Trade-off between shooting and leaf developing of woody species saplings in subtropical evergreen broad-leaved forests

doi:10.17521/cjpe.2020.0143

Abstract

Abstract:

Aims Own to their genetic characteristics and long-term adaptation to the understory environment, the saplings of subtropical evergreen broad-leaved forest woody species could shoot twigs and develop new leaves several times a year, in which how they survive in the habitats and ultimately grow to adult trees are vital. The objective of this study was to examine what specific adaptation strategies have woody plants taken in the face of environmental pressure in subtropical evergreen broad-leaved forests, especially the growth priorities of twig elongation, stem thickening and leaf area increasing during the shooting process.
Methods The study site is located in Qingcheng Mountain scenic area, Sichuan Province. We chose five species with high second shooting rate in similar habits. Five plants with no disease and insect pests of each species were randomly selected for tree height measurement and long-term shooting observation. Each plant was randomly labeled with three young current-year twigs from different direction outside of tree canopy, and the twig length, twig diameter, leaf number and area were recorded when the twigs burst. The scaling relationships between traits of twig and leaf were analyzed by standardized major axis estimation (SMA).
Important findings 1) The first and second shootings started from spring (April) and late summer (the late August) respectively. The proportion of the second shooting of trees was lower than that of shrubs, and the proportion of second shooting of evergreen plants was lower than that of deciduous counterparts respectively. 2) The twig length and individual leaf area, the twig diameter and leaf number (expect for the Symplocos grandis) of the first shooting were all higher than those of the second shooting, but the relative growth rate of individual area and leaf mass per area of the first shooting were lower than those of the second shooting. 3) The maximum relative growth rates of the twig length and leaf number, the twig diameter (expect for Eurya loquaiana and Castanopsis carlesii var. spinulosa) and total leaf area (expect for Castanopsis carlesii var. spinulosa) of the first shooting were all higher than those of the second shooting, and appeared in the first and second weeks of shooting. 4) In the two shootings, all the plants put priorities on the growth of leaf area and number, then on the growth of twig length, and finally on the twig diameter. The individual and total leaf area showed a significant allometric scaling relationship with the increasing of twig length and diameter, indicating that the growth rate of leaves was higher than that of twigs. The relationship between the individual leaf area and the leaf number was significantly greater than 1, suggesting that the growth rate of the individual leaf area was higher than that of the leaf number. Besides, the relationship between the twig length and diameter was also significantly greater than 1, suggesting that the growth rate of the twig length was higher than that of twig diameter. The study reveals the shooting strategies formed by plants improved their survival and reproductive ability by obtaining more resources (especially intercept the light resources).

Key words: shooting, second shooting, relative growth rate, allometry, trade-off, subtropical evergreen broad-leaved forest

MO Dan, WANG Zhen-Meng, ZUO You-Lu, XIANG Shuang. Trade-off between shooting and leaf developing of woody species saplings in subtropical evergreen broad-leaved forests[J]. Chin J Plant Ecol, 2020, 44(10): 995-1006.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0143

