Difference in adaptation strategy between Haloxylon ammodendron and Alhagi sparsifolia to drought

doi:10.17521/cjpe.2021.0338

Abstract

Abstract:

Aims The plant mortality induced by drought has significant impact on forest ecosystems around the world. It thus has brought intensive research attention on the plant adaptive strategy to drought in the field of physiological ecology. This study aims to investigate the differences in adaptation strategies to drought between two dominant species in arid desert areas, i.e., Haloxylon ammodendron and Alhagi sparsifolia.

Methods Three types of functional traits (i.e., leaf, photosynthetic and hydraulic traits) of A. sparsifolia and H. ammodendron were measured in response to a natural drought gradient (mild, moderate and severe) in Ebinur Lake Nature Reserve in Xinjiang, China. The changes of functional traits with drought gradient, and the differences of functional traits and adaptation strategies to drought between the two species were analyzed.

Important findings The functional traits of A. sparsifolia and H. ammodendron changed differently across drought gradient. All the functional traits were significantly different between the two species except for leaf dry matter content. However, the differences in functional traits between the two species showed a decrease due to the synergetic influence of drought stress and species convergence. Pearson correlation among the traits for the two species indicated that only 10 pairs of functional traits are significantly correlated for A. sparsifolia, while 15 pairs were significantly correlated for H. ammodendron. Principal component analysis (PCA) showed that two typical trait combinations related to drought resistance can be obtained from 11 functional traits of H. ammodendron, namely drought resistance-carbon acquisition group and drought resistance group. However, the trait combinations in coping with drought were not identified for A. sparsifolia. The results suggested that A. sparsifolia,was a conservative species, having greater drought tolerance than H. ammodendron. The traits in A. sparsifolia was less associated than that in H. ammodendron. In contrast, H. ammodendron used the trade-offs and compensatory relationships among functional traits to reduce drought stress. This study provided insights into the relationship between functional traits and drought adaptation strategies of different plant life forms, which advanced the fundamental theories of plant physiological ecology, and provided implications and references for the protection and diversity maintenance of desert ecosystem.

Key words: leaf functional trait, photosynthetic parameter, hydraulic trait, drought stress, trait combination

ZHOU Jie, YANG Xiao-Dong, WANG Ya-Yun, LONG Yan-Xin, WANG Yan, LI Bo-Rui, SUN Qi-Xing, SUN Nan. Difference in adaptation strategy between Haloxylon ammodendron and Alhagi sparsifolia to drought[J]. Chin J Plant Ecol, 2022, 46(9): 1064-1076.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0338

https://www.plant-ecology.com/EN/Y2022/V46/I9/1064

Figures/Tables 8

Fig. 1 Sample sites in study region of Ebinur Lake Basin. D1, D2, and D3 represent sampling plots with mild, moderate, and severe drought.

Table 1 Division of drought gradient of Ebinur Lake Basin (mean ± SD)

编号 Number	土壤含水量 Soil water content (%)	干旱程度 Drought level
D1	12.74 ± 1.25	轻度 Mild
D2	9.38 ± 0.80	中度 Moderate
D3	3.63 ± 0.66	重度 Severe

Fig. 2 Variance of leaf traits across the drought levels and between Alhagi sparsifolia (As) and Haloxylon ammodendron (Ha) (mean ± SD). D1, D2 and D3 are mild, moderate and severe drought, respectively. Uppercase letters are the result of one-way AVOVA, different letters show significant difference under different drought levels of same species (p < 0.05). Lowercase letters are the result of independent sample t test, different letters show significant difference between species under same drought level (p < 0.05).

Fig. 3 Variance of photosynthetic traits across the drought levels and between Alhagi sparsifolia (As) and Haloxylon ammodendron (Ha)(mean ± SD). D1, D2 and D3 are mild, moderate and severe drought, respectively. Uppercase letters are the result of one-way AVOVA, different letters show significant difference under different drought levels of same species (p < 0.05). Lowercase letters are the result of independent sample t test, different letters show significant difference between species under same drought level (p < 0.05).

