FIGURE 1. Radial ion profiles for vacuolar Na+ and K+ concentrations (mol m-3) of transversely fractured root cells of control (open circles) and salt-treated (closed circles) plants. GM: growth medium; EP: epidermis; OH: outer hypodermis; IH: inner hypodermis; C1, C2: first and second cortex cell row; ED: endodermis; PC: pericycle; XV: xylem vessels. From Werner and Stelzer, 1990.
exchange system in leaves. Any Na+ ions that evade the filtration system are thus gradually pushed back downwards to the roots. Figure 1 (from Werner and Stelzer, 1989) depicts Na+ and K+ concentrations measured at various layers of root tissue, starting at the growth medium and going inwards to the xylem vessels. The general trend seems that most Na+ and Cl- ions are filtered at the epidermis, and generally exhibit decreasing concentrations further inward. Werner and Stelzers' model includes the trapping of ions in the vacuoles of cortex cells. Each successive layer of the cortex is exposed to a lower concentration of ions. As the root elongates, ion-saturated filter cells are sealed by suberinization. Sodium ions that penetrate the ultrafilter must next pass through the xylem and the hypocotyl. Here Werner and Stelzer hypothesize ion pumps that act as a second Na+ barrier by transporting Na+ back down in exchange for K+ ions transported upwards. The third barrier is a similar ion exchange process inside the leaves.
This model suggests that metabolic processes play some role in overall salt regulation, in contradict Scholander's findings. Although Werner and Stelzer do not offer a complete explanation of the ultrafiltration mechanism, they offer a plausible model that can be tested experimentally.
Unlike the red mangrove, the black mangrove secretes excess salt through specialized glands on the surface of leaves in addition to carrying out root ultrafiltration. In the western Atlantic and Caribbean A. germinans typically grows further inland than R. mangle, often between zones of red and white mangroves (Laguncularia racemosa) (FMRI, 2001; SMSFP, 2001). The black mangrove is nearly as tall as the red mangrove, reaching heights of 15-20 m (Law and Arny, 2001; NHMI, 2001). Its root system employs pneumatophores rather than stilt roots (Figure 2). The black mangrove is found in the western Atlantic, Bahamas, Gulf of Mexico, and on the eastern Pacific coast including Ecuador, Peru, and Galapagos Islands (SMSFP, 2001; Dodd et. al., 2000; PUCNCPP, 1983a). The black mangrove is often found in more saline environments than the red mangrove, although their distributions may overlap across salinity gradients (Morrow and Nickerson, 1973).
FIGURE 2. Diagram illustrating typical differences between the pneumatophores (left) and the stilt roots (right)
FIGURE 3. Salt gland of A. germinans. SC: subtending cell; CO: collecting compartment; S: stalk cell; V: vacuole. From Dschida et. al, 1992.
Black mangrove roots can filter 90% of the salt from sea water (Tomlinson, 1986; Scholander, 1968), although some investigators report considerably smaller percentages, some as low a 30% (Field, 1984). To cope with the additional salt, the salt glands secrete solutions that evaporate, leaving behind salt crystals on the leaf surface (Tomlinson, 1986; Scholander et. al., 1962). Salt glands are microscopic and occur in epidermal depressions on the upper leaf surface. Each gland has 8-12 outer secretory cells, a lower stalk cell, and two to four other subtending, or basal cells, enclosed in a cuticle (Figure 3) (Dschida et. al., 1992). Evidence suggests that these salt glands, unlike the ultrafilter of R. mangle, rely on metabolic processes to function. The gland cells have elevated numbers of mitochondria, ribosomes, and other organelles (Tomlinson, 1986). They are impeded by metabolic inhibitors, implying a dependence on an energy source such as ATP (Dschida et. al., 1992).
Based on analysis of the application of specific metabolic inhibitors, Dschida et. al. (1992) suggest ions are actively transported from mesophyll cells into the gland across the basal cell membrane. Their analysis also suggests that mitochondria provide the energy source for sustaining secretion. Furthermore, it is highly possible that "an electrochemical potential established by H+ ATPase underlies the secretory process" (Dschida et. al., 1992).
Dschida et. al. also investigated the relationship of glandular secretion to changes in physiological inputs. Peels of adaxial leaf surfaces were floated on treatment solutions containing various concentrations of NaCl, and exposed to different temperatures. Volume of secretion varied directly with temperature, and varied indirectly with NaCl concentration. The rate of Cl- secretion peaked at a NaCl concentration of approximately 100 mol m-3 (Figure 4). These findings suggest the salt glands respond to the need to conserve water under saline conditions by secreting Cl- more efficiently. It would be interesting to compare the NaCl concentration of xylem sap reaching the leaves to the NaCl concentration of peak Cl- secretion reported by these investigators.
