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Physiology and Biochemistry |
Environmental Research Laboratory, 2601 East Airport Drive, Tucson, Arizona 85706 USA; 3U.S. Geological Survey, USGS Patuxent Wildlife Research Center, 12100 Beech Forest Road, Suite 4039, Laurel, Maryland 20708-4039 USA; and 4Delaware River Fisheries Coordinator, U.S. Fish and Wildlife Service, 26120 Whitehall Neck Road, Smyrna, Delaware 19977 USA
Received for publication May 5, 2006. Accepted for publication September 29, 2006.
ABSTRACT
An invasive variety of Phragmites australis (Poaceae, common reed), the M haplotype, has been implicated in the spread of this species into North American salt marshes that are normally dominated by the salt marsh grass Spartina alterniflora (Poaceae, smooth cordgrass). In some European marshes, on the other hand, Spartina spp. derived from S. alterniflora have spread into brackish P. australis marshes. In both cases, the non-native grass is thought to degrade the habitat value of the marsh for wildlife, and it is important to understand the physiological processes that lead to these species replacements. We compared the growth, salt tolerance, and osmotic adjustment of M haplotype P. australis and S. alterniflora along a salinity gradient in greenhouse experiments. Spartina alterniflora produced new biomass up to 0.6 M NaCl, whereas P. australis did not grow well above 0.2 M NaCl. The greater salt tolerance of S. alterniflora compared with P. australis was due to its ability to use Na+ for osmotic adjustment in the shoots. On the other hand, at low salinities P. australis produced more shoots per gram of rhizome tissue than did S. alterniflora. This study illustrates how ecophysiological differences can shift the competitive advantage from one species to another along a stress gradient. Phragmites australis is spreading into North American coastal marshes that are experiencing reduced salinities, while Spartina spp. are spreading into northern European brackish marshes that are experiencing increased salinities as land use patterns change on the two continents.
Key Words: brackish marsh • halophyte • invasive species • osmotic adjustment • salinity tolerance • salt marsh
The common reed Phragmites australis (Cav.) Trin. ex Steud (Poaceae) is an emergent grass found in wetlands around the world (Cronk and Fennessy, 2001
). A salt-tolerant (Vasquez et al., 2005
) haplotype of this species was recently discovered and has been implicated in the recent invasion of this species into salt marshes that are normally dominated by the perennial salt marsh grass Spartina alterniflora Loisel (Poaceae) (Saltonstall, 2002
, 2003
; Saltonstall et al., 2004
). The salt-tolerant haplotype was apparently introduced to North America from populations in Eurasia about 100 years ago, and within the past 30 years it has become invasive in the salt marshes of the northeastern United States (Chambers et al., 1999
; Havens et al., 2003
). The extensive spread of P. australis throughout brackish marshes on the Atlantic Coast of the United States has become a major issue with regard to coastal management and restoration (e.g., Able et al., 2003
; Lathrop et al., 2003
; Windham and Myerson, 2003
; Weis and Weis, 2003
).
Most populations of the reed P. australis have low salt tolerance relative to that of the marsh grass S. alterniflora (Glenn, 1987
; Bart and Hartman, 2003
; Burdick and Konisky, 2003
). However, we recently showed that the M haplotype of P. australis has a higher growth rate and greater salt tolerance than native haplotypes, allowing it to become established in Spartina marshes (Vasquez et al., 2005
). The reed rapidly colonizes disturbed sites, where it tends to form monodominant communities in Spartina marshes. The predominance of the reed in Spartina marshes alters biogeochemical and ecological functions of the marsh (Rooth et al., 2003
; Ravit et al., 2003
) and complicates wetland mitigation efforts (Havens et al., 2003
).
