Next Article in Journal
High-Resolution Mapping and Impact Assessment of Forest Aboveground Carbon Stock in the Pinglu Canal Basin: A Multi-Sensor and Multi-Model Machine Learning Approach
Previous Article in Journal
Relationship Between Urban Forest Structure and Seasonal Variation in Vegetation Cover in Jinhua City, China
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 16
Issue 7
10.3390/f16071131
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Not Only Heteromorphic Leaves but Also Heteromorphic Twigs Determine the Growth Adaptation Strategy of Populus euphratica Oliv.

by
Yujie Xue
1,2,
Benmo Li
1,2,
Shuai Shao
1,2,
Hang Zhao
1,2,
Shuai Nie
1,2,
Zhijun Li
3 and
Jingwen Li
1,2,*
1
School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083, China
2
State Key Laboratory of Efficient Production of Forest Resources, Beijing 100083, China
3
Xinjiang Production & Construction Corps Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin, Alar 843300, China
*
Author to whom correspondence should be addressed.
Forests 2025, 16(7), 1131; https://doi.org/10.3390/f16071131
Submission received: 13 June 2025 / Revised: 5 July 2025 / Accepted: 7 July 2025 / Published: 9 July 2025
(This article belongs to the Section Forest Ecophysiology and Biology)
Browse Figures
Versions Notes

Abstract

The distinctive leaf and twig heteromorphism in Euphrates poplar (Populus euphratica Oliv.) reflects its adaptive strategies to cope with arid environments across ontogenetic stages. In the key distribution area of P. euphratica forests in China, we sampled P. euphratica twigs (which grow in the current year) at different age classes (1-, 3-, 5-, 8-, and 11-year-old trees), then analyzed their morphological traits, biomass allocation, as well as allometric relationships. Results revealed significant ontogenetic shifts: seedlings prioritized vertical growth by lengthening stems (32.06 ± 10.28 cm in 1-year-olds) and increasing stem biomass allocation (0.36 ± 0.14 g), while subadult trees developed shorter stems (6.80 ± 2.42 cm in 11-year-olds) with increasesd petiole length (2.997 ± 0.63 cm) and lamina biomass (1.035 ± 0.406 g). Variance partitioning showed that 93%–99% of the trait variation originated from age and individual differences. Standardized major axis analysis demonstrated a consistent “diminishing returns” allometry in biomass allocation (lamina–stem slope = 0.737, lamina–petiole slope = 0.827), with age-modulated intercepts reflecting developmental adjustments. These patterns revealed an evolutionary trade-off strategy where subadult trees optimized photosynthetic efficiency through compact architecture and enhanced hydraulic safety, while seedlings prioritized vertical space occupation. Our findings revealed that heteromorphic twigs play a pivotal role in modular trait coordination, providing mechanistic insights into P. euphratica’s adaptation to extreme aridity throughout its lifespan.

1. Introduction

Plant functional traits refer to a suite of pivotal morphological, physiological, and biochemical characteristics that plants develop to maximize their survival rate and functional performance in variable environments, thereby reflecting their capabilities in resource acquisition, utilization, and conservation [1,2,3]. Stems and leaves are two principal structural units of canopies, and their interactions determine plant strategies for utilizing resources such as light and space. Twigs, young branches (including stems and leaves) that grow in the current year, are the most dynamic part of plants, and are more sensitive to environmental conditions than the entire plant [4,5,6]. A twig comprises a stem with attached leaves (lamina and petiole). Leaves, especially laminas, as primary photosynthetic organs, substantially influence light interception efficiency and carbon assimilation through variations in size, quantity, and spatial deployment patterns. They serve as both a cornerstone of energy conversion in plants and an environmental response indicator, and their functional traits reflect the phenotypic adaptations and physiological adjustments of plants to external conditions [7,8]. Petioles, which connect laminas to stems, play a dual role: hydraulically transporting water, nutrients, and biochemical signals, while mechanically supporting and adjusting leaf positions to optimize sunlight capture, thus resembling the functions of stems [9,10,11,12,13]. Stems, serving as the structural framework of twigs, not only physically support leaves and petioles but also enable canopy spatial expansion through adjustments in branch length, diameter, and distribution patterns [6,14]. Different stem components collectively form an efficient light-capture system, and their intrinsic relationships reflect the resource utilization efficiency, allocation strategies, and trade-offs between hydraulic transport efficiency and safety of plants during the construction of stem and leaf traits [14,15].
Euphrates poplar (Populus euphratica Oliv.) is well known as a key species of the desert riparian forests in arid northwestern China. As the sole tree species capable of spontaneously forming extensive forests in the arid desert areas, P. euphratica provides vital ecosystem services, including desertification mitigation, windbreak and sand stabilization, microclimate regulation, and maintenance of regional ecological security. Thus, P. euphratica plays a pivotal role in stabilizing oasis ecosystems [16,17]. To survive extreme desert conditions, P. euphratica has evolved a suite of morphological and physiological adaptations, enabling it to thrive in water-limited and high-stress environments [18,19,20,21,22]. Among these adaptations, the ontogenetic process of heterophyllous leaf development in P. euphratica has garnered considerable attention. During the developmental process of P. euphratica, seedlings typically exhibit strip-shaped leaves. As the trees gradually mature, various leaf shapes such as lanceolate, ovate, and broad ovate leaves successively appear in the canopy. Substantial evidence confirms that leaf morphotypes exhibit significant divergence in morphology and marked differences in hydraulics, elemental composition, leaf–stem trade-offs, and twig architecture [6,20,21,23]. This dynamic leaf polymorphism mirrors ontogenetic optimization, enabling P. euphratica to maximize resource acquisition (e.g., light, water) while mitigating trade-offs imposed by arid environments. However, most studies have focused on heterophyllous leaves variations, the comparisons between leaves and petioles [23], and leaf–stem allometry [20,24,25]. These works largely overlooked the interactions between stems, petioles, and leaves. On the other hand, numerous studies have consistently shown that P. euphratica’s leaf shape changes continuously throughout its growth process. But these studies mostly used DBH (diameter at breast height) as an indicator of the species’ developmental stage. Although robust evidence has demonstrated a positive correlation between trunk diameter and tree age, these two parameters are not entirely interchangeable. Tree age, which reflects the actual chronological growth span of an individual, is closely related to the phenological growth events of trees (such as reproduction), while trunk diameter tends to be a marker of the overall growth condition of trees, being more strongly influenced by factors related to stem diameter. These two metrics reflect different aspects of the ontogenetic processes in P. euphratica [26]. Therefore, elucidating the morphological characteristics of the twigs and leaves of P. euphratica at different ages can facilitate a deeper understanding of its trade-off mechanisms in twig and leaf traits.
In this study, we investigated the morphological plasticity of P. euphratica twigs at different ages. The field survey was conducted at an experimental forest farm under controlled conditions to minimize environmental variability. By measuring 12 twig traits across five age classes of P. euphratica (1-, 3-, 5-, 8-, and 11-year-olds), this study aimed to: (i) determine whether these traits exhibit significant relationships with tree age; (ii) identify potential trade-offs in length and biomass allocation among plant modules (lamina, petiole, and stem); and (iii) assess whether these traits follow consistent scaling relationships, and whether such scaling patterns change significantly with age. Through this approach, we sought to unravel age-dependent trait variation and resource allocation strategies in P. euphratica, thereby advancing mechanistic understanding of its phenotypic plasticity regulation in arid environments.

