Microbial Ecology

, Volume 72, Issue 2, pp 313–323 | Cite as

Deterministic assembly processes govern bacterial community structure in the Fynbos, South Africa

  • I. Moroenyane
  • S. B. M. Chimphango
  • J. Wang
  • H-K. Kim
  • Jonathan Miles Adams
Environmental Microbiology


The Mediterranean Fynbos vegetation of South Africa is well known for its high levels of diversity, endemism, and the existence of very distinct plant communities on different soil types. Studies have documented the broad taxonomic classification and diversity patterns of soil microbial diversity, but none has focused on the community assembly processes. We hypothesised that bacterial phylogenetic community structure in the Fynbos is highly governed by deterministic processes. We sampled soils in four Fynbos vegetation types and examined bacterial communities using Illumina HiSeq platform with the 16S rRNA gene marker. UniFrac analysis showed that the community clustered strongly by vegetation type, suggesting a history of evolutionary specialisation in relation to habitats or plant communities. The standardised beta mean nearest taxon distance (ses. β NTD) index showed no association with vegetation type. However, the overall phylogenetic signal indicates that distantly related OTUs do tend to co-occur. Both NTI (nearest taxon index) and ses. β NTD deviated significantly from null models, indicating that deterministic processes were important in the assembly of bacterial communities. Furthermore, ses. β NTD was significantly higher than that of null expectations, indicating that co-occurrence of related bacterial lineages (over-dispersion in phylogenetic beta diversity) is determined by the differences in environmental conditions among the sites, even though the co-occurrence pattern did not correlate with any measured environmental parameter, except for a weak correlation with soil texture. We suggest that in the Fynbos, there are frequent shifts of niches by bacterial lineages, which then become constrained and evolutionary conserved in their new environments. Overall, this study sheds light on the relative roles of both deterministic and neutral processes in governing bacterial communities in the Fynbos. It seems that deterministic processes play a major role in assembling the bacterial community, with neutral processes playing a more minor role.


Bacteria Fynbos 16S rRNA gene Phylogenetic diversity Community assembly 



The authors would like to thank the South African National Parks (SANParks) and Cape Nature for giving us access to the study sites (permit number 0028-AAA005-00161, 25/01/2010: SBM Chimphango), as well as Dr. James C Stegen and Dr. Binu M Tribathi for providing invaluable advice with the analysis of the data. This work was supported by a grant from the National Research Foundation (NRF) funded by the Korean Government Ministry of Education, Science and Technology (MEST) (NRF2013-031400). Also, the authors would like to thank the Department of Biological Science, University of Cape Town for use of their laboratory facilities.

Supplementary material

248_2016_761_MOESM1_ESM.docx (108 kb)
ESM 1 (DOCX 107 kb)
248_2016_761_MOESM2_ESM.docx (73 kb)
ESM 2 (DOCX 72 kb)
248_2016_761_MOESM3_ESM.docx (1.2 mb)
ESM 3 (DOCX 1180 kb)
248_2016_761_MOESM4_ESM.docx (201 kb)
ESM 4 (DOCX 200 kb)
248_2016_761_MOESM5_ESM.docx (16 kb)
ESM 5 (DOCX 16 kb)
248_2016_761_MOESM6_ESM.docx (12 kb)
ESM 6 (DOCX 12 kb)
248_2016_761_MOESM7_ESM.docx (12 kb)
ESM 7 (DOCX 12 kb)


