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Article

A Comparative Analysis of the Hydraulic Strategies of Non-Native and Native Perennial Forbs in Arid and Semiarid Areas of China

by
Yanjun Dong
1,2,
Zongshan Li
1,*,
Maierdang Keyimu
3,4,
Ying Chen
5,
Guangyao Gao
1,
Cong Wang
1 and
Xiaochun Wang
5
1
State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
3
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
4
Xinjiang Key Laboratory of Desert Plant Roots Ecology and Vegetation Restoration, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
5
Center for Ecological Research, Northeast Forestry University, Harbin 150040, China
*
Author to whom correspondence should be addressed.
Forests 2022, 13(2), 193; https://doi.org/10.3390/f13020193
Submission received: 7 November 2021 / Revised: 15 January 2022 / Accepted: 18 January 2022 / Published: 27 January 2022
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

(1) Background: Water transport systems play an important role in maintaining plant growth and development. The plasticity responses of the xylem anatomical traits of different species to the environment are different. Studies have shown that there are annual growth rings in the secondary root xylem of perennial herbaceous species. Studies on xylem anatomical traits, however, have mainly focused on woody species, with little attention given to herbaceous species. (2) Methods: We set 14 sampling sites along a rainfall gradient in arid and semiarid regions, and collected the main roots of native (Potentilla) and non-native (Medicago) perennial forbs. The xylem anatomical traits of the plant roots were obtained by paraffin section, and the relationships between the xylem traits of forbs were analyzed by a Pearson correlation. (3) Results: In the fixed measurement area (850 μm × 850 μm), the vessel number (NV) of Potentilla species was higher than that of Medicago species, while the hydraulic diameter (Dh) and mean vessel area (MVA) of Potentilla species were lower than those of Medicago species. With the increase in precipitation along the rainfall gradient, the Dh (R2 = 0.403, p = 0.03) and MVA (R2 = 0.489, p = 0.01) of Medicago species increased significantly, and NV (R2 = 0.252, p = 0.09) decreased, while the hydraulic traits of Potentilla species showed no significant trend with regard to the rainfall gradient. (4) Conclusions: The hydraulic efficiency of non-native Medicago forbs was higher than that of native Potentilla forbs, and the hydraulic safety of native Potentilla forbs was higher than that of non-native Medicago forbs. With the decrease in precipitation, the hydraulic strategies of non-native Medicago forbs changed from efficiency to safety, while native Potentilla forbs were not sensitive to variations in precipitation.

1. Introduction

Grasslands are one of the main biological communities on Earth, covering nearly 1/5 of the land surface [1]. In China, grassland is the vegetation type with the largest coverage area, and is distributed in arid and alpine areas with the most fragile ecological environment. The frequency and magnitude of drought events caused by global climate change are expected to be greater, affecting the structure and function of terrestrial ecosystems [2]. Climate change will affect water and carbon cycling, mineral cycling and the composition of the plant community, thus directly and indirectly affecting the primary productivity of grasslands [3,4]. Under the background of global climate change, the warm drought phenomenon in arid and semiarid areas of China has caused soil drought, and the natural water deficit has become an important factor limiting grassland productivity [5]. Grassland vegetation is sensitive to climate change [1], and research on the response of grassland to climate change has gradually attracted people’s attention [6,7,8]. Studies have shown that the impact of climate change on grassland biomass varies with different grassland types [9] and is different throughout the growing season [10].
Although more than half of the Earth’s land is covered by non-forest vegetation [11], vessel anatomical traits of plants are largely represented by anatomical and dendrochronological studies on trees and shrubs [12,13,14,15,16,17,18,19,20,21,22,23], with relatively few similar studies on herbaceous species [11,24,25,26,27]. Studies have shown that there are annual growth rings in the secondary root xylem of perennial herbaceous species [11,28], with wider vessels at the beginning of the growing season and narrower vessels at the end of the growing season [29]. The anatomy of herbaceous plants is of great significance to the development of herb chronology [30,31,32]. Recently, research on plasticity responses in vessel traits upon drought stress has gained importance because of frequent drought events, and there have been increasing studies focusing on the anatomical characteristics in the annual rings of plants [33,34]. The phenotypic plasticity of vessel traits enables plants to adjust their xylem structure to the water limitation experienced throughout their lifetimes [35]. The range of differences in vessel traits observed between two herbaceous species highlights the plasticity of hydraulic and vessel structures [36].
Plant xylem is prone to vessel embolism that blocks the process of water transport inside a conduit under drought stress [37], which could exert an adverse impact on the growth and development of the plant [38]. Severe water stress may cause the collapse of plant hydraulic systems, eventually causing plant death [39]. The increased level of embolism resistance, therefore, is one of the most important adaptations for plant survival under drought stress. The sensitivity of plants to embolism is determined by many anatomical traits, such as the thickness of intervessel pit membranes [40], vessel diameter [41] and mechanical characters [42], of which vessel diameter is directly related to embolism resistance [41]. It is generally believed that narrow xylem vessels have higher resistance to cavitation, but lower hydraulic conductivity than wide vessels [41], whereas wide vessels contribute to high hydraulic conductivity, but are vulnerable to hydraulic failure caused by gas embolism that forms under negative water potential [37,43]. Therefore, this may lead to trade-offs between efficiency and safety [43,44]; species with high hydraulic efficiency are prone to cavitation events, giving rise to low safety, while species with low water transport efficiency are safer and more resistant to embolism [45]. Differences in vessel plasticity responses and adaptation strategies between different species are necessary for exploring the plastic ability to adapt to climate change.
Medicago is a perennial deep-rooted forage introduced in arid and semiarid areas. Potentilla is a good ecological restoration species in this area that can adapt to different geological soils. The species of these two genera are sensitive to climate change and are often used in anatomical studies [28,46]. Previous studies have related the annual ring structures of plant roots [28], leaf anatomical structures [46,47] and the plasticity response of anatomical features to climate change [35,48]. It is not yet understood how the xylem anatomical features of the two genera respond to precipitation or what the differences are in xylem anatomical structure between non-native and native forbs.
In this study, we set eight sampling sites along a rainfall gradient in arid and semiarid regions of China and collected the main roots of Medicago and Potentilla forbs. We used the paraffin section method to obtain the vessel anatomical traits (vessel number, vessel fraction, vessel area, hydraulic conductivity and hydraulic diameter). Our aims were (1) to compare the differences in vessel anatomical traits between non-native and native forbs; (2) to examine the variation in vessel anatomical traits of non-native and native forbs along the precipitation gradient; (3) to explore the hydraulic strategies of non-native and native forbs growing in arid and semiarid regions.

