FLOWERING RECRUITMENT INTO A NEWLY RESTORED IN

ELKHORN SLOUGH~ CALIFORNIA.

A Thesis Presented to The Faculty of Moss Landing Marine Laboratories San Jose State University

In Partial Fulfillment of the Requirements for the Degree Master of Science in Marine Science

by

Melanie A. Mayer June 1987 ii

ABSTRACT

The colonization of a newly restored salt marsh by flowering was dominated by· the perennial, Salicornia virginica, and the annual, marina, Recruitment of both was higher at upper (1.4 - 1.6m above MLLW) than lower (1.2 - 1.4m) tidal elevations and near the entrance compared to areas furthest away, Total number of seedlings varied between 0 - 17/square meters during the first year, while there •·ere hundreds of~ virginica and thousands of S. marina seedlings/square meter during the second year.

At the end of the first year, the highest total cover was 25%. It increased to as hi~h as 90% by the end of the second year. Salicornia virginica increased froG an average cover of 3% after one year to 43% after t~o years.

Sper£ularia marina cover increased from an average of 6% after one year to 14% after two years. The third most common colonist, the annual Atriplex patula, primarily invaded the narrow wrack zone where debris was deposited by . Both h virginica and~ patula flo•·ered in the fall. S. marina flo~ered in late winter to fall, having the longest period of flowering and germination. Despite the tremendous recruitment of S. marina, the higher canopy of h virginica apparently shades the smaller h rna,ina plants and s~ould eventually cover mc,st of the ne~ ma~sh in one to two additional years. iii

TABLE OF CONTENTS

Page

ABSTRACT ii

ACKNOWLEDGEMENTS iv

LIST OF TABLES vi

LIST OF FIGGRES vii

INTRODUCTIO!i l

METHODS 5

RESETS l l

DISCUSSI'J!i 16

REFERE!iCES 22

TABLES 26

".-~a iv

ACKNO~LEDGEMENTS

There are a great number of people without whose help this research would not have been·completed, Thanks and appreciation are extended to Dr. Michael Foster, for providing invaluable assistance and guidance as the chairman of my committee. Thanks are extended to Dr. John Oliver for field direction, stimulating conversation, and for participating on my committee, Dr. Greg~r Caillie: is gratefully ackno~ledged for offering constructive criticis~ and for participating on my com1~ittee.

This research vas funde~ in part by NOAA, Office of Ocean and Coastal Resources Management, Sanctuary Programs Division.

Administrative support ~as provided by the Elkhorn Slough

Foundation.

Tnis research ~~s also su~~ported by the Elkhorn Slough

National Estuarine Research Reserve. The Reserve is managed by the California Department of Fish and Game whose support, especially that of manager Ken ~oore, is grate~ully ackno~ledged.

I wa11t to thank all of the Mos• Landing Marine

Laboratories staff personnel for their time and valued assistance throughout this project, in particular: Sheila

Baldridge, our librarian for her concern, patience and skills in locating references; Larry Jones, Preston Watwood, and [en

Delopst for 5ssistance with equipment, tools, and various v emergencies; Lynn McMasters for the excellent maps and graphics, Gail Johnston for general support and leading me through paperwork, and Dorthy Lydick for general assistance.

I wish to extend my gratitude to Dr. George Knauer for lending me a plankton net and TSK meter, and to Meritt Tuel for his help in designing the surface water sampling procedure,

I am grateful to all those who assisted with field research, Field assistants included my fellow Moss Landing

Marine Laboratory students, Special kudos to Brian Fadely for always being there, for dragging boats (and himself) through the mud, and for all the cookies. Special thanks are also due the Elkhorn Slourh Interpretive Guides in particular Peter and

Toni Young, Ruby Peterson, and Marge Reidpath.

Special thanks to the Benthic Buts for their unique insight and contagious enthusia~. I would also like to thank the Bubs for use of their co~puter.

My sincere apprecia~ion to my good friends Mark Sliger,

Keiko Sekiguchi, Mark Silberstein, Frances Cress~ell, and Steve

Horn. Their uns~aying support, tolerance, humor, and love made it all possible.

Finally, I extend tl1e deepest aprreciation to my fa~ily: to my parents for their support, love, understanding, and encouragement and to my brother Eric for his field assistance and g~neral SUf•port. vi

LIST OF TABLES

Table 1. Percentage of flowering Salicornia virginica in low and high elevations during the peak of the flowering season in August 1985. Plant number in parentheses. 26

Table 2. Comparison of the common flowering plant colonizers reported during the first year for the following restoration projects: Salmon River - Oregon, Muzzie Marsh - Sac Francisco , Hayward Shoreline - San Francisco Bay, Elkhorn Slough - Monterey Bay. 27 vii

LIST OF FIGURES

Figure 1. Map and location of the restoration area relative to Elkhorn Slough. Surface water samples were taken from the main channel of Elk"horn Slough down of the new marsh channel, (noted by o symbol). 28

Figure 2. South Marsh restoration area in the Elkhorn Slough National Estuarine Research Reserve. The three major study sites were the front, middle, and back benches. 30

Figure 3. Mean percent cover of Salicornia virginica and Spergularia marina at high and low elevations for the front, middle, and back benches at the end of the first and the second growing season. Each vertical bar represents one standard error above the mean (N=10). 32