2. Materials and Methods

2.1. Study Area

This study was conducted at the Ejina Banner State-Owned Forest Farm (39°53′–42°47′ N, 97°10′–103°07′ E), located in Ejina Banner, Alxa League, Inner Mongolia Autonomous Region, China, with elevations ranging from 716 m to 1333 m. The region experiences a temperate continental monsoon climate, characterized by low annual precipitation. According to data from the Ejina Banner Meteorological Station (2012–2022), the average annual precipitation is 38.6 mm, the average annual evaporation is 3398.59 mm, while the mean annual temperature is 10.5 °C. The main soil type in this area is Gypsi Sali-Orthic Aridosols.
Ejina Banner State-Owned Forest Farm possesses extensive expertise in P. euphratica cultivation and maintains a stable annual production of P. euphratica seedlings. In this study, we planted P. euphratica seedlings in 2013, 2016, 2019, 2021, and 2023, respectively. Each year’s planting covered a 100 m × 100 m area with 4 m × 4 m spacing between seedlings, with a planting density of approximately 625 trees per hectare. All seedlings were nurtured from seeds planted in the previous year at the farm’s greenhouse, and then transplanted to the experimental plots when the seedlings were 1 year old. Therefore, in 2023, these seedlings were 1, 3, 5, 8, and 11 years old, with their corresponding biometric characteristics detailed in Table S1. In each year, uniform site preparation and seedling cultivation measures were implemented. The water source for these P. euphratica seedlings primarily consisted of artificial water supplementation. Irrigation was performed 6 to 8 times annually in the greenhouse to ensure P. euphratica seed germination and seedling survival, and 2 to 3 times annually in experimental plots to match the natural rhythm of river inflows.

2.2. Sampling Design and Trait Measurement

The sampling was conducted in August 2023, during the late growth season of P. euphratica seedlings, a suitable stage to measure the variation in twig and leaf traits as well as their trade-off patterns. In the experimental plot, 15 individuals were selected randomly from five age classes (1-, 3-, 5-, 8-, and 11-year-olds) as the subjects. Each selected individual was healthy, with no signs of disease or pest damage. For each individual, five twigs (terminal stems of current-year shoots) were randomly collected from the upper-middle canopy in all four cardinal directions. Each selected twig was unshaded, undamaged, and growing normally. To account for the heteromorphic leaf characteristics, the collected shoots were ensured to bear as many morphological types of leaves as possible. The diverse morphological forms of P. euphratica leaves in each seedling age are illustrated in Figure S1. All samples were sealed in zip-lock bags and stored at a temperature of 0–4 °C during transportation to the laboratory. Upon arrival, the collection and measurement of various traits were conducted immediately. The overview of the study area and the morphology of twigs at different ages are illustrated in Figure 1.
Each twig sample was separated into three components: stem, lamina, and petiole. These components were then scanned individually using a scanner (CanoScan LiDE 700F, Canon, Tokyo, Japan). Lamina length (L_L), individual lamina area (L_A), individual petiole length (P_L), stem length (S_L), total lamina area in a twig (TLA), and total leaf number in a twig (TLN) were measured using ImageJ (version 1.54f). Subsequently, these components were placed in envelopes and dried to a constant weight in an oven set at 60 °C, and then stem mass (S_M), lamina mass (L_M), and petiole mass (P_M) were respectively recorded. Specific stem length (SSL) and specific petiole length (SPL) were defined as the ratio of stem length to stem mass and petiole length to petiole mass, respectively, while specific leaf area (SLA) was calculated as the ratio of leaf area to leaf mass. Leafing intensity based on stem mass (LIM) was calculated as the ratio of total leaf number to stem mass.

2.3. Data Analysis

The differences in the mean traits of P. euphratica among different ages were analyzed using one-way ANOVA with post hoc Tukey’s HSD test (α = 0.05). Significant differences among ages for each trait are indicated by different lowercase letters in Table 1. To evaluate the amount of variations in the traits, we assessed variations in traits across 4 hierarchical ecological scales: 1—among different ages of P. euphratica; 2—among individuals of the same age; 3—among twigs within an individual; and 4—unexplained proportion. A nested ANOVA coupled with variance partitioning was applied to calculate the variance components between the different levels [27,28]. Linear models were employed to assess whether these traits vary with plant age. To examine the trade-offs between paired traits across different ages, the data were standardized, and the root mean square error (RMSE) of individual traits was calculated to quantify the trade-offs between paired traits. Traits tend to favor one of the two in a paired trait relationship. The distance of the RMSE coordinates of the traits from the zero-trade-off line (i.e., the 1:1 diagonal) represents the overall benefit of a particular trait [29,30,31]. To analyze the relationships between different traits, allometric growth equations were expressed as:
y = b x a
This equation was log-transformed for analysis:
log 10 y = log 10 b + a log 10 x
Here, x and y represent two trait parameters;  log 10 b  is the intercept of the trait relationship; and a is the slope of the relationship, i.e., the allometric growth parameter. When |a| ≠ 1, it indicates an allometric relationship between the two traits. Standardized major axis (SMA) estimation was further employed to analyze the differences in allometric relationships between paired traits across different ages in P. euphratica.
All of the above statistical analyses and graphing were performed in R-4.4.1.

3. Results

3.1. Distribution of Twig and Leaf Traits of P. euphratica Across Age Classes

A significant variation was observed in all of the twig and leaf traits of P. euphratica across different age classes (p < 0.05, Table 1). Among these traits, petiole length increased markedly from 1-year-old to 11-year-old, while lamina length and total leaf number in a twig decreased markedly. Among adjacent age groups, these traits exhibited different variation patterns. For 1- vs. 3-year-old seedlings, most traits showed no significant differences except for S_L, S_M, and TLA. Between 3- and 5-year-olds, only three traits (L_L, SLA, and TLN) lacked significant differences. Strikingly, 5- vs. 8-year-olds exhibited significant differences in all traits except P_L. And 8- vs. 11-year-olds showed non-significant differences in half of the examined traits (S_L, S_M, L_M, TLA, SLA, TLN). Collectively, these results may suggest two critical transition phases in twig morphological development of P. euphratica: between 3–5 years and 5–8 years of age.
According to the variance decomposition results from nested ANOVA (Figure 2), the three hierarchical levels collectively accounted for 93%~99% of the total variation in twig and leaf traits. Variations at the age and individual levels predominantly contributed to the observed differences in all of the traits, while variations at the twig level contributed minimally. These findings indicated that age and individual differences were the primary drivers of trait variation in P. euphratica, and that twig and leaf traits of the same individual exhibited greater uniformity.
Regression analysis revealed that the leaf and twig traits of P. euphratica were significantly correlated with age (p < 0.001, Figure 3). Specifically, stem length and lamina length declined as age increased, while petiole length showed an opposite trend. In terms of biomass, stem mass decreased with age, whereas petiole mass and lamina mass increased with age. Also, specific stem length, specific petiole length, specific lamina area, total leaf number, and leafing intensity (based on stem mass) decreased significantly with tree age (p < 0.001), while total lamina area per twig showed an age-dependent increase (Figure 3). These findings highlighted the age-dependent patterns of the morphological and biomass allocation strategies of P. euphratica, reflecting its adaptive responses to developmental changes and environmental constraints.

