Hydraulic architecture and safety margin in ten afforestation species in a lower subtropical region

doi:10.17521/cjpe.2021.0391

Abstract

Abstract:

Aims In the lower subtropical region of China, there are large areas of single-species plantations. These plantations have simple community structure and thus are sensitive to climate change. Under the background of regional climate drying, the eco-physiological strategies of these afforestation species and their response to seasonal drought should be investigated.

Methods We selected ten tree species that are commonly planted in this region including six native species and four exotic species. Based on measurements of the mean growth rate, hydraulic traits, and economics traits, we analyzed the trait-growth correlations within each species and compared the differences in hydraulic safety margin and stomatal safety margin among species.

Important findings (1) The growth rate was significantly and positively correlated with hydraulic conductivity, but not with the economic traits, such as wood density, specific leaf area, and hydraulic safety-related traits. (2) There was no significant trade-off between hydraulic efficiency and safety. Two of the exotic tree species, Acacia crassicarpa and Eucalyptus grandis × urophylla, showed both high hydraulic conductivity and great cavitation resistance. (3) There were significant differences in hydraulic safety margin and stomatal safety margin among the tested species. During the dry season, Acacia auriculiformis, Castanopsis hystrix, Mytilaria laosensis and Cinnamomum burmannii would suffer from higher risks of hydraulic failure than the other species. We suggest that tree hydraulic traits should be included into the index system of ecological monitoring of subtropical plantations, which can provide important references for sustainable management of these plantations.

Key words: hydraulic conductivity, cavitation resistance, growth rate, hydraulic safety, plantation management

HUANG Dong-Liu, XIANG Wei, LI Zhong-Guo, ZHU Shi-Dan. Hydraulic architecture and safety margin in ten afforestation species in a lower subtropical region[J]. Chin J Plant Ecol, 2022, 46(5): 602-612.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0391

https://www.plant-ecology.com/EN/Y2022/V46/I5/602

Figures/Tables 5

Table 1 Basic information of the ten afforestation tree species in a lower subtropical region, China

物种 Species	科 Family	缩写 Abbreviation	符号 Symbol	林龄 Stand age (a)	DGR (cm·a^-1)	HGR (m·a^-1)	MVL (cm)
大叶相思 Acacia auriculiformis	豆科 Leguminosae	Aa	◆	16	1.02	2.13	124
厚荚相思 Acacia crassicarpa	豆科 Leguminosae	Ac	■	19	1.12	0.85	136
马占相思 Acacia mangium	豆科 Leguminosae	Am	●	17	0.86	1.37	120
阴香 Cinnamomum burmannii	樟科 Lauraceae	Cb	○	30	0.50	0.44	68
红锥 Castanopsis hystrix	壳斗科 Fagaceae	Ch	◇	31	0.53	0.45	142
杉木 Cunninghamia lanceolata	杉科 Taxodiaceae	Cl	⊕	35	0.53	0.51	20
桉树 Eucalyptus grandis × urophylla	桃金娘科 Myrtaceae	Eg	▲	8	1.97	2.85	307
壳菜果 Mytilaria laosensis	金缕梅科 Hamamelidaceae	Ml	▽	33	0.60	0.58	85
马尾松 Pinus massoniana	松科 Pinaceae	Pm	△	31	0.63	0.94	56
木荷 Schima superba	山茶科 Theaceae	Ss	□	30	0.72	0.65	54

Fig. 1 Principal component analysis of 12 traits for the ten afforestation species in a lower subtropical region, China. Species symbols are shown in Table 1. Ψmidday, midday leaf water potential; Ψtlp, leaf turgor loss point; Dh, hydraulically-weighted vessel (or tracheid) diameter; HSM50, hydraulic safety margin; HSMtlp, stomatal safety margin; HV, Huber value; kl, leaf specific hydraulic conductivity; ks, sapwood specific hydraulic conductivity; P50, cavitation resistance; SLA, specific leaf area; VD, vessel (or tracheid) density; WD, wood density.

