Medina, E., 1999.

Mangrove physiology: the challenge of salt, heat, and light

stress under recurrent flooding, p. 109-126. In: A. Yáñez-Arancibia y A. L. Lara-

9
Domínguez (eds.). Ecosistemas de Manglar en América Tropical. Instituto de
Ecología A.C. México, UICN/ORMA, Costa Rica, NOAA/NMFS Silver Spring MD
USA. 380 p.

Mangrove Physiology: the Challenge

of Salt, Heat, and Light Stress
Under Recurrent Flooding

Ernesto Medina
Centro de Ecología Instituto Venezolano de Investigaciones Científicas, Venezuela

Abstract

Mangroves have developed a wide array of Compartmentalization is crucial for separating salt
morphological and physiological traits that deal sensitive enzymes in the cytoplasm and cell
successfully with salt stress and oxygen demands for organelles from the incoming salts in the
root function. Water uptake from an environment transpiratory stream. Maintenance of appropriate
enriched in highly permeable ions, mainly chloride hydration of the cytoplasm and organelles appears
and sodium, require the capability of excluding ions to be related to the accumulation of “compatible
at the root level, get rid of the excess of salts taken solutes”, particularly organic nitrogen compounds
up, or develop compartments where large amounts of and cyclitols.
salt can be accumulated without the risk of damaging
Restrictions of water uptake of mangrove trees
the photosynthetic apparatus. These alternatives
from a highly saline substrate reduce the
have significant physiological costs associated.
evaporative cooling of the photosynthetic surfaces.
Energy demands are particularly strong for
This is potentially harmful in tropical and
maintaining ion selectivity (high K+/Na+ ratios relative
subtropical, high temperature, high irradiation,
to soil water) and membrane stability. These
environments because it may lead to
processes depend on the supply of carbohydrates
photoinhibition and heat damage of the
from the leaf canopy as energy source, and the
photosynthetic machinery. Mechanisms avoiding
supply of oxygen for the respiratory chain to operate
these damages are mostly related with reduction of
efficiently. Development of aerenchyma-rich roots
incident radiation (leaf inclination and size) and
has been shown to be essential for successful growth
perhaps buffering of thermal changes (leaf
of mangroves. Salt excretion is efficient in
succulence). In fact, within the same species leaf
maintaining a salt balance at the leaf level, but
size decreases with increasing aridity and/or
requires large amounts of photosynthetic energy for
salinity, but also nutrient availability, of the coastal
the excretory tissues to operate continuously. The
environment.
presence of hypodermises, or water parenchyma
usually found in mangrove leaves, has been Mangal communities generally show a well defined
associated with the differential accumulation of zonation, with particular species substituting one
sodium and chloride at the leaf level. The operation another along gradients of salinity, and duration of
of salt accumulating compartments demands tidal flooding. This zonation results from the
photosynthates both for structure development and competitive exclusion of species differing in their
for pumping ions into the specialized tissues. tolerance to salinity and/or anoxic soils. Zonation,

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Ecosistemas de Manglar E. Medina

therefore, is highly dependent on the general climatic higher plants. In humid coastal areas, on the
conditions where the mangrove forests are found. In contrary, salinity decreases landwards, therefore
relatively arid coastal environments salinity increases mangrove forests change slowly into brackish and
landwards, resulting in the formation of areas where swampy communities, where many non-salt
salinity levels change strongly during the rainy and tolerant tree species can develop successfully.
dry seasons, avoiding permanent establishment of

Resumen

Los manglares han desarrollado una amplia compatibles” particularmente compuestos de

organización de rasgos morfológicos y fisiológicos nitrógeno orgánico y ciclitoles.
que tratan exitosamente con el estrés de sal y las
demandas de oxígeno para las funciones de las Las restricciones en el consumo de agua de los
raíces. La toma de agua desde un ambiente árboles de manglar de un sustrato altamente
enriquecido en iones altamente permeables, salino, reduce el enfriamiento evaporítico de las
principalmente cloruros y sodio, requieren la superficies fotosintéticas. Esto es particularmente
capacidad de exclusión a nivel de las raíces, dañino en ambientes tropicales y subtropicales, de
deshacerse del exceso de sales absorbidas, o alta temperatura y elevada radiación solar debido a
desarrolla compartimentos donde grandes que pueden resultar en fotoinhibición y el calor
cantidades de sal pueden ser acumuladas sin el daña la maquinaria fotosintética. Los mecanismos
riesgo de dañar el aparato fotosintético. Estas que evitan estos daños están principalmente
alternativas tienen asociado un significativo costo relacionados con la reducción de radiación
fisiológico. La demanda de energía son incidental (inclinación y tamaño de la hoja) y quizás
particularmente fuertes para el mantenimiento de la el amortiguamiento de los cambios climáticos
selectividad iónica (alta relación de K+/Na+ relativa al (hojas suculentas). En efecto, dentro de las
agua del suelo) y estabilidad de la membrana. Estos mismas especies el tamaño de la hoja decrece con
procesos dependen del suministro de carbohidratos el incremento de la aridez y/o salinidad, pero
desde las hojas del dosel como fuente de energía, y también la disponibilidad de nutrientes del
el suministro de oxígeno para la cadena respiratoria ambiente costero. Las comunidades de manglar
operar eficientemente. El desarrollo de raíces ricas generalmente muestran una zonación bien
en aerénquimas ha demostrado ser esencial para el definida, con especies particulares sustituyendo
exitoso crecimiento de los manglares. La excreción una a la otra a lo largo de de los gradientes de
de sal es eficiente en el mantenimiento del balance salinidad y duración de la inundación mareal. Ésta
de sal en el nivel de la hoja, pero requiere de zonación Resulta de la exclusión competitiva de
grandes cantidades de energía fotosintética para las especies difiriendo en su tolerancia a la
que los tejidos excretores operen continuamente. La salinidad y/o suelos anóxicos. Por lo tanto, la
presencia de hipodermis o parénquima de agua zonación es altamente dependiente de las
usualmente encontrado en las hojas del manglar, ha condiciones climáticas generales donde los
sido asociado con la acumulación diferencial de bosques de manglar se encuentran. En ambientes
sodio y cloruros a nivel de la hoja. La operación de costeros relativamente áridos, la salinidad
acumulando sal, los compartimentos demandan incrementa hacia el continente, resultando en la
fotosíntesis tanto para las estructuras de desarrollo formación de áreas donde los niveles de salinidad
y para bombeo de iones dentro de los tejidos varíian fuertemente entre las estaciones de lluvias
especializados. y secas, evitando establecimientos permanentes
de plantas superiores. En áreas costeras húmedas,
La compartimentalización es crucial para las enzimas por el contrario, la salinidad disminuye hacia el
sensitivas a la separación de la sal en el citoplasma continente, por lo tanto los bosques de manglar
y los organelos celulares que entran en la corriente cambian lentamente en comunidades salobres a
respiratoria. El mantenimiento de hidratación pantanosas, donde muchas especies de árboles no
apropiada del citoplasma y organelos parece estar tolerantes a la sal pueden desarrollarse
relacionada a la acumulación de “solutos exitosamente..

