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Effects of light on branch growth and death vary at different organization levels of branching units in Sakhalin spruce

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This study proves the existence of correlative inhibition, and demonstrates that role of light intensity in the growth and death varies among different levels of branching units.

Abstract

Within a tree crown, local light conditions vary within a branch and among different branches. Although the role of light intensity in the growth and survival of branches has been studied extensively, the effects of the spatial heterogeneity of light intensity on different levels of branching units are poorly understood. We investigated the effects of light intensity on the growth and death of primary branches (those branching off from the main stem) and secondary branches (those branching off from the primary branches) in the whole crown of Sakhalin spruce (Picea glehnii). The growth of shoot extension on a primary branch or secondary branch may be inhibited on sunlit trees compared to shaded trees when branches under relatively low local light intensity (rPPFD) levels, but it was increased with increasing rPPFD more rapidly on sunlit trees than on shaded trees. A relative importance analysis showed that, in the primary branches, branch growth was mainly influenced by rPPFD, and less influenced by its vertical position within the crown. However, the probability of death of a primary branch was equally influenced by its position within the crown and rPPFD. In contrast, rPPFD played a dominant role in both the growth and death of secondary branches. The results of our study suggest that local light intensity alone cannot fully explain the growth and survival of primary branches simultaneously, and the effects of light intensity vary among different levels of branching units.

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References

  • Bartoń K (2016) MuMIn: multi-model inference. R package version, 1.15.6. https://CRAN.R-project.org/package =MuMIn

  • Buston PM, Elith J (2011) Determinants of reproductive success in dominant pairs of clownfish: a boosted regression tree analysis. J Anim Ecol 80:528–538

    Article  PubMed  Google Scholar 

  • Cain ML, Dudle DA, Evans JP (1996) Spatial models of foraging in clonal plant species. Am J Bot:76–85

  • Chen L, Sumida A (2017) Patterns of branch growth and death in crowns of Sakhalin spruce, Picea glehnii (F. Schmidt). Mast Forests 8:26. https://doi.org/10.3390/f8010026

    Article  Google Scholar 

  • de Kroons H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143–152

    Article  Google Scholar 

  • De Kroon H, Huber H, Stuefer JF, Van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82

    Article  PubMed  Google Scholar 

  • De’Ath G (2007) Boosted trees for ecological modeling and prediction. Ecology 88:243–251

    Article  PubMed  Google Scholar 

  • Desalme D, Priault P, Gérant D, Dannoura M, Maillard P, Plain C, Epron D (2017) Seasonal variations drive short-term dynamics and partitioning of recently assimilated carbon in the foliage of adult beech and pine. New Phytol 213:140–153

    Article  PubMed  CAS  Google Scholar 

  • Dong T, Li J, Zhang Y, Korpelainen H, Niinemets Ü, Li C (2015) Partial shading of lateral branches affects growth, and foliage nitrogen-and water-use efficiencies in the conifer Cunninghamia lanceolata growing in a warm monsoon climate. Tree Physio 35:632–643

    Article  CAS  Google Scholar 

  • Duchesneau R, Lesage I, Messier C, Morin H (2001) Effects of light and intraspecific competition on growth and crown morphology of two size classes of understory balsam fir saplings. For Ecol Manage 140:215–225

    Article  Google Scholar 

  • Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813

    Article  PubMed  CAS  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347

    Article  PubMed  CAS  Google Scholar 

  • Fourcaud T, Zhang X, Stokes A, Lambers H, Körner C (2008) Plant growth modelling and applications: the increasing importance of plant architecture in growth models. Ann Bot 101:1053–1063

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedman JH, Meulman JJ (2003) Multiple additive regression trees with application in epidemiology. Stat Med 22:1365–1381

    Article  PubMed  Google Scholar 

  • Galipaud M, Gillingham MA, David M, Dechaume-Moncharmont FX (2014) Ecologists overestimate the importance of predictor variables in model averaging: a plea for cautious interpretations. Methods Ecol Evol 5:983–991

