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Review

Trade-Off between Hydraulic Safety and Efficiency in Plant Xylem and Its Influencing Factors

by
Shan Li
1,
Jing Wang
1,
Sen Lu
1,
Yann Salmon
2,3,
Peng Liu
1 and
Junkang Guo
1,*
1
Department of Environmental Science and Ecology, School of Environmental Science and Engineering, Shaanxi University of Science and Technology, Xi’an 710021, China
2
Institute for Atmospheric and Earth System Research (INAR)/Forest Sciences, Faculty of Agriculture and Forestry, University of Helsinki, 00014 Helsinki, Finland
3
Institute for Atmospheric and Earth System Research (INAR)/Physics, Faculty of Science, University of Helsinki, 00014 Helsinki, Finland
*
Author to whom correspondence should be addressed.
Forests 2023, 14(9), 1817; https://doi.org/10.3390/f14091817
Submission received: 23 June 2023 / Revised: 30 August 2023 / Accepted: 4 September 2023 / Published: 5 September 2023
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
Forests are vital ecosystems that are increasingly threatened by environmental stress; exploring the possible trade-off between hydraulic safety and efficiency in plant xylem is crucial to understanding their environmental adaptation strategies. However, to date, there is no consensus whether such trade-offs exist among and within species. To better comprehend the mechanism of xylem water transport, in this review, we summarized previously published work on xylem hydraulic safety and efficiency trade-off from the inter-species, intra-species, and intra-tree perspectives and its influencing factors. We gathered data on xylem hydraulic safety and efficiency and their related anatomical traits, i.e., conduit diameter and inter-conduit pit membrane thickness, from a total of 653 plant species analyzed in 80 published papers. At the inter-species level, we confirmed that there is a weak hydraulic safety and efficiency trade-off. For gymnosperms and herbaceous species, the observed trade-off is stronger. At the intra-species level, the hydraulic safety and efficiency trade-off was found in individuals of the same species investigated in the literature. At the intra-tree level, there is a trade-off between hydraulic safety and efficiency for leaves, stems, and roots, and we confirmed the vessel widening hypothesis, i.e., vessel diameter in the outer wood increases from the top to the bottom of the tree. Additionally, pit membrane thickness increases as the tree height decreases, thus increasing the xylem hydraulic efficiency and affecting the trade-off. Finally, we discussed the environmental factors affecting the trade-off between hydraulic safety and efficiency in the xylem, such as plant habitats, temperature, rainfall, altitude, and soil. Further investigations of the bordered pit membrane from the three-dimensional perspective would be useful to understand the hydraulic safety and efficiency trade-off at the nanoscale.