Fig. 4 Variance of hydraulic traits across the drought levels and between Alhagi sparsifolia (As) and Haloxylon ammodendron (Ha)(mean ± SD). D1, D2 and D3 are mild, moderate and severe drought, respectively. Uppercase letters are the result of one-way AVOVA, different letters show significant difference under different drought levels of same species (p < 0.05). Lowercase letters are the result of independent sample t test, different letters show significant difference between species under same drought level (p < 0.05).

Table 2 Collaborative influences of drought level and species on functional traits of Alhagi sparsifolia and Haloxylon ammodendron tested using two-way ANOVA

功能性状 Functional trait		干旱程度×物种 Drought level × species
功能性状 Functional trait		F	p
叶性状 Leaf trait	叶厚或嫩枝叶直径 Leaf thickness or shoot diameter	0.43	0.81
	叶面积 Leaf area	0.30	0.75
	比叶面积 Specific leaf area	8.91	<0.01
	干物质含量 Dry matter content	1.22	0.54
光合性状 Photosynthetic trait	净光合速率 Net photosynthetic rate	0.85	0.66
	气孔导度 Stomatal conductance	1.89	0.39
	蒸腾速率 Transpiration rate	0.01	0.99
	水分利用效率 Water use efficiency	14.28	<0.01
水力性状 Hydraulic trait	叶水势 Leaf water potential	6.46	<0.05
	枝水势 Twig water potential	5.23	<0.05
	枝比导率 Twig specific hydraulic conductance	2.11	0.17

Fig. 5 Correlation among functional traits of Alhagi sparsifolia (As) and Haloxylon ammodendron (Ha). Cond, stomatal conductance; Ks, twig specific hydraulic conductance; LA, leaf area; LD, leaf diameter; LDMC, leaf dry matter content; LP, leaf water potential; LT, leaf thickness; Pn, net photosynthetic rate; SLA, specific leaf area; TP, twig water potential; Tr, transpiration rate; WUE, water use efficiency.

Fig. 6 Principal component (PC) analysis of 11 functional traits of Alhagi sparsifolia (A) and Haloxylon ammodendron (B) under drought stress. Cond, stomatal conductance; Ks, twig specific hydraulic conductance; LA, leaf area; LD, leaf diameter; LDMC, leaf dry matter content; LP, leaf water potential; LT, leaf thickness; Pn, net photosynthetic rate; SLA, specific leaf area; TP, twig water potential; Tr, transpiration rate; WUE, water use efficiency.

