Estuaries
Vol. 26, No. 2B, p. 495–510
April 2003
Determination of Food Web Support and Trophic Position of the
Mummichog, Fundulus heteroclitus, in New Jersey Smooth
Cordgrass (Spartina alterniflora), Common Reed (Phragmites
australis), and Restored Salt Marshes
C. A. CURRIN1,*, S. C. WAINRIGHT2, K. W. ABLE3, M. P. WEINSTEIN4, and C. M. FULLER5
1
National Oceanic and Atmospheric Administration, Center for Coastal Fisheries and Habitat
Research, 101 Pivers Island Road, Beaufort, North Carolina 28516-9722
2 U.S. Coast Guard Academy, 27 Mohegan Avenue, New London, Connecticut 06320-8101
3 Marine Field Station, Institute of Marine and Coastal Sciences, Rutgers University, 800 Great
Bay Boulevard, Tuckerton, New Jersey 08087
4 New Jersey Marine Sciences Consortium, Building 22, Fort Hancock, New Jersey 07732
5 Institute of Marine and Coastal Sciences, 71 Dudley Road, Rutgers University, New Brunswick
New Jersey 08901-8521
ABSTRACT: The invasion of Phragmites australis into tidal marshes formerly dominated by Spartina alterniflora has
resulted in considerable interest in the consequences of this invasion for the ecological functions of marsh habitat. We
examined the provision of trophic support for a resident marsh fish, Fundulus heteroclitus, in marshes dominated by P.
australis, by S. alterniflora, and in restored marshes, using multiple stable isotope analysis. We first evaluated our ability
to distinguish among potential primary producers using the multiple stable isotope approach. Within a tidal creek system
we found significant marsh and elevation effects on microalgal isotope values, and sufficient variability and overlap in
primary producer isotope values to create some difficulty in identifying unique end members. The food webs supporting
F. heteroclitus production were examined using dual isotope plots. At both sites, the d13C values of F. heteroclitus were
clustered over values for benthic microalgae (BMI) and approximately midway between d13C values of Spartina and
Phragmites. Based on comparisons of fish and primary producer d13C, d15N, and d34S values, and consideration of F.
heteroclitus feeding habits, we conclude that BMI were a significant component of the food web supporting F. heteroclitus
in these brackish marshes, especially recently-hatched fish occupying pools on the marsh surface. A 2‰ difference in
d13C between Fundulus occupying nearly adjacent Spartina and Phragmites marshes may be indicative of relatively less
reliance on BMI and greater reliance on Phragmites production in Phragmites-dominated marshes, a conclusion consistent
with the reduced BMI biomass found in Phragmites marshes. The mean d13C value of F. heteroclitus from restored marshes
was intermediate between values of fish from naturally occurring Spartina marshes and areas invaded by Phragmites. We
also examined the isotopic evidence for ontogenetic changes in the trophic position of larval and juvenile F. heteroclitus.
We found significant positive relationships between F. heteroclitus d15N values and total length, reflective of an increase
in trophic position as fish grow. F. heteroclitus d15N values indicate that these fish are feeding approximately two trophic
levels above primary producers.
(Weinstein and Balletto 1999; Able et al. 2003).
Previous studies have demonstrated the incorporation of P. australis into the food web supporting
mummichogs (Fundulus heteroclitus), white perch
(Morone americana), and bay anchovy (Anchoa mitchilli) in the Delaware Bay (Wainright et al. 2000;
Weinstein et al. 2000). Those studies used stable
isotope analysis to estimate the contribution of P.
australis to fish production, and estimated that
Phragmites made a significant contribution to fishery food webs in Delaware Bay. This estimate was
primarily based on the depleted d13C and enriched
d34S values found in fish sampled from regions of
Delaware Bay occupied by P. australis.
Introduction
The replacement of Spartina alterniflora-dominated marsh habitat with stands of Phragmites australis has occurred across large areas of the coastal
United States, particularly in the northeast and
mid-Atlantic (Chambers et al. 1999; Windham and
Lathrop 1999). Debate continues on the consequences of this change for one of the most important ecological functions of salt marsh habitat: the
provision of trophic support for fishery organisms
* Corresponding author; tele: 252/728-8749; fax: 252/7288784; e-mail: [email protected].
Q 2003 Estuarine Research Federation
495
496
C. A. Currin et al.
A potential confounding factor for the use of
stable isotopes in estimating the role of P. australis
in brackish marsh food webs is the concurrent depletion in d13C values of phytoplankton and benthic microalgae (BMI) in oligohaline systems,
which occurs as a consequence of changes in the
d13C value of dissolved inorganic carbon in lowersalinity waters (Fogel et al. 1992; Chanton and Lewis 1996; Wainright et al. 1999). It has also proven
very difficult to obtain accurate d34S values for phytoplankton in brackish marsh waters (Chanton and
Lewis 1996; Wainright et al. 2000; Weinstein et al.
