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Experimental and Applied Acarology

, Volume 74, Issue 3, pp 317–328 | Cite as

Ecological preferences and seasonal dynamics of ticks (Acari: Ixodidae) on and off bovine hosts in the Eastern Cape Province, South Africa

  • M. Yawa
  • N. Nyangiwe
  • V. Muchenje
  • C. T. Kadzere
  • T. C. Mpendulo
  • M. C. Marufu
Article

Abstract

A total of 31,425 ticks were collected from 10 cattle and also from six drag-samples during the 12-month study period. Adult ticks were removed from the right hand side of each animal and all instars of ticks were placed in containers filled with 70% ethanol. Based on morphological traits, 10 tick species were identified: Rhipicephalus (Boophilus) decoloratus (32.5%), R. evertsi evertsi (18.8%), R. appendiculatus (17.3%), Amblyomma hebraeum (16.3%), R. simus (7.7%), Ixodes pilosus (3.8%), Hyalomma rufipes (3.5%), R. follis (0.08%), Haemaphysalis elliptica (0.04%), H. silacea (0.02%). The southern African yellow dog tick, H. elliptica, was only found on vegetation. The agro-ecological zones differ significantly in tick species and their distribution. The A. hebraeum and R. evertsi evertsi counts were higher in Kowie Thicket (KT) during summer season (2.05 ± 0.01 and 1.00 ± 0.09, respectively) compared to Bedford Dry Grassland (BDG) and Bhisho Thornveld (BT) veld types. In all vegetation types, R. appendiculatus had higher counts in KT in spring (0.91 ± 0.08), summer (0.78 ± 0.08) and winter (0.78 ± 0.08). Rhipicephalus (Boophilus) decoloratus was more frequent in the BT (1.78 ± 0.11) during the summer season. BDG had lower tick infestation with R. evertsi evertsi being the most frequent species in summer. No H. rufipes was collected in the KT. Of epidemiological interest, R. (B.) microplus was absent in the study area which needs further investigation. Within the context of this study, we found agro-ecological differences and seasonal variations to have influence on tick species distribution.

Keywords

Agro-ecological zones Cattle Eastern Cape Province Season Tick distribution 

Notes

Acknowledgements

We sincerely thank the Eastern Cape Department of Rural Development and Agrarian Reform (DRDAR) for allowing us to use its facilities and animals for the success of this study. A special thank you goes to the staff and colleagues at the Department of Livestock and Pasture, University of Fort Hare, who provided moral and intellectual support throughout the study. Lastly, we value the financial support from National Research Foundation (NRF) (Grant Number: 102941) for this study. The grant holder acknowledges that opinions, findings and conclusions or recommendations expressed in any publication generated by the NRF-supported research are those of the authors and are not necessarily to be attributed to the NRF.

