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Diurnal variation in egg excretion by Heterakis gallinarum

Published online by Cambridge University Press:  06 July 2018

Gürbüz Daş Open the ORCID record for Gürbüz Daş [Opens in a new window] ,
Pål O. Westermark  and
Matthias Gauly
Gürbüz Daş*
Affiliation:
Institute of Nutritional Physiology ‘Oskar Kellner’, Leibniz Institute for Farm Animal Biology, 18196, Dummerstorf, Germany
Pål O. Westermark
Affiliation:
Bioinformatics and Biomathematics Unit, Institute of Genetics and Biometry, Leibniz Institute for Farm Animal Biology, 18196 Dummerstorf, Germany
Matthias Gauly
Affiliation:
Faculty of Science and Technology, Free University of Bozen-Bolzano, Piazza Domenicani 3, 39100 Bolzano, Italy
*
Author for correspondence: Gürbüz Daş, E-mail: [email protected]
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Abstract

Periodicity in nematode egg excretion may be of evolutionary origin as it can favour dispersal of the eggs in the environment. We investigated whether egg excretion by Heterakis gallinarum shows a repeatable pattern of periodicity. The faecal egg concentration and total number of eggs excreted within 4-h intervals were significantly affected by the sampling time within 1 day, but remained unaffected by the sampling day or interaction effects. By contrast, the total number of eggs excreted within 24 h did not differ among the 4 days of the study, collectively indicating repeatable egg excretion patterns. Both host feces and parasite egg excretion increased from night to late afternoon, followed by a decrease in the evening, resulting in higher egg excretion during daytime than the dark period. Feces excretion and worm fecundity showed overlapping diurnal rhythms with similarly timed phases, suggesting the existence of synchronicity between the host feces and nematode egg excretion patterns. We conclude that egg excretion by H. gallinarum is synchronized with host feces excretion and is higher during the daytime than during the dark period. This overlaps with the maximum activity of the day-active host and allows a maximal dispersal of the eggs in the environment.

Keywords

Diurnalhelminthhostnematodeperiodicity
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 206 - 212
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Copyright
Copyright © Cambridge University Press 2018 

