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Small-scale resource heterogeneity among halophytic plant species in an upper salt marsh community
Aquatic Botany 78 (2004) 337–448
Small-scale resource heterogeneity among halophytic plant species in an upper salt marsh community Lucy St. Omer∗ Department of Biological Sciences, San Jose State University, One Washington Square, San Jose, CA 95192, USA Received 7 May 2003; received in revised form 12 November 2003; accepted 16 December 2003
Abstract The focus of the present study was to determine whether spatial and temporal variation, in soil and plant factors of upper salt marsh areas, exists among microsites of three coexisting halophytic plant species, Grindelia humilis, Jaumea carnosa and Limonium californicum, on the Pacific coasts of California. Low frequencies in tidal inundations coupled with variation in temperature and rainfall patterns often result in wide seasonal salinity variations in these upper salt marsh zones. The study was carried out to evaluate (1) variation in soil osmolalities and soil water contents for the three species; (2) differences in chemical soil factors associated with the three species; (3) variation in leaf succulence associated with saline stress; and (4) levels of plant nutrients present in each of the three species. The results indicated that soil osmolalities associated with Limonium, a salt excreting halophyte were markedly different from those recorded for the other two species. Nitrogen levels in soils associated with Jaumea as well as levels in composite plant samples were significantly lower than those of the other two species. Also noted were variations in nutrient ions in plants as well as soil environments. © 2004 Elsevier B.V. All rights reserved. Keywords: Species diversity; Community structure; Soil osmolalities; Leaf succulence; Plant nutrients
1. Introduction Along intertidal Pacific coasts, salt marsh environments are directly controlled by frequencies of tidal inundations and topographical characteristics. Together, these combined factors are primarily responsible for defining soil gradients which support distinct vege∗ Fax: +1-408-924-4840. E-mail address: [email protected] (L. St. Omer).
0304-3770/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2003.12.002
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tated zones—upper, middle, and lower marsh vegetation zones. Each one is dominated by halophytic plant species that are adapted to specific salinity and hydrologic regimes present in the region (Chapman, 1974; Armstrong et al., 1985; Eleuterius and Caldwell, 1985; Bertness and Ellison, 1987; Woerner and Hackney, 1997; Alvarez Rogel et al., 2000). The lower marsh zone is dominated by Spartina foliosa while the middle zone is heavily covered with Salicornia virginica plants in addition to a few individuals of plant species from the upper marsh zone. The upper marsh zone is composed of a mixture of the following halophytes—Jaumea carnosa, Distichlis spicata, Atriplex semibaccata, Frankenia grandifolia, Limonium californicum, Grindelia humilis and a few Salicornia plants. To the casual observer, the nature of each of the three vegetated zones present in intertidal saltmarsh communities can be mistakenly interpreted as homogeneous environments. However, upon closer examinations, heterogeneous patterns become increasingly obvious in both the biotic and abiotic components. Although salinity and moisture levels are predominant in regulating plant species composition within these zones, biotic factors such as competition and facilitation also participate in controlling species distributional patterns (Silander and Antonovics, 1982; Snow and Vince, 1984; Pennings and Callaway, 1992; Bertness and Shumway, 1993). Whilst salt marsh environments are considered regions of very high productivities, community structure is, nevertheless, characterized by low species richness (low numbers of species) as compared to other known natural communities of high productivity. This pattern of low diversity is, no doubt due to the high saline stress associated with that community (Reinhold and Queen, 1974; Schamp et al., 2002). In addition to the greater diversity of the upper marsh region, that zone is also subject to greater temporal changes in abiotic factors as compared with the lower and middle regions. Fluctuations in soil salinity, resulting from changes in rainfall and tidal patterns, are especially common in these upper regions (Coultas and Hsieh, 1997). The upper marsh zones are less frequently inundated by tides as compared with lower marsh areas where tidal flows are continual. As a result of this infrequency in tidal inundations, soil surface regions in the upper marsh areas are prone to extreme saline environmental conditions during the dry summer periods when evaporative rates increase (Callaway et al., 1990; Callaway, 1994). Following heavy winter rains, the upper marsh regions are subject to much lower soil salinities as salts are leached from root zones (Barbour and Major, 1997; Zedler, 1982; Noe and Zedler, 2001). Coexisting plants growing in close proximity in upper marsh communities must partition soil regions around them if they are to adequately absorb sufficient water and minerals necessary for survival during these stressful periods (Caldwell, 1994; Smilauerova and Smilauer, 2002). Temporal heterogeneity in environmental conditions has been observed in several other types of plant communities, and several authors have underlined the importance of this variability in maintaining complex community structure (Wu and Loucks, 1995; Beck, 1998; Benedetti-Cecchi et al., 2000; Noe and Zedler, 2001; Bliss et al., 2002). Although earlier studies of salt marsh environments have examined variation among the vegetated zones, there is little information on spatial and temporal heterogeneity in soil and plant resources among coexisting plant species at smaller spatial scales. This study explores spatial and temporal differences at plant and soil microsites of three coexisting halophytes in order to discern the role of heterogeneity in partitioning species
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habitats. Three plant species were chosen based on their different responses to saline stress. L. californicum (Boiss), a species known to excrete salt on shoot surfaces, is noted for possessing leaves that are often densely covered with salt crystals during the drier summer months (Kassas and Zahran, 1967). J. carnosa (Less) a succulent halophytic plant, increases its osmotic balance by accumulating ions that are later diluted as soil solutions become less saline (St. Omer and Schlesinger, 1980; Purer, 1942). In an earlier study, G. humilis (Hook and Arn) exposed to increasing salts at root zones was shown to exclude salts from entering root tissues (Ravetta et al., 1977). The study addresses the following main questions: (1) Are soil osmolality and soil water content different among microsites covered by these three selected halophytes? (2) Is soil chemical composition different for each species? (3) Does leaf succulence, a structural feature common to plants growing in saline stress, differ among the three species? and (4) Do levels of plant tissue nutrients vary among the three species? 