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Gastrointestinal parasites in relation to host traits and group factors in wild meerkats Suricata suricatta

Published online by Cambridge University Press:  20 February 2014

SARAH LECLAIRE*
Affiliation:
Department of Zoology, University of Cambridge, UK Kalahari Meerkat Project, Kuruman River Reserve, 8467 Van Zylsrus, Northern Cape, South Africa CNRS, Université Toulouse 3 Paul Sabatier, ENFA; UMR5174 EDB (Laboratoire évolution et Diversité Biologique); 118 route de Narbonne, 31062 Toulouse, France
CHARLES T. FAULKNER
Affiliation:
College of Veterinary and Comparative Medicine, Lincoln Memorial University, 6965 Cumberland Gap Parkway, Harrogate, TN 37752, USA
*
*Corresponding author: Present address: Laboratoire Ecologie et Evolution UMR7625 – 7 quai St Bernard – 75252 Paris Cedex 5 – France. E-mail: sarah.leclaire@free.fr

Summary

Meerkats are one of the most endearing of South African's wildlife celebrities and one of the most highly studied social mammals. However, although parasites are widely recognized as important regulatory factors in animal population, basic knowledge on meerkats’ parasites is lacking. Here 100 fresh fecal samples of wild meerkats were examined for the presence of endoparasitic infection. Endoparasitic taxa identified by the presence of eggs or oocysts included Toxocara suricattae, Oxynema suricattae, Pseudandrya suricattae, Cystoisospora sp. and Eimeria sp. Non-specific diagnoses were made for parasites in the Order Strongylida, Order Spirurida and coccidian based on the morphology and size of the eggs and oocysts. The prevalence of infection with T. suricattae and the strongylate species increased with age, while prevalence of coccidia and intensity of infection by the strongylate species increased with decreasing group size, suggesting that stress associated with living in smaller group may increase susceptibility to parasitism. Moreover, parasite communities were more similar between individuals from the same group than between individuals from different groups, suggesting an important role of the environment in parasite infestation. We did not detect any differences between males and females. This study represents the first detailed report of gastrointestinal parasites in wild meerkats, and is a key starting point for future studies on the effect of endoparasite load in the life history of this species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics 5, 325383.Google Scholar
Alzaga, V., Vicente, J., Villanua, D., Acevedo, P., Casas, F. and Gortazar, C. (2008). Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behavioral Ecology and Sociobiology 62, 769775. doi: 10.1007/s00265-007-0502-3.Google Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219247. doi: 10.2307/3933.Google Scholar
Baer, J. G. (1959). Helminthes Parasites. Institut des Parcs Nationaux du Congo Belge. Missions J.G. Baer – W. Gerber (1958). Fasc. 1. Brussels.Google Scholar
Bateman, A. W., Ozgul, A., Nielsen, J. F., Coulson, T. and Clutton-Brock, T. H. (2013). Social structure mediates environmental effects on group size in an obligate cooperative breeder, Suricata suricatta . Ecology 94, 587597.Google Scholar
Becker, A. C., Rohen, M., Epe, C. and Schnieder, T. (2012). Prevalence of endoparasites in stray and fostered dogs and cats in Northern Germany. Parasitology Research 111, 849857. doi: 10.1007/s00436-012-2909-7.Google Scholar
Behnke, J. M., Lewis, J. W., Mohd Zain, S. and Gilbert, F. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 3144.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.Google Scholar
Castinel, A., Duignan, P. J., Lyons, E. T., Pomroy, W. E., Gibbs, N., López-Villalobos, N., Chilvers, B. L. and Wilkinson, I. S. (2007). Epidemiology of hookworm (Uncinaria spp.) infection in New Zealand (Hooker's) sea lion (Phocarctos hookeri) pups on Enderby Island, Auckland Islands (New Zealand) during the breeding seasons from 1999/2000 to 2004/2005. Parasitology Research 101, 5362. doi: 10.1007/s00436-006-0453-z.Google Scholar
Clutton-Brock, T. H., Gaynor, D., Kansky, R., MacColl, A. D. C., McIlrath, G. M., Chadwick, P., Brotherton, P. N. M., O'Riain, J. M., Manser, M. and Skinner, J. D. (1998). Costs of cooperative behaviour in suricates (Suricata suricatta). Proceedings of the Royal Society B – Biological Sciences 265, 185190.Google Scholar