3.2. The Allocation Trade-Offs Among Different Parts of P. euphratica Twigs

Biomass and length allocation shifted across different parts of P. euphratica twigs with increasing age. Specifically, the proportion of biomass allocated to stems progressively declined with increasing age, while that allocated to laminas and petioles correspondingly increased. The proportion of length allocated to stems remained relatively stable as age increased, while that allocated to laminas and petioles exhibited a descending and ascending trend, respectively (Figure 4a,e). Paired trade-off analyses indicated that P. euphratica exhibited distinct preferences in the twig biomass and length allocation across age classes. In the trade-off between laminas and stems (Figure 4b,f), except for 1-year-olds, the species demonstrated a preference for leaf biomass and stem length investment. Regarding the trade-off between laminas and petioles, most seedlings (except 11-year-olds) tend to invest more in leaf biomass (Figure 4c), while length allocation showed age-dependent trade-offs (Figure 4g): shifting from lamina elongation (1- and 3-year-olds) to petiole elongation (8- and 11-year-olds). In the context of stems vs. petioles, 11- and 8-year-olds showed a preference for petiole biomass investment (Figure 4d), and seedlings (except 11-year-olds) preferred stem elongation (Figure 4h).
Consequently, in terms of biomass investment (Figure 4b–d), 1-year-olds allocated more biomass to stems than to laminas or petioles, 3-year-old and 5-year-old saplings prioritized laminas over stems and petioles, 8-year-old saplings prioritized laminas over petioles and stems, and 11-year-old saplings gave priority to petioles over laminas and stems. The result reflects shifting priorities from structural support to photosynthetic efficiency and crown optimization. With respect to length investment (Figure 4f–h), 1-year-old saplings prioritized stems over laminas and petioles, 3-year-old and 5-year-old saplings prioritized laminas over stems and petioles, and 8-year-old and 11-year-old saplings prioritized petioles over laminas and stems. The results suggest adaptive adjustments in light-capture strategies from vertical growth to three-dimensional canopy display.

3.3. Trade-Offs in Current-Year Twigs of P. euphratica Across Age Classes

At the twig level, almost all pairwise relationships among the measured traits were statistically significant (p < 0.05; Figure 5). Notably, positive pairwise correlations were found among stem, petiole, and lamina mass, whereas relationships among stem, petiole, and lamina lengths showed distinct patterns, in which petiole length was negatively correlated with both stem length and lamina length, while lamina length maintained a positive correlation with stem length. Regarding resource acquisition efficiency, specific twig length, specific petiole length, and specific lamina area were all positively interrelated. Moreover, leafing intensity (based on stem mass) showed significant positive correlations with each of the three efficiency-related traits (specific twig length, specific petiole length, and specific lamina area).
Standardized major axis (SMA) analysis revealed significant positive allometric relationships of lamina mass with both stem mass (Figure 6a) and petiole mass (Figure 6b) in current-year twigs of P. euphratica across different age classes. The common slopes were 0.737 (95% CI: 0.695–0.781) and 0.827 (95% CI: 0.789–0.866), respectively, both significantly lower than 1.0 (p < 0.05, Table S2), indicating significant allometric relationships where lamina mass increased at a lower rate compared to stem and petiole mass. Simultaneously, as age increased, the y-intercept of the common slope relationship between lamina mass and stem mass showed an upward trend. This finding indicated that current-year twigs of the same stem mass supported greater lamina mass as the trees matured. In contrast, the y-intercept of the relationship between lamina mass and petiole mass exhibited a downward trend, suggesting that petioles of the same mass bore progressively less lamina mass as the trees matured. A significant positive relationship was observed between stem mass and petiole mass across all age classes, but no common slope was detected (Figure 6c). Specifically, the slope for 1-year-old seedlings was significantly less than 1.0 (p < 0.05), indicating an allometric relationship where stem mass accumulation was less efficient than that of petioles. In contrast, the slopes for 3-, 5-, and 8-year-old seedlings were significantly greater than 1.0 (p < 0.05), implying an allometric growth pattern with higher stem mass accumulation efficiency. However, 11-year-old trees displayed no allometric relationship between stem mass and petiole mass (p > 0.05), suggesting comparable growth efficiencies between these organs.
In terms of length, there were significant allometric relationships between lamina length and stem length across age classes (p < 0.05), with no common slope being detected (Figure 6d, Table S2). Specifically, 1-year-old and 5-year-old P. euphratica showed leaf–stem allometric indices significantly greater than 1 (p < 0.05), indicating higher growth efficiency in lamina length compared to stem length. In contrast, other age classes displayed allometric indices significantly less than 1 (p < 0.05), suggesting that stem growth efficiency surpassed leaf growth efficiency. All age classes except for 8-year-old trees showed significant allometric relationships between lamina length and petiole length (Figure 6e, Table S2, p < 0.05), implying that petiole length increased more efficiently than lamina length. Additionally, a significant allometric relationship was found between petiole length and stem length across all age classes (Figure 6f, Table S2). However, only 11-year-old trees exhibited a petiole-stem allometric index significantly different from 1 (p < 0.05), while the allometric index of other age classes showed no significant deviation from isometry (p > 0.05), indicating consistent growth efficiencies between stems and petioles.

