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Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa

Published online by Cambridge University Press:  09 May 2017

ANDREA SPICKETT ,
KERSTIN JUNKER ,
BORIS R. KRASNOV ,
VOITTO HAUKISALMI  and
SONJA MATTHEE Open the ORCID record for SONJA MATTHEE [Opens in a new window]
ANDREA SPICKETT
Affiliation:
Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort, 0110, South Africa Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa
KERSTIN JUNKER
Affiliation:
Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort, 0110, South Africa
BORIS R. KRASNOV
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
VOITTO HAUKISALMI
Affiliation:
Piettasenkatu 38 A 23 33580 Tampere, Finland
SONJA MATTHEE*
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa
*
*Corresponding author: Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa. E-mail: smatthee@sun.ac.za
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Summary

To reveal factors responsible for spatial variation in parasite community composition we studied patterns of similarity in helminth species composition in two closely-related rodents (Rhabdomys pumilio and Rhabdomys dilectus) that differ in their social and spatial behaviour and live under different environmental conditions across 20 localities in South Africa. We asked whether the two hosts harbour similar assemblages, whether these are more dissimilar between than within hosts and if host social structure, behaviour or environment affects similarity patterns in helminth infracommunities within and among localities. We also investigated whether similarity in species composition of helminth component communities decreases with an increase of geographic distance between host populations. We found that the pattern of space use by the hosts rather than their social behaviour promotes differences in helminth species composition between host species as well as among host populations from different localities. The rate of distance decay of similarity in species composition of helminth component communities differed between the two hosts due to difference in the degree of environmental variation across their geographic ranges. We conclude that patterns of spatial variation in helminth species composition are driven mainly by host spatial behaviour and, to a lesser extent, by environment-associated factors.