COMPARISON OF STRATEGIES
Some of the main differences between the mangroves include the types of mechanisms employed, the effectiveness of mechanisms, metabolic requirements, and osmotic potential of xylem sap. Based on the literature reviewed, the salt glands of A. germinans probably have a higher metabolic cost than the ultrafilter of R. mangle. This may be a factor in the zonation of these two species. For instance, R. mangle is often found closest to the coastline or in brackish water upstream from river mouths. Here one might expect the roots to encounter water that circulates more freely, preventing ion buildup around the roots. Further inland, where A. germinans is usually found, repeated inundations and draining can cause groundwater to become hypersaline (Morrow and Nickerson, 1973). The more saline the groundwater, the more negative the osmotic potential needed in the xylem sap of the tree to maintain water flow. Since R. mangle has a more effective ultrafilter, the water potential of its sap would be expected to be less negative. Indeed, xylem sap of A. germinans has an osmotic potential of 300 to 600 kPa, much lower than that of R. mangle, 50 to 150 kPa (Field, 1984). This could be a competitive disadvantage for the red mangrove in areas of especially high salinity. However, in seawater or brackish water, A. germinans has the competitive disadvantage of metabolically maintaining its salt glands. One should note that in some locations, such as the coast of Australia, species of the Rhizophora genus are typically found further inland than species of Avicennia, which is found at the water's edge. However R. mangle and A. germinans are not found in these locations (Tomlinson, 1986).
Despite studies of both salt balance strategies, many fundamental questions remain. One area of uncertainty is the cellular process by which the roots of all mangroves, particularly of R. mangle, block salt. Salt glands of A. germinans are becoming better understood in many ways. The gland ultrastructure has been described but questions remain regarding processes inside the cells as well as ion transport from the secretory cells to the cuticle. Furthermore, models explaining water relations in mangroves in general are under debate (Field, 1984).
While there is no doubt that salt balance plays an important part in the ecophysiology of these trees, numerous other factors are also important. Since many features of mangrove roots are adaptions to unique soil characteristics, such as stability, oxygen content, and flood-toleration (Tomlinson, 1986), variations in soil characteristics also play a part in mangrove distribution. True plant vivipary, unique to mangroves, would also have an impact on plant site selection. Any of these topics alone would provide an opportunity for in-depth research. Knowledge of all these factors contributes to a better overall understanding of mangrove ecology. These factors, in addition to salt regulation, undoubtedly play an important role in zonation of these mangroves.
Dr. Hays Cummins provided the Macintosh and Zisman article as well as feedback on the original outline and sources.
Dodd, R.S., Z. Afzal Rafii, and A. Bousquet-Melou. 2000. Evolutionary divergence in the pan-Atlantic mangrove Avicennia germinans. New Phytologist. 145:115-125.
Dschida, W.J., K.A. Platt-Aoloia, and W.W. Thomson. 1992. Epidermal peels of Avicennia germinans (L.) Stearn: A useful system to study the function of salt glands. Annals of Botany. 70:501-509.
Field, C.D. 1984. Ions in mangroves. In: Teas, H.J., ed. Physiology and Management of Mangroves. The Hague, Netherlands: Dr W. Junk Publishers: 43-48.
Florida Plants Online. Accessed 2001. Electronic reprint of: Department of Environmental Protection, Florida Marine Research Institute. Florida's Mangroves: "Walking Trees." Available at http://www.floridaplants.com/horticulture/mangrove.htm. (Referenced as FMRI, 2001)
Law, B.E., and N.P. Arny. Accessed 2001. Mangroves-Florida's coastal trees. Available at http://www.sfrc.ufl.edu/Extension/pubtxt/for43.htm.
Macintosh, D., and S. Zisman. Accessed 1999. The status of mangrove ecosystems: trends in the utilisation and management of mangrove resources. Available at http://iufro.ffp.csiro.au/iufro/iufronet/d1/wu10700/unpub/macint95.htm.
Morrow, L., and N.H. Nickerson. 1973. Salt concentrations in ground waters beneath Rhizophora mangle and Avicennia germinans. Rhodora. 75:102-106.
Newfound Harbor Marine Institute: Species Identification. Accessed 2001. Available at http://www.nhmi.org/mangroves/id.htm. (Referenced as NHMI, 2001)
Purdue University Center for New Crops & Plants Products: Avicennia germinans L. Accessed 2001. Available at http://www.hort.purdue.edu/newcrop/duke_energy/Avicennia_germinans.html. (Referenced as PUCNCPP, 2001a)
Purdue University Center for New Crops & Plants Products: Rhizophora mangle L. Accessed 2001. Available at http://www.hort.purdue.edu/newcrop/duke_energy/Avicennia_germinans.html. (Referenced as PUCNCPP, 2001b)
Scholander, P.F. 1968. How mangroves desalinate water. Physiologia Plantarum. 21:251-261.
Scholander, P.F., H.T. Hammel, E. Hemmingsen, and W. Garey. 1962. Salt balance in mangroves. Plant Physiology. 37:722-729.
Smithsonian Marine Station at Ft Pierce: Avicennia germinans. Accessed 2001. Available at http://www.serc.si.edu/sms/IRLSpec/Avicen_germin.htm. (Referenced as SMSFP, 2001a)
Smithsonian Marine Station at Ft Pierce: Rhizophora mangle. Accessed 2001. Available at http://www.serc.si.edu/sms/irlspec/Rhizop_mangle.htm. (Referenced as SMSFP, 2001b)
Tomlinson, P.B. 1986. The Botany of Mangroves. London: Cambridge University Press.
Werner, A. and R. Stelzer. 1990. Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. Plant, Cell, and Environment. 13:243-255.
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