An interesting reversal of this replacement process has occurred in some European marshes. There, P. australis is the dominant emergent grass in many coastal and inland wetland systems, but many stands have declined in vigor in recent decades through reed dieback (Van der Putten, 1997
; Folgi et al., 2002
; Poulin et al., 2002
). In many northern European coastal marshes, P. australis has been or is being replaced by Spartina townsendii H. and J. Groves and S. anglica Loisel (Esselink et al., 2000
), both of which originated from the hybridization of the native European marsh grass S. maritima (M.A. Curtis) Fern. with S. alterniflora, which was introduced to Europe from North America in the 1800s (Ranwell, 1964
; Hubbard, 1965
; Ayres and Strong, 2001
). In Europe, the invasion of P. australis marshes by Spartina spp. adversely affects the local marsh ecology and has become a challenge to natural resource managers (Thompson, 1991
; Esselink et al., 2000
).
The key to understanding and managing these ecological replacement processes appears to lie in the relative salt tolerance of invasive and the natural plant populations along salinity gradients. The invasion of the reed into North American salt marshes is associated with salinity reduction from anthropogenic alterations such as redirecting storm runoff into the backwaters of marshes (Bart and Hartman, 2003
; Weis and Weis, 2003
; Silliman and Bertness, 2004
). Similarly, in Europe, where historically reed-dominated salt marshes have been drained to permit cattle grazing, the resulting increase in salinity has facilitated the invasion of Spartina spp. into those areas (Esselink et al., 2000
).
The response of plants to salinity is determined by their general growth characteristics and by their physiological mechanisms of salt tolerance. Two forms of salt tolerance are known for grasses: Na+ exclusion (e.g., Peng et al., 2004
) and Na+ accumulation (e.g., Bell and O'Leary, 2003
). The reed P. australis has been characterized as an excluder that restricts entry of Na+ into the shoots and uses K+ as the main cation for osmotic adjustment in the leaves (Matoh et al., 1988
; Lissner et al., 1999
; Vasquez et al., 2005
). On the other hand, Na+ is the main cation contributing to osmotic adjustment in the salt marsh grass S. alterniflora. This species accumulates Na+ in its shoots, and it secretes excess salts through salt glands onto the leaf surfaces (Bradley and Morris, 1991
). Although grasses are characterized as either excluders or accumulators (Bell and O'Leary, 2003
), even the accumulators exclude >95% of the Na+ in the external medium from entering the shoots in the transpiration stream (Bradley and Morris, 1991
). The key distinction between the groups may be that the so-called accumulators have efficient mechanisms to sequester Na+ in cell vacuoles and excrete excess NaCl onto leaf surfaces. Hence, they can use the controlled uptake of Na+ balanced by organic solutes in the cytoplasm for osmotic adjustment at the cellular level (Glenn et al., 1999
). Although few side-by-side comparisons have been conducted, grasses that exclude Na+ may not have the same degree of salt tolerance as those species that can use Na+ for osmotic adjustment (Glenn et al., 1999
; Hester et al., 2001
; Bell and O'Leary, 2003
).
To determine the potential role that salt tolerance plays in salt marsh invasions, we used replicated greenhouse experiments to examine the growth and physiological mechanisms of osmotic adjustment both of the M haplotype of the reed and of S. alterniflora in response to a salinity gradient.
MATERIALS AND METHODS
Salinity tolerance
We compared the growth of M haplotype P. australis and S. alterniflora plants across a salinity gradient from 0.01 M NaCl to 0.60 M NaCl in greenhouse experiments at the Environmental Research Laboratory (ERL) in Tucson, Arizona, USA. Methods followed those in Vasquez et al. (2005)
, in which native haplotypes of P. australis were compared with the M haplotype used here. We grew plants at seven salinity levels with five replicates per treatment in a randomized complete block design. After 12 weeks of growth, we measured wet and dry masses of rhizomes and shoots of all plants. We conducted an elemental analysis of the belowground and shoot tissues at harvest, and in a separate experiment we measured the osmolality in the roots, rhizomes, and leaves of each species along a salinity gradient.