References

  1. Abera B, Biadegelgen F, Bezabih B (2010) Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar Town, Northwest Ethiopia. Ethiop J Health Dev 24:55–68Google Scholar
  2. Allsopp BA (2015) Heartwater-Ehrlichia ruminantium infection. Rev Sci Tech Off Int Epiz 34:557–568CrossRefGoogle Scholar
  3. Allsopp MT, Allsopp BA (2006) Molecular sequence evidence for the reclassification of some Babesia species. Ann N Y Acad Sci 1081:509–517CrossRefPubMedGoogle Scholar
  4. Allsopp MT, Van Strijp MF, Faber E, Josemans AI, Allsopp BA (2007) Ehrlichia ruminantium variants which do not cause heartwater found in South Africa. Vet Microbiol 120:158–166CrossRefPubMedGoogle Scholar
  5. Apanaskevich DA, Horak IG, Camicas JL (2007) Rediscription of Haemaphysalis (Rhipistoma) elliptica (Koch, 1844), an old taxon of the Haemaphysalis (Rhipistoma) leachi group from East and southern Africa, and of Haemaphysalis (Rhipistoma) leachi (Audouin, 1826) (Ixodida, Ixodidae). Onderstepoort J Vet Res 74:181–208CrossRefPubMedGoogle Scholar
  6. Awa DN, Adakal H, Luogboua NDD, Wachonga KHI, Leinyuya I, Achukwi MD (2015) Cattle ticks in Cameroon: is Rhipicephalus (Boophilus) microplus absent in Cameroon and the Central African region? Ticks Tick Borne Dis 6:117–122CrossRefPubMedGoogle Scholar
  7. Aydin MF, Aktas M, Dumanli N (2015) Molecular identif ication of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey. Parasitol Res 114:65–69CrossRefPubMedGoogle Scholar
  8. Begum RA, Siwar C, Abidin RDZRZ, Pereira JJ (2011) Vulnerability of climate change and hardcore poverty in Malaysia. Environ Sci Technol 4:112–117CrossRefGoogle Scholar
  9. Braack LEO, Horak IG, Jordaan Leonora C, Segerman J, Louw JP (1996) The comparative host status of red veld rats (Aethomys chrysophilus) and bushveld gerbils (Tatera leucogaster) for epifaunal arthropods in the southern Kruger National Park, South Africa. Onderstepoort J Vet Res 63:149–158PubMedGoogle Scholar
  10. Bryson NR, Tice GA, Horak IG, Stewart CG, Du Plessis BJA (2002) Ixodid ticks on indigenous goats owned by small-scale farmers in four communal grazing areas in South Africa. J S Afr Vet Assoc 73:26–30PubMedGoogle Scholar
  11. Cahn CM, Line S (2005) The Merck veterinary manual, vol 78. Merck Sharp & Dohme Corp, Whitehouse Station, pp 441–1128Google Scholar
  12. Cummings GS (2002) Comparing climate and vegetation as limiting factors for species ranges of African ticks. Ecology 83:255–268CrossRefGoogle Scholar
  13. Dantas-Torres F, Figueredo LA, Otranto D (2011) Seasonal variation in the effect of climate on the biology of Rhipicephalus sanguineus in southern Europe. Parasitoloy 138:527–536CrossRefGoogle Scholar
  14. De Castro JJ (1997) Sustainable tick and disease control in livestock improvement in developing countries. Vet Parasitol 71:77–97CrossRefPubMedGoogle Scholar
  15. Eastern Cape Socio-Economic Consultative Council (ECSECC) (2012) Eastern Cape Development Indicators—2012. http://www.ecsecc.org/files/library/documents/EasternCape_withDMs.pdf. Accessed 25 Oct 2016
  16. Estrada-Peña A (2003) Climate change decreases habitat suitability for some tick species (Acari: Ixodidea) in South Africa. Onderstepoort J Vet Res 70:79–93PubMedGoogle Scholar
  17. Eygelaar D, Jori F, Mokopasetso M, Sibeko KP, Collins NE, Vorster I, Troskie M, Oosthuizen MC (2015) Tick-borne haemoparasites in African buffalo (Syncerus caffer) from two wildlife areas in Northern Botswana. Parasitol Vectors 8:26CrossRefGoogle Scholar
  18. Gallivivan GJ, Spickett A, Heyne H, Spickett AM, Horak IG (2011) The dynamic of questing ticks collected for 164 consecutive months off the vegetation of two landscape zones in the Kruger National Park (1988–2002). Part III. The less commonly collected species. Onderstepoort J Vet Res 78:41–49Google Scholar