Figure 4. Seasonal changes in mean densities (number per square meter) of Salicornia virginica plants at high and low elevation for the front, middle, and back benches for the second year Nov. 1984 to Oct. 1985. Each vertical bar represents one sta&dard error above the mean (N=lO). Note scale changes. 34

Figure 5. Seasonal changes in mean densities (number per square meter) of Spergularia marina plants at high and low elevation for the front, middle, and back benches for tl1e second year from Nov. 1984 to Oct. 1985. Each vertical bar represents one standard error above the mean (N=lO). Notice scale changes. 36

Figure 6. Germination and flowering chronology (months) for the three most abundant colonists in the restoration area: Sa1icornia virginica (perennial), Spergularia marina (annual), and Atriplex patu1a (annual) from Nov. 1984 to Oct. 1985. 38

Figure 7. Seasonal change in mean number of seeds per cubic meter of filtered surface water for the three most comm~n plants fou~d in the surface waters of Elkhorn Slough from Jan. 1985 to April 1986. No samples were taken in March, April, May, or July of 1985 or in March of 1986. Each vertical bar represents one standard error above the mean (li=4). Note scale changes. 40 1

INTRODGCTION

Plants invade new habitats primarily by dispersing seeds.

Such invasion is important over long periods of ecological or geological time for all plants, but dominates short-term changes in the population structure of annual plants (Cavers and Harper, 1967; Howe and Smallwood, 1982). Historical invasion patterns may be responsible for the zonation of adult plants in many communities (Cavers and Harper, 1967; Ranwell,

1972; Harper, 1917). Therefore, seed dispersal, germination, and seedling survival are of utmost importance in understanding the colonization of new habitats (Cavers and Harper, 1967;

Stalter and Batson, 19S9; ~iesen and Josselyn, 1981).

Despi:e the probable great importance of early life history traits to adult co~~u~ity structure, less is known about recruitment than about the ecology of established adult plants. Our knowled?e of seed dispersal, germination and growth comes primarily from laboratory and greenhouse studies.

Bhsic descriptions or experime~~s examining the recruitment process in the field are few (Harper, 1977; Fenner, 1985).

The history of occupation of the shoreline by salt marsh plants has been explored by coring intertidal sediments in marshes from several geog~aphic locations. Root mats and pollen in the~e cores can reveal shifts i~ the species co~position of established plants over thousands of years (Niering and Warren,

1980). Such cores suggest a model of morst development that 2 involves a gradual seaward and landward extension of salt marsh plants strongly tied to changes in sea level (Redfield, 1972;

Keene, 1971; Niering and Warren, 1980, Schwartz, et al., 1986).

This extension can result from vegetative growth of established plants or from recruitment but core data cannot reveal the relative importance of recruitment process because recruitment occurs over a short time period. In addition to vegetative expansion at margins, cores reveal that episodic disturbances such as freezing and ice gouging (~iering and Warren, 1975;

Clark and Patterson, 1985) can create open space for colonization within an established mars~.

Studies of present day syste~s have found episodic disturbances such as storms (Zedler, et al., 1986), wrack deposition (Ran~ell, 196~; Oliver afid ~ayer, in review), fires, salinity changes (Zedler et al., 1930), and other erosion and depositional events (Redfield, 1972; Jefferies, et al., 1979;

Harris, 19S4) als0 cause ope~ings in the est3blished marsh where colonizatic·n can occur.

We know little about the importance of recruitment to plant distribution in salt marshes. Most field work has been descriptive, and has de< with one annual species (Salicornia europea) where yearly recruitment is clearly important in maintaining population and community patterns (Wiehe, 1935;

Ungar, 1981; Jefferies, et al. 1981). Most salt marshes a~e dominated by perennial plants, and changes in the cornffiunity structure after recruitment primarily involves vegetative 3 growth (Ranwell, 1972; Zedler, 1982; Josselyn, 1983; Clark and

Patterson, 1985).

Before vegetative processes can dominate, the seeds must reach the area and germinated seedlings must survive. There is general agreement that salt marsh seeds are dispersed to new uncolonized areas primarily by seawater (Stevenson and Emery,

1958; Dalby, 1963; Ranwell, 1972; Waisel, 1972). Some salt marsh plants may be better adapted to colonize open areas than others (Ball and Brown, 1970). Once a seed germinates in a new area, there are a variety of physical factors such as soil, light, nutrients, and moisture that may effect a seedlings survival C•aisel, 1972; Fenner, 1985). Submergence and tides is can be a factor in establishing new areas (Stevenson and Emerv,

1958). However, a seedling may be greatly affected by the presence of other species' seedliGgs (Ball and Brown, 1970) acd the presence of neighboring plants and seedlings may be the greatest single factor affecting survival (Fenner, 1985).

As seed recruitruent, germina~ion, and seedling survival are essential in establishing ne~ marshes and are important in invading parts of existing systems after disturbance (Ranwell,

1972; Niesen and Josselyn, 1951), the initial colonization period is particularly interesting for it can be used to examine the importance of initial colonization to patterns observej in the established marsh. Ma~-rnade salt marsh restoration areas are ideal places for study of recruitment anrl coloniza~_ion. SiEce over 90% of California 4 coastal wetlands has been destroyed by human activities

(Atwater, 1979; Josselyn, 1983), there is now a major effort to

restore coastal wetland habitats (Zedler, 1983; Josselyn, 1982;

Josselyn, et al., 1984) and to gather needed colonization

information useful in planning and designing additional

restoration projects (Race, 1985).