Origin of plant material
On 28 September 2003, we obtained rhizome sections of P. australis (the invasive M haplotype) from reed populations in Delaware, USA. The population sampled was among those originally sampled by Saltonstall (2002)
, who provided detailed directions by which we located the collection site (K. Saltonstall, University of Maryland, personal communication). The M accession was growing in the Appoquinimink River, in New Castle County, Delaware (39°26.578'N, 75°39.601'W), southeast of Odessa. The site is an oligohaline tidal marsh that drains into the Delaware Estuary. The site is located on the Delmarva Peninsula, on the Atlantic coastal plain. These plants were clonely propagated in pots in a greenhouse at the ERL.
In June 2004, fresh seeds of S. alterniflora were purchased from Environmental Concern, Inc. (St. Michaels, Maryland, USA). The seeds were collected from the Delmarva Peninsula area between the eastern shores of Maryland and Virginia and the western shores of Delaware and then shipped to the ERL. The seeds were rinsed with fresh water to remove salts and then sown into germinating trays and watered with fresh water until germination. Once the initial shoots were about 4 cm in height, they were transferred to 4-L pots and placed under sprinkler irrigation with fresh water and allowed to grow to fill the pots.
Growth experiment
To obtain similar plants for the experimental cultures we transferred 140 small rhizome sections (approximately 5 g each) of both species into 4-L pots containing sand and potting mix, similar to the method we used to initiate the experiment with P. australis haplotypes in Vasquez et al. (2005)
. All rhizome sections had one or more buds from which new shoots emerge. Pots were placed under sprinkler irrigation with fresh water to initiate shoots prior to the salinity treatments. All the P. australis rhizomes sprouted numerous shoots within 60 days; however, only 8% of the S. alterniflora rhizomes developed shoots. Hence, it was not possible to start the experiment with equal masses of rhizome tissue because the species differed markedly in their capacity for shoot initiation from rhizomes.
To circumvent this problem, we propagated rhizome sections that already had initiated shoots by cutting up whole plants into sections containing rhizomes plus shoots. Shoots (1–3 per plant) were trimmed back to 2 cm height, then plants were weighed and planted in pots. Initial fresh masses of S. alterniflora rhizome-shoot sections (3.8 g, SE = 0.3 g) were greater than those of P. australis rhizome–shoot sections (1.8 g, SE = 0.2 g) because S. alterniflora produced fewer shoots per gram of rhizome tissue (see Results).
Rhizome–shoot sections were transferred to 4-L pots containing a 2 : 1 mixture of river-washed sand and peat. Sixty pots of each species were propagated (one plant per pot). The pots were placed under sprinkler irrigation and allowed to grow under fresh water for 30 days. On 11 February 2005 pots were assigned numbers and 35 pots each of both P. australis and S. alterniflora were randomly selected by lot from the newly propagated rhizomes and placed into five randomized blocks, each with 7 pots of each species, along a section of a greenhouse bench. Within each block and species, each plant was further randomly separated into 0 M, 0.09 M, 0.18 M, 0.27 M, 0.36 M, 0.45 M, and 0.54 M NaCl treatment groups (five plants per species per salinity). Stock solutions were based on mass measurements, adding NaCl to municipal water (ca. 250 ppm total dissolved solids). Each pot was then irrigated with one liter of the appropriate salt solution every other day starting 11 February 2005. In addition, each pot was fertilized every other week with Grow More (20-20-20) fertilizer (Grow More, Inc., Gardena, California, USA), which was added to the irrigation solutions to deliver 25 mg · L–1 of N, P, and K to the plants. Plant height was recorded weekly by measuring from the rim of the pot to the tip of the tallest shoot. The number of shoots per pot was also recorded for each species in monoculture and mixture. After 87 days, belowground tissues (roots + rhizomes) and shoots were collected and their fresh mass determined. The samples were then dried to constant mass in a solar drier, and dry mass of each sample was recorded.
