Trees (2006) 20:679?687
DOI 10.1007/s00468-006-0083-1
ORIGINAL ARTICLE
Ecophysiological characteristics of Avicennia germinans
and Laguncularia racemosa coexisting in a scrub mangrove
forest at the Indian River Lagoon, Florida
M. A. Sobrado ? Sharon M. L. Ewe
Received: 23 February 2006 / Revised: 3 July 2006 / Accepted: 11 July 2006 / Published online: 24 August 2006
C? Springer-Verlag 2006
Abstract The purpose of this work is to increase ecological
understanding of Avicennia germinans L. and Laguncularia
racemosa (L.) Gaertn. F. growing in hypersaline habitats
with a seasonal climate. The area has a dry season (DS)
with low temperature and vapour pressure deficit (vpd), and
a wet season (WS) with high temperature and slightly higher
vpd. Seasonal patterns in interstitial soil water salinity sug-
gested a lack of tidal flushing in this area to remove salt
along the soil profile. The soil solution sodium/potassium
(Na+/K+) ratio differed slightly along the soil profile during
the DS, but during the WS it was significantly higher at the
soil surface. Diurnal changes in xylem osmolality between
predawn (higher) and midday (lower) were observed in both
species. However, A. germinans had higher xylem osmolality
compared to L. racemosa. Xylem Na+/K+ suggested higher
selectivity of K+ over Na+ in both species and seasons. The
water relations parameters derived from pressure?volume
P?V curves were relatively stable between seasons for each
species. The range of water potentials (
), measured in the
field, was within estimated values for turgor maintenance
Communicated by P. Millard
M. A. Sobrado (