2000). This is problematic because sulfur (S) isotopes are often extremely important in distinguishing estuarine food webs, and particularly between
benthic and pelagic sources of primary production
(Peterson et al. 1985; Deegan and Garritt 1997).
Food web analysis in marsh ecosystems is further
confounded by the numerous potential sources of
primary production, making the use and interpretation of mixing models difficult (Fry and Sherr
1984; Post 2002).
Because of the perceived loss of habitat value
associated with the invasion of S. alterniflora marsh
by P. australis, there are large-scale management
efforts underway to restore invaded areas to Spartina marsh. One such restoration is being done on
Alloway Creek, on the eastern shore of Delaware
Bay (Weinstein et al. 1997). Although Wainright et
al. (2000) described food webs associated with F.
heteroclitus in P. australis habitat in Alloway Creek,
there has been no examination of the recovery of
trophic support in these restored salt marshes.
Fundulus spp. are among the most abundant resident fishes in salt marshes on the Atlantic, Gulf,
and Pacific Coasts of the U.S. (Able and Fahay
1998; Kneib 2000; Talley 2000). Fundulus spp.
spawn on the marsh surface, and reside within the
marsh and tidal creek ecosystem for their entire
life. Mark-recapture studies suggest that the homerange of juvenile fish is on the order of 10s to 100s
of meters, and stable isotope studies suggest there
is considerable site fidelity in these resident fish
(Lotrich 1975; Talley 2000; Wainright et al. 2000;
Teo and Able In press). Gut content analysis of
Fundulus indicates that small fish (, 25 mm) are
primarily carnivores, consuming copepods, amphipods, gastropods, and other benthic invertebrates
that occur on the sediment surface. Larger fish
have a more varied diet, and a larger proportion
of the gut contents consists of algae and detrital
matter (Kneib et al. 1980; Allen et al. 1994; Smith
et al. 2000; Talley 2000). Fundulus utilization of
marsh primary production, followed by Fundulus
consumption by marine transient species, is one of
the primary ways that marsh production enters the
estuarine ecosystem. Fundulus have been described
as providing a trophic relay of marsh production
(Kneib 2000) and are important in the diets of
many predators (Tupper and Able 2000; Nemerson and Able In press).
Several studies comparing fish abundance and
species composition between marshes invaded by
P. australis and native S. alterniflora and Typha latifolia marshes have concluded that the fish population using P. australis marshes is very similar to
that found in native marshes, especially when elevation is not a factor (Fell et al. 1998; Meyer et al.
2000; Able et al. 2001). Larval and small juvenile
F. heteroclitus are not as abundant on the P. australis
marsh plain, and apparently P. australis does not
provide the same nursery habitat as S. alterniflora
(Able and Hagan 2000, 2003). The discrepancies
between these studies may be a result of the varying effects of Phragmites on Fundulus relative to the
stage of the invasion (Able et al. 2003).
We consider several questions in this paper by
examining the stable isotope composition of primary producers and F. heteroclitus in several New
Jersey salt marshes. We extend the analysis begun
in Wainright et al. (2000) by examining the food
webs supporting F. heteroclitus from P. australis and
S. alterniflora marsh habitat within the same tidal
creek system. We also sampled restored marshes in
the same tidal creek system in order to assess the
recovery of trophic function in these restored systems. We hypothesized that restored marsh isotope
values would be intermediate to those in P. australis
and S. alterniflora marshes. We also hypothesized
that the height of the P. australis canopy would reduce irradiance at the marsh sediment surface, reducing the benthic microalgal contribution to Fundulus food webs relative to that in S. alterniflora and
restored marshes, and that the seasonal increase in
marsh canopy biomass may also result in a temporal change in the benthic microalgal contribution to marsh food webs. We examined the isotopic
evidence for ontogenetic changes in the trophic
position of juvenile F. heteroclitus, and provide the
first multiple stable isotope analysis of the food
web used by small juvenile Fundulus (8–22 mm)
residing on the marsh surface.
Methods
SITE DESCRIPTIONS
Sampling in 1998 occurred at Alloway Creek,
(398309170N, 758299500W), a brackish marsh system
on Delaware Bay. Sampling in 1999 occurred at
Hog Islands, located on the Mullica River upstream of Great Bay on the Atlantic Ocean side of
New Jersey (398339040N, 748229320W). The Alloway
Creek sites included two P. australis-dominated sites
that correspond to the lower and upper Alloway
Brackish Marsh Food Webs
Creek Phragmites sites described in Wainright et al.
(2000). Two sites were also located within an area
of former P. australis dominated marsh, which had
been treated by Public Service Enterprise Group
to restore S. alterniflora (Weinstein et al. 1997; Able
et al. 2003), and are hereafter referred to as restored marsh. Restored sites were established in
treated areas in the lower and upper portions of
Alloway Creek, to match the approximate location
of the lower and upper Phragmites sites. Another
site, designated Spartina, was located in upper Alloway Creek and within a c. 10,000 m2 area that
was dominated by S. alterniflora. We sampled suspended particulate matter (SPM) from a station
approximately 3 km upstream from the upper
marsh sites. This station is designated as DOCK.
