Features of the exogenic development of Passalurus ambiguus (Nematoda, Oxyuroidae) at different temperature regimes
AbstractPassalurosis is a prevalent disease among helminthiases of domestic rabbits. This invasion is caused by the nematode Passalurus ambiguus (Nematoda, Oxyuroidae), which is cosmopolitan and localized in the cecum and colon of rabbits. Passalurosis is highly contagious and capable of unlimited spread, due to the biological characteristics of its pathogen, such as the conditions that ensure maximum preservation of parasites at exogenous stages of their development. Experimental research in the laboratory established the timing of development of P. ambiguus eggs isolated from the gonads of female helminths, depending on temperature regimes and features of their growth and development. According to the morphological features of Passalurus eggs, four stages were distinguished in their exogenous development: zygote, cleavage and formation of blastomeres, formation of larvae and motile larvae. Depending on the cultivation temperature, the duration of embryogenesis ranged from 4 to 9 days, and egg viability ranged from 59.3% to 72.7%. The most favourable temperature regime for the development of P. ambiguus eggs was the temperature of 35 °C, at which 72.7% of eggs with motile larvae were formed within 4 days. At this temperature, the zygote stage lasted for 1 day of cultivation, the stage of cleaving and formation of blastomeres occurred on days 1–2, the stage of larval formation on days 1–3, and the stage of formation of motile larva on days 3–4. At lower temperatures, the term of development of Passalurus eggs increased, and the number of viable eggs decreased. At temperatures of 30 °С and 25 °С, the development of Passalurus eggs took place during 5 and 7 days, respectively, and the viability was 66.7% and 62.7%. At these temperatures, the zygote stage lasted 1–2 and 1–3 days, the stage of cleaving and formation of blastomeres occurred on days 1–3 and 1–4, the stage of larval formation lasted from days 2–4 and 2–6, and the stage of formation of motile larvae took place on days 3–5 and 4–7, respectively. The least favourable temperature for the development of P. ambiguus eggs was the temperature of 20 °С, at which the formation of motile larvae occurred in 9 days, and their viability was only 59.3%. At this temperature, the zygote stage lasted 1–4 days, the stage of cleaving and blastomere formation occurred on days 2–6, and the larval formation stage on days 3–8, and the motile larval stage happened on days 5–9. The growth and development of P. ambiguus eggs was accompanied by significant changes in morphometric parameters, such as the increase in egg width and thinning of egg shell at the egg shell plug. The obtained data will allow preventive measures to be effectively implemented on rabbit farms that are susceptible to pinworms, taking into account the terms of exogenous development of pathogens in different seasons.
Anderson, R. C. (2000). Nematode parasites of vertebrates: Their development and transmission. CABI Publish, Wallingford.
Aripsheva, B. M., Bittirov, A. M., & Kanokova, A. S. (2010). Ekologoepizootologicheskaja kharakteristika oksiuroza loshadej v KabardinoBalkarskoj Respublike [Features of ecology and epizootology of oxyurosis of horses in Kabardino-Balkarian Republic]. Russian Journal of Parazitology, 2, 24–28 (in Russian).
Auld, S. K., & Tinsley, M. C. (2015). The evolutionary ecology of complex lifecycle parasites: Linking phenomena with mechanisms. Heredity, 114(2), 125–132.
Benesh, D. P., Lafferty, K. D., & Kuris, A. (2017). A life cycle database for parasitic acanthocephalans, cestodes, and nematodes. Ecology, 98(3), 882.
Benesh, D. P., Parker, G., & Chubb, J. C. (2021). Life-cycle complexity in helminths: What are the benefits? Evolution, 75(8), 1936–1952.
Beveridge, I., Pullman, A. L., Martin, R. R., & Barelds, A. (1989). Effects of temperature and relative humidity on development and survival of the free-living stages of Trichostrongylus colubriformis, T. rugatus and T. vitrinus. Veterinary Parasitology, 33(2), 143–153.
Blasco-Costa, I., & Poulin, R. (2017). Parasite life-cycle studies: A plea to resurrect an old parasitological tradition. Journal of Helminthology, 91(6), 647–656.
Blaxter, M. L. (2003). Nematoda: Genes, genomes and the evolution of parasitism. Advances in Parasitology, 54, 101–195.
Blaxter, M., & Koutsovoulos, G. (2015). The evolution of parasitism in Nematoda. Parasitology, 142(1), 26–39.
Boag, B., & Iason, G. (1986). The occurrence and abundance of helminth parasites of the mountain hare Lepus timidus (L.) and the wild rabbit Oryctolagus cuniculus (L.) in Aberdeenshire, Scotland. Journal of Helminthology, 60(2), 92–98.
Danheim, B. L., & Ackert, J. E. (1929). On the anatomy of the nematode Passalurus ambiguus (Rudolphi). Transactions of the American Microscopical Society, 48, 80–85.
De Jong, Y., Verbeek, M., Michelsen, V., Bjørn, P. de P., Los, W., Steeman, F., Bailly, N., Basire, C., Chylarecki, P., Stloukal, E., Hagedorn, G., Wetzel, F. T., Glöckler, F., Kroupa, A., Korb, G., Hoffmann, A., Häuser, C., Kohlbecker, A., Müller, A., Güntsch, A., Stoev, P., & Penev, L. (2014). Fauna Europaea – all European animal species on the web. Biodiversity Data Journal, 2, e4034.
