The relative importance of sulfate availability in the growth of Spartina alterniflora and Spartina cynosuroides

Aquatic botany ELSWIER

Aquatic Botany 56 ( 1997) 131- 143

The relative importance of sulfate availability in the growth of Spartina alternifZoraand Spartina cynosuroides Judith M. Stribling

’

Depurtment of Biological Sciences, Salisbury State University, I IO1 Cumden Avenue. Salkbury, MD 21801, USA Accepted 25 September 1996

Abstract The marsh cordgrass Sparrina alterniflora Loisel. dominates temperate coastal marshes on the Atlantic coast of North America, and it is an aggressive invader in other coastal wetlands around the world. However, it also flourishes at much lower salinities, extending well into the mesohaline region of major estuaries such as Chesapeake Bay. This species survives even in oligohaline marshes, usually disappearing in the natural environment at salinities below about 2%0. The possibility that this distribution is related to sulfate limitation was investigated in a long-term greenhouse experiment. Sulfate uptake kinetics were first determined for S. alternifora. The long-term growth response to four different concentrations of sulfate was then evaluated for S. alterniflora and for Spartina cynosuroides (L.) Roth, a low salinity species of overlapping distribution. Growth indices included the total number of leaves, total leaf length, and the relative growth rate of shoots and of whole plants. Spartina alterniflora responded positively to increasing sulfate concentration; however, S. cynosuroides did not exhibit a growth response. These results suggest that S. alterniflora distribution in oligohaline marshes is limited by sulfate supply, and that the plant may have an uncommonly high sulfate requirement. Keywords: Sulfate; Spartina alterniflora; Uptake kinetics; Salinity gradient; Marshes

1. Introduction The cordgrass Spartina altemijlora Loisel. is unique among marsh macrophytes on the Atlantic Coast of North America in its adaptation to a wide salinity range. This plant

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dominates coastal wetlands that often exceed seawater salinity, yet it can also thrive in estuarine marshes exposed to fresh water for part of the year. This distribution makes S. alfernifl~-a an ideal subject for the study of physiological characteristics associated with salinity. One environmental feature that varies markedly with salinity is the availability of sulfate. Sulfur is an essential nutrient for S. affernifloru, as for most plants. The question of sulfur limitation of growth in this species is moot in euhaline marshes, where seawater sulfate is usually present in high concentrations. The study of potentially limiting nutrients for S. ulfemij7oru has focused on nitrogen and phosphorus, with the former most frequently found to limit growth of this and other species in salt marshes (Valiela and Teal, 1974; Gallagher, 1975; Jefferies, 1977; Buresh et al., 1980; Hopkinson and Schubauer, 1984). With respect to sulfur, interest has focused on the deleterious effects of porewater sulfide on marsh plants (e.g. King et al., 1982; Ingold and Havill, 1984; Bradley and Morris, 1990; Koch et al., 1990). However, S. ulfemifloru growing in upper estuarine waters is exposed to extreme fluctuations in salinity, both tidally and meteorologically driven. Sulfate concentration varies temporally and spatially in oligohaline marshes (Stribling, 1994), and it is affected not only by variation in the salinity of estuarine waters, but by sulfur cycling in the sediments as well. In anoxic marsh sediments, sulfate serves as the primary terminal electron acceptor in decomposition of organic matter, even in relatively low salinity wetlands (Lord and Church, 1983; Howarth, 1984; Capone and Kiene, 1988). High rates of sulfate reduction, combined with low concentrations of sulfate in the overlying water, may leave the rhizosphere depleted of sulfate (Wiebe et al., 1981; Peterson and Howarth, 1987; Stribling, 1994). Spurtinu ulfernifloru usually disappears in the natural environment at salinities below about 2%0 and is replaced upstream by more typically freshwater species such as Pelfundru uirginicu (L.) Kunth (arrow arum> and Ponfederiu cordufu L. (pickerelweed) (Anderson et al., 1968). However, S. ulferniforu is dominant in some systems at salinities that are only slightly higher (Stribling, 1994). The role of marine sulfate inputs and porewater sulfate availability in the distribution of S. ulferniforu in brackish systems is not understood. There is evidence that this species, so well adapted to the euhaline environment, has a relatively high requirement for sulfate. In a preliminary experiment (J. Stribling, unpublished data, 19941, S. ulfemifloru, grown hydroponically in a nutrient solution which had sulfate salts replaced with chloride salts, exhibited marked reduction in growth after four to five weeks and severe chlorosis by the end of seven weeks. The importance of sulfur in the growth of crop plants has been recognized for many years, and the requirement for this nutrient often equals that of phosphorus (Tabatabai, 1984). Sulfur functions in S. ulfernifloru in ways common to most plants: it is a component of the amino acids cystine, cysteine, and methionine, of the co-factors biotin, thiamine, lipoic acid and co-enzyme A, and of sulfolipids, which form chloroplast membranes (Schmidt, 1986). Moreover, S. ulfemiforu may contain other essential forms of sulfur; its total sulfur content is higher than for most plants, with measured concentrations of up to 1.2% (Carlson, 1980; Carlson and Forrest, 1982; Omes and Kaplan, 1989). Molar nitrogen/sulfur ratios may be as great as 30: 1 in plants not deficient in sulfur (Epstein,

