A revised checklist of Cooperia nematodes (Trichostrogyloidea), common parasites of wild and domestic ruminants

M. Albrechtová; I. Langrová; J. Vadlejch; M. Špakulová

doi:10.2478/helm-2020-0034

Abstract

This review updates the current knowledge on the taxonomy of intestinal nematodes of the genus Cooperia parasitizing in wild and domestic ruminants. The emphasis is put on revision of 19 valid species belonging to the genus. This analysis focuses on main features of the genus Cooperia, including its geographic occurrence and the life cycle details. The most widespread congeners are Cooperia curticei, C. oncophora, C. pectinata, and C. punctata, having nearly worldwide distribution. The fifth species, referred by electronic databases from the European territory as Cooperia asamatiSpiridonov, 1985, is unveiled here originally as nomen nudum.

References

Amarante, M.R., Bassetto, C.C., Neves, J.H., Amarante, A.F. (2014): Species-specific PCR for the identification of Cooperia curticei (Nematoda: Trichostrongylidae) in sheep. J. Helminthol. 88(4): 447–452. 10.1017/S0022149X13000412
Open DOI Search in Google Scholar Back to article
Armour, J., Duncan, M. (1987): Arrested larval development in cattle nematodes. Parasitol. Today, 3(6): 171–176. 10.1016/0169-4758(87)90173-6
Open DOI Search in Google Scholar Back to article
Avramenko, R.W., Redman, E.M., Lewis, R., Yazwinski, T.A., Wasmuth, J.D., Gileard, J.S. (2015): Exploring the gastrointestinal “Nemabiome”: Deep amplicon sequencing to quantify the species composition of parasitic nematode communities. PLoS ONE, 10(12): e0143559. 10.1371/journal.pone.014355
Open DOI Search in Google Scholar Back to article
Avramenko, R.W., Redman, E.M., Lewis, R., Bichuette, M.A., Palmeira, B.M., Yazwinski, T.A. Gileard, J.S. (2017): The use of nemabiome metabarcoding to explore gastro-intestinal nematode species diversity and anthelmintic treatment effectiveness in beef calves. Int. J. Parasitol. 47(13): 893–902. 10.1016/j.ijpara.2017.06.006
Open DOI Search in Google Scholar Back to article
Besch, E.D. (1963): Studies on the biology of Cooperia punctata (von Linstow, 1907) Ransom, 1907 (Nematoda: Trichostrongylidae) in the domestic rabbit, Oryctolagus cuniculus L. PhD. Thesis. Faculty of the Graduate School of the Oklahoma State University, Oklahoma, U.S.A. 97pp.
Search in Google Scholar Back to article
Besch, E. D. (1965): Biology of Cooperia punctata (Nematoda: Trichostrongylidae) in the domestic rabbit. J. Parasitol. 51(2): 139–144. 10.2307/3276067
Open DOI Search in Google Scholar Back to article
Boomker, J. (1982): Cooperia acutispiculum n. sp. (Nematoda: Trichostrongylidae) from the kudu, Tragelaphus strepsiceros (Pallas, 1766). Onderstepoort J. Vet. Res. 49: 95–97. DOI: http://hdl.handle.net/2263/51103
Search in Google Scholar Back to article
Boomker, J., Taylor, W.A. (2004): Parasites of South African wildlife. XVIII. Cooperia pigachei n. sp. (Nematoda: Cooperiidae) from the mountain reedbuck, Redunca fulvorufula (Afzelius, 1815). Onderstepoort J. Vet. Res. 71: 171–174. 10.4102/ojvr. v7li3.256
Open DOI Search in Google Scholar Back to article
Borloo, J., De Graef, J., Peelaers, I., Nguyen, D.L., Mitreva, M., Devreese, B., Hokke, C.H., Vercruysse, J., Claerebout, E., Geldhof, P. (2013): In-depth proteomic and glycomic analysis of the adult-stage Cooperia oncophora excretome/secretome. J. Proteome Res. 12(9): 3900–3911. 10.1021/pr400114y.
Open DOI Search in Google Scholar Back to article
Ciordia, H., Bizzel, W.E. (1963): The effects of various constant temperatures on the development of the free living-stages of some nematode parasites of cattle. J. Parasitol. 49(1): 60–63. 10.2307/3275675
Open DOI Search in Google Scholar Back to article
