Comparative morphology and biology of nematodes of genus Heterakis (Nematoda, Heterakidae), parasites of the domestic goose (Anser anser) in Ukraine

Keywords: heterakiasis, Heterakis gallinarum; Heterakis dispar; identification characters; embryogenesis; metrical parameters


The genus Heterakis Dujardin, 1845 is one of the most widely distributed genera of nematode parasites of domestic and wild birds. Geographically and ecologically predominant species include Heterakis gallinarum Schrank, 1788 and Heterakis dispar Schrank, 1790. Prevalence and occurrence of these nematodes in the domestic goose (Anser anser dom.) depend on their biological and morphological specifics which ensure the highest viability, fast growth and maximum fertility in the host. This study presents the abundance and species composition of nematodes of the genus Heterakis in the domestic goose in Ukraine. Comparative study of morphological and metrical characteristics of H. gallinarum and H. dispar adult females and males is presented. Additional morphometric characteristics are proposed for easier identification of the two species. Stages and periods of embryonic development of H. gallinarum and H. dispar nematodes obtained from domestic geese are established according to morphological and metrical characters. Of the two species, H. dispar is prevalent in domestic geese from Poltava, Kharkiv and Kyiv regions. Abundance index of this species is 9.8 specimens, and intensity of infection index is up to 62 specimens. H. gallinarum is rarer, its abundance index is 1.2 specimens and maximum intensity of infection is 30 specimens. Species-specific morphological differences are more distinct in male nematodes in the size and structure of the spicules, lateral wing-like protrusions of pseudobursas, numbers and position of tail papillae. Additional metrical characteristics differ between H. gallinarum and H. dispar nematodes, allowing us to identify not only adult specimens but also eggs. Embryonic development of both species occurs in four morphologically distinct stages: protoplast, blastomere cleavage, formation of first and second stage larvae. Eggs of H. gallinarum nematodes become infectious in eight days at 27 °С, eggs of H. dispar in four days, their viability in laboratory culture is 84.3 ± 0.58 and 91.3 ± 1.53% respectively.


Abou Znada, N. Y. (1993). First record and prevalence of the caecal nematodes, Heterakis gallinarum and Subulura suctoria from the Guinea Fowl, Nume dia meliagris in Saudi Arabia. Journal of King Saud University, 5(1), 59–65.

Al-Moussawi, A. A. (2016). Nematodes of the Turkey Meleagris gallopavo (Gal liformes: Phasianidae) from Al-Nasiryah, Iraq. Journal of Biodiversity and Environmental Sciences, 8(4), 126–131.

Amundson, C. L., Traub, N. J., Smith-Herron, A. J., & Flint, P. L. (2016). Hel minth community structure in two species of arctic-breeding waterfowl para sites and wildlife. International Journal for Parasitology, 5, 263–272.

Avcioglu, H., Burgu, A., & Bölükbaş, C. S. (2008). Ascaridia numidae (Leiper, 1908; Travassos, 1913) in Rock Partridge (Alectoris chukar) in Turkey. Parasitology Research, 102(3), 527–530.

Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T., & Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, 392(6671), 71–75.

Bogach, M. V., & Taranenko, I. L. (2003). Parazytarni hvoroby indykiv fermers' kyh i prysadybnyh gospodarstv Pivdnja Ukrai'ny [Parasitic diseases in tur keys in commercial and household farms of Southern Ukraine]. Ukrainian Black Sea Region Agrarian Science, 21, 311–317 (in Ukrainian).

Bongers, T., & Ferris, H. (1999). Nematode community structure as a bioindicator in environmental monitoring. Тrends in Ecology and Evolution, 14(6), 224–228.

Boone, E. C., Meiners, S. J., & Laursen, J. R. (2017). Gut helminth composition in newly comigrating light geese (lesser snow goose Chen caerulescens caeru lescens and ross’ goose Chen rossii). Comparative Parasitology, 84(1), 36–41.

Brener, B., Tortelly, R., Menezes, R. C., Muniz-Pereira, L. C., & Pinto, R. M. (2006). Prevalence and pathology of the nematode Heterakis gallinarum, the trema tode Paratanaisia bragai, and the protozoan Histomonas meleagridis in the turkey, Meleagris gallopavo. Memórias do Instituto Oswaldo Cruz, 101(6), 677–681.

Castagnone-Sereno, P., & Danchin, E. G. (2014). Parasitic success without sex – the nematode experience. Journal of Evolutionary Biology, 27(7), 1323–1333.

Clapham, P. A. (1933). On the life-history of Heterakis gallinае. Journal of Hel minthology, 11(2), 67–86.

