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Long-term occurrence of Trichuris species in wild ruminants in the Czech Republic

Abstract

The aim of this study was to identify Trichuris species in wild ruminants from 32 localities in the Czech Republic using morphological and molecular methods (ITS1-5.8S RNA-ITS2 region polymorphisms). Trichurids were obtained from 176 wild ruminants (roe deer, sika deer, red deer, fallow deer and mouflons) that were culled between 2009 and 2017. Trichuris discolor is the predominant trichurid of all of the above-mentioned wild ruminants, whereas Trichuris ovis was identified less frequently in roe deer, fallow deer, sika deer and mouflons. Red deer were parasitised exclusively by T. discolor. Young hosts under 1 year of age were more intensively infected by trichurids than were adults (χ2 = 32.02, p = 0.00). Trichurid prevalence results obtained through coprological methods and those based on parasitological dissections differed significantly (χ2 = 16.26, p = 0.00). The regression analysis indicated that the eggs per gram (EPG) threshold (20 EPG) was exceeded only if the host was parasitised by more than 7 trichurid females. Full concordance between the positive results obtained by the coprological methods and those obtained via direct dissections was achieved when the number of trichurid females per host exceeded 51.

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References

  1. Balicka-Ramisz A, Cisek A, Ramisz A, Pilarczyk B (2003) Investigation of the lung, stomach and intestine helminth infections of roe deer in North-West Poland. Tiearztl Umsch 58:489–491

  2. Barth D, Schaich K (1971) Zur Wirksamkeit von thibenzole beim Magen-Darmwurmbefall des Rehwildes. Z Jagdwiss 17:240–243. https://doi.org/10.1007/BF01901783

  3. Baruš V, Kotrlá B, Tenora F (1978) Scanning electron microscopic study of the vulva of some trichurids (Nematoda). Folia Parasitol 25:31–34

  4. Baylis HA (1932) LIV.—three notes on parasitic nematodes. Ann Mag Nat Hist 10:497–502

  5. Becker AC, Kraemer A, Epe C, Strube C (2016) Sensitivity and efficiency of selected coproscopical methods-sedimentation, combined zinc sulphate sedimentation-flotation, and McMaster method. Parasitol Res 115:2581–2587. https://doi.org/10.1007/s00436-016-5003-8

  6. Bernard J, Biesemans W, Mathy P (1988) Nematodes parasites gastrointestinaux des Ongules gibier dans les Ardennes belges. Schweiz Arch Tierheilkd 130:77–103

  7. Body G, Ferte H, Gaillard JM, Delorme D, Klein F, Gilot-Fromont E (2011) Population density and phenotypic attributes influence the level of nematode parasitism in roe deer. Oecologia 167:635–646. https://doi.org/10.1007/s00442-011-2018-9

  8. Borgsteede FHM, Jansen J, Van Nispen Tot Pannerden HPM, Van Der Burg WPJ, Noorman N, Poutsma J, Kotter JF (1990) An investigation of the endoparasitic helminth fauna of roe deer (Capreolus capreolus L.) in the Netherlands. Z Jagdwiss 36:104–109

  9. Bütner K (1978) Untersuchungen zur Parasitierung des Rehwildes bei steigendem Jagddruck. Z Jagdwiss 24:139–155

  10. Callejón R, Halajian A, de Rojas M, Marrugal A, Guevara D, Cutillas C (2012) 16S partial gene mitochondrial DNA and internal transcribed spacers ribosomal DNA as differential markers of Trichuris discolor populations. Vet Parasitol 186:350–363. https://doi.org/10.1016/j.vetpar.2011.11.033

  11. Čermák P, Mrkva R (2003) Browsing damage to broadleaves in some national nature reserves (Czech Republic) in 2000-2001. Ekológia Bratislava 22:394–403

  12. Cisek A, Balicka-Ramisz A, Ramisz A, Pilarczyk B (2003) Occurrence of gastro-intestinal nematodes in cervids (Cervidae) of North-Western Poland. Electron J Pol Agric Univ 6(2), available online http://www.ejpau.media.pl/volume6/issue2/animal/art-09.html. Accessed 19 December 2017

  13. Dell Inc. (2015) Dell Statistica (data analysis software system), version 13. http://www.dell.com. Accessed 19 Dec 2017