)
Laboratorio de Biolog??a Ambiental de Plantas, Departamento de
Biolog??a de Organismos, Divisio?n de Ciencias Biolo?gicas,
Universidad Simo?n Bol??var,
Apartado 89.000, Caracas 1080A, Venezuela
e-mail: msobrado@usb.ve
S. M. L. Ewe
Southeast Environmental Research Center,
Florida International University,
Miami, FL 33199, USA
S. M. L. Ewe
Smithsonian Marine Station,
701 Seaway Drive, Fort Pierce, FL 34949, USA
from P?V curves. Thus the leaves of both species were os-
motically adapted to maintain continued water uptake in this
hypersaline mangrove environment.
Keywords Leaf nitrogen partition . Potassium uptake
selectivity . Soil salinity . Water relations . Xylem
osmolality . Scrub forest
Introduction
Mangroves are trees that grow at the interface between
land and sea in tropical and subtropical latitudes. They can
thrive in a range of salinity conditions with low tidal ampli-
tudes, tolerate strong winds and high temperatures as well as
muddy anaerobic soils (Lugo and Snedaker 1974; Ball 1996;
Kathiresan and Bingham 2001). Mangroves are salinity tol-
erant and have mechanisms for water uptake despite low
soil water potential (Scholander 1968). However, there is a
trade-off between plant water uptake and soil water potential.
Water uptake under saline conditions tends to accumulate salt
around the roots which lowers soil water potentials further
(Passioura et al. 1992). Therefore, if mangroves use water
rapidly under highly saline conditions, the chance of run-
away embolisms would increase (Ball and Passioura 1994).
Increased salinity tolerance in mangroves is directly related
to improved water use efficiency (Ball 1988, 1996). This
conservative water use with salinity increase is a result of
the decrease in mangrove water transport capacity as well
(Sobrado 2000, 2001a). Low leaf-water-loss rates also limit
carbon gain rates which ultimately negatively affect the man-
grove growth as salinity increases (Ball et al. 1988; Ball and
Pidsley 1995).
Scrub mangroves are mature forests with individuals of
low stature and stunted growth which occur at high ele-
Springer
680 Trees (2006) 20:679?687
vation in the intertidal zone (Lugo and Snedaker 1974),
on high sulphide (McKee et al. 1988) and/or hypersaline
soils (Lin and Stemberg 1992a), as well as on nitrogen (N)
and phosphorus (P) poor soils (Feller et al. 2002, 2003).
There seems to be a threshold beyond which mangroves
change their life form as a result of lower input of nutri-
ents caused by infrequent flooding through the annual cycle
(Lo?pez-Portillo and Ezcurra 1989). Decline in photosynthe-
sis and growth as well as increase in water use efficiency
under hypersaline conditions seem to be common in scrub
mangrove forests (Lin and Stemberg 1992a, 1992b). Despite
the fact that hypersalinity poses problems for growth in all
mangroves, many species can survive under such conditions
(Saenger et al. 1977; Cintro?n et al. 1978; Field 1998). Scrub
mangrove forests along the Indian River Lagoon (Florida)
occupy areas where soil salt removal by tidal flushing is
infrequent, and evaporation rates are high (Lovelock and
Feller 2003). This hypersaline environment is also N-limited
(Feller et al. 2003). Avicennia germinans is the dominant
species and coexists with scattered L. racemosa (Feller et al.
2003; Lovelock and Feller 2003). Limited ecological success
of L. racemosa in this area is to some extent a consequence of
this resource-poor environment (McKee 1995). The purpose
of our work is to increase ecological understanding of this
hypersaline mangrove environment and explore the physio-
logical mechanisms that contribute to plant persistence and
tolerance under these conditions. The objectives of this work
were to investigate if
1. soil salinity changed with soil depth and season;
2. leaf characteristics and nutrient concentrations were cou-
pled through the seasons to the prevailing salinity condi-
tions; and
3. leaf water relations adjusted to maintain water uptake over
seasons.
Materials and methods
Study site and plant species
This study was conducted in Impoundment no. 23, located
in the northern Indian River Lagoon at North Hutchinson Is-
land, St. Lucie County, FL (27?33?N, 80?20?W). Details and
the history of this site are described in Lovelock and Feller
(2003).This area has a seasonal climate with a cool and rel-
atively dry season (DS) between November and April, and
a warmer rainy season (WS) between May and November
(Lovelock and Feller 2003). Mangrove stands within Im-
poundment 23 show three very-well-defined zones perpen-
dicular to the water?s edge (Feller et al. 2003; Lovelock and
Feller 2003). The narrow fringe is dominated by Rhizophora
mangle L., the transition zone is dominated by tall saplings of
L. racemosa and A. germinans, and the interior scrub zone
is dominated by A. germinans with scattered L. racemosa
(Feller et al. 2003).
This study was performed on A. germinans and L. race-
mosa plants growing in the scrub zone which is an open
stand of stunted trees. Here, the soil is hypersaline and re-
mains drained most of the year due to the low occurrence of
tidal flooding (Feller et al. 2003).
Field measurements were conducted between January and
July 2005. In January 2005, we tagged 10 pairs of randomly
selected trees of A. germinans and L. racemosa. As most of
the methods were destructive and the mangroves were small
( ? 1 m tall), we subsampled to minimize the impact on any
one plant. Plants were sampled at the end of DS (April) as
well as during the WS (July) 2005. We used the youngest
fully expanded leaves (second to fourth pair) of terminal
branches for all measurements. This overcame drastic age
differences within each sampling date. Leaf age influences