1. Introduction

Forests are one of the most important ecosystems, providing us with valuable ecological and economic services [1]. However, global climate-change-associated drought has triggered an increase in forest mortality worldwide [2,3,4]. Compelling evidence has shown that forest and tree mortality is often associated with failure of trees to transport water [5], so-called “hydraulic failure”. Therefore, exploring the adaptation of the plant hydraulic system to its environment is critical to our ability to understand and predict forest response to climate change, as well as guide their management.
According to the theory of cohesion–tension, water in trees is transported along a negative pressure gradient in the xylem conduits (tracheid or vessels). The air seeding hypothesis postulates that xylem embolism occurs when the pressure in a conduit becomes sufficiently negative—under certain conditions such as drought—causing external air bubbles to enter the conduit from neighboring embolized conduits through the pits [6]. Under continuous drought, the embolism spreads from conduit to conduit, causing catastrophic blockage of the xylem water transport network, i.e., xylem hydraulic failure [7].
Plants develop adaptive strategies to low water availability, they adjust their growth, physiology, and xylem structure to ensure water transport [8]. Plant xylem is a complex multicellular network composed mainly of different types of cells, such as tracheary elements, parenchyma cells, and fibers [9], which are responsible for plant water transport, nutrient storage, and mechanical support, respectively. There are two well-known physiological indicators evaluating xylem water transport function, xylem hydraulic safety and efficiency, which are closely related to the anatomical characteristics of the xylem [10]. Hydraulic efficiency describes the rate of water transport through a given area and length of sapwood, across a given pressure gradient, and is most often measured as xylem-specific hydraulic conductivity (KS). Because KS scales to the fourth power of the conduit diameter, larger conduits have higher KS. Also, as KS represents the water transport capacity of the xylem, it is related to the photosynthetic capacity and the water balance of the whole plant [11]. However, the values of KS within a species may vary depending on the applied measurement methods [12]. Hydraulic safety represents the negative pressure that can be sustained by the xylem water before embolism causes a meaningful loss of hydraulic conductivity (PX) [13]. The PX at which 50% loss of conductivity occurs (P50) is the most commonly used hydraulic trait for evaluating xylem embolism resistance [14]. When PX falls below P50, the xylem’s water transport function is markedly altered and the plant is exposed to a considerable risk of accelerated embolism, leading to long-term reductions in productivity, tissue damage, and ultimately death [15]. Therefore, the xylem embolism resistance of plants is the key to preventing hydraulic failure [16].
Previous studies have shown that more efficient xylem comes at the cost of being more vulnerable to hydraulic failure [14,17,18,19]. Nevertheless, whether there is a general trade-off between hydraulic safety and efficiency remains controversial, and there is growing evidence that this trade-off might only exist in some cases or be weak [13]. However, thorough investigations of this trade-off and its existence for different types of plant species are still lacking.
Xylem conduit traits, for example, conduit diameter, conduit wall thickness, and conduit density, largely determine hydraulic safety and hydraulic efficiency [20,21,22]. The larger the xylem conduit diameter, the lower the conduit density and the more likely it is xylem embolism will occur [23]. Additionally, longer conduits are associated with greater vulnerability [24]. Neighboring conduits are hydraulically connected by numerous tiny bordered pits that provide channels for water transport but also allow xylem embolism propagation [25]. Increasing evidence indicates that pits are crucial structures in determining xylem hydraulic conductivity and embolism resistance [26]. What’s more, species with vessel groupings often have less embolism resistance than species with isolated conduits, which is probably due to inter-conduit connectivity (i.e., total pit area), pit membrane thickness, and porosity [27]. In addition, xylem with a higher axial parenchyma fraction and greater connectivity between vessels and the axial parenchyma can achieve a co-optimization of safety and efficiency [28]. Nevertheless, how the wood anatomical traits affect the hydraulic traits and thus the potential trade-off requires further investigation.
The adaptation of xylem hydraulic traits is a key strategy for plants in coping with environmental stresses such as drought. In addition to the anatomy of the xylem, internal factors of plants, such as species types and plant sex, and environmental factors, such as the growing conditions of the plants (field or garden), soil moisture, season, rainfall, geographical location, and elevational trends, have also been reported to influence the trade-off between hydraulic safety and efficiency [29,30,31]. However, the influences of internal and external factors on the potential trade-off have been rarely summarized.
Previous work has shown that whether the hydraulic efficiency and safety trade-off exists depends on the plant type studied; however, investigations based on detailed categories of plant types are still lacking. There are still open questions, such as the following: Is there a trade-off between hydraulic safety and efficiency among different tree species? Are they within the same family or genus? Are they among different organs within the same tree? If there is a trade-off, which factors could influence the trade-off? By reviewing the literature on the hydraulic safety versus efficiency trade-off reported at the inter-species, intra-species, and intra-tree levels and their influencing factors, as well as adding the results from our investigations, we aimed to test the relationship between hydraulic safety and efficiency at multiple levels and explore its controlling factors.
In this study, we analyzed data on hydraulic safety and efficiency and related anatomical traits from 653 plant species analyzed in 80 published papers. We used exponential and linear models to fit the data, and all statistical analyses were performed using the software Origin Pro 2023, version Origin 2023 pro Bata (OriginLab Corporation, Northampton, MA, USA). Mann–Whitney U and Kruskal–Wallis were used for the significance test in the software IBM SPSS Statistics for Windows, version 27.0 (IBM Corp., Armonk, NY, USA).

2. Inter-Species Trade-Offs

Plant xylem is the main tissue responsible for water transport, and different plant species have different xylem structures to adapt to their growing conditions [27]. In general, the xylem of gymnosperm species consists of the tracheid, while most angiosperm species xylems are made of vessels except for the basal angiosperm species xylem, which mainly consists of tracheids [32,33]. Angiosperm species have higher hydraulic efficiency, whereas gymnosperm species have higher hydraulic safety [34]. However, there is no agreement on whether there is a trade-off between hydraulic safety and efficiency in the xylem among gymnosperm and angiosperm species. Numerous studies have shown that differences in the xylem structure of gymnosperms and angiosperms affect and alter the plant’s safety and efficiency trade-off [35,36,37,38]. In general, species that are embolism-resistant have thicker conduit walls, and the cell wall reinforcement factor [(t/b)2] (t is the double cell wall thickness and b is the conduit wall span) has been proposed as an alternative trait to estimate xylem embolism resistance [21].
From the data of xylem hydraulic efficiency and safety we collected for 533 species, including 415 angiosperms, 88 gymnosperms, and 30 ferns, we found a weak relationship (R2 = 0.041, p < 0.05) between hydraulic efficiency and safety from 320 of these species, including 256 angiosperms, 45 gymnosperms, and 19 ferns (Table 1, Figure 1a). Here, we used the linear fit for the log-transformed data, which showed a stronger relationship between xylem hydraulic efficiency and safety, confirming the trade-off (log(P50) − log(KS), Figure 1). Compared to ferns and angiosperm species, gymnosperm species have significantly higher hydraulic safety (p < 0.05). We also observed that ferns and angiosperms have a broader range of xylem hydraulic efficiency than gymnosperms (Figure 1b). Note that caution should be exercised with the comparison result due to the limited data available for the hydraulic traits of ferns.

