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Are biotic factors significant in influencing the distribution of halophytes in saline habitats?

II. Introduction

Tidal action, flooding, and salinity are considered to be controlling factors in the establishment and distribution of species in salt marsh and salt desert plant communities (Adams, 1963; Ranwell, 1972; Waisel, 1972; Chapman, 1974; Congdon, 1981; Adam, 1990; Ungar, 1991; Sanchez et al., 1996). Environmental factors determining the recruitment and distribution of halophytes have been examined by a number of investigators (Ungar, 1965, 1966, 1991; Clarke & Hannon, 1971; Brereton, 1971; Cooper & Waits, 1973; Mahall & Park, 1976; Snow & Vince, 1984; Adam, 1990; Pennings & Callaway, 1992; Khan & Ungar, 1995; Woerner & Hackney, 1997). Abrasive and depositional effects of tides have a significant effect on plant establishment and survival in coastal marshes (Johnson & York, 1915; Wiehe, 1935; Miller & Egler, 1950; Runge, 1972; Adam, 1990). Halophytes must adapt to the hypoxic or anoxic conditions of flooding in salt marshes and nutrient deficiencies in these habitats (Chapman, 1974; Gallagher, 1975; Patrick & Delaune, 1976; Langlois & Ungar, 1976; Lieffers & Shay, 1980; Mendelssohn, 1979; Cooper, 1982; Karimi & Ungar, 1986; Loveland & Ungar, 1983; Covin & Zedler, 1988; Adam, 1990; Ungar, 1991; Van Diggelen, 1991; Keiffer et al., 1994). Phenological adaptations include seed germination during periods of reduced salinity and the production of soil seed banks (Milton, 1939; Boorman, 1968; Hopkins & Parker, 1984; Bakker et al., 1985; Woodell, 1985; Ungar, 1987b, 1991; Hartmann, 1988; Leck et al., 1989; Hutchings & Russell, 1989; Bakker & deVries, 1992; Ungar & Woodell, 1993, 1996). Physiologically, halophytes have developed a number of mechanisms to avoid and resist salt stress: salt hairs and salt glands, succulence, dilution of salinity by increased growth, osmotic adjustment, compatible osmotica, root excretion of salts, root molecular sieve, selective ion uptake (Waisel, 1972; Flowers et al., 1977, 1986; Adam, 1990; Ungar, 1991).

A number of researchers have concluded that the zonational distribution pattern of species in inland and coastal salt marshes is determined by both biotic and abiotic factors (Stalter, 1973; Pielou & Routledge, 1976; Mahall & Park, 1976; Ungar, 1979; Silander & Antonovics, 1982; Ellison, 1987; Bertness & Ellison, 1987; Ungar, 1991; Pennings & Callaway, 1992; Mulder et al., 1996). Generally, it is reported that the lower limits of halophyte distribution in saline habitats are determined by physicochemical factors of the environment, such as tolerance to the salinity concentration, flooding, and the abrasive action of tides, whereas the upper limits of plant distribution in areas of lower salinity and reduced flooding are determined by competition (Ungar, 1966, 1978; Snow 8: Vince, 1984; Vince & Snow, 1984; Pennings & Callaway, 1992; Mulder et al., 1996). The more salt-tolerant halophytes either are less competitive in nonsaline habitats or have an obligate requirement for salt, which prevents them from growing in freshwater marshes (Ungar, 1966; Barbour, 1970; Bertness, 1991a, 1991b; Kenkel et al., 1991). A review of the literature on this subject indicates that there is a significant amount of evidence to support the above conclusion but that other biotic factors such as predation, parasitism, allelopathy, chemical inhibition, and facilitation also could play an important role in influencing the growth and survival of halophytes in saline habitats (Fireman & Hayward, 1952; Walsel, 1972; Chapman, 1974; Adam, 1990; Pennings & Callaway, 1996).

III. Competition

Plant species are often found to form zonational community patterns of vegetation in inland and coastal salt marshes (Ungar, 1965, 1974a, 1974b; Chapman, 1974; McMahon & Ungar, 1978; Snow & Vince, 1984; Bertness & Ellison, 1987; Adam, 1990; Table I). A number of environmental variables may play a significant role in determining the distribution of species in salt marshes, but the physiological limits of salt tolerance of each species often are strongly correlated with their distribution pattern (Ungar, 1962; Barbour, 1970; Bertness & Ellison, 1987; Adam, 1990; Wilson et al., 1996). Since most halophytes can grow and reproduce under nonsaline conditions, it is often more difficult to explain their absence from brackish and nonsaline habitats than to interpret their presence in high-salinity zonal communities (Ungar, 1966, 1991; Barbour, 1970). Absence of halophytes from the less saline soils in upper zones of salt marshes often is hypothesized to be due to their inability to compete with less salt-tolerant glycophytes that dominate these brackish and freshwater habitats (Purer, 1942; Hinde, 1954; Ungar et al., 1979; Bertness & Ellison, 1987; Bertness, 1991a, 1991b; Wilson et al., 1996). Competition for light often is a significant factor in determining which species survive in a particular marsh zone. Jerling and Liljelund (1984) determined that Plantago maritima distribution in the upper portions of a Baltic seashore meadow was restricted by competition for light, since it prevented plants from flowering and inhibited successful seedling establishment.

Table I Relative cover (percent) of plant species along a salinity gradient in a salt marsh in Park County, Colorado (adapted from Ungar, 1974a).
 Plant communities

 Distichlis Triglochin Wet Triglochm

Distichlis stricta 93 <1 0
Triglochin maritima 4 82 58
Puccinellia maritima <1 11 22
Salicornia rubra 3 5 2
Suaeda depressa <1 0 0
Ranunculus cymbalaria 0 1 14
Scirpus americanus 0 <1 3
Aster brachyactis 0 <1 <1
Aster pauciflorus 0 <1 <1
Juncus bufonius 0 0 <1

 Plant communities

 Puccinellia Salicornia

Distichlis stricta 0 0
Triglochin maritima 7 <1
Puccinellia maritima 64 1
Salicornia rubra 28 78
Suaeda depressa 0 21
Ranunculus cymbalaria 0 0
Scirpus americanus 0 0
Aster brachyactis 0 0
Aster pauciflorus 0 0
Juncus bufonius 0 0


Competition is considered to be a significant factor in determining both the species composition of salt marsh communities and the zonational patterns found in salt marsh and salt desert regions (Ungar et al., 1979; Russell et al., 1985; Bertness & Ellison, 1987; Scholten et al., 1987; Partridge & Wilson, 1988; Bertness, 1991a, 1991b; Pennings & Callaway, 1992; Mulder et al., 1996; Rejmankova et al., 1996). The significance of competitive effects in saline habitats is sometimes difficult to establish because of the overriding effect of saline conditions on plant establishment (Ungar, 1984, 1987a). However, a number of researchers have concluded that halophytes may be limited to saline habitats because of their inability to compete with the less salt-tolerant glycophytes in nonsaline areas (Ungar, 1966; Barbour, 1970; Ungar et al., 1979; Kenkel et al., 1991; Rahman & Ungar, 1994; Wilson et al., 1996). Transplant and removal experiments in salt marsh habitats have demonstrated either that a competitive interaction occurs when new species are added to a community or that the effect of competition is released when species are removed (Ungar et al., 1979; Silander & Antonovics, 1982; Snow & Vince, 1984; Bertness, 1991a, 1991b; Fig. 1). Silander and Antonovics (1982) and Scholten et al. (1987) determined from removal experiments that competition was a significant factor influencing plant distribution in salt marshes. Scholten et al. (1987) found that competition for light is a significant factor influencing the success of young emerging shoots and seedlings; therefore, they hypothesized, early emergence was an advantage for shade-intolerant species attempting to establish in salt marsh habitats.