4. Discussion

4.1. Age-Dependent Changes in Current-Year Twig Traits of P. euphratica

The twigs of P. euphratica serve as crucial organs for environmental interaction, and variations in twig traits reflect the trade-off strategies of the species for satisfying growth demands in arid environments [24,32,33]. Our study revealed substantial differences in twig traits across age classes, with trait variations at the age level consistently exceeding inter-individual variations (Figure 2), aligning with previous findings [18,22,26]. These results demonstrate that P. euphratica at different age stages achieves efficient resource utilization through differential allocation of traits among organs, leading to significant variations across all examined traits.
Based on the trait distribution patterns across age classes and the actual growth dynamics of P. euphratica (Table S1 and Figure S1), the seedling development can be categorized into three distinct phases. (1) Seedlings: the early establishment phase (1- and 3-year-olds) is characterized by small-sized seedlings bearing exclusively linear leaves without morphological differentiation. During this stage, seedlings prioritize rapid vertical growth to secure spatial dominance, exhibiting trait combinations of high stem length, substantial stem biomass, and elongated laminae (Table 1). (2) Intermediate samplings: the accelerated growth phase (5- and 8-year-olds) marks leaf morphological transitions with emerging lanceolate and oblong leaves, coinciding with peak biomass accumulation—evidenced by maximal total lamina area (TLA) and escalating petiole investment. (3) Subadult trees: the pre-reproductive maturation phase (11-year-olds) features predominant ovate to reniform leaves with rare narrow forms, coupled with initial fruiting. This stage shows a strategic resource reallocation that maintains vegetative growth while progressively shifting investment toward reproductive fitness, demonstrated by minimized stem growth, stabilized high petiole mass, and reduced but thicker laminas—traits optimizing hydraulic safety and carbon economy in mature canopies. These phase-specific trait syndromes reflect P. euphratica’s evolutionary strategy to balance growth-survival-reproduction trade-offs along its ontogeny in arid environments. The delineation of these growth stages corresponds with established ontogenetic patterns reported in previous studies [34,35].

4.2. Age-Dependent Trade-Offs in Twig Architecture Reveal P. euphratica’s Growth Strategies

The biomass allocation to different parts of twigs is crucial for plants to meet growth requirements. Our study demonstrated that in P. euphratica, lamina mass and petiole mass of twigs showed a significant positive relationship with age, while stem mass exhibited a negative relationship with age (Figure 3). Although the proportion of biomass allocated to leaves and petioles increased with age, whereas that allocated to stems decreased with age, their relative contributions consistently followed the pattern of leaf > stem > petiole (Figure 4). Plants may increase investment in leaf mass and leaf area to enhance the absorption capacity for light and carbon dioxide, thereby improving photosynthesis to maximize organic matter accumulation [36,37]. In addition, increased biomass allocation to stems and petioles provides a mechanical reinforcement to current-year twigs to resist physical damage from the extreme climatic conditions in arid desert regions characterized by high irradiance and strong wind [38]. Studies have demonstrated that during the growth and development of P. euphratica, increasing plant size may lead to greater demands for energy and water, which consequently enhances the photosynthetic capacity and drought resistance of P. euphratica [21,39,40]. To meet the growing requirements for nutrients and water, P. euphratica employed a dual strategy of progressively increasing the total biomass of current-year twigs while simultaneously augmenting investment in leaf mass and leaf area (Figure 3) to sustain growth. Correspondingly, the species established stronger support structures through increased biomass allocation to petioles, ensuring effective bearing of larger leaves while preventing mechanical damage.
Conversely, the growth strategy of P. euphratica twigs in terms of length not only acts as a pivotal component of canopy architecture, but also participates in the internal transport of nutrients and moisture [19,20,21]. Our study revealed that P. euphratica exhibited a significant decrease in stem length and leaf length but a marked increase in petiole length with increasing age (Figure 3). Regarding length allocation strategies, the proportion of twig length allocated to stems remained relatively constant, that allocated to leaves gradually declined, and that allocated to petioles progressively increased and eventually surpassed that to stems (Figure 4). The transport of nutrients and water in plants primarily relies on the xylem and phloem vessels within plant tissues. Relevant studies have demonstrated that taller trees are more vulnerable to drought-induced embolism caused by gravitational effects [21,41].
Both stems and petioles of P. euphratica twigs serve crucial supportive roles but exhibit divergent trends with increasing age. Stems progressively shortened while petioles lengthened as P. euphratica trees matured, though their combined lengths declined with age. This result demonstrates that mature P. euphratica trees optimize hydraulic efficiency by minimizing twig extension to reduce transport distances for resources [42]. Concurrently, increased quantities of leaf/petiole (Figure 3) promote structural branching, where longer petioles facilitate crown expansion, enabling more effective spatial occupation and environmental resource utilization to complete developmental life history [19,43].
Thus, the investment strategies for biomass and length allocation among different parts of P. euphratica twigs exhibited age-dependent variations. 1-year-old seedlings prioritized stem investment, which was characterized by limited branching, rapid twig elongation, smaller petioles, and numerous leaves, with greater energy allocated to stem growth to facilitate vertical expansion. As seedlings matured, they prioritized leaf investment, which was characterized by increasing leaf area and expanding crown dimensions, thereby improving photosynthetic efficiency to support developmental requirements. Upon reaching maturity, the now-open crown redirected investment toward petioles, which not only supported larger leaves but also optimized light capture within canopy gaps. Concurrently, the combination of shortened stems, lengthened petioles, and rounded leaves increases crown density, thereby enhancing plant resistance to extreme conditions (strong wind, drought, and high temperature) and improving survival capacity in hyper-arid environments.

4.3. Allometric Relationships Between Twig and Leaf Traits of P. euphratica Varied Significantly Across Age Classes

Numerous studies have confirmed that there are close interdependencies among plant functional traits, and that plants adapt themselves to specific environments by adjusting trait relationships [44,45,46,47]. Our study revealed strong correlations among traits (Figure 5), with SMA results demonstrating that while biomass allocation proportions varied across age classes, age exerted a minimal influence on the allometric relationships between leaf mass and stem mass or between leaf mass and petiole mass in current-year twigs. The allometric model effectively explained the age-related biomass allocation patterns in P. euphratica, a conclusion substantiated by other studies [48,49,50].
Across age classes, consistent positive allometric relationships were observed between leaf mass and petiole mass, leaf mass and stem mass, and leaf length and petiole length, with slopes significantly less than 1 (p < 0.05), indicating that the growth rates of leaves in both biomass and length were significantly lower than those of their supporting structures, conforming to the classic “diminishing returns” effect [10,51,52]. While stems and petioles have a function in supporting leaves and transporting water/nutrients, the “pipe model” theory posits that the cross-sectional area of petioles or stems scales proportionally with the supported leaf area to maintain adequate hydraulic supply [53]. However, beyond vascular transport, these structures must also withstand gravitational loading and wind-induced stresses, necessitating additional biomass investment that drives the observed allometry [54,55]. Similarly, allometric indices significantly greater than 1 (p < 0.05) between stem mass and petiole mass reflect greater structural investment in stems, as they assume more substantial mechanical support roles. For length allometry, inconsistent leaf–stem scaling across ages revealed divergent allocation strategies: 1- and 5-year-old seedlings prioritized leaf elongation for photosynthetic efficiency, while other age classes favored stem elongation for crown architecture. In contrast, stem-petiole length relationships showed isometry due to their shared hydraulic function without differential mechanical demands.

