Plant Growth and Productivity Along Complex Gradients in a Pacific Northwest Brackish Intertidal Marsh Author(S): Kern Ewing Source: Estuaries, Vol

Coastal and Estuarine Research Federation

Plant Growth and Productivity along Complex Gradients in a Pacific Northwest Brackish Intertidal Marsh Author(s): Kern Ewing Source: Estuaries, Vol. 9, No. 1 (Mar., 1986), pp. 49-62 Published by: Coastal and Estuarine Research Federation Stable URL: http://www.jstor.org/stable/1352193 Accessed: 30/07/2010 19:11

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http://www.jstor.org Estuaries Vol. 9, No. 1, p. 49-62 March1986

Plant Growth and ProductivityAlong Complex Gradients in a Pacific Northwest Brackish IntertidalMarsh

KERN EWING Department of Biology McMaster University Hamilton, Ontario L8S 4K1, Canada

ABSTRACT: Environmental characteristics were measured and recorded in the Skagit Marsh, a brackish intertidal marsh on Puget Sound, Washington. Four transects were placed perpendicular to a known gradient of increasing salinity which began with fresh water at the bank of one of the outlets of the Skagit River and reached a surface water salinity of 22%oat a point alongshore 5 km north of the outlet. The environmental characteristics which were measured varied along gradients (soil texture, organic carbon in fines, soil column temperature, free soil water salinity) or had a patchy distribution (soil redox potential, soil macro-organic matter). Growth and production vary across the marsh. The maximum aboveground standing crop (1,742 g m-2 dry weight) was measured at a site with 0-4%o free soil water salinity, dominated by the sedge Carex lyngbyei. In more saline areas (8-12%o), the bulrush Scirpus americanus was dominant and standing crop values dropped to a third of the maximum. Species performance varied in a complex manner as did the environment. C. lyngbyei had diminished growth and decreased standing crop in areas where salinity was higher. S. americanus was equally productive in low elevation, high salinity sites and in high elevation, low salinity sites. An increase in shoot density for dominant species occurred in saline areas as individual shoot weights and leaf areas decreased. Because species responded differently, environmental variation was magnified in the population and community responses of the marsh vegetation.

Introduction mances which plants are capable of when Environmental gradients have extensive so constrained, combined with environ- effects upon the structure of plant com- mental variability, play a very great role in munities and upon the performance and determining the observed pattern in coastal success of individual species (Chapman and estuarine wetlands. 1976). Although conditions in brackish in- This study was carried out in the inter- tertidal marshes may be stressful to some tidal brackish marsh formed by the Skagit species and only a limited number are able River as it enters the bay system of Puget to survive, production is comparable to the Sound in Washington. At the Skagit Marsh, most productive systems on earth (Chap- substantial environmental gradients exist. man 1960; Odum 1975; Jefferies et al. 1977). Large salinity differences can be found, as Many species reach the limits of their com- can gradients of soil temperature, soil de- petitive ability or of their tolerance to com- velopment, length of tidal inundation, soil bined stresses in parts of any marsh while textures, organic content of the soil, and re- a few are able to adapt across a great range dox potential. These gradients are neither of environmental variation and survive linear nor parallel, and their cumulative ef- (Mason 1957; Ranwell 1972). Plant reac- fect is a complex environmental pattern. tions to variable environments may be Responding to this pattern is a limited num- viewed as the results of their strategies, or ber of dominant plant species of wide North genetically defined and limited responses to American or circumboreal distribution ranges and combinations of environmental (Disraeli and Fonda 1978; Drinnan et al. conditions (Grime 1979). The perfor- 1978; Kistritz 1978; Taylor 1980; Liverman 0 1986 EstuarineResearch Federation 49 0160-8347/86/010049-14$01.50/0 50 K. Ewing

1982; Ewing 1983). The object of the analysis of this system is to measuregrowth and productivity of five common and locally dominant plant species in the family Cyper- aceae across the range of environmental conditions existing in the marsh, and show the relationshipbetween the local environment and species performance. 1- ~~~r~ Study Area 0-1 3 The study area is located along the east shoreof SkagitBay in PugetSound (48?18'N, 122?24'W), where the Skagit River has cre- 0 .5 i km ated a progradingsubaerial and subaqueous delta. The climate along the eastern shore of Puget Sound is maritime, with cool sum- mers, mild winters, moist air and a small daily range of temperatures.There are two high tides and two low tides in each tidal Fig. 1. Locationmap. Area of the intertidalSkagit period. On neap tides, tidal range may be Marshcovered in this study. Survey transectsare in- as low as 2 m; on spring tides, tidal range dicatedby heavy lines and are numbered. increasesto 4 m (U.S. Departmentof Com- merce 1980). The annualrange of day length varies from a minimum of 8 h to almost 16 marily these data presentedhere. The data h, while the sun angle increasesfrom 18?to collected show little variation from year to 65? above the horizon, so potential insola- year. The climatological conditions over tion increases rapidly in spring and early those years were also little different from summer. those recorded in previous years, demon- Salinities in Skagit Bay are as low as 25- strating the evenness of the maritime cli- 28%oat the surface (Collias et al. 1973). mate of the area. These loweredlevels are producedby runoff Four transects 0.8 to 2.0 km apart and from rainfalland melting snow and glaciers 500 to 750 m long were established from in rivers drainingthe Cascadeand Olympic the dike to the seaward edge of intertidal mountainsand by restrictedmixing with the emergentvegetation along a 5 km reach of salt water in the open sound. Within the 5- shoreline(see Fig. 1). Transect1 was located km long band of vegetation where the study near FreshwaterSlough, the main channel was carriedout, surfacewater salinities dur- of the South Fork of the SkagitRiver. Tran- ing the growingseason vary from 0%ooto that sects 2 through 4 were to the north of the of the open bay. Surface water salinity in slough, in areas inundated by waters of in- channels, tidal pools, and on incoming or creasingsalinity. Four environmentalmea- recedingtides varies substantially.Salinities suring stations were established on each generally increase alongshore away from transect,evenly spaced. At each station, in- rivers and out into the bay, and they are tensive sampling of vegetation and mea- seasonally lower during winter rains and surementof environmentalfactors was car- spring snowmelt runoff. ried out at regular intervals during the growing season. Less intensive measure- Methods ment between stations was used to verify the regularityof variation from station to ENVIRONMENTALMEASUREMENT station. That station closest to the dike at Field work was carried out during the the upland end of each transect was desig- growing seasons of 1978, 1979, and 1980. nated station A, and stations B, C, and D A complete data set for all comparisons of were progressivelylower and closer to the plant performanceand environmentalcon- open water of the bay and the seawardedge ditions was obtained for 1980, and it is pri- of emergentvegetation. Environmental data NorthwestIntertidal Marsh Productivity 51

