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Ecological implications of tolerance of salinity and inundation by Spartina maritima
Dot'any ELSEVIER
Aquatic Botany 52 (1995) 183-191
Ecological implications of tolerance of salinity and inundation by Spartina maritima J.B. Adams, G.C. Bate Department of Botany, Institutefor Coastal Research, Universityof Port Elizabeth, P.O. Box 1600, Port Elizabeth, 6000, South Africa Accepted 22 June 1995
Abstract Laboratory studies of Spartina maritima Curtis (Fernald) showed that stem and leaf elongation did not differ significantly for completely submerged or tidally inundated plants. Growth was reduced for dry treatments and at salinity levels greater than 35 ppt. S. maritima is absent from periodically closed South African estuaries which may be attributed to the requirement for tidal flooding and saturated substrates. Where S. maritima occurs in estuaries, it is important that freshwater should be discharged in such a manner as to maintain an open mouth in order to achieve the essential tidal flushing. Keywords: Salinity; Estuary; Salt marsh; Inundation; Spartina maritiraa
1. Introduction Spartina maritima (Curtis) Fernald (cord grass) forms extensive monotypic stands in estuaries along the south coast o f South Africa. In permanently open estuaries where there is adequate tidal exchange intertidal salt marshes are well-zoned. The seagrass Zostera capensis Setchell occurs at the low water mark, followed by S. maritima. Above the S. maritima zone, Sarcocornia perennis (Mill.) Scott occurs, which is replaced at higher levels by Triglochin spp., Limonium scabrum (Thunb.) Kuntze and Chenolea diffusa Thunb. According to Pierce (1982) Spartina maritima may be an exotic which increases sediment stability in estuaries. It was considered to be encroaching into the Z. capensis zone. Whether or not S. maritima is an exotic, it has become an important primary producer in a number of South African estuaries. Autochtonous carbon supplied by marsh plants such as S. maritima is very important during periods of low freshwater inflow (Taylor, 1987). The 0304-3770/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSD10304-3770(95 )00496-3
184
J.B. Adams, G.C. Bate~Aquatic Botany 52 (1995) 183-191
marsh area also forms an extensive habitat for typical estuarine faunal species e.g. the marsh crab, Sesarma catenata Ort. Past work in South Africa on estuarine macrophytes has mainly been on ecologically descriptive studies. A few have documented ecophysiological tolerances (Breen et al., 1977; Naidoo and Rughunanan, 1990; Naidoo and Naidoo, 1992; Naidoo and Naicker, 1992). However, these studies considered plant tolerances only over a narrow salinity range. Our surveys of east Cape estuaries have shown that during drought conditions salinity can rise to above the normal 35 ppt. of seawater. In many estuaries, evaporation causes the upper estuarine reaches to become more saline than the mouth region. It is possible that hypersaline conditions in estuaries will increase due to the growing need for dams to supply urban and agricultural freshwater. Therefore, this study aimed to document the effect of a wide range of salinity ( 0 - 7 5 ppt.) on the growth of S. maritima. Besides the salinity studies, the response of S. maritima to three inundation treatments was also tested. The first treatment simulated dry conditions with a simultaneous increase in salinity. This is a real situation in South African estuaries as mouth dimensions are shrinking due to reduced freshwater inflow. Dams in estuarine catchment areas reduce the frequency and magnitude of floods (Whitfield and Bruton, 1989) leading to less effective scour of marine sediment accumulation in tidal inlets (Reddering, 1988). The estuary tidal prism is reduced, thus reducing both tidal exchange and flushing of marshes. The second inundation treatment simulated diurnal tidal fluctuations, while the third treatment was stagnant with completely submerged conditions.
