Effects of hydraulic traits and anatomical structures on leaf morphological changes of Populus euphratica

doi:10.17521/cjpe.2025.0049

Abstract

Abstract:

Aims Leaves, exhibiting the highest ecological plasticity, are sensitive to environmental change. They also act as both the hydraulic bottleneck and safety valve against hydraulic dysfunctions. Populus euphratica is well-adapted to extreme arid environments and possesses heteromorphic leaves that are distributed differentially along the vertical heights of the tree. This study aims to explore the variations of hydraulic and anatomical traits of heteromorphic leaves and their interaction, as well as to elucidate the mechanisms underlying morphological divergence along gradients of groundwater depth (GWD) and vertical heights. The findings are expected to enhance our understanding of their adaptation strategies to adverse environments and provide a scientific basis for the protection and restoration of desert P. euphratica forest in the context of global change.

Methods Through a community survey along a gradient of GWD, we measured the hydraulic, structural and morphological traits of three different leaf shapes from adult P. euphratica trees at different vertical heights within canopy. We then examined the differences in morphological traits, hydraulic traits (e.g., hydraulic conductance, vein, stomata) and anatomical structures, and analyzed their interrelationship.

Important findings (1) Under different GWD conditions, significant differences were observed in the morphological, hydraulic and anatomical traits of leaves with the same shape, while under the same GWD, the three heteromorphic leaves exhibited notable variations in these traits across different canopy heights. For a given leaf type, traits such as minor vein density, loopiness of veins, free-end density, vessel density, leaf thickness, palisade-to-spongy mesophyll ratio, epidermal and cuticular thickness all increased with greater GWD, similarly, these functional traits (e.g., minor vein density, vessel density and palisade-to-spongy mesophyll ratio) increased along vertical canopy height under the same GWD. Deeper GWD and higher canopy positions were associated with enhanced vein development and more xeromorphic anatomical structures in heteromorphic leaves. (2) Compared with the heteromorphic leaves in the lower-middle canopy, the serrated broad-oval leaves in the upper canopy are wider and thicker, with more developed palisade tissue and complex venation networks. These structural adaptations have evolved in response to intense light, high temperatures and increased transpiration demand, resulting in a more efficient hydraulic system and a robust defensive architecture. This enhances the water transport efficiency and water retention capacity, thereby improving embolism resistance and drought tolerance. (3) The leaf length-width ratio (LI) and dissection index (DI) were significantly correlated with most hydraulic and anatomical traits. Hydraulic traits contributed more to leaf morphological variation than anatomical features, with the interval distance between veins, closed-loop area, vein density and proportion of minor veins playing predominant roles in shaping leaf morphology. (4) Most leaf morphological traits showed a highly significant correlation with hydraulic path length and leaf attachment height. Hydraulic path length mediates leaf morphological variation (LI, DI) by influencing hydraulic and anatomical structures, indicating that hydraulic constraints along the vertical canopy gradient are a key factor driving leaf shape differentiation in P. euphratica.(5) The coupling between hydraulic traits and anatomical structures enhances hydraulic functionality and boosts stress resilience in P. euphratica. Leaf shape differentiation represents an ecological strategy evolved by the species to adapt to contrasting hydraulic environments throughout its life cycle.

Key words: hydraulic trait, anatomical structure, groundwater depth, vertical height, leaf shape differentiation, Populus euphratica

WANG Hai-Zhen, WANG Yu-Qing, MA Fu-Long, HAN Lu. Effects of hydraulic traits and anatomical structures on leaf morphological changes of Populus euphratica[J]. Chin J Plant Ecol, 2026, 50(6): 1419-1435.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2025.0049

https://www.plant-ecology.com/EN/Y2026/V50/I6/1419

Figures/Tables 9

Table 1 Overview of the survey plots and characteristics of Populus euphratica population in study area

样地 Site	经纬度 Longitude and latitude	地下水埋深 Groundwater depth (m)	胡杨 Populus euphratica
样地 Site	经纬度 Longitude and latitude	地下水埋深 Groundwater depth (m)	平均胸径 Average DBH (cm)	平均树高 Average height (m)	密度 Density (inds·hm^-2)
肖夹克 Xiaojiake (U₁)	80.95° E, 40.48° N	1.0-1.5	26.3	6.4	290.5
塔南镇 Tanan Town (U₂)	81.15° E, 40.44° N	2.3-2.7	22.6	8.5	171.3
阿瓦提县 Awat County (U₃)	80.39° E, 40.33° N	4.5-5.0	21.1	7.9	268.1
沙雅县 Shaya County (U₄)	82.01° E, 40.69° N	7.5-8.0	36.4	7.8	120.2

Fig. 1 Morphological characteristics of three heteromorphic leaves of Populus euphratica. A, Lanceolate leaf at lower layer. B, Oval leaf at middle-upper layer. C, Serrated broad-oval leaf at upper layer. D, Distribution of different leaf shapes on vertical height.

