Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Influence of Massive and Long Distance Migration on Parasite Epidemiology: Lessons from the Great Wildebeest Migration

Abstract

Very little is known about the influence of massive and long distance migration on parasite epidemiology. Migration can simultaneously minimize exposure to common parasites in their habitats and increase exposure to novel pathogens from new environments and habitats encountered during migration, while physiological stress during long distance movement can lead to immune suppression, which makes migrants vulnerable to parasites. In this paper, we investigated the diversity, prevalence, parasite load, co-infection patterns and predilection sites of adult gastrointestinal helminths in 130 migrating wildebeests and tested for their relation with animal age, sex and migration time (which also could indicate different migration routes), and compared them with the non-migratory wildebeest. Surprisingly, only four parasite species were found, Oesophagostomum columbianum, Haemonchus placei, Calicophoron raja and Moniezia expansa, which were lower than in non-migratory wildebeest reported in the literature. These parasites were generalists, infecting livestock, and suggests that wildebeest and livestock, because of their interaction during migration, have a cross-infection risk. There was a negative relation between parasites diversity, prevalence and intensity of infection, and host age, which suggests that wildebeests acquire protective immunity against these parasites as they get older. Prevalence and intensity of infection were higher among wildebeest crossing the Mara Bridge (early migrants) compared to those crossing the Serena (late migrants), which suggests that early migrants (or migrants originating from different areas) have varying infection intensities. The prevalence and intensity of infection were higher in males compared to females and may be due to ecological, behavioural, or physiological differences between males and females. Our findings compared to those of previous studies suggest that migration may provide a mechanism to minimize exposure of hosts to common parasites through migratory escape, but this result awaits examination of helminths epidemiology of non-migratory wildebeests from areas of migrant origins. The potential parasitic cross-infection between wildebeests and livestock is a real risk to be taken into account in the management of wildebeest migration corridors.

This is a preview of subscription content, log in to check access.

Figure 1
Figure 2
Figure 3

Abbreviations

MMNP:

Masai mara national reserve

GIT:

Gastro-intestinal tract

GLM:

General linear model

KWS:

Kenya wildlife service

References

  1. Altizer, S., R. Bartel, and B. A. Han. 2011. Animal migration and infectious disease risk. Science 331:296-302.

  2. Attwell, C. A. M. 1980. Age determination of the blue wildebeest Connochaetes taurinus in Zululand. South African Journal of Zoology 15:121-130.

  3. Avgar, T., G. Street, and J. Fryxell. 2013. On the adaptive benefits of mammal migration. Canadian Journal of Zoology 92:481-490.

  4. Baird, J. K. 1998. Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Ann Trop Med Parasitol 92:367-390.

  5. Beveridge. 1994. Family Anoplocephalidae Cholodkovsky, 1902. Pages 315-366. in L. F. Khalil, A. Jones, and R. A. Bray, editors. Keys to the Cestode Parasites of Vertebrates. CABI Publishing, Wallingford.

  6. Cattadori, I. M., R. Albert, and B. Boag. 2007. Variation in host susceptibility and infectiousness generated by co-infection: the myxoma–Trichostrongylus retortaeformis case in wild rabbits. Journal of the Royal Society Interface 4:831-840.

  7. Cobey, S., and M. Lipsitch. 2013. Pathogen diversity and hidden regimes of apparent competition. The American naturalist 181:12.

  8. Crompton, D. W. T. 1973. The sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews 48:27-83.

  9. Dash, K. 1973. The life cycle of Oesophagostomum columbianum (Curtice, 1890) in sheep. International Journal for Parasitology 3:843-851.

  10. Dobson, R. J., and E. H. Barnes. 1995. Interaction between Ostertagia circumcincta and Haemonchus contortus infection in young lambs. International Journal for Parasitology 25:495-501.

  11. Dobson, R. J., E. H. Barnes, and R. G. Windon. 1992. Population dynamics of Trichostrongylus colubriformis and Ostertagia circumcincta in single and concurrent infections. International Journal for Parasitology 22:997-1004.

  12. Dube, S., A. Siwela, K. Masanganise, and C. Dube. 2004. Abattoir studies on paramphistomes recovered from cattle from Maswingo and Manicaland provinces of Zimbabwe. Folia Vet 48:123-129.

  13. Durette-Desset, M. C. 1983. No. 10. Keys to genera of the superfamilies Trichistrongyroidea. in C. A. Anderson RC, Willmott S editor. CIH Keys to the Nematode Parasites of Vertebrates. Commonwealth Agricultural Bureaux, Farnham Royal, England.

  14. Eduardo, S. 1983. The taxonomy of the family Paramphistomidae Fischoeder, 1901 with special reference to the morphology of species occurring in ruminants. III. Revision of the genus Calicophoron Näsmark, 1937. Systematic Parasitology 5:25-79.

  15. Fenton, A., and S. E. Perkins. 2010. Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137:1027-1038.

  16. Folstad, I., A. C. Nilssen, O. Halvorsen, and J. Andersen. 1991. Parasite avoidance: the cause of post-calving migrations in Rangifer? Canadian Journal of Zoology 69:2423-2429.