Clutton-Brock, T. H., Gaynor, D., McIlrath, G. M., Maccoll, A. D. C., Kansky, R., Chadwick, P., Manser, M., Skinner, J. D. and Brotherton, P. N. M. (1999). Predation, group size and mortality in a cooperative mongoose, Suricata suricatta . Journal of Animal Ecology 68, 672683. doi: 10.1046/j.1365-2656.1999.00317.x.CrossRefGoogle Scholar
Clutton-Brock, T. H., Russell, A. F., Sharpe, L. L., Young, A. J., Balmforth, Z. and McIlrath, G. M. (2002). Evolution and development of sex differences in cooperative behavior in meerkats. Science 297, 253256.Google Scholar
Clutton-Brock, T. H., Hodge, S. J. and Flower, T. P. (2008). Group size and the suppression of subordinate reproduction in Kalahari meerkats. Animal Behaviour 76, 689700.Google Scholar
Côté, I. M. and Poulin, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159165.Google Scholar
Doolan, S. P. and Macdonald, D. W. (1996). Dispersal and extra-territorial prospecting by slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari. Journal of Zoology 240, 5973.Google Scholar
Doolan, S. P. and Macdonald, D. W. (1997). Band structure and failures of reproductive suppression in a cooperatively breeding carnivore, the slender-tailed meerkat (Suricata suricatta). Behaviour 134, 827848. doi: 10.1163/156853997x00179.Google Scholar
Dryden, M. (1996). Diagnosis and control of gastrointestinal parasites in dogs and cats. Veterinary Quarterly 18, 4243.Google Scholar
El-Gayar, A. K., Holman, P. J., Craig, T. M., Demaar, T. W., Wilson, S. C., Chung, P., Woods, K. M., Norris, C. and Upton, S. J. (2008). A new species of coccidia (Apicomplexa: Sarcocystidae) from the slender-tailed meerkat Suricata suricatta (Scheber, 1776) from South Africa. Acta Protozoologica 47, 6976.Google Scholar
Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology 15, 446454.Google Scholar
Foster, W. A. and Treherne, J. E. (1981). Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293, 466467.Google Scholar
Fugazzola, M. C. and Stancampiano, L. (2012). Host social rank and parasites: plains zebra (Equus quagga) and intestinal helminths in Uganda. Veterinary Parasitology 188, 115119.Google Scholar
Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology 27, 11291143. doi: 10.1007/s10764-006-9064-x.Google Scholar
Hoogland, J. L. and Sherman, P. W. (1976). Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecological Monographs 46, 3358.Google Scholar
Hudson, P. and Dobson, A. (1997). Host-parasite processes and demographic consequences. In Host-parasite Evolution: General Principles and Avian Models (ed. Clayton, D. and Moore, J.), pp. 128154. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1992 a). Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology 61, 681692.Google Scholar
Hudson, P. J., Newborn, D. and Dobson, A. P. (1992 b). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. 1. Monitoring and parasite reduction experiments. Journal of Animal Ecology 61, 477486. doi: 10.2307/5338.Google Scholar
Inglis, W. G. (1955). On the family Parasubuluridae van den Berghe & Vuylsteke, 1938, and the subfamily Numidicinae López-Neyra, 1945 (Nematoda). Parasitology 45, 431440.Google Scholar
Krams, I. A., Suraka, V., Rantala, M. J., Sepp, T., Mierauskas, P., Vrublevska, J. and Krama, T. (2013). Acute infection of avian malaria impairs concentration of haemoglobin and survival in juvenile altricial birds. Journal of Zoology 291, 3441.Google Scholar
Krause, J. and Ruxton, G. D. (eds.) (2002). Living in Groups. Oxford University Press, Oxford, UK.Google Scholar
Littell, R. C., Milliken, G. A., Stroup, W. W., Wolfinger, R. D. and Schabenberger, O. (2006). SAS for Mixed Models, 2nd Edn. SAS Institute Inc., Cary, NC, USA. Google Scholar
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika research site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555573.Google Scholar
Lynch, C. D. (1980). Ecology of the Suricate, Suricata suricatta and Yellow Mongoose, Cynictis penicillata with Special Reference to Their Reproduction. Memoirs van die Nasionale Museum, Bloemfontein, South Africa.Google Scholar
Monnig, H. (1931). Two new nematodes from the Suricat (Viverridae). 17th Report Director. Veterinary Services and Animal Industry, Union South Africa 1, 277282.Google Scholar
Müller-Graf, C. D. (1995). A coprological survey of intestinal parasites of wild lions (Panthera leo) in the Serengeti and the Ngorongoro Crater, Tanzania, East Africa. Journal of Parasitology 81, 812814.Google Scholar