Keywords

Rhabdomys pumilioRhabdomys dilectushelminthssimilarity
Type
Research Article
Information
Parasitology , Volume 144 , Issue 9 , August 2017 , pp. 1211 - 1220
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Anderson, R. C. (2000). Nematode Parasites of Vertebrates. Their development and transmission, 2nd Edn. CABI, Wallingford.CrossRefGoogle Scholar
Boomker, J., Horak, I. G., Watermeyer, R. and Booyse, D. G. (2000). Parasites of South African Wildlife XVI. Helminths of some antelope species from the Eastern and Western Cape Provinces. Onderstepoort Journal of Veterinary Research 67, 31–41.Google Scholar
Bordes, F., Blumstein, D. and Morand, S. (2007). Rodent sociality and parasite diversity. Biological Letters 3, 692–694.Google Scholar
Bordes, F., Guégan, J. F. and Morand, S. (2011). Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size. Oikos 120, 1889–1896.Google Scholar
Bordes, F., Nicolas Ponlet, N., Goüy de Bellocq, J., Ribas, A., Krasnov, B. R. and Morand, S. (2012). Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecologia 170, 123–135.CrossRefGoogle ScholarPubMed
Bordes, F., Morand, S., Pilosof, S., Claude, J., Krasnov, B. R., Cosson, J. F., Chaval, Y., Ribas, A., Chaisiri, K., Blasdell, K. and Herbreteau, V. (2015). Habitat fragmentation alters the properties of a host–parasite network: rodents and their helminths in South East Asia. Journal of Animal Ecology 84, 1253–1263.Google Scholar
Bray, J. R. and Curtis, J. T. (1957). An ordination of upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349.CrossRefGoogle Scholar
Brouat, C., Kane, M., Diouf, M. and Bâ, K. (2007). Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437–450.Google Scholar
Bush, A. O. (1990). Helminth communities in avian hosts: determinants of pattern. In Parasite Communities: Patterns and Processes (ed. by Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 197–232. Chapman and Hall, London.Google Scholar
Bush, A. O., Aho, J. M. and Kennedy, C. R. (1990). Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4, 1–20.Google Scholar
Calvete, C., Blanco-Aguiar, J. A., Virgós, E., Cabezas-Díaz, S. and Villafuerte, R. (2004). Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.Google Scholar
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555.Google Scholar
Clarke, K. R. and Gorley, R. N. (2015). Primer v7: User Manual/Tutorial. Primer-E Ltd, Plymouth Marine Laboratory, Plymouth.Google Scholar
Clarke, K. R. and Green, R. H. (1988). Statistical design and analysis for a “biological effects” study. Marine Ecology Progress Series 46, 213–226.CrossRefGoogle Scholar
Clarke, K. R. and Warwick, R. M. (2001). Change in Marine Communities: An approach to Statistical Analysis and Interpretation, 2nd Edn. Primer-E Ltd, Plymouth Marine Laboratory, Plymouth.Google Scholar
du Toit, N., Jansen van Vuuren, B., Matthee, S. and Matthee, C. A. (2012). Biome specificity of distinct genetic lineages within the four-striped mouse Rhabdomys pumilio (Rodentia: Muridae) from southern Africa with implications for taxonomy. Molecular Phylogenetics and Evolution 65, 75–86.Google Scholar
Dybing, N. A., Fleming, P. A. and Adams, J. (2013). Environmental conditions predict helminth prevalence in red foxes in Western Australia. International Journal for Parasitology: Parasites and Wildlife 2, 165–172.Google Scholar
Froeschke, G., Harf, R., Sommer, S. and Matthee, S. (2010). Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa – implications for possible shifts in infestation patterns due to global changes. Oikos 119, 1029–1039.Google Scholar
Georgiev, B. B., Bray, R. A. and Littlewood, D. T. J. (2006). Cestodes of small mammals: Taxonomy and life cycles. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 29–62. Springer Verlag, Tokyo, Japan.Google Scholar
Goslee, S. C. and Urban, D. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22, 1–19.Google Scholar
Hudson, P. J., Cattadori, M., Boag, B. and Dobson, A. P. (2006). Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175–182.Google Scholar
Hulbert, I. A. R. and Boag, B. (2001). The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus . Journal of Helminthology 75, 345–349.Google Scholar
Karvonen, A. and Valtonen, E. T. (2009). Between-population similarity in intestinal parasite community structure of pike (Esox lucius) – effects of distance and historical connections. Journal of Parasitology 95, 505–511.Google Scholar
Karvonen, A., Cheng, G.-H. and Valtonen, E. T. (2005). Within-lake dynamics in the similarity of parasite assemblages of perch (Perca fluviatilis). Parasitology 131, 817–823.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Khokhlova, I. S. and Vashchenok, V. S. (1998). Habitat-dependence of a parasite-host relationship: flea assemblages in two gerbil species of the Negev Desert. Journal of Medical Entomology 35, 303–313.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002). Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 70–81.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2005). Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? Journal of Biogeography 32, 633–644.Google Scholar
Legendre, P. and Legendre, L. (1998). Numerical Ecology, 2nd English.Edn. Elsevier, Amsterdam.Google Scholar
Lichstein, J. W. (2007). Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology 188, 117–131.CrossRefGoogle Scholar
