Hydraulic Architecture and Xylem Sap Flow

For assessment of water potential gradients in plants as driving forces for xylem sap flow in trees Scholander and coworkers introduced the pressure chamber technique. In view of the particular situation of mangroves in their saline substratum they devoted much of their pioneering work to mangrove trees, where xylem tensions of 3.8-5.2 MPa were recorded and accepted as sufficiently exceeding the osmotic pressure of sea water (2.5 MPa) to produce the driving force for sap ascent and a transpiration stream according to the cohesion-tension theory (Scholander 1968; Scholander et al. 1965, 1966). Conversely, Zimmermann et al. (1994a, 2002) argue that the balancing pressure used in the pressure chamber technique overestimates xylem tension. Using staining techniques they detected high-molecular-weight polymeric polysaccharide-mucilage in the xylem vessels of Rhizophora mangle. They argue that such mucilage would tend to strongly support gas bubble formation, which would prevent stable xylem tensions larger than 0.1 MPa. Moreover, the mucilage would hinder a mass flow of water. Xylem conductivity would decrease with saps of extreme salinities controlled by swelling and shrinking of pectin-based hydrogels in the pit membranes (Lopez-Portillo et al. 2005), but also reduced leaf conductivity for water vapour with increasing salinity is involved due to stomatal regulation (Sobrado 2001). Zimmermann et al. (1994a, 2002) observed sap flow rates in mangrove trees of 0.05-0.14 mms-1 which they consider to be quite low.

They suggest then, that sap ascent is driven by gravity-independent streaming at gas/water interfaces (given by the gas bubbles) as well as a gradient of chemical activity of water established by the potentially highly hygroscopic mucilage attracting and holding the water. This raised much dispute in relation to the standard cohesion-tension theory of sap flow in the xylem (Zimmermann et al. 1994b; Tyree 1997; Losch 1998; Wei et al. 1999a,b), and although this is not the place to get involved in detail in this controversy it is noteworthy that mangroves are important players in this game. Thus, Becker et al. (1997) note that xylem clogging by mucilage in mangroves cannot be generalized and they report sap flow rates in mangrove trees of 0.09-0.16mms-1, which they think are not that low and compare well with those of other tropical trees. We may conclude with Becker et al. (1997) that "like plants of other vegetation types, mangrove species will probably exhibit a range of transpirational behaviours in response to their saline habitat once they have been more fully investigated".

Hydraulic architecture plays a large role in such comparisons (Ball 1996). Sobrado (2000) found that the hydraulic systems of the three mangrove species Avicen-nia germinans, Laguncularia racemosa and Rhizophora mangle were comparable to the lowest end of the range reported for tropical trees. Wood and bark anatomy are adapted to water availability, salinity and oxygen supply in relation to the frequency and duration of flooding periods (Yáñez-Espinoza et al. 2001). Specific hydraulic conductivity of leaves declines with increasing salinity (Lovelock et al. 2006b). Under salinity stress controlled by the phytohormone auxin trees tend to form xylem vessels with smaller diameters which also applies to mangroves (Junghans et al. 2006). Mangrove species of the Rhizophoraceae have smaller vessel diameters than non-mangrove species of the same family (Janssonius 1950).

7.3.3 Vivipary

Some mangrove species are viviparious (Fig. 7.7). After fertilization they develop from the zygotes as embryos and then seedlings, which grow out of the flowers and fruits and remain for some while on the mother plant. Once liberated the viviparious seedlings can establish directly in the sediment at low tide or float in the sea water and are dispersed. Establishment appears to be particularly important since traits related to it appear to be stronger predictors of distribution than those associated with dispersal (Clarke et al. 2001). In general, however, advantages of vivipary are not clear since it is observed in only some mangrove tree taxa (e.g. Rhizophora mangle).