2. Materials and Methods

2.1. Study Area and Field Sampling

In this study, samples were collected annually in arid and semiarid regions of China in July and August from 2017 to 2020. To avoid the influence of plant size on vessel size, healthy, mature and similar-sized Medicago and Potentilla forbs were carefully sampled. The average annual precipitation ranged from 230 mm to 500 mm, the average annual temperature ranged from −2.08 °C to 8.2 °C and the altitude ranged from 275 m to 1526 m in the entire sampling area (Table 1). Climate data from 1981 to 2019 were obtained from the China Meteorological Information Center (http://data.cma.cn/, accessed on 3 June 2021). A total of 120 healthy Medicago and Potentilla forbs (5 per species) were sampled (Table 1). Main roots of forbs were collected from approximately 3–10 cm beneath the ground surface and placed into FAA fixation solution (70% ethanol: 35–40% formaldehyde: acetic acid = 90:5:5) for preservation. They belong to the taproot system with obvious distinctions between main roots and lateral roots (Figure 1).

2.2. Experimental Procedure

The collected samples were made into sections according to the paraffin section method [49]. With a Leica RM2245 rotary microtome (Leica, Heidelberg, Germany), the 8–12 μm thick sections were obtained. Safranine and Fast Green were used for double dyeing. Finally, the samples were observed and photographed with the same magnification (×40) under an Olympus DP73 light microscope (Olympus, Tokyo, Japan) after sealing on the slides with neutral balsam.

2.3. Data Processing and Statistical Analysis

The ImageJ program (http://rsb.info.nih.gov/ij/index.html, accessed on 11 May 2021) was used to analyze the images. To reduce the effects of different ages on the results, an analyzed area (850 μm × 850 μm) was selected from the xylem periphery (close to the periderm), and the percentage of parenchyma rays in the fixed area should be equal to the percentage of parenchyma rays in each cross-section (Figure 2). Vessel number (NV), mean vessel area (MVA, μm2), major and minor axis of the cross-section of each vessel and vessel fraction (VF, %) were measured. The vessel fraction was determined as the ratio of the total vessel area to the measured area. Annual rings were analyzed by recognizing earlywood and latewood in root xylem [50]. Plant age was determined by counting the number of annual rings in the digital images [35] (Figure 3). Since the cross-sections of vessels are mostly elliptical, the diameter of the vessel lumen was calculated as follows:
D = [3(ab)3/(2a2 + 2b2)]1/4,
where a and b are the major and minor axis dimensions, respectively [51]. According to the Hagen–Poiseuille law [37], the potential hydraulic conductivity (Kh, kg m MPa−1 s−1) was calculated as follows:
Kh = ( π ρ 128 η ) ∑ i = 1 n ( D i ) 4 ,
where ρ   is the density of water (998.2 kg m−3) and η is the viscosity of water at 20 °C (1.002 × 10−9 MPa s). The hydraulic diameter (Dh, μm) [52] was calculated as follows:
Dh = ∑ i = 1 n ( D i ) 5 / ∑ i = 1 n ( D i ) 4 .
The formula for calculating plasticity index is as follows:
PI = 1 − x/X,
where x is the minimum mean value and X is the maximum mean value [53].
To increase the normality of the distributions, the original data were log10-transformed [54]. Pearson correlations were used to analyze the relationship between precipitation and vessel anatomical and hydraulic traits, as well as the relationship between vessel area and vessel number.

3. Results

3.1. Vessel Anatomical Traits of Non-Native and Native Forbs

By comparing the root vessel structure of Medicago and Potentilla forbs (Figure 4), we found that there were few differences in their age, vessel fraction (VF) and the potential hydraulic conductivity (Kh). The average ages of the Medicago and Potentilla forbs were (5 ± 2.29) years and (7 ± 2.61) years, respectively; the average vessel fractions were (7.50 ± 3.04)% and (8.61 ± 3.57)% and the average potential hydraulic conductivities were (165.11 ± 102.05) kg m MPa−1 s−1 and (106.51 ± 81.82) kg m MPa−1 s−1, respectively. In the fixed measurement area, the average vessel number (NV) of Potentilla (147 ± 35.06) was higher than that of Medicago (86 ± 31.97), while the mean vessel area (MVA) and hydraulic diameter (Dh) of Potentilla were lower than those of Medicago.
The ranked order of the plasticity index (PI) of root vessel anatomical traits of Medicago was as follows: Kh > MVA > VF > NV > Dh. The ranked order of the PI of root vessel anatomical traits of Potentilla was as follows: Kh > VF > MVA > NV > Dh (Table 2). The plasticity index of all vessel anatomical traits of Medicago species was higher than that of Potentilla species.

3.2. Correlations of the Major Hydraulic Traits of Non-Native and Native Forbs

There were negative correlations between NV and MVA, and Dh in Medicago species, but these correlations were not significant, while there were no correlations between NV and MVA, and Dh in Potentilla (Figure 5a,c). In contrast to Medicago, there was a positive correlation between NV and Kh in Potentilla, but it was not significant (Figure 5b). The correlations between VF and hydraulic traits (MVA, Kh and Dh) reached the extremely significant level in both Medicago and Potentilla species (Figure 5d–f).

