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Avoiding bias in parasite excretion estimates: the effect of sampling time and type of faeces

  • D. VILLANÚA (a1), L. PÉREZ-RODRÍGUEZ (a1), C. GORTÁZAR (a1), U. HÖFLE (a2) and J. VIÑUELA (a1)...

The study of host-parasite relationships usually requires reliable estimates of parasite intensity, which is often estimated from parasite propagule concentration in faeces. However, parasite excretion in faeces may be subject to variation due to endogenous or exogenous factors that must be identified to obtain reliable results. We analysed the effect of the hour of sample collection on propagule counts of 2 intestinal parasites infecting the red-legged partridge: the capillarid nematode Aonchoteca caudinflata and coccidia of the genus Eimeria (Protozoa). Also, we test whether there are differences in propagule counts between caecal and intestinal faeces. Individual faecal samples from infected birds were collected daily at 4 different hours during several days. The hour of the day exerted a very strong effect on propagule counts, excretion of both types of parasites showing a clear and constant increase from dawn to dusk. Also, capillarid eggs were more abundant in intestinal than in caecal faeces, whereas the inverse pattern was found for coccidian oocysts. Standardization of the hour of sample collection or statistical control of this variable is recommendable to prevent bias. Similarly, in bird species with long caeca, consistent collection of one type of faeces may avoid significant errors in parasite burden estimates.