  17. Galvani, A. P. 2005. Age-Dependent Epidemiological Patterns and Strain Diversity in Helminth Parasites. The Journal of Parasitology 91:24-30.

  18. Graham, A. L. 2008. Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences 105:566-570.

  19. Hausfater, G., and B. J. Meade. 1982. Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates 23:287-297.

  20. Hawley, D. M., and S. M. Altizer. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25:48-60.

  21. Holdo, R. M., R. D. Holt, and J. M. Fryxell. 2009. Opposing rainfall and plant nutritional gradients best explain the wildebeest migration in the Serengeti. The American Naturalist 173:431-445.

  22. Horak, I., V. De Vos, and M. R. Brown. 1983. Parasites of domestic and wild animals in South Africa. XVI. Helminth and arthropod parasites of blue and black wildebeest (Connochaetes taurinus and Connochaetes gnou). Onderstepoort Journal of Veterinary Research 50:243-255.

  23. Horak, I., D. Meltzer, and V. De Vos. 1982. Helminth and arthropod parasites of springbok, Antidorcas marsupialis, in the Transvaal and western Cape Province. Onderstepoort Journal of Veterinary Research 49:7-10.

  24. Johns, S., and A. K. Shaw. 2016. Theoretical insight into three disease-related benefits of migration. Population Ecology 58:213-221.

  25. Jones, A. 2005. Family Fasciolidae Railliet, 1895. Keys to the Trematoda, Vol. 2. CABI Publishing, Wallingford, 79-85. Pages 79-85 in Jones A., Bray RA, and Gibson. D.I., editors. Keys to the Trematoda, Vol. 2.. CABI Publishing,, Wallingford.

  26. Junker, K., I. G. Horak, and B. Penzhorn. 2014. History and development of research on wildlife parasites in southern Africa, with emphasis on terrestrial mammals, especially ungulates. International Journal for Parasitology: Parasites and Wildlife. 4 50-70.

  27. Kloosterman, A., G. A. A. Albers, and R. Van den Brink. 1984. Negative interactions between Ostertagia ostertagi and Cooperia oncophora in calves. Veterinary parasitology 15:135-150.

  28. Kloosterman, A., and K. Frankena. 1988. Interactions between lungworms and gastrointestinal worms in calves. Veterinary parasitology 26:305-320.

  29. Kloosterman, A., H. W. Ploeger, and K. Frankena. 1990. Increased establishment of lungworms after exposure to a combined infection of Ostertagia ostertagi and Cooperia oncophora. Veterinary parasitology 36:117-122.

  30. Kloosterman, A., H. W. Ploeger, and K. Frankena. 1991. Age resistance in calves to Ostertagia ostertagi and Cooperia oncophora. Veterinary parasitology 39:101-113.

  31. Lichtenfels, J. R. 1980. Keys to genera of the superfamilies Strongyroidea. In: Anderson R.C, Chabaud A.G, and Willmott S, editors. CIH Keys to the Nematode Parasites of Vertebrates. Commonwealth Agricultural Bureaux., Farnham Royal.

  32. Lichtenfels, J. R., P. A. Pilitt, and P. Hoberg. 1994. New morphological characters for identifying individual specimens of Haemonchus spp. (Nematoda: Trichostrongyloidea) and a key to species in ruminants of North America. Journal of Parasitology 78:E1-E11.

  33. Lo, C. M., S. Morand, and R. Galzin. 1998. Parasite diversity\host age and size relationship in three coral-reef fishes from French Polynesia. International Journal for Parasitology 28:1695-1708.

  34. Lone, B. A., M. Z. Chisti, F. Ahmad, and H. Tak. 2011. Serodiagnosis of Oesophagostomum Columbianum infection in Goats using indirect ELISA. Vet World 4:503-506.

  35. Mideo, N. 2009. Parasite adaptations to within-host competition. Trends in parasitology 25:261-268.

  36. Mijele, D., V. Obanda, P. Omondi, R. C. Soriguer, F. Gakuya, M. Otiende, P. Hongo, and S. Alasaad. 2013. Spatio-temporal distribution of injured elephants in Masai Mara and the putative negative and positive roles of the local community. PloS one 8:e71179.

  37. Mutapi, F., R. Burchmore, T. Mduluza, N. Midzi, C. M. R. Turner, and R. M. Maizels. 2008. Age-Related and Infection Intensity-Related Shifts in Antibody Recognition of Defined Protein Antigens in a Schistosome-Exposed Population. Journal of Infectious Diseases 198:167-175.

  38. Nwosu, C. O., A. F. Ogunrinade, and B. O. Fagbemi. 1996. Prevalence and seasonal changes in the gastro-intestinal helminths of Nigerian goats. Journal of Helminthology 70:329-333.

  39. Pedersen, A. B., and A. Fenton. 2007. Emphasizing the ecology in parasite community ecology. Trends in ecology & evolution 22:133-139.

