Infectivity of gastrointestinal nematode parasites of sika deer (Cervus nippon) for calves and lambs
DOI:
https://doi.org/10.17420/ap71.554Keywords:
sika deer, cattle, sheep, gastrointestinal nematodes, Spiculopteragia houdemeri, experimental transmissionAbstract
Sika deer, mainly of Japanese origin, have been introduced into the British Isles and central Europe and established free-ranging populations, expanding in several countries. Introduction of the sika deer was associated with the transfer of Spiculopteragia houdemeri which has been reported for the first time in 2003 from Germany and thereafter from sika deer and other cervid species in some countries in Europe. Surveys of livestock parasites have shown that cervid-specific gastrointestinal nematodes of native deer occur in natural infections in cattle and sheep, usually at low level, and infections were experimentally transferred. However, to date there is no such information for sika deer-specific nematodes to livestock. To investigate the establishment of sika deer-derived gastrointestinal nematodes in domestic ruminants, three calves and two lambs were challenged with mixed burdens of infective larvae (~90% ostertagids, ~10% Oesophagostomum) cultured from the faeces of free-ranging sika deer; calves received 20,000 or 30,000 larvae, lambs 12,000 or 13,000. Establishment rate of ostertagids varied from 0.4% to 3.1% in the calves and was 1.3% and 8.4% in the lambs. Spiculopteragia houdemeri, index ostertagid of Japanese sika deer, was the dominant species, recovered from all animals. In addition, Ostertagia leptospicularis and Spiculopteragia boehmi, index ostertagids of native roe deer (Capreolus capreolus) and red deer (Cervus elaphus), respectively, were isolated from calf and lamb and Cooperia pectinata from one lamb. Oesophagostomum venulosum established in the lambs at ~6% but no Oesophagostomum was found in any calf. This investigation indicates that both calves and lambs are permissive to the sika deer-specific S. houdemeri and other deer-derived nematodes which reached maturity, but susceptibility to infections was apparently low.
References
[1] Böhm M., White P.C.L., Chambers J., Hutchings M.R. 2007. Wild deer as a source of infection for livestock and humans in the UK. Veterinary Journal 174: 260–276. https://doi.org/10.1016/j.tvjl.2006.11.003
[2] Walker J.G., Morgan E.R. 2014. Generalists at the interface: natural transmission between wild and domestic ungulates. International Journal for Parasitology: Parasites and Wildlife 3: 242–250. https://doi.org/10.1016/j.ijppaw.2014.08.001
[3]Winter J., Rehbein S., Joachim A. 2018. Transmission of helminths between species of ruminants in Austria appears to be more likely to occur than generally assumed. Frontiers in Veterinary Science 5: 30. https://doi.org/10.3389/fvets.2018.00030
[4] Wyrobisz-Papiewska A., Kowal J., Nosal P., Chovancová G., Rehbein S. 2018. Host specificity and species diversity of the Ostertagiinae Lopez- Neyra, 1947 in ruminants: a European perspective. Parasites & Vectors 11: 369. https://doi.org/10.1186/s13071-018-2958-6
[5] Barone C.D., Wit J., Hoberg E.P., Gilleard J.S., Zarlenga D.S. 2020. Wild ruminants as reservoirs of domestic livestock gastrointestinal nematodes. Veterinary Parasitology 279: 109041. https://doi.org/10.1016/j.vetpar.2020.109041
[6] Brown T.L., Morgan E.R. 2024. Helminth prevalence in European deer with a focus on abomasal nematodes and the influence of livestock pasture contact: a meta-analysis. Pathogens 13: 378. https://doi.org/10.3390/pathogens13050378
[7] Wetzel R., Fortmeyer H.P. 1964. Experimentelle Untersuchungen über die Wirtsspezifität parasitischer Rundwürmer des jagdbaren Wildes. Zeitschrift für Parasitenkunde 23: 108–134. https://doi.org/10.1007/BF00259951
[8] Barth D., Dollinger D. 1976. Investigations of the host specificity of gastro-intestinal nematodes of roedeer, sheep and cattle. In: Wildlife diseases. (Ed. A. Page). Plenum Publ. Corp., New York: 615–618.
