Plant Ecology

, Volume 215, Issue 8, pp 795–807 | Cite as

The contribution of understory light availability and biotic neighborhood to seedling survival in secondary versus old-growth temperate forest

  • Fei Lin
  • Liza S. Comita
  • Xugao Wang
  • Xuejiao Bai
  • Zuoqiang Yuan
  • Dingliang Xing
  • Zhanqing Hao


Seedling survival plays an important role in the maintenance of species diversity and forest dynamics. Although substantial gains have been made in understanding the factors driving patterns of seedling survival in forests, few studies have considered the simultaneous contribution of understory light availability and the local biotic neighborhood to seedling survival in temperate forests at different successional stages. Here, we used generalized linear mixed models to assess the relative importance of understory light availability and biotic neighborhood variables on seedling survival in secondary and old-growth temperate forest in north eastern China at two levels (community and guild). At the community level, biotic neighborhood effects on seedling survival were more important than understory light availability in both forests. In both the old-growth and secondary forests, conspecific basal area had a negative effect on seedling survival, consistent with negative conspecific density dependence. At guild levels, the relative importance of light and biotic neighborhood on seedling survival showed considerable variation among guilds in both forests. Available understory light tended to have positive effects on seedling survival for shrub and light-demanding species in the old-growth forest, but negative effects on survival of shade-tolerant seedlings in the secondary forest. For tree species and shade-tolerant species, the best fit models included neighborhood variables, but that was not the case for shrubs, light-demanding, or mid shade-tolerant species. Overall, our results demonstrate that the relative importance of understory light availability and biotic factors on seedling survival vary with species life-history strategy and forest successional stage.


Canopy openness Density dependence Shade tolerance Species coexistence Temperate forests 

Supplementary material

11258_2014_332_MOESM1_ESM.pdf (74 kb)
Supplementary material 1 (PDF 74 kb)