References 51

[1]	Anderegg WRL, Anderegg LDL (2013). Hydraulic and carbohydrate changes in experimental drought-induced mortality of saplings in two conifer species. Tree Physiology, 33, 252-260. DOI PMID
[2]	Bai XF, Zhu JJ, Wang ZL, Tan YQ, Liu LD (2012). Relationship between the salt accumulation and the drought resistance in several woody plants in arid zone. Scientia Silvae Sinicae, 48(7), 45-49.
	[柏新富, 朱建军, 王仲礼, 谭永芹, 刘林德 (2012). 干旱区木本植物盐分积累与其耐旱性的关系. 林业科学, 48(7), 45-49.]
[3]	Bouche PS, Larter M, Domec JC, Burlett R, Gasson P, Jansen S, Delzon S (2014). A broad survey of hydraulic and mechanical safety in the xylem of conifers. Journal of Experimental Botany, 65, 4419-4431. DOI PMID
[4]	Cai HX, Wu FZ, Yang WQ (2011). Effects of drought stress on the photosynthesis of Salix paraqplesia and Hippophae rhamnoides seedlings. Acta Ecologica Sinica, 31, 2430-2436.
	[蔡海霞, 吴福忠, 杨万勤 (2011). 干旱胁迫对高山柳和沙棘幼苗光合生理特征的影响. 生态学报, 31, 2430-2436.]
[5]	Chen YP, Zhou HH, Zhu CG (2021). A review of water transport processes of Populus euphratica in the lower reaches of Tarim River. Arid Land Geography, 44, 612-619.
	[陈亚鹏, 周洪华, 朱成刚 (2021). 塔里木河下游胡杨水分传输过程研究综述. 干旱区地理, 44, 612-619.]
[6]	Choat B (2013). Predicting thresholds of drought-induced mortality in woody plant species. Tree Physiology, 33, 669-671. DOI PMID
[7]	Dai AG (2011). Drought under global warming: a review. Wiley Interdisciplinary Reviews: Climate Change, 2, 45-65. DOI URL
[8]	Dai YX, Wang L, Wang XC (2015). Progress on researches of drought-induced tree mortality mechanisms. Chinese Journal of Ecology, 34, 3228-3236.
	[代永欣, 王林, 万贤崇 (2015). 干旱导致树木死亡机制研究进展. 生态学杂志, 34, 3228-3236.]
[9]	DeSoto L, Cailleret M, Sterck F, Jansen S, Kramer K, Robert EMR, Aakala T, Amoroso MM, Bigler C, Camarero JJ, Čufar K, Gea-Izquierdo G, Gillner S, Haavik LJ, Hereş AM, et al. (2020). Low growth resilience to drought is related to future mortality risk in trees. Nature Communications, 11, 545. DOI: 10.1038/s41467-020-14300-5. DOI
[10]	Feng QH, Shi ZM, Dong LL, Liu SR (2010). Relationships among functional traits of Quercus species and their response to meteorological factors in the temperate zone of the North-South Transect of Eastern China. Chinese Journal of Plant Ecology, 34, 619-627.
	[冯秋红, 史作民, 董莉莉, 刘世荣 (2010). 南北样带温带区栎属树种功能性状间的关系及其对气象因子的响应. 植物生态学报, 34, 619-627.] DOI
[11]	Fu GQ, Xu XY, Xu MS, Meng YY, Zhao P, Liu J (2016). A study of fractal properties of spatial distribution of Reaumuria soongorica population and its influencing factors in Minqin Oasis fringe. Acta Ecologica Sinica, 36, 5768-5776.
	[付贵全, 徐先英, 徐梦莎, 孟源源, 赵鹏, 刘江 (2016). 民勤绿洲边缘2种生境红砂种群分形特征及影响因素. 生态学报, 36, 5768-5776.]
[12]	Galle A, Esper J, Feller U, Ribas-Carbo M, Fonti P (2010). Responses of wood anatomy and carbon isotope composition of Quercus pubescens saplings subjected to two consecutive years of summer drought. Annals of Forest Science, 67, 809. DOI: 10.1051/forest/2010045. DOI
[13]	Gong XW, Lü GH (2017). Species diversity and dominant species’ niches of eremophyte communities of the Tugai forest in the Ebinur basin of Xinjiang, China. Biodiversity Science, 25, 34-45.