2.1. Angiosperm Species

In angiosperms, vessels transport water longitudinally, i.e., along the long axis of the plant, while fibers mainly provide mechanical support [39]. Species with vessel groups have higher hydraulic conductivity due to having greater conduit-to-conduit connectivity than isolated conduits, at the cost of increased embolism vulnerability, illustrating a trade-off between efficiency and safety [40]. Generally, xylem parenchyma consists of axial and ray parenchyma, with axial parenchyma existing primarily in angiosperms species [41]. Angiosperm xylem with a higher axial parenchyma fraction and greater connectivity between vessels and axial parenchyma achieved a weak trade-off between safety and efficiency [28]. Species with a higher axial parenchyma fraction had higher hydraulic safety, which could be related to the role of the parenchyma in adjusting osmotic potential and possibly embolism repair [42]. Previous studies have shown that a hydraulic safety and efficiency trade-off exists in most angiosperm species. For example, seven Acer species, ten Prunus species, and eleven Rosaceae species showed a trade-off between hydraulic safety and efficiency, which appeared to be determined by a very complex vessel network and pit characteristics [43,44,45]. Similarly, in the present study, angiosperm species showed a hydraulic safety and efficiency trade-off (Figure 2a, R2 = 0.018, p < 0.05). Moreover, our results show that a weak negative relationship between hydraulic efficiency and safety is found within diffuse-porous species (Table 1, R2 = 0.006, p < 0.05), whereas a weak and positive relationship between hydraulic safety and efficiency (Table 1, R2 = 0.077, p < 0.05) was found in ring-porous species.
Diffuse-porous and ring-porous species have significantly different spatial arrangements of xylem vessels. Ring-porous species have a larger xylem/vessel area ratio and are thus structurally more efficient at transporting water than diffuse-porous species, having a higher hydraulic efficiency [37]. However, there is considerable debate about the estimation of the hydraulic safety in ring-porous species, as contradictory results for individual species have been found depending on the methods used to measure P50. Such methodological problems are remarkably frequent for species having large xylem conduits (such as ring-porous), potentially leading to a substantial overestimation of embolism vulnerability [46]. Diffuse-porous species have smaller vessel diameters, higher vessel density, and larger vessel wall thickness ratios, making them more embolism-resistant than ring-porous species and better able to ensure tree survival under water stress [34]. This difference between ring- and diffuse-porous species is further supported by the present study of 12 ring-porous species and 103 diffuse-porous species (Figure 2b), in which we found that diffuse-porous species had significantly higher xylem hydraulic safety than ring-porous species (p < 0.05), but no significant difference regarding KS was found for the two different wood types (p > 0.05).

2.2. Gymnosperm Species

There was a trade-off between hydraulic safety and efficiency in the 88 gymnosperm species studied here (Table 1, R2 = 0.393, p < 0.05). Similarly, some studies showed that reduced hydraulic efficiency was partly compensated by an increase in the hydraulic safety between gymnosperm species [47,48,49]. A possible explanation is that conifer species with higher embolism resistance possess a narrower tracheid and hence have lower xylem hydraulic efficiency [50]. However, species from Picea and Pinus do not exhibit such a trade-off, and the trade-off might depend on the studied species [13,51]. Additionally, leaf stomatal regulation behavior across species correlates with the trade-off between xylem hydraulic safety and efficiency. Isohydric species display tight regulation of leaf water potential through large declines in leaf stomatal conductance, whereas anisohydric species maintain stomatal conductance at the cost of letting the water potential decrease [52]. Many conifer species tend to be on the more isohydric end along the iso/anisohydric continuum [53], having higher xylem hydraulic efficiency and lower xylem hydraulic safety than the more anisohydric conifers [54].

2.3. Ferns

Despite the taxonomic diversity and ecological importance of ferns in tropical environments, the structure–function relationship of tropical fern xylem remains unexplored, especially regarding the hydraulic safety and efficiency of hydraulic transport in these species. The data on the hydraulic safety and hydraulic efficiency of 19 fern species show very weak a trade-off (Table 1, R2 = 0.006), which is consistent with previous studies [6,55]. Additionally, it has also been shown that the hydraulic relationship between function and structure, e.g., thicker pit membranes provide higher hydraulic safety [56], further affects ferns’ hydraulic safety and efficiency trade-off. However, other studies showed no hydraulic trade-off in ferns [57], which is the opposite of our result. Perhaps because of inter-species variability, we need to continue to explore research on hydraulic safety and efficiency trade-offs in ferns.

2.4. Life Types of Plants

Different life types also have different xylem hydraulic safety and efficiency trade-offs [58]. We used polynomial regression to fit the log-transformed data because the raw data did not conform to the residual normal distribution, and our results show a specific hydraulic safety and efficiency trade-off for the data merged from the four life types because KS–P50 is correlated for trees, shrubs, herbaceous species, and lianas (Figure 3a). Xylem safety and efficiency vary depending on the type of plant (Figure 3b, p < 0.05). Trees have relatively higher hydraulic safety, while shrubs have relatively higher hydraulic efficiency. It should be noted that the herbaceous plants in our investigation also had high hydraulic safety, possibly because of their lignification [59].