[Figure 1 ILLUSTRATION OMITTED]

The downstream and downshore distribution of plant species into more saline environments along brackish riverbanks in New Zealand indicated that there was a high correlation between the salt tolerance of species and their occurrence in these habitats (Wilson et al., 1996). However, Wilson et al. (1996) concluded that the upstream distribution of plant species is not related to salinity, but that either intolerance to water deficits or competitiveness of species could significantly affect the zonational pattern of plants. Two environmental factors, salinity and flooding, were determined to be limiting species distribution in the Carpinteria salt marsh (California). Salicornia virginica was better able to tolerate flooding and persisted in the lower marsh, whereas Arthrocnemum subterminale was more tolerant of high salinities and occurred in the high marsh zone (Pennings & Callaway, 1992). When these two halophytes were transplanted into cleared plots they could both grow in the low marsh Salicornia zone and high marsh Arthrocnemum zone, indicating that competition was a significant factor limiting the upward and downward distribution of both of these species. Growth of Salicornia transplants in cleared plots in the Arthrocnemum zone was better than in the lower flooded zone dominated by Salicornia, but Salicornia growth was significantly inhibited when Arthrocnemum was not removed. Arthrocnemum growth was inhibited by Salicornia in the high Salicornia zone, preventing it from establishing at these sites. Pennings and Callaway (1992) concluded that competition was the factor limiting Salicornia establishment in the drier and more saline Arthrocnemum zone.

The annual halophyte Spergularia marina was determined to be negatively associated with Arthrocnemum subterminale, and its survival percentages increased with the removal of Arthrocnemum (Callaway, 1994). However, two other annuals, Hutchinsia procumbens and Parapholis incurva, were positively associated with Arthrocnemum and their survival percentages decreased when the shrub was removed. Light levels were lower beneath the shrub, which could be a negative factor for the establishment of some annual species of heliophytes. However, the salinity concentration was 27% lower and soil moisture 13% higher under shrubs, providing a more moderate edaphic environment for the recruitment of annual species. Facilitation of growth and establishment of plants in salt marshes, where one species may ameliorate the habitat for another, has also been reported for species in Rhode Island salt marshes (Bertness & Shumway, 1993; Bertness & Yeh, 1994; Bertness & Hacker, 1994; Hacker & Bertness, 1995). Also, associations with animals proved facilitative to plant growth and establishment. Tall-form Spartina alterniflora growth was reported to be stimulated by the presence of the ribbed mussel Geukensia demissa (Bertness, 1984). An increase in soil nitrogen levels in mussel beds is thought to be responsible for this increase in plant growth. Fiddler crab (Uca pugnax) density significantly influenced an increase in biomass production in Spartina alterniflora (Bertness, 1985). Reduction in fiddler crab density decreased aboveground biomass production by 47%. Burrows made by fiddler crabs changed the physical environment by increasing soil drainage, soil oxidation-reduction potential, and decomposition of below-ground plant debris (Bertness, 1985). In most instances of facilitation there was an amelioration of edaphic conditions, including a reduction in both flooding and salinity stress that permitted less tolerant species to establish. Positive interactions among species could play a significant role in determining the species composition of zonal salt marsh communities (Bertness & Hacker, 1994).

Studies of interspecific competition in the laboratory have demonstrated that the relative salt tolerance of halophytes is a significant factor in determining their success in competition with glycophytes or less tolerant halophytes under saline conditions. Halophytes are reported to be more competitive under saline conditions and less competitive in nonsaline conditions (Cords, 1960; Wilson, 1967; Goldsmith, 1973; Szwarcbaum & Waisel, 1973; Gray & Scott, 1977; Barbour, 1978; Ungar et al., 1979; Suehiro & Ogawa, 1980; Badger & Ungar, 1990; Kenkel et al., 1991). The degree of competitiveness of Poa pratensis, Hordeum jubatum, and Puccinellia nuttalliana was shown to be directly related to their level of salt tolerance (Kenkel et al., 1991). The glycophyte Poa pratensis was the strongest competitor in nonsaline conditions, while the most salt-tolerant of these species, Puccinellia nuttalliana, was the most successful species at higher salinities (Fig. 2). Kenkel et al. (1991) were able to demonstrate a negative relationship between the competitiveness of species and their level of tolerance to salt stress, with the most salt-tolerant species P nuttalliana being the least competitive in freshwater conditions. Badger and Ungar (1990) reported that salt stress was an overriding factor in determining seedling dry mass of Hordeum jubatum. However, H. jubatum dry mass production was inhibited by Atriplex prostrata in 0.5% NaCl but not in 0% and 1% NaCl. Conversely, the dry mass production of A. prostrata seedlings was inhibited by H. jubatum in 0% and 0.5% NaCl but not in the 1% NaCl treatment. These data indicate that A. prostrata distribution may be limited by competition with H. jubatum in less saline environments and that salt stress may be the primary factor limiting H. jubatum recruitment in more saline habitats. Rahman and Ungar (1994) determined that the distribution of Echinochloa crus-galli on a saline pond border was limited by salinity stress in the lower high-salinity zone and by competition with Atriplex prostrata in the upper low-salinity zone. Mean biomass of E. crus-galli decreased to 66% of controls in the presence of Atriplex triangularis at a 3:1 ratio in a replacement series (Table II). Laboratory experiments indicated that salt stress was inhibitory to E. crus-galli, which had an 83% decrease in dry mass between the 0% controls and the 1.0% NaCl treatment (Table III).

