Conspecific negative density dependence in rainy season enhanced seedling diversity across habitats in a tropical forest

Abstract

Conspecific negative density dependence (CNDD) could be one of the most important local-scale mechanisms shaping plant species coexistence. However, the spatial and temporal changes in the strength CNDD and the implications for the plant diversity remain unknown. We used 10 years of seedling data, in a seasonal tropical rainforest, to discover how CNDD influences tree seedling survival across habitats and seasons. We also evaluated the relation between CNDD and species diversity. We found the strength of CNDD in the valley habitat was significantly stronger than in ridge habitat in rainy season, but not significantly different in dry season. Corresponding to expectations of CNDD as mechanism of diversity maintenance, seedling species diversity was significantly higher in valley habitat than in ridge habitat and significantly correlated with CNDD. Additionally, conspecific and heterospecific seedling neighbour densities positively affected the survival of tree seedlings, but heterospecific adult neighbour density had a weak effect. Our study finds that CNDD varied significantly across habitats and was correlated with local seedling diversity. Our results highlight the importance of CNDD in driving species diversity at the local scale. Recognizing the spatial and temporal variation in the strength of CNDD will aid efforts to model and understand species coexistence.

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References

  1. Aide TM (1992) Dry season leaf production—an escape from herbivory. Biotropica 24:532–537. https://doi.org/10.2307/2389016

    Article  Google Scholar 

  2. 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 506:85–88. https://doi.org/10.1038/nature12911

    CAS  Article  PubMed  Google Scholar 

  3. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1

  4. Bell T, Freckleton RP, Lewis OT (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol Lett 9:569–574. https://doi.org/10.1111/j.1461-0248.2006.00905.x

    Article  PubMed  Google Scholar 

  5. Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283. https://doi.org/10.1146/annurev-micro-092611-150107

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Brenes-Arguedas T, Coley PD, Kursar TA (2009) Pests vs. drought as determinants of plant distribution along a tropical rainfall gradient. Ecology 90:1751–1761. https://doi.org/10.1890/08-1271.1

    Article  PubMed  Google Scholar 

  7. Bunker DE, Carson WP (2005) Drought stress and tropical forest woody seedlings: effect on community structure and composition. J Ecol 93:794–806. https://doi.org/10.1111/j.1365-2745.2005.01019.x

    Article  Google Scholar 

  8. Cao M, Zou XM, Warren M, Zhu H (2006) Tropical forests of Xishuangbanna, China. Biotropica 38:306–309. https://doi.org/10.1111/j.1744-7429.2006.00146.x

    Article  Google Scholar 

  9. Carson WP, Anderson JT, Leigh EG, Schnitzer SA (2008) Challenges associated with testing and falsifying the Janzen-Connell hypothesis: a review and critique. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Blackwell Publishing Ltd, Oxford, pp 210–241

    Google Scholar 

  10. Chen L, Mi X, Comita LS, Zhang L, Ren H, Ma K (2010) Community-level consequences of density dependence and habitat association in a subtropical broad-leaved forest. Ecol Lett 13:695–704. https://doi.org/10.1111/j.1461-0248.2010.01468.x

    Article  PubMed  Google Scholar 

  11. Chesson P (1994) Multispecies competition in variable environments. Theor Popul Biol 45:227–276

    Article  Google Scholar 

  12. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. https://doi.org/10.1146/annurev.ecolsys.31.1.343

    Article  Google Scholar 

  13. Coley PD (1998) Possible effects of climate change on plant/herbivore interactions in moist tropical forests. Clim Change 39:455–472

    Article  Google Scholar 

  14. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335. https://doi.org/10.1146/annurev.ecolsys.27.1.305

    Article  Google Scholar 

  15. Comita LS, Hubbell SP (2009) Local neighborhood and species' shade tolerance influence survival in a diverse seedling bank. Ecology 90:328–334. https://doi.org/10.1890/08-0451.1

    Article  PubMed  Google Scholar 

  16. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332. https://doi.org/10.1126/science.1190772

    CAS  Article  PubMed  Google Scholar 

  17. 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 102:845–856. https://doi.org/10.1111/1365-2745.12232

    Article  PubMed  PubMed Central  Google Scholar 

  18. Condit R (1998) Tropical forest census plots: methods and results from Barro Colorado Island, Panama and a comparison with other plots. Springer Science & Business Media, New York