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19721, and a typical ratio is about 2O:l (Tabatabai, 1984; Cram, 1990). In contrast, nitrogen/sulfur ratios of less than 3: 1 were present in S. altemifloru at peak biomass in a low salinity Maryland marsh (Stribling, 1994), and similarly low ratios were found for S. altemij7oru in a South Carolina salt marsh (Omes and Kaplan, 1989). If sulfur compounds are uncommonly important in S. ultemifloru, sulfate availability may influence the plant’s distribution in oligohaline marshes. There are two potential mechanisms for growth limitation. First, high rates of dissimilatory sulfate reduction may result in limiting concentrations of sulfate within the rhizosphere. Ponnamperuma (1972) suggested that sulfate reduction could lead to inadequate sulfur available for rice cultivation. Although sulfide has been proposed as a sulfur source for S. ulternifloru, there is conflicting evidence as to whether it is actually incorporated directly or is first oxidized in the root zone (Carlson and Forrest, 1982; Fry et al., 1982; Trust and Fry, 1992; Stribling, 1994). If the plants depend on rhizosphere oxidation of sulfide, their sulfate supply may be insufficient. Second, at the upper reaches of estuaries, sulfate inputs to marshes from overlying water may be low enough to limit S. ultemifloru growth, even in the absence of high rates of sulfate reduction. The objective of this study was to determine the difference, if any, in response to different levels of sulfate by S. ulternzyoru. I simultaneously tested an equal number of individuals of Spurtinu cynosuroides CL.) Roth in order to determine the relative sulfate requirement of this congeneric species, the distribution of which overlaps S. ulternifloru at low salinities. In order to establish an appropriate range of sulfate concentrations among those found in estuarine waters, I first evaluated sulfate uptake kinetics for S. ulternifloru, which had not previously been described.