This study explores the first two years of salt marsh

plant colonization in a restored marsh in the Elkhorn Slough

National Estuarine Research Reserve. The objectives were to

identify the initial vascular plant colonists, to describe

their distribution and abundance patterns, to investigate

seedling abundance relative to elevation, and to examine the

importance of water dispersal to colonization. 5

METHODS

Studv Site

All field work, except collection of surface seed samples, was done in the newly restored South Marsh of the

Elkhorn Slough National Estuarine Research Reserve, directly adjacent to the eastern side of Elkhorn Slough (Figure 1).

Elkhorn Slough is a tidally influenced coastal embayment and seasonal estuary located in Monterey Bay, California, and the main channel, averaging 100 meters in width, is bordered by extensive tidal Salicornia virginica salt marsh and intertidal (Gordon, 1972; MacDonald and Barbour, 1974). Suartina spp. are conspicuously absent from Elkhorn Slough (MacDonald and Barbour, 1974). Core analyses have shown that the salt marshes of Elkhorn Sloug~ historically have expanded toward the slough's axis by slo~ sedimentation, but the installation of jetties in Moss Landing Harbor at the slough mouth in the 1940s has changed the natural sequence creating a stable estuarine embayment (Schwartz, et al., 1986).

The 200+ acre marsh restoration site was originally a salt marsh, but 40 years ago it was isolated by dikes and draining, and the inner area subsided. Therefore, parts of the area were built up in a series of small and benches parallel to each other and separated by channels prior to re-opening (Figure 2). In all, 24 benches roughly 91 m long and 15 m wide were built that had elevations suitable for the colonization of salt marsh plants. Elevation varied between and 6 within benches, and many had elevations closer to upland marsh

[+1.8 m (+6.0 ft.) MLLW and greater] near the extreme ends and low marsh [+0.9 m (+3.0 ft) MLLW and less] in mid-bench, . Therefore, few of these benches were identical or even similar.

The entire restored area had been watered dairy cow pasture for over 40 years. Qualitative walking surveys taken in

1981 before restoration found the area to be nearly devoid of salt marsh plants.

Colonization Studies

The new marsh was opene~ to tidal influence on October 6,

1983. All the benches on the east (Figure 2) were sampled for the first time in May 1984, when the first seedlings were located on benches. No seedlings were observed in monthly walks of the area prior to this time. The benches were sampled at a low [-1.2- l.4c ( 4- 4.5 ft.) above MLLW] and high [-1.4 - l.6m (-4.5 - 5 ft.) above MLLW] elevation.

The eleva~ion was determined by observing the level of tidal inundation for known peaks and lows, and from early plant patterns. The total number of seedlings in each of ten square meter random quadrats was counted for each species. Seedlings were identified based on prior observations of seedlings growing to adults. Sampling was repeated for the same benches in October 1984, and the percent cover of each species for each qua~rat ~ere visually esti~ated.

In October 1984 three benches were chosen for long-term monitoring at the front, middle, and back of the new marsh 7

(Figure 2), These benches were chosen because they had less variation in form and elevation, Personal observations of the three chosen benches indicated that other factors, such as sediment, dessication, nutrients, and grazing pressure were similar so I assumed that conditions were adequate for this study, Because of the form and elevation variations between all other benches, the data collected during the first year from these dissimilar benches were not used. The three benches were located at the front, middle, and back of the neK area to evaluate distribution relative to the mouth.

A high and a lo~ elevation permanent station was selected on each bench based on tidal inundation observations and the location of earliest plant patterns (e.g., where

Atriplex patula occured in the Krack line) and on an elevational survey tied to a railroad benchmark. The low elevation was 1.2 - 1.4 m (4.0 - 4.6 ft) above MLLW, and the high elevation was 1.4- 1.5 m (4.6- 5.2 ft) above MLL~. Each elevational area was staked during the elevational survey,

Coloniza:ioE at each staked station was quantified by counting the number of vascular plants in ten 1 square meter,

625 square centimeters, or 225 square centimeters randomly placed quadrats, Quadrat size was subjectively determined by the density of seedlings, with smaller quadrats used during the germination season (De:e~ter-May) and the large quadrats during the summer growing season vhen numbers declined. It is unlikely that the change in quadrat size affected results as the numbers 8 were very high (hundreds to thousands) when smaller quadrats were used. Patchiness was not considered a factor as patches only occurred on small scale (-lOcm) within each station and the quadrat size and number of random ~amples were large. These counts were made monthly in mid-month for each species starting in November 1984 and were used to determine changes in the average number of each species over two years.

Because Salicornia virginica is dioecious, counts of the number of plants of each sex in flower in each quadrat were recorded during the 1985 flowering season (August- September).

The number of S. virginica males and females in bloom were tested for a 1:1 sex ratio usin2 a Chi-Square test (Zar, 1974).

The percent of~ virginica in flo,

Colonization was further documented by determining the percent cover. Near and at the end of the growing season

(August through November, 1985) of the second year, the percent cover for each species was visually estimated in the same quadrats and at the same staked stations as the counts. The highest percent cover average for each station was compared betwee~ 19~! and 1985.