  1. 1.
    Dunbar J, Barns SM, Ticknor LO, Kuske CR (2002) Empirical and theoretical bacterial diversity in four Arizona soils. Appl Environ Microbiol 68:3035–3045CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Torsvik V, Goksoyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787PubMedPubMedCentralGoogle Scholar
  3. 3.
    Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245CrossRefPubMedGoogle Scholar
  4. 4.
    Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066CrossRefPubMedGoogle Scholar
  5. 5.
    Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 105:11505–11511CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112CrossRefPubMedGoogle Scholar
  8. 8.
    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506PubMedGoogle Scholar
  9. 9.
    Mcarthur JV, Kovacic DA, Smith MH (1988) Genetic diversity in natural-populations of a soil bacterium across a landscape gradient. Proc Natl Acad Sci U S A 85:9621–9624CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183CrossRefGoogle Scholar
  11. 11.
    Ramette A, Tiedje JM (2007) Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. Proc Natl Acad Sci U S A 104:2761–2766CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensic 12:333–341CrossRefGoogle Scholar
  13. 13.
    Cottenie K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecol Lett 8:1175–1182CrossRefPubMedGoogle Scholar
  14. 14.
    Yergeau E, Bezemer TM, Hedlund K, Mortimer SR, Kowalchuk GA, van der Putten WH (2010) Influences of space, soil, nematodes and plants on microbial community composition of chalk grassland soils. Environ Microbiol 12:2096–2106PubMedGoogle Scholar
  15. 15.
    Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci U S A 108:7850–7854CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206CrossRefPubMedGoogle Scholar
  17. 17.
    Langenheder S, Szekely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–1094CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Besemer K, Peter H, Logue JB, Langenheder S, Lindstrom ES, Tranvik LJ, Battin TJ (2012) Unraveling assembly of stream biofilm communities. ISME J 6:1459–1468CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Stegen JC, Lin XJ, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345CrossRefPubMedGoogle Scholar
  21. 21.
    Caruso T, Chan YK, Lacap DC, Lau MCY, Mckay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  23. 23.
    Morlon H, Schwilk DW, Bryant JA, Marquet PA, Rebelo AG, Tauss C, Bohannan BJM, Green JL (2011) Spatial patterns of phylogenetic diversity. Ecol Lett 14:141–149CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Zaneveld JRR, Parfrey LW, Van Treuren W, Lozupone C, Clemente JC, Knights D, Stombaugh J, Kuczynski J, Knight R (2011) Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation. Trends Microbiol 19:472–482CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Stegen JC, Lin XJ, Fredrickson JK, Chen XY, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Wang JJ, Shen J, Wu YC, Tu C, Soininen J, Stegen JC, He JZ, Liu XQ, Zhang L, Zhang EL (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Wang JJ, Soininen J, He JZ, Shen J (2012) Phylogenetic clustering increases with elevation for microbes. Environ Microbiol Rep 4:217–226CrossRefPubMedGoogle Scholar
  28. 28.
    Wang JJ, Soininen J, Shen J (2013) Habitat species pools for phylogenetic structure in microbes. Environ Microbiol Rep 5:464–467CrossRefPubMedGoogle Scholar
  29. 29.
    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Monographs in population biology 32. Princeton University Press,, Princeton, pp. 1 online resource (xiv, 375 p.) ill., map.Google Scholar
  30. 30.
    Chave J (2004) Neutral theory and community ecology. Ecol Lett 7:241–253CrossRefGoogle Scholar
  31. 31.
    Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Etienne RS, Latimer AM, Silander JA, Cowling RM (2006) Comment on “Neutral ecological theory reveals isolation and rapid speciation in a biodiversity hot spot”. Science 311:610BCrossRefGoogle Scholar
  33. 33.
    Latimer AM, Silander JA, Cowling RM (2005) Neutral ecological theory reveals isolation and rapid speciation in a biodiversity hot spot. Science 309:1722–1725CrossRefPubMedGoogle Scholar
  34. 34.
    Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155CrossRefPubMedGoogle Scholar
  35. 35.
    Graham CH, Fine PVA (2008) Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecol Lett 11:1265–1277CrossRefPubMedGoogle Scholar
  36. 36.
    Keddy PA (1992) Assembly and response rules—2 goals for predictive community ecology. J Veg Sci 3:157–164CrossRefGoogle Scholar
  37. 37.
    Cody ML, Diamond JM (1975) Ecology and evolution of communities. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  38. 38.
    Wintle BA, Bekessy SA, Keith DA, van Wilgen BW, Cabeza M, Schroder B, Carvalho SB, Falcucci A, Maiorano L, Regan TJ, Rondinini C, Boitani L, Possingham HP (2011) Ecological-economic optimization of biodiversity conservation under climate change. Nat Clim Chang 1:355–359CrossRefGoogle Scholar