  19. Geeta P, Daya S, Amit KJ, Vikrant S, Santosh KV (2013) Prevalence and seasonal variation in ixodid ticks on buffaloes of Mathura District, Uttar Pradesh, India. Parasitology 34:1–7Google Scholar
  20. Horak IG (1999) Parasites of domestic and wild animals in South Africa. XXXVII. Ixodid ticks on cattle on Kikuyu grass pastures and in Valley Bushveld in the Eastern Cape Province. Onderstepoort J Vet Res 66:175–184PubMedGoogle Scholar
  21. Horak IG, Jacot G, Moolman LC, De Vos V (1987) Parasites of domestic and wild animals in South Africa. XXII. Ixodid ticks on domestic dogs and on wild carnivores. Onderstepoort J Vet Res 54:573–580PubMedGoogle Scholar
  22. Horak IG, Fourie LJ, Novellie PA, Williams EJ (1991) Parasites of domestic and wild animals in South Africa. XXVI. The mosaic of ixodid tick infestations on birds and mammals in the Mountain Zebra National Park. Onderstepoort J Vet Res 58:125–136PubMedGoogle Scholar
  23. Horak IG, Boomker J, Spickett AM, De Vos V (1992) Parasites of domestic and wild animals in South Africa. XXX. Ectoparasites of kudus in the eastern Transvaal Lowveld and the Eastern Cape Province. Onderstepoort J Vet Res 59:259–273PubMedGoogle Scholar
  24. Horak IG, Braack LEO, Fourie LJ, Walker JB (2000) Parasites of domestic and wild animals in South Africa. XXXVIII. Ixodid ticks collected from 23 wild carnivore species. Onderstepoort J Vet Res 67:239–250PubMedGoogle Scholar
  25. Horak IG, Nyangiwe N, De Matos C, Neves L (2009) Species composition and geographic distribution of ticks infesting cattle, goats and dogs in a temperate and a subtropical coastal region of south-eastern Africa. Onderstepoort J Vet Res 76:263–278PubMedGoogle Scholar
  26. Horak IG, Gallivan GJ, Spickett AM (2011) The dynamics of questing ticks collected for 164 consecutive months off the vegetation of two landscape zones in the Kruger National Park (1988–2002). I. Total ticks, Amblyomma hebraeum and Rhipicephalus decoloratus. Onderstepoort J Vet Res 78:32–44PubMedGoogle Scholar
  27. Howell CJ, Walker JB, Nevill EM (1978) Ticks, mites and insects infesting domestic animals in South Africa. Part 1. Descriptions and biology. Pretoria: department of Agricultural Technical Services, Republic of South Africa. Sci Bull 393:69Google Scholar
  28. Ikpeze O O (2012) Ecology of ticks (Acarina: Ixodidae) on cattle in Nnamdiazikiwe University, Awka Anambra State, Nigeria. Ph.D. thesis Department of Parasitology and Entomology Faculty of Biosciences Nnamdi Azikiwe University, Awka. Advances Bioresearch 7: 124–131Google Scholar
  29. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129(Suppl):S3–S14PubMedGoogle Scholar
  30. Katiyatiya CLF, Muchenje V, Mushunje A (2014) Farmers’ perceptions and knowledge of cattle adaptation to heat stress and tick resistance in the Eastern Cape, South Africa. Asian-Australas J Anim Sci 27:16–63CrossRefGoogle Scholar
  31. Knust B, Medetov ZB, Kyraubayev KB, Bumburidi Y, Erickson BR, MacNeil A, Nichol ST, Bayserkin BS, Ospanov KS (2012) Crimean-Congo Hemorrhagic Fever, Kazakhstan, 2009–2010. Emerg Infect Dis 18:643–655CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lindström A, Jaenson TGT (2003) Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. J Med Entomol 40:375–378CrossRefPubMedGoogle Scholar
  33. Lynen G, Zeman P, Bakuname C, Di Giulio G, Mtui P, Sanka P, Jongejan F (2008) Shifts in the distributional changes of Boophilus ticks, in Tanzania: evidence that a parapatric boundary between Boophilus microplus and Boophilus decoloratus follows climate gradients. Exp Appl Acarol 44:147–164CrossRefPubMedGoogle Scholar
  34. Madder M, Thys E, Geysen D, Baudoux C, Horak I (2007) Boophilus microplus ticks found in West Africa. Exp Appl Acarol 43:233–234CrossRefPubMedGoogle Scholar
  35. Madder M, Thys E, Achi L, Touré A, De Deken R (2011) Rhipicephalus (Boophilus) microplus: a most successful invasive tick species in West-Africa. Exp Appl Acarol 53:139–145CrossRefPubMedGoogle Scholar