  14. Dollinger P (1973) Beitrag zur Kenntnis der Magen-Darm-Parasitenfauna des Rehwildes der Nordostschweiz. Z Jagdwiss 19:14–25

  15. Dróżdż J (1966) Studies on helminths and helminthiasis in Cervidae. II. The helminth fauna in Cervidae in Poland. Acta Parasitol Pol 14:1–13

  16. Dróżdż J, Demiaskiewicz AW, Lachowicz J (1994) The effect of culling red deer, Cervus elaphus (L.), on their helminth fauna in the Słowiňski National Park (Poland). Acta Parasitol 39:92–94

  17. Dyk V, Chroust T (1974) Helminths and Coccidia of roe deer in two neighbouring ecologically different regions. Acta Vet Brno 43:65–77

  18. Erhartová B, Kotrlý A (1955) Cizopasní červi zažívacího ústrojí našich volně žijících přežvýkavců. Česk Parazitologie 2:41–68

  19. Gagarin VG (1972) Analiz vidogo sostava trichicefalov zvačnyh zaregistrirovanyh v Sovetskom Sojuze. Trudy Vsesojuznogo Ordena Trudovogo Krasnogo Znameni Instituta Gel'mintologii Imeni K I Skrjabina 19:39–57

  20. Galuppi R, Aureli S, Bonoli S, Caffara M, Tampieri MP (2011) Detection and molecular characterization of Theileria sp. in fallow deer (Dama dama) and ticks from an Italian natural preserve. Res Vet Sci 91:110–115. https://doi.org/10.1016/j.rvsc.2010.07.029

  21. Gassó D, Feliu C, Ferrer D, Mentaberre G, Casas-Díaz E, Velarde R, Fernández-Aguilar X, Colom-Cadena A, Navarro-Gonzalez N, López-Olvera JR, Lavín S, Fenández-Llario P, Segalés J, Serrano E (2015) Uses and limitations of faecal egg count for assessing worm burden in wild boars. Vet Parasitol 209:133–137. https://doi.org/10.1016/j.vetpar.2015.02.006

  22. Gortázar C, Acevedo P, Ruiz-Fons F, Vicente J (2006) Disease risks and overabundance of game species. Eur J Wildl Res 52:81–87. https://doi.org/10.1007/s10344-005-0022-2

  23. Hall A, Latham MC, Crompton DWT, Stephenson LS (1981) Taenia saginata (Cestoda) in western Kenya: the reliability of faecal examinations in diagnosis. Parasitology 83:91–101. https://doi.org/10.1017/S003118200005006X

  24. Haupt W, Stubbe I (1973) Untersuchungen zur Parasitierung der Rehwildpopulation im Wildforschungsgebiet Hakel unter besonderer Berucksichtigung von Alter, Geschlecht und Gewicht. Beiträge zur Jagd- und Wildforschung 8:171–185

  25. Hofmann RR (1985) Digestive physiology of the deer—their morphophysiological specialisation and adaptation. In: Fenessy PF, Drew KR (ed) Biology of deer production. Proceedings of an International Conference held at Dunedin. Bulletin 22 of the Royal Society of New Zealand, New Zealand, pp 393407

  26. Hoste H, Sotiraki S, Landau SY, Jackson F, Beveridge I (2010) Goat–nematode interactions: think differently. Trends Parasitol 26:376–381. https://doi.org/10.1016/j.pt.2010.04.007

  27. Huntley JF, Patterson M, Mackellar A, Jackson F, Stevenson LM, Coop RL (1995) A comparison of the mast cell and eosinophil responses of sheep and goats to gastrointestinal nematode infections. Res Vet Sci 58:5–10. https://doi.org/10.1016/0034-5288(95)90080-2

  28. Itagaki T, Ohtori M, Aki M, Ichinomiya M (2007) Molecular phylogenetic analysis of gastrointestinal helminth from Japanese serow (Capricornis crispus) in North region. National Center for Biotechnology Information, published only in dataset. http://www.ncbi.nlm.nih.gov/nuccore/AB367795. Accessed 19 Dec 2017

  29. Jallow OA, McGregor BA, Anderson N, Holmes JH (1994) Intake of trichostrongylid larvae by goats and sheep grazing together. Aust Vet J 71:361–364. https://doi.org/10.1111/j.1751-0813.1994.tb00927.x