2. Materials and methods 2.1. Study sites and plant species The study site was located at the upper regions of the salt marsh at the Palo Alto Baylands, located along the southern end of the San Francisco Bay in California (37◦ 27 N, 122◦ 08 W). This salt marsh has a Mediterranean climate characterized by heavy winter rains followed by hot dry summers. Associated with this climatic pattern is the seasonal pattern of low winter and high summer soil salinities. Sampling times were specifically chosen to match this marked seasonal environmental change, which controls plant growth. The three species selected are all perennial plants that actively grow from March to October, spring to late summer, and die back during the winter months (Purer, 1942; Macdonald and Barbour, 1974). 2.2. Soil sampling and analysis Plant and soil samples were collected on 13 and 14 April, 15 and 16 June, and 22 and 23 August 2000. The randomly chosen sites in the upper salt marsh zone (>90 m above mean low water) consisted of a mixture of the three selected plant species and received less frequent tidal inundations as compared with sites in the middle and low marsh zones. Samples were removed during low tide intervals, and stored in ice chests for transport back to the laboratory. Ten uniform vegetation stands (average 3 m × 4 m) containing the three chosen coexisting plant species, were randomly chosen for sampling. Plant samples and soils directly below each species were randomly removed from marked quadrats (20 cm ×50 cm) within these chosen stands. Five soil cores (3.2 cm diameter; 25 cm depth) were removed from root zones of each species using soil core samples for analysis of soil water content and soil osmolality. Water content (%) of soil samples was determined by weight lost after drying (60 ◦ C). Soil osmolalities were determined following the methods of Mahall and Park (1976) using a vapor pressure osmometer (Wescor, model 5520) and reported salinities (mmol kg−1 water) were based on the volume of water present in the soils. Five similar soil cores were randomly collected during April and August for comparisons of soil nutrients present in soil associated with each of the three species. Soil nutrient
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analyses were carried out at Soil Control Laboratory, Inc. (Watsonville, CA). Soil chemical analyses followed standard methods (Gavlak et al., 1994). Soil saturation pastes were used for determining soil pH (Robbins and Wiegand, 1990). Soil organic matter and organic C were determined by the Walkley–Black procedures (Mebius, 1960). Atomic absorption spectrophotometry (AAS) was used for determining Ca and Mg while atomic emission (atomic emission spectroscopy (AES)) was used for Na and K. Phosphorus was analyzed colorimetrically (Olsen and Sommers, 1982). Concentrations of nitrate, sulphate, and chloride were determined using ion chromatography while ammoniun N was analyzed with a selected ion electrode procedure. 2.3. Plant samples and analysis Nutrient analysis was carried out on composite leaf samples (10 sets) collected during the August sampling for each of the three species. Chemical analysis was carried out following the methods of the Association of Official Analytical Chemists (AOAC, 1990). Following digestion, filtration and dilution, samples were analyzed using atomic absorption spectrophotometry for Ca, Mg and atomic emission spectroscopy (AES) for Na and K. Determination of phosphorus was carried out colorimetrically following the vanadomolybdate method. Total nitrogen was quantified by Kjeldahl digestion with steam distillations followed by titrations (Jones et al., 1991). Ion chromatography was used for determination of chloride and sulphate (Eaton et al., 1995). Ten sets of randomly collected leaf samples at each of the chosen random sampling sites for each of the three species were used in estimating tissue succulence and surface salts. Leaf succulence was estimated after drying leaves in a forced air oven at 60 ◦ C and 48 h and obtaining dry mass of leaves for each of the three species. Leaf tissue succulence (water present) was expressed as a percent of fresh mass of leaves. Concentrations of surface salts were estimated on a leaf area basis. Comparable surface areas (300 cm2 ) were determined using a leaf area meter and salts present on the leaf surfaces were washed off with glass-distilled water and the osmolalities of the collected solutions determined on a vapor pressure osmometer (Wescor, model 5520). 2.4. Data analysis Data analysis was carried out using SYSTAT (SPSS 2000). Data were transformed and standardized prior to MANOVA repeated measures analysis (Sokal and Rohlf, 1995; Tabachnick and Fidell, 1996). Whenever needed posterior comparisons were carried out using Bonferroni (α = 0.05 level) adjusted multiple comparisons.
3. Results The results of the MANOVA for soil and plant characteristics as well as chemical composition of soils indicated a significant distinction among species related spatial and temporal distributions (Wilks’ Lambda, P < 0.01; Tables 1 and 2). Soil osmolalities were seasonally
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Table 1 ANOVA results for multivariate and univariate analyses of plant and soil variables for the three plant species—Grindelia, Jaumea, and Limonium Source of variation
d.f.
Wilks’ lambda
(A) Multivariate test for soil osmolality, soil water, surface salts and succulence Species 8, 66 0.027 Months 8, 66 0.05 Species × months 16, 101 0.131 Source of variation
d.f.
(B) Univariate tests: repeated measure Soil osmolality Species 2 Months 2
MS
F
P
42.353 28.715 6.003
0.001 0.001 0.001
F
P
0.015 0.344
4.663 107.914
<0.001 <0.001
Soil water Species Months
2 2
10.625 99.306
0.668 4.813
0.531 0.017
Plant surface salts Species Months
2 2
1.776 1.618
30.435 24.924
<0.001 <0.001
Plant succulence Species Months
2 2
110.76 126.535
<0.001 <0.001
182.97 155.26
different (P < 0.001), with the highest osmolalities recorded during August (Table 1 and Fig. 1a). Among species, Limonium had significantly higher (P < 0.01) soil osmolalities in August as compared with those for Jaumea and Grindelia. Soil water contents were consistently similar (P = 0.531) for soils associated with all species. However significantly higher (P < 0.017) water contents were recorded in June as compared with those of the other months (Table 1 and Fig. 1b). Plant surface salts were significantly different (P < 0.001) during the three sampling periods for all the species. Examinations of variation between species indicated greatest amounts of surface salts on Limonium leaves (Table 1 and Fig. 1c) a response pattern to saline stress, previously reported for that species. Plant tissue succulence was lowest (P < 0.001) in the August samples as compared with those of April and June (Table 1 and Fig. 1d). Significantly lower (P < 0.001) tissue succulence was recorded for Limonium and Grindelia. Jaumea, a known succulent halophytic plant, had the highest water content in leaf tissues throughout the sampling times. Temporal comparisons of soil chemistry indicated heterogeneous seasonal conditions among the three species. There were significant differences (P < 0.004) in ionic concentrations with sampling times as well as among the species examined (P < 0.001) (Tables 2 and 3). Significant seasonal differences (P < 0.05) were recorded for N, S, K, Mg, Na, and Cl, with concentrations highest in the August samples, except for N which registered highest concentrations in April (Table 4). No such differences were recorded for P, Ca,
342 L. St. Omer / Aquatic Botany 78 (2004) 337–448 Fig. 1. (a–d) Among-species and among-month variability in soil and plant characteristics. Different uppercase letters indicate that the species differ, and different lowercase letters indicate significant pair wise differences between means (P < 0.005; Bonferroni correction α = 0.05).
