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Johnson et al 03
Estuaries Vol. 26, No. 1, p. 106–115 February 2003
Changes in the Abundance of the Seagrasses Zostera marina L.
(eelgrass) and Ruppia maritima L. (widgeongrass) in San Diego,
California, Following an El Nino Event
˜
MEGAN R. JOHNSON*, SUSAN L. WILLIAMS†, CAROLYN H. LIEBERMAN, and ARNE SOLBAK
Department of Biology, San Diego State University, San Diego, California 92182-4614
ABSTRACT: Changes in environmental conditions can be accompanied by shifts in the distribution and abundances of
organisms. When physical factors become unsuitable for growth of Zostera marina (eelgrass), which is a dominant seagrass
species in North America, other more ruderal seagrass species, including Ruppia maritima (widgeongrass), often increase
in abundance or replace the dominant species. We report the proliferation of widgeongrass into eelgrass beds in Mission
Bay and San Diego Bay in San Diego, California, during the 1997 to 1998 El Nino Southern Oscillation (ENSO). Wid-
˜
geongrass persisted in these eelgrass beds at least one year after a return to non-ENSO conditions and an increase in
eelgrass density. We suggest that a warming of the water in two bays in San Diego by 1.5–2.5 C could result in a permanent
shift in the local seagrass vegetation from eelgrass to widgeongrass. This shift could have substantial ecosystem-level
ramifications.
Introduction research has considered the effects of global cli-
Shifts in the distributions of species are major mate change, or its implications, on seagrasses
consequences of environmental change (Kareiva et (Thom 1990; Beer and Koch 1996; Williams and
al. 1993; Holbrook et al. 1997), and estuaries are Davis 1996; Short and Neckles 1999).
experiencing rapid changes in environmental con- El Nino Southern Oscillation (ENSO) events are
˜
ditions (Pulich and White 1981; Robblee et al. associated with conditions predicted to occur dur-
1991; Walker and McComb 1992; Short and Wyllie- ing global climate change (Schneider 1993), e.g.,
Echeverria 1996). The effects of anthropogenic increases in sea surface temperature and storm fre-
changes such as eutrophication and resultant an- quency and a rise in sea level (Tegner and Dayton
oxia, hydrologic modifications, dredging and fill- 1987). ENSOs provide scientists with an opportu-
ing, introduction of non-native species, and loss of nity to study ecological effects anticipated as the
wetlands have been well documented. The effects climate continues to change. An ENSO event in
of global climate change that are being superim- 1983 received public attention in southern Califor-
posed upon these other effects are poorly under- nia due to the costly damage to coastal ecosystems
stood. Increasing sea surface temperature and ris- and developments. Since the ENSO of 1983 there
ing sea level have been predicted to have impor- have been ENSOs in 1987, 1992, and 1997. The
tant effects on estuarine ecosystems (Michener et 1997 ENSO is referred to as May 1997–April 1998
al. 1997). Under global climate change, a shift in in this manuscript because National Oceanic and
the distribution of a foundation plant species Atmospheric Administration data indicate that ear-
could have major implications for ecosystem func- ly signs of the ENSO (including high sea-surface
tion because such plants play dominant roles in temperatures) were observed in the summer of
marine biogeochemical cycles and in providing 1997 and lasted until early 1998 (http://www.
habitat support for living resources. Effects of cli- elnino.noaa.gov). Based on ocean temperature
mate change on submersed plant species such as anomalies, the 1997 ENSO was the strongest of this
seagrass beds and salt marshes are of particular century and was twice as intense as the ENSOs of
concern because of the current extent of their loss 1987 and 1992 (http://www.elnino.noaa.gov).
and continued degradation and the importance of This study describes the expansion of Ruppia
the ecological functions they provide. Almost no maritima (widgeongrass) into Zostera marina (eel-
grass) beds in San Diego, California, during the
* Current address: Merkel and Associates, Inc., 5434 Ruffin 1997 ENSO. An emerging scenario in seagrass hab-
Road, San Diego, California 92123.
† Corresponding author; current address: Bodega Marine
itats is the replacement of well-studied dominant
Laboratory, University of California at Davis, P. O. Box 247, Bo- species, such as eelgrass, with marginal ones, such
dega Bay, California 94923; e-mail: slwilliams@ucdavis.edu. as widgeongrass, for which there is limited infor-
2003 Estuarine Research Federation 106
Changes in Seagrass Abundance 107
TABLE 1. Sampling dates, variables, techniques, frequencies, and sample sizes used at two sites in San Diego Bay and one in Mission
Bay. Sampling dates for water temperature data were during either El Nino Southern Oscillation (ENSO) or non-ENSO logging
˜
periods. Shoot density was measured for eelgrass. Seed crop and % cover were measured for wideongrass.
Bay/Site Variable Date Technique Frequency n
San Diego
Coronado Cays Seed Crop Jul 1998–Mar 2000 0.04-m2 cores Monthly 10
Silver Strand Water May 19–Jul 18, 1997 (ENSO); HOBO Every 70 min
Temperature May 19, 1998–Jul 31, 1999 and
Aug 20–Nov 18, 1999 (non-ENSO)
Shoot Density Jun 1993–Dec 1999; 0.25-m2 quadrats Monthly 40
Mission
Kendall-Frost Water Jan 1–Mar 3, 1996 (non-ENSO); HOBO Every 70 min
Temperature Sep 11, 1997–Feb 9, 1998 (ENSO);
Feb 10, 1998–Apr 9, 1998 and
May 30, 1998–Feb 9, 2000
(non-ENSO)
Shoot Density Jun 1993–Dec 1999; 0.25-m2 quadrats Monthly 40
% Cover Feb 1999–Aug 2000 0.5-m2 grided quadrats Monthly 10
mation. Environmental conditions in many coastal Materials and Methods
areas have changed or been degraded so severely This study was conducted at three eelgrass beds
that formerly abundant and dominant seagrasses and with various sampling techniques (Table 1).
like eelgrass and turtlegrass (Thalassia testudinum) The Kendall-Frost Reserve site is located in Mission
have declined greatly in abundance and have been Bay (32 47 29 N, 117 13 24 W), and the Silver
replaced by species that formerly were subdomi- Strand (32 38 08 N, 117 08 16 W) and Coronado
nant or ruderal (Lukatelich et al. 1987; Orth and
Cays (32 37 15 N, 117 07 36 W) are in south San
Moore 1988; Powell et al. 1991; Robblee et al.
Diego Bay, San Diego, California. Prior to and
1991; Fourqurean et al. 1995). Until environmen-
throughout the ENSO these three eelgrass beds
tal conditions again become favorable for the dom-
were healthy and persistent, and Silver Strand was
inant seagrasses, only subdominant or ruderal sea-
the largest and most genetically diverse eelgrass
grass species might be able to tolerate changed or
degraded environments (Thorne-Miller et al. 1983; population in San Diego County (Williams and Da-
Burkholder et al. 1994; Dunton 1996). vis 1996). Before 1997, widgeongrass had not been
Widgeongrass is a ruderal or opportunistic spe- quantified at Silver Strand or the Coronado Cays,
cies with wide environmental tolerances associated and was observed only in the intertidal mudflat ar-
with a virtually cosmopolitan distribution from the eas of Kendall-Frost. Our study was necessarily op-
arctic to the tropics (Setchell 1924; Anderson 1972; portunistic because we had not anticipated that
Verhoeven 1979; Kantrud 1991). Widgeongrass widgeongrass, which had been so limited within lo-
typically exists in more marginal seagrass habitats cal bays, would change so obviously in distribution
or as a subdominant species when conditions favor and abundance.
growth of the dominant seagrass species in North At Kendall-Frost, Silver Strand, and the Coro-
America (Orth 1977; Pulich 1985; Lazar and Dawes nado Cays widgeongrass typically grew from 0 to
1991). When environmental conditions are unfa- 1 m MLLW, which exposed the shallowest por-
vorable for the dominant seagrasses, widgeongrass tion of its distribution. The distribution of eelgrass
can proliferate. Broad environmental tolerances began at the lower depth limit of the widgeongrass
also account for the observation that widgeongrass and extended to approximately 3 m MLLW. Eel-
was the only species of the diverse aquatic angio- grass and widgeongrass coexisted within a small
sperm community to remain in the mesohaline to zone where the two species met. In San Diego, the
tidal freshwater portions of the upper Chesapeake period of maximum growth for widgeongrass and
Bay in 1990, after the major degradation of water eelgrass is from approximately May to October
quality bay-wide (Dennison et al. 1993). (Ewanchuk 1995; Lieberman 2002).