  36. Marcelino I, De Almedia AM, Ventosa M, Pruneau L, Meyer DF, Martinez D, Lenfrancois T, Vachiery N, Coelho AV (2012) Tick borne disease in cattle: applications of proteomics to develop new generation vaccines. J Proteom Bioinform 7:4232–4250Google Scholar
  37. Marufu MC, Chimonyo M, Mapiye C, Dzama K (2011) Tick loads in cattle raised on sweet and sour rangelands in the low-input farming areas of South Africa. Trop Anim Health Prod 43:307–313CrossRefPubMedGoogle Scholar
  38. Mashebe P, Lyaku JR, Mausse F (2014) Occurrence of ticks and tick-borne diseases of livestock in Zambezi region: a review. J Agric Sci 6:142–147Google Scholar
  39. Mohammed M, Tukur SM, Watanabe M, ABD-RANI PAM, Lau SF, Shettima YL, Watanabe M (2016) Factors Influencing the prevalence and distribution of ticks and tick- borne pathogens among domestic animals in Malaysia. Pertanika J Schol Res Rev 2:12–22Google Scholar
  40. Moorling MS, Mazhowu W, Scott CA (2004) The effect of rainfall on tick challenge at Kyle Recreational Park, Zimbabwe. Exp Appl Acarol 18:507–520CrossRefGoogle Scholar
  41. Moyo B, Masika PJ (2008) Tick control methods used by resource-limited farmers and the effect of ticks in cattle in rural areas of the Eastern Cape Province, South Africa. Trop Anim Health Prod 41:517–523CrossRefPubMedGoogle Scholar
  42. Muchenje V, Dzama K, Chimonyo M, Raats JG, Strydom PE (2008) Tick susceptibility and its effects on growth performance and carcass characteristics on Nguni, Bonsmara and Angus steers raised on natural pasture. Anim Sci 2:298–304Google Scholar
  43. Mucina L, Hoare DB, Lötter MC, du Preez PJ, Rutherford MC, Scott-Shaw CR, Bredenkamp GJ, Powrie LW, Scott L, Camp KGT, Cilliers SS, Bezuidenhout H, Mostert TH, Siebert SJ, Winter PJD, Burrows JE, Dobson L, Ward RA, Stalmans M, Oliver EGH, Siebert F, Schimidt E, Kobisi K, Kose L, Smit JHL, Goodman PS, Ellis F, Henning BJ, Venter CE, Matthews WS, van Rooyen N, Williamson S, Hurter PJH, Vlok JHJ, Euston-Brown DIW, Palmer AR, Lechmere-Oertel RG, Proches SM, Dold AP, Ward RA (2006) Grassland Biome, Savanna biome and Albany Thicket Biome. In: Mucina L, Rutherford MC (eds) The vegetation of South Africa, Lesotho and Swaziland, vol 19. South African National Biodiversity Institute, Pretoria, pp 347–558Google Scholar
  44. Mulonga S, Suich H, Murphy C (2003) DEA Research Discussion Paper Number 59: The conflict continues: human wildlife conflict and livelihoods in Caprivi. http://www.dea.met.gov.na. Accessed 4 Oct 2017
  45. Nijhof AM, Bodaan C, Postigo M, Nieuwenhuijs H, Opsteegh M, Franssen L, Jebbink F, Jongejan F (2007) Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector Borne Zoonotic Dis 7:585–596CrossRefPubMedGoogle Scholar
  46. Norval RAI, Horak IG (2004) Vectors: ticks. In: Coetzer JAW, Tustin RC (eds) Infectious diseases of livestock. Oxford University Press, Cape Town, pp 3–42Google Scholar
  47. Norval RAI, Mason CA (1981) The transfer of Boophilus microplus (Acarina, Ixodidae) from infested to uninfested cattle under field conditions. Vet Parasitol 8:185–188CrossRefGoogle Scholar
  48. Norval RAI, Perry BD, Young AS (1992) The epidemiology of theileriosis in Africa. Academic Press, LondonGoogle Scholar
  49. Norval RAI, Sutherst RW, Kerr JD (1996) Infestations of the bont tick Amblyomma hebraeum (Acari: Ixodidae) on different breeds of cattle in Zimbabwe. Exp Appl Acarol 20:599–605CrossRefPubMedGoogle Scholar
  50. Nyangiwe N, Horak IG (2007) Goats as alternative hosts of cattle ticks. Onderstepoort J Vet Res 74:1–7CrossRefPubMedGoogle Scholar
  51. Nyangiwe N, Horak IG, Bryson NR (2006) Ixodid ticks on dogs in the eastern region of the Eastern Cape Province, South Africa. Onderstepoort J Vet Res 73:305–309PubMedGoogle Scholar
  52. Nyangiwe N, Goni S, Hervé-Claude LP, Ruddat I, Horak IG (2011) Ticks on pastures and on two breeds of cattle in the Eastern Cape Province, South Africa. Onderstepoort J Vet Res 78:1–9CrossRefGoogle Scholar
