Skip to main content Accessibility help
×
Home

Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity

  • LUTHER VAN DER MESCHT (a1) (a2), BORIS R. KRASNOV (a3), CONRAD A. MATTHEE (a2) and SONJA MATTHEE (a1)

Summary

We studied nestedness and its relationships with beta-diversity in flea communities harboured by three closely related rodent species (Rhabdomys pumilio, Rhabdomys intermedius, Rhabdomys dilectus) at two spatial scales (within and among host populations) in South Africa and asked (a) whether variation in species composition of flea communities within and among host populations follows a non-random pattern; if yes, (b) what are the contributions of nestedness and species turnover to dissimilarity (= beta-diversity) among flea communities at the two scales; and (c) do the degree of nestedness and its contribution to beta-diversity differ among host species (social vs solitary) and between scales. We found that nestedness in flea assemblages was more pronounced (a) in social than solitary host species and (b) at lower (among host individuals within populations) than at higher scale (among host populations). We also found that higher degree of nestedness was associated with its higher contribution to beta-diversity. Our findings support earlier ideas that parasite community structure results from the processes of parasite accumulation by hosts rather than from the processes acting within parasite communities.

Copyright

Corresponding author

*Corresponding author. Department of Conservation Ecology and Entomology, Private bag X1, Stellenbosch University, Matieland, 7602, South Africa. Tel.: +27 (21) 808 4777. Fax: + 27 (21) 808 4821. E-mail: smatthee@sun.ac.za