Fig. 2 Relationship between growth rate and hydraulic conductivity across ten afforestation species in a lower subtropical region, China. Species symbols are shown in Table 1. All, all the tree species; Exotic, exotic tree species; Native, native tree species. DGR, diameter at breast height growth rate; HGR, height growth rate; kl, leaf specific hydraulic conductivity; ks, sapwood specific hydraulic conductivity.The error bars are standard errors. ns, p > 0.05; *, p < 0.05.

Fig. 3 Relationship between cavitation resistance and sapwood specific hydraulic conductivity (ks) across ten afforestation species in a lower subtropical region, China. P50, the xylem water potential causing 50% loss of hydraulic conductivity. All, all tree species; Exotic, exotic tree species; Native, native tree species. The species symbols are shown in Table 1. ns, p > 0.05.

Fig. 4 Inter-specific comparison of hydraulic safety margin (HSM50)(A) and stomatal safety margin (HSMtlp)(B), and their relationship (C) across ten afforestation species in a low subtropical region, China. Species abbreviations and symbols are shown in Table 1. The white and black bars indicate the native and exotic tree species, respectively. The error bars are standard errors. Different lowercase letters indicate significant difference (p < 0.05).

References 61

[1]	Allen CD, Breshears DD, McDowell NG (2015). On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere, 6, 1-55.
[2]	Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016). Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought- induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America, 113, 5024-5029. DOI PMID
[3]	Aritsara ANA, Razakandraibe VM, Ramananantoandro T, Gleason SM, Cao KF (2021). Increasing axial parenchyma fraction in the Malagasy Magnoliids facilitated the co-optimisation of hydraulic efficiency and safety. New Phytologist, 229, 1467-1480. DOI URL
[4]	Barotto AJ, Fernandez ME, Gyenge J, Meyra A, Martinez- Meier A, Monteoliva S (2016). First insights into the functional role of vasicentric tracheids and parenchyma in Eucalyptus species with solitary vessels: Do they contribute to xylem efficiency or safety? Tree Physiology, 36, 1485-1497. DOI URL
[5]	Brodribb TJ, Cochard H (2009). Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology, 149, 575-584. DOI PMID
[6]	Cai XA, Peng SP, Zhao P, Liu H, Rao XQ (2005). Ecophysiological characteristics of three native species used in two forest reconstructing models. Chinese Journal of Ecology, 24, 243-250.
	[ 蔡锡安, 彭少麟, 赵平, 刘惠, 饶兴权 (2005). 三种乡土树种在二种林分改造模式下的生理生态比较. 生态学杂志, 24, 243-250.]
[7]	Cao XG, Hu HB, Li YJ, Dong ZP, Lu XR, Bai MW, Zheng ZP, Fang KY (2021). Differences in the ecological resilience of planted and natural Pinus massoniana and Cunninghamia lanceolata forests in response to drought in subtropical China. Chinese Journal of Applied Ecology, 32, 3531- 3538.
	[ 曹新光, 胡红兵, 李颖俊, 董志鹏, 卢晓蓉, 白毛伟, 郑壮鹏, 方克艳 (2021). 亚热带人工和天然马尾松、杉木林生长对干旱的生态弹性差异. 应用生态学报, 32, 3531-3538.]
[8]	Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018). Triggers of tree mortality under drought. Nature, 558, 531-539. DOI URL