4.4. Research Limitations and Perspectives

Building upon existing research, our study emphasizes the ontogenetic morphological changes in P. euphratica twigs prior to reproductive maturity, establishing a novel three-stage growth classification. For forestry management, this developmental framework enables rapid assessment of tree growth strategies through diagnostic twig morphology and fruiting status evaluation, allowing for stage-specific silvicultural interventions to optimize individual productivity. However, our study primarily describes structural adaptations without addressing their physiological consequences, particularly how these morphological shifts influence photosynthetic efficiency, transpiration rates, or hydraulic conductivity, which ultimately determine whole-plant performance. Future investigations should integrate ecophysiological measurements (e.g., chlorophyll fluorescence, stomatal conductance, and δ13C analysis) to mechanistically link observed twig architectures with functional traits governing carbon-water balance. Such interdisciplinary approaches would provide a holistic understanding of P. euphratica’s developmental plasticity in arid ecosystems.

5. Conclusions

We systematically elucidated how twig and leaf trait coordination satisfied the ecological demands of P. euphratica across ontogenetic stages. Three key adaptive strategies emerged during the growth of P. euphratica. (1) Seedlings (1–3 years old) adopted a vertical expansion strategy and allocated greater twig biomass to stems to compete for light, as evidenced by high specific stem length and leafing intensity. (2) Intermediate samplings (5–8 years old) increased lamina mass allocation and developed longer petioles to enhance light-capture efficiency and optimize photosynthesis. (3) Subadult trees (11 years old) developed stress-resistant architectures characterized by increased petiole biomass allocation and length (exceeding stem length), with a negative correlation between petiole and stem lengths, forming compact crowns resistant to hydraulic failure. The conserved allometric slopes (0.737 for lamina–stem mass, 0.827 for lamina–petiole mass) across age classes confirmed universal scaling principles, while the shifting intercepts revealed plastic responses to developmental constraints. These findings advance our understanding of desert plant adaptation by demonstrating how modular trait integration, from juvenile “growth-first” to mature “safety-first” strategies, enables P. euphratica to balance competing demands in hyper-arid environments. Future studies should explore how these ontogenetic trajectories interact with microclimate gradients to influence population dynamics under climate change.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f16071131/s1, Figure S1: The diverse morphological forms of P. euphratica leaves (a–e) and twigs (f) in each seedling age (1-,3-,5-,8- and 11-year-old); Table S1: Basic characteristics of P. euphratica at different tree ages; Table S2: Results of standardized major axis regression (SMA) analysis of pairwise relationships among twig and leaf traits of P. euphratica across different age classes.

Author Contributions

Conceptualization, J.L. and Y.X.; methodology, software, and visualization, Y.X. and S.N.; investigation and data curation, B.L., H.Z., S.S. and Y.X.; writing—original draft preparation, Y.X.; writing—review and editing, Y.X., Z.L. and J.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Science and Technology Program of Inner Mongolia, China (2023KJHZ0022), and the National Natural Science Foundation of China (item identification no. 32271703).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
S_Lstem length
S_Mstem mass
SSLspecific stem length
P_Lpetiole length
P_Mpetiole mass
SPLspecific petiole length
L_Llamina length
L_Mlamina mass
TLAtotal leaf area
SLAspecific leaf area
TLNtotal leaf number
LIMleafing intensity based on stem mass

