Mortality of the Salt Marsh Species Salicornia Europaea and Atriplex Prostrata (Chenopodiaceae) in Response to Inundation

Waterlogging and salinity are considered to be the two major factors affecting growth and plant distribution in salt marshes. But while the effects of salinity are well known, few studies have investigated the impact of the former on plant survival. The purpose of this laboratory experiment was to determine the effects of water level on growth and survival of the halophytes Salicornia europaea andAtriplex prostrata. Plants were grown in the laboratory at the following levels of inundation: 1) roots and shoots completely submerged (high water), 2) roots completely submerged (medium water), 3) water level at the bottom of the pot (low water). The high water treatment caused 100% mortality in both species within one week. Survival was high for both species when grown in the other treatments, but there was an indication of lower survival (70%) in the medium water treatment for A prostrata than in the low water treatment (90%) after three weeks submersion. There was no significant difference (P >0.05) in biomass production between medium and low water treatments in either species. OHIO J SCI 100 (2):24-27, 2000 INTRODUCTION Flooded soils with reduced aeration are considered to be a major factor affecting plant distribution in salt marshes, but few studies have documented its impact on plant survival (Adam 1990; Ungar 1991). Salicornia europaea L. (common glasswort or samphire) and Atriplex prostrata Willd. (orache) are halophytes that inhabit inland and coastal salt marshes (Gleason and Cronquist 1991) where they are subjected to seasonal changes in water level due to precipitation in the colder months and dehydration in the summer months. Prolonged periods of flooding in soils can be detrimental to plant growth, because these soils become anoxic except for a thin oxygenated layer near the surface (Ponnamperuma 1984). Anoxic conditions may develop in just hours or up to several days after flooding as water fills the air spaces around soil particles and plant roots and microbial activity consume the remaining oxygen (Ponnamperuma 1984). When this occurs, the resulting anoxic conditions may inhibit plant growth by preventing plants from exporting salt and metabolic wastes such as ethanol and fatty acids from their roots (Van Diggelen 1991). Prolonged periods of saturated soils also induce a specific ion toxicity in halophytes from sulfide accumulated in the soils and promote the uptake of excessive amounts of reduced iron and manganese (Jeffrey 1987). Finally, because of the inhibitory effects mentioned above, waterlogged soils cause an inhibition of photosynthesis and disrupt plant hormonal balance (Van Diggelen 1991). Salicornia europaea is one of the most salt tolerant plants in general and is capable of growing under highly saline conditions on the lowest part of salt marshes Manuscript received 20 July 1999 and in revised form 17 April 2000 (#99-21). Corresponding author: Department of Biological Sciences, University of Wisconsin Milwaukee, PO Box 413, Milwaukee, WI 53201. E-mail: [email protected]. (Ungar 1977). It occurs predominantly in salt marsh soils that are water saturated and often flooded (Ungar 1977). However, S. europaea has little aerenchyma (7.1% root volume) tissue present in the roots compared to other species that grow under anoxic soil condition, including Agropyronpungens (Pers.) Roem. and Schult., Aster tripolium L., and Oryza sativa L, which contain 15.9 to 16.5% aerenchyma in their roots (Pearson and Havill 1988). Therefore, S. europaea must employ other means for supplying oxygen to its roots. It is possible that oxygen is brought in from the plant shoot. Jeschke and others (1995) determined that high atmospheric pressures from a Scholander pressure chamber were needed to remove sap from Atriplex hortensis L. which had little aerenchyma tissue compared to Leptochloa fusca (L.) Kunth, where pressure exerted caused the sap to easily pass through aerenchyma tissue in the root. It is therefore likely that S. europaea and A. prostrata oxygenate their roots via aboveground shoots. An investigation comparing two species, Salicornia dolichostachya Moss and Salicornia ramosissima J. Woods, demonstrated that anaerobic environments caused a decrease in their relative growth rates (Schat and others 1987), so the supply of oxygen to the roots of S. europaea is very important to plant growth and survival. When A. prostrata plants were grown hydroponically, mechanically aerated plants were able to accumulate more Na and Cl~ in their leaves than plants that were not aerated (Karimi and Ungar 1986), so root aeration is important to salt tolerance. Root oxygenation from the aboveground vegetation is likely to be