Next Article in Journal
Radiographic Imaging as a Quality Index Proxy for Brachiaria brizantha Seeds
Next Article in Special Issue
The Influence of the Partitioning of Sugars, Starch, and Free Proline in Various Organs of Cyclamen graecum on the Biology of the Species and Its Resistance to Abiotic Stressors
Previous Article in Journal
Evaluation of Chelating Agents Used in Phytoextraction by Switchgrass of Lead Contaminated Soil
Previous Article in Special Issue
Impact of Grazing on Diversity of Semi-Arid Rangelands in Crete Island in the Context of Climatic Change
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 11
Issue 8
10.3390/plants11081013
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

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

Hydraulic Response of Deciduous and Evergreen Broadleaved Shrubs, Grown on Olympus Mountain in Greece, to Vapour Pressure Deficit

by
Maria Karatassiou
1,*,
Panagiota Karaiskou
1,
Eleni Verykouki
2 and
Sophia Rhizopoulou
3
1
Laboratory of Rangeland Ecology, School of Forestry and Natural Environment, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
2
Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Fytokou St., 38446 Volos, Greece
3
Section of Botany, Department of Biology, National and Kapodistrian University of Athens, 15784 Athens, Greece
*
Author to whom correspondence should be addressed.
Plants 2022, 11(8), 1013; https://doi.org/10.3390/plants11081013
Submission received: 5 March 2022 / Revised: 30 March 2022 / Accepted: 5 April 2022 / Published: 8 April 2022
(This article belongs to the Special Issue Mediterranean Plants)
Browse Figures
Versions Notes

Abstract

:
In this study, leaf hydraulic functionality of co-occurring evergreen and deciduous shrubs, grown on Olympus Mountain, has been compared. Four evergreen species (Arbutus andrachne, Arbutus unedo, Quercus ilex and Quercus coccifera) and four deciduous species (Carpinus betulus, Cercis siliquastrum, Coronilla emeroides and Pistacia terebinthus) were selected for this study. Predawn and midday leaf water potential, transpiration, stomatal conductance, leaf temperature and leaf hydraulic conductance were estimated during the summer period. The results demonstrate different hydraulic tactics between the deciduous and evergreen shrubs. Higher hydraulic conductance and lower stomatal conductance were obtained in deciduous plants compared to the evergreens. Additionally, positive correlations were detected between water potential and transpiration in the deciduous shrubs. The seasonal leaf hydraulic conductance declined in both deciduous and evergreens under conditions of elevated vapor pressure deficit during the summer; however, at midday, leaf water potential reached comparable low values, but the deciduous shrubs exhibited higher hydraulic conductance compared to the evergreens. It seems likely that hydraulic traits of the coexisting evergreen and deciduous plants indicate water spending and saving tactics, respectively; this may also represent a limit to drought tolerance of these species grown in a natural environment, which is expected to be affected by global warming.

1. Introduction

The climate in the Mediterranean region is characterized by a prolonged summer drought period, which according to the majority of climate change scenarios, is expected to become more severe in the future [1,2,3]. Drought is the main environmental stress directly linked to plant survival, growth, competitiveness, persistence, and productivity in Mediterranean habitats that are under an increasing risk of degradation [1,4,5,6,7]. On the other hand, plants have evolved a variety of morphological and physiological tactics [8] to withstand drought stress [9,10]; these include (a) hydraulic strategies via deep, tap root systems to extract water from deep soil layers, enabling the plants to sustain elevated water potential and xylem pressure during drought and (b) morphological and physiological adaptations at the leaf level in order to reduce water loss [11,12]. The importance of the hydraulic system in water consumption has led to the hypothesis of the functional convergence in the regulation of water use among phylogenetically diverse species [13,14]. Nonetheless, few studies have been performed to characterize the differences in leaf hydraulic conductance and hydraulic status among phylogenetically different plant species, such as deciduous and evergreen shrubs, in Mediterranean habitats [15,16]. Leaf is a substantial organ for the transport of water throughout the plant and hence leaf hydraulic conductance is an important parameter to determine plant water status [15,17,18,19,20]. To the best of our knowledge, a comparative study among hydraulic characteristics at the leaf level of evergreen and deciduous species co-occurring in the same habitat, with respect to the impact of climatic stimuli on functionality, has not hitherto been published.
In order to comprehensively address differences between evergreen and deciduous plants concerning physiological responses to drought, the hydraulic and stomatal performance should be examined with well-established approaches. The water status for each individual, specific plant depends on the difference between transpiration (Ε) and water absorption (A), but it is not clear which of these factors is more important for plants’ gas exchanges in response to drought stress [12]. If the soil water shortage increases, water stress will increase over time, negatively affecting many physiological and metabolic aspects of the plants [8,21,22]. Plants close the stomatal pores to regulate water loss [12,23] through transpiration when the available soil water decreases and/or an increase in the difference between the saturation (i.e., amount of water vapor that the air can hold, namely the saturation vapor pressure) and actual vapor pressure, i.e., the Vapour Pressure Deficit (VPD), is detected.
VPD has been recognized as an important parameter for plant functionality and survival, which is influenced by the so-called hydraulic failure [24,25,26,27,28,29]. Oren et al. [30] fount in drought tolerant species a regulation of water potential (Ψ) as VPD increases and recommended different sensitivity of stomatal apparatus to VPD among different functional groups. However, Ε could either increase or decrease in response to an increased VPD [27,31]; the first response is known as “feedback” response while the second as “feed forward” response. The transpiration rate is influenced by atmospheric conditions and, over a short time-scale, is regulated by the function of stomatal apparatus [32]. It has been argued that a declining stomatal conductance (gs) concomitantly with increasing VPD would rather occur as a feedback response to E and water loss from the leaf, than as a direct response to humidity [33,34,35].
The function of the stomatal apparatus under global climate change is an essential subject in plant ecophysiological research because it affects plant growth, vegetation distribution and ecosystem function [36]. The stomatal response to VPD varies either across and within species, or within the same species [37,38,39,40]. Partial stomatal closure under elevated VPD, especially during midday, will negatively affect CO2 assimilation rate [7,41].
The movement of water in the soil–plant–atmosphere (SPA) continuum is a function of the difference between hydrostatic pressure and hydraulic conductance along this pathway. Water flows through the SPA continuum driven by a gradient in Ψ, which depends on the water flow rate and the hydraulic conductivity of the different pathways [32]. The amount of water that will be absorbed by the roots of the plants and the amount that will move from the roots to the leaves and then to the atmosphere depends mainly on gs, VPD and hydraulic conductance (K). The differences between plant species in Ψ, E and gs, determine to a greater or lesser extent the plants’ response to various water stresses [12,42,43,44,45]. However, the effects of rising VPD on vegetation and hydraulic dynamics remain poorly studied. It has been reported that significant higher leaf and stem hydraulic conductance [25,46,47] under increased irradiance are due to the regulation of aquaporins [46,47,48]. A midday decline of gs has been obtained in many plant species and has been related with variation in midday stem water status [49,50]; this aspect supports the idea that stomatal response to VPD is substantially related to the hydraulic characteristics at both the whole plant scale and the leaf level [27,51]. There is a fundamental role of hydraulics on stomatal sensitivity to VPD [27,41], while inverse and non-linear relationship between conductance and VPD have been observed [36]. The opening and closing of the stomata seem to be controlled by complex mechanisms, which include chemical and hydraulic signals from roots, to shoots and leaves [52]. In this frame, hydraulic traits could be an important factor buffering the negative impact of drought on plant function [53].
A lot of research has been devoted to understanding how plants’ hydraulic systems have evolved to accommodate survival under different environments. However, concerning old-grown, trees and shrubs the relationship between K and the response of gs to VPD has not explicitly evaluated, in situ. Despite the above-mentioned trends, species grown under the same environmental conditions may exhibit entirely different hydraulic properties [54,55]. This interspecific variation sometimes may be ascribed to different functional types, such as deciduous and evergreen [56]. Nevertheless, variation of hydraulic traits cannot only be explained by categorization of species in functional types [56,57]. Forest and shrub communities’ response to climate change are most closely related to microclimatic change and not to macroclimatic change [58,59].
In considering that the water balance (W) is expressed by the relationship W = A − Ε, it is very interesting to study whether: (1) variation of hydraulic conductance in Mediterranean shrubs during the dry summer period is reflected in the leaf phenology (i.e., evergreen vs. deciduous), and (2) changes of VPD and consequently of microclimatic conditions influence the physiological mechanism and the performance of evergreen vs. deciduous shrubs.
The main objective of this study was to compare the ability of co-existing deciduous and evergreen broadleaved shrubs grown on the Olympus Mountain to maintain their water status and control their stomatal conductance throughout the dry season, as well as to evaluate the response of deciduous and evergreen shrubs to enhanced vapor pressure deficit. It is likely that hydraulic responses of co-occurring deciduous and evergreen shrubs, which are to some extent linked to water exploitation and effectiveness of plants’ life forms during a period of soil drying, have not been reported.