2.4.1. Trees and Lianas

All 242 tree species we collected data exhibited a trade-off between hydraulic efficiency and hydraulic safety (Table 1, R2 = 0.047, p < 0.05), in agreement with other studies.
Similarly, for the 29 lianas species we studied, a weak trade-off was found between hydraulic safety and efficiency (Table 1, R2 = 0.001, p < 0.05). Although, according to our data, both trees and lianas show a weak trade-off, previous studies showed that lianas are more susceptible to embolism caused by drought stress and have a greater ability to transport water than trees [51,60]. This may be related to lianas relying on the maintenance of leaf hydraulic conductivity for their survival, whereas trees rely more on water stored in the stems [50]. However, contrary to our results, some studies showed that the hydraulic safety and efficiency trade-off does not exist in lianas. The uncoupling of efficiency and safety could allow them to have high hydraulic efficiency, and therefore high growth rates, without compromising their embolism resistance during drought, thus providing them with a growth advantage over trees under drier conditions [12].

2.4.2. Shrubs and Herbaceous

Among the 30 shrub species studied, a weak trade-off between hydraulic safety and efficiency was observed (Table 1, R2 = 0.001, p < 0.05), and an adaptive adjustment in hydraulic traits was necessary for shrubs to cope with different environmental conditions. For example, shrubs species with greater embolism resistance growing at dry sites also tended to have lower xylem hydraulic efficiency [61]. Additionally, the vulnerability of shrub species to embolism varies seasonally, with greater susceptibility to water-stress-induced embolism observed during the wet season [62].
The data collected from 60 herbaceous species showed a hydraulic safety and efficiency trade-off (Table 1, R2 = 0.52, p < 0.05), where the hydraulic safety was relatively higher than that in shrubs due to herbaceous lignification (Figure 3b). Compared with the other three life types, there are less reports on the hydraulic trade-off in herbaceous plants and no clear evidence that a hydraulic safety and efficiency trade-off exists [63]. The xylem water transport in herbaceous species is assumed to be more vulnerable to the environment due to the frequent formation of embolisms [64]. Moreover, embolism resistance generally comes at a lignification cost in herbaceous plants, which leads to the selection of species with more lignified stems in grasslands under drought conditions [59].

2.4.3. Deciduous and Evergreen

We observed that of the deciduous (Table 1, R2 = 0.001, p < 0.05) and evergreen (Table 1, R2 = 0.004, p < 0.05) species studies, 51 and 49 of them, respectively, have a trade-off between hydraulic safety and efficiency) (Figure 4a). Most studies showed a trade-off between hydraulic safety and efficiency [65,66]; similarly, deciduous species showed significantly higher hydraulic efficiency (p < 0.05) and significantly lower hydraulic safety (p < 0.05) than evergreen species (Figure 4b). They also tended to adopt a riskier water transport and drought avoidance strategy, which prioritizes hydraulic efficiency to ensure adequate water supply to the canopy [67]. Thus, they develop larger conduits with corresponding higher hydraulic conductivity. Evergreen tree species prioritize embolism resistance to withstand the driest season of the year and maintain function throughout the year [7]; thus, they develop a more conservative water transport system [68], which involves the evolution of larger density conduits and thicker pit membranes to improve embolism resistance [7].
In an Asian dry karst forest with co-occurring evergreen and deciduous species, there is an apparent difference in stem hydraulic traits and leaf water stress tolerance. Specifically, deciduous trees had higher stem hydraulic efficiency, and evergreen species had higher resistance to xylem embolism; furthermore, a correlation between the hydraulic efficiency of the xylem and embolism was observed [69]. Moreover, when the hydraulic safety of deciduous and evergreen species did not differ, the hydraulic efficiency of deciduous species was higher than that of evergreen species (Figure 3b).

3. Intra-Species Trade-Offs

Individuals from different hybrids of the same species exhibit a trade-off between hydraulic safety and efficiency. For example, eight Zea mays hybrids showed a trade-off, with high hydraulic efficiency and low hydraulic safety. Additionally, tree individuals from Populus fremontii growing at different latitudes also displayed such a trade-off, with those having higher hydraulic efficiency showing lower hydraulic safety [70]. Moreover, when exposed to high temperatures, individual trees from the same species showed a trade-off with higher efficiency and lower safety than those grown under cooler conditions [71].
Xylem hydraulic safety and efficiency differ among male and female individuals. Under well-watered conditions, females of Populus cathayana possessed a bigger area of xylem lumen and theoretically higher hydraulic efficiency. Conversely, males had a lower lumen area of xylem but greater conduit density and a higher cell wall thickness, suggesting a theoretically conservative water use strategy geared towards resistance to drought [72]. This is consistent with another study reporting evidence of contrasting approaches to water use between sexes, with females having a more efficient water transport system than males to support their higher reproductive costs, while males focus on safety-related strategies that favor survival [73]. Similarly, females of dioecious conifer species had higher conductivity but were more prone to experience embolism than males. This observation is further supported by a study in which the wood anatomical features of female individuals from Juniperus thurifera were associated with higher hydraulic efficiency (higher theoretical hydraulic conductivity) rather than safety (thinner cell walls), while the male individuals had a more conservative strategy, especially at drier sites [30].
In summary, individuals within the same species have various hydraulic trade-offs, which is inconsistent with the generally accepted view that closely related tree species have a similar hydraulic safety and efficiency trade-off. While the hydraulic trade-off between different tree species depends mainly on xylem anatomy [74], intra-species plasticity allows adaptation of the xylem morphology and structure to the environment in which individual trees are growing [75].