[Figure 2 ILLUSTRATION OMITTED]

Table II Effect of interspecific competition under field conditions between Echinochloa crus-galli and Atriplex triangularis on mean ([+ or -] S.E.) shoot, reproductive, and total shoot dry mass of E. crus-galli under field conditions (adapted from Rahman & Ungar, 1994).
Density Shoot

4 Echinochloa crus-galli (EC) 5.2 [+ or -] 0.40(c)
3 EC + 1 Atriplex prostrata (AP) 3.8 [+ or -] 0.77(b),(c)
2 EC + 2 AP 2.5 [+ or -] 0.53(a),(b)
1 EC + 3 AP 1.3 [+ or -] 0.47(a)

 Dry mass (g/plant)
Density Reproductive

4 Echinochloa crus-galli (EC) 1.2 [+ or -] 0.34(a)
3 EC + 1 Atriplex prostrata (AP) 1.2 [+ or -] 0.18(a)
2 EC + 2 AP 0.9 [+ or -] 0.22(a)
1 EC + 3 AP 0.9 [+ or -] 0.02(a)

Density Total

4 Echinochloa crus-galli (EC) 6.4 [+ or -] 0.47(b)
3 EC + 1 Atriplex prostrata (AP) 5.0 [+ or -] 0.82(b)
2 EC + 2 AP 3.4 [+ or -] 0.71(a)
1 EC + 3 AP 2.2 [+ or -] 0.07(a)


Note: Means in a column followed by the same letter are not significantly different at P < 0.05.

Table III The effect of interspecific competition under different salinity levels on the mean ([+ or -] S.E.) dry mass of shoots of Echinochloa crus-galli (adapted from Rahman & Ungar, 1994).
 Dry mass (g/plant)

Density 0% NaCl

4 Echinochloa crus-galli (EC) 3.1 [+ or -] 0.22(a)
3 EC + 1 Atriplex prostrata (AP) 3.4 [+ or -] 0.01(a)
2 EC + 2 AP 2.7 [+ or -] 0.34(a)
1 EC + 3 AP 2.8 [+ or -] 1.04(a)

 Dry mass (g/plant)

Density 0.5% NaCl

4 Echinochloa crus-galli (EC) 1.6 [+ or -] 0.51(b)
3 EC + 1 Atriplex prostrata (AP) 1.0 [+ or -] 0.09(b)
2 EC + 2 AP 1.9 [+ or -] 0.53(b)
1 EC + 3 AP 1.6 [+ or -] 0.30(b)

 Dry mass (g/plant)

Density 1.0% NaCl

4 Echinochloa crus-galli (EC) 0.5 [+ or -] 0.17(c)
3 EC + 1 Atriplex prostrata (AP) 0.9 [+ or -] 0.24(b)
2 EC + 2 AP 0.6 [+ or -] 0.14(c)
1 EC + 3 AP 0.6 [+ or -] 0.17(c)


Note: Means in a column followed by the same letter are not significantly different at P < 0.05.

Clarke and Hannon (1971) concluded that both physical factors of the environment and competition interacted to determine the zonational pattern of salt marsh communities in the Sydney District, Australia. Arthrocnemum australasicum is a very salt tolerant species that occurred mainly in a zone between the seaward Avicennia marina and the landward Juncus maritimus zones, but apparently it did not invade in either of these directions. Competition for light inhibited the invasion of the high-light requiring Arthrocnemum perenne into both of these zones of taller vegetation, because shading by the taller species limited its biomass production. Rabinowitz (1978) and McKee (1994) determined that reproductive propagule size and dispersal were important factors in determining plant distribution in mangrove communities. Species growing in deeper water had larger and heavier reproductive propagules than those found on higher ground (Rabinowitz, 1978).

Barbour (1978) determined from competition experiments carried out in the laboratory that the halophyte Jaumea carnosa did not compete successfully with the glycophyte Lolium perenne in freshwater conditions, but it was not inhibited by competition with the latter in the high-salinity treatment. He concluded that halophytes would be restricted in nature to saline habitats because of their inability to compete with glycophytes on nonsaline soils. Highest germination percentages of halophyte seeds sewn on abandoned salt marshes in the Netherlands occurred in freshwater areas (Bakker et al., 1985). Although seeds of halophytes germinated well in glycophyte communities, the salt-tolerant species were unable to compete and did not survive. Bakker et al. (1985) concluded that upper salt marsh and dune species could not establish in the lower salt marsh because of their low salt tolerance and that low marsh species had the potential to invade the upper marsh since they make optimal growth in less saline habitats, but were absent from these habitats because they did not compete well with glycophytes and facultative halophytes. Zedler et al. (1990) determined that in Australian salt marshes Juncus kraussii was more salt tolerant than Typha orientalis at all stages of its life cycle. Mixed cultures of these two species indicated that Typha outcompeted Juncus in freshwater conditions but that at 0.5% salinity Juncus was the better competitor. They concluded that Typha had a narrow regeneration niche and that it could invade Juncus stands only following a reduction in salinity and a disruption of the native vegetation. Typha domingensis also dominated high-fertility and high- water level habitats in wetlands on the Yucatan peninsula, where it outcompeted other, more salt-tolerant species (Rejmakova et al., 1996).

Biomass production of seedlings of the mangrove Avicennia germinans was reduced about 50% in mixed competition treatments when growing with Spartina alterniflora under permanently flooded greenhouse conditions in comparison to controls in pure stands (Patterson et al., 1993). Survival of field transplants of A. germinans after 184 days in the field varied with the different vegetation zones; 75% survival in the Avicennia zone, 81% survival in the High Spartina zone, and 44% survival in the Low Spartina zone in unclipped plots, and 50%, 12%, and 0% survival, respectively, in plots in which the surrounding vegetation was clipped. Mechanical damage by tidal action may have caused higher mortality in clipped plots when the protection from Spartina was removed (Patterson et al., 1993). After 27 weeks the seedling biomass was reduced by [is greater than] 50% in the Spartina zone compared with transplants in the Avicennia zone. Patterson et al. (1993) concluded that, for the period studied, A. germinans could withstand flooding but that both physicochemical conditions and competition might prevent A. germinans from establishing in the Spartina zone over time.

Changes in soil salinity along environmental gradients may alter the competitive ability of halophytes and affect their distribution in salt deserts. Mahmood et al. (1993) reported that biomass production of Leptochloa fusca was reduced 70% by Suaeda fruticosa in high-salinity treatments (16.1 dS/cm) but was not reduced at low salinity (6.1 dS/cm). Cynodon dactylon inhibited L. fusca dry mass production at low salinity and had less of an inhibitory effect at high salinity. They concluded that competition for nutrients at high salinities may explain the competitive success of S. fruticosa over L. fusca in salt desert habitats. Both Paspalum paspalodes and Aeluropus littoralis form monospecific stands in the Camargue region of France (Mesleard et al., 1993). A replacement series investigation carried out in the laboratory at different salinities indicated that P. paspalodes was the better competitor under non-saline conditions when grown in mixed cultures with A. littoralis. However, the reverse was true in saline conditions, where A. littoralis proved to be the better competitor. Aeluropus littoralis growth was not inhibited in up to 6 g Cl/L, whereas P. paspalodes was strongly inhibited by salinity of 2 g Cl/L and also by competition with A. littoralis at all salinity concentrations. Mesleard et al. (1993) concluded that the salt concentration of the habitat could be used to predict those habitats in which the two species could not grow, but because of competitive effects it could not predict where they would be found in nature.