2. Materials and methods
Plants were collected in the Swartkops estuary (33°5 I'S 25°37'E) from stands that were uniform in size and density of stems (Kirkman and Sharitz, 1993). The salinity prevailing at the time of collection was 32 ppt. The plants were collected with an associated 25 x 30 cm soil column and transferred to pots of similar dimensions and kept inside a glasshouse. Temperatures in the glasshouse ranged between 18-38°C, The plants were allowed an acclimation period ( 1 week prior to the initiation of the experiment). They were initially watered with 32 ppt. and over the one week period salinity was incrementally reduced or increased to obtain the treatment salinity. Hypersaline media were obtained by adding coarse sea salts (National Ingredients, Port Elizabeth) to filtered seawater. Hyposaline media were obtained by diluting filtered seawater with distilled water. A 5x3 factorial experiment was established, with five salinity (0, 15, 35, 55 and 75 ppt.) and three inundation treatments (I1, 12 and I3). For the I1 treatment, plant pots were placed in plastic trays and watered three times a week with the relevant salinity. This simulated dry marsh conditions. In the 12 treatment, plant pots were placed in larger containers. Pumps and timers were set up so that the plants were subjected to a tidal regime with 6 h between high and low tides (Fig. 1). Completely submerged conditions (13) were achieved by placing the plant pots in larger containers and maintaining the water level at 60 cm above the sediment surface. Small stones were placed on the surface of the pots to minimize algal growth. The nutrient contained in the initial soil-root cores was the only nutrient source available. These condi-
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
185
Tank with plants
inlet pipe
pump Holding tank Fig. 1. The tank design for the 12, tidal S. maritima treatment. The pump filled the plant tank with water, so that the plants were inundated. Water then drained slowlythrough the outlet pipe into the holdingtank over a 6 h period. tions simulate the natural marsh environment, i.e. low nutrient concentrations and natural marsh substrate. Four replicate pots were used for each treatment and in each pot five plants were monitored. The experiment began in August (late winter) and the plants were harvested after three months. Growth rate was monitored by measuring stem and leaf elongation and stem density at weekly intervals. Every second week a sediment sample was collected from each pot for salinity determination as described by Adams and Bate (1994). Plant pots were placed in containers with freshwater after the three month treatment. Recovery of the plants was assessed by measuring plant height and the percentage of alive and dead above-ground material at weekly intervals for 6 weeks. Plants in the dry, 15 and 35 ppt, treatments were the only ones that showed any signs of recovery after six weeks in freshwater. The percentage alive above-ground material increased for these plants as new green leaves were produced. The 55 and 75 ppt. plants showed no signs of recovery. Approximately 50% of the above-ground material was necrotic and dead at the end of the three month saline treatment. Data were subjected to analyses of variance using the SOLO statistical package (BMDP Statistical Software, 1988).
186
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
3. Results Both salinity ( F = 8 . 1 0 , P<0.005, d . f . = 4 ) and inundation ( F = 6 . 9 9 , P<0.005, d.f. = 2) had a significant effect on stem elongation (Fig. 2). However a two-way ANOVA showed that there was no significant interaction between salinity and the inundation treatment ( F = 1.02, P > 0.05, d.f. = 8 ) . Stem elongation was significantly reduced by the dry treatment (I1), at all salinity levels, compared with the tidal (I2) and submerged treatments (13). Plants grew equally well whether submitted to tidal or completely submerged conditions. Stem elongation was greatest for the 0 and 15 ppt. submerged treatments and was reduced at 55 and 75 ppt. for all inundation treatments (Fig. 2). After 3 weeks there were signs of salinity stress, i.e. leaves were rolled and necrotic. Stem production for the submerged (13) treatment was significantly lower than for the dry and tidal treatments ( F = 8.99, P < 0.001, d.f. = 2). The number of stems produced per week remained fairly constant for the dry and tidal treatment between 0 and 35 ppt. (Fig. 3). Stem production was reduced at 55 and 75 ppt. Leaf elongation was greatest at 15 and 35 ppt. for the dry treatment (Fig. 4). Leaf elongation was significantly faster for the dry treatment compared with the tidal and submerged treatment ( F = 7.67, P < 0.01, d.f. = 2). Sediment salinity increased in accordance with treatment salinity (Fig. 5). At 0, 15 and 35 ppt., sediment salinity for the dry treatment was higher than for the tidal and submerged 5'
-~ 4 0~ E o z
_o
3
(5 z 2 0,,--I LU LLI l-- 1
0
15
35
55
75
SALINITY (ppt.) II
II11
12II3
I
Fig. 2. The effect of salinity and inundation on the rate of S. maritima stemelongation in the glasshousefor a 3month period. (Bars representstandarderror,n = 20.) Treatments:I1, occasionallywatered;I2, tidallyinundated; 13, submerged.
J.B. Adams, G.C. Bate~Aquatic Botany 52 (1995) 183-191
187
2w LM or" LU 12. 0 W 0
1.5
a 0 nel 6o ILl I-6O ii 0 er" W rn
0.5
Z
0"--
0
15
35
55
75
SALINITY (ppt.)
]~
I1 ~
121~1 13 ]
Fig. 3. The number of stems produced per week by S. maritima at five salinity levels and three inundation treatments. (Bars represent standard error, n = 20. )
5
-~ E E
v
i
4-
3"
z
0
(.9
Z 2
T
O .-I
W LL
< Lu 1,..I
0---
0
15 35 55 SALINITY (ppt.) ["---111
~12~13
75
]
Fig. 4. Spartina maritima rate of leaf elongation during 3 months growth at five salinity levels and three inundation treatments. ( Bars represent standard error, n = 20.)
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
188
1412 10v
8" < CO I-Z
6-
III
N W
4 20
1 0
I
15 35 55 SALINITY (ppt.)