We present 6 years of monthly census data for The Kendall-Frost and Silver Strand study sites
eelgrass in two bays in San Diego, California, and were part of a long-term eelgrass monitoring pro-
describe the previously unobserved proliferation ject, which documented eelgrass leaf shoot density
of widgeongrass into local eelgrass beds during the and water temperature for over 6 years. From June
1997 ENSO. 1993 to December 1999, we censused the shoot
108 M. R. Johnson et al.
density of eelgrass at Kendall-Frost and Silver
Strand each month, except when weather or water
conditions prevented diving. Eelgrass shoots were
counted in 0.25-m2 quadrats (n 40) placed ran-
domly from a haphazardly chosen starting point in
the center of the bed. Within the eelgrass quadrats,
the presence of widgeongrass was noted but shoot
density was not counted. We present the percent
of all quadrats containing widgeongrass.
In order to assess the recruitment potential of
widgeongrass, we present data on the seed bank
and germination success collected at Coronado
Cays during a separate but concurrent study. Seeds
were collected on 5 dates between December 1999
and June 2000 using cores (400 cm2 to 10 cm sed-
iment depth, n 10) and seed density and ger- Fig. 1. Monthly average ( 95% CI) of the daily maximum
water temperature in the eelgrass bed at the Kendall-Frost Re-
mination status were measured. The average num- serve, Mission Bay, California. The graph displays temperatures
ber of seeds ( 1 SD) is presented. for the years 1996–2000. The ENSO period is May 1997–April
We began to monitor changes in the abundance 1998.
and distribution of widgeongrass at Kendall-Frost
because its proliferation was noted during a
monthly eelgrass survey. Widgeongrass at Kendall-
Frost was monitored on 11 sampling dates, sepa- due to a lack of data, water temperature was not
rated by at least 1 month, between February 1999 available for every month. Water temperature was
and August 2000. In order to describe the distri- compared at Silver Strand between ENSO (May–
bution of widgeongrass, permanent census sites (n July 1997, n 3) and non-ENSO years (May–July
10) were established every 5 m along two 50-m 1998 and 1999, n 6) and at Kendall-Frost be-
transects. These transects extended across the tween ENSO (September 1997–February 1998, n
depth range of the widgeongrass-eelgrass bed and 6) and non-ENSO years (September 1998–Feb-
were centered at the widgeongrass-eelgrass transi- ruary 1999 and September 1999–February 2000, n
tion zone. At each census site along the transects 12), where monthly averages were available for
a grided quadrat (0.5 m2) was used to estimate sea- all years. Because this study opportunistically in-
grass percent cover. Percent cover was used as an vestigated the effects of the ENSO, water temper-
estimate of seagrass abundance because widgeon- ature data before 1997 are discontinuous, necessi-
grass shoots are too dense and fine to count effi- tating the comparison of water temperatures in the
ciently in situ. The mean percent covers ( 1 SD) months during the ENSO to the temperatures in
of census Stations 1–5 (n 5) and 6–10 (n 5) the same months of the following years. Average
were calculated for each sampling date. Transect 2 monthly rainfall data were obtained from the Na-
was not censused from May 1999–August 2000 be- tional Weather Service for Lindberg Field, San Di-
cause it was lost due to human interference, but it ego, which is located on San Diego Bay roughly
was re-established in August 2000. The measure- halfway between Kendall-Frost in Mission Bay and
ment of widgeongrass percent cover was conduct- Silver Strand in San Diego Bay.
ed only at the Kendall-Frost site for logistic rea-
sons. Results
Throughout the eelgrass monitoring project, wa- Our data indicate an increase in the daily max-
ter temperature near the edge of each eelgrass bed imum water temperature of 1.5–2.5 C, depending
was logged (HOBO XT and Optic Stowaway, On- on the month, during the 1997 ENSO (May 1997–
set, Pocasset, Massachusetts 02559-3450) every 70 April 1998) in San Diego and Mission Bays (Figs.
min at Kendall-Frost and Silver Strand (Table 1). 1 and 2). There was little overlap between CIs
The water temperature at the Coronado Cays was around the average daily maximum water temper-
assumed to be similar to Silver Strand because of ature calculated for each month. The grand mean
close proximity ( Johnson 2000). In order to com- ( 95% CI) of the daily maximum water temper-
pare water temperature between ENSO and non- ature in Mission Bay (Kendall-Frost) averaged each
ENSO years, we calculated the 95% confidence in- month that data were available during the ENSO
tervals (CI) for monthly means of daily maximum (September 1997–Februar y 1998) was slightly
water temperature at both study sites. The ENSO higher (18.7 C 3.1, n 6) than during the same
time period was May 1997–April 1998 (12 mo) but, months of the non-ENSO years 1998 and 1999
Changes in Seagrass Abundance 109
TABLE 2. The number of days during which daily maximum
water temperatures exceeded critical thermal limits for eelgrass
in San Diego during 1997 (ENSO) and 1998 (non-ENSO). Data
represent the following time periods when temperature data
were available for both years: Kendall-Frost, Mission Bay: Sep-
tember 11–November 25, December 2–8, December 10–April 9
(total 204 d); Silver Strand, San Diego Bay: May 20–July 18
(total 60 d).
Critical Kendall Frost Silver Strand
Thermal
Limits1 ENSO Non-ENSO ENSO Non-ENSO
21 C 44 45 60 60
25 C 21 1 38 10
30 C 2 0 0 0
1 20 C is considered favorable for growth of Z. marina in this
region; 25 C is stressful; 30 C can result in shoot declines
(Phillips 1984; Thayer et al. 1984; Zimmerman et al. 1989).
Fig. 2. Monthly average ( 95% CI) of the daily maximum
water temperature in the eelgrass bed at Silver Strand, San Di-
ego Bay, California. The graph displays temperatures for the
years 1997–1999. The ENSO period is May 1997–April 1998.
clines during and following the ENSO (Fig. 3).
Starting with Kendall-Frost, the lowest densities ob-
served in the study occurred during the winter of
1995 (21 shoots m 2 36, mean 1 SD, n 40)
(17.4 C 1.9, n 12). The grand mean ( 95% when winter storms were very severe. Eelgrass den-
CI) of the daily maximum water temperature in sity recovered from the 1995 winter minimum only
San Diego Bay (Silver Strand) during the ENSO to decline again during ENSO to a similar mini-
(May–July 1997) was higher (25.4 C 0.6, n 3) mum and for a longer period (Fig. 3). The ENSO-
than the same months in 1998, 1999, and 2000 associated decline in eelgrass density lagged slight-
(23.3 C 1.6, n 6). Although water tempera- ly behind the rise in water temperature and con-
tures increased in both bays during the ENSO, the tinued through the summer of 1998. We compared
increase was greater in San Diego Bay (2.1 C) than mean densities in summer months (Figs. 4 and 5)
in Mission Bay (1.3 C). Although our temperature when water temperatures can exceed critical
records are discontinuous, they suggest that bay thresholds for eelgrass stress (Table 2). Prior to the
water temperatures were affected by the ENSO ENSO, the lowest monthly shoot density (125
event much like the ocean waters off San Diego, shoots m 2 45, n 40) observed during a sum-
where records are more continuous (http://
meteora.ucsd.edu/wx pages/scripps.html). During
ENSO, eelgrass was exposed to daily maximum wa-
ter temperatures above 25 C for 20–30 d longer
than during a normal year (Table 2). This temper-
ature represents a threshold above which eelgrass
typically exhibits stress (see Discussion).
Precipitation data for Lindbergh Field, on San Di-
ego Bay, (www.wrh.noaa.gov/sandiego/prec.html)
reveal that the average annual rainfall was 25.17
cm from 1950 to 2001 and 45.67 cm during the
ENSO period in 1997–1998. Precipitation was ap-
proximately 81% greater than the 50-yr average
during the period of time we refer to as the 1997
ENSO.