	[龚雪伟, 吕光辉 (2017). 艾比湖流域杜加依林荒漠植物群落多样性及优势种生态位. 生物多样性, 25, 34-45.] DOI
[14]	Han G, Zhao Z (2010). Light response characteristics of photosynthesis of four xerophilous shrubs under different soil moistures. Acta Ecologica Sinica, 30, 4019-4026.
	[韩刚, 赵忠 (2010). 不同土壤水分下4种沙生灌木的光合光响应特性. 生态学报, 30, 4019-4026.]
[15]	Hartmann H, Adams HD, Anderegg WRL, Jansen S, Zeppel MJB (2015). Research frontiers in drought-induced tree mortality: crossing scales and disciplines. New Phytologist, 205, 965-969. DOI PMID
[16]	He YY, Guo SL, Wang Z (2019). Research progress of trade-off relationships of plant functional traits. Chinese Journal of Plant Ecology, 43, 1021-1035. DOI URL
	[何芸雨, 郭水良, 王喆 (2019). 植物功能性状权衡关系的研究进展. 植物生态学报, 43, 1021-1035.] DOI
[17]	Huang CB, Zeng FJ, Lei JQ (2016). Growth and functional trait responses of Alhagi sparsifolia seedlings to water and nitrogen addition. Acta Prataculturae Sinica, 25, 150-160.
	[黄彩变, 曾凡江, 雷加强 (2016). 骆驼刺幼苗生长和功能性状对不同水氮添加的响应. 草业学报, 25, 150-160.]
[18]	Jin Y, Wang CK (2015). Trade-offs between plant leaf hydraulic and economic traits. Chinese Journal of Plant Ecology, 39, 1021-1032. DOI
	[金鹰, 王传宽 (2015). 植物叶片水力与经济性状权衡关系的研究进展. 植物生态学报, 39, 1021-1032.] DOI
[19]	Li SJ, Su PX, Zhang HN, Zhou ZJ, Xie TT (2013). Characteristics and relationships of foliar water and leaf functional traits of desert plants. Plant Physiology Journal, 49, 153-160.
	[李善家, 苏培玺, 张海娜, 周紫鹃, 解婷婷 (2013). 荒漠植物叶片水分和功能性状特征及其相互关系. 植物生理学报, 49, 153-160.]
[20]	Li WJ, Li Y, Lv J, He XM, Wang JL, Teng DX, Jiang LM, Wang HF, Lü GH (2022). Rhizosphere effect alters the soil microbiome composition and C, N transformation in an arid ecosystem. Applied Soil Ecology, 170, 104296. DOI URL
[21]	Li XY, Zhang XM, He XY, Zeng FJ, Foetzki A, Thomas F (2004). Water relation characteristics of four perennial plant species growing in the transition zone between oasis and open desert. Acta Ecologica Sinica, 24, 1164-1171.
	[李向义, 张希明, 何兴元, 曾凡江, Foetzki A, Thomas F (2004). 沙漠-绿洲过渡带四种多年生植物水分关系特征. 生态学报, 24, 1164-1171.]
[22]	Liu YB, Li XR, Li MM, Liu D, Zhang WL (2016). Leaf (or assimilation branch) epidermal micromorphology of desert plant in arid and semiarid areas of China. Chinese Journal of Plant Ecology, 40, 1189-1207. DOI URL
	[刘玉冰, 李新荣, 李蒙蒙, 刘丹, 张雯莉 (2016). 中国干旱半干旱区荒漠植物叶片(或同化枝)表皮微形态特征. 植物生态学报, 40, 1189-1207.] DOI
[23]	Luo WT, Zuo XA, Ma W, Xu C, Li A, Yu Q, Knapp AK, Tognetti R, Dijkstra FA, Li MH, Han GD, Wang ZW, Han XG (2018). Differential responses of canopy nutrients to experimental drought along a natural aridity gradient. Ecology, 99, 2230-2239. DOI PMID
[24]	Ma HY, Yang XD, Lü GH, He XM, Zhang XN, Wang XY, Li Y (2017). Water sources of dominant desert species in ebinur lake wetland nature reserve, Xinjiang, China. Acta Ecologica Sinica, 37, 829-840.
	[马辉英, 杨晓东, 吕光辉, 何学敏, 张雪妮, 汪溪远, 李岩 (2017). 新疆艾比湖湿地自然保护区荒漠优势种体内的水分来源. 生态学报, 37, 829-840.]
[25]	Ma TG, Li XY, Lin LS, Li L, Li SM, Wang B (2018). The effects of shade on leaf traits and water physiological characteristics in Alhagi sparsifolia. Acta Ecologica Sinica, 38, 8466-8474.