were collected for soil texture, soil organic arated while fresh, then dried at 70 ?C for material content, free soil water salinity, soil 24 h. redox potential, soil column temperature For the measurement of height, dry weight profiles, and site elevations. Soils were sam- and leaf area per shoot, five randomly se- pled with replicate cores at each station. lected samples of each species in the canopy Nested sieve and hydrometer grain-size layer were collected at each station during analyses were performed on samples after every measurement period. Leaf areas were removal of iron and organic material. Or- calculated from measured dimensions. One ganic material was measured by physical surface of laminar leaves is used in the data separation and by use of the Walkley-Black presentation, while for conical, cylindrical method for fines. Free soil water salinity was or pyramidal shaped leaves or photosyn- determined by using a refraction salinom- thetic stems, total external area is reported eter to measure the salinity of water col- (Sestak et al. 1971). lected in standpipes with perforations from 15 to 25 cm below the soil surface. Soil Results redox potential was measured in the laboratory using a platinum electrode on soil ENVIRONMENTAL CONDITIONS cores which had been collected, sealed and The four transects established for this transported. Soil temperature profiles were study cut across habitats and species and constructed using readings obtained from environmental gradients, and the sampling thermocouples with junctions placed at 10, stations spaced along the transects are con- 20, 30, 40, and 50 cm. Site elevations were sequently located in unique combinations obtained from level circuits tied to simul- of environmental characteristics and plant taneous high tides. See Ewing (1983) for assemblages. complete methods. Elevation PLANT SAMPLING Along each transect, the elevation of mea- At each of the 16 environmental measuring stations decreases regularly from the suring stations along the transects, a 5 x 5 dike to bay edge of vegetation. Emergent m sampling plot was established for ob- vegetation exists from an elevation of about serving phenology and for collecting sam- 2 m (which is near mean tide level) to 3.4 ples for measurement of plant growth. m. Below 2 m is sandy bay bottom which Aboveground standing crop was measured supports seasonal algal blooms. Above 3.4 from a single harvest, and shoot density, m, terrestrial extratidal species begin to plant height, shoot weight, leaf area, and dominate. High spring tides of 3.6 to 3.8 m belowground macro-organic matter (organ- are common. Along transects 3 and 4 (the ic matter retained on a 1 mm sieve, MOM) more saline transects), areas of erosional to- were measured by repeated sampling during pography occur. In these areas, sod pedes- the growing season. Quadrats within sam- tals are surrounded by channels as deep as pling plots were chosen randomly. Mea- 0.5 m. The channels are few at the inland surements were repeated at each station edge of this topography. At the seaward edge, every 1 to 2 wk between early April and late the channels have enlarged and joined so August. that fewer and fewer pedestals remain; be- An estimate of aboveground net produc- yond a certain point they have been eroded tion was made by harvesting and weighing entirely away. live and dead plant material at the time of peak standing crop. Harvest was com- Soil Texture menced when growth characteristics such as Soils along transect 1 are clayey silts. height and weight per shoot showed com- Transect 2 has a combination of clayey silt pletion of the initial fast growth phase. At and silty clays; transect 3 has mostly silty each station, 3 to 5 replicates were collected clay. Soils on transect 4 are almost all silty using 0.1 m2 (0.2 x 0.5 m) quadrats. Ma- sands, as is most of the subaerial delta at terial present was considered to have been elevations below that at which emergent produced the current year. Species were sep- vegetation survives. 52 K. Ewing