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Table 2 ANOVA results for multivariate and univariate analyses of chemical factors for soils associated with the three species—Grindelia, Jaumea, and Limonium Source of variation
d.f.
Wilks’ lambda
F
P
(A) Multivariate test Species Months Species × months
16, 34 8, 17 16, 34
0.092 0.076 0.217
4.88 25.71 2.433
<0.01 <0.01 <0.14
Source of variation
d.f.
MS
F
P
(B) Univariate tests: repeated measures Organic matter Species 2 Months 1
0.308 0.006
1.934 0.035
0.187 0.855
Organic C Species Months
2 1
0.205 0.037
1.123 0.211
0.357 0.654
N-total Species Months
2 1
2.432 3.508
16.888 13.378
0.001 0.003
PO4 Species Months
2 1
0.044 0.059
2.777 0.999
0.102 0.337
SO4 Species Months
2 1
0.384 5.704
4.873 77.708
0.028 0.001
Species Months
2 1
0.030 0.475
0.766 20.116
0.486 0.001
Ca Species Months
2 1
0.097 0.135
1.745 1.505
0.216 0.243
Mg Species Months
2 1
0.039 0.177
1.343 5.064
0.298 0.044
Na Species Months
2 1
0.097 3.315
1.149 52.67
0.349 0.001
2 1
0.679 7.024
7.987 23.639
0.006 0.001
K
Cl Species Months
organic C and organic matter, which were all similar over the sampling periods (Table 3). Spatial differences in soil chemistry were also significant among the three plant species. Comparisons of ionic concentrations associated with species indicated similar concentrations of P, K, Ca, and Na among soils associated with all three species (Table 3). In contrast,
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Table 3 Chemical analysis of soils collected in mono-specific stands of Grindelia, Jaumea and Limonium present in upper salt marsh zones during the sampling periods of April and August Date
Grindelia
Jaumea
Limonium
pH
April August
7.31 ± 0.0 7.33 ± 0.0
7.21 ± 0.0 7.11 ± 0.0
7.21 ± 0.0 7.08 ± 0.0
Organic matter (%)
April August
8.96 ± 2.1 12.56 ± 1.6
12.72 ± 1.1 11.50 ± 1.1
10.38 ± 1.4 8.88 ± 1.2
Organic C (%)
April August
5.24 ± 1.2 7.10 ± 0.9
7.44 ± 0.7 6.66 ± 0.6
6.1 ± 1.0 5.24 ± 0.7
N-total (mg/kg)
April∗ August
80.48 ± 15.5 56.68 ± 4.7
48.06 ± 4.8∗ 15.19 ± 4.2∗
80.52 ± 17.5 45.65 ± 10.4
PO4 (mg/kg)
April August
101.0 ± 10.4 90.8 ± 8.8
90.4 ± 3.8 76.6 ± 2.2
91.8 ± 7.3 94 ± 10.8
SO4 (mg/l)
April August∗
20.8 ± 2.9 32.4 ± 4.1
14.0 ± 0.8 50.2 ± 6.5
23.6 ± 3.9 57.0 ± 3.4∗
K (mg/kg)
April∗ August
690 ± 72.3 812 ± 26.7
592 ± 10.7 784 ± 50.5
664 ± 74.5 884 ± 71.7
Ca (mg/kg)
April August
1900 ± 181 2120 ± 336
2060 ± 260 1460 ± 222
1740 ± 201 1520 ± 101
Mg (mg/kg)
April August∗
1560 ± 156 1680 ± 80
1740 ± 50.9 1820 ± 73.4
1600 ± 122 2040 ± 177∗
Na (mg/kg)
April August∗
4320 ± 787 6529 ± 285
4120 ± 120 8940 ± 742
4380 ± 680 9020 ± 891
Cl (mg/kg)
April August∗
180 ± 44.4 232 ± 24.9
102 ± 7.4 450 ± 66.0
184 ± 29.9 704 ± 226∗
Results are means of five replicates plus (S.E.). ∗ Significant differences are indicated at P < 0.05. Bonferroni correction α = 0.05.
Table 4 Plant nutrients (% dry weight) present in leaf tissues of three halophytic species Nutrients
Grindelia
Jaumea
Limonium
N-total PO4 SO4 K Ca Mg Na Cl
1.50 0.21 0.17 2.30 0.60 0.21 0.90 3.00
1.10 0.17 0.81 0.70 0.96 0.94 8.00 9.70
2.10 0.13 0.77 1.30 0.49 0.46 4.10 9.50
Results are for composite samples (10 sets) collected during the August sampling.
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concentrations of S, Mg, Cl were highest (P < 0.05) in Limonium soils while Jaumea soils had the lowest concentrations (P < 0.001) of N as compared with the other two species (Tables 2 and 3). Examinations of plant nutrients, present in composite tissue samples of the three plant species, indicated lower concentrations of several nutrients in tissues of Grindelia as compared with the other two species (Table 4). Lower concentrations of S, Mg, Na, and Cl were recorded for Grindelia, with the latter two ions registering three or more times lower than concentrations in the other two species. However, the pattern for concentrations of K was the reverse with Grindelia registering higher concentrations (Table 4). Total N in plant tissues for Jaumea was the lowest among the three species, a pattern similar to those recorded for soil nutrients in the present study (Tables 3 and 4).