  30. Jansen J (1992) On the nematode parasite fauna of Friesian roe deer (Capreolus capreolus). In: Hernandez, S. (Ed.), “In memoriam” al Profesor Dr. Francisco de Paula Martinez Gomez. Servicio de Comunicaciones de la Universidad de Cordoba, Cordoba. 301–307

  31. Kamler J, Homolka M, Barančeková M, Krojerová-Prokešová (2010) Reduction of herbivore density as a tool for reduction of herbivore browsing on palatable tree species. Eur J Forest Res 129:155–162. https://doi.org/10.1007/s10342-009-0309-z

  32. Klimpel S, Abdel-Ghaffar F, Al-Rasheid KA, Aksu G, Fischer K, Strassen B, Mehlhorn H (2011) The effects of different plant extracts on nematodes. Parasitol Res 108:1047–1054. https://doi.org/10.1007/s00436-010-2168-4

  33. Knight RA (1971) Redescriptions of Trichuris discolor (von Linstow, 1906) and T. skrjabini (Baskakov, 1924) from domestic ruminants in the United States and comparisons with T. ovis (Abildgaard, 1795). J Parasitol 57:302–310

  34. Knight RA (1984) Morphological differences in Trichuris ovis associated with different host species. J Parasitol 70:842–843

  35. Kotrlá B, Kotrlý A (1977) Helminths of wild ruminants introduced into Czechoslovakia. Folia Parasitol 24:35–40

  36. Kutzer E, Knaus E (1969) Untersuchungen über die Endoparasitenfauna eines Rehbestandes in der freien Wildbahn. Z Jagdwiss 15:62–72

  37. Kutzer E, Sugár L, Buchacher-Tonitz S (1987) Beiträge zur Parasitenfauna der wildlebenden Wiederkäuer Ungarns. I. Zur Parasitenfauna von Rehkitzen und Jungrehen (Capreolus c. capreolus). Parasitologia Hungarica 20:81–90

  38. Kutzer E, Sugar L, Buchacher-Tonitz S (1988) Beitrage zur Parasitenfauna der wildlebenden Wiederkauer Ungarns. II. Aufbauentwicklung des Parasitenbefalles bei Rehen (Capreolus c. capreolus). Parasitologia Hungarica 21:85–97

  39. Kuzmina TA, Kharchenko VA, Malega AM (2010) Helminth fauna of roe deer (Capreolus capreolus) in Ukraine: biodiversity and parasite community. Vestnik zoologii 44:15–22

  40. Lanfredi RM, Souza WD, Gomes DC (1995) Comparative study of four species of Trichuris roederer, 1761 (Nematoda, Trichurinae) by scanning electron microscopy. Mem Inst Oswaldo Cruz 90:489–496. https://doi.org/10.1590/S0074-02761995000400011

  41. Le Jambre L, Royal WM (1976) A comparison of worm burdens in grazing merino sheep and angora goats. Aust Vet J 52:181–183. https://doi.org/10.1111/j.1751-0813.1976.tb09467.x

  42. Liu GH, Wang Y, Xu MJ, Zhou DH, Ye YG, Li JY, Song HQ, Lin RQ, Zhu XQ (2012) Characterization of the complete mitochondrial genomes of two whipworms Trichuris ovis and Trichuris discolor (Nematoda: Trichuridae). Infect Genet Evol 12:1635–1641. https://doi.org/10.1016/j.meegid.2012.08.005

  43. Macháček Z, Dvořák S, Ježek M, Zahradník D (2014) Impact of interspecific relations between native red deer (Cervus elaphus) and introduced sika deer (Cervus nippon) on their rutting season in the Doupovské hory Mts. J For Sci 60:272–280

  44. Martínez-Jauregui M, Herruzo AC (2014) A note on the effectiveness of incorporating management objectives with ecological variables when modeling red deer abundance. Eur J Wildl Res 60:511–517. https://doi.org/10.1007/s10344-014-0813-4

  45. Meana A, Luzon M, Corchero J, Gómez-Bautista M (1998) Reliability of coprological diagnosis of Anoplocephala perfoliata infection. Vet Parasitol 74:79–83. https://doi.org/10.1016/S0304-4017(97)00145-3