After eight years (1983-1991) of fertilization, the early successional seagrass Halodule wrightii made up 87% of the plant biomass in Florida Bay, replacing monocultures of Thalassia testudinum (Fourqurean et al., 1995). Interpretation of the results of this study varied with time, since during the first two years of this experiment the later successional species T. testudinum dominated, but after eight years of fertilization it was almost completely replaced by the earlier successional species H. wrightii. Fourqurean et al. (1995) concluded that T. testudinum was the better competitor for nutrients and grew well at low nutrient levels but that H. wrightii was a better competitor for light, and that it was the successful competitor under high-nutrient conditions when it was not nutrient limited by T. testudinum. Long-term field experiments may also provide us with conclusive evidence of the significance of competition for nutrients and light in salt marsh and salt desert habitats.

New England salt marshes have a characteristic zonational pattern, with the low marsh dominated by Spartina alterniflora, high marsh by Spartina patens, and upper marsh border by Juncus gerardi (Bertness & Ellison, 1987). Edaphic physicochemical factors vary along the elevational gradients on these marshes, tidal flooding is more prevalent, salinities are higher, and redox potentials are more negative in the low marsh than in higher elevations on the salt marsh border. Bertness and Ellison (1987) determined that disturbance bare patches were formed on the high marsh due mainly to deposition of wrack. Wrack burial led to differential plant mortality, with Distichlis spicata and Salicornia europaea being more tolerant of burial than were the dominant graminoids of the high marsh. Field observations in the Spartina patens zone indicated that after two years the wrack disturbance patches had about 25% Distichlis spicata cover, 40% Salicornia europaea cover, 6% Spartina alterniflora cover, and 40% Spartina patens cover. By the third year the cover of the early invaders decreased to about 18% for D. spicata and 10% for Salicornia europaea, while Spartina alterniflora cover remained at about 6%, and Spartina patens cover increased to [is greater than] 90% in patches on the S. patens zone. A similar pattern was found in wrack disturbance patches in the Juncus zone, with Distichlis spicata cover decreasing from 50% to 10%, Salicornia europaea cover decreasing from 13% to 1%, and Juncus gerardi cover increasing from 60% to 95% between the second and third year of patch revegetation (Bertness & Ellison, 1987). Bertness and Ellison (1987) concluded from transplant experiments that Spartina alterniflora grew well in all marsh zones and that it was prevented from growing on the high marsh because of competition from the turf-forming species Spartina patens and Juncus gerardi. Physicochemical factors inhibited the growth of S. patens in the low marsh zone. The marsh border Juncus zone was a favorable habitat for Spartina alterniflora, S. patens, and Distichlis spicata biomass production, but competition with Juncus probably prevented these species from establishing in this marsh border zone. Ellison (1987) determined that the annual Salicornia europaea was usually limited to disturbance generated patches on the Rumstick Cove salt marsh. Eventually grasses such as Distichlis spicata and Spartina alterniflora would outcompete it for light resources and replace Salicornia europaea. Artificial shading experiments indicated that diffuse competition was limiting the growth and distribution of S. europaea. Diffuse competition indicates that all of the graminoids had equivalent inhibitory effects on the growth and survival of S. europaea. Other factors, including disturbance, seed dispersal patterns, and herbivory affected the growth and distribution of S. europaea on these salt marshes (Ellison, 1987).

Disturbances in salt marshes often result in unvegetated salt pannes. Loss of vegetation may be due to tidal deposition of wrack and deposition or removal of silt in various salt marsh zones (Runge, 1972; Redfield, 1972; Bertness & Ellison, 1987; Hartman, 1988; Valiela & Rietsma, 1995; Allison, 1995). Revegetation of bare areas may be from the establishment of new seedlings or by vegetative invasion of graminoids (Redfield, 1972; Allison, 1995). Allison (1995) determined that seedling establishment was rare and that reproduction in California salt marshes was mainly by vegetative growth into bare patches or by growth of buried plants up through the sediment. Disturbance caused by flooding and sediment deposition in highly saline soils of the coastal salt marshes at Bolinas Lagoon, Marin County, California, inhibited seed germination and plant growth (Allison, 1996). However, reduced salt stress allowed some seedlings to survive, and rapid establishment of the halophytes Salicornia virginica, Frankenia grandifolia, and Distichlis spicata occurred with clonal growth. Salicornia virginica is the most salt tolerant of these species, but in 1989, a year of high rainfall during March, other species increased in growth and cover relative to Salicornia virginica. Perennial halophytes in these salt marshes are dependent upon freshwater flooding or periods of increased precipitation for their successful establishment in disturbed areas (Allison, 1996). Similar results have been reported for revegetation of bare areas produced by disturbance in New England salt marshes (Redfield, 1972; Hartman, 1988). Redfield (1972) observed seedling establishment only in bare areas raised up sufficiently by silt deposition. Lower areas that were more affected by tidal deposition and scarification had no successful invasion of Spartina alterniflora. Salt marsh communities are resilient because of the relatively rapid revegetation of bare disturbance patches by rhizomatous growth of graminoids (Redfield, 1972; Hartman, 1988).

Silander and Antonovics (1982) determined from removal experiments that interspecific competition among salt marsh species were both specific and diffuse. Removal of Spartina alterniflora from low marsh communities resulted in an increase in yield for the associated species Spartina patens, Limonium carolinianurn, and Aster spp. but not Fimbristylis spadiceae, whereas the removal of Spartina patens did not result in a significant increase in the yield of Spartina alterniflora, Aster sp., or Limonium carolinianum. Plant species composition changed gradually along an elevational gradient on the Tijuana estuary in southern California. Zedler (1977) found that the distribution of the low marsh dominant Spartina foliosa, which was replaced by Salicornia virginica along the gradient, could be limited to the lowest elevation because of competition with Salicornia. Competition with Batis rnaritima and Salicornia bigelovii in the middle of its range could be the cause of the bimodal distribution of S. virginica. Covin and Zedler (1988) also reported that competitive effects between species were not reciprocal in removal experiments that they carried out in salt marsh communities on the Tijuana estuary. Removal of Salicornia virginica from mixed stands resulted in an increase in Spartina foliosa. However, Spartina removal from mixed stands did not cause a reciprocal increase in Salicornia biomass.

