Photosynthetic performance of magroves … 577

PHOTOSYNTHETIC PERFORMANCE OF MANGROVES Rhizophora mangle

AND Laguncularia racemosa UNDER FIELD CONDITIONS 1

Antelmo Ralph Falqueto 2, Diolina Moura Silva 3, Renata Venturim Fontes4

ABSTRACT – In mature mangrove plants Rhizophora mangle L. and Laguncularia racemosa Gaerth. growing
under field conditions, photosystem 2 (PS2) photochemical efficiency, determined by the ratio of variable
to maximum fluorescence (Fv /F m), increased during the day in response to salinity in the rainy seasons. During
the dry season, fluorescence values ( Fo) were higher than those observed in rainy season. In addition, Fo
decreased during the day in both season and species, except for R. mangle during the dry season. A positive
correlation among F v /F m and salinity values was obtained for R. mangle and L. Racemosa during the dry and
rainy seasons, showing that photosynthetic performance is maintained in both species under high salinities.
Carotenoid content was higher in L. Racemosa in both seasons, which represents an additional mechanism
against damage to the photosynthetic machinery. The chlorophyll content was not affected by salinity in
either species.

Keywords: chlorophyll fluorescence, photosynthetic pigments, photosystem.

DESEMPENHO FOTOSSINTÉTICO DE Rhizophora mangle E Laguncularia

racemosa EM CONDIÇÕES DE CAMPO

RESUMO – Em plantas adultas de Rhizophora mangle L. e Laguncularia racemosa Gaerth. crescendo

em condições de campo, a eficiência fotoquímica do fotossistema 2 (FS2), determinada pela razão
fluorescência variável : fluorescência máxima (F v /F m), aumentou durante o dia em resposta à salinidade,
durante a estação chuvosa. Durante a estação seca, os valores de Fo foram superiores aos observados
durante a estação chuvosa. Além disso, Fo reduziu-se ao longo do dia em ambas as estações e espécies,
exceto para R. mangle durante a estação seca. Uma correlação positiva entre os valores de F v /F m e
da salinidade foi obtida em R. mangle e L. racemosa durante as estações seca e chuvosa, mostrando
que o desempenho fotossintético é mantido em ambas as espécies sob altas salinidades. O conteúdo
de carotenóides foi maior em L. racemosa, em ambas as estações, representando um mecanismo adicional
contra danos à maquinaria fotossintética. O conteúdo de clorofila não foi afetado pela salinidade
das espécies estudadas.

Palavras-chave: Fluorescência da clorofila, pigmentos fotossintéticos e fotossistema.

1
Recebido em 09.03.2007 e aceito para publicação em 19.05.2008.
2
Departamento de Ciências da Saúde, Biológicas e Agrárias da Universidade Federal do Espírito Santo (UFES), São Mateus-ES.
3
Departamento de Ciências Biológicas da UFES. E-mail:<biovegetal@terra.com.br>
4
Programa de Pós-Graduação em Ciências Biológicas da UFES.

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 578 FALQUETO, A.R. et al.