  46. Nickel S, Hiepe T, Ness H, Pingel H (1978) Beitrage zur Parasitenfauna der DDR. 2. Untersuchungen zum Helminthenvorkommen beim Reh (Capreolus capreolus). Angew Parasitol 19:194–202

  47. Oliveros R, Cutillas Barrios C (2003) Redescripción de Trichuris ovis (Nematoda) (Abildgaard, 1795) parásito de Ovis aries (Linné, 1758) y Capra hircus (Linné, 1758). Rev Iber Parasitol 63:77–83

  48. Osakwe IR (1970) Morphometry of geohelminthic roe-deer intestine nematodes in two southern Moravian enclosures. Acta scientiarum naturalium Academiae Scientiarum Bohemicae, Brno 4:145

  49. Pato FJ, Vázquez L, Díez-Baños N, López C, Sámchez-Andrade, Fernádez G, Díez-Banos P, Panadero R, Díaz P, Morrodo P (2013) Gastrointestinal nematode infections in roe deer (Capreolus capreolus) from the NW of the Iberian peninsula: assessment of some risk factors. Vet Parasitol 196:136–142. https://doi.org/10.1016/j.vetpar.2013.01.027

  50. Pilarczyk B, Balicka-Ramisz A, Ramisz A, Lachowska S (2005) Wysteopowanie pasozytów przewodu pokarmowego u saren i jeleni na terenie województva zachodniopomorskiego. Wiad Parazytol 4:307–310

  51. Pomroy WE, Lambert MG, Betteridge K (1986) Comparison of faecal strongylate egg counts of goats and sheep on the same pasture. NZVJ 34:36–37. https://doi.org/10.1080/00480169.1986.35272

  52. Rehbein S (2010) Die Endoparasiten des Sikawildes in Deutschland und Österreich. Dissertation, Universität Salzburg, 415pp

  53. Rehbein S, Visser M (2007) Die Endoparasiten des Sikawildes (Cervus nippon) in Österreich. Wien Klin Wochenschr 119:96–101. https://doi.org/10.1007/s00508-007-0865-5

  54. Rehbein S, Lutz W, Visser M, Winter R (2000) Beiträge zur Kenntnis der Parasitenfauna des Wildes in Nordrhein-Westfalen. 1. Der Endoparasitenbefall des Rehwildes. Z Jagdwiss 46:248–269. https://doi.org/10.1007/BF02241594

  55. Rehbein S, Lutz W, Visser M, Winter R (2001) Beiträge zur Kenntnis der Parasitenfauna des Wildes in Nordrhein-Westfalen. 2. Der Endoparasitenbefall des Damwildes. Z Jagdwiss 47:1–16. https://doi.org/10.1007/BF02242409

  56. Rehbein S, Lutz W, Visser M, Winter R (2002) Beiträge zur Kenntnis der Parasitenfauna des Wildes in Nordrhein-Westfalen. 3. Der Endoparasitenbefall des Rotwildes. Z Jagdwiss 48:69–93. https://doi.org/10.1007/BF02193546

  57. Rieu E, Recca A, Bénet JJ, Saana M, Dorchies P, Guillot J (2007) Reliability of coprological diagnosis of Paramphistomum sp. infection in cows. Vet Parasitol 146:249–253. https://doi.org/10.1016/j.vetpar.2007.02.033

  58. Roepstorff A, Nansen P (1998) Epidemiology, diagnosis and control of helminth parasites of swine. FAO Animal Health Manual, Rome

  59. Salaba O, Rylková K, Vadlejch J, Petrtýl M, Scháňková Š, Brožová A, Jankovská I, Jebavý L, Langrová I (2013) The first determination of Trichuris sp. from roe deer by amplification and sequenation of the ITS1-5.8S-ITS2 segment of ribosomal DNA. Parasitol Res 112:955–960. https://doi.org/10.1007/s00436-012-3215-0

  60. Sarwar MM (1945) Two new records of the species of the genus Trichuris from Indian ruminants. Curr Sci 14:156

  61. Sarwar MM (1959) Reconstruction of the genus Trichuris and a short review of its taxonomy and morphology. Biologia (Lahore) 5:19–35