  53. Nyangiwe N, Harrison A, Horak IG (2013) Displacement of Rhipicephalus decoloratus by Rhipicephalus microplus (Acari: Ixodidae) in the Eastern Cape Province, South Africa. Exp Appl Acarol 61:371–382CrossRefPubMedGoogle Scholar
  54. Nyangiwe N, Horak IG, Van der Mescht L, Sonja M (2017) Range expansion of the economically important Asiatic blue tick, Rhipicephalus microplus, in South Africa. J S Afr Vet Assoc 88:a1482.  https://doi.org/10.4102/jsava.v88i0.1482 CrossRefGoogle Scholar
  55. Okello-Onen J, Tukahirwa EM, Perry BD, Rowlands GJ, Nagda SM, Musisi G, Bode E, Heinonen R, Mwayi W, Opuda-Asibo J (1999) Population dynamics of ticks on indigenous cattle in a pastoral dry to semi-arid rangeland zone of Uganda. Exp Appl Acarol 23:79–88CrossRefPubMedGoogle Scholar
  56. Olwoch JM, Rautenbach CJW, Erasmus BFN, Engelbrecht BFA, Jaarsveld AS (2003) Simulating tick distributions over sub-Saharan Africa: the use of observed and simulates climate surfaces. J Biogeogr 30:1221–1232CrossRefGoogle Scholar
  57. Ostfeld RS, Keesing F (2012) Effects of host diversity on infectious disease. Annu Rev Ecol Evol Syst 43:157–182CrossRefGoogle Scholar
  58. Petney TN, Horak IG, Howell DJ, Meyer S (2004) Striped mice, Rhabdomys pumilio, and other murid rodents as hosts for immature ixodid ticks in the Eastern Cape Province. Onderstepoort J Vet Res 71:313–318CrossRefPubMedGoogle Scholar
  59. Ruiz-Fons F, Gilbert L (2010) The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. Int J Parasitol 40:1013–1020CrossRefPubMedGoogle Scholar
  60. SAS (Statistical Analysis System) (2003) Statistical Analysis System Institute Inc. Users Guide, Version 9, Carry, NC, USAGoogle Scholar
  61. Scholtz MM, Spickett AM, Lombard PE, Enslin CB (1991) The effect of tick infestation on the productivity of cows of three breeds of cattle. Onderstepoort J Vet Res 58:71–74PubMedGoogle Scholar
  62. Schroder B, Uys AC, Reilly BK (2006) A survey of free-living ixodid ticks on a commercial game farm in the Thabazimbi District, Limpopo Province, South Africa. J S Afr Vet Assoc 77:141–144CrossRefPubMedGoogle Scholar
  63. Sungirai M, Madder M, Moyo DZ, De Clercq P, Abatih EN (2015) An update on the ecological distribution of the Ixodidae ticks in Zimbabwe. Exp Appl Acarol 66:269–280CrossRefPubMedGoogle Scholar
  64. Tack W, Madder M, Baeten L, Vanhellemont GR, Verheyn K (2012) Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. Forest Ecol Manag 265:30–36CrossRefGoogle Scholar
  65. Tønnesen MH, Penzhorn BL, Bryson NR, Stoltsz WH, Masibigiri T (2004) Displacement of Boophilus decoloratus by Boophilus microplus in the Soutpansberg region, Limpopo Province, South Africa. Exp Appl Acarol 32:199–208CrossRefPubMedGoogle Scholar
  66. Walker AR, Bouattour A, Camicas JL, Estrada-Pena A, Horak IG, Latif A, Pegram RG, Preston PM (2003) Ticks of domestic animals in Africa. A guide to identification of species. Biosci Rep 157:1–179Google Scholar
  67. Walker JB, Keirans JE, Horak IG (2000) The genus Rhipicephalus (Acari, Ixodidae): a guide to the brown ticks of the world. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  68. Wolde A, Mohamed A (2014) Prevalence of Ixodid ticks on bovine in Soddo Zuria Districts, Wolaita Zone, Ethiopia. Acta Parasitol Glob 5:188–197Google Scholar
  69. Zhang J, Kelly P, Guo W, Xu C, Wei L, Jongejan F, Loftis A, Wang C (2015) Development of a generic Ehrlichia FRET-qPCR and investigation of ehrlichioses in domestic ruminants on five Caribbean islands. Parasitol Vectors 8:506–512CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Livestock and Pasture Science, Faculty of Science and AgricultureUniversity of Fort HareAliceSouth Africa
  2. 2.Dohne Agricultural Development InstituteStutterheimSouth Africa
  3. 3.Faculty of Veterinary SciencesUniversity of PretoriaOnderstepoortSouth Africa

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