1. INTRODUCTION under high irradiance, it might cause damage in to PS2,

as well as alterations in photosynthetic pigment
Rhizophora mangle L . and the Laguncularia
composition (MISHRA et al. 1991; MORALES et al.,
racemosa Gaerth. mangroves are two major species
1992; BELKODJA et al., 1994; TUFFERS et al., 2001;
in the district of Vitoria, Espírito Santo, Brazil and dominant
NAIDOO et al., 2002). However, most of these studies
in the American Atlantic coastlines. These species grow
were done in greenhouses, under controlled conditions,
in environments with widely ranging salinity, from near
using mature mangroves propgules as a source of the
freshwater to above seawater salinity (LOVELOCK and
plant material. Information about the physiological
FELLER, 2003; SUARÉZ, 2003; SOBRADO, 2004;
behavior of mature plants ofR. mangle and L. racemosa
SOBRADO, 2005). Salinity constitutes the main stressor
under field conditions is scarce. Thus, the objective
and regulator of the development and productivity
of the present study was to evaluate the photosynthetic
of mangrove forests (MEDINA et al., 1990; SOBRADO
performance of R. mangle and L. racemosa during the
and BALL, 1999). Mangrove species more tolerant to
day in the dry and rainy seasons of the year and relate
salinity may function with less efficient water transport,
this performance to variations in interstitial water salinity.
which may be related to more conservative water use
(SOBRADO, 2004). Krauss and Allen (2003) suggested 2. MATERIAL AND METHODS
high salinity tends to favor the development,
establishment and physiology of R. mangle. However, The study was conducted in the mangrove forest
other studies show that L racemosa is more tolerant around of the Universidade Federal do Espírito Santo
to the negative effects of salinity (SOBRADO, 2004). (20°15 '48"S and 40°18'17"N), Vitoria district, Espirito
Evidence for less salt sensitivity in mangrove species Santo, Brazil. Tidal amplitudes at the study area range
includes biochemical adaptations by wich mangroves between 0.3 and > 1 m. Mangrove forest is abundant
counter the high osmolarity of salt, like accumulation on clay and loam areas situated above mean high water
of compatible solutes or enhanced gland secretion level. The relative air humidity at the study site was
(TAKEMURA et al., 2000; KRAUSS and ALLEN, 2003; approximately 89% and annual average air temperature
SOBRADO, 2004). In contrast, responses of mangrove 26ºC. During the investigation period, annual precipitation
to salinity reflect alterations in photosynthesis, was 1250 mm, distributed in a dry (April to September)
photosynthetic pigment content, trasnpiration rate, and a rainy (October to March) season. Mangrove forest
and enzyme activities. Generally, these negative effects at the study site is composed of three tree species:
also associated with other environmental factors, e.g., Rhizophora mangle L. (Rhizophoraceae), Laguncularia
high light levels (TAKEMURA et al., 2000; KRAUSS racemosa Gaerth. (Combretaceae) and Avicennia
and ALLEN, 2003). germinans Stearn. (Avicenniaceae). R. mangle and
L. Racemosa are the dominant trees at the study site,
The photosynthetic performance of R. mangle and
while A. Germinans is little represented. All data were
L. racemosa mangrove species in the equatorial region
collected from ten trees, which varied in height from
of Brazil is little understood. It is known that integrity
2-4 m. Interstitial water was collected in the morning
of membranes, activity of several enzymes, nutrient
(9 a. m.), midday (1 p. m.) and afternoon (5 p. m.) using
acquisition, photosynthetic pigment content, gas
2.5 cm diameter PVC tube inserted at -0.2 m sediment
exchange and photosynthetic apparatus function are
depth, according to the method of Miller and Ullman
affected by high NaCl concentrations (ZHU, 2001).
(2004). Salinity measures of interstitial water were
In halophytes, some studies have showed that salinity
accomplished immediately after collecting the water
inhibits photosystem 2 (PS2) activity, while others indicate
in the tubes, using a portable condutometer SCHOT
the opposite (TAKEMURA et al., 2000; LU et al., 2002;
Mod. LF1.
QIU-FANG et al., 2005). Avicennia corniculatum and
Bruguiera gymnorrhiza showed a decrease in the Chlorophyll fluorescence parameters were
photosynthesis, whereas A. marina was not affected determined in situ on fully expanded young leaves
by the salinity (TAKEMURA et al., 2000). Other studies of R. mangle and L. Racemosa, in the morning, midday
showed that salt stress by itself has little effect on and afternoon using a portable Chlorophyll Fluorescence
the PS2 photochemical efficiency and on photosynthetic System (Handy-PEA, Hansatech, Norfolk, England)
pigment content under relatively low light levels. But, after 30 min of dark adaptation, using specially designed

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Photosynthetic performance of magroves … 579

clips attached to the leaves. These same leaves were and afternoon, respectively (Table 1). In contrast, Fv/
used for the determination of photosynthetic pigment Fm values increased significantly during the day for
contents (below). Each leaf was exposed to a saturation L. racemosa: 0.66, 0.74 and 0.80 at 9 a. m., 1 and 5 p.
pulse of light (750 µmol m -2 s-1; the value was obtained m., respectively. For R. mangle, the Fv/Fm values were
from a saturation curve) for 5 s. Initial fluorescence 0.68 at 9 a. m. and 0.77 at 1 and 5 p. m. (Table 1). Carotenoid
(Fo) and PS2 photochemical efficiency (Fv/Fm) were content was higher to L. racemosa in both seasons.
calculated automatically. There were no significant differences for chlorophyll
content between species and between seasons.
Chlorophyll and carotenoid contents were
determined in the morning using the spectrophotometric Fv/Fm reflects the PS2 potential efficiency and it
method suggested by Arnon (1949). Chlorophyll a (Chl is used as indicators of plant photosynthetic performance
a), chlorophyll b (Clh b), chlorophyll a/b ratio and (KAO and TSAI, 1999; SHIRKE and PATHRE, 2003;
carotenoids (Car) were calculated using the following RIBEIRO et al., 2004). In this study, the increase observed
equations, suggested by Hendry Grime (1993): Chl in Fv/Fm during the day for R. mangle and L. racemosa,
a (mg/L) = 12,7 x A663 - 2,69 x A645; Chl b (mg/l) = 22,9 in both seasons, can be attributed to a decrease in
x A 645 - 4,68 x A 663; Car = [A480 + 0,114 x A663 - 0,638 Fo, although the Fo values did not present a statistically
x A645) x V / 112,5 x Weight of the fresh matter of the reduction in R. mangle during the dry season. Fo
leaf (g)], where V = volume of the acetone extract in originates exclusively from the PS2 light harvest complex
cm3 and A = absorbance at the specified wavelength (LHC2) after the application of low red light on leaves
(nm), measured with a 1 cm cuvette. adapted to the dark (LICHTENTHALER et al., 2005)
and its values are, generally, strongly related to
Each data collection consisted of ten repetitions, photoinhibition phenomena. In addition, during the
in a randomized block design. For salinity, Fo and Fv/ rainy season, Fv/Fm of dark-adapted leaves increased
Fm, statistical comparisons were made between dry similarly during the day in response to increases in
and rainy seasons and between times during the day. salinity for both species. These results strongly suggest
Chlorophyll and carotenoid content values were compared that R. mangle and L. racemosa increase their
between species and between seasons. Salinity and photosynthetic efficiency in response to increases
Fv/Fm values were correlated in both species and seasons. in salinity levels.
Results were examined by one-way analysis of variance
(ANOVA) and differences between means were assessed Several studies have shown that high salinity causes
using Tukey test at 5% significance level (STATSOFT, a decrease of photosynthetic efficiency in mangrove
1995). species grown in greenhouses under different
concentrations of NaCl. However, the effects of salinity
3. RESULTS AND DISCUSSION on photosynthetic parameters of mangrove species
under field conditions are contradictory. The main reason
Significant increase in salinity was observed in for this contradiction is the large variation of field
the rainy season at 1 p. m. and 5 p. m. in relation to environmental conditions. Thus, results obtained in
that at 9 a. m. (Table 1). Furthermore, the salinity values a specific mangrove are cannot be extrapolated to
obtained in this season were higher than those in the mangroves situated in other regions.
dry season. During the rainy season, PS2 photochemical
efficiency (Fv/Fm) of dark-adapted leaves sampled at In this study, a positive correlation (r2 = 0.99) (not
9 a. m. were 0.73 and 0.69 forR. mangle and L. Racemosa, shown) among Fv/Fm and salinity values was obtained
respectively (Table 1). These values were significantly for both species and seasons, indicating that R. mangle
and L. racemosa presented high tolerance and
lower than those obtained at 1 and 5 p. m. and were
adaptability at high salinity. Halophytic plants are
inversely related to initial fluorescence values ( Fo).
tolerant to salinity because they are able to take up
During the dry season, Fo mean values were higher water through the accumulation of inorganic ions or
than those observed in the rainy season for both other compatible solutes such as betaine and proline.
mangrove species. In the dry season, Fo values Consequently, the osmotic potential decreases, which
decreased significantly in L. racemosa during the day, in turn attracts water into the cell and enables to maintain
from 1027 in the morning, to 875 and 675 in the midday pressure potential (MOGHAIEB et al., 2004).

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 580 FALQUETO, A.R. et al.

Table 1 - Photosynthetic efficiency ( F v /F m), initial fluorescence ( Fo), chlorophyll content (Chl a, Chl b, Chl a/b ratio)
and carotenoid content (Car) in leaves of Rhizophora mangle L. and Laguncularia racemosa Gaerth, subjected
to different salinity levels under field conditions. (n = 10)
Tabela 1 - Eficiência fotossintética (F v /F m), fluorescência inicial (Fo), conteúdo de clorofila (Chl a, Chl b, Chl a/b ratio)
e conteúdo de carotenóides (Car) em folhas de Rhizophora mangle L. e Laguncularia racemosa Gaerth. sujeitas
a diferenças da salinidade em condições de campo (n = 10)

Parameters Dry season Rainy season

mean mean
9 a.m. 1 p.m. 5 p.m. 9 a.m. 1 p.m. 5 p.m.
Rhizophora mangle L.
Salinity 10.5±3.4 12.04±1.9 11.7±1.4 11.4±0.81 B 13.4±0.3 b 19.8±3.6 a 20.94±0.8 a 18.04±4.0 A
Fv/Fm 0.68±0.02 b 0.77±0.03 a 0.77±0.03 a 0.74±0.05 0.73±0.02 b 0.8±0.003 a 0.82±0.001 a 0.78±0.04
Fo 986±267 886±192 844±200 905±72.94 A 840±133 a 581±0.0 b 546±11.8 b 655±160.5 B
Chl a 0.96±0.2 - - - 1.10±0.13 - - -
Chl b 0.64±0.1 - - - 0.77±0.14 - - -
Chl a/b ratio 1.47±0.12 - - - 1.4±0.0 - - -
Car 0.22±0.03 * - - - 0.26±0.03 * - - -
Laguncularia racemosa Gaerth.
Salinity 10.5±3.4 12.04±1.9 11.7±1.4 11.4±0.81 B 13.4±0.3 b 19.8±3.6 a 20.94±0.8 a 18.04±4,0 A
Fv/Fm 0.66±0.02 b 0.74±0.001 a 0.8±0.004 a 0.73±0.07 0.69±0.02 b 0.8±0.01a 0.83±0.0 a 0.77±0.07
Fo 1027±38.5 a 875±33.5 b 675±24 c 859±176.5 A 893±17.5 a 653±51 b 530±10.8 c 692±184.6 B
Chl a 1.03±0.2 - - - 1.13±0.16 - - -
Chl b 0.59±0.19 - - - 0.82±0.13 - - -
Chl a/b ratio 1.5±0.0 - - - 1.47±0.06 - - -
Car 0.3±0.04 * - - - 0.34±0.03 * - - -
Small letters indicate statistical difference along the day within of each season, while capital letters indicate statistical
difference between seasons.
Significant differences in carotenoid content between species in each season are represented by an asterisk (*) (Tukey test at 5%
probability level)

Leaf chlorophyll content (Chl a, Chl b and a/b which are also involved in protection against
ratio) on a fresh mass basis showed no significant photoinhibition. This is a photoprotective mechanism
difference for both (daily and seasonal) periods (Table and allows excess energy to be dissipated.Conversion
1). Lu et al. (2002) observed that salt stress had no of violaxanthin to zeaxanthin has been observed in
effects on the photosynthetic pigment composition other mangrove species under high salinity (SOBRADO
in halophyte Suaeda salsa, grown outdoors in plastic and BALL, 1999).
pots, subjected to salt concentrations up to 400 mM.
It is probable that the increase in both synthesis
Thus, chlorophyll content in R. mangle andL. racemosa
and accumulation of antioxidative pigments (carotenoids)
seems to be insensitive to salinity variations during
in L. racemosa during both dry and rainy seasons
the day and in both dry and rainy seasons.
represents an additional mechanism against damage
Rhizophora mangle and L. racemosa differed in to the photosynthetic machinery. Since Fv/Fm ratios
carotenoid content (Table 1). Higher carotenoid content of 0.75 - 0.85 have been considered normal for unstressed
was observed in L. racemosa in both seasons. plants (HUNT, 2003; OLIVEIRA et al., 2006), it can be
Carotenoids play important roles in plants: they act suggested that R. mangle and L. racemosa were able
as pigment antenna, enhancing the reception of luminous to maintain photosynthetic activity in response to salinity
energy for the reaction centers, and protect chlorophyll increases because of their protection mechanisms.
against photoxidative damage (GONÇALVES et al., 2001;
BEHERA and CHOUDHURY, 2002). During the protective 4. ACKNOWLEDGEMENTS
action, they are degraded. It is possible thatL. racemosa
is adapted to maintain higher carotenoid levels in its The authors would like to thank to Fundo de Apoio
cells. On the other hand, low carotenoid contents can à Pesquisa e Tecnologia do Município de Vitória
be a consequence of β -carotene degradation and (FACITEC) for the financial support, and the Laboratório
subsequent zeaxantin synthesis (through de-epoxidation de Ecofisiologia Vegetal of the Universidade Federal
of violaxanthin to antheraxanthin and to zeaxanthin), do Espírito Santo for supporting this work.

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Photosynthetic performance of magroves … 581

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