https://www.plant-ecology.com/EN/Y2020/V44/I10/995

Figures/Tables 7

References 52

[1]	Aanderud ZT, Bledsoe CS, Richards JH (2003). Contribution of relative growth rate to root foraging by annual and perennial grasses from California oak woodlands. Oecologia, 136, 424-430. DOI URL
[2]	Calle Z, Schlumpberger BO, Piedrahita L, Leftin A, Hammer SA, Tye A, Borchert R (2010). Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics. Trees, 24, 865-877.
[3]	Chabot BF, Hicks DJ (1982). The ecology of leaf life spans. Annual Review of Ecology and Systematics, 13, 229-259.
[4]	Chmielewski FM, Rötzer T (2001). Response of tree phenology to climate change across Europe. Agricultural and Forest Meteorology, 108, 101-112.
[5]	Conesa MÀ, Mus M, Galmés J (2019). Leaf size as a key determinant of contrasting growth patterns in closely related Limonium (Plumbaginaceae) species. Journal of Plant Physiology, 240, 152984. DOI: 10.1016/j.jplph.2019.05.011.
[6]	Corner EJH (1949). The durian theory or the origin of the modern tree. Annals of Botany, 13, 367-414.
[7]	Dale JE (1982). The Growth of Leaves. Edward Arnold Limited, London. 31-41.
[8]	Doi H, Gordo O, Katano I (2008). Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Climate Research, 36, 181-190.
[9]	Dombroskie SL, Aarssen LW (2012). The leaf size/number trade-off within species and within plants for woody angiosperms. Plant Ecology and Evolution, 145, 38-45.
[10]	Falster DS, Warton DI, Wright IJ (2006). User’s Guide to SMATR: Standardised Major Axis Tests & Routines Version 2.0. [2012-03-11]. http://www.bio.mq.edu.au/ecology/SMATR/.
[11]	Guo QX, Chai J, Qian F, Zhang TD, Liu WD, Tao JP (2013). Leaf and stem traits of current-year twigs vary with different functional types of woody plant. Chinese Journal of Ecology, 32, 1465-1470.
	[ 郭庆学, 柴捷, 钱凤, 张腾达, 刘文丹, 陶建平 (2013). 不同木本植物功能型当年生小枝功能性状差异. 生态学杂志, 32, 1465-1470.]
[12]	He WM, Zhong ZC (2000). Morphological and growth responses of the climbing plant, Gynostemma pentaphyllum seedlings to varying light intensity. Acta Phytoecologica Sinica, 24, 375-378.
	[ 何维明, 钟章成 (2000). 攀援植物绞股蓝幼苗对光照强度的形态和生长反应. 植物生态学报, 24, 375-378.]
[13]	Hutchings MJ, de Kroon H (1994). Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research, 25, 159-238.
[14]	Koriba K (1958). On the periodicity of the tree-growth in the tropics, with reference to the mode of branching, the leaf-fall, and the formation of the resting bud. Gardens Bulletin, 17, 11-81.
[15]	le Hir R, Leduc N, Jeannette E, Viemont JD, Pelleschi-Travier S (2006). Variations in sucrose and ABA concentrations are concomitant with heteroblastic leaf shape changes in a rhythmically growing species (Quercus robur). Tree Physiology, 26, 229-238.
[16]	Liu FJ, Xiang S, Yang XC, Sun SC (2010). Comparison of leaf mass per area, photosynthetic capacity and chemical defense traits of four evergreen broad-leaved tree species under contrasting light conditions. Chinese Journal of Applied and Environmental Biology, 16, 462-467.
	[ 柳凤娟, 向双, 阳小成, 孙书存 (2010). 两种光照生境下4种常绿阔叶树的单位叶面积干重、光合能力与化学防御物质含量比较. 应用与环境生物学报, 16, 462-467.]
[17]	Lohier T, Jabot F, Meziane D, Shipley B, Reich PB, Deffuant G (2014). Explaining ontogenetic shifts in root-shoot scaling with transient dynamics. Annals of Botany, 114, 513-524.
[18]	Long JY, Zhao YM, Kong XQ, Chen ZY, Wang XS, Zhao K, Cao R, Huang LS, Lü J, Cui Y, Yu YL, Xu CY (2018). Trade-offs between twig and leaf traits of ornamental shrubs grown in shade. Acta Ecologica Sinica, 38, 8022-8030.
