bewick House, 22 Thorpe Road, Norwich NR1 1RY, UK
D. H. NUSSEY
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh, UK Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh, UK
*
*Corresponding author: Disease Control, Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian, UK. Tel: +44 131 445 5111. Fax: +44 131 445 6111. E-mail: jacqui.matthews@moredun.ac.uk
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Summary

Cyathostomins are the most prevalent equine intestinal parasites and resistance has been reported in these nematodes against all 3 licensed anthelmintic classes. Strategies need to be developed that are less dependent upon drugs and more reliant on management-based control. To develop these we need to understand natural transmission patterns better. Here, we analysed longitudinal fecal egg count (FEC) data from 5 pony populations used for conservation purposes. We tested how egg excretion varied amongst populations and individuals, and how this was affected by age and climate. There was evidence for consistency in FECs over time at the individual level; this was generally weak and accounted for <10% of the total variance. Animals <5 years old had higher FECs and there was profound seasonal variation in FECs, with highest levels recorded in spring/summer. Effects of monthly temperature and rainfall explained most, but not all, of the observed seasonal variation and associations between climate measures and FECs were stronger in younger versus adult animals. One population was occasionally treated with anthelmintics and analysis of this population suggested that treatment substantially altered the seasonal dynamics. This paper highlights the variability in strongyle egg excretion amongst individuals and the factors involved in this variation.

Keywords

horsesnematodescyathostominsfaecal egg countsconsistencyageclimate
Type
Research Article
Information
Parasitology , Volume 140 , Issue 1 , January 2013 , pp. 115 - 128
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Baudena, M. A., Chapman, M. R., French, D. D. and Klei, T. R. (2000). Seasonal development and survival of equine cyathostome larvae on pasture in south Louisiana. Veterinary Parasitology, 88, 51–60.CrossRefGoogle ScholarPubMed
Becher, A. M., Mahling, M., Nielsen, M. K. and Pfister, K. (2010). Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): an investigation into strongyle egg shedding consistency. Veterinary Parasitology 171, 116–122.CrossRefGoogle ScholarPubMed
Cabaret, J. and Berrag, B. (2004). Faecal egg count reduction test for assessing anthelmintic efficacy: average versus individually based estimations. Veterinary Parasitology 121, 105–113.CrossRefGoogle ScholarPubMed
Calder, P. C. and Kew, S. (2002). The immune system: a target for functional foods? British Journal of Nutrition 88, S165–S176.CrossRefGoogle ScholarPubMed
Coop, R. L. and Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology 26, 951–962.CrossRefGoogle ScholarPubMed
Corning, S. (2009). Equine cyathostomins: a review of biology, clinical significance and therapy. Parasites & Vectors 2, Suppl. 1.CrossRefGoogle ScholarPubMed
Couto, M. C. M., Quinelato, S., Santos, C. N., Souza, L. S., Sampaio, I. B. M. and Rodrigues, M. L. A. (2008). Environmental influence in cyathostominae ecology. Veterinarni Medicina 53, 243–249.CrossRefGoogle Scholar
Crawley, M. J. (2007). The R Book. John Wiley and Sons Ltd, West Sussex, UK.CrossRefGoogle Scholar
Döpfer, D., Kerssens, C. M., Meijer, Y. G., Boersema, J. H. and Eysker, M. (2004). Shedding consistency of strongyle-type eggs in Dutch boarding horses. Veterinary Parasitology 124, 249–258.CrossRefGoogle ScholarPubMed
Dowdall, S. M. J., Matthews, J. B., Mair, T., Murphy, D., Love, S. and Proudman, C. J. (2002). Antigen-specific IgG(T) responses in natural and experimental Cyathostominae infection in horses. Veterinary Parasitology 106, 225–242.CrossRefGoogle ScholarPubMed