While sampling each area, qualitative observations of the sizE of seedlings and presence of flowers for species other 9

than~ virginica were recorded. This information was used to

create a germination and flowering history for the three most abundant plants in the new area,

All the east shore benches were surveyed each summer for relatively rare plant colonists (those that occurred in only

<1% of all quadrats or none of the quadrats). The locations of

these colonists were recorded on a map. When possible, the

source of the rare species was identified as seed or vegetative

growth. Rarer species were marked with treated stakes (to

reduce stake rotting in water).

To determine the avai1ablity of seeds dispersed in water,

the relative numbers and kinds of seeds found floatinG on the

water surface in the main channel of Elkhorn Slough were

sa~pled from January 1985 to April 1986 with a 0.3 mm mesh, 1 m

diameter mouth ope~ing plankton net. Four sa~ples were taken in

the middle of an outgoing following a high of at least

1.Sm (5.0 ft) above MLLW and the following low, Surface water

was sampled when such a tidal series occured during the

daytime. A 4.8 m (16 ft) Boston whaler was anchored within the

main channel (Figure 1) and the net held halfway below the

surface for three minutes, allowing the current to passively

move through the net. The volume of water passing through the

net was measured with a TSK current meter inside the net mouth.

The nu~ber an1 identification of seeds for each sample were

determined using a dissecting microscope. Salt marsh seeds

were identified by comparison with seeds collected from known 10 adult plants, Because it was very difficult to distinguish

Atriplex semibaccata seeds from Atriplex patula seeds, these seeds were grouped together as Atriplex spp .• Number of seeds for all salt marsh species was calculated as mean densities per cubic meter of water filtered. 11

RESULTS

Three species were the most abundant during the first two

years: Atriplex patula (annual), Spergularia marina (annual),

and Salicornia virginica (perenniai). Atriplex patula was only

observed in the area near the railroad dike before the return

to tidal influence and it was virtually the only species in the

wrack line after restoration. In contrast, Spergularia marina and Saliconia virginica tended to do~inate the

below the wrack area.

Other salt marsh species were relatively rare colonists,

including the perennials, Distichlis spicata that colonized

from small patches of vegetative pieces, and Frankenia

grandifolia that was not present before restoration and

colonized only the front of the ne~ marsh from seeds. A total

of 24 £...,_ grandifolia seedlings were found on the benches by the

end of the second year and all were on the west end of the

bench closest to the mouth. Other rare colonists invaded zones

above the high elevation sampling stations, these included

Atriplex seoibeccata, Grindelia latifolia, Cotula

coronopifolia, and Polvpogon monospeliensis. At the end of the

second year all seven species, other than the three most

abundant, were found to have plants in flower.

By the end of the first growing season (October 19S4) the

highest pla~= cover (25f) occurred at the high elevation on the

front bench (Figure 3). Spergularia marina was the most

important cover sp~cies. 12

Plant cover increased significantly by the end of the second growing season (October 1985), when the greatest plant cover was recorded at the high station on the middle bench.

Salicornia virginica and ~marina together covered 90% of this station. In the second year ~ virginca was the most abundant species in terms of cover.

Percent cover was higher at high elevations especially at the front and middle benches with the back bench occupied by less percent cover for .2._,__ virginica and .2._,__ marina for both years between elevations and with distance from the mouth

(Figure 3). Plant cover vas generally highest on the front and middle benches and much lover on the back bench with only one exception. The difference in pl!nt cover between the front/middle and back benches was most dramatic for~ marinE.

Seedling colonization duri~g the second year was unlike the first year, when the numbers of all species ranged froc

0-17/square meter on the benches. Durin£ the second year there

•·ere hundreds of~ viroinica seedlings and thousands of S. marina seedlings per s~uare meter on the sa~e benches.

In the second year, numbers of~ viroinica seedlings

peaked during Ja~uery throu§h April, especially at the high e!evaticn at the at the frunt and middle stations and at the

lo~ elevation front station (Figure 4). The high and low back, and lo~ rriddle stations ~ere cGlo~ized later and less abundantly. At both elevations mor? seedlings were found at the front be~ch staticr.s. 13

After initial colonization, high mortality generally occurred during late winter and spring (Figure 4). There were two lows (a result of mortality) for the high and low front stations in February and in spring, and a low at the high middle station in March and in spring. The low middle and high and low back station mortality occurred in the spring.

Mortality decreased for the summer and fall with numbers staying relatively stable.

Numbers of S. marina seedlings peaked highest during

January through April in the second year, especially at the front and back bench stations (Figure 5). A second, milder peak occurred at the high elevation stations of the front and midd2e benches in August. The back bench stations were colonized later and less abundantly. More seedlings ~ere found at the high elevatio~ stations of tl:e front and ba:k be~ches than at ot~er stations.

After initial colo~ization, high mo~tality generally occurred in spring (Figure 5) for all stations except the low middle station. At the lo~ middle station, numbers decreased from January to February followed by a mild increase in numbers

~ith spring mortality.

Salicornia virginica flo~ered synchronously in AuguEt and

Septerrber, when the ratio of male to fe~ale plants was not significertiy different fro~ 1:1 (ChJ square te•:; P>O.lO).