Bertness (1991a) determined that the removal of either Distichlis spicata or Spartina patens from a Rhode Island salt marsh facilitated dry mass production (19-38%) and tiller production (20-30%) in the remaining species. However, Juncus gerardi production was not stimulated by the removal of D. spicata and S. patens, even though its removal stimulated (28-67%) the biomass production of the latter species. Transplants of D. spicata were suppressed (64%) by S. patens and or. gerardi. Transplants of S. patens were suppressed by the other species, whereas dry mass of J. gerardi transplants increased in the S. patens zone. On the upper marsh border the less salt- and flooding-tolerant but more competitive Juncus gerardi replaced the other graminoids because it initiated growth earlier in late February, whereas other species began growth in late May. The lower limit of Spartina patens distribution on the marsh was restricted by the competitive dominance of Spartina alterniflora and the high frequency of flooding in the low marsh habitat (Bertness, 1991a, 1991b). Distichlis spicata recruitment, the most salt tolerant of these species, is favored by disturbance because of the long rhizomes it produces, whereas the better competitors Spartina patens and Juncus gerardi formed dense turfs (Bertness & Ellison, 1987; Brewer & Bertness, 1996). Invasion of hypersaline gaps by D. spicata is facilitated by physiological integration with ramets located in less saline and more moderate environmental conditions, which gives it an advantage over the species that produce turfs (Brewer & Bertness, 1996). Transplants of S. patens to the low marsh were inhibited by the flooding and anoxic conditions of the low marsh in the presence or absence of the dominant S. alterniflora (Bertness, 1991b). However, S. alterniflora transplants grew well in the high marsh when transplanted into plots without S. patens, but its growth was significantly inhibited in the presence of S. patens. Spartina alterniflora is able to persist in anoxic low marsh soils, but it was competitively excluded from the high marsh by S. patens. Similar results were found in coastal salt marshes of southeast Spain in which Arthrocnemum perenne plants in higher areas were better competitors for well-aerated soils on raised areas than was the primary invader of low marsh soils, Spartina maritima (Castellanos et al., 1994). Spartina maritima was the primary invader of bare mud flats and produced raised hummocks on the Odiel salt marsh (Spain). With the better drainage and aeration on these hummocks, A. perenne was able to establish in the higher microelevations where S. maritima clones were degenerating. Arthrocnemum perenne shades the [C.sub.4] species S. maritima, which eventually replaces the former species completely by impeding its growth through both root and shoot competition for resources (Castellanos et al., 1994). Reciprocal transplant experiments to various levels of a New Zealand marsh also indicated that the salt tolerance of species was a critical factor determining success in lowest sites on salt marshes, but that interspecific competition limited the distribution of halophytes when they were competing with glycophytes in nonsaline habitats (Partridge & Wilson, 1988). These field data support other investigations that indicated a reciprocal relationship between a species' tolerance to salt stress and the competitive ability of that species in nonsaline or low-salinity habitats (Ungar et al., 1979; Kenkel et al., 1991).

IV. Allelopathy

Waisel (1972) indicated that little information is available concerning the effects of competition and allelopathy on the growth and distribution of halophytes. The sharp zonational boundaries found in many halophyte communities indicates that either abiotic stress levels are changing precipitously or that some form of biotic inhibition may be limiting seed germination, growth, and distribution of species in the various salt marsh and salt desert zonal communities.

Saxena (1994) indicated that an allelopathic inhibitor in Indian populations of Prosopis juliflora prevented the germination of other species. The distribution of Suaeda fruticosa may be limited by either an allelopathic inhibitor produced in the leaves of P. juliflora, or because of its large crown diameter that shades out other species. I could only find one other reference which examined the possibility that allelopathy might play a significant role in determining species composition in saline habitats. Mahmood et al. (1989) investigated the influence of six competitors on seed germination and growth of Leptochloa fusca in saline soils of Pakistan. Aqueous extracts of shoots of other species were found to decrease seed germination percentages of L. fusca: reductions from control values in extracts were Suaeda fruticosa (80%), Kochia indica (42%), Sporobolus arabicus (38%), and Polypogon monspeliensis (29%). Autoallelopathy was also determined to be significant, in that 5% shoot extracts of L. fusca caused a 50% reduction in the germination of its own seeds. Decaying shoot material of invading species caused reductions from the control in L. fusca shoot dry mass, ranging from 18% (Suaeda fruticosa) to 69% (Polypogon monspeliensis). Autoallelopathy also occurred, with L. fusca litter decreasing yields to 39% of control values (257.5 mg/plant).

No investigations have reported the effects of allelopathy on the growth or distribution of salt marsh species from temperate climates. This may be due to the fact that it is very difficult to distinguish competitive from allelopathic effects from one another and there is also the problem of resolving these effects in highly saline habitats. It is also difficult to separate the effects of an allelopathic compound from that of salt accumulation in plant tissues, which could cause an osmotic inhibition or specific ion toxicity to seed germination or growth of the target species. However, future efforts should be made to determine if allelopathy is a significant factor in determining the distribution of species in saline habitats.

V. Chemical Inhibition

Accumulation of inorganic elements by halophytes may in itself be inhibitory to other species, because as plant parts senesce, more highly saline conditions may occur in the vicinity of these salt-accumulating species than in the surrounding vegetation. Fireman and Hayward (1952) demonstrated that soils beneath the salt-accumulating halophyte Sarcobatus vermiculatus in the Escalente Desert, Utah, were much higher in exchangeable [Na.sup.+] percentage than under Artemisia tridentata or in the surrounding soils that were unvegetated (Table IV). Mean values for the surface 5 cm were 41.3% beneath S. vermiculatus, 2.6% beneath A. tridentata, and 3.2% exchangeable [Na.sup.+] in bare soil between plants. They also determined that the crown diameter of S. vermiculatus was directly correlated with exchangeable [Na.sup.+] percentages in the soil, ranging from 8% for a plant with a 15 cm diameter to 59.8% in plants with a 127 cm crown diameter. These high exchangeable [Na.sup.+] percentages would inhibit the establishment of intolerant species in these communities through two factors: first, a specific ion toxicity caused by high [Na.sup.+] concentrations; second, nutrient deficiencies caused by the replacement on clays of essential macronutrient cations such as [Ca.sup.2+] and [Mg.sup.2+] by [Na.sup.+].

Table IV Percent of exchangeable sodium under shrubs in soil profiles in the Escalante Desert, Utah (adapted from Fireman & Hayward, 1952).
Sample depth Artemisia Bare ground Sarcobatus
 (cm) tridentata vermiculatus

 0-5 2.6 3.2 41.3
 5-15 2.9 2.5 33.9
 15-40 3.7 2.0 26.7
 40-63 8.9 8.5 26.5
 63-80 14.4 19.7 30.2


Vivrette and Muller (1977) investigated the invasion of Mesembryanthemum crystallinum in coastal California grasslands to determine whether biotic or abiotic factors were most significant in its successful establishment. They found that inhibition of grasses such as Festuca megalura was most significant under newly dried M. crystallinum plants. Soil osmotic potentials ranged from [is less than] 25 milliosmols in grassland to 125 milliosmols in the M. crystallinum sites, indicating that M. crystallinum is a salt-accumulating species. Isotonic equivalent extracts of M. crystallinum shoots, NaCl, and mannitol equally inhibited radicle growth of F. megalura. The inhibitory effect of the lowered soil osmotic potential could explain the inability of grassland species to invade areas containing M. crystallinum. Growth of grass seedlings was significantly inhibited by [is greater than] 100 milliosmols, whereas M. crystallinum seedlings were not inhibited at this concentration.

