Journal of Arid Environmenrs (1994) 28: 207-213

The effect of environmental conditions on the growth and development of the oilseed halophyte Salicornia bigelovii Torr. in arid , México

Enrique Troyo-Diéguez, Alfredo Ortega-Rubio, Yolanda Maya & José Luis León

Centro de Investigaciones Biológicas de Baja California Sur, A .C. Apartado Postal 128, La Paz, B.C.S. México, C.P. 23000

(Received 9 January 1993, accepted 16 March 1993)

Due to its geographical situation, Baja California Sur is the most arid Mexican state, with the longest length of coast in the country. Hence, the study of halophytes for incorporation into rural agriculture is a priority for this region. In this research, the growth and development of a natural population of the oilseed halophyte Salicornia bigelovii Torr. as affected by environmental factors are analysed. Four transects were traced in the field, with sample sites of 1 mZevery 3m along each transect from which samples of soil and for laboratory analysis were taken, starting at the lowest seashore tide line. Edaphic and environmental factors as well as biomass, density, size, and dry matter were analysed through multivariate statistical methods. Three edaphic factors showed correlation with growth and development of individuals: growth was positively correlated with soil organic matter, and negatively correlated with the percentage of sand as a component of texture and with the balance of sodium (SAR parameter) in the soil saturated paste. Part of the results are unexpected because most of the previous work had dealt only with the salinity factor. The results will enable us to determine the next steps to promote the economic use of this species in the study region.

Keywords: Salicornia bigelovii; halophytes; salt marsh vegetation; growth success; soil factors; new crops; Baja California Sur

Introduction

Baja California Sur is one of the most arid states of , with an average of 80 mrn of annual precipitation; other arid states in north-west Mexico are and Baja California. Al1 these states contain large areas that may not receive any rain for severa1 years; they are also without lakes, rivers or other surface hydrological resources. Hence, in this zone, it is of considerable importance to introduce halophyte plants into the local agriculture, not only as alternative crops to ensure the economic development of the region, but also for fresh water conservation and social development. On the other hand, the Mexican state of Baja California Sur can almost be considered as an island surrounded by two seas: the Sea of Cortés (Gulf of California) and the Pacific Ocean; this State takes up 20% of the total Mexican shore line. The combination of large areas of coastline irrigated

0140-19631941030207 + 07 $08~0010 1994 Academic Press Limited 208 E. TROYO-DIÉGUEZ ET AL.

with saline water and the severe aridity of the region creates an environment suitable for halophytes as an alternative crop. Salicornia bigelovii Torr. (Chenopodiaceae), is an annual halophyte which inhabits the salt marshes of the Pacific coast from tropical Central America to southern California. This species has succulent, erect, photosynthetic shoots with articulated and apparently leafless stems; it flowers from July-November (Wiggins, 1980). Other Salicornia species are also common to the Pacific coast: S. virginica L. (S. ambigua Michx., S. Pacifica Standl.); S. subterminalis Parish (Munz & Keck, 1968; Wiggins, 1980); andS. europaea L., which is also common to salt marshes and beaches in eastern North America (Ellison, 1987; Ellison & Niklas, 1988). The seeds of S. bigelovii have potential as an alternative source of oil and flour, and consequently have potential as a seawater-irrigated oilseed crop. Glenn et al. (1991) conducted a long-term experiment in Puerto Peñasco, Sonora (Mexico), in order to evaluate the performance of S. bigelovii under daily seawater irrigations and the properties of the seed and oil. The oil content ranged from 26 to 33% and protein from 30 to 33%. The oil was high in polyunsaturated fatty acids, particularly linoleic acid, which accounted for 73 to 75% of the oil. They concluded that this halophyte appears to be a potentially valuable new high-yield oilseed crop for coastal desert regions, yielding a vegetable oil, amenable to commercial oilseed extraction methods. Severa1 investigations have been conducted in order to study the effect of soil moisture and soil salinity on the growth of Salicornia bigelovii (Webb, 1966; Rivers & Weber, 1971). So far, however, most of the research has been performed on other halophyte species, such as S. europaea (Ungar, 1977, 1987a, b; McGraw & Ungar, 1981; Riehl & Ungar, 1982), S. stricta Dumort (Langlois, 1967), Puccinellia sp. (Macke & Ungar, 1971), Atriplex sp. (McMahon & Ungar, 1978) and sp. (Tiku, 1976). They have focused mainly on the analysis of soil water factors and the distribution of these halophytes in saline marshes and salt pans. Biotic and abiotic factors play a significant role in determining biomass production and reproductive development in halophytes. Survival may be affected by a number of environmental variables, including soil salinity, deposition and erosion of substrate by tidal action, depth of the water table, amount of precipitation, temperature, and other microenvironmental variables. The success of annuals in saline habitats is determined by their ability to survive through each growing season and to reach the reproductive stage. Two general adaptations seem to be prevalent: first, species such as Spergularia marina (L.) Griseb., which produce seeds during most of the growing season; second, species, such as Salicornia europaea L. and Atriplex triangularis Willd., which produce seeds only in the late fall, but maintain a persistent seed bank beyond the normal germination period (Ungar, 19873). Ungar et al. (1979) indicated that the distribution of Salicornia europaea on an inland salt pan at Rittman, Ohio, was closely related to two environmental factors, soil salinity stress and competition; S. europaea was found to be strongly competitive in highly saline soils, because it showed optimal growth at salinity levels that were limiting to other species. In this study, the environmental conditions as they affect growth and development of a natural population of S. bigelovii during the growing season (spring) in a coastal salt marsh of the state of Baja California Sur, Mexico, are reported. The main objective of this study was to determine which environmental factors, besides soil salinity, were associated with the growth of this species under field conditions.

