Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 307--313
© 1996 Heron Publishing----Victoria, Canada
Interaction of flooding and salinity stress on baldcypress (Taxodium
distichum)
JAMES A. ALLEN,1 S. REZA PEZESHKI2 and JIM L. CHAMBERS3
1
National Biological Service, Southern Science Center, 700 Cajundome Blvd., Lafayette, LA 70506, USA
2
Biology Department, Division of Ecology and Organismal Biology, University of Memphis, Memphis, TN 38152, USA
3
School of Forestry, Wildlife and Fisheries, Louisiana State University, Louisiana Agricultural Experiment Station, Baton Rouge, LA 70803, USA
Received March 2, 1995
Summary Coastal wetlands of the southeastern United
States are threatened by increases in flooding and salinity as a
result of both natural processes and man-induced hydrologic
alterations. Furthermore, global climate change scenarios suggest that, as a consequence of rising sea levels, much larger
areas of coastal wetlands may be affected by flooding and
salinity in the next 50 to 100 years. In this paper, we review
studies designed to improve our ability to predict and ameliorate the impacts of increased flooding and salinity stress on
baldcypress (Taxodium distichum (L.) Rich.), which is a dominant species of many coastal forested wetlands. Specifically,
we review studies on species-level responses to flooding and
salinity stress, alone and in combination, we summarize two
studies on intraspecific variation in response to flooding and
salinity stress, we analyze the physiological mechanisms
thought to be responsible for the interaction between flooding
and salinity stress, and we discuss the implications for coastal
wetland loss and the prospects for developing salt-tolerant lines
of baldcypress.
Keywords: multiple stress, salt tolerance, stress interaction,
waterlogging.
Introduction
Forested wetlands in which baldcypress (Taxodium distichum
(L.) Rich.) is a dominant overstory tree species are common in
the southeastern U.S. coastal plain (Larsen 1980, Wilhite and
Toliver 1990), often at elevations of 2 m or less above mean sea
level (Salinas et al. 1986, DeLaune et al. 1987). Many of these
coastal wetlands have recently been exposed to increases in
flooding or salinity stress, or both, as a result of a combination
of natural processes (e.g., land subsidence) and man-induced
alterations of hydrology and sedimentation (Figure 1; Craig et
al. 1979, Wicker et al. 1981, Templet and Meyer-Arendt 1988,
Conner and Toliver 1990, Allen 1992). If predicted climate
changes occur, the consequent rise in sea level will cause
flooding and saltwater intrusion in many coastal areas (Titus
1988, Smith and Tirpak 1989, Kerr 1991, Daniels 1992,
Wigley and Raper 1993). In the southeastern U.S., such intru-
sion will compound the already significant problems of degradation and loss of forested coastal wetlands (Figure 2).
Although much is known about the general responses of
baldcypress and associated species to flooding and salinity
(Pezeshki et al. 1986, 1987, 1988, 1990, Pezeshki 1990, 1993,
Conner and Askew 1992, Conner 1994), less is known about
the responses of baldcypress to both stresses combined. However, in many other plant species, a combination of flooding
and salinity stress reduces survival and growth more than
either stress alone (Van der Moezel et al. 1988, 1991, Marcar
et al. 1993, Noble and Rogers 1994). For example, Pezeshki
(1992) found that flooding with 3 g l −1 artificial seawater
reduced net photosynthesis of loblolly pine (Pinus taeda L.), a
species moderately tolerant of soil waterlogging (Hook 1984),
by 96% compared to flooding with freshwater.
In this paper, we review species-level effects on baldcypress
of flooding alone, salinity alone, and flooding in combination
with salinity. We then summarize two studies on intraspecific
variation in response to a combination of flooding and salinity
stress. We also consider possible mechanisms that may underlie the interaction between flooding and salinity stress on
baldcypress, and briefly discuss possible strategies for the
protection, management and restoration of coastal baldcypress
forests. We focus on baldcypress because of its economic and
ecological importance and its perceived vulnerability to both
current environmental changes and predicted global climate
change.
Species-level effects of flooding and salinity
Effects of flooding
Baldcypress is considered to be highly tolerant of flooding and
soil waterlogging (McKnight et al. 1981, Hook 1984, Brown
and Montz 1986, Keeland 1994). Nevertheless, the increasing
depth and duration of flooding to which coastal swamps are
being subjected is threatening the long-term existence of baldcypress in some areas, even without the additional factor of
salinity (DeLaune et al. 1987, Conner and Brody 1989). One
reason for this is that baldcypress seeds generally do not
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ALLEN, PEZESHKI AND CHAMBERS
Figure 1. Louisiana Gulf Coast forests (including baldcypress–water tupelo swamps) currently experiencing increased flooding or saltwater
intrusion, or both. Reproduced from Pezeshki et al. 1987, by permission of the Society of Wetland Scientists.