4. Intra-Tree Trade-Off

According to the analogy between hydraulic resistance and electrical resistance as described by Ohm’s law, the xylem water transport system can be described as being composed of three primary hydraulic resistances arranged in series: the root system, the stem, and the leaf [76]. We analyzed data on the hydraulic properties of these three organs for 165 tree species and found trade-offs between hydraulic safety and efficiency at the organ level (Figure 5a, Table S4), which is consistent with the vulnerability segmentation hypothesis [8]. The vulnerability segmentation hypothesis proposes that plant branches are more embolism-resistant than their terminal leaves. This allows leaves to act as safety valves’ to protect the woody hydraulic pathway from dysfunction. Hydraulic segmentation has been commonly reported in species from arid regions but not necessarily for species growing in humid areas [77]. Moreover, the xylem embolism resistance of the root is greater than that of the stem. For example, in mangroves, the roots’ embolism resistance is higher than that of the branches. While vulnerability segmentation has been found in some tree species, it is still unclear whether it also occurs in herbaceous species [78].

4.1. Leaf

The leaf is an essential part of the plant, being the primary location for photosynthesis, and its photosynthetic ability could influence the trade-off between hydraulic safety and efficiency. A weak trade-off between hydraulic safety and efficiency has been reported in leaves [79,80], which is consistent with our own observation across published studies (Table 1, R2 = 0.029, p < 0.05). The safety and efficiency trade-off in the xylem can also be considered from the angle of a trade-off between the hydraulic safety and photosynthetic ability of the plant, as xylem hydraulic efficiency and leaf stomatal conductance are closely linked, and the latter is correlated with leaf photosynthetic ability [11,81,82]. Additionally, the compensation effect (CE), i.e., the positive relationship between safety and efficiency, is the dominating force facilitating photosynthetic ability [83].
There is also a link between the structure of the leaf xylem and hydraulic function [15]. Leaf vein density and conduit diameter are two characteristics of the xylem that are closely connected to leaf hydraulic efficiency [84]. Leaf water potential and hydraulic conductivity are negatively correlated, and hydraulic conductivity increases with leaf age [19]. Furthermore, leaf hydraulic safety is influenced by the characteristics of the tissues outside the xylem, such as the turgor loss point, and by the vein xylem’s characteristics, such as vein structure [85]. In addition, mesophyll can contribute to leaf hydraulic dysfunction, further affecting leaf hydraulic safety [15]. In addition, when the CO2 concentration is high, stomata close to ensure the hydraulic safety of the plant [86]. These all ultimately affect the hydraulic safety and efficiency trade-off.

4.2. Stem

The stem plays an essential role in plants’ hydraulic transport. The stems of the 72 species for which we collected data exhibited a trade-off between hydraulic safety and efficiency (Table 1, R2 = 0.093, p < 0.09). In line with our results, many studies also showed that there is a trade-off between hydraulic safety and efficiency in stems. Stem xylem conductivity is critical to plant water balance, and increased xylem-specific conductivity may also be associated with reduced hydraulic safety [86,87,88]. For instance, a distinct trade-off between safety and efficiency was found in maize and Vaccinium uliginosum stem xylem [89]. In addition, the stem xylem of Robinia pseudoacacia species had a low safety and high hydraulic efficiency trade-off, but the stem xylem of Rhus typhina species had a high hydraulic safety and low hydraulic efficiency trade-off [90].

4.3. Root

A plant’s root system plays a crucial role in absorbing water and nutrients [91]. Our results for 15 species show a weak trade-off between hydraulic efficiency and safety in the roots (Table 1, R2 = 0.038, p < 0.05) (Figure 5b), which is consistent with previous findings. The relatively stable water condition in the soil, especially in the deep layers, is favorable for the development of larger-diameter vessels in the root xylem. Deep roots have a greater water transport ability due to their larger vessel diameter, but higher embolism vulnerability and lower hydraulic safety, indicating an apparent trade-off between conducting water efficiently and safely [83]. High elevations reduce root hydraulic efficiency, but do not affect hydraulic safety, indicating that roots growing at a high altitude can overcome higher stress levels due to their considerable embolism resistance [29]. Although the roots show more vulnerable xylem compared with the branches, resprouting after aboveground mortality begins at the roots, suggesting that caution should be exercised in evaluating the drought resistance of plants considering their xylem embolism resistance alone [92,93].