Study area and methods

The study site was located in a naturally formed saline marsh at the mouth of a seasonal stream, located at 24O05'N and 110°20'W, 17 km to the north of La Paz, capital city of the State of Baja California Sur. This site is characterized by three major vegetation zones, GROWTH AND DEVELOPMENT OF SALZCORNZA BZGELOVZZ 209

Salicorrzia bigelovii ; Monantochloe ; Jouvea pilosa & ; llttoralis 1 Laguncularia 1 1 racemosa I l ~ ~

Figure 1. General sketch of the vegetation zones delimited by the dominant species in the study area. depending on the relative abundance of four species: Salicornia bigelovii, Monanthochloe littoralis Engelm., Jouvea pilosa (Presl) Scribn., and Laguncularia racemosa (L.) Gaertn. (Fig. 1). Salicornia plantlets emerged during March, following the short and mild winter rains during February (Fig. 2); the growing season is from March to August. Sampling was carried out during the flowering stage, which occurred in the hot season (Fig. 2). During September 1988, four transects were established in the study area from the high tide leve1 to the plant population. Each transect was divided in plotlsample sites every 3m; each sample site covered an area of 1 m'. Transects were traced in the field by selecting at random four out of 10 pre-selected points related to possible transects which cross that part of the population with average

" Jan Fet) Mar Apr May .Jun .lul Aug Scp Oct Nov Ilrc Months Figure 2. Mean values of temperature (-O-= average temperature; 4- = maximum temperature) and precipitation (m) in La Paz area during 1988. 210 E. TROYO-DIÉGUEZ ET AL. characteristics for the salt marsh. The first transect comprised 15 sample sites and the others nine sites. The following data were recorded in each station: number of transects, number of sample sites, distance to the sea shore and the distance to the highest tide level. For the S. bigelovii individuals at each sample site, severa1 growth variables were recorded: number of plants, average height, phenological stage, and fresh and dry weight. Weather variables were excluded for simplicity because in previous work we found that Salicornia populations reach their highest stand in spring, after the winter rainy season (Troyo-Diéguez & Breceda, 1992). To determine the dry weight, the collected plants were dried in an oven to 65°C for 72 h until they became weight constant. Then, the specimens of al1 species were weighed to the nearest 0.01 g. On each sample site, the superficial 30 cm of soil were sampled according to the horizons A and C. Conventional soil and plant physical-chemical analysis was conducted to determine the texture class (using a Bouyoucos densimeter), organic matcer concen- tration (by titration with ferrous sulfate), salinity of the saturated paste (using the Wheatston's electrical conductivity bridge), sodium balance expressed as SAR (numerical calculation of the sodium adsorption relationship parameter, quantifying caz+and by the EDTA method), and the concentration of major nutrients through bromatological analysis (Richards, 1970; Jackson, 1982). A Principal Component Analysis (Morrison, 1978) was performed using al1 the recorded variables in order to select those with the highest correlation to explain the greatest percentage of variance related to the variables recorded for the habitat. For those variables highly associated with the growth features of S. bigelovii, a multiple regression analysis (Steel & Torrie, 1960; Smith, 1988) was conducted to determine correlations with the plant features.

Results

Mean values for the edaphic features are given in Table 1; the extremely low availability of nitrogen is noteworthy. Results of the Principal Component Analysis performed with al1 the recorded variables are shown in Table 2. Three of the Principal Components account for 67.44% of the total variance. The variables with the highest significance on the second Principal Component were the abundance of S. bigelovii, the average weight of the plants, average height of the individuals and the soil sodium balance (SAR), soil texture and organic matter. The association between plant abundance and soil characteristics can be easily observed when the factor loading of the second and third components are plotted. Figure 3 shows both sets of variables which are closely related.

