Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altman I, Byers JE (2014) Large-scale spatial variation in parasite communities influenced by anthropogenic factors. Ecology 95:1876–1887. https://doi.org/10.1890/13-0509.1
Anderson RC (2000) Nematode parasites of vertebrates. Their development and transmission, 2nd edn. CABI, Wallingford
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
Arneberg P, Skorping A, Read AF (1997) Is population density a species character? Comparative analyses of the nematode parasites of mammals. Oikos 80:289–300. https://doi.org/10.2307/3546597
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
Blasco-Costa I, Waters JM, Poulin R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Mol Ecol 21:207–217. https://doi.org/10.1111/j.1365-294X.2011.05374.x
Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. https://doi.org/10.1016/S0304-3800(01)00501-4
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R, 2nd edn. Springer, New York. https://doi.org/10.1007/978-3-319-71404-2
Botha M, Siebert SJ, van den Berg J (2016) Do arthropod assemblages fit the grassland and savanna biomes of South Africa? S Afr J Sci 112:1–10. https://doi.org/10.17159/sajs.2016/20150424
Brouat C, Kane M, Diouf M, Bâ K, Sall-Dramé R, Duplantier JM (2007) Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134:437–450. https://doi.org/10.1017/S003118200600151X
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227
Cramer MD, Hoffman MT (2015) The consequences of precipitation seasonality for Mediterranean-ecosystem vegetation of South Africa. PLoS One 10:1–21. https://doi.org/10.1371/journal.pone.0144512
Cribari-Neto F, Zeileis A (2010) Beta regression in R. J Stat Softw 34:1–24. https://doi.org/10.18637/jss.v034.i02
da Silva PG, Hernández MIM, Heino J (2018) Disentangling the correlates of species and site contributions to beta diversity in dung beetle assemblages. Divers Distrib 24:1674–1686. https://doi.org/10.1111/ddi.12785
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
Dufour CMS, Meynard C, Watson J, Rioux C, Benhamou S, Perez J, du Plessis JJ, Avenant N, Pillay N, Ganem G (2015) Space use variation in co-occurring sister species: Response to environmental variation or competition? PLoS One 10:1–15
Dybing NA, Fleming PA, Adams J (2013) Environmental conditions predict helminth prevalence in red foxes in Western Australia. Int J Parasitol Parasites Wildl 2:165–172. https://doi.org/10.1016/j.ijppaw.2013.04.004
Ellison AM (2010) Partitioning diversity. Ecology 91:1962–1963. https://doi.org/10.1890/09-1692.1
Ezenwa VO (2004) Host social behavior and parasitic infection: a multifactorial approach. Behav Ecol 15:446–454. https://doi.org/10.1093/beheco/arh028
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 13:107–110
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
Galbreath KE, Hoberg EP (2012) Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas. Proc R Soc Lond B Biol 279:371–378. https://doi.org/10.1098/rspb.2011.0482
Guernier V, Hochberg ME, Guégan JF (2004) Ecology drives the worldwide distribution of human infectious diseases. PLoS Biol 2:e186. https://doi.org/10.1371/journal.pbio.0020186
Harrison S, Ross SJ, Lawton JH (1992) Beta-diversity on geographic gradients in Britain. J Anim Ecol 61:151–158. https://doi.org/10.2307/5518
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
Haukisalmi V, Ribas A, Junker K, Spickett A, Matthee S, Henttonen H, Jrijer J, Halajian A, Ander JL, Nakao M (2018) Molecular systematics and evolutionary history of catenotaeniid cestodes (Cyclophyllidea). Zool Scr 47:221–230. https://doi.org/10.1111/zsc.1227
Heino J, Grönroos M (2017) Exploring species and site contributions to beta diversity in stream insect assemblages. Oecologia 183:151–160. https://doi.org/10.1007/s00442-016-3754-7
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Hoberg EP, Brooks DR (2015) Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philos Trans R Soc B 370:20130553. https://doi.org/10.1098/rstb.2013.0553
Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73:1121–1128. https://doi.org/10.1111/j.0021-8790.2004.00883.x
Krasnov BR, Khokhlova IS, Arakelyain MS, Degen AA (2005) Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Funct Ecol 19:625–631. https://doi.org/10.1111/j.1365-2435.2005.01015.x
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
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
Landeiro VL, Franz B, Heino J, Siqueira T, Bini LM (2018) Species-poor and low-lying sites are more ecologically unique in a hyperdiverse Amazon region: evidence from multiple taxonomic groups. Divers Distrib 24:966–977. https://doi.org/10.1111/ddi.12734
Legendre P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1:3–8. https://doi.org/10.1093/jpe/rtm001
Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Glob Ecol Biogeogr 23:1324–1334. https://doi.org/10.1111/geb.12207
Legendre P, de Cáceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963. https://doi.org/10.1111/ele.12141
Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75:435–450. https://doi.org/10.1890/05-0549
Lennon JJ, Koleff P, Greenwood JJD, Gaston KJ (2001) The geographical structure of British bird distributions: diversity, spatial turnover and scale. J Anim Ecol 70:966–979. https://doi.org/10.1046/j.0021-8790.2001.00563.x
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
