Beta diversity of gastrointestinal helminths in two closely related South African rodents: species and site contributions
A fundamental aim of parasite ecology is to understand the mechanisms behind spatial variation in diversity and structure of parasite assemblages. To understand the contribution of individual parasite species and their assemblages to spatial variation in parasite communities, we examined species contributions to beta diversity (SCBD) and local contributions to beta diversity (LCBD) of parasitic gastrointestinal helminths (nematodes and cestodes) in two closely related rodents, Rhabdomys dilectus and Rhabdomys pumilio, from 20 localities across South Africa. Although the two Rhabdomys spp. are morphologically similar, they differ substantially in body size, habitat preference, and sociality. We asked whether the variation in life history traits and infection parameters are associated with SCBD of helminths and whether variation in environmental factors, host population density, and species richness of host communities are associated with LCBD of component assemblages of helminths. We also considered spatial factors to test whether LCBD of helminth assemblages demonstrate geographic structure. We found that the contribution of helminth species parasitic in both hosts to beta diversity significantly increased with characteristic prevalence of these species, whereas mean abundance, type of life cycle, and location in the host’s gut had no effect on SCBD. The LCBD of helminth assemblages showed a significant positive correlation with environmental factors in both host species. Our results suggest that predictors of variation in SCBD and LCBD may substantially differ between parasites with different infection parameters and/or parasite communities at different hierarchical scales.
KeywordsBeta diversity Rhabdomys Gastrointestinal helminths Environment LCBD SCBD
We thank private landowners and nature reserve authorities for permitting us to conduct fieldwork on their properties, under the following provincial permit numbers: Eastern Cape, CRO37/11CR; KwaZulu-Natal, OP4990/2010; Western Cape, 0035-AAA007-00423; Northern Cape, FAUNA 1076/2011, Free State, 01/8091; Gauteng, CPF 6-0153, and Mpumalanga, MPB. 5331. We thank G. Froeschke for the identification of helminths that were recovered from most of the Fynbos localities as well as N. Avenant, M.D. Chipana, J. Coetsee, L. Cohen, N. Du Toit, A. Engelbrecht, G. Froeschke, R.F. Masubelle, C.A. Matthee, and L. Richards for help with field and technical work. This is publication no. 1025 of the Mitrani Department of Desert Ecology.
The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
Financial support for the project was provided by the National Research Foundation (NRF), Agricultural Research Council – Onderstepoort Veterinary Institute and Stellenbosch University. LVDM received financial support through a postdoctoral fellowship from the Claude Leon Foundation. 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 that the NRF accepts no liability whatsoever in this regard.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (Stellenbosch University - Research Ethics Committee: Animal Care and Use, permit numbers 2006B01007 and SU-ACUM11-00004 and Onderstepoort Veterinary Institute - Animal Ethics Committee, permit number AEC32.11).
- Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, Harrison SP, Kraft NJB, Stegen JC, Swenson NG (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28. https://doi.org/10.1111/j.1461-0248.2010.01552.x CrossRefPubMedGoogle Scholar
- Biguezoton A, Adehan S, Adakal H, Zoungrana S, Farougou S, Chevillon C (2016) Community structure, seasonal variations and interactions between native and invasive cattle tick species in Benin and Burkina Faso. Parasit Vectors 9:43. https://doi.org/10.1186/s13071-016-1305-z CrossRefPubMedPubMedCentralGoogle Scholar
- Dray S, Bauman D, Blanchet G, Borcard D, Clappe S, Guenard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2018) adespatial: multivariate multiscale spatial analysis. R package version 0.2–0. https://CRAN.R-project.org/package=adespatial
- du Toit N, Jansen van Vuuren B, Matthee S, Matthee CA (2012) Biome specificity of distinct genetic lineages within the four-striped mouse Rhabdomys pumilio (Rodentia: Muridae) from southern Africa with implications for taxonomy. Mol Phylogenet Evol 65:75–86. https://doi.org/10.1016/j.ympev.2012.05.036 CrossRefPubMedGoogle Scholar
- Faleh AB, Annabi A, López S, Said K, Ribas A (2012) On the helminth parasites of the genus Jaculus (Rodentia: Dipodidae) in Tunisia: a preliminary survey study. Leb Sci J 13:107–110Google Scholar
- Froeschke G, Harf R, Sommer S, 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. https://doi.org/10.1111/j.1600-0706.2009.18124.x CrossRefGoogle Scholar
- Haukisalmi V, Hardman LM, Fedorov VB, Hoberg EP, Henttonen H (2016) Molecular systematics and Holarctic phylogeography of cestodes of the genus Anoplocephaloides Baer, 1923 s. s. (Cyclophyllidea, Anoplocephalidae) in lemmings (Lemmus, Synaptomys). Zool Scr 45:88–102. https://doi.org/10.1111/zsc.12136 CrossRefGoogle Scholar
- Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2010) Deconstructing spatial patterns in species composition of ectoparasite communities: the relative contribution of host composition, environmental variables and geography. Glob Ecol Biogeogr 19:515–526. https://doi.org/10.1111/j.1466-8238.2010.00529.x CrossRefGoogle Scholar
- Krasnov BR, Shenbrot GI, Warburton EM, van der Mescht L, Surkova EN, Medvedev SG, Pechnikova N, Ermolova N, Kotti BK, Khokhlova IS (2018) Species and site contributions to beta diversity in fleas parasitic on the Palearctic small mammals: ecology, geography and host species composition matter the most. Parasitol 146:653–661. https://doi.org/10.1017/S0031182018001944 CrossRefGoogle Scholar
- Lenth R (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.2. https://CRAN.R-project.org/package=emmeans
- Lindenfors P, Nunn CL, Jones KE, Cunningham AA, Sechrest W, Gittleman JL (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Glob Ecol Biogeogr 16:496–509. https://doi.org/10.1111/j.1466-8238.2006.00301.x CrossRefGoogle Scholar
- Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155–171. https://doi.org/10.1046/j.1095-8312.2003.00141.x CrossRefGoogle Scholar
- Morand S, Krasnov BR (eds) (2010) The biogeography of host-parasite interactions. Oxford Univ. Press, OxfordGoogle Scholar
- Morgan BB, Hawkins PA (1951) Veterinary helminthology. Burgess Publishing Company, MinneapolisGoogle Scholar
- Oksanen J, Blanchet G, Friendly M, Kindt P, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan
- Procheş Ş, Cowling R (2007) Do insect distributions fit our biomes? S A J Sci 103:258–261Google Scholar
- Schradin C, Pillay N (2005) Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107. https://doi.org/10.1644/1545-1542(2005)086<0099:IVITSA>2.0.CO;2 CrossRefGoogle Scholar
- Stuart C, Stuart T (2007) Field guide to mammals of southern Africa, revised edition. Struik Nature, Cape TownGoogle Scholar
- Torre I, Arrizabalaga A, Feliu C, Ribas A (2013) The helminth infracommunities of the wood mouse (Apodemus sylvaticus) two years after the fire in Mediterranean forests. Helminthologia 50(1):27–38. https://doi.org/10.2478/s11687-013-0104-8
- van der Mescht L (2011) Ectoparasite assemblage of the four-striped mouse, Rhabdomys pumilio: the effect of anthropogenic habitat transformation and temporal variation. Stellenbosch University, MSc DissertationGoogle Scholar
- von Nickisch-Rosenegk M, Brown WM, Boore JL (2001) Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are eutrochozoans. Mol Biol Evol 18:721–730. https://doi.org/10.1093/oxfordjournals.molbev.a003854 CrossRefGoogle Scholar
- Yamaguti S (1961) Systema helminthum. III. The nematode parasites of vertebrates, part I. Interscience Publishers, New YorkGoogle Scholar