3.3. Variation in Vessel Anatomical Traits of Non-Native and Native Forbs along a Precipitation Gradient

With the increase in precipitation, there were no significant changes in NV and VF for the Medicago species (Figure 6b,c), but there were significant uptrends in age (Figure 6a). There were significant positive correlations between precipitation and MVA (r = 0.699, p < 0.05), and Dh (r = 0.635, p < 0.05) in Medicago species (Figure 6d,f). Precipitation was positively correlated with Kh in Medicago, but not significantly (Figure 6e). On the rainfall gradient, the age and all xylem anatomical traits of Potentilla species had a stable fluctuation without notable changing trends (Figure 6).

4. Discussion

4.1. Differences in Xylem Features and Plasticity between Native and Non-Native Forbs

The xylem anatomical features of perennial forbs varied from species to species, which was consistent with the observations of xylem anatomical structures in other regions [55,56]. In this study, there were notable differences in the vessel anatomical traits between native Potentilla forbs and non-native Medicago forbs. The vessel size (MVA and Dh) of Medicago was larger than that of Potentilla (Figure 4d,f). Studies have shown that most leguminous plants have relatively wide vessels compared with other forbs, which allows leguminous plants to have a higher growth rate and larger root systems [57]. The NV of Potentilla is significantly higher than that of Medicago (Figure 4b), and there is no difference in Kh and VF between the two genera (Figure 4e), which may suggest that Potentilla forbs compensate for the small vessels with more vessels to ensure the required water transport.
Under stress conditions, the xylem pressure becomes more negative, which increases the risk of xylem embolism [43]. Embolisms could then spread from gas-filled conduits to adjacent water-filled conduits through interconduit pit membranes, a process known as air-seeding [58]. The larger a conduit’s diameter is, the larger the pitted area will be, which will reduce the resistance of end walls and improve hydraulic efficiency, but give rise to vulnerability to cavitation [59]. A high vessel density contributes to hydraulic safety by leaving a larger proportion of vessels functional when cavitation occurs [60,61]. Moreover, intervessel pit characters also seem to play a role in ensuring hydraulic safety [40]. The larger vessel size in Medicago means that non-native Medicago forbs have higher hydraulic efficiency, while the smaller vessel size and more vessels in Potentilla mean that native Potentilla forbs may have higher hydraulic safety. Additionally, some studies have reported that compared with native grassland, Medicago grassland can strongly deplete deep soil water, even to the degree of desiccation in deeper soil layers, which eventually results in serious degradation of alfalfa grassland [62,63]. Therefore, more suitable native species should be selected in ecological restoration programs [57].
The evolution of plants in heterogeneous environments may lead to adaptation to a wide range of environments, and phenotypic plasticity plays an important role in this adaptation [64]. The plasticity index can reflect the ability of plants to overcome heterogeneous environments, and species with high plasticity often have extensive tolerance to different environmental conditions [64]. The xylem anatomical traits of plants with strong resilience often have good plasticity. The plasticity indexes of xylem anatomical traits in Medicago were higher than those of Potentilla (Table 2), which may suggest that Medicago forbs have a wider range of adaptation to the environment. The greater plasticity of key traits can promote an organism’s establishment in a short time [65], which corresponds with greater plasticity of xylem traits in non-native Medicago forbs.

4.2. Differences in the Relationship between Vessel Traits of Non-Native and Native Forbs

There was a negative correlation between NV and MVA in Medicago (Figure 5a), which was consistent with the hypothesis of a trade-off between hydraulic efficiency and safety [43]. The size and number of vessels are related to the efficiency and safety of water transport. To ensure the efficiency and safety of water transport, there is usually a trade-off between the size and number of vessels [43]. Small vessels and many vessels are not prone to embolism under drought stress and have high hydraulic safety; large vessels and few vessels have high water transport efficiency, but they are more prone to embolism [66,67]. However, there was no similar trade-off relationship in Potentilla species (Figure 5a), and a positive correlation between NV and Kh (Figure 5b), which may indicate that Potentilla species can improve hydraulic efficiency while maintaining a high level of hydraulic safety. The significant positive correlations between VF and MVA, and Kh of Potentilla were higher than those of Medicago (Figure 5d,e), which may be related to the fact that there was almost no trade-off relationship between the vessel number and size in Potentilla.
The trade-off between efficiency and safety is not only related to xylem structures, but also affected by the plant growth environment. If plants grow in soil with high moisture, there is no need to reduce hydraulic efficiency to ensure safety. On the contrary, if the root system is seriously subjected to water stress, it is necessary to improve the hydraulic safety to ensure normal water transport [68]. However, some studies have also shown that the trade-off between efficiency and safety is independent of the moisture status of the plant growth environment [69]. Therefore, the trade-off between xylem efficiency and safety may be affected by many factors and is likely to be species-specific.

4.3. Response Differences of Vessel Traits of Non-Native and Native Forbs to Precipitation

Precipitation is one of the important factors influencing plant growth, particularly in arid and semiarid areas [70]. For Medicago forbs, precipitation was positively correlated with hydraulic traits (MVA, Kh and Dh) (Figure 6d–f), indicating that Medicago species may improve hydraulic efficiency in areas with more precipitation and ensure hydraulic safety to survive in areas with less precipitation. Species’ embolism resistance would vary with the degree of drought the species experienced; species in water-limited environments are more cavitation-resistant than plants in good water conditions [71]. García-Cervigón et al. [72] studied the variation in xylem traits of Embothrium coccineum along the precipitation gradient, and results showed that the hydraulic diameter decreased significantly, the vessel density increased significantly, but the vessel fraction did not change significantly from wet sites to dry sites. Boughalleb et al. [73] designed a water control experiment to study the effects of water deficit on Astragalus gombiformis Pomel., and the results showed that the vessel diameter of root xylem decreased and the vessel density increased under water deficit, which was consistent with the results of our study. Quercus canariensis in the Mediterranean region responded to water stress by reducing the vessel area and increasing the vessel density [12], which was consistent with the results of this paper. There was no correlation between the xylem anatomical features of Potentilla and precipitation, which may suggest that precipitation has little effect on the hydraulic strategies of Potentilla. Some studies have reported that introduced species were more sensitive to climatic factors than native species [57,74], which was consistent with our results. Other climatic factors such as temperature may also affect xylem features [25,75]. More studies are needed to reveal the response mechanism of xylem traits of Potentilla to other abiotic and maybe biotic factors.