Fayek, S. A., El Bahy, N. M., & El Khair, A. (1995). Contributions on the Passalurus ambiguous life cycle and scanning electron microscopy studies. Veterinary Medical Journal, 43(4), 449–453.
Foronda, P., Valladares, B., Lorenzo-Morales, J., Ribas, A., Feliu, C., & Casanova, J. C. (2003). Helminths of the wild rabbit (Oryctolagus cuniculus) in Macaronesia. Journal of Parasitology, 89(5), 952–957.
Frank, R., Kuhn, T., Mehlhorn, H., Rueckert, S., Pham, D., & Klimpel, S. (2013). Parasites of wild rabbits (Oryctolagus cuniculus) from an urban area in Germany, in relation to worldwide results. Parasitology Research, 112(12), 4255–4266.
Gemmill, A. W., Skorping, A., & Read, A. F. (1999). Optimal timing of first reproduction in parasitic nematodes. Journal of Evolutionary Biology, 12, 1148–1156.
Gibson, D. I., Bray, R. A., Hunt, D., Georgiev, B. B., Scholz, T., Harris, P. D., Bakke, T. A., Pojmanska, T., Niewiadomska, K., Kostadinova, A., Tkach, V., Bain, O., Durette-Desset, M. C., Gibbons, L., Moravec, F., Petter, A., Dimitrova, Z. M., Buchmann, K., Valtonen, E. T., & de Jong, Y. (2014). Fauna Europaea: Helminths (animal parasitic). Biodiversity Data Journal, 2, e1060.
Gvozdev, E. V., Kontrimavichus, V. L., Ryzhikov, K. M., & Shaldybin, L. S. (1970). Opredelitel’ gel’mintov zajceobraznyh SSSR [Key to the helminth parasites of Lagomorpha in the USSR]. Nauka, Moscow (in Russian).
Hajipour, N., & Zavarshani, M. (2020). Ectoparasites and endoparasites of New Zealand white rabbits from North West of Iran. Iranian Journal of Parasitology, 15(2), 266–271.
Khorolskyi, A., Yevstafieva, V., Kravchenko, S., Pishchalenko, M., Vakulenko, Y., & Gutyj, B. (2021). Specifics of the morphological identification of the pathogen of passaluariasis of rabbits. Regulatory Mechanisms in Biosystems, 12(4), 702–709.
Kornaś, S., Kowal, J., Wierzbowska, I., Basiaga, M., Nosal, P., & Niedbała, P. (2015). The alice – “Follow the white rabbit” – parasites of farm rabbits based on coproscopy. Annals of Parasitology, 61(4), 257–261.
Lafferty, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today, 13(7), 251–255.
Manning, P. J., Ringler, D. H., & Newcomer, C. E. (1994). The biology of the laboratory rabbit. Academic Press, London.
McSorley, R. (2003). Adaptations of nematides to environmental extremes. Florida Entomologist, 86(2), 138–142.
Mykhailiutenko, S. M., Kruchynenko, O. V., Klymenko, O. S., Serdioucov, J. K., Dmytrenko, N. I., & Tkachenko, V. V. (2019). Pathomorphological changes in the large intestine of rabbits parasitised by Passalurus ambiguus (Nematoda, Oxyuridae). Regulatory Mechanisms in Biosystems, 10(1), 69–74.
Perry, R. N. (2011). Understanding the survival strategies of nematodes. CAB Reviews: Perspectives in agriculture veterinary science nutrition and natural resources, 6(22), 99–104.
Rinaldi, L., Russo, T., Schioppi, M., Pennacchio, S., & Cringoli, G. (2007). Passalurus ambiguus: new insights into copromicroscopic diagnosis and circadian rhythm of egg excretion. Parasitology Research, 101, 557–561.
Skjabin, K. I., Shikhobalova, N. P., & Lagodovskaya, E. A. (1967). Osnovy nematodologii. Oksiuraty [Essentials of nematodology. Oxyurates]. Nauka, Moscow (in Russian).
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).
Taffs, L. F. (1976). Gusanos intestinales en roedores: Revisión. Laboratory Animals, 10, 1–11.
Yevstafieva, V. А., Kravchenko, S. O., Gutyj, B. V., Melnychuk, V. V., Kovalenko, P. N., & Volovyk, L. B. (2019). Morphobiological analysis of Trichuris vulpis (Nematoda, Trichuridae), obtained from domestic dogs. Regulatory Mechanisms in Biosystems, 10(2), 165–171.
Yevstafieva, V. А., Yuskiv, I. D., & Melnychuk, V. V. (2016). An investigation of embryo and eggshell development in Trichuris suis (Nematoda, Trichuridae) under laboratory conditions. Vestnik Zoologii, 50(2), 173–178.
Yevstafieva, V. О., Khorolskyi, A. A., & Melnychuk, V. V. (2021). Efektyvnist’ zaproponovanogo sposobu kul’tyvuvannja jajec’ nematod Passalurus ambiguus, shho parazytujut’ u kroliv [The effectiveness of the proposed method of culturing eggs of nematodes Passalurus ambiguus, parasitic in rabbits]. Scientific Messenger of Lviv National University of Veterinary Medicine and Biotechnologies, 23(101), 26–30 (in Ukrainian).
This work is licensed under a Creative Commons Attribution 4.0 International License.