VI. Herbivory

Herbivory has been reported to both increase and decrease species richness in salt marshes (Adam, 1990; Bakker & de Vries, 1992). Both mowing and grazing were found to cause a change in the relative cover of species and species composition of communities on salt marshes in the Netherlands (Bakker, 1978). Species richness increased in both the Festuca rubra/Limonium vulgare and Juncus maritimus communities when they were mowed or grazed. Grazing opened up gaps in the salt marsh vegetation and allowed both annuals and perennials from the low marsh to establish higher up on the marsh. Salinity content of the soil decreased more in the control area than in the grazed and mowed areas (Bakker & Ruyter, 1981). Bakker (1985) reported that grazing caused a reversal of succession and that mid-salt marsh zones changed to lower salt marsh with grazing. He hypothesized that because of an increase in bare areas, lower marsh species invaded mid marshes, and species richness after 10 years increased in the mid- and upper-salt marsh zones from a mean of 7-12 species in grazed marshes versus a mean of [is less than] 5 species in ungrazed marshes.

Jerling and Andersson (1982) reported that cattle were selective in their grazing of species in a Baltic seashore meadow. They determined that grazing reduced the production of seeds but increased seedling survival in Plantago maritima. Selective herbivory by feral horses is suggested to be a significant factor in determining the competitive success of grasses Spartina alterniflora and Distichlis spicata in Maryland salt marshes (Furbish & Albano, 1994; Table V). Their observations from exclosure treatments and examination of fecal material indicated that S. alterniflora cover decreased with grazing because it was a selectively grazed by horses, while the less desirable D. spicata was not grazed and its coverage increased. Therefore, grazing pressure can significantly influence the competitive success of species and alter the relative abundance and biomass of species in salt marsh zones. Taylor et al. (1997) determined, with the use of exclosure fences, that competition and facilitation could not be detected in the presence of intense herbivory along a salinity gradient. Herbivory reduced the biomass production of species by 75%. In the absence of herbivory Spartina alterniflora was the most successful competitor on the mesohaline site, whereas the biomass of Panicum virgatum was reduced by 60% in the presence of competitors at this location. The biomass of Spartina patens was strongly reduced ([is greater than] 75%) in the presence of competitors at the freshwater and oligohaline site, but yield was facilitated at the mesohaline location. The inhibitory effects of competition increased with increasing salinity for P. virgatum, whereas the effects of competition on S. patens was reduced with an increase in salinity (Taylor et al., 1997).

Table V Percent of change in plant cover after two growing seasons' exposure to simulated preferential and nonpreferential heavy grazing pressure on Spartina alterniflora (adapted from Furbish & Albano, 1994).
 Control

Spartina alterniflora 33.7 [+ or -] 5.1(a)

Distichlis spicata 50.0 [+ or -] 8.8(a)

 Preferential grazing

Spartina alterniflora 3.3 [+ or -] 1.5(b)

Distichlis spicata 75.2 [+ or -] 6.0(a)

 Nonpreferential grazing

Spartina alterniflora 14.2 [+ or -] 2.3(b)

Distichlis spicata 19.6 [+ or -] 6.6(b)


Similar to the species composition of British marshes in South Wales (Adam, 1990), the heavily grazed salt marshes of northern Germany (10 sheep/ha) were dominated by the perennial grass Puccinellia maritima and annuals Suaeda maritima and Salicornia europaea (Kiehl et al., 1996). Two perennial species, Halimione portulacoides and Aster tripolium, became rare on these marshes when they were exposed to heavy grazing. Plant height was only 7.5 [+ or -] 1.2 cm in heavily grazed areas (10 sheep/ha), 9.5 + 0.8 with 3 sheep/ha, 19.3 + 3.8 em with 1.5 sheep/ha, and 17.9 [+ or -] 4.6 cm in ungrazed areas. After four years without grazing, the cover of Festuca rubra, Aster tripolium, and Halimione portulacoides increased, and cover of P. maritima, Suaeda depressa, and Salicornia europaea decreased. Kiehl et al. (1996) concluded that grazing caused an upward shift of zonation boundaries between lower-, mid-, and upper-salt marsh vegetation. Increased salinity and soil compaction, because of grazing and trampling, opened up the higher areas of the marshes in Germany and the Netherlands for invasion by lower marsh species (Bakker, 1985; Kiehl et al., 1996). Gaps produced in marsh vegetation by grazing animals were the most significant factor determining the establishment of annual species since the more competitive perennial species were absent (Jensen, 1985; Ellison, 1987; Gibson & Brown, 1991; Bakker & de Vries, 1992; Kiehl et al., 1996).

Bakker (1985) determined that the species richness of the mid- and upper marsh between 1971 and 1981 increased with grazing (13 species) compared to mowing (9 species) or untreated salt marshes (2 species). A Festuca rubra turf developed on the high marsh in ungrazed Dutch salt marshes. Cattle grazing provided the bare patches necessary for the invasion of new species and accounted for the increase in species richness in mid- and upper marsh locations (Bakker, 1985). Salt marshes in Denmark that were grazed for hundreds of years are dominated by Puccinellia maritima (Jensen, 1985). Six years after exclosures were established, P. maritima cover decreased from 40% to 5%, whereas the percent cover of a rubra and Halimione portulacoides increased. Trampling by animals and the accompanying compaction of the soil both have a negative effect on Halimione portulacoides, Limonium vulgate, and the annuals Suaeda maritima and Salicornia europaea. Grazing retards plant succession from the Puccinellia community to the Halimione community stage and maintains a community dominated by P. maritima and Salicornia europaea in Danish salt marshes (Jensen, 1985). Similar effects of grazing were reported by Ranwell (1972) and Adam (1990) for British salt marshes. They determined that sheep grazing prevented the invasion of F. rubra and maintained a P. maritima community near the upper limit of its distribution by reducing litter accumulation and compacting the soil, which held the marsh at a microtopographic level and successional stage that was suitable for P maritima growth.

Both edaphic factors and sheep grazing influenced the species composition of shrubland communities in saline soils in Western Australia (Hacker, 1987). The density of species such as Aizoon quadrifidum, Atriplex vesicaria, and Maireana pyramidata decreased with grazing, while other species such as Eremophila maculata and E. delisseri increased in density. Hacker (1987) hypothesized that grazing pressure might be reduced in the most highly saline habitats, which are degraded less, because sheep avoided plant species that contain a high leaf salt content.