Eysker, M., Boersema, J. H. and Kooyman, F. N. (1990). Seasonally inhibited development of cyathostomine nematodes in Shetland ponies in The Netherlands. Veterinary Parasitology 36, 259–264.CrossRefGoogle ScholarPubMed
Eysker, M., Van Doorn, D. C., Lems, S. N., Weteling, A. and Ploeger, H. W. (2006). Frequent deworming in horses; it usually does not do any good, but it often harms. Tijdschr Diergeneeskd 131, 524–530.Google Scholar
Falconer, D. S. and Mackay, T. F. C. (1996). Introduction to Quantitative Genetics. 4th Edn, Prentice Hall, London, UK.Google Scholar
Fleurance, G., Duncan, P., Fritz, H., Cabaret, J., Cortet, J. and Gordon, I. J. (2007). Selection of feeding sites by horses at pasture: Testing the anti-parasite theory. Applied Animal Behaviour Science 108, 288–301.CrossRefGoogle Scholar
Giles, C. J., Urquhart, K. A. and Longstaffe, J. A. (1985). Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases. Equine Veterinary Journal 17, 196–201.CrossRefGoogle ScholarPubMed
Grenfell, B. T., Wilson, K., Isham, V. S., Boyd, H. E. G. and Dietz, K. (1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminat interactions as a case study. Parasitology 111, S135–S151.CrossRefGoogle ScholarPubMed
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: Environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London, B 276, 3477–3485.Google Scholar
Hodgkinson, J. E., Freeman, K. L., Lichtenfels, J. R., Palfreman, S., Love, S. and Matthews, J. B. (2005). Identification of strongyle eggs from anthelmintic-treated horses using a PCR-ELISA based on intergenic DNA sequences. Parasitology Research 95, 287–292.CrossRefGoogle ScholarPubMed
Horohov, D. W., Adams, A. A. and Chambers, T. M. (2010). Immunosenescence of the equine immune system. Journal of Comparative Pathology 142, S78–S84.CrossRefGoogle ScholarPubMed
Kaplan, R. M. and Nielsen, M. K. (2010). An evidence-based approach to equine parasite control: It ain't the 60 s anymore. Equine Veterinary Education 22, 306–316.CrossRefGoogle Scholar
Klei, T. R. and Chapman, M. R. (1999). Immunity in equine cyathostome infections. Veterinary Parasitology 85, 123–133.CrossRefGoogle ScholarPubMed
Kornas, S., Cabaret, J., Skalska, M. and Nowosad, B. (2010). Horse infection with intestinal helminths in relation to age, sex, access to grass and farm system. Veterinary Parasitology 174, 285–291.CrossRefGoogle ScholarPubMed
Larsen, M. L. L. M. L., Ritz, C., Petersen, S. L. and Nielsen, M. K. (2011). Determination of ivermectin efficacy against cyathostomins and Parascaris equorum on horse farms using selective therapy. The Veterinary Journal 188, 44–47.CrossRefGoogle ScholarPubMed
Lessells, C. M. and Boag, P. T. (1987). Unrepeatable repeatabilities: A common mistake. The Auk 104, 116–121.CrossRefGoogle Scholar
Lichtenfels, J. R., Kharchenko, V. A. and Dvojnos, G. M. (2008). Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Veterinary Parasitology 156, 4–161.CrossRefGoogle ScholarPubMed
Love, S. and Duncan, J. L. (1992). The development of naturally acquired cyathstome infection in ponies. Veterinary Parasitology 44, 127–142.CrossRefGoogle ScholarPubMed
Matthews, J. B. (2008). An update on cyathostomins: Anthelmintic resistance and worm control. Equine Veterinary Education 20, 552–560.CrossRefGoogle Scholar
Matthews, J. B. (2011). Facing the threat of equine parasitic disease. Equine Veterinary Journal 43, 126–132.CrossRefGoogle ScholarPubMed
McKellar, Q. A. (1997). Ecotoxicology and residues of anthelmintic compounds. Veterinary Parasitology 72, 413–435.CrossRefGoogle ScholarPubMed
Naeraho, A., Vainio, K. and Oksanen, A. (2011). Impaired efficacy of ivermectin against Parascaris equorum, and both ivermectin and pyrantel against strongyle infections in trotter foals in Finland. Veterinary Parasitology 182, 372–377.CrossRefGoogle Scholar