II1 I
12 ~
75
13
Fig. 5. Sediment salinity of S. maritima pots treated with five salinity levels and three inundation treatments over a 3-month period. ( Bars represent standard error, n = 4. )
treatments. There was no significant difference between the sediment salinity values for the tidal and submerged treatments ( F = 0.22, P > 0.05, d.f. = 1 ). Plants in the dry, 15 and 35 ppt. treatments were the only ones that showed any signs of recovery after 6 weeks in freshwater. The percentage alive above-ground material increased for these plants as new green leaves were produced. The 55 and 75 ppt. plants showed no signs of recovery. Approximately 50% of the above-ground material was necrotic and dead at the end of the 3-month saline treatment.
4. Discussion Stem elongation, leaf elongation and stem production responded differently to the three inundation treatments. Stem elongation was reduced in the dry treatment, stem production was reduced in the submerged treatment and leaf elongation was greatest in the dry treatment. All three measured parameters responded similarly to salinity, i.e.S, maritima grew equally well at salinity between 0 and 35 ppt. but growth was reduced at 55 and 75 ppt. Plants showed typical signs of stress after 3 weeks, i.e. leaves were tightly rolled and twisted, with the outer leaves showing signs of chlorosis. Spartina alterniflora Loisel. appears to have a similar salinity tolerance range to that of S. maritima. The optimum growth salinity of S. alterniflora has been estimated between 0--20 ppt. (Haines and Dunn, 1976; Linthurst and Seneca, 1980). Woodhouse et al. ( 1974; in Linthurst and Seneca, 1981) found that salinity concentrations greater than 45 ppt. caused die-back.
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
189
The rate of S. maritima stem elongation was greatest for the completely submerged plants treated at 0 ppt. Some other species are stimulated to elongate their stems under submerged conditions (Jackson and Drew, 1984). Adams and Bate (1994) reported this for the succulent estuarine plant Sarcocornia perennis. This 'depth accommodation' permits wetland plants to emerge quickly so that leaves can function in gas phase exchanges (Kirkman and Sharitz, 1993). The rates of leaf and stem elongation for S. maritima did not differ significantly between tidal or completely submerged plants. Spartina spp. can survive periodic tidal submergence for longer periods than other plants and therefore occupy the lower elevation of salt marshes. This ability to withstand tidal inundation for longer periods than other halophytes enables it to colonize barren intertidal areas (Redfield, 1972; Gammill and Hosier, 1992). The dry treatment inhibited growth of S. maritima, suggesting its requirement for waterlogged conditions. S. alterniflora thrives in waterlogged anoxic low marsh habitats due to its ability to oxygenate its roots and rhizophere (Teal and Kanwisher, 1966; Howes et al., 1981; Bertness, 1991; Naidoo et al., 1992), the same may apply for S. maritima. The plants possess extensive aerenchyma, which includes internal gas spaces that extend from the leaves to the root tips (Teal and Kanwisher, 1966). Oxygen is transferred to the root zone from the photosynthetic portion of the plant, especially aerial leaves (Bertness, 1991). In order to cope with the waterlogged anoxic environment it is important that the aerial parts of the plant are not completely submerged. In South African estuaries S. maritima is not found in periodically closed estuaries, as in such systems the intertidal zone is not well defined. Other plants adapted to drier conditions possibly outcompete Spartina. Spartina alterniflora occurs in the same low salt marsh zone as S. maritima. Bertness ( 199l ) used transplant experiments and found that S. alterniflora was competitively excluded from the high dry marsh habitat. Weekly stem production was low, and did not exceed two stems per week for any treatment. According to Pierce (1983) growth of S. maritima is aseasonal (continuous) but very slow. In the Swartkops estuary 1 year after clipping there were no signs of any regrowth (Pierce 1983). Lubke and Curtis (1977; in Pierce, 1983) found that the mean number of shoots produced 9 months after transplant varied from two to a maximum of 14 shoots. The production of new stems was significantly reduced for the completely submerged treatments compared with the tidal and dry treatments. Anoxic sediment conditions may inhibit stem production or more energy may be allocated into stem elongation under completely submerged conditions. A large allocation to stem elongation is probably necessary to keep the leaves above the water level (Pearcy and Ustin, 1984). Mendelssohn and Seneca (1980) found that under stagnant, standing water conditions, growth of S. alterniflora was inhibited. Their experiment monitored growth over 5 months. The combined effects of sea-level rise and subsidence tend to increase plant submergence, which often leads to plant death and open waterbodies (Mendelssohn and McKee, 1988). In this study, 3 months of submergence did not affect stem elongation in S. maritima. Plants were covered with 60 cm of water and approximately 25% of the aerial parts remained above water. This closely simulated in situ high tide conditions. The diffusion of atmospheric oxygen to the roots via the stem was, therefore, not completely blocked (Mendelssohn and Seneca, 1980).