7.4 Exclusion, Inclusion and Excretion of Salt

Mangroves, like all other halophytes (which are plants growing in saline habitats), utilize strategies where they function as

• salt excluders or

• salt includers with intracellular salt dilution (succulence) and compartmenta-tion,

• salt excluders or

• salt includers with intracellular salt dilution (succulence) and compartmenta-tion, and in addition operate with

• salt excretion

Salt exclusion normally only affords resistance against mild or intermediate salinity stress, mainly for osmotic reasons (see Box 6.1). In order to maintain osmotic balance and keep a water potential gradient from the substratum to the plants, salt excluding plants would have to synthesise alternative organic solutes, which would consume energy and tie-up a large amount of important resources in terms of carbon skeletons, nitrogen and sulphur (see Box 7.1). Thus, the alternative is salt inclusion whereby the salt itself is used as a readily available and "cheap" osmoticum. In species which have special salt glands on their leaves, surplus salt may be eliminated by salt excretion.

The relative effectiveness of these mechanisms is illustrated by comparing salt levels in the leaves and in the xylem sap of mangrove species with and without salt glands (Fig. 7.8). Species with salt glands appear to have higher salt concentrations in the xylem sap than species without salt glands. Analyses in the field suggest that Rhizophora mucronata, is a salt excluder as shown by the rather low Cl--levels in the xylem sap while Aegialitis annulata is a salt includer as indicated by the larger xylem sap Cl--concentration. In contrast to the salt excluder, A. annulata has salt glands and is capable of salt excretion. Irrespective of the large differences in xylem sap salt concentrations adult leaves had similar salt levels in both species. Hence, the different strategies for dealing with salt, whether by exclusion at the root level or excretion at the leaf level and dilution via succulence (see below) lead to the same salt level in leaves.

However, the distinction between salt excluders and salt includers is only relative. There is always some control of salt uptake at the root level. This is the case in all mangroves, and the salt concentration in the xylem sap is always much smaller than in seawater, where the Cl- concentration is over 500 mM (Scholander 1968; Fitzgerald and Allaway 1991). The levels of Na+ and Cl- in the xylem sap of the examples shown in Fig. 7.8 are five to more than ten times less than those of sea water, in contrast to the levels in leaves. Table 7.1 gives a compilation of NaCl-levels in 23 different mangrove species collected from all over the world. Generally, the salt concentrations in the leaves were similar to that of seawater. Deviations of tissue contents of Na+ and Cl- from the average contents of these ions in sea water are small and mostly not larger than ca. ±100mM although in some cases deviations of ca. +200mM and ca. -400mM have been reported (Table 7.1). This is

Fig. 7.8 Na+ and Cl- concentrations in leaves (white columns) and xylem sap (X, black columns) of mangrove tree species analysed in the field (Rhizophora mucronata, Aegialitis annulata: Atkinson et al. 1967) and grown in sea water in a glass house (Laguncularia racemosa, Aegiceras cor-niculatum: Polanía 1990), respectively, with and without salt glands, respectively, in their leaves. (From Lüttge 2002)

Fig. 7.8 Na+ and Cl- concentrations in leaves (white columns) and xylem sap (X, black columns) of mangrove tree species analysed in the field (Rhizophora mucronata, Aegialitis annulata: Atkinson et al. 1967) and grown in sea water in a glass house (Laguncularia racemosa, Aegiceras cor-niculatum: Polanía 1990), respectively, with and without salt glands, respectively, in their leaves. (From Lüttge 2002)

due to accumulation of salt from the lower concentrations in the xylem sap into the leaf cells which is fast during leaf expansion but continues gradually in mature and senescing leaves (Cram et al. 2002). However, a comparison of salt concentrations in the xylem sap and in the sea water rooting medium shows that strictly speaking at the root level all mangroves are salt excluders. This can add to salinization of the substratum, which, may have ecophysiological implications for photosynthetic CO2-uptake and transpiration (Passioura et al. 1992; see Sect. 7.5.1). Salt accumulation in the leaves almost equally affects both ions Na+ and Cl- with a small tendency to a larger Cl- accumulation. While the average Cl-/Na+ -ratio in sea wa-