2. Results

2.1. Climatic Conditions

The seasonal pattern of VPD during the experimental period is given in Figure 1. Overall, predawn vapour pressure deficit (VPDp) was significantly lower (p < 0.05) than midday vapour pressure deficit (VPDm), except from the first measurement (mid-May) (p ≥ 0.05). Predawn VPDp ranged from 0.769 ± 0.019 kPa to 1.731 ± 0.054 kPa, while VPDm ranged from 0.974 ± 0.044 kPa to 4.043 ± 0.106 kPa. The relative humidity (RH) followed a reverse course relatively to VPD during the experimental period (Figure 1). The Photosynthetic Photon Flux Density (PPFD) was maintained at a relatively high level (i.e., >1500 μmol m−2 s−1) (Figure 2) from the end of May to the end of August; only during the first measurement (end of spring) PPFD was relatively low, approximately 800 μmol m−2 s−1.
Data analysis revealed that only the date was a significant predictor for leaf temperature (Tl) (p < 0.001), whereas the shrub life form (deciduous, evergreen) and the interaction between date and shrub life form were not significant (p ≥ 0.05). Leaf temperature (Tl) during the study period almost coincided with the midday ambient air temperature (Tm), ranging from 19.86 °C to 33.04 °C and 19.29 °C to 33.61 °C, respectively (Figure 2). Predawn air temperature (Tp) ranged from 17.80 °C to 23.21 °C. The differences between Tp and Tm were statistically significant (p < 0.05) throughout the experimental period, except from the first measurement (mid-May).

2.2. Physiological Parameters

The principal component analysis (PCA, Figure 3) of the physiological parameters showed that the eight species are classified into the groups they belong to, deciduous and evergreen, and characterize the first principal component (Axis x), i.e., the species Coronilla emeroides Boiss. and Spruner, Carpinus betulus L., Pistasia terebinthus L. and Cercis siliquastrum L. are deciduous, while the species Arbutus unedo L., Arbutus adrachnae L., Quercus coccifera L. and Quercus ilex L. are evergreens. Additionally, variables such as predawn leaf water potential (Ψp), gs and leaf hydraulic conductance (KLeaf) are negatively correlated with VPDp, VPDm, the Julian date of the measurements and the second principal component (Axis y). Midday leaf water potential (Ψm) characterizes both components, while E does not characterize any of the two components. The deciduous species presented higher values (less negative) of Ψp, Ψm, gs and KLeaf relatively to evergreen species (Table 1).

2.3. Leaf Water Potential

On one hand, data analysis revealed that the date was a significant predictor for Ψp and Ψm (p = 0.021 and p < 0.001, respectively). On the other hand, the shrub life form (deciduous, evergreen) significantly affected the Ψm (p < 0.001). The interaction between date and shrub life form was not significant concerning the two variables (p ≥ 0.05) (Figure 4a). The estimated Ψm values were significantly lower in the considered evergreen shrubs in comparison to the deciduous shrubs during the experimental period (p < 0.001), (Figure 4b). Ψp ranged in deciduous shrubs from –0.87 MPa to −1.21 Mpa and in the evergreens from −0.92 Mpa to −1.14 Mpa, while Ψm from −1.4 Mpa to −2.59 Mpa and from −1.88 Mpa to −2.86 Mpa, respectively. The average values of the studied parameters are presented in Table 1.

2.4. Transpiration Rate, Stomatal and Leaf Hydraulic Conductance

Data analysis revealed that the date was a significant (p < 0.001) predictor for E, gs and KLeaf. The shrub life form (deciduous, evergreen) significantly affected variable KLeaf (p < 0.001). The interaction between date and shrub life form was significant only for gs (p < 0.05). The seasonal pattern of E (at solar noon) of evergreen and deciduous shrubs did not fluctuate substantially during the experimental period and significant difference was not observed in E between deciduous and evergreen shrubs (p > 0.05). The average values of E were found 16.12 ± 0.89 and 15.87 ± 0.68 mmol m−2 s−1 for deciduous and evergreen shrubs, respectively (Table 1). In particular during the dry season, E ranged from 11.71 to 20.29 mmol m−2 s−1 in the deciduous and from 13.04 to 17.02 mmol m−2 s−1 in the evergreen shrubs (Figure 5).
Seasonal pattern of gs was different (p < 0.05) between the two groups of plants. The deciduous shrubs presented significantly lower values (p < 0.05) of gs in relation to the evergreens during dry period (from July until mid-August). The gs during dry period ranged from 416.5± 22.7 to 585.25 ± 42.5 mmol m−2 s−1 in deciduous and from 413.5 ± 27.4 to 644.75 ± 43.5 mmol m−2 s−1 in evergreen shrubs (Figure 6).
The KLeaf was significantly higher in deciduous compared to evergreen shrubs (p < 0.001), (Figure 7), especially during the dry season. The mean KLeaf was significantly higher in deciduous 17.18 ± 1.45 mmol Mpa−1 m−2 s−1 compared to evergreens 13.15 ± 1.57 mmol Mpa−1 m−2 s−1 (p < 0.001), (Figure 7, Table 1). However, the seasonal changes of KLeaf in both groups of plants revealed a decrease in the KLeaf when VPDm increased during the dry period (Figure 7).
The relationship between KLeaf and Ψm is presented in Figure 8. It is likely that as the growing season proceeded KLeaf decreased and exhibited the lowest values concomitantly with the lowest Ψm values. It is worth mentioning that for the same low values of Ψm, the deciduous shrubs exhibited higher KLeaf in relations to the evergreens.
In Table 2, the Pearson correlation between physiological parameters and VPDm is presented. In deciduous species a significant positive correlation was detected between VPDm and E and a negative between Ψm and gs, while in evergreen shrubs VPDm was negatively correlated with Ψm and KLeaf.