[9] Borgsteede F.H.M. 1982. Infectivity of some nematode parasites of reindeer (Rangifer tarandus L.) and elk (Alces alces L.) for cattle and sheep. Zeitschrift für Parasitenkunde 67: 211–215. https://doi.org/10.1007/BF00928116
[10] Korsholm M. 1988. Nematodeninfektioner hod r.vildt og kvaeg. Behijsning af reservoiraerts - problematikken. Licentiatafhandling, Den. kgl. Vetog Landbokshoskole K.benhavn, Denmark.
[11] Kutzer E. 1988. Bedeutung parasitärer Wechselinfektionen bei Haus-und Wildwiederkäuern. Monatshefte für Veterinärmedizin 43: 577–580.
[12] Rehbein S., Haupt W. 1994. Ansteckungsmöglichkeiten mit Magen-Darm- und Lungen-Nematoden von Damwild für Rind, Schaf und Ziege bei gemeinsamer Haltung mit Damwild in einem Wildgehege. Deutsche Tierärztliche Wochenschrift 101: 456–459.
[13] Dróżdż J., Malczewski A., Demiaszkiewicz A.W., Lachowicz J. 1998. Domestic sheep and goat – hosts of deer gastrointestinal nematodes. Wiadomości Para zy tologiczne 44: 448.
[14] Manninen S.A., Thamsborg S.M., Laaksonen S., Oksanen A. 2014. The reindeer abomasal nematode (Ostertagia gruehneri) is naturally transmitted to sheep when sharing pastures. Parasitology Research 113: 4033–4038.
[15] Bartoš L. 2009. Sika deer in continental Europe. In: Sika deer: biology and management of native and introduced populations. (Eds. D.R. McCullogh, S. Takatsuki, K. Kaji). Springer, Tokyo: 573–594. https://doi.org/10.1007/978-4-431-09429-6_39
[16] Swanson G.M., Putman R. 2009. Sika deer in British Isles. In: Sika deer: biology and management of native and introduced populations. (Eds. D.R. McCullogh, S. Takatsuki, K. Kaji). Springer, Tokyo: 595–614. https://doi.org/10.1007/978-4-431-09429-6_40
[17] Linnell J.D.C., Zachos F.E. 2010. Status and distribution patterns of European ungulates: genetics, population history and conservation. In: Ungulate management in Europe. Problems and practices. (Eds. R. Putman, M. Apollonio, R. Andersen). Cambridge Univ. Pres, Cambridge: 12–53.
[18] Barboiron A., Saint-Andrieux C., Maillard J.F., Guibert B. 2020. La presence du daim et du cerf sika en France – situation en 2018. Faune Sauvage 326: 4–9.
[19] Saggiomo L., Esattore B., Bartoš L. 2021. Evaluating the management success of an alien species through its hunting bags: the case of sika deer (Cervus nippon) in the Czech Republic. Acta Universitatis Agriculturae at Silviculturae Mendelianae Brunensis 69: 327–336. https://doi.org/10.11118/actaun.2021.030
[20] Putman R., Krojerová-Prokešová J., Barančeková M. 2022. Sika Cervus nippon Temminck, 1838. In: Handbook of the mammals of Europe. Terrestrial Cetartiodactyla. (Eds. L. Corlatti, F.E. Zachos). Springer Nature, Cham: 87–114.
[21] Rehbein S., Velling M., Visser M., Heurich M., Hamel D. 2025. Successful establishment of Ashworthius sidemi in red deer (Cervus elaphus) in Germany, with a summary of worldwide A. sidemi records. European Journal of Wildlife Research 71: 2. https://doi.org/10.1007/s10344-024-01882-4
[22] Rehbein S. 2010. Die Endoparasiten des Sikawildes in Deutschland und Österreich. PhD Dissertation, Paris-Lodron-Universität, Salzburg, Austria.
