Microbial communities associated with distance- and density-dependent seedling mortality in a tropical rainforest

  • J. L. WoodEmail author
  • P. T. Green
  • J. J. Vido
  • C. Celestina
  • K. E. Harms
  • A. E. Franks


The high levels of diversity within tropical rainforest communities has been linked to non-random patterns of seedling mortality with several studies implicating pathogenic plant–microbe interactions in driving mortality processes. Despite the proposed importance of microorganisms in maintaining rainforest diversity, few studies have investigated soil community dynamics in relation to non-random mortality processes. A mechanistic understanding of microbial processes that help create rainforest diversity is critical for the conservation of these ecosystems. This study investigated microbial community dynamics that may underpin distance- and density-dependent mortality in the long-term forest dynamics plot, Davies Creek, in tropical Far North Queensland using community fingerprinting. We hypothesized that: (1) microbial involvement in distance-dependent seedling mortality would result in an increase in community similarity or the presence of predictor OTUs in conspecific adult tree rhizospheres, relative to physically nearby heterospecifics; (2) on average, plant species identified as having a history of distance dependent seedling mortality would exhibit more similar microbial communities among their conspecific individuals, than those that did not; and (3) dense patches of conspecific seedlings would promote the assembly of distinct soil microbial communities, which may be involved in density-dependent seedling mortality. We found no evidence of rhizosphere community similarity amongst adult plant rhizospheres. However, the presence of densely germinating seedlings altered the soil communities relative to seedling-sparse soils, enriching different OTUs depending on the patch location.


Janzen–Connell Rainforest diversity Soil pathogens Tropical 



This research was supported by the La Trobe University Securing Food water and Environment Research Focus Area. A.E.F. and J.L.W also received supported from the Defense Science Institute, Office of Naval Research Global (Award No N626909-13–1-N259) AOARD (award FA2386-14–1-4032) and the Australian Research Council Linkage Grants (LP140100459). P.T.G. is also supported by the Long-Term Ecological Research Network.

Author contributions

Experimental designs were conceived by JLW, PTG and AEF. Integration of long-term plant demographic data into microbial community sampling designs was carried out by KEH and PTG. Sample collection was carried out by JLW, PTG and AEF. Soil DNA extraction, Data QC, bioinformatics analysis, trait-based analysis and statistical tests of ARISA and rRNA were performed by JLW. Soil physico-chemical analyses were carried out by CC JV and JLW. Manuscript was drafted by JLW and JLW, KEH, PTG, AEF, CC and JV contributed to the revision and copy-editing of the final manuscript.

