Growth and Survival of the Halophyte Salicornia Europaera L. Under

GROWTH AND SURVIVAL OF THE HALOPHYTE SALICORNIA EUROPAEA L. UNDER SALINE FIELD CONDITIONS1

DAVID C. McGRAW and IRWIN A. UNGAR, Department of Botany, Ohio University, Athens, OH 43701 A bstrad. Field investigations were carried out to determine growth and survival rates of Salicornia europaea L. in a saline environment at Rittman, Ohio. Collected data indicated that from 02% to 100% of the seedlings within the 'A saline zones investigated did not survive to maturity. Seedling mortality was statistically correlated at P<().()1 to rising soil salinity stress during late spring and summer. Plant growth was minimal between April and June, increasing sharply during late summer and fall. OHIO J. SCI. 81(8): 109, 1981

, Salicornia europaea L. is an annual often increasing the rate of mortality halophyte, in the family Chenopodiaceae, during drought periods (Ungar 1973). with succulent erect photosynthetic The optimum salinity for growth of shoots (5-40 cm). The species is widely some species of halophytes is often distributed and is known to inhabit between 1% and 2% NaCl (Webb 1966, inland and coastal salt marshes of North Langlois 1967, Tiku 1976, Ungar 1978); America, Europe, and Africa (Fernald however, all halophytes exhibit reduced 1950). growth when salt concentrations exceed Germination, mortality, and growth their limits of tolerance (Williams and of halophytic species are often controlled Ungar 1972, Hansen et al (1976). Popu- in nature by the interaction of two lation dynamics, particularly of inland environmental factors: soil moisture and salt marsh communities, are likely to be soil salinity, which are codeterminants greatly affected by the seasonal distribu- of soil water potential (Waisel 1972). tion of precipitation peculiar to each Seed germination in many halophytic geographic location (Weaver 1918, Ungar species occurs early in the growing 1974). For example, in a salt marsh on season when moisture is plentiful and the property at Rittman, Ohio, Ungar the soil salinity concentrations are (1973) related the death of Salicornia reduced (Barbour 1970, Macke and europaea seedlings to below normal Ungar 1971). Retardation of seed germi- precipitation during the summer months. nation has been attributed to an osmot- The purpose of our investigation was ically induced salinity stress that is to determine how plant growth and reversible (Rivers and Weber 1971, mortality are related to changing field Ungar 1978). soil salinities during the 1976 growing season. Increased salinity stress due to METHODS AND MATERIALS droughts and to a higher rate of evapora- Location. The study area is located in a tion during summer months may cause saline marsh formed due to mining operations rapid changes in the density and diversity of the Morton Salt Company plant located in of species in halophyte communities Rittman, Ohio. A shallow salt pan (approximately 10 m x 40 m) was located in the center (Ungar 1974). Seasonal precipitation of the site where we collected field data. The patterns are often a major factor deter- study area as characterized by 4 major vegeta- mining soil water potentials. This factor tion zones: a Meadow zone, a Hordeum jubatum in turn affects establishment of seedlings, zone, an Atriplex triangularis zone, and a Sali- cornia europaea zone. 'Manuscript received 10 January 1080 and in Dynamics of Populations. Monthly visits ; revised form 2 May 1080 (#80-2). " were made to the study site during the 1976 100 110 D. C. McGRAW AND I. A. UNGAR Vol. 81