[23] Rehbein S., Visser M., Lutz W. 2003. Erstnachweis von Spiculopteragia houdemeri (Schwartz, 1926) (Nematoda, Trichostrongylidae, Ostertagiinae) außerhalb Asiens bei Sikahirschen (Cervus nippon) in Deutschland. Zeitschrift für Jagdwissenschaft 49: 201–210. https://doi.org/10.1007/BF02189738
[24] Kotrlá B., Kotrlý A., Koždoň O. 1976. Studies on the specificity of the nematode Ashworthius sidemi Schulz, 1933. Acta Veterinaria Brno 45: 123–126.
[25] Moskwa B., Bień J., Cybulska A., Kornacka A., Krzysiak M., Cenek T., Cabaj W. 2015. The first identification of a blood-sucking abomasal nematode Ashworthius sidemi in cattle (Bos taurus) using simple polymerase chain reaction (PCR). Veterinary Parasitology 211: 106–109. https://doi.org/10.1016/j.vetpar.2015.04.013
[26] Rehbein S., Visser M. 2007. Die Endoparasiten des Sikawildes (Cervus nippon) in Österreich. Wiener Klinische Wochenschrift 119 (Suppl. 3): 96–101. https://doi.org/10.1007/s00508-007-0865-5
[27] MAFF 1986. Manual of veterinary parasitological laboratory techniques. Reference Book 418. 3rd ed. Her Majesty’s Stationary Office, London.
[28] Skr.bin K.I., Šihobalova N.P., Šul’c R.S. 1954. Trihostrongylidy životnyh i čeloveka. In: Osnovy Nematodologii, Vol. 3. (Ed. K.I. Skr.bin), Izdatel’stvo Akademii Nauk SSSR, Moskva.
[29] Dróżdż J. 1965. Studies on helminths and helminthiasis in Cervidae. I. Acta Parasitologica Polonica 12: 445–481.
[30] Hartwich G. 1994. II. Strongylida: Strongyloidea und Ancylostomatoidea. Die Tierwelt Deutschlands 68. Teil. G. Fischer, Jena.
[31] Kawamura T., Koda R., Tatsuzawa S. 2013. Pasture utilization by sika deer (Cervus nippon yakushimae): what factors affect deer density utilizing the pastures on Yakushima Island? Mammal Science 53: 345–350 (in Japanese with summary in English).
[32] Takayama K., Sonoda A., Hayashida Y., Ishii D., Yanagita D., Matsumoto S., Katahira K., Oshima I., Nakanishi Y., Inome T., Shioya K., Akai K. 2017. Wild sika deer invasions of the grassland within livestock farms. Journal of the Warm Regional Society of Animal Science Japan 60: 21–26 (in Japanese with summary in English).
[33] Nakamura N., Sonoda A., Sueno Y., Tominaga A., Yanagita D., Ishii D., Isakari A., Matsumoto S., Katahira K., Inadome T. 2019. Diurnal, seasonal and annual variations of sika deer (Cervus nippon nippon) invasions in the grassland. Bulletin of the Experimental Farm, Faculty of Agriculture, Kagoshima University 40: 13–18 (in Japanese with summary in English).
[34] Inoue K., Shishida K., Kawarai S., Takeda S., Minami M., Taira K. 2022. Helminths detected from wild sika deer (Cervus nippon centralis) in Kanto- Chubu region, Japan. Parasitology International 87: 102485. https://doi.org/10.1016/j.parint.2021.102485
[35] Sultan K., Omar M., Makouloutou P., Kaneshiro Y., Saita E., Yokoyama M., Suzuki K., Hosoi E., Sato E. 2014. Molecular genetic conspecificity of Spiculopteragia houdemeri (Schwartz, 1926) and S. andreevae (Dróżdż, 1965) (Nematoda: Ostertagiinae) from wild ruminants in Japan. Journal of Helminthology 88: 1–12. https://doi.org/10.1017/S0022149X12000521
[36] Taylor S.H., Cawthrone J.G. 1972. Species of gastrointestinal helminths of lambs in Northern Ireland. Journal of Helminthology 46: 285–290. https://doi.org/10.1017/s0022149x00024433
[37] Bernard J. 1974. Comparaison entre la fauna parasitaire gastro-intestinale des nématodes du mouton (Ovis aries L.) en Belgique et dans le bassin méditerranéen. Archives de l‘Institut Pasteur de Tunis 51: 275–292.