Soil Organic Material to the freshwater source. Salinity tended to The percent of carbon in the < 1 mm frac- increase away from the river and toward tion of the soil ranges from 5% in areas of lower elevations. In April and May, read- high clay content to 0.5% in sandy soils. ings of 0 and 1%owere found along the river. MOM in the soil is at its highest level in In June, July, and August, salinities in- areas of full growth of Carex lyngbyei.In creased at all stations as freshwater flow in most C. lyngbyei swards, the MOM per- the river decreased. The highest free soil centage of soil dry weight is 4-6%. In ero- water salinity measured was 15%o,while the sional topography where pedestals support- highest salinity on an incoming tide was ing C. lyngbyei occur, it is 9-13%. measured at 22%o.Free soil water salinities along transects 1 and 2 were 4%oand lower Soil Redox Potential during the growing season, while values transects 3 and 4 between 8 The redox potential of a submerged soil along averaged and 12%o. is the result of a complex combination of physical, chemical, and biological factors. PRODUCTIVITY The redox and the amount of potential oxy- Thirty vascular plant species were found in a soil do not a gen exhibit linear rela- in the Skagit intertidal. The dominant low tionship, but at very redox potentials it species in terms of aboveground production in is likely that all oxygen a soil has been as well as in frequency of occurrence in Potential read- depleted (Armstrong 1967). quadrats were Carex lyngbyei Hornem. and are around roots because ings higher oxygen Scirpus americanus Pers. The other species diffuses from them into the soil (Ponnam- analyzed, Eleocharis palustris (L.) R. & S., At the peruma 1972). Skagit Marsh, the Scirpus validus Vahl., and Scirpus mariti- lowest redox to -425 potentials (-320 mv, mus var. paludosus (A. Nels.) Kuek., ranked to were found in adjusted pH 7.0) poorly closely behind the two dominants in these consolidated fine soils in which there was categories. Community productivity, as re- no sod or from which sod had development flected in the harvest of the peak above- These conditions existed in disappeared. ground standing crop (Table 1), shows large pannes and channels. Well-drained sandy differences between transects. The less sa- soils showed the redox highest potentials line transects 1 and 2 produce more above- 150 to (+ mv, adjusted pH 7.0). ground material than do the more saline transects 3 and 4. There was no trend along Soil Temperatures transects toward greater productivity, Soil temperature profiles showed little dif- though species diversity dropped sharply ference between stations on 8 April, a few toward the bay. The trend was alongshore, weeks before the beginning of the growing decreasing away from the river. Sites on season. Profiles of temperature to a depth transect 2 were most productive, with all of 50 cm were vertical, the mean was 9 ?C, stations producing above 1,500 g m-2. Har- and the temperatures across the marsh var- vest values for sites along transects 3 and 4 ied by no more than 2 ?C. During the period were about half of those on transects 1 and 2. of maximum aboveground growth, late April The three-dimensional representations in to mid-June, stations adjacent to the river Fig. 2 are response surfaces for the above- (i.e., on transect 1) were kept cool by over- ground production for Carex lyngbyei, El- flow of the snowmelt-fed stream, while soils eocharis palustris, Scirpus validus, S. mar- away from the river (i.e., on transect 4) were itimus, and S. americanus across the study warmed by tidal water passing over the ex- area. Dimensions of the study site on the tensive tidal flats. The difference between ground are approximately 5 km by V/2 km, stations was as high as 8 ?C at that time. but the figure is constructed as a wider rec- tangle in order to better display the pro- Salinity ductivity variation. The trend in commu- The lowest salinities were measured in nity productivity is tied closely to that of the early part of the growing season in the Carex lyngbyei. The production of C. lyng- highest parts of the intertidal marsh, next byei makes up most of the community bio- NorthwestIntertidal Marsh Productivity 53

TABLE 1. Peak aboveground standing crop (mean ? SE, n = 5) in g m-2 dry weight, harvested 4 June to 15 July 1980. Scirpus validusis not recordedbecause of the clumped natureof its distributionpattern. At some stations,indicated by the abbreviationpan, Scirpusamericanus was measuredin largepannes adjacent to sample plots used for other species. Along transects 3 and 4, measurements made atop pedestals or in channels are designatedwith the abbreviationsped or ch.

Station Carex lyngbyei Eleocharis palustris Scirpus maritimus Scirpus americanus Community IA 1,412 + 57 53 ?+ 14 1,497 +? 61 lB 1,432 +? 156 22 ?+ 13 1,503 ?+ 152 1C 1,392 ? 134 10 ? 5 550 ? 56"n 1,488 ? 151 ID 988 ? 55 84 ?+ 28 515 +? 12^ 1,115 ? 84 2A 1,579 ?+ 206 72 ?+ 17 1,677 +? 236 2B 1,388 ?+73 23 7 1,511 ? 58 2C 1,553 + 281 2 +2 106 +? 7P 1,555 ?+ 281 2D 1,738 ?+ 130 596 ? 62p^ 1,742 +? 124 3A 4 + 3 63 + 14 878 ? 63 3B ch 307 + 65 71 +? 23 448 ?+ 52 3B ped 233 + 58 8 ?+ 4 666 +? 38 3C ch 428 +? 59 61 ? 23 499 ?+ 36 3C ped 531 + 30 19 ?+ 7 729 ?+ 81 3D 529 ?+ 64 529 +? 64 4A 36 ?+ 20 670 ?+ 159 4B ch 426 + 141 + 1 443 +? 8 4B ped 362 +? 89 20 +? 3 699 ?+ 95 4C ch 480 +? 37 64 + 20 546 ?+ 52 4C ped 393 + 39 54 ?+ 17 716 ?+ 39 4D 622 ?+ 62 626+ ?75