  1. Bai X, Qeenborough SA, Wang X et al (2012) Effects of local biotic neighbors and habitat heterogeneity on tree and shrub seedling survival in an old-growth temperate forest. Oecologia 170(3):755–765PubMedCrossRefGoogle Scholar
  2. Bartels SF, Chen HY (2010) Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91(7):1931–1938PubMedCrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. R package version: 0.999999-0.
  4. Beckage B, Clark JS (2003) Seedling survival and growth of three forest tree species: the role of spatial heterogeneity. Ecology 84(7):1861–1894Google Scholar
  5. Brown MJ, Parker GC (1994) Canopy light transmittance in a chronosequence of mixed-species deciduous forests. Can J For Res 24:1694–1703CrossRefGoogle Scholar
  6. Bruelheide H, BÖhnke M, Both S et al (2011) Community assembly during secondary forest succession in a Chinese subtropical forest. Ecol Monogr 81(1):25–41CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Models selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  8. Burton JI, Zenner EK, Frelich LE, Cornett MW (2009) Patterns of plant community structure within and among primary and second-growth northern hardwood forest stands. For Ecol Manag 258:2556–2568CrossRefGoogle Scholar
  9. Canham CD (1989) Different responses to gaps among shade-tolerant tree species. Ecology 70(3):548–550CrossRefGoogle Scholar
  10. Canham CD, Lepage PT, Coates KD (2004) A neighborhood analysis of canopy tree competition: effects of shading versus crowding. Can J For Res 34:778–787CrossRefGoogle Scholar
  11. Chazdon RL (2008) Chance and determinism in tropical forest succession. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Wiley-Blackwell, Chichester, pp 384–408Google Scholar
  12. 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(6):695–704PubMedCrossRefGoogle Scholar
  13. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  14. Clark DB, Clark DA (1985) Seedling dynamics of a tropical tree: impact of herbivory and meristem damage. Ecology 66(6):1884–1892CrossRefGoogle Scholar
  15. Clark DB, Clark DA, Rich PM, Weiss S, Oberbauer SF (1996) Landscape-scale analyses of forest structure and understory light environments in a neotropical lowland rain forest. Can J ForRes 26:747–757CrossRefGoogle Scholar
  16. Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  17. Comita LS, Hubbell SP (2009) Local neighborhood and species’ shade tolerance influence survival in a diverse seedling bank. Ecology 90(2):328–334PubMedCrossRefGoogle Scholar
  18. Comita LS, Uriarte M, Thompson J, Jonckheere I, Canham CD, Zimmerman JK (2009) Abiotic and biotic drivers of seedling survival in a hurricane-impacted tropical forest. J Ecol 97:1346–1359CrossRefGoogle Scholar
  19. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332PubMedCrossRefGoogle Scholar
  20. Condit R (1998) Tropical forest census plots. Springer, BerlinCrossRefGoogle Scholar
  21. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR (eds) Dynamics of populations. Center for Agricultural Publishing and Documentation, Wageningen, pp 298–312Google Scholar
  22. Constabel AJ, Lieffers VJ (1996) Seasonal patterns of light transmission through boreal mixedwood canopy. Can J For Res 26:1008–1014CrossRefGoogle Scholar
  23. Denslow JS, Sandra GG (2000) Variation in stand structure, light and seedling abundance across a tropical moist forest chronosequence, Panama. J Veg Sci 11:201–212CrossRefGoogle Scholar
  24. Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyser (GLA), version 2.0: imaging software to extract canopy structure and gap light indices from true-colour fisheye photographs, users’ manual and program documentation. Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New YorkGoogle Scholar
  25. Gelman A, Hill J (2006) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  26. Gendron F, Messier C, Comeau PG (2001) Temporal variations in the understory photosynthetic photon flux density of a deciduous stand: the effects of canopy development, solar elevation, and sky conditions. Agric For Meteorol 106:23–40CrossRefGoogle Scholar
  27. Gravel D, Canham CD, Beaudet M, Messier C (2010) Shade tolerance, canopy gaps and mechanisms of coexistence of forest trees. Oikos 119:475–484CrossRefGoogle Scholar
  28. Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52(1):107–145CrossRefGoogle Scholar
  29. Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206CrossRefGoogle Scholar
  30. Hao Z, Li B, Zhang J, Wang X, Ye J, Yao X (2008a) Broad-leaved Korean pine (Pinus koraiensis) mixed forest plot in Changbai (CBS) of China: community composition and structure. J Plant Ecol 32(2):238–250 (in Chinese)Google Scholar