Table 1. Recorded values for edaphic variables in a Salicornia salt marsh, located near La Paz, BCS, México - Variable Units n Minimum Maximum Mean -- PH - 14 8.07 8.61 8.38 Organic matter Yo 24 0.13 1-40 0.36 Electrical conductance mmhos cm-' 24 12.40 22.08 17.24 Sodium ratio SAR - 24 16.22 31.40 18.10 Sodium (Na+) meq 1-' 24 114.80 200.80 160.98 Potassium (KzO) kg ha-' 24 252.00 804.00 526.40 Calcium (caz+) meq 1- ' 24 50.00 50.00 50.00 Magnesium (M~~+) meq 1- ' 24 50.00 150.00 70.80 Phosphorous (P20,) kg ha- ' 24 7-00 54.00 22.13 Nitrogen (total) % 14 0.01 0.07 0.02 GROWTH AND DEVELOPMENT OF SALZCORNIA BIGELOVII 211

Table 2. Results of the Principal Component Analysis perfomed with the recorded plant and soil variables

Principal Component

Variable 1 2 3

Shore distance 0.841 Tide distance 0.841 Soil salinity -0.814 Sodium concentration - 0.771 Phosphorus concentration 0.740 ~Magnesiumconcentration - 0.733 Soil humidity - 0.623 Potassium concentration - 0.503 Organic matter - 0.054 Plant abundance O. 1O0 Sodium balance (SAR) - 0.359 Soil texture - 0.004 Plant weight (average) 0.104 Plant height (average) 0.043 Plant weight (individual) 0.01 1 Phenological stage 0.056 Calcium concentration 0.441 Nitrogen concentration 0.441

Variance explained by rotated components 4,947 Percent of the total variance explained 27.482

The results of the Multiple Regression performed with the weight of the plants, using this variable as an index of their growth success, and the three soil characteristics, were found to be the more important factors through the Principal Component Analysis, and can be summarized in the following equation [Fc3,20)= 47.342**, R' = 0.877 and p < 0.001]:

W = 845.948 + 2321*700(OM)- 662.141 (ST) - 3.665 (SD) (1) Where: W = Salicornia biomass (fresh weight), in gm-2, OM = Organic matter, entered as a %, ST = Soil texture, ranging as an integer value from 1 through 4, as follows: ST = 4,(sands), ST = 3, (sandy loams), ST = 2, (silts and loamy mid-type soils), ST = 1, (loamy clays and clays), and SD = Sodium balance, expressed as SAR (Sodium adsorption relation) parameter. SAR = (N~+)I[(o.~)(c~''+ M~'')]~~~ Note: Na', caz' and M~'+in meq 1- .

Discussion

Of al1 the environmental features considered, it was found that the three soil characteristics are closely related to the adaptation and growth success of S. bigelovii in the study area. Based on these results, growth was positively correlated with soil organic matter, and -1.0 -0.5 0.0 0.5 1.0 Factor 2 Figure 3. Association between plant abundance, growth and physico-chemicalcharacteristics of soil (see Table 2).

negatively correlated with the percentage of sand and soil sodium balance (SAR parameter). The positive correlation with soil organic matter seems to be a natural characteristic of a logical pattern of distribution, although no previous reports have mentioned this kind of relationship for halophytes. We assume that organic matter at this site is the result of both mangrove decay and the seasonal stream deposition. However, it was unexpected that growth of this halophyte was promoted by a smaller quantity of sand than by a loamy soil and, at the same time, successful growth started to decrease when the soil sodicity, expressed as SAR (Sodium Adsorption Ratio), was near 20.0, a value that can be interpreted as a high risk of sodium toxicity, depending on the cation balance with calcium and magnesium (Richards, 1970). A lesser SAR magnitude of the soil can reflect that the value of Na+ is less than caz+and ME'+.u This means that Na+ is the main factor in soil salinity, and that it can be substituted by caz+.Consequently, the balance of sodium in the soil can be considered as one of the parameters required to evaluate stress factors affecting Salicornia plants in a hypersaline environment. As regards soil texture, the higher content of loamy particles increases the soil capacity and thus the possibility to hold water for plants (Gavande, 1972); in this sense, it was observed that S. bigelovii is sensitive to water depletion and only grows where the substrate humidity remains near the field capacity (FC) value. It will be necessary to confirm these hypotheses through experimental studies. Nevertheless, this work provides a better understanding of the environmental variables which affect growth of S. bigelovii, which could become an alternative crop in Baja California Sur, Mexico, as well as in other arid or semi-arid coasts.

We would like to thank the personnel of the Soil and Water Analysis Laboratory of Secretaría de Agricultura y Recursos Hidráulicos, in La Paz (Mexico), for their helpful assistance in the soil analysis, to Laura Arriaga for her kind help in the statistical analysis and to Francisco de Lachica, Marcos Acevedo and Franco Cota for their help in the field. We would also like to thank three anonymous reviewers for their comments and suggestions. This work was conducted with economic support from the Centro de Investigaciones Biológicas de Baja California Sur (Project 321), Coordinación Sectorial of the Secretaría de Educación Pública, and the Consejo Nacional de Ciencia y Tecnología of México (D 112-904584). GROWTH AND DEVELOPMENT OF SALICORNIA BIGELOVII 213

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