Fig. 7.9A, B Cross-sections of a young (A) and a mature (B) leaf of the mangrove Sonneratia sp. The mature leaf is much thicker, having a much larger water content to area ratio (= leaf succulence) due to enlargement and high vacuolization of the inner mesophyll cells. (Lear and Turner 1977, with kind permission of University of Queensland Press)

Fig. 7.9A, B Cross-sections of a young (A) and a mature (B) leaf of the mangrove Sonneratia sp. The mature leaf is much thicker, having a much larger water content to area ratio (= leaf succulence) due to enlargement and high vacuolization of the inner mesophyll cells. (Lear and Turner 1977, with kind permission of University of Queensland Press)

ter is ca. 1.2, the Cl-/Na+ -ratios of the mangrove trees shown in Table 7.1 average at 1.4 ± 0.2, with the exception of the three species where the salt content was ca. 400 mM less than that of sea water.

Many mangrove tree species can also grow in fresh water and behave as facultative halophytes. As in other halophytes, up to a certain level salinity stimulates growth, but high salinities inhibit growth to different extents in different mangrove species (Ball 1996, 2002). The optimum salt concentration for growth may be well below the NaCl-concentration of sea water, e.g. in the mangrove tree Avicennia ger-minans it was found to be at 170 mM and higher concentrations (680 and 940 mM) were inhibitory (Suarez and Medina 2005). Thus, there is a range of comportments from moderate to high salt tolerance and obligate halophily (Ball 1996).

Salt accumulation as a consequence of salt inclusion and the concentrating effect of transpiration has important correlates at the cellular level, namely salt compart-mentation and dilution. Salt is sequestered (compartmented) in the cell sap vacuoles where it can be diluted by osmotic uptake of water. However, this requires an increased volume if the overall salt concentration were to be maintained at a constant level. Therefore, such salt dilution is associated with succulence ("salt succulence"), with the formation of large central vacuoles. This supports maintenance of water relations and turgor pressure according to the relationship

where f is water potential, P turgor potential and n osmotic potential (see Box 6.1). Succulence of mangrove leaves may increase as leaves age (Cram et al. 2002), and

Fig. 7.10 Cl- content (molm-2 leaf surface) and Cl- concentration (moll-1 tissue water at saturation) in leaves of the mangrove La-guncularia racemosa related to the degree of succulence. The latter is given by the ratio of the leaf-water content at water saturation and the surface of both sides of the leaves (kgm-2). (After Biebl and Kinzel 1965, from Kinzel 1982, with kind permission of the author and R. Ulmer)

0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 Degree of succulence ( kg rrf2)

0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 Degree of succulence ( kg rrf2)

this is mainly due to an enlargement of leaf cells, providing larger vacuoles in which salt can be accumulated and diluted to some extent (Fig. 7.9). Thus, the total chloride content of leaves, when expressed on a leaf area basis, increases considerably, whereas chloride concentration remains rather constant as succulence increases. This clearly demonstrates the dilution effect enabled by succulence (Fig. 7.10). An anatomical disadvantage of salt succulence is a reduction of CO2-diffusion within the leaves to the chloroplasts decreasing photosynthetic capacity (Parida et al. 2004a).