  40. Peyerl-Hoffmann, G., T. Jelinek, A. Kilian, G. Kabagambe, W. G. Metzger, and F. Von Sonnenburg. 2001. Genetic diversity of Plasmodium falciparum and its relationship to parasite density in an area with different malaria endemicities in West Uganda. Tropical Medicine & International Health 6:607-613.

  41. Pfukenyi, D. M., S. Mukaratirwa, A. L. Willingham, and J. Monrad. 2005. Epidemiological studies of amphistome infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research 72:p. 67-86.

  42. Piersma, T. 1997. Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80 623-631.

  43. Ploeger, H. W., A. Kloosterman, and F. W. Rietveld. 1995. Acquired immunity against Cooperia spp. and Ostertagia spp. in calves: effect of level of exposure and timing of the midsummer increase. Veterinary parasitology 58:61-74.

  44. Popova, T. I. 1958. Essentials of Nematodology Vol. VII. Strongyloids of Animals and Man: Trichonematidae.. Academy of Science of the USSR, (Translated by ArtmanM., Israel Program for Scientific Translations (1965)), Moscow.

  45. Poulin, R. 1996. Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147 287-295.

  46. R Core Team. 2014. R: a language and environment for statistical computing, Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.3

  47. Roeber, F., A. R. Jex, and R. B. Gasser. 2013. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance-an Australian perspective. Parasites Vectors 6:153.

  48. Schmidt, G. D. 1986. CRC handbook of tape worm identification. CRC Press, Boca Raton, Florida, pp 675

  49. Sutherland, I., and I. Scott. 2009. Gastrointestinal nematodes of sheep and cattle: biology and control. John Wiley & Sons, Chichester

  50. Talbot, L. M., and M. H. Talbot (1963) Vol 12, The Wildebeest in Western Masailand East Africa Wildlife Monographs. Wiley, New York, pp 3-88.

  51. Tariq, K. A., M. Z. Chishti, F. Ahmad, and A. S. Shawl. 2008. Epidemiology of gastrointestinal nematodes of sheep managed under traditional husbandry system in Kashmir valley. Veterinary parasitology 158:138-143.

  52. Telfer, S., X. Lambin, R. Birtles, P. Beldomenico, S. Burthe, S. Paterson, and M. Begon. 2010. Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243-246.

  53. Ulrich, Y., and P. Schmid-Hempel. 2012. Host modulation of parasite competition in multiple infections. Proceedings of the Royal Society B: Biological Sciences 279:2982-2989.

  54. Zuk, M., and K. A. McKean. 1996. Sex differences in parasite infections: patterns and processes. International journal for parasitology 26:1009-1024.

Download references

Acknowledgments

The authors wish to thank the Director of Kenya Wildlife Service (KWS) and all the staff at KWS veterinary department for their assistance in data collection and analysis. We thank the Masai Mara National Reserve management particularly Dr. Asuka Takita and Mr. Brian Heath for their help in locating dead wildebeests along the Mara River and assisting in parasites samples collection. The authors thank Dr. Eberhard Zehle from the Africa Medical Research Foundation (AMREF) for helping in wildebeest post-mortem and collection of parasite samples. The authors also thank KWS for funding the research, and Sophia Masila for editing the manuscript.

Authors’ Contributions

DM, PC, MO, SA, and TI conceived and designed the experiments for the paper. DM, PC, VO, LR, RCS, LR, RCS, SA have been involved in drafting the manuscript or revising it critically for important intellectual content. Manuscript was analyzed, discussed and written by all co-authors. All authors read and approved the final manuscript.

Author information

Correspondence to Domnic Mijele or Samer Angelone-Alasaad.

Ethics declarations

Conflict of interest

The authors declare that there were no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1. Images showing identification features of the four gastrointestinal parasites of wildebeest. A is a whole worm of M. expansa, B is a scolex of M. expansa after pressing and staining, C is a whole body of C. raja, D is the whole C. raja worm flattened and cleared, E is the genital atrium of C. raja hand sectioned and cleared, F is the head end of O. columbianum with corona radiate, G is the tail of a male O. columbianum showing bursa and spicules, H shows the tail of female O. columbianum with vulva, I shows the tail of a male H. placei, and J shows a cross section of a female H. placei at about ¼ of body length from head end. Figure S2. Predilection sites in the gastrointestinal parasites for the common adult helminths infecting migratory wildebeests. Supplementary material 1 (DOCX 377 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mijele, D., Iwaki, T., Chiyo, P.I. et al. Influence of Massive and Long Distance Migration on Parasite Epidemiology: Lessons from the Great Wildebeest Migration. EcoHealth 13, 708–719 (2016). https://doi.org/10.1007/s10393-016-1156-2

Download citation

Keywords

  • gastrointestinal helminthes
  • Serengeti-Mara ecosystem
  • Oesophagostomum columbianum
  • Haemonchus placei
  • Calicophoron raja
  • Moniezia expansa
  • co-infection
  • parasite competition
  • parasite predilection sites
  • parasite load