The Hog Islands sites are located on the Mullica
River, and were chosen because of the well-documented spread of Phragmites in this relatively undisturbed area (Windham and Lathrop 1999;
Wainright et al. 2000). P. australis is the dominant
marsh vegetation at this site, and S. alterniflora is
relegated to small patches (10–100 m wide) bordering the perimeter of the islands. The Mullica
River has relatively little anthropogenic impact,
and the Hog Islands sites are within the Jacques
Cousteau National Estuarine Research Reserve.
The sites are approximately 17 km from Great Bay,
and salinity during the study period ranged from
2‰ to 22‰, with an average of 9.7‰ (Able and
Hagan 2003). Further description of the sites, including measures of site elevation, vegetation cover, and fish utilization are in Able and Hagan
(2003) and Able et al. (2003). Three sites designated as Phragmites were within large areas dominated by P. australis, while three nearby sites designated as Spartina were smaller areas dominated
by S. alterniflora. Spartina patens and Spartina cynosuroides were also found in Spartina sites. All sampling occurred from the end of June through August 1999.
BENTHIC MICROALGAL BIOMASS
Five surface sediment cores were obtained with
a 5 cc syringe-corer to 0.5 mm depth from each
elevation at each Alloway Creek site. Samples were
frozen on dry ice and pigments extracted and analyzed as described in Wainright et al. (2000).
STABLE ISOTOPE SAMPLE COLLECTIONS
Leaves of S. alterniflora and P. australis were collected from at least 5 different plants at each site
in Alloway Creek and Hog Islands. Three pooled
samples were analyzed per site. When available,
standing dead material (detritus) and flowers were
collected as well. Macrophyte material was rinsed
with distilled water, dried, and ground prior to iso-
497
tope analysis as described in Wainright et al.
(2000).
SPM samples were obtained by filtering water
collected on the incoming tide through pre-combusted glass fiber filters. BMI were collected from
vegetated (marsh elevation) and unvegetated
(creek bank or mudflat elevation) portions of each
site. Microalgal collections from the marsh surface
were done by bringing sediment sections back to
the laboratory, and microalgae that vertically migrated through a 63-mm nitex mesh and silica layer
were concentrated on precombusted glass fiber filters (Wainright et al. 2000). A similar procedure
was used in situ for collecting microalgae from
creek bank elevations at Alloway Creek sites. Instead of removing sediments to a tray, the silica and
nitex mesh were placed directly on the sediment
surface, and the area shaded by fiberglass window
screen stretched over a 16 cm diam PVC ring. The
different procedures were necessitated by the different vertical migration response of the microalgal community; creek bank algae responded very
quickly (60–90 min) to shading by a fiberglass
screen, while microalgae on the marsh surface required an 18-h to 24-h period before sufficient biomass was obtained on the mesh screen. In each
instance, microalgae collected from the mesh
screens were concentrated on precombusted glass
fiber filters. Filters were visually examined through
a dissecting microscope and contaminant particles
removed. Samples for carbon (C) and nitrogen
(N) isotope analysis were treated with 1 N HCl prior to analysis, while filters for S analysis were only
rinsed with distilled water. Further details on isotope analysis are in Wainright et al. (2000).
F. heteroclitus in Alloway Creek were obtained using either a seine or minnow traps deployed at
each site (Wainright et al. 2000), during 1-wk periods in June and August. F. heteroclitus from Hog
Island sites were obtained with pit traps biweekly
from late June through August, as described in
Able and Hagan (2000). The total length (TL) of
each fish was measured, and fish were individually
analyzed for stable isotope composition, following
the protocol described in Wainright et al. (2000).
STATISTICAL ANALYSIS
BMI chlorophyll data were log-transformed prior to analysis of variance to eliminate heteroscedasticity. Isotope data were checked for normality
using the Shapiro-Wilk statistic. Because numerous
groups were not normally distributed, all stable isotope data from Alloway Creek were rank-transformed prior to analysis of variance. Data from
Hog Islands exhibited a normal distribution and
were not rank-transformed. One-way and two-way
analysis of variance (ANOVA) tests were done to
498
C. A. Currin et al.
test the effects of marsh type and time of collection
on stable isotope values, and the Tukey method,
appropriate for unequal cell sizes, was used for a
posteriori means testing.
Results
MICROALGAL BIOMASS
Mean BMI biomass on marsh surfaces in Alloway
Creek ranged between 13.7 and 90.4 mg chl m22
over the course of the study. BMI biomass was significantly reduced in Phragmites marsh sediments
in both June and August (F2 5 3.85, p 5 0.0377;
F2 5 9.80, p 5 0.0009), while Spartina marsh sediments always supported the highest BMI biomass
(Fig. 1). Benthic microalgae on mudflats adjacent
to the marshes exhibited a significant site effect
only in June (F2 5 3.57, p 5 0.0454), when mudflats at restored marshes had a significantly higher
biomass than those at the Phragmites sites (Fig. 1).