Eelgrass density in both bays varied seasonally
with minima typically occurring in late summer Fig. 3. Eelgrass leaf shoot density (mean 1 SD, n 40)
and early fall when bay temperatures, macroalgae, at Kendall-Frost Reserve, Mission Bay and Silver Strand, San Di-
and epiphytic anemones are highest (Ewanchuk ego Bay, California, from June 1993 to December 1999. The
1995; Sewell 1996) and in winter during periods of presence of widgeongrass (percent of quadrats with widgeon-
intense storms and rains and high turbidity (Sewell grass) within the eelgrass bed at Kendall-Frost was censused
from June 1998 to December 1999. Widgeongrass was observed
1996; Fig. 3, e.g., 1995). Superimposed upon such in census quadrats at Silver Strand on two dates, indicated by R
seasonal cycles were longer-term trends, such as re- on the graph. A line indicates the approximate duration of the
covery from the severe winter in 1995 and also de- ENSO.
110 M. R. Johnson et al.
Fig. 4. Comparison of eelgrass leaf shoot density (mean
1 SD, n 40) during the summer in years prior to, during, and Fig. 5. Comparison of eelgrass leaf shoot density (mean
following the ENSO at Kendall-Frost Reserve, Mission Bay, Cal- 1 SD, n 40) during the summer in years prior to, during, and
ifornia. following the ENSO at Silver Strand, San Diego Bay, California.
The eelgrass bed was sampled in September rather than August
during 1998.
mer month ( June, July, and August) at Kendall-
Strand recovered to pre-ENSO densities within
Frost occurred in August 1995 when eelgrass was
two years (Fig. 3).
rebounding from a bad winter (Fig. 4). During the
During the ENSO at Kendall-Frost, widgeongrass
6 years of observation, the lowest summer eelgrass
was observed in the eelgrass bed for the first time
density (32 shoots m 2 28, n 40) occurred
in our long-term subtidal census areas (Fig. 3). Its
following the ENSO in August 1999, a value 75%
abundance, measured as the percent of censused
less than the previous summer minimum, which
quadrats that contained widgeongrass, was high
occurred in August 1995. By the end of the study,
during October and November 1998 but after pro-
the monthly average densities in each season had
ducing flowering shoots in the fall, the bed began
not yet recovered to pre-ENSO values (Fig. 3).
to die back in December. The occurrence of wid-
Lack of a strong rebound in eelgrass after ENSO geongrass began to increase again in March 1999.
was associated with a proliferation of widgeongrass Although widgeongrass had been observed grow-
in the bed (Fig. 3, results to follow). ing in the adjacent salt marsh (Talley personal
Similar declines in eelgrass shoot density were communication), it had not previously been re-
observed at Silver Strand during the ENSO. Prior ported from this subtidal or intertidal eelgrass hab-
to the ENSO, eelgrass shoot densities tended to itat.
decline during the summer months when bay Following our initial observations of widgeon-
temperatures were maximum. Compared to Ken- grass in the eelgrass bed at Kendall-Frost, we as-
dall-Frost, shoot densities at Silver Strand were sessed the extent to which widgeongrass prolifer-
not as strongly affected by the winter conditions ated into the eelgrass bed by monitoring transects
of 1995. Prior to the ENSO, the lowest eelgrass at this site. During the ENSO, widgeongrass dis-
shoot densities (63 shoots m 2 49, n 40) at placed eelgrass at water depths of approximately 0
Silver Strand occurred in September 1993 (Fig. to 1 m MLLW (Stations 1–5) and was mixed with
3). The lowest density (23 shoots m 2 23, n eelgrass at the center of the bed (Figs. 6 and 7);
40) in this eelgrass bed over 6 yr of monitoring eelgrass dominated the areas at approximately 1 to
was observed in January 1998 during the ENSO. 3 m MLLW (Stations 6–10). For the 11 sampling
Eelgrass declined by 96% from the highest ob- dates that widgeongrass was measured, the grand
served density in February 1996 (593 shoots m 2 mean ( 1 SD) of widgeongrass percent cover at
189, n 40), which represented the most se- Stations 1–5 (34.2% 33.7, n 55) was about 6
vere decline in eelgrass density we observed in times greater than eelgrass cover (5.7% 13.5, n
this study. During the ENSO, the minimum sum- 55), but percent cover was highly variable for
mer density observed (85 shoots m 2 42, n both species. At Stations 6–10, the grand mean (
40) at Silver Strand occurred in August 1997 and 1 SD) of widgeongrass percent cover (11.8%
was 35% less than the lowest pre-ENSO summer 28.0, n 55) was about one third that of eelgrass
density (130 shoots m 2 96, n 40), which oc- (31.2% 38.5, n 55), but percent cover was also
curred in August 1993 (Fig. 5). Eelgrass at Silver highly variable for both species at these stations.
Changes in Seagrass Abundance 111
Fig. 6. Seasonal relative abundance (mean percent cover Fig. 7. Seasonal relative abundance (mean percent cover
1 SD, n 10) of eelgrass and widgeongrass along Transect 1 at 1 SD, n 10) of eelgrass and widgeongrass along Transect 2 at
Kendall-Frost Reserve, Mission Bay, California. Stations 1–5 are Kendall-Frost Reserve, Mission Bay, California. Stations 1–5 are
the shallow depths (approximately 0 to 1 m MLLW) and Sta- the shallow depths (approximately 0 to 1 m MLLW) and Sta-
tions 6–10 are the deeper depths (approximately 1 to 3 m tions 6–10 are the deeper depths (approximately 1 to 3 m
MLLW). MLLW). No data were collected from April 1999–August 2000
due to human interference.
The widgeongrass canopy died back dramatically
at the shallower stations in November, at the end pling of our established transect through the eel-
of the growing season for both seagrass species. grass bed, widgeongrass had completely died off
The eelgrass canopy persisted over the winter and along the transect, which was totally dominated by
began to increase in August when widgeongrass eelgrass (Figs. 6 and 7). In February 2000 we also
had not yet begun to grow back. Although our observed eelgrass seedlings in the widgeongrass
qualitative observations indicated that widgeon- bed above the mixed widgeongrass-eelgrass zone,
grass dominated the shallow portions of the tran- suggesting that eelgrass was beginning to regain
sect at Kendall-Frost (Transect 1; Fig. 6), its overall this habitat.
dominance along this transect might have been Prior to the ENSO, widgeongrass was observed
specific to that site. On the replicate transect that only once in the Silver Strand eelgrass bed in the
was lost during the sampling period (Transect 2; intertidal portion of the bed ( June 1992, Williams
Fig. 7), widgeongrass was more abundant than eel- personal observation). During the ENSO, wid-
grass in the shallow depths in the spring of 1999 geongrass was observed in eelgrass census quadrats
but had declined by August, based on the few sam- on two occasions in the Silver Strand eelgrass bed
pling dates. This and our qualitative observations (Fig. 3). Widgeongrass established better in the
at the site suggest the pattern along Transect 1 was shallower subtidal and intertidal portions of the
general at Kendall-Frost. bed, where we did not census eelgrass ( Johnson
Widgeongrass persisted at Kendall-Frost through 2000).
the summer of 2000 (Lieberman personal obser- When we began the study, we did not know
vation), despite increasing eelgrass abundance whether widgeongrass would survive the winter in
(Fig. 3). At one point in the sampling, widgeon- San Diego. Although it did die back dramatically
grass was observed beyond the lower depth limit in winter, it recovered in spring due to a combi-
of eelgrass ( 3 to 4 m MLLW). Widgeongrass nation of vegetative proliferation (Lieberman per-
did not continue to propagate into the eelgrass sonal observation) and possibly seedling recruit-
bed, at least along the transect. On the last sam- ment. We found a large seed crop of widgeongrass
112 M. R. Johnson et al.
TABLE 3. Total seed crop and seed germination of widgeon- petition from diminished eelgrass (Orth 1977;
grass (mean [ 1 SD], n 10) at Coronado Cays, San Diego Bird et al. 1994; Lieberman 2002) and more fa-
Bay. Seed crop is both germinated and ungerminated seeds.
vorable environmental conditions could have con-
Total Seed Crop
Seed Crop that
Germinated
tributed to the increased abundance of widgeon-
Date (seeds m 2) (seeds m 2) grass. Widgeongrass can maintain a maximum
December 8, 1999 2,103.4 (1,113.9) 0 photosynthetic rate at higher temperatures, and
January 10, 2000 915.7 (370.9) 73.1 (31.7) has a higher temperature optimum for growth,
March 26, 2000 2,506.1 (1,454.1) 23.5 (43.1) than eelgrass (Setchell 1924; Verhoeven 1979;
May 1, 2000 1,715.3 (893.0) 11.0 (23.1) Wetzel and Penhale 1983; Evans et al. 1986).