References

Hide All
Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Loyola, D. and Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 12271239.
Almeida-Neto, M., Frensel, D. M. B. and Ulrich, W. (2012). Rethinking the relationship between nestedness and beta diversity: a comment on Baselga (2010). Global Ecology and Biogeography 21, 772777.
Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pedersen, A. B., Poss, M. and Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution and Systematics 34, 517547.
Andersson, M. G. I., Berga, M., Lindstrõm, E. S. and Langenheder, S. (2014). The spatial structure of bacterial communities is influenced by historical environmental conditions. Ecology 95, 11341140.
Baselga, A. (2008). Determinants of species richness, endemism and turnover in European longhorn beetles. Ecography 31, 263271.
Baselga, A. (2010). Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19, 134143.
Baselga, A. (2013). Multiple site dissimilarity quantifies compositional heterogeneity among several sites, while average pairwise dissimilarity may be misleading. Ecography 36, 124128.
Baselga, A., Jiménez-Valverde, A. and Niccolini, G. (2007). A multiple-site similarity measure independent of richness. Biology Letters 3, 642645.
Baselga, A., Gómez-Rodríguez, C. and Lobo, J. M. (2012). Historical legacies in world amphibian diversity revealed by the turnover and nestedness components of beta diversity. PLoS ONE 7, e32341.
Bordes, F., Blumstein, D. T. and Morand, S. (2007). Rodent sociality and parasite diversity. Biology Letters 3, 692694.
Brooks, D. R., León-Règagnon, V., McLennan, D. A., Zelmer, D. and Leon-Règagnon, V. (2006). Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, S76S85.
Carvalho, J. C., Cardoso, P. and Gomes, P. (2012). Determining the relative roles of species replacement and species richness differences in generating beta-diversity patterns. Global Ecology and Biogeography 21, 760771.
Diserud, O. H. and Ødegaard, F. (2007). A multiple-site similarity measure. Biology Letters 3, 2022.
Dupont, Y. L., Hansen, D. M. and Olesen, J. M. (2003). Structure of a plant-flower-visitor network in the high–altitude sub-alpine desert of Tenerife, Canary Islands. Ecography 26, 301310.
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, 7586.
Engelbrecht, A., Matthee, S., du Toit, N. and Matthee, C. A. (2016). Limited dispersal in an ectoparasitic mite, Laelaps giganteus, contributes to significant phylogeographic congruence with their rodent hosts, Rhabdomys . Molecular Ecology 25, 10061021.
Fargione, J. and Tilman, D. (2002). Competition and coexistence in terrestrial plants. In Competition and Coexistence (ed. Sommer, U. and Worm, B.), pp. 165198. Springer, New York, USA.
Gaston, K. J., Davies, R. G., Orme, D. L., Olson, V. A., Thomas, G. H., Ding, T-S., Rasmussen, P. C., Lennon, J. L., Bennett, P. M., Owens, I. P. F. and Blackburn, T. M. (2007). Spatial turnover in the global avifauna. Proceedings of the Royal Society B 274, 15671574.
González, M. T. and Oliva, M. E. (2009). Is the nestedness of metazoan parasite assemblages of marine fishes from the southeastern Pacific coast a pattern associated with the geographical distributional range of the host? Parasitology 136, 401409.
González, M. T. and Poulin, R. (2005). Nested patterns in parasite component communities of a marine fish along its latitudinal range on the Pacific coast of South America. Parasitology 131, 569577.
Gotelli, N. J. and Ellison, A. M. (2002). Assembly rules for New England ant assemblages. Oikos 99, 591599.
Gotelli, N. J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 8694.
Goüy de Bellocq, J. G., Sarà, M., Casanova, J. C., Feliu, C., Morand, S. (2003). A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitological Research 90, 6470.
Harrison, S., Ross, S. J. and Lawton, J. H. (1992). Beta diversity on geographic gradients in Britain. Journal Animal Ecology 61, 151158.
Heino, J. (2009). Species co-occurrence, nestedness and guild-environment relationships in stream macroinvertebrates. Freshwater Biology 54, 19471959.
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. Anderson, D. J. and Kikkawa, J.), pp. 187213. Blackwell Scientific Publications, Oxford, UK.
Hoset, K. S., Kyrö, K., Oksanen, T., Oksanen, L., Olofsson, J. (2014). Spatial variation in vegetation damage relative to primary productivity, small rodent abundance and predation. Ecography 37, 894901.
Izsak, C. and Price, R. G. (2001). Measuring β-diversity using a taxonomic similarity index, and its relation to spatial scale. Marine Ecology Progress Series 215, 6977.
Kadowaki, K. and Inouye, B. D. (2015). Habitat configuration affects spatial pattern of β diversity of insect communities breeding in oyster mushrooms. Ecosphere 6, 72.
Koleff, P., Gaston, K. J., Lennon, J. J. (2003). Measuring beta diversity for presence–absence data. Journal of Animal Ecology 72, 367382.
Korallo-Vinarskaya, N. P., Krasnov, B. R., Vinarski, M. V., Shenbrot, G. I., Mouillot, D., Poulin, R. (2009). Stability in abundance and niche breadth of gamasid mites across environmental conditions, parasite identity and host pools. Evolutionary Ecology 23, 329345.
Korallo-Vinarskaya, N. P., Vinarski, M. V., Khokhlova, I. S., Krasnov, B. R. (2013). Body size and coexistence in gamasid mites parasitic on small mammals: null model analyses at three hierarchical scales. Ecography 36, 508517.