STABLE ISOTOPE ANALYSIS
Alloway Creek Plant Signatures
Stable isotope values of primary producers collected from Alloway Creek indicated an approximately 13 per mil separation in the mean d13C values of primary producers, while variation within
each taxon among sites and seasons was less than
2 per mil (Table 1). There was a small though significant site effect on the C isotopic values of both
P. australis (F2 5 14.47, p , 0.0001) and S. alterniflora (F2 5 9.12, p 5 0.0002). The N isotope values of these marsh macrophytes showed little variation, although there were significant month (P.
australis, F2 5 5.73, p 5 0.0223) and site (S. alterniflora, F2 5 4.48, p 5 0.0112) effects on macrophyte d15N values. The range in d34S values among
primary producers was nearly 15 per mil, though
as noted below, d34S values for SPM are suspect.
There was also considerable variation in the S isotope value of P. australis with mean values ranging
from 10.8 to 17.8 per mil (Table 1).
The stable isotope composition of a few samples
of macrophyte detritus from Alloway Creek was
also determined. Both S. alterniflora and P. australis
detritus exhibited small (1 to 3 per mil) decreases
in d15N values relative to live material. S. alterniflora
detritus also exhibited a small decrease in d13C (Table 1). Only 4 P. australis detritus samples were analyzed for d34S, and these were within 2 per mil of
leaf tissue analyzed at the same time.
BMI were successfully collected from unvegetated mudflat or creek bank sites using the in situ
shading ring in 60–90 min incubations (BMImud). BMI from the marsh surface were successfully collected by returning sediment to the laboratory in a tray, and performing overnight incu-
Fig. 1. Benthic microalgal biomass (mg chl m22, mean and
standard error) in marsh and mudflat sediments at Alloway
Creek sites. Samples were obtained from Phragmites (Phra), Spartina (Spar), and restored (Rest) marshes. Within a month and
marsh grouping, different letters inside bars indicate means different at p , 0.05 (ANOVA using Tukey’s means testing).
bations (BMI-marsh). Collections from these two
locations yielded results with significantly different
C and S isotope values (F2 5 23.19, p , 0.0001; F2
5 11.73, p 5 0.0028, respectively). Relative to BMI-
Brackish Marsh Food Webs
499
TABLE 1. Mean C, N, and S isotope values of primary producers collected from the Alloway Creek system in June and August 1998.
Samples were obtained from three marsh types; Phragmites-dominated (Phra), Spartina-dominated (Spar), and restored marshes (Rest),
which were former Phra marshes treated to replace Phragmites with Spartina. Dock refers to a collection station 3 km upstream of the
marsh stations. Mean values provided with standard error and number of replicate samples in parentheses. Missing values indicated
by a period. Means given by month and site when analysis of variance indicated a significant month or site effect for at least one of
the elements (see text). Sample types are explained in the text and match those symbols used in Fig. 3.
Sample Type
Month
Marsh
Mean d13C
Mean d15N
Mean d34S
Creek bank benthic microalgae
BMImud
August
BMImud
August
BMImud
August
BMImud
June
BMImud
June
BMImud
June
Phra
Rest
Spar
Phra
Rest
Spar
217.20 (0.10, 8)
217.96 (0.93, 9)
217.17 (0.34, 3)
218.27 (0.45, 4)
216.86 (0.18, 8)
217.31 (0.34, 4)
9.07 (0.39, 8)
8.01 (0.25, 9)
5.89 (1.16, 3)
9.00 (0.46, 4)
10.28 (0.14, 8)
10.45 (0.08, 4)
8.66 (0.91, 8)
7.35 (0.77, 9)
8.20 (1.35, 3)
5.37 (0.74, 4)
n50
n50
Marsh surface benthic microalgae
BMImar
Both
BMImar
Both
BMImar
Both
Phra
Rest
Spar
222.05 (0.44, 7)
221.88 (0.93, 7)
220.92 (0.60, 3)
9.49 (0.62, 7)
8.21 (0.65, 7)
8.94 (0.34, 3)
5.02 (0.89, 6)
11.58 (—, 1)
n50
Phragmites australis leaves
Pa
June
Pa
June
Pa
June
Pa
August
Pa
August
Pa
August
Phra
Rest
Spar
Phra
Rest
Spar
226.36 (0.12, 6)
225.10 (0.18, 6)
225.42 (0.18, 3)
226.82 (0.17, 14)
225.98 (0.14, 13)
225.74 (0.06, 2)
9.95 (0.51, 6)
8.91 (0.70, 6)
7.57 (0.41, 3)
9.90 (0.26, 14)
10.54 (0.36, 13)