4. Discussion Soil osmolalities for all three species were seasonally consistent, and steadily increasing as temperatures increased during the spring and summer months (Fig. 1a). Temporal variation in salinity and moisture levels arising from seasonal rainfall patterns have been documented in earlier reports for upper salt marsh regions (Callaway, 1994; Noe and Zedler, 2001). In the present study, the lower soil osmolalities during April following heavy winter rains and the increases in osmolalities during August when temperatures increased are consistent with those of earlier reports on variations in salinity levels of salt marsh soils (Macdonald and Barbour, 1974; Mahall and Park, 1976; St. Omer and Schlesinger, 1980). Also noted in this study were spatially heterogeneous conditions for soil osmolalities among the three species. Soil osmolalities for Limonium recorded in the August samples were significantly higher than those recorded for Jaunea and Grindelia (Fig. 1a). This increase recorded for Limonium can be attributed to salt crystals excreted from leaf surfaces, which fall out and accumulate in surrounding soils. Excretion of salts from leaf surfaces is known to increase during periods of high transpiration rates associated with increased summer temperatures (Alvarez Rogel et al., 2000; Rozema et al., 1981). No spatial differences were recorded in soil water levels among the three plant species, a pattern consistent with earlier salt marsh investigations (Burke et al., 2002). The temporal increases in water content in soils collected during the month of June may have resulted from increased soil shading provided by shoot biomass during a period of relatively low temperatures. In addition, the effect of tidal flow to these areas may have also contributed to these higher soil water levels. Examinations of spatial variation in soil nutrients for the three species indicated differences among soil environments (Tables 2 and 3). Soils associated with Limonium indicated higher concentrations of C1, Mg, and S, whereas nitrogen levels were significantly lower for Jaumea. This lower concentration of nitrogen in Jaumea soils may be meaningful, since other researchers have concluded that nitrogen may limit plant biomass in salt marsh regions (Ungar, 1991). The general pattern of higher ionic concentrations of soil nutrients in the August samples can again be attributed to higher ionic accumulation rates in surface soils, accompanying increased evaporation (Mahall and Park, 1976).
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The lowest levels of Na and Cl ions were found in Grindelia tissue (Table 4). This finding is supported by earlier studies in which relatively low accumulations of salts were measured in tissues of Grindelia plants exposed to solutions of increasing NaCl levels (Ravetta et al., 1977). Nevertheless, in spite of the low accumulation of NaCl in Grindelia, growth was inhibited by the higher saline concentration of the growth media. Among the three species, Limonium is considered best able to withstand soils of higher salinity, since it is known to release large amounts of salts from shoot tissues (Kassas and Zahran, 1967). The higher ionic concentrations of Na and Cl ions in plant tissues of Jaumea is consistent with its method of salt tolerance, namely accumulating ions and maintenance of tissue succulence in shoots (Purer, 1942). In general, data for surface salts and leaf succulence are consistent with methods of salt tolerance for all the three species, with the highest surface concentrations occurring in the salt excreting species, Limonium (Table 1 and Fig. 1; St. Omer and Schlesinger, 1980; Kassas and Zahran, 1967). Earlier ecological studies have underlined the importance of soil heterogeneity in establishing species composition in natural communities including grasslands and deserts (Hook et al., 1991; Schlesinger et al., 1996). Earlier controlled laboratory studies of the saltmarsh species examined in this study have documented levels of resources for species survival that are similar to those recorded in this field study (Kassas and Zahran, 1967; Ravetta et al., 1977; St. Omer and Schlesinger, 1980). The significant differences in soil and plant characteristics among species, reported in this study, add support to the idea that the role played by small-scale differences in both biotic and abiotic factors present in plant communities should be considered in ecological studies. References Alvarez Rogel, J., Alcaraz Ariza, F., Ortiz Silla, R., 2000. Soil salinity and moisture gradients and plant zonation in Mediterranean salt marshes of Southeast Spain. Wetlands 20, 357–372. AOAC, 1990. Official Methods of Analysis. Association of Official Analytical Chemists Inc., Arlington, VA. Armstrong, W., Wright, E., Lythe, S., Gaynard, T., 1985. Plant zonation and the effects of the spring—neap tidal cycle on soil aeration in a salt marsh. J. Ecol. 73, 323–339. Barbour, M., Major, J., 1997. Terrestrial Vegetation of California. Wiley, New York, USA. Beck, M.W., 1998. Comparison of the measurement and effects of habitat structure on gastropods in rock intertidal and mangrove habitats. Mar. Ecol. Progr. Ser. 169, 165–178. Benedetti-Cecchi, L., Bulleri, F., Cinelli, F., 2000. The interplay of physical and biological factors in maintaining mid-shore and low-shore assemblages on rocky coasts in the northwest Mediterranean. Oecologia 123, 406–417. Bertness, M.D., Shumway, S.W., 1993. Competition and facilitation in marsh plants. Am. Nat. 142, 718–724. Bertness, M.D., Ellison, A.M., 1987. Determinants of pattern in a New England salt marsh plant community. Ecol. Monogr. 57, 129–147. Bliss, K., Jones, R., Mitchell, R., Mou, P., 2002. Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior? New Phytol. 154, 409–417. Burke, D., Hamerlynch, E., Hahn, D., 2002. Interactions among plant species and microorganisms in salt marsh sediments. Appl. Environ. Micro. 68, 1157–1164. Caldwell, M., 1994. Exploiting nutrients in fertile soil microsites. In: Caldwell, M., Pearcy, R.W. (Eds.), Exploitation of Environmental Heterogeneity by Plants. Academic Press, San Diego, CA, USA, pp. 325–347. Callaway, R.M., Jones, S., Ferren, W.R., Parikh, A., 1990. Ecology of a Mediterranean-climate estuarine wetland at Carpinteria, California: plant distributions and soil salinity in the upper marsh. Can. J. Bot. 68, 1139–1146. Callaway, R.M., 1994. Facilitative and interfering effects of Arthrocnemum subterminale on winter annuals. Ecology 75, 681–686.