5. Conclusions

Our study revealed the hydraulic strategies to cope with precipitation of native and non-native forbs in arid and semiarid areas of China by comparing their xylem anatomical traits. Our results showed that there were notable differences in xylem anatomical traits between native Potentilla and non-native Medicago forbs in arid and semiarid areas of China. The water transport system of native Potentilla forbs, built of higher vessel number, and smaller vessel size, contrasts with that of non-native Medicago forbs and is expected to be safer. Because vessel traits are only part of the plant system, other anatomical and functional traits have to be studied to verify these results. There was a trade-off between safety and efficiency in the xylem of Medicago forbs, while there was no similar trade-off relationship in Potentilla species. The plasticity of vessel traits in non-native forbs was greater, which gave Medicago forbs higher hydraulic efficiency in areas with more precipitation and higher hydraulic safety in areas with less precipitation, whereas native Potentilla forbs were not sensitive to variation in precipitation. Further research is needed to explore the effects of other abiotic and maybe biotic factors on the hydraulic strategies and growth of perennial herbs in arid and semiarid areas of China.

Author Contributions

Conceptualization, Y.D. and Z.L.; methodology, Z.L. and X.W.; software, Y.D.; investigation, Y.D., Z.L., M.K., Y.C., G.G. and C.W.; data curation, Y.D.; writing—original draft preparation, Y.D.; writing—review and editing, Y.D. and M.K.; supervision, Z.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Major Program of National Natural Science Foundation of China (41991233) and National Natural Science Foundation of China (41877539, 42101104).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available yet due to the authors are writing some other papers by excavating these data.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript or in the decision to publish the results.

