Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-25T23:56:42.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Survival and development of chicken ascarid eggs in temperate pastures

Published online by Cambridge University Press:  09 May 2017

SUNDAR THAPA ,
STIG M. THAMSBORG ,
NICOLAI V. MEYLING ,
SURAJ DHAKAL  and
HELENA MEJER
SUNDAR THAPA*
Affiliation:
Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, Section for Parasitology and Aquatic Diseases, University of Copenhagen, Dyrlægevej 100, 1870 Frederiksberg C, Denmark
STIG M. THAMSBORG
Affiliation:
Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, Section for Parasitology and Aquatic Diseases, University of Copenhagen, Dyrlægevej 100, 1870 Frederiksberg C, Denmark
NICOLAI V. MEYLING
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, Section for Organismal Biology, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
SURAJ DHAKAL
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, Section for Organismal Biology, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
HELENA MEJER
Affiliation:
Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, Section for Parasitology and Aquatic Diseases, University of Copenhagen, Dyrlægevej 100, 1870 Frederiksberg C, Denmark
*
*Corresponding author: Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, Section for Parasitology and Aquatic Diseases, University of Copenhagen, Dyrlægevej 100, 1870 Frederiksberg C, Denmark. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Eggs of chicken ascarids (Ascaridia galli and Heterakis spp.) are believed to be hardy and survive for long periods. However, this has not been evaluated quantitatively and our study therefore aimed to determine development and recovery of chicken ascarid eggs after burying in pasture soil. Unembryonated eggs were mixed with soil, placed in sealed nylon bags and buried at 7 cm depth in pasture plots April (spring, n = 72) and December 2014 (winter, n = 72). Eight randomly selected bags per season were used to estimate pre-burial egg recovery [0 week post-burial (wpb)]. Eight random bags were removed at 5, 12, 23, 38, 52, 71 wpb per season and additionally at 104 wpb for spring burial. The content of each bag was analysed for numbers and development stages of eggs. Eggs buried in spring were fully embryonated within 12 wpb. In contrast, eggs buried in winter were developing between 23 and 38 wpb, so that all viable eggs seemed to be fully developed by 38 wpb. About 90% eggs disappeared within 23 wpb (spring) and 38 wpb (winter). Small proportions (2–3%) of seemingly viable and infective eggs were still recovered up to 2 years after deposition. In conclusion, most eggs buried in temperate pasture soil seem to experience a heavy mortality within a few months after the deposition, especially during warm periods. However, a small proportion of eggs may survive and remain infective for at least 2 years.

Keywords

Ascaridia galliHeterakisseasonegg mortality
Type
Research Article
Information
Parasitology , Volume 144 , Issue 9 , August 2017 , pp. 1243 - 1252
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

Ackert, J. E. (1931). The morphology and life history of the fowl nematode Ascaridia lineata (Schneider). Parasitology 23, 360–379.Google Scholar
Ackert, J. E. and Cauthen, G. E. (1931). Viability of the eggs of the fowl nematode Ascaridia lineata (Schneider) exposed to natural climatic Factors. Journal of Parasitology 18, 113–134.Google Scholar
Anonymous (1999). Council directive 1999/74/EC of 19 July 1999, laying down minimum standards for the protection of laying hens. Official Journal of the European Communities L 203/53, 1–5.Google Scholar
Anonymous (2008). Commission regulation (EC) No 889/2008 of 5 September 2008, laying down detailed rules for the implementation of council regulation (EC) No 834/2007 on organic production and labelling of organic products with regard to organic production, labelling and c. Official Journal of the European Union L 250, 1–84.Google Scholar