  31. Hao Z, Zhang J, Li B, Ye J, Wang X, Yao X (2008b) Natural secondary poplar-birch forest in Changbai Mountain: species composition and community structure. J Plant Ecol 32(2):251–261 (in Chinese)Google Scholar
  32. HilleRisLambers JHR, Clark JS, Beckage B (2002) Density dependent mortality and the latitudinal gradient in species diversity. Nature 417:732–735CrossRefGoogle Scholar
  33. Hubbell SP, Ahumada JA, Condit R, Foster RB (2001) Local neighborhood effects on long-term survival of individual trees in a neotropical forest. Ecol Res 16:859–875CrossRefGoogle Scholar
  34. Janzen DH (1970) Herbivores and the number of tree species in tropical forest. Am Nat 104:501–528CrossRefGoogle Scholar
  35. Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative dependence and forest diversity. Science 336:904–907PubMedCrossRefGoogle Scholar
  36. Kobe RK (1999) Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80:187–201CrossRefGoogle Scholar
  37. Kobe RK, Pacala SW, Silander JA (1995) Juvenile tree survivorship as a component of shade tolerance. Ecol Appl 5(2):517–532CrossRefGoogle Scholar
  38. Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352CrossRefGoogle Scholar
  39. Kunstler G, Curt T, Bouchaud M, Lepart J (2005) Growth, mortality, and morphological response of European beech and downy oak along a light gradient in a sub-Mediterranean forest. Can J For Res 35:1657–1658CrossRefGoogle Scholar
  40. Li BH, Wang XG, Zhang J, Bai XJ et al (2010) Changbaishan temperate forest dynamics plots: broad-leaved korean pine mixed forest and secondary poplar-birch forest species composition and their spatial pattern. China Forestry Publishing House, BeijingGoogle Scholar
  41. Lieffers VJ, Stadt KJ (1994) Growth of understory Picea glauca, Calamagrostis canadensis, and Epilobium angustifolium in relation to overstory light transmission. Can J For Res 24:1193–1198CrossRefGoogle Scholar
  42. Lieffers VJ, Messier C, Stadt KJ, Gendron F, Comeau PG (1999) Predicting and managing light in the understory of boreal forests. Can J Forest Res 29(6):796–811CrossRefGoogle Scholar
  43. Lin LX, Comita LS, Zheng Z, Cao M (2012) Seasonal differentiation in density-dependent seedling survival in a tropical rain forest. J Ecol 100(4):905–914CrossRefGoogle Scholar
  44. Lusk CH, Del Pozo A (2002) Survival and growth of seedlings of 12 Chilean rainforest trees in two light environments: gas exchange and biomass distribution correlates. Austral Ecol 27:173–182CrossRefGoogle 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 466:752–755PubMedCrossRefGoogle Scholar
  46. McCarthy-Neumann S, Kobe RK (2008) Tolerance of soil pathogens co-varies with shade tolerance across species of tropical tree seedlings. Ecology 89(7):1883–1892PubMedCrossRefGoogle Scholar
  47. Mejía-Domínguez NR, Meave JA, Díaz-Ávalos C (2012) Spatial structure of the abiotic environment and its association with sapling community structure and dynamics in a cloud forest. Int J Biometeorol 56(2):305–318PubMedCrossRefGoogle Scholar
  48. Messier C (1996) Managing light and understory vegetation in boreal and temperate broadleaf-conifer forests. In: Comeau PG, Thomas KD (eds) Silviculture of temperate and boreal broadleaf-conifer mixtures Land management handbook 36. BC Ministry of Forests, Victoria, pp 59–81Google Scholar
  49. Messier C, Sylvain P, Yves B (1998) Effects of overstory and understory vegetation on the understory light environment in mixed boreal forests. J Veg Sci 9:511–520CrossRefGoogle Scholar
  50. Messier C, Posada J, Aubin I, Beaudet M (2009) Functional relationships between old-growth forest canopies, understory light and vegetation dynamics. In: Wirth C, Gleixner G, Heimann M (eds) Old-growth forests, ecological studies 207. Springer, Berlin Heidelberg, pp 115–139CrossRefGoogle Scholar
  51. Montes F, Rubio A, Barbeito I, Canellas I (2008) Characterization of the spatial structure of the canopy in Pinus silvestris L. stands in Central Spain from hemispherical photographs. For Ecol Manag 255:580–590CrossRefGoogle Scholar
  52. Montgomery RA, Chazdon RL (2001) Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology 82:2707–2718CrossRefGoogle Scholar
  53. Montgomery RA, Chazdon RL (2002) Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165–174CrossRefGoogle Scholar
  54. Nakashizuka T (2001) Species coexistence in temperate, mixed deciduous forests. Trend Ecol Evol 16:205–210CrossRefGoogle Scholar
  55. Nicotra AB, Chazdon RL, Iriarte S (1999) Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80:1908–1926CrossRefGoogle Scholar
  56. Osunkjoya OO, Ash JE, Hopkins MS, Graham AW (1992) Factors affecting survival of tree seedlings in North Queensland rainforests. Oecologia 91:569–578CrossRefGoogle Scholar