    Article  Google Scholar 

  • Goulet J, Messier C, Nikinmaa E (2000) Effect of branch position and light availability on shoot growth of understory sugar maple and yellow birch saplings. Can J Bot 78:1077–1085

    Google Scholar 

  • Gratzer G, Darabant A, Chhetri PB, Rai PB, Eckmüllner O (2004) Interspecific variation in the response of growth, crown morphology, and survivorship to light of six tree species in the conifer belt of the Bhutan Himalayas. Can J For Res 34:1093–1107

    Article  Google Scholar 

  • Gustafsson C, Boström C (2013) Influence of neighboring plants on shading stress resistance and recovery of eelgrass, Zostera marina L. PLoS One 8:e64064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han Q, Chiba Y (2009) Leaf photosynthetic responses and related nitrogen changes associated with crown reclosure after thinning in a young Chamaecyparis obtusa stand. J For Res 14:349–357

    Article  CAS  Google Scholar 

  • Harper J (1981) The concept of population in modular organisms. In: May RM (ed) Theoretical ecology: principles and applications. Blackwell Scientific Publications, Oxford, pp 53–77

    Google Scholar 

  • He W, Dong M (2003) Physiological acclimation and growth response to partial shading in Salix matsudana in the Mu Us Sandland in China. Trees 17:87–93

    Article  Google Scholar 

  • Henriksson J (2001) Differential shading of branches or whole trees: survival, growth, and reproduction. Oecologia 126:482–486

    Article  PubMed  Google Scholar 

  • Hikosaka K (2014) Optimal nitrogen distribution within a leaf canopy under direct and diffuse light. Plant Cell Environ 37:2077–2085

    Article  PubMed  CAS  Google Scholar 

  • Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659

    Article  CAS  Google Scholar 

  • Iio A, Fukasawa H, Nose Y, Naramoto M, Mizunaga H, Kakubari Y (2009) Within-branch heterogeneity of the light environment and leaf temperature in a Fagus crenata crown and its significance for photosynthesis calculations. Trees 23:1053–1064

    Article  Google Scholar 

  • Kawamura K (2010) A conceptual framework for the study of modular responses to local environmental heterogeneity within the plant crown and a review of related concepts. Ecol Res 25:733–744

    Article  Google Scholar 

  • Kayama M, Choi D, Sasa K, Satoh F, Nomura M, Koike T (2007) A trial for reforestation after forest fires with Sakhalin spruce in the northern most Japan. Eurasian J For Res 10:31–39

    Google Scholar 

  • Kojima S (1991) Classification and ecological characterization of coniferous forest phytogeocoenoses of Hokkaido, Japan. Plant Ecol 96:25–42

    Article  Google Scholar 

  • Lacointe A, Deleens E, Ameglio T, Saint-Joanis B, Lelarge C, Vandame M, Song G, Daudet F (2004) Testing the branch autonomy theory: a 13C/14C double-labelling experiment on differentially shaded branches. Plant Cell Environ 27:1159–1168

    Article  CAS  Google Scholar 

  • Larbi A, Vázquez S, El-Jendoubi H, Msallem M, Abadía J, Abadía A, Morales F (2015) Canopy light heterogeneity drives leaf anatomical, eco-physiological, and photosynthetic changes in olive trees grown in a high-density plantation. Photosynthesis Res 123:141–155

    Article  CAS  Google Scholar 

  • Lintunen A, Kaitaniemi P (2010) Responses of crown architecture in Betula pendula to competition are dependent on the species of neighbouring trees. Trees 24:411–424

    Article  Google Scholar 

  • Lintunen A, Sievänen R, Kaitaniemi P, Perttunen J (2011) Models of 3D crown structure for Scots pine (Pinus sylvestris) and silver birch (Betula pendula) grown in mixed forest. Can J For Res 41:1779–1794