References

  1. Liu, X.; Ma, K. Plant Functional Traits & mdash; Concepts, Applications and Future Directions. Sci. Sin.-Vitae 2015, 45, 325–339. [Google Scholar] [CrossRef]
  2. Bruelheide, H.; Dengler, J.; Purschke, O.; Lenoir, J.; Jiménez-Alfaro, B.; Hennekens, S.; Botta-Dukát, Z.; Chytry, M.; Field, R.; Jansen, F.; et al. Global Trait-Environment Relationships of Plant Communities. Nat. Ecol. Evol. 2018, 2, 1906–1917. [Google Scholar] [CrossRef]
  3. Niu, S.; Classen, A.T.; Luo, Y. Functional Traits along a Transect. Funct. Ecol. 2018, 32, 4–9. [Google Scholar] [CrossRef]
  4. Xu, Y.; Yang, X.; Xie, Y.; Xu, Y.; Chang, S.X.; Yan, E. Twig size-number trade-off among woody plants in Tiantong region, Zhejiang Province of China. Chin. J. Plant Ecol. 2012, 36, 1268–1276. [Google Scholar]
  5. Song, H.; Zhang, J.; Zhao, Y.; Teng, J.; Liu, J. Effects of rocky desertification on growth and biomass accumulation and distribution of terminal twigs in Viburnum chinshanense Graebn. Plant Sci. J. 2018, 36, 103–111. [Google Scholar] [CrossRef]
  6. Wang, X.; Cao, J.; Zhang, X.; Kong, Y.; Tian, H.; Li, M.; Xu, X.; Gong, Y. Effects of topographic factors on leaf traits of apricot in the Loess Plateau, Northwest China. Chin. J. Appl. Ecol. 2019, 30, 2591. [Google Scholar] [CrossRef]
  7. Read, Q.D.; Moorhead, L.C.; Swenson, N.G.; Bailey, J.K.; Sanders, N.J. Convergent Effects of Elevation on Functional Leaf Traits within and among Species. Funct. Ecol. 2014, 28, 37–45. [Google Scholar] [CrossRef]
  8. Wei, M.; Wang, S.; Wu, B.; Jiang, K.; Zhou, J.; Wang, C. Variability of Leaf Functional Traits of Invasive Tree Rhus typhina L. in North China. J. Cent. South Univ. 2020, 27, 155–163. [Google Scholar] [CrossRef]
  9. Niklas, K.J. Testing “Economy in Design” in Plants: Are the Petioles and Rachises of Leaves “Designed” According to the Principle of Uniform Strength? Ann. Bot. 1993, 71, 33–41. [Google Scholar] [CrossRef]
  10. Niinemets, Ü.; Fleck, S. Petiole Mechanics, Leaf Inclination, Morphology, and Investment in Support in Relation to Light Availability in the Canopy of Liriodendron Tulipifera. Oecologia 2002, 132, 21–33. [Google Scholar] [CrossRef]
  11. Yang, D.; Li, G.; Sun, S. The Generality of Leaf Size versus Number Trade-off in Temperate Woody Species. Ann. Bot. 2008, 102, 623–629. [Google Scholar] [CrossRef] [PubMed]
  12. Anten, N.P.R.; Alcalá-Herrera, R.; Schieving, F.; Onoda, Y. Wind and Mechanical Stimuli Differentially Affect Leaf Traits in Plantago Major. New Phytol. 2010, 188, 554–564. [Google Scholar] [CrossRef]
  13. Filartiga, A.L.; Klimeš, A.; Altman, J.; Nobis, M.P.; Crivellaro, A.; Schweingruber, F.; Doležal, J. Comparative Anatomy of Leaf Petioles in Temperate Trees and Shrubs: The Role of Plant Size, Environment and Phylogeny. Ann. Bot. 2022, 129, 567–582. [Google Scholar] [CrossRef] [PubMed]
  14. Li, J.; Peng, G.; Yang, D. Effect of stem length to stem slender ratio of current-year twigs on the leaf display efficiency in evergreen and deciduous broadleaved trees. Chin. J. Plant Ecol. 2017, 41, 650–660. [Google Scholar]
  15. Sun, S.; Jin, D.; Shi, P. The Leaf Size-Twig Size Spectrum of Temperate Woody Species along an Altitudinal Gradient: An Invariant Allometric Scaling Relationship. Ann. Bot. 2006, 97, 97–107. [Google Scholar] [CrossRef] [PubMed]
  16. Wang, S. Current Status, Conservation, and Restoration Strategies of Global Populus euphratica Forests. Word For. Res. 1996, 38–45. [Google Scholar]
  17. Tian, Y.; Cheng, Y.; Bai, Y.; Xie, Z. Comprehensive Restoration Strategies for Degraded Ecosystems in the Ejina Oasis. Prot. For. Sci. Technol. 2009, 2, 42–44+81. [Google Scholar] [CrossRef]
  18. Li, J.; Liu, S.; Li, Z. Morphometric changes in stems, leaves and flower buds of Populus euphratica at different developmental stages. Chin. J. Ecol. 2015, 34, 941–946. [Google Scholar] [CrossRef]
  19. Yu, X.; Tian, Z.; Li, G.; Lv, X.; Zhuang, L. Study on the Plasticity of Branch System Architecture in the Desert Plant Populus euphratica across Different Developmental Stages. Xinjiang Agric. Sci. 2015, 52, 2076–2084. [Google Scholar]
  20. Kong, C.; Anwar, E.; Ma, L.; Long, Y.; Wang, Y.; Yang, X. Response of Twig—Leaf Size Relationships Populus euphratica with Heteromorphic Leaves to Drought Stress. Sci. Silvae Sinsac 2022, 58, 42–51. [Google Scholar]
  21. Cheng, L.; Han, H.; Liu, T.; Feng, J. Research on Water Use Efficiency of Heteromorphic Leaves in Populus euphratica at Different Canopy Heights. J. MUC (Nat. Sci. Ed.) 2023, 32, 5–12. [Google Scholar]
  22. Zou, X.; Wang, Y.; Wang, J.; Qu, M.; Zhu, W.; Zhao, H.; Xi, J.; Li, J. Coordination and trade-off of leaf functional traits in Populus euphratica and their response to tree age and soil factors. J. Beijing For. Univ. 2024, 46, 82–92. [Google Scholar]
  23. Yang, Q.; Li, Z.; Fu, Q.; Feng, J. Relationship among Leaf Trait and Developing Process in Populus euphratica. J. Desert Res. 2016, 36, 659. [Google Scholar] [CrossRef]
  24. Li, H.; Ma, R.; Qiang, B.; He, C.; Han, L.; Wang, H. Effect of current-year twig stem configuration on the leaf display efficiency of Populus euphratica. Chin. J. Plant Ecol. 2021, 45, 1251–1262. [Google Scholar]
  25. Zhai, J.; Chen, X.; Li, X.; Zhang, S.; Han, X.; Li, Z. Sexual dimorphism in allometric growth relationship between branch and leaf traits of Populus euphratica with changes in developmental stage and canopy height. J. Desert Res. 2023, 43, 116–127. [Google Scholar] [CrossRef]
  26. Wang, W.; Lv, H.; Zhong, Y.; Chen, L.; Li, J.; Ma, Q. Relationship between heteromorphic leaf traits of Populus euphratica and its individual development. J. Beijing For. Univ. 2019, 41, 62–69. [Google Scholar] [CrossRef]
  27. Messier, J.; McGill, B.J.; Lechowicz, M.J. How Do Traits Vary across Ecological Scales? A Case for Trait-Based Ecology. Ecol. Lett. 2010, 13, 838–848. [Google Scholar] [CrossRef]
  28. Liu, C.; Jin, G.; Liu, Z. Importance of Organ Age in Driving Intraspecific Trait Variation and Coordination for Three Evergreen Coniferous Species. Ecol. Indic. 2021, 121, 107099. [Google Scholar] [CrossRef]
  29. Bradford, J.B.; D’Amato, A.W. Recognizing Trade-Offs in Multi-Objective Land Management. Front. Ecol. Environ. 2012, 10, 210–216. [Google Scholar] [CrossRef]
  30. He, J.; Wang, J.; Zhou, T.; Song, Y.; Shi, N.; Naudiyal, N.; Wu, Y. Effects of growth stage and altitude on twig functional traits and biomass allocation of Rho dodendron przewalskii in the headwater region of Minjiang River, China. Chin. J. Appl. Ecol. 2020, 31, 4027–4034. [Google Scholar] [CrossRef]