    Book  Google Scholar 

  19. Connell J (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees, Dynamics of Population. In: Den Boer PJ, Gradwell GR (eds) Dynamics of populations centre for agricultural publishing and documentation. Wageningen, The Netherlands, pp 298–312

    Google Scholar 

  20. Crawford KM, Bauer JT, Comita LS, Eppinga MB, Johnson DJ, Mangan SA, Queenborough SA, Strand AE, Suding KN, Umbanhowar J, Bever JD (2019) When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol Lett 22:1274–1284. https://doi.org/10.1111/ele.13278

    Article  PubMed  Google Scholar 

  21. Detto M, Visser MD, Wright SJ, Pacala SW (2019) Bias in the detection of negative density dependence in plant communities. Ecol Lett. https://doi.org/10.1111/ele.13372

    Article  PubMed  Google Scholar 

  22. Dirzo R, Boege K (2008) Patterns of herbivory and defense in tropical dry and rain forests. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Blackwell Publishing Ltd, Oxford, pp 63–78

    Google Scholar 

  23. Forrister DL, Endara MJ, Younkin GC, Coley PD, Kursar TA (2019) Herbivores as drivers of negative density dependence in tropical forest saplings. Science 363:1213–1216. https://doi.org/10.1126/science.aau9460

    CAS  Article  PubMed  Google Scholar 

  24. Gilbert GS, Parker IM (2016) The evolutionary ecology of plant disease: a phylogenetic perspective. Annu Rev Phytopathol 54:549–578. https://doi.org/10.1146/annurev-phyto-102313-045959

    CAS  Article  PubMed  Google Scholar 

  25. Harms KE, Wright SJ, Calderon O, Hernandez A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495. https://doi.org/10.1038/35006630

    CAS  Article  PubMed  Google Scholar 

  26. He FL, Duncan RP (2000) Density-dependent effects on tree survival in an old-growth Douglas fir forest. J Ecol 88:676–688. https://doi.org/10.1046/j.1365-2745.2000.00482.x

    Article  Google Scholar 

  27. HilleRisLambers J, Adler P, Harpole W, Levine J, Mayfield M (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248. https://doi.org/10.1146/annurev-ecolsys-110411-160411

    Article  Google Scholar 

  28. Hossain M, Veneklaas EJ, Hardy GES, Poot P (2019) Tree host-pathogen interactions as influenced by drought timing: linking physiological performance, biochemical defence and disease severity. Tree Physiol 39:6–18. https://doi.org/10.1093/treephys/tpy113

    CAS  Article  PubMed  Google Scholar 

  29. Hu YH (2010) A study on the habitat variation and distribution patterns of tree species in a 20-ha forest dynamics plot at Bubeng, Xishuangbanna, SW China. PhD thesis, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences

  30. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528. https://doi.org/10.1086/282687

    Article  Google Scholar 

  31. Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative density dependence and forest diversity. Science 336:904–907. https://doi.org/10.1126/science.1220269

    CAS  Article  PubMed  Google Scholar 

  32. Johnson DJ, Bourg NA, Howe R, McShea WJ, Wolf A, Clay K (2014) Conspecific negative density-dependent mortality and the structure of temperate forests. Ecology 95:2493–2503

    Article  Google Scholar 

  33. Johnson DJ, Condit R, Hubbell SP, Comita LS (2017) Abiotic niche partitioning and negative density dependence drive tree seedling survival in a tropical forest. Proc R Soc B 284:8. https://doi.org/10.1098/rspb.2017.2210

    Article  Google Scholar 

  34. LaManna JA, Walton ML, Turner BL, Myers JA (2016) Negative density dependence is stronger in resource-rich environments and diversifies communities when stronger for common but not rare species. Ecol Lett 19:657–667. https://doi.org/10.1111/ele.12603

    Article  PubMed  Google Scholar 

  35. LaManna JA, Mangan SA, Alonso A, Bourg NA, Brockelman WY, Bunyavejchewin S, Chang LW, Chiang JM, Chuyong GB, Clay K, Condit R, Cordell S, Davies SJ, Furniss TJ, Giardina CP, Gunatilleke IAUN, Gunatilleke CVS, He FL, Howe RW, Hubbell SP, Hsieh CF, Inman-Narahari FM, Janik D, Johnson DJ, Kenfack D, Korte L, Kral K, Larson AJ, Lutz JA, McMahon SM, McShea WJ, Memiaghe HR, Nathalang A, Novotny V, Ong PS, Orwig DA, Ostertag R, Parker GG, Phillips RP, Sack L, Sun IF, Tello JS, Thomas DW, Turner BL, Diaz DMV, Vrska T, Weiblen GD, Wolf A, Yap S, Myers JA (2017) Plant diversity increases with the strength of negative density dependence at the global scale. Science 356:1389–1392