Cordón, G. Р., Prados, A. Н., Romero, D., Moreno, M. S., Pontes, A., Osuna, A., & Rosales, M. J. (2009). Intestinal and haematic parasitism in the birds of the Almuñecar (Granada, Spain) ornithological garden. Veterinary Рarasitology, 165(3–4), 361–366.

Dube, S., Zindi, P., Mbanga, J., & Dube, C. (2010). A study of scavenging poultry gastrointestinal and ecto-parasites in rural areas of Matebeleland province, Zimbabwe. International Journal of Poultry Science, 9(9), 911–915.

Fedynich, A. M., Finger, R. S., Ballard, B. M., Garvon, J. M., & Mayfield, M. J. (2005). Helminths of ross' and greater white-fronted geese wintering in South Texas, U.S.A. Comparative Parasitology, 72(1), 33–38.

Gicik, Y., & Arslan, M. O. (2003). The prevalence of helminths in the alimentary tract of geese (Anser anser domesticus) in Kars District, Turkey. Veterinary Research Communications, 27(5), 391–395.

Harradine, J. (1982). Some mortality patterns of greater magellan geese on the Falkland Islands. Wildfowl, 33, 7–11.

Hildenblat, A. A. (1956). Biologija vozbuditelej ganguleterakidoza gusej Heterakis dispar [Biology of Heterakis dispar, pathogen of ganguleterakido sis in geese]. Collection of Scientific Works of Moscow Veterinary Acade my, 12, 207–213 (in Russian).

Hoque, M. A., Hassan, M. M., Haque, E., Shaikat, A. H., Khan, S. A., Alim, A., Skerratt, L. F., Islam, A., Tun, H. M., Dissanayake, R., Day, T. K., Debnath, N. C., & Yamage, M. (2014). A survey of gastro-intestinal parasitic infection in domestic and wild birds in Chittagong and Greater Sylhet, Bangladesh. Preventive Veterinary Medicine, 117(1), 305–312.

Hoque, M. A., Skerratt, L. F., Rahman, M. A., Alim, M. A., Grace, D., Gummow, B., Rabiul Alam Beg, A. B., & Debnath, N. C. (2011). Monitoring the health and production of household jinding ducks on Hatia Island of Bangladesh. Tropical Animal Health and Production, 43(2), 431–440.

Kaufmann, F., Daş, G., Sohnrey, B., & Gauly, M. (2011). Helminth infections in laying hens kept in organic free range systems in Germany. Livestock Science, 141(2–3), 182–187.

Kornaś, S., Basiaga, M., Kowal, J., Nosal, P., Wierzbowska, I., & Kapkowska, E. (2015). Zatorska goose – a subject of parasitological research. Annals of Parasitology, 61(4), 253–256.

Lok, J. B. (2016). Signaling in parasitic nematodes: Physicochemical communica tion between host and parasite and endogenous molecular transduction pathways governing worm development and survival. Current Clinical Microbiology, 3(4), 186–197.

Madsen, H. (1950). Studies on species of Heterakis (nematodes) in birds. Danish Review of Game Biology, 1(3), 1–43.

Malatji, D. P., Tsotetsi, A. M., van Marle-Koster, E., & Muchadeyi, F. C. (2016). A description of village chicken production systems and prevalence of gast rointestinal parasites: Case studies in Limpopo and KwaZulu-Natal provinces of South Africa. Onderstepoort Journal of Veterinary Research, 83(1), a968.

Menezes, R. C., Mattos, J. D. G., & Tortelly, R. (2001). Freqüência e patologia das infecções causadas por nematóides e cestóides em galinhas-d’angola (Numida meleagris Linnaeus, 1758) criadas extensivamente no estado do Rio de Janeiro, Brasil. Revista Brasileira de Ciência Veterinária, 8, 35–39.

Moore, J., & Simberloff, D. (1990). Gastrointestinal helminth communities of Bobwhite Quail. Ecology, 71(1), 344–359.

Nagwa, E. A., Loubna, M. A., El-Madawy, R. S., & Toulan‏, E. I. (2013). Studies on helminthes of poultry in Gharbia governorate Benha. Veterinary Medical Journal, 25(2), 139–144.

Ogbaje, C. I., Agbo, E. O., & Ajanusi, O. J. (2012). Prevalence of Ascaridia galli, Heterakis gallinarum and tapeworm infections in birds slaughtered in makurdi township. International Journal of Poultry Science, 11(2), 103–107.

Park, S. I., & Shin, S. S. (2010). Concurrent Capillaria and Heterakis infections in zoo rock partridges, Alectoris graeca. Korean Journal of Parasitology, 48(3), 253–257.