10.51 (0.53, 2)
10.86 (0.78, 6)
17.79 (1.45, 6)
14.12 (0.34, 3)
10.77 (0.59, 13)
n50
n50
Phragmites detritus
Padet
Padet
June
August
Phra
Phra
226.30 (0.05, 2)
226.04 (0.23, 3)
8.62 (0.69, 2)
9.10 (0.61, 3)
13.93 (4.35, 2)
9.31 (1.03, 2)
Suspended particulate matter
SPM
June
SPM
June
SPM
June
SPM
June
SPM
August
SPM
August
SPM
August
SPM
August
Dock
Phra
Rest
Spar
Dock
Phra
Rest
Spar
226.50 (0.076, 3)
223.37 (0.15, 6)
224.10 (0.18, 6)
223.37 (0.06, 3)
225.22 (0.01, 3)
223.72 (0.19, 6)
223.29 (0.18, 6)
223.10 (0.17, 3)
7.51 (0.10, 3)
8.26 (0.32, 6)
8.55 (0.29, 6)
7.98 (0.19, 3)
7.51 (0.059, 3)
6.99 (0.23, 6)
6.58 (0.25, 6)
5.93 (0.09, 3)
1.24 (—, 1)
1.94 (0.66, 6)
1.63 (0.83, 5)
0.96 (0.65, 3)
n50
2.63 (0.74, 6)
n50
n50
Spartina alterniflora leaves
Sa
June
Sa
June
Sa
August
Sa
August
Rest
Spar
Rest
Spar
212.27 (0.26, 5)
212.45 (0.04, 3)
212.76 (0.42, 13)
213.25 (0.10, 7)
11.33 (0.29, 5)
11.78 (0.23, 3)
12.40 (0.41, 13)
11.54 (0.12, 7)
15.12 (1.98, 5)
13.19 (1.19, 3)
n50
n50
Spartina alterniflora detritus
Sadet
August
Spar
214.49 (0.29, 2)
8.85 (0.55, 2)
n50
mud samples, BMI-marsh were approximately 4
per mil depleted in 13C, while the difference in d34S
was approximately 1.5 per mil (Table 1). Although
these differences could be due to artifacts associated with the collection techniques, results from
trials at Hog Islands (Wainright and Fuller unpublished data) and elsewhere (Currin unpublished
data) suggest that the differences are real, and may
result from differences in environmental variables
such as irradiance, sulphate reduction rates, and
water velocity between the two habitats (Currin et
al. 1995). In addition to these differences, BMImud samples exhibited a significant effect of site
on d13C values (F2 5 3.36, p 5 0.0241) and signif-
icant month effect on d15N (F2 5 48.12, p ,
0.0001) and d34S (F2 5 6.35, p 5 0.0220) values.
BMI collected from the marsh surface did not exhibit any significant site or month effects on C, N,
or S stable isotope values.
C isotopic composition of SPM varied significantly with site and month, with significant interaction (F2 5 15.60, p , 0.0001). Mean d13C values
from each site ranged from 226.5 at the DOCK
station located 3 km upstream of the upper Spartina site in June to 223.9 at the upper Alloway
Creek restored site in August. There were no consistent trends in the SPM d13C collected at restored
Spartina and Phragmites sites. The mean d15N value
500
C. A. Currin et al.
TABLE 2. Results of regression analysis of relationship between
juvenile Fundulus total length and d13C, d15N, and d34S for fish
collected from Alloway Creek. Marsh types are Phra 5 Phragmites-dominated, Rest 5 former Phragmites marsh restored to
Spartina, and Spar 5 Spartina-dominated, ALL 5 all marshes
combined.
Isotope
Marsh
F-value
p
Intercept
Slope
Adj R2
13
d C
Phra
Rest
Spar
ALL
9.76
21.69
2.15
51.23
0.0030
,0.0001
0.1537
,0.0001
219.318
218.065
218.346
218.096
20.0302
20.0389
20.0144
20.0402
0.1491
0.2097
0.0382
0.2401
d15N
Phra
Rest
Spar
ALL
19.06
12.75
29.73
69.89
,0.0001
,0.0001
,0.0001
,0.0001
13.205
12.751
13.036
13.064
0.0357
0.0425
0.0635
0.041
0.2654
0.3106
0.4976
0.3023
d34S
Phra
Rest
Spar
ALL
0.02
7.01
10.91
5.18
0.6611
0.0159
0.0092
0.0269
12.371
5.974
4.638
7.931
20.0110
0.0596
0.0839
0.0416
0.0364
0.2311
0.4977
0.0706
of SPM collected in June (8.18, 0.16, n 5 18) was
significantly higher than in August (6.76, 0.16, n
5 18) with no site interaction. There were no significant site or month effects on SPM d34S values
(p . 0.05) with mean values per site ranging between 1.2 and 6.2 per mil. We consider that these
reported d34S values for SPM are likely in error,
and are a greater indication of the inorganic S in
suspended sediments trapped on the filter than
the organic sulfur fraction associated with phytoplankton. This conclusion is based on visual observations of filtered SPM, which were uniformly
brown in color and clearly contained a large inorganic fraction, as well as theoretical considerations (Chanton and Lewis 1999; Wainright et al.