References

  1. Zavaleta, E.S.; Shaw, M.R.; Chiariello, N.R.; Thomas, B.D.; Cleland, E.E.; Field, C.B.; Mooney, H.A. Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol. Monogr. 2003, 73, 585–604. [Google Scholar] [CrossRef]
  2. Easterling, D.R. Climate extremes: Observations, modelling, and impacts. Science 2000, 289, 2068–2074. [Google Scholar] [CrossRef] [PubMed]
  3. Brookshire, E.N.J.; Weaver, T. Long-term decline in grassland productivity driven by increasing dryness. Nat. Commun. 2015, 6, 7148. [Google Scholar] [CrossRef]
  4. Liu, H.Y.; Mi, Z.R.; Lin, L.; Wang, Y.H.; Zhang, Z.H.; Zhang, F.W.; Wang, H.; Liu, L.L.; Zhu, B.; Cao, G.M.; et al. Shifting plant species composition in response to climate change stabilizes grassland primary production. Proc. Natl. Acad. Sci. USA 2018, 115, 4051–4056. [Google Scholar] [CrossRef]
  5. Knapp, A.K.; Briggs, J.M.; Koelliker, J.K. Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems 2001, 4, 19–28. [Google Scholar] [CrossRef]
  6. Gao, Q.Z.; Zhu, W.Q.; Schwartz, M.W.; Ganjurjav, H.; Wan, Y.F.; Qin, X.B.; Ma, X.; Williamson, M.A.; Li, Y. Climatic change controls productivity variation in global grasslands. Sci. Rep. 2016, 6, 26958. [Google Scholar] [CrossRef] [PubMed]
  7. Grime, J.P.; Brown, V.K.; Thompson, K.; Masters, G.J.; Hillier, S.H.; Clarke, I.P.; Askew, A.P.; Corker, D.; Kielty, J.P. The response of two contrasting limestone grasslands to simulated climate change. Science 2000, 289, 762–765. [Google Scholar] [CrossRef]
  8. White, S.R.; Carlyle, C.N.; Fraser, L.H.; Cahill, J.F. Climate change experiments in temperate grasslands: Synthesis and future directions. Biol. Lett. 2012, 8, 484–487. [Google Scholar] [CrossRef]
  9. Ma, W.H.; Fang, J.Y.; Yang, Y.H.; Mohammat, A. Biomass carbon stocks and their changes in northern China’s grasslands during 1982–2006. Sci. China Life Sci. 2010, 53, 841–850. [Google Scholar] [CrossRef]
  10. Ma, W.H.; Liu, Z.L.; Wang, Z.H.; Wang, W.; Liang, C.Z.; Tang, Y.H.; He, J.S.; Fang, J.Y. Climate change alters interannual variation of grassland aboveground productivity: Evidence from a 22-year measurement series in the Inner Mongolian grassland. J. Plant Res. 2010, 123, 509–517. [Google Scholar] [CrossRef]
  11. Büntgen, U.; Psomas, A.; Schweingruber, F.H. Introducing wood anatomical and dendrochronological aspects of herbaceous plants: Applications of the Xylem Database to vegetation science. J. Veg. Sci. 2014, 25, 967–977. [Google Scholar] [CrossRef]
  12. Gea-Izquierdo, G.; Fonti, P.; Cherubini, P.; Martín-Benito, D.; Chaar, H.; Caellas, I. Xylem hydraulic adjustment and growth response of Quercus canariensis Willd. to climatic variability. Tree Physiol. 2012, 32, 401–413. [Google Scholar] [CrossRef]
  13. Martínez-Sancho, E.; Dorado-Lián, I.; Heinrich, I.; Helle, G.; Menzel, A. Xylem adjustment of sessile oak at its southern distribution limits. Tree Physiol. 2017, 37, 903–914. [Google Scholar] [CrossRef] [PubMed]
  14. Pérez-de-Lis, G.; Rozas, V.; Vázquez-Ruiz, R.A.; García-González, I. Do ring-porous oaks prioritize earlywood vessel efficiency over safety? Environmental effects on vessel diameter and tyloses formation. Agric. For. Meteorol. 2018, 248, 205–214. [Google Scholar] [CrossRef]
  15. Hallinger, M.; Manthey, M.; Wilmking, M. Establishing a missing link: Warm summers and winter snow cover promote shrub expansion into alpine tundra in Scandinavia. New Phytol. 2010, 186, 890–899. [Google Scholar] [CrossRef]
  16. Schweingruber, F.H.; Hellmann, L.; Tegel, W.; Braun, S.; Nievergelt, D.; Büntgen, U. Evaluating the wood anatomical and dendroecological potential of Arctic dwarf shrubs communities. IAWA J. 2013, 34, 485–497. [Google Scholar] [CrossRef]
  17. Buras, A.; Lehejček, J.; Michalová, Z.; Morrissey, R.C.; Svoboda, M.; Wilmking, M. Shrubs shed light on 20th century Greenland Ice Sheet melting. Boreas 2017, 46, 667–677. [Google Scholar] [CrossRef]
  18. Unterholzner, L.; Carrer, M.; Bär, A.; Beikircher, B.; Dämon, B.; Losso, A.; Prendin, A.L.; Mayr, S. Juniperus communis populations exhibit low variability in hydraulic safety and efficiency. Tree Physiol. 2020, 40, 1668–1679. [Google Scholar] [CrossRef]
  19. Rodríguez-Ramírez, E.C.; Vázquez-García, J.A.; García-González, I.; Alcántara-Ayala, O.; Luna-Vega, I. Drought effects on the plasticity in vessel traits of two endemic Magnolia species in the tropical montane cloud forests of eastern Mexico. J. Plant Ecol. 2020, 13, 331–340. [Google Scholar] [CrossRef]
  20. Rodríguez-Ramírez, E.C.; Valdez-Nieto, J.A.; Vázquez-García, J.A.; Dieringer, G.; Luna-Vega, I. Plastic responses of Magnolia schiedeana Schltdl., a relict-endangered Mexican Cloud Forest tree, to climatic events: Evidences from leaf venation and wood vessel anatomy. Forests 2020, 11, 737. [Google Scholar] [CrossRef]
  21. Zhang, H.X.; Yuan, F.H.; Wu, J.B.; Jin, C.J.; Pivovaroff, A.L.; Tian, J.Y.; Li, W.B.; Guan, D.X.; Wang, A.Z.; McDowell, N.G. Responses of functional traits to seven-year nitrogen addition in two tree species: Coordination of hydraulics, gas exchange and carbon reserves. Tree Physiol. 2021, 41, 190–205. [Google Scholar] [CrossRef] [PubMed]
  22. Ganthaler, A.; Mayr, S. Subalpine dwarf shrubs differ in vulnerability to xylem cavitation: An innovative staining approach enables new insights. Physiol. Plantarum 2021, 172, 2011–2021. [Google Scholar] [CrossRef] [PubMed]
  23. García-Cervigón, A.I.; García-López, M.A.; Pistón, N.; Pugnaire, F.I.; Olano, J.M. Co-ordination between xylem anatomy, plant architecture and leaf functional traits in response to abiotic and biotic drivers in a nurse cushion plant. Ann. Bot. 2021, 127, 919–929. [Google Scholar] [CrossRef]
  24. Schweingruber, F.H.; Dietz, H. Annual rings in the xylem of dwarf shrubs and perennial dicotyledonous herbs. Dendrochronologia 2001, 19, 115–126. [Google Scholar]