Manly, B. F. (1986). Randomization and regression methods for testing for associations with geographical, environmental and biological distances between populations. Research in Population Ecology 28, 201–218.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1991). Importance of lake characteristics in structuring parasite communities of salmonids from insular Newfoundland. Canadian Journal of Zoology 69, 2962–2967.Google Scholar
Milton, S. J. and Dean, W. R. J. (1999). Biogeographic patterns and the driving variables. In The Karoo: Ecological Patterns and Processes (ed. Dean, W. R. J. and Milton, S. J.), pp. 3–16. Cambridge University Press, Cambridge, UK.Google Scholar
Mucina, L. and Rutherford, M. C. (Eds) (2006). The Vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19, South African National Biodiversity Institute, Pretoria.Google Scholar
Nekola, J. C. and White, P. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867–878.Google Scholar
Ostfeld, R. S. (1990). The ecology of territoriality in small mammals. Trends in Ecology and Evolution 5, 411–415.Google Scholar
Palmeirim, M., Bordes, F., Chaisiri, K., Siribat, P., Ribas, A. and Morand, S. (2014). Helminth parasite species richness in rodents from Southeast Asia: role of host species and habitat. Parasitology Research 113, 3713–3726.Google Scholar
Perrin, M. R., Ercoli, C. and Dempster, E. R. (2001). The role of agonistic behaviour in the population regulation of two syntopic African grassland rodents, the striped mouse Rhabdomys pumilio (Sparrman 1784) and the multimammate mouse Mastomys natalensis (A. Smith 1834) (Mammalia Rodentia). Tropical Zoology 14, 7–29.Google Scholar
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.Google Scholar
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 1609–1615.Google Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776.Google Scholar
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.Google Scholar
R Core Team (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Google Scholar
Rohde, K. (1992). Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514–527.Google Scholar
Sarà, M. and Morand, S. (2002). Island incidence and mainland population density: mammals from Mediterranean islands. Diversity and Distributions 8, 1–9.Google Scholar
Schradin, C. (2005). When to live alone and when to live in groups: ecological determinants of sociality in the African striped mouse (Rhabdomys pumilio, Sparrman, 1784). Belgian Journal of Zoology 135, 77–82.Google Scholar
Schradin, C. and Pillay, N. (2003). Paternal care in the social and diurnal striped mouse (Rhabdomys pumilio): laboratory and field evidence. Journal of Comparative Psychology 117, 317–324.Google Scholar
Schradin, C. and Pillay, N. (2004). The striped mouse (Rhabdomys pumilio) from the Succulent Karoo, South Africa: a territorial group living solitary forager with communal breeding and helpers at the nest. Journal of Comparative Psychology 118, 37–47.Google Scholar
Schradin, C. and Pillay, N. (2005 a). Intraspecific variation in the spatial and social organization of the African striped mouse. Journal of Mammalogy 86, 99–107.Google Scholar
Schradin, C., and Pillay, N. (2005 b). Demography of the striped mouse (Rhabdomys pumilio) in the succulent karoo. Mammalian Biology 70, 84–92.Google Scholar
Schradin, C. and Pillay, N. (2006). Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability. Behavioral Ecology 17, 452–458.Google Scholar
Schradin, C., Schmohl, G., Rödel, H. G., Schoepf, I., Treffler, S. T., Brenner, J., Bleeker, M., Schubert, M., König, B., and Pillay, N. (2010). Female home range size is regulated by resource distribution and intraspecific competition: a long-term field study. Animal Behaviour 79, 195–203.Google Scholar
Simkova, A., Sitko, J., Okulewicz, J. and Morand, S. (2003). Occurrence of intermediate hosts and structure of digenean communities of the black-headed gull, Larus ridibundus (L.). Parasitology 126, 69–78.Google Scholar
Skinner, J. D. and Chimimba, C. T. (2005). The Mammals of the Southern African Subregion, 3rd Edn. Cambridge University Press, Cape Town.Google Scholar
Spickett, A., Junker, K., Krasnov, B. R., Haukisalmi, V. and Matthee, S. (2017). Helminth parasitism in two closely-related South African rodents: abundance, prevalence, species richness and impinging factors. Parasitology Research 116, 1395–1409 CrossRefGoogle ScholarPubMed
Taffs, L. F. (1976). Pinworm infections in laboratory rodents: a review. Laboratory Animals 10, 1–13.Google Scholar
Timi, J. T. and Poulin, R. (2003). Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it? International Journal for Parasitology 33, 1353–1362.Google Scholar
Timi, J. T., Luque, J. L. and Poulin, R. (2010). Host ontogeny and the temporal decay of similarity in parasite communities of marine fish. International Journal for Parasitology 40, 963–968.Google Scholar
Turner, W. C. and Getz, W. M. (2010). Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. Journal of Wildlife Diseases 46, 1108–1119.Google Scholar
Van der Mescht, L., Krasnov, B. R., Matthee, C. A., and Matthee, S. (2016). Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity. Parasitology 143, 1268–1278.Google Scholar
Vinarski, M. V., Korallo, N. P., Krasnov, B. R., Shenbrot, G. I., Poulin, R. (2007). Decay of similarity of gamasid mite assemblages parasitic on Palaearctic small mammals: geographic distance, host-species composition or environment. Journal of Biogeography 34, 1691–1700.Google Scholar