190
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
Leaves grew faster in the dry treatment compared with the tidal and submerged treatments. Leaf growth in all plants is extremely sensitive to flooding and possible root anoxia. Leaf expansion can slow within 20--40 min of submergence (Jackson and Drew, 1984). The dominant factors that control salinity of salt marsh soils are evaporation, duration of tidal flooding, frequency and amount of rainfall and the salinity of tidal waters (Mahall and Park, 1976). In southern California salt marshes, heavy rainfall caused flooding of the marshes, and a 40% increase in the biomass of Spartinafoliosa Trin. (Zedler, 1983) was recorded. In the Kromme estuary (South Africa) high water column salinity (35 ppt.) due to freshwater impoundment has resulted in salt accumulation in the intertidal marshes and reduced macrophyte distribution and growth (Adams et al., 1992). It is important that freshwater input into estuaries is managed. This study and others (Clarke and Hannon, 1970; Breen et al., 1977; Adams and Bate, 1994) have shown that the growth of most salt marsh plants is reduced at salinities greater than 35 ppt. Daily tidal flushing is important because stem elongation of Spartina maritima was reduced when plants were exposed to dry conditions. Reduced freshwater input can cause marine sediments to accumulate in the estuary mouth, shrinking the mouth dimensions (Reddering, 1988) and reducing tidal flushing of the marshes. If the mouth of an estuary closes due to reduced freshwater input there is the possibility that S. maritima communities may disappear. Spartina maritima is absent from periodically closed South African estuaries which may be attributed to the plant' s requirement for tidal flooding and saturated substrates. It is recommended that in permanently open estuaries, freshwater should be discharged in such a manner as to maintain an open mouth. This state is required to achieve the tidal flushing essential for intertidal salt marsh environments. Tidal exchange is also important in maintaining salt marsh zonation patterns.
Acknowledgements The Water Research Commission is thanked for funding this project. The Foundation for Research and Development provided a bursary for the first author. Mr M. Van der Merwe and Mr M. Brassil are thanked for technical assistance.
References Adams,J.B., Knoop,W.T.and Bate,G.C., 1992.Thedistributionofestuarinemacrophytesin relationto freshwater. Bot. Mar., 35: 215-226. Adams,J.B. and Bate, G.C., 1994. The effectof salinity and inundation on the estnarinemacrophyteSarcocornia perennis (Mill.) A. J. Scott. Aquat. Bot.,47: 341-348. Bertness,M.D., 1991.Zonationof Spartinapatens and Spartina alterniflorain a NewEnglandsalt marsh.Ecology, 72: 138-148. BMDP Statistical Software, 1988. Los Angeles,CA. Breen, C.M., Everson,E.C. and Rogers,K., 1977. Ecological studies on Sporobolus virginicus (L.) Kunth with particular referenceto salinity and inundation. Hydrobiologia,54: 135-140. Clarke, L.D. and Hannon, N.J., 1970. The mangroveswampsand salt marshcommunitiesof the SydneyDistrict. 3. Plant growth in relation to salinity and waterlogging.J. Ecol., 58:351-369.
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Gammill, S.P. and Hosier, P.E., 1992. Coastal saltmarsh development at Southern Topsail Sound, North Carolina. Estuaries, 15: 122-129. Haines, B.L. and Dunn, E.L., 1976. Growth and resource allocation responses of Spartina alterniflora and Juncus roemerianus plant stands in a Georgia salt marsh. Ecology, 61: 303-312. Howes, B.L,, Howarth, R.W., Teal, J.M. and Valiela, I., 1981. Oxidation-reduction potentials in a salt marsh: Spatial patterns and interactions with primary production. Limnol. Oceanogr., 26: 350-360. Jackson, M.D. and Drew, M.C., 1984. Effects of flooding on herbaceous plants. In: T.T. Kozlowski (Editor), Flooding and Plant Growth. Academic Press, New York, pp. 47-128. Kirkman, L.K. and Sharitz, R.R., 1993. Growth in controlled water regimes of three grasses common in freshwater wetlands of the southeastern U.S.A. Aquat. Bot,, 44: 345-359. Linthurst, R.A. and Seneca, E.D., 1980. The effects of standing water and drainage potential on the Spartina alterniflora substrate complex in a North Carolina salt marsh. Estuar. Coast. Mar. Sci., 11: 41-52. Linthurst, R.A. and Seneca, E.D., 1981. Aeration, nitrogen and salinity as determinants of Spartina alterniflora Loisel. growth response. Estuaries, 4: 53~53. Mahall, B.E. and Park, R.B., 1976. The ecotone between Spartinafoliosa Trin. and Salicornia cirginica L. in salt marshes of Northern San Francisco Bay. II Soil water and salinity. J. Ecol., 64: 793-809. Mendelssohn, I.A. and