  39. 39.
    Allsopp N (2014) Fynbos : ecology, evolution, and conservation of a megadiverse region. Oxford University Press, OxfordCrossRefGoogle Scholar
  40. 40.
    Cowling RM (1992) The ecology of fynbos : nutrients, fire and diversity. Oxford University Press, Cape TownGoogle Scholar
  41. 41.
    Cowling RM, Pressey RL, Rouget M, Lombard AT (2003) A conservation plan for a global biodiversity hotspot—the Cape Floristic Region, South Africa. Biol Conserv 112:191–216CrossRefGoogle Scholar
  42. 42.
    Mucina L, Rutherford MC (2006) The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, PretoriaGoogle Scholar
  43. 43.
    Keith DA, Akcakaya HR, Thuiller W, Midgley GF, Pearson RG, Phillips SJ, Regan HM, Araujo MB, Rebelo TG (2008) Predicting extinction risks under climate change: coupling stochastic population models with dynamic bioclimatic habitat models. Biol Lett 4:560–563CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Slabbert E, Jacobs SM, Jacobs K (2014) The soil bacterial communities of South African Fynbos riparian ecosystems invaded by Australian acacia species. Plos One 9(1):1–10CrossRefGoogle Scholar
  45. 45.
    Slabbert E, Kongor RY, Esler KJ, Jacobs K (2010) Microbial diversity and community structure in Fynbos soil. Mol Ecol 19:1031–1041CrossRefPubMedGoogle Scholar
  46. 46.
    Stafford WHL, Baker GC, Brown SA, Burton SG, Cowan DA (2005) Bacterial diversity in the rhizosphere of Proteaceae species. Environ Microbiol 7:1755–1768CrossRefPubMedGoogle Scholar
  47. 47.
    Tripathi BM, Kim M, Tateno R, Kim W, Wang JJ, Lai-Hoe A, Ab Shukor NA, Rahim RA, Go R, Adams JM (2015) Soil pH and biome are both key determinants of soil archaeal community structure. Soil Biol Biochem 88:1–8CrossRefGoogle Scholar
  48. 48.
    Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910CrossRefGoogle Scholar
  49. 49.
    Stegen JC, Freestone AL, Crist TO, Anderson MJ, Chase JM, Comita LS, Cornell HV, Davies KF, Harrison SP, Hurlbert AH, Inouye BD, Kraft NJB, Myers JA, Sanders NJ, Swenson NG, Vellend M (2013) Stochastic and deterministic drivers of spatial and temporal turnover in breeding bird communities. Glob Ecol Biogeogr 22:202–212CrossRefGoogle Scholar
  50. 50.
    Ofiteru ID, Lunn M, Curtis TP, Wells GF, Criddle CS, Francis CA, Sloan WT (2010) Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci U S A 107:15345–15350CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Hardy OJ, Couteron P, Munoz F, Ramesh BR, Pelissier R (2012) Phylogenetic turnover in tropical tree communities: impact of environmental filtering, biogeography and mesoclimatic niche conservatism. Glob Ecol Biogeogr 21:1007–1016CrossRefGoogle Scholar
  52. 52.
    Manning J, Goldblatt P (2012) Plants of the Greater Cape Floristic Region. SANBI, Biodiversity for Life, PretoriaGoogle Scholar
  53. 53.
    Zhou HW, Li DF, Tam NFY, Jiang XT, Zhang H, Sheng HF, Qin J, Liu X, Zou F (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME J 5:741–749CrossRefPubMedGoogle Scholar
  54. 54.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Micribiol 57:2259–2261CrossRefGoogle Scholar
  56. 56.
    Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464CrossRefPubMedGoogle Scholar
  57. 57.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. Plos One 5(3):1–10CrossRefGoogle Scholar
  58. 58.
    Diniz JAF, Terribile LC, da Cruz MJR, Vieira LCG (2010) Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence. Glob Ecol Biogeogr 19:916–926CrossRefGoogle Scholar
  59. 59.
    Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10CrossRefGoogle Scholar
  60. 60.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  62. 62.
    Fine PVA, Kembel SW (2011) Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34:552–565CrossRefGoogle Scholar
  63. 63.
    Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior—a permutational regression approach. Evolution 48:1487–1499CrossRefGoogle Scholar
  64. 64.
    Cavender-Bares J, Holbrook NM (2001) Hydraulic properties and freezing-induced cavitation in sympatric evergreen and deciduous oaks with, contrasting habitats. Plant Cell Environ 24:1243–1256CrossRefGoogle Scholar
  65. 65.
    Pontarp M, Canback B, Tunlid A, Lundberg P (2012) Phylogenetic analysis suggests that habitat filtering is structuring marine bacterial communities across the globe. Microb Ecol 64:8–17CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Anderson LC, Wesselingh FP, Hartman JH (2010) A phylogenetic and morphologic context for the radiation of an endemic fauna in a long-lived lake: Corbulidae (Bivalvia; Myoida) in the Miocene Pebas Formation of western Amazonia. Paleobiology 36:534–554CrossRefGoogle Scholar
  67. 67.
    Ackerly DD, Schwilk DW, Webb CO (2006) Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 87:S50–S61CrossRefPubMedGoogle Scholar
  68. 68.
    Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003CrossRefPubMedGoogle Scholar
  69. 69.
    Miles DB (1991) The comparative method in evolutionary biology—Harvey, Ph, Pagel, Md. Science 254:134–136CrossRefPubMedGoogle Scholar
