Morphological variation of fine root systems and leaves in primary and secondary tropical forests of Hainan Island, China

Abstract

Key message

In older, unlogged rainforest of Hainan Island, China, leaves of saplings were larger, and fine root systems of saplings were thicker with fewer root tips than in historically logged areas. These results were consistent among 15 Angiosperm lineages, even though families differed widely in their leaf and root traits.

Context

How plant organ morphologies vary with environment is key for inferring plant functional strategies.

Aims

We were interested in quantifying any changes in fine root and leaf morphology of saplings with local-scale environmental variation in tropical forest, and if any variation in organ morphologies differed with plant lineage.

Methods

We measured functional traits of fine root systems and leaves of saplings from 15 families in historically logged and unlogged Chinese tropical forest, where soil fertility and texture slightly decreased with greater forest age.

Results

Root morphological traits were more conservative, while leaf morphologies were more acquisitive in primary forest than in secondary forest. From secondary to primary forests, mean root system diameter increased 0.4 mm, mean specific root length decreased 3.5 m kg−1, and mean root system branching intensity decreased by 0.3 tips cm−1. Similarly, from secondary to primary forests, average leaf area increased 7 cm2 and specific leaf area decreased 0.8 m2 kg−1. Leaf thickness and root tissue density were not different. Among the selected plant families, root and leaf morphological differences between forest types were consistent.

Conclusion

Within lineage (i.e., intraspecific) root and leaf morphological variation showed contrasting patterns. Local-scale variation in soil phosphorus and base saturation affected intraspecific variation in root diameter and specific root length.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data availability

The datasets generated and analyzed for this study are available on the FigShare repository: https://doi.org/10.6084/m9.figshare.7996328

References

  1. Ackerly D, Knight C, Weiss S, Barton K, Starmer K (2002) Leaf size specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia 130:449–457

    CAS  PubMed  Google Scholar 

  2. Addo-Danso SD, Defrenne CE, McCormack ML, Ostonen IV, Addo-Danso A, Foli EG, Borden KA, Isaac ME, Prescott CE (2019) Fine-root morphological trait variation in tropical forest ecosystems: an evidence synthesis. Plant Ecol 221:1–13

    Google Scholar 

  3. Baraloto C, Paine CET, Poorter L, Beauchene J, Bonal D, Domenach A-M, Hérault B, Patiño S, Roggy J-C, Chave J (2010) Decoupled leaf and stem economics in rain forest trees. Ecol Lett 13:1338–1347

    PubMed  Google Scholar 

  4. Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699

    PubMed  Google Scholar 

  5. Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu Rev Ecol Evol Syst 16:363–392

    Google Scholar 

  6. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366

    PubMed  Google Scholar 

  7. Chen W, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. P Natl Acad Sci USA 113:8741–8746

    CAS  Google Scholar 

  8. Christensen NL, Peet RK (1984) Convergence during secondary forest succession. J Ecol 72:25–36

    Google Scholar 

  9. Comas L, Eissenstat D (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytol 182:919–928

    CAS  PubMed  Google Scholar 

  10. Craine JM (2006) Competition for nutrients and optimal root allocation. Plant Soil 285:171–185

    CAS  Google Scholar 

  11. Craine JM, Froehle J, Tilman D, Wedin D, Chapin FS (2001) The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos 93:274–285

    Google Scholar 

  12. Defrenne CE, McCormack ML, Roach WJ, Addo-Danso SD, Simard SW (2019) Intraspecific Fine-root trait-environment relationships across interior Douglas-fir forests of Western Canada. Plants 8:199

    CAS  PubMed Central  Google Scholar 

  13. Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC (2016) The global spectrum of plant form and function. Nature 529:167–171

    PubMed  Google Scholar 

  14. Eissenstat D, Wells C, Yanai R, Whitbeck J (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42

    CAS  Google Scholar 

  15. Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124

    PubMed  Google Scholar 

  16. Flores O, Garnier E, Wright IJ, Reich PB, Pierce S, Diaz S, Pakeman RJ, Rusch GM, Bernard-Verdier M, Testi B, Bakker JP (2014) An evolutionary perspective on leaf economics: phylogenetics of leaf mass per area in vascular plants. Ecol Evol 4:2799–2811