Supplementary material

11258_2019_989_MOESM1_ESM.docx (6.6 mb)
Electronic supplementary material 1 (DOCX 6802 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26(1):32–46Google Scholar
  2. Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6(8):769–779PubMedCrossRefPubMedCentralGoogle Scholar
  3. Aoki T, O'Donnell K, Geiser DM (2014) Systematics of key phytopathogenic fusarium species: Current status and future challenges. J Gen Plant Pathol 80(3):189–201CrossRefGoogle Scholar
  4. Augspurger CK (1983) Seed dispersal of the tropical tree, platypodium elegans, and the escape of its seedlings from fungal pathogens. J Ecol 71(3):759–771CrossRefGoogle Scholar
  5. Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65(6):1705–1712CrossRefGoogle Scholar
  6. Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings: Experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61(2):211–217PubMedCrossRefGoogle Scholar
  7. Bachelot B, Uriarte M, McGuire KL, Thompson J, Zimmerman J (2017) Arbuscular mycorrhizal fungal diversity and natural enemies promote coexistence of tropical tree species. Ecology 98(3):712–720PubMedCrossRefGoogle Scholar
  8. Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506(7486):85–88PubMedCrossRefGoogle Scholar
  9. Baldeck CA, Harms KE, Yavitt JB, John R, Turner BL, Valencia R, Navarrete H, Davies SJ, Chuyong GB, Kenfack D, Thomas DW, Madawala S, Gunatilleke N, Gunatilleke S, Bunyavejchewin S, Kiratiprayoon S, Yaacob A, Supardi MN, Dalling JW (2012) Soil resources and topography shape local tree community structure in tropical forests. Proceedings. Biological sciences 280(1753):20122532PubMedCrossRefGoogle Scholar
  10. Balunas MJ, Kinghorn AD (2005) Drug discovery from medicinal plants. Life Sci 78(5):431–441PubMedCrossRefGoogle Scholar
  11. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clément C, Ouhdouch Y, Van Wezeld GP (2016) Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80(1):1–43PubMedCrossRefGoogle Scholar
  12. Bell T, Freckleton RP, Lewis OT (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol Lett 9(5):569–574PubMedCrossRefGoogle Scholar
  13. Benítez MS, Hersh MH, Vilgalys R, Clark JS (2013) Pathogen regulation of plant diversity via effective specialization. Trends Ecol Evol 28(12):705–711PubMedCrossRefGoogle Scholar
  14. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13CrossRefGoogle Scholar
  15. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256(1):67–83CrossRefGoogle Scholar
  16. Bever JD, Mangan SA, Alexander HM (2015) "Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325CrossRefGoogle Scholar
  17. Chaer G, Fernandes M, Myrold D, Bottomley P (2009) Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils. Microb Ecol 58(2):414–424PubMedCrossRefGoogle Scholar
  18. Chen ZS, Hsieh CF, Jiang FY, Hsieh TH, Sun IF (1997) Relations of soil properties to topography and vegetation in a subtropical rain forest in southern taiwan. Plant Ecol 132(2):229–241CrossRefGoogle Scholar
  19. Chen L, Xiang W, Wu H, Ouyang S, Zhou B, Zeng Y, Chen Y, Kuzyakov Y (2019) Tree species identity surpasses richness in affecting soil microbial richness and community composition in subtropical forests. Soil Biol Biochemistry 130:113–121CrossRefGoogle Scholar
  20. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143CrossRefGoogle Scholar
  21. Comita LS, Queenborough SA, Murphy SJ, Eck JL, Xu K, Krishnadas M, Beckman N, Zhu Y (2014) Testing predictions of the janzen-connell hypothesis: A meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J Ecol 102(4):845–856PubMedPubMedCentralCrossRefGoogle Scholar
  22. Connell JH, Green PT (2000) Seedling dynamics over thirty-two years in a tropical rain forest tree. Ecology 81(2):568–584CrossRefGoogle Scholar
  23. Connell JH, Tracey JG, Webb LJ (1984) Compensatory recruitment, growth, and mortality as factors maintaining rain forest tree diversity. Ecol Monogr 54(2):141–164CrossRefGoogle Scholar
  24. Connell JH, Debski I, Gehring CA, Goldwasser L, Green PT, Harms KE et al (2005) Dynamics of seedling recruitment in an australian tropical rainforest. In: Bermingham E, Moritz C (eds) Tropical rainforests: past, present, and future. Chicago University Press, Chicago, pp 486–506.Google Scholar
  25. da Silva AR, Ferro JA, Reinach FD, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NA, Alves LM, Do Amaral AM (2002) Comparison of the genomes of two xanthomonas pathogens with differing host specificities. Nature 417(6887):459–463PubMedCrossRefGoogle Scholar
  26. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol Monogr 67(3):345–366Google Scholar