	[ 龙嘉翼, 赵宇萌, 孔祥琦, 陈治羊, 王秀松, 赵凯, 曹然, 黄丽莎, 吕娇, 崔义, 余玉磊, 徐程扬 (2018). 观赏灌木小枝和叶性状在林下庇荫环境中的权衡关系. 生态学报, 38, 8022-8030.]
[19]	Lu E, Tsai C, Lin J, Yang S (2012). Leaf emergence, shedding, and lifespan of dominant hardwood species in Chitou, central Taiwan. Botanical Studies, 53, 255-264.
[20]	Ma DW, Zhang G, Wang YH, Wang DM (2002). Studies on species diversity of forest vegetation on Qingcheng Mountain. Journal of Sichuan University (Natural Science Edition), 39, 115-123.
	[ 马丹炜, 张果, 王跃华, 王道模 (2002). 青城山森林植被物种多样性的研究. 四川大学学报(自然科学版), 39, 115-123.]
[21]	Martinez KA, Fridley JD (2018). Acclimation of leaf traits in seasonal light environments: Are non-native species more plastic? Journal of Ecology, 106, 2019-2030.
[22]	Meng FQ, Zhang GF, Li XC, Niklas KJ, Sun SC (2015). Growth synchrony between leaves and stems during twig development differs among plant functional types of subtropical rainforest woody species. Tree Physiology, 35, 621-631.
[23]	Messier J, Lechowicz MJ, McGill BJ, Violle C, Enquist BJ (2017). Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network. Journal of Ecology, 105, 1775-1790.
[24]	Mizumachi E, Mori A, Osawa N, Akiyama R, Tokuchi N (2006). Shoot development and extension of Quercus serrata saplings in response to insect damage and nutrient conditions. Annals of Botany, 98, 219-226.
[25]	Moles AT, Westoby M (2000). Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos, 90, 517-524.
[26]	Nitta I, Ohsawa M (1997). Leaf dynamics and shoot phenology of eleven warm-temperate evergreen broad-leaved trees near their northern limit in central Japan. Plant Ecology, 130, 71-88.
[27]	Ozawa H, Itoh K, Hori Y (2000). Shoot structure and dynamics of saplings and canopies of three deciduous broad-leaved trees of a coppice forest in central Japan. Trees, 14, 206-214.
[28]	Pichon C, Hladik A, Hladik M, Tarnaud L, Roger E (2015). Leaf phenological patterns of trees, shrubs and lianas in a dry semi-deciduous forest of northwestern Madagascar: functional types and adaptive significance. Revue D Ecologie, 70, 197-212.
[29]	Pickup M, Westoby M, Basden A (2005). Dry mass costs of deploying leaf area in relation to leaf size. Functional Ecology, 19, 88-97.
[30]	Ralhan PK, Khanna RK, Singh SP, Singh JS (1985). Certain phenological characters of the shrub layer of Kumaun Himalayan forests. Vegetatio, 63, 113-119.
[31]	Rathcke B, Lacey EP (1985). Patterns of terrestrial plants. Annual Review of Ecology and Systematics, 16, 179-214.
[32]	Sultan SE (2000). Phenotypic plasticity for plant development, function and life history. Trends in Plant Science, 5, 537-542.
[33]	Shi P (2016). Proportion and Dynamic of the Second Shooting in Woody Species from Deciduous Broad-leaved Forest in Xianlin, Nanjing. Master degree dissertation, Nanjing Normal University, Nanjing
	[ 时盼 (2016). 南京仙林地区落叶阔叶林中木本植物二次抽枝的发生比例及动态研究. 硕士学位论文, 南京师范大学, 南京.]
[34]	Shi YC, Zhao CZ, Song QH, Du J, Chen J, Wang JW (2015). Slope-related variations in twig and leaf traits of Robinia pseudoacacia in the northern mountains of Lanzhou. Chinese Journal of Plant Ecology, 39, 362-370.
	[ 史元春, 赵成章, 宋清华, 杜晶, 陈静, 王继伟 (2015). 兰州北山刺槐枝叶性状的坡向差异性. 植物生态学报, 39, 362-370.]
[35]	Sun M, Tian K, Zhang Y, Wang H, Guan DX, Yue HT (2017). Research on leaf functional traits and their environmental adaptation. Plant Science Journal, 35, 940-949.
	[ 孙梅, 田昆, 张贇, 王行, 管东旭, 岳海涛 (2017). 植物叶片功能性状及其环境适应研究. 植物科学学报, 35, 940-949.]
[36]	Sun SC, Jin DM, Shi PL (2006). The leaf size-twig size spectrum of temperate woody species along an altitudinal gradient: an invariant allometric scaling relationship. Annals of Botany, 97, 97-107.