2000). Inorganic S in estuarine sediments has d34S
values ranging between 210 and 220 (Peterson et
al. 1986), while seawater sulphate d34S is between
118 to 121 (Peterson and Howarth 1987; Stribling
et al. 1998; Chanton and Lewis 1999). The inclusion of macrophyte detritus into the collected SPM
fraction could also alter the observed C and S isotopic value. Previous SPM collections from Alloway
Creek and the Mullica River had C : N ratios of between 5:1 to 10:1, indicative of organic matter of
primarily algal origin (Wainright et al. 1999, 2000).
ALLOWAY CREEK FUNDULUS
Regression analysis of TL and d13C, d15N, and
34
d S was used to determine whether there were any
ontogenetic effects on the stable isotope signature
of F. heteroclitus. Regression analysis was done both
by marsh type and by combining all marshes (Table 2, Fig. 2). There was a strongly significant relationship (p , 0.0001) between fish length and
d13C and d15N when all data are combined. The
relationship between d34S and length is weaker and
Fig. 2. Length versus d13C, d15N, and d34S values for juvenile
Fundulus heteroclitus collected in Alloway Creek. Fish were obtained from three marsh types: Phragmites (Phra), Spartina
(Spar), and restored (Rest). Regression analysis revealed a significant relationship between length and each of the isotopes
when data from all marsh types was combined. Regression coefficients and adjusted r2 values are provided for the combined
set (all marsh types). p-values and regression coefficients for
regressions performed by marsh type are in Table 2.
only significant for fish collected from the Spartina
and restored marshes, where larger fish showed a
significant enrichment in 34S (Table 2). Overall, F.
heteroclitus became depleted in d13C and enriched
in d15N as they grew. Changes in d13C were most
evident in the restored and Phragmites marshes,
while the effect of length on d15N was greatest in
the Spartina marsh (Table 2, Fig. 2).
There was a significant site by month interaction
on the length of juvenile F. heteroclitus collected at
the Alloway Creek sites (F2 5 3.77, p 5 0.0120).
The mean TL of F. heteroclitus collected in June was
64.4 mm, while the mean length for all fish collected in August was 35.4 mm. In June, significantly larger fish were collected from Phragmites
sites, while in August the opposite trend was true
(Table 3). Fish collected in June also exhibited sig-
Brackish Marsh Food Webs
501
TABLE 3. Isotope and total length data for juvenile Fundulus heteroclitus collected from Hog Islands and Alloway Creek sites. Means
presented with standard errors and number of replicate samples in parentheses. Letters in columns indicate results of analysis of
variance tests on effects of site on variables within a column; means with different letters are significantly different at the p 5 0.05
level. All tests were on sites within the major headings (Hog Islands, Alloway Creek—June, and Alloway Creek—August).
Site/Vegetation
Hog Islands—June–August
Phragmites australis
Spartina alterniflora
Alloway Creek—June
Phragmites australis
Restored Spartina
Spartina alterniflora
Alloway Creek—August
Phragmites australis
Restored Spartina
Spartina alterniflora
Length (mm)
d13C
A
A
B
C
D
11.1 (0.6 14) A
13.4 (0.6, 16) AB
15.1 (1.2, 20) AB
17.1 (0.8, 68) B
16.1 (1.0, 25) B
16.1 (0.5, 129) B
222.5 (0.2, 14) C
220.0 (0.4, 16) A
220.9 (0.3, 20) AB
221.7 (0.1, 68) BC
221.4 (0.2, 25) BC
221.3 (0.1, 129) AB
9.2 (0.1, 14) AB
8.8 (0.2, 16) AB
9.3 (0.1, 20) A
8.7 (0.1, 68) B
9.1 (0.2, 25) AB
8.9 (0.1, 129) A
8.3 (0.4, 10) A
7.5 (0.7, 6) A
7.9 (0.8, 12) A
8.4 (0.3, 48) A
8.6 (0.3, 20) A
8.4 (0.2, 86) A
Upper
Lower
Upper
Lower
Upper
72.1 (2.9, 13) A
63.9 (2.0, 13) AB
64.7 (2.3, 15) AB
63.8 (1.8, 15) AB
58.5 (3.0, 15) B
221.2 (0.5, 13) BC
221.4 (0.3, 13) C
220.7 (0.6, 15) AB
220.5 (0.4, 15) BC
219.2 (0.2, 15) A
16.2 (0.3, 13) AB
15.9 (0.2, 13) A
15.4 (0.3, 15) A
16.1 (0.2, 15) AB
17.1 (0.2, 15) B
11.7 (0.7, 7) A
11.7 (0.3, 12) A
9.8 (0.5, 7) B
10.2 (0.4, 9) B
9.8 (0.4, 11) B
Upper
Lower
Upper
Lower
Upper
na
48.1 (4.8, 25) A
25.9 (0.9, 14) B
32.9 (2.8, 35) B
28.7 (1.0, 15) B
na
220.9 (0.3, 26) C
218.2 (0.2, 14) A
219.6 (0.2, 36) B
218.7 (0.3, 15) A
na
14.5 (0.3, 26) B
12.2 (0.2, 14) A
14.6 (0.1, 36) B
14.6 (0.2, 15) B
na
11.5 (0.3, 5) A
na
9.6 (0.5, 5) B
na
Location
Site
Site
Site
Site
Site
All
nificantly higher d15N values. We will consider F.
heteroclitus isotopic signatures and marsh effects on
the food web by month.