Cattle grazing in the salt desert shrublands of Utah inhibited plant growth, causing a change in species composition and a retrogression in the process of plant succession (Whisenant & Wagstaff, 1991). These salt desert communities are dominated by shrubs, including Ceratoides lanata, Artemisia spinescens, Atriplex confertifolia, and Chrysothamnus viscidiflorus. There was an increase in the number of annual species in grazed plots, and the season of grazing played a significant role in determining the direction of successional change. Spring grazing, when shrubs are actively growing, is reported to be the most damaging for plants. These data agree with the results from salt marsh investigations that indicate both a zonational and temporal shift in species composition of plant communities because of grazing (Bakker, 1985; Kiehl et al., 1996). Chambers and Norton (1993) found that A triplex confertifolia was able to reproduce in heavily grazed pastures but that its mortality was very high during drought periods. Heavy grazing during periods of drought had a very negative effect on plant survival.

Grazed upland and lowland sites of flooded pampa grassland in Argentina had higher soil specific conductance than did ungrazed sites (lowland = 3.9 dS/m vs. 1.0 dS/m, upland = 6.9 dS/m vs. 0.8 dS/m; Chaneton & Lavado, 1996). They concluded that increased soil salinity in plots grazed by cattle was due to a reduction in both aerial plant cover and litter cover that caused an increase in evaporation from the exposed soil surface and also an increase in soil salinity.

Because lesser snow geese (Anser caerulescens) uproot vegetation and consume roots and rhizomes, the rate at which plant cover is lost in marshes occupied by this species is increasing (Cargill & Jefferies, 1984; Srivastava & Jefferies, 1995; Miller et al., 1996). Long-term records of emergent marshes on the San Bernard National Wildlife Refuge in Texas indicated that 95% of the marsh was continuously covered with vegetation and 4% sparsely vegetated in 1939. Little change occurred in the amount of unvegetated area ([is less than] 2%) until 1965, but there was a 17% increase in unvegetated area by 1991. Goose abundance ranged from 50,000 to 100,000 from 1972 to 1975, but increased to 152,000 in 1981. Large areas of the salt marshes dominated by Distichlis spicata and Spartina patens are used for feeding by geese. Vegetation loss accelerated in 1982-1983, but goose abundance remained high even though there was a loss of plant biomass. Persistent unvegetated mudflats replaced emergent salt marsh vegetation in areas of intense use by geese. Cattle grazing and abiotic stress may also have contributed to the decrease in plant coven Loss of salt marsh vegetation in areas highly used by geese is caused by prolonged tidal flooding, soil erosion, and higher salinities that prevent seedlings from establishing and result in the death of plant rhizomes (Miller et al., 1996).

Mulder et al. (1996) determined that geese may affect the distribution of Triglochin maritima in salt marshes of southwestern Alaska. Factors affected by geese such as fertility, light, and soil salinity were investigated. Increased nutrient availability negatively affected T. maritima, indicating that goose feces probably would be more beneficial to competitors and cause a reduction in light available to T. maritima. However, an increase in disturbance of the vegetation because of the activity of geese would reduce competition and increase light availability for T. maritima. They concluded that the effects of fertilization may be negative to the smaller T. maritima in communities where it is a preferred forage species and less abundant in comparison to the more dominant species (Puccinellia phryganodes and Carex spp.). This is because increased fertilization would favor the more robust and abundant dominants by increasing the level of interspecific competition for light and nutrients (Mulder et al., 1996).

Puccinellia phryganodes is the primary colonizer of salt marshes in arctic North America (Jefferies, 1977), with Carex subspathacea increasing in the upper portion of this zone at La Perouse Bay (Jefferies et al., 1979). Srivastava and Jefferies (1995) determined from direct measurements of change in biomass production that lesser snow geese progressively destroyed salt marsh vegetation and produced soil conditions that were unfavorable to plant growth. At La Perouse Bay, Manitoba, the population of geese grew from 2000 to 23,000 breeding pairs between 1968 and 1992. Ungrazed salt marsh plots had about 40 g/[m.sup.2] greater biomass than did grazed plots. Evaporation from the soil surface is reduced by the presence of vegetation and organic litter. Loss of both plant cover and organic litter caused an increase in both the evaporation rate at the soil surface and soil salinity content (Cargill & Jefferies, 1984; Iacobelli & Jefferies, 1991; Bertness et al., 1992). Srivastava and Jefferies (1995) determined that evaporation rates on grazed salt marshes increased from 28% to 155% over those in vegetated salt marsh areas at La Perouse Bay. High biomass sites had soil salinities in July 1992 of 0.6%, while bare areas averaged 2% total salts. Soil salinities were 33% lower in the ungrazed exclosure versus grazed plots, and increases in plant biomass were found to be significantly negatively correlated to soil salinity concentrations. They determined that reductions in above-ground biomass caused by heavy grazing by geese led to an increase in soil salinity (Srivastava & Jefferies, 1995).

Bazely and Jefferies (1986) reported that removal of lesser snow geese by exclosures caused an increase in species richness from 6 to 16 species in the ungrazed salt marsh plots after 5 years. The graminoid Puccinellia phryganodes was replaced as the dominant by Carex subspathacea. Increased soil salinity because of grazing by geese would have a negative effect on the less salt-tolerant species by either reducing the species richness of communities or causing changes in the relative species composition of marsh communities. Cargill and Jefferies (1984) found that both Puccinellia phryganodes and Carex subspathacea were selectively grazed and replaced on grazed sites by other species, including Calamagrostis neglecta, Potentilla egedii, Ranunculus cymbalaria, and Plantago maritima. Geese activity produced pools in heavily grazed areas, whose margins are invaded by Carex glareosa, C. aquatilis, Triglochin maritirna, and Potentilla egedii (Jefferies et al., 1979).

Esselink et al. (1997) determined that Greylag geese (Anser anser) fed on rhizomes and winter buds of the graminoids Scirpus maritimus and Spartina anglica in tidal marshes in Germany and the Netherlands. There was a decrease in biomass of Scirpus maritimus and an increase in the cover of the annual halophyte Salicornia europaea in plots grazed by Greylags. The cover of Phragmites communis increased 30% in the plots where Scirpus maritimus decreased. Exploitation of juvenile Spartina anglica plants by geese prevented the establishment of this species in bare plots and caused an increase in area with no vegetation. Esselink et al. (1997) hypothesize that the population size of the geese is increasing because of their use of agricultural lands during a part of the year and then subsequent overgrazing the marsh in seasons when agricultural plants are not available.

Flower and seed predation by insects may effect the success of populations of salt marsh species (Bertness et al., 1987). Time of flowering of salt marsh graminoids was a significant factor in determining if mature seeds were dispersed. There was little predation observed on Juncus gerardi flowers before the second week in July, but at the time of dehiscence, 54% of the capsules were destroyed by chewing insects. Spike damage to inflorescences from insects averaged 80% in Spartina patens, 51% in Distichlis spicata, and 68% in Spartina alterniflora. Most of the consumption was due to the grasshopper Conocephalus spartinae which reaches its peak density in mid-summer (Bertness et al., 1987). Insects that consume flowers reduced seed production of salt marsh grasses and the frequency of male flowers (Bertness & Shumway, 1992). Pollen limitation could prevent seed-set even when an ovule was present and thus indirectly limit seed production for some species, which could make other species that are not consumed better competitors for open sites on the marshes.