	[马天光, 李向义, 林丽莎, 李磊, 李世民, 王波 (2018). 遮阴对骆驼刺叶性状和水分生理的影响. 生态学报, 38, 8466-8474.]
[26]	Markham J (2019). Niche differentiation of tallgrass prairie plants species along soil hydrological gradients. Botany, 97, 487-494. DOI
[27]	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
[28]	McDowell NG (2011). Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology, 155, 1051-1059. DOI PMID
[29]	Pan YF, Chen XB, Jiang Y, Liang SC, Lu ZR, Huang YX, Ni MY, Qin CL, Liu RH (2018). Changes in leaf functional traits and soil environmental factors in response to slope gradient in karst hills of Guilin. Acta Ecologica Sinica, 38, 1581-1589.
	[盘远方, 陈兴彬, 姜勇, 梁士楚, 陆志任, 黄宇欣, 倪鸣源, 覃彩丽, 刘润红 (2018). 桂林岩溶石山灌丛植物叶功能性状和土壤因子对坡向的响应. 生态学报, 38, 1581-1589.]
[30]	Qie YD, Jiang LM, Lü GH, Yang XD, Wang HF, Teng DX (2018). Response of plant leaf functional traits to soil aridity and salinity in temperate desert ecosystem. Ecology and Environmental Sciences, 27, 2000-2010.
	[郄亚栋, 蒋腊梅, 吕光辉, 杨晓东, 王恒方, 滕德雄 (2018). 温带荒漠植物叶片功能性状对土壤水盐的响应. 生态环境学报, 27, 2000-2010.]
[31]	Réjou-Méchain M, Mortier F, Bastin JF, Cornu G, Barbier N, Bayol N, Bénédet F, Bry X, Dauby G, Deblauwe V, Doucet JL, Doumenge C, Fayolle A, Garcia C, Kibambe Lubamba JP, et al. (2021). Unveiling African rainforest composition and vulnerability to global change. Nature, 593, 90-94. DOI URL
[32]	Ren Y, Lu Q, Wu B, Liu MH (2015). Specific leaf area and leaf dry matter content of Nitraria tangutorum in the artificially simulated precipitation. Acta Ecologica Sinica, 35, 4707-4715.
	[任昱, 卢琦, 吴波, 刘明虎 (2015). 不同模拟增雨下白刺比叶面积和叶干物质含量的比较. 生态学报, 35, 4707-4715.]
[33]	Sala AN, Piper F, Hoch G (2010). Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist, 186, 274-281. DOI PMID
[34]	Scholz A, Stein A, Choat B, Jansen S (2014). How drought and deciduousness shape xylem plasticity in three Costa Rican woody plant species. IAWA Journal, 35, 337-355. DOI URL
[35]	Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014). How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment, 37, 153-161.
[36]	Stephenson NL, Das AJ (2020). Height-related changes in forest composition explain increasing tree mortality with height during an extreme drought. Nature Communications, 11, 3402. DOI: 10.1038/s41467-019-12380-6. DOI
[37]	Tang GL, Li XY, Lin LS, Li L, Lu JR (2013). Change of different shading on moisture conditions and the physiological response in Alhagi sparsifolia. Chinese Journal of Plant Ecology, 37, 354-364. DOI URL
	[唐钢梁, 李向义, 林丽莎, 李磊, 鲁建荣 (2013). 骆驼刺在不同遮阴下的水分状况变化及其生理响应. 植物生态学报, 37, 354-364.] DOI
[38]	Vastag E, Orlović S, Konôpková A, Kurjak D, Cocozza C, Pšidová E, Lapin K, Kesić L, Stojnić S (2020). Magnolia grandiflora L. shows better responses to drought than Magnolia × soulangeana in urban environment. IForest, 13, 575-583. DOI URL
[39]	Volaire F (2018). A unified framework of plant adaptive strategies to drought: crossing scales and disciplines. Global Change Biology, 24, 2929-2938. DOI PMID