McKee, K.L., 1988. Spartina alterniflora die-back in Louisiana: Time-course investigation of soil waterlogging effects. J. Ecol., 76:509-521. Mendelssohn, I.A. and Seneca, E.D,, 1980. The influence of soil drainage on the growth of salt marsh cordgrass Spartina alterniflora in North Carolina. Estuar. Coast. Mar. Sci., 11: 27-40. Naidoo, G. and Rughunanan, R., 1990. Salt tolerance in succulent, coastal halophyte, Sarcocornia natalensis. J. Exp. Bot., 41 : 497-502. Naidoo, G. and Naicker, K., 1992. Seed germination in the coastal halophytes Triglochin bulbosa and Triglochin striata. Aquat. Bot., 42: 217-229. Naidoo, G. and Naidoo, S., 1992. Waterlogging response of Sporobolus virginicus (L.) Kunth. Oecologia, 90: 445-450. Naidoo, G., McKee, K.L. and Mendelssohn, I.A., 1992. Anatomical and metabolic responses to waterlogging and salinity in Spartina alterniflora and S. patens (Poaceae). Am. J. Bot., 79: 765-770. Pearcy, R.W. and Ustin, S.L., 1984. Effects of salinity on growth and photosynthesis of three California tidal marsh species. Oecologia, 62: 68-73. Pierce, S.M., 1982. What is Spartina doing in our estuaries? S. Afr. J. Sci., 78: 229-230. Pierce, SM., 1983. Estimation of the non-seasonal production of Spartina maritima (Curtis) Fernald in a South African estuary. Est. Coast. Shelf Sci., 16: 241-254. Reddering, J.S.V., 1988. Prediction of the effects of reduced river discharge on the estuaries of the south-eastern Cape Province, South Africa. S. Afr. J. Sci., 84: 726-730. Redfield, A.C., 1972, Development of a New England salt marsh. Ecol. Monogr., 42: 201-237. Taylor, D.I., 1987. Tidally-mediated carbon, nitrogen and phosphorus exchange between a salt marsh and the Kariega estuary and the role of salt marsh Brachyura in the transfer. PhD thesis. Rhodes University, Grahamstown. Teal, J.M. and Kanwisher, J.W., 1966. Gas transport in the marsh grass, Spartina alterniflora. J. Exp. Bot., 17: 355-361. Whitfield, A.K. and Bruton, M.N., 1989. Some biological implications of reduced fresh water inflow into eastern Cape estuaries: a preliminary assessment. S. Afr. J. Sci., 85: 691-694. Zedler, J.B.. 1983. Freshwater impacts in normally hypersaline marshes. Estuaries, 6: 346-355.
Aquatic Botany 52 (1995) 183-191
Ecological implications of tolerance of salinity and inundation by Spartina maritima J.B. Adams, G.C. Bate Department of Botany, Institutefor Coastal Research, Universityof Port Elizabeth, P.O. Box 1600, Port Elizabeth, 6000, South Africa Accepted 22 June 1995
Abstract Laboratory studies of Spartina maritima Curtis (Fernald) showed that stem and leaf elongation did not differ significantly for completely submerged or tidally inundated plants. Growth was reduced for dry treatments and at salinity levels greater than 35 ppt. S. maritima is absent from periodically closed South African estuaries which may be attributed to the requirement for tidal flooding and saturated substrates. Where S. maritima occurs in estuaries, it is important that freshwater should be discharged in such a manner as to maintain an open mouth in order to achieve the essential tidal flushing. Keywords: Salinity; Estuary; Salt marsh; Inundation; Spartina maritiraa
1. Introduction Spartina maritima (Curtis) Fernald (cord grass) forms extensive monotypic stands in estuaries along the south coast o f South Africa. In permanently open estuaries where there is adequate tidal exchange intertidal salt marshes are well-zoned. The seagrass Zostera capensis Setchell occurs at the low water mark, followed by S. maritima. Above the S. maritima zone, Sarcocornia perennis (Mill.) Scott occurs, which is replaced at higher levels by Triglochin spp., Limonium scabrum (Thunb.) Kuntze and Chenolea diffusa Thunb. According to Pierce (1982) Spartina maritima may be an exotic which increases sediment stability in estuaries. It was considered to be encroaching into the Z. capensis zone. Whether or not S. maritima is an exotic, it has become an important primary producer in a number of South African estuaries. Autochtonous carbon supplied by marsh plants such as S. maritima is very important during periods of low freshwater inflow (Taylor, 1987). The 0304-3770/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSD10304-3770(95 )00496-3
184
J.B. Adams, G.C. Bate~Aquatic Botany 52 (1995) 183-191