There was a small but significant site effect on
the C, N, and S isotope values of F. heteroclitus collected in June (F2 5 7.91, p , 0.0001; F2 5 5.38,
p , 0.0008; F2 5 6.24, p 5 0.0005, for C, N, and
S, respectively). Fish from both Phragmites marshes
had depleted C and enriched S isotope values compared to fish collected from the Spartina and restored sites (Table 3). Fish collected from the two
restored sites had intermediate C and S isotope
values. The site variation in N signal was not consistent among marsh types, although F. heteroclitus
from the Spartina site were the most 15N enriched
(mean 5 17.1 per mil), despite also having the
smallest mean length (Table 3).
Site also had a small but significant effect on C,
N, and S isotopic signatures of F. heteroclitus collected in August (F2 5 21.21, p , 0.0001; F2 5
11.22, p , 0.0001; F2 5 10.00, p 5 0.0134 for C,
N, and S, respectively). We were able to collect F.
heteroclitus from only the lower Alloway Creek
Phragmites site in August; the mean d13C signature
of those fish (220.9) was depleted relative to fish
collected from both restored and Spartina sites.
Fish collected from the restored sites had intermediate d13C values, relative to fish collected from
Spartina and Phragmites sites, which is the same
trend observed in June. Fish from the upper restored site had a mean d15N value of 12.2, which
was significantly depleted relative to fish collected
from all other sites. S isotope data was available
d15N
d34S
from only 2 sites in August; the mean d34S value
for fish from the upper restored site was 9.6, which
was significantly lower than the mean d34S value for
fish from the Phragmites site (mean 5 11.5), again
a repeat of the pattern observed in June (Table 3).
The food webs supporting F. heteroclitus production in Alloway Creek were examined using C-S
and C-N dual isotope plots. We did not use mixing
models, as there are four or more primary producers potentially contributing to the food web at
each site, often with overlapping isotopic signatures (see Table 1), and we did not want to either
arbitrarily select certain combinations for modeling, or present the myriad possible combinations.
The analysis will focus on those combinations that
dual-isotope plots reveal to be mathematically possible, and on the combinations that appear most
likely based on the distribution and production of
producers and the natural history and feeding habits of Fundulus and their prey. In all plots, values
from Table 1 are used to calculate mean 6 standard error boxes for the primary producers with
one important exception; a theoretical value of
116 to 118 is used for the SPM d34S end member,
instead of the analytical results listed in Table 1.
The end-member boxes for the macrophytes S. alterniflora and P. australis include values for detritus
at Alloway Creek (Fig. 3) and for flowers and detritus at Hog Islands (Fig. 4). In interpreting these
plots, isotopic fractionation associated with assimilation of C, N, and S needs to be considered. The
d13C values of consumers are usually about 0.5 to
1 per mil heavier than their food, and the enrich-
502
C. A. Currin et al.
Fig. 3. Dual isotope (d13C versus d15N and d13C versus d34S) plots of primary producers and juvenile Fundulus heteroclitus from
Alloway Creek sites. Primary producers portrayed as squares representing the mean 6 standard error for values in that month (see
text for details). Primary producers include SPM (suspended particulate matter), Pa (Phragmites australis), BMImar (benthic microalgae
collected from marsh surface), BMImud (benthic microalgae collected from mudflats), and Sa (Spartina alterniflora). Fish obtained
from Phragmites (Phra), Spartina (Spar), and restored (Rest) marshes. Arrows indicate direction and magnitude of expected shift in
C and N isotope values from a primary producer to consumer feeding at the second trophic level (see text for details).
ment is additive up the food chain (Peterson and
Howarth 1987; Post 2002). Fractionation associated with assimilation of N is much greater, averaging 3.4 per mil per trophic level in aquatic ecosystems (Peterson and Howarth 1987; Post 2002). Few
studies of the fractionation associated with S are
available, though fractionation appears to be 1 per
mil or less per trophic level, and may be either
positive or negative (Peterson et al. 1986; Peterson
and Howarth 1987).