growing season, from 12 April to 26 October. Groups of twenty-five 100 cm2 quadrats were established in each of 3 separate regions of the zone dominated by Salicornia europaea. One group was situated in the standing water (5 cm 20 cm deep) of the pan, another was placed in a transitional zone at the water's edge (edge zone), while a third was located near the point of transition with the zone dominated by Atriplex triangularis (field zone). We made monthly counts of plants for each quadrat and deter- CONDUCTIVIT Y mined values for mean and standard error of the (MMHO/C M A T 25'C I mean densities for each of the three regions. Analysis of Dry Weights. On 12 April, 9 May, 6 June, and 14 August, we collected Salicornia europaea from the edge and field locations for dry weight comparison. Soil contain- JUNE JULY ing numerous rooted specimens was collected FIGURE 1. Monthly measurements of soil from the region adjacent to the Atriplex zone solution conductivity (mmho/cm at 25 °C) and from the region near the edge of the pan made with in situ conductivity sensors. water. We took the collections to the laboratory where 100 plants from each group were used for the determination of plant dry weight. Sepa- tered a peak in conductivity at the time rate root and shoot dry weights were determined of the 5 July readings. The remaining on 12 April, 6 June and 14 August 1976. The plants were dried to constant weight at 105 °C sensors displayed their highest values on in a forced draft drying oven, and the specimens 14 August. After this mid-summer con- were weighed in groups of 10 to the nearest ductivity peak was attained, a decrease 0.1 mg with a Mettler (H15) balance. in soil solution conductivity occurred in Field Soil Solution Conductivity. A series of September and October to levels found 13 conductivity sensors were implanted in the earlier in the growing season (fig. 1). root zone of the plants approximately 10 cm beneath the soil surface. These were placed Samples of standing water in the pan along a transect at regular intervals between collected at each visit to the research site the meadow and the center of the pan. We displayed a pattern of seasonal con- made monthly measurements of in situ soil solu- ductivity changes independent from that tion conductivity using a Soil Moisture Equip- ment Corp. #5500 salinity bridge. Samples of established for the soil solution. For pan water were collected and taken to the example, April, July, and October soil laboratory for measurements of conductivity solution conductivity values were 29.4, with a Radiometer (CDM2d) conductivity 109.9 and 39.5 mmhos/cm, while stand- meter. ing water on the pan at these locations RESULTS had conductivities of 64, 48, and 23 Soil Solution Conductivity. The soil mmhos/cm over the same time period. solution conductivity data indicates the Soil moisture levels in all zones were presence of a soil salinity gradient. High- above 50%, ranging from 50.9%to 61.4% est values were recorded from conducti- over the growing season. These data vity sensors located in the central area of indicate that these soils did not have a the pan, and lowest conductivity was mea- significant soil matric water stress during sured at sensors located in the meadow the period of active growth. (fig 1). The amplitude of the gradient Seedling Density and Mortality. In displayed seasonal variability. On 12 the Salicornia population, bordering the April, it ranged from 1.1 mmhos/cm in Atriplex zone (field), on 12 April 1976, the meadow to 48.0 mmhos/cm on the the mean density was 276 plants per 100 pan, while on 14 August, this range had cm2 quadrat (fig. 2). The density of 51. increased from 2.4 mmhos/cm in the europaea reached a peak of 362 on 9 May, meadow to 142.8 mmhos/cm on the pan. followed by the greatest mortality re- A seasonal fluctuation of soil solution corded for any region during the entire conductivity was apparent at all loca- growing season, the reduction in plant tions. The sensors located in the meadow density reaching 77% by 6 June. The zone had the earliest peak of soil solution high mortality early in the growing sea- conductivity, occurring on 6 June. Sen- son resulted in a gradual decrease in plant sors located in the Salicornia zone regis- number stabilized by 14 August, when the Ohio J. Sci. GROWTH AND SURVIVAL OF SALICORNIA 111

2 mean density was 56 plants per 100 cm TABLE 1 quadrat. The decrease in density in the Maximum and minimum survival levels for field zone from 9 May to 26 October was Salicornia europaea in 100 cm2 85%, and in 24% of the plots fewer than quadrats in three marsh zones. 5 plants survived (table 1). Initial Plant Final Plant Zone Number Number (12 April) (26 October) A triplex Border >x^ Min. 230 0* Max. 560 150* Pan ]Edge Min. 130 0* Max. 392 105* Pan Min. 1 0* Max. 28 0*