2. Methods 2.1. Uptake kinetics Spurtinu ultemijloru seedlings were grown in a greenhouse in sterile sand, saturated with a 10% modified Hoagland’s solution (Epstein, 19721, in which the major sulfate salts had been replaced with chloride salts (Table 1). This solution was amended with Na,SO, to a concentration of 8 Frnol l- ’. When the plants reached a height of approximately 25 cm, they were placed individually in hydroponic chambers, consisting of 500 ml brown polyethylene wide-mouth bottles, submerged 8 cm deep in water cooled to 2O”C,and connected to water-saturated air bubblers to gently mix the solution. To provide a relatively uniform light intensity and photoperiod, a 400 W metal halide lamp was used to provide 14 h of constant illumination. On a cloudless day, the peak photosynthetically active radiation at plant height was 1800 pmol mm2 s- ‘. Prior to testing, all plants were exposed to the nutrient solution, amended with 80 p_mol 1-l Na,SO,, for 2 days. For uptake kinetics determination, five plants each were exposed to sulfate concentrations of 40, 80, 160, 400 and 800 p,mol 1-l sulfate. A uniform ionic strength was maintained in the hydroponic solutions by adjusting with NaCl to that of the highest sulfate concentration. After 2 h acclimation, 5 ml samples of the solution for sulfate uptake determination were collected twice daily for 72 h, with replacement of the

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Table 1 Modified Hoagland’s in the text

nutrient solution. Concentrations

Compound

IQJo3

Ca(NO,),.4H,O NH,H,PO, MgCl,*6H,O KC1 H,BO MnCl,.4H,O ZnCl, CuSO,.SH,O

Botany 56 (1997) 131-143

are for full strength,

Element

Final cont. of element (pm01 1-l)

N K Ca P

16000 6ooo 4ooo 2ooo loo0 2000 2.5 2 2 0.5 0.5 20

Mg Cl B Mn zn cu MO Fe

(NH,),M0,0,, Fe-EDTA

dilutions were made as described

sample volume. Water lost by evapotranspiration was calculated at each sampling interval, and the uptake calculation was adjusted for the effect of water loss on concentration. Sulfate concentration was determined using a Dionex ion chromatograph. 2.2. Growth experiment Seeds were germinated in sterile sand saturated with deionized water. They were grown under ambient light in a greenhouse until the average height was approximately 7 cm. They were fertilized with a 50% modified Hoagland’s nutrient solution (see above), with no added sulfate. I used six seedlings of each species for initial dry weight determination. The experiment employed four concentrations of sulfate (8, 80, 800 and 1600 krnol l- ’> as Na,SO,, with six plants of each species per treatment. Based on the results of the sulfate uptake experiment, the concentration range included the approximate V,,, for S. altemiflora (see below); it also included the sulfate concentration of seawater diluted to 2%a salinity (approximately 1600 p,mol l-‘1. I maintained the plants for 6.5 (S.

Table 2 Summarv

of results of Soartina alterniflora

[SO,1

uotake kinetics determination Lineweaver-Burke

(km01 I- ‘)

Uptake rate (nmol g- ’b- ‘1

40.5 14.4 151.3 388.7 773.3

48.8 139.6 165.4 362.3 363.6

y-intercept x-intercept VInlX K,

transformation

results

0.00089 0.00126 1121 790.6

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Table 3 Summary of results of sulfate growth experiment. Calculation of the relative growth rate (RGR) is explained in the text. The highest significance level from ANOVA is indicated by asterisks: *P < 0.05; * *P < 0.01. Letters refer to post-hoc comparison between means. All data are means f 1 SD; N represents the number of individual plants tested (five plants died during the experiment). S.a., Spartina alternij7ora; Xc., Spartina cynosuroides

mJ

Plant RGR (g g- ’day- ‘)

Shoot RGR

Leaf length

(km01 I- ‘)

(g g- ’ day- ‘1

km)

.%a.

*

*

**

1600

0.42 0.43 0.48 0.50

s. c. 8 80 800 1600

NS 0.56 0.66 0.52 0.61

8 80 800

0.066 + 0.002a 0.068 + O.O07a,b 0.074fO.OOla,b 0.078 + 0.008b

i 0.02a * O.O5a,b + 0.OOa.b It 0.06b

NS 0.083 kO.014 0.097*0.013 0.077 rt 0.015 0.090 * 0.009

+ 0.10 * 0.09 + 0.10 kO.06

No. of leaves

N

NS

15.4f2.6a 23.2 i 6.7a,b 3 1.5 i 6.7b.c 38.0 + 8.2~

16.5 + 20.6+ 29.3 f 29.5 f

NS 23.7+7.1 37.3 i 6.4 28.5* 11.3 31.9+6.‘2

5.7 11.5 13.2 22.2

NS 2.3+ 1.4 5.3* 1.2 4.2 + 2.2 4.3+2.1

S. cynosuroides

40

I

a

80

800

Sulfate concentration, Fig.