Introduction

True mangroves are “tropical trees restricted to 1936). Salt, water, and energy balances,
intertidal and adjacent communities” (Tomlinson, therefore, constitute simultaneous constraints for
1986), growing in saline, generally anoxic soils, mangrove photosynthetic productivity. These
under climatic conditions characterized by a constraints acquire particular significance in
combination of high temperature and irradiance mangal habitats where supply of fresh water
(Stewart and Popp, 1987). They are typical through rainfall or riverine flow is severely
halophytes developing up to reproductive stage in restricted during periods of more than a month
sea water, accumulating large amounts of sodium duration. An additional factor of stress which has
chloride in their cell vacuoles (Walter and Steiner, received comparatively little attention is the role

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Ecosistemas de Manglar E. Medina

of nutrient supply in modulating the responses of am tacitly assuming that differences in fresh
mangroves to environmental stresses (Boto, water availability will be closely associated with
1983). In a modeling study Lugo et al. (1976) nutrient inputs from the land. The paper includes
concluded that nutrient supply to mangrove most relevant papers on physiology of
ecosystems is predominantly associated with mangroves; however, it does not provide a full
terrestrial drainage, which is nutrient rich literature list of all recently papers published on
compared to sea water. Development of the subject. There are a number of recent
management strategies of natural and man-made reviews and books on the ecology and
mangrove ecosystems has to be based on an physiology of mangroves which are highly
integrative approach, considering the multivariate recommendable for the interested readers.
interactions of the above factors. Tomlinson (1986) wrote an authoritative account
In this chapter I will focuses on the on mangroves which clarifies their botanical
ecophysiology of photosynthesis and water status and biogeography. A book covering most
relations of true mangroves, that is, plants which relevant aspects of ecology and productivity of
can complete their life cycle in sea water, and mangroves was published by Hutchings and
require a certain salinity level for optimum Saenger (1987). It includes a comprehensive
development. The responses of the literature review and constitute a very good
photosynthetic apparatus to water logging and guide for the work carried out in Australian
salinity under natural conditions will be used as a mangroves. Two excellent reviews dealing
basis for understanding structure and species specifically with ecophysiological aspects are
composition of mangrove communities in arid and those of Stewart and Popp (1987) and Ball
humid coastal environments. With this approach I (1988a).

Environmental Constraints and Ecophysiological Adaptations

Understanding of variations in structure, and towards the sea side (36 ‰ salinity, about 1000
distribution of species in mangrove communities mmol/kg osmotic active solutes, or approxi-
requires a precise knowledge of the fresh water mately 25 bars of osmotic pressure at 25 oC).
sources from terrestrial drainage. Walter and Landwards this level is reduced during the rainy
Steiner (1936) differentiated among coastal, season as a consequence of rainfall in situ or
estuarine, and coral reefs mangrove communities. freshwater drainage from land. In the back of the
Lugo and Snedaker (1974) proposed a more mangrove community, salinity can fall to zero,
detailed classification of mangrove ecosystems but daily and seasonal oscillations of salinity can
including: a) riverine mangroves growing on river be observed according to the tidal regime and
floodplains where lateral flow of water of low the distribution of rainfall. In arid coasts (or with
salinity predominates; b) basin mangroves highly seasonal rainfall) on the contrary, salinity
growing in depressions where water flows are increases landwards, because in the coastal
slow and the seasonal vertical flow predominate areas covered by sea water at high tide the soil
over the lateral flow; c) fringe mangroves growing solution is concentrated during low tide creating
at the edge of the sea or other water bodies conditions of hypersalinity. Behind the mangrove
directly exposed to vertical water fluctuations; and community areas of extreme salinity oscillations
d) mangrove “islands” which may occur at the sea during the year are created, low salinity at the
as overwash island or inland as mangrove soil surface during the rainy season, and almost
“hammocks”. Basically these types are salt saturated soil solution during the dry
differentiated according to the level of salinity season. These areas are hostile to any kind of
stress and the availability of nutrients. In this vegetation and constitute vegetation-less salt
respect, riverine (or estuarine) mangroves are the flats in many coastal areas in the tropics (Walter
most complex because of the irregular distribution and Steiner, 1936; Walter 1977; Medina et al.,
of saline and fresh water. Mangrove communities 1989). These two contrasting hydrological
growing on coral reefs are always protected regimes determine community structure
against wave impacts. The mangrove trees grow according to salinity tolerance in dry coastal
directly on top of the coral rock above the sea areas, and capability of fast resource utilization
water level during low tides. These communities in wet coasts. In both cases salinity stress and
generally do not show a clear structural pattern. nutrient availability can be detected trough the
analysis of osmolality and mineral composition
Coastal mangroves (fringe mangroves) may be of mangrove tissues.
found growing in arid or wet coast lines, differing
in the amount of drainage water available and There are about 38 species considered as true
seasonally of rainfall (Walter 1977). In wet coast mangroves because of their distribution and
lines salinity decreases landwards, so that apparent salinity requirements. These species
maximum salinity is found at the fringe itself are distributed in only 8 families and most of the

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Ecosistemas de Manglar E. Medina

species are confined to the Australasian tropics published by Gill and Tomlinson (1971), and
(Tomlinson, 1986) (Table 1). The following genera Tomlinson (1986).
of mangroves present secretory structures in the
Diffusion of gases through the lenticels and
leaves that in some cases have been shown to
the highly developed aerenchyma of the
secrete salts, mainly sodium chloride: Aegialitis,
underground roots is probably a most important
Aegiceras, Avicennia, Laguncularia and
mechanism for supplying growing root tips with
Sonneratia. From these species most studies
oxygen and to get rid of the excess of CO2
have been conducted in species of the genus
produced by root respiration. In addition, diurnal
Avicennia.
variations in internal gas pressure in aerial roots
have been shown to play a role in gas
Flooding and Gaseous exchange, particularly in aerial roots under a
Exchange at the Root Level daily flooding regime (Scholander et al., 1955).
When pneumatophores of Avicenia germinans
As plant communities living in the intertidal zone are completely covered by water during high
mangroves are frequently flooded. This causes a tide, the internal gas pressure decreases rapidly,
reduction in the oxygen partial pressure at the root as a consequence of the fast consumption of
level which might impair the processes of ion oxygen in the respiration of root cells, and the
uptake due to the disturbance of the respiratory relatively high solubility in water of the resulting
metabolism in root cells. Most mangrove species CO2. The underpressure developed in this
develop strongly aerenchymatic aerial roots, which process is about 0.5 bars, but the water can not
play a role in the oxygenation of underground root enter the pneumatophores, because the
tissues, and provide ways for expelling gases hydrostatic pressure is not enough to overcome
originated in aerobic or anaerobic respiratory the surface tension at this level. At low tide, air
processes (Table 2). Three genera of mangroves, penetrates easily through the pores providing
however, do not develop aerial roots, and they are oxygen to the respiring cells. This mechanism is
presumably less resistant to flooding as may be not operative, or is not so effective, in aerial
inferred from their distribution in mangrove roots not submitted to flooding. Mangrove roots
communities (Tomlinson 1986). The anatomical in these areas, are always relatively superficial,
description of the aerial roots of the mangroves is therefore, aereation is probably guaranteed by
outside of the scope of this chapter, and the diffusion (Scholander et al., 1955; Tomlinson
reader is referred to the excellent accounts 1986).