  25. Olano, J.M.; Almería, I.; Eugenio, M.; von Arx, G.; Tjoelker, M. Under pressure: How a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints. Funct. Ecol. 2013, 27, 1295–1303. [Google Scholar] [CrossRef]
  26. Dee, J.R.; Palmer, M.W. Application of herb-chronology: Annual fertilization and climate reveal annual ring signatures within the roots of U.S. tallgrass prairie plants. Botany 2016, 94, 277–288. [Google Scholar] [CrossRef]
  27. Hummel, I.; Vile, D.; Violle, C.; Devaux, J.; Ricci, B.; Blanchard, A.; Garnier, E.; Roumet, C. Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species. New Phytol. 2007, 173, 313–321. [Google Scholar] [CrossRef]
  28. Dietz, H.; Fattorini, M. Comparative analysis of growth rings in perennial forbs grown in an alpine restoration experiment. Ann. Bot. 2002, 90, 663–668. [Google Scholar] [CrossRef]
  29. Dietz, H.; von Arx, G.; Dietz, S. Growth increment patterns in the roots of two alpine forbs growing in the center and at the periphery of a snowbank. Arct. Antarct. Alp. Res. 2004, 36, 591–597. [Google Scholar] [CrossRef]
  30. Schweingruber, F.H.; Büntgen, U. What is ‘wood’—An anatomical re-definition. Dendrochronologia 2013, 31, 187–191. [Google Scholar] [CrossRef]
  31. Dietz, H.; von Arx, G. Climatic fluctuation causes large-scale synchronous variation in radial root increments of perennial forbs. Ecology 2005, 86, 327–333. [Google Scholar] [CrossRef]
  32. Dee, J.R.; Stambaugh, M.C. A new approach towards climate monitoring in Rocky Mountain alpine plant communities: A case study using herb-chronology and Penstemon whippleanus. Arct. Antarct. Alp. Res. 2019, 51, 84–95. [Google Scholar] [CrossRef]
  33. Fonti, P.; von Arx, G.; García-González, I.; Eilmann, B.; Sass-Klaassen, U.; Gärtner, H.; Eckstein, D. Studying global change through investigation of the plastic responses of xylem anatomy in tree rings research. New Phytol. 2010, 185, 42–53. [Google Scholar] [CrossRef] [PubMed]
  34. Venegas-González, A.; Chagas, M.P.; Anholetto Júnior, C.R.; Alvares, C.A.; Roig, F.A.; Tomazello Filho, M. Sensitivity of tree ring growth to local and large-scale climate variability in a region of southeastern Brazil. Theor. Appl. Climatol. 2016, 123, 233–245. [Google Scholar] [CrossRef]
  35. von Arx, G.; Archer, S.R.; Hughes, M.K. Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture. Ann. Bot. 2012, 109, 1091–1100. [Google Scholar] [CrossRef]
  36. Castagneri, D.; Carrer, M.; Regev, L.; Boaretto, E. Precipitation variability differently affects radial growth, xylem traits and ring porosity of three Mediterranean oak species at xeric and mesic sites. Sci. Total Environ. 2020, 699, 134285. [Google Scholar] [CrossRef]
  37. Tyree, M.T.; Ewers, F.W. The hydraulic architecture of trees and other woody plants. New Phytol. 1991, 119, 345–360. [Google Scholar] [CrossRef]
  38. Choat, B.; Jansen, S.; Brodribb, T.J.; Cochard, H.; Delzon, S.; Bhaskar, R.; Bucci, S.J.; Feild, T.S.; Gleason, S.M.; Hacke, U.G.; et al. Global convergence in thevulnerability of forests to drought. Nature 2012, 491, 752–755. [Google Scholar] [CrossRef]
  39. McDowell, N.G. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 2011, 155, 1051–1059. [Google Scholar] [CrossRef]
  40. Schmitz, N.; Jansen, S.; Verheyden, A.; Kairo, J.G.; Beeckman, H.; Koedam, N. Comparative anatomy of intervessel pits in two mangrove species growing along a natural salinity gradient in Gazi Bay, Kenya. Ann. Bot. 2007, 100, 271–281. [Google Scholar] [CrossRef]
  41. Cochard, H.; Tyree, M.T. Xylem dysfunction in Quercus: Vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol. 1990, 6, 393–407. [Google Scholar] [CrossRef] [PubMed]
  42. Hacke, U.G.; Sperry, J.S.; Pockman, W.T.; Davis, S.D.; McCulloh, K.A. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 2001, 126, 457–461. [Google Scholar] [CrossRef] [PubMed]
  43. Sperry, J.S.; Meinzer, F.C.; Mcculloh, K.A. Safety and efficiency conflicts in hydraulic architecture: Scaling from tissues to trees. Plant Cell Environ. 2008, 31, 632–645. [Google Scholar] [CrossRef] [PubMed]
  44. Hacke, U.G.; Jacobsen, A.L.; Pratt, R.B. Xylem function of arid-land shrubs from California, USA: An ecological and evolutionary analysis. Plant Cell Environ. 2009, 32, 1324–1333. [Google Scholar] [CrossRef]
  45. Hacke, U.G.; Sperry, J.S.; Wheeler, J.K.; Castro, L. Scaling of angiosperm xylem structure with safety and eficiency. Tree Physiol. 2006, 26, 89–701. [Google Scholar] [CrossRef]
  46. Kołodziejek, J.; Glińska, S.; Michlewska, S. Seasonal leaf dimorphism in Potentilla argentea L. var. tenuiloba (Jord.) Sw. (Rosaceae). Acta Bot. Croat. 2015, 74, 53–70. [Google Scholar] [CrossRef][Green Version]
  47. Munir, M.; Khan, M.A.; Ahmad, M.; Abbasi, A.M.; Zafar, M.; Khan, K.Y.; Tariq, K.; Tabassum, S.; Ahmed, S.N.; Habiba, U.; et al. Taxonomic potential of foliar epidermal anatomy among the wild culinary vegetables of Pakistan. J. Med. Plants Res. 2011, 5, 2857–2862. [Google Scholar]
  48. Liu, W.S.; Zheng, L.; Qi, D.H. Variation in leaf traits at different altitudes reflects the adaptive strategy of plants to environmental changes. Ecol. Evol. 2020, 10, 8166–8175. [Google Scholar] [CrossRef]
  49. Purnobasuki, H.; Nurhidayati, T.; Hariyanto, S.; Jadid, N. Data of root anatomical responses to periodic waterlogging stress of tobacco (Nicotiana tabacum) varieties. Data Brief 2018, 20, 2012–2016. [Google Scholar] [CrossRef]
  50. von Arx, G.; Dietz, H. Growth rings in the roots of temperate forbs are robust annual markers. Plant Biol. 2006, 8, 224–233. [Google Scholar] [CrossRef]
  51. Lewis, A.M.; Boose, E.R. Estimating volume flow rates through xylem conduits. Am. J. Bot. 1995, 82, 1112–1116. [Google Scholar] [CrossRef]
  52. Sperry, J.S.; Nichols, K.L. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of Northern Utah and Interior Alaska. Ecology 1994, 75, 1736–1752. [Google Scholar] [CrossRef]
  53. Ashton, P.M.S.; Olander, L.P.; Berlyn, G.P.; Thadani, R.; Cameron, I.R. Changes in leaf structure in relation to crown position and tree size of Betula papyrifera within fire-origin stands of interior cedar-hemlock. Can. J. Bot. 1998, 76, 1180–1187. [Google Scholar]
  54. Kerkhoff, A.J.; Enquist, B.J. Multiplicative by nature: Why logarithmic transformation is necessary in allometry. J. Theor. Biol. 2009, 257, 519–521. [Google Scholar] [CrossRef]
  55. Liu, Y.B.; Zhang, Q.B. Growth rings of roots in perennial forbs in Duolun Grassland, Inner Mongolia, China. J. Integr. Plant Biol. 2007, 49, 144–149. [Google Scholar] [CrossRef]
  56. Dietz, H.; Schweingruber, F.H. Annual rings in native and introduced forbs of lower Michigan, USA. Can. J. Bot. 2002, 80, 642–649. [Google Scholar] [CrossRef]
  57. Shi, S.L.; Li, Z.S.; Wang, H.; von Arx, G.; Lü, Y.H.; Wu, X.; Wang, X.C.; Liu, G.H.; Fu, B.J. Roots of forbs sense climate fluctuations in the semi-arid Loess Plateau: Herb-chronology based analysis. Sci. Rep. 2016, 6, 28435. [Google Scholar] [CrossRef]
  58. Brodribb, T.J.; Bowman, D.; Nichols, S.; Delzon, S.; Burlett, R. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol. 2010, 188, 533–542. [Google Scholar] [CrossRef]
  59. Sperry, J.S.; Hacke, U.W.; Wheeler, J.K. Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ. 2005, 28, 456–465. [Google Scholar] [CrossRef]
  60. Schmitz, N.; Verheyden, A.; Beeckman, H.; Kairo, J.G.; Koedam, N. Influence of a salinity gradient on the vessel characters of the mangrove species Rhizophora mucronata. Ann. Bot. 2006, 98, 1321–1330. [Google Scholar] [CrossRef]
  61. Verheyden, A.; De Ridder, F.; Schmitz, N.; Beeckman, H.; Koedam, N. High-resolution time series of vessel density in Kenyan mangrove trees reveal a link with climate. New Phytol. 2005, 167, 425–435. [Google Scholar] [CrossRef] [PubMed]
  62. Yang, L.; Wei, W.; Chen, L.D.; Mo, B.R. Response of deep soil moisture to land use and afforestation in the semi-arid Loess Plateau, China. J. Hydrol. 2012, 475, 111–122. [Google Scholar] [CrossRef]
  63. Liu, B.X.; Shao, M.A. Modeling soil-water dynamics and soil-water carrying capacity for vegetation on the Loess Plateau, China. Agric. Water Manag. 2015, 159, 176–184. [Google Scholar] [CrossRef]
  64. Abrams, M.D.; Kubiske, M.E.; Mostoller, S.A. Relating wet and dry year ecophysiology to leaf structure in contrasting temperate tree species. Ecology 1994, 75, 123–133. [Google Scholar] [CrossRef]
  65. Nicotra, A.B.; Davidson, A. Adaptive phenotypic plasticity and plant water use. Funct. Plant Biol. 2010, 37, 117–127. [Google Scholar] [CrossRef]
  66. Zimmermann, M.H. Hydraulic architecture of some diffuse-porous trees. Can. J. Bot. 1978, 56, 2286–2295. [Google Scholar] [CrossRef]
  67. Yáñez-Espinosa, L.; Terrazas, T.; López-Mata, L. Effects of flooding on wood and bark anatomy of four species in a mangrove forest community. Trees 2001, 15, 91–97. [Google Scholar] [CrossRef]
  68. Cochard, H. Vulnerability of several conifers to air embolism. Tree Physiol. 1992, 11, 73–83. [Google Scholar] [CrossRef]
  69. Kavanagh, K.L.; Bond, B.J.; Aitken, S.N.; Gartner, B.L.; Knowe, S. Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. Tree Physiol. 1999, 19, 31–37. [Google Scholar] [CrossRef]
  70. Wilcox, K.R.; von Fischer, J.C.; Muscha, J.M.; Petersen, M.K.; Knapp, A.K. Contrasting above- and belowground sensitivity of three Great Plains grasslands to altered rainfall regimes. Glob. Chang. Biol. 2015, 21, 335–344. [Google Scholar] [CrossRef]
  71. Pockman, W.T.; Sperry, J.S. Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. Am. J. Bot. 2000, 89, 1287–1299. [Google Scholar] [CrossRef]
  72. García-Cervigón, A.I.; Olano, J.M.; von Arx, G.; Fajardo, A. Xylem adjusts to maintain efficiency across a steep precipitation gradient in two coexisting generalist species. Ann. Bot. 2018, 122, 461–472. [Google Scholar] [CrossRef] [PubMed]
  73. Boughalleb, F.; Abdellaoui, R.; Ben-Brahim, N.; Neffati, M. Anatomical adaptations of Astragalus gombiformis Pomel. under drought stress. Cent. Eur. J. Biol. 2014, 9, 1215–1225. [Google Scholar] [CrossRef]
  74. Williams, A.L.; Wills, K.E.; Janes, J.K.; Schoor, J.; Newton, P.; Hovenden, M.J. Warming and free-air CO2 enrichment alter demographics in four co-occurring grassland species. New Phytol. 2007, 176, 365–374. [Google Scholar] [CrossRef] [PubMed]
  75. Zhu, L.J.; Liu, S.J.; Arzac, A.; Cooper, D.J.; Jin, Y.; Yuan, D.Y.; Zhu, Y.; Zhang, X.; Li, Z.S.; Zhang, Y.D.; et al. Different response of earlywood vessel features of Fraxinus mandshurica to rapid warming in warm-dry and cold-wet areas. Agric. For. Meteorol. 2021, 307, 108523. [Google Scholar] [CrossRef]
Forests 13 00193 g001
Figure 1. The picture of the research material (Potentilla tanacetifolia). The yellow box indicates the intercepted part.
Figure 1. The picture of the research material (Potentilla tanacetifolia). The yellow box indicates the intercepted part.
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Figure 2. Root cross-section of Potentilla chinensis. (a,b) Cross-section from the same individual. The percentage of parenchyma rays in root cross-section (a) is 50.96%; the percentage of parenchyma rays in the analyzed area (b) is 51.09%. Scale bars = 200 μm.
Figure 2. Root cross-section of Potentilla chinensis. (a,b) Cross-section from the same individual. The percentage of parenchyma rays in root cross-section (a) is 50.96%; the percentage of parenchyma rays in the analyzed area (b) is 51.09%. Scale bars = 200 μm.
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Figure 3. Root cross-sections of perennial forbs. (a) Potentilla chinensis; (b) Potentilla tanacetifolia; (c) Medicago falcata; (d) Medicago sativa. Yellow markers indicate annual ring boundaries. Scale bars = 200 μm.