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press, New York, USA.
Krasnov, B. R. and Khokhlova, I. S. (2001). The effect of behavioural interactions on the exchange of flea (Siphonaptera) between two rodents. Journal Vector Ecology 26, 181190.
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Degen, A. A. (2004). Flea species richness and parameters of host body, host geography and host “milieu”. Journal of Animal Ecology 73, 11211128.
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. (2005). Nested flea assemblages across the host's geographic range. Ecography 28, 475484.
Krasnov, B. R., Stanko, M., Miklisova, D. and Morand, S. (2006 a). Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecological Research 21, 460469.
Krasnov, B. R., Stanko, M. and Morand, S. (2006 b). Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 13301339.
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S., Hawlena, H. and Degen, A. A. (2006 c). Temporal variation in parasite infestation of a host individual: does a parasite-free host remain infested permanently? Parasitology Research 99, 541545.
Krasnov, B. R., Matthee, S., Lareschi, M., Karollo-Vinarskaya, N. P. and Vinarski, M. V. (2010 a). Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos 119, 120128.
Krasnov, B. R., Mouillot, D., Shenbrot, G. I., Khokhlova, I. S., Vinarski, M. V., Korallo-Vinarskaya, N. P. and Poulin, R. (2010 b). Similarity in ectoparasite faunas of Palaearctic rodents as a function of host phylogenetic, geographic or environmental distances: which matters the most? International Journal of Parasitology 40, 807817.
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S., Stanko, M., Morand, S. and Mouillot, D. (2015). Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38, 184197.
Krasnov, B. R., Stanko, M., Khokhlova, I. S., Shenbrot, G. I., Morand, S., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2011). Nestedness and β-diversity in ectoparasite assemblages of small mammalian hosts: effects of parasite affinity, host biology and scale. Oikos 120, 630639.
Kucheruk, V. V. (1983). Mammal burrows – their structure, topology and use. Fauna and Ecology of Rodents 15, 554 (in Russian).
Lareschi, M. and Krasnov, B. R. (2010). Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Medical and Veterinary Entomology 24, 284292.
Legendre, P., Borcard, D. and Peres-Neto, P. R. (2005). Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological Monographs 75, 435450.
Leprieur, F., Tedesco, P. A., Hugueny, B., Beauchard, O., Dürr, H. H., Brosse, S. and Oberdorff, T. (2011). Partitioning global patterns of freshwater fish beta diversity reveals contrasting signatures of past climate changes. Ecology Letters 14, 325334.
Levin, S. A. (1992). The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology 73, 19431967.
Lewinsohn, T. M., Inácio Prado, P., Jordano, P., Bascompte, J., Bascompte, M. and Olesen, J. (2006). Structure in plant–animal interaction assemblages. Oikos 113, 174184.
Loreau, M., Naeem, S. and Inchausti, P. (2002). Biodiversity and Ecosystem Functioning: Synthesis and Perspectives. Oxford University Press, Oxford, UK.
Marshall, A. G. (1981). The Ecology of Ectoparasite Insects. Academic Press, London, UK.
Matthee, S. and Krasnov, B. R. (2009). Searching for generality in the patterns of parasite abundance and distribution: ectoparasites of a South African rodent, Rhabdomys pumilio . International Journal of Parasitology 39, 781788.
Matthews, W. J. (1982). Small fish community structure in Ozark streams: structured assembly patterns or random abundance of species? American Midland Naturalist 107, 4254.
McKnight, M. W., White, P. S., McDonald, R. I., Lamoreux, J. F., Sechrest, W., Ridgley, R. S. and Stuart, S. N. (2007). Putting beta-diversity on the map: broad-scale congruence and coincidence in the extremes. PLoS Biology 5, e272.
Melo, A. S., Rangel, T. F. L. V. B. and Diniz-Filho, F. (2009). Environmental drivers of beta-diversity patterns in New-World birds and mammals. Ecography 32, 226236.
Meyer, C. F. J. and Kalko, E. K. V. (2008). Bat assemblages on Neotropical land-bridge islands: nested subsets and null model analyses of species co-occurrence patterns. Diversity and Distributions 14, 644654.
Morand, S., Rohde, K. and Hayward, C. (2002). Order in ectoparasite communities of marine fish is explained by epidemiological processes. Parasitology 124, S57S63.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2015). vegan: Community Ecology Package. R package version 2.3–2. http://CRAN.R-project.org/package=vegan
Patterson, B. D. and Atmar, W. (1986). Nested subsets and the structure of insular mammalian faunas and archipelagos. Biological Journal of the Linnean Society 28, 6582.
Patterson, B. D., Dick, C. W. and Dittmar, K. (2009). Nested distributions of bat flies (Diptera: Streblidae) on Neotropical bats: artefact and specificity in host-parasite studies. Ecography 32, 481487.
Pitzalis, M., Luiselli, L. and Bologna, M. A. (2010). Co-occurrence analyses show that non-random community structure is disrupted by fire in two groups of soil arthropods (Isopoda, Oniscidea and Collembola). Acta Oecologia 36, 100106.