Figure 2. Baldcypress swamp near Dulac,
LA, that has been killed by saltwater intrusion.
germinate under water (Demaree 1932), and therefore, natural
regeneration is unlikely or even impossible under conditions
of permanent flooding. Also, growth is substantially reduced
in deep (> 1 m), permanently flooded swamps compared to
swamps with intermittent flooding (Conner and Day 1976). In
some cases, permanent deep flooding has accelerated the decline and death of established baldcypress trees (Demaree
1932, Eggler and Moore 1961, Harms et al. 1980, Brown and
Montz 1986).
Several studies have indicated that baldcypress seedlings
generally tolerate shallow flooding, but that flooded seedlings
go through an initial period of stress and adaptation during
which they are outperformed by unflooded well-watered controls. For example, Shanklin and Kozlowski (1985) reported
that, following 14 weeks of flooding at 2 cm above the soil
surface, baldcypress seedlings were 30% shorter, had 56%
less leaf area, and had 51% less total dry weight than
unflooded controls. Flynn (1986) observed that seedlings in a
drained treatment had slightly higher above- and belowground
biomass, and significantly greater total biomass than seedlings
FLOODING AND SALINITY STRESS IN BALDCYPRESS
flooded to a depth of 15 to 20 cm for 126 days.
Seedlings generally recover from the stress imposed by
continuous shallow flooding and may grow as rapidly as seedlings subjected to well-watered conditions or periodic flooding. Megonigal and Day (1992), who conducted a 3-year study
in large outdoor rhizotrons, found that, after 1 year, continuously flooded seedlings had approximately one third the
biomass of seedlings subjected to periodic flooding. By the
second year, growth of the continuously flooded seedlings had
improved substantially, and by the end of the third year, there
were no significant differences in total biomass between seedlings in the two treatments. Improved growth in the second
year coincided with morphological changes in the roots, including the development of water roots and changes in root
distribution.
Physiological studies have demonstrated that although baldcypress seedlings survive and grow when flooded, their physiological performance is initially impaired. For example, root
elongation is inhibited in baldcypress seedlings subjected to
hypoxic (+200 mV soil redox potential) soil conditions for
2 weeks (Pezeshki 1991). Short-term declines in Rubisco activity have also been reported in response to flooding
(Pezeshki 1994b). Pezeshki et al. (1986) found that net photosynthesis (A) and stomatal conductance (gw) of baldcypress
seedlings subjected to shallow flooding for 40 days declined
by 21 and 41%, respectively, compared with the values for
unflooded controls; however, both A and gw recovered to 80
and 90%, respectively, of pretreatment values within 2 to
3 weeks (Pezeshki et al. 1987, Pezeshki 1993). This recovery
may be related to a resumption of root function following
development of intercellular air spaces (aerenchyma), which
begin to develop in the first 2 weeks of flooding (Pezeshki
1991), and have been shown to play a vital role in maintaining
root functioning of numerous wetland species (Blom et al.
1994, Pezeshki 1994a)
Effects of salinity
Baldcypress seedlings are moderately salt-tolerant. Pezeshki
(1990) found no significant effects on height growth, net photosynthesis or stomatal conductance when baldcypress seedlings were watered with a 3 g l −1 saltwater solution for 60 days
(Figure 3). Even in seedlings regularly watered with a 10 g l −1
saltwater solution for 3 months, survival was 100% and their
mean height was 83% of controls watered with freshwater
(Conner 1994).
Effects of a combination of flooding and salinity
Several studies have shown that a combination of flooding and
salinity is considerably more detrimental to baldcypress seedlings than the effect of either stress alone, and the detrimental
effects of a combination of flooding and salinity increase with
increasing salinity (Javanshir and Ewel 1993, Conner 1994).
Flooding seedlings with 3 g l −1 saltwater for 60 days reduced
both height growth and A by about 50% compared with wellwatered controls; however, the differences were only significant for height growth (Pezeshki 1990) (Figure 3). In contrast,
seedlings watered with 10 g l −1 saltwater survived and grew
309
Figure 3. Mean values of net photosynthesis, leaf conductance and
height growth as affected by flooding (F), salinity (S, 3 g l − 1) and
flooding plus salinity (FS); C represents a well-watered, but unflooded
control.
reasonably well, whereas seedlings continuously flooded with
10 g l −1 saltwater all died within 2 weeks (Conner 1994).
Wicker et al. (1981) concluded that baldcypress wetlands are
limited to areas where salinity does not exceed 2 g l −1 for more
than 50% of the time that the trees are exposed to inundation
or soil saturation (cf. Chabrek 1972). However, Myers et al.
(1995) report that seedlings planted from 1 to 4 years previously in a frequently flooded marsh were thriving despite a
nearly constant groundwater salinity of 2.8 g l −1.