1600

pmoles I-’

1. The effect of sulfate concentration on total leaf length in Spartina cynosuroides and Spartina Error bars denote rt 1 SD. Letters associated with each treatment represent the results of post-hoc comparisons (see Table 3).

alterm~ora.

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6,

S. cynosuroides

Botany 56 (1997) 131-143

T

T

T

8’0

860

1600

Sulfate concentration,

pmoles I-’

Fig. 2. The effect of sulfate concentration on number of leaves in Spartim cynosuroides and Spartina alterniflora. Error bars denote f 1 SD. Differences behveen treatments were not statistically significant for this feature.

cynosuroides) and 11 (S. alterniforu) weeks in the greenhouse in individual hydroponic chambers (see Uptake Kinetics above). The hydroponic solution was 50% Hoagland’s formula, modified as described above, and adjusted to uniform ionic strength with NaCI. The solutions were replaced weekly. Concentrations of sulfate, nitrate and phosphate, measured by ion chromatography, indicated that this regime satisfactorily maintained the initial concentrations. The experiment was terminated for each species when the plants reached a maximum height of 55 cm. Plants were rinsed in deionized water, separated into root and shoot fractions, and oven dried at 65°C to constant weight. Plant properties measured included total number of leaves per plant and total leaf length. In addition, as an index of the treatment effects on production, relative growth rate (RGR) (after Pearson and Havill, 1988) was calculated for the whole plant and the shoots based on the change in dry weight (W > over time (T) log,W, - log,W, RGR = (a-‘day-‘) Ti - To

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Botany 56 (1997) 131-143

Growth effects were analyzed using one-way analysis of variance; post-hoc comparisons used Tukey’s HSD (Multiple General Linear Model, Systat 5.1; Wilkinson, 1990).

3. Results 3.1. Uptake kinetics The velocity of sulfate uptake increased with increasing sulfate concentration (Table 2). Although the number of test concentrations was too small for a precise characterization of uptake kinetics, values for V,,, and K, were estimated by performing the Lineweaver-Burke linear transformation of the sulfate uptake data to fit MichaelisMenten kinetics (Nobel, 1970). In this calculation, the reciprocal of the initial velocity (u,) is plotted as a function of the reciprocal of the sulfate concentration; the value of

S. cynosuroides

8

80

800

1600

Sulfate concentration, pmoles I-’ Fig. 3. The effect of sulfate concentration on whole plant relative growth rate (RGR) in Spartim cynosuroides and Spartina alternijlora. Error bars denote k 1 SD. Letters associated with each treatment represent the results of post-hoc comparisons (see Table 3).

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J.M. Stribling/Aquatic S. cynoauroides

In

3 5

Botany 56 (1997) 131-143 T

0.08 0.06

S. alterfliflora

0.08

8

80 Sulfate

concentration,

800 pmoles

1600 I-’

Fig. 4. The effect of sulfate concentration on shoot relative growth rate (RGR) in Spartino cynosuroides and Spartino alterniflora. Error bars denote f 1 SD. Letters associated with each treatment represent the results of post-hoc comparisons (see Table 3).