physiological function in mangrove species and particularly
in L. racemosa (Cram et al. 2002; Medina 1999).
Climatic characteristics
Meteorological data was retrieved from the nearest weather
station at Vero Beach Airport, approximately 10 km (27.6?N
80.4?W) from the study site (www.wunderground.com). To-
tal daily rainfall, maximum and minimum temperatures (t)
and air humidity (rh) data, from October 2004 to Octo-
ber 2005, were analysed. Midday temperature and rela-
tive humidity were used to calculate the air?water vapour
pressure deficit (vpd) by using the relationship: vpd = Ps?
(Psrh), where Ps is the saturation vapour pressure. Hence,
Ps = 610.78 ? e(t/(t+238.3)?17.2694) (Monteith and Unsworth
1990). This information allowed contextualizing the results
within an overview of the major climatic event of this area
during the period of work.
Soil salinity
Soil salinity was determined on rainless days during both
the dry (DS) and the wet (WS) season, as well as imme-
diately after rains in each season. Thus four soil salinity
sampling dates were taken. Interstitial water was collected
in the vicinity of each of the 20 tagged plants from wells
at 0, 0.3, 0.6 and 0.9 m depth. Well water was collected
and salinity was measured with a handheld refractometer
(RHS-10, Sinoptics Co., Fujian, China). In both seasons, six
interstitial water subsamples were adequately diluted and
sodium (Na+) and potassium (K+) content determined for
each depth with atomic absorption spectrometry. The objec-
tive of this was to determine the ratios of these elements and
compare them with those obtained from the plant xylem and
leaves.
Springer
Trees (2006) 20:679?687 681
Xylem analysis
At PD and MD during each season, samples of xylem sap
were extracted from terminal twigs by means of a pres-
sure chamber (Model 1400, PMS, Corvallis, OR) with a
microscope on top (Model 03890-40, Cole Parmer, Ver-
non Hills, IL). Stem xylem was extracted from a total of
six tagged plants of each species per season. Xylem sap
extracted by this method is vulnerable to contamination
(Pate 1976). Thus, to avoid contamination of xylem sap,
debarked twigs were rinsed with distilled water, and the
first drops of exuded xylem discarded. Afterwards, xylem
sap was collected on filter paper, and the osmolality mea-
sured immediately in a vapour pressure osmometer (Model
5500, Wescor Inc., Logan, UT). The filter paper samples
were dried in a convection oven and xylem sap was subse-
quently extracted in hot water for Na+ and K+ determination
via atomic absorption spectrometry. The selectivity ratio of
K+ over Na+ (SK,Na; Pitman 1965) uptake was calculated
by using K+ and N+ ratios for soil (from previous sec-
tion; Ks/Nas) and xylem (Kx/Nax). Thus, SK,Na = (Kx/Nax)/
(Ks/Nas).
Leaf characteristics and water relations
Each season, 12?20 leaves were collected from six plants
per species. The number of leaves collected depended on
leaf size as we required sufficient dried material for nutrient
and isotopic analyses. Immediately after collection, leaf fresh
weights and areas were determined. Leaf samples were then
oven-dried (70?C) for 24 h and dry mass measured. For each
sample, leaf mass to area ratio (Sw) was determined and wa-
ter content (WC) was expressed per dry mass and area basis.
These dried leaves were ground and homogenized for sub-
sequent chemical and isotopic analysis. Concentrations of P,
K+ and Na+ were analysed via atomic absorption spectrom-
etry after leaf digestion (Agricultural Analytical Services
Laboratory, Pennsylvania State University, University Park,
PA). Details of the procedures for microwave digestion, for
elemental analysis, are described elsewhere (Miller 1998).
Leaf carbon isotopic signatures (?13C) were also analysed in
the same six plants. These analyses were done in the Sta-
ble Isotope Research Facility for Ecological Research of the
University of Utah (Salt Lake City, USA) using an isotope
ratio mass spectrometer (Model delta S, Finnigan MAT, San
Jose, CA). Detailed description of the procedures can be
found in Ehleringer et al. (1992).
Three to five leaves of each of six plants per treatment were
collected, during the DS and WS, and frozen on dry ice im-
mediately after collection for determination of pigment com-
position. Chlorophylls (Chla+b) and carotenoids (xantophylls
and carotenoids) were extracted with 80% acetone and mea-
sured with a spectrophotometer (Model UV-265, Shimadzu,
Japan). Parameters were calculated following Lichtenthaler
and Wellburn (1983).
Leaf water relations
Pressure?volume (P?V) curves were determined on ran-
domly selected twigs during the DS and WS. On the af-
ternoon of the day prior to measurements, twigs selected
were rinsed with distilled water and bagged to allow maxi-
mal rehydration during nighttime. This procedure avoids the
problems associated with the rehydration of cut branches
(Kubiske and Abrams 1991). The following day, bagged
twigs were cut and transported to the laboratory for mea-
surements. Eight twigs per species (collected from differ-
ent plants) were allowed to dehydrate naturally on the lab-
oratory bench and P?V curves were constructed. During
dehydration, weight loss was determined on an analytical
balance (Model AE260, Mettler-Toledo Inc., Switzerland)
and water potential (
) measured immediately by using
the pressure chamber. The water content at full turgidity
was estimated for each sample according to Ladiges (1975).
Then the reciprocal of 
 (1/
) as a function of relative wa-
ter content (RWC) was plotted. These plots were used to
calculate osmotic potential at full (
(100)) and zero (
(0))
turgor, RWC at zero turgor (RWC0) as well as apoplas-
tic (A) water content (Tyree and Hammel 1982; Turner
1981).
The leaf 
 and its components 