Table 1. Families and genera of true mangroves based on their distribution and apparent
requirements of saline environments (from Tomlinson 1986)

Family and Genera No. of species American species

Anniaceae A. germinans
Avicennia 9 A. schaueriana
Combretaceae
Laguncularia 1 L. racemosa
Lumnitzera 3
Conocarpus 1 C. erectus
Meliaceae
Xylocarpus 3
Myrsinaceae
Aegiceras 2
Pellicieraceae
1 P. rhizophoreae
Pelliciera
Plumbaginaceae
Aegialitis 2

Rhizophoraceae
Bruguiera 6
Ceriops 2
Kandelia 1
Rhizophora 3 R. mangle
R. racemosa
Sonneratiaceae
Sonneratia 5
Total: 13 genera 39 species 7 American species

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Ecosistemas de Manglar E. Medina

Table 2. Types of aerial root systems in strict mangroves (Gill and Tomlinson 1971)
Morphological adaptations of the root
Genera of mangroves
system to flooding
Stilt roots Rhizophora, Bruguiera, Ceriops, Avicennia (sporadically)
Pneumatophores Avicennia, Sonneratia, Laguncularia (facultative)
Root knees Bruguiera and Ceriops, Lumnitzera, Xylocarpus
Plank roots Xylocarpus
Fluted buttresses Pelliciera
Without special aerial roots Aegiceras, Aegialitis, Kandelia

In Avicenia marina the pneumatophores present there exists a differentiation in the salinity
little resistance to oxygen diffusion, the structure tolerance at least of the adult plants. In South
of the pneumatophores represent a compromise America, Rhizophora mangle and Laguncularia
between the needs for expedite gas exchange and racemosa are frequently found growing best at
the need to exclude water (Curran, 1985). In the salinities near sea water level or below, while
horizontal roots oxygen can diffuse freely and Avicennia germinans is found growing at
differences in oxygen concentration along these salinities near sea water and above (Lugo and
roots are unlikely in healthy roots. Snedaker, 1974; Cintrón et al., 1978).
Frequently the occurrence of zonation of
Avicenia germinans can oxidize the substrate mangrove species along salinity gradients is
surrounding its roots in considerable extension, obscured by the complexities of the hydrological
and when air supply trough the pneumatophores regime, particularly in estuarine mangroves. The
is impeded by flooding the reduction of the analyses of leaf sap osmolality indicate the long-
rhizosphere is rapid and reach levels similar to term salinity conditions of the species occurring
unrooted soils (Thibodeau and Nickerson, 1986). in mangrove communities (Walter and Steiner
Roots of Rhizophora mangle, however, although 1936). The general differences in salinity of the
developing a thick aerenchyma when underground preferred sites of occurrence of mangrove and
(Gill and Tomlinson, 1971) are not able to oxidize some associated mangal species was shown by
their rhizosphere to a similar extent. These Harris (1934) in Florida through the analysis of
differences are probably associated with the leaf saps (Fig. 1). Avicennia germinans has the
distribution of these two species in natural highest average value (38.5 bars) and can reach
conditions. Avicennia spp grow quite actively in values above 50 bars. Rhizophora mangle and
heavy soils which may be flooded for prolonged Laguncularia racemosa are similar in the
periods, while Rhizophora spp occupies generally distribution of their osmotic pressure values. The
areas which are flooded periodically, but with associate species Conocarpus erectus and
continuous movement of water, probably Acrostichum aureum show average values that
facilitating aeration of the upper soil layers. indicate clearly their occurrence in low salinity
In six months old seedlings of Avicenia sites. These results correspond to the salinity
germinans flooding can increase mortality, and tolerance of adult plants.
induces the activity of alcohol dehydrogenase On the other hand, growth experiments
(Steward and Popp, 1987). This biochemical conducted with seedlings during periods varying
response is of general occurrence in higher plants from a few weeks to several months indicate that
submitted to flooding. In adult plants this effect is optimum growth of several mangrove species is
probably of lesser importance because reached at salinities well below that of sea
anaerobiosis is prevented by the development of water. In Rhizophora mangle Pannier (1959)
pneumatophores. This increase in the activity of measured a maximum production of leaves and
ADH can be counteracted by the addition of NaCl, roots in 6 months old seedlings at 25% of sea
but the nature of the effect is not well understood water without added nutrients; similar growth
(Steward and Popp, 1987). response to salinity, but with added nutrients,
was reported for 12 months old seedlings of R.
Salinity Stress and Osmotic stylosa (Clough, 1984). For Avicennia marina
Relationships in Mangroves Downton (1982) recorded maximum growth in
Growth of mangrove species under different 11 months old seedlings growing at salinities
salinities equivalent to 25 to 50% sea water, while
Burchett et al. (1984) and Clough (1984) for the
Mangroves can be found in nature growing in a same species recorded optimal growth at 25%
large range of salinities. It appears, however, that sea water. Lower salinities for optimum growth

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Ecosistemas de Manglar E. Medina

Figure 1. Box plots of the osmotic pressures of leaf sap measured in true mangrove and associated species in a range
of habitats in Florida (with data from Harris 1934). The osmotic pressures were measured with a crioscopic method.