  27. Eck JL, Stump SM, Delavaux CS, Mangan SA, Comita LS (2019) Evidence of within-species specialization by soil microbes and the implications for plant community diversity. Proc Natl Acad Sci 116(15):7371–7376PubMedCrossRefGoogle Scholar
  28. Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65(10):4630–4636PubMedPubMedCentralGoogle Scholar
  29. Gilbert GS, Foster RB, Hubbell SP (1994) Density and distance-to-adult effects of a canker disease of trees in a moist tropical forest. Oecologia 98(1):100–108PubMedCrossRefGoogle Scholar
  30. Gobet A, Boetius A, Ramette A (2014) Ecological coherence of diversity patterns derived from classical fingerprinting and next generation sequencing techniques. Environ Microbiol 16(9):2672–2681PubMedCrossRefPubMedCentralGoogle Scholar
  31. Green PT, Harms KE, Connell JH (2014) "Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest. Proc Natl Acad Sci USA 111(52):18649–18654PubMedCrossRefPubMedCentralGoogle Scholar
  32. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37(2):112–129PubMedCrossRefPubMedCentralGoogle Scholar
  33. Hilbert DW, Ostendorf B, Hopkins MS (2001) Sensitivity of tropical forests to climate change in the humid tropics of north queensland. Aust Ecol 26(6):590–603CrossRefGoogle Scholar
  34. Hughes L (2003) Climate change and australia: Trends, projections and impacts. Aust Ecol 28(4):423–443CrossRefGoogle Scholar
  35. Iinuma M, Tosa H, Tanaka T, Shimano R, Asai F, Yonemori S (1994) Two xanthones from root bark of garcinia subelliptica. Phytochemistry 35(5):1355–1360CrossRefGoogle Scholar
  36. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104(940):501–528CrossRefGoogle Scholar
  37. Jari Oksanen, FGB, Michael F, Roeland K, Pierre L, Dan McGlinn, Peter RM, O'Hara RB, Simpson GL, Peter Solymos M, Stevens HH, Eduard S, Helene W (2019)
  38. Jay KR, Popkin-Hall ZR, Coblens MJ, Oberski JT, Sharma PP, Boyer SL (2016) "New species of austropurcellia, cryptic short-range endemic mite harvestmen (arachnida, opiliones, cyphophthalmi) from australia’s wet tropics biodiversity hotspot. ZooKeys 2016(586):37–93Google Scholar
  39. Kovacs A, Yacoby K, Gophna U (2010) A systematic assessment of automated ribosomal intergenic spacer analysis (arisa) as a tool for estimating bacterial richness. Res Microbiol 161(3):192–197PubMedCrossRefGoogle Scholar
  40. Kuete V (2010) Potential of cameroonian plants and derived products against microbial infections: a review. Planta Med 76(14):1479–1491PubMedCrossRefPubMedCentralGoogle Scholar
  41. Lamichhane JR, Dürr C, Schwanck AA, Robin MH, Sarthou JP, Cellier V, Messéan A, Aubertot JN (2017) Integrated management of damping-off diseases. A review. Agron Sustain Dev 37(2):10CrossRefGoogle Scholar
  42. Lee SB, Taylor JW (1992) Phylogeny of five fungus-like protoctistan phytophthora species, inferred from the internal transcribed spacers of ribosomal DNA. Mol Biol Evol 9(4):636–653PubMedGoogle Scholar
  43. Liu Y, Fang S, Chesson P, He F (2015) The effect of soil-borne pathogens depends on the abundance of host tree species. Nat Commun 6:10017PubMedPubMedCentralCrossRefGoogle Scholar
  44. Mackeen MM, Ali AM, Lajis NH, Kawazu K, Hassan Z, Amran M, Habsah M, Mooi LY, Mohamed SM (2000) Antimicrobial, antioxidant, antitumour-promoting and cytotoxic activities of different plant part extracts of garcinia atroviridis griff. Ex t. Anders. J Ethnopharmacol 72(3):395–402CrossRefGoogle Scholar
  45. Mangan SA, Schnitzer SA, Herre EA, MacK KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466(7307):752–755PubMedCrossRefGoogle Scholar
  46. Maňourová A, Leuner O, Tchoundjeu Z, Van Damme P, Verner V, Přibyl O, Lojka B (2019) Medicinal potential, utilization and domestication status of bitter kola (garcinia kola heckel) in west and central africa. Forests 10(2):124CrossRefGoogle Scholar
  47. McCarthy-Neumann S, Nez I (2013) Plant-soil feedback links negative distance dependence and light gradient partitioning during seedling establishment. Ecology 94(4):780–786CrossRefGoogle Scholar
  48. McDonald KR, Rowley JJL, Richards SJ, Frankham GJ (2016) A new species of treefrog (litoria) from cape york peninsula, australia. Zootaxa 4171(1):153–169PubMedCrossRefGoogle Scholar
  49. Mendes LW, Tsai SM, Navarrete AA, de Hollander M, van Veen JA, Kuramae EE (2015) Soil-borne microbiome: Linking diversity to function.". Microb Ecol 70(1):255–265PubMedCrossRefGoogle Scholar