?
and 
 t were deter-
mined during both WS and DS. Predawn and midday 
 were
measured in terminal twigs from six plants per species. A
pressure chamber with a shop microscope on top was used to
determine the balancing pressure of each twig. This balance
pressure is analogous to the matric potential (
m; Passioura
1980). The 
m is similar to total 
 provided that xylem 
?
is near zero (Boyer 1967, 1969; Kramer and Boyer 1995). In
mangrove species, xylem 

?
is well below zero representing
an important fraction of their 
 (Scholander et al. 1966).
Therefore, we added the xylem 

?
to 
m to estimate 
 val-
ues. The xylem 

?
was obtained by expressing xylem osmo-
lality in pressure units (see the section Xylem analysis). Once
measurement with the pressure chamber was completed,
leaf samples (excluding major veins) were placed in plastic
syringes and frozen immediately on dry ice. Upon return to
the laboratory, samples were thawed 30 min. The leaf sap
was squeezed and measured in a vapour pressure osmometer
to determine leaf osmotic pressure (

?
). Then the 

?
values
were corrected by the dilution of apoplastic water by using
values obtained from P?V curves (see below). Leaf turgor
pressure (
 t) was calculated as the difference between 

and 

?
.
Springer
682 Trees (2006) 20:679?687
Statistical analysis
Within each season, differences in salinity and Na+/K+ with
soil depth were obtained by one-way analysis of variance
(ANOVA). Homogeneity in variance was tested and a post
hoc test to determine least significant difference (LSD) was
performed. For each season, salinity comparison (rainy vs.
rainless days) at each soil depth was conducted using in-
dependent samples Student?s t test. This test was also used
to compare soil Na+/K+ between seasons at each depth.
Within each species, the significance seasonal differences of
each parameter were tested by using independent samples
Student?s t test. Diurnal changes (predawn vs. midday) in 

and its components were tested by using one-way ANOVA
and a post hoc test to determine the LSD between seasons for
each species. Details of the statistical procedures followed
Sokal and Rohlf (1969).
Results and discussion
Climatic conditions
Accumulated precipitation, monthly mean of daily maxi-
mum and minimum air temperatures, and air saturation vpd
are shown in Figure 1. January and April were relatively drier
(dry season), with lower temperatures and slightly lower vpd
compared to July (wet season). Thus the DS was mild in
terms of evaporative demand of the atmosphere as suggested
R
ai
nf
al
l (m
m)
0
500
1000
1500
(
 T
o
)C
0
10
20
30
 dp
v
)
aPk(
0.5
1.0
1.5
2.0
2.5
O     N     D     J      F     M      A     M     J      J       A     S      O
Months
A
B
C
Fig. 1 A Cumulative rainfall, B monthly average of daily maximum
(?) and minimum ( ? ) temperatures, and C midday air?water vapour
pressure deficit (vpd) as a function of time. Values (October 2004?
October 2005) were redrawn using data from the Vero Beach Meteo-
rological Station. Values are means and bars represent standard error
(SE). Standard errors were sometimes less than the width of the symbol
Dry Season               Wet Season
0 50 100
So
il 
de
pt
h 
(m
)
0.0
0.3
0.6
0.9
0 50 100
A B
Salinity (?)
50 60 70
Soil Na+/K+
50 60 70
So
il 
de
pt
h 
(m
)
0.0
0.3
0.6
0.9
a
b
c
d
ab
a
b
C D
a
b
c
a
b
c
d
a
ab
b
ab
a
b
b
b
b b
Fig. 2 Dry and wet season soil salinity A, B and Na+/K+ ratios C,
D as a function of soil depth. Soil salinity was measured either just
after rains (open circles) or during rainless days (closed symbols) in
20 wells at each depth. Soil Na+/K+ were determined at the time of
plant measurements (rainless days) in selected samples from six wells
at each depth. Values are mean ( ? SE) and with each data set, values
followed by different letters were statistically different at p<0.05
by the low temperature and vpd. By contrast, during the
WS, the prevailing high temperature and slightly higher vpd
suggested a large evaporative potential.
Soil salinity
Interstitial soil water salinity showed the largest fluctuations
at the soil surface, reflecting the prevailing weather condi-
tions. In early as well as late DS, salinity was approximately
40 parts per thousand (?) at the soil surface and about
51? at 0.30 m during rainless days (Fig. 2A). How-
ever, just after rains, salinity declined significantly to about
26? (p<0.001) at the soil surface but increased significantly
to 58? (p<0.001) at 0.30 m. Thus, salt seemed to be washed
into the soil after rains. However, interstitial salinity showed
greater fluctuations during the WS (Fig. 2B). Thus, during
rainless periods, soil salinity rose significantly (p>0.001)
up to 73? at the soil surface, but remained at about 51? at
Springer
Trees (2006) 20:679?687 683
0.30 m (Fig. 2B). After heavy rains, soil surface salinity
declined significantly (p<0.001) to about 37? and con-
comitantly increased significantly (p<0.001) at 0.30 m to
65? (p<0.001). The rains reduced surface soil salinity for
a few days until water drained. Plant root water uptake and
salt exclusion could also potentially contribute to shallow
interstitial salinity fluctuations during the active growing
season. Unlike the shallower depths, interstitial soil salinity
at 0.60 m ( ? 67?) and 0.9 m ( ? 75?) were remarkably
constant over two seasons and independent of rainfall
patterns. Seasonal patterns in soil salinity suggested a lack
of tidal flushing in this area to remove salt from these depths.
Therefore, our results support the hypersaline observations
of this mangrove area (Feller et al. 2003) and showed that
the hypersalinity encountered was not seasonally relieved
despite increased rainfall during the summer.
All plant measurements in this study were done during
rainless periods in both seasons. The soil solution Na+/K+
ratio differed slightly along the soil profile during the DS
(Fig. 2C). Conversely, Na+/K+ was significantly higher at
the soil surface and showed slight variation within the soil
profile during the WS (Fig. 2D). Indeed, at the soil surface the
Na+/K+ was significantly (p<0.01) higher at the soil surface
during WS compared to DS. The selective uptake of K+
over Na+ would contribute to increased Na+/K+ particularly
during growing season. Therefore, our results suggest that
a seasonal switch in water sources could take place. During
the cool DS, roots potentially utilized water from below
the soil surface ( ? 0.3 m) where the thermal environment
would be less severe and water viscosity lower (i.e. less
saline). During the WS, the frequency and availability of
rainfall derived freshwater inputs, despite high temperatures
at the soil surface, would support surface plant water uptake.
Therefore, plant water uptake by roots could be switched to
this zone. These observations indicate that mangrove roots
in this habitat would be generally concentrated at the upper
parts (<0.5 m) of the soil profile. Overall, mangrove species
are characterized as having shallow roots (Tomlinson 1986).
Xylem sap composition
Xylem salt concentration in mangroves decreases hyperbol-
ically with water flux (Ball and Passioura 1994). Diurnal
changes in xylem osmolality between predawn (PD, high
xylem osmolality) and midday (MD, low xylem osmolality)
values were observed in both species in concordance with
Ball and Passioura (1994). Xylem osmolality of A. germi-
nans varied diurnally from 244 ? 48 (PD) to 188 ? 18 (MD)
mosmol kg?1 and between 279 ? 18 (PD) and 231 ? 17
(MD) mosmol kg?1 during the DS and WS, respectively. In
L. racemosa xylem osmolality ranged from 109 ? 34 (PD)
to 50 ? 21 (MD) mosmol kg?1 during the DS, and during the
WS values of 106 ? 13 (PD) to 85 ? 7 (MD) mosmol kg?1
Xy
le
m
 N
a+
 
/ K
+
 
(m
o
lm
o
l-1
)
0
2
4
6
A
A. germinans       L. racemosa
D         W             D        W
S K
,N
a
0
10
20 B
Fig. 3 A Xylem Na+ to K+ ratios and B selectivity of K+ over Na+
(SK,Na) measured in A. germinans and L. racemosa during both wet (W)
and dry (D) season. Each value is the mean of 5?11 samples and bars
represent SE. There were no seasonal differences within each species
were observed. It has been repeatedly determined that salt-
secreting Avicennia species can transport relatively greater
salt concentrations in their xylem stream relative to other
mangrove species (Scholander et al. 1962, 1966; Waisel
et al. 1966; Ball 1988; Sobrado 2001b). In this case, despite
the fact that both species are salt-secreting, A. germinans is
able to sustain higher secretion rates than L. racemosa under
comparable salinities (Sobrado 2002, 2004). Xylem ionic
composition of salt-tolerant plants changes and Na+/K+ in-
creases (Munns 1985, 1988). Here, xylem Na+/K+ did not
show differences between seasons in each species (Fig. 3B).
Values of Na+/K+ in both mangrove species were within
the same range. Compared to soil Na+/K+ values however,
xylem values between 1.8 and 2.8 in both species were con-
siderably lower than the ratios observed in the soil (Fig. 3A).
This confirmed a preferential plant uptake of K+ over Na+.
Indeed, plant roots have higher selectivity of K+ over Na+
as shown by the SK,Na (Fig. 3B). Overall, values reported
here compared well with previous mangrove studies (Med-
ina 1999). The xylem Na+/K+ ratio seemed to be dependent
on transpiration rate suggesting that the root system was un-
able to modify the ion composition of the xylem at very high
flow rates (Munns 1985). It is well known that channels al-
lowing K+ uptake are highly selective and that Na+ enters
these channels when its concentration is very high in the soil
solution (Amtman and Sanders 1999).
Leaf mineral and pigment composition
In both species, leaf dry mass per unit leaf area was signif-
icantly higher in more mature leaves collected during DS
Springer
684 Trees (2006) 20:679?687
Table 1 Leaf mass to leaf area
ratio (Sw), content of nitrogen
(N), phosphorous (P), potassium
(K+), sodium (Na+), Na+ to K+
ratio (Na+/K+), chlorophylls
(Chl), total carotenoids (Car)
and carbon isotopic composition
(?13C) in A. germinans and L.
racemosa
A. germinans L. racemosa
Parameter Dry Wet Dry Wet
Sw (g m?2) 206 (6)?? 164 (11) 186 (9)??? 139 (7)
N (mmol m?2) 189 (6)?? 163 (5) 116 (1)?? 94 (3)
P (mmol m?2) 7.2 (0.5) 6.4 (0.4) 4.6 (0.1) 4.6 (0.3)
K+ (mmol m?2) 52 (3)?? 39 (3) 36 (2)? 29 (1)
Na+ (mmol m?2) 211 (4)? 182 (9) 138 (11)? 104 (9)
Na+/K+ 4.1 (0.3) 4.7 (0.4) 3.9 (0.4) 3.7 (0.3)
Chla (mmol m?2) 257 (34) 299 (20) 317 (63) 271 (7)
Chlb (mmol m?2) 65 (7)?? 93 (5) 85 (9) 100 (5)
Chl(a/b) 3.9 (0.4) 3.2 (0.1) 3.8 (0.3)? 2.7 (0.2)
Car(x+c) (mg m?2) 113 (10) 90 (4) 89 (6)?? 63 (2)
?
13C (parts per mil) ? 26.6 (0.2) ? 26.8 (0.2) ? 26.7 (0.2) ? 27.2 (0.1)
Values are mean and standard error (SE) of samples taken in six plants per species taken during the dry season
(DS; April 2005) and wet season (WS; July 2005).
Seasonal differences between means are indicated as ?p<0.05; ??p<0.01; ???p<0.001 for each species.
than during the younger leaves collected during WS (Table
1). Similarly, leaf N, K+ and Na+ per unit leaf area tended to
increase significantly during the DS in both species, whereas
leaf P remained unchanged. Values of leaf elemental compo-
sition were very similar to those previously found in this site
and in other habitats (Feller et al. 2003; Medina and Fran-
cisco 1997). As expected, leaf Na+/K+ concentrations were
comparable to those detected in the xylem stream (Fig. 3).
Total chlorophyll (Chl(a+b)) was comparable in both
species over the two seasons (Fig. 4). The Chla concen-
Ch
l (a
+b
) (
mo
l m
-
2 )
0.0
0.1
0.2
0.3
0.4
0.5
Ch
l (a
+b
) / 
N 
(m
ol 
mo
l-1
)
0
1
2
3
4
5
A
B
D       W         D  W
A. germinans   L. racemosa
*
Fig. 4 Total chlorophyll (Chl(a+b)) and ratio of Chl(a+b) to nitrogen
(Chl(a+b)/N) measured in A. germinans (black) and L. racemosa (white)
during both wet (W) and dry (D) seasons. Each value is the mean of
six plants, and bars represents SE. Seasonal differences within each
species is indicated by ?p<0.05
trations remained stable over seasons while Chlb tended to
decline in A. germinans during DS. The Chla to Chlb ratio
was significantly lower in L. racemosa during the WS which
suggested that leaves might not have been fully mature (Table
1; ?Sesta?k 1985). However, the observed values were typical
of sunny and healthy leaves ( ?Sesta?k 1985). Total carotenoids
tended to be higher during DS but it was significant only in
L. racemosa. Pigment composition in both species was in-
dicative of healthy and photosynthetically active leaves and
comparable to values from previous workers (Medina and
Francisco 1997; Sobrado 1999). Nitrogen investment in leaf
chlorophylls (Chl(a+b)/N) was higher in L. racemosa com-
pared to A. germinans (Fig. 3). In A. germinans, Chl(a+b)/N
was significantly (p<0.05) lower during the DS despite the
fact that leaf N tended to increase. This pattern of N alloca-
tion into Chl(a+b) in A. germinans reflects a trade-off between
N investment in photosynthetic machinery and in synthesis
of compatible solutes (Medina and Francisco 1997; Sobrado
1999; Ball and Sobrado 2001). Under hypersaline conditions,
there is enhancement in the synthesis of compatible organic
solutes in mangrove species (Popp 1984; Popp et al. 1984).
This shunting of N to organic solutes therefore reduces the
potential nitrogen use efficiency of A. germinans (Sobrado
1999). Comparison of A. germinans and L. racemosa at this
site has shown that L. racemosa had higher potential nitrogen
use efficiency (Lovelock and Feller 2003). Carbon isotopic
composition (?13C) showed similar high values which sug-
gested comparably high long-term water use efficiency in
both species. By contrast, short-term water use efficiency
has been shown to be significantly higher in A. germinans in
a previous study at this site (Lovelock and Feller 2003).
Leaf water relations parameters
Significant seasonal changes in leaf water content (Wc) were
found in A. germinans but not in L. racemosa (Table 2)
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Trees (2006) 20:679?687 685
Table 2 Leaf water content (Wc), osmotic potential at full (
? (100)) and zero (
? (0)) turgor, relative water content at zero turgor (RWC0) and
apoplastic water content (A) estimated from pressure?volume curves in A. germinans and L. racemosa leaves during both dry and wet season
A. germinans L. racemosa
Parameter Dry Wet Dry Wet
Wc (g m?2) 335 (11) 353 (53) 533 (53) 486 (48)


?(100) (MPa) ? 3.09 (0.13) ? 3.27 (0.15) ? 2.69 (0.16) ? 2.86 (0.10)


?(0) (MPa) ? 4.94 (0.12) ? 5.24 (0.15) ? 3.64 (0.15)??? ? 4.49 (0.09)
RWC0 (%) 76.7 (1.9) 72.8 (0.9) 84.4 (1.2)??? 73.7 (0.5)
A (%) 36.9 (5.5) 27.7 (2.4) 40.9 (4.4)? 26.6 (3.6)
Each value is the mean ( ? SE) of eight samples per species per season.
Within each species, statistical differences between seasons are indicated as ?p<0.05; ???p<0.001.
although L. racemosa tended to have higher Wc. The water
relations parameters derived from P?V curves proved to be
relatively stable between seasons for each species as well
(Table 2). Overall, P?V parameters agreed entirely with pre-
vious studies with these species growing in the field under
high salinity (Sua?rez et al. 1998; Sobrado 2004).
Plant osmotic potential at full (

?(100)) did not differ sea-
sonally within species although osmotic potential at zero
turgor (

?(0)) was slightly lower in L. racemosa during the
WS. This would suggest more elastic cells in more recently
expanded leaves of L. racemosa during the WS, as sup-
ported by the observed lower relative water content at zero
turgor (RWC0) as well. Thus, we did not find evidence of
seasonal changes in osmotic adjustment within either man-
grove species. This suggested a lack of seasonal variation in
salinity at the active root water uptake zone of both species.
Nevertheless, the lowest 

?(100) and 
?(0) were recorded
in A. germinans compared to L. racemosa. In both species,
Na+ and Cl? accounts for most of the leaf osmotic po-
tential (

?
) which increases as salinity increases (Medina
and Francisco 1997). In this study, leaf Na+ tended to be
higher in A. germinans with lower 

?
than in L. racemosa
(Table 2). Apoplastic water content (A) tended to increase
slightly during DS but this was statistically significantly only
in L. racemosa (Table 3). In other mangroves species, it has
been reported that A also tends to increase during drought,
and consequently the symplasmic water fraction declines
(Rada et al. 1989). Nevertheless, A derived from P?V curves
is an extremely variable parameter even in homogeneous
material (Richter 1997).
Diurnal changes of 
 and its components, namely 

?
and turgor pressure (
 t) are shown in Fig. 5. Predawn
and midday xylem osmolalities (osmotic component) were
used to correct measurements with the pressure chamber
(hydrostatic pressure) to obtain 
. We found that in A.
germinans, the osmotic component represented 15.7 ? 0.6%
and 9.1 ? 0.2% of predawn and midday 
, respectively. In
L. racemosa it represented 6.9 ? 0.6% and 4.4 ? 0.1%, re-
spectively. This suggested the importance of this correction
for mangrove species thriving on hypersaline habitats. The

 declined significantly from predawn to midday in both
species during the DS and WS (Fig. 5B). In both species, a
similar trend emerged in predawn and midday leaf osmotic
potentials (Fig. 5C). The lowest midday leaf turgor (
 t) was
recorded during the hot rainy season in both A. germinans
and L. racemosa (Fig. 5A). These midday changes in 
 and
its components during the WS was the result of plants being
exposed to high temperature, vpd, and soil salinity (Figs. 1
and 2B). Overall, the range of 
 measured in the field for
both species (Fig. 5B) were within estimated 
 and turgor
maintenance from P?V curves. This suggests the capability
of both species to maintain turgor-dependent physiological
process (Jones et al. 1981). However, A. germinans would be
able to sustain lower 
 without turgor loss which suggested
enhanced capability in this species for water uptake in
hypersaline soils through establishment of large 
 gradients
between leaf and soil. This would aid the maintenance of pos-
itive leaf gas exchange under hypersalinity. Conversely, L.
racemosa plants were evidently less adjusted to hypersalin-
ity. Indeed, L. racemosa experienced lower diurnal water
deficits as shown by relatively high midday 
 (Fig. 5B). The
maintenance of leaf 
 above turgor loss in L. racemosa may
be achieved at the expense of controlling water loss which
would decrease carbon gain as well, and finally plant growth.
The possibility of L. racemosa roots occupying low saline
soil patches was low in this particular site. However, we
could not discard the possibility that L. racemosa maximized
carbon gain and growth during the short periods after rains
when salinity was low at the soil surface. Nevertheless, both
species were similarly efficient in their long-term water use
patterns, as shown by their high ?13C signatures (Table 1).
Concluding remarks
In conclusion, A. germinans and L. racemosa were subjected
to seasonal differences in rainfall, amount and frequency,
as well as temperature and vpd. During the WS, rains
occurred at high frequency but potential evaporation was
also higher. Conversely, during the DS, drought spells were
Springer
686 Trees (2006) 20:679?687
?






	


		
?
?






	


		
?







	


   

 	
 
 	
	



a
a
b
aba b
c
c
a
a
b
ac
b
a
a
a
aab
ab
b
c c
a
a
Fig. 5 Turgor pressure (
 t), water potential (
) and osmotic potential
(

?
) measured at predawn (white bars) and midday (black bars) in A.
germinans and L. racemosa leaves during both dry (D) and wet (W)
seasons. Each value is the mean of six plants, and bars represent SE.
Within each species, different letters indicate statistical differences at
p<0.05
more frequent but potential evaporation was lower than
in the WS because of lower ambient temperatures. The
seasonal conditions led to a relatively stable year-round
hypersaline environment. Leaves of both species were
well adapted to thrive under these hypersaline conditions
through adjustment in their water relations and maintaining
a preferential uptake of K+ over Na+. Thus, the leaves
of both species were osmotically adjusted to hypersalinity
during both seasons which would allow water uptake and
turgor maintenance. However, plants of A. germinans were
adapted to develop lower 
 without turgor loss compared
to L. racemosa. In spite of the limited N investment in
chlorophyll (part of the photosynthetic machinery) found
in A. germinans in this N-limited habitat, it seemed better
adjusted in its water relations characteristics compared to L.
racemosa. This may foster the dominance of A. germinans
over L. racemosa in this environment. A number of ecophys-
iological studies with Avicennia sp. have showed greater
tolerance of harsh environmental conditions accounting for
its survival and dominance over other mangrove species.
However, the possibility of differential switching between
surface water and groundwater use between the dry and
wet seasons is worth further investigation to understand the
long-term coexistence of these mangrove species.
Acknowledgements This is a Smithsonian Marine Station (SMS)
Contribution No. 663, Southeast Environmental Research Center Con-
tribution No. 330 and Universidad Simo?n Bol??var (DID-FT-2005). We
are pleased to thank Dr. V. Paul for giving us the opportunity to con-
duct this study at SMS, J. Kaminski, H. Reichardt, J. Piraino and
W. Lee for logistic and technical support at the SMS at Fort Pierce,
as well as the referees and Professor E. Medina (IVIC, Venezuela)
for helpful suggestions on this manuscript. Ewe was in part sup-
ported by the National Science Foundation (DEB-9910514) during this
study.
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