  57. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  58. Paine CET, Harms KE, Schnitzer SA, Carson WP (2008) Weak competition among tropical tree seedlings: implication for species coexistence. Biotropica 40(4):432–440CrossRefGoogle Scholar
  59. Peña-Claros M (2003) Changes in forest structure and species composition during secondary forest succession in the Bolivian Amazon. Biotropica 35(4):450–461CrossRefGoogle Scholar
  60. Piao T, Comita LS, Jin G, Kim JH (2013) Density dependence across multiple life stages in a temperate old-growth forest of northeast China. Oecologia 172:207–217PubMedCentralPubMedCrossRefGoogle Scholar
  61. Poorter L, Arets EJMM (2003) Light environment and tree strategies in a Bolivian tropical moist forest: an evaluation of the light partitioning hypothesis. Plant Ecol 166:295–306CrossRefGoogle Scholar
  62. Queenborough SA, Burslem D, Garwood NC, Valencia R (2007) Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88:2248–2258PubMedCrossRefGoogle Scholar
  63. Queenborough SA, Burslem DFRP, Garwodd NC, Valencia R (2009) Taxonomic scale-dependence of habitat niche partitioning and biotic neighbourhood on survival of tropical tree seedlings. Proc Roy Soc B Biol Sci 276:4197–4205CrossRefGoogle Scholar
  64. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
  65. Rüger N, Huth A, Hubbell SP, Condit R (2009) Response of recruitment to light availability across a tropical lowland rain forest community. J Ecol 97:1360–1368CrossRefGoogle Scholar
  66. Rüger N, Huth A, Hubbell SP, Condit R (2011) Determinants of mortality across a tropical lowland rainforest community. Oikos 120:1047–1056CrossRefGoogle Scholar
  67. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33:481–518CrossRefGoogle Scholar
  68. Svenning JC (2000) Small canopy gaps influence plant distributions in the rain forest understory. Biotropica 32:252–261CrossRefGoogle Scholar
  69. Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJGoogle Scholar
  70. Valladares F, Guzmán B (2006) Canopy structure and spatial heterogeneity of understory light in an abandoned Holm oak woodland. Ann For Sci 63:749–761CrossRefGoogle Scholar
  71. Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257CrossRefGoogle Scholar
  72. Walters MB, Reich PB (1996) Are shade tolerance, survival, and growth linked? Low light and nitrogen effect on hardwood seedlings. Ecology 77:841–853CrossRefGoogle Scholar
  73. Wang X, Hao Z, Zhang J, Lian J, Li B et al (2009) Tree size distributions in an old-growth temperate forest. Oikos 118:25–36CrossRefGoogle Scholar
  74. Wang L, Li B, Ye J, Bai X, Yuan Z et al (2011) Dynamics of short-term tree mortality in broad-leaved Korean pine (Pinus koraiensis) mixed forest in the Changbai Mountains. Biodivers Sci 19(2):260–270 (in Chinese)CrossRefGoogle Scholar
  75. Wang X, Comita LS, Hao Z, Davies SJ et al (2012) Local-scale drives of tree survival in a temperate forest. PLoS ONE 7(2):e29469PubMedCentralPubMedCrossRefGoogle Scholar
  76. Wayne PM, Bazzaz FA (1993) Birch seedling responses to daily time courses of light in experimental forest gaps and shadehouses. Ecology 74(5):1500–1515CrossRefGoogle Scholar
  77. Webb CO, Peart DR (1999) Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80:2006–2017CrossRefGoogle Scholar
  78. Webb CO, Peart DR (2000) Habitat associations of trees and seedlings in a Bornean rain forest. J Ecol 88:464–478CrossRefGoogle Scholar
  79. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14Google Scholar
  80. Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91(12):3664–3674PubMedCrossRefGoogle Scholar
  81. Yang H, Li D (1985) Distribution patterns of dominant tree species on northern slope of Changbai Mountain. Res For Ecosyst 5:1–14 (in Chinese)Google Scholar
  82. Zhang M, Guan D, Han S, Wu J, Zhang J, Jin M et al (2005) Climatic dynamics of broadleaved Korean pine forest in Changbai Mountain during the last 22 Years. Chin J Ecol 24(9):1007–1012 (in Chinese)Google Scholar
  83. Zhang Z, Hao Z, Ye J, Lin F, Yuan Z (2013) Short-term death dynamics of trees in natural secondary poplar-birch forest in Changbai Mountains of Northeast China. Chin J Ecol 24(2):303–310 (in Chinese)Google Scholar
  84. Zurr AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Fei Lin
    • 1
    • 2
  • Liza S. Comita
    • 3
    • 4
  • Xugao Wang
    • 1
  • Xuejiao Bai
    • 5
  • Zuoqiang Yuan
    • 1
  • Dingliang Xing
    • 1
    • 2
  • Zhanqing Hao
    • 1
  1. 1.State Key Laboratory of Forest and Soil Ecology, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Evolution, Ecology and Organismal BiologyThe Ohio State UniversityColumbusUSA
  4. 4.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  5. 5.College of ForestryShenyang Agricultural UniversityShenyangChina

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