  50. Norghauer JM, Newbery DM, Tedersoo L, Chuyong GB (2010) Do fungal pathogens drive density-dependent mortality in established seedlings of two dominant african rain-forest trees? J Trop Ecol 26(3):293–301CrossRefGoogle Scholar
  51. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313(5790):1115–1118PubMedCrossRefGoogle Scholar
  52. Nuccio EE, Anderson-Furgeson J, Estera KY, Pett-Ridge J, De Valpine P, Brodie EL, Firestone MK (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97(5):1307–1318PubMedCrossRefGoogle Scholar
  53. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Williams SE (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355(6332):eaai9214PubMedCrossRefGoogle Scholar
  54. Pedraza-Chaverri J, Cárdenas-Rodríguez N, Orozco-Ibarra M, Pérez-Rojas JM (2008) Medicinal properties of mangosteen (garcinia mangostana). Food Chem Toxicol 46(10):3227–3239PubMedCrossRefGoogle Scholar
  55. Perigo CV, Torres RB, Bernacci LC, Guimarães EF, Haber LL, Facanali R, Vieira MA, Quecini V, Marques MO (2016) The chemical composition and antibacterial activity of eleven piper species from distinct rainforest areas in southeastern brazil. Ind Crops Prod 94:528–539CrossRefGoogle Scholar
  56. Poorter L, Bongers L, Bongers F (2006) Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups. Ecology 87(5):1289–1301PubMedCrossRefGoogle Scholar
  57. Prideaux, B. (2014). Rainforest tourism, conservation and management: Challenges for sustainable development.CrossRefGoogle Scholar
  58. Pringle EG, Álvarez-Loayza P, Terborgh J (2007) Seed characteristics and susceptibility to pathogen attack in tree seeds of the peruvian amazon. Plant Ecol 193(2):211–222CrossRefGoogle Scholar
  59. R Core Team (2018).
  60. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75(8):2495–2505PubMedPubMedCentralCrossRefGoogle Scholar
  61. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2(4):404–416PubMedCrossRefGoogle Scholar
  62. Sapkota R, Nicolaisen M (2015) An improved high throughput sequencing method for studying oomycete communities. J Microbiol Methods 110:33–39PubMedCrossRefGoogle Scholar
  63. Schappe T, Albornoz FE, Turner BL, Neat A, Condit R, Jones FA (2017) The role of soil chemistry and plant neighbourhoods in structuring fungal communities in three panamanian rainforests. J Ecol 105(3):569–579CrossRefGoogle Scholar
  64. Smith LM, Reynolds HL (2015) Plant-soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96(9):2523–2532PubMedCrossRefGoogle Scholar
  65. Terborgh J (2012) Enemies maintain hyperdiverse tropical forests. Am Nat 179(3):303–314PubMedCrossRefGoogle Scholar
  66. Theimer TC, Gehring CA, Green PT, Connell JH (2011) Terrestrial vertebrates alter seedling composition and richness but not diversity in an australian tropical rain forest. Ecology 92(8):1637–1647PubMedCrossRefGoogle Scholar
  67. Tripathi BM, Song W, Slik JWF, Sukri RS, Jaafar S, Dong K, Adams JM (2016) Distinctive tropical forest variants have unique soil microbial communities, but not always low microbial diversity. Front Microbiol 7:376PubMedPubMedCentralCrossRefGoogle Scholar
  68. Tsui CC, Chen ZS, Hsieh CF (2004) Relationships between soil properties and slope position in a lowland rain forest of southern taiwan. Geoderma 123(1–2):131–142CrossRefGoogle Scholar
  69. Wilson JB, Peet RK, Dengler J, Pärtel M (2012) Plant species richness: The world records. J Veget Sci 23(4):796–802CrossRefGoogle Scholar
  70. Wood JL, Tang C, Franks AE (2018) Competitive traits are more important than stress-tolerance traits in a cadmium-contaminated rhizosphere: a role for trait theory in microbial ecology. Front Microbiol 9:121PubMedPubMedCentralCrossRefGoogle Scholar
  71. Wright SJ (2002) Plant diversity in tropical forests: A review of mechanisms of species coexistence. Oecologia 130(1):1–14PubMedCrossRefPubMedCentralGoogle Scholar
  72. Zhang X, Lin L, Chen M, Zhu Z, Yang W, Chen B, Yang Q, An Q (2012) A nonpathogenic fusarium oxysporum strain enhances phytoextraction of heavy metals by the hyperaccumulator sedum alfredii hance. J Hazard Mater 229–230:361–370PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Physiology, Anatomy and MicrobiologyLa Trobe University, Melbourne CampusVictoriaAustralia
  2. 2.Research Centre for Future LandscapesLa Trobe University, Melbourne CampusVictoriaAustralia
  3. 3.Department of Ecology, Environment and EvolutionLa Trobe University, Melbourne CampusVictoriaAustralia
  4. 4.Department of Animal, Plant and Soil SciencesAgriBio the Centre for AgriBiosciences, La Trobe UniversityBundooraAustralia
  5. 5.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA

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