  62. Schulze ED, Bouriaud O, Wäldchen J, Eisenhauer N, Walentowski H, Seele C, Heinze E, Pruschitzki U, Danila G, Marin G, Hessenmöller D, Bouriaud L, Teodosiu M (2014) Ungulate browsing causes species loss in deciduous forests independent of community dynamics and silvicultural management in central and southeastern Europe. Ann For Res 57:267–288. https://doi.org/10.15287/afr.2014.273

  63. Schwarz L, Frena M, Skalicky M, Prosl H (2011) Endoparasitenbefall von Rehen in einem Revier in Niederösterreich. Wien Tierarztl Monatsschr 98:285–291

  64. Shimalov VV, Shimalov VT (2003) Helminth fauna of cervids in Belorussian Polesie. Parasitol Res 89:75–76. https://doi.org/10.1007/s00436-002-0700-x

  65. Skrjabin KI, Shikhobalova NP, Orlov IV (1957) Trichosefalidy i kapillariidy zhivotnykh i cheloveka i vyzyvaemye imi zabolevaniya. Izdavatel’stvo Akademii Nauk SSSR, Moskva

  66. Špakulová M (1994) Discriminant analysis as a method for the numerical evaluation of taxonomic characters in male trichurid nematodes. Syst Parasitol 29:113–119. https://doi.org/10.1007/BF00009807

  67. Spellmeyer O (1996) Untersuchungen zur Helminthenfauna von Reh- und Schwarzwild aus Norddeutschland. Dissertation, Freie Universität Berlin

  68. Tománek J (1967) Příspěvek k poznání helmintofauny srnčí zvěře severomoravského kraje. Vet Med (Praha) 12:739–744

  69. Vadlejch J, Petrtýl M, Zaichenko I, Čadková Z, Jankovská I, Langrová I, Moravec M (2011) Which McMaster egg counting technique is the most reliable? Parasitol Res 109:1387–1394. https://doi.org/10.1007/s00436-011-2385-5

  70. Van Wieren SE (1995) The potential role of large herbivores in nature conservation and extensive land use in Europe. Biol J Linn Soc Lond 56:11–23. https://doi.org/10.1111/j.1095-8312.1995.tb01114.x

  71. Vejl P, Nechybová S, Peřinková P, Melounová M, Sedláková V, Vašek J, Čílová D, Rylková K, Jankovská I, Vadlejch J, Langrová I (2017) Reliable molecular differentiation of Trichuris ovis and Trichuris discolor from sheep (Ovis orientalis aries) and roe deer (Capreolus capreolus) and morphological characterisation of their females: morphology does not work sufficiently. Parasitol Res 116:2199–2210. https://doi.org/10.1007/s00436-017-5524-9

  72. Vetýška V (1980) Endoparasites of roe deer in the Strakonice region. Acta Vet Brno 49:91–103

  73. Vlassoff A, Bisset SA, McMurty LW (1999) Faecal egg counts in Angora goats following natural or experimental challenge with nematode parasites: within flock variability and repeatabilities. Vet Parasitol 84:113–123. https://doi.org/10.1016/S0304-4017(99)00072-2

  74. Wetzel E (1951) Verbesserte McMaster-Kammer zum Auszählen von Wurmeiern. Tierärztl Umsch 6:209–210

  75. Zajíček D (1978) Comparision of the efficiency of two quantitative ovoskopic methods (article in Czech). Vet Med 23:275–280

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Acknowledgments

This study has been funded by the Grant of National Agency for Agricultural Research of the Czech Republic, No. QJ1510038. The authors gratefully acknowledge certain sheep farmers and gamekeepers from various areas of the Czech Republic for providing biological materials. The authors gratefully acknowledge certain sheep farmers and gamekeepers from various areas of the Czech Republic for providing biological materials. The authors are also grateful to Mr. Brian Kavalir (Ontario, Canada) for the proofreading.

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Correspondence to Pavel Vejl.

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Nechybová, S., Vejl, P., Hart, V. et al. Long-term occurrence of Trichuris species in wild ruminants in the Czech Republic. Parasitol Res 117, 1699–1708 (2018). https://doi.org/10.1007/s00436-018-5841-7

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Keywords

  • Trichuris discolor
  • Trichuris ovis
  • Game ruminants
  • ITS1-5.8S rRNA-ITS2 region
  • Prevalence
  • Effectiveness of coprology