Table 2 Morphological characteristics of three heteromorphic leaf types in Populus euphratica (mean ± SD)

垂直高度 Vertical height	叶形 Leaf Shape	地下水埋深 GWD (m)	叶长 Leaf length (cm)	叶宽 Leaf width (cm)	叶面积 Leaf area (cm²)	周长 Leaf perimeter (cm)	长宽比 Length/ width	叶圆度指数 Roundness index	叶锯齿化指数 Dissection index
下层 Lower	L	1.0-1.5	11.89 ± 1.65^a/A	1.25 ± 0.24^a/C	11.77 ± 3.11^a/B	25.80 ± 3.65^a/b	9.67 ± 4.75^a/A	0.22 ± 0.03^a/C	2.14 ± 0.16^a/A
		2.3-2.7	9.39 ± 1.49^b/A	1.01 ± 0.20^b/C	7.56 ± 2.42^b/B	20.35 ± 3.22^b/a	9.59 ± 1.80^a/A	0.23 ± 0.03^a/B	2.12 ± 0.16^a/A
		4.5-5.0	9.86 ± 2.91^b/A	1.09 ± 0.15a^b/C	8.36 ± 1.80^b/C	22.60 ± 4.80^ab/b	9.40 ± 3.52^a/A	0.22 ± 0.05^a/B	2.20 ± 0.30^a/A
		7.5-8.0	9.88 ± 1.30^b/A	0.91 ± 0.12^b/C	7.09 ± 1.37^b/B	21.41 ± 2.87^b/a	10.96 ± 1.65^a/A	0.20 ± 0.03^a/B	2.27 ± 0.15^a/A
均值 Mean			10.26 ± 1.11	1.06 ± 0.15	8.70 ± 2.12	22.54 ± 2.36	9.91 ± 0.71	0.21 ± 0.01	2.19 ± 0.07
中层 Middle	O	1.0-1.5	8.49 ± 1.72^A/B	3.40 ± 1.00^a/B	17.21 ± 5.55^ab/B	20.77 ± 3.65^A/c	2.63 ± 0.72^a/B	0.50 ± 0.08^a/A	1.43 ± 0.11^ab/B
		2.3-2.7	8.07 ± 1.55^A/A	3.07 ± 0.76^a/B	14.48 ± 4.37^b/A	19.27 ± 3.25^A/a	2.75 ± 0.75^a/B	0.49 ± 0.09^aA	1.44 ± 0.13^a/B
		4.5-5.0	8.16 ± 0.83^A/A	3.63 ± 0.74^a/B	17.94 ± 4.22^a/B	20.06 ± 2.01^A/c	2.32 ± 0.45^a/B	0.56 ± 0.07^aA	1.35 ± 0.08^b/B
		7.5-8.0	6.03 ± 1.24^B/B	2.37 ± 0.57^b/B	8.82 ± 3.47^c/B	14.50 ± 2.80^B/c	2.63 ± 0.64^a/B	0.51 ± 0.07^a/A	1.40 ± 0.09^ab/C
均值 Mean			7.69 ± 1.12	3.12 ± 0.55	14.61 ± 4.14	18.65 ± 2.83	2.58 ± 0.18	0.51 ± 0.03	1.41 ± 0.04
上层 Upper	S	1.0-1.5	4.55 ± 0.72^B/C	8.53 ± 0.90^A/A	27.72 ± 5.09^A/A	31.10 ± 2.86^A/a	0.54 ± 0.06^c/C	0.36 ± 0.03^C/B	1.67 ± 0.08^A/B
		2.3-2.7	3.76 ± 0.58^C/B	5.77 ± 0.67^C/A	15.17 ± 3.79^B/A	19.83 ± 2.26^C/a	0.65 ± 0.05^b/C	0.48 ± 0.05^B/A	1.45 ± 0.08^B/B
		4.5-5.0	5.67 ± 0.68^A/B	7.63 ± 0.58^B/A	30.94 ± 4.65^A/A	25.19 ± 2.45^B/a	0.74 ± 0.08^a/B	0.61 ± 0.06^A/A	1.28 ± 0.07^C/B
		7.5-8.0	3.65 ± 0.41^C/C	5.15 ± 0.57^C/A	13.74 ± 2.68^B/A	18.72 ± 2.78^C/b	0.71 ± 0.04^a/C	0.50 ± 0.06^B/A	1.43 ± 0.09^B/B
均值 Mean			4.40 ± 0.93	6.77 ± 1.58	21.89 ± 8.61	23.71 ± 5.58	0.66 ± 0.09	0.49 ± 0.10	1.46 ± 0.16
GWD			**	**	**	**	ns	**	**
VH			**	**	**	**	**	**	**
VH × GWD			**	**	**	**	ns	**	**