3. Discussion

The results of this study demonstrate that the water status of co-occurring evergreen and deciduous broadleaved shrubs in semi-arid Mediterranean conditions under rising VPDm is different. Additionally, it seems likely that deciduous shrubs control more efficiently their water status during the dry season, by exhibiting lower stomatal conductance and higher hydraulic conductance than the evergreens. In other words, the deciduous plants possess a more water spending behaviour than the evergreens.
The increase of air temperature accompanied by decreasing RH and increasing heat load due to incident radiation on the leaf, in combination with air speed, may elevate VPD in the atmosphere [60]. It has been reported that RH concerning future climatic scenarios will remain either constant at the global scale [61], or a negative [62] and/or positive trend between VPD and RH at a regional scale [27] will be observed. In our research, the values of PPFD were generally maintained at high levels, as it was expected concerning the characteristics of the Mediterranean climate in the experimental site. The same values in air and leaf temperature imply that broadleaved shrubs possess such leaf tissues, where the transpiration flow is not sufficient to reduce leaf temperature in relation to the ambient temperature. The increase of Tm and VPDm under drought conditions (after June) may be linked to the physiological performance and survival of deciduous and evergreen shrubs via either reducing gs and gas exchanges (feedforward mechanism), or increasing plant water loss (feedback mechanism) [63].
The seasonal patterns of Ψp and Ψm suggest that the co-occurring deciduous and evergreen shrubs on Olympus Mountain were able to regulate water loss and ensuring adequate hydration of leaf tissues overnight, even during the dry season, therefore Ψp was retained to approximately −1.0 MPa; such scale of the Ψp values is sufficient for the Mediterranean region (Quercetalia ilicis zone) where the studied species are growing [64]. Ψp is an essential index to study the response of plants to drought, because its value can be considered equal to soil water potential, since plants and soil reach a hydration equilibrium during the night [65,66,67,68].
The higher (less negative) Ψm in deciduous shrubs indicates higher values of relative water content, E and gs in comparison to the evergreen shrubs. The Ψm seems to be the main factors for stomatal regulation because is directly linked to the turgor of guard cells [49,69,70]. After sunrise, the leaf water potential in Mediterranean plants decreases steadily, reaching its lower value at noon, while it begins to recover again during the afternoon [71,72,73]. This reflects a decline of stored water, and therefore water shortage [60]. The plants are the best indicators of soil water availability, which affect their water status [74,75]. Plants with both elevated (less negative) Ψm and water transport capacity can better control their leaf water status during midday, and hence they experience a smaller decline of midday gs [49].
It is likely that the relatively higher E in deciduous species during midday is due to their elevated water status, i.e., higher Ψm in leaves (Figure 4a and Figure 5); a slight variation of E values was detected between deciduous and evergreen shrubs, while the lowest values of E occurred in the two groups of shrubs during the dry season (June–August), (Figure 5). Apparently, low E values during the dry season remained rather stable and above zero values, which indicates influx of carbon dioxide [49,76].
The deciduous shrubs exhibited higher Ψm and lower midday gs than the evergreens; this may indicate that midday stomatal conductance is more related to stem rather than leaf water status, which is in accordance with earlier results [49]. In fact, gs was negatively correlated with VPDm (Table 2), suggesting a response to environmental conditions, which is in agreement with the published results by Auge et al. [77] from other deciduous species. This trait may help deciduous species to regulate their stomatal apparatus in order to maintained Ψm in a range of values that will support their water status and avoid xylem embolism under drought conditions [49,78]. Our results show that there was not any synchronization between gs and Ψm in both shrub groups, which may also be due to the fact the evergreens are hypostomatic plants [79,80,81]. However, it is not clear which microclimate parameter, i.e., temperature and/or relative humidity, was directly linked to stomatal behaviour. It has been proposed that temperature had a greater impact on stomatal conductance and assimilation rate in the amphistomatic leaves of Eucalyptus tetrodonta independently of VPD [82,83]. Addington et al. [35] reported that the stomatal apparatus controls Ψ in a way that the tension on the water column created by decreasing Ψ did not cause extreme xylem cavitation. Several studies suggested that high VPD reduces gs, consequently affecting assimilation rate and growth [84,85]. On the contrary, it has been argued that the impact of high VPD on gs may not possess any impact on assimilation rate and growth [86]. Nevertheless, the impact of VPD on gs and/or assimilation rate varies amongst plant species [82]. In addition, the stomatal anatomy and structure affect water loss and carbon assimilation, demonstrating the evolution and adaptations of the plants to environmental conditions [84,87].
Plants in order to grow and survive under water limited conditions evolved mechanisms to control stomatal aperture and xylem water capacity [88]. The differences in water-use strategies might be partially due to various hydraulic properties between the considered groups. The hydrodynamic status of leaf tissue expressed via leaf water potential [89] is determined by two mail functions taking place in the SPA continuum, i.e., transpiration rate and hydraulic conductance. Therefore, the favourable water status in deciduous shrubs could be attributed to the higher values of transpiration rate and/or at the highest values of the hydraulic conductance. The deciduous shrubs exhibited higher values of KLeaf when compared to evergreen shrubs, especially during the dry summer period. This advantage of deciduous shrubs could be attributed to their water status and anatomical features. The positive correlation between KLeaf and Ψm, and E in deciduous shrubs (Table 2) and the negative correlation between KLeaf and VPDm suggest that the water transport from root to the leaf plays a role to the fluctuations of leaf water status. The seasonal KLeaf declined in both groups of plants when VPD increased during the summer dry period (Figure 7) especially at the end of July, when the highest value of VPD (3.99 KPa) was recorded. Probably, at a given transpiration rate in deciduous shrubs the leaf water status is maintained due to high hydraulic conductance [17,90,91]. Manzoni et al. [88] reported that, in some ecosystems, deciduous species have been found to be more hydraulically efficient than evergreen species. Choat et al. [92] suggested that deciduous species are more hydraulically efficient, but also more vulnerable to drought-induced embolism, than co-existing evergreens in a rainforest. It is well known that embolism occurs in plants under drought conditions when Ψ reaches very low values; however, the plants have the capacity to repair damage when the environmental conditions are favourable [89].
Our data are somehow in agreement with BIumler [93], who argued that although the Mediterranean climate is associated with evergreen species, some coexisting deciduous species exhibit some advantages in response to drought [92,94]. It is noteworthy that in our work deciduous and evergreen species are presented as two distinct life-history groups [91], although they probably form a continuum of variation in leaf life-history span [95].

4. Materials and Methods

4.1. Study Area and Climate

The study was conducted on Olympus Mountain (40°06′54″ N, 22°28′42″ E), which is a great, long-lived natural laboratory [96,97,98] in 2009, at an altitude of 554 m a.s.l., in an area located 5 Km from the town of Litochoro, 95 km south-east of Thessaloniki, in Greece. The climate of the study area is characterized as Cfa in the Köppen-Geiger system (http://www.en.climate-data.org, 7 January 2022) and as Mediterranean with cold and wet winters, dry and warm summer according to the bioclimatogram of Emberger. The mean annual rainfall in the study area ranges from 800 to 1000 mm, while substantially elevated precipitation is recorded during winter. The minimum air temperature ranges from 13 to 6 °C (during summer and winter, respectively). The maximum air temperature ranges from 4.9 to 6.7 °C during winter, and from 20 to 26 °C during summer. The warmest month is July and the coldest is December. The mean annual relative humidity (RH) ranges from 75 to 80%. Average RH values during the most humid month (December) is 85–90% and during the driest month (July) 30–50%. The monthly changes of temperature and precipitation (ombrothermic diagram) during the year of the measurements, from the nearest meteorological station of Dion (40°12′00″ N, 22°30′00″ E), are presented in Figure 9.
The microclimatic conditions (temperature, humidity), in the study area during the experimental period was measured with the Hobo H8 Pro (Hobo H8 Pro Series 1997–2003, Onset Computer Coorporation, Bourne, MA, USA). Furthermore, on specific Julian dates and hours when plant physiological parameters were investigated, ambient air predawn and midday temperature and RH were measured using a Novasima MS1 microclimatic sensor (Novatron Scientific Ltd., Horsham, UK). Predawn (VPDp) and midday (VPDm) vapour pressure deficit were calculated according to Abtew and Melesse (2013). The Photosynthetic Photon Flux Density was measured with the steady-state diffusion porometer LI-1600 (LI- COR, Inc., Lincoln, NE, USA). The presented values of VPDp, VPDm, RH, PPFD, Tp and Tm are means of twenty-four measurements.