have been reported in Africa for Avicennia marina al. (1962) showed that mangrove species with
(Naidoo, 1987) and Bruguiera gymnorrhyza salt-secreting glands in their leaves have usually
(Naidoo, 1990). Increase in growth induced by higher NaCl concentrations in the xylem sap
salinity around 40% of sea water has been than those without those structures (Table 3).
recently confirmed for Rhizophora mangle
(Werner and Stelzer, 1990). The improvement in In all cases NaCl concentration in xylem sap is
organic matter production induced by NaCl well below that in sea water (36‰). That means
reflects the halophytic character of true that if all the species are absorbing water from
mangroves, and is certainly associated with the sea, NaCl is being efficiently rejected at the
improved water relations (Werner and Stelzer, root level. There is no indication in the original
1990). paper of Scholander et al. (1962) that the root
systems of all the species investigated were
Ball (1988a) measured maximum growth rates absorbing water from sources of similar salinity.
of Avicennia marina at 50% sea water, while
Aegiceras corniculatum reached maximum growth The actual Cl- concentration in the xylem sap
at 10% sea water (Clarke and Hannon, 1970). varies with concentration of the bathing solution
However, when the seedlings are mature and not of the roots. It was proposed that those species
dependent on the reserves provided by the with the lowest Cl- concentrations in the xylem
mother tree, growth decreases with salinity from sap were those which act as salt excluders at
50 to 500 mmol m-3, A. corniculatum being more the root level (Scholander et al., 1962), while the
sensitive than A. marina (Ball, 1988b). species with higher concentration were those
which have the capability of secreting salt by
Salt balance
special salt glands in the leaves. It is clear,
Roots developing in an aqueous high saline however, that irrespective of the actual Cl-
environment absorb salts readily, which are concentration in the xylem sap, transpiring
transported to the leaves in the transpiration mangrove leaves do accumulate large amounts
stream. Ions such as Cl- and Na+ are highly of Cl- and Na+ in their leaves (Popp, 1984). The
permeable in most root cells of higher plants. The degree of salt exclusion may vary from species
concentration of sodium chloride in the xylem sap to species, and also in relation to the actual
has been used as an indicator of the degree of saline concentration of soil solution in which the
exclusion of salts at the root level. Scholander et roots are growing.

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Ecosistemas de Manglar E. Medina

Table 3. Concentration of salt in xylem sap (Scholander et al. 1962)

NaCl [g/l] Leaves with salt secreting glands

Rhizophora mucronata 0.2-0.4 -
Sonneratia alba 0.2-0.5 -
Bruguiera cf. exaristata 0.3-0.5 -
Aegiceras corniculatum 0.8-2.8 +
Avicennia marina 1.2-4.0 +
Aegialitis annulata 3.6-8.0 +

The accumulation of salt in the leaves is also a

function of leaf age. Old leaves have always
higher salt content in their sap. This accumulation
tends to be compensated by an increase in leaf
succulence (water content per unit leaf area). The
increase in leaf succulence with salinity of the
growth medium has been shown under natural
conditions in Laguncularia racemosa (Biebl and
Kinzel 1965), and Rhizophora mangle (Camillieri
and Ribi 1983), and under cultivated conditions in
Rhizophora mangle (Werner and Stelzer 1990),
Rhizophora stylosa and Avicennia marina
(Clough 1984). The increase in succulence with
leaf age has been also shown by Atkinson et al.,
1967 in Rhizophora mucronata, and in this
species it correlated with increases in Na+ and Cl-
contents, both on a whole leaf basis and on a leaf
water basis. The studies in Laguncularia
racemosa leaves of increasing age showed that
the pro-gressive increase in Na+ and Cl-
concentration per unit leaf area was almost
quantitatively compensated by a similar increase
in the leaf water content. The result is that the
concentrations of those ions per unit of leaf water
remain almost constant (Fig. 2).
The difference in membrane permeability
reflected in the salt concentration of the xylem sap -
Figure 2. Variations in the concentration of Cl per unit
of mangrove species with and without active salt leaf area or per unit leaf water, and the content of
secreting glands is observed when seedlings of cations in leaf sap expressed per unit leaf area. On an
- +
area basis the amount of Cl and Na is showed to
those species are cultivated under the same increase with the degree of succulence of the leaves.
salinity conditions. Avicennia marina accumulates + +
That is not the case for K and Ca2 . Notice that the Cl
-

more Na+ and Cl- ions than Rhizophora stylosa concentration per unit leaf water remains constant
growing in nutrient solutions with exactly the same indicating that the ion uptake is accompanied by water
salt composition (Clough, 1984). With higher salt uptake (data from Biebl and Kinzel, 1965).
concentrations of the solution the Na+ content of
Avicennia marina increased continuously, while calculated from the K+/Na+ ratio in the plant
the K+ content either remained constant or tissue divided by the K+/Na+ ratio in the nutrient
increased slightly. In Rhizophora stylosa to the solution (Table 4).
contrary, Na+ content stabilized after 25% of sea The strong preference for K+ absorption in the
water but K+ concentration decreased steadily. presence of large amounts of Na+ was
These differences in ion absorption might be demonstrated by Rains and Epstein (1967) in
associated with the salinity tolerance of these Avicennia marina. In this species the operation
species under natural conditions. The differences of two absorption mechanisms with different
in K+ uptake relative to Na+ uptake at increasing affinities for K+ was demonstrated. These two
levels of salinity can be appropriately expressed mechanisms are of general occurrence in higher
as selectivity ratios (Pitman, 1965). This ratio is plants. In Avicennia marina the Michaelis

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Ecosistemas de Manglar E. Medina

