Seasonal Dynamics and Microenvironmental Drivers of Transpiration in Scrub Rhizophora mangle L. Trees from Yucatan

Abstract

Scrub mangrove forests, dominated by Rhizophora mangle L., are characterized by high porewater salinity, which might compromise individual sap flow rates (SF) due to seasonal and diurnal microenvironmental variations. We tested the functional, anatomical, and SF responses of 12 individuals to microenvironmental variables such as solar radiation, photosynthetic photon flux, wind speed, evaporative demand, and porewater salinity, measured using an in situ weather station. Measurements were made in the dry and rainy seasons in the Yucatan Peninsula, using Granier heat dissipation sensors, installed on tree branches. During the rainy season, SF was twice as high as that during the dry season (0.22 ± 0.00 L h⁻¹ and 0.11 ± 0.00 L h⁻¹, respectively), despite lower evaporative demand. In both seasons, negative relationships between SF with vapor pressure deficit (VPD; dry τ = −0.54; rainy τ = −0.56) and with photosynthetic photon flux (PPF; dry τ = −0.97; rainy τ = −0.98) were found, indicating a strong hydraulic coupling to atmospheric conditions. Sap flow and transpiration rates of this R. mangle scrub mangrove forest exceeded those of some tropical dry deciduous forests, suggesting adaptations that support water transport in saline environments. The clustered xylem vessels of R. mangle ensure safe sap flow year-round. As an evergreen species, it contributes water to the atmosphere all year-round, underscoring its critical role in the tropical ecohydrological environment.

1. Introduction

Mangrove forests are wetlands found along tropical and subtropical coasts, whose species exhibit distinct morphological and physical traits to cope with factors such as hydroperiod, salinity, and microtopography [1]. Consequently, mangrove species occupy different ecological niches, thus determining the structure, composition, and attributes of mangrove forests. In the Yucatan Peninsula, there are four main ecological types of mangroves, i.e., fringe, basin, petén, and scrub [2,3]. Among these, the scrub mangrove has the widest distribution in the region. Each ecological type provides unique ecosystem benefits depending on its composition and environmental conditions [4,5,6].

Understanding the ecohydrological processes of scrub mangroves, particularly their contributions to transpiration and water exchange with the atmosphere, provides insights into how these ecosystems function under varying environmental conditions. This knowledge will provide information for conservation and management strategies for mangrove forests worldwide, related to the provision of ecosystem services and climate regulation at different scales, especially in the face of climate change and increasing anthropogenic pressures [7].

The environmental conditions of scrub mangroves are challenging due to high salinity and their dependence on freshwater inputs from precipitation. Indeed, Rhizophora mangle L. has unique adaptations to seawater conditions, particularly salinity and flooding levels. As a facultative halophyte, R. mangle is capable of coping with varying salinities by storing Cl⁻ and Na⁺ ions to maintain osmotic balance. These adaptations facilitate significant belowground carbon accumulation [8,9,10]. High evaporation rates, especially during drought, elevate porewater salinity levels, further impacting the vascular system. These forested wetlands are distinguished by a strong hydraulic connection along the soil–plant–atmosphere continuum that facilitates the continuous exchanges of freshwater and energy through transpiration. However, despite their significance, few studies have explored the contribution of transpiration to atmospheric water in mangrove forests [11,12,13,14,15,16,17].

Transpiration is regulated by stomatal conductance, which controls gas exchange, including CO₂ uptake and water release. Stomatal conductance is, in turn, influenced by environmental factors, including vapor pressure deficit (VPD), solar radiation (SR), and wind speed (WS) [18]. Exploring the balance between these processes is critical because they reveal how stomatal and canopy conductance are coupled with the atmosphere [19,20,21]. To document the variability in the rates of transpiration, sap flow measurements are an ideal tool, as they work as a key indicator of this hydraulic connection [22,23,24,25].

A significant amount of water is returned to the atmosphere through transpiration, accounting for up to 40% of the water supplied to land through precipitation and 70% of total evapotranspiration [26]. This process can be measured at different levels, including leaves, branches, trunks, whole plants, and ecosystems. Measuring transpiration at the individual plant level is particularly practical, as it exhibits less variability compared to leaf-level measurements [27].

Transpiration is closely linked to the transport of water from roots to leaves through the sap flow in the plant’s vascular system. Thermometric sap flow methods are widely used to measure these dynamics, as they provide insights into daily and interannual variations [26]. Moreover, sap flow measurements can be upscaled to the whole plant, enabling continuous quantification of the plant’s water use [28]. This information also allows estimation of the contribution of water to the atmosphere through transpiration.

On the other hand, the anatomical traits of the leaves and vascular system, such as the xylem, reflect the adaptations of R. mangle to flooded environments and high salinity in the porewater. Their leaves contain intercellular spaces formed by aerenchyma tissue, a type of parenchyma found in mangrove species, associated with the transport and movement of gases, as well as with the storage water within the parenchyma. This tissue also facilitates the movement of water vapor from the internal plant tissues to the atmosphere [29]. The characteristics of the xylem vessels, such as diameter, vessel density, and vessel grouping, provide valuable information about the plant’s hydraulic architecture, revealing its relationship with environmental variables, such as salinity, nutrients, and temperature [30]. Given that R. mangle plays a crucial role in ecohydrological processes, filtering seawater at the root level, which is subsequently transported to the leaves and released into the atmosphere as water vapor through transpiration [31], it is critical to understand the contribution of scrub mangroves, dominated by R. mangle, to the ecohydrological processes through transpiration, and to depict the intrinsic (anatomical and functional traits), as well as the extrinsic abiotic environmental factors that control both sap flow and transpiration [32,33,34]. Therefore, this research pursues the following aims: (1) to assess the diurnal and seasonal variation of sap flow; (2) to test the relationship of sap flow with microenvironmental variables, such as solar radiation, photosynthetic photon flux (PPF), VPD, porewater salinity, and wind speed; and (3) to estimate ecosystem transpiration based on sap flow. We hypothesize that, during the rainy season, lower VPD will result in decreased sap flow whereas, in the dry season, sap flow will be strongly influenced by solar radiation and VPD. Overall, our results will lead to refined ecohydrological models, taking into account the relevance of this vastly distributed ecosystem within the Yucatan Peninsula, as well as in other equivalent mangrove ecosystems in the tropics.

Mangrove forests play a critical role in mitigating climate change, maintaining biodiversity, and supporting ecosystem services, such as carbon storage and water cycling. Understanding the ecohydrological processes of scrub mangroves, particularly their contributions to transpiration and water exchange with the atmosphere, provides insights into how these ecosystems function under varying environmental conditions. This knowledge can inform conservation and management strategies for mangrove forests worldwide, especially in the face of climate change and increasing anthropogenic pressures.

2. Materials and Methods

2.1. Study Area

The Ría Celestun Biosphere Reserve was selected as the study area (Figure 1A). The area is characterized by a salinity gradient associated with the lagoon, where many ecosystems, such as deciduous forests, dunes and mangrove ecotypes are present, including fringe, scrub, petén and basin [35,36]. The Celestun reserve has a seasonal variation related to rainfall, distinguishing dry (March–May), rainy (June–October), and early dry (nortes; November–February) seasons. The porewater salinity during the rainy season in scrub mangrove ranges from 42.7–51.42 ppm, mean sediment water potential is −1.91 MPa, and a maximum vapor pressure deficit (VPD) range from 0.94 to 1.38 kPa [8]. The climate is predominantly semi-arid, with rain in the summer (767 mm mean precipitation) [35]. Most of this preserve is in good conservation condition. It has been designated as a Ramsar site (site no. 133) and is a long-term study site to understand the different ecosystem services that are provided locally and regionally [37,38].

2.2. Microenvironment

Microenvironmental data were collected in the study site (20° 51.400′ N, 90° 22.248′ W) during the dry (April) and rainy (October) seasons in 2021. Air temperature and relative humidity were measured with a temperature probe (12 bit temp/rh sensor S-TMB-M003, Onset Computer Corporation, Bourne, MA, USA), wind speed with a cup anemometer, wind direction with a wind vane (S-WCA-M003, Onset Computer Corporation, Bourne, MA, USA), photosynthetic photon flux (PPF) with a quantometer (S-LIA-M003, Onset, Bourne, MA, USA), solar radiation with a pyranometer (S-LIB-M003, Onset, Bourne, MA, USA) and dew deposition with a leaf wetness sensor (S-LWA-M003, Onset, Bourne, MA, USA) (this variable was only measured during the dry season based on the availability of the sensor). The data were recorded using a datalogger (U30-NRC Weather Station, Onset, Bourne, MA, USA) every 10 s and averaged in intervals of 10 min. The VPD was calculated according to ref. [40], as follows:

(1)$VPD=e_S\left(T\right)-e$

where e is the partial pressure of water vapor in air, and $e_S\left(T\right)$ is the saturation partial pressure of water vapor as a function of temperature. The saturation partial pressure $e_S\left(T\right)$ can be calculated using the following formula:

(2)$e_S\left(T\right)=6.112\cdot exp\left({\displaystyle \frac{18.678-\frac{T}{234.5}}{257.14+T}}\right)$

The partial pressure of water vapor $\left(e\right)$ is calculated as $e=RH{e}_S\left(T\right)$. The relation between air temperature (T) and relative humidity (RH) is known as evaporative demand due to the increase in the temperature.

A sample of porewater was drawn using an acrylic tube at a depth of 30 cm and salinity was measured with a multiparameter probe (Model Pro2030, YSI, Yellow Springs, OH, USA) at every sampled tree.

2.3. Sap Flow Measurements

Sap flux density (F_d) was continuously recorded for eight days during the dry and rainy seasons in branches of twelve individual trees, with mean diameter of 4.5 cm, using custom-made Granier [25] type sensors (Figure 1C). The selection of branches with these diameters was based on previous observations during a related study, where we noted that the conductive sapwood in R. mangle branches was sufficiently large to accommodate the temperature probes without exceeding the conductive portion. Pairs of 30-mm-long, 2-mm temperature probes were inserted into the sapwood of the branches. The upper probe was heated continuously with a constant power supply (0.2 W), supplied by a 12-V deep cycle marine battery connected to a solar panel, while the bottom unheated probe (10 cm below) recorded the sapwood temperature. This steady temperature approach allows for the identification of dynamic changes and low sap flow rates, reducing biases. The protruding portions of both probes were insulated with a layer of foam surrounded by an outer shield of reflective material and transparent plastic. Probe temperatures were recorded continuously at 10-s intervals with a datalogger (CR3000, Campbell Scientific, Logan, UT, USA), and 10-min averages were downloaded. Temperature differences between both sensor probes were used to calculate F_d (L m⁻² h⁻¹), using the following equation:

(3)$F_d=118.99\times {10}^{-6}{\left[{\displaystyle \frac{∆Tmax-∆T}{∆T}}\right]}^{1.231}$

where $∆$T_max is the maximum temperature difference between sensor probes at zero flux and $∆T$ is the temperature difference at a given F_d.

To calculate sap flow (SF), the sapwood cross-sectional area ($A_{sw}$) was determined by injecting vegetable dye into cores from branches, at the same height at which the sap flow sensors were installed, after the dry and rainy measurements were completed. The dye was allowed to move through the vascular system for one hour before extracting the cores using an increment borer (5.5 mm diameter, Haglöf, Längsele, Sweden). Then, the length of the sapwood was measured using a caliper (Scherr-Tumico, Syracuse, NY, USA), and the area ($A_{sw}$; cm²) was obtained using the following equation:

(4)$A_{sw}={\displaystyle \frac{\pi }{4}}(D^2-d^2)$

where π = pi value, D = larger diameter (cm), and d = shorter diameter (cm). Sap flow (SF; L h⁻¹) was calculated as follows:

(5)$SF=Fd\ast A_{sw}$

2.4. Transpiration

Transpiration per branch was estimated from sap flow (SF) scaled by the total leaf area (TLA) of the branch. The TLA was calculated by multiplying the branch’s canopy cover area by the leaf area index (LAI). The branch canopy cover area was mapped at ground level, and the LAI was measured using a Plant Canopy Analyzer (LAI-2200C, LI-COR Biosciences, Lincoln, NE, USA) by taking four measurements in the cardinal direction at 90°, with one additional measurement outside the canopy under full light conditions for reference.

Additionally, TLA was independently estimated by counting the total number of leaves on the branch and multiplying by the average leaf area measured with an area meter (LI-3100, LI-COR, Lincoln, NE, USA) [20].

Finally, transpiration per branch was multiplied by the branch density per hectare to upscale (E_L) the stand transpiration (mm day⁻¹). This approach allowed the integration of sap flow (SF) measurements to estimate transpiration at the stand level.

2.5. Vascular System and Leaf Anatomy

The wood samples of the 12 stems were collected at the end of the sap flow measurements. The wood segments were cut at a height of 1.3 m and 20 cm in length, then fixed in FAA (formaldehyde–ethanol-glacial acetic acid, distilled water 10:50:5:35) for 48 h. Afterward, they were washed with tap water and stored in glycerin–ethanol-distilled water (1:1:1) until sectioning. Each stem sample was sectioned into subsamples of 5 × 7 × 3 cm. Xylem transverse, radial and tangential sections were obtained using a sliding microtome (GSL-1, Swiss Federal Research Institute WLS, Birmensdorf, Switzerland) at a thickness of 50 µm. The sections were rinsed, bleached with commercial chlorine (50%), then washed with tap water. The sections were dehydrated in a degraded ethanol series through 50%, 70% and 95% and stored until sectioning. The sections were stained with safranin-fast green and mounted in synthetic resin.

The slides were observed with an Olympus optical microscope (U-CMAD3, Tokyo, Japan) with an integrated camera (Infinity 1, Teledyne Lumenera, Ottawa, ON, Canada). Six images were taken for each individual slide. The radial and tangential vessel diameter, lumen area, and the vessel density were measured. The obtained images were analyzed using ImageJ (U.S. National Institutes of Health, Bethesda, MD, USA).

During both the rainy and dry season measurements, three mature leaves per stem branch of the third order (considering the main axis as the first order) were collected, from which sap flow (SF) was measured. Immediately after cutting the leaves, they were fixed in FAA (formalin–ethanol-glacial acetic acid, distilled water 10:50:5:35) for 24 h. Afterwards, they were washed with tap water and stored in glycerin–ethanol-distilled water (1:1:1) until sectioning. Subsequently, leaves were infiltrated in a graded glycol–methacrylate (GMA) (7100, Techno-vit. Kulzer & Co., Hanau, Germany) [41] series from ethanol through 10%, 20%, 50%, 70%, 100%, embedded in glycol–methacrylate to obtain 3-μm-thick transverse sections with a rotatory microtone and stained with 0.6% brilliant cresyl blue. Next, the leaf samples were polymerized and mounted on wooden blocks to make cuts using the manual rotary microtome RM2125RT, Leica Biosystems, Richmond, IL, USA). The sections were stained on slides for observation under an optical microscope (Olympus, U-CMAD3, Tokyo, Japan) and photographed with an integrated camera (Infinity 1). The sub-stomatal cavity area was measured from eight slices of each individual. The obtained images were analyzed using ImageJ (U.S. National Institutes of Health, Bethesda, MD, USA).

2.6. Statistical Analysis

All collected data were subjected to normality and homoscedasticity using the Shapiro–Wilk and Levene tests, respectively. Data on SF and microenvironmental variables, such as VPD, SR, PPF, and dew, as well as F_d, SF, and transpiration, were separated into two groups based on the observed onset of SF movement: daytime (7:30–19:20 h) and nighttime (19:30–7:20 h). Microenvironmental variables, such as VPD, PPF, SR, and porewater salinity were compared between seasons for daily maximum values using the nonparametric Mann–Whitney U test. To evaluate daily and seasonal variability in sap flow, the interquartile range test (IQR) was applied. Linear and polynomial regressions were performed between SF and microenvironmental variables. The Generalized Additive Model (GAM) was used to test the hypothesis regarding the effect of microenvironmental variables on sap flow (SF) within seasons, as no linear relationship was observed between the predictor and response variables. The model was evaluated using the Generalized Cross-Validation (GCV) criterion, and the smooth functions helped prevent overfitting through penalization. Additionally, the model’s intercept represents the expected value of the response variable when the explanatory variables are zero, serving as a reference point to adjust the model and calculate the effects of the predictors. To assess the relationship between functional, anatomical and microenvironmental variables, mean values per season were analyzed using a Kendall correlation. Microenvironmental, SF and anatomical data were averaged over the same seasonal period to ensure temporal alignment for the correlation analysis. The substomatal cavity area was compared between seasons using the Mann–Whitney U test. All analyses were conducted using R language (4.3.2) [42].

3. Results

3.1. Microenvironmental Conditions

Significant differences were observed between seasons in the daily maximum values of the microenvironmental variables, including PPF, wind speed (WS), solar radiation (SR), and VPD (p < 0.001). Additionally, significant differences between seasons were detected in the daytime average values of these variables (p < 0.05; Table 1). Porewater salinity also differed between seasons (p < 0.001; Table 1).

3.2. Sap Flux Density, Sap Flow and Transpiration

Sap flux density (F_d) provided valuable insights into the intrinsic water transport capacity of the xylem. Seasonal differences in F_d were evident both during the daytime (p < 0.001) and nighttime (p = 0). During the rainy season, higher variability was observed during the day (IQR = 44.40) and night (IQR = 11.88) compared to the dry season (daytime IQR = 21.3; nighttime IQR = 1.68).

Sap flow (SF) values revealed significant differences in average daytime values between seasons (p = 0.001). When comparing nighttime SF values, sap movement was detected exclusively during the rainy season, which was highly significant (p < 0.001) (Figure 2A). The SF distribution displayed a bimodal pattern in both seasons, indicating distinct temporal dynamics (Figure 2B).

Differences in transpiration were primarily linked to increased leaf area index (LAI) during the rainy season. Transpiration varied significantly between seasons and between daytime and nighttime (p < 0.001).

3.3. Sap Flow and Microenvironment

Correlation analysis revealed distinct patterns in the relationships between variables across the dry and rainy seasons (Figure 3). During the dry season, a strong positive correlation was observed between SR and PPF (τ = 0.97), indicating a strong dependence of photosynthetic activity on light availability. Additionally, a significant negative correlation was found between xylem vessel density and xylem radial diameter (τ = −0.5), suggesting a potential hydraulic adjustment strategy in response to water stress (Figure 3A). During the rainy season, while the relationship between SR and PPF persisted (τ = 0.98), the correlation between xylem vessel density and xylem radial diameter (τ = 0.59) attenuated, and SF and VPD showed a strong correlation (τ = 0.56) which could indicate a shift in water conduction efficiency (Figure 3B).

Although the Kendall correlation showed a strong relationship between SF and PPF, the GAM analysis evaluated the effect of all the microenvironmental variables and detected that VPD was the main driver of sap flow in both seasons, as it allowed the modeling of nonlinear relationships. During the dry season, VPD showed a significant third-degree polynomial relationship with SF (p < 0.001), explaining 49% of its variability (adjusted R-squared = 0.47, intercept value = 0.05 ± 0.001, deviance explained of 48.9%) (Figure 4A). Dew also had a significant impact on SF (p < 0.001), with a second-degree polynomial relationship, suggesting the importance of water availability in modulating xylem transport (Figure 4E). Secondary effects were observed for SR, PPF, wind speed, and salinity, but their influence was weak (Figure 4B,C).

During the rainy season, VPD remained the only significant variable affecting SF (p < 0.001), with a nonlinear relationship that stabilized at higher values (Figure 5A). Other variables, including PPF, solar radiation, wind speed, and salinity, had no significant effect (p > 0.2) (Figure 5B–E). SF doubled during the rainy season compared to the dry season, highlighting the importance of atmospheric variables over porewater salinity in driving sap flow.

Additionally, SF exhibited a twofold increase during the rainy season when VPD, PPF and salinity were low. Despite the significance of salinity in mangroves, there is an insufficiently strong relationship between porewater salinity and SF in the dry and rainy seasons, emphasizing the importance of atmospheric variables in regulating SF depending on the seasonality.

3.4. Vascular System and Leaf Anatomy

Xylem vessel elements are principally grouped, rather than solitary (Table 2). During the dry season, SF was strongly and positively correlated with solar radiation, PPF and VPD; however, there was not a significant relationship between SF and the number of vessels during the dry season. In the rainy season, a negative correlation was observed between the number of vessels and tangential diameter (TD), whereas its correlation with porewater salinity was weak (Figure 6). In addition, the substomatal cavity area (µm²) was not affected by seasonality (dry season 5035 ± 351 µm²; rainy season 5077 ± 438 µm²) (p = 0.93) (Figure 6D).

4. Discussion

The sap flow (SF) of Rhiizophora mangle L. was strongly correlated with microenvironmental variables, such as VPD, PPF, and SR, which exhibited daily and seasonal variations, with lower values during the dry season compared to the rainy season. Additionally, total leaf area was 3.5 times greater during the rainy season than in the dry season, influencing transpiration at both the individual and stand levels. Notably, SF remained high during the rainy season, even at night, indicating continuous water uptake.

4.1. Sap Flow and Transpiration

Scrub mangroves exhibit a sympodial growth pattern (Aubréville’s model) instead of a monopodial pattern (Attim’s model), forming branches that grow to a certain extent before subdividing. This creates multiple pathways for water flow within the tree, influencing how sap flow is distributed and determining the hydraulic functions within the tree [2,43]. This architectural adaptation may play a significant role in the ability of scrub mangroves to transport water effectively, even under challenging environmental conditions.

Sap flux density (Fd) in scrub mangroves reached mean values of up to 49.34 g m⁻² s⁻¹ during the rainy season, which is notably higher than the 20 g m⁻² s⁻¹ reported for Byrsonima crassa (L.) Kunth in savanna ecosystems [44]. Species such as R. mangle and Laguncularia racemosa (L.) Gaertn have been reported to exhibit Fd values of 19.0 g m⁻² s⁻¹ and 26.1 g m⁻² s⁻¹, respectively, in mangrove ecosystems [12]. In contrast, our study found mean Fd values of up to 26.36 g m⁻² s⁻¹ for scrub mangroves during the dry season, aligning closely with these previously reported values. Furthermore, our study adjusted the Fd values to express transpiration as mmol m⁻² s⁻¹, considering the conductive area of the xylem, providing a more direct comparison with other reports.

Fringe or riverine mangroves with waterlogged soils and species like L. racemosa and R. mangle, of similar sizes to those in this study, exhibit comparable sap flow density (Fd) values. In contrast, Avicennia germinans L., which thrives under higher salinity conditions, shows lower Fd in both waterlogged and drained soils. This suggests that short-statured mangroves, with a high leaf area index, can efficiently mobilize water, even in saline environments, while more conservative ecotypes, like A. germinans, maintain lower water transport rates [12].

Scrub mangrove forests in the Sundarbans, averaging 5 m in height, have shown maximum evapotranspiration rates of 5.5 mmol m⁻² s⁻¹, which account for both transpiration and evaporation [45]. In our study, considering only transpiration, we recorded maximum values of 5.89 mmol m⁻² s⁻¹, indicating notably high transpiration rates. Upscaled sap flow in mangrove forests has been reported to reach values as high as 4 mm day⁻¹, while species such as Picea, Fagus, and Quercus in mature forests show average values of 2.5 mm day⁻¹ in some terrestrial ecosystems [46]. This comparison highlights the significant role that scrub mangroves of the Yucatan Peninsula play in filtering seawater and transporting it through their vascular system as sap flow, emphasizing their unique ecological importance.

It is essential to note that the magnitude of sap flow can vary depending on seasonal factors. Previous studies have shown that sap flow distribution in mangrove forests does not follow a normal distribution but is instead bimodal and highly influenced by seasonality [34]. This finding is consistent with our results, suggesting that seasonal variability must be considered when evaluating sap flow rates in these ecosystems.

Sap flow and transpiration in forests are regulated by plant diversity and physiology [47]. Previous studies have utilized various scales and techniques, including sap flow measurements and evapotranspiration estimates derived from eddy covariance methods, to quantify transpiration and evapotranspiration rates in mangroves and tropical forests [48,49,50,51]. Consistent with these studies, the stand transpiration values reported in our study are higher in both seasons (dry season: 1.8 mmol m⁻² s⁻¹; rainy season: 17 mmol m⁻² s⁻¹) compared to those observed in a tropical dry deciduous forest on the Yucatan Peninsula [52] (late dry season: 0.36 mmol m⁻² s⁻¹; late rainy season: 0.44 mmol m⁻² s⁻¹).

Burman et al. [53] reported that scrub Rhizophora spp. and Avicennia marina (Forssk.) Vierh. exhibited similar LAI values to those observed in this study. Additionally, using the eddy covariance method, they found that transpiration rates were higher than evaporation, even during the dry season. At least, despite the limitations of the Granier method, such as zero and reverse flows, it can detect high, medium, and low sap flow densities [54]. Furthermore, the steady-temperature approach in Granier probes minimizes the influence of heat storage in the trunk, thereby reducing bias in sap flow measurements [55]. Nighttime sap flow has also been reported using this methodology [56,57].

These findings contribute to a better understanding of the significance of transpiration in scrub mangrove ecosystems. Similarly, our results indicate that, during the rainy season, not only was higher sap flow recorded, but an increase in total leaf area was observed. This may be linked to enhanced carbon capture and storage in scrub mangroves of the Yucatan Peninsula.

4.2. Nocturnal Transpiration

Nocturnal transpiration is influenced by several factors, including nighttime stomatal opening, water recharge to restore embolisms, nutrient uptake, and carbohydrate transport [58,59,60]. This phenomenon has been documented in tropical ecosystems characterized by warmer or drier climates and nutrient-poor soils. Mangroves have been observed to sustain some water movement during the night [61,62]. In scrub mangrove species, such as Kandelia obovata (S., L.) Yong and Aegiceras corniculatum (L.) Blanco, nocturnal sap flow plays a critical role in water recharge, embolism repair, and water storage in parenchymal tissue [63]. Furthermore, Avicennia marina has been shown to absorb water through its leaves to repair embolisms.

Additionally, nocturnal transpiration in mangroves can vary by species and has been associated with increases in vapor pressure deficit (VPD) [64]. Nocturnal transpiration is crucial for several ecosystem processes, such as early morning carbon fixation, stomatal opening, oxygenation, and nutrient uptake. However, information on nocturnal transpiration in scrub mangrove species remains limited. Generally, sap flow at night remains unaffected unless extreme stress occurs, making nocturnal transpiration relatively stable under normal conditions. Neglecting nocturnal transpiration could result in underestimations of its contributions to ecosystem functioning [65,66].

Nighttime water movement also promotes hydrological connectivity within the ecosystem through hydraulic redistribution, facilitating water transfer between different soil layers or even neighboring plants [60].

4.3. Sap Flow and Microenvironment Relationships

Increases in VPD promote the column water maintaining stomatal closure; otherwise, transpiration rises, leading to reduced water potential and potential embolism formation [67,68]. This process may be more complex in environments such as mangrove forests, as suggested by our results, where seasonal variations in VPD, followed by changes in radiation and porewater salinity, influenced sap flow depending on seasonality [53,69]. Our findings indicate a coupling with the atmosphere, as suggested by the decreased sap flow and transpiration during the dry season.

Studies have explored the relationship between whole-tree canopy conductance, derived from sap flow, and VPD, identifying VPD as a main driver of water flow in trees [70,71]. However, in Indian mangroves, porewater salinity was strongly related to transpiration, with seasonal variations: during the pre-monsoon, the greatest amount of transpiration is released to the atmosphere, reducing the dry sensible heat from the soil to the atmosphere [72]. Globally, VPD is often the main driver of water flow in tree canopies, although this relationship varies across biomes [69]. In tropical mangrove forests, VPD, PPF, and soil water content (SWC) primarily influence sap flow [73,74,75,76,77,78]. Our study supports VPD as the main driver of sap flow in mangroves, accounting for seasonal variability.

The anatomical traits of the R. mangle xylem in the scrub mangrove ecotype showed a high vessel density and larger tangential and radial diameters compared to previous reports [9]. High vessel density is associated with efficient water transport, essential for coping with high porewater salinity and minimizing embolisms [79,80]. This adaptation, along with increased hydrostatic pressure and osmotic potential, facilitates water movement and distribution to leaves [81,82]. Scrub R. mangle exhibited a lower tangential and radial vessel diameter compared to the values reported by Cisneros-de la Cruz et al. [9] in adult individuals of the same species. The vessel density in this study was also higher than that of the previous study [9] (50.66 vessels/mm², compared to 32 vessels/mm²). Furthermore, compared with fringe mangroves of R. mangle, scrub R. mangle has higher vessel density and shorter tangential and radial diameters because of the lower salinity in the former mangrove ecotype. High vessel density, narrow vessel diameter, warm climate, and high salinity allow for a secure water transport capacity [9]. On the other hand, high vessel density is negatively correlated with the average vessel diameter (Figure 6), a trait closely associated with resistance to hydraulic dysfunction, which is reflected in the length of the conductive aboveground hydraulic pathways [83]. Given that the average tree height of the scrub mangroves is 2 m, it can be expected that individuals withstanding this environment should have more resistance to drought than taller trees in other geo-forms; however, to our knowledge, such a test has not been performed.

Drought resistance may involve strategies such as accelerated leaf senescence and cellular osmoregulation, which help limit transpiration [77]. Leaf senescence during drought conditions reduces water loss through transpiration [84]. In some species, leaves may exhibit differences in tissue responses to seasonal variations. The substomatal cavity influences transpiration and CO₂ assimilation. Reduced water availability can expand the cavity area, allowing for greater CO₂ storage [85,86,87]. Nevertheless, in this study, no differences were found in the substomatal cavity area between seasons, despite variations in the main driver, the VPD.

This finding is particularly relevant for scrub mangroves, as the lack of seasonal differences in substomatal cavity area suggests that they can continue capturing and storing carbon without limiting productivity. In fact, their carbon storage has been reported to be quite high, and greater than that of other mangrove ecotypes, due to their distribution [8]. This could be attributed to contrasting microclimatic conditions among ecotypes.

In this context, it can be observed that anatomical traits influence not only transpiration but also the carbon cycle. Moreover, the consistently large substomatal cavity in R. mangle across seasons suggests a stomatal coupling with the atmosphere that limits water loss, particularly during the dry season (Figure 6). Larger substomatal cavities and intercellular spaces can enhance internal CO₂ concentration, boosting photosynthesis while reducing water loss through transpiration, especially in drought-tolerant species [30,88,89,90].

It would be important to explore the relationship between substomatal cavity size and water exchange to better understand drought tolerance strategies [89,91]. Mangroves are known to be highly efficient in water use, a mechanism to cope with the high salinity of their habitats. Scrub mangroves are specialized for survival in high-salinity environments, playing a critical role in mitigating climate change by storing large amounts of belowground carbon [92]. Additionally, we highlight their significant role in the water cycle through transpiration.

The relationship between leaf area index (LAI) and the influence of VPD and SWC indicates that higher LAI weakens the relationship with VPD and SWC [93]. Nevertheless, in our research, during the rainy season, we observed an increase in LAI and a strong relationship with VPD, despite lower VPD values compared to the dry season. This suggests that increased LAI combined with low VPD might promote consistently higher levels of SF.

Other variables, such as salinity, wind speed, and dew, which did not show strong correlations with SF, might be more associated with other biogeochemical or physiological processes [94]. The study of sap flow and transpiration is critical due to its ecohydrological implications at both local and global levels in the water cycle, especially considering drastic seasonal changes driven by climate change [14,95]. Moreover, the humidity generated by plant transpiration can benefit the biodiversity of other plants, such as epiphytes, and various animal groups in mangrove forests (e.g., insects, vertebrates) [96,97]. Furthermore, transpiration and salinity are closely related to photosynthesis, impacting the carbon cycle [97,98]. The low availability of porewater during the dry season can affect the maintenance of the water column, especially when atmospheric evaporative demand is high. This promotes strict stomatal control to prevent excessive water loss [77,98,99]. However, because our research in scrub mangroves of R. mangle suggests that correlation of salinity with transpiration is not stronger enough, more research is needed.

Our results highlight the importance of scrub mangroves, which can show seasonal transitions, modulating their response based on soil water availability and the evaporative demand of the atmosphere. Although transpiration is low during the dry season, it remains continuous, while in the rainy season, it is compensated by higher transpiration, making it a key system for energy and ecohydrological balance, particularly in tropical areas, and in the context of climate change scenarios.

Considering that, in Celestún, the mean precipitation during the dry season is around 30 mm and increases to approximately 140 mm during the rainy season [100], this suggests that a significant amount of water is returned to the environment not only during the day but also at night. This underscores the ecological importance of scrub mangroves in water cycling. It is crucial to understand these aspects in other types of mangroves to ensure their conservation, as each provides unique ecosystem services. In this regard, protecting mangroves that regulate the local climate through transpiration not only helps to regulate climatic conditions but also benefits human communities and the biodiversity on which they depend for sustainable use.

5. Conclusions

Even when salinity is often regarded as a critical factor influencing sap flow in mangroves, our findings emphasize the importance of atmospheric variables, such as vapor pressure deficit (VPD), solar radiation, and photosynthetic photon flux (PPF), as significant determinants of sap flow variations. These atmospheric factors can have a substantial impact on sap flow, underscoring the need to account for multiple environmental variables when studying sap flow dynamics in mangrove ecosystems.

Seasonality plays a crucial role in sap flow variations, with the rainy season showing higher sap flow rates, increased transpiration (both day and night), and an expansion in total leaf area. These changes can have important implications for ecohydrological processes and energy balance. However, further studies are needed to fully understand these dynamics in mangroves, especially in ecosystems as widespread as those in the Yucatan Peninsula. Interestingly, the observed increase in nocturnal sap flow during the rainy season suggests hydraulic recovery and canopy leaf area growth strategies in scrub R. mangle, further suggesting adaptations not only to diurnal changes but also to seasonal variability.

The anatomy of the vascular system plays a crucial role in ensuring the safe transport of sap flow in scrub R. mangle, as it increases vessel density and decreases vessel diameter to prevent embolisms, regardless of seasonal changes. On the other hand, although there is no seasonal variation in substomatal cavity area, their large area promotes gas exchange, including water vapor, particularly during the rainy season.

This study underscores the significance of scrub R. mangle mangroves in Yucatán, not only due to their extensive distribution and substantial carbon storage but also for their contribution to atmospheric water flux through year-round transpiration, supported by their evergreen strategy. Understanding the role of transpiration in mangroves is crucial not only for regulating local climate but also for recognizing their potential in water filtration, particularly in coping with and mitigating salinity impacts. This knowledge could lead to increased efforts to harness mangroves for nature-based solutions (NbS), such as improving water quality in coastal zones.

Moreover, the carbon storage potential of mangroves, combined with their role in water filtration, opens the door for innovative market opportunities. For instance, mangrove forests could be integrated into emerging markets that connect global carbon markets with water-related services, creating a dual benefit for conservation and sustainable resource management. Understanding water-related processes in mangroves provides a baseline for expanding knowledge on the importance of these ecosystems, particularly concerning carbon storage, and can serve as a foundation for forecasting the future of these ecosystems under climate change scenarios. It will be crucial to integrate these findings into mangrove management strategies, focusing on enhancing their role in climate change mitigation and the potential development of markets around both carbon and water provisioning through effective conservation and restoration efforts.

Author Contributions

Conceptualization, methodology and supervision, G.C.-A., J.L.A., L.Y.-E. and J.A.S.-R.; field sampling, G.C.-A., R.U.-S., K.E.G.-M. and J.H.-S.; formal analysis, G.C.-A., K.E.G.-M. and J.A.S.-R.; writing–original draft, G.C.-A., J.L.A.; funding acquisition, G.C.-A., J.A.S.-R. and J.L.A.; and review and editing I.E.-M., R.M.-A. and J.H.-S. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

The original contributions presented in the study are included in the article; further inquiries can be made to the corresponding author.

Acknowledgments

We thank CONANP for the facilities provided to carry out the research. We also thank Jesús Garrido and Aarón Casanova for their great support with fieldwork. Our gratitude goes to Azucena Canto and Rosalina Rodríguez for their assistance with the use of the microscope.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Figures and Tables

Figure 1. Location of the study site is in the Celestun Biosphere Reserve. Yellow dots indicate the study site. Created with QGIS (3.22.14-Białowieża) [39] (A). Scrub R. mangle trees (B), Granier’s sensor probes (heat dissipation method) placed in the tree branches (C).

Figure 2. Diurnal mean patterns of sap flow (SF) measured over a continuous 8-day period during the dry and rainy seasons for R. mangle scrub mangroves. (A) Mean sap flow throughout a 24-h cycle. (B) Relative frequency of mean sap flow with a bimodal pattern in both seasons.

Figure 3. Kendall correlation matrix for environmental and anatomical variables and Sap Flow (SF) during both seasons. (A) Dry season; (B) Rainy season. Variables include Sap Flow (SF), Vapor Pressure Deficit (VPD), Solar Radiation (SR), Photosynthetic Photon Flux (PPF), and Wind Speed (WS).

Figure 4. Smooth effects of environmental variables on sap flow (SF) during dry seasons analyzed using Generalized Additive Models (GAM). (A) Effects of Vapor Pressure Deficit (VPD); (B) Photosynthetic Photon Flux (PPF); (C) solar radiation (SR); (D) wind speed (WS); (E) dew; and (F) porewater salinity.

Figure 5. Smooth effects of environmental variables on sap flow (SF) during rainy season analyzed using Generalized Additive Models (GAM). (A) Effects of Vapor Pressure Deficit (VPD); (B) Photosynthetic Photon Flux (PPF); (C) solar radiation (SR); (D) wind speed (WS); and (E) porewater salinity.

Figure 6. Stem secondary xylem: (A) transverse section showing diffuse porosity and vessel density, with a scale bar of 100 µm; (B) tangential section showing the scalariform perforation plate, scalariform intervascular pits of xylem vessels and wide xylem rays, with a scale bar of 50 µm; (C) radial sections showing detail of scalariform perforation plates overlapping at the tips of two vessel elements, with a scale bar of 10 µm; (D) dry season leaf transverse section showing epidermis, stomata, sub-stomatal chamber area (delimited by dotted line) and mesophyll parenchyma, with a scale bar of 100 µm. pp: perforation plates; f: fibers; ip: intervascular pits; ve: vessel elements; r: parenchymatous ray; sc: substomatal cavity; st: stomata; p: parenchyma.

Table 1

Microenvironmental variables, plant physiological variables divided by day and night, and upscaled sap flow per season. PPF: Photosynthetic Photon Flux; VPD: Vapor Pressure Deficit; Fd: Sap flux density. Data are presented as means ± standard error. Significant differences between seasons, revealed by Mann–Whitney U tests (p < 0.05), are indicated by an asterisk (*).

Variable	Season
	Dry	Rainy
Microenvironment
PPF (µmol m−2 s−1)	1989.4 ± 7.02 *	1123.54 ± 8.83
Solar radiation (W m−2)	1050.45 ± 6.04 *	526.33 ± 4.63
Air temperature (°C)	35.14 ± 0.96 *	31.19 ± 0.02
Relative humidity (%)	50.97 ± 4.20 *	65.5 ± 0.07
VPD (kPa)	2.88 ± 0.35 *	1.40 ± 0.05
Wind speed (m s-1)	2.69 ± 0.03 *	1.85 ± 0.02
Porewater salinity (ppm)	39.9 ± 3.00 *	28.66 ± 0.84
Plant physiology
Cumulative sap flow (L d−1)	8.14 ± 0.59 *	19.9 ± 1.9
Total leaf area	1.16 ± 0.24 *	3.97 ± 1.21
Leaf area index (m2 m−2)	1.39 ± 0.64 *	2.19 ± 0.33
Daytime
Fd (g m−2 s−1)	26.36 ± 0.24 *	49.34 ± 0.52
Sap flow (L h−1)	0.11 ± 0.00 *	0.22 ± 00
Transpiration (mmol m−2 s−1)	1.80 ± 0.958 *	17 ± 0.691
Nighttime
Fd (g m−2 s−1)	1.93 ± 0.04 *	11.25 ± 0.19
Transpiration (mmol m−2 s−1)	0.162 ± 0.0236 *	5.89 ± 0.184
Upscaled
Sap Flow (L h−1 ha−1)	3041.21	5767.82
Transpiration (mm day−1)	7.29	13.8

Table 2

Mean ± (standard error) of R. mangle stem xylem vessel traits.

Variables
Vessel radial diameter (RD)	59.55 µm ± 12.2
Vessel tangential diameter (TD)	59.45 µm ± 38.64
Lumen area (LA)	2582.95 µm2 ± 869.8
Vessel density	50.66 (no. of vessels mm2) ± 20.85

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