[9]	Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, et al. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752-755. DOI URL
[10]	Dixon P (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14, 927- 930. DOI URL
[11]	Duan HL, Li YY, Xu Y, Zhou SX, Liu J, Tissue DT, Liu JX (2019). Contrasting drought sensitivity and post-drought resilience among three co-occurring tree species in subtropical China. Agricultural and Forest Meteorology, 272- 273, 55-68.
[12]	Duursma R, Choat B (2017). Fitplc—An R package to fit hydraulic vulnerability curves. Journal of Plant Hydraulics, 4, e002. DOI: 10.20870/jph.2017.e002. DOI URL
[13]	Fan ZX, Zhang SB, Hao GY, Ferry Slik JW, Cao KF (2012). Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. Journal of Ecology, 100, 732-741. DOI URL
[14]	Gao JG, Zhao P, Shen WJ, Niu JF, Zhu LW, Ni GY (2015). Biophysical limits to responses of water flux to vapor pressure deficit in seven tree species with contrasting land use regimes. Agricultural and Forest Meteorology, 200, 258-269. DOI URL
[15]	He PC, Gleason SM, Wright IJ, Weng ES, Liu H, Zhu SD, Lu MZ, Luo Q, Li RH, Wu GL, Yan ER, Song YJ, Mi XC, Hao GY, Reich PB, et al. (2020). Growing-season temperature and precipitation are independent drivers of global variation in xylem hydraulic conductivity. Global Change Biology, 26, 1833-1841. DOI URL
[16]	Hu XY, Duan AG, Zhang JG, Du HL, Zhang XQ, Guo WF, Sun JJ (2020). Stoichiometry of carbon, nitrogen, and phosphorus of Chinese fir plantations in Daqing Mountain, Guangxi. Acta Ecologica Sinica, 40, 1207-1218.
	[ 胡小燕, 段爱国, 张建国, 杜海伦, 张雄清, 郭文福, 孙建军 (2020). 广西大青山杉木人工林碳氮磷生态化学计量特征. 生态学报, 40, 1207-1218.]
[17]	Johnson KM, Brodersen C, Carins-Murphy MR, Choat B, Brodribb TJ (2020). Xylem embolism spreads by single- conduit events in three dry forest angiosperm stems. Plant Physiology, 184, 212-222. DOI PMID
[18]	Kiorapostolou N, da Sois L, Petruzzellis F, Savi T, Trifilò P, Nardini A, Petit G (2019). Vulnerability to xylem embolism correlates to wood parenchyma fraction in angiosperms but not in gymnosperms. Tree Physiology, 39, 1675-1684. DOI PMID
[19]	King DA, Davies SJ, Tan S, Noor NM (2006). The role of wood density and stem support costs in the growth and mortality of tropical trees: tree demography and stem support costs. Journal of Ecology, 94, 670-680. DOI URL
[20]	Liu H, Ye Q, Gleason SM, He PC, Yin DY (2021). Weak tradeoff between xylem hydraulic efficiency and safety: climatic seasonality matters. New Phytologist, 229, 1440- 1452. DOI URL
[21]	Liu SR, Yang YJ, Wang H (2018). Development strategy and management countermeasures of planted forests in China: transforming from timber-centered single objective management towards multi-purpose management for enhancing quality and benefits of ecosystem services. Acta Ecologica Sinica, 38, 1-10. DOI URL
	[ 刘世荣, 杨予静, 王晖 (2018). 中国人工林经营发展战略与对策: 从追求木材产量的单一目标经营转向提升生态系统服务质量和效益的多目标经营. 生态学报, 38, 1-10.]
[22]	Luo JX, Zang RG, Li CY (2006). Physiological and morphological variations of Picea asperata populations originating from different altitudes in the mountains of southwestern China. Forest Ecology and Management, 221, 285- 290. DOI URL