marsh area also forms an extensive habitat for typical estuarine faunal species e.g. the marsh crab, Sesarma catenata Ort. Past work in South Africa on estuarine macrophytes has mainly been on ecologically descriptive studies. A few have documented ecophysiological tolerances (Breen et al., 1977; Naidoo and Rughunanan, 1990; Naidoo and Naidoo, 1992; Naidoo and Naicker, 1992). However, these studies considered plant tolerances only over a narrow salinity range. Our surveys of east Cape estuaries have shown that during drought conditions salinity can rise to above the normal 35 ppt. of seawater. In many estuaries, evaporation causes the upper estuarine reaches to become more saline than the mouth region. It is possible that hypersaline conditions in estuaries will increase due to the growing need for dams to supply urban and agricultural freshwater. Therefore, this study aimed to document the effect of a wide range of salinity ( 0 - 7 5 ppt.) on the growth of S. maritima. Besides the salinity studies, the response of S. maritima to three inundation treatments was also tested. The first treatment simulated dry conditions with a simultaneous increase in salinity. This is a real situation in South African estuaries as mouth dimensions are shrinking due to reduced freshwater inflow. Dams in estuarine catchment areas reduce the frequency and magnitude of floods (Whitfield and Bruton, 1989) leading to less effective scour of marine sediment accumulation in tidal inlets (Reddering, 1988). The estuary tidal prism is reduced, thus reducing both tidal exchange and flushing of marshes. The second inundation treatment simulated diurnal tidal fluctuations, while the third treatment was stagnant with completely submerged conditions.
2. Materials and methods
Plants were collected in the Swartkops estuary (33°5 I'S 25°37'E) from stands that were uniform in size and density of stems (Kirkman and Sharitz, 1993). The salinity prevailing at the time of collection was 32 ppt. The plants were collected with an associated 25 x 30 cm soil column and transferred to pots of similar dimensions and kept inside a glasshouse. Temperatures in the glasshouse ranged between 18-38°C, The plants were allowed an acclimation period ( 1 week prior to the initiation of the experiment). They were initially watered with 32 ppt. and over the one week period salinity was incrementally reduced or increased to obtain the treatment salinity. Hypersaline media were obtained by adding coarse sea salts (National Ingredients, Port Elizabeth) to filtered seawater. Hyposaline media were obtained by diluting filtered seawater with distilled water. A 5x3 factorial experiment was established, with five salinity (0, 15, 35, 55 and 75 ppt.) and three inundation treatments (I1, 12 and I3). For the I1 treatment, plant pots were placed in plastic trays and watered three times a week with the relevant salinity. This simulated dry marsh conditions. In the 12 treatment, plant pots were placed in larger containers. Pumps and timers were set up so that the plants were subjected to a tidal regime with 6 h between high and low tides (Fig. 1). Completely submerged conditions (13) were achieved by placing the plant pots in larger containers and maintaining the water level at 60 cm above the sediment surface. Small stones were placed on the surface of the pots to minimize algal growth. The nutrient contained in the initial soil-root cores was the only nutrient source available. These condi-
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
185
Tank with plants
inlet pipe
pump Holding tank Fig. 1. The tank design for the 12, tidal S. maritima treatment. The pump filled the plant tank with water, so that the plants were inundated. Water then drained slowlythrough the outlet pipe into the holdingtank over a 6 h period. tions simulate the natural marsh environment, i.e. low nutrient concentrations and natural marsh substrate. Four replicate pots were used for each treatment and in each pot five plants were monitored. The experiment began in August (late winter) and the plants were harvested after three months. Growth rate was monitored by measuring stem and leaf elongation and stem density at weekly intervals. Every second week a sediment sample was collected from each pot for salinity determination as described by Adams and Bate (1994). Plant pots were placed in containers with freshwater after the three month treatment. Recovery of the plants was assessed by measuring plant height and the percentage of alive and dead above-ground material at weekly intervals for 6 weeks. Plants in the dry, 15 and 35 ppt, treatments were the only ones that showed any signs of recovery after six weeks in freshwater. The percentage alive above-ground material increased for these plants as new green leaves were produced. The 55 and 75 ppt. plants showed no signs of recovery. Approximately 50% of the above-ground material was necrotic and dead at the end of the three month saline treatment. Data were subjected to analyses of variance using the SOLO statistical package (BMDP Statistical Software, 1988).