    PubMed  PubMed Central  Google Scholar 

  17. Fitter A (1991) Characteristics and functions of root systems. In: Waisel Y, Eschel A, Beeckman T, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Decker Inc., New York, pp 49–78

    Google Scholar 

  18. Fitter A, Stickland T (1991) Architectural analysis of plant root systems 2. Influence of nutrient supply on architecture in contrasting plant species. New Phytol 118:383–389

    Google Scholar 

  19. Fortunel C, Fine PVA, Baraloto C (2012) Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct Ecol 26:1153–1161

    Google Scholar 

  20. Freschet GT, Roumet C (2017) Sampling roots to capture plant and soil functions. Funct Ecol 31:1506–1518

    Google Scholar 

  21. Freschet GT, Valverde-Barrantes OJ, Tucker CM, Craine JM, McCormack ML, Violle C, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM (2017) Climate soil and plant functional types as drivers of global fine-root trait variation. J Ecol 105:1182–1196

    Google Scholar 

  22. Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol 15:688–695

    Google Scholar 

  23. Giehl RF, Gruber BD, von Wirén N (2013) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778

    PubMed  Google Scholar 

  24. Givnish T (1984) Leaf and canopy adaptations in tropical forests. In: Medina E, Mooney HA, Vasquez-Yanes C (eds) Physiological ecology of plants of the wet tropics. Springer, The Netherlands, pp 51–84

    Google Scholar 

  25. Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683

    PubMed  Google Scholar 

  26. Hertel D, Leuschner C, Hölscher D (2003) Size and strucutre of fine root systems in old-growth and secondary tropical montane forests (Costa Rica). Biotropica 35:143–153

    Google Scholar 

  27. Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth architecture and function. Plant Soil 321:153–187

    CAS  Google Scholar 

  28. Hogan JA, Baraloto C, Valverde-Barrantes O, Xu H, Ding Q (2019) Sapling leaf and root traits from 6.6 km Jianfengling transect. Figshare repository. [Dataset]. V3. https://doi.org/10.6084/m9.figshare.7996328.v3

  29. Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns of fine root traits along a 120000-year soil chronosequence in temperate rainforest. J Ecol 99:954–963

    Google Scholar 

  30. Hopkins MS, Redell P, Hewett RK, Graham AW (1996) Comparison of root and mycorrhizal characterstics in primary and secondary forests on a metamorphoic soil in North Queensland, Australia. J Trop Ecol 12:871–885

    Google Scholar 

  31. Huang Q, Li Y, Zheng D, Zhang J, Wan L, Jiang Y, Zhao Y (1995) Study on tropical vegetation series in Jianfengling Hainan Island. In: Zeng Q, Zhou G, Yide L, Wu Z, Chen B (eds) Researches on tropical forest ecosystems in Jianfengling of China. China Forestry Publishing House, Beijing China, pp 5–25

    Google Scholar 

  32. Iversen CM, McCormack ML, Powell AS, Blackwood CB, Freschet GT, Kattge J, Roumet C, Stover DB, Soudzilovskaia NA, Valverde-Barrantes OJ (2017) A global Fine-Root Ecology Database to address below-ground challenges in plant ecology. New Phytol 215:15–26

    PubMed  Google Scholar 

  33. Jackson R, Canadell J, Ehleringer JR, Mooney H, Sala O, Schulze E (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411

    CAS  PubMed  Google Scholar 

  34. Jin D, Cao X, Ma K (2013) Leaf functional traits vary with the adult height of plant species in forest communities. J Plant Ecol 7:68–76

    Google Scholar 

  35. Keddy P (1992) A pragmatic approach to functional ecology. Funct Ecol 6:621–626

    Google Scholar 

  36. Keenan TF, Niinemets Ü (2017) Global leaf trait estimates biased due to plasticity in the shade. Nat Plants 3:16201

    Google Scholar 

  37. Kembel SW, Cahill JF Jr (2011) Independent evolution of leaf and root triats within and aming temperate grassland plant communities. PLoS One 6:e19992

    CAS  PubMed  PubMed Central  Google Scholar 

  38. King DA (1996) Allometry and life history of tropical trees. J Trop Ecol 12:25–44

    Google Scholar 

  39. Kong D, Ma C, Zhang Q, Li L, Chen X, Zeng H, Guo D (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872

    PubMed  Google Scholar 

  40. Kong D, Wang J, Zeng H, Liu M, Miao Y, Wu H, Kardol P (2017) The nutrient absorption–transportation hypothesis: optimizing structural traits in absorptive roots. New Phytol 213:1569–1572