4.2. Plant Material

The study area is part of the Mediterranean zone of the evergreen broadleaved plants Quercus ilex L. and Arbutus andrachne L. Deciduous and evergreen shrubs and small trees such as Acer monspesulanum L., Carpinus betulus L., Cercis siliquastrum L., Cotinus coggygria Scop., Fraxinus ornus L., Pistacia terebinthus L., Coronilla emeroides Boiss. and Spruner, Quercus coccifera L., Arbutus unedo L., Phillyrea media L., and Juniperus oxycedrus L. are widespread in the study area.
Four evergreen shrubs Arbutus andrachne (commonly known as Grecian strawberry tree), Arbutus unedo (strawberry tree), Quercus ilex (holm oak) and Quercus coccifera (kermes oak) and four deciduous shrubs Carpinus betulus (common hornbeam), Cercis siliquastrum (Juda’s tree), Coronilla emeroides (scorpion senna), and Pistacia terebinthus (terebinth) were selected for this study. The shrubs were randomly selected for sampling. More specifically, the area of interest was equal to 20 ha. We divided this area into 20 tiles, 1 ha each, and then we randomly selected 6 tiles where each one of the eight species was randomly chosen. Concerning dendrometric parameters, the considered species possessed the same height (3–4 m) and diameter (1.5–2.0 m).

4.3. Physiological Parameters

Leaf water potential (Ψ), transpiration rate (Ε), stomatal conductance (gs) and leaf temperature (Tl) were measured on the newest fully developed mature leaves of six different individuals from sun-exposed terminal branches. Using the pressure-bomb technique (PMS, Albany, OR, USA), leaf water potential was measured twice during the day, i.e., at predawn (Ψp) and midday (Ψm). Transpiration rate, gs and Tl were measured using steady state porometer (Li1600, LI-COR Lincoln, NE, USA). Seasonal measurements of Ψp were obtained before sunrise, while the measurements of Ψm, E, and gs were obtained on clear sunny days at around solar noon (12:00–14:30 h), approximately 10–15 days intervals. The presented values, for each of the parameters, are means of six replications per studied shrub.
Leaf hydraulic conductance (KLeaf) was calculating according to Ohm’s law following the formula:
K Leaf = E ( Ψ soil − Ψ Leaf ) = E ( Ψ p − Ψ m )
It has been assumed that Ψsoil is in equilibrium with Ψp and the lowest diurnal Ψleaf is equal to Ψm [66,67,99]. However, sometimes the first assumption may lead to overestimation of Kplant [100]. Additionally, values of KLeaf reflect the capacity of evergreen and deciduous plants, grown under ambient conditions, for water exploitation during a period of soil drying.

4.4. Statistical Analysis

The Kolmogorov–Smirnov test was employed to evaluate data normality. To explore whether the ecophysiological response of deciduous and evergreen shrubs vary during the dry season, a two-way analysis of variance (ANOVA) was performed on the studied parameters (TL, Ψp, Ψm, E, gs, Kleaf) [81]. Student’s t-test for independent samples was used to examine differences in TL, E, gs, Ψm, Ψp and KLeaf between deciduous and evergreen shrubs. The climatic parameters VPDp, VPDm, Tp, and Tm at each sampling date were compared using also the Student’s t-test for independent samples. Polynomial regression analysis was used to determine the relationship between ΚLeaf and Ψm, between deciduous and evergreen shrubs. In addition, a Principal Component Analysis (PCA) with varimax rotation was used to assess the relationships among the measurements of interest between the eight shrubs to see whether they could be classified according to their ecophysiological response in the life form in which belong (deciduous, evergreen). Pearson correlation was used to explore links among VPDm, E, gs, Ψp, Ψm and KLeaf. P-values lower than 0.05 were considered statistically significant. All statistical analyses were performed using the SPSS statistical package v. 27.0 (IBM Corp. in Armonk, NY, USA).

5. Conclusions

The results of this research work demonstrate different hydraulic strategies between co-occurring deciduous and evergreen shrubs grown on Olympus Mountain. The deciduous life-form presented a strategy of higher hydraulic and lower stomatal conductance, while the evergreen exhibited lower hydraulic and higher stomatal conductance. Although, seasonal leaf hydraulic conductance declined in both groups of plants when vapor pressure deficit increased during the summer dry period, evergreen shrubs sustain a water transport to their foliage at a rate sufficient to prevent severe damage due to desiccation.

Author Contributions

Conceptualization: M.K.; methodology: M.K., E.V. and S.R.; software: M.K., P.K. and E.V.; validation: M.K.; formal analysis: M.K., E.V. and S.R.; investigation: M.K. and P.K.; resources: M.K.; writing—original draft preparation: M.K. and S.R.; writing—review and editing: M.K., E.V. and S.R.; visualization: M.K.; supervision: M.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable for studies not involving humans or animals.

Informed Consent Statement

Not applicable for studies not involving humans or animals.