4.4. Tree Height

There are differences in the hydraulic trade-off among organs in the same plant. Increased tree height implies a longer hydraulic path and affects the hydraulic efficiency and safety of the xylem [94]. The diameter of the xylem conduit decreased gradually from the root to the stem to the leaf among the 87 species for which we collected data (Figure 6a). It has been found in numerous species that within individuals, the conduit widens from the stem tip towards the base, and even into the roots (“vessel widening”) [95]. This is regarded as an adaptive pattern, i.e., the xylem conduits gradually become thinner towards the crown, resulting in a structure that minimizes the overall hydraulic resistance and favors tree growth [96]. Meanwhile, as tree height increased, the pit membrane thickness gradually decreased (Figure 6b). Changes in pit traits can also influence the hydraulic safety and efficiency trade-off of plant xylem. A larger pit membrane area but lower pit density within individual cycad plants may provide higher hydraulic efficiency, which affects the hydraulic trade-off between safety and efficiency [97]. Although it has been shown that the structure of the pit affects the hydraulic trade-off, the exact mechanism underlying this is not clear. Indeed, because characterizing the three-dimensional structure of the xylem pit membrane is challenging, studying the hydraulic safety and efficiency trade-off at the pit membrane level is challenging.
The more conductive xylem at the top of taller trees compared with shorter trees from the same species allows full compensation for height-related hydraulic constraints, at the cost of a corresponding increase in vulnerability to embolism, showing that hydraulic efficiency is prioritized over safety with increasing height [98]. This adaptation to increasing height therefore transforms into a shift of the trade-off between safety and efficiency from higher safety to higher efficiency [86] and shows that intra-individual differences in the hydraulic system exist not only between organs but also within them [99].
In summary, there is a weak trade-off between hydraulic safety and efficiency for most plant organs (Figure 5a), supporting the hypothesis of hydraulic segmentation. However, this trade-off varies among plant organs, with the roots having higher hydraulic safety than the stems and the leaves. There is no clear pattern regarding hydraulic efficiency (Figure 5b), which may be due to the fact that the stems and leaves have different water transport distances and morphological structures and are exposed to different environmental conditions compared to the roots.

5. Influencing Factors

The trade-off between hydraulic safety and efficiency in plant xylem is not only affected by internal factors (see above) but also responds to various external factors [100], including plant habitats, temperature, rainfall, altitude, soil environment, etc. (Figure 7).

5.1. Plant Habitats (Field and Garden)

Differences in plant habitats can cause changes in the hydraulic efficiency and safety of the xylem. Hydraulic efficiency is higher for plants growing in the field, but embolism resistance is higher for those growing in gardens [101]. For example, for three gymnosperm species, Pseudolarix amabilis, Cunninghamia lanceolata, and Cedrus deodara, individuals have lower hydraulic efficiency and higher embolism resistance when growing in gardens than in fields, due to the complexity of those species’ adaptation strategies [80,102]. Compared with those grown in gardens, species found in fields with low soil moisture availability show an increased pit membrane diameter due to the need for higher hydraulic efficiency. Additionally, plants growing in fields can avoid embolism by having increased wood density and a larger tracheid diameter [24].

5.2. Temperature, Rainfall, and Altitude

Seasonal and annual average temperature and rainfall variations impact xylem structure and function across and within species [76]. Higher hydraulic efficiency was found in habitats with higher temperatures and higher precipitation on a global scale [103]. Additionally, plants adapt their trade-off between embolism resistance and hydraulic efficiency in response to aridity. Populations from xeric sites with higher temperatures were less vulnerable to embolism than those growing at mesic sites [104]. In the winter time, due to the low solubility of gas in ice, bubbles could induce xylem embolism formation and lower plants’ xylem hydraulic safety during freeze–thaw cycles [105,106,107].
The hydraulic response of plants to rainfall variability remains poorly understood. Plant productivity and the amount of water they use (inferred from the enhanced vegetation index) during the summer is independent of the total amount of winter rainfall [108] when winter rainfall is not stored and utilized by plants, and vice versa. However, this does not mean that rainfall amount cannot affect the hydraulic safety and efficiency of plants at the individual level. Further research has revealed that the annual amount of rainfall can affect species’ hydraulic safety and efficiency trade-off [103], because rainfall amount influences the degree of drought, which in turn impacts the trade-off [109]. For instance, species from different locations along rainfall gradients show a strong trade-off between hydraulic safety and efficiency [110].
Altitude also affects some of the xylem hydraulic properties. At high elevation, xylogenesis is limited by a low temperature, which in turn causes reduced hydraulic efficiency and hence affects hydraulic transport, limiting the longitudinal growth of Picea abies [111]. Moreover, the [(t/b)2] of plant stem xylem increases with elevation [33], which is related to increased mechanical stress (wind, snow, and ice loads) at higher elevation. Therefore, higher hydraulic efficiency of the plant xylem was found at low elevation, while higher hydraulic safety was found at high elevation [112].