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Small-scale resource heterogeneity among halophytic plant species in an upper salt marsh community Lucy St. Omer∗ Department of Biological Sciences, San Jose State University, One Washington Square, San Jose, CA 95192, USA Received 7 May 2003; received in revised form 12 November 2003; accepted 16 December 2003
Abstract The focus of the present study was to determine whether spatial and temporal variation, in soil and plant factors of upper salt marsh areas, exists among microsites of three coexisting halophytic plant species, Grindelia humilis, Jaumea carnosa and Limonium californicum, on the Pacific coasts of California. Low frequencies in tidal inundations coupled with variation in temperature and rainfall patterns often result in wide seasonal salinity variations in these upper salt marsh zones. The study was carried out to evaluate (1) variation in soil osmolalities and soil water contents for the three species; (2) differences in chemical soil factors associated with the three species; (3) variation in leaf succulence associated with saline stress; and (4) levels of plant nutrients present in each of the three species. The results indicated that soil osmolalities associated with Limonium, a salt excreting halophyte were markedly different from those recorded for the other two species. Nitrogen levels in soils associated with Jaumea as well as levels in composite plant samples were significantly lower than those of the other two species. Also noted were variations in nutrient ions in plants as well as soil environments. © 2004 Elsevier B.V. All rights reserved. Keywords: Species diversity; Community structure; Soil osmolalities; Leaf succulence; Plant nutrients
1. Introduction Along intertidal Pacific coasts, salt marsh environments are directly controlled by frequencies of tidal inundations and topographical characteristics. Together, these combined factors are primarily responsible for defining soil gradients which support distinct vege∗ Fax: +1-408-924-4840. E-mail address: [email protected] (L. St. Omer).
0304-3770/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2003.12.002
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tated zones—upper, middle, and lower marsh vegetation zones. Each one is dominated by halophytic plant species that are adapted to specific salinity and hydrologic regimes present in the region (Chapman, 1974; Armstrong et al., 1985; Eleuterius and Caldwell, 1985; Bertness and Ellison, 1987; Woerner and Hackney, 1997; Alvarez Rogel et al., 2000). The lower marsh zone is dominated by Spartina foliosa while the middle zone is heavily covered with Salicornia virginica plants in addition to a few individuals of plant species from the upper marsh zone. The upper marsh zone is composed of a mixture of the following halophytes—Jaumea carnosa, Distichlis spicata, Atriplex semibaccata, Frankenia grandifolia, Limonium californicum, Grindelia humilis and a few Salicornia plants. To the casual observer, the nature of each of the three vegetated zones present in intertidal saltmarsh communities can be mistakenly interpreted as homogeneous environments. However, upon closer examinations, heterogeneous patterns become increasingly obvious in both the biotic and abiotic components. Although salinity and moisture levels are predominant in regulating plant species composition within these zones, biotic factors such as competition and facilitation also participate in controlling species distributional patterns (Silander and Antonovics, 1982; Snow and Vince, 1984; Pennings and Callaway, 1992; Bertness and Shumway, 1993). Whilst salt marsh environments are considered regions of very high productivities, community structure is, nevertheless, characterized by low species richness (low numbers of species) as compared to other known natural communities of high productivity. This pattern of low diversity is, no doubt due to the high saline stress associated with that community (Reinhold and Queen, 1974; Schamp et al., 2002). In addition to the greater diversity of the upper marsh region, that zone is also subject to greater temporal changes in abiotic factors as compared with the lower and middle regions. Fluctuations in soil salinity, resulting from changes in rainfall and tidal patterns, are especially common in these upper regions (Coultas and Hsieh, 1997). The upper marsh zones are less frequently inundated by tides as compared with lower marsh areas where tidal flows are continual. As a result of this infrequency in tidal inundations, soil surface regions in the upper marsh areas are prone to extreme saline environmental conditions during the dry summer periods when evaporative rates increase (Callaway et al., 1990; Callaway, 1994). Following heavy winter rains, the upper marsh regions are subject to much lower soil salinities as salts are leached from root zones (Barbour and Major, 1997; Zedler, 1982; Noe and Zedler, 2001). Coexisting plants growing in close proximity in upper marsh communities must partition soil regions around them if they are to adequately absorb sufficient water and minerals necessary for survival during these stressful periods (Caldwell, 1994; Smilauerova and Smilauer, 2002). Temporal heterogeneity in environmental conditions has been observed in several other types of plant communities, and several authors have underlined the importance of this variability in maintaining complex community structure (Wu and Loucks, 1995; Beck, 1998; Benedetti-Cecchi et al., 2000; Noe and Zedler, 2001; Bliss et al., 2002). Although earlier studies of salt marsh environments have examined variation among the vegetated zones, there is little information on spatial and temporal heterogeneity in soil and plant resources among coexisting plant species at smaller spatial scales. This study explores spatial and temporal differences at plant and soil microsites of three coexisting halophytes in order to discern the role of heterogeneity in partitioning species
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habitats. Three plant species were chosen based on their different responses to saline stress. L. californicum (Boiss), a species known to excrete salt on shoot surfaces, is noted for possessing leaves that are often densely covered with salt crystals during the drier summer months (Kassas and Zahran, 1967). J. carnosa (Less) a succulent halophytic plant, increases its osmotic balance by accumulating ions that are later diluted as soil solutions become less saline (St. Omer and Schlesinger, 1980; Purer, 1942). In an earlier study, G. humilis (Hook and Arn) exposed to increasing salts at root zones was shown to exclude salts from entering root tissues (Ravetta et al., 1977). The study addresses the following main questions: (1) Are soil osmolality and soil water content different among microsites covered by these three selected halophytes? (2) Is soil chemical composition different for each species? (3) Does leaf succulence, a structural feature common to plants growing in saline stress, differ among the three species? and (4) Do levels of plant tissue nutrients vary among the three species? 