Munyeme, M., Munang'andu, H., Muma, J., Nambota, A., Biffa, D. and Siamudaala, V. (2010). Investigating effects of parasite infection on body condition of the Kafue lechwe (Kobus leche kafuensis) in the Kafue basin. BMC Research Notes 3, 346.Google Scholar
Nunn, C. L. and Dokey, A. T.-W. (2006). Ranging patterns and parasitism in primates. Biology Letters 2, 351354. doi: 10.1098/rsbl.2006.0485.Google Scholar
Oates, S. C., Miller, M. A., Hardin, D., Conrad, P. A., Melli, A., Jessup, D. A., Dominik, C., Roug, A., Tinker, M. T. and Miller, W. A. (2012). Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the central California coast. Applied and Environmental Microbiology 78, 87628772. doi: 10.1128/aem.02422-12.Google Scholar
Ortlepp, R. (1925). On Arthrocephilus gambiensis n.g., n. sp., a new Ankylostome from an African Moongoose. Journal of Helminthology 3, 151156.Google Scholar
Ortlepp, R. T. (1938). South African helminths. III. Some mammalian and avian cestodes. Onderstepoort Journal of Veterinary Science and Animal Industry 11, 2350.Google Scholar
Ortlepp, R. T. (1940). South African helminths. VII. Miscellaneous helminths, chiefly cestodes. Onderstepoort Journal of Veterinary Science and Animal Industry 14, 97110.Google Scholar
Parkins, J. J. and Holmes, P. H. (1989). Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews 2, 227246. doi: 10.1079/nrr19890016.Google Scholar
Patterson, J. E. H. and Ruckstuhl, K. E. (2013). Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803813.Google Scholar
Phillippi, K. M. and Clarke, M. R. (1992). Survey of parasites of rhesus monkeys housed in small social groups. American Journal of Primatology 27, 293302.Google Scholar
Quentin, J. C. (1969). Cycle biologique de Protospirura muricola (Gedoelst, 1916) (Nematoda; Spiruridae). Annales de Parasitologie 44, 485504.Google Scholar
R Development Core Team (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables, 3rd Edn. W. H. Freeman and Company, San Francisco, CA, USA.Google Scholar
Round, M. C. (1968). Checklist of the helminth parasites of African mammals of the orders Carnivora, Tubulidentata, Proboscidea, Hyracoidea, Artiodactyla, and Perissodactyla. Technical communication No. 38. Commonwealth Bureau of Helminthology, St. Albans, UK.Google Scholar
Sen, K. and Anantaraman, M. (1971). Some observations on the development of Spirocerca lupi in its intermediate and definitive hosts. Journal of Helminthology 45, 123132.Google Scholar
Setchell, J. M., Bedjabaga, I.-B., Goossens, B., Reed, P., Wickings, E. J. and Knapp, L. A. (2007). Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. International Journal of Primatology 28, 13451362. doi: 10.1007/s10764-007-9225-6.Google Scholar
Soulsby, E. (1982). Helminths, Arthropods and Protozoa of Domesticated Animals. Baillière Tindall, London, UK.Google Scholar
Stirnadel, H. A. and Ebert, D. (1997). Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. Journal of Animal Ecology 66, 212222.Google Scholar
Thurber, M. I., O'Connell-Rodwell, C. E., Turner, W. C., Nambandi, K., Kinzley, C., Rodwel, T. C., Faulkner, C. T., Felt, S. A. and Bouley, D. M. (2011). Effects of rainfall, host demography, and musth on strongyle fecal egg counts in African elephants (Loxodonta africana) in Namibia. Journal of Wildlife Diseases 47, 172181.Google Scholar
Turner, W. C., Versfeld, W. D., Kilian, J. W. and Getz, W. M. (2012). Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition. Journal of Animal Ecology 81, 5869. doi: 10.1111/j.1365-2656.2011.01892.x.Google Scholar
van Staaden, M. (1994). Suricata suricatta . Mammalian Species 483, 18.Google Scholar
Visco, R. J., Corwin, R. M. and Selby, L. A. (1978). Effect of age and sex on prevalence of intestinal parasitism in cats. Journal of the American Veterinary Medical Association 172, 797800.Google ScholarPubMed
Warren, G. (1970). Studies on the morphology and taxonomy of the genera Toxocara Stiles, 1905 and Neoascaris Travassos, 1927. Zoologischer Anzeiger 185, 393442.Google Scholar
Young, A. J., Spong, G. and Clutton-Brock, T. (2007). Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal. Proceedings of the Royal Society B – Biological Sciences 274, 16031609.Google Scholar
Zajac, A. and Conboy, G. (2012). Veterinary Clinical Parasitology. John Wiley & Sons, Chichester, UK.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 10091024. doi: http://dx.doi.org/10.1016/S0020-7519(96)80001-4.Google Scholar