[23]	Manzoni S, Vico G, Katul G, Palmroth S, Jackson RB, Porporato A (2013). Hydraulic limits on maximum plant transpiration and the emergence of the safety-efficiency trade- off. New Phytologist, 198, 169-178. DOI URL
[24]	Martin-StPaul N, Delzon S, Cochard H (2017). Plant resistance to drought depends on timely stomatal closure. Ecology Letters, 20, 1437-1447. DOI PMID
[25]	McDowell N, Allen CD, Anderson-Teixeira K, Brando P, Brienen R, Chambers J, Christoffersen B, Davies S, Doughty C, Duque A, Espirito-Santo F, Fisher R, Fontes CG, Galbraith D, Goodsman D, et al. (2018). Drivers and mechanisms of tree mortality in moist tropical forests. New Phytologist, 219, 851-869. DOI PMID
[26]	McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008). Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist, 178, 719-739. DOI PMID
[27]	Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009). Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology, 23, 922-930. DOI URL
[28]	Nolan RH, Gauthey A, Losso A, Medlyn BE, Smith R, Chhajed SS, Fuller K, Song M, Li XE, Beaumont LJ, Boer MM, Wright IJ, Choat B (2021). Hydraulic failure and tree size linked with canopy die-back in eucalypt forest during extreme drought. New Phytologist, 230, 1354-1365. DOI URL
[29]	Novriyanti E, Watanabe M, Makoto K, Takeda T, Hashidoko Y, Koike T (2012). Photosynthetic nitrogen and water use efficiency of acacia and eucalypt seedlings as afforestation species. Photosynthetica, 50, 273-281. DOI URL
[30]	Oliveira RS, Eller CB, de V Barros F, Hirota M, Brum M, Bittencourt P (2021). Linking plant hydraulics and the fast-slow continuum to understand resilience to drought in tropical ecosystems. New Phytologist, 230, 904-923. DOI PMID
[31]	Peng SL (2003). Research and Practice of Tropical and Subtropical Restoration Ecology. Science Press, Beijing.
	[ 彭少麟 (2003). 热带亚热带恢复生态学研究与实践. 科学出版社, 北京.]
[32]	Pereira L, Miranda MT, Pires GS, Pacheco VS, Guan XY, Kaack L, Karimi Z, Machado EC, Jansen S, Tyree MT, Ribeiro RV (2020). A semi-automated method for measuring xylem vessel length distribution. Theoretical and Experimental Plant Physiology, 32, 331-340. DOI URL
[33]	Poorter L, McDonald I, Alarcón A, Fichtler E, Licona JC, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010). The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytologist, 185, 481-492. DOI URL
[34]	Qi JH, Fan ZX, Fu PL, Zhang YJ, Sterck F (2021). Differential determinants of growth rates in subtropical evergreen and deciduous juvenile trees: carbon gain, hydraulics and nutrient-use efficiencies. Tree Physiology, 41, 12-23. DOI URL
[35]	Qin XH, Liang Y, Chen CF, Qin L (2021). Effects of different tree species plantations on soil bacterial community diversity in south subtropical China. Forest Research, 34(4), 120-127.
	[ 覃鑫浩, 梁艳, 陈超凡, 覃林 (2021). 南亚热带不同树种人工林对土壤细菌群落多样性的影响. 林业科学研究, 34(4), 120-127.]
[36]	Russo SE, Jenkins KL, Wiser SK, Uriarte M, Duncan RP, Coomes DA (2010). Interspecific relationships among growth, mortality and xylem traits of woody species from New Zealand. Functional Ecology, 24, 253-262. DOI URL