Data Availability Statement

The data presented in this study are available in figures and tables provided in the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pachauri, R.K.; Allen, M.R.; Barros, V.R.; Broome, J.; Cramer, W.; Christ, R.; Church, J.A.; Clarke, L.; Dahe, Q.; Dasgupta, P. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; IPCC: Geneva, Switzerland, 2014. [Google Scholar]
  2. Moreno, M.; Simioni, G.; Limousin, J.M.; Rodriguez-Calcerrada, J.; Ruffault, J.; Cochard, H.; Torres, J.; Delzon, S.; Tournant, A.; Dumas, P.J. Mediterranean trees vulnerability to climate change will not be minimized through hydraulic safety traits adjustments. In Proceedings of the EGU General Assembly Conference Abstracts, vEGU21: Gather Online, 19–30 April 2021; p. EGU21-3850. [Google Scholar]
  3. Zindros, A.; Radoglou, K.; Milios, E.; Kitikidou, K. Tree Line Shift in the Olympus Mountain (Greece) and Climate Change. Forests 2020, 11, 985. [Google Scholar] [CrossRef]
  4. Kramer, P.J. Drought stress and the origin of adaptations. In Adaptation of Plants to Water and High Temperature Stress; Turner, N.C., Kramer, P.J., Eds.; John Wiley & Sons: New York, NY, USA, 1980; pp. 7–21. [Google Scholar]
  5. Chaves, M.M.; Pereira, J.S.; Maroco, J.; Rodrigues, M.L.; Ricardo, C.P.; Osorio, M.L.; Carvalho, I.; Faria, T.; Pinheiro, C. How plants cope with water stress in the field. Photosynthesis and growth. Ann. Bot. 2002, 89, 907–916. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Margolis, H.A.; Ryan, M.G. A physiological basis for biosphere-atmosphere interactions in the boreal forest: An overview. Tree Physiol. 1997, 17, 491–499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Sanchez, M.; Sinclair, T.R.; Pradhan, D. Transpiration response to vapor pressure deficit and soil drying among quinoa genotypes (Chenopodium quinoa Willd.). J. Crop Improv. 2020, 35, 291–302. [Google Scholar] [CrossRef]
  8. Pereira, J.S. Plant water deficits in Mediterranean ecosystems. In Water Deficits: Plant Response from Cell to Community; Smith, J.A.C., Griffiths, H., Eds.; Bios Scientific Publishers: Oxford, UK, 1993; pp. 237–251. [Google Scholar]
  9. Kapsali, E.-I.; Karatassiou, M. Seasonal changes in leaf tissue rehydration of one annual and two perennial grass forage species induced by bioclimate. Not. Bot. Horti Agrobot. Cluj-Napoca 2015, 43, 479–487. [Google Scholar] [CrossRef] [Green Version]
  10. Karatassiou, M.; Noitsakis, B. Changes of the photosynthetic behaviour in annual C3 species at late successional stage under environmental drought conditions. Photosynthetica 2010, 48, 377–382. [Google Scholar] [CrossRef]
  11. Choat, B.; Brodribb, T.J.; Brodersen, C.R.; Duursma, R.A.; Lopez, R.; Medlyn, B.E. Triggers of tree mortality under drought. Nature 2018, 558, 531–539. [Google Scholar] [CrossRef]
  12. Fang, Y.L.; Leung, L.R.; Wolfe, B.T.; Detto, M.; Knox, R.G.; McDowell, N.G.; Grossiord, C.; Xu, C.G.; Christoffersen, B.O.; Gentine, P.; et al. Disentangling the effects of Vapor Pressure Deficit and Soil Water Availability on Canopy Conductance in a Seasonal Tropical Forest During the 2015 El Nino Drought. J. Geophys. Res.-Atmos. 2021, 126, e2021JD035004. [Google Scholar] [CrossRef]
  13. Aranda, I.; Gil, L.; Pardos, J. Seasonal changes in apparent hydraulic conductance and their implications for water use of European beech (Fagus sylvatica L.) and sessile oak [Quercus petraea (Matt.) Liebl] in South Europe. Plant Ecol. 2005, 179, 155–167. [Google Scholar] [CrossRef]
  14. Meinzer, F.C.; Clearwater, M.J.; Goldstein, G. Water transport in trees: Current perspectives, new insights and some controversies. Environ. Exp. Bot. 2001, 45, 239–262. [Google Scholar] [CrossRef]
  15. Sack, L.; Cowan, P.D.; Jaikumar, N.; Holbrook, N.M. The ‘hydrology’ of leaves: Co-ordination of structure and function in temperate woody species. Plant Cell Environ. 2003, 26, 1343–1356. [Google Scholar] [CrossRef] [Green Version]
  16. Lo Gullo, M.A.; Castro Noval, L.; Salleo, S.; Nardini, A. Hydraulic architecture of plants of Helianthus annuus L. cv. Margot: Evidence for plant segmentation in herbs. J. Exp. Bot. 2004, 55, 1549–1556. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Nardini, A.; Salleo, S. Limitation of stomatal conductance by hydraulic traits: Sensing or preventing xylem cavitation? Trees 2000, 15, 14–24. [Google Scholar] [CrossRef]
  18. Tyree, M.; Sobrado, M.; Stratton, L.; Becker, P. Diversity of hydraulic conductance in leaves of temperate and tropical species: Possible causes and consequences. J. Trop. For. Sci. 1999, 11, 47–60. [Google Scholar]
  19. Brodribb, T.J.; Holbrook, N.M. Leaf physiology does not predict leaf habit; examples from tropical dry forest. Trees 2005, 19, 290–295. [Google Scholar] [CrossRef]
  20. Sack, L.; Tyree, M.T. Leaf Hydraulics and Its Implications in Plant Structure and Function. In Vascular Transport in Plants; Holbrook, N.M., Zwieniecki, M.A., Eds.; Elsevier: Amsterdam, The Netherlands; Academic Press: Cambridge, MA, USA, 2005; pp. 93–114. [Google Scholar]
  21. Pereira, J.S.; Pallardy, S. Water stress limitations to tree productivity. In Biomass Production by Fast-Growing Trees; Pereira, J.S., Landsberg, J.J., Eds.; Springer: Dordrecht, The Netherlands, 1989; pp. 37–56. [Google Scholar]
  22. Jordan, W.R.; Dugas, W.A., Jr.; Shouse, P.J. Strategies for crop improvement for drought-prone regions. Agric. Water Manage. 1983, 7, 281–299. [Google Scholar] [CrossRef]
  23. Daszkowska-Golec, A.; Szarejko, I. Open or close the gate–stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci. 2013, 4, 138. [Google Scholar] [CrossRef] [Green Version]
  24. 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 the vulnerability of forests to drought. Nature 2012, 491, 752–755. [Google Scholar] [CrossRef] [Green Version]
  25. Baert, A.; De Schepper, V.; Steppe, K. Variable hydraulic resistances and their impact on plant drought response modelling. Tree Physiol. 2015, 35, 439–449. [Google Scholar] [CrossRef]
  26. Martınez-Vilalta, J.; Piñol, J.; Beven, K. A hydraulic model to predict drought-induced mortality in woody plants: An application to climate change in the Mediterranean. Ecol. Modell. 2002, 155, 127–147. [Google Scholar] [CrossRef]
  27. Grossiord, C.; Buckley, T.N.; Cernusak, L.A.; Novick, K.A.; Poulter, B.; Siegwolf, R.T.W.; Sperry, J.S.; McDowell, N.G. Plant responses to rising vapor pressure deficit. New Phytol. 2020, 226, 1550–1566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Breshears, D.D.; Adams, H.D.; Eamus, D.; McDowell, N.G.; Law, D.J.; Will, R.E.; Williams, A.P.; Zou, C.B. The critical amplifying role of increasing atmospheric moisture demand on tree mortality and associated regional die-off. Front. Plant Sci. 2013, 4, 266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Stovall, A.E.L.; Shugart, H.; Yang, X. Tree height explains mortality risk during an intense drought. Nat. Commun. 2019, 10, 4385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Oren, R.; Sperry, J.S.; Katul, G.G.; Pataki, D.E.; Ewers, B.E.; Phillips, N.; Schäfer, K.V.R. Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ. 1999, 22, 1515–1526. [Google Scholar] [CrossRef] [Green Version]
  31. Franks, P.; Cowan, I.; Farquhar, G. The apparent feedforward response of stomata to air vapour pressure deficit: Information revealed by different experimental procedures with two rainforest trees. Plant Cell Environ. 1997, 20, 142–145. [Google Scholar] [CrossRef]