There ~ere variations in percent flo~ering along the front, 14 middle, and back stations but no consistent trends were apparent,

Quantitative counts of ~ virginica and qualitative observations of the three most abundant colonists revealed variation in the timing of both germination and flowering

(Figure 6). Salicornia virginica germinated primarily from

January through March and flowered from August to September.

Spergularia marina had a longer period of flowering and germination, Atriplex patula had one distinct seasonal period of flowering and germination during the year like ~ virginica

•·hich is a perennial. Unlike h patula, ~marina had at least two generations present within one year. Many plants germinated in late fall and produced flowers by early spring. As the presence of floKers and germina:ion of seeds continued for many m~nths, two generations could co-occur by the end of the growing season. After an early period of rain during August

1985, mac.y new S. marina seedlings were found on the benches, further indicating that more than t~o generations of this species can be produced in one year.

Salicornia virginica seeds were relatively more abundant than those of any other species in surface water samples from the main channel of Elkhorn Slough (Figure 7), The mean number of ~ virginica seeds per cubic meter of •·ater filtered peaked in late fall and early winter with the highest numbers 3 occurring in January [means: 4.7 seeds/m ± 2.8 SD in 1985 and

4.6 seeds/m3 + 2.3 in 1936, (K=4)], Spergularia marina seed 15 numbers peaked in fall and early winter with the highest mean number of seeds occurring in October 1985, [mean = 0.6 seeds/m3

± 0.2, (N=4)]. In addition,~ marina seeds were present throughout the summer providing a possible seed source for a second germination after a summer storm. Atriplex spp. was less common than the other two most abundant plants and peaked in late fall and early winter. The largest peak in mean number of 3 seeds was in Febuary 1985 [1.0 seeds/m + 0.2, (N=4 for each)]. Atriplex spp. seeds were the only ones present in water samples throughout the year. Other salt marsh plant seeds were not found in water samples.

A fe~ germinated seeds of S. virginica were found in the 3 January plankton samples [0.045 sproutsirn + 0.066 in 1985 and

0.040 sprouts/m 3 ± 0.057 in 1985, (N=4)]. The germinated seeds occurrerl at the sa~e tiGe as initial geriina:ion in the ne~ marsh. 16

DISCUSSION

Two of the three most abundant species dominated the

intertidal zone of the new marsh. Salicornia virginica was the . dominant plant cover in the restored marsh within two years

after restoration (Figure 2). This was not surprising asS.

virginica is known to be an early colonist of new marsh habitat

(Niesen and Josselyn, 1981; Zedler, 1982). The bench habitats

were constructed at the elevation of the vegetated salt marsh

in the adjacent Elkhorn Slough (1.2 - 1.9 m above MLLW), where h virginica accounted for over 90;; of the plant cover (MacDonald and Barbour, 1974). Unlike h virginice, Spergularie

marina, the co-domi~ant pl3nt in the restored marsh, was

extremely rare i~ the adjacent wetland habitats in and around

Elk.horn Slough. Nevertheless, S. marina accounted for more

plant cover than S. vi:-)?ir:ica during the first year (Figure 3),

and produced an order of magnitude more seedlings than h

virginica during the second year (Figures 4 and 5). Both

domina~t intertidal colonizers ~ere also dominants in other

~est restorations during the first year following

restoration (Table 2).

The winter/early spring peak in numbers of both h

virginica and h marina was related to a higher amount of seed

germination (Figures 4 and 5). The increase in seed germination

was rt:,c:: likely cause~ by the highe; amount of rainfall during

this seasoq, As seeds gErminated over the rainy season there

was an increase in the number of plants. That rain effects 17 germination is further indicated by the August increase in numbers of ~ marina which occurred following a summer rain

(Figure 5). A gradual decrease in overall numbers was caused by seedling mortality (Figures 4 a"nd 5). This mortality may have been caused by a variety of factors such as desiccation, submergence, light, and crowding. However, it is not possible to determine the exact cause of overall mortality as these factors were not monitored during this study.

Desiccation may be the major factor for the drop in S. virginica numbers observed on the front bench and high middle bench stations in late winter (Figure 4). Unlike the front bench, the front station on the middle bench vas somewhat shaded by an oak tree. Therefore, the seedling numbers here may have been less affected by dessication.

The general colonization pattern and water sam~les indicate that floating seeds entered the front marsh through the main entrance channel and spread to the back marsh.

Frankenia grandifolia seedlings were only observed close to the opening. Since very few salt marsh plants were present in the irrigated pasture before the restoration of tidal action, the entrance channel must have been the primary source of marsh seeds. This hypothesis is also supported by the presence of the seeds of the three major colonists in the surface waters of

Elkhorn Slou~~- The seeds of S. viroinica were most abundant.

These seeds appear to be adapted for dispersing to new areas by water. 18

While it appears from colonization patterns that~ grandifolia is water dispersed, its seeds were not found in surface water samples, Perhaps~ grandifolia seeds were absent because of their rarity or because"sampling was not done every month and dispersal periods were missed.

Greater plant cover and higher numbers of seedlings at most high elevation stations suggests elevation influenced plant patterns. Although the proportion of seeds germinating at the lo~er elevations was lo~er for S. marina, the total numbers of seedlings of ~ marina and ~ virginica were actually similar at the lo~ elevation (Figures 4 and 5). Very fe~ of the seedlings of either species at low elevations survived the entire growing season. Increased tidal submergence has been suggested as a major influence on established marsh patterns (Hinde, 1954; Ze.:ller, 19S2; Josselyr., 1983; Selika~, et al., 1983). ~y data suggest these patterns may result from the effects of submergence during initial colonization.