important for halotolerance in A. prostrata because its roots do not contain aerenchyma tissue (Egan 1999). Field observations of ^triplex prostrata, a less salt tolerant halophyte than S. europaea, indicated that it grew in less saline soils in our study area, bordering the zone dominated by S. europaea which grew directly in the salt pan in the Rittman salt marsh (Egan and Ungar 2000). OHIO JOURNAL OF SCIENCE '1". I'. EC.AN AND I. A. UNGAR 25 Field observations at a salt marsh in Rittman, OH, indicated that unseasonably high flooding for up to two weeks appears to have caused high mortality in an area of the marsh dominated by S. europaea and A. prostrata (Egan 1999). In April 1996 there were approximately 140,000 S. europaea and 54,500 A. prostrata seedlings per square meter. By mid June 1996 the area was flooded and no plants survived in the plots monitored in April. Because of the high field mortality under complete submersion of these species, we were interested in determining how different levels of submersion affected these halophytes under controlled experimental conditions. The purpose of this laboratory experiment was to determine 1) the effect of water level on growth of these two halophytes and 2) the influence of different levels of submersion on survival of plants. MATERIALS AND METHODS Salicornia europaea seedlings were collected from a salt marsh in Rittman, Wayne County, in the northeast corner of the state of Ohio (long. 81°47'39" W; lat. 40°57'30" N) on 14 June 1996 from an area of the marsh with little to no standing water. Atrip lex prostrata plants were obtained by germinating seeds collected from the same location on 17 November 1995. Medium sized (1.5-2.0 mm diameter, Khan and Ungar 1984) seeds were germinated in an incubator with a 12 hr thermoperiod of 5° C:25° C, and a 12 hr photoperiod of dark:light (20.0 Ltmol photons msec, 400-700 nm). Both species were grown in a growth chamber for two months at a 15 hr photoperiod of dark:light (276.3 Limol photons rn^sec, 400-700 nm) before inundation treatments (Khan and Ungar 1984). At the beginning of the experiment mean height for S. europaea was 67.5 mm ± 2.3, A. prostrata was 119.5 mm ± 5.0. Salicornia europaea and A. prostrata plants were placed in one of three levels of 1/2 strength Hoagland and Arnon No. 2 nutrient solution (Moore I960) containing 170 mM NaCl to prevent S. europaea from wilting while not overstressing A. prostrata (Khan and Ungar 1984; Ungar 1991). Ten 4 L plastic containers (25 cm high x 23.5 cm wide x 14 cm deep) were used for each experiment (n = 10 replicates). Three different treatments were contained within each of the ten blocks by positioning pots at different levels: 1) roots and shoots completely submerged (high water), 2) roots completely submerged (medium water), and 3) water level at the bottom of the pot (low water). The medium and low levels were chosen because S. europaea and A. prostrata often grow under these conditions and we wanted to determine which condition was most advantageous for plant growth. The high water condition was chosen to replicate the observed flooded field conditions and we wanted to determine how long these species could tolerate complete inundation. Salicornia europaea plants were grown in pots containing field soil cores thinned down to avoid damaging the fragile root systems (10 plants per 7.5 cm diameter pot) from 20 June to 10 July 1996. Atriplex prostrata plants were transplanted from petri dishes to fine sand (1 plant per 9 cm diameter pot) from 18 July to 12 August 1996 during their peak growing season. Dissolved oxygen in each of the 4 L receptacles was measured weekly with a Ciba-Corning' oxygen probe (M90 Checkmate Modular Testing System) at low, medium, and high levels of inundation. Mean values for S. europaea and A. prostrata treatments were 7.19 ± 0.12 S.E. ppm and 8.48 ± 0.35 S.E. ppm O;, respectively. Data were analyzed using a one-way ANOVA (however, height data for A. prostrata failed the assumptions for normality and homoscedasticity and a Wilcoxon-Signed Rank test was used (NCSS 1995)). A Chi-square test was used to determine significant differences in the proportional data of percent survival among treatments (NCSS 1995). RESULTS There was 100% mortality of the completely inundated (high water) S. europaea and A. prostrata plants after one week. Therefore, the statistical tests compared the characteristics of plants from only medium and low water levels. Mean values between medium and low treatments did not differ between any pairs tested for height, number of internodes, number of internodes with branches, and diy mass (Table 1 and 2; P >0.05). There was no significant difference (P >0.80) in dissolved oxygen concentration at any water level. Survival for S. europaea in medium (96% ± 0.24) and