June 1, 2000 1,151.0 (660.0) 0
These optima are reported to occur around 25 C
and widgeongrass can apparently flourish in 36 C
(Edwards 1978) and tolerate 43 C in some cases
(Koch and Seeliger 1988). Widgeongrass, like eel-
at Coronado Cays and a small percentage of ger- grass, exhibits acclimation and adaptation to local
minated widgeongrass seeds (Table 3). conditions (Koch and Seeliger 1988; Koch and
Dawes 1991), and these limits should be consid-
Discussion ered as relative and average for this region. Re-
Coincident with ENSO conditions, eelgrass de- sults from experiments conducted in San Diego
clined and widgeongrass increased in some areas on the relative growth of widgeongrass and eel-
sampled in two bays in San Diego. Previous to this grass in response to temperature along with field
ENSO, widgeongrass was restricted to its typical tests of interspecific competition revealed that the
habitats, including salt marsh pans, on intertidal ability of eelgrass to outcompete widgeongrass was
flats of a commercial salt plant, and in the warm- compromised under ENSO temperatures (Lieber-
water effluent from a power plant (Williams per- man 2002).
sonal observation). Although we have insufficient There are other factors that limit the distribu-
environmental and experimental data to con- tion of widgeongrass, which we did not investigate.
clude that the shifts in distributions and abun- Widgeongrass can tolerate a wide range of salini-
dance were due to ENSO, water temperatures in- ties, but it tends to germinate and grow best in low-
creased well beyond the typical summer temper- salinity waters (Setchell 1924; Seeliger et al. 1984;
atures when eelgrass in San Diego is subject to Kantrud 1991; Koch and Dawes 1991). Unusually
chronic declines (Ewanchuk 1995; Sewell 1996). high rainfall resulting in lowered salinity observed
Eelgrass grows well between 10–20 C and reaches in south San Diego Bay during the ENSO (Merkel
maximum photosynthetic rates between 19–22 C, unpublished data) might have been a factor in the
although both acclimation and adaptation to local local expansion of widgeongrass through en-
conditions are important (reviewed in Phillips hanced seed germination and subsequent recruit-
1984 and Thayer et al. 1984; Zimmerman et al. ment. The limits of widgeongrass distribution are
1989). Zimmerman et al. (1989) suggested that also influenced by competition from other species,
temperatures 25 C represented stressful con- light, nutrients, and sea level (studies above; Orth
ditions for eelgrass growth and temperatures near and Moore 1988; Burkholder et al. 1994), factors
30 C could exceed the capacity for acclimation, not addressed in this study.
resulting in eelgrass decline. During ENSO, the Widgeongrass abundance might increase in
duration of exposure to temperatures stressful to many areas as the oceans warm, a premise based
eelgrass was substantially longer than a non-ENSO on the temperature tolerance and geographic dis-
year (Table 2). tribution of this species as well as the observations
We have since confirmed experimentally that we report here. Widgeongrass is distributed more
the temperatures reached during the ENSO event widely than other ruderal and subdominant sea-
stressed San Diego eelgrass. When grown outdoors grasses, including Halodule spp. and Halophila
in temperature-regulated mesocosms and allowed spp., which are restricted to warmer waters. Stud-
to acclimate for several months, local eelgrass pro- ies of seasonal dynamics in seagrass communities
duced 15–30% fewer shoots under ENSO water where widgeongrass is present indicate that it be-
temperatures than in waters 2–4 C cooler (Wil- comes abundant in summer months (Nixon and
liams 2001). These results were supported when a Oviatt 1973; Richardson 1980; Harrison 1982;
similar experiment was conducted in another year Evans et al. 1986; Kinnery and Roman 1998), and
(Lieberman 2002). widgeongrass has an annual growth cycle in lo-
To proliferate in eelgrass habitat, widgeongrass cations where ambient temperatures are too cool
would have to recruit after dispersing from its typ- (Harrison 1982; Pulich 1985; Flores-Verdugo et al.
ical habitats or from a seed bank. Reduced com- 1988; Dunton 1990). These studies support the
Changes in Seagrass Abundance 113
expectation that the distribution of widgeongrass any of its subagencies. M. R. Johnson was supported on a Sea
Grant traineeship on grant #NA666RGO477 to S. L. Williams
could increase with increasing ocean tempera- from the National Sea Grant College Program. M. R. Johnson
tures. Widgeongrass recruits would be expected was partially supported by a Grant in Aid of Research from the
to recruit relatively rapidly to new areas because Sigma Xi Society and a grant from the Lerner-Grey fund for
it has many vectors for dispersal as waterfowl and Marine Research. This is contribution no. 293 of the Coastal
fishes consume its seeds (Martin et al. 1961; Aga- and Marine Institute, San Diego State University and no. 2170
of the Bodega Marine Laboratory.
mi and Waisel 1988). It also recruits very well
from seeds (Van Vierssen et al. 1984; Koch and LITERATURE CITED
Seeliger 1988). The increase in the distribution of
AGAMI, M. AND Y. WAISEL. 1988. The role of fish in distribution
widgeongrass might be evident already (Bortulus and germination of seeds of the submerged macrophytes Na-
et al. 1998). jas marina L. and Ruppia maritima L. Oecologia 76:83–88.
If the proliferation of widgeongrass and the de- ANDERSON, R. R. 1972. Tentative outline for inventory of sub-
cline of eelgrass during the 1997 ENSO indicates merged aquatic vascular plants: Ruppia maritima L. (ditch-
grass). Chesapeake Science 13:S172–S174.
the future under a global warming scenario, then BEER, S. AND E. W. KOCH. 1996. Photosynthesis of marine ma-
there is an important need to understand the con- croalgae and seagrasses in globally changing CO2 environ-
sequences for seagrass ecosystems. The larger ments. Marine Ecology Progress Series 141:199–204.
dominant species in the Northern Hemisphere, BIRD, K. T., J. JEWETT-SMITH, AND M. S. FONSECA. 1994. Use of
e.g., eelgrass and turtlegrass, tend to have higher in vitro propagated Ruppia maritima for seagrass meadow res-
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ı
mary production than the subdominant species, lationship between waterfowl and the seagrass Ruppia maritima
which tend to have thinner leaves and higher or- in a southwestern Atlantic Coastal Lagoon. Estuaries 21:710–
ders of branching (McRoy and McMillan 1977; 717.
BURKHOLDER, J. M., H. B. GLASGOW, JR., AND J. E. COOKE. 1994.
Zieman and Wetzel 1980; Williams and McRoy Comparative effects of water-column nitrate enrichment on
1982; Thorne-Miller and Harlin 1984). The com- eelgrass Zostera marina, shoalgrass Halodule wrightii, and wid-
munity structure of associated fauna also can dif- geongrass Ruppia maritima. Marine Ecology Progress Series 105:
fer among seagrass species (Stoner 1980; Middle- 121–138.
ton et al. 1984; Jernakoff and Nielsen 1998; Wil- DENNISON, W. C., R. J. ORTH, K. A. MOORE, J. C. STEVENSON, V.
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widgeongrass beds, the proliferation of widgeon- DUNTON, K. H. 1990. Production ecology of Ruppia maritima L.
grass was studied at two additional sites in San s.l. and Halodule wrightii Aschers. in two subtropical estuaries.
Journal of Experimental Marine Biology and Ecology 143:147–164.
Diego Bay during a concurrent but separate study DUNTON, K. H. 1996. Photosynthetic production and biomass
that compared trophic support functions of eel- of the subtropical seagrass Halodule wrightii along an estuarine
grass and widgeongrass beds ( Johnson 2000). gradient. Estuaries 19:436–447.