In June, most F. heteroclitus had a d13C value approximately midway between the two macrophyte
end members, and nearly coincident with BMI values. Fish from the restored marshes showed the
greatest range in d13C signature, with a bimodal
distribution along the C axis (Fig. 3). Fish from
the Phragmites marshes were, on average, most depleted in d13C values, and so had a C signature
indicative of utilization of P. australis, SPM, and
BMI-marsh. However, many F. heteroclitus collected
from the Phragmites marshes had d13C signatures
greater than 223 per mil, and so require a significant contribution from a primary producer other
than Phragmites and SPM. F. heteroclitus from the
Spartina marsh had d3C values ranging from 218
to 221 per mil. These values are 4 to 9 per mil
removed from Spartina, demonstrating that Spartina cannot be the dominant source of C in the F.
heteroclitus food web (Fig. 3). The d13C values of F.
heteroclitus from Spartina marshes overlap with the
d13C values for benthic microalgae collected from
the marsh and mudflat surface.
There was less difference in the mean d15N value
of primary producers, so that changes in the N
isotope value of F. heteroclitus may be due to trophic
effects as much as changes in the composition of
the food web. SPM consistently exhibited the most
depleted d15N values, while Spartina was the most
enriched (Table 1). The overall average d15N value
for F. heteroclitus collected in June was 16.14 (n 5
71, SE 5 0.13), which is 5 to 8 per mil enriched
from mean primary producer values. In June, the
most depleted F. heteroclitus d15N values were associated with the most depleted d13C values, in fish
collected from Phragmites and restored marshes.
The d34S of fish collected in June also exhibit a
wide range (7 to 15 per mil). F. heteroclitus d34S values lay between the SPM and BMI end members,
and showed some overlap with macrophyte d34S signals, although Phragmites was enriched in 34S compared to most fish.
F. heteroclitus d13C values in August were similar
Brackish Marsh Food Webs
503
HOG ISLANDS PRIMARY PRODUCERS
Fig. 4. Dual isotope (d13C versus d15N and d13C versus d34S)
plots of primary producers and juvenile Fundulus heteroclitus
from Hog Islands sites. Primary producers portrayed as rectangles which represent the mean 6 standard error for all values
(see text for details). Primary producers include SPM (suspended particulate matter), Pa (Phragmites australis), BMI-Pa (benthic
microalgae collected from Phragmites marsh surface), BMI-Sa
(benthic microalgae collected from Spartina marsh surface), Sa
(Spartina alterniflora), Sc (Spartina cynosuroides), and Sp (Spartina
patens). Fish were obtained from Phragmites (filled circles) and
Spartina (diamond) marshes. Arrow indicates direction and
magnitude of expected shift in C and N isotope values from a
primary producer to consumer feeding at the second trophic
level (see text for details).
to those obtained in June, exhibiting nearly a 10
per mil range (Fig. 3). August d13C values of fish
from the restored and Spartina marshes were approximately midway between the SPM and Spartina
end members, and overlapped with BMI collected
from marsh and mudflat sediments. F. heteroclitus
with the most enriched d13C values in August also
exhibited the most depleted d15N values, opposite
the pattern observed in June. There were fewer
d34S analyses of F. heteroclitus collected in August,
and the range in values is less than in June. C and
S values for fish collected in August from Phragmites and restored marshes were nearest to the BMI
end members.
For Hog Islands primary producers, SPM had
the most depleted d13C value (227.9), and three
species of Spartina were the most enriched with average d13C values ranging between 212.5 to 213.6.
Vascular plants from the Hog Islands sites had similar d13C values as those from Alloway Creek (Table
1), while algal samples (SPM and BMI) were relatively depleted. BMI were only collected from the
marsh surface at Hog Islands, but as found at Alloway Creek, BMI from Phragmites marshes had a
more negative d13C value than BMI from Spartina
marshes (Table 4).
The d15N values of primary producers from Hog
Islands were depleted relative to those in Alloway
Creek, with values ranging from 3.9 to 5.6, in contrast to the 5.9 to 12.4 range found in Alloway
Creek (Tables 1 and 3). This effect was evident in
every category of primary producer, but was most
pronounced in S. alterniflora leaves, which exhibited a mean d15N value of 4.7 at Hog Islands and
11.7 at Alloway Creek sites. This difference is likely
due to the differences in dissolved N inputs to the
two systems with a much greater anthropogenic input to Alloway Creek (Cifuentes et al. 1988; Wainright et al. 1996, 1999).
In general, d34S values of Hog Islands primary
producers were depleted relative to Alloway Creek.
This was particularly true for BMI and S. alterniflora
leaves, which were depleted by 8 to 9 per mil as
compared to samples from Alloway Creek. P. australis d34S values differed by only one or two per
mil between the two sites, while SPM values were
virtually identical (Tables 1 and 4).
HOG ISLANDS FUNDULUS
F. heteroclitus were collected by pit traps at Hog
Islands sites in order to target larvae and juveniles
occupying the marsh surface (Able and Hagan
2000). F. heteroclitus from Hog Islands were much
smaller than the fish sampled by seine and minnow
trap in Alloway Creek. The TL of fish collected
from Hog Islands Phragmites and Spartina marshes
for isotopic analysis ranged from 8 to 22 mm in
length. There was no effect of month on the
length of fish collected from Hog Islands, and fish
collected at