[38] Eisenegger H., Eckert J. 1975. Zur Epizootiologie und Prophylaxe der Dictyocaulose und der Trichostrongylidosen des Rindes. Schweizer Archiv für Tierheilkunde 117: 255–286.
[39] El-Moukdad A.R. 1977. Untersuchungen über die Endoparasiten der Schafe in Österreich. Wiener Tierärztliche Monatsschrift 64: 283–288.
[40] Hinaidy H.K., Prosl H., Supperer R. 1979. Ein weiterer Beitrag zur Gastrointestinal- Helminthenfauna des Rindes in Österreich. Wiener Tierärztliche Monatsschrift 66: 77–82.
[41] Barth D., Bernhard D., Lamina J. 1981: Das Vorkommen von Magendarmwürmern bei Milchkühen. Berliner Münchener Tierärztliche Wochenschrift 94: 68–71.
[42] Hong C., Lancaster M.B., Michel J.F. 1981. Worm burdens of dairy heifers in England and Wales. Veterinary Record 109: 12–14. https://doi.org/10.1136/vr.109.1.12
[43] Borgsteede F.H.M., Burg W.P.J. 1982. Worm burdens in cows. II. An analysis of the population of nematodes in the abomasa of adult dairy cows. Veterinary Parasitology 10: 323–330. https://doi.org/10.1016/0304-4017(82)90084-x
[44] Eysker M., Jansen J. 1982. Population build-up of gastro-intestinal nematode infection in ewes and lambs on pasture grazed by calves in the previous year. Research in Veterinary Science 32: 203–205. https://doi.org/10.1016/S0034-5288(18)32415-9
[45] Kaufmann J., Pfister K. 1986. Magen-Darm- Strongylidenbefall bei jungen Kühen und dessen Auswirkungen auf ausgewählte blutchemische Parameter. Deutsche Tierärztliche Wochenschrift 93: 397–399.
[46] Marnu W., Winterstaller E., Prosl H. 1987. Monthly and seasonal fluctuations in abomasal nematode worm burden of naturally infected cattle in Austria. Veterinary Parasitology 23: 237–248. https://doi.org/10.1016/0304-4017(87)90009-4
[47] Rehbein S., Visser M., Winter R. 1998. Ein Beitrag zur Kenntnis des Endoparasitenbefalls der Schafe auf der Schwäbischen Alb. Deutsche Tierärztliche Wochenschrift 105: 419–424.
[48] Rehbein S., Visser M., Winter R. 2003. Beitrag zur Kenntnis des Helminthenbefalls von Rindern aus Schleswig-Holstein nach einer Weidesaison. Berliner Münchener Tierärztliche Wochenschrift 116: 41–44.
[49] Rehbein S., Knaus M., Visser M., Winter R., Yoon S., Anderson A., Cramer L. 2015. Activity of ivermectin long-acting injectable (Ivomec® Gold) in first-season grazing cattle exposed to natural challenge conditions in Germany. Parasitology Research 114: 47–54. https://doi.org/10.1007/s00436-014-4158-4
[50] Rehbein S., Visser M., Mayr S., Kühnert A., Lindner T., Sommer M.F., Beelitz P., Hamel D. 2018. Endoparasite infections of first season grazing cattle at extensive permanent grassland in the Alps of Germany. Joint Meet. Belg. Soc. Parasitol. Protistol. (BSPP), British Ass. Vet. Parasitol. (BAVP), Irish Soc. Parasitol. (ISP), Eur. Vet. Parasitol. Coll. (EVPC), Brussels, Belgium, 03–04 May 2018, Abstracts: 76.