mass along transects 1 and 2 but drops to transects 3 and 4, and in extensive pannes a third of the total at sites along 3 and 4. on transects 1 and 2. It contributes sub- On transects 1 and 2, E. palustrisis almost stantially to community production (Table always present,but makes up no more than 1), and is probablysecond to C. lyngbyeiin ten percent of the C. lyngbyei-dominated total primary production at the Skagit biomass. Eleocharis palustris is essentially Marsh. At the upper end of transects 3 and absent from transects 3 and 4. Scirpus val- 4, the dominance of the five species inves- idus is found in widely distributedpatches, tigatedhere is substantiallydiminished, and the most vigorous of which had an above- other marsh species such as Juncus balticus, ground harvest yield of 1,600 g m-2 dry Agrostis alba, Potentilla pacifica, and Tri- weight. At lower, more saline sites, S. val- glochin maritimum become more impor- idus clones show lowered stem density and tant. weight, and cease to produceseed heads. At Both binary discriminant analysis of the low elevation end of transects 3 and 4, community data (Ewing 1983) and regres- the species is not presentat all. Scirpusmar- sion analysis of growth characteristics(Ew- itimus is excluded from transects 1 and 2, ing 1982) show that free soil water salinity, but forms pure populations at middle ele- elevation, soil texture, and redox potential vations on transects3 and 4. It is also found of the soil are environmental variables that growing with patches of S. validus, and are good predictors of growth and distri- merges with stands of S. americanusat the bution of plant species in the marsh. By lower limits of its local distribution.Above- looking at three-dimensionalplots of these ground standing crop values for S. mariti- variables (Fig. 3), it may be seen that there mus reachonly about 30%of the maximum are substantial differences in the factors value for the marsh and are slightly lower across the marsh, and they do not vary to- than those for S. americanusat stationsjust gether.The salinity for May is shown in Fig. to seaward.Scirpus americanus occupies the 3; the variabilityof salinity across the marsh bayside sites in the marsh, exclusively on is high during this month, and at the same 54 K. Ewing

SCIRPUSMAR/TIMUS

, ec . , I'"

' 4

ELEOCHAR/SPALUJSTR/S -0.0 SCiRPUSVA/LIDUS

_ 50 100

_1500

.1000

. 500

Fig. 2. Productivity response surfaces for Carex lyngbyei, Eleocharis palustris, Scirpus validus, S. maritimus, S. americanus, and for community productivity of all species. Values in g m-2 dry weight from aboveground harvest at peak of 1980 growing season (except for S. validus for which values are dry weight per shoot in g) at sixteen stations in Skagit Marsh. Relative transect and station locations are indicated on the right and left base, respectively, of each figure. Ratio of horizontal dimensions not to scale and extra grid lines are added between transectlines to better define the response surfaces. NorthwestIntertidal Marsh Productivity 55

_- K00 m

4 \

MAYSALINITY 35 m

0 0 c 1- c

\ 4 4 \ Fig. 3. Environmental conditions. Values for free soil water salinity in May 1980, elevation of soil surface, percent of sand in the soil, and average soil redox potential in summer of 1980. Conventions same as for Fig. 2. time, growth rates are at their maximum. then in a sequence that might be expected Salinity values along the river side of the in natural river levee formation, soils of site (transect 1) are very low, actually mea- progressively smaller particle sizes occur. suring 0%ooat three stations. Salinity in- Sands are found at lower elevations, pos- creases alongshore, reaching its peak adja- sibly because of the loss of fines due to re- cent to the bay on transect 4. Elevation suspension by tidal and wave action. differencesin the marshare slight, but slight Depressedredox potentialin a zone about elevation changes in coastal marshes are two-thirds of the way from the bay edge of often sufficientto be reflectedin community the site to the dike is shown strikingly in composition (Ranwell 1972). Maximum el- Fig. 3 as a trough which runs the length of evation changesalong transects 1, 2, 3, and the study site, parallelto the dike. This zone 4, respectively,are 0.8 m in 500 m, 0.6 m of lowered redox potential coincides with in 450 m, 1.6 m in 700 m, and 1.3 m in an area of poor drainage.It is inundated at 500 m. The lowest elevations are at the out- almost every high tide, and slopes are flat er ends of transects3 and 4, and the highest and the marsh not greatlydissected by dis- elevations are at the landwardends of the tributaries so far back from the bay, so same transects. Upper parts of the marsh drainageis slow. The resultis standingwater are quite flat, with slopes increasingslightly over much of the surface even at low tide, to seaward.Soil texture varies with the dis- probablya contributingfactor in the lack of tance from the river. More coarse-grained oxygenation in the soil. clayey silts are found adjacentto the river, A comparison of the three-dimensional 56 K. Ewing