the y-intercept is equal to l/V,,, and the x-intercept represents the value of - l/K,. From the Lineweaver-Burke transformation (Table 21, V,,, for S. ultemifloru was approximately 1100 p,mol l- ‘, and the half-saturation constant K, was 790 p,mol l- ‘, or 7.9 X 10m4 mol 1-l. The reported range of K, values for sulfate uptake in bacteria, fungi, algae, and higher plants is 10 -5-10-4 mol 1-l (Schiff and Hodson, 1973); Nissen (1973) found multiphasic sulfate uptake in plant roots in which K, ranged from 10m5 to lo-*. The experimentally determined value for V,,, was encompassed within the range of concentrations used in the growth experiment. 3.2. Growth efsects During the-course of the growth experiment, a total of five S. altemzfloru plants died or turned completely yellow (see Table 3); these were excluded from the analysis of growth effects. Increasing sulfate concentration was positively associated with most of the plant properties measured for S. altemifloru (Figs. l-4). Sulfate concentration had a significant positive effect on S. ultemifloru total leaf length (P < 0.001; Fig. l>, on

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relative growth rate of the whole plant (P < 0.035; Fig. 3), and on relative growth rate of the shoot fraction (P < 0.02; Fig. 4). The number of leaves per plant for S. aherniflora also appeared to increase with increasing sulfate concentration (Fig. 2); however, this effect was not statistically significant. In general, for the S. alferniflora plant variables, the greatest response to increasing sulfate concentrations seemed to be manifested between 8 and 800 p,mol l- ‘, with a less marked effect from 800 to 1600 km01 1-l. Spartina cynosuroides did not respond to increasing concentrations of sulfate. No significant growth effects were exhibited in this species in any of the variables tested (Figs. 1-4). However, the experiment was not optimally designed for study of S. cynosuroides, which usually attains a considerably greater maximum plant height than does S. alterniflora. It is possible that termination of the experiment when the plants reached 55 cm was premature for disclosure of treatment effects in S. cynosuroides. The results of the growth experiment are summarized in Table 1.

4. Discussion Considerable study has been made of ion uptake in salt marsh plants with respect to osmotic adjustment, with disproportionate emphasis on sodium and chloride ions (Flowers et al., 1977). Based in part on high concentrations of potassium, nitrate and sulfate in halophytes grown in normal nutrient solutions, these authors proposed a higher than normal mineral requirement for halophytes. Of the three most abundant ions in seawater, sulfate is the only macronutrient, and thus might be expected to figure strongly in such a constitutive requirement. One sulfur compound that may be involved in a high sulfur requirement in Spartina alterniflora is dimethylsulfoniopropionate (DMSP). Sparfina species are the only macrophytes known to contain large quantities of DMSP (Ernst, 19901, which may comprise up to 30% of total plant sulfur in S. alterniflora (Dacey et al., 1987; Weber et al., 1991), and 50% in Spartina anglica Hubbard (Van Diggelen et al., 1987). The role of DMSP in these two higher plant species is undetermined (Van Diggelen et al., 1986; Rhodes and Hanson, 1993; Otte and Morris, 1996). Although DMSP functions as an osmolyte in marine phytoplankton, no correlation was found between DMSP and salinity in S. anglica (Van Diggelen et al., 1986), or between DMSP and sodium chloride or sulfate in S. altemiflora (Calmer et al., 1996). It is also unlikely that this compound functions in sulfide detoxification or in storage of excess sulfur (Havill et al., 1985); DMSP levels in S. alterniflora also did not increase with increasing sulfide (Otte and Morris, 1996). This evidence strongly suggests that DMSP has some physiological role other than osmotic adjustment or sulfide detoxification. The positive response to sulfate concentration by S. altemiflora in this study supports the hypothesis that adaptation to high salinity in this species is linked to a high sulfate requirement, and that sulfate availability may limit S. alterniflora distribution in low salinity marshes. The range of sulfate concentrations in this experiment overlapped that found in natural systems where S. altemiflora gives way to other, low salinity species. For example, porewater sulfate concentrations of 500 p_mol 1-l or less were common at