Table 2 Morphological characteristics of three heteromorphic leaf types in Populus euphratica (mean ± SD)

垂直高度 Vertical height	叶形 Leaf Shape	地下水埋深 GWD (m)	叶长 Leaf length (cm)	叶宽 Leaf width (cm)	叶面积 Leaf area (cm²)	周长 Leaf perimeter (cm)	长宽比 Length/ width	叶圆度指数 Roundness index	叶锯齿化指数 Dissection index
下层 Lower	L	1.0-1.5	11.89 ± 1.65^a/A	1.25 ± 0.24^a/C	11.77 ± 3.11^a/B	25.80 ± 3.65^a/b	9.67 ± 4.75^a/A	0.22 ± 0.03^a/C	2.14 ± 0.16^a/A
		2.3-2.7	9.39 ± 1.49^b/A	1.01 ± 0.20^b/C	7.56 ± 2.42^b/B	20.35 ± 3.22^b/a	9.59 ± 1.80^a/A	0.23 ± 0.03^a/B	2.12 ± 0.16^a/A
		4.5-5.0	9.86 ± 2.91^b/A	1.09 ± 0.15a^b/C	8.36 ± 1.80^b/C	22.60 ± 4.80^ab/b	9.40 ± 3.52^a/A	0.22 ± 0.05^a/B	2.20 ± 0.30^a/A
		7.5-8.0	9.88 ± 1.30^b/A	0.91 ± 0.12^b/C	7.09 ± 1.37^b/B	21.41 ± 2.87^b/a	10.96 ± 1.65^a/A	0.20 ± 0.03^a/B	2.27 ± 0.15^a/A
均值 Mean			10.26 ± 1.11	1.06 ± 0.15	8.70 ± 2.12	22.54 ± 2.36	9.91 ± 0.71	0.21 ± 0.01	2.19 ± 0.07
中层 Middle	O	1.0-1.5	8.49 ± 1.72^A/B	3.40 ± 1.00^a/B	17.21 ± 5.55^ab/B	20.77 ± 3.65^A/c	2.63 ± 0.72^a/B	0.50 ± 0.08^a/A	1.43 ± 0.11^ab/B
		2.3-2.7	8.07 ± 1.55^A/A	3.07 ± 0.76^a/B	14.48 ± 4.37^b/A	19.27 ± 3.25^A/a	2.75 ± 0.75^a/B	0.49 ± 0.09^aA	1.44 ± 0.13^a/B
		4.5-5.0	8.16 ± 0.83^A/A	3.63 ± 0.74^a/B	17.94 ± 4.22^a/B	20.06 ± 2.01^A/c	2.32 ± 0.45^a/B	0.56 ± 0.07^aA	1.35 ± 0.08^b/B
		7.5-8.0	6.03 ± 1.24^B/B	2.37 ± 0.57^b/B	8.82 ± 3.47^c/B	14.50 ± 2.80^B/c	2.63 ± 0.64^a/B	0.51 ± 0.07^a/A	1.40 ± 0.09^ab/C
均值 Mean			7.69 ± 1.12	3.12 ± 0.55	14.61 ± 4.14	18.65 ± 2.83	2.58 ± 0.18	0.51 ± 0.03	1.41 ± 0.04
上层 Upper	S	1.0-1.5	4.55 ± 0.72^B/C	8.53 ± 0.90^A/A	27.72 ± 5.09^A/A	31.10 ± 2.86^A/a	0.54 ± 0.06^c/C	0.36 ± 0.03^C/B	1.67 ± 0.08^A/B
		2.3-2.7	3.76 ± 0.58^C/B	5.77 ± 0.67^C/A	15.17 ± 3.79^B/A	19.83 ± 2.26^C/a	0.65 ± 0.05^b/C	0.48 ± 0.05^B/A	1.45 ± 0.08^B/B
		4.5-5.0	5.67 ± 0.68^A/B	7.63 ± 0.58^B/A	30.94 ± 4.65^A/A	25.19 ± 2.45^B/a	0.74 ± 0.08^a/B	0.61 ± 0.06^A/A	1.28 ± 0.07^C/B
		7.5-8.0	3.65 ± 0.41^C/C	5.15 ± 0.57^C/A	13.74 ± 2.68^B/A	18.72 ± 2.78^C/b	0.71 ± 0.04^a/C	0.50 ± 0.06^B/A	1.43 ± 0.09^B/B
均值 Mean			4.40 ± 0.93	6.77 ± 1.58	21.89 ± 8.61	23.71 ± 5.58	0.66 ± 0.09	0.49 ± 0.10	1.46 ± 0.16
GWD			**	**	**	**	ns	**	**
VH			**	**	**	**	**	**	**
VH × GWD			**	**	**	**	ns	**	**