plots for plant productivity and those for redox potential is very low, and it is also salinity, elevation, sand content, and redox found growingin anoxic pannes in standing potential quickly reveals several interac- water; whereas S. validus is found in this tions. Productivity in the more saline part habitat in less saline sites, S. maritimus is of the marsh is definitely depressed. Com- ubiquitous there on the more saline tran- munity productivity drops, but that part sects. Scirpus americanus does not show a contributed by C. lyngbyei displays a pro- general preferencefor anoxic sites, but its portionally larger drop; C. lyngbyei is not most vigorous growth and robust mor- present at all at the bay end of transects 3 phology is found in anoxic pannes near the and 4. Eleocharis palustris is likewise ex- outeredge of vegetationon transects1 and 2. cluded from more saline sites; it is limited to only one or two scatteredoccurrences at PLANTGROWTH higherelevations on transects3 and 4. Scir- Repeated measurementsof the growthof pus validus is found in high and low ele- the five investigated species allow com- vation sites in the less saline parts of the parisonsof their performancein Northwest marsh and only in high elevation sites in intertidalbrackish marshes and provide in- the more saline areas. Scirpus maritimusis sight into the relationships of the perfor- not found on the less saline transects 1 and mance and environmentalconditions. From 2, but this species reaches its best produc- growthmeasurements at each station, plots tivity at mid-elevation, low redox potential of height, weight and leaf area over time sites on transects 3 and 4. Finally, Scirpus permitted the calculation of growth rates americanusshows little responseto the range duringthe initial period of fast growth.The of salinities at the Skagit Marsh. plots also allowedthe determinationof dates Regression analysis shows soil texture to for phenological events such as peak of be correlatedwith productivity only along growth, leaf deployment, and onset of se- the less saline transects 1 and 2. There, both nescence. Shoot density was recordedeach C. lyngbyei and E. palustris are more pro- time growth was measured. ductive in sites with more clay and less sand. Althoughelevation differencesare not great, Carex lyngbyei S. americanus consistently dominates the Growthof Carex lyngbyeifollowed a pat- lowest sites in the marsh and is found all tern which generallydescribes the growthof along the outeredge of emergentvegetation. the other species investigated. The over- The three-dimensionalplot shows its yield winter dormancywas broken in mid-April, as a ridge at this outer edge, along the bay. and height,leaf area per shoot and dryweight None of the other five species show such a per shoot increased rapidly until a plateau definite relationship between productivity was reachedin mid- to late June. Rates and and elevation; S. americanusis often found maximum values of this growth increased at the deepest riverside and bayside sites in from transect 1 to 2, then decreased, often brackish marshes, and has been found by markedly,through transects 3 and 4. While the author and others in such sites across the curve described was generally of a sig- North America (Riley and McKay 1980; moid-shape on transects 1 and 2, it became Ewing and Kershaw 1985). more flattenedon transect 4 (Fig. 4); there, The effects of redox potential are gener- growthoften continued at a constant, lower ally masked by the presence of other gra- rate until senescence occurred. The maxi- dients at the Skagit.Community production mum average height of C. lyngbyei shoots and that of Carex lyngbyei show a slight ranged from a high of 182 cm on transect decline in areas of low redox potential. The 2 to a low of 42 cm on transect 4. At the relationship in smaller areas with many same locations, maximum rates of increase pannes is more apparent. Scirpus validus were 17 and 5 cm wk-', respectively. The seems to be little affectedby low redox po- same trends may be seen for dry weight per tentials; one of its preferredhabitats within shoot and leaf area per shoot (Table 2), with C. lyngbyeiswards is in anoxic pannes from an eight-fold differencebetween maximum which the Carex is excluded. Scirpus mar- dry weights and an almost ten-fold differ- itimus is found extensively in swardswhere ence between maximum leaf area per shoot NorthwestIntertidal Marsh Productivity 57

2m which was also delayed in comparison with Trans.ct I the other species. Its maximum average height was 132 cm on transect 2, while it only reached 43 cm on transect 4. At those --A-fI=-['; i same sites, maximum rates of increasewere " [ Im \///,- -j 12 and 6 cm wk-~, respectively. Differences /;//i Di' in dry weight per shoot and leaf area per ?shoot between the less saline transects 1 and 2, H^ D/:/ 2 and the more saline transects3 and 4 were .?-<,/: much less than those observed for C. lyng- ^D-g> byei. Though the highest values occurred April May June July August along transect2, as they did for C. lyngbyei, transects 1 and 3 were essentially at parity, cm while the lowest values were on transect 4 (Table 2). For S. americanus,as for C. lyngbyei, shoot densities increase both from the land side towardthe bay, and from transect 1 to transect 4. Productivities of S. ameri- Im canus did not drop along the salinity gradient from transect 1 to 4 as did those of C. lyngbyei,but there was still a decreasein 7~ -i>~. dry weight and leaf area per shoot which c/, "" ^^ -^*T was counteredby an increasein the number ?.^ | of shoots produced (Table 3). In anoxic April May June July August pannes in the less saline parts of the marsh, Fig. 4. Heightof Carexlyngbyei during 1980grow- S. americanus developed a growth-form ing se~ason. Recordedobservations from stationsA with stems thicker, and composed of more (neare,st dike) to D (nearestopen water)on each tran- enlarged aerenchyma cells, than those at sect. Tvlean values ? SD are plotted (n = 5). other stations. Scirpus validus Scirpus validus is easily the most robust when sites on less saline and more saline plant in the SkagitMarsh, reachinga height transects are compared. While its height, of 3 m in some locations, with by far the leaf area, and weight per shoot drop from fastest rates of increase in height (26 cm transect 1 to 4, Carex lyngbyeicompensates wk-1), dry weight/shoot (121 mg d- 1), and for the decrease in photosynthetic surface leafarea/shoot(11 cm2d-l) of the five species per shoot by increasing its shoot density. for which these values were measured. It The average number of shoots per square follows a pattern of growth similar to that meter doubles from transect 1 to transect4. of C. lyngbyei,but after reachingpeak val- In addition,there is a significantprogression ues for these three indicators, it character- (a = 0.01) of increasingshoot density from istically shows a decrease which is in part higherelevation sites to the bay for C. lyng- attributableto senescenceof the top portion byei (Table 3). of this tall, thin, cylindrical bulrush. Not presentin some of the more saline parts of Scirpus americanus the marsh, it still occurs on all four of the The growth of Scirpus americanus was transectsestablished in this study. Its max- slower than that of C. lyngbyei, but while imum heights on transects 1 (206 cm) and the aboveground growth of C. lyngbyei 2 (199 cm) are not a great deal more than characteristicallystopped after reaching a the maximum height on transect4 (135 cm), peak value, that of S. americanusdisplayed and the dry weights per shoot show some an inflectionin its growthcurve and slowed comparablevalues on all transects.Leaf area down. At some sites S. americanuscontin- differencesare substantial,however, with 5 ued its growthup to the time of senescence, to 8 times more leaf area per shoot on tran- 58 K. Ewing