This study indicated that widgeongrass main- EDWARDS, R. R. C. 1978. Ecology of a coastal lagoon complex in
tained biomass equivalent to that of eelgrass, but Mexico. Estuarine and Coastal Marine Science 6:75–92.
EVANS, A. S., K. L WEBB, AND P. A. PENHALE. 1986. Photosyn-
only in summer, and also provided nutritious food thetic temperature acclimation in two coexisting seagrasses,
to benthic detritivores. Results from this study and Zostera marina L. and Ruppia maritima L. Aquatic Botany 24:
ones cited above indicate that displacements of 185–197.
dominant species by subdominants, like widgeon- EWANCHUK, P. J. 1995. Population growth of eelgrass (Zostera
marina L.): The relative importance of sexual versus asexual
grass, could have complex effects on seagrass eco- reproduction. M.S. Thesis, San Diego State University, San
system functions. Diego, California.
FLORES-VERDUGO, F. F., J. W. DAY, L. MEE, AND R. BRISENO- ˜
ACKNOWLEDGMENTS DUENAS. 1988. Phytoplankton production and seasonal bio-
˜
mass variation of seagrass, Ruppia maritima L., in a tropical
We thank many for helping with diving and data manage- Mexican lagoon with an ephemeral inlet. Estuaries 11:51–56.
ment over the years of the eelgrass censuses: Chris Davis, Pat FOURQUREAN, J. W., G. V. N. POWELL, W. J. KENWORTHY, AND J.
Ewanchuk, Amy Sewell, Val Vucich, Shelley Glenn, Alex Cher- C. ZIEMAN. 1995. The effects of long-term manipulation of
oske, Bengt Allen, Jake Sibley, and Holly Hanson. Sampling nutrient supply on competition between the seagrasses Thal-
was conducted with permits from the Mission Bay Northern assia testudinum and Halodule wrightii in Florida Bay. Oikos 72:
Wildlife Refuge of the City of San Diego, Department of Parks 349–358.
and Recreation, and the Kendall-Frost Reserve of the Univer- HARRISON, P. G. 1982. Seasonal and year-to-year variations in
sity of California; we thank the managers for expediting the mixed intertidal populations of Zostera japonica Aschers. and
permit process. The manuscript was improved greatly by com- Graebn. and Ruppia maritima L. Aquatic Botany 14:357–371.
ments from Dr. Hilary Neckles and an anonymous reviewer. HOLBROOK, S. J., R. J. SCHMITT, AND J. S. STEPHENS. 1997. Chang-
This research was supported by grants to S. L. Williams from es in an assemblage of temperate reef fishes associated with
the National Oceanic and Atmospheric Administration a climate shift. Ecological Applications 7:1299–1310.
(NOAA) under grant #NA36RG0469 through the Coastal JERNAKOFF, P. AND J. NIELSEN. 1998. Plant-animal associations in
Ocean Program. The views expressed herein are those of the two species of seagrasses in Western Australia. Aquatic Botany
author and do not necessarily reflect the views of NOAA or 60:359–376.
114 M. R. Johnson et al.
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Changes in the Abundance of the Seagrasses Zostera marina L.
(eelgrass) and Ruppia maritima L. (widgeongrass) in San Diego,
California, Following an El Nino Event
˜
MEGAN R. JOHNSON*, SUSAN L. WILLIAMS†, CAROLYN H. LIEBERMAN, and ARNE SOLBAK
Department of Biology, San Diego State University, San Diego, California 92182-4614
ABSTRACT: Changes in environmental conditions can be accompanied by shifts in the distribution and abundances of
organisms. When physical factors become unsuitable for growth of Zostera marina (eelgrass), which is a dominant seagrass
species in North America, other more ruderal seagrass species, including Ruppia maritima (widgeongrass), often increase
in abundance or replace the dominant species. We report the proliferation of widgeongrass into eelgrass beds in Mission
Bay and San Diego Bay in San Diego, California, during the 1997 to 1998 El Nino Southern Oscillation (ENSO). Wid-
˜
geongrass persisted in these eelgrass beds at least one year after a return to non-ENSO conditions and an increase in
eelgrass density. We suggest that a warming of the water in two bays in San Diego by 1.5–2.5 C could result in a permanent
shift in the local seagrass vegetation from eelgrass to widgeongrass. This shift could have substantial ecosystem-level
ramifications.
Introduction research has considered the effects of global cli-
Shifts in the distributions of species are major mate change, or its implications, on seagrasses
consequences of environmental change (Kareiva et (Thom 1990; Beer and Koch 1996; Williams and
al. 1993; Holbrook et al. 1997), and estuaries are Davis 1996; Short and Neckles 1999).
experiencing rapid changes in environmental con- El Nino Southern Oscillation (ENSO) events are
˜
ditions (Pulich and White 1981; Robblee et al. associated with conditions predicted to occur dur-
1991; Walker and McComb 1992; Short and Wyllie- ing global climate change (Schneider 1993), e.g.,
Echeverria 1996). The effects of anthropogenic increases in sea surface temperature and storm fre-
changes such as eutrophication and resultant an- quency and a rise in sea level (Tegner and Dayton
oxia, hydrologic modifications, dredging and fill- 1987). ENSOs provide scientists with an opportu-
ing, introduction of non-native species, and loss of nity to study ecological effects anticipated as the
wetlands have been well documented. The effects climate continues to change. An ENSO event in
of global climate change that are being superim- 1983 received public attention in southern Califor-
posed upon these other effects are poorly under- nia due to the costly damage to coastal ecosystems
stood. Increasing sea surface temperature and ris- and developments. Since the ENSO of 1983 there
ing sea level have been predicted to have impor- have been ENSOs in 1987, 1992, and 1997. The
tant effects on estuarine ecosystems (Michener et 1997 ENSO is referred to as May 1997–April 1998
al. 1997). Under global climate change, a shift in in this manuscript because National Oceanic and
the distribution of a foundation plant species Atmospheric Administration data indicate that ear-
could have major implications for ecosystem func- ly signs of the ENSO (including high sea-surface
tion because such plants play dominant roles in temperatures) were observed in the summer of
marine biogeochemical cycles and in providing 1997 and lasted until early 1998 (http://www.
habitat support for living resources. Effects of cli- elnino.noaa.gov). Based on ocean temperature
mate change on submersed plant species such as anomalies, the 1997 ENSO was the strongest of this
seagrass beds and salt marshes are of particular century and was twice as intense as the ENSOs of
concern because of the current extent of their loss 1987 and 1992 (http://www.elnino.noaa.gov).
and continued degradation and the importance of This study describes the expansion of Ruppia
the ecological functions they provide. Almost no maritima (widgeongrass) into Zostera marina (eel-
grass) beds in San Diego, California, during the
* Current address: Merkel and Associates, Inc., 5434 Ruffin 1997 ENSO. An emerging scenario in seagrass hab-
Road, San Diego, California 92123.
† Corresponding author; current address: Bodega Marine
itats is the replacement of well-studied dominant
Laboratory, University of California at Davis, P. O. Box 247, Bo- species, such as eelgrass, with marginal ones, such
dega Bay, California 94923; e-mail: slwilliams@ucdavis.edu. as widgeongrass, for which there is limited infor-
2003 Estuarine Research Federation 106
Changes in Seagrass Abundance 107
TABLE 1. Sampling dates, variables, techniques, frequencies, and sample sizes used at two sites in San Diego Bay and one in Mission
Bay. Sampling dates for water temperature data were during either El Nino Southern Oscillation (ENSO) or non-ENSO logging
˜
periods. Shoot density was measured for eelgrass. Seed crop and % cover were measured for wideongrass.