Table 3 Relationship between morphological characteristics of heteromorphic leaves in Populus euphratica and factors

项目 Item	叶面积 Leaf area	周长 Leaf perimeter	叶长 Leaf length	叶宽 Leaf width	长宽比 Length/ width	叶圆度指数 Roundness index	叶锯齿化指数 Dissection index
地下水埋深 Groundwater depth	-0.287^**	-0.424^**	-0.173^**	-0.171^**	0.039	0.106	-0.039
树高 Tree height	-0.168^**	-0.149^*	-0.067	-0.071	0.008	-0.073	0.029
胸径 Diameter at breast height	-0.187^**	-0.222^**	-0.099	-0.090	0.010	0.017	-0.016
叶着生高度 Blade attachment height	0.514^**	-0.097	-0.734^**	0.737^**	-0.898^**	0.776^**	-0.834^**
水力路径长度 Hydraulic path length	0.122	-0.381^**	-0.612^**	0.357^**	-0.560^**	0.589^**	-0.577^**

Fig. 2 Effect of vertical height and groundwater depth on hydraulic traits and anatomical structure of Populus euphratica heteromorphic leaves (mean ± SD). VH, vertical height; GWD, groundwater depth; L, lanceolate leaf; O, oval leaf; S, serrated broad-oval leaf. Different lowercase letters indicate significant difference among heteromorphic leaves at different canopy heights under the same groundwater depths (p < 0.05), different uppercase letters denote significant difference in the same leaf morphology across varying groundwater depths (p < 0.05). **, p < 0.01; *, p < 0.05; ns, p > 0.05.

Fig. 3 Differences in morphological, hydraulic and anatomical traits of heteromorphic leaves in Populus euphratica. A, C, U1 plot with groundwater depth (GWD) 1.2 m; B, F, U4 plot with GWD 7.8 m; D, U2 plot with GWD 2.5 m; E, U3 plot with GWD 4.8 m. L, lanceolate leaf; O, oval leaf; S, serrated broad-oval leaf. BXA, xylem-bundle ratio; CLA, closed loop area; CT, cuticle thickness; DBC, depth of subcavity; FED, free-end density; IBV, interval between veins; KL, hydraulic conductance; LET, aba-epidermis thickness; LPV, loopiness of veins; LT, leaf thickness; MVBA, major vein bundle area; MVD, vessel diameter of major vein; MVXA, major vein xylem area; PMV, percentage of minor vein (%); PA, phloem area; PT, palisade tissue thickness; SA, stomatal area; SD, stomatal density; SL, stomatal length; ST, spongy tissue thickness; SW, stomatal width; UET, ada-epidermal thickness; VA, vessel area; VC, vessel diameter; VD, vessel density; VLA, total vein density; VLAM, major vein density; VLAS, minor vein density; VN, vessel number; VV, total vein volume.

Fig. 4 Intrinsic factors driving the leaf shape of heteromorphic leaves in Populus euphratica. ULET, ada-aba epidermal thickness; See Fig. 3 for details of other index. **, p < 0.01; *, p < 0.05; ns, p > 0.05.

Fig. 5 Bivariate relationships between leaf dissection index and influencing factors of Populus euphratica. PC1, principal component 1.

Fig. 6 Path diagram of structural equation model with direct and indirect path coefficients of driving factors of leaf morphology in Populus euphratica. AIC, akaike information criterion; AS, anatomical structure; CLA, Closed loop area; CT, cuticle thickness; DBC, depth of subcavity; DI, Leaf dissection index; df, degree of freedom; FED, free-end density; HPL, hydraulic path length; HT, hydraulic structure; IBV, interval between veins; KL, hydraulic conductance; LI, Length/width ratio; SD, stomatal density; ULET: ada-aba epidermal thickness; VLAM, major vein density; VN, vessel number. The dotted line indicates no significant correlation, blue and red lines indicate the positive and negative effects, respectively. Width of the lines shows the strength of the causal relationship, the numbers on lines are standardized path coefficients. All of the drivers of the DI/LI were chosen based on previous associations and random forest analysis. The R2conditional and R2marginal represent the proportion of variance explained by all predictors without and with accounting for random effects. ***, p < 0.001; **, p < 0.01; *, p < 0.05.

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