The actual salinities in the pots were somewhat higher than those of the irrigation water because the plants remove some of the water with each irrigation and leave the salts behind. Each irrigation produced approximately 600 mL of drainage water. Following the protocol of Vasquez et al. (2005)
, we measured the electrical conductivity (EC) of irrigation solutions and drainage water from three randomly selected pots on each salinity treatment at Day 40 and Day 80 during the study. The salinity meter (Markson, Inc., Henderson, North Carolina, USA) was calibrated against a NaCl standard for each salinity treatment. Drainage water salinity was consistently 33% higher than irrigation water salinity over the experiment (Fig. 1). Salinity in the pots, estimated as the mean of the irrigation water and the drainage water salinities, was 16.5% higher than irrigation salinities. Pot salinities were used in the final analyses. The NaCl treatment levels based on pot salinities were therefore 0.01 (control), 0.11, 0.21, 0.32, 0.42, 0.50, and 0.60 M. Expressed in parts per thousand, these salinities are 0.57, 6.3, 12, 18, 24, 29, and 34 ppt, respectively.
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Osmotic adjustment experiment
A second experiment was conducted to compare the extent to which Na+ and K+ contributed to the osmotic adjustment of each species. Rhizome sections with roots and shoots (ca. 30 g each) were transplanted into pots and established under sprinkler irrigation for 30 days, then placed on salinity treatments (pot salinities = 0.01, 0.11, 0.21, 0.32, and 0.42 M) (five plants per species per salinity) for 70 days as in the growth experiment. In this experiment, however, root and rhizome tissues were analyzed separately.
Root, rhizome, and leaf samples were taken from each plant to determine osmolality of the cell sap and water, Na+, and K+ contents. Spartina alterniflora leaf samples were wiped briefly with a wet paper towel to remove external salts, then all tissues were frozen. Two grams fresh mass of each tissue sample was thawed for analysis. One gram of tissue was dried in an oven at 75°C to constant mass to determine water content then analyzed for Na+ and K+ content by IAS Laboratories. The five samples of tissue at each salinity were pooled for these analyses. The other gram of tissue was ground immediately after thawing in a mortar with pestle over ice to extract osmotically active compounds. Undiluted tissue samples did not produce a liquid sample on grinding because moisture was reabsorbed into the tissue debris. Hence, tissues were ground in distilled water. Two milliliters of water per gram fresh mass of tissue were used for all tissues except P. australis leaves, which required 3 mL of water to produce a liquid extract that could be sampled. Osmolality was measured for an 8-µL sample of tissue extract with a Wescor (Logan, Utah, USA) Vapor Pressure Model 5130C osmometer calibrated with 0.1, 0.29, and 1.0 M standards. The five samples of tissue at each salinity were measured separately for these analyses.
The osmolality of undiluted tissue water was calculated from the osmometer reading and the dilution factor of the tissue water after addition of distilled water. The osmolality that could be attributed to Na+ and K+ ions was calculated from the ion and water contents of the rhizomes and shoots, assuming that each cation was balanced by one Cl– ion and that all ions were uniformly dissolved in the cell sap and had an activity coefficient of 1.0 (Glenn, 1987
; Vasquez et al., 2005
).
Statistical analyses and other methods
Statistical analyses were conducted with SYSTAT 10.2 software (Point Richmond, California, USA). Growth parameters were compared for each species by a two-way ANOVA, with species and salinity as independent variables and with initial mass of rhizomes as a covariate. For rhizome and shoot dry masses, variances increased in proportion to the treatment means; hence they were log transformed prior to the ANOVAs (Sokal and Rohlf, 1995
). The 
level for significance was P < 0.05 for all tests. Degrees of freedom were 1 for species and 5 for salinity (one treatment was excluded, see Results).