*These values represent extremes and indi- APRIL MAY JUNE JULY AUGUST SEPT. OCT. cate the very high mortality. Differences in all plots significant at P<0.01. FIGURE 2. Monthly measurements of Sali- cornia europaea population densities (No./ 100 cm2) in the region adjacent to the 5 July. By 14 August, no S. europaea A triplex triangularis zone (FIELD), the survived in the pan zone (fig. 2). region at the edge of the pan (EDGE), and the region in the standing water of the pan Dry Weight Analysis. Plants growing (PAN). Bars represent standard error of in the field and edge zones were analyzed the mean. for root and shoot dry weight on 12 April, 6 June, and 14 August (fig. 3). A similar fluctuation of density was Salicornia europaea plants collected on noted for 25 quadrats situated in the 12 April and 6 June from soils within the Salicornia zone at the water's edge (fig. field zone had greater dry weights than 2). The mean density in this region on 12 April 1976 was 479 plants per quadrat, a number greater than the mean density of the zone bordering A triplex. Field FIELD, ROOT counts on 9 May revealed a 19% reduc- | | FIELD,SHOOT tion in plant density. The highest o> 40 mortality for the edge zone occurred be- E ESS? EDGE, ROOT tween 9 May and 6 June when a 62% ED6E SHOOT reduction in the density of Salicornia was observed. A gradual decrease in density followed until 14 August, after which the density of this population re- DR Y WEIGH T (mg ) mained stable. A 90% decrease in plant density occurred between 12 April and 26 October, and 8% of the quadrats had no survivors (table 1). The population density of S. europaea ZL for the pan region displayed a high de- APRIL JUNE AUGUST gree of variability between quadrats, FIGURE 3. Seasonal pattern of root and shoot dry weight accumulation for Sali- ranging from 0 to 28 plants per quadrat. cornia europaea plants growing in the region On 12 April, the highest density per adjacent to the A triplex triangularis zone quadrat was 28, while 70% of the quad- (FIELD) and in the region at the edge of the pan (EDGE). Bars represent standard rats contained 0 to 4 plants. The mean error of the mean and are omitted for April density per quadrat dropped from a high and June data because SEM was less than point of 4.3 plants per quadrat to 0.3 on ±5mg. 112 D. C. McGRAW AND I. A. UNGAR Vol. 81 plants from the edge zone. Collections salinities of approximately 39.8 and 18.9 on 14 August and 12 September showed mmhos/cm respectively. The very low an apparent reversal of the early season rate of S. europaea seedling establishment pattern of growth. Shoot dry weights observed in the pan region was probably for S. europaea plants growing in the due to the high salinity of the standing edge zone were 25% greater than for water early in the growing season and those growing in the field zone on 14 the high soil solution conductivities on August, and by September, the disparity the pan, reaching a mean of 129 mmhos/ between the two regions increased to cm by August. 75%.. Seasonal changes in dry weight The root:shoot ratio for Salicornia accumulation observed in this investiga- europaea collected from the region ad- tion appear to be directly related to jacent to the A triplex zone decreased soil salinity stress. The greatest increase from 0.60 on 6 June to 0.42 on 14 August. in dry matter production occurred Salicornia europaea plants collected from between the August and September the region at the edge of the pan showed sampling period when the soil salinity a similar trend, with their root:shoot levels began declining. Although seeds ratio decreasing from 0.75 on 6 June to of S. europaea were found germinating 0.34 on 14 August. in March, little dry weight production occurred until the latter part of the DISCUSSION growing season. Data collected during A lower density was recorded for the 1977 growing season corroborated Salicornia europaea plants in April, May, these findings, indicating that there is and June 1976 for the field zone, bordering essentially no increase in dry matter the region dominated by Atriplex tri- production between early and mid- angularis, than in the region at the summer (Ungar, unpublished data). In water's edge. The initially higher den- the late summer between 7 August and sity of S. europaea in the edge zone 16 September, dry weights increased to was probably due to higher soil moisture four times the previous value, and these levels that facilitated seedling establish- values doubled again between 16 Septem- ment. In August, September, and ber and 10 October. This rapid increase October, 61. europaea plants growing in in biomass production late in the growing the field zone displayed up to 14% higher season may be a mechanism that has average densities than those inhabiting evolved in this species to avoid decreasing the edge zone. The survival of 6". water potentials and the accompanying europaea in different regions of the site osmotic and ionic stress during the was low, ranging from 0 to 38% in any early and mid-summer months. The single quadrat. Plant death was sig- very low increase in dry weight between nificantly correlated at the P=.01 level May and July indicates that the low (Field, r = 0.8887, Edge, r = 0.7628, Pan, soil water potentials at this time were r = 0.6311) with the increase in soil limiting to plant growth. This long salinity from May to August. A similar term cessation of plant growth during situation was described by Weaver the middle of the growing season has (1918), Ungar (1967), and McMahon not been previously reported for halo- and Ungar (1978) for populations of phytes. The period of maximum growth Suaeda depressa and Atriplex triangularis, occurred just prior to the time of flower indicating that seedling mortality is and seed production. Waisel (1972) and closely related to an increase in soil Chapman (1974) have reported that salinity levels. halophytes often exhibit stunted growth Despite the presence of an abundance when found under saline conditions of floating Salicornia europaea seedlings approaching their tolerance limits, indi- in April and May in the pan zone, few cating that increased salinity stress plants rooted in the submerged areas. during the summer months could account In April, mean conductivity readings for for the decreased growth and high the pan water was 64 mmhos/cm, while mortality found for these populations of the edge and field zones displayed S. europaea. Ohio J. Sci. GROWTH AND SURVIVAL OF SALICORNIA 113