Corresponding author
Instituto de Investigación en Recursos Cinegéticos (IREC, CSIC-UCLM-JCCM) Ronda de Toledo s/n, 13071 Ciudad Real, Spain. Tel: +0034 926295450. Fax: +0034 926295451. E-mail:
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Albon, S. D., Stien, A., Irvine, R. J., Ropstad, R. and Halvorsen, O. ( 2002). The role of parasites in the dynamic of a reindeer population. Proceedings of the Royal Society of London, B 269, 16251632.
Anderson, R. C. ( 2000). Nematode Parasites of the Vertebrates: their Development and Transmission, 2nd Edn. CAB International, Wallingford, UK.
Anderson, R. M. and Schad, G. A. ( 1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812825.
Besedovsky, H. O. and del Rey, A. ( 1996). Immune-neuro-endocrine interactions: facts and hypotheses. Endocrine reviews 17, 6469.
Boughton, D. C. ( 1933). Diurnal gametic periodicity in avian Isospora. American Journal of Hygiene 18, 161184.
Brawner, W. R. III and Hill, G. E. ( 1999). Temporal variation in shedding of coccidian oocysts: implications for sexual-selection studies. Canadian Journal of Zoology 77, 347350.
Buchholz, R. ( 1995). Female choice, parasite load and ornamentation in wild turkeys. Animal Behaviour 50, 384387.
Clarke, P. L. ( 1979). Coccidial infection with Eimeria tenella and caecal defaecation in chicks. British Poultry Science 20, 317332.
Clayton, D. L. and Moore, J. ( 1997). Host-Parasite Evolution: General Principles and Avian Models. Oxford University Press, Oxford, UK.
Cordero del Campillo, M. and Rojo, F. A. ( 1999). Parasitología Veterinaria. McGraw-Hill-Interamericana, Madrid, Spain.
Delahay, R. J., Speakman, J. R. and Moss, R. ( 1995). The energetic consequences of parasitism: effect of a developing infection of Trichostrongylus tennuis on Red Grouse (Lagopus lagopus scoticus) energy balance, body weight and condition. Parasitology 110, 473482.
Giver, H., de Vlas, S. J., Johansen, M. V., Christensen, N. O. and Nansen, P. ( 2000). Schistosoma japonicum: day-to-day variation in excretion and hatchability of parasite eggs in the domestic pig, Suis suis. Experimental Parasitology 95, 818.
Gordon, H. Mc. and Whitlock, H. V. ( 1939). A new technique for counting nematode eggs in sheep faeces. Journal of the Council for Scientific and Industrial Research (Australia) 12, 5052.
Graat, E. A., Henken, A. M., Ploeger, H. W., Noordhuizen, J. P. and Vertommen, M. H. ( 1994). Rate and course of sporulation of oocysts of Eimeria acervulina under different environmental conditions. Parasitology 108, 497502.
Gulland, F. M. D. ( 1995). Impact of infectious diseases on wild animals. In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. and Dobson, A. P.), pp. 2051. Cambridge University Press, Cambridge, UK.
Guyatt, H. L. and Bundy, D. A. P. ( 1993). Estimation of intestinal nematode prevalence: influence of parasite mating patterns. Parasitology 107, 99106.
Hall, A. ( 1985). Nutritional aspects of parasitic infection. Progress in Food and Nutrition Science 9, 227256.
Hillgarth, N. ( 1990). Parasites and female choice in the ring-necked pheasant. American Zoologist 30, 227233.
Holmes, J. C. ( 1982). Impact of infectious disease agents in the population growth and geographical distribution of animals. In Population Biology of Infectious Diseases ( ed. Anderson, R. M. and May, R. M.), pp. 3751. Springer-Verlag, Berlin, Germany.
Hudman, S. P., Ketterson, E. D. and Val Nolan, Jr ( 2000). Effects of time of sampling on oocyst detection and effects of age and experimentally elevated testosterone on prevalence of coccidia in male dark-eyed juncos. Auk 117, 10481051.
Hudson, P. J., Dobson, A. P. and Newborn, B. ( 1998). Prevention of population cycles by parasite removal. Science 282, 22562258.
Kumba, F. F., Katjivena, H., Kauta, G. and Lutaaya, E. ( 2003). Seasonal evolution of faecal egg output by gastrointestinal worms in goats on communal farms in eastern Namibia. The Onderstepoort Journal of Veterinary Research 70, 265271.
McKenzie, M. E., Colnago, G. L., Lee, S. R. and Long, P. L. ( 1987). Gut stasis in chickens infected with Eimeria. Poultry Science 66, 264269.
McLennan, D. A. and Brooks, D. R. ( 1991). Parasites and sexual selection: a macroevolutionary perspective. The Quarterly Review of Biology 66, 255286.
Mehlhorn, H., Düwell, D. and Raether, W. ( 1992). Atlas de Parasitología Veterinaria. GRASS, Madrid, Spain.
Misof, K. ( 2004). Diurnal cycle of Isospora spp. oocyst shedding in Eurasian blackbirds (Turdus merula). Canadian Journal of Zoology 82, 764768.
Murray, D. L. ( 2002). Differential body condition and vulnerability to predation of snowshoe hares. Journal of Animal Ecology 71, 614625.
Murray, D. L., Cary, J. R. and Keith, L. B. ( 1997). Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology 66, 250264.
Newey, S. and Thirgood, S. ( 2004). Parasite-mediated reduction in fecundity of mountain hares. Proceedings of the Royal Society of London, B 271, 413415.
Rickard, L. G. and Zimmerman, G. L. ( 1992). The epizootiology of gastrointestinal nematodes of sheep, cattle and deer. Journal of Helminthology 69, 357362.
Ruiz de Ybáñez, M. R., Goyena, M., Abaigar, T., Garito, M. M., Martínez-Carrasco, C., Espeso, G., Cano, M. and Ortiz, J. M. ( 2004). Periparturient increase in faecal egg counts in a captive population of mohor Gazella (Gazella dama mhorr). Veterinary Record 154, 4952.
Sapolsky, R. M. ( 1992). Neuroendrocrinology of the stress response. In Behavioural Endocrinology ( ed. Becker, J. B., Breedlove, S. M. and Crews, D.), pp. 287324. MIT Press, Cambridge, UK.
Seivwright, L. J., Redpath, S. M., Mougeot, F., Watt, L. and Hudson, P. J. ( 2004). Faecal egg counts provide reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. Journal of Helminthology 78, 6976.
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, 253258.
Skryabin, K. I. ( 1991). Key to Parasitic Nematodes. E. J. Brill Publishing Company. New Delhi.
Theodoropoulos, G., Koutsotolis, K., Nikolaou, E., Kalogiannis, D. and Petrakos, G. ( 1998). Seasonal variations of gastrointestinal nematodes of sheep in the region of Joannina, Greece. International Journal for Parasitology 28, 12871292.
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, 417423.
Tompkins, D. M., Dobson, A. P., Arneberg, P., Begon, M. E., Cattadori, I. M., Greenman, J. V., Heesterbeek, H., Hudson, P. J., Newborn, B., Pugliese, A., Rizzoli, A. P., Rosa, R., Rosso, F. and Wilson, K. ( 2001). Parasites and Host Population Dynamics. Oxford University Press, Oxford, UK.
Vicente, J., Fierro, Y. and Gortázar, C. ( 2005). Seasonal dynamics of the fecal excretion of Elaphostrongylus cervi (Nematoda, Metastrongyloidea) first-stage larvae in Iberian red deer (Cervus elaphus hispanicus) from southern Spain. Parasitology Research 95, 6064.
Villanúa, D., Acevedo, P., Höfle, U., Rodríguez, O. and Gortázar, C. ( 2006). Changes in transmission stage excretion after pheasant release. Journal of Helminthology (in the Press).
Vorísek, P., Votýpka, J., Zvára, K. and Svobodova, M. ( 1998). Heteroxenous coccidia increase the predation risk of parasited rodents. Parasitology 117, 521524.
Welch, D. A., Pybus, M. J., Samuel, W. M. and Wilke, C. J. ( 1991). Reliability of fecal examination for detecting infections of meningeal worm in elk. Wildlife Society Bulletin 19, 326331.
Whitford, W. G., Forbes, G. S. and Kerley, G. I. ( 1995). Diversity, spatial variability, and functional roles of invertebrates in desert grassland ecosystems. In The Desert Grassland ( ed. McClaran, M. P. and Van Devender, T. R.), pp. 152190. Arizona Press, Tuscon, USA.
Yu, J. M., de Vlas, S. J., Yuan, H. C. and Gryseels, B. ( 1998). Variations in fecal Schistosoma japonicum eggs counts. The American Journal of Tropical Medicine and Hygiene 59, 370375.
Zuk, M. ( 1992) The role of parasites in sexual selection: current evidence and future directions. Advances in the Study of Behaviour 21, 3968.
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