[37]	The Editorial Committee of Flora Reipubulicae Popularis Sinicae(1980). Flora Reipubulicae Popularis Sinicae. Science Press, Beijing.
	[ 中国科学院中国植物志编辑委员会(1980). 中国植物志. 科学出版社, 北京.]
[38]	Vitasse Y, Lenz A, Hoch G, Körner C (2014). Earlier leaf-out rather than difference in freezing resistance puts juvenile trees at greater risk of damage than adult trees. Journal of Ecology, 102, 981-988.
[39]	Volkenburgh EV (1999). Leaf expansion: an integrating plant behaviour. Plant, Cell & Environment, 22, 1463-1473.
[40]	Wang RX (2015). Leaf Population Dynamic of Main Plant Species from Deciduous Broad-leaved Forest in Xianlin, Nanjing.. Master degree dissertation, Nanjing Normal University, Nanjing.
	[ 王瑞雪 (2015). 南京仙林落叶阔叶林中主要植物的叶群体动态. 硕士学位论文, 南京师范大学, 南京.]
[41]	Wang ZM (2018). The Strategies of Woody Saplings Adapting to the Light and Temperature Environments in the Subtropical Evergreen Broad-leaved Forests. Master degree dissertation, Chengdu Institute of Biology, Chinese Academy of Science, Chengdu.
	[ 王振孟 (2018). 亚热带常绿阔叶林木本植物幼树阶段光温适应对策研究. 硕士学位论文, 中国科学院成都生物研究所, 成都.]
[42]	Warton DI, Weber NC (2002). Common slope tests for bivariate errors-in-variables models. Biometrical Journal, 44, 161-174.
[43]	Weed AS, Gassmann A, Casagrande RA (2011). Effects of leaf and root herbivory by potential insect biological control agents on the performance of invasive Vincetoxicum spp. Biological Control, 56, 50-58.
[44]	Westoby M, Wright IJ (2003). The leaf size-twig size spectrum and its relationship to other important spectra of variation among species. Oecologia, 135, 621-628.
[45]	Xia YJ, Tang JQ, Zhang GF, Huang C, Meng FQ, Sun SC (2013). First and second sets of shoots in five evergreen woody species from Tiantong National Forest Park of Zhejiang, China. Chinese Journal of Plant Ecology, 37, 220-229. DOI URL
	[ 夏洋洁, 唐坚强, 张光富, 黄超, 蒙凤群, 孙书存 (2013). 浙江天童国家森林公园5种常绿阔叶植物的一次和二次抽枝进程. 植物生态学报, 37, 220-229.]
[46]	Xiang S, Wu N, Sun SC (2009). Within-twig biomass allocation in subtropical evergreen broad-leaved species along an altitudinal gradient: allometric scaling analysis. Trees, 23, 637-647.
[47]	Xu GX, Luo SX, Guo QS, Pei SX, Shi ZM, Zhu L, Zhu NN (2014). Responses of leaf unfolding and flowering to climate change in 12 tropical evergreen broadleaf tree species in Jianfengling, Hainan Island. Chinese Journal of Plant Ecology, 38, 585-598.
	[ 许格希, 罗水兴, 郭泉水, 裴顺祥, 史作民, 朱莉, 朱妮妮 (2014). 海南岛尖峰岭12种热带常绿阔叶乔木展叶期与开花期对气候变化的响应. 植物生态学报, 38, 585-598.]
[48]	Yan ER, Wang XH, Chang SX, He FL (2013). Scaling relationships among twig size, leaf size and leafing intensity in a successional series of subtropical forests. Tree Physiology, 33, 609-617.
[49]	Yang F, Wang ZM, Zhu DH, Yang XC, Xiang S (2019). Dynamic characteristics of non-structural carbohydrates in leaves of six woody plants from an evergreen broad-leaved forest. Chinese Journal of Applied and Environmental Biology, 25, 1075-1083.
	[ 杨芳, 王振孟, 朱大海, 阳小成, 向双 (2019). 常绿阔叶林林下6种木本植物叶片非结构性碳水化合物的动态特征. 应用与环境生物学报, 25, 1075-1083.]
[50]	Zhu XB, Liu YM, Sun SC (2005). Leaf expansion of the dominant woody species of three deciduous oak forests in Nanjing, East China. Acta Phytoecologica Sinica, 29, 128-136.
	[ 朱旭斌, 刘娅梅, 孙书存 (2005). 南京地区落叶栎林主要木本植物的展叶动态研究. 植物生态学报, 29, 128-136.]
[51]	Zou ZL (1980). Insect Ecology. Shanghai Scientific & Technical Publishers. Shanghai.
	[ 邹钟琳 (1980). 昆虫生态学. 上海科学技术出版社, 上海.]
[52]	Zvereva EL, Kozlov MV (2006). Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta analysis. Global Change Biology, 12, 27-41.