Intraspecific variation in tolerance to combined flooding
and salinity stress
Baldcypress seedlings exhibit intraspecific variation in tolerance to a combination of flooding and salinity stress (Allen
1994, Pezeshki et al. 1995). Pezeshki et al. (1995) evaluated
the flooding and salt tolerance of baldcypress seedlings from
two sources in Louisiana----a coastal, brackish area and an
inland freshwater area----by subjecting the seedlings to shallow
flooding with 0, 4 or 8 g l −1 salt in a controlled-environment
chamber for 6 weeks. Although gas exchange rates of seedlings from the two sources were comparable in the various
treatments, seedlings from the freshwater source had significantly greater growth than seedlings from the brackish source.
In the shallow flooding with 4 g l −1 salt treatment, net shoot
and root biomass of freshwater plants were 86 and 97%
greater, respectively, than those of brackish plants. In the
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ALLEN, PEZESHKI AND CHAMBERS
shallow flooding with 8 g l −1 salt treatment, shoot biomass was
60% greater in freshwater plants than in brackish plants but
root growth was not significantly different between sources.
Allen (1994) evaluated intraspecific variation in responses
to combined flooding and salinity stress of seedlings from 15
open-pollinated families. Ten families were from coastal locations in Louisiana or Alabama that had surface water salinities
between 0.4 and 15.3 g l −1 at the time of seed collection in
November (brackish sources). The other five families were
from areas slightly further inland that were not subject to
saltwater intrusion (freshwater sources). Seedlings were
flooded to about 5 cm above the soil surface with 0, 2, 4, 6 or
8 g l −1 artificial seawater for 4 months.
All 15 families were tolerant of 2 g l −1 salt in combination
with shallow flooding, although there was a significant overall
decline in mean leaf area per seedling between the 0 and 2 g
l −1 treatments. In the shallow flooding with 4 g l −1 salt treatment, some families exhibited moderate declines in survival
and substantial decreases in leaf area and biomass. In the
shallow flooding with 6 and 8 g l −1 salt treatments, survival
ranged from 42 to 97%, and there were large differences
among families in mean leaf area and biomass. In general,
families from brackish sources were more tolerant of the combined salinity and flooding stresses than families from freshwater sources, suggesting a moderate degree of heritability. In
the shallow flooding with 6 g l −1 salt treatment, the mean leaf
area per seedling for the 10 families from brackish sources
(93 cm2) was more than four times greater than the mean for
the five families from freshwater sources (22 cm2). Overall
differences between the two sources were substantially less in
the shallow flooding with 8 g l −1 salt treatment, although
several families from brackish sources still greatly outperformed all five families from freshwater sources.
A notable difference among families was the differential
pattern of leaf retention and loss. The more tolerant families
gradually lost older basal leaves, while retaining or producing
healthy younger leaves. At the end of the study, individual
seedlings often had only a small cluster of leaves at the top of
the stem. These individuals did not exhibit dieback at the top
of the plant. Less tolerant seedlings exhibited partial stem
dieback and partial refoliation along the lower portion of the
stem. These leaf responses are similar to those described in
Australian tree species differing in tolerance to salinity or
flooding plus salinity stress (Van der Moezel et al. 1988). Thus
it appears that there is a substantial degree of variation within
the baldcypress species, with some individuals exhibiting responses characteristic of moderately tolerant species and others having responses more typical of salt-sensitive species.
Significant differences in gas exchange were found among
the 15 families (Figure 4). Two of the families (LS1 and SW1)
maintained rates of A consistently above the overall mean for
the 15 families. Two other families (PB1 and PR1) had consistently below-average photosynthetic rates. Within-family variation was also high, and some individual seedlings in the
shallow flooding with 6 and 8 g l −1 salt treatments maintained
rates of photosynthesis as high as the overall mean for the
controls.
Figure 4. Effect of salinity on mean net photosynthesis in four selected
baldcypress families (Allen 1994).
Although significant differences among families were found
for all physiological response variables except midday leaf
water potential, only differences in nutrient uptake were correlated with tolerance to flooding and salinity. The three most
tolerant families had 34% lower Na+ and 20% lower Cl− concentrations in their leaf tissue than the overall mean for the 15
families.
Possible mechanisms for flooding and salinity interaction
Although many adaptations to saline environments are known
to exist in plants, exclusion of Na+, Cl− and other ions from leaf
tissue is believed to be the primary means by which most
glycophytes tolerate salinity (Greenway and Munns 1980,
Lauchli 1984, Ashraf 1994). The consequences of failure to
exclude Na+, Cl− and other ions from leaf tissue may include
water stress, ion toxicity or imbalances, and hormonal imbalances (Flowers et al. 1977, Greenway and Munns 1980,
Poljakoff-Mayber 1988). However, some species of glycophytes tolerate salt by a strategy more typical of halophytes,
whereby Na+ or Cl−, or both, is taken up into leaves and
compartmentalized in cell vacuoles (Van Steveninck et al.
1982), usually with the concomitant production of organic
solutes in the cytoplasm for osmotic adjustment (Flowers et al.
1977).
In baldcypress, sensitivity to salinity is probably related to
its relative inability to exclude ions or effectively compartmentalize them in cell vacuoles. The finding that the more tolerant
families of baldcypress had lower Na+ and Cl− concentrations
in leaf tissue than the less tolerant families (Allen 1994)
suggests that that regulation of Na+ and Cl− uptake is a critical
factor affecting salt tolerance of baldcypress. Pezeshki et al.
(1988, 1990) and Allen (1994) found that leaf tissue ionic
concentration of baldcypress seedlings increased with increasing salinity of the floodwater, and relatively strong and negative relationships between leaf ionic content and A were found
FLOODING AND SALINITY STRESS IN BALDCYPRESS
311
Conclusions
Figure 5. Relationship between leaf tissue Na+ concentration and net
photosynthesis (A). Reproduced from Pezeshki et al. 1988, by permission of the University of Notre Dame.
for all ions tested (Figure 5). The results of both studies suggest
that the excess accumulation of ions disrupts photosynthesis,
perhaps through inhibition of carboxylating enzyme activities.
The relationship between A and leaf ion concentrations also
indicates that the ion compartmentation process was not efficient enough to prevent metabolic dysfunction.
The decline in photosynthesis associated with relatively
small increases in leaf Na+ and Cl− concentrations may inhibit
root functioning. For example, some adaptations to flooding,
such as the development of new aerenchymatous roots, which
oxidize the rhizosphere and make temporary use of anaerobic
metabolic pathways (Flynn 1986, Pezeshki 1991, Yamamoto
1992, Kludze et al. 1994), require energy, and therefore may
be adversely affected by declines in assimilate production.
Little is known about the mechanism of ion exclusion in
baldcypress roots, but if it is an active process, then it may
become increasingly ineffective as the energy status of the
plant declines, thereby allowing more ions into the leaves,
further disrupting photosynthesis and eventually causing leaf
mortality.
Allen (1994) found that as salinity of floodwater increased
from 0 to 4 g l −1, leaf biomass declined substantially more than
root biomass. The Na+/Ca2+ and Na+/K+ ratios in root tissue
remained stable at low salinities. Above 4 g l −1, however, the
relative proportion of biomass allocated to roots declined. At
the same time, the Na+/Ca2+ and Na+/K+ ratios in the roots
began to increase dramatically, suggesting that ion imbalances
were occurring in the roots, and that root functions (including
active exclusion mechanisms) were being severely impaired.
The high Na+/Ca2+ and Na+/K+ ratios may also indicate a
breakdown in root membrane integrity, which would affect
passive uptake of ions (Alam 1993).
We conclude that baldcypress is highly susceptible to the
combined stress of flooding and salinity. Depending on the
severity of the stress imposed, one possible outcome of a rise
in sea level and other alterations of baldcypress-dominated
forests is the loss of wetlands on the scale depicted in Figure 1.
Alternatively, a shift in species dominance toward native associates or exotics such as Chinese tallow (Sapium sebiferum (L.)
Roxb.) (Pezeshki et al. 1990, Conner 1994) could occur.
It may be possible to slow or even reverse the effects of
flooding and salinity stress on coastal wetlands by a combination of engineering and genetic approaches (sensu Epstein et
al. 1980). Engineering approaches designed to reintroduce
freshwater and sediments to coastal wetlands have been widely
advocated and some projects have been initiated (Templet and
Meyer-Arendt 1988, Wetland Conservation and Restoration
Task Force 1990).
The genetic approach seeks to develop lines with increased
tolerance to combined flooding and salinity stress. The potential of this approach has not been realized; however, it is
encouraging to note that intraspecific variability in tolerance
of baldcypress seedlings to the two stresses combined has been
demonstrated (Allen 1994, Pezeshki et al. 1995). Although the
most tolerant families in Allen’s (1994) study came from the
more brackish sites, the study of Pezeshki et al. (1995) suggests that tolerant genotypes may also come from freshwater
sources, indicating the need to screen a wide selection of
genotypes.
The development of reliable screening methods will depend
on a detailed understanding of the mechanisms by which
salinity and flooding affect baldcypress. In particular, we need
more information about intraspecific variation in root morphology, and translocation and storage of Na+ and Cl− in young
and old leaves, as well as a better understanding of ion exclusion mechanisms and how they are affected by a combination
of flooding and salinity stress. Early formation of Casparian
bands may be a major factor affecting differential ion exclusion of Eucalyptus camaldulensis Dehnh. genotypes (Thomson 1988). Casparian band development at the lateral
root--endodermis interface (Marschner 1986, Shannon et al.
1988) and at the periderm and exodermis (Moon et al. 1986)
may also be important in determining flooding and salinity
tolerance.
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© 1996 Heron Publishing----Victoria, Canada
Interaction of flooding and salinity stress on baldcypress (Taxodium
distichum)
JAMES A. ALLEN,1 S. REZA PEZESHKI2 and JIM L. CHAMBERS3
1
National Biological Service, Southern Science Center, 700 Cajundome Blvd., Lafayette, LA 70506, USA
2
Biology Department, Division of Ecology and Organismal Biology, University of Memphis, Memphis, TN 38152, USA
3
School of Forestry, Wildlife and Fisheries, Louisiana State University, Louisiana Agricultural Experiment Station, Baton Rouge, LA 70803, USA
Received March 2, 1995
Summary Coastal wetlands of the southeastern United
States are threatened by increases in flooding and salinity as a
result of both natural processes and man-induced hydrologic
alterations. Furthermore, global climate change scenarios suggest that, as a consequence of rising sea levels, much larger
areas of coastal wetlands may be affected by flooding and
salinity in the next 50 to 100 years. In this paper, we review
studies designed to improve our ability to predict and ameliorate the impacts of increased flooding and salinity stress on
baldcypress (Taxodium distichum (L.) Rich.), which is a dominant species of many coastal forested wetlands. Specifically,
we review studies on species-level responses to flooding and
salinity stress, alone and in combination, we summarize two
studies on intraspecific variation in response to flooding and
salinity stress, we analyze the physiological mechanisms
thought to be responsible for the interaction between flooding
and salinity stress, and we discuss the implications for coastal
wetland loss and the prospects for developing salt-tolerant lines
of baldcypress.
Keywords: multiple stress, salt tolerance, stress interaction,
waterlogging.
Introduction
Forested wetlands in which baldcypress (Taxodium distichum
(L.) Rich.) is a dominant overstory tree species are common in
the southeastern U.S. coastal plain (Larsen 1980, Wilhite and
Toliver 1990), often at elevations of 2 m or less above mean sea
level (Salinas et al. 1986, DeLaune et al. 1987). Many of these
coastal wetlands have recently been exposed to increases in
flooding or salinity stress, or both, as a result of a combination
of natural processes (e.g., land subsidence) and man-induced
alterations of hydrology and sedimentation (Figure 1; Craig et
al. 1979, Wicker et al. 1981, Templet and Meyer-Arendt 1988,
Conner and Toliver 1990, Allen 1992). If predicted climate
changes occur, the consequent rise in sea level will cause
flooding and saltwater intrusion in many coastal areas (Titus
1988, Smith and Tirpak 1989, Kerr 1991, Daniels 1992,
Wigley and Raper 1993). In the southeastern U.S., such intru-
sion will compound the already significant problems of degradation and loss of forested coastal wetlands (Figure 2).
Although much is known about the general responses of
baldcypress and associated species to flooding and salinity
(Pezeshki et al. 1986, 1987, 1988, 1990, Pezeshki 1990, 1993,
Conner and Askew 1992, Conner 1994), less is known about
the responses of baldcypress to both stresses combined. However, in many other plant species, a combination of flooding
and salinity stress reduces survival and growth more than
either stress alone (Van der Moezel et al. 1988, 1991, Marcar
et al. 1993, Noble and Rogers 1994). For example, Pezeshki
(1992) found that flooding with 3 g l −1 artificial seawater
reduced net photosynthesis of loblolly pine (Pinus taeda L.), a
species moderately tolerant of soil waterlogging (Hook 1984),
by 96% compared to flooding with freshwater.
In this paper, we review species-level effects on baldcypress
of flooding alone, salinity alone, and flooding in combination
with salinity. We then summarize two studies on intraspecific
variation in response to a combination of flooding and salinity
stress. We also consider possible mechanisms that may underlie the interaction between flooding and salinity stress on
baldcypress, and briefly discuss possible strategies for the
protection, management and restoration of coastal baldcypress
forests. We focus on baldcypress because of its economic and
ecological importance and its perceived vulnerability to both
current environmental changes and predicted global climate
change.
Species-level effects of flooding and salinity
Effects of flooding
Baldcypress is considered to be highly tolerant of flooding and
soil waterlogging (McKnight et al. 1981, Hook 1984, Brown
and Montz 1986, Keeland 1994). Nevertheless, the increasing
depth and duration of flooding to which coastal swamps are
being subjected is threatening the long-term existence of baldcypress in some areas, even without the additional factor of
salinity (DeLaune et al. 1987, Conner and Brody 1989). One
reason for this is that baldcypress seeds generally do not
308
ALLEN, PEZESHKI AND CHAMBERS
Figure 1. Louisiana Gulf Coast forests (including baldcypress–water tupelo swamps) currently experiencing increased flooding or saltwater
intrusion, or both. Reproduced from Pezeshki et al. 1987, by permission of the Society of Wetland Scientists.
Figure 2. Baldcypress swamp near Dulac,
LA, that has been killed by saltwater intrusion.
germinate under water (Demaree 1932), and therefore, natural
regeneration is unlikely or even impossible under conditions
of permanent flooding. Also, growth is substantially reduced
in deep (> 1 m), permanently flooded swamps compared to
swamps with intermittent flooding (Conner and Day 1976). In
some cases, permanent deep flooding has accelerated the decline and death of established baldcypress trees (Demaree
1932, Eggler and Moore 1961, Harms et al. 1980, Brown and
Montz 1986).
Several studies have indicated that baldcypress seedlings
generally tolerate shallow flooding, but that flooded seedlings
go through an initial period of stress and adaptation during
which they are outperformed by unflooded well-watered controls. For example, Shanklin and Kozlowski (1985) reported
that, following 14 weeks of flooding at 2 cm above the soil
surface, baldcypress seedlings were 30% shorter, had 56%
less leaf area, and had 51% less total dry weight than
unflooded controls. Flynn (1986) observed that seedlings in a
drained treatment had slightly higher above- and belowground
biomass, and significantly greater total biomass than seedlings
FLOODING AND SALINITY STRESS IN BALDCYPRESS
flooded to a depth of 15 to 20 cm for 126 days.
Seedlings generally recover from the stress imposed by
continuous shallow flooding and may grow as rapidly as seedlings subjected to well-watered conditions or periodic flooding. Megonigal and Day (1992), who conducted a 3-year study
in large outdoor rhizotrons, found that, after 1 year, continuously flooded seedlings had approximately one third the
biomass of seedlings subjected to periodic flooding. By the
second year, growth of the continuously flooded seedlings had
improved substantially, and by the end of the third year, there
were no significant differences in total biomass between seedlings in the two treatments. Improved growth in the second
year coincided with morphological changes in the roots, including the development of water roots and changes in root
distribution.
Physiological studies have demonstrated that although baldcypress seedlings survive and grow when flooded, their physiological performance is initially impaired. For example, root
elongation is inhibited in baldcypress seedlings subjected to
hypoxic (+200 mV soil redox potential) soil conditions for
2 weeks (Pezeshki 1991). Short-term declines in Rubisco activity have also been reported in response to flooding
(Pezeshki 1994b). Pezeshki et al. (1986) found that net photosynthesis (A) and stomatal conductance (gw) of baldcypress
seedlings subjected to shallow flooding for 40 days declined
by 21 and 41%, respectively, compared with the values for
unflooded controls; however, both A and gw recovered to 80
and 90%, respectively, of pretreatment values within 2 to
3 weeks (Pezeshki et al. 1987, Pezeshki 1993). This recovery
may be related to a resumption of root function following
development of intercellular air spaces (aerenchyma), which
begin to develop in the first 2 weeks of flooding (Pezeshki
1991), and have been shown to play a vital role in maintaining
root functioning of numerous wetland species (Blom et al.
1994, Pezeshki 1994a)
Effects of salinity
Baldcypress seedlings are moderately salt-tolerant. Pezeshki
(1990) found no significant effects on height growth, net photosynthesis or stomatal conductance when baldcypress seedlings were watered with a 3 g l −1 saltwater solution for 60 days
(Figure 3). Even in seedlings regularly watered with a 10 g l −1
saltwater solution for 3 months, survival was 100% and their
mean height was 83% of controls watered with freshwater
(Conner 1994).
Effects of a combination of flooding and salinity
Several studies have shown that a combination of flooding and
salinity is considerably more detrimental to baldcypress seedlings than the effect of either stress alone, and the detrimental
effects of a combination of flooding and salinity increase with
increasing salinity (Javanshir and Ewel 1993, Conner 1994).
Flooding seedlings with 3 g l −1 saltwater for 60 days reduced
both height growth and A by about 50% compared with wellwatered controls; however, the differences were only significant for height growth (Pezeshki 1990) (Figure 3). In contrast,
seedlings watered with 10 g l −1 saltwater survived and grew
309
Figure 3. Mean values of net photosynthesis, leaf conductance and
height growth as affected by flooding (F), salinity (S, 3 g l − 1) and
flooding plus salinity (FS); C represents a well-watered, but unflooded
control.
reasonably well, whereas seedlings continuously flooded with
10 g l −1 saltwater all died within 2 weeks (Conner 1994).
Wicker et al. (1981) concluded that baldcypress wetlands are
limited to areas where salinity does not exceed 2 g l −1 for more
than 50% of the time that the trees are exposed to inundation
or soil saturation (cf. Chabrek 1972). However, Myers et al.
(1995) report that seedlings planted from 1 to 4 years previously in a frequently flooded marsh were thriving despite a
nearly constant groundwater salinity of 2.8 g l −1.
Intraspecific variation in tolerance to combined flooding
and salinity stress
Baldcypress seedlings exhibit intraspecific variation in tolerance to a combination of flooding and salinity stress (Allen
1994, Pezeshki et al. 1995). Pezeshki et al. (1995) evaluated
the flooding and salt tolerance of baldcypress seedlings from
two sources in Louisiana----a coastal, brackish area and an
inland freshwater area----by subjecting the seedlings to shallow
flooding with 0, 4 or 8 g l −1 salt in a controlled-environment
chamber for 6 weeks. Although gas exchange rates of seedlings from the two sources were comparable in the various
treatments, seedlings from the freshwater source had significantly greater growth than seedlings from the brackish source.
In the shallow flooding with 4 g l −1 salt treatment, net shoot
and root biomass of freshwater plants were 86 and 97%
greater, respectively, than those of brackish plants. In the
310
ALLEN, PEZESHKI AND CHAMBERS
shallow flooding with 8 g l −1 salt treatment, shoot biomass was
60% greater in freshwater plants than in brackish plants but
root growth was not significantly different between sources.
Allen (1994) evaluated intraspecific variation in responses
to combined flooding and salinity stress of seedlings from 15
open-pollinated families. Ten families were from coastal locations in Louisiana or Alabama that had surface water salinities
between 0.4 and 15.3 g l −1 at the time of seed collection in
November (brackish sources). The other five families were
from areas slightly further inland that were not subject to
saltwater intrusion (freshwater sources). Seedlings were
flooded to about 5 cm above the soil surface with 0, 2, 4, 6 or
8 g l −1 artificial seawater for 4 months.
All 15 families were tolerant of 2 g l −1 salt in combination
with shallow flooding, although there was a significant overall
decline in mean leaf area per seedling between the 0 and 2 g
l −1 treatments. In the shallow flooding with 4 g l −1 salt treatment, some families exhibited moderate declines in survival
and substantial decreases in leaf area and biomass. In the
shallow flooding with 6 and 8 g l −1 salt treatments, survival
ranged from 42 to 97%, and there were large differences
among families in mean leaf area and biomass. In general,
families from brackish sources were more tolerant of the combined salinity and flooding stresses than families from freshwater sources, suggesting a moderate degree of heritability. In
the shallow flooding with 6 g l −1 salt treatment, the mean leaf
area per seedling for the 10 families from brackish sources
(93 cm2) was more than four times greater than the mean for
the five families from freshwater sources (22 cm2). Overall
differences between the two sources were substantially less in
the shallow flooding with 8 g l −1 salt treatment, although
several families from brackish sources still greatly outperformed all five families from freshwater sources.
A notable difference among families was the differential
pattern of leaf retention and loss. The more tolerant families
gradually lost older basal leaves, while retaining or producing
healthy younger leaves. At the end of the study, individual
seedlings often had only a small cluster of leaves at the top of
the stem. These individuals did not exhibit dieback at the top
of the plant. Less tolerant seedlings exhibited partial stem
dieback and partial refoliation along the lower portion of the
stem. These leaf responses are similar to those described in
Australian tree species differing in tolerance to salinity or
flooding plus salinity stress (Van der Moezel et al. 1988). Thus
it appears that there is a substantial degree of variation within
the baldcypress species, with some individuals exhibiting responses characteristic of moderately tolerant species and others having responses more typical of salt-sensitive species.
Significant differences in gas exchange were found among
the 15 families (Figure 4). Two of the families (LS1 and SW1)
maintained rates of A consistently above the overall mean for
the 15 families. Two other families (PB1 and PR1) had consistently below-average photosynthetic rates. Within-family variation was also high, and some individual seedlings in the
shallow flooding with 6 and 8 g l −1 salt treatments maintained
rates of photosynthesis as high as the overall mean for the
controls.
Figure 4. Effect of salinity on mean net photosynthesis in four selected
baldcypress families (Allen 1994).
Although significant differences among families were found
for all physiological response variables except midday leaf
water potential, only differences in nutrient uptake were correlated with tolerance to flooding and salinity. The three most
tolerant families had 34% lower Na+ and 20% lower Cl− concentrations in their leaf tissue than the overall mean for the 15
families.
Possible mechanisms for flooding and salinity interaction
Although many adaptations to saline environments are known
to exist in plants, exclusion of Na+, Cl− and other ions from leaf
tissue is believed to be the primary means by which most
glycophytes tolerate salinity (Greenway and Munns 1980,
Lauchli 1984, Ashraf 1994). The consequences of failure to
exclude Na+, Cl− and other ions from leaf tissue may include
water stress, ion toxicity or imbalances, and hormonal imbalances (Flowers et al. 1977, Greenway and Munns 1980,
Poljakoff-Mayber 1988). However, some species of glycophytes tolerate salt by a strategy more typical of halophytes,
whereby Na+ or Cl−, or both, is taken up into leaves and
compartmentalized in cell vacuoles (Van Steveninck et al.
1982), usually with the concomitant production of organic
solutes in the cytoplasm for osmotic adjustment (Flowers et al.
1977).
In baldcypress, sensitivity to salinity is probably related to
its relative inability to exclude ions or effectively compartmentalize them in cell vacuoles. The finding that the more tolerant
families of baldcypress had lower Na+ and Cl− concentrations
in leaf tissue than the less tolerant families (Allen 1994)
suggests that that regulation of Na+ and Cl− uptake is a critical
factor affecting salt tolerance of baldcypress. Pezeshki et al.
(1988, 1990) and Allen (1994) found that leaf tissue ionic
concentration of baldcypress seedlings increased with increasing salinity of the floodwater, and relatively strong and negative relationships between leaf ionic content and A were found
FLOODING AND SALINITY STRESS IN BALDCYPRESS
311
Conclusions
Figure 5. Relationship between leaf tissue Na+ concentration and net
photosynthesis (A). Reproduced from Pezeshki et al. 1988, by permission of the University of Notre Dame.
for all ions tested (Figure 5). The results of both studies suggest
that the excess accumulation of ions disrupts photosynthesis,
perhaps through inhibition of carboxylating enzyme activities.
The relationship between A and leaf ion concentrations also
indicates that the ion compartmentation process was not efficient enough to prevent metabolic dysfunction.
The decline in photosynthesis associated with relatively
small increases in leaf Na+ and Cl− concentrations may inhibit
root functioning. For example, some adaptations to flooding,
such as the development of new aerenchymatous roots, which
oxidize the rhizosphere and make temporary use of anaerobic
metabolic pathways (Flynn 1986, Pezeshki 1991, Yamamoto
1992, Kludze et al. 1994), require energy, and therefore may
be adversely affected by declines in assimilate production.
Little is known about the mechanism of ion exclusion in
baldcypress roots, but if it is an active process, then it may
become increasingly ineffective as the energy status of the
plant declines, thereby allowing more ions into the leaves,
further disrupting photosynthesis and eventually causing leaf
mortality.
Allen (1994) found that as salinity of floodwater increased
from 0 to 4 g l −1, leaf biomass declined substantially more than
root biomass. The Na+/Ca2+ and Na+/K+ ratios in root tissue
remained stable at low salinities. Above 4 g l −1, however, the
relative proportion of biomass allocated to roots declined. At
the same time, the Na+/Ca2+ and Na+/K+ ratios in the roots
began to increase dramatically, suggesting that ion imbalances
were occurring in the roots, and that root functions (including
active exclusion mechanisms) were being severely impaired.
The high Na+/Ca2+ and Na+/K+ ratios may also indicate a
breakdown in root membrane integrity, which would affect
passive uptake of ions (Alam 1993).
We conclude that baldcypress is highly susceptible to the
combined stress of flooding and salinity. Depending on the
severity of the stress imposed, one possible outcome of a rise
in sea level and other alterations of baldcypress-dominated
forests is the loss of wetlands on the scale depicted in Figure 1.
Alternatively, a shift in species dominance toward native associates or exotics such as Chinese tallow (Sapium sebiferum (L.)
Roxb.) (Pezeshki et al. 1990, Conner 1994) could occur.
It may be possible to slow or even reverse the effects of
flooding and salinity stress on coastal wetlands by a combination of engineering and genetic approaches (sensu Epstein et
al. 1980). Engineering approaches designed to reintroduce
freshwater and sediments to coastal wetlands have been widely
advocated and some projects have been initiated (Templet and
Meyer-Arendt 1988, Wetland Conservation and Restoration
Task Force 1990).
The genetic approach seeks to develop lines with increased
tolerance to combined flooding and salinity stress. The potential of this approach has not been realized; however, it is
encouraging to note that intraspecific variability in tolerance
of baldcypress seedlings to the two stresses combined has been
demonstrated (Allen 1994, Pezeshki et al. 1995). Although the
most tolerant families in Allen’s (1994) study came from the
more brackish sites, the study of Pezeshki et al. (1995) suggests that tolerant genotypes may also come from freshwater
sources, indicating the need to screen a wide selection of
genotypes.
The development of reliable screening methods will depend
on a detailed understanding of the mechanisms by which
salinity and flooding affect baldcypress. In particular, we need
more information about intraspecific variation in root morphology, and translocation and storage of Na+ and Cl− in young
and old leaves, as well as a better understanding of ion exclusion mechanisms and how they are affected by a combination
of flooding and salinity stress. Early formation of Casparian
bands may be a major factor affecting differential ion exclusion of Eucalyptus camaldulensis Dehnh. genotypes (Thomson 1988). Casparian band development at the lateral
root--endodermis interface (Marschner 1986, Shannon et al.
1988) and at the periderm and exodermis (Moon et al. 1986)
may also be important in determining flooding and salinity
tolerance.
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