  31. Zhang, Y.-Y.; Yan, J.-M.; Zhou, X.-B.; Zhang, Y.-M.; Tao, Y. Effects of N and P Additions on Twig Traits of Wild Apple (Malus sieversii) Seedlings. BMC Plant Biol. 2023, 23, 257. [Google Scholar] [CrossRef]
  32. Yang, D.; Zhang, J.; Zhou, D.; Qian, M.; Zheng, Y.; Jin, L. Leaf and twig functional traits of woody plants and their relationships with environmental change: A review. Chin. J. Ecol. 2012, 31, 702–713. [Google Scholar] [CrossRef]
  33. Hou, X.; Li, N. Variation and trade-offs of twig and leaf traits among different broad-leaved life form plants in the primitive broad-leaved Korean pine forest. J. Nanjing For. Univ. (Nat. Sci. Ed.) 2025, 49, 163–171. [Google Scholar]
  34. Yu, W.; Li, J.; Yao, L. Study on forest structure and renew of Pouplur euphratica Oliv. in Ejna. J. Inn. Mong. For. Sci. Technol. 2014, 40, 1–8. [Google Scholar]
  35. Wang, J.; Huang, W.; Yao, S.; Peng, C.; Song, S. Populus euphratica ion distribution, absorption and transport characteristics at different growth stages and its relationship with soil salinity. Acta Agric. Boreali-Occident. Sin. 2025, 34, 140–152. [Google Scholar]
  36. Li, G.; Yang, D.; Sun, S. Allometric Relationships between Lamina Area, Lamina Mass and Petiole Mass of 93 Temperate Woody Species Vary with Leaf Habit, Leaf Form and Altitude. Funct. Ecol. 2008, 22, 557–564. [Google Scholar] [CrossRef]
  37. Sun, J.; Wang, M.; Lyu, M.; Niklas, K.J.; Zhong, Q.; Li, M.; Cheng, D. Stem Diameter (and Not Length) Limits Twig Leaf Biomass. Front. Plant Sci. 2019, 10, 185. [Google Scholar] [CrossRef]
  38. Langer, M.; Kelbel, M.C.; Speck, T.; Müller, C.; Speck, O. Twist-to-Bend Ratios and Safety Factors of Petioles Having Various Geometries, Sizes and Shapes. Front. Plant Sci. 2021, 12, 765605. [Google Scholar] [CrossRef]
  39. Liu, S.; Jiao, P.; Li, Z. Types and spatial-temporal characteristics of heteromorphic leaves of Populus pruinosa. Arid Zone Res. 2016, 33, 1098–1103. [Google Scholar] [CrossRef]
  40. Shi, Z.; Wu, S.; Guan, W.; Han, W.; Yue, Y.; He, Y. Effects of different tree ages on leaf water potential and photosynthetic characteristics of Populus euphratica. Xinjiang Agric. Sci. 2022, 59, 1119–1127. [Google Scholar]
  41. Couvreur, V.; Ledder, G.; Manzoni, S.; Way, D.A.; Muller, E.B.; Russo, S.E. Water Transport through Tall Trees: A Vertically Explicit, Analytical Model of Xylem Hydraulic Conductance in Stems. Plant Cell Environ. 2018, 41, 1821–1839. [Google Scholar] [CrossRef] [PubMed]
  42. Fan, Z.-X.; Sterck, F.; Zhang, S.-B.; Fu, P.-L.; Hao, G.-Y. Tradeoff between Stem Hydraulic Efficiency and Mechanical Strength Affects Leaf–Stem Allometry in 28 Ficus Tree Species. Front. Plant Sci. 2017, 8, 1619. [Google Scholar] [CrossRef]
  43. Zhang, D.; Huang, W.; Xu, C.; Chen, F.; Zhang, Z.; Li, Z. The Branching Architecture Characteristic of Endangered Species Populus pruinosa in Different Developmental Stages. J. Tarim Univ. 2014, 26, 6–10. [Google Scholar]
  44. Reich, P.B. The World-Wide ‘Fast–Slow’ Plant Economics Spectrum: A Traits Manifesto. J. Ecol. 2014, 102, 275–301. [Google Scholar] [CrossRef]
  45. Kraft, N.; Godoy, O.; Levine, J. Plant Functional Traits and the Multidimensional Nature of Species Coexistence. Proc. Natl. Acad. Sci. USA 2015, 112, 797–802. [Google Scholar] [CrossRef]
  46. Skelton, R.; West, A.; Dawson, T. Predicting Plant Vulnerability to Drought in Biodiverse Regions Using Functional Traits. Proc. Natl. Acad. Sci. USA 2015, 112, 5744–5749. [Google Scholar] [CrossRef]
  47. Lam, W.N.; Huang, J.; Tay, A.H.T.; Sim, H.J.; Chan, P.J.; Lim, K.E.; Lei, M.; Aritsara, A.N.A.; Chong, R.; Ting, Y.Y.; et al. Leaf and Twig Traits Predict Habitat Adaptation and Demographic Strategies in Tropical Freshwater Swamp Forest Trees. New Phytol. 2024, 243, 881–893. [Google Scholar] [CrossRef]
  48. Zhai, J.; Lin, X.; Wu, R.; Xu, Y.; Jin, H.; Jin, G.; Liu, Z. Trade-offs between petiole and lamina of different functional plants in Xiao Hinggan Mountains, China. Chin. J. Plant Ecol. 2022, 46, 700–711. [Google Scholar]
  49. Li, L.; Jin, G.; Liu, Z. Variations and correlations of lamina and petiole traits of three broadleaved species in a broadleaved Korean pine forest. Chin. J. Plant Ecol. 2022, 46, 687–699. [Google Scholar]
  50. Eziz, A.; Yan, Z.; Tian, D.; Han, W.; Tang, Z.; Fang, J. Drought Effect on Plant Biomass Allocation: A Meta-Analysis. Ecol. Evol. 2017, 7, 11002–11010. [Google Scholar] [CrossRef]
  51. Zhu, G.; Niklas, K.J.; Li, M.; Sun, J.; Lyu, M.; Chen, X.; Wang, M.; Zhong, Q.; Cheng, D. “Diminishing Returns” in the Scaling between Leaf Area and Twig Size in Three Forest Communities Along an Elevation Gradient of Wuyi Mountain, China. Forests 2019, 10, 1138. [Google Scholar] [CrossRef]
  52. Zhu, J.; Meng, T.; Ni, J.; Su, H.; Xie, Z.; Zhang, S.; Zheng, Y.; Xiao, C. Within-leaf allometric relationships of mature forests in different bioclimatic zones vary with plant functional types. Chin. J. Plant Ecol. 2011, 35, 687–698. [Google Scholar]
  53. Lehnebach, R.; Beyer, R.; Letort, V.; Heuret, P. The Pipe Model Theory Half a Century on: A Review. Ann. Bot. 2018, 121, 773–795. [Google Scholar] [CrossRef] [PubMed]
  54. Niklas, K.J. Plant Allometry: Is There a Grand Unifying Theory? Biol. Rev. 2004, 79, 871–889. [Google Scholar] [CrossRef]
  55. Enquist, B.J. Universal Scaling in Tree and Vascular Plant Allometry: Toward a General Quantitative Theory Linking Plant Form and Function from Cells to Ecosystems. Tree Physiol. 2002, 22, 1045–1064. [Google Scholar] [CrossRef]
Forests 16 01131 g001
Figure 1. The overview of the study area and the morphology of twigs of Populus euphratica Oliv. at different ages.
Figure 1. The overview of the study area and the morphology of twigs of Populus euphratica Oliv. at different ages.
Forests 16 01131 g001
Forests 16 01131 g002
Figure 2. Variance partitioning of 12 traits from all the individuals across four nested levels: age, individual, twig, and unexplained. The proportion of variation explained here is based on the observed value derived by a nested ANOVA variance partitioning procedure. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Figure 2. Variance partitioning of 12 traits from all the individuals across four nested levels: age, individual, twig, and unexplained. The proportion of variation explained here is based on the observed value derived by a nested ANOVA variance partitioning procedure. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Forests 16 01131 g002
Forests 16 01131 g003