  32. Carminati, A.; Javaux, M. Soil Rather than Xylem Vulnerability Controls Stomatal Response to Drought. Trends Plant Sci. 2020, 25, 868–880. [Google Scholar] [CrossRef]
  33. Meinzer, F.; Hinckley, T.; Ceulemans, R. Apparent responses of stomata to transpiration and humidity in a hybrid poplar canopy. Plant Cell Environ. 1997, 20, 1301–1308. [Google Scholar] [CrossRef]
  34. Monteith, J. A reinterpretation of stomatal responses to humidity. Plant Cell Environ. 1995, 18, 357–364. [Google Scholar] [CrossRef]
  35. Addington, R.N.; Mitchell, R.J.; Oren, R.; Donovan, L.A. Stomatal sensitivity to vapor pressure deficit and its relationship to hydraulic conductance in Pinus palustris. Tree Physiol. 2004, 24, 561–569. [Google Scholar] [CrossRef] [Green Version]
  36. Li, J.; Zhang, G.Z.; Li, X.; Wang, Y.; Wang, F.Z.; Li, X.M. Seasonal change in response of stomatal conductance to vapor pressure deficit and three phytohormones in three tree species. Plant Signal Behav. 2019, 14, 1682341. [Google Scholar] [CrossRef] [Green Version]
  37. Körner, C.; Neumayer, M.; Menendez-Riedl, S.P.; Smeets-Scheel, A. Functional morphology of mountain plants. Flora 1989, 182, 353–383. [Google Scholar] [CrossRef]
  38. McNaughton, K.; Jarvis, P. Effects of spatial scale on stomatal control of transpiration. Agric. For. Meteorol. 1991, 54, 279–302. [Google Scholar] [CrossRef]
  39. Cunningham, S.C. Photosynthetic responses to vapour pressure deficit in temperate and tropical evergreen rainforest trees of Australia. Oecologia 2005, 142, 521–528. [Google Scholar] [CrossRef] [PubMed]
  40. Gao, J.; Zhao, P.; Shen, W.; Niu, J.; Zhu, L.; Ni, G. Biophysical limits to responses of water flux to vapor pressure deficit in seven tree species with contrasting land use regimes. Agric. For. Meteorol. 2015, 200, 258–269. [Google Scholar] [CrossRef]
  41. Aasamaa, K.; Sõber, A.; Rahi, M. Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Funct. Plant Biol. 2001, 28, 765–774. [Google Scholar] [CrossRef]
  42. Raftoyannis, Y.; Radoglou, K. Physiological responses of beech and sessile oak in a natural mixed stand during a dry summer. Ann. Bot. 2002, 89, 723–730. [Google Scholar] [CrossRef] [Green Version]
  43. Schütz, W.; Milberg, P.; Lamont, B.B. Germination requirements and seedling responses to water availability and soil type in four eucalypt species. Acta Oecol. 2002, 23, 23–30. [Google Scholar] [CrossRef]
  44. Klein, T. The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct. Ecol. 2014, 28, 1313–1320. [Google Scholar] [CrossRef]
  45. Karatassiou, M.; Noitsakis, B.; Koukoura, Z. Drought adaptation ecophysiological mechanisms of two annual legumes on semi-arid Mediterranean grassland. Sci. Res. Essays 2009, 4, 493–500. [Google Scholar] [CrossRef]
  46. Cochard, H.; Venisse, J.-S.; Barigah, T.S.; Brunel, N.; Herbette, S.; Guilliot, A.; Tyree, M.T.; Sakr, S. Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol. 2007, 143, 122–133. [Google Scholar] [CrossRef] [Green Version]
  47. Guyot, G.; Scoffoni, C.; Sack, L. Combined impacts of irradiance and dehydration on leaf hydraulic conductance: Insights into vulnerability and stomatal control. Plant Cell Environ. 2012, 35, 857–871. [Google Scholar] [CrossRef] [PubMed]
  48. Sellin, A.; Sack, L.; Ounapuu, E.; Karusion, A. Impact of light quality on leaf and shoot hydraulic properties: A case study in silver birch (Betula pendula). Plant Cell Environ. 2011, 34, 1079–1087. [Google Scholar] [CrossRef] [PubMed]
  49. Zhang, Y.J.; Meinzer, F.C.; Qi, J.H.; Goldstein, G.; Cao, K.F. Midday stomatal conductance is more related to stem rather than leaf water status in subtropical deciduous and evergreen broadleaf trees. Plant Cell Environ. 2013, 36, 149–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Grassi, G.; Ripullone, F.; Borghetti, M.; Raddi, S.; Magnani, F. Contribution of diffusional and non-diffusional limitations to midday depression of photosynthesis in Arbutus unedo L. Trees 2009, 23, 1149–1161. [Google Scholar] [CrossRef]
  51. Brodribb, T.J.; Jordan, G.J. Internal coordination between hydraulics and stomatal control in leaves. Plant Cell Environ. 2008, 31, 1557–1564. [Google Scholar] [CrossRef] [PubMed]
  52. Comstock, J.P. Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. J. Exp. Bot. 2002, 53, 195–200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Aranda, I.; Cano, F.J.; Gasco, A.; Cochard, H.; Nardini, A.; Mancha, J.A.; Lopez, R.; Sanchez-Gomez, D. Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress. Tree Physiol. 2015, 35, 34–46. [Google Scholar] [CrossRef]
  54. Martínez-Vilalta, J.; Cochard, H.; Mencuccini, M.; Sterck, F.; Herrero, A.; Korhonen, J.; Llorens, P.; Nikinmaa, E.; Nole, A.; Poyatos, R. Hydraulic adjustment of Scots pine across Europe. New Phytol. 2009, 184, 353–364. [Google Scholar] [CrossRef]
  55. Kolb, K.J.; Davis, S.D. Drought tolerance and xylem embolism in co-occurring species of coastal sage and chaparral. Ecology 1994, 75, 648–659. [Google Scholar] [CrossRef]
  56. Iovi, K.; Kolovou, C.; Kyparissis, A. An ecophysiological approach of hydraulic performance for nine Mediterranean species. Tree Physiol. 2009, 29, 889–900. [Google Scholar] [CrossRef] [Green Version]
  57. Nardini, A. Are sclerophylls and malacophylls hydraulically different? Biol. Plant. 2001, 44, 239–245. [Google Scholar] [CrossRef]
  58. Zellweger, F.; De Frenne, P.; Lenoir, J.; Vangansbeke, P.; Verheyen, K.; Bernhardt-Römermann, M.; Baeten, L.; Hédl, R.; Berki, I.; Brunet, J. Forest microclimate dynamics drive plant responses to warming. Science 2020, 368, 772–775. [Google Scholar] [CrossRef] [PubMed]
  59. McDaniel, M.D.; Wagner, R.J.; Rollinson, C.R.; Kimball, B.A.; Kaye, M.W.; Kaye, J.P. Microclimate and ecological threshold responses in a warming and wetting experiment following whole tree harvest. Theor. Appl. Climatol. 2014, 116, 287–299. [Google Scholar] [CrossRef]
  60. Jones, H.G. Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology; Cambridge University Press: Cambridge, UK, 2013. [Google Scholar]
  61. Dai, A. Recent climatology, variability, and trends in global surface humidity. J. Clim. 2006, 19, 3589–3606. [Google Scholar] [CrossRef] [Green Version]
  62. Byrne, M.P.; O’Gorman, P.A. Trends in continental temperature and humidity directly linked to ocean warming. Proc. Natl. Acad. Sci. USA 2018, 115, 4863–4868. [Google Scholar] [CrossRef] [Green Version]
  63. Will, R.E.; Wilson, S.M.; Zou, C.B.; Hennessey, T.C. Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone. New Phytol. 2013, 200, 366–374. [Google Scholar] [CrossRef]
  64. Rhizopoulou, S.; Mitrakos, K. Water relations of evergreen sclerophylls. I. Seasonal changes in the water relations of eleven species from the same environment. Ann. Bot. 1990, 65, 171–178. [Google Scholar] [CrossRef]
  65. Sellin, A. Does pre-dawn water potential reflect conditions of equilibrium in plant and soil water status? Acta Oecol. 1999, 20, 51–59. [Google Scholar] [CrossRef]
  66. Williams, L.E.; Trout, T.J. Relationships among vine-and soil-based measures of water status in a Thompson Seedless vineyard in response to high-frequency drip irrigation. Am. J. Enol. Vitic. 2005, 56, 357–366. [Google Scholar]
  67. Cai, G.; Ahmed, M.A.; Dippold, M.A.; Zarebanadkouki, M.; Carminati, A. Linear relation between leaf xylem water potential and transpiration in pearl millet during soil drying. Plant Soil 2020, 447, 565–578. [Google Scholar] [CrossRef]