    PubMed  Google Scholar 

  41. Körner C (2018) Concepts in empirical plant ecology. Plant Ecol Divers 11:405–428

    Google Scholar 

  42. Kramer-Walter KR, Bellingham PJ, Smissen RD MTR, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310

    Google Scholar 

  43. Laliberté E (2017) Below-ground frontiers in trait-based plant ecology. New Phytol 213:1597–1603

    PubMed  Google Scholar 

  44. Laliberté E, Lambers H, Burgess TI, Wright SJ (2015) Phosphorus limitation soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. New Phytol 206:507–521

    PubMed  Google Scholar 

  45. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    PubMed  PubMed Central  Google Scholar 

  46. Lambers H, Albornoz F, Kotula L, Laliberté E, Ranathunge K, Teste FP, Zemunik G (2017) How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:1–23

    Google Scholar 

  47. Lenth R. (2018) Emmeans: estimated marginal means aka least-squares means R Package Version 1. https://CRAN.R-project.org/package=emmeans

  48. Leuschner C, Harteveld M, Hertel D (2009) Consequences of increasing forest use intensity for biomass, morphology and growth of fine roots in a tropical moist forest on Sulawesi, Indonesia. Agric Ecosyst Environ 129:474–481

    Google Scholar 

  49. Li F, Hu H, McCormack ML, Feng DF, Liu X, Bao W (2018) Community-level economics spectrum of fine roots driven by nutrient limitations in subalpine forests. J Ecol 107:1238–1249

    Google Scholar 

  50. Liu Y, Dawson W, Prati D, Haeuser E, Feng Y, van Kluenen M (2016) Does greater specific leaf area plasticity help plants maintain a high performance when shaded? Ann Bot 118:1329–1336

    PubMed  PubMed Central  Google Scholar 

  51. López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    PubMed  Google Scholar 

  52. Lu M, Hedin LO (2019) Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modeling. Nat Ecol Evol 3:239–250

    PubMed  Google Scholar 

  53. Lüdecke D. (2019) sjstats: statistical function for regression models (version 0.17.3). R packge: https://www.cran.r-project.org/package=sjstats. https://doi.org/10.5281/zenodo.1284472

  54. Lynch J (2005) Root architecture and nutrient acquisition. In: BassiriRad H (ed) Nutrient acquisition by plants (analysis and synthesis), vol 181. Springer, Berlin, pp 147–183

    Google Scholar 

  55. Ma Z, Guo D, Xu X, Lu M, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97

    CAS  PubMed  Google Scholar 

  56. Maherali H (2017) The evolutionary ecology of roots. New Phytol 215:1295–1297

    PubMed  Google Scholar 

  57. McCormack ML, Iversen CM (2019) Physical and functional constraints on viable belowground acquisition strategies. Front Plant Sci 10:1215

    PubMed  PubMed Central  Google Scholar 

  58. McCormack ML, Adams TS, Smithwick EA, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831

    Google Scholar 

  59. McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Iversen CM HEA, Jackson RB (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    PubMed  Google Scholar 

  60. Mommer L, Weemstra M (2012) The role of roots in the resource economics spectrum. New Phytol 195:725–727

    PubMed  Google Scholar 

  61. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408

    CAS  PubMed  Google Scholar 

  62. Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker M, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn A, Pronk A (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442

    Google Scholar 

  63. Parish JAD, Bazzaz FA (1976) Underground niche separation in succesional plants. Ecology 57:1281–1288

    Google Scholar 

  64. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51

    CAS  PubMed  Google Scholar 

  65. Powers JS, Peréz-Aviles D (2013) Edaphic factors are a more important control on surface roots than stand age in secondary tropical dry forests. Biotropica 45:1–9

    Google Scholar 

  66. Qui J (2008) Relationship between tropical forest canopy structure, understory vegetation and soil organic carbon content in Jianfengling, Hainan Island. Master’s Thesis. Chinese Academy of Foresty. https://doi.org/10.7666/d.D602796

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

  68. Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Google Scholar 

  69. Rijkers T, Pons T, Bongers F (2000) The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct Ecol 14:77–86

    Google Scholar 

  70. Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016) Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto-and arbuscular mycorrhizal trees. New Phytol 209:1184–1195