Coelho, W.M.D., Amarante, A.F.T., Bresciani, K.D.S. (2012): Occurrence of gastrointestinal parasites in goat kids. Rev. Brasil. Parasitol. Vet., 21(1): 65–67. 10.1590/S1984-29612012000100013
Open DOI Search in Google Scholar Back to article
de Jong, Y. et al. (2014): Fauna Europaea - all European animal species on the web. Biodiv. Data J. 2: e4034. 10.3897/BDJ.2.e4034. (Date of access: August 19, 2019).
Open DOI Search in Google Scholar Back to article
De Ley, P., Blaxter, M.L. (2002): Systematic position and phylogeny. In Lee, D. (Ed) The Biology of Nematodes. London, UK: Taylor & Francis, pp. 1–30
Search in Google Scholar Back to article
Durette-Desset, M-C. (1969): Les systemes d’aretes cuticulaires chez les Nematodes Heligmosomes parasites de Murides australiens [Cuticular ridge systems in nematodes Heligmosomes parasites of Australian Murids]. Ann. Parasitol. Hum. Comp. 44(6): 733–747. 10.1051/parasite/1969446733 (In French)
Open DOI Search in Google Scholar Back to article
Durette-Desset, M-C. (1974): Keys to genera of the superfamily Trichostrongyloidea. No. 10. In Anderson, R.C., Chabaud, A.G., Wilmott, S. (Eds) CIH Keys to the Nematode Parasites of Vertebrates. Farnham Royal, Bucks, England: Commonwealth Agricultural Bureaux, pp. 1–85
Search in Google Scholar Back to article
Edmonds, M.D., Jonson, E.G., Edmonds, J.D. (2010): Anthelmintic resistance of Ostertagia ostertagi and Cooperia oncophora to macrocyclic lactones in cattle from the western United States. Vet. Parasitol. 170(3-4): 224–229. 10.1016/j.vetpar.2010.02.036
Open DOI Search in Google Scholar Back to article
Eysker, M. (1993): The role of inhibited development in the epidemiology of Ostertagia infections. Vet. Parasitol. 46(1-4): 259–269. 10.1016/03044017(93)90063-S
Open DOI Search in Google Scholar Back to article
Fiel, C.A., Fernández, A.S., Rodíguez, E.M., Fusé, L.A., Steffan, P.E. (2012): Observations on the free-living stages of cattle gastrointestinal nematodes. Vet. Parasitol. 187(1-2): 217–226. 10.1016/j.vetpar.2012.01.011
Open DOI Search in Google Scholar Back to article
Gasbarre, L.C., Smith, L.L., Lichtenfels, J.R., Pilitt, P.A. (2009): The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US. Vet. Parasitol. 166(3-4): 281–285. 10.1016/j.vetpar.2009.08.018
Open DOI Search in Google Scholar Back to article
Gibons, L.M. (1981): Revision of the African species of the genus Cooperia Ransom, 1907 (Nematoda, Trichostrongylidae). Syst. Parasitol. 2(4): 219–252. 10.1007/BF00009344
Open DOI Search in Google Scholar Back to article
Gibson, D. (2017): Fauna Europaea: Cooperia. Fauna Europaea, version 2017.06. https://fauna-eu.org Accessed 17.8.2019
Search in Google Scholar Back to article
Giudici, C., Aumont, G., Mahieu, M., Saulai, M., Cabaret, J. (1999): Changes in gastro-intestinal helminth species diversity in lambs under mixed grazing on irrigated pastures in the tropics (Franch West Indies). Vet. Res. 30: 573–581.
Search in Google Scholar Back to article
Heizer, E., Zarlenga, D.S., Rosa, B., Gao, X., Gasser, R.B., De Graef, J., Geldhof, P., Mitreva, M. (2013): Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora. BMC Genomics, 14: 118. 10.1186/1471-2164-14-118.
Open DOI Search in Google Scholar Back to article
Humbert, J.F., Cabaret, J. (1995): Use of random amplified polymorphic DNA for identification of ruminant trichostrongylid nematodes. Parasitol. Res. 81(1): 1–5. 10.1007/BF00932409
Open DOI Search in Google Scholar Back to article
Isenstein, R.S. (1971a): The polymorphic relationship of Cooperia oncophora (Railliet, 1898) Ransom, 1907, to Cooperia surnabada Antipin, 1931 (Nematoda: Trichostrongylidae). J. Parasitol. 57(2): 316–319. 10.2307/3278034