[37]	Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003). The “hydrology” of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment, 26, 1343-1356.
[38]	Santiago LS, de Guzman ME, Baraloto C, Vogenberg JE, Brodie M, Hérault B, Fortunel C, Bonal D (2018). Coordination and trade-offs among hydraulic safety, efficiency and drought avoidance traits in Amazonian rainforest canopy tree species. New Phytologist, 218, 1015-1024. DOI PMID
[39]	Santini NS, Cleverly J, Faux R, Lestrange C, Rumman R, Eamus D (2016). Xylem traits and water-use efficiency of woody species co-occurring in the Ti Tree Basin arid zone. Trees, 30, 295-303. DOI URL
[40]	Scoffoni C, Sack L (2017). The causes and consequences of leaf hydraulic decline with dehydration. Journal of Experimental Botany, 68, 4479-4496. DOI URL
[41]	Skelton RP, West AG, Dawson TE (2015). Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proceedings of the National Academy of Sciences of the United States of America, 112, 5744-5749. DOI PMID
[42]	Song HQ, Ni MY, Zhu SD (2020). Hydraulic and photosynthetic characteristics differ between co-generic tree and liana species: a case study of Millettia and Gnetum in tropical forest. Chinese Journal of Plant Ecology, 44, 192-204. DOI URL
	[ 宋慧清, 倪鸣源, 朱师丹 (2020). 乔木与木质藤本的水力与光合性状的差异: 以热带森林崖豆藤属和买麻藤属为例. 植物生态学报, 44, 192-204.] DOI
[43]	Sperry JS, Hacke UG, Wheeler JK (2005). Comparative analysis of end wall resistivity in xylem conduits. Plant, Cell & Environment, 28, 456-465.
[44]	Sun GC, Zhao P, Zeng XP, Cai XA (2009). Hydraulic responses of stomatal conductance in leaves of successional tree species in subtropical forest to environmental moisture. Acta Ecologica Sinica, 29, 698-705.
	[ 孙谷畴, 赵平, 曾小平, 蔡锡安 (2009). 亚热带森林演替树种叶片气孔导度对环境水分的水力响应. 生态学报, 29, 698-705.]
[45]	Sun ZW, Zhao P, Niu JF, Ni GY, Zhu LW, Gao JG, Zhao XH, Zhang ZZ, Zhou J (2014). Seasonal variations of sap flow and transpiration water consumption of introduced tree species Acacia auriculaeformis and Eucalyptus citriodora. Chinese Journal of Ecology, 33, 2588-2595.
	[ 孙振伟, 赵平, 牛俊峰, 倪广艳, 朱丽薇, 高建国, 赵秀华, 张振振, 周娟 (2014). 外来引种树种大叶相思和柠檬桉树干液流和蒸腾耗水的季节变异. 生态学杂志, 33, 2588- 2595.]
[46]	Tan FS, Song HQ, Fu PL, Chen YJ, Siddiq Z, Cao KF, Zhu SD (2020). Hydraulic safety margins of co-occurring woody plants in a tropical karst forest experiencing frequent extreme droughts. Agricultural and Forest Meteorology, 292-293, 108107. DOI: 10.1016/j.agrformet.2020.108107. DOI
[47]	Wang FM, Zhu WX, Zou B, Neher DA, Fu SL, Xia HP, Li ZA (2013). Seedling growth and soil nutrient availability in exotic and native tree species: implications for afforestation in Southern China. Plant and Soil, 364, 207-218. DOI URL
[48]	Wang H, Liu SR, Mo JM, Wang JX, Makeschin F, Wolff M (2010). Soil organic carbon stock and chemical composition in four plantations of indigenous tree species in subtropical China. Ecological Research, 25, 1071-1079. DOI URL
[49]	Wen YG, Zhang ZF, Zhou XG, Zhu HG, Wang L, Cai DX, Jia HY, Ming AG, Lu LH (2020). Effects of mixing precious indigenous tree species and Eucalyptus on ecosystem biomass and carbon stocks. Guangxi Sciences, 27, 111-119.