2. Materials and methods 2.1. Study sites and plant species The study site was located at the upper regions of the salt marsh at the Palo Alto Baylands, located along the southern end of the San Francisco Bay in California (37◦ 27 N, 122◦ 08 W). This salt marsh has a Mediterranean climate characterized by heavy winter rains followed by hot dry summers. Associated with this climatic pattern is the seasonal pattern of low winter and high summer soil salinities. Sampling times were specifically chosen to match this marked seasonal environmental change, which controls plant growth. The three species selected are all perennial plants that actively grow from March to October, spring to late summer, and die back during the winter months (Purer, 1942; Macdonald and Barbour, 1974). 2.2. Soil sampling and analysis Plant and soil samples were collected on 13 and 14 April, 15 and 16 June, and 22 and 23 August 2000. The randomly chosen sites in the upper salt marsh zone (>90 m above mean low water) consisted of a mixture of the three selected plant species and received less frequent tidal inundations as compared with sites in the middle and low marsh zones. Samples were removed during low tide intervals, and stored in ice chests for transport back to the laboratory. Ten uniform vegetation stands (average 3 m × 4 m) containing the three chosen coexisting plant species, were randomly chosen for sampling. Plant samples and soils directly below each species were randomly removed from marked quadrats (20 cm ×50 cm) within these chosen stands. Five soil cores (3.2 cm diameter; 25 cm depth) were removed from root zones of each species using soil core samples for analysis of soil water content and soil osmolality. Water content (%) of soil samples was determined by weight lost after drying (60 ◦ C). Soil osmolalities were determined following the methods of Mahall and Park (1976) using a vapor pressure osmometer (Wescor, model 5520) and reported salinities (mmol kg−1 water) were based on the volume of water present in the soils. Five similar soil cores were randomly collected during April and August for comparisons of soil nutrients present in soil associated with each of the three species. Soil nutrient
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analyses were carried out at Soil Control Laboratory, Inc. (Watsonville, CA). Soil chemical analyses followed standard methods (Gavlak et al., 1994). Soil saturation pastes were used for determining soil pH (Robbins and Wiegand, 1990). Soil organic matter and organic C were determined by the Walkley–Black procedures (Mebius, 1960). Atomic absorption spectrophotometry (AAS) was used for determining Ca and Mg while atomic emission (atomic emission spectroscopy (AES)) was used for Na and K. Phosphorus was analyzed colorimetrically (Olsen and Sommers, 1982). Concentrations of nitrate, sulphate, and chloride were determined using ion chromatography while ammoniun N was analyzed with a selected ion electrode procedure. 2.3. Plant samples and analysis Nutrient analysis was carried out on composite leaf samples (10 sets) collected during the August sampling for each of the three species. Chemical analysis was carried out following the methods of the Association of Official Analytical Chemists (AOAC, 1990). Following digestion, filtration and dilution, samples were analyzed using atomic absorption spectrophotometry for Ca, Mg and atomic emission spectroscopy (AES) for Na and K. Determination of phosphorus was carried out colorimetrically following the vanadomolybdate method. Total nitrogen was quantified by Kjeldahl digestion with steam distillations followed by titrations (Jones et al., 1991). Ion chromatography was used for determination of chloride and sulphate (Eaton et al., 1995). Ten sets of randomly collected leaf samples at each of the chosen random sampling sites for each of the three species were used in estimating tissue succulence and surface salts. Leaf succulence was estimated after drying leaves in a forced air oven at 60 ◦ C and 48 h and obtaining dry mass of leaves for each of the three species. Leaf tissue succulence (water present) was expressed as a percent of fresh mass of leaves. Concentrations of surface salts were estimated on a leaf area basis. Comparable surface areas (300 cm2 ) were determined using a leaf area meter and salts present on the leaf surfaces were washed off with glass-distilled water and the osmolalities of the collected solutions determined on a vapor pressure osmometer (Wescor, model 5520). 2.4. Data analysis Data analysis was carried out using SYSTAT (SPSS 2000). Data were transformed and standardized prior to MANOVA repeated measures analysis (Sokal and Rohlf, 1995; Tabachnick and Fidell, 1996). Whenever needed posterior comparisons were carried out using Bonferroni (α = 0.05 level) adjusted multiple comparisons.
3. Results The results of the MANOVA for soil and plant characteristics as well as chemical composition of soils indicated a significant distinction among species related spatial and temporal distributions (Wilks’ Lambda, P < 0.01; Tables 1 and 2). Soil osmolalities were seasonally
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Table 1 ANOVA results for multivariate and univariate analyses of plant and soil variables for the three plant species—Grindelia, Jaumea, and Limonium Source of variation
d.f.
Wilks’ lambda
(A) Multivariate test for soil osmolality, soil water, surface salts and succulence Species 8, 66 0.027 Months 8, 66 0.05 Species × months 16, 101 0.131 Source of variation
d.f.
(B) Univariate tests: repeated measure Soil osmolality Species 2 Months 2
MS
F
P
42.353 28.715 6.003
0.001 0.001 0.001
F
P
0.015 0.344
4.663 107.914
<0.001 <0.001
Soil water Species Months
2 2
10.625 99.306
0.668 4.813
0.531 0.017
Plant surface salts Species Months
2 2
1.776 1.618
30.435 24.924
<0.001 <0.001
Plant succulence Species Months
2 2
110.76 126.535
<0.001 <0.001
182.97 155.26
different (P < 0.001), with the highest osmolalities recorded during August (Table 1 and Fig. 1a). Among species, Limonium had significantly higher (P < 0.01) soil osmolalities in August as compared with those for Jaumea and Grindelia. Soil water contents were consistently similar (P = 0.531) for soils associated with all species. However significantly higher (P < 0.017) water contents were recorded in June as compared with those of the other months (Table 1 and Fig. 1b). Plant surface salts were significantly different (P < 0.001) during the three sampling periods for all the species. Examinations of variation between species indicated greatest amounts of surface salts on Limonium leaves (Table 1 and Fig. 1c) a response pattern to saline stress, previously reported for that species. Plant tissue succulence was lowest (P < 0.001) in the August samples as compared with those of April and June (Table 1 and Fig. 1d). Significantly lower (P < 0.001) tissue succulence was recorded for Limonium and Grindelia. Jaumea, a known succulent halophytic plant, had the highest water content in leaf tissues throughout the sampling times. Temporal comparisons of soil chemistry indicated heterogeneous seasonal conditions among the three species. There were significant differences (P < 0.004) in ionic concentrations with sampling times as well as among the species examined (P < 0.001) (Tables 2 and 3). Significant seasonal differences (P < 0.05) were recorded for N, S, K, Mg, Na, and Cl, with concentrations highest in the August samples, except for N which registered highest concentrations in April (Table 4). No such differences were recorded for P, Ca,
342 L. St. Omer / Aquatic Botany 78 (2004) 337–448 Fig. 1. (a–d) Among-species and among-month variability in soil and plant characteristics. Different uppercase letters indicate that the species differ, and different lowercase letters indicate significant pair wise differences between means (P < 0.005; Bonferroni correction α = 0.05).