    PubMed  Google Scholar 

  71. Schenk HJ, Jackson RB (2002) Rooting depths lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–494

    Google Scholar 

  72. Shipley B. (1995) Structured interspecific determinants of specific leaf area in 34 species of herbaceous angiosperms. Funct Ecol 312–319

  73. Shipley B, De Bello F, Cornelissen JHC, Laliberté E, Laughlin DC, Reich PB (2016) Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180:923–931

    PubMed  Google Scholar 

  74. Turner BL (2008) Resource partitioning for soil phosphorus: a hypothesis. J Ecol 96:698–702

    CAS  Google Scholar 

  75. Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370

    CAS  PubMed  Google Scholar 

  76. Ushio M, Fujiki Y, Hidaka A, Kitayama K (2015) Linkage of root physiology and morphology as an adaptation to soil phosphorus impoverishment in tropical montane forests. Funct Ecol 29:1235–1245

    Google Scholar 

  77. Valverde-Barrantes OJ, Blackwood CB (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum: commentary on Kramer-Walter et al. (2016). J Ecol 104:1311–1313

    Google Scholar 

  78. Valverde-Barrantes OJ, Horning AL, Smemo KA, Blackwood CB (2016) Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant Soil 404:1–12

    CAS  Google Scholar 

  79. Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: the influence of ancestry growth form climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215:1562–1573

    PubMed  Google Scholar 

  80. Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    PubMed  Google Scholar 

  81. Wang R, Wang Q, Zhao N, Yu G, He N (2017) Complex trait relationships between leaves and absorptive roots: coordiunation in tissue N concentration but divergence in morphology. Ecol Evol 7:2697–2705

    PubMed  PubMed Central  Google Scholar 

  82. Wang R, Wang Q, Zhao N, Xu Z, Zhu X, Jiao C, Yu G, He N (2018) Different phylogenetic and environmental controls of first-order root morphological and nutrient traits: evidence of multidimensional root traits. Funct Ecol 32:29–39

    Google Scholar 

  83. Wang C, McCormack ML, Guo D, Li J (2019) Global meta-analysis reveals different patterns of root tip adjustments by angiosperm and gymnosperm trees in response to environmental gradients. J Biogeogr 46:123–133

    Google Scholar 

  84. Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD (2015) Root structural and functional dynamics in bioshpere models—evaluation and recommendations. New Phytol 205:59–78

    PubMed  Google Scholar 

  85. Weemstra M, Mommer L, Visser EJ, Ruijven J, Kuyper TW, Mohren GM, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169

    CAS  PubMed  Google Scholar 

  86. Weiher E, Werf A, Thompson K, Roderick M, Garnier E, Eriksson O (1999) Challenging Theophrastus: a common core list of plant traits for functional ecology. J Veg Sci 10:609–620

    Google Scholar 

  87. Wenhua L (2004) Degradation and restoration of forest ecosystems in China. For Ecol Manag 201:33–41

    Google Scholar 

  88. Werner P (1984) Changes in soil properties with wet forest succession in Costa Rica. Biotropica 16:43–50

    Google Scholar 

  89. Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268

    PubMed  Google Scholar 

  90. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin ST, Cornelissen JH, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Google Scholar 

  91. Wright SJ, Kitajima K, Kraft NJ, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Diaz S (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91:3664–3674

    PubMed  Google Scholar 

  92. Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S, Gallagher RV, Jacobs BF, Kooyman R, Law EA, Leishman MR (2017) Global climatic drivers of leaf size. Science. 357(6354):917–921

    CAS  PubMed  Google Scholar 

  93. Wu Z (1995) An introduction to the tropical forest soils and effect of shifting cultivation on soils in Jianfengling Hainan Island. In: Zeng Q, Zhou G, Yide L, Wu Z, Chen B (eds) Researches on tropical forest ecosystems in Jianfengling of China. China Forestry Publishing House, Beijing, pp 5–25

    Google Scholar 

  94. Xu H, Li Y, Liu S, Zang R, He F, Spence JR (2015) Partial recovery of a tropical rain forest a half-century after clear-cut and selective logging. J Appl Ecol 52:1044–1052

    Google Scholar 

  95. Zadworny M, McCormack ML, Mucha J, Reich PB, Oleksyn J (2016) Scots pine fine roots adjust along a 2000-km latitudinal climatic gradient. New Phytol 212:389–399