Figure 3. Relationships of leaf and twig traits with tree age shown by a linear model. Each dot represents a sample value. The text in each panel provides the slope, R2 values, and p value. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Figure 3. Relationships of leaf and twig traits with tree age shown by a linear model. Each dot represents a sample value. The text in each panel provides the slope, R2 values, and p value. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Forests 16 01131 g003
Forests 16 01131 g004
Figure 4. Allocation patterns and trade-off relationships of length and mass in current-year twig components (lamina, petiole, and stem) of P. euphratica across different age classes. (a,e) show the proportional allocation of mass and length to twig components, respectively; (b–d) depict pairwise trade-offs in mass allocation between twig components; (f–h) depict pairwise trade-offs in length allocation between twig components. S_L, stem length; S_M, stem mass; P_L, petiole length; P_M, petiole mass; L_L, lamina length; L_M, lamina mass.
Figure 4. Allocation patterns and trade-off relationships of length and mass in current-year twig components (lamina, petiole, and stem) of P. euphratica across different age classes. (a,e) show the proportional allocation of mass and length to twig components, respectively; (b–d) depict pairwise trade-offs in mass allocation between twig components; (f–h) depict pairwise trade-offs in length allocation between twig components. S_L, stem length; S_M, stem mass; P_L, petiole length; P_M, petiole mass; L_L, lamina length; L_M, lamina mass.
Forests 16 01131 g004
Forests 16 01131 g005
Figure 5. Correlations among current-year twig and leaf traits of Populus euphratica. The lower-left triangle displays pairwise Pearson correlation coefficients between traits, while the upper-right triangle visualizes these relationships through bivariate ellipses, where narrower ellipses indicate stronger correlations. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Figure 5. Correlations among current-year twig and leaf traits of Populus euphratica. The lower-left triangle displays pairwise Pearson correlation coefficients between traits, while the upper-right triangle visualizes these relationships through bivariate ellipses, where narrower ellipses indicate stronger correlations. S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Forests 16 01131 g005
Forests 16 01131 g006
Figure 6. Allometric relationships between (a) lamina mass and stem mass; (b) lamina mass and petiole mass; (c) stem mass and petiole mass; (d) lamina length and stem length; (e) lamina length and petiole length; (f) stem length and petiole length of P. euphratica across different age classes. Both axes represent log10-transformed trait values. Distinct line colors and point shapes indicate different tree age classes. Solid lines denote significant correlations (p < 0.05), while dashed lines represent non-significant relationships (p > 0.05). Significance levels are marked as: ** p < 0.01, and *** p < 0.001. S_L, stem length; S_M, stem mass; P_L, petiole length; P_M, petiole mass; L_L, lamina length; L_M, lamina mass.
Figure 6. Allometric relationships between (a) lamina mass and stem mass; (b) lamina mass and petiole mass; (c) stem mass and petiole mass; (d) lamina length and stem length; (e) lamina length and petiole length; (f) stem length and petiole length of P. euphratica across different age classes. Both axes represent log10-transformed trait values. Distinct line colors and point shapes indicate different tree age classes. Solid lines denote significant correlations (p < 0.05), while dashed lines represent non-significant relationships (p > 0.05). Significance levels are marked as: ** p < 0.01, and *** p < 0.001. S_L, stem length; S_M, stem mass; P_L, petiole length; P_M, petiole mass; L_L, lamina length; L_M, lamina mass.
Forests 16 01131 g006
Table 1. Differences in functional traits of twigs and leaves across different age classes.
Table 1. Differences in functional traits of twigs and leaves across different age classes.
TraitAge
135811
StemS_L (cm)32.06 ± 10.281 a16.638 ± 4.523 b27.125 ± 8.909 a10.107 ± 4.091 c6.797 ± 2.422 c
S_M (g)0.36 ± 0.141 a0.169 ± 0.118 b0.527 ± 0.278 a0.096 ± 0.043 b0.175 ± 0.11 b
SSL (cm/g)109.567 ± 41.665 a169.657 ± 88.558 a67.019 ± 21.929 b122.026 ± 33.085 a51.138 ± 15.642 b
PetioleP_L (cm)0.255 ± 0.234 c0.323 ± 0.168 c1.665 ± 0.633 b1.922 ± 0.648 b2.997 ± 0.63 a
P_M (g)0.009 ± 0.007 c0.01 ± 0.008 c0.075 ± 0.03 a0.038 ± 0.016 b0.079 ± 0.038 a
SPL (cm/g)835.712 ± 502.825 a618.294 ± 232.969 a290.233 ± 63.713 bc375.47 ± 116.884 b253.947 ± 65.029 c
LaminaL_L (cm)7.662 ± 0.944 a6.431 ± 1.183 ab7.754 ± 1.519 a5.559 ± 0.845 b4.299 ± 0.744 c
L_M (g)0.665 ± 0.324 bc0.409 ± 0.245 c1.346 ± 0.54 a0.709 ± 0.226 b1.035 ± 0.406 ab
TLA (cm2)59.757 ± 25.557 b29.874 ± 12.84 c92.935 ± 37.166 a52.698 ± 14.891 b72.485 ± 26.932 ab
SLA (cm2/g)95.279 ± 18.728 a84.471 ± 19.876 ab69.842 ± 6.154 b76.569 ± 9.346 b71.788 ± 6.367 b
TwigTLN23.1 ± 5.484 a14.28 ± 3.147 b12.427 ± 4.305 b6.773 ± 1.87 c5.773 ± 1.309 c
LIM80.424 ± 28.149 a186.933 ± 124.919 a34.788 ± 17.097 b96.058 ± 45.853 a47.601 ± 21.71 b
Mean ± standard error, different letters in the same row indicate significant differences (p < 0.05). S_L, stem length; S_M, stem mass; SSL, specific stem length; P_L, petiole length; P_M, petiole mass; SPL, specific petiole length; L_L, lamina length; L_M, lamina mass; TLA, total lamina area in a twig; SLA, specific leaf area; TLN, total leaf number in a twig; LIM, Leafing intensity based on stem mass.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Xue, Y.; Li, B.; Shao, S.; Zhao, H.; Nie, S.; Li, Z.; Li, J. Not Only Heteromorphic Leaves but Also Heteromorphic Twigs Determine the Growth Adaptation Strategy of Populus euphratica Oliv. Forests 2025, 16, 1131. https://doi.org/10.3390/f16071131

AMA Style

Xue Y, Li B, Shao S, Zhao H, Nie S, Li Z, Li J. Not Only Heteromorphic Leaves but Also Heteromorphic Twigs Determine the Growth Adaptation Strategy of Populus euphratica Oliv. Forests. 2025; 16(7):1131. https://doi.org/10.3390/f16071131

Chicago/Turabian Style

Xue, Yujie, Benmo Li, Shuai Shao, Hang Zhao, Shuai Nie, Zhijun Li, and Jingwen Li. 2025. "Not Only Heteromorphic Leaves but Also Heteromorphic Twigs Determine the Growth Adaptation Strategy of Populus euphratica Oliv." Forests 16, no. 7: 1131. https://doi.org/10.3390/f16071131

APA Style

Xue, Y., Li, B., Shao, S., Zhao, H., Nie, S., Li, Z., & Li, J. (2025). Not Only Heteromorphic Leaves but Also Heteromorphic Twigs Determine the Growth Adaptation Strategy of Populus euphratica Oliv. Forests, 16(7), 1131. https://doi.org/10.3390/f16071131

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop