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Keywords:

  • hydraulic parameters;
  • Laguncularia racemosa;
  • leaf anatomy;
  • leaf hydraulics;
  • mangroves;
  • salinity;
  • vessel dimensions;
  • xylem anatomy

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References
  • • 
    The purpose of this study was to investigate the xylem anatomy and hydraulic characteristics of the mangrove Laguncularia racemosa grown under contrasting salinities. The study addressed the hypothesis that, at high salinity, water transport capacity may decrease in association with higher water use efficiency.
  • • 
    Plants were grown in media to which 0, 15 and 30 NaCl was added. Vessel density and diameter were determined in transverse sections of stem and midrib leaves in terminal shoots, and hydraulic parameters were measured.
  • • 
    In stems, the vessel density increased with salinity, while the anatomical diameter (da) and hydraulic diameter (dh) declined; in leaves, these parameters remained unchanged with salinity. Huber value and hydraulic and specific conductivities decreased with salinity. Leaf blade resistance increased with salinity and represented the largest fraction of twig resistance.
  • • 
    Xylem anatomy and leaf tissue of L. racemosa appeared to be modulated by salinity, which led to a coordinated decline in hydraulic properties as salinity increased. Therefore, these structural changes would reflect functional water use characteristics of leaves under salinity.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References

Among phylogenetic groups, xylem structure varies, which affects water transport capacity and embolism vulnerability (Bolton & Robson, 1988; Lindorf, 1994; Tyree et al., 1994; Tyree & Zimmerman, 2002; Choat et al., 2005; Hacke et al., 2006). Consequently, xylem conduit evolution from hydroids through tracheids to vessels reflects the trade-off between resistance to implosion and cavitation and maximum hydraulic conductance (Sperry, 2003). Xylem characteristics have been related to leaf structure and habitat as well (Rury & Dickinson, 1984; Guthrie, 1989; Sack et al., 2005). Consequently, the ability of xylem to support negative pressure varies with the particular environmental constraints of a given species (Sperry & Tyree, 1990).

Mangroves are characterized as thriving under saline conditions, where large leaf-soil pressure gradients are required for water uptake to maintain transpiration rates (Scholander et al., 1962). These allow mangroves to maintain water uptake in substrates with high osmotic pressure without apparent xylem cavitation (Sperry et al., 1988; Becker et al., 1997; Sobrado, 2000, 2001; Melcher et al., 2001; Ewers et al., 2004). In addition, leaf water use in mangrove species becomes highly conservative as salinity increases (Ball, 1996). Their water transport efficiency has been related to leaf water use efficiency under field conditions (Sobrado, 2001).

Laguncularia racemosa is an important component of mangrove forests present on the American continent as well as West Africa (Duke et al., 1998). However, the physiology of L. racemosa has been less studied than other mangrove species in these biogeographical regions, such as Rhizophora mangle and Avicennia germinans. L. racemosa is a leaf salt-secreting mangrove thriving in habitats with contrasting salinities (Tomlinson, 1986). When salinity increases, its leaves become conservative in water use (Sobrado, 2005), which would contribute to the avoidance of excessive large tensions to maintain water uptake. L. racemosa has been reported to be highly vulnerable to xylem embolisms (Ewers et al., 2004). Furthermore, the response of conduit size and number to changes in leaf water use efficiency is important because it spreads the hydraulic load over the entire transport system. This would reduce the probability of the hydraulic system reaching the point of catastrophic xylem failure (Kocacinar & Sage, 2005). Therefore, the purpose of this study was to investigate xylem anatomy and hydraulic characteristics of L. racemosa grown under contrasting salinities. The study addressed the hypothesis that, as salinity increases, water transport capacity may decrease in association with the higher water use efficiency observed at high salinity. Terminal branches were used because they are the most likely ones to fail under an extreme water potential drop.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References

Plant material

Four-yr-old plants of Laguncularia racemosa (L.) Gaertn (Combretaceae) were maintained in 5 l pots filled with sand, in a glasshouse under natural sunlight and photoperiod. The pots were placed on trays 10 cm high to maintain a constant water supply. Additionally, the soil surface was covered with a plastic sheet to avoid evaporation. Soil salinity was checked and adjusted twice weekly by using solutions prepared with marine salt and amended with nutrients. Three groups of 10 plants each were grown in 0, 15 and 30 NaCl. For all the measurements, young peripheral and sun-exposed shoots bearing three to four leaf pairs were used. These terminal shoots are the most vulnerable part of plants because of the low tensions likely to be present in their vessels (Yang & Tyree, 1994; Tyree & Zimmerman, 2002).

Stem and leaf anatomy

Transverse sections of stem segments from four plants of each group were manually sliced, stained with toluidine blue (0.5%) and mounted permanently in glycerol. Photographs were taken with a camera (MC80, Zeiss) attached to a microscope (Axioskop, Zeiss). Quantitative analysis was made on the photographic material. The cross-sectional area of stem and xylem tissue was measured. The number of vessels and diameter of each one were measured for each stem. The diameter (anatomical ratio; da) was calculated as the equivalent circle diameter. The variables used to characterize the twig xylem anatomy were vessel density (number of vessels mm−2), mean conduit diameter, predicted hydraulic conductance, and estimated mean hydraulic diameter. The sum of all vessel diameters to the fourth power (inline image) was used to predict hydraulic conductance according to the Hagen-Poiseuille Law (Sperry & Saliendra, 1994; Choat et al., 2005). The frequency distribution by da class was determined for each plant group. Similarly, the contribution to water conductance of each diameter class was expressed as a percentage of total inline image. The hydraulic diameter (dh) was calculated by weighting each conduit to its contribution to inline image by using the relationship inline image/inline image (Sperry & Sullivan, 1992; Sperry & Saliendra, 1994).

Leaf blade cross-sections parallel to the midrib were prepared from leaves collected from four plants of each group. Tissue from the leaf blade centre was dehydrated progressively in an ethanol series (70–100%) and infiltrated with warm (56–58°C) paraffin. Leaf slides of 2–3 µm were obtained with a rotary microtome (Leitz, Wetzlar, Germany). The slides were deparaffinized, rehydrated and stained with safranin/fast green (1% aqueous safranin and 0.5% fast green in 95% ethanol). The sections were mounted in glycerol, photographed and used to measure leaf thickness as well as the diameters of all the vessels in the midrib. Procedures for leaf xylem characteristics were similar to those for stem sections. Leaf pieces (1 × 1 cm) were treated with bleach (NaOCl) to eliminate the mesophyll tissue. Once the two epidermises were separated and the leaf mesophyll remains eliminated, the pieces were stained with toluidine blue and mounted in glycerol. From these leaf preparations, adaxial and abaxial stomata were counted for all treatments.

Hydraulic measurements

Measurements of branch hydraulic properties were performed with a high-pressure flowmeter (HPFM, Dynamax, Inc., Houston, TX, USA). The HPFM allows examination of the dynamics of water flow (F, kg s−1) through tissues as a function of the pressure difference causing the flow (P, MPa). These measurements allow calculation of absolute conductance through the tissue as the ratio of F : P, which may be normalized to leaf area (Ab). Further details of devices used in the assembly of HPFM as well as the methodological bases can be found elsewhere (Tyree et al., 1994b, 1995). Three to four stems for each of the 10 plants per treatment were sampled. Stems with a length of c. 40 cm were selected from the outer part of the canopy and stored in water. Before measurement, terminal shoots having three to five leaf pairs were cut under water to 20 cm. Natural apices of shoots were maintained to assure water flow only through leaves when required. Once mounted in the HPFM, stems were perfused at 0.5 MPa with distilled water filtered to 0.1 µm. This condition was maintained until the recorded flux remained constant, which took 30–60 min. Leaf infiltration was necessary to ensure that leaf water potential reach zero and the measured water flow was not the result of refilling dehydrated tissue. Measurements with leaves and without leaves were taken in each shoot and length (l), diameter and subtended leaf area (Ab) were determined. In shoots with leaves, the water flow (F+L) was recorded as a function of pressure difference (P) to determine whole-shoot resistance (Rws) as Rws = (P × Ab)/F+L. Afterwards, the leaves were removed from the shoot and the water flow (F–L) measured again as a function of pressure difference in order to calculate shoot resistance without leaves (R–L) as R–L = (P × Ab)/F–L. Whole-shoot leaf-specific hydraulic conductance (Kws) for each sample was calculated as 1/(R+L). The leaf blade resistance (Rb) was calculated as Rb = RwsR–L. Afterwards, Rb was expressed as percentage of Rws for each shoot. Leaf conductance (Kb) per unit of leaf area was calculated as Kb = 1/Rb. Hydraulic conductance of shoot stems was computed as Kh = (F–L × l)/P (l, segment length), specific conductivity as Ks = Kh/Ax (Ax = cross-section of xylem), and leaf specific conductivity as Kl = Kh/Ab. Huber values (Hv) were also calculated for each sample as cross-section of stem xylem per unit of leaf blade area (Hv = Ax/Ab).

K b was also estimated from midday water potential (Ψ) of uncovered and covered leaves (approx. xylem Ψ; Ψx), in conjunction with leaf transpiration (E). Pairs of adjacent twigs were tagged from the sun-exposed part of the canopy. One of the tagged twigs was bagged and covered with aluminium foil at predawn, while the other twig was left to transpire freely. Two pairs of measurements were taken from each of the 10 plants per treatment. Leaf Ψ was determined with a pressure chamber (Mod. 1400, PMS, Corvallis, OR, USA) and E was measured with a gas exchange equipment (Mod. LCA-2, ADC, Hoddesdon, England). Thus, Kb was calculated as E/(Ψx– Ψ). These values of Kb were compared with those obtained from HPFM.

Statistical analysis

Differences between the means of each parameter in the three treatments were examined using one-way analysis of variance (anova). After the homogeneity of variance was tested, least significant differences (LSD) were determined. The procedures followed Sokal & Rohlf (1995).

Results and Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References

The cross-sectional area (At) of terminal branches of L. racemosa declined slightly with salinity but this trend was not statistically significant (Table 1). However, the cross-sectional area of xylem tissue (Ax), as well as the percentage of stem cross-sectional area occupied by xylem tissue declined significantly (P < 0.05) with salinity (Table 1). Conversely, vessel density showed a clear increase under high salinity conditions. Both vessel anatomical diameter (da) and hydraulic diameter (dh) were larger in plants grown without salt than in both salt treatments (Table 1). Thus, da tended to decline significantly by c. 25% in both salinity treatments, and dh declined by c. 15 and 23% in plants grown at 15 and 30, respectively. Consequently, plants grown under salinity relied on abundant narrow vessels (Figs 1, 2). The clear salinity effect on vessel density and diameter was the result of a shift in the frequency and not in the absolute absence of larger vessels under saline conditions (Figs 1, 2). Under salinity, the xylem tissue was composed of more frequent vessels of small diameter (Figs 1, 2). Predicted hydraulic conductivity (inline image) per diameter class was also shifted towards narrow vessels in plants grown under salt conditions (Fig. 1). However, when the predicted hydraulic conductivity was expressed per xylem area (inline image)/(Ax), values tended to decline significantly under salt conditions (Table 1). This indicated that a higher density of narrow vessels would not compensate for larger vessels in terms of potential for water flow. Vessels with large diameter and pore size in intervessel pit membranes are evolutionarily favoured for efficient water conduction (Tyree et al., 1994). Thus, large vessels allow for low investment in xylem structures while maintaining high permeability. Salinity influences the anatomy of cambial derivatives in such a way that xylem vessels are more numerous and narrower than those found under nonsaline conditions (Kozlowski, 1997). Changes in the dimensions of vascular elements are explained by auxin concentrations (Aloni, 1980; Aloni & Zimmermann, 1983; Lev-Yadun & Aloni, 1995). When production of indol acetic acid (AIA) is high, xylem tissue contains many more and narrower vessels. Conversely, xylem tissue from plants with low auxin concentrations has fewer and wider vessels (Klee & Estelle, 1991). Additionally, tree age can lead to production of wider vessels (Tyree & Ewers, 1991; Cruizat et al., 2002). However, age effects were precluded as a cause in this study because plants were of similar age.

Table 1.  Influence of salinity on stem characteristics of Laguncularia racemosa: transverse area (At), xylem area (Ax), percentage of xylem tissue, anatomical (da) and hydraulic (dh) diameters, vessel density and predicted hydraulic conductance (inline image) per unit xylem area
ParameterSalinity
01530
  1. Values are means and standard errors (SE) of measurements taken in four plants. Means followed for different letters were statistically different at P < 0.05.

A t (× 10−6 m2)4.9 (0.3)4.3 (0.3)4.4 (0.2)
A x (× 10−6 m2)2.6 (0.2) a1.8 (0.1) b1.5 (0.1) c
Xylem tissue (%)52.9 (3.5) a41.9 (1.3) b34.9 (0.4) c
d a (µm)26.5 (0.9) a20.6 (0.5) b19.6 (0.6) b
d h (µm)41.9 (2.8) a35.6 (4.7) ab32.2 (1.9) b
Vessels/area (number mm−2)160 (36) a213 (44) ab258 (54) b
inline image/Ax (m2)192 (23) a134 (25) ab112 (25) b
image

Figure 1. Percentage of conduits in 10 µm diameter classes in the stems of Laguncularia racemosa grown at contrasting salinities (a, 0; b, 15; c, 30). Percentages based on total vessel number, closed bars; percentage of conductance based on the sum of all vessel diameters to the fourth power (inline image), open bars. This reflects the relative hydraulic importance of each diameter class as estimated by the Hagen- Poiseuille Law. The bars are the means (+ SE) of four plants.

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image

Figure 2. Stem cross-sections showing the xylem tissue details in Laguncularia racemosa plants grown without salt (a) or at 15 (b) and 30 NaCl (c), respectively. Bars, 100 µm.

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Stem hydraulic properties varied according to changes in xylem structure (Fig. 3). Thus, plants grown without salt had significantly greater Huber value (Hv), hydraulic conductivity (Kh) and specific conductivity (Ks), compared with plants grown at 15 and 30 NaCl. The Kl of L. racemosa also declined with salinity, suggesting that larger pressure gradients would be required to maintain high transpiration rates. Therefore, as salinity increased, water transport through the xylem was less efficient. The hydraulic parameters found in this study were of a similar order of magnitude as those reported for other tropical species (Zotz et al., 1998; Tyree & Zimmerman, 2002). The xylem hydraulic conductance resulting from vessel dimensions is a major factor in determining water potential drop in a transpiring plant (Tyree et al., 1994a). Thus, vessel cavitation has been related to interconduit pit diameter, which increases linearly with vessel diameter (Calkin et al., 1986; Tyree & Sperry, 1988; Lo Gullo et al., 1995; Martínez-Vilalta et al., 2002; Hacke et al., 2006). A trade-off between xylem conductivity and resistance to cavitation has been suggested in a number of studies (Tyree & Sperry, 1988; Sperry & Saliendra, 1994; Lo Gullo et al., 1995; Pockman & Sperry, 2000; Martínez-Vilalta et al., 2002; Tyree & Zimmerman, 2002). Risk of embolism could also be minimized in mangrove species because of diurnal regulation of conductivity through cycles of shrinking and swelling of hydrogels in the pit membranes (López-Portillo et al., 2005). Water conductance efficiency, provided by wider vessels, would be advantageous to L. racemosa grown without salt because a large plant water potential drop would not be required to assure high transpiration rates. By contrast, as soil salinity increases, water uptake would be limited by a low soil water potential which would require a large plant water potential decrease for water uptake by roots. However, salinity enhances short- and long-term leaf water use efficiency of L. racemosa (Medina & Francisco, 1997; Sobrado, 2005). Thus, selection for narrow vessels in response to improved leaf water use efficiency would reduce the risk of xylem embolisms in saline habitats.