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Table 2 ANOVA results for multivariate and univariate analyses of chemical factors for soils associated with the three species—Grindelia, Jaumea, and Limonium Source of variation
d.f.
Wilks’ lambda
F
P
(A) Multivariate test Species Months Species × months
16, 34 8, 17 16, 34
0.092 0.076 0.217
4.88 25.71 2.433
<0.01 <0.01 <0.14
Source of variation
d.f.
MS
F
P
(B) Univariate tests: repeated measures Organic matter Species 2 Months 1
0.308 0.006
1.934 0.035
0.187 0.855
Organic C Species Months
2 1
0.205 0.037
1.123 0.211
0.357 0.654
N-total Species Months
2 1
2.432 3.508
16.888 13.378
0.001 0.003
PO4 Species Months
2 1
0.044 0.059
2.777 0.999
0.102 0.337
SO4 Species Months
2 1
0.384 5.704
4.873 77.708
0.028 0.001
Species Months
2 1
0.030 0.475
0.766 20.116
0.486 0.001
Ca Species Months
2 1
0.097 0.135
1.745 1.505
0.216 0.243
Mg Species Months
2 1
0.039 0.177
1.343 5.064
0.298 0.044
Na Species Months
2 1
0.097 3.315
1.149 52.67
0.349 0.001
2 1
0.679 7.024
7.987 23.639
0.006 0.001
K
Cl Species Months
organic C and organic matter, which were all similar over the sampling periods (Table 3). Spatial differences in soil chemistry were also significant among the three plant species. Comparisons of ionic concentrations associated with species indicated similar concentrations of P, K, Ca, and Na among soils associated with all three species (Table 3). In contrast,
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Table 3 Chemical analysis of soils collected in mono-specific stands of Grindelia, Jaumea and Limonium present in upper salt marsh zones during the sampling periods of April and August Date
Grindelia
Jaumea
Limonium
pH
April August
7.31 ± 0.0 7.33 ± 0.0
7.21 ± 0.0 7.11 ± 0.0
7.21 ± 0.0 7.08 ± 0.0
Organic matter (%)
April August
8.96 ± 2.1 12.56 ± 1.6
12.72 ± 1.1 11.50 ± 1.1
10.38 ± 1.4 8.88 ± 1.2
Organic C (%)
April August
5.24 ± 1.2 7.10 ± 0.9
7.44 ± 0.7 6.66 ± 0.6
6.1 ± 1.0 5.24 ± 0.7
N-total (mg/kg)
April∗ August
80.48 ± 15.5 56.68 ± 4.7
48.06 ± 4.8∗ 15.19 ± 4.2∗
80.52 ± 17.5 45.65 ± 10.4
PO4 (mg/kg)
April August
101.0 ± 10.4 90.8 ± 8.8
90.4 ± 3.8 76.6 ± 2.2
91.8 ± 7.3 94 ± 10.8
SO4 (mg/l)
April August∗
20.8 ± 2.9 32.4 ± 4.1
14.0 ± 0.8 50.2 ± 6.5
23.6 ± 3.9 57.0 ± 3.4∗
K (mg/kg)
April∗ August
690 ± 72.3 812 ± 26.7
592 ± 10.7 784 ± 50.5
664 ± 74.5 884 ± 71.7
Ca (mg/kg)
April August
1900 ± 181 2120 ± 336
2060 ± 260 1460 ± 222
1740 ± 201 1520 ± 101
Mg (mg/kg)
April August∗
1560 ± 156 1680 ± 80
1740 ± 50.9 1820 ± 73.4
1600 ± 122 2040 ± 177∗
Na (mg/kg)
April August∗
4320 ± 787 6529 ± 285
4120 ± 120 8940 ± 742
4380 ± 680 9020 ± 891
Cl (mg/kg)
April August∗
180 ± 44.4 232 ± 24.9
102 ± 7.4 450 ± 66.0
184 ± 29.9 704 ± 226∗
Results are means of five replicates plus (S.E.). ∗ Significant differences are indicated at P < 0.05. Bonferroni correction α = 0.05.
Table 4 Plant nutrients (% dry weight) present in leaf tissues of three halophytic species Nutrients
Grindelia
Jaumea
Limonium
N-total PO4 SO4 K Ca Mg Na Cl
1.50 0.21 0.17 2.30 0.60 0.21 0.90 3.00
1.10 0.17 0.81 0.70 0.96 0.94 8.00 9.70
2.10 0.13 0.77 1.30 0.49 0.46 4.10 9.50
Results are for composite samples (10 sets) collected during the August sampling.
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concentrations of S, Mg, Cl were highest (P < 0.05) in Limonium soils while Jaumea soils had the lowest concentrations (P < 0.001) of N as compared with the other two species (Tables 2 and 3). Examinations of plant nutrients, present in composite tissue samples of the three plant species, indicated lower concentrations of several nutrients in tissues of Grindelia as compared with the other two species (Table 4). Lower concentrations of S, Mg, Na, and Cl were recorded for Grindelia, with the latter two ions registering three or more times lower than concentrations in the other two species. However, the pattern for concentrations of K was the reverse with Grindelia registering higher concentrations (Table 4). Total N in plant tissues for Jaumea was the lowest among the three species, a pattern similar to those recorded for soil nutrients in the present study (Tables 3 and 4).