5.3. Soil

Changes in soil moisture directly impact plant hydraulic transport, thereby affecting plant growth and development. In general, forests growing in relatively wet areas should be as susceptible to drought as those growing in dry environments, due to the tendency for trees to operate within narrow hydraulic safety margins, i.e., the most negative water potential experienced by plants minus the water potential leading to significant hydraulic failure [74,113]. Under drought stress, most plants have to sacrifice hydraulic efficiency for higher hydraulic safety in order to develop drought tolerance strategies that ensure proper growth [114]. Plants’ hydraulic properties are also affected by the plant’s stress history; while plants are recovering from high levels of embolism after drought by producing new xylem, which ultimately increases their hydraulic safety, they are more prone to xylem embolism during the recovery itself [115]. Under salt stress, high tensile force (low water potentials) in the xylem could create a relatively high risk of embolism for mangrove species [42]. High nitrogen availability can also increase hydraulic conductivity by promoting conduit expansion and tends to increase vulnerability to embolism [116]. Additionally, heavy metal stress also affects xylem hydraulic transport. Metals are able to decelerate short-distance water transfer both in the symplast and apoplast, which in turn reduces the movement of water into the vascular system and affects water supply to the shoot [117].
The physical properties and texture of the soil can also affect the plant xylem hydraulic trade-off. Xylem hydraulic traits are likely to be strongly affected by soil texture, which is a major determinant of both the amount of soil water available to plants and the hydraulic conductivity between soil and roots [118], thereby affecting the hydraulic safety and efficiency trade-off of plants. For example, trees growing in sandy soil show higher hydraulic safety than trees growing in more sandy soils, which may be due to the higher area of contact of the root with the soil particles [119,120] Furthermore, the depth of the soil can also affect plants’ xylem hydraulic performance. For instance, higher hydraulic efficiency was found in plants growing in shallow soils, as a result of having a bigger xylem conduit area [121].
Additionally, soil microorganisms can influence plants’ absorption and utilization of water [122]. Mycorrhiza can enhance water transport by the roots, increase the soil water content, and lower the soil temperature, thereby improving root hydraulic efficiency [123] and altering the hydraulic trade-off. Additionally, studies have shown that increasing fungal biomass can improve soil moisture conditions and plant nutrient efficiency [124]. A high content of fungal biomass may improve the physical structure and water retention of the soil [125], thereby influencing the hydraulic trade-off.
In summary, abiotic stresses in the soil, e.g., drought, salinity, and heavy metals, mainly prompt plants to increase hydraulic safety, while soil environmental conditions influence hydraulic efficiency by altering plant water absorption and utilization, thereby affecting the trade-off between plant hydraulic efficiency and safety.

6. Conclusions

We summarize different findings regarding the hydraulic safety and efficiency trade-off in plant xylem from previous research and analyze the P50 and KS and the related hydraulic traits of various species. We found a weak trade-off between hydraulic safety and efficiency in the plant xylem. At the inter-species level, ferns, gymnosperms, and angiosperms have hydraulic safety and efficiency trade-offs, and regarding angiosperms, ring-porous species have higher hydraulic efficiency than diffuse-porous species. Additionally, evergreen species have safer hydraulic strategies than deciduous species. At the intra-species level, we observed that male and female plants of dioecious species have different hydraulic features, with females being more efficient and males being safer. At the intra-individual level, hydraulic efficiency decreases and hydraulic safety increases with increasing tree height. Various factors influence the studied trade-off, including the plant xylem structure, plant habitats, temperature, rainfall, altitude, and soil environment. Given the crucial role of the xylem pit membrane in plant hydraulics, further investigations from three-dimensional perspectives, such as studying micro- and nano-sized pores, would be useful to understand the hydraulic safety and efficiency trade-off at the nanoscale.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f14091817/s1. Table S1: data for hydraulic safety and efficiency of ferns, gymnosperms, and angiosperm species; Table S2: data for hydraulic safety and efficiency of ring-porous and diffuse-porous angiosperm species; Table S3: data for hydraulic safety and efficiency of six different life types, i.e., trees, lianas, shrubs, herbaceous species, evergreens, and deciduous species; Table S4: data for hydraulic safety and efficiency of different organs (root, stem, and leaf); Table S5: data for inter-conduit pit membrane thickness and conduit diameter in xylem from various organs of different species.