TABLE2. Peak dry weight per canopy shoot in g (mean ? SE, n = 5), and peak leaf area per canopy shoot in cm2 (mean ? SE, n = 5), in 1980. Conventions of annotationsame as in Table 1.

Station Carexlyngbyei Eleocharispalustris Scirpusvalidus Scirpusmaritimus Scirpusamericanus Dry weight per shoot 1A 2.7 ? 0.2 0.15 ? 0.04 5.5 ? 0.5 1B 2.3 ? 0.2 0.15 ? 0.07 8.4 ? 0.9 0.8 ? 0.2Pn 1C 2.7? 0.3 0.15 ? 0.08 10.0 ? 1.0 1.0 ? 0.pan 1D 1.4? 0.1 0.14 ? 0.05 1.0 ? 0.1 pan 2A 4.0 ? 0.5 0.31 ? 0.07 5.6 ? 0.8 2B 2.8 ? 0.2 0.29 ? 0.09 8.4 ? 0.3 2C 2.3 ? 0.4 0.19 ? 0.06 7.3 ? 1.3 1.1 ? 0.1pan 2D 1.6? 0.1 0.28 ? 0.07 4.5 ? 0.9 1.0 ? 0."an 3A 1.5 ? 0.2 5.4 ? 0.2 4.2 _?0.9 0.7 ? 0.2 3B ch 4.8 ? 1.0 0.5 ? 0.2 3B ped 0.7 ? 0.2 0.3 ? 0.1 3C ch 4.8? 0.7 0.7 ? 0.2 3C ped 0.7? 0.1 0.3 ? 0.1 3D 1.0 ? 0.1 4A 0.7 ? 0.2 3.9 ? 0.3 3.0 _?0.3 0.3 ? 0.1 4B ch 2.9? 0.1 0.4 ? 0.1 4B ped 0.5 ? 0.1 0.2 ? 0.1 4C ch 2.7 ? 0.3 0.4 ? 0.1 4C ped 0.6 ? 0.1 0.2 ? 0.0 4D 0.5 ? 0.1 Leaf area per shoot 1A 257 ? 38 61 ? 7 541 ? 14 1B 282 ? 6 35 ? 1 604 ? 24 118 ? 3"n 1C 338 ? 9 55 ? 6 679 ? 20 196 ? 52" 1D 174 ? 7 43 ? 4 183 ? 9a 2A 528 _? 43 74 ? 1 469 ? 33 2B 341 ? 19 66 ? 5 518 ? 17 2C 320 ? 26 61 ? 8 555 ? 23 173 ? 41" 2D 316 ? 64 76 ? 4 423 ? 17 198 ? 26an 3A 223 ? 37 406 ? 41 268 ? 43 142 ? 4 3B ch 326 ? 27 368 ? 18 72 ? 4 3B ped 88 ? 9 53 ? 4 3C ch 249 ? 27 103 ? 10 3C ped 81 ? 20 49 ? 2 3D 140 ? 3 4A 87 ? 27 87 ? 27 300 ? 27 49 ? 3 4B ch 258 ? 54 63 ? 6 4B ped 55 ? 9 32 ? 5 4C ch 282 ? 38 62 ? 5 4C ped 71 ? 20 32 ? 2 4D 75 ? 15

sects 1, 2, and 3 than on transect 4. The water sites, it was much less successful at pattern of stem densities throughout the salinities above 10%o. marsh was not measured for S. validusbe- cause of its dispersed clumping pattern of Eleocharispalustris growth, but measurements made within pure A component of Carex lyngbyei-domi- clones showed 200 to 300 shoots per square nated communities wherever it is found, El- meter to be a common range for the species. eocharis palustris occurred all along tran- While growing well at sites with free soil sects 1 and 2, but was almost totally absent water salinities of 4-8%o as well as at fresh- from the more saline areas of Skagit Marsh. NorthwestIntertidal Marsh Productivity 59

TABLE 3. Shoot densities over the April to August 1980 growing season in shoots per m2 (mean ? SE, n = 5). Density values were not obtained for Scirpusvalidus because of its dispersedclumping distribution pattern. Conventionsof annotationsame as in Table 1.