生长型/生活型 Growth form/ Life form	个体数 Number of individual	物种数 Number of species	二次抽枝率 (%)(平均值±标准误差) Proportion of the second shooting (%)(mean ± SE)
乔木 Tree	198	43	20.97 ± 0.042^a
灌木 Shrub	210	44	47.72 ± 0.053^b
常绿 Evergreen	281	52	31.39 ± 0.044^a
落叶 Deciduous	127	35	37.39 ± 0.062^b

生长型/生活型 Growth form/ Life form	个体数 Number of individual	物种数 Number of species	二次抽枝率 (%)(平均值±标准误差) Proportion of the second shooting (%)(mean ± SE)
乔木 Tree	198	43	20.97 ± 0.042^a
灌木 Shrub	210	44	47.72 ± 0.053^b
常绿 Evergreen	281	52	31.39 ± 0.044^a
落叶 Deciduous	127	35	37.39 ± 0.062^b

y-x	抽枝批次 Batch of shooting	回归系数 Regression coefficient	p	分组斜率(置信区间) Group slope (CIs)	截距(置信区间) Intercept (CIs)	共同斜率(置信区间) Common slope (CIs)	p₀	截距 Intercept
单叶面积-小枝长 Individual leaf area-Twig length	I	0.741	<0.001	1.358 (1.172, 1.573)	-0.455 (-0.619, -0.291)	1.347 (1.198, 1.515)	0.855	-0.446^a
单叶面积-小枝长 Individual leaf area-Twig length	II	0.679	<0.001	1.327 (1.087, 1.620)	-0.309 (-0.545, -0.074)			-0.326^b
单叶面积-小枝直径 Individual leaf area-Twig diameter	I	0.447	<0.001	1.930 (1.558, 2.390)	-1.037 (-1.398, -0.676)	2.206 (1.942, 2.487)	0.136	-1.268^a
单叶面积-小枝直径 Individual leaf area-Twig diameter	II	0.826	<0.001	2.342 (2.021, 2.713)	-1.274 (-1.588, -0.960)			-1.151^b
单叶面积-叶片数 Individual leaf area-Leaf number	I	0.633	<0.001	1.334 (1.120, 1.589)	-0.426 (-0.618, -0.234)	1.570	0.001
单叶面积-叶片数 Individual leaf area-Leaf number	II	0.443	<0.001	2.317 (1.784, 3.010)	-1.361 (-1.947, -0.775)
小枝长-小枝直径 Twig length-Twig diameter	I	0.645	<0.001	1.421 (1.196, 1.688)	-0.429 (-0.642, -0.216)	1.554 (1.355, 1.778)	0.111	-0.540^a
小枝长-小枝直径 Twig length-Twig diameter	II	0.653	<0.001	1.764 (1.434, 2.170)	-0.727 (-1.061, -0.393)			-0.537^a
总叶面积-小枝长 Total leaf area-Stem length	I	0.720	<0.001	1.369 (1.175, 1.596)	-0.488 (-0.660, -0.315)	1.350 (1.205, 1.512)	0.794	-0.473^a
总叶面积-小枝长 Total leaf area-Stem length	II	0.761	<0.001	1.327 (1.117, 1.576)	-0.312 (-0.515, -0.109)			-0.332^b
总叶面积-小枝直径 Total leaf area-Twig diameter	I	0.427	<0.001	1.945 (1.565, 2.419)	-1.075 (-1.446, -0.704)	2.207 (1.937, 2.498)	0.168	-1.294^a

y-x	抽枝批次 Batch of shooting	回归系数 Regression coefficient	p	分组斜率(置信区间) Group slope (CIs)	截距(置信区间) Intercept (CIs)	共同斜率(置信区间) Common slope (CIs)	p₀	截距 Intercept
单叶面积-小枝长 Individual leaf area-Twig length	I	0.741	<0.001	1.358 (1.172, 1.573)	-0.455 (-0.619, -0.291)	1.347 (1.198, 1.515)	0.855	-0.446^a
单叶面积-小枝长 Individual leaf area-Twig length	II	0.679	<0.001	1.327 (1.087, 1.620)	-0.309 (-0.545, -0.074)			-0.326^b
单叶面积-小枝直径 Individual leaf area-Twig diameter	I	0.447	<0.001	1.930 (1.558, 2.390)	-1.037 (-1.398, -0.676)	2.206 (1.942, 2.487)	0.136	-1.268^a
单叶面积-小枝直径 Individual leaf area-Twig diameter	II	0.826	<0.001	2.342 (2.021, 2.713)	-1.274 (-1.588, -0.960)			-1.151^b
单叶面积-叶片数 Individual leaf area-Leaf number	I	0.633	<0.001	1.334 (1.120, 1.589)	-0.426 (-0.618, -0.234)	1.570	0.001
单叶面积-叶片数 Individual leaf area-Leaf number	II	0.443	<0.001	2.317 (1.784, 3.010)	-1.361 (-1.947, -0.775)
小枝长-小枝直径 Twig length-Twig diameter	I	0.645	<0.001	1.421 (1.196, 1.688)	-0.429 (-0.642, -0.216)	1.554 (1.355, 1.778)	0.111	-0.540^a
小枝长-小枝直径 Twig length-Twig diameter	II	0.653	<0.001	1.764 (1.434, 2.170)	-0.727 (-1.061, -0.393)			-0.537^a
总叶面积-小枝长 Total leaf area-Stem length	I	0.720	<0.001	1.369 (1.175, 1.596)	-0.488 (-0.660, -0.315)	1.350 (1.205, 1.512)	0.794	-0.473^a
总叶面积-小枝长 Total leaf area-Stem length	II	0.761	<0.001	1.327 (1.117, 1.576)	-0.312 (-0.515, -0.109)			-0.332^b
总叶面积-小枝直径 Total leaf area-Twig diameter	I	0.427	<0.001	1.945 (1.565, 2.419)	-1.075 (-1.446, -0.704)	2.207 (1.937, 2.498)	0.168	-1.294^a