  68. Knipfer, T.; Bambach, N.; Hernandez, M.I.; Bartlett, M.K.; Sinclair, G.; Duong, F.; Kluepfel, D.A.; McElrone, A.J. Predicting stomatal closure and turgor loss in woody plants using predawn and midday water potential. Plant Physiol. 2020, 184, 881–894. [Google Scholar] [CrossRef] [PubMed]
  69. Brodribb, T.J.; Holbrook, N.M. Stomatal Closure during Leaf Dehydration, Correlation with Other Leaf Physiological Traits. Plant Physiol. 2003, 132, 2166–2173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Meinzer, F.C.; Johnson, D.M.; Lachenbruch, B.; McCulloh, K.A.; Woodruff, D.R. Xylem hydraulic safety margins in woody plants: Coordination of stomatal control of xylem tension with hydraulic capacitance. Funct. Ecol. 2009, 23, 922–930. [Google Scholar] [CrossRef]
  71. Rhizopoulou, S.; Heberlein, K.; Kassianou, A. Field water relations of Capparis spinosa L. J. Arid Environ. 1997, 36, 237–248. [Google Scholar] [CrossRef] [Green Version]
  72. Meletiou-Christou, M.-S.; Rhizopoulou, S. Constraints of photosynthetic performance and water status of four evergreen species co-occurring under field conditions. Bot. Stud. 2012, 53, 325–334. [Google Scholar]
  73. Meletiou-Christou, M.-S.; Rhizopoulou, S. Leaf functional traits of four evergreen species growing in Mediterranean environmental conditions. Acta Physiol. Plant. 2017, 39, 34. [Google Scholar] [CrossRef]
  74. Kramer, P.J.; Boyer, J.S. Water Relations of Plants and Soils; Academic Press: San Diego, CA, USA, 1995. [Google Scholar]
  75. Rhizopoulou, S.; Kapolas, G. In situ study of deep roots of Capparis spinosa L. during the dry season: Evidence from a natural “rhizotron” in the ancient catacombs of Milos Island (Greece). J. Arid Environ. 2015, 119, 27–30. [Google Scholar] [CrossRef]
  76. Kosugi, Y.; Matsuo, N. Seasonal fluctuations and temperature dependence of leaf gas exchange parameters of co-occurring evergreen and deciduous trees in a temperate broad-leaved forest. Tree Physiol. 2006, 26, 1173–1184. [Google Scholar] [CrossRef] [Green Version]
  77. Auge, R.M.; Green, C.D.; Stodola, A.J.; Saxton, A.M.; Olinick, J.B.; Evans, R.M. Correlations of stomatal conductance with hydraulic and chemical factors in several deciduous tree species in a natural habitat. New Phytol. 2000, 145, 483–500. [Google Scholar] [CrossRef] [Green Version]
  78. Medrano, H.; Flexas, J.; Galmes, J. Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. Plant Soil 2009, 317, 17–29. [Google Scholar] [CrossRef]
  79. Koukos, D.; Meletiou-Christou, M.-S.; Rhizopoulou, S. Leaf surface wettability and fatty acid composition of Arbutus unedo and Arbutus andrachne grown under ambient conditions in a natural macchia. Acta Bot. Gall. 2015, 162, 225–232. [Google Scholar] [CrossRef] [Green Version]
  80. Christodoulakis, N.S.; Lampri, P.-N.; Fasseas, C. Structural and cytochemical investigation of the leaf of silverleaf nightshade (Solanum elaeagnifolium), a drought-resistant alien weed of the Greek flora. Aust. J. Bot. 2009, 57, 432–438. [Google Scholar] [CrossRef]
  81. Río, S.D.; Álvarez Nogal, R.; Candelas, A.; González-Sierra, S.; Herrero, L.; Penas, A. Preliminary study on taxonomic review using histological sections of some Iberian species from the genus Quercus L. (Fagaceae). Am. J. Plant Sci. 2014, 5, 2773–2784. [Google Scholar] [CrossRef] [Green Version]
  82. Duff, G.A.; Myers, B.A.; Williams, R.J.; Eamus, D.; OGrady, A.; Fordyce, I.R. Seasonal patterns in soil moisture, vapour pressure deficit, tree canopy cover and pre-dawn water potential in a northern Australian savanna. Aust. J. Bot. 1997, 45, 211–224. [Google Scholar] [CrossRef]
  83. Prior, L.; Eamus, D.; Duff, G. Seasonal and diurnal patterns of carbon assimilation, stomatal conductance and leaf water potential in Eucalyptus tetrodonta saplings in a wet–dry savanna in northern Australia. Aust. J. Bot. 1997, 45, 241–258. [Google Scholar] [CrossRef]
  84. Devi, M.J.; Reddy, V.R. Transpiration response of cotton to vapor pressure deficit and its relationship with stomatal traits. Front. Plant Sci. 2018, 9, 1572. [Google Scholar] [CrossRef] [Green Version]
  85. Ben-Asher, J.; y Garcia, A.G.; Flitcroft, I.; Hoogenboom, G. Effect of atmospheric water vapor on photosynthesis, transpiration and canopy conductance: A case study in corn. Plant Soil Environ. 2013, 59, 549–555. [Google Scholar] [CrossRef] [Green Version]
  86. Shibuya, T.; Kano, K.; Endo, R.; Kitaya, Y. Photosynthetic properties and response to drought in cucumber seedlings acclimatized to different vapor-pressure-deficit levels. Hort. J. 2017, 86, 334–339. [Google Scholar] [CrossRef] [Green Version]
  87. Larcher, W. Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups; Springer Science & Business Media: Berlin/Heidelberg, Germany, 2003. [Google Scholar]
  88. Manzoni, S.; Vico, G.; Katul, G.; Palmroth, S.; Jackson, R.B.; Porporato, A. Hydraulic limits on maximum plant transpiration and the emergence of the safety–efficiency trade-off. New Phytol. 2013, 198, 169–178. [Google Scholar] [CrossRef]
  89. Hopkins, W.G. Introduction to Plant Physiology, 4th ed.; John Wiley & Sons: Devon, UK, 2009. [Google Scholar]
  90. Bucci, S.J.; Goldstein, G.; Meinzer, F.C.; Scholz, F.G.; Franco, A.C.; Bustamante, M. Functional convergence in hydraulic architecture and water relations of tropical savanna trees: From leaf to whole plant. Tree Physiol. 2004, 24, 891–899. [Google Scholar] [CrossRef] [Green Version]
  91. Markesteijn, L.; Poorter, L.; Bongers, F.; Paz, H.; Sack, L. Hydraulics and life history of tropical dry forest tree species: Coordination of species’ drought and shade tolerance. New Phytol. 2011, 191, 480–495. [Google Scholar] [CrossRef] [PubMed]
  92. Choat, B.; Ball, M.C.; Luly, J.G.; Holtum, J.A. Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees 2005, 19, 305–311. [Google Scholar] [CrossRef]
  93. Blumler, M.A. Winter-Deciduous Versus Evergreen Habit in Mediterranean Regions: A Model; Gen. Tech. Report PSW-126; USDA Forest Service: Berkeley, CA, USA, 1991; pp. 194–197.
  94. Holbrook, N.M.; Whitebeck, J.; Mooney, H. Drought responses of neotropical dry forests. In Seasonally Dry Tropical Forests; Bullock, S.H., Mooney, H.A., Medina, E., Eds.; Cambridge University Press: Cambridge, UK, 1995; pp. 243–276. [Google Scholar]
  95. Borchert, R. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 1994, 75, 1437–1449. [Google Scholar] [CrossRef]
  96. Filippidis, E.; Mitsopoulos, I. Mapping forest fire risk zones based on historical fire data in Mount Olympus, Greece, using geographical information systems. WIT Trans. Ecol. Environ. 2004, 77, 13. [Google Scholar] [CrossRef]
  97. Klesse, S.; Ziehmer, M.; Rousakis, G.; Trouet, V.; Frank, D. Synoptic drivers of 400 years of summer temperature and precipitation variability on Mt. Olympus, Greece. Clim. Dyn. 2015, 45, 807–824. [Google Scholar] [CrossRef]
  98. Strid, A. The botanical exploration of Greece. Plant Syst. Evol. 2020, 306, 27. [Google Scholar] [CrossRef]
  99. Donovan, L.; Grise, D.; West, J.; Pappert, R.; Alder, N.; Richards, J. Predawn disequilibrium between plant and soil water potentials in two cold-desert shrubs. Oecologia 1999, 120, 209–217. [Google Scholar] [CrossRef]
  100. Kavanagh, K.; Bond, B.; Aitken, S.; Gartner, B.; 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] [Green Version]
Plants 11 01013 g001 550