Salicornia europaea growth and reproductive capacity is influenced by insect herbivory (the beetle Erynephola maritima and larvae of the moth Coleophora spp.). Insect damage to S. europaea was significant in open patches and where the perennial graminoid species Juncus gerardi and Spartina patens were removed, but no damage was observed to Salicornia europaea in the short Spartina alterniflora zone. Damage from moth larvae was more severe to seeds of Salicornia europaea in areas where Juncus gerardi was removed than beneath the graminoid canopy (Ellison, 1987). Feller (1995) concluded that the availability of P was the main factor limiting the growth rate and size of Rhizophora mangle L. plants at Twin Cays, Belize. Increased fertilization led to an increase in the phenolic content of plants, but also there was an unexpected increase in activity of specialized endophyte stem miner herbivores and no decrease in general herbage feeders.

The amphipod Corophiurn volutator could be a significant factor in determining the lower limits of Salicornia europaea distribution (Gerdol & Hughes, 1993). The upper limits of its distribution coincided with the lower limits of S. europaea distribution on British salt marshes. Survival of seedlings was negatively correlated to the presence of the herbivore Corophiurn volutator. When insecticide was sprayed on plots, 64% of S. europaea seedlings survived compared to only 33% in the control plots. Prevention of establishment of S. europaea populations by the amphipod C. volutator may be due to seed burial or disturbance of the sediment. They concluded that besides the negative effects of tidal action, the infauna of mud flats may reduce soil stability, increase the rate of erosion, and prevent the normal successional process on mud flats from developing salt marsh vegetation (Gerdol & Hughes, 1993).

VII. Parasitism

Parasites may preferentially attack one salt marsh species rather than another and therefore affect the species composition of zonal salt marsh communities. The preferred host of the parasitic flowering plant Cuscuta salina in the Carpinteria salt marsh of California is Salicornia virginica in the high-Salicornia zone (Pennings & Callaway, 1996). Other species, including Frankenia salina, Lirnoniurn californica, and Arthrocnernurn subterminale, are parasitized by Cuscuta, but at much lower rates. Uninfected control areas of the marsh are dominated by Salicornia, while recently infected areas of the high-Salicornia zone are characterized by Frankenia and Lirnoniurn and contained few individuals of Salicornia. Parasitism of Salicornia by Cuscuta opens up bare unvegetated patches on the marsh, which indirectly facilitates the establishment of the rarer species Lirnoniurn californica and Frankenia salina. Pennings and Callaway (1996) hypothesized that the vegetation cycle from Cuscuta infection of Salicornia to the establishment of rarer species Frankenia and Lirnoniurn took from 1 to 3 years. The probability of Cuscuta invading a stand of vegetation was correlated positively to the percentage cover of Salicornia. The effect of Cuscuta was most pronounced in the high-Salicornia zone, while in the low-Salicornia zone there was little invasion of the rarer species Frankenia and Lirnoniurn. It could be that increased flooding in the lower zone limited the establishment of both Lirnoniurn and Frankenia. Salicornia did not occur in the drier and more saline Arthrocnernurn zone.

VIII. Conclusions

Although physicochemical factors such as flooding, tidal action, and salinity may play a significant role in determining which species establish and survive in zonal plant communities in salt marshes and salt deserts, it will be necessary in future investigations to consider the effect of biotic factors on the formation of plant communities in saline habitats. Factors such as competition, facilitation, allelopathy, chemical inhibition, herbivory, and parasitism all play a significant part, under certain circumstances, in determining whether or not a species can successfully establish itself in saline habitats. Both the upper and lower limits of a species' distribution in salt marshes may be delimited by interspecific competition. Competition may also play a significant role in determining the sharp boundaries between certain salt marsh communities. It has been demonstrated by removal and addition competition experiments in the field that the relative cover and abundance of species within a particular community is determined by competition. There is apparently a reciprocal relation between the salt tolerance of a species and its ability to compete in nonsaline habitats. The most salt-tolerant species often are good competitors on saline soils but are poor competitors with glycophytes in nonsaline habitats. Chemical inhibition, because of sodium accumulation in plant tissues and surface soils surrounding salt-accumulating species, has been shown to limit the establishment of intolerant species in salt desert and mediterranean environments. Little is known about the effects of chemical inhibition in salt marshes. Similarly, allelopathy has been shown to affect the distribution of species in salt deserts, but no investigations have been carried out to determine its influence on the establishment and distribution of salt marsh species.

Herbivory has been shown to influence seed production, growth, and survival of halophytes. The effects of grazing are not clear, since some investigations demonstrated a decrease in species richness and others clearly showed an increase in species richness with grazing. It may be that the intensity of grazing in these different habitats resulted in a different outcome in species richness. Gaps produced in the high marsh by grazing often modify the habitat, by increasing salinity and reducing soil moisture content. This permits annual and perennial species from the low marsh to invade the mid- and high marsh communities. Selective grazing by horses and cattle promoted the establishment of some species but inhibited those that are selected by the grazers. Grazing could also effect a number of environmental variables, including light availability, erosion rates, soil nutrients, moisture, compaction, and salinity. Grazing by geese increased soil nutrient levels, which reduced the competitive ability of smaller and slower-growing species and promoted the establishment of taller species that could take advantage of the raised soil nitrogen levels.

Parasitic flowering plants may determine the species composition in a zonal marsh community. The preferred host will be eliminated and less abundant species could colonize the gaps produced by the death of parasitized plants. Rarer species apparently benefit from the high toll taken by parasites. Little is known about the effects of the microbial parasites on the germination, establishment, and reproduction of halophytes in saline habitats.

There is evidence that competition and herbivory could play significant roles in determining both the species composition of plant communities and the zonational pattern of species along salt marsh and salt desert environmental gradients. Some investigations indicated that allelopathy, chemical inhibition, and parasitism could influence plant establishment in saline habitats. However, although an effect has been demonstrated in salt desert habitats, there is no evidence that allelopathy or chemical inhibition are determining plant distributions in salt marsh environments.

IX. Acknowledgments

I would like to thank the Petroleum Environmental Research Forum and the National Science Foundation for their support of this research. My special thanks goes to my graduate students and research associates who have participated with me in the study of halophyte ecology: David Benner, David McGraw, Jeyarany Philipupillai, Barbara Wertis, William Hogan, Allan Macke, Jira Katembe, Jean Boucaud, Carolyn H. Keiffer, M. Ajmal Khan, Kemuel S. Badger, Jira Katembe, Jackie Adams, Marlis Rahman, Margaret Foderaro, Terrence E. Riehl, Donald Drake, Oblukanla T. Okusanya, Jackie Adams, Karen McMahon, Li-Wen Wang, Todd Egan, and Harold Karimi.

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