Bay/Site Variable Date Technique Frequency n
San Diego
Coronado Cays Seed Crop Jul 1998–Mar 2000 0.04-m2 cores Monthly 10
Silver Strand Water May 19–Jul 18, 1997 (ENSO); HOBO Every 70 min
Temperature May 19, 1998–Jul 31, 1999 and
Aug 20–Nov 18, 1999 (non-ENSO)
Shoot Density Jun 1993–Dec 1999; 0.25-m2 quadrats Monthly 40
Mission
Kendall-Frost Water Jan 1–Mar 3, 1996 (non-ENSO); HOBO Every 70 min
Temperature Sep 11, 1997–Feb 9, 1998 (ENSO);
Feb 10, 1998–Apr 9, 1998 and
May 30, 1998–Feb 9, 2000
(non-ENSO)
Shoot Density Jun 1993–Dec 1999; 0.25-m2 quadrats Monthly 40
% Cover Feb 1999–Aug 2000 0.5-m2 grided quadrats Monthly 10
mation. Environmental conditions in many coastal Materials and Methods
areas have changed or been degraded so severely This study was conducted at three eelgrass beds
that formerly abundant and dominant seagrasses and with various sampling techniques (Table 1).
like eelgrass and turtlegrass (Thalassia testudinum) The Kendall-Frost Reserve site is located in Mission
have declined greatly in abundance and have been Bay (32 47 29 N, 117 13 24 W), and the Silver
replaced by species that formerly were subdomi- Strand (32 38 08 N, 117 08 16 W) and Coronado
nant or ruderal (Lukatelich et al. 1987; Orth and
Cays (32 37 15 N, 117 07 36 W) are in south San
Moore 1988; Powell et al. 1991; Robblee et al.
Diego Bay, San Diego, California. Prior to and
1991; Fourqurean et al. 1995). Until environmen-
throughout the ENSO these three eelgrass beds
tal conditions again become favorable for the dom-
were healthy and persistent, and Silver Strand was
inant seagrasses, only subdominant or ruderal sea-
the largest and most genetically diverse eelgrass
grass species might be able to tolerate changed or
degraded environments (Thorne-Miller et al. 1983; population in San Diego County (Williams and Da-
Burkholder et al. 1994; Dunton 1996). vis 1996). Before 1997, widgeongrass had not been
Widgeongrass is a ruderal or opportunistic spe- quantified at Silver Strand or the Coronado Cays,
cies with wide environmental tolerances associated and was observed only in the intertidal mudflat ar-
with a virtually cosmopolitan distribution from the eas of Kendall-Frost. Our study was necessarily op-
arctic to the tropics (Setchell 1924; Anderson 1972; portunistic because we had not anticipated that
Verhoeven 1979; Kantrud 1991). Widgeongrass widgeongrass, which had been so limited within lo-
typically exists in more marginal seagrass habitats cal bays, would change so obviously in distribution
or as a subdominant species when conditions favor and abundance.
growth of the dominant seagrass species in North At Kendall-Frost, Silver Strand, and the Coro-
America (Orth 1977; Pulich 1985; Lazar and Dawes nado Cays widgeongrass typically grew from 0 to
1991). When environmental conditions are unfa- 1 m MLLW, which exposed the shallowest por-
vorable for the dominant seagrasses, widgeongrass tion of its distribution. The distribution of eelgrass
can proliferate. Broad environmental tolerances began at the lower depth limit of the widgeongrass
also account for the observation that widgeongrass and extended to approximately 3 m MLLW. Eel-
was the only species of the diverse aquatic angio- grass and widgeongrass coexisted within a small
sperm community to remain in the mesohaline to zone where the two species met. In San Diego, the
tidal freshwater portions of the upper Chesapeake period of maximum growth for widgeongrass and
Bay in 1990, after the major degradation of water eelgrass is from approximately May to October
quality bay-wide (Dennison et al. 1993). (Ewanchuk 1995; Lieberman 2002).
We present 6 years of monthly census data for The Kendall-Frost and Silver Strand study sites
eelgrass in two bays in San Diego, California, and were part of a long-term eelgrass monitoring pro-
describe the previously unobserved proliferation ject, which documented eelgrass leaf shoot density
of widgeongrass into local eelgrass beds during the and water temperature for over 6 years. From June
1997 ENSO. 1993 to December 1999, we censused the shoot
108 M. R. Johnson et al.
density of eelgrass at Kendall-Frost and Silver
Strand each month, except when weather or water
conditions prevented diving. Eelgrass shoots were
counted in 0.25-m2 quadrats (n 40) placed ran-
domly from a haphazardly chosen starting point in
the center of the bed. Within the eelgrass quadrats,
the presence of widgeongrass was noted but shoot
density was not counted. We present the percent
of all quadrats containing widgeongrass.
In order to assess the recruitment potential of
widgeongrass, we present data on the seed bank
and germination success collected at Coronado
Cays during a separate but concurrent study. Seeds
were collected on 5 dates between December 1999
and June 2000 using cores (400 cm2 to 10 cm sed-
iment depth, n 10) and seed density and ger- Fig. 1. Monthly average ( 95% CI) of the daily maximum
water temperature in the eelgrass bed at the Kendall-Frost Re-
mination status were measured. The average num- serve, Mission Bay, California. The graph displays temperatures
ber of seeds ( 1 SD) is presented. for the years 1996–2000. The ENSO period is May 1997–April
We began to monitor changes in the abundance 1998.
and distribution of widgeongrass at Kendall-Frost
because its proliferation was noted during a
monthly eelgrass survey. Widgeongrass at Kendall-
Frost was monitored on 11 sampling dates, sepa- due to a lack of data, water temperature was not
rated by at least 1 month, between February 1999 available for every month. Water temperature was
and August 2000. In order to describe the distri- compared at Silver Strand between ENSO (May–
bution of widgeongrass, permanent census sites (n July 1997, n 3) and non-ENSO years (May–July
10) were established every 5 m along two 50-m 1998 and 1999, n 6) and at Kendall-Frost be-
transects. These transects extended across the tween ENSO (September 1997–February 1998, n
depth range of the widgeongrass-eelgrass bed and 6) and non-ENSO years (September 1998–Feb-
were centered at the widgeongrass-eelgrass transi- ruary 1999 and September 1999–February 2000, n
tion zone. At each census site along the transects 12), where monthly averages were available for
a grided quadrat (0.5 m2) was used to estimate sea- all years. Because this study opportunistically in-
grass percent cover. Percent cover was used as an vestigated the effects of the ENSO, water temper-
estimate of seagrass abundance because widgeon- ature data before 1997 are discontinuous, necessi-
grass shoots are too dense and fine to count effi- tating the comparison of water temperatures in the
ciently in situ. The mean percent covers ( 1 SD) months during the ENSO to the temperatures in
of census Stations 1–5 (n 5) and 6–10 (n 5) the same months of the following years. Average
were calculated for each sampling date. Transect 2 monthly rainfall data were obtained from the Na-
was not censused from May 1999–August 2000 be- tional Weather Service for Lindberg Field, San Di-
cause it was lost due to human interference, but it ego, which is located on San Diego Bay roughly
was re-established in August 2000. The measure- halfway between Kendall-Frost in Mission Bay and
ment of widgeongrass percent cover was conduct- Silver Strand in San Diego Bay.
ed only at the Kendall-Frost site for logistic rea-
sons. Results
Throughout the eelgrass monitoring project, wa- Our data indicate an increase in the daily max-
ter temperature near the edge of each eelgrass bed imum water temperature of 1.5–2.5 C, depending
was logged (HOBO XT and Optic Stowaway, On- on the month, during the 1997 ENSO (May 1997–
set, Pocasset, Massachusetts 02559-3450) every 70 April 1998) in San Diego and Mission Bays (Figs.
min at Kendall-Frost and Silver Strand (Table 1). 1 and 2). There was little overlap between CIs
The water temperature at the Coronado Cays was around the average daily maximum water temper-
assumed to be similar to Silver Strand because of ature calculated for each month. The grand mean
close proximity ( Johnson 2000). In order to com- ( 95% CI) of the daily maximum water temper-
pare water temperature between ENSO and non- ature in Mission Bay (Kendall-Frost) averaged each
ENSO years, we calculated the 95% confidence in- month that data were available during the ENSO
tervals (CI) for monthly means of daily maximum (September 1997–Februar y 1998) was slightly
water temperature at both study sites. The ENSO higher (18.7 C 3.1, n 6) than during the same
time period was May 1997–April 1998 (12 mo) but, months of the non-ENSO years 1998 and 1999
Changes in Seagrass Abundance 109
TABLE 2. The number of days during which daily maximum
water temperatures exceeded critical thermal limits for eelgrass
in San Diego during 1997 (ENSO) and 1998 (non-ENSO). Data
represent the following time periods when temperature data
were available for both years: Kendall-Frost, Mission Bay: Sep-
tember 11–November 25, December 2–8, December 10–April 9
(total 204 d); Silver Strand, San Diego Bay: May 20–July 18
(total 60 d).