    Article  Google Scholar 

  • Marty C, Lamaze T, Pornon A (2009) Endogenous sink-source interactions and soil nitrogen regulate leaf life-span in an evergreen shrub. New Phytol 183:1114–1123

    Article  PubMed  CAS  Google Scholar 

  • Millard P, Grelet G-a (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  PubMed  CAS  Google Scholar 

  • Niinemets U (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071

    Article  PubMed  CAS  Google Scholar 

  • Novoplansky A, Cohen D, Sachs T (1989) Ecological implications of correlative inhibition between plant shoots. Physiol Plant 77:136–140

    Article  Google Scholar 

  • Osada N, Okabe Y, Hayashi D, Katsuyama T, Tokuchi N (2014) Differences between height-and light-dependent changes in shoot traits in five deciduous tree species. Oecologia 174:1–12

    Article  PubMed  Google Scholar 

  • Pallardy SG (2010) Physiology of woody plants. Academic Press, New York

    Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Ridgeway G (2007) Generalized boosted models: a guide to the gbm package. http://cran.r-project.org/web/packages/gbm/vignettes/gbm.pdf

  • Royall RM (1997) Statistical evidence: a likelihood paradigm. Chapman and Hall, New York

    Google Scholar 

  • Sakai A, Okada S (1971) Freezing resistance of conifers. Silvae Genet 20:91–97

    Google Scholar 

  • Sprugel DG (2002) When branch autonomy fails: Milton’s Law of resource availability and allocation. Tree Physiol 22:1119–1124

    Article  PubMed  Google Scholar 

  • Sprugel D, Hinckley T, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334

    Article  Google Scholar 

  • Stoll P, Schmid B (1998) Plant foraging and dynamic competition between branches of Pinus sylvestris in contrasting light environments. J Ecol 86:934–945

    Article  Google Scholar 

  • Sugiura D, Tateno M (2013) Concentrative nitrogen allocation to sun-lit branches and the effects on whole-plant growth under heterogeneous light environments. Oecologia 172:949–960

    Article  PubMed  CAS  Google Scholar 

  • Sumida A (1993) Growth of tree species in a broadleaved secondary forest as related to the light environments of crowns. J Jpn For Soc 75:278–286

    Google Scholar 

  • Symonds MR, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21

    Article  Google Scholar 

  • Takenaka A (2000) Shoot growth responses to light microenvironment and correlative inhibition in tree seedlings under a forest canopy. Tree Physiol 20:987–991

    Article  PubMed  CAS  Google Scholar 

  • Tegeder M, Masclaux-Daubresse C (2017) Source and sink mechanisms of nitrogen transport and use. New Phytol. https://doi.org/10.1111/nph.14876

    Article  PubMed  Google Scholar 

  • Volpe G, Bianco RL, Rieger M (2008) Carbon autonomy of peach shoots determined by 13C-photoassimilate transport. Tree Physiol 28:1805–1812

    Article  PubMed  CAS  Google Scholar 

  • Williams H, Messier C, Kneeshaw DD (1999) Effects of light availability and sapling size on the growth and crown morphology of understory Douglas-fir and lodgepole pine. Can J For Res 29:222–231

    Article  Google Scholar 

  • Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25

    Google Scholar 

Download references

Acknowledgements

We thank the staff of the Sapporo Experimental Forest, Field Science Center for Northern Biosphere, Hokkaido University, for the use of their facilities. Lei Chen acknowledges the State Scholarship Fund provided by the China Scholarship Council, which supported his study in Japan. This work was supported in part by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant no. 24580209 and 16K14933). We thank Jennifer Smith, Ph.D., from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

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Correspondence to Lei Chen.

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Communicated by W. Bilger.

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Chen, L., Sumida, A. Effects of light on branch growth and death vary at different organization levels of branching units in Sakhalin spruce. Trees 32, 1123–1134 (2018). https://doi.org/10.1007/s00468-018-1700-5

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