Station Carexlyngbyei Eleocharispalustris Scirpusmarilimus Scirpusamericanus IA 1,014 ? 56 974 ? 95 260apan lB 1,094 ? 85 485 ? 60 300 ? 80pan" 1C 1,290+?61 610 ?53 460 ? 68pan ID 1,269 ? 102 626 ? 95 511 ? 60pan 2A 717 ? 56 494 ? 60 2B 903 ? 58 370 ? 65 2C 1,600 ? 123 1,110 + 285 197 ? 20P- 2D 1,989 ? 95 583 ? 154 804 ? 97p" 3A 152 ? 24 3Bch 153 ? 14 225 ? 27 3Bped 1,025 ? 122 3Cch 214 ? 15 264 ? 36 3C ped 1,394 ? 107 3D 867 ? 62 4A 4B ch 236 ?19 371 ? 70 4B ped 2,744 ? 275 4C ch 240 ? 11 392 ? 31 4C ped 2,761 ? 230 4D 1,062 ? 112 One measurementrecorded.

The growth of individual plants was greatest for S. maritimus surpass the maximum val- on transect 2, with a maximum average ues for C. lyngbyei, and leaf areas per shoot height of 157 cm and a maximum rate of are comparable when S. maritimus in saline height increase of 16 cm wk-1. Values on sites on transects 3 and 4 is compared with transect 1 were only slightly lower. E. pa- C. lyngbyei in freshwater sites on transect 1 lustris is only about 1.5 mm in diameter in (Table 2). Shoot densities for S. maritimus, the majority of sites at the Skagit, but it however, are much lower than those of C. increases surface area at the rate of about 1 lyngbyei (Table 3). Scirpus maritimus is not cm2 d-1, developing 35 to 76 cm2 of surface found in a wide range of environments at per shoot (Table 2). Increased shoot density the Skagit. It flourishes in soft, poorly con- was correlated with less investment per solidated soils, which are almost always an- shoot, a trend noted for C. lyngbyei. Within oxic, at higher salinities (8-12%o), and with- the range of sites where E. palustris grows, in a narrow range of elevations. is not a of its salinity good predictor growth. Discussion Sand and clay content of the soil are the best predictors (Ewing 1982), with the best PRODUCTIVITY growth occurring where clay content is high- The maximum standing crop at the Skagit est and sand content lowest. (1,742 g m-2 dry weight) may be compared to other maxima measured in Carex lyng- maritimus Scirpus byei-dominated Northwest coastal marsh- Scirpus maritimus was limited to the two es: 1,390 g m-2 in southern Puget Sound more saline transects at the site. A robust (Burg et al. 1976), 2,629 g m-2 on the Or- plant, S. maritimus displayed growth of in- egon coast (Eilers 1975), 1,355 gm-2 in Brit- dividual shoots in saline sites which was ish Columbia (Levings and Moody 1976), comparable to that of C. lyngbyei in fresh- 1,629 g m-2 at Nooksack Bay, Washington water sites. Its maximum average height was (Disraeli and Fonda 1978), 735 g m-2 in 124 cm. The maximum rate of height in- British Columbia (Kistritz and Yesaki 1979), crease was 8 cm wk-~1.The shoot dry weights 1,280 g m-2 in Oregon (Kibby et al. 1980), 60 K. Ewing

1,081 g m-2 in Oregon (Hoffnagle 1980), less productive (and more saline) areas, 466 g m-2 in Oregon (Taylor 1980). Because growth rates are lower, and an early and brackish intertidal marshes are often dis- pronounced cessation of growth is less com- tributed along complex environmental gra- mon. dients, the use of a single productivity value GROWTHTRENDS to characterize a marsh or from which to Species which occur in both saline and calculate total production not be ac- may freshwater parts of the marsh exhibit a trend curate. The use of weighted means for cal- toward less investment per shoot as sites culating marsh productivity (Glooschenko become more saline. Leaf area per shoot and Clarke 1982) may also be misleading; also decreases, even for Scirpus americanus, this technique assumes a constant biomass which does not show a loss of aboveground value within each vegetation zone and productivity as salinity increases. For Carex weights the value by multiplying it by the lyngbyei, shoot density increases as the in- zone width. Kershaw (1976) found that what vestment per shoot and leaf area per shoot appeared to be distinct salt marsh zonation decrease. The same compensation occurs for from the air was actually "a continuous se- Eleocharis palustris and for S. americanus quence of species distribution" (page The 8). in its bayside locations; for S. americanus visual impression was a function of the dis- the increased density is sufficient to main- tributional limits of dominant species with tain its aboveground yield at about the same contrasting morphologies. The variation in level at all four of the bayside measuring performance of a single species within its stations, even where increases and distributional limits has been demonstrated salinity while per shoot decreases. in this and it is linked with weight study, closely A second trend observed in shoot den- environmental factors. Standing crop, as well sities is a significant increase toward the bay as plant growth rates, timing, and growth for C. S. americanus, and S. mar- form are sensitive to environmental differ- lyngbyei, itimus, the species which dominate the three ences. Although the maximum value of community types covering most of the area standing crop in an almost pure C. lyngbyei of Skagit Marsh. For these species, the in- sward in the less saline part of the Skagit crease in shoot density from the dike at the Marsh was over 1,700 g m-2 dry weight, upper edge of the intertidal to the outer values decreased toward edge average alongshore of at is more saline areas of the marsh, where the vegetation bayside accompanied by a drop in community diversity. Not only do average standing crop was about 600 g m-2 most competing species of the canopy dis- dry weight. No trend in yield was apparent appear, but so do the smaller species which from the upper marsh toward the bay. Pro- grow predominantly in the mud layer and ductivity changed alongshore, and so did in pannes. community structure and composition, with Tied to increases in aboveground pro- C. lyngbyei becoming less of a dominant duction of C. lyngbyei, S. americanus, and species in more saline sites, absent alto- S. maritimus is a decrease in the proportion gether at some of the bayside sites where of MOM (live and dead) in the soil Scirpus americanus contributed all but a (Ewing 1982). Although not a direct measure of the small percentage of the standing crop. ratio of annual aboveground and be- As productivity varied alongshore at the lowground productivity, the changing ratio Skagit, so did a number of other parameters of aboveground production to organic mat- of growth. Production and growth occur very ter in the soil indicate either an increase rapidly in Northwest brackish intertidal may in the root-shoot ratio or a marshes, with almost all of the greater propor- aboveground tional allocation to the crop produced in the six weeks between the belowground storage compartment or structural tis- first of May and mid-June. Shoot belowground elongation sue in more stressful environments. and the increase of dry weight and leaf area stop between mid-June and the first of July COMPLEXITY OF RESPONSES at many of the measuring stations in the Salinity in the free soil water, soil texture, more productive parts of the marsh. In the elevation, and soil redox potential all vary NorthwestIntertidal Marsh Productivity 61