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References

Anonymous (2014) Sunrise and sunset in Goettingen, Germany. Available at https://www.timeanddate.com/sun/germany/gottingen?month=5&year=2013 (Accessed 7 May 2018).Google Scholar
Clarke, PL (1979) Coccidial infection with Eimeria tenella and caecal defaecation in chicks. British Poultry Science 20, 317–322.Google Scholar
Clench, HM and Mathias, JR (1995) The avian cecum: a review. The Wilson Bulletin 107, 93–121.Google Scholar
Coelho, CD, Berto, BP, Neves, DM, Oliveira, VM, Flausino, W and Lopes, CW (2013) Oocyst shedding by green-winged-saltator (Saltator similis) in the diagnostic of coccidiosis and Isospora similisi n. sp. (Apicomplexa: Eimeriidae). Brazilian Journal of Veterinary Parasitology 22, 64–70.Google Scholar
Cringoli, G, Rinaldi, L, Maurelli, MP and Utzinger, J (2010) FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503–515.Google Scholar
Daş, G and Gauly, M (2014) Density related effects on lifetime fecundity of Heterakis gallinarum in chickens. Parasites & Vectors 7, 334.Google Scholar
Daş, G, Abel, H, Humburg, J, Schwarz, A, Rautenschlein, S, Breves, G and Gauly, M (2011 a) Non-starch polysaccharides alter interactions between Heterakis gallinarum and Histomonas meleagridis. Veterinary Parasitology 176, 208–216.Google Scholar
Daş, G, Savas, T, Kaufmann, F, Idris, A, Abel, H and Gauly, M (2011 b) Precision, repeatability and representative ability of faecal egg counts in Heterakis gallinarum infected chickens. Veterinary Parasitology 183, 87–94.Google Scholar
Daş, G, Abel, H, Rautenschlein, S, Humburg, J, Schwarz, A, Breves, G and Gauly, M (2011 c) Effects of dietary non-starch polysaccharides on establishment and fecundity of Heterakis gallinarum in grower layers. Veterinary Parasitology 178, 121–128.Google Scholar
Daş, G, Abel, H, Savaş, T, Sohnrey, B and Gauly, M (2014) Egg production dynamics and fecundity of Heterakis gallinarum residing in different caecal environments induced by fibre-rich diets. Veterinary Parasitology 205, 606–618.Google Scholar
Dolnik, OV, Metzger, BJ and Maarten, JJEL (2011) Keeping the clock set under the midnight sun: diurnal periodicity and synchrony of avian Isospora parasites cycle in the High Arctic. Parasitology 138, 1077–1081.Google Scholar
Ekesbo, I (2011) Farm Animal Behaviour: Characteristics for Assessment of Health and Welfare. Cambridge, UK: Cambridge University Press.Google Scholar
Engels, D, Sinzinkayo, E and Gryseels, B (1996) Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implication. The American Journal of Tropical Medicine and Hygiene 54, 379–324.Google Scholar
Giver, H, de Vlas, SJ, Johansen, MV, Christensen, NO 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, 8–18.Google Scholar
Katakam, KK, Thamsborg, SM, Kyvsgaard, NC, Dalsgaard, A and Mejer, H (2014) Development and survival of Ascaris suum eggs in deep litter of pigs. Parasitology 141, 1646–1656.Google Scholar
Kaufmann, J (1996) Parasitic Infections of Domestic Animals: A Diagnostic Manual. Berlin, Germany: Birkhäuser Verlag (pp. 423; pp. ref.357–358).Google Scholar
Kennedy, CR (1976) Reproduction and dispersal. In Kennedy, CR (ed.) Ecological Aspects of Parasitology. Amsterdam, The Netherlands: North-Holland Publishing Company, pp. 143–160.Google Scholar
McDougald, LR (2005) Blackhead disease (Histomoniasis) in poultry: a critical review. Avian Diseases 49, 462–476.Google Scholar
Misof, K (2004) Diurnal cycle of Isospora spp. oocyst shedding in Eurasian blackbirds (Turdus merula). Canadian Journal of Zoology 82, 764–768.Google Scholar
Morin-Adeline, V, Vogelnest, L, Dhand, NK, Shiels, M, Angus, W and Šlapeta, J (2011) Afternoon shedding of a new species of Isospora (Apicomplexa) in the endangered Regent Honeyeater (Xanthomyza phrygia). Parasitology 138, 713–724.Google Scholar
Nadler, SA, Carreno, RA, Mejía-Madrid, H, Ullberg, J, Pagan, C, Houston, R and Hugot, JP (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134, 1421–1442.Google Scholar
Oikawa, H and Kawaguchi, H (1974) Effect of coccidial infection on acetylcholine-induced contraction of the digestive tract in chickens. I. Eimeria tenella and E. acervulina infection. Japanese Journal of Veterinary Science 36, 433–440.Google Scholar
Oju, JPE and Mpoame, M (2006) Periodic release of gastrointestinal helminth eggs in native chickens from Dschang in the western highlands of Cameroon. Veterinary Research Communications 30, 39–43.Google Scholar
Platt, TR, Hussey, GL and Zelmer, DA (2013) Circadian egg production by Echinostoma caproni (Digenea: echinostomatidae) in ICR mice. Journal of Parasitology 99,179–182.Google Scholar
SAS Institute Inc (2016) SAS OnlineDoc® Version 9.4, Cary, North Carolina, USA.Google Scholar
Thaben, PF and Westermark, PO (2016) Differential rhythmicity: detecting altered rhythmicity in biological data. Bioinformatics (Oxford, England) 32, 2800–2808.Google Scholar
Thapa, S, Thamsborg, S, Meyling, N, Dhakal, S and Mejer, H (2017) Survival and development of chicken ascarid eggs in temperate pastures. Parasitology 144, 1243–1252.Google Scholar
Villanоúa, D, Pérez-Rodriíguez, L, Gortázar, C, Höfle, U and Viñuela, J (2006) Avoiding bias in parasite excretion estimates: the effect of sampling time and type of faeces. Parasitology 133, 251–259.Google Scholar
Wang, BJ, Gu, XB, Yang, GY, Wang, T, Lai, WM, Zhong, ZJ and Liu, GH (2016) Mitochondrial genomes of Heterakis gallinae and Heterakis beramporia support that they belong to the infraorder Ascaridomorpha. Infection, Genetics and Evolution 40, 228–235.Google Scholar
Wongrak, K, Gauly, M and Das, G (2015) Diurnal fluctuations in nematode egg excretion in naturally and experimentally infected chickens. Veterinary Parasitology 208,195–203.Google Scholar
Yazwinski, TA, Chapman, HD, Davis, RB, Letonja, T, Pote, L, Maes, L, Vercruysse, J and Jacobs, DE (2003) World Association for the advancement of veterinary parasitology (W.A.A.V.P.) guidelines for evaluating the effectiveness of anthelmintics in chickens and turkeys. Veterinary Parasitology 116, 159–173.Google Scholar
Yu, JM, de Vlas, SJ, Yuan, HC and Gryseels, B (1998) Variations in fecal Schistosoma japonicum eggs counts. The American Journal of Tropical Medicine and Hygiene 59, 370–375.Google Scholar
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