Nielsen, M. K., Baptiste, K. E., Tolliver, S. C., Collins, S. S. and Lyons, E. T. (2010 b). Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present. Veterinary Parasitology 174, 77–84.CrossRefGoogle ScholarPubMed
Nielsen, M. K., Fritzen, B., Duncan, J. L., Guillot, J., Eysker, M., Dorchies, P., Laugier, C., Beugnet, F., Meana, A., Lussot-Kervern, I. and von Samson-Himmelstjerna, G. (2010 a). Practical aspects of equine parasite control: A review based upon a workshop discussion consensus. Equine Veterinary Journal 42, 460–468.CrossRefGoogle ScholarPubMed
Nielsen, M. K., Haaning, N. and Olsen, S. N. (2006). Strongyle egg shedding consistency in horses on farms using selective therapy in Denmark. Veterinary Parasitology 135, 333–335.CrossRefGoogle ScholarPubMed
Ogbourne, C. P. (1975). Epidemiological studies on horses infected with nematodes of the family Trichonematidae (Wittenberg, 1925). International Journal for Parasitology 5, 667–672.CrossRefGoogle Scholar
Ogbourne, C. P. (1976). The prevalence, relative abundance and site distribution of nematodes of the subfamily Cyathostominae in horses killed in Britain. Journal of Helminthology 50, 203–224.CrossRefGoogle ScholarPubMed
Pinheiro, J. C. and Bates, D. M. (2000). Mixed-Effects Models in S and S-Plus. Springer-Verlag, New York, USA.CrossRefGoogle Scholar
Proudman, C. J. and Matthews, J. B. (2000). Control of equine intestinal helminths. In Practice 22, 90–97.CrossRefGoogle Scholar
Quinelato, S., Couto, M. C. M., Ribeiro, B. C., Santos, C. N., De Souza, L. S., Dos Anjos, D. H. S., Sampaio, I. B. M. and Rodrigues, L. M. A. (2008). The ecology of horse cyathostomin infective larvae (Nematoda-Cyathostominae) in tropical southeast Brazil. Veterinary Parasitology 153, 100–107.CrossRefGoogle ScholarPubMed
R Core Development Team (2005). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ramsey, Y. H., Christley, R. M., Matthews, J. B., Hodgkinson, J. E., McGoldrick, J. and Love, S. (2004). Seasonal development of Cyathostominae larvae on pasture in a northern temperate region of the United Kingdom. Veterinary Parasitology 119, 307–318.CrossRefGoogle Scholar
Reid, S. W., Mair, T. S., Hillyer, M. H. and Love, S. (1995). Epidemiological risk factors associated with a diagnosis of clinical cyathostomiasis in the horse. Equine Veterinary Journal 27, 127–130.CrossRefGoogle ScholarPubMed
Santos, C. N., De Souza, L. S., Quinelato, S. B., Do Couto, M. C. M., Pinheiro, J. and Rodrigues, M. L. D. (2011). Seasonal dynamics of cyathostomin (Nematoda – Cyathostominae) infective larvae in Brachiaria humidicola grass in tropical southeast Brazil. Veterinary Parasitology 180, 274–278.CrossRefGoogle ScholarPubMed
von Samson-Himmelstjerna, G., Fritzen, B., Demeler, J., Schürmann, S., Rohn, K., Schnieder, T. and Epe, C. (2007). Cases of reduced cyathostomin egg-reappearance period and failure of Parascaris equorum egg count reduction following ivermectin treatment as well as survey on pyrantel efficacy on German horse farms. Veterinary Parasitology 144, 74–80.CrossRefGoogle ScholarPubMed
von Samson-Himmelstjerna, G., Traversa, D., Demeler, J., Rohn, K., Milillo, P., Schurmann, S., Lia, R., Perrucci, S., Di Regalbono, A. F., Beraldo, P., Barnes, H., Cobb, R. and Boeckh, A. (2009). Effects of worm control practices examined by a combined faecal egg count and questionnaire survey on horse farms in Germany, Italy and the UK. Parasites & Vectors 2 (Suppl 2), S3.CrossRefGoogle ScholarPubMed
Wilson, A. J. (2008). Why h2 does not always equal VA/VP? Journal of Evolutionary Biology 21, 647–650.CrossRefGoogle ScholarPubMed
Wollack, M. E., Fairbairn, D. J. and Paulsen, Y. R. (2012). Guidelines for estimating repeatability. Methods in Ecology and Evolution 3, 129–137.CrossRefGoogle Scholar
Wood, S. N. (2006). Generalized Additive Models: An Introduction With R. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. Springer, New York, USA.CrossRefGoogle Scholar