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an oligohaline S. alterniflora marsh in Maryland where the plant was at the upper limit of its range along the salinity gradient (Stribling, 1994). It appears that sulfate concentrations between 0.5 and 1 mmol 1-l represent a critical level of availability of this nutrient for S. alrerniflora. This range is representative of the sulfate concentrations in estuarine waters of approximately 1%0salinity, and it is consistent with the observed distribution of this species. The lack of response to increased sulfate levels in S. cynosuroides also supports the hypothesis that S. alternij7ora has an uncommonly high sulfur requirement. Investigation of growth effects in other potential competitors such as Peltandra uirginica, Pontederia cordata, or Leersia oryzoides CL.) Swartz, should provide further insight into their relative sulfate requirements. In addition, similar study of other halophytic species with high sulfur content, in particular S. anglica, would help clarify this question. The distribution of salt marsh macrophytes in general is associated with environmental factors (Adam, 1990). Spartim alrernijora distribution within salt marshes has been linked to physical features such as redox potential, porewater sulfide concentration and salinity (Howes et al., 1981; Mendelssohn et al., 1981; King et al., 1982; Howes et al., 1986), most of which are related to elevation of the marsh site (Bertness and Ellison, 1987). Species distribution in European salt marshes has also been shown to be related to soil salinity, flooding of the root zone, and the presence and concentration of sulfide (Gray and Scott, 1977; Ingold and Havill, 1984; Van Diggelen et al., 1987). Harsh extremes in such sediment conditions limit the survival of potential glycophytic competitors of low marsh halophytes (Bertness and Ellison, 1987; Koch and Mendelssohn, 1989). On the other hand, halophytes appear to be restricted to the low marsh habitat, not by greater survival under those same extreme conditions, but by competitive interaction with other species. For example, S. alterniflora growth is unaffected or is enhanced by transplantation to higher elevations in salt marshes when competitors are removed (Bertness and Ellison, 1987). Whereas the distribution of salt marsh macrophytes along an elevation gradient is determined largely by competition, distribution along the salinity gradient may be more directly related to physiological responses to the environmental conditions, in particular, salinity. In a 3-year study of a very low salinity Maryland marsh, freshwater annuals were abundant in a year of high spring rainfall and declined in subsequent, drier years when salinity increased. Low salinity was, on the other hand, associated with reduced success of S. alterniflora; its peak biomass increased in that system in the years of lower spring rainfall. Seasonal dynamics of S. alterniflora growth in the same study suggest that the increase in S. alternifora abundance during years of higher salinity was related to sulfate availability. At an oligohaline site, porewater sulfate concentrations below 0.5 mm01 1-l were associated with a 2 month delay in peak standing crop relative to a higher salinity location in the same system (Stribling, 1994). Spartina alterniflora usually first colonizes low, unvegetated areas on the edge of marshes, where anoxic conditions and sulfate depletion are often extensive (Bertness, 1988). The possibility for sulfate limitation of S. alterniflora growth in oligohaline marshes, then, should be greatest in the habitat most likely to be invaded. Longer-term study of the community dynamics of low salinity S. alferniflora marshes, including transplant and fertilization experiments, should help define the relative importance of

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salinity in S. alfernifora distribution. The results of this study, combined with observations of sulfate concentrations and S. akrniflora distribution in oligohaline marshes. indicate that sulfate availability is a potentially important environmental variable in the success of this species at low salinities.

Acknowledgements

Sincere thanks to Drs. John Gallagher, Court Stevenson, Jeffrey Cornwell and Laura Murray and to two anonymous reviewers for constructive comments and suggestions. Plants and seeds were generously supplied by Suzanne McIninch of Environmental Concern and George Benedict, Jr. and Margaret Biddle of Benedict the Florist. I am indebted to Brian Sturgis for laboratory assistance and equipment setup. This work was supported in part by the National Oceanic and Atmospheric Administration National Estuarine Research Reserve System and by the National Science Foundation Land Margin Ecosystem Research Program (BSR-8814272).

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