186
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
3. Results Both salinity ( F = 8 . 1 0 , P<0.005, d . f . = 4 ) and inundation ( F = 6 . 9 9 , P<0.005, d.f. = 2) had a significant effect on stem elongation (Fig. 2). However a two-way ANOVA showed that there was no significant interaction between salinity and the inundation treatment ( F = 1.02, P > 0.05, d.f. = 8 ) . Stem elongation was significantly reduced by the dry treatment (I1), at all salinity levels, compared with the tidal (I2) and submerged treatments (13). Plants grew equally well whether submitted to tidal or completely submerged conditions. Stem elongation was greatest for the 0 and 15 ppt. submerged treatments and was reduced at 55 and 75 ppt. for all inundation treatments (Fig. 2). After 3 weeks there were signs of salinity stress, i.e. leaves were rolled and necrotic. Stem production for the submerged (13) treatment was significantly lower than for the dry and tidal treatments ( F = 8.99, P < 0.001, d.f. = 2). The number of stems produced per week remained fairly constant for the dry and tidal treatment between 0 and 35 ppt. (Fig. 3). Stem production was reduced at 55 and 75 ppt. Leaf elongation was greatest at 15 and 35 ppt. for the dry treatment (Fig. 4). Leaf elongation was significantly faster for the dry treatment compared with the tidal and submerged treatment ( F = 7.67, P < 0.01, d.f. = 2). Sediment salinity increased in accordance with treatment salinity (Fig. 5). At 0, 15 and 35 ppt., sediment salinity for the dry treatment was higher than for the tidal and submerged 5'
-~ 4 0~ E o z
_o
3
(5 z 2 0,,--I LU LLI l-- 1
0
15
35
55
75
SALINITY (ppt.) II
II11
12II3
I
Fig. 2. The effect of salinity and inundation on the rate of S. maritima stemelongation in the glasshousefor a 3month period. (Bars representstandarderror,n = 20.) Treatments:I1, occasionallywatered;I2, tidallyinundated; 13, submerged.
J.B. Adams, G.C. Bate~Aquatic Botany 52 (1995) 183-191
187
2w LM or" LU 12. 0 W 0
1.5
a 0 nel 6o ILl I-6O ii 0 er" W rn
0.5
Z
0"--
0
15
35
55
75
SALINITY (ppt.)
]~
I1 ~
121~1 13 ]
Fig. 3. The number of stems produced per week by S. maritima at five salinity levels and three inundation treatments. (Bars represent standard error, n = 20. )
5
-~ E E
v
i
4-
3"
z
0
(.9
Z 2
T
O .-I
W LL
< Lu 1,..I
0---
0
15 35 55 SALINITY (ppt.) ["---111
~12~13
75
]
Fig. 4. Spartina maritima rate of leaf elongation during 3 months growth at five salinity levels and three inundation treatments. ( Bars represent standard error, n = 20.)
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
188
1412 10v
8" < CO I-Z
6-
III
N W
4 20
1 0
I
15 35 55 SALINITY (ppt.)
II1 I
12 ~
75
13
Fig. 5. Sediment salinity of S. maritima pots treated with five salinity levels and three inundation treatments over a 3-month period. ( Bars represent standard error, n = 4. )
treatments. There was no significant difference between the sediment salinity values for the tidal and submerged treatments ( F = 0.22, P > 0.05, d.f. = 1 ). Plants in the dry, 15 and 35 ppt. treatments were the only ones that showed any signs of recovery after 6 weeks in freshwater. The percentage alive above-ground material increased for these plants as new green leaves were produced. The 55 and 75 ppt. plants showed no signs of recovery. Approximately 50% of the above-ground material was necrotic and dead at the end of the 3-month saline treatment.
4. Discussion Stem elongation, leaf elongation and stem production responded differently to the three inundation treatments. Stem elongation was reduced in the dry treatment, stem production was reduced in the submerged treatment and leaf elongation was greatest in the dry treatment. All three measured parameters responded similarly to salinity, i.e.S, maritima grew equally well at salinity between 0 and 35 ppt. but growth was reduced at 55 and 75 ppt. Plants showed typical signs of stress after 3 weeks, i.e. leaves were tightly rolled and twisted, with the outer leaves showing signs of chlorosis. Spartina alterniflora Loisel. appears to have a similar salinity tolerance range to that of S. maritima. The optimum growth salinity of S. alterniflora has been estimated between 0--20 ppt. (Haines and Dunn, 1976; Linthurst and Seneca, 1980). Woodhouse et al. ( 1974; in Linthurst and Seneca, 1981) found that salinity concentrations greater than 45 ppt. caused die-back.