However, submergence may not be a factor that affects the flowering of S. virginica. Once established ~ virginica is known to be tolerant of many potentially stressful factors

(Zedler, 198:').

The life history of S. marina is well suited to initial invasion and rapid spread. The first~ marina colonists were obse~~ej in Moy 198,, They produced flo~ers before the end of the summer and large numbers of seeds germinated with the first fall rains (Figure 5). Some of these seedlings produced 19 flowers and seeds that germinated during the next spring.

Flowers and germinating seeds of~ marina were present for long periods during the year. In contrast, germinated seeds and flowers of ~ virginica and ~ patula were present for only a few months (Figure 6). Despite this ability to invade, S. marina spread to the back bench more slowly and accounted for much less of the second year plant cover than~ virginica.

Salicornia virginica apparently outcompetes Spergularia marina during the colonization of the new marsh. The limiting resource is probably light. The higher canopy of ~ virginica apparently shades the shorter ~ marina plants or inhibits the seed germination and/or seedling gro•·th of~ marina. The fe•· surviving seedlings of S. virginica gre ...; much larger and developed a higher canopy than S. marina. Such light reducing canopy effects have been found in other plant systems (Barbour, et al., 1973; Zedler, 1982; FenC~er, 1935), If this is the primary factor, ~marina shoulj have greater cover and persist for a longer time ~o·hen the ~ virginica canopy is experimentally removed. This experiment is in progress.

I" addition to desiccation, submergence and light, there are several factors that may affect seedling survival, such as soil type, nutrients, and chemistry. It is difficult to separate all the factors involved as they are probably not indepe~~ent of each other and they were not monitored during this study. Ho>."ever, because ~ virginica eventually dominated at all sta~ions and all species at all stations flowered, these 20 factors are probably suitable at all stations and there is no indication that they play a major role in producing the trends discussed here. If~ marina is less adapted to the physical conditions, it would not have been' as successful during the first year and should continue to do poorly even when ~ virginica is removed by weeding.

The third most abundant colonist in the marsh, Atriplex patula, primarily invaded the wrack line at the upper intertidal edge of the bench habitats, It has been an upper edge dominant in other restoration projects (Table 2; see also

Zedler, 1982). Wrack is deposited at the upper tidal level and seedlings in this area receive less subcergence, Perhaps A. patula seeds need the airv scbs~rete of woody debris to gErminate and/or tl1e seeds' outer ~ has a bouyancy similar to the wrack.

Although Jaucea carnosa is commonly found in Elkhorn

Slough, it had not colonized the new marsh after two years and has not been an initial col8nist in other restorations either

(Mitchell, 1981; Niesen and Josselyn, 1951; Faber, 1983). It is a Compositae and members of this family do not generally have water dispersed seeds (Fenner, 1985). Moreover, because seeds were not found in surface water sa~ples, ~ carnosa may depend on a less effective mea~s of dispersing to salt marsh habitat such as ~ind.

Colonists that were relatively rare and accounted for less than 1% of the plant cover two years after restoration may 21 also disperse by means other than water.

Distichlis spicata, Frankenia grandifolia, and Jaumea carnosa are perennial plants that commonly occupy tidal elevations above the broad Salico"rnia virginica zone in West

Coast marshes (MacDonald and Barbour, 1974; Zedler, 1982) including Elkhorn Slough (MacDonald and Barbour, 1974). Similar wetland zonation in other marshes has been explained by tolerance to salt water and emersion (Hinde, 1954; Selikar and

Gallagher, 1953) or by competition (Grace and Wetzel, 1951).

This zonatioo may also be caused by the colonizing ability of h virginica, "'·hich invades ne~· ~·etlar·r! habitat via water dispersal faster than any other perennial plant (Niesen and

Josselyn, 1961) and apparently outcompetes the annual species that colo~iz~ the sa~e zcne. Once the zone is occupied by the

persistent h vir£inic2, it rr.e.y be imr;oss2.~le for another

perenni5l species to invade the area, thus creating the pattern

of an established marsh within the first few years. While the

recruitl!.lent period occu~s over shorter "ecological" time, this

short period may have long lasting influeuce over "geological''

time. Invasion of ne~ wetland habitats may be the major

process that establishes plant zonation ~hen a perennial is

a~ong the first to colo~ize. 22

REFERENCES

Atwater, B.F., S.G. Conrad, T.N. Dowden, C.W. Redel, R.L. MacDonald, and W. Savage. 1979. History, , and vegetation of the estuarie~ tidal marshes, Pages 347-386 in Conomos, T.J. ed. San Francisco Bay: the urbanized estuary. Pacific Division, Amer. Assoc. for Advancement of Science, San Francisco, Calif.

Ball, P.W. and K.G. Brown. 1970. A biosystematic and ecological study of Salicornia in Dee estuary. Watsonia 8:27-40.

Barbour, M., R. Craig, F. Drysdale, and M. Ghiselin. 1973. Coastal ecology Bodega Head. Univ. Calif. Press, Berkeley, CA, 321pp.

Cavers, P. and T. Harper. 1967. Studies in the dynamics of plant populations, 1. The fate of seed and transplants introduced into various habitats. J. Ecol. 55:59-71.