across the Skagit Marsh. They do not vary mouth of a river or some other source of together, but form a complex pattern of en- fresh water, salinities vary, sediment dis- vironmental conditions. Each has been tribution varies, and soil texture varies. shown to be a good predictor of some aspect River currents, flooding, tides, coastal cur- of the performance, whether it be measured rents and storm energy each may create dif- by productivity, variation in growth param- ferent effects at any given location in the eters, or distribution, of the five species in- marsh. The resultant establishment of dif- vestigated. With the different combinations ferent plant communities across the marsh of environmental conditions which occur in leads to differences in sediment accretion, physically different locations in the marsh erosion, organic deposition, and soil oxy- come changes in the performance of each genation. Subsequently, conditions at a site of the species. Because the response of each impede establishment of the propagules of species is different, the complexity of the species not at that site. Within the distri- environment is magnified in the response butional range of those species which do of the species. populate a given community, productivity, Rather than evolving toward a common growth characteristics, phenology, and al- solution for dealing with the stresses of ex- location of photosynthate vary in a nonlin- isting in a coastal intertidal wetland, Carex ear fashion. The plant strategies that limit lyngbyei, Scirpus americanus, S. validus, S. and influence these performance character- maritimus, and Eleocharis palustris have istics and allocation patterns operate through each arrived at a unique functional solution, physiological mechanisms, and an under- using a particular strategy to reach it. When standing of them is important for the un- their performances are compared, there are derstanding of community processes such responses to environmental variation which as production, competition, and succession, are similar for some but not for all of the and species capabilities such as defense species. For example, all but S. americanus against stress, response to disturbance, and show decreased aboveground productivity response to resource availability. when salinities increase. Other responses are ACKNOWLEDGMENT similar for all species, e.g., shoot growth rates are depressed for individual shoots as sa- I wish to thankL. C. Bliss for supportingthis research linities increase. Some environmental con- at the University of Washington.Partial funding was provided by National Science Foundation grant no. ditions seem to be important for only one DEB-8009337. I would also like to thank K. A. Ker- or two species, e.g., soil texture for E. pa- shaw for the use of facilities of his laboratory at lustris and S. validus. For each species, some McMasterUniversity. J. H. H. Looney provided in- combination of environmental stress and valuableassistance with computeranalysis and critical review of the biotic stress is sufficient to eliminate it from manuscript. at least part of the study site: C. lyngbyei is LITERATURECITED not in low saline S. present elevation, sites; ARMSTRONG,W. 1967. The relationship between ox- americanus is not present at higher eleva- idation-reductionpotentials and oxygen diffusion tion, freshwater sites; S. palustris is found levels in some waterloggedorganic soils. Soil Sci. only in freshwater sites, S. maritimus only 18:27-33. in more saline sites, and S. validus strikes BURG,M. E., E. ROSENBERG,AND D. R. TRIPP. 1976. Vegetationassociations and primaryproductivity of a medium between them. On a smaller scale, the Nisqually salt marsh on southernPuget Sound, C. lyngbyei is absent from anoxic pannes, Washington,p. 104-109. In S. G. Herman and A. though E. palustris, S. validus and S. ameri- M. Wiedemann(eds.), Contributionsto the Natural canus are found there in freshwater sites, Historyof the SouthernPuget Sound Region, Wash- and ington. EvergreenState College, Olympia. S. maritimus and S. americanus, and CHAPMAN,V. J. 1960. Salt Marshes and Salt Deserts sometimes S. validus are found in them in of the World. Interscience,New York. more saline sites. CHAPMAN,V. J. 1976. Coastal Vegetation, 2nd Edi- Brackish intertidal wetlands can be poor tion. PergamonPress, Oxford. E. C. A. AND examples of species responding uniformly COLLIAS, E., BARNES, J. H. LINCOLN. 1973. Skagit Bay study: Dynamical oceanography to uniform changes in the environment. Be- final report.University of Washington,Department cause they are most often formed at the of Oceanography,Seattle. 62 K. Ewing

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