	[ 温远光, 张祖峰, 周晓果, 朱宏光, 王磊, 蔡道雄, 贾宏炎, 明安刚, 卢立华 (2020). 珍贵乡土树种与桉树混交对生态系统生物量和碳储量的影响. 广西科学, 27, 111-119.]
[50]	Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013). Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment, 36, 1938-1949.
[51]	Xu GL, Zhou GY, Mo JM, Zhou XY, Peng SJ (2005). The responses of soil fauna composition to forest restoration in Heshan. Acta Ecologica Sinica, 25, 1670-1677.
	[ 徐国良, 周国逸, 莫江明, 周小勇, 彭闪江 (2005). 鹤山丘陵退化生态系统植被恢复的土壤动物群落结构. 生态学报, 25, 1670-1677.]
[52]	Zach A, Schuldt B, Brix S, Horna V, Culmsee H, Leuschner C (2010). Vessel diameter and xylem hydraulic conductivity increase with tree height in tropical rainforest trees in Sulawesi, Indonesia. Flora, 205, 506-512. DOI URL
[53]	Zhang JL, Cao KF (2009). Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Functional Ecology, 23, 658-667. DOI URL
[54]	Zhang QW, Zhu SD, Jansen S, Cao KF (2021a). Topography strongly affects drought stress and xylem embolism resistance in woody plants from a karst forest in Southwest China. Functional Ecology, 35, 566-577. DOI URL
[55]	Zhang T, Liang XY, Ye Q, BassiriRad H, Liu H, He PC, Wu GL, Lu XK, Mo JM, Cai XA, Rao XQ, Yan JH, Fu SL (2021b). Leaf hydraulic acclimation to nitrogen addition of two dominant tree species in a subtropical forest. Science of the Total Environment, 771, 145415. DOI: 10.1016/j.scitotenv.2021.145415. DOI URL
[56]	Zhao P, Rao XQ, Ma L, Cai XA, Zeng XP (2006). Sap flow-scaled stand transpiration and canopy stomatal conductance in an acacia mangium forest. Journal of Plant Ecology (Chinese Version), 30, 655-665.
	[ 赵平, 饶兴权, 马玲, 蔡锡安, 曾小平 (2006). 基于树干液流测定值进行尺度扩展的马占相思林段蒸腾和冠层气孔导度. 植物生态学报, 30, 655-665.] DOI
[57]	Zhao P, Zeng XP, Peng SL (2003). Ecological adaptation of leaf gas exchange of trees used for re-vegetation under different experimental light regimes. Chinese Journal of Ecology, 22, 1-8.
	[ 赵平, 曾小平, 彭少麟 (2003). 植被恢复树种在不同实验光环境下叶片气体交换的生态适应特点. 生态学杂志, 22, 1-8.]
[58]	Zhao PQ, Zhao P, Niu JF, Zhu LW, Ni GY, Gao JG, Zhang ZZ (2014). Relationship between vessel characteristics and sap flow of eight subtropical tree species. Journal of Tropical and Subtropical Botany, 22, 537-548.
	[ 赵培强, 赵平, 牛俊峰, 朱丽薇, 倪广艳, 高建国, 张振振 (2014). 华南地区常见树种导管特征与树干液流的关系. 热带亚热带植物学报, 22, 537-548.]
[59]	Zhou GY, Houlton BZ, Wang WT, Huang WJ, Xiao Y, Zhang QM, Liu SZ, Cao M, Wang XH, Wang SL, Zhang YP, Yan JH, Liu JX, Tang XL, Zhang DQ (2014). Substantial reorganization of China’s tropical and subtropical forests: based on the permanent plots. Global Change Biology, 20, 240-250. DOI URL
[60]	Zhou LL, Li SB, Pan H, Wang WP, Wu YL, Zheng RP (2021). Characteristics of soil nutrient and enzyme activities in plantations of Eucalyptus urophylla × E. grandis and five Acacia species. Journal of Tropical and Subtropical Botany, 29, 483-493.
	[ 周丽丽, 李树斌, 潘辉, 王万萍, 吴亚岚, 郑茹萍 (2021). 5种相思树和尾巨桉人工林土壤养分和酶活性特征. 热带亚热带植物学报, 29, 483-493.]
[61]	Zhu SD, Li RH, He PC, Siddiq Z, Cao KF, Ye Q (2019). Large branch and leaf hydraulic safety margins in subtropical evergreen broadleaved forest. Tree Physiology, 39, 1405- 1415. DOI URL