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.
Poulin, R. (2011). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, USA.
Poulin, R. and Valtonen, E. T. (2001). Nested assemblages resulting from host-size variation: the case of endoparasite communities in fish hosts. International Journal of Parasitology 31, 194204.
Presley, S. J. (2007). Streblid bat fly assemblage structure on Paraguayan Noctilio leporinus (Chiroptera: Noctilionidae): nestedness and species co-occurrence. Journal of Tropical Ecology 23, 409417.
Qian, H., Ricklefs, R. E. and White, P. S. (2005). Beta diversity of angiosperms in temperate floras of eastern Asia and eastern North America. Ecology Letters 8, 1522.
R Development Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, URL http://www.R-project.org/
Ricotta, C. and Pavoine, S. (2015). A multiple-site dissimilarity measure for species presence/absence data and its relationship with nestedness and turnover. Ecological Indicators 54, 203206.
Rodríguez, D. and Ojeda, R. A. (2013). Scaling coexistence and assemblage patterns of desert small mammals. Mammalian Biology 78, 313321.
Rohde, K., Worthen, W. B., Heap, M., Hugueny, B. and Guégan, J-F. (1998). Nestedness in assemblages of metazoan ecto- and endoparasites of marine fish. International Journal of Parasitology 28, 543549.
Rymer, T. L., Pillay, N. and Schradin, C. (2013). Extinction or survival? Behavioural flexibility in response to environmental change in the African striped mouse Rhabdomys . Sustainability 5, 163186.
Sanders, N. J., Gotelli, N. J., Wittman, S. E., Ratchford, J. S., Ellison, A. M. and Jules, E. S. (2007). Assembly rules of ground-foraging ant assemblages are contingent on disturbance, habitat and spatial scale. Journal of Biogeography 34, 16321641.
Schoepf, I., Scmohl, G., König, B., Pillay, N. and Schradin, C. (2015). Manipulation of population density and food availability affects home range sizes of African striped mouse females. Animal Behaviour 99, 5360.
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, 7782.
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, 3747.
Schradin, C. and Pillay, N. (2005). Intraspecific variation in the spatial and social organization of the African striped mouse. Journal of Mammalogy 86, 99107.
Schradin, C., König, B. and Pillay, N. (2010). Reproductive competition favours solitary living while ecological constraints impose group-living in African striped mice. Journal of Animal Ecology 79, 515521.
Segerman, J. (1995). Siphonaptera of Southern Africa. Handbook for the identification of fleas. Publications of The South African Institute for Medical Research No. 57. South African Institute for Medical Research, Johannesburg, South Africa.
Seidler, T. G. and Plotkin, J. B. (2006). Seed dispersal and spatial pattern in tropical trees. PLoS Biology 4, e344.
Si, X., Baselga, A. and Ding, P. (2015). Revealing beta-diversity patterns of breeding bird and lizard communities on inundated land-bridge islands by separating the turnover and nestedness components. PLoS ONE 10, e0127692.
Simaiakis, S. M. and Martínez-Morales, M. A. (2010). Nestedness in centipede (Chilopoda) assemblages on continental islands (Aegen, Greece). Acta Oecologia 36, 282290.
Šimková, A., Gelnar, M. and Morand, S. (2001). Order and disorder in ectoparasite communities: the case of congeneric gill monogeneans (Dactylogyrus spp.). International Journal of Parasitology 31, 12051210.
Stanko, M., Miklisová, D., Goüy de Bellocq, J. and Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289295.
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 of Parasitology 33, 13531362.
Ulrich, W. and Gotelli, N. J. (2007). Disentangling community patterns of nestedness and species co-occurrence. Oikos 116, 20532061.
Ulrich, W., Almeida-Neto, M. and Gotelli, N. J. (2009). A consumer's guide to nestedness analysis. Oikos 118, 317.
Valtonen, E. T., Pulkkinen, K., Poulin, R. and Julkunen, M. (2001). The structure of parasite component communities in brackish water fishes of the northeastern Baltic Sea. Parasitology 122, 471481.
Van der Mescht, L., le Roux, P. C. and Matthee, S. (2013). Remnant fragments within an agricultural matrix enhance conditions for a rodent host and its fleas. Parasitology 140, 368377.
Vinarski, M. V., Korallo, N. P., Krasnov, B. R., Shenbrot, G. I. and 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, 16911700.
Wethered, R. and Lawes, M. J. (2005). Nestedness of bird assemblages in fragmented Afromontane forest: the effect of plantation forestry in the matrix. Biological Conservation 123, 125137.
Whittaker, R. H. (1972). Evolution and measurement of species diversity. Taxon 21, 213251.
Wright, D. H. and Reeves, J. H. (1992). On the meaning and measurement of nestedness of species assemblages. Oecologia 92, 416428.
Xu, J., Su, G., Xiong, Y., Akasaka, M., Molinos, J. C., Matsuzaki, S. S. and Zhang, M. (2015). Complimentary analysis of metacommunity nestedness and diversity partitioning highlights the need for a holistic conservation strategy for highland lake fish assemblages. Global Ecology and Conservation 3, 288296.

Keywords

Type Description Title
WORD
Supplementary materials

Van der Mescht supplementary material
Tables S1-S3

 Word (16 KB)
16 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed