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2U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Blvd., Lafayette, Louisiana 70506; and 3Wetlands Biogeochemistry Institute, Louisiana State University, Baton Rouge, Louisiana 70803
Received for publication February 13, 1998. Accepted for publication October 30, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: coastal marsh • Louisiana • plant growth recovery • resiliency • salinity stress • wetlands
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Odum, 1988
; Earle and Kershaw, 1989
). Geological processes involved in forming the Louisiana gulf coast (Byrne, Leroy, and Reilly, 1959
; Coleman and Gagliano, 1964
; Penland and Suter, 1989
) have facilitated the development of extensive marsh areas (9.7 x 105 ha; Field et al., 1991
). These marshes are characterized by very low elevation, and salinity gradients within them can be easily affected by hydrologic events.
Natural phenomena that can lead to temporary salinity increases followed by freshwater flushing in coastal marshes include strong frontal passages and hurricanes. Jackson, Foote, and Balistrieri (1995)
deployed automated data loggers in a southeast Louisiana oligohaline marsh located 
38 km from the path of a hurricane. They found a 1.5-m storm surge and a surface water salinity increase from 0.5–1 g/L to 10–15 g/L over a 4-h period during the storm, and they measured a residual salt wedge in soil water 55 d after the hurricane. Other researchers documenting ephemeral salinity changes associated with hurricanes include Meeder (1987)
, who noted a 10 g/L elevation in a Louisiana bayou system, and Alexander (1967)
, who measured a 16.4 g/L increase in soil chloride 3 wk following a hurricane in Florida.
Field observations on the effects of temporary salinity changes associated with hurricane passage on plant communities indicated that species composition may be altered (Alexander, 1967
; Valentine, 1977
). Although the impact of increased salinity on wetland plant growth and distribution has been described in many studies (e.g., Haller, Sutton, and Barlow, 1974
; Cooper, 1982
; DeLaune, Pezeshki, and Patrick, 1987
; Pezeshki, DeLaune, and Patrick, 1987a
, b
; Matoh, Matsushita, and Takahashi, 1988
; McKee and Mendelssohn, 1989
; Whigham, Jordan, and Miklas, 1989
; Zedler, Pauling, and McComb, 1990
; Blits and Gallagher, 1991
; Bertness, Gough, and Shumway, 1992
; Marcum and Murdoch, 1992
; Bandyopadhyay et al., 1993
; Baldwin, McKee, and Mendelssohn, 1996
), relatively few controlled experiments have focused on plant recovery after salinity stress. Grace and Ford (1996)
devised a field experiment to examine the effects of temporary saltwater intrusion, flooding, and simulated herbivory on Sagittaria lancifolia, an oligohaline marsh perennial. Following 1 wk of elevated salinity, ambient conditions were reestablished and plants were allowed an 8-mo recovery period; the authors concluded that S. lancifolia had a substantial capacity for recovery (Grace and Ford, 1996
).
In a greenhouse study, Flynn, McKee, and Mendelssohn (1995)
increased salinity to cause complete dieback of aboveground tissue in freshwater marsh mesocosms and then manipulated salinity and water depth over a 10-mo recovery period. They found that several species exhibited some ability to recover and that the effect of elevated salinity became more pronounced under flooded as opposed to drained conditions during the recovery phase. Reduced photosynthesis was found in a growth chamber study with the salt marsh species Spartina alterniflora during transient (5-d) fluctuations in salinity; the response was reversed when salinity values were returned to original levels (Hwang and Morris, 1994
). Llewellyn and Shaffer (1993)
used very short-term (i.e., hours) salinity increases in a greenhouse study to simulate storm surges; after 72 h of exposure to salinity as high as 15 g/L, the freshwater perennial herb Justicia lanceolata recovered fully when flushed with freshwater.
These studies have demonstrated that plants can recover from temporary salinity stress under certain conditions. Questions remain, however, concerning the effect of variations in the components of a salinity stress event, such as intensity and duration, on plant recovery and survival. In a companion paper, we measured the growth response of four common oligohaline marsh species to short-term salinity increases (Howard and Mendelssohn, 1999
). In the present paper, we describe the ability of these species to recover (i.e., attain growth equivalent to that of unstressed plants) during a single growing season after exposure to pulses of increased salinity. Our objectives were to quantify the influences of final salinity, rate of salinity increase, and duration of salinity exposure on plant recovery after stress has been relieved. This study is the first to investigate the effects of these salinity pulse components on plant recovery.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Specimens of Eleocharis palustris (L.) Roemer and J. A. Schultes, Panicum hemitomon J. A. Schultes, Sagittaria lancifolia L., and Scirpus americanus Pers. were collected in April 1990 from low salinity (average less than 2 g/L) emergent marshes in coastal southeastern Louisiana. Details on collection site characteristics and plant material handling and acclimation are provided in Howard and Mendelssohn (1999)
.
Initial conditions for the experiment were 0 g/L salinity and water depth 1 cm above the soil surface. The five treatments, which were maintained for 1, 2, and 3 mo, were (1) 0 g/L salinity, (2) final salinity of 6 g/L reached in 3 wk, (3) final salinity of 6 g/L reached in 3 d, (4) final salinity of 12 g/L reached in 3 wk, and (5) final salinity of 12 g/L reached in 3 d. Treatments were applied to large (625 L) fiberglass tanks into which monoculture pots of the four species were randomly placed. Forty Fathoms Marine Mix (Marine Enterprises International, Inc., Baltimore, Maryland) was used as the salinity source, and water depth in all treatments was maintained 1 cm above the sediment surface. The split-plot design was blocked on the whole plot (treatment) with a randomized subplot (duration of exposure was 1, 2, or 3 mo). Two pots of each species were removed from each treatment at the end of each exposure duration. Growth responses of the immediately harvested pot of each pair removed were discussed in Howard and Mendelssohn (1999)
. The second pot was moved to a recovery tank with initial conditions (i.e., 0 g/L, 1 cm water depth). A drain hole in each pot was plugged before and during transfer and re-opened after transfer to the recovery tanks; this allowed a gradual exchange of interstitial pot water with the fresh tank water. The 0 g/L treatment plants were placed in separate recovery tanks to avoid exposure to leached salt. Plants were maintained in recovery conditions until harvest, 120 d (4 mo) after the experiment was initiated (i.e., time in recovery depended on duration of stress exposure).
Tank water salinity and depth were monitored daily and adjusted as necessary until conditions became stable; tanks were thereafter monitored every other day. Following transfer to recovery tanks, conditions were again monitored daily and tank water was replaced when salinity exceeded 1 g/L; during this replacement the pot drain holes were again plugged. We measured stem (or leaf, for Sagittaria lancifolia) density, total stem/leaf height, and mean stem/leaf height every 2 wk; any mortality, defined as complete death of aboveground tissue, was noted. Relative stem elongation was obtained at 4-wk intervals by measuring total height of a stem marked with a nontoxic silicone sealant and remeasuring the stem a few days later. This measure of relative growth rate (RGR) was calculated as (adapted from Hunt, 1990
):
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We harvested plants at the end of the experiment and divided the material into aboveground and belowground portions. Aboveground material was separated into live and dead. It was not possible to distinguish live from dead in the belowground material, so reported values for the belowground component include both. Plant tissue was dried at 75°C to a constant mass for biomass determination.
To assess ability to recover, three types of comparisons were used. The effect of salinity level on recovery was assessed by comparing growth in the 6 and 12 g/L salinity treatments to growth at 0 g/L. Influx rate effects were assessed by comparing the slow (3-wk) to fast (3-d) rate within a given salinity. The 2- and 3-mo exposures were compared to the 1-mo exposure duration, which was the least stressful, to determine the effect of increasing duration on ability to recover.
Statistical analyses
Data were analyzed separately by species. All analyses were performed by using SAS/STAT software (SAS, 1989). The initial model regarded treatment and duration as main effects. Dependent variables for a series of univariate analyses of variance (ANOVA) were total biomass, aboveground live biomass, belowground biomass, ratio of belowground to aboveground biomass, final (i.e., at time of harvest) stem/leaf density, final total stem/leaf height, and final mean stem/leaf height. Initial dry biomass (Howard and Mendelssohn, 1999
) was included as a covariate for total, aboveground, and belowground biomass analyses; initial measurements of stem density, total stem height, and mean stem height were used as covariates with their corresponding response measures. The interaction between treatment and covariate was tested, and analysis of covariance proceeded in cases of nonsignificance. The error term for treatment was block x treatment, and interactions between main effects were tested. A priori linear contrasts (Table 1) were used to determine effects of final salinity level, influx rate, and duration of exposure on recovery ability.
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; Potvin, Lechowicz, and Tardif, 1990
). The Huynh-Feldt corrected significance level was used in the univariate ANOVAR when the criterion of sphericity of orthogonal components could not be met (Potvin, Lechowicz, and Tardif, 1990
). For stem count and height data, the number of observations (three) was much less than the number of repeated measures (nine), generating insufficient degrees of freedom to test for sphericity in the univariate approach. Therefore, conservative significance values for generated F values were calculated by using Box's correction (Milliken and Johnson, 1984). Both ANOVA and ANOVAR models were assumed to be robust for the normality assumption since all model factors were fixed (Montgomery, 1991
). We transformed data when residual plots indicated failure to meet the assumption of variance homogeneity (transformations indicated in tables in the Results); a significance level of 0.05 was used for all tests. |
RESULTS |
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Salt concentration
Treatment, which was composed of final salt concentration and influx rate, had a significant effect on several plant response measures (Table 2). Total biomass recovery was generally prevented by increased salinity in all species except Scirpus, which appeared to be stimulated by 6 g/L salinity (Fig. 1). When a main effect interaction (treatment x duration) was absent, contrasts were used to quantify response to salinity level (Table 1, contrasts 1 and 2). Inability to recover biomass associated with increased salinity was found in Eleocharis (belowground), Panicum (total and belowground), and Sagittaria (aboveground). In contrast, Scirpus total biomass in the 6 g/L treatments exceeded that in the 0 g/L treatment, as did the ratio of belowground to total biomass (Fig. 2). Final (i.e., at harvest) stem characteristics of Eleocharis and Panicum (Fig. 3) also indicated failure to recover at increased salinity levels. Sagittaria was able to recover mean leaf height at both 6 and 12 g/L salinity, and Scirpus stem density and total height were higher at 6 g/L than at 0 g/L (Fig. 3).
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Duration of salinity exposure
All species failed to recover some aspects of biomass (Fig. 4) or stem characteristics (Fig. 5) with increased length of stress duration (analyses lacking interaction between main effects). These negative responses for Scirpus occurred primarily in the 3-mo duration rather than the 2-mo duration (as compared to 1-mo duration).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
The impact of increased salinity (averaged over influx rate and exposure duration) on ability to recover was most evident in Eleocharis and Panicum (Figs. 2, 3). For example, stem density of plants in salinity treatments compared to that of plants at 0 g/L was reduced by 44% at 6 g/L and 63% at 12 g/L in Eleocharis, and by 17% (6 g/L) and 67% (12 g/L) in Panicum. Sagittaria total biomass recovery was suppressed by increased salinity at exposure durations exceeding 1 mo (Fig. 1), and aboveground biomass of plants in the 12 g/L treatments was 59% that of plants in 0 g/L. Recovery potential of Sagittaria plants exposed to less stressful conditions is unclear considering the fact that this species began to senesce 6 wk into the experiment; recovery may have been more rapid or pronounced if the experiment had coincided with the active phase of growth. The resiliency of Sagittaria following short-term salinity exposure is consistent with the results of Grace and Ford's (1996)
field study; they found that aboveground biomass in this species was not affected by 7 d of exposure to 15 g/L salinity followed by an 8-mo recovery period under ambient field conditions. Scirpus growth was actually stimulated by 6 g/L in our study, and this species was able to fully recover following exposure to 12 g/L. The negative influence of rapid influx rate on recovery in Eleocharis, Panicum and Sagittaria was minor compared to the influence of final salinity level; influx rate had no effect on Scirpus recovery.
The significant interaction between main effects in the ANOVA was likely due to the fact that increased duration reflects increased age in plants growing at 0 g/L (i.e., the duration variable for these plants simply represents the time of transfer from one freshwater tank to another), while increased duration in the salinity treatments reflects extended stress exposure as well as age. In analyses with a significant interaction, plant growth at 0 g/L either increased or remained steady with increasing exposure duration (Fig. 6). Plants in other treatments, however, displayed complex responses that varied from steadily decreasing growth to initially decreasing and then increasing growth as exposure time increased (Fig. 6). Scirpus, growth of which was stimulated in the 6 g/L treatments (Fig. 2), is an exception to this generalization. Scirpus growth enhancement after short-term, moderate salinity stress in our experiment may be a species-specific fertilizer effect resulting from the constituents of the salinity source used. This enhancement was not evident under short-term salinity pulses that did not include a recovery period (Howard and Mendelssohn, 1999
). Scirpus response therefore differs from that of the brackish marsh species Kosteletzkya virginica, which increased growth over 60 d in a hydroponic solution with a moderate salinity increase to 85 mol/m3 NaCl (5 g/L) (Blits and Gallagher, 1990
).
Increased exposure duration (averaged over influx rate and salinity) suppressed ability to recover in all species (Figs. 4, 5). For Scirpus, it is likely that reduced growth with increased exposure duration does not reflect failure to recover, but rather an absence of the growth stimulation that occurred at <3 mo exposure to moderate (6 g/L) salinity. The reason for this species' relatively low biomass in the 0 g/L, 2-mo duration treatment (Fig. 1) is unknown, but it may have been affected by small sample size (N = 3).
General growth trends in the various treatments can be identified from graphs of response over time. By the conclusion of the experiment, Panicum plants subjected to salinity stress were able to attain total stem length similar to that of plants at 0 g/L (i.e., recover) after 1 mo of exposure to 6 g/L (both the fast and slow influx rates), and to 12 g/L (slow influx only) (Fig. 7). After 2 mo, however, plants in the 12 g/L treatments were unable to recover, and after 3 mo plants in both the 6 g/L and 12 g/L treatments failed to attain total stem height similar to that of the 0 g/L plants by harvest (Fig. 7). There were three pots in which plants produced new leaf tissue in recovery conditions after complete death of aboveground tissue at 12 g/L. Sagittaria, which was second to Panicum in mortality rate due to experimental conditions, exhibited a different pattern in the recovery of total leaf height over time. Stressed Sagittaria plants were able to attain height similar to the senescing unstressed (0 g/L) plants even after 3 mo, with the exception of the most extreme treatment (treatment 5) (Fig. 7). In contrast to Panicum, there were no instances of Sagittaria regrowth after total aboveground tissue mortality. The constant production of new leaves that survived only a short period, which was characteristic of Sagittaria under stress conditions, may have depleted belowground carbohydrate and/or nutrient reserves. New leaves, however, were formed in recovery conditions by surviving Sagittaria plants if even very little photosynthetic tissue was present at the time of transfer. For example, one plant in treatment 4 had just two leaves with a combined height of 7 cm remaining after 3 mo of salt exposure, but at harvest (after a 1-mo recovery period) had six leaves totaling 170 cm in height.
Despite complete survival of Eleocharis, this species responded somewhat similarly to Panicum in total height recovery when salinity stress was alleviated. After 2 mo of exposure, Eleocharis plants in the 6 g/L and 12 g/L treatments were unable to reach the total height of plants growing at 0 g/L (Figs. 5, 7); in comparison, Panicum plants exposed to 6 g/L salinity for 2 mo approached growth of plants at 0 g/L by the conclusion of the experiment (Fig. 7). Failure to recover after 3 mo was apparent for both species, but some regrowth did occur in Eleocharis while Panicum appeared to simply maintain tissue present at time of transfer to freshwater conditions.
Ability to recover may be related to different growth strategies for each species. Although all four species are perennial, Sagittaria has a very large rhizome that produces leaves rather than stems; this species reproduces by forming a new meristem. As long as the rhizome remains viable, new leaves can be rapidly produced when environmental conditions improve. Panicum has vigorous rhizome production and often forms nearly monospecific stands, but the rhizomes are slender and typically produce relatively few large stems. Apparently, Panicum growth can continue for some time under stressful conditions, but eventually belowground reserves are depleted and high tissue mortality results. In comparison, Eleocharis produces many relatively short, thin stems and reproduces by vigorous extension of slender rhizomes. It characteristically produces many new stems quickly in favorable conditions. Scirpus produces one stem from each node on extensively branching, rather robust rhizomes; stems produced are much larger than those formed by Eleocharis.
Effects on plant community dynamics
Species variation in the capacity for recovery after salinity pulses may alter marsh plant community composition, but such changes may be of only short duration. Chabreck and Palmisano (1973)
found that salinity in a freshwater marsh was increased from 0.9 g/L to 3.6 g/L after passage of Hurricane Camille. One year following the storm, however, salinity was similar to the prehurricane condition; vegetation cover, which had been reduced by the hurricane from a mean of 81.1 to 56.6%, had recovered to 75.2%. Panicum hemitomon, which composed just 1.3% of the vegetation cover before the hurricane, was absent 3 wk following the hurricane and remained absent 1 yr later (Chabreck and Palmisano, 1973
). Cover of Sagittaria falcata (synonymous with S. lancifolia; Kartesz, 1994
) and Eleocharis sp. increased slightly 3 wk after the storm, while S. americanus cover was unaffected. All three of these species, however, had slightly increased cover 1 yr after the hurricane (Chabreck and Palmisano, 1973
). These results are consistent with our finding that, while all four macrophyte species studied were capable of resuming growth following salinity pulses of relatively low intensity and/or duration, Panicum would be the first species to be eliminated when stress conditions exceed a certain (undefined) level.
The plant responses we found are also consistent with recovery of the freshwater marsh plant Justicia lanceolata, as observed by Llewellyn and Shaffer (1993)
. In their study, which was conducted over 1 mo, recovery was apparent following <72 h of exposure to 15 g/L salinity when freshwater flushing occurred. Recovery of J. lanceolata after longer exposure, however, was not addressed in their study. Some field studies have in fact found residual increased salinity in freshwater and oligohaline marshes several weeks to months after hurricanes (Alexander, 1967
; Meeder, 1987
; Jackson, Foote and Balistrieri, 1995
). Justicia lanceolata has a similar distribution to P. hemitomon in that it is most abundant at the freshwater extreme in coastal wetlands.
Field observations in other wetland habitats provide additional evidence of the ability of plants in such systems to recover from salinity perturbations. Following passage of Hurricane Andrew through the Gulf of Mexico in 1992, Guntenspergen et al. (1995)
noted that vegetation affected by increased salinity (i.e., salt burning) was able to recovery readily. Whigham, Jordan, and Miklas (1989)
found 2 yr of increased salinity in brackish marshes of Chesapeake Bay, Maryland, reduced biomass and density of Typha angustifolia, the dominant species, but these effects were reversed within 1 yr after return to normal salinity conditions. Coastal salt marsh plant species also respond to changes in hydrologic regimes that affect salinity; such changes, however, usually resulted in an alleviation of stress conditions. Zedler et al. (1986)
found growth enhancement of Spartina foliosa following freshwater inflow into hypersaline marshes was reversed with the return of hypersaline conditions. They suggested that both the duration and timing of the freshwater influence were critical in determining the nature of the growth response (i.e., height increase vs. density increase) in this species (Zedler et al., 1986
). Zedler (1983)
found vegetation in three southern California salt marshes to be resilient to freshwater flooding, but she suggested that artificially prolonged flooding caused shifts in species composition that may persist for long periods.
Our results suggest that the structure and composition of oligohaline marsh vegetation following pulses of increased salinity depend on the recovery ability, or resiliency, of various species, which in turn depend on the intensity and duration of the stress. This experiment, however, was conducted over a single growing season, and we therefore did not address recovery following a dormant period. Although more information is needed to ascertain whether any changes in composition will persist over time or whether the community will revert to a state closely resembling that preceding a salinity pulse event, this study was unique in demonstrating that salinity pulse factors can affect plant recovery.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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———, ———, and ———. 1987b Response of the freshwater marsh species, Panicum hemitomon Shult., to increased salinity. Freshwater Biology 17: 195–200.[CrossRef][ISI]
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  R. J. Howard and I. A. Mendelssohn Salinity as a constraint on growth of oligohaline marsh macrophytes. I. Species variation in stress tolerance Am. J. Botany, June 1, 1999; 86(6): 785 - 794. [Abstract] [Full Text] [PDF]
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