    CAS  Article  Google Scholar 

  36. Leigh EG, Davidar P, Dick CW, Puyravaud JP, Terborgh J, ter Steege H, Wright SJ (2004) Why do some tropical forests have so many species of trees? Biotropica 36:447–473. https://doi.org/10.1111/j.1744-7429.2004.tb00342.x

    Article  Google Scholar 

  37. Liang M, Liu X, Gilbert GS, Zheng Y, Luo S, Huang F, Yu S (2016) Adult trees cause density-dependent mortality in conspecific seedlings by regulating the frequency of pathogenic soil fungi. Ecol Lett 19:1448–1456. https://doi.org/10.1111/ele.12694

    Article  PubMed  Google Scholar 

  38. Lin L, Comita LS, Zheng Z, Cao M (2012) Seasonal differentiation in density-dependent seedling survival in a tropical rain forest. J Ecol 100:905–914. https://doi.org/10.1111/j.1365-2745.2012.01964.x

    Article  Google Scholar 

  39. Lu J, Johnson DJ, Qiao X, Lu Z, Wang Q, Jiang M (2015) Density dependence and habitat preference shape seedling survival in a subtropical forest in central China. J Plant Ecol 8:568–577

    Article  Google Scholar 

  40. Martinez-Camilo R, Gonzalez-Espinosa M, Ramirez-Marcial N, Cayuela L, Angel Perez-Farrera M (2018) Tropical tree species diversity in a mountain system in southern Mexico: local and regional patterns and determinant factors. Biotropica 50:499–509. https://doi.org/10.1111/btp.12535

    Article  Google Scholar 

  41. Martinkova Z, Honek A (2011) Asymmetrical intraspecific competition in Echinochloa crus-galli is related to differences in the timing of seedling emergence and seedling vigour. Plant Ecol 212:1831–1839. https://doi.org/10.1007/s11258-011-9953-8

    Article  Google Scholar 

  42. Meinzer FC, Andrade JL, Goldstein G, Holbrook NM, Cavelier J, Wright SJ (1999) Partitioning of soil water among canopy trees in a seasonally dry tropical forest. Oecologia 121:293–301. https://doi.org/10.1007/s004420050931

    CAS  Article  PubMed  Google Scholar 

  43. Murphy SJ, Wiegand T, Comita LS (2017) Distance-dependent seedling mortality and long-term spacing dynamics in a neotropical forest community. Ecol Lett 20:1469–1478. https://doi.org/10.1111/ele.12856

    Article  PubMed  Google Scholar 

  44. O'Brien MJ, Reynolds G, Ong R, Hector A (2017) Resistance of tropical seedlings to drought is mediated by neighbourhood diversity. Nat Ecol Evol 1:1643–1648. https://doi.org/10.1038/s41559-017-0326-0

    Article  PubMed  Google Scholar 

  45. Paine CET, Harms KE, Schnitzer SA, Carson WP (2008) Weak competition among tropical tree seedlings: Implications for species coexistence. Biotropica 40:432–440. https://doi.org/10.1111/j.1744-7429.2007.00390.x

    Article  Google Scholar 

  46. Peters HA (2003) Neighbour-regulated mortality: the influence of positive and negative density dependence on tree populations in species-rich tropical forests. Ecol Lett 6:757–765. https://doi.org/10.1046/j.1461-0248.2003.00492.x

    Article  Google Scholar 

  47. Pu X, Zhu Y, Jin G (2017) Effects of local biotic neighbors and habitat heterogeneity on seedling survival in a spruce-fir valley forest, northeastern China. Ecol Evol 7:4582–4591. https://doi.org/10.1002/ece3.3030

    Article  PubMed  PubMed Central  Google Scholar 

  48. Queenborough SA, Burslem D, Garwood NC, Valencia R (2007) Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88:2248–2258. https://doi.org/10.1890/06-0737.1

    Article  PubMed  Google Scholar 

  49. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  50. Song QH, Tan ZH, Zhang YP, Cao M, Sha LQ, Tang Y, Liang NS, Schaefer D, Zhao JF, Zhao JB, Zhang X, Yu L, Deng XB (2013) Spatial heterogeneity of soil respiration in a seasonal rainforest with complex terrain. Iforest-Biogeosci For 6:65–72. https://doi.org/10.3832/ifor0681-006