Open DOI Search in Google Scholar Back to article
Isenstein, R.S. (1971b): Hybridization of two species of nematodes parasitic in ruminants, Cooperia oncophora (Railliet, 1898) Ransom, 1907, and Cooperia pectinata Ransom, 1907. J. Parasitol. 57(2): 320–326. 10.2307/3278036
Open DOI Search in Google Scholar Back to article
Jennings, F.W., Armour, J., Lawson, D.D., Roberts, R. (1966): Experimental Ostertagia infections in calves: Studies with abomasal cannulas. Am. J. Vet. Res. 27(120): 1249–1257.
Search in Google Scholar Back to article
Karamendin, O.S. (1967): Identification of the nematodes Cooperia zurnabada and C. mcmasteri. Helminthologia 7(1/4): 81–90
Search in Google Scholar Back to article
Knapp-Lawitzke, F., Samson-Himmelstjerna, G., Demeler, J. (2016): Elevated temperatures and long drought periods have a negative impact on survival and fitness of strongylid third stage larvae. Int. J. Parasitol. 46(4): 229–237. 10.1016/j.ijpara.2015.10.006
Open DOI Search in Google Scholar Back to article
Kotrlá, B., Černý, V., Kotrlý, A., Minář, J., Ryšavý, B., Šebek, Z. (1984): Parazitózy zvěřeGame parasitoses Prague, Czech Republic, Academia Publishing, 192 pp. (In Czech)
Search in Google Scholar Back to article
Kulišić, Z., Nevenka , A., Dordević, M., Gajićm, M., Tambur, Z., Jevrosima , S., Stanimicović, Z. (2013): Prevalence and intensity of infection with gastrointestinal nematodes in sheep in Eastern Serbia. Acta vet. (Beograd) 63(4): 429–436. 10.2298/AVB1304429K
Open DOI Search in Google Scholar Back to article
Leland, S.E. Jr. (1967): In in-vitro development of Cooperia pectinata, a nematode parasite of cattle from third-stage larvae to adults including egg production. J. Parasitol. 53(3): 630–633.
Search in Google Scholar Back to article
Lichtenfels, J.R. (1977): Differences in cuticular ridges among Cooperia spp. of North American ruminants with an illustrated key to species. Proc. Helm. Soc. Washington, 44(2): 111–119
Search in Google Scholar Back to article
Lichtenfels, J.R., Hoberg, E.P, Zarlenga, D.S. (1997): Systematics of gastrointestinal nematodes of domestic ruminants: advances between 1992 and 1995 and proposals for future research. Vet. Parasitol. 72(3-4): 225–245. 10.1016/S0304-4017, (97)00099-X
Open DOI Search in Google Scholar Back to article
Mahmuda, A., Yakubu, Y., Raji, A.A., Lawal, N., Saidu, B., Danmaigoro, A., Bello, A. (2012): Prevalence of gastrointestinal round worms in calves in Sokoto, northwestern Nigeria. Sci. J. Zool. 1(2): 26–30. 10.14196/sjz.vli2.190
Open DOI Search in Google Scholar Back to article
Michel, J.F., Lancaster, M.B., Hong, C. (1974): Studies on arrested development of Ostertagia ostertagi and Cooperia oncophora. J. Comp. Pathol., 84(4): 539–554. 10.1016/0021-9975(74)90046-2
Open DOI Search in Google Scholar Back to article
Newton, L.A., Chilton, N.B., Beveridge, I., Gasser, R.B. (1998): Genetic evidence indicating that Cooperia surnabada and Cooperia oncophora are one species. Int. J. Parasitol. 28(2): 331–336. 10.1016/S0020-7519(97)00149-5
Open DOI Search in Google Scholar Back to article
Radavelli, W.M., Pazinato, R., Klauck, V., Volpa to, A., Balzan, A., Rossett, J., Cazarotto, Ch.J., Lopes, L.S., Kessler, J.D., Cucco, D.C., Tonin, A.A., da Silva, A.S. (2014): Occurrence of gastrointestinal parasites in goats from the Western Santa Catarina, Brazil. Rev. Bras. Parasitol. Vet. 23(1): 101–104. 10.1590/S1984-29612014016
Open DOI Search in Google Scholar Back to article
Ramünke, S., Borges, F.A., Fernex, E.S., Samson-Himmelstjerna, G., Krücken, J. (2018): Molecular marker sequences of cattle Cooperia species identify Cooperia spatulata as a morphotype of Cooperia punctata. PloS One, 13(7):e0200390. 10.1371/journal.pone.0200390