Anonymous (2012). Bekendtgørelse om økologisk jordbrugsproduktion m.v. BEK nr 716 af 27/06/2012 (In English: Act on organic agricultural production). NaturErhvervstyrelsen, nr.: 12-0117-000001, Fødevaremin, Denmark.Google Scholar
Anonymous (2015). Det Danske Fjerkræraad Årsberetning 2015 (In English: The Danish Poultry Council Annual Report 2015).Google Scholar
Bestman, M. and Wagenaar, J. P. (2014). Health and welfare in Dutch organic laying hens. Animals 4, 374–390.Google Scholar
Brownell, S. A. and Nelson, K. L. (2006). Inactivation of single-celled Ascaris suum eggs by low-pressure UV radiation. Applied and Environmental Microbiology 72, 2178–2184.CrossRefGoogle ScholarPubMed
Burden, D. J. and Hammet, N. C. (1979). The development and survival of Trichuris suis ova on pasture plots in the south of England. Research in Veterinary Science 26, 66–70.CrossRefGoogle ScholarPubMed
Chadfield, M., Permin, A., Nansen, P. and Bisgaard, M. (2001). Investigation of the parasitic nematode Ascaridia galli (Shrank 1788) as a potential vector for Salmonella enterica dissemination in poultry. Parasitology Research 87, 317–325.Google Scholar
Chen, J., Moore, W. H., Yuen, G. Y., Kobayashi, D. and Caswell-Chen, E. P. (2006). Influence of Lysobacter enzymogenes strain C3 on nematodes. Journal of Nematology 38, 233–239.Google Scholar
Christenson, R. O., Earle, H. H., Butler, R. L. and Creel, H. H. (1942). Studies on the eggs of Ascaridia galli and Heterakis gallinae . Transactions of the American Microscopical Society 61, 191.CrossRefGoogle Scholar
Dubinský, P. (1969). Durch ultraviolettstrahlung induzierte morphologische veränderungen der eier von Ascaridia galli und Heterakis gallinarum . Biologia, Bratislava 24, 595–600.Google Scholar
Elliott, A. (1954). Relationship of aging of larvae, food reserves, and infectivity of Ascaridia galli . Experimental Parasitology 3, 307–320.CrossRefGoogle ScholarPubMed
Farr, M. M. (1956). Survival of the protozoan parasite, Histomonas meleagridis, in feces of infected birds. Cornell Veterinarian 46, 178–187.Google Scholar
Farr, M. M. (1961). Further observations on the survival of the protozoan parasite, Histomonas meleagridis and eggs of poultry nematdoes in feces of infected birds. Cornell Veterinarian 51, 3–13.Google Scholar
Gaasenbeek, C. P. H. and Borgsteede, F. H. M. (1998). Studies on the survival of Ascaris suum eggs under laboratory and simulated field conditions. Veterinary Parasitology 75, 227–234.Google Scholar
Gauly, M., Duss, C. and Erhardt, G. (2007). Influence of Ascaridia galli infections and anthelmintic treatments on the behaviour and social ranks of laying hens (Gallus gallus domesticus). Veterinary Parasitology 146, 271–280.CrossRefGoogle ScholarPubMed
Geenen, P. L., Bresciani, J., Boes, J., Pedersen, A., Eriksen, L., Fagerholm, H. P. and Nansen, P. (1999). The morphogenesis of Ascaris suum to the infective third-stage larvae within the egg. Journal of Parasitology 85, 616–622.Google Scholar
Hermansen, J. E., Munkholm, L., Bruus, M., Eriksen, J., Poulsen, H. D., Kronvang, B., Bak, J. L., Dalgaard, T., Kristensen, H. L., Rasmussen, A., Adamsen, A. P., Hansen, B., Brüsch, W., Thorling, L., Magid, J., Rasmussen, S. K. and Jensen, L. S. (2015). Miljø. In Økologiens bidrag til samfundsgoder – Vidensyntese 2015 (ed. Lizzie Melby Jespersen), pp. 107–167. Internationalt Center for Forskning i Økologisk Jordbrug og Fødevaresystemer (ICROFS), Denmark.Google Scholar
Hinrichsen, L. K., Riber, A. B. and Labouriau, R. (2016). Associations between and development of welfare indicators in organic layers. Animal 10, 953–960.CrossRefGoogle ScholarPubMed
Ihler, C. F. (1995). The distribution of Parascaris equorum eggs in the soil profile of bare paddocks in some Norwegian studs. Veterinary Research Communications 19, 495–501.Google Scholar