    PubMed  Google Scholar 

  96. Zangaro W, Alves RA, Lescano LE, Ansanelo AP (2012) Investment in fine roots and arbuscular mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica 44:141–151

    Google Scholar 

  97. Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050

    CAS  Google Scholar 

  98. Zeng Q (1995) Survey of water-heat condition and vegetation ecological series in Jianfengling. In: Zeng Q, Zhou G, Yide L, Wu Z, Chen B (eds) Researches on tropical forest ecosystems in Jianfengling of China. China Forestry Publishing House, Beijing China, pp 5–25

    Google Scholar 

  99. Zhou G (1995) Ecological effects of human activities in Jianfenglin Forest Region Hainan Island. In: Zeng Q, Zhou G, Yide L, Wu Z, Chen B (eds) Researches on tropical forest ecosystems in Jianfengling of China. China Forestry Publishing House, Beijing China, pp 38–48

    Google Scholar 

  100. Zhu H (2017) A biogeographical study on the flora of southern China. Ecol Evol 7:10398–10408

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the anonymous reviewers for comments that improved this work. We thank Sheyla Santana from the FIU GIS lab for her help producing Fig. 1. We acknowledge the assistance of the following people who helped in the field and with the processing of plant samples: Shaojun Ling, Yaxin Xie, Jaming Wang, Siqi Yang, Wenguang Tang, Shitaing Ma, Qiqi Zhang, and Jiazhu Shi. Assistance with taxonomic field identification was provided by Professor Yu from the Jianfengling Forest Bureau.

Funding

JAH received support via a short-term fellowship from CTFS-ForestGEO at the Smithsonian. We thank Stuart J. Davies. Additionally, we are grateful for many small personal donations that helped fund the soil analyses (http://www.experiment.com/chinaroots).

Author information

Affiliations

Authors

Corresponding author

Correspondence to J. Aaron Hogan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributions of the co-authors

Conceptualization: JAH, OJV-B, CB; Methodology: JAH, OJV-B, QD; Software: NA; Validation: JAH; Formal analysis: JAH; Investigation: JAH; Resources: JAH, CB, QD, XH; Data Curation: JAH; Writing—original draft: JAH; Writing—review and editing: JAH,OJV-B, QD, XH, CB ; Visualization: JAH; Supervision: CD, XH; Project administration: JAH; Funding acquisition: JAH

Handling Editor: Andreas Bolte

Appendix

Appendix

Fig. 6
figure6

Detailed topographic map (a) and topographic profile (b) of the 6.6- km transect in the Jianfengling Forest Reserve, Hainan Island, China, where functional traits of saplings were sampled. The transect started near the Jianfengling field house, at the entrance of the forest reserve. It progressed over one mountain, and over a stream (at km 4 of the transect), which delineated the secondary and primary areas of forest. At roughly km 5.5 of the transect, the transect entered the 60-ha CTFS-ForestGEO permanent forest dynamic plot

Fig. 7
figure7

Principle component analysis (variable scores plotted) of 7 leaf traits measured on 423 saplings of 72 species. Raw trait measurements were first scaled and centered

Table 4 PCA loadings for the first three principal components for 7 leaf traits. Traits used in analysis of variance models are bolded
Fig. 8
figure8

Principle components analysis (variable scores plotted) of 7 key root traits measured on 423 saplings of 72 species. Raw trait measurements were first scaled and centered

Table 5 PCA loadings for the first three principal components for 7 root traits. Traits used in analysis of variance models are bolded
Table 6 Individual collection counts of species along the 6-km JFL transect (Figs. 1 and 6) by forest type. For each individual sapling three to five fine root systems and three leaves were collected. Bolded species denote those where soil samples were analyzed each primary and secondary forest, totaling 300 individuals of 50 species. Data from those 300 individuals are used in Fig. 5 and Table 3)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hogan, J.A., Valverde-Barrantes, O.J., Ding, Q. et al. Morphological variation of fine root systems and leaves in primary and secondary tropical forests of Hainan Island, China. Annals of Forest Science 77, 79 (2020). https://doi.org/10.1007/s13595-020-00977-7

Download citation

Keywords

  • Plant functional traits
  • Trait variation
  • Root morphology
  • Leaf morphology
  • Tropical forest
  • Jianfengling
  • Hainan Island