    Article  Google Scholar 

  51. Song X, Hogan JA, Lin L, Wen H, Cao M, Yang J (2018a) Canopy openness and topographic habitat drive tree seedling recruitment after snow damage in an old-growth subtropical forest. For Ecol Manage 429:493–502. https://doi.org/10.1016/j.foreco.2018.07.038

    Article  Google Scholar 

  52. Song X, Johnson DJ, Cao M, Umana MN, Deng XB, Yang XF, Zhang WF, Yang J (2018b) The strength of density-dependent mortality is contingent on climate and seedling size. J Veg Sci 29:662–670. https://doi.org/10.1111/jvs.12645

    Article  Google Scholar 

  53. Spear ER, Coley PD, Kursar TA (2015) Do pathogens limit the distributions of tropical trees across a rainfall gradient? J Ecol 103:165–174. https://doi.org/10.1111/1365-2745.12339

    Article  Google Scholar 

  54. Sterck F, Markesteijn L, Schieving F, Poorter L (2011) Functional traits determine trade-offs and niches in a tropical forest community. P Natl Acad Sci USA 108:20627–20632. https://doi.org/10.1073/pnas.1106950108

    Article  Google Scholar 

  55. Svenning JC, Fabbro T, Wright SJ (2008) Seedling interactions in a tropical forest in Panama. Oecologia 155:143–150. https://doi.org/10.1007/s00442-007-0884-y

    Article  PubMed  Google Scholar 

  56. Swinfield T, Lewis OT, Bagchi R, Freckleton RP (2012) Consequences of changing rainfall for fungal pathogen-induced mortality in tropical tree seedlings. Ecol Evol 2:1408–1413. https://doi.org/10.1002/ece3.252

    Article  PubMed  PubMed Central  Google Scholar 

  57. Terborgh J (2012) Enemies maintain hyperdiverse tropical forests. Am Nat 179:303–314. https://doi.org/10.1086/664183

    Article  PubMed  Google Scholar 

  58. Wright JS (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14

    Article  Google Scholar 

  59. Wu J, Swenson NG, Brown C, Zhang C, Yang J, Ci X, Li J, Sha L, Cao M, Lin L (2016) How does habitat filtering affect the detection of conspecific and phylogenetic density dependence? Ecology 97:1182–1193. https://doi.org/10.1890/14-2465.1

    Article  PubMed  Google Scholar 

  60. Zhang C, Yang J, Sha L, Ci X, Li J, Cao M, Brown C, Swenson NG, Lin L (2017) Lack of phylogenetic signals within environmental niches of tropical tree species across life stages. Sci Rep. https://doi.org/10.1038/srep42007

    Article  PubMed  PubMed Central  Google Scholar 

  61. Zhu Y, Comita LS, Hubbell SP, Ma K (2015) Conspecific and phylogenetic density-dependent survival differs across life stages in a tropical forest. J Ecol 103:957–966. https://doi.org/10.1111/1365-2745.12414

    Article  Google Scholar 

  62. Zhu Y, Queenborough SA, Condit R, Hubbell SP, Ma KP, Comita LS (2018) Density-dependent survival varies with species life-history strategy in a tropical forest. Ecol Lett 21:506–515. https://doi.org/10.1111/ele.12915

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (31800353, 31870410 and 31670442), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000), the CAS 135 program (no. 2017XTBG-T01), and the West Light Foundation of Chinese Academy of Sciences. We thank Xishuangbanna Station for Tropical Rain Forest Ecosystem Studies of Xishuangbanna Tropical Botanical Garden for assistance with the field work.

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XS, WZ, JY and MC designed the study, XS performed analyses, WZ, XD and XY collected data, XS, WZ, DJ, JY and MA led the writing of the manuscript; other authors provided editorial advice.

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Correspondence to Jie Yang.

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Communicated by Marie-Josée Fortin.

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Song, X., Zhang, W., Johnson, D.J. et al. Conspecific negative density dependence in rainy season enhanced seedling diversity across habitats in a tropical forest. Oecologia 193, 949–957 (2020). https://doi.org/10.1007/s00442-020-04729-2

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Keywords

  • Intraspecific
  • Janzen–Connell hypothesis
  • Plant–soil feedback
  • Plant–plant interaction
  • Species diversity