Ikeme, M. M. (1971). Observations on the pathogenecity and pathology of Ascaridia galli . Parasitology 63, 169–179.Google Scholar
Jansson, D. S., Nyman, A., Vågsholm, I., Christensson, D., Göransson, M., Fossum, O. and Höglund, J. (2010). Ascarid infections in laying hens kept in different housing systems. Avian Pathology 39, 525–532.Google Scholar
Jasoski, B. J. (1954). A comparative study of detergent effects on ascarid development. The American Midland Naturalist 52, 142–148.Google Scholar
Katakam, K. K., Mejer, H., Dalsgaard, A., Kyvsgaard, N. C. and Thamsborg, S. M. (2014). Survival of Ascaris suum and Ascaridia galli eggs in liquid manure at different ammonia concentrations and temperatures. Veterinary Parasitology 204, 249–257.Google Scholar
Katakam, K. K., Thamsborg, S. M., Dalsgaard, A., Kyvsgaard, N. C. and Mejer, H. (2016). Environmental contamination and transmission of Ascaris suum in Danish organic pig farms. Parasites & Vectors 9, 80.CrossRefGoogle ScholarPubMed
Kates, K. C. and Colglazier, M. L. (1970). Differential morphology of adult Ascaridia galli (Schrank, 1788) and Ascaridia dissimilis Perez Vigueras, 1931. Proceedings of the Helminthological Society of Washington 37, 80–84.Google Scholar
Kaufmann, F., Daş, G., Sohnrey, B. and Gauly, M. (2011). Helminth infections in laying hens kept in organic free range systems in Germany. Livestock Science 141, 182–187.CrossRefGoogle Scholar
Khan, A., Williams, K. L. and Nevalainen, H. K. M. (2004). Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biological Control 31, 346–352.Google Scholar
Kraglund, H.-O. R. (1999). Survival, development and dispersal of the free-living stages of Ascaris suum, Oesophagostomum dentatum and Trichuris suis at the pasture. Ph.D. thesis. The Royal Veterinary and Agricultural University, Denmark.Google Scholar
Kraglund, H.-O. R., Grønvold, J., Roepstorff, A. and Rawat, H. (1998). Interactions between the nematode parasite of pigs, Ascaris suum, and the earthworm Aporrectodea longa . Acta Veterinaria Scandinavica 39, 453–460.Google Scholar
Lapage, G. (1956). Veterinary Parasitology, 1st Edn. Oliver and Boyd, London.Google Scholar
Larsen, M. N. and Roepstorff, A. (1999). Seasonal variation in development and survival of Ascaris suum and Trichuris suis eggs on pastures. Parasitology 119, 209–220.Google Scholar
Lee, D. L. and Lešťan, P. (1971). Oogenesis and egg shell formation in Heterakis gallinarum (Nematoda). Journal of Zoology 164, 189–196.CrossRefGoogle Scholar
Levine, P. P. (1937). The viability of the ova of Ascaridia lineata when exposed to various environmental conditions. Journal of Parasitology 23, 368–375.Google Scholar
Madsen, H. (1962). On the interaction between Heterakis gallinarum, Ascaridia galli, “Blackhead” and the chicken. Journal of Hehelminthology 36, 107–142.Google Scholar
McDougald, L. R. (2005). Blackhead disease (histomoniasis) in poultry: a critical review. Avian diseases 49, 462–476.Google Scholar
Padgham, J. L. and Sikora, R. A. (2007). Biological control potential and modes of action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop Protection 26, 971–977.Google Scholar
Pankavich, J. A., Emro, J. E., Poeschel, G. P. and Richard, G. A. (1974). Observations on the life history of Ascaridia dissimilis (Perez Vigueras, 1931) and its relationship to Ascaridia galli (Schrank, 1788). The Journal of Parasitology 60, 963–971.Google Scholar
Permin, A., Bisgaard, M., Frandsen, F., Pearman, M., Kold, J. and Nansen, P. (1999). Prevalence of gastrointestinal helminths in different poultry production systems. British Poultry Science 40, 439–443.CrossRefGoogle ScholarPubMed
Phiri, I. K., Phiri, A. M., Ziela, M., Chota, A., Masuku, M. and Monrad, J. (2007). Prevalence and distribution of gastrointestinal helminths and their effects on weight gain in free-range chickens in Central Zambia. Tropical Animal Health and Production 39, 309–315.Google Scholar