Box 7.1 Compatible Solutes

Box 7.1 Compatible Solutes

As for all halophytes, the cytoplasm, the enzymes and membranes of mangrove cells are as equally sensitive to higher Na+ -concentrations as those of glycophytes (Ball and Anderson 1986; Sommer et al. 1990). Due to their large hydration shells, Na+ ions disturb the molecular water structures, i.e. the specific arrangement of the dipole molecules of H2O at the surfaces of proteins and membranes. This leads to the requirement for compartmentation. The NaCl taken up is sequestered in the vacuoles, where it is accumulated and may be effectively diluted as shown above. However, an osmotic balance is required in the cytoplasm because turgor pressure (Eq. 7.1) can only build up at the plasmalemma/cell wall boundary. The tonoplast membrane itself does not offer enough elastic resistance, and there can not be a gradient of n across the tonoplast, i.e. ncytoplasm must equal nvacuole. To this end, halophytes normally synthesise small organic molecules which serve as osmolytes, and are also called compatible solutes, as they both serve as cytoplasmic osmotica and are compatible with water structures. Their function in stabilizing cytoplasmic water structures is based on their molecular electron and charge distribution being similar enough to water-dipoles to be compatible with maintenance of cytoplasmic structures. Box 7.1 presents a variety of compounds, which are known to function as compatible solutes. Sorbitol, mannitol and pinitol are particularly frequent among mangroves (Popp 1984; Popp and Polania 1989; Richter et al. 1990). Accumulation of compatible solutes in the cytoplasm alone is much more efficient in terms of resources and energy needed than if organic molecules were used throughout the whole cell as osmotica to withstand salt stress of the medium. In succulent tissues the relative volume of the cytoplasm is only 1 - 2% of the total cell volume, so that vacuolar salt accumulation accompanied by cytoplasmic accumulation of compatible solutes is a very cost effective mechanism of osmotic adjustment.

Fig. 7.11A-F Development of the salt gland hairs of the mangrove Avicennia marina. A-E various stages of development. F Mature salt gland (Fahn and Shimony 1977, with kind permission of the author and Linnean Society). A Terminal cell; Ba basal cell; C cuticle; E epidermal cell; S secretory cell; St stalk cell; W cell wall

Fig. 7.11A-F Development of the salt gland hairs of the mangrove Avicennia marina. A-E various stages of development. F Mature salt gland (Fahn and Shimony 1977, with kind permission of the author and Linnean Society). A Terminal cell; Ba basal cell; C cuticle; E epidermal cell; S secretory cell; St stalk cell; W cell wall

Fig. 7.12 Leaves of Avicennia germinans with salt crystals (above) and dissolving salt at high air humidity (below)

The mechanism of salt excretion by glands has been studied extensively in nontropical halophytes (Luttge 1975). It is an energy dependent, active transport process, moving ions against large gradients of their electro-chemical potential. Figure 7.11 shows the development of the glandular hairs of the mangrove Avicennia marina (Fahn and Shimony 1977). The mature salt gland is covered and encircled by a cuticle, so that an apoplastic, cell-wall route of salt excretion is not available (Fitzgerald and Allaway 1991). The salt is moved via basal cells, often called "collecting cells", and stalk cells to the secretory cells, which excrete it into a subcuticular space at the head of the gland. Water follows osmotically. The pressure of the excreted fluid increases in the subcuticular space, and the salt is eventually released through pores in the cuticle opening under the hydrostatic pressure. During hot and dry days numerous salt crystals form on the leaves as the excreted salt solution dries (Fig. 7.12). Conversely, in the early morning, when air humidity is high, the excreted salt on the leaf surface hygroscopically absorbs water and a salty "rain" may drip down from the mangrove trees.

Excretion is also under adaptive regulation. With increases of xylem osmolality due to drought in Avicennia germinans (Sobrado 2002) or salinity in Laguncularia racemosa (Sobrado 2004) excretion tends to rise exponentially (Fig. 7.13), and at

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Renewable Energy 101

Renewable energy is energy that is generated from sunlight, rain, tides, geothermal heat and wind. These sources are naturally and constantly replenished, which is why they are deemed as renewable. The usage of renewable energy sources is very important when considering the sustainability of the existing energy usage of the world. While there is currently an abundance of non-renewable energy sources, such as nuclear fuels, these energy sources are depleting. In addition to being a non-renewable supply, the non-renewable energy sources release emissions into the air, which has an adverse effect on the environment.

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