Acknowledgments. This research was sup- Rivers, W. G. and D. J. Weber 1971 The in- ported in part by NSF grants BMS 74-19435 fluence of salinity and temperature on seed and DEB 76-00444 and Ohio University Re- germination in Salicornia bigelovii. Physiol. search Committee grant no. 578. We wish to Plant. 24: 73-75. thank the Morton Salt Company for allowing Tiku, B. L. 1976 Effect of salinity on the us to carry out this research project on their photosynthesis of the halophyte Salicornia property and Professor W. A. Wistendahl for rubra and Distichlis stricta. Physiol. Plant. his comments on this manuscript. 37:23-28. Ungar, I. A. 1967 Vegetation-soil relation- LITERATURE CITED ships on saline soils in northern Kansas. Barbour, M. G. 1970 Is any angiosperm an Amer. Midi. Nat. 78: 98-120. obligate halophyte? Amer. Midi. Nat. 84: 1973 Salinity tolerance of inland halo- 105-120. phytic vegetation of North America. Bull. Chapman, V. J. 1974 Salt marshes and salt Soc. Bot. (France) 120: 217-222. deserts of the world. Verlag von J. Cramer. 1974 Population dynamics of inland Bremerhaven, Fed. Rep. Germany. 494 pp. halophytic communities. Bull. Soc. Bot. Fernald, M. L. 1950 Gray's manual of Bot- (France) 121: 287-292. any. D. Van Nostrand Co., New York. 1978 The effects of salinity and hor- 1632 pp. monal treatments on growth and ion uptake Hansen, D. J., P. Dayanandan, P. B. Kaufman of Salicornia europaea. Bull. Soc. Bot. and J. D. Brotherson 1976 Ecological adap- (France) 125: 95-104. tations of salt marsh grass Distichlis spicata 1978 Halophyte seed germination. (Gramineae), and environmental factors af- Bot. Rev. 44: 233-264. fecting its growth and distribution. Amer. Waisel, Y. 1972 Biology of halophytes. Aca- J. Bot. 63: 635-650. demic Press, New York. 395 pp. Langlois, J. 1967 Cultures sans sol de Sali- cornia stricta Dumort. Rev. Gen. Bot. 74: Weaver, T- E. 1918 The quadrat method in 176-196. teaching ecology. Plant World 21: 267-283. McMahon, K. and I. A. Ungar 1978 Phenol- Webb, K. L. 1966 NaCl effects on growth ogy, distribution and survival of A triplex and transpiration of Salicornia bigelovii a salt triangularis Willd. in an Ohio salt pan. Amer. marsh halophyte. Plant Soil 24: 261-268. Midi. Nat. 100: 1-14. Williams, D. W. and I. A. Ungar 1972 The Macke, A. J. and I. A. Ungar 1971 The ef- effect of environmental parameters on the fects of salinity on germination and early germination, growth, and development of growth of Puccinellia nuttalliana. Canadian Suaeda depressa (Pursh) Wats. Amer. J. J. Bot. 49: 515-520. Bot. 59: 912-918.