[40]	Wang F, Guo SJ, Fan BL, Zhang WX, Wang FL, Han FG, Zhang YN, Sun T (2020). Variation in leaf functional traits of different-aged Haloxylon ammodendron communities, and the relationship with soil factors. Pratacultural Science, 37, 2486-2496.
	[王飞, 郭树江, 樊宝丽, 张卫星, 王方琳, 韩福贵, 张裕年, 孙涛 (2020). 不同年代梭梭叶功能性状差异及其与土壤因子的关系. 草业科学, 37, 2486-2496.]
[41]	Xue BL, Wang GQ, Xiao JF, Helman D, Sun WC, Wang JH, Liu TX (2020). Global convergence but regional disparity in the hydrological resilience of ecosystems and watersheds to drought. Journal of Hydrology, 591, 125589. DOI URL
[42]	Yang XD, Gong XW, Zhu LA, Lü GH (2017). Relationships among Populous euphratica hydraulic redistribution, niche breadth and biodiversity of its companion species in Tugai forests. Journal of Desert Research, 37, 933-941.
	[杨晓东, 龚雪伟, 朱丽安, 吕光辉 (2017). 胡杨(Populus euphratica)水分再分配与其伴生种多样性和生态位的关系. 中国沙漠, 37, 933-941.]
[43]	Yang XD, Lü GH (2011). Estimation of hydraulic redistribution of Populus euphratica in Ebinur Lake Wetland Nature Reserve in Xinjiang Uygur Autonomous Region, China. Chinese Journal of Plant Ecology, 35, 816-824. DOI URL
	[杨晓东, 吕光辉 (2011). 新疆艾比湖湿地自然保护区胡杨根系水分再分配的估算. 植物生态学报, 35, 816-824.] DOI
[44]	Yuan Y (2009). Photosynthetic and Water Physiological Characteristics of Populus euphratica in Ebinhu Lake Basin. Master degree dissertation, Xinjiang University, Ürümqi.
	[ 袁月 (2009). 艾比湖流域胡杨光合与水分生理特征研究. 硕士学位论文, 新疆大学, 乌鲁木齐.]
[45]	Yue XY, Zuo XA, Yu Q, Xu C, Lv P, Zhang J (2018). Effects of precipitation and short term extreme drought on leaf traits in Inner Mongolia typical steppe. Journal of Desert Research, 38, 1009-1016.
	[岳喜元, 左小安, 庾强, 徐翀, 吕朋, 张晶 (2018). 降水量和短期极端干旱对典型草原植物群落及优势种羊草(Leymus chinensis)叶性状的影响. 中国沙漠, 38, 1009-1016.]
[46]	Zhang XL, Zeng FJ, Liu B, Liu Z, An GX, Zhang H (2011). Effects of irrigation on root growth and distribution of the seedlings of Alhagi sparsifolia Shap. in the Taklimakan Desert. Journal of Desert Research, 31, 1459-1466.
	[张晓蕾, 曾凡江, 刘波, 刘镇, 安桂香, 张慧 (2011). 塔干沙漠南缘骆驼刺幼苗根系生长和分布对不同灌溉量的响应. 中国沙漠, 31, 1459-1466.]
[47]	Zhang XN, Yang XD, Li Y, He XM, Lü GH, Yang JJ (2018). Influence of edaphic factors on plant distribution and diversity in the arid area of Xinjiang, Northwest China. Arid Land Research and Management, 32, 38-56. DOI URL
[48]	Zhao SL, Zeng FJ, Zhang B, Liu B, Gao HH, Luo HL (2016). Effects of salt stress on leaf traits of Alhagi sparsifolia. Pratacultural Science, 33, 1770-1778.
	[赵生龙, 曾凡江, 张波, 刘波, 高欢欢, 罗瀚林 (2016). 盐分胁迫对骆驼刺幼苗叶片性状的影响. 草业科学, 33, 1770-1778.]
[49]	Zhou HH, Li WH, Ayup M, Xu Q (2012). Xylem hydraulic conductivity and embolism properties of desert riparian forest plants and its response to drought stress. Chinese Journal of Plant Ecology, 36, 19-29. DOI URL
	[周洪华, 李卫红, 木巴热克·阿尤普, 徐茜(2012). 荒漠河岸林植物木质部导水与栓塞特征及其对干旱胁迫的响应. 植物生态学报, 36, 19-29.] DOI
[50]	Zhou ZB, Li PJ (2002). A review on the phytotomy research of xerophytes in China. Arid Zone Research, 19, 35-40.
	[周智彬, 李培军 (2002). 我国旱生植物的形态解剖学研究. 干旱区研究, 19, 35-40.]
[51]	Zhu YH, Wu YQ (2003). Water consumption of natural plant Alhagi sparsifalia in arid desert region. Bulletin of Soil and Water Conservation, 23, 43-45.
	[朱永华, 仵彦卿 (2003). 干旱荒漠区植物骆驼刺的耗水规律. 水土保持通报, 23, 43-45.]