Open DOI Search in Google Scholar Back to article
Rees T. (2018): The Interim Register of Marine and Nonmarine Genera. IRMNG. Cooperia Ransom, 1907. Accessed at: http://www.irmng.org/aphia.php?p=taxdetails&id=1276395 on 2019-12-03
Search in Google Scholar Back to article
Singh, P.P., Pande, B.P. (1963): Helminths collected from the Indian Antelope, Antilope cervicapra. Ann. Parasitol. Hum. Comp. 38(3): 439–457. 10.1051/parasite/1963383439
Open DOI Search in Google Scholar Back to article
Skrjabin, K.I., Shikhobalova, N.P., Shults, R.E.S. (1954): Osnovy nematodologii. Trikhostrongilidy zhivotnykh i cheloveka [Fundamentals of Nematodology: Trichostrongylids of Animals and Man], Volume 3. Moscow, USSR: Akademia Nauk SSSR, 683 pp. (In Russian)
Search in Google Scholar Back to article
Spiridonov, S.E. (1985): Angiostoma asamati sp. n. (Angiostomatidae: Rhabditida) – new species of nematodes from slugs (Mollusca). Helminthologia, 22(4): 253–261
Search in Google Scholar Back to article
Stromberg, B. E., Gasbarre, L.C., Waite, A., Bechtol, D.T., Brown, M.S., Robinson, N.A., Olson, E.J., Newcomb, H. (2012): Cooperia punctata Effect on cattle productivity? Vet. Parasitol. 183(3-4): 284–291. 10.1016/j.vetpar.2011.07.030.
Open DOI Search in Google Scholar Back to article
Sun, M-M., Han, L., Zhou, C-Y., Liu, G-H., Zhu, X-Q., Ma, J. (2020): Mitochondrial genome evidence suggests Cooperia sp. from China may represent a distinct species from Cooperia oncophora from Australia. Parasitol. Int. 75:102001. 10.1016/j.parint.2019.102001
Open DOI Search in Google Scholar Back to article
Taylor, W.A., Skinner, J.D., Boomker, J. (2013): Nematodes of the small intestine of African buffaloes, Syncerus caffer, in the Kruger National Park, South Africa. Onderstepoort J. Vet. Res. 80: E1 – E4. 10.4102/ojvr.v80i1.562
Open DOI Search in Google Scholar Back to article
van der Veer, M., de Vries E. (2003): Genetic intrapopulation variation, revealed by amplified fragment length polymorphism, within a population of the trichostrongylid nematode Cooperia oncophora. Exp. Parasitol. 104: 70–73. 10.1016/S0014-4894(03)00116-4
Open DOI Search in Google Scholar Back to article
van der Veer, M., Kanobana, K., Ploeger, H.W., de Vries, E. (2003): Cytochrome oxidase c subunit 1 polymorphisms show significant differences in distribution between a laboratory maintained population and a field isolate of Cooperia oncophora. Vet. Parasitol. 116: 231–238. 10.1016/j.vetpar.2003.07.007
Open DOI Search in Google Scholar Back to article
Vlassoff, A., McKenna, P.B. (1994): Nematode parasites of economic importance in sheep in New Zealand. N. Zealand J. Zool. 21: 1–8. 10.1080/03014223.1994.9517971
Open DOI Search in Google Scholar Back to article
Walker, M.L., Becklund, W.W. (1968): A note on the morphology of Cooperia punctata (Linstow, 1907) and Cooperia spatulata Baylis, 1938. Proc. Helm. Soc. Washington 35: 49–51
Search in Google Scholar Back to article
Wu, S.W. (1965): A new species of Cooperia (Nematoda: Trichostrongylidae). Acta Vet. Zootech. Sinica, 8 (4), 293–296
Search in Google Scholar Back to article
Wyrobisz, A., Kowal, J., Nosal, P. (2016): Insight into species diversity of the Trichostrongylidae Leiper, 1912 (Nematoda: Strongylida) in ruminants. J. Helminthol. 90(6): 639–646. 10.1017/S0022149X15001017
Open DOI Search in Google Scholar Back to article
Yamaguti, S. (1961): Systema Helminthum. Vol. III. The Nematodes of Vertebrates, Pt. II & I. New York & London, Interscience Publishers, 1261pp.
Search in Google Scholar Back to article

A revised checklist of Cooperia nematodes (Trichostrogyloidea), common parasites of wild and domestic ruminants

Abstract

Paradigm

My account