Pennycott, T. W., & Steel, F. (2001). Parasitic worms in commercial free-range poultry flocks in England and Wales. Veterinary Record, 149(14), 428.

Phiri, I. K., Phiri, A. M., Ziela, M., Chota, A., Masuku, M., & 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(4), 309–315.

Rahman, W. A., & Manap, N. H. (2014). Descriptions on the morphology of some nematodes of the Malaysian domestic chicken (Gallus domesticus) using scanning electron microscopy. Malaysian Journal of Veterinary Research, 5(1), 35–42.

Roberts, F. H. S. (1937). Studies on the life history and economic importance of Heterakis gallinae (Gmelin, 1790 Freeborn, 1923), the caecum worm of fowls. Australian Journal of Experimental Biology and Medical Science, 15(4), 429–439.

Sheikh, B. A., Ahmad, F., & Sof, T. A. (2016). Morphology and prevalence of some helminth parasites in Gallus domesticus from Gurez Valley of Jammu and Kashmir, India. Journal of Fisheries and Livestock Production, 4(1), 159.

Sherwin, C. M., Nasr, M. A., Gale, E., Petek, M., Stafford, K., Turp, M., & Coles, G. C. (2013). Prevalence of nematode infection and faecal egg counts in free-range laying hens: Relations to housing and husbandry. British Poultry Science, 54(1), 12–23.

Shutler, D., Alisauskas, R. T., & McLaughlin, J. D. (2012). Associations between body composition and helminths of lesser snow geese during winter and spring migration. International Journal for Parasitology, 42(8), 755–760.

Skrjabin, K. I. (1928). Metod polnyh gel'mintologicheskih vskrytij pozvonochnyh, vkljuchaja cheloveka [The method of complete helminthological autopsy of vertebrates, including humans]. Moscow State University, Moscow (in Russian).

Skrjabin, K. I., Shikhobalova, N. P., Lagodovskaya, E. A. (1961). Osnovy nemato dologii: Oksiuratozy zhivotnyh i cheloveka [Essentials of nematodology. Oxy urata of animals and man]. Russian Academy of Sciences, Moscow (in Russian).

Tanveer, S., Ahad, S., & Chishti, M. Z. (2015). Morphological characterization of nematodes of the genera Capillaria, Acuaria, Amidostomum, Streptocara, Heterakis, and Ascaridia isolated from intestine and gizzard of domestic birds from different regions of the temperate Kashmir valley. Journal of Parasitic Diseases, 39(4), 745–760.

Tompkins, D. M., Greenman, J. V., Robertson, P. A., & Hudson, P. J. (2000). The role of shared parasites in the exclusion of wildlife hosts: Heterakis gallina rum in the ring-necked pheasant and the grey partridge. Journal of Animal Ecology, 69(5), 829–840.

Viney, M. (2017). How can we understand the genomic basis of nematode parasitism? Trends in Parasitology, 33(6), 444–452.

Wang, X. Q., Lin, R. Q., Gao, Y., Cheng, T., Zou, S. S., He, Y., Li, G. Y., Weng, Y. B., & Zhu, X. Q. (2012). Prevalence of intestinal helminths in domestic goose (Anser domesticus) in Qingyuan, Guangdong Province, China. Afri can Journal of Microbiology Research, 6(40), 6843–6846.

Wongrak, K., Daş, G., Moors, E., Sohnrey, B., & Gauly, M. (2014). Establish ment of gastro-intestinal helminth infections in free-range chickens: A longi tudinal on farm study. Berliner und Münchener tierärztliche Wochenschrift, 127, 314–321.

Wuthijaree, K., Lambertz, C., & Gauly, M. (2017). Prevalence of gastrointestinal helminth infections in free-range laying hens under mountain farming production conditions. British Poultry Science, 58(6), 649–655.

Zaikina, G. V., & Marshalkina, T. V. (2015). Epizootychna sytuacija shhodo shlun kovo-kyshkovyh invazij sil's'kogospodars'koi' ptyci central'nogo regionnu Ukrainy [Epizootic situation of gastrointestinal invasions of poultry of the central region of Ukraine]. Journal of Veterinary Medicine of Ukraine, 5, 13–15 (in Ukrainian).

How to Cite
Yevstafyeva, V. A., Melnychuk, V. V., NikiforovaО. V., SuprunenkoК. V., Korchan, L. N., Lokes-KrupkaТ. Р., Nehrebetskyi, I. S., & KorchanN. І. (2018). Comparative morphology and biology of nematodes of genus Heterakis (Nematoda, Heterakidae), parasites of the domestic goose (Anser anser) in Ukraine. Regulatory Mechanisms in Biosystems, 9(2), 229-236.