  70. 70.
    Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108CrossRefPubMedGoogle Scholar
  71. 71.
    Tripathi BM, Kim M, Singh D, Lee-Cruz L, Lai-Hoe A, Ainuddin AN, Go R, Rahim RA, Husni MHA, Chun J, Adams JM (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb Ecol 64:474–484CrossRefPubMedGoogle Scholar
  72. 72.
    Singh D, Lee-Cruz L, Kim WS, Kerfahi D, Chun JH, Adams JM (2014) Strong elevational trends in soil bacterial community composition on Mt. Ha lla, South Korea. Soil Biol Biochem 68:140–149CrossRefGoogle Scholar
  73. 73.
    Ren L, Jeppesen E, He D, Wang J, Liboriussen L, Xing P, Wu QL (2015) pH influences the importance of niche-related and neutral processes in lacustrine bacterioplankton assembly. Appl Environ Microbiol 81:3104–3114CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Lauber CL, Fierer N (2009) Using pyrosequencing to compare the phylogenetic and functional attributes of soil bacterial communities. J Nematol 41:346–347Google Scholar
  75. 75.
    Slabbert E, van Heerden CJ, Jacobs K (2010) Optimisation of automated ribosomal intergenic spacer analysis for the estimation of microbial diversity in Fynbos soil. S Afr J Sci 106:52–55CrossRefGoogle Scholar
  76. 76.
    Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960CrossRefPubMedGoogle Scholar
  77. 77.
    Nunan N, Wu K, Young IM, Crawford JW, Ritz K (2002) In situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil. Microb Ecol 44:296–305CrossRefPubMedGoogle Scholar
  78. 78.
    Nunan N, Wu KJ, Young IM, Crawford JW, Ritz K (2003) Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil. FEMS Microbiol Ecol 44:203–215CrossRefPubMedGoogle Scholar
  79. 79.
    Grundmann GL, Debouzie D (2000) Geostatistical analysis of the distribution of NH4+ and NO2--oxidizing bacteria and serotypes at the millimeter scale along a soil transect. FEMS Microbiol Ecol 34:57–62PubMedGoogle Scholar
  80. 80.
    Bent SJ, Gucker CL, Oda Y, Forney LJ (2003) Spatial distribution of Rhodopseudomonas palustris ecotypes on a local scale. Appl Environ Microbiol 69:5192–5197CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Bundt M, Widmer F, Pesaro M, Zeyer J, Blaser P (2001) Preferential flow paths: biological ‘hot spots’ in soils. Soil Biol Biochem 33:729–738CrossRefGoogle Scholar
  82. 82.
    Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci U S A 112:E1326–E1332CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Weiher E, Freund D, Bunton T, Stefanski A, Lee T, Bentivenga S (2011) Advances, challenges and a developing synthesis of ecological community assembly theory. Philos Trans R Soc B Biol Sci 366:2403–2413CrossRefGoogle Scholar
  84. 84.
    Vreulink JM, Esterhuyse A, Jacobs K, Botha A (2007) Soil properties that impact yeast and actinomycete numbers in sandy low nutrient soils. Can J Microbiol 53:1369–1374CrossRefPubMedGoogle Scholar
  85. 85.
    De Marco A, Gentile AE, Arena C, De Santo AV (2005) Organic matter, nutrient content and biological activity in burned and unburned soils of a Mediterranean maquis area of southern Italy. Int J Wildland Fire 14:365–377CrossRefGoogle Scholar
  86. 86.
    Neary DG, Klopatek CC, DeBano LF, Ffolliott PF (1999) Fire effects on belowground sustainability: a review and synthesis. For Ecol Manag 122:51–71CrossRefGoogle Scholar
  87. 87.
    Witkowski ETF, Mitchell DT (1987) Variations in soil phosphorus in the Fynbos biome, South-Africa. J Ecol 75:1159–1171CrossRefGoogle Scholar
  88. 88.
    Jhonson C, ebrary Inc. (2009) Biology of soil science. Oxford Book Co.,, Jaipur, India, pp. 301 p. ill.Google Scholar
  89. 89.
    Bardgett RD (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, New YorkCrossRefGoogle Scholar
  90. 90.
    Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321CrossRefGoogle Scholar
  91. 91.
    Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  92. 92.
    Singh JS, Raghubanshi AS, Singh RS, Srivastava SC (1989) Microbial biomass acts as a source of plant nutrients in dry tropical forest and savannah. Nature 338:499–500CrossRefGoogle Scholar
  93. 93.
    De Deyn GB, Van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633CrossRefPubMedGoogle Scholar
  94. 94.
    Cowling RM, Proches S, Partridge TC (2009) Explaining the uniqueness of the Cape flora: incorporating geomorphic evolution as a factor for explaining its diversification. Mol Phylogenet Evol 51:64–74CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • I. Moroenyane
    • 1
  • S. B. M. Chimphango
    • 2
  • J. Wang
    • 3
  • H-K. Kim
    • 4
  • Jonathan Miles Adams
    • 1
  1. 1.School of Biological Sciences, College of Natural SciencesSeoul National UniversitySeoulSouth Korea
  2. 2.Department of Biological SciencesUniversity of Cape TownCape TownSouth Africa
  3. 3.Nanjing Institute of Geography and LimnologyChinese Academy of ScienceNanjingChina
  4. 4.Celemics, Inc612 Avison Biomedican Research Center, Yonsei Medical CenterSeoulSouth Korea

Personalised recommendations