[51] Rehbein S., Hamel D., Lackerschmid J., Mayr S., Visser M. 2023. Multispecies helminth parasitism of grazing dairy cows in Germany and Austria, examined during the housing period. Veterinary Parasitology Regional Studies and Reports 40: 100860. https://doi.org/10.1016/j.vprsr.2023.100860
[52] Torina A., Dara S., Marino A.M.F., Sparagano O.A.E., Vitale F., Reale S., Caracappa S. 2004. Study of gastrointestinal nematodes in Sicilian sheep and goats. Annals of the New York Academy of Sciences 1026: 187–194. https://doi.org/10.1196/annals.1307.028
[53] Wyrobisz-Papiewska A., Kowal J., Łopieńska- Biernat E., Nosal P., Polak I., Paukszto Ł., Rehbein S. 2021. Morphometric and molecular analyses of Ostertagia leptospicularis Assadov 1953 from ruminants: species diversity or host influence? Animals 11: 182. https://doi.org/10.3390/ani11010182
[54] Rehbein S., Lutz W., Visser M., Winter R. 2001. Beiträge zur Kenntnis der Parasitenfauna des Wildes in Nordrhein-Westfalen. 2. Der Endoparasitenbefall des Damwildes. Zeitschrift für Jagdwissenschaft 47: 248–269. https://doi.org/10.1007/BF02242409
[55] Rehbein S., Lutz W., Visser M., Winter R. 2002. Beiträge zur Kenntnis der Parasitenfauna des Wildes in Nordrhein-Westfalen. 3. Der Endoparasitenbefall des Rotwildes. Zeitschrift für Jagdwissenschaft 48: 69–93. https://doi.org/10.1007/BF02193546
[56] Rehbein S., Barth D., Visser M., Winter R., Langholff W.K. 2000. Efficacy of an ivermectin controlled-release capsule against some rarer nematode parasites of sheep. Veterinary Parasitology 88: 293–298. https://doi.org/10.1016/s0304-4017(99)00220-4
[57] .rhardova B., Luli M., Prokopič .., Ryšavy B. 1960. K voprosu izučeni. gel’mintofauny domašnyh životnyh v Albanii. Československá Parasitologie 7: 99–114.
[58] Marinov M.N. 1997. Helminth parasites of sheep on highland pastures in intensive sheep-breeding regions in the Middle Stara Planina Mts (Bulgaria). Acta Zoologica Bulgarica 49: 86–93.
[59] Albrechtová M., Štefková Kašparová E., Langrová I., Hart V., Neuhaus B., Jankovská I., Petrtýl M., Magdálek J., Špakulová M. 2024. A revision of the trichostrongylid nematode Cooperia Ransom, 1907, from deer game: integrative research confirms the existence of the ancient host-specific Cooperia ventricosa (Rudolphi, 1809). Frontiers in Veterinary Science 11: 1346417. https://doi.org/10.3389/fvets.2024.1346417
[60] Steward T.B., Gasbarre L.C. 1989. The veterinary importance of nodular worms (Oesophagostomum spp.). Parasitology Today 5: 209–213. https://doi.org/10.1016/0169-4758(89)90269-x
[61] Rehbein S., Hamel D., Yoon S., Johnson C. 2022. Efficacy of eprinomectin topical solution and eprinomectin extended-release injection treatments against developing larval and adult Chabertia ovina and Oesophagostomum venulosum – two less common cattle nematode parasites. Veterinary Parasitology 312: 109837. https://doi.org/10.1016/j.vetpar.2022.109837
[62] Borgsteede F.H.M. 1981. Experimental crossinfections with gastrointestinal nematodes of cattle and sheep. Zeitschrift für Parasitenkunde 65: 1–10. https://doi.org/10.1007/BF00926548
[63] Chylinski C., Cortet J., Sallé G., Jacquiet P., Cabaret J. 2015. Storage of gastrointestinal nematode infective larvae for species preservation and experimental infections. Parasitology Research 114: 715–720. https://doi.org/10.1007/s00436-014-4238-5