Figure 3. Root cross-sections of perennial forbs. (a) Potentilla chinensis; (b) Potentilla tanacetifolia; (c) Medicago falcata; (d) Medicago sativa. Yellow markers indicate annual ring boundaries. Scale bars = 200 μm.
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Figure 4. Boxplot of the major hydraulic traits in secondary root xylem of non-native and native forbs in arid and semiarid areas. (a) age; (b) vessel number (NV); (c) vessel fraction (VF); (d) mean vessel area (MVA); (e) the potential hydraulic conductivity (Kh); (f) hydraulic diameter (Dh). The blue and red boxes indicate Medicago and Potentilla herbaceous species, respectively. The t-test results between Medicago and Potentilla forbs are highlighted. * p < 0.05; ** p < 0.01.
Figure 4. Boxplot of the major hydraulic traits in secondary root xylem of non-native and native forbs in arid and semiarid areas. (a) age; (b) vessel number (NV); (c) vessel fraction (VF); (d) mean vessel area (MVA); (e) the potential hydraulic conductivity (Kh); (f) hydraulic diameter (Dh). The blue and red boxes indicate Medicago and Potentilla herbaceous species, respectively. The t-test results between Medicago and Potentilla forbs are highlighted. * p < 0.05; ** p < 0.01.
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Figure 5. Correlation relationships between NV, VF and major hydraulic traits in secondary root xylem of non-native and native forbs in arid and semiarid areas. (a–c) Relationships between vessel number and hydraulic traits; (d–f) Relationships between vessel fraction and hydraulic traits. NV—vessel number; VF—vessel fraction; MVA—mean vessel area; Kh—the potential hydraulic conductivity; Dh—hydraulic diameter. The blue and red dots indicate Medicago and Potentilla herbaceous species, respectively. ** p < 0.01.
Figure 5. Correlation relationships between NV, VF and major hydraulic traits in secondary root xylem of non-native and native forbs in arid and semiarid areas. (a–c) Relationships between vessel number and hydraulic traits; (d–f) Relationships between vessel fraction and hydraulic traits. NV—vessel number; VF—vessel fraction; MVA—mean vessel area; Kh—the potential hydraulic conductivity; Dh—hydraulic diameter. The blue and red dots indicate Medicago and Potentilla herbaceous species, respectively. ** p < 0.01.
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Figure 6. The changing trends of age and the major hydraulic traits in secondary root xylem of non-native and native forbs along a precipitation gradient in arid and semiarid areas. (a) age; (b) vessel number (NV); (c) vessel fraction (VF); (d) mean vessel area (MVA); (e) the potential hydraulic conductivity (Kh); (f) hydraulic diameter (Dh). The blue and red dots indicate Medicago and Potentilla herbaceous species, respectively. * p < 0.05.
Figure 6. The changing trends of age and the major hydraulic traits in secondary root xylem of non-native and native forbs along a precipitation gradient in arid and semiarid areas. (a) age; (b) vessel number (NV); (c) vessel fraction (VF); (d) mean vessel area (MVA); (e) the potential hydraulic conductivity (Kh); (f) hydraulic diameter (Dh). The blue and red dots indicate Medicago and Potentilla herbaceous species, respectively. * p < 0.05.
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Table 1. Site characteristics of non-native and native herbaceous species in arid and semiarid areas of China.
Table 1. Site characteristics of non-native and native herbaceous species in arid and semiarid areas of China.
Site
Code		Location (Latitude N,
Longitude E)		Precipitation
(mm)		Temperature
(°C)		Elevation
(m)		SpeciesNumber of Samples
S137.10°,
108.22°		4457.801372MF, MS10
S236.65°,
108.32°		5008.201526MF, MS, ML,
MR, MM, PT		30
S344.27°,
116.53°		2821.391140MR, PT10
S443.55°,
116.67°		3211.511260MS5
S550.20°,
119.39°		357−2.08525MR5
S643.91°,
115.50°		2271.801131MR5
S745.14°,
121.53°		4045.76275MR5
S836.98°,
107.85°		4306.801405PT, PC10
S944.37°,
116.11°		2532.58938PT5
S1143.55°,
116.67°		3201.521271PT, PA, PC15
S1247.94°,
117.32°		2300.60595PT5
S1345.04°,
118.92°		3581.031015PT5
S1448.52°,
119.74°		360−1.31749PT, PA10
MF—Medicago falcata; ML—M. lupulina; MM—M. minima; MR—M. ruthenica; MS—M. sativa; PA—Potentilla acaulis; PC—P. chinensis; PT—P. tanacetifolia.
Table 2. Plasticity index (PI) of anatomical traits of non-native and native forbs.
Table 2. Plasticity index (PI) of anatomical traits of non-native and native forbs.
TraitsGenera
MedicagoPotentilla
NV0.4300.295
VF (%)0.5580.466
MVA (μm2)0.5680.430
Kh (kg m MPa−1 s−1)0.6840.697
Dh (μm)0.3640.285
PI mean0.5210.435
NV—vessel number; VF—vessel fraction; MVA—mean vessel area; Kh—the potential hydraulic conductivity; Dh—hydraulic diameter.
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Dong, Y.; Li, Z.; Keyimu, M.; Chen, Y.; Gao, G.; Wang, C.; Wang, X. A Comparative Analysis of the Hydraulic Strategies of Non-Native and Native Perennial Forbs in Arid and Semiarid Areas of China. Forests 2022, 13, 193. https://doi.org/10.3390/f13020193

AMA Style

Dong Y, Li Z, Keyimu M, Chen Y, Gao G, Wang C, Wang X. A Comparative Analysis of the Hydraulic Strategies of Non-Native and Native Perennial Forbs in Arid and Semiarid Areas of China. Forests. 2022; 13(2):193. https://doi.org/10.3390/f13020193

Chicago/Turabian Style

Dong, Yanjun, Zongshan Li, Maierdang Keyimu, Ying Chen, Guangyao Gao, Cong Wang, and Xiaochun Wang. 2022. "A Comparative Analysis of the Hydraulic Strategies of Non-Native and Native Perennial Forbs in Arid and Semiarid Areas of China" Forests 13, no. 2: 193. https://doi.org/10.3390/f13020193

APA Style

Dong, Y., Li, Z., Keyimu, M., Chen, Y., Gao, G., Wang, C., & Wang, X. (2022). A Comparative Analysis of the Hydraulic Strategies of Non-Native and Native Perennial Forbs in Arid and Semiarid Areas of China. Forests, 13(2), 193. https://doi.org/10.3390/f13020193

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