4. Discussion Soil osmolalities for all three species were seasonally consistent, and steadily increasing as temperatures increased during the spring and summer months (Fig. 1a). Temporal variation in salinity and moisture levels arising from seasonal rainfall patterns have been documented in earlier reports for upper salt marsh regions (Callaway, 1994; Noe and Zedler, 2001). In the present study, the lower soil osmolalities during April following heavy winter rains and the increases in osmolalities during August when temperatures increased are consistent with those of earlier reports on variations in salinity levels of salt marsh soils (Macdonald and Barbour, 1974; Mahall and Park, 1976; St. Omer and Schlesinger, 1980). Also noted in this study were spatially heterogeneous conditions for soil osmolalities among the three species. Soil osmolalities for Limonium recorded in the August samples were significantly higher than those recorded for Jaunea and Grindelia (Fig. 1a). This increase recorded for Limonium can be attributed to salt crystals excreted from leaf surfaces, which fall out and accumulate in surrounding soils. Excretion of salts from leaf surfaces is known to increase during periods of high transpiration rates associated with increased summer temperatures (Alvarez Rogel et al., 2000; Rozema et al., 1981). No spatial differences were recorded in soil water levels among the three plant species, a pattern consistent with earlier salt marsh investigations (Burke et al., 2002). The temporal increases in water content in soils collected during the month of June may have resulted from increased soil shading provided by shoot biomass during a period of relatively low temperatures. In addition, the effect of tidal flow to these areas may have also contributed to these higher soil water levels. Examinations of spatial variation in soil nutrients for the three species indicated differences among soil environments (Tables 2 and 3). Soils associated with Limonium indicated higher concentrations of C1, Mg, and S, whereas nitrogen levels were significantly lower for Jaumea. This lower concentration of nitrogen in Jaumea soils may be meaningful, since other researchers have concluded that nitrogen may limit plant biomass in salt marsh regions (Ungar, 1991). The general pattern of higher ionic concentrations of soil nutrients in the August samples can again be attributed to higher ionic accumulation rates in surface soils, accompanying increased evaporation (Mahall and Park, 1976).
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The lowest levels of Na and Cl ions were found in Grindelia tissue (Table 4). This finding is supported by earlier studies in which relatively low accumulations of salts were measured in tissues of Grindelia plants exposed to solutions of increasing NaCl levels (Ravetta et al., 1977). Nevertheless, in spite of the low accumulation of NaCl in Grindelia, growth was inhibited by the higher saline concentration of the growth media. Among the three species, Limonium is considered best able to withstand soils of higher salinity, since it is known to release large amounts of salts from shoot tissues (Kassas and Zahran, 1967). The higher ionic concentrations of Na and Cl ions in plant tissues of Jaumea is consistent with its method of salt tolerance, namely accumulating ions and maintenance of tissue succulence in shoots (Purer, 1942). In general, data for surface salts and leaf succulence are consistent with methods of salt tolerance for all the three species, with the highest surface concentrations occurring in the salt excreting species, Limonium (Table 1 and Fig. 1; St. Omer and Schlesinger, 1980; Kassas and Zahran, 1967). Earlier ecological studies have underlined the importance of soil heterogeneity in establishing species composition in natural communities including grasslands and deserts (Hook et al., 1991; Schlesinger et al., 1996). Earlier controlled laboratory studies of the saltmarsh species examined in this study have documented levels of resources for species survival that are similar to those recorded in this field study (Kassas and Zahran, 1967; Ravetta et al., 1977; St. Omer and Schlesinger, 1980). The significant differences in soil and plant characteristics among species, reported in this study, add support to the idea that the role played by small-scale differences in both biotic and abiotic factors present in plant communities should be considered in ecological studies. References Alvarez Rogel, J., Alcaraz Ariza, F., Ortiz Silla, R., 2000. Soil salinity and moisture gradients and plant zonation in Mediterranean salt marshes of Southeast Spain. Wetlands 20, 357–372. AOAC, 1990. Official Methods of Analysis. Association of Official Analytical Chemists Inc., Arlington, VA. Armstrong, W., Wright, E., Lythe, S., Gaynard, T., 1985. Plant zonation and the effects of the spring—neap tidal cycle on soil aeration in a salt marsh. J. Ecol. 73, 323–339. Barbour, M., Major, J., 1997. Terrestrial Vegetation of California. Wiley, New York, USA. Beck, M.W., 1998. Comparison of the measurement and effects of habitat structure on gastropods in rock intertidal and mangrove habitats. Mar. Ecol. Progr. Ser. 169, 165–178. Benedetti-Cecchi, L., Bulleri, F., Cinelli, F., 2000. The interplay of physical and biological factors in maintaining mid-shore and low-shore assemblages on rocky coasts in the northwest Mediterranean. Oecologia 123, 406–417. Bertness, M.D., Shumway, S.W., 1993. Competition and facilitation in marsh plants. Am. Nat. 142, 718–724. Bertness, M.D., Ellison, A.M., 1987. Determinants of pattern in a New England salt marsh plant community. Ecol. Monogr. 57, 129–147. Bliss, K., Jones, R., Mitchell, R., Mou, P., 2002. Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior? New Phytol. 154, 409–417. Burke, D., Hamerlynch, E., Hahn, D., 2002. Interactions among plant species and microorganisms in salt marsh sediments. Appl. Environ. Micro. 68, 1157–1164. Caldwell, M., 1994. Exploiting nutrients in fertile soil microsites. In: Caldwell, M., Pearcy, R.W. (Eds.), Exploitation of Environmental Heterogeneity by Plants. Academic Press, San Diego, CA, USA, pp. 325–347. Callaway, R.M., Jones, S., Ferren, W.R., Parikh, A., 1990. Ecology of a Mediterranean-climate estuarine wetland at Carpinteria, California: plant distributions and soil salinity in the upper marsh. Can. J. Bot. 68, 1139–1146. Callaway, R.M., 1994. Facilitative and interfering effects of Arthrocnemum subterminale on winter annuals. Ecology 75, 681–686.
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Ungar, I., 1991. Ecophysiology of Vascular Plants. CRC Press, Boston, USA. Woerner, L.S., Hackney, C.T., 1997. Distribution of Juncus roemerianus in North Carolina tidal marshes: the importance of physical and biotic variables. Wetlands 17, 284–291. Wu, J., Loucks, O.L., 1995. From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Q. Rev. Biol. 70, 439–466. Zedler, J., 1982. The Ecology of Southern California’s Coastal Salt Marshes: A Community Profile. United States Fish and Wildlife Service, FWS/OBS-81/54.