constant for the mechanism 1 was 0.2 mM, or be collected with microburettes for chemical
about 10 times higher than the values recorded for analyses. It was found that the daily course of
other species, although it has the same specificity salt excretion was very pronounced during the
(Rains and Epstein, 1967). At 1 mM K+ and 0.5 day in Aegialitis annulata, less pronounced in
mM Ca2+ in the external solution the absorption of Aegiceras corniculatum and absent in Avicennia
K+ was interfered by the presence of Na+ only marina. For the latter species the same lack of a
when the Na+/K+ ratio was above 100. The day-night pattern of secretion was reported by
mechanism 2 however, operating at K+ Waisel et al. (1986). Nearly 90% of the secreted
concentrations above 10 mM K+ and 10 mM Ca2+ salts was NaCl, and only 4% of the Cl- was
(at a similar level as in sea water), the K+ matched by K+. The concentration of NaCl in the
absorption was not interfered by concentrations of secretion varied between 1.8 and 4.8% in
Na+ as high as 500 mM, therefore showing a Aegialitis annulata and between 0.9 and 2.9% in
much higher specificity than that of the Aegiceras corniculatum, while in Avicennia
mechanism 2 described for non-halophytes. In marina it reached 4.1%. Similar results for
sea water K+ concentration is around 12 mM, secretion composition have been reported by
therefore the insensitivity of mechanism 2 to high Ball (1988) for Aegiceras corniculatum and
Na concentrations is of high ecological Avicennia marina. In these species the rate of
significance. The operation of this mechanism 2 secretion increases with the salinity of the
with high preference for K+ does not impede the nutrient solution. The highest values of Cl-
uptake of Na+ but raises the K+/Na+ ratio from secretion were 343 nmol Cl m-2 s-1 for Aegiceras
about 1/40 in sea water, to 1/7 in the leaf tissues. corniculatum (at 500 mol m-3 NaCl in the solution
and 6 mb leaf-air vapor pressure deficit), and
The operation of similar mechanisms at the
264 mmol Cl- m-2 s-1 for Avicennia marina (500
cellular level in other mangrove species has not
molm-3 NaCl and 24 mb vpd). These rates were
been documented yet, although such studies may
measured in whole seedlings. The salt balance
provide a basic physiological explanation for the
of these two species shows some interesting
zonation of mangroves. Indirect evidences for
patterns (Table 5). In Aegiceras corniculatum the
differential ion permeability in mangroves species
species with lower salt tolerance, the net water
with and without salt-excreting glands in their
use efficiency is higher at 50 mol m-3 NaCl
leaves may be implied from studies of the
(approximately 10% sea water), while in
composition of the xylem sap. Atkinson et al.
Avicennia marina the highest value is reached at
(1967) measured the transport of sodium chloride
500 mol m-3 NaCl. Salt uptake increases with
through transpiration in the xylem sap of intact
salinity in nutrient solution in both species, but
trees of Rhizophora mucronata and Aegialitis
the efficiency of salt secretion, both at the whole
annulata growing under natural conditions in
plant and at the leaf level, is quite higher in
northern Australia. The concentration of Cl- in the
Aegiceras corniculatum compared to Avicennia
xylem sap was smaller in Rhizophora mucronata
marina.
compared to that of Aegialitis annulata (17 vs 85-
122 mmol Cl-/l, res-pectively). In a sequence of
In whole seedlings of Avicennia marina the
leaf pairs of increasing age of Rhizophora
rate of salt excretion is larger during the night
mucronata the total Na+ and Cl- contents per leaf
and increases with salinity of the root-bathing
increased markedly with age, as a result of the
solution (Drennan and Pammeter, 1982).
accumulation of about 17 mol of Cl- per leaf per
Concentration of Na+ in xylem sap and roots
day. The K+ content however, decreased
increased linearly with salinity of the nutrient
markedly. The concentration of Na+ and Cl- on a
solution. However, in the leaves the
leaf water basis remained nearly constant (515-
concentration reached a plateau at about 50% of
522 mmol Cl-/l leaf sap), indicating that the leaf
sea water, amounting to 1.5 mmol Na per g dry
water content also increased. In Aegialitis
weight.
annulata, on the contrary, both Na+ and Cl-
content diminished with increasing leaf age,
Under hypersaline conditions in nature Waisel
although the daily input of Cl- to the leaf was about
et al. (1986) showed that for the salt balance of
100 mol per day. This results from the salt
the salt-excreting species Avicennia marina the
secreting activity of glands in the adaxial leaf
most important process is the rejection of salt at
surface. The secretion was mainly NaCl but it
the root level (about 80%). The measurements
contained also a small fraction of K. In the intact
were performed on trees of this species growing
tree the secretion takes place mainly during the
under natural conditions in a site at the Red Sea
day time.
characterized by very high salinities (0.70 M ≈
Scholander et al. (1962) measured the activity 41 ‰). It was calculated that 0.77 mmol NaCl
of salt-secreting glands in several mangroves per g dry weight per day were being transported
species. They covered mangrove leaves with oil to the leaf, instead of the 3.57 that would be
drops to avoid drying of the secreted solution. The expected from the concentration of the Red Sea
solution accumulated under the oil drop and could water and the transpiration rates measured

116
Ecosistemas de Manglar E. Medina

Table 4. Selectivity ratios (SK.Na= (Kt/Nat)/(Kc/Nac) in leaf and root tissues of Avicennia marina
and Rhizophora stylosa cultivated under different salinities (from Clough, 1984)

SK.Na % sea water

Species and Tissue
0 25 50 65 100
leaves 0.1 10.1 12.1 17.0 11.1
A. marina
roots 0.2 14.6 16.4 18.7 18.1
leaves 0.2 11.1 9.4 10.3 7.0
R. stylosa
roots 0.1 2.1 4.2 4.4 3.2

Table 5. Salt balance of seedling of salt excreting species Aegiceras corniculatum and
Avicennia marina (from Ball, 1988)

A. cornuculatum A. marina
Growth salinity
-3 50 250 500 50 250 500
(mol m NaCl)
Net water use efficiency
-3 73.8 45.0 41.4 81.0 79.2 91.8
(mg dr.wt. mol water)
-1
Net Cl uptake
-1 -1
(μmol Cl mol water)
total uptake 91.2 144.4 195.3 102.1 150.9 283.3
secretion 28.7 85.6 157.0 13.4 64.2 94.8
% 31 59 80 13 43 33
Salt balance at the leaf level
-
total Cl flow to leaf 54.8 111.6 173.9 47.6 98.8 142.1
% 52 77 90 28 65 67

(a reduction of about 80%). This exclusion may The experiments discussed in this section
have had taken place through the process of indicate that the exclusion of salts at the root
ultrafiltration as proposed by Scholander (1968). level is the most important process for reduction
The amount of salt excretion reached 0.302 mmol of salt uptake for all mangrove species, both with
NaCl per g dry weight per 24 hours, corresponding and without salt-secreting glands in the leaves.
to about 40% of the actual amount transported by In all mangrove species studied the salt
the transpiration stream to the leaves. The concentration in the xylem sap increases linearly
conclusion is that salt secretion in this species, at with the concentration of the solution bathing the
the salinities of the waters where it is growing, is roots. The salt-secreting mangroves have
not sufficient to account for the relative constancy always higher salt concentrations in their xylem
of the salt content of the leaves. Another important sap, but the rate of salt accumulation in the
role of secretion discussed by the authors is the leaves is partially reduced by the activity of the
selective character of the secretion. Almost all the salt-secreting glands. Finally, the salt tolerance
salts secreted is NaCl, this could contribute to at high levels of salinity is apparently associated
maintain a favorable K+/Na+ ratio in the leaf cells. with the capability of maintaining a high K+/Na+
This may allow the cells to metabolize normally in ratio in the plant tissues.
spite of the high total salt content.
Compartmentation of salt
With excised leaves of A. marina Boon and
Allaway (1986) measured rates of excretion of Cl- The relative fast rates of salt accumulation due
of up to 3.5 mol m-2 s-1 when the petioles of the to salt transport in the transpiration stream leads
excised leaves were immersed in concentrated to the accumulation of large amounts of salts in
solutions of NaCl. The maximum rates of Cl- the leaf tissues of mangrove species (Steward
secretion were reached at an external and Popp, 1987). However, when transpiration
concentration of 1 M NaCl. The rate of secretion rates are measured and the amount of salt that
was reduced at very high concentrations (>2.0 M). should be delivered to the leaves is calculated,
These rates are one order of magnitude higher the actual amount found in the leaves is
than those measured in intact plants in the field. considerably smaller. The missing salt is

117
Ecosistemas de Manglar E. Medina

probably removed during transportation through plants. How this discrimination takes place is
the stem xylem and accumulated in stem probably explained by the pathways of
parenchyma, or retranslocated from the leaves. transpiration water.
Stem tissues can have similar salt concentrations
as the leaves, at least in the case of Avicennia Cytoplasm-Vacuole Osmotic
germinans (Steward and Popp, 1987). Relationships: The Role
of Organic Osmolites
The salt reaching the leaves is incorporated into
the vacuoles to a great extent as is usual in The large amounts of salt accumulated mainly
halophytes (Harvey et al., 1981). The distribution in the leaf tissues, but also in stems and roots,
within the leaves, however, can be highly create special osmotic conditions at the cellular
asymmetric. Practically all mangrove species are level. Probably most of these salts are
characterized by the development of a accumulated in the vacuoles, maintaining the
hypodermic in the adaxial side of the leaf (Walter salt sensitive enzymes in the cytoplasm
and Steiner, 1936; Tomlinson 1986). This separated from high saline concentrations. This
hypodermics is hyaline, and it thickness increases leads to a reduction of the water potential of the
with substrate salinity. Therefore it has been cytoplasm, either through dehydration (decrease
proposed that it may act as a salt accumulating in matrix potential) or by the accumulation of
tissue. Walter and Steiner (1936) showed the organic osmolites, which do not impair
accumulation of salt in this tissue using enzymatic functioning even at relatively high
histochemical techniques. More recently, Werner concentrations (compatible solutes). A number
and Stelzer (1990) used energy-dispersive X-ray of these organic osmolites, increasingly
microprobe analysis to measure the distribution of synthesized at high salinities, have been
sodium chloride within leaf tissues. It was shown described in mangroves (Popp 1984b, Popp et
that the concentration of Na+ was lowest in the al., 1984). Several cyclitols, nitrogen compounds
mesophyll and epidermises of leaves from including aminoacids, have been described and
seedlings of Rhizophora mangle grown in salt occur in a wide range of concentrations (Table
solutions containing 200 mol m-3 NaCl (Fig. 3). 6). The role of these compatible solutes is
The distribution of K+ was more homogeneous in probably the maintenance of an appropriate
the different leaf tissues, but the control had degree of cytoplasm hydration for enzyme
clearly higher K+ contents than the salt treated function.

+ +
Figure 3. Differences in K and Na concentration in leaf tissues of Rhizophora mangle grown in salt-free nutrient
-3
solution and a nutrient solution with 200 mol m NaCl. Measurements were conducted in fractured leaves using X-ray
microprobe analysis (data from Werner and Stelzer, 1990).

118
Ecosistemas de Manglar E. Medina

Table 6. Concentration of organic solutes of low molecular weight in

mangroves (from Stewart and Popp 1987)
-3
Species Solute mol m tissue water
pinitol 105
Aegialitis annulata chiroinositol 150
proline 28
Aegiceras corniculatum mannitol 230
Avicennia marina glicin betaine 61
Bruguiera gymnorrhiza pinitol 80
Ceriops tagal pinitol 150
Lumnitzera littorea mannitol 110
Rhizophora apiculata pinitol 220
Sonneratia alba mannitol 200
Xylocarpus mekongensis proline 57

Photosynthesis and Water Relations of Mangroves

Mangroves grow in environments characterized

by high irradiation, and, at least in tropical
latitudes, homogeneous and high temperatures
throughout the year. Under these conditions the
demands for water to cover daily transpirational
losses are very high. Water uptake from a saline
substrate imposes severe osmotic restrictions,
and as discussed before, leads to strong
accumulation of salt in the transpiring surfaces.
Transpiration rates of mangrove species under
natural conditions are relatively low compared to
non-halophytic vegetation (Moore et al., 1973;
Lugo et al., 1975; Miller et al., 1975), therefore the
potential damage by overheating due to
insufficient evaporative cooling of the leaf surfaces
is a serious ecological constraint for mangroves in
nature. Photosynthetic rates are correspondingly
Figure 4. Relationship between leaf conductance
low, therefore mangroves are exposed to a large
excess of excitation energy leading potentially to and photosynthetic rate of mangrove species with (•)
problems of photoinhibition of the photosynthetic and without salt excreting glands (o). Salt excreting
species: Avicennia marina, A. officinalis, Aegiceras
apparatus (Björkman et al., 1988). corniculatum, Aegialitis annulata. Non-salt excreting
species: Rhizophora apiculata, R. mucronata, R.
In a large survey of photosynthesis of mangrove stylosa (data from Clough and Sim 1989).
species under natural conditions conducted by
Clough and Sim (1989), a number of patterns The survey of Clough and Sim (1989) confirm
relating photosynthesis and conductance with leaf- previous measurements on Rhizophora stylosa
air vapor pressure deficits (vpd) and substrate (Andrews and Muller, 1985). In this species
salinity have been established. Avicennia marina photosynthesis under natural conditions reach
consistently had the higher photosynthetic rates, maximum levels of around 10-11 μmol CO2 m-2
and leaf conductances. In a particular locality all s-1, and there was a linear relationship between
species showed the same fractional reduction of photosynthesis and leaf conductance, therefore
assimilation with leaf conductance, therefore they allowing the maintenance of a nearly constant ci
had similar internal CO2 concentrations at under a large range of conditions (ca. 166 μbar).
irradiances above 800 μmol m-2 s-1, and the same Maximum leaf conductances were always
water use efficiency (Fig. 4). Stomatal around 100 mmol m-2 s-1. The water use
conductance and assimilation rate decreased with efficiency was high under these conditions. (5.3,
salinity and increased vpds. It is concluded that in 3.9, 4.7, 5.1 and 5.0 mmol CO2/mol H2O). It was
mangroves water use efficiency increases with shown that leaf inclination was very important for
stress (increased salinity and lowered vpds). temperature regulation. In a leaf held

119
Ecosistemas de Manglar E. Medina

horizontally the leaf-air temperature difference Shaded leaves were larger, had a higher
reached 11 oC in a clear day. Photosynthetic gas projected fraction of leaf area, and were less
exchange was shown to be strongly sensitive to succulent than leaves growing under full sun
leaf temperature and leaf-air vpd. (Table 8). These observations are associated
with the fact that mangroves are conservative in
The analysis of CO2 uptake, oxygen photon
their water use, but living in an environment of
yields, and fluorescence kinetics in leaves of
high radiation the most effective way of avoiding
several mangrove species growing naturally at
overheating without evaporative cooling is
different degrees of sun exposure showed that
reducing the absorbed light energy.
leaves under full sun are partially photoinhibited
(Björkman et al., 1988, see Table 7). It was found Growing under saline conditions in high
that shade leaves have a photon yield of O2 radiation environments is certainly a severe
evolution as high as non-mangrove leaves, their stress for mangroves, but true mangrove
fluorescence characteristics were normal, requires a certain level of NaCl in their substrate
therefore the energy conversion efficiency was for optimal growth. However, the reports
unaffected by the high salinity. Sun leaves had indicating that the photochemical activity of
markedly depressed photon yields and photosystem II of isolated chloroplasts and
fluorescence was severely quenched showing that thylacoids of Avicennia marina are stimulated in
the efficiency of the photo-chemistry of their electron transport and oxygen evolution by
photosystem II was reduced. No such depression concentrations up to 500 mM NaCl (Critchley,
was detected in sun leaves of non-mangrove 1982) have been shown to be an artifact of the
species growing in adjacent non-saline sites. The chloroplast isolation procedure (Ball and
reduction in efficiency of energy conversion could Anderson, 1986). In halophytes salt
be reversed by shading sun leaves, but in general concentration in cytoplasmic compartments are
more than a week was required to reach the usually much smaller than that of the vacuoles
efficiency of shade leaves. Plants cultivated under (Harvey et al., 1981) reflecting the sensitivity of
full sun but with 10% sea water had conversion enzymes to high levels of Na+ and Cl-.
efficiencies slightly higher than those of plants
The photosynthetic rate and leaf conductance
grown with full strength sea water, but salinity had
of mangroves may be affected both by transient
little influence on the increase of efficiency upon
changes in salinity and long term exposure to
shading. The measurements indicate that the
high saline concentrations. Seedlings of
reduced efficiency is due to a large increase in the
Avicennia marina submitted to increasing
rate constant of radiationless energy dissipation in
salinities, showed a decrease in photosynthesis
the antenna chlorophyll rather than a damage to
photosystem II reaction centers. The apparent from 14.9 ± 0.7 μmol CO2 at 50 mM NaCl to 9.1
quantum yield was reduced in leaves grown under ±1.0 at 500 mM NaCl (nearly full sea water) (Ball
fully exposed conditions, probably with angles and Farquhar, 1984a). Similarly, conductance
smaller than 45o. was reduced from about 250 to 80-100 mmol m-2
s-1. It is shown that the CO2 dependent part of
Under natural conditions healthy mangrove the curve was not affected by salinity, while CO2
leaves have usually high degree of leaf inclination, saturation point remained similar but rates of
a factor reducing considerably the amount of CO2 uptake decreased considerably with salinity.
radiation effectively impinging upon the leaf. Ball These short term changes were substantially
et al. (1988) showed that degree of leaf inclination reversible. Apparently the salt accumulated
is quite significant in mangrove species of during the 8 days periods reduced
northern Australia, accounting for a large photosynthetic rates at the end of the
reduction of the heat load of the mangrove leaves. experiment only by a small amount.

Table 7. Variations of apparent quantum yield leaves grown under full exposure or partial
shade of mangrove species on northern Australia (Björkman et al., 1988)
φO2
Species Exposure -1
(mol O2 mol photons)
Partial shade 0.078
Aegialitis annulata
Exposed 0.054
shade 0.084
Aegiceras corniculatum
Exposed 0.044
Partial shade 0.078
Avicennia marina
Exposed 0.043
Partial shade 0.075
Rhizophora stylosa
Exposed 0.047
o
80 leaf angle 0.078
Sonneratia alba o
47 0.036

120
Ecosistemas de Manglar E. Medina

Table 8. Variation in the leaf inclination with the degree of exposure in five mangrove species in Hinchinbrook
Island, North Queensland (Ball et al., 1988). (The projected fraction of leaf area= cos α, where a is the angle of
the leaf respective to the horizontal; exposure is expressed as shade (Sh), medium sun (MS), and full sun (FS)

Species Exposure Leaf Area (cm2) Projected fraction Succulence (g/m2)

Sh 67 ± 5 0.83 ± 0.04 236.5 ± 8.0
B. gymnorrhiza MS 70 ± 14 0.79 ± 0.01 332.0 ± 35.4
FS 58 0.56 262.5
Sh 78 ± 9 0.94 ± 0.01 262.4 ± 21.9
MS 75 ± 5
R. apiculata FS 69 ± 7 0.60 ± 0.04 285.9 ± 16.8
0.37 ± 0.09 384.4 ± 41.1
Sh 61 ± 7 0.95 ± 0.03 258.5
R. stylosa MS 60 ± 20 0.57 ± 0.04 321.4 ± 11.2
FS 44 ± 2 0.30 ± 0.03 387.9 ± 35.5
Sh 49 ± 1 0.93 ± 0.03 310.1 ± 9.2
C. tagal MS 20 ±3 0.63 ± 0.05 351.9 ± 33.9
FS 8±1 0.36 ± 0.08 463.2 ± 55.4

The effects of long term increases in salinities operating in higher plants (Farquhar et al., 1989).
and contrasting leaf-air vapor pressure deficits The theory of enzymatic and diffusive fractionation
(vpd) on mangrove species with different salt during CO2 uptake in photosynthesis of C3 plants
tolerance indicate that the photosynthetic rate is establishes a linear relationship between the ratio
affected by vpd certainly through a reduction of of internal to external CO2 concentrations in the
leaf conductance (Ball and Farquhar, 1984b). leaves and their water use efficiency (Farquhar et
Aegiceras corniculatum appears to be more al., 1982). All mangrove species measured have
sensitive to salinity than Avicennia marina but δ13C values typical of C3 plants, with a range of
both species respond quickly to reductions in vpd. values extending from -32‰ in Ceriops tagal to
Particularly at salt concentrations near 100% sea -26.3 ‰ in Xylocarpus australasicum (Andrews et
water photosynthetic rate of Aegiceras al., 1984). Higher δ13C values are indicative of
corniculatum is strongly reduced, even at low higher water use efficiency, because photo-
synthesis is more limited by diffusion (lower
vpds, being less than half of that of A. marina ,
stomatal conductance) than by the carboxylation
while at low salinities (10% sea water) there are
step. Mangrove species have higher water use
no differences in the photosynthetic rates of both efficiencies under saline conditions (Clough and
species. Part of the lower tolerance of Aegiceras Sim, 1989) or drought (Smith et al., 1989), it is then
corniculatum to high salinity might be explained by expected that mangroves from drier sites (lower
the rapid reduction of the K+/Na+ ratio with fresh water availability) or higher salinities will have
increasing salinity. higher δ13C values. Some indications that this is the
The measurement of the natural abundance of case have been advanced by Farquhar et al.,
carbon 13 in plant tissues has been used effectively (1982).
to establish the type of photosynthetic pathway

Salinity and Seasonal Variations in Performance

in True Mangroves and Associates

Throughout this chapter I have dealt with true optimum development but may be quite salt
mangroves, those tree species growing in the tolerant. Two common associate species of the
intertidal zone in tropical shores. The implication is mangrove communities in the american tropics
that true mangroves have a comparatively high are Conocarpus erectus (Combretaceae) and
salinity resistance, and that they require salt for Acrostichum aureum, the mangrove fern.
their optimum development. The absence of
certain amount of NaCl is not only detrimental to Conocarpus erectus grows in the back of
their competitive capacity against non-halophytes, mangrove communities, frequently outside of the
but also increases their mortality. Many of the influence of the tides. In many circumstances,
species labeled as associate mangroves however, it grows in coastal areas where the
(Tomlinson, 1986) do not require salt for their incidence of salt spray or salt water in the

121
Ecosistemas de Manglar E. Medina

underground can modify strongly their leaf

succulence and photosynthetic charac- teristics.
Smith et al. (1989) studied the occurrence of
Avicennia germinans, the most salt tolerant
mangrove species in the neotropics, and
Conocarpus erectus in vegetation islands in salt
flats of northern Venezuela. It was shown that
Conocarpus erectus can accumulate quite large
amounts of NaCl in their leaves, particularly during
the dry season, but the Na+/K+ ratios are much
higher than those of Avicennia germinans (Table
9). The different sources of soil water for the two
species in these complex vegetation are revealed
by the concentration of ions in the leaf sap. In
spite of the higher transpiration rates of
Conocarpus erectus during the dry season, the
concentration of Na+ and Cl- were nearly 40%
lower, while the K+ content was 60% lower compa-
red to Avicennia germinans. The photosynthetic
capacity of C. erectus appeared to be more
sensitive both to the larger vpds and higher soil
salinities experienced during the dry season.
The case of the mangrove fern is also indicative 18
of differences in the availability of fresh water, in Figure 5. Relationship between δD and δ O values
measured in plant tissues of hardwood hammock species
spite of its co-occurrence with true mangrove and true mangrove species growing on keys of southern
species in the same communities. In sites of Florida. The squares show the range of expected values
increasing salinity of interstitial water in the for ocean water and freshwater. Ocean water is richer
northern coast of Puerto Rico Acrostichum both in oxygen 18 and deuterium than fresh water
aureum had always lower osmolalities than (redrawn from Sternberg et al., 1989)
Laguncularia racemosa and Rhizophora mangle
(Medina et al., 1990; see Table 10).

+ -
Table 9. Seasonal variations of gas exchange characteristics, cell sap osmolality and Na and Cl content in
Avicennia germinans and Conocarpus erectus growing in salt flats (From Smith et al., 1989)

Avicennia germinans Conocarpus erectus

Rainy Dry Rainy Dry

season season season season
-1
Osmolality (mmol kg ) 1300 2650 760 1640
- -3
Cl (mol m ) 744 935 421 600
Na+ 261 891 154 504
K+ 130 107 49 35
+ +
Na / K 2.0 8.3 3.1 14.4
Photosynthetic rate near saturation
5.61 3.87 4.27 2.07
(μmol m-2 s-1)
Total net CO2 uptake during the light
173 105 133 40
period (mmol m-2 12 h-1)
Total transpiration per light period
101 31 154 8
(mol H2O m-2 (12h)-1)
Water use efficiency during the light
1.7 x 10-3 3.3 x 10-3 1.3 x 10-3 4.3 x 10-3
period (mol CO2 mol-1 H2O)

122
Ecosistemas de Manglar E. Medina

o + -
Table 10. Comparison of osmotic pressure (at 25 C) and Na and Cl contents of leaf sap of the
associate species Acrostichum aureum growing together with Laguncularia racemosa and Rhizophora
mangle (from Medina et al., 1990)
- +
Interstitial water salinity Leaf sap osmolality Cl Na - +
Species Cl /Na
mmol/kg π MPa mmol/kg π MPa mol m
-3
mol m
-3

A. aureum 914 2.26 240 89 2.7

L. racemosa 520 1.28 1138 2.81 490 269 1.8
R. mangle 1422 2.51 461 434 1.1
A. aureum 989 2.44 279 121 2.3
L. racemosa 565 1.39 1183 2.92 465 428 1.1
R. mangle 1527 3.77 571 427 1.3
A. aureum 1019 2.52 282 119 2.4
839 2.07
L. racemosa 1243 3.07 561 354 1.6

Besides, the Cl-/Na+ ratios are always higher in mangrove communities found on keys in
the Acrostichum aureum, indicating differences in southern Florida Sternberg et al. (1989)
permeability against these two ions. The measured the relative utilization of freshwater
occurrence of Acrostichum aureum in mangrove and ocean water using this technique. They
communities is restricted to wet coasts or to concluded that plants occurring towards the
estuarine environments, with a large supply of center of the key were using mostly fresh water,
fresh water at least during most of the year. The while those growing near the edge were using
supply of fresh water is necessary for the ocean water. The distribution of δD and δ18O
successful sexual reproduction of the fern, values of hardwood hammock species and those
because the gametophytic generation appears to of typical mangrove species shows clearly the
be very salt sensitive, compared to the large salt range of variation in the source of water (Fig. 5).
tolerance of the sporophytic generation (Medina et Mangrove species appear to use both fresh-and
al., 1990). ocean water, while the hardwood hammock
The proportion of fresh water supply to different species are practically restricted to freshwater
species in a mangrove community can be sources. This technique may prove to be
accurately estimated mea-suring the abundance valuable in clarifying complex zonations,
of stable isotopes of hydrogen and oxygen. In particularly in estuarine mangroves.

Concluding Remarks and Suggestions for Further Research

From the previous discussion on the physiology organic matter under high levels of
of mangrove species several points may be environmental stresses. Their physiological
highlighted as orientation for further research: analysis, therefore, has a large potential as a
tool to detect environmental change.
1. Mangrove species are good indicators of
long term salinity in their environment. The level 2. The occurrence, concentration, and
of exposure to salinity can be assessed through induction of synthesis of organic osmolites is
the analysis of the ionic composition of the an important field of research which will shed
leaves, root, and stem saps. Analysis of xylem light on the tolerance mechanisms of the
sap in particular, may be useful for the cytoplasm towards high osmotic
assessment of short term pollution and concentration in the vacuoles.
changes in the availability of fresh water. Xylem
sap composition reflects the differential 3. Analyses of cell permeability, as
permeability of root cells membranes and exemplified by the studies on Avicennia
therefore can be used as a sensitive indicator marina, have to be extended to other species
of metabolic or physical disturbances at the root with different tolerance to environmental
level. Mangrove ecosystems occur in the land- salinity. These studies could contribute to
sea interface, and are geared to produce explain the distribution of mangrove species

123
 Ecosistemas de Manglar E. Medina

in nature, and more important, may provide the introduce such characteristics into crop plants
basis to understand salinity tolerance in higher and contribute to the fulfillment of a very old
plants, particularly the maintenance of high K+ dream, the irrigation of farm lands with sea
levels in the presence of large amounts of Na+. water.
Modern molecular techniques may help to

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