RESULTS
Spartina alterniflora has greater salt tolerance than Phragmites australis
All plants survived to the end of the experiment. However, P. australis plants on the 0.60 M NaCl treatment produced no new growth and had predominantly necrotic shoot tissues; hence this treatment was eliminated from the statistical analyses. Salinity had a significant negative effect on plant height (Fig. 2a) (F1,5 = 20, P = 0.000), number of shoots (Fig. 2b) (F1,5 = 20.3, P = 0.000), and the dry mass of shoots (Fig. 2c) (F1,5 = 22.4, P = 0.000) and rhizomes (Fig. 2d) of both species. Species effect and the interaction of species and salinity were significant for plant height (F1,5 = 80, P = 0.000; F1,5 = 2.9, P = 0.016, respectively), number of shoots (F1,5 = 7.2, P = 0.01; F1,5 = 2.3, P = 0.045), and dry mass of shoots (F1,5 = 72.4, P = 0.000; F1,5 = 2.9, P = 0.015). Spartina alterniflora retained the capacity to initiate new shoots and produce biomass over the entire salinity range, whereas P. australis did not grow well above 0.21 M NaCl. Shoot dry masses (Fig. 2c) also decreased with salinity for both species but were higher for S. alterniflora than P. australis at all salinities, and they decreased more rapidly with salinity for P. australis than for S. alterniflora. Rhizome dry masses of plants (Fig. 2d) decreased with salinity for both species (F1,5 = 20.1, P = 0.000). Species differences were significant (F1,5 = 29.9, P = 0.000), but the interaction term was marginally not significant (F1,5 = 2.2, P = 0.059).
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Spartina alterniflora accumulates Na+, whereas Phragmites australis tends to exclude Na+ from shoots
For both species, water content was higher in rhizomes than shoots and tended to increase with salinity in rhizomes and decrease with salinity in shoots (Fig. 3). Water content of the shoots was consistently higher in S. alterniflora than in P. australis across the salinity range. Two-way ANOVAs of N, P, and S in shoot tissues showed no significant differences (P > 0.05) by species or salinity, and mean values as percentage of dry mass (and SE) were 2.71% (0.08), 0.36% (0.012), and 0.38% (0.014), respectively. The contents of monovalent and divalent cations in shoots are shown (Fig. 4). The contents of K+, Ca++, and Mg++ did not vary greatly by species or over the salinity range. On the other hand, Na+ was much higher in S. alterniflora than in P. australis shoots. Also in S. alterniflora tissues, Na+ increased in proportion to the external salinity gradient, whereas Na+ was relatively constant over the salinity gradient in P. australis shoots.
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). In Fig. 6a–c, measured tissue osmolality values are compared with those calculated based on Na+ and K+ contents. Osmolality values in roots (Fig. 6a) and rhizomes (Fig. 6b) of P. australis and S. alterniflora gave the same pattern of response to external salinity, and measured and calculated values were similar. Tissue osmolality values exceeded the external osmolality up to 0.2 M NaCl but were about the same as the external osmolality by 0.42 M NaCl. In leaves, tissue osmolality exceeded the external osmolality for both species across the salinity range. Measured osmolality was approximately 30% higher than values calculated from Na+ and K+ for both P. australis and S. alterniflora leaves. Calculated and measured osmolality of S. alterniflora leaves increased over the salinity range, hence this species can be considered an osmoconformer. However, P. australis leaves had lower osmolality than S. alterniflora, and the osmolality was nearly constant across the salinity range; hence this species can be designated as an osmoregulator.
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Considerable effort has been expended in both the USA and Europe in an attempt to understand the factors that lead to the spread of exotic species into native marsh habitats (Zedler and Kercher, 2003
). The differential effect of salinity on growth between P. australis and S. alterniflora sheds light on the physiological mechanisms underlying the ecological replacements in North American and European salt marshes. From our results, in combination with those of previous research, a picture emerges of how salt tolerance shapes the course of the Phragmites–Spartina interactions. However, it should be noted that single sampling locations were used for each species; hence, caution is needed in extrapolating the present results to other locations.