Clark, J.S. and W.A. Patterson III. 1965. The development of a : upland and oceanic influences. Ecol. Monogr. 55:189-217.

Dalby, D. 1963. Seed dispersal in Salicornia pusilla. Nature. 199:197-195.

Faber, P. 1981. Marsh restoration: a case history froc California. Proceecings 6th annual conf. Coastal Soc, Arlington, Virginia, pp.

Fenner, M. 1985. Seed Ecology. Chapman and Hall, N.Y. 15lpp.

Gordon, B. 1977. Monterey Bay area: natural history and cultural ioprints. 2nd edition, Boxwood Press, Pacific Grove, CA, 321pp.

Harper, J. 1977. Population biology of plants. Academic Press, London, B92pp.

Harris, L.G. 198~. Community recovery after storm damage: a case of facilitation in primary succession. Science. 224:1336-1337.

Hinde, H. 1954. The vertical distribution of salt marsh p\An~~oga~~ in relation to tide levels. Ecol. Monogr. ~4:209-225. 23

Howe, H. and J. Smallwood. 1982. Ecology of seed dispersal. Ann. Rev. Ecol. Syst. 13:201-228.

Jefferies, R., A. Davy, and T. Rudmik. 1981. Population biology of the salt marsh annual Salicornia europea agg. J. Ecol. 69:17-31.

Jefferies, R., A. Jenson, and K.F. Braham. 1979. Vegetational development and the effect of geese on vegetation at La Perouse Bay, Manitoba. Canadian J. Bot. 57:1439-1450.

Josselyn, M. 1983. The ecology of San Francisco Bay tidal marshes: a community profile. U.S. Fish and Widl. Serv., Washington, D.C. FWS/OBS-83/23, 102pp.

Josselyn, M., J. Bucholz, and P. Romberg. 198L.. Marsh restoration in San Francisco Bay: a guide to design and planning. Tiburon Center for Environmental Studies. Tech. Rpt., Tiburon, Calif., 103pp.

Keene, H.W. 1971. Postglacial submergence and salt marsh evolution in New Hampshire. Maritime Sediments. 7:64-68.

MacDonald, K. and M. Barbour. 1974. and salt marsh vegetation of the North American Pacific coast. pp. 175-234, in R. Reimold and W. Queen, eds. Ecology of Halophytes. Academic Press, N.Y.

Mitchell, D.L. 1981. Salt marsh re-establishment after dike removal in the Salmon River Estuary, Lincoln County, Oregon. (abstracts of the sixth bier.nial conference), 4:261.

Niering, W.A. and R.S. Warren. 1975. Tidal wetlands of Connecticut I: vegetation and asso:iated animal populations. Dept. Env. Protection, State of Conn., Hartford, Conn.

Niering, W.A. and R.S. Warren. 1980. Vegetation patterns and processes in New England salt marshes. BioSci. 30:301-306.

Xiesen, T. and M. Josselyn. 1981. The Hayward Regional Shoreline Marsh restoration: biological succession during the first year following dike removal, Tech. Rpt. 1., Tiburon Cente~ for Environmental Studies, Tiburon, CA, 185pp.

Oliver, J.S. and M.A. Mayer. In review. Development of plant zonation and pre-emption of space during the colonization of a salt ffiBrsh. 24

Race, M.S. 1985. Critique of present wetlands mitigation policies in the United States based on an analysis of past restoration projects in San Francisco Bay. Env. Mgmt. 9:71-82.

Ranwell, D.S. 1964. III. Rates of establishment, succession, and nutrient supply at Bridgewater Bay, Somerset. J. Ecol. 52:95-105.

Ranwell, D.S. 1972. Ecology of salt marshes and . Chapman and Hall, London, 25Bpp.

Redfield, A.C. 1972. Development of a New England salt marsh. Ecol. Monogr. 42:201-237.

Schwartz, D.L., H.T. Mullins, and D.F. Belknap. 1986. Holocene geologic history of a transform mar~in estuary: Elkhorn Slough, Central California. Estuarine, Coast, end Shelf Sci. 22:285-302.

Selikar, D.~. and J.L. Gallagher. 1983. The ecology of tidal marshes of the Pacific Northwest coast: a community profile. U.S. Fish and Wildlife Service, Division of Biological Services, Washington, D.C. FWS/OBS-82/32, 65pp.

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Waisel, Y. 1972. Biologv of halophytes. Academic Press,London 395pp.

Wiehe, P. 1935. A quantitative study of the influence of tide upon populations of Salicornia europea. J. Ecol. 23:323-333.

Zar, J. 1974. Biostatistical Analysis. Prentice-Hall, Inc,, Engle~ood Cliffs, N.J., 62~pp. 25

Zedler, J.B. 1982. The ecology of Southern California coastal salt marshes: a community profile. U.S. Fish and ~ildlife Serv., Biol. Serv. Prog., Wash., D.C. FWS/OBS-81/54, llOpp.

Zedler, J.B. 1983. Salt marsh restoration: the experimental approach. Am. Soc. Civil Engr., New York. Coastal Zone 1983, 3:2578-2586.