Reid, W. M. (1960). Effects of temperature on the development of the eggs of Ascaridia galli . The Journal of Parasitology 46, 63–67.Google Scholar
Saunders, L. M., Tompkins, D. M. and Hudson, P. J. (2000). The role of oxygen availability in the embryonation of Heterakis gallinarum eggs. International Journal for Parasitology 30, 1481–1485.Google Scholar
Schwarz, A., Gauly, M., Abel, H., Daş, G., Humburg, J., Rohn, K., Breves, G. and Rautenschlein, S. (2011 a). Immunopathogenesis of Ascaridia galli infection in layer chicken. Developmental and Comparative Immunology 35, 774–784.CrossRefGoogle ScholarPubMed
Schwarz, A., Gauly, M., Abel, H., Daş, G., Humburg, J., Weiss, A. T. A., Breves, G. and Rautenschlein, S. (2011 b). Pathobiology of Heterakis gallinarum mono-infection and co-infection with Histomonas meleagridis in layer chickens. Avian Pathology 40, 277–287.Google Scholar
Skallerup, P., Luna, L. A., Johansen, M. V. and Kyvsgaard, N. C. (2005). The impact of natural helminth infections and supplementary protein on growth performance of free-range chickens on smallholder farms in El Sauce, Nicaragua. Preventive Veterinary Medicine 69, 229–244.Google Scholar
Stein, K. K. and Golden, A. (2015). The C. elegans eggshell. In WormBook, pp. 1–35.Google Scholar
Storey, G. W. and Phillips, R. A. (1985). The survival of parasite eggs throughout the soil profile. Parasitology 91, 585–590.Google Scholar
Sutherland, I. A. and Leathwick, D. M. (2011). Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends in Parasitology 27, 176–181.CrossRefGoogle ScholarPubMed
Tarbiat, B., Jansson, D. S. and Höglund, J. (2015). Environmental tolerance of free-living stages of the poultry roundworm Ascaridia galli . Veterinary Parasitology 209, 101–107.Google Scholar
Thamsborg, S. M., Roepstorff, A. and Larsen, M. (1999). Integrated and biological control of parasites in organic and conventional production systems. Veterinary Parasitology 84, 169–186.Google Scholar
Thapa, S., Hinrichsen, L. K., Brenninkmeyer, C., Gunnarsson, S., Heerkens, J. L. T., Verwer, C., Niebuhr, K., Willett, A., Grilli, G., Thamsborg, S. M., Sørensen, J. T. and Mejer, H. (2015 a). Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 214, 118–124.CrossRefGoogle ScholarPubMed
Thapa, S., Meyling, N. V., Katakam, K. K., Thamsborg, S. M. and Mejer, H. (2015 b). A method to evaluate relative ovicidal effects of soil microfungi on thick-shelled eggs of animal-parasitic nematodes. Biocontrol Science and Technology 25, 756–767.Google Scholar
Thapa, S., Mejer, H., Thamsborg, S. M., Jensen, B. and Meyling, N. V. (2015 c). Can chitinolytic microfungi be used to reduce the number of chicken ascarid eggs in soil? In 25th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP), Liverpool, London.Google Scholar
Velichkin, P. A. and Merkulov, E. V. (1970). Persistence of ascarid eggs in poultry houses and runs. Veterinarija Moskva 1, 35–36.Google Scholar
Wall, H., Jeremiasson, A., Jeremiasson, M., Odelros, Å., Eriksson, H. and Jansson, D. S. (2016). Svensk äggnäring efter omställningen, del 1 Inhysning och aktuella trender (In English: Egg production in Sweden after the change to alternative housing systems, part 1. Housing of laying hens and current trends). Svenskveterinartidning 10, 11–18.Google Scholar
Wharton, D. A. (1979). Ascaris Sp.: water loss during desiccation of embryonating eggs. Experimental Parasitology 48, 398–406.CrossRefGoogle ScholarPubMed
Wharton, D. (1980). Nematode egg-shells. Parasitology 81, 447.Google Scholar
Williams, D. L., Pepper, I. L. and Gerba, C. P. (2012). Survival of Ascaris ova in desert soils: a risk assessment. Journal of Residuals Science & Technology 9, 151–157.Google Scholar
Windhorst, H.-W. (2005). Development of organic egg production and marketing in the EU. World's Poultry Science Journal 61, 451–462.Google Scholar