Both S. alterniflora and the invasive M haplotype of the reed, P. australis, had reduced growth at high salinities, with S. alterniflora more tolerant than P. australis. We previously showed that the M haplotype had greater salt tolerance than native haplotypes of P. australis from the Atlantic coast of North America (Vasquez et al., 2005
). The results of the two studies are summarized in Fig. 7. Native haplotypes (F and AC) are the least salt tolerant. Their relative growth was reduced 50% at approximately 0.2 M NaCl, and they did not survive above 0.3 M NaCl. In contrast, growth was reduced 50% at 0.4 M NaCl for the M haplotype P. australis and at 0.6 M NaCl (equivalent to full seawater salinity) for S. alterniflora, but both groups survived up to the highest salinity level. These results explain why only the M haplotype of P. australis has been able to expand into brackish parts of Atlantic coastal salt marshes of the USA. The data also suggest an upper salinity limit exists for this penetration.
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also found that the M haplotype produced markedly more shoots per gram of rhizome tissue than did the native haplotypes. This type of growth habit has been described as a "phalanx" life strategy, by which a clonal plant expands its patch size slowly while excluding other plants from invading by means of its high density of shoots (Hamilton et al., 1987
). On the other hand, S. alterniflora and the native P. australis haplotypes produce fewer, more widely spaced shoots per unit of rhizome tissue. This has been called a "guerilla" strategy, by which a clonal plant can colonize bare soil rapidly (Hamilton et al., 1987
). However, a species with a higher density of shoots such as M haplotype P. australis might be able to interdigitate within these patches and eventually become the dominant plant species.
Our results support field experiments and observations relating the distribution of P. australis and S. alterniflora to salinity gradients in salt marshes. For example, Burdick and Konisky (2003)
conducted reciprocal transplant experiments with P. australis (presumably the M type), S. alterniflora, and other emergent marsh species in New England, USA, salt marshes at low (14 ppt), intermediate (18 ppt), and high (23 ppt) salinity levels. Phragmites australis was a "robust competitor" with S. alterniflora and the other salt marsh species on the low, but not the high, salinity plots. In addition, Farnsworth and Meyerson (2003)
reported that P. australis and Typha latifolia L. (cattail) consistently exceeded S. alterniflora in standing biomass, leaf area, length of growing season, and leaf longevity in freshwater and brackish tidal marshes in southern Connecticut, USA.
The results are also consistent with studies showing that disturbance factors that decrease the salinity of coastal marshes encourage the spread of P. australis. Bart and Hartman (2003)
showed that invasion of S. alterniflora marshes often occurs along drainage ditches that have reduced sulfide and salinity levels and that P. australis then spreads more slowly into adjacent areas that are more saline. In addition, Silliman and Bertness (2004)
showed that in 22 salt marshes in Narragansett Bay, USA, 80% of the intramarsh variation in P. australis cover could be explained by shoreline development associated with decreased marsh salinities and increased nitrogen availability. The main factor reducing salinity in those marshes was removal of trees and shrubs bordering the marshes, which allowed increased freshwater influx into the marsh. In other marshes, salinity has been reduced by the restriction of tidal exchange and the concomitant discharge of floodwaters into the backwaters (Burdick et al., 2001
). Furthermore, Chambers et al. (1999)
reported that initial sites of vigorous spread of P. australis in tidal wetlands are limited to marsh sections where salinity is <10 ppt, which supports our conclusion that P. australis does not grow well above 0.2 M NaCl (11.4 ppt salinity).
Similar interactions are occurring between P. australis and Spartina spp. in northern Europe. There, coastal marshes are often less saline than U.S. marshes, a result of large volumes of terrestrial runoff (Dijkema, 1990
). Marshes around the North Sea and Baltic Sea have salinities of 3–14 ppt and have traditionally been dominated by species such as P. australis, Scirpus spp., and other nonhalophytic grasses and sedges. However, land use practices such as grazing, hay mowing, sod cutting, and drainage ditch installation have increased salinities and have led to the replacement of brackish-tolerant plants by halophytes, including S. anglica and S. townsendii (Hubbard, 1965
; Thompson, 1991
; Esselink et al., 2000
). Thus, differences in relative salt tolerance interacting with patterns of land use change can explain why Spartina spp. are considered invasive in European reed marshes, whereas P. australis is considered invasive in Spartina marshes of the North American Atlantic.