Littlewood DT, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. https://doi.org/10.1006/mpev.2000.0802
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
Morand S, Guégan JF (2000) Distribution and abundance of parasite nematodes: Ecological specialisation, phylogenetic constraint or simply epidemiology? Oikos 88:563–573. https://doi.org/10.1034/j.1600-0706.2000.880313.x
Morand S, Krasnov BR (eds) (2010) The biogeography of host-parasite interactions. Oxford Univ. Press, Oxford
Morgan BB, Hawkins PA (1951) Veterinary helminthology. Burgess Publishing Company, Minneapolis
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
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Poisot T, Guéeveneux-Julien C, Fortin M-J, Gravel D, Legendre P (2017) Hosts, parasites and their interactions respond to different climatic variables. Glob Ecol Biogeogr 26:242–251. https://doi.org/10.1111/geb.12602
Poulin R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. J Biogeogr 30:1609–1615. https://doi.org/10.1046/j.1365-2699.2003.00949.x
Poulin R (2006) Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. Int J Parasitol 36:877–885. https://doi.org/10.1016/j.ijpara.2006.02.021
Poulin R, Guégan J-F (2000) Nestedness, anti-nestedness and the relationship between prevalence and intensity in ectoparasite assemblages of marine fish: a special model of species coexistence. Int J Parasitol 30:1147–1152. https://doi.org/10.1016/S0020-7519(00)00102-8
Procheş Ş, Cowling R (2007) Do insect distributions fit our biomes? S A J Sci 103:258–261
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/
Rambau RV, Robinson TJ, Stanyon R (2003) Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Mol Phylogenet Evol 28:564–575. https://doi.org/10.1016/S1055-7903(03)00058-7)
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
Schradin C, Pillay N (2006) Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability. Behav Ecol 17:452–458. https://doi.org/10.1093/beheco/arj04
Skinner JD, Chimimba CT (2005) The mammals of the southern African subregion, 3rd edn. Cambridge University Press, Cape Town
Spickett A, Junker K, Krasnov BR, Haukisalmi V, Matthee S (2017a) Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa. Parasitology 144:1211–1220. https://doi.org/10.1017/S003118201700049X
Spickett A, Junker K, Krasnov BR, Haukisalmi V, Matthee S (2017b) Helminth parasitism in two closely related South African rodents: abundance, prevalence, species richness and impinging factors. Parasitol Res 116:1395–1409. https://doi.org/10.1007/s00436-017-5419-9
Spickett A, Junker K, Krasnov BR, Haukisalmi V, Matthee S (2017c) Community structure of helminth parasites in two closely related South African rodents differing in sociality and spatial behaviour. Parasitol Res 116:2299–2312. https://doi.org/10.1007/s00436-017-5538-3
Stromberg BE (1997) Environmental factors influencing transmission. Vet Parasitol 72:247–264. https://doi.org/10.1016/S0304-4017(97)00100-3
Stuart C, Stuart T (2007) Field guide to mammals of southern Africa, revised edition. Struik Nature, Cape Town
Tonkin JD, Heino J, Sundermann A, Haase P, Jähnig SC (2016) Context dependency in biodiversity patterns of central German stream metacommunities. Freshw Biol 61:607–620. https://doi.org/10.1111/fwb.12728
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 Dissertation
van Schaik J, Kerth G (2017) Host social organization and mating system shape parasite transmission opportunities in three European bat species. Parasitol Res 116:589–599. https://doi.org/10.1007/s00436-016-5323-8
Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206. https://doi.org/10.1086/652373
Vestey MR, McMurry ST, Lochmiller RL (1993) Influence of dietary protein on selected measures of humoral and cellular immunity in the cotton rat Sigmodon hispidus. Can J Zool 71:579–586. https://doi.org/10.1139/z93-079
Vilmi A, Karjalainen SM, Heino J (2017) Ecological uniqueness of stream and lake diatom communities shows different macroecological patterns. Divers Distrib 23:1042–1053. https://doi.org/10.1111/ddi.12594
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
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338. https://doi.org/10.2307/1943563
Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251. https://doi.org/10.2307/1218190
Williams PH (1996) Mapping variations in the strength and breadth of biogeographic transition zones using species turnover. Proc R Soc B 263:579–588. https://doi.org/10.1098/rspb.1996.0087
Yamaguti S (1961) Systema helminthum. III. The nematode parasites of vertebrates, part I. Interscience Publishers, New York
Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10 https://CRAN.R-project.org/doc/Rnews/
Acknowledgments
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.
Data accessibility
The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
Funding
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
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).
Additional information
Section Editor: Elizabeth Marie Warburton
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Table 1
(DOCX 17 kb)
Rights and permissions
About this article
Cite this article
Spickett, A., van der Mescht, L., Junker, K. et al. Beta diversity of gastrointestinal helminths in two closely related South African rodents: species and site contributions. Parasitol Res 118, 2863–2875 (2019). https://doi.org/10.1007/s00436-019-06411-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06411-w