image

Figure 3. Huber value, hydraulic conductivity (Kh), specific conductivity (Ks) and leaf-specific conductivity (Kl) of Laguncularia racemosa as a function of salinity. Values are means (+ SE) of 10 plants and SE. Different letters indicate significant differences (P < 0.05).

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Leaves of L. racemosa also showed significant changes in their morphology and anatomy with salinity (Table 2, Fig. 4). Leaf size tended to be smaller in plants grown under salinity. However, leaves had a higher water content on leaf area as well as on a dry mass basis, which resulted in thicker leaves (Table 2, Fig. 4). Conversely, the leaf area to dry mass ratio remained unchanged with salinity treatment. Stomatal density (adaxial plus abaxial) declined with salinity, but 60.7 ± 1.1% of the stomata were located in the abaxial surface in all treatments. The vessel density in the midrib did not show a clear trend with salinity (Table 2). Vessel da and dh in the midrib tended to increase slightly with salinity but this was not statistically significant (Table 2). Consistent with this finding, the frequency of vessel distribution did not change with salinity (Fig. 5). The predicted hydraulic conductivity per diameter class was also very similar in all treatments (Fig. 5). This suggested that the leaf midrib vein would provide comparable water transport capability for water flow in all treatments. Despite of this, the leaf blade thickness was affected by salinity.

Table 2.  Influence of salinity on leaf characteristics of Laguncularia racemosa: area per leaf (A), leaf area to leaf dry mass ratio (A/dm), water content on dry mass and area basis, leaf thickness, stomatal density, midrib anatomical (da) and hydraulic (dh) diameters, and vessel density
ParameterSalinity
01530
  1. Values are means (SE) measured in four plants. Means followed for different letters were statistically different at P < 0.05.

A (× 10−4 m225 (1) a22 (5) ab21 (1) b
A/dm (× 10−4 m2 g−172 (2)77 (2)75 (3)
W c (g g−1)2.2 (0.1) a3.1 (0.1) b3.5 (0.2) c
W c (g m−2)297 (7) a335 (6) a403 (25) b
Thickness (µm)326 (14) a445 (23) b635 (14) c
Stomata density (number mm−2)163 (25) a137 (16) ab118 (7) a
d a (µm)14.5 (0.7)15.7 (0.6)16.3 (0.6)
d h (µm)19.3 (1.6)19.9 (1.8)20.7 (0.4)
Vessels/area (number mm−2)965 (52)870 (60)951 (49)
image

Figure 4. Leaf blade cross-sections showing leaf thickness changes in Laguncularia racemosa plants grown without salt (a) or at 15 (b) and 30 NaCl (c), respectively. Bars, 200 µm.

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image

Figure 5. Percentage of conduits in 10 µm diameter classes in the leaf midrib of Laguncularia racemosa grown at contrasting salinities. Percentages based on total vessel number, closed bars; percentage conductance based on the sum of all vessel diameter to the fourth power (inline image), open bars. This reflects the relative hydraulic importance of each diameter class as estimated by the Hagen- Poiseuille Law. Bars are the mean (+ SE) of four plants.