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
189
The rate of S. maritima stem elongation was greatest for the completely submerged plants treated at 0 ppt. Some other species are stimulated to elongate their stems under submerged conditions (Jackson and Drew, 1984). Adams and Bate (1994) reported this for the succulent estuarine plant Sarcocornia perennis. This 'depth accommodation' permits wetland plants to emerge quickly so that leaves can function in gas phase exchanges (Kirkman and Sharitz, 1993). The rates of leaf and stem elongation for S. maritima did not differ significantly between tidal or completely submerged plants. Spartina spp. can survive periodic tidal submergence for longer periods than other plants and therefore occupy the lower elevation of salt marshes. This ability to withstand tidal inundation for longer periods than other halophytes enables it to colonize barren intertidal areas (Redfield, 1972; Gammill and Hosier, 1992). The dry treatment inhibited growth of S. maritima, suggesting its requirement for waterlogged conditions. S. alterniflora thrives in waterlogged anoxic low marsh habitats due to its ability to oxygenate its roots and rhizophere (Teal and Kanwisher, 1966; Howes et al., 1981; Bertness, 1991; Naidoo et al., 1992), the same may apply for S. maritima. The plants possess extensive aerenchyma, which includes internal gas spaces that extend from the leaves to the root tips (Teal and Kanwisher, 1966). Oxygen is transferred to the root zone from the photosynthetic portion of the plant, especially aerial leaves (Bertness, 1991). In order to cope with the waterlogged anoxic environment it is important that the aerial parts of the plant are not completely submerged. In South African estuaries S. maritima is not found in periodically closed estuaries, as in such systems the intertidal zone is not well defined. Other plants adapted to drier conditions possibly outcompete Spartina. Spartina alterniflora occurs in the same low salt marsh zone as S. maritima. Bertness ( 199l ) used transplant experiments and found that S. alterniflora was competitively excluded from the high dry marsh habitat. Weekly stem production was low, and did not exceed two stems per week for any treatment. According to Pierce (1983) growth of S. maritima is aseasonal (continuous) but very slow. In the Swartkops estuary 1 year after clipping there were no signs of any regrowth (Pierce 1983). Lubke and Curtis (1977; in Pierce, 1983) found that the mean number of shoots produced 9 months after transplant varied from two to a maximum of 14 shoots. The production of new stems was significantly reduced for the completely submerged treatments compared with the tidal and dry treatments. Anoxic sediment conditions may inhibit stem production or more energy may be allocated into stem elongation under completely submerged conditions. A large allocation to stem elongation is probably necessary to keep the leaves above the water level (Pearcy and Ustin, 1984). Mendelssohn and Seneca (1980) found that under stagnant, standing water conditions, growth of S. alterniflora was inhibited. Their experiment monitored growth over 5 months. The combined effects of sea-level rise and subsidence tend to increase plant submergence, which often leads to plant death and open waterbodies (Mendelssohn and McKee, 1988). In this study, 3 months of submergence did not affect stem elongation in S. maritima. Plants were covered with 60 cm of water and approximately 25% of the aerial parts remained above water. This closely simulated in situ high tide conditions. The diffusion of atmospheric oxygen to the roots via the stem was, therefore, not completely blocked (Mendelssohn and Seneca, 1980).
190
J.B. Adams, G.C. Bate/Aquatic Botany 52 (1995) 183-191
Leaves grew faster in the dry treatment compared with the tidal and submerged treatments. Leaf growth in all plants is extremely sensitive to flooding and possible root anoxia. Leaf expansion can slow within 20--40 min of submergence (Jackson and Drew, 1984). The dominant factors that control salinity of salt marsh soils are evaporation, duration of tidal flooding, frequency and amount of rainfall and the salinity of tidal waters (Mahall and Park, 1976). In southern California salt marshes, heavy rainfall caused flooding of the marshes, and a 40% increase in the biomass of Spartinafoliosa Trin. (Zedler, 1983) was recorded. In the Kromme estuary (South Africa) high water column salinity (35 ppt.) due to freshwater impoundment has resulted in salt accumulation in the intertidal marshes and reduced macrophyte distribution and growth (Adams et al., 1992). It is important that freshwater input into estuaries is managed. This study and others (Clarke and Hannon, 1970; Breen et al., 1977; Adams and Bate, 1994) have shown that the growth of most salt marsh plants is reduced at salinities greater than 35 ppt. Daily tidal flushing is important because stem elongation of Spartina maritima was reduced when plants were exposed to dry conditions. Reduced freshwater input can cause marine sediments to accumulate in the estuary mouth, shrinking the mouth dimensions (Reddering, 1988) and reducing tidal flushing of the marshes. If the mouth of an estuary closes due to reduced freshwater input there is the possibility that S. maritima communities may disappear. Spartina maritima is absent from periodically closed South African estuaries which may be attributed to the plant' s requirement for tidal flooding and saturated substrates. It is recommended that in permanently open estuaries, freshwater should be discharged in such a manner as to maintain an open mouth. This state is required to achieve the tidal flushing essential for intertidal salt marsh environments. Tidal exchange is also important in maintaining salt marsh zonation patterns.
Acknowledgements The Water Research Commission is thanked for funding this project. The Foundation for Research and Development provided a bursary for the first author. Mr M. Van der Merwe and Mr M. Brassil are thanked for technical assistance.
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