Author Contributions

Conceptualization, S.L. (Shan Li) and J.W.; methodology, J.W. and Y.S.; validation, S.L. (Shan Li), S.L. (Sen Lu) and J.G.; investigation, P.L.; data curation, J.W.; writing—original draft preparation, J.W.; writing—review and editing, S.L. (Shan Li), S.L. (Sen Lu) and Y.S.; supervision, S.L. (Shan Li), Y.S. and J.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, under grant number 32001291 and 41977274, the Talent Project of Shaanxi University of Science and Technology, under grant number 126022037, the Shaanxi Province Science and Technology Innovation Team, under grant number 2022TD-09, and the Key Industrial Chain Project of Shaanxi Province, under grant number 2022ZDLNY02-02, the Research Council of Finland, under grant number 323843.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Hydraulic safety (P50) and efficiency (KS of ferns, angiosperms, and gymnosperms species. (a) Relationship between KS and P50 across all species (p < 0.05); (b) KS and P50 of ferns, angiosperms, and gymnosperms, respectively. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S1.
Figure 1. Hydraulic safety (P50) and efficiency (KS of ferns, angiosperms, and gymnosperms species. (a) Relationship between KS and P50 across all species (p < 0.05); (b) KS and P50 of ferns, angiosperms, and gymnosperms, respectively. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S1.
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Figure 2. Hydraulic safety (P50) and efficiency (KS) plots for ring-porous and diffuse-porous angiosperm species. (a) Relationship between KS and P50 in both ring-porous and diffuse-porous species (p < 0.05); (b) distributions of KS and P50 values among ring-porous and diffuse-porous species, respectively. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S2.
Figure 2. Hydraulic safety (P50) and efficiency (KS) plots for ring-porous and diffuse-porous angiosperm species. (a) Relationship between KS and P50 in both ring-porous and diffuse-porous species (p < 0.05); (b) distributions of KS and P50 values among ring-porous and diffuse-porous species, respectively. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S2.
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Figure 3. Hydraulic safety (P50) and efficiency (KS) of trees, lianas, shrubs, and herbaceous species. (a) Relationship between KS and P50 of different life type species, i.e., trees, lianas shrubs, and herbaceous species (p < 0.05); (b) KS and P50 of trees, lianas, shrubs, and herbaceous species. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S3.
Figure 3. Hydraulic safety (P50) and efficiency (KS) of trees, lianas, shrubs, and herbaceous species. (a) Relationship between KS and P50 of different life type species, i.e., trees, lianas shrubs, and herbaceous species (p < 0.05); (b) KS and P50 of trees, lianas, shrubs, and herbaceous species. Boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S3.
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Figure 4. Hydraulic safety (P50) and efficiency (KS) of evergreen and deciduous species. (a) Relationship between KS and P50 across all life type species, i.e., evergreen and deciduous (p = 0.05); (b) KS and P50 of evergreen and deciduous species, respectively. For Figure (a), the purple areas represent 95% confidence bands and the pink areas represent 95% prediction bands. For Figure (b), boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S3.
Figure 4. Hydraulic safety (P50) and efficiency (KS) of evergreen and deciduous species. (a) Relationship between KS and P50 across all life type species, i.e., evergreen and deciduous (p = 0.05); (b) KS and P50 of evergreen and deciduous species, respectively. For Figure (a), the purple areas represent 95% confidence bands and the pink areas represent 95% prediction bands. For Figure (b), boxes show the 25th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S3.
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Figure 5. Hydraulic safety (P50) and efficiency (KS) of different plant organs. (a) Correlation between KS and P50 across all organs: root, stem, and leaf (p = 0.05); (b) KS and P50 of plants’ different organs. For Figure (a), the purple areas in the figure represent 95% confidence bands and the pink areas represent 95% prediction bands. For Figure (b), boxes show the 27th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S4.
Figure 5. Hydraulic safety (P50) and efficiency (KS) of different plant organs. (a) Correlation between KS and P50 across all organs: root, stem, and leaf (p = 0.05); (b) KS and P50 of plants’ different organs. For Figure (a), the purple areas in the figure represent 95% confidence bands and the pink areas represent 95% prediction bands. For Figure (b), boxes show the 27th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S4.
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Figure 6. Distributions across the xylem of different species of conduit diameter (a) and pit thickness (b) from various organs. Boxes show the 27th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S5.
Figure 6. Distributions across the xylem of different species of conduit diameter (a) and pit thickness (b) from various organs. Boxes show the 27th to 75th percentiles, horizontal lines within boxes represent median values, horizontal lines outside of boxes represent 10th and 90th percentiles, the upward pointing triangle represents the minimum value, the downward pointing triangle represents the maximum value, and the circle represents the mean value. For raw data, see Table S5.
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Figure 7. Factors influencing species’ hydraulic safety and efficiency trade-off.
Figure 7. Factors influencing species’ hydraulic safety and efficiency trade-off.
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Table 1. Relationship (R2) established between hydraulic safety and efficiency of different species types, where linear regression was used to fit the data. Asterisks indicate levels of significance (*, p < 0.05).
Table 1. Relationship (R2) established between hydraulic safety and efficiency of different species types, where linear regression was used to fit the data. Asterisks indicate levels of significance (*, p < 0.05).
TypesR2SlopeData Source
Inter-species Table S1
ferns0.006 *0.403
gymnosperms0.393 *0.341
angiosperms0.011 *−0.448
Wood types Table S2
ring-porous0.077 *−0.926
diffuse-porous0.006 *0.279
Life types Table S3
trees0.047 *0.294
lianas0.001 *0.069
shrubs0.0010.104
herbaceous0.517 *2.031
evergreen0.004 *0.226
deciduous0.001 *0.071
Intra-tree Table S4
leaf0.029 *0.803
stem0.093 *0.624
root0.038 *2.207
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Li, S.; Wang, J.; Lu, S.; Salmon, Y.; Liu, P.; Guo, J. Trade-Off between Hydraulic Safety and Efficiency in Plant Xylem and Its Influencing Factors. Forests 2023, 14, 1817. https://doi.org/10.3390/f14091817

AMA Style

Li S, Wang J, Lu S, Salmon Y, Liu P, Guo J. Trade-Off between Hydraulic Safety and Efficiency in Plant Xylem and Its Influencing Factors. Forests. 2023; 14(9):1817. https://doi.org/10.3390/f14091817

Chicago/Turabian Style

Li, Shan, Jing Wang, Sen Lu, Yann Salmon, Peng Liu, and Junkang Guo. 2023. "Trade-Off between Hydraulic Safety and Efficiency in Plant Xylem and Its Influencing Factors" Forests 14, no. 9: 1817. https://doi.org/10.3390/f14091817

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