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Leaf blade resistance (Rb) represents the largest fraction of whole-shoot resistance (Rws; Yang & Tyree, 1994; Sack et al., 2002). We found that Rb increased with salinity and became increasingly important in whole-shoot resistance as salinity increased (Fig. 6a). The Kb values measured with HPFM were slightly, but consistently, higher than those calculated with transpiration rates and midday water potential in covered and uncovered leaves from Table 3 (Fig. 6b). The HPFM may overestimate Kb because leaves were fully rehydrated before measurement. Additionally, Kb values from HPFM could be affected by the difference in the hydraulic pathway of leaf blades induced by positive pressure during HPFM perfusion, or by using branches with several leaves, as well as by taking measurements under full sunlight (Yang & Tyree, 1994; Sack et al., 2002; Tyree et al., 2005; Sack & Holbrook, 2006). Nevertheless, we found in L. racemosa that the trends of leaf blade conductances (Kb) measured with the HPFM were consistent across treatments with those calculated (Fig. 6b). In L. racemosa, Kb values were within the range reported in leaves from tropical woody angiosperms (Sack & Holbrook, 2006); Kb was negatively related to leaf thickness, while midrib xylem conductance remained unchanged. By contrast, across-species comparison has shown that midrib xylem conductance increases with leaf thickness, as a result of more and wider conduits (Sack & Frole, 2006). The Kb as determined here does not distinguish between vascular and mesophyll contributions to its value (Tyree et al., 1999). Considering that midrib xylem anatomy did not change with salinity but mesophyll thickness did, we can surmise that mesophyll tissue may have been responsible for Kb reduction with salinity as a result of the increased length of the extracellular and transcellular pathways.

image

Figure 6. (a) Influence of salinity on leaf blade conductance (Kb) measured with a high-pressure flow meter (HPFM, black bars) or calculated (white bars) with parameters from Table 3. (b) Resistance (R) of whole shoot (grey bars) and leaves (black bars) measured with a HPFM; percentages indicate the leaf contribution to whole-shoot resistance. Values are means (+ SE) of 10 plants. For each data set, means followed by different letters indicate statistically different values at P < 0.05.

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Table 3.  Influence of salinity on midday leaf water potential (Ψ) and transpiration rates (E) measured in plants of Laguncularia racemosa
ParameterSalinity
01530
  1. Measurements of Ψ were taken in leaves covered to avoid transpiration or left uncovered to transpire freely. These values were used to calculate leaf blade conductance (Kb; Fig. 6a). Values are means of measurements taken in 10 plants. Means followed by different letters were statistically different at P < 0.05.

Midday Ψ (MPa)
 Covered−2.2 (0.2) a−3.9 (0.2) b−4.8 (0.5) b
 Uncovered−2.4 (0.2) a−4.4 (0.2) b−5.3 (0.6) c
E (× 10−5 kg m−2 s−1) 9.4 (0.4) a 7.4 (0.5) b 6.0 (0.3) c

In conclusion, our results suggest that, in L. racemosa, the characteristics of stem xylem tissue and of leaf blade may be modulated by salinity. This leads to a coordinated decline in hydraulic properties of stem and leaves as salinity increases. In the absence of NaCl, the plants had a highly permeable tissue (wide vessels), enabling high flow rates. Under salinity, conversely, xylem tissue was less permeable, reducing the upper limit of water flow. Therefore, xylem structure would reflect the enhanced leaf water use efficiency found in L. racemosa under salinity. The association between hydraulic conductance of stems and functional water use characteristics of leaves could contribute to the ecological success of mangroves in general as well as of other halophyte species.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References

Financial support was provided by DID-USB (FT-2005/2006). I am pleased to thank Drs E. Raimundez and M. I. Camejo for allowing the use of the microscopic unit, Ms Norbelys Garcés for preparing the anatomical material and anonymous referees and Dr S. M. L. Ewe for critical review of this paper.

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  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. Acknowledgements
  7. References
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