The contrast in salt tolerances between P. australis and S. alterniflora is explained in part by their different methods of osmotic adjustment. Phragmites australis maintained a relatively constant Na+ concentration within the shoot tissue that was much lower than that of Spartina across all salinity treatment levels. Studies conducted by Matoh et al. (1988)
and Matsushita and Matoh (1991)
suggest the occurrence of downward Na+ transport from shoot base to root in reed plants such as Phragmites spp. Thus, sodium accumulation in the shoot tissue is limited. In contrast, the ability of Spartina to survive at higher salinities may be in part due to its ability to use Na+ in the shoots for osmotic adjustment (Bradley and Morris, 1991
; Glenn et al., 1999
; Hester et al., 2001
, Parida and Das, 2005
). We found that Na+ accumulated in the shoot tissue to over 2.0 mol · kg–1 on 0.42 M NaCl pot salinity. In addition, Spartina excreted about half the Na+ that entered the shoots, which would allow the plant to maintain transpiration while avoiding toxic buildup of Na+ in the apoplastic tissues of the leaves (Bradley and Morris, 1991
; Bell and O'Leary, 2003
).
Sodium appears to be the major cation involved in the relatively greater salt tolerance of S. alterniflora from data in Figs. 5 and 6. On 0.42 M NaCl, Na+ (balanced by Cl–) could account for 55% of the osmotic adjustment of S. alterniflora shoots but only 28% of the osmotic adjustment of P. australis shoots. The remainder of osmotic adjustment was due to K+ uptake and (presumably) synthesis of organic molecules; for example, Matoh et al. (1988)
reported sucrose accounted for 30% of the osmotic adjustment of P. australis leaves on 0.4 M NaCl. Na+ is considered a "cheap osmoticum" in plant tissues (Pardo and Quintero, 2002
) because it is abundant in the external medium. The ability of S. alterniflora to accumulate Na+ within its shoot tissue as a mechanism for osmotic regulation appears to give it an advantage over P. australis at salinities above 0.2 M NaCl.
The species differ in other ways that may contribute to their competitive abilities in salt marshes. For example, P. australis is less tolerant of sulfide than is S. alterniflora, and sulfide in sediments increases with salinity because of the reduction of sulfate present in seawater (Chambers et al., 1999
). The plants also differ in photosynthetic pathway. Phragmites australis is a C3 plant (Choi et al., 2005
) and S. alterniflora is a C4 plant (Bradley and Morris, 1991
). In general, C4 plants have a greater water use efficiency than C3 because of the higher assimilation rate of CO2, and this contributes to the salt tolerance by reducing the amount of water and therefore salt that the roots must process to support growth (Flowers et al., 1977
). Choi et al. (2005)
showed that salinity reduced CO2 assimilation in P. australis, leading to reduced biomass accumulation. By contrast, the photosynthetic capacity of S. alterniflora is seldom altered by usual changes of soil salinity and redox potential encountered in salt marsh environments (Dai and Wiegert, 1997
; Farnsworth and Meyerson, 2003
).
Both S. alterniflora and P. australis are considered invasive species in some locations yet are valuable ecosystem components in their native habitats. It is probably best to avoid the value-laden term "invasive" for this species pair and simply to model species interactions in the context of a particular environment. Now that the M haplotype of P. australis is widespread in the USA, this species is likely to encroach into Spartina marshes that have been altered so that salinities are below 0.2 M NaCl. On the other hand, the European hybrids of S. alterniflora are likely to encroach into European marshes when salinities are increased above 0.2 M NaCl. Hence, on both continents management should emphasize creating a hydrological regime that produces salinities that favor the establishment of the desired plant community.
FOOTNOTES
2 Author for correspondence (e-mail: eglenn{at}ag.Arizona.edu
) 
101 6 Present address: U.S. Fish and Wildlife Service, Central New England Fishery Resources Office, 151 Broad Street, Nashua, NH 03063 USA
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