Zedler, J.B., J. Covin, C. Nordby, P. Williams, and J. Boland. 1986. Catastrophic events reveal the dyna~ic nature of salt-marsh vegetation in Southern California. Estuaries, 9:75-80. Zedler, J.B., T. Winfield, and P. Williams. 1980. Salt marsh productivity with natural and altered tidal circulation. Oecol. 44:236-240. 26

Table l, Percentage of flowering Salicornia virginica in low and high elevations during the height of the flowering season in August 1985. Plant number in parentheses,

Bench Location LOil' • HIGH

Front 36% (15) 45% (68)

Middle 88% (25) 57% (14)

Back 65% (20) NA 27

Table 2. Comparison of the common flowering plant colonizers reported during the first year for the following restoration projects: Salmon River Estuary - Oregon, Muzzie Marsh - San Francisco Bay, Hayward Shoreline - San Francisco Bay, and Elkhorn Slough- Monterey Bay.

Project

Salmon 1 Muzzie 2 Hayward 3 Elkhorn Species:

Salicornia virginica D D D D

Salicornia europea p

Spergularia marina D D D D

Spergularia rubra p

Atriplex patula D p D D

Atriplex semibaccata p p

Cotula coronopifolia p p

Polypod on monospeliensis p

Distich lis spicata p

Frankenia grandifolia p p

Parapholis incurva p

Car ex lyngb>Ei D

Jaurnea carnosa p

D - present and dominant P- present, may or may not be dominant

1 Mitchell, 1981 2 Faber, 1933

3 Niesen and Josselyn, l9El 28

Figure l, Map and location of the restoration area relative to Elkhorn Slough. Surface water samples were taken from the main channel of Elkhorn Slough down current of the new marsh channel, (noted by o sy~b0l), Slough HALL ROAD

ELKHORN ROAD

0 Surface Water t Samples N '---' 1000 ft

". ' " 30

Figure 2, South Marsh restoration area in the Elkhorn Slough National Estuarine Research Reserve. The three major study sites were the front, middle, and back benches. terre stria I upland . marsh D. habitat tidal flats/ Dwater

<> islands ;~. ·:--..~ ~~ 32

Figure 3. Mean percent cover of Salicornia virginica and Spergularia marina at high and low elevations for the front, middle, and back benches at the end of the first and the second growing season. Each vertical bar represents one standard error above the mean (N=lO). HIGH LOW

75 75 Salicornia Salicornia

50 50

% o;o 25 25

0

75 §J:lerg u !aria 75 §_pergularia

50 50 year 1 o;o o/o -D year 2 25 25

0 Front Middle Back Front Middle Back 34

Figure 4, Seasonal change in mean densities (number per square meter) of Salicornia virginica plants at high and low elevation for the front, middle, and back benches from Nov. 1984 to Oct, 1985. Each vertical bar represents one standard error above the mean (N=lO), Note scale changes. Salicornia HIGH LOW 250 250

200 200

2 150 150 Front Front No./m 100 lOO

50 50

0 0 N J F M A J J A S 0 N J F M A J J A S 0

60 60

40 40 2 Middle Middle No./m

20 20

0 N J F M A J J A S 0 N J F M A J J A S 0

60 60

40 40 2 No./m Back Back

20 20

0 +--~....-..- N J F M A J J A S 0 N J F M A J J A S 0 1985 1985 Months Months 36

Figure 5. Seasonal changes in mean densities (number per square meter) of Spergularia marina plants at high and low elevation for the front, middle, and back benches from Nov. 1984 to Oct. 1985. Each vertical bar represents one standard error above the mean (N=10). Note scale changes. Spergularia HIGH LOW 10000 200

8000 150

6000 Front . Front 2 100 No./m 4000

50 2000

0 0 N J F M A J J A S 0 N J F M A J J A S 0

10000 200

8000 150 Middle Middle 6000 2 100 No./m 4000

50 2000

0 0 N J F M A J J A s 0 N J F M A J J A s 0 :u Back :u Back I ...... - -""" "'' N J F M A J J A S 0 N J F M A J J A S 0 1985 •• 1985 Months Months 38

Figure 6. Germination and flowering chronology (months) for the three most abundant colonists in the restoration area: Salicornia virginica (perennial), Spergularia marina (annual), and Atriplex patula (annual) from Nov. 1984 to Oct. 1985. JFMAMJJASOND Salicornia HHHl

1··.. I §r;1ergularia

HHHl

'-'-'---'1 germination lt'i'tttl flowering 40

Figure 7. Seasonal change in mean number of seeds per cubic meter of filtered surface water for the three most common plants found in the surface waters of Elkhorn Slough from Jan. 1985 to April 1986. No samples were taken in March, April, May, or July of 1985 or in March of 1986. Each vertical bar represents one standard error above the mean (N=4). Note scale changes. 6 Salicornia virginica--- 5 4 3 2

0 0 .I....Jif-J /alfl Ja Fb Jn Ag Sp Oe Nv De Ja Fb Ap 1985 1986

1 .00 Spergularia marina

0.75 Seeds/ m3 0.50

0.25

0.00 o~. '/ Ja Fb Jn Ag Sp Oe Nv De Ja Fb "Ap 1985 1986

Atriplex 2f!.f!.· 1.5

1.0

0.5

0.0 ,. "I'" It "f' ''·~·· ' "f' " Ja Fb Jn Ag Sp Oe Nv •De Ja• Fb Ap 1985 ' ' 1986