Figure 1. Seasonal predawn (VPDp) and midday (VPDm) vapour pressure deficit and relative humidity (RH) in the study site, during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Figure 1. Seasonal predawn (VPDp) and midday (VPDm) vapour pressure deficit and relative humidity (RH) in the study site, during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Plants 11 01013 g001
Plants 11 01013 g002 550
Figure 2. Seasonal Photosynthetic Photon Flux Density (PPFD), leaf temperature (Tl), morning (Tp) and midday (Tm) ambient air temperature during the experimental period from 27 May to 28 August. The values are means ± SE (nTp,Tm = 24, nTl = 48).
Figure 2. Seasonal Photosynthetic Photon Flux Density (PPFD), leaf temperature (Tl), morning (Tp) and midday (Tm) ambient air temperature during the experimental period from 27 May to 28 August. The values are means ± SE (nTp,Tm = 24, nTl = 48).
Plants 11 01013 g002
Plants 11 01013 g003 550
Figure 3. Principal component analysis (PCA) loading plot representing the variables and the species characterizing the two components. Black dots indicated predawn (Ψp) and midday (Ψm) leaf water potential, midday transpiration rate (E), midday stomatal conductance (gs), midday leaf hydraulic conductance (KLeaf) and midday vapour pressure deficit (VPDm); brown squares indicated the deciduous species: Coronilla emeroides (C.e.), Carpinus betulus (C.b.), Pistasia terebinthus (C.t.). Cercis siliquastrum (C.s.), while green triangles indicated the evergreen species: Arbutus unedo (A.u.), Arbutus adrachnae (A.a.), Quercus coccifera (Q.c.) and Quercus ilex (Q.i.).
Figure 3. Principal component analysis (PCA) loading plot representing the variables and the species characterizing the two components. Black dots indicated predawn (Ψp) and midday (Ψm) leaf water potential, midday transpiration rate (E), midday stomatal conductance (gs), midday leaf hydraulic conductance (KLeaf) and midday vapour pressure deficit (VPDm); brown squares indicated the deciduous species: Coronilla emeroides (C.e.), Carpinus betulus (C.b.), Pistasia terebinthus (C.t.). Cercis siliquastrum (C.s.), while green triangles indicated the evergreen species: Arbutus unedo (A.u.), Arbutus adrachnae (A.a.), Quercus coccifera (Q.c.) and Quercus ilex (Q.i.).
Plants 11 01013 g003
Plants 11 01013 g004 550
Figure 4. Seasonal (a) predawn (Ψp) and (b) midday (Ψm) leaf water potential of deciduous and evergreen shrubs during the experimental period from 27 May to 28 August. The values are means ± SE (n = 24).
Figure 4. Seasonal (a) predawn (Ψp) and (b) midday (Ψm) leaf water potential of deciduous and evergreen shrubs during the experimental period from 27 May to 28 August. The values are means ± SE (n = 24).
Plants 11 01013 g004
Plants 11 01013 g005 550
Figure 5. Seasonal transpiration rate (Ε) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Figure 5. Seasonal transpiration rate (Ε) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Plants 11 01013 g005
Plants 11 01013 g006 550
Figure 6. Seasonal stomatal conductance (gs) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Figure 6. Seasonal stomatal conductance (gs) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. The values are means ± SE (n = 24).
Plants 11 01013 g006
Plants 11 01013 g007 550
Figure 7. Seasonal midday vapour pressure deficit (VPDm) and leaf hydraulic conductance (KLeaf) of the considered deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. Values are means ± SE (nKleaf = 24, nVPDm = 48).
Figure 7. Seasonal midday vapour pressure deficit (VPDm) and leaf hydraulic conductance (KLeaf) of the considered deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. Values are means ± SE (nKleaf = 24, nVPDm = 48).
Plants 11 01013 g007
Plants 11 01013 g008 550
Figure 8. The relationship between midday leaf water potential (Ψm) and hydraulic conductance (KLeaf) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. Values are means ± SE (n = 24). Polynomial regression analysis was used to assess the relationship between KLeaf and Ψm.
Figure 8. The relationship between midday leaf water potential (Ψm) and hydraulic conductance (KLeaf) of deciduous and evergreen shrubs during the experimental period, from 27 May to 28 August. Values are means ± SE (n = 24). Polynomial regression analysis was used to assess the relationship between KLeaf and Ψm.
Plants 11 01013 g008
Plants 11 01013 g009 550
Figure 9. Ombrothermic diagram in the study area throughout a year.
Figure 9. Ombrothermic diagram in the study area throughout a year.
Plants 11 01013 g009
Table
Table 1. Mean values of predawn (Ψp) and midday (Ψm) leaf water potential, midday transpiration rate (E), midday stomatal conductance (gs), midday leaf hydraulic conductance (KLeaf) and midday vapour pressure deficit (VPDm) in deciduous and evergreen shrubs during the study period.
Table 1. Mean values of predawn (Ψp) and midday (Ψm) leaf water potential, midday transpiration rate (E), midday stomatal conductance (gs), midday leaf hydraulic conductance (KLeaf) and midday vapour pressure deficit (VPDm) in deciduous and evergreen shrubs during the study period.
ParameterDeciduousEvergreensp-Value
Mean ± SEMean ± SE
Ψp (MPa)−0.94 ± 0.04−1.04 ± 0.030.876 NS
Ψm (MPa)−2.09 ± 0.06−2.53 ± 0.050.001 **
E (mmol m−2 s−1)16.12 ± 0.8915.87 ± 0.680.734 NS
gs (mmol m−2 s−1)575.97 ± 21.00585.5 ± 27.930.487 NS
KLeaf (mmol MPa−1 m−2 s−1)17.18 ± 1.4513.15 ± 1.570.033 *
VPDm (kPa)2.79 ± 0.132.67± 0.110.149
* Significant for p < 0.05, ** significant for p < 0.001, NS—nο significance. Μean values were compared with independent samples Student’s t-test.
Table
Table 2. Pearson correlation between predawn (Ψp) and midday leaf water potential (Ψm), transpiration rate (E), stomatal conductance (gs), leaf hydraulic conductance (KLeaf) and midday Vapour Pressure Deficit (VPDm) for deciduous (left) and evergreen (right) shrubs.
Table 2. Pearson correlation between predawn (Ψp) and midday leaf water potential (Ψm), transpiration rate (E), stomatal conductance (gs), leaf hydraulic conductance (KLeaf) and midday Vapour Pressure Deficit (VPDm) for deciduous (left) and evergreen (right) shrubs.
DeciduousΨpΨmEgsKLeafVPDmEvergreens
Ψp10.387 **0.020−0.139−0.039−0.108Ψp
Ψm0.524 **1−0.311 **−0.1620.544 **−0.451 **Ψm
E0.234 *−0.0131−0.328 **0.1350.147E
gs0.357 **0.620 **−0.1101−0.0370.157gs
KLeaf0.0840.478 **0.562 **0.2091−0.298 **KLeaf
VPDm−0.088−0.443 **0.271 **−0.315 **−0.1471VPDm
* Significant for p < 0.05, ** significant for p < 0.001.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Karatassiou, M.; Karaiskou, P.; Verykouki, E.; Rhizopoulou, S. Hydraulic Response of Deciduous and Evergreen Broadleaved Shrubs, Grown on Olympus Mountain in Greece, to Vapour Pressure Deficit. Plants 2022, 11, 1013. https://doi.org/10.3390/plants11081013

AMA Style

Karatassiou M, Karaiskou P, Verykouki E, Rhizopoulou S. Hydraulic Response of Deciduous and Evergreen Broadleaved Shrubs, Grown on Olympus Mountain in Greece, to Vapour Pressure Deficit. Plants. 2022; 11(8):1013. https://doi.org/10.3390/plants11081013

Chicago/Turabian Style

Karatassiou, Maria, Panagiota Karaiskou, Eleni Verykouki, and Sophia Rhizopoulou. 2022. "Hydraulic Response of Deciduous and Evergreen Broadleaved Shrubs, Grown on Olympus Mountain in Greece, to Vapour Pressure Deficit" Plants 11, no. 8: 1013. https://doi.org/10.3390/plants11081013

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

Article Metrics

Back to TopTop