Critical Kendall Frost Silver Strand
Thermal
Limits1 ENSO Non-ENSO ENSO Non-ENSO
21 C 44 45 60 60
25 C 21 1 38 10
30 C 2 0 0 0
1 20 C is considered favorable for growth of Z. marina in this
region; 25 C is stressful; 30 C can result in shoot declines
(Phillips 1984; Thayer et al. 1984; Zimmerman et al. 1989).
Fig. 2. Monthly average ( 95% CI) of the daily maximum
water temperature in the eelgrass bed at Silver Strand, San Di-
ego Bay, California. The graph displays temperatures for the
years 1997–1999. The ENSO period is May 1997–April 1998.
clines during and following the ENSO (Fig. 3).
Starting with Kendall-Frost, the lowest densities ob-
served in the study occurred during the winter of
1995 (21 shoots m 2 36, mean 1 SD, n 40)
(17.4 C 1.9, n 12). The grand mean ( 95% when winter storms were very severe. Eelgrass den-
CI) of the daily maximum water temperature in sity recovered from the 1995 winter minimum only
San Diego Bay (Silver Strand) during the ENSO to decline again during ENSO to a similar mini-
(May–July 1997) was higher (25.4 C 0.6, n 3) mum and for a longer period (Fig. 3). The ENSO-
than the same months in 1998, 1999, and 2000 associated decline in eelgrass density lagged slight-
(23.3 C 1.6, n 6). Although water tempera- ly behind the rise in water temperature and con-
tures increased in both bays during the ENSO, the tinued through the summer of 1998. We compared
increase was greater in San Diego Bay (2.1 C) than mean densities in summer months (Figs. 4 and 5)
in Mission Bay (1.3 C). Although our temperature when water temperatures can exceed critical
records are discontinuous, they suggest that bay thresholds for eelgrass stress (Table 2). Prior to the
water temperatures were affected by the ENSO ENSO, the lowest monthly shoot density (125
event much like the ocean waters off San Diego, shoots m 2 45, n 40) observed during a sum-
where records are more continuous (http://
meteora.ucsd.edu/wx pages/scripps.html). During
ENSO, eelgrass was exposed to daily maximum wa-
ter temperatures above 25 C for 20–30 d longer
than during a normal year (Table 2). This temper-
ature represents a threshold above which eelgrass
typically exhibits stress (see Discussion).
Precipitation data for Lindbergh Field, on San Di-
ego Bay, (www.wrh.noaa.gov/sandiego/prec.html)
reveal that the average annual rainfall was 25.17
cm from 1950 to 2001 and 45.67 cm during the
ENSO period in 1997–1998. Precipitation was ap-
proximately 81% greater than the 50-yr average
during the period of time we refer to as the 1997
ENSO.
Eelgrass density in both bays varied seasonally
with minima typically occurring in late summer Fig. 3. Eelgrass leaf shoot density (mean 1 SD, n 40)
and early fall when bay temperatures, macroalgae, at Kendall-Frost Reserve, Mission Bay and Silver Strand, San Di-
and epiphytic anemones are highest (Ewanchuk ego Bay, California, from June 1993 to December 1999. The
1995; Sewell 1996) and in winter during periods of presence of widgeongrass (percent of quadrats with widgeon-
intense storms and rains and high turbidity (Sewell grass) within the eelgrass bed at Kendall-Frost was censused
from June 1998 to December 1999. Widgeongrass was observed
1996; Fig. 3, e.g., 1995). Superimposed upon such in census quadrats at Silver Strand on two dates, indicated by R
seasonal cycles were longer-term trends, such as re- on the graph. A line indicates the approximate duration of the
covery from the severe winter in 1995 and also de- ENSO.
110 M. R. Johnson et al.
Fig. 4. Comparison of eelgrass leaf shoot density (mean
1 SD, n 40) during the summer in years prior to, during, and Fig. 5. Comparison of eelgrass leaf shoot density (mean
following the ENSO at Kendall-Frost Reserve, Mission Bay, Cal- 1 SD, n 40) during the summer in years prior to, during, and
ifornia. following the ENSO at Silver Strand, San Diego Bay, California.
The eelgrass bed was sampled in September rather than August
during 1998.
mer month ( June, July, and August) at Kendall-
Strand recovered to pre-ENSO densities within
Frost occurred in August 1995 when eelgrass was
two years (Fig. 3).
rebounding from a bad winter (Fig. 4). During the
During the ENSO at Kendall-Frost, widgeongrass
6 years of observation, the lowest summer eelgrass
was observed in the eelgrass bed for the first time
density (32 shoots m 2 28, n 40) occurred
in our long-term subtidal census areas (Fig. 3). Its
following the ENSO in August 1999, a value 75%
abundance, measured as the percent of censused
less than the previous summer minimum, which
quadrats that contained widgeongrass, was high
occurred in August 1995. By the end of the study,
during October and November 1998 but after pro-
the monthly average densities in each season had
ducing flowering shoots in the fall, the bed began
not yet recovered to pre-ENSO values (Fig. 3).
to die back in December. The occurrence of wid-
Lack of a strong rebound in eelgrass after ENSO geongrass began to increase again in March 1999.
was associated with a proliferation of widgeongrass Although widgeongrass had been observed grow-
in the bed (Fig. 3, results to follow). ing in the adjacent salt marsh (Talley personal
Similar declines in eelgrass shoot density were communication), it had not previously been re-
observed at Silver Strand during the ENSO. Prior ported from this subtidal or intertidal eelgrass hab-
to the ENSO, eelgrass shoot densities tended to itat.
decline during the summer months when bay Following our initial observations of widgeon-
temperatures were maximum. Compared to Ken- grass in the eelgrass bed at Kendall-Frost, we as-
dall-Frost, shoot densities at Silver Strand were sessed the extent to which widgeongrass prolifer-
not as strongly affected by the winter conditions ated into the eelgrass bed by monitoring transects
of 1995. Prior to the ENSO, the lowest eelgrass at this site. During the ENSO, widgeongrass dis-
shoot densities (63 shoots m 2 49, n 40) at placed eelgrass at water depths of approximately 0
Silver Strand occurred in September 1993 (Fig. to 1 m MLLW (Stations 1–5) and was mixed with
3). The lowest density (23 shoots m 2 23, n eelgrass at the center of the bed (Figs. 6 and 7);
40) in this eelgrass bed over 6 yr of monitoring eelgrass dominated the areas at approximately 1 to
was observed in January 1998 during the ENSO. 3 m MLLW (Stations 6–10). For the 11 sampling
Eelgrass declined by 96% from the highest ob- dates that widgeongrass was measured, the grand
served density in February 1996 (593 shoots m 2 mean ( 1 SD) of widgeongrass percent cover at
189, n 40), which represented the most se- Stations 1–5 (34.2% 33.7, n 55) was about 6
vere decline in eelgrass density we observed in times greater than eelgrass cover (5.7% 13.5, n
this study. During the ENSO, the minimum sum- 55), but percent cover was highly variable for
mer density observed (85 shoots m 2 42, n both species. At Stations 6–10, the grand mean (
40) at Silver Strand occurred in August 1997 and 1 SD) of widgeongrass percent cover (11.8%
was 35% less than the lowest pre-ENSO summer 28.0, n 55) was about one third that of eelgrass
density (130 shoots m 2 96, n 40), which oc- (31.2% 38.5, n 55), but percent cover was also
curred in August 1993 (Fig. 5). Eelgrass at Silver highly variable for both species at these stations.
Changes in Seagrass Abundance 111
Fig. 6. Seasonal relative abundance (mean percent cover Fig. 7. Seasonal relative abundance (mean percent cover
1 SD, n 10) of eelgrass and widgeongrass along Transect 1 at 1 SD, n 10) of eelgrass and widgeongrass along Transect 2 at
Kendall-Frost Reserve, Mission Bay, California. Stations 1–5 are Kendall-Frost Reserve, Mission Bay, California. Stations 1–5 are
the shallow depths (approximately 0 to 1 m MLLW) and Sta- the shallow depths (approximately 0 to 1 m MLLW) and Sta-
tions 6–10 are the deeper depths (approximately 1 to 3 m tions 6–10 are the deeper depths (approximately 1 to 3 m
MLLW). MLLW). No data were collected from April 1999–August 2000
due to human interference.
The widgeongrass canopy died back dramatically
at the shallower stations in November, at the end pling of our established transect through the eel-
of the growing season for both seagrass species. grass bed, widgeongrass had completely died off
The eelgrass canopy persisted over the winter and along the transect, which was totally dominated by
began to increase in August when widgeongrass eelgrass (Figs. 6 and 7). In February 2000 we also
had not yet begun to grow back. Although our observed eelgrass seedlings in the widgeongrass
qualitative observations indicated that widgeon- bed above the mixed widgeongrass-eelgrass zone,
grass dominated the shallow portions of the tran- suggesting that eelgrass was beginning to regain
sect at Kendall-Frost (Transect 1; Fig. 6), its overall this habitat.
dominance along this transect might have been Prior to the ENSO, widgeongrass was observed
specific to that site. On the replicate transect that only once in the Silver Strand eelgrass bed in the
was lost during the sampling period (Transect 2; intertidal portion of the bed ( June 1992, Williams
Fig. 7), widgeongrass was more abundant than eel- personal observation). During the ENSO, wid-
grass in the shallow depths in the spring of 1999 geongrass was observed in eelgrass census quadrats
but had declined by August, based on the few sam- on two occasions in the Silver Strand eelgrass bed
pling dates. This and our qualitative observations (Fig. 3). Widgeongrass established better in the
at the site suggest the pattern along Transect 1 was shallower subtidal and intertidal portions of the
general at Kendall-Frost. bed, where we did not census eelgrass ( Johnson
Widgeongrass persisted at Kendall-Frost through 2000).
the summer of 2000 (Lieberman personal obser- When we began the study, we did not know
vation), despite increasing eelgrass abundance whether widgeongrass would survive the winter in
(Fig. 3). At one point in the sampling, widgeon- San Diego. Although it did die back dramatically
grass was observed beyond the lower depth limit in winter, it recovered in spring due to a combi-
of eelgrass ( 3 to 4 m MLLW). Widgeongrass nation of vegetative proliferation (Lieberman per-
did not continue to propagate into the eelgrass sonal observation) and possibly seedling recruit-
bed, at least along the transect. On the last sam- ment. We found a large seed crop of widgeongrass
112 M. R. Johnson et al.
TABLE 3. Total seed crop and seed germination of widgeon- petition from diminished eelgrass (Orth 1977;
grass (mean [ 1 SD], n 10) at Coronado Cays, San Diego Bird et al. 1994; Lieberman 2002) and more fa-
Bay. Seed crop is both germinated and ungerminated seeds.
vorable environmental conditions could have con-
Total Seed Crop
Seed Crop that
Germinated
tributed to the increased abundance of widgeon-
Date (seeds m 2) (seeds m 2) grass. Widgeongrass can maintain a maximum
December 8, 1999 2,103.4 (1,113.9) 0 photosynthetic rate at higher temperatures, and
January 10, 2000 915.7 (370.9) 73.1 (31.7) has a higher temperature optimum for growth,
March 26, 2000 2,506.1 (1,454.1) 23.5 (43.1) than eelgrass (Setchell 1924; Verhoeven 1979;
May 1, 2000 1,715.3 (893.0) 11.0 (23.1) Wetzel and Penhale 1983; Evans et al. 1986).
June 1, 2000 1,151.0 (660.0) 0
These optima are reported to occur around 25 C
and widgeongrass can apparently flourish in 36 C
(Edwards 1978) and tolerate 43 C in some cases
(Koch and Seeliger 1988). Widgeongrass, like eel-
at Coronado Cays and a small percentage of ger- grass, exhibits acclimation and adaptation to local
minated widgeongrass seeds (Table 3). conditions (Koch and Seeliger 1988; Koch and
Dawes 1991), and these limits should be consid-
Discussion ered as relative and average for this region. Re-
Coincident with ENSO conditions, eelgrass de- sults from experiments conducted in San Diego
clined and widgeongrass increased in some areas on the relative growth of widgeongrass and eel-
sampled in two bays in San Diego. Previous to this grass in response to temperature along with field
ENSO, widgeongrass was restricted to its typical tests of interspecific competition revealed that the
habitats, including salt marsh pans, on intertidal ability of eelgrass to outcompete widgeongrass was
flats of a commercial salt plant, and in the warm- compromised under ENSO temperatures (Lieber-
water effluent from a power plant (Williams per- man 2002).
sonal observation). Although we have insufficient There are other factors that limit the distribu-
environmental and experimental data to con- tion of widgeongrass, which we did not investigate.
clude that the shifts in distributions and abun- Widgeongrass can tolerate a wide range of salini-
dance were due to ENSO, water temperatures in- ties, but it tends to germinate and grow best in low-
creased well beyond the typical summer temper- salinity waters (Setchell 1924; Seeliger et al. 1984;
atures when eelgrass in San Diego is subject to Kantrud 1991; Koch and Dawes 1991). Unusually
chronic declines (Ewanchuk 1995; Sewell 1996). high rainfall resulting in lowered salinity observed
Eelgrass grows well between 10–20 C and reaches in south San Diego Bay during the ENSO (Merkel
maximum photosynthetic rates between 19–22 C, unpublished data) might have been a factor in the
although both acclimation and adaptation to local local expansion of widgeongrass through en-
conditions are important (reviewed in Phillips hanced seed germination and subsequent recruit-
1984 and Thayer et al. 1984; Zimmerman et al. ment. The limits of widgeongrass distribution are
1989). Zimmerman et al. (1989) suggested that also influenced by competition from other species,
temperatures 25 C represented stressful con- light, nutrients, and sea level (studies above; Orth
ditions for eelgrass growth and temperatures near and Moore 1988; Burkholder et al. 1994), factors
30 C could exceed the capacity for acclimation, not addressed in this study.
resulting in eelgrass decline. During ENSO, the Widgeongrass abundance might increase in
duration of exposure to temperatures stressful to many areas as the oceans warm, a premise based
eelgrass was substantially longer than a non-ENSO on the temperature tolerance and geographic dis-
year (Table 2). tribution of this species as well as the observations
We have since confirmed experimentally that we report here. Widgeongrass is distributed more
the temperatures reached during the ENSO event widely than other ruderal and subdominant sea-
stressed San Diego eelgrass. When grown outdoors grasses, including Halodule spp. and Halophila
in temperature-regulated mesocosms and allowed spp., which are restricted to warmer waters. Stud-
to acclimate for several months, local eelgrass pro- ies of seasonal dynamics in seagrass communities
duced 15–30% fewer shoots under ENSO water where widgeongrass is present indicate that it be-
temperatures than in waters 2–4 C cooler (Wil- comes abundant in summer months (Nixon and
liams 2001). These results were supported when a Oviatt 1973; Richardson 1980; Harrison 1982;
similar experiment was conducted in another year Evans et al. 1986; Kinnery and Roman 1998), and
(Lieberman 2002). widgeongrass has an annual growth cycle in lo-
To proliferate in eelgrass habitat, widgeongrass cations where ambient temperatures are too cool
would have to recruit after dispersing from its typ- (Harrison 1982; Pulich 1985; Flores-Verdugo et al.
ical habitats or from a seed bank. Reduced com- 1988; Dunton 1990). These studies support the
Changes in Seagrass Abundance 113
expectation that the distribution of widgeongrass any of its subagencies. M. R. Johnson was supported on a Sea
Grant traineeship on grant #NA666RGO477 to S. L. Williams
could increase with increasing ocean tempera- from the National Sea Grant College Program. M. R. Johnson
tures. Widgeongrass recruits would be expected was partially supported by a Grant in Aid of Research from the
to recruit relatively rapidly to new areas because Sigma Xi Society and a grant from the Lerner-Grey fund for
it has many vectors for dispersal as waterfowl and Marine Research. This is contribution no. 293 of the Coastal
fishes consume its seeds (Martin et al. 1961; Aga- and Marine Institute, San Diego State University and no. 2170
of the Bodega Marine Laboratory.
mi and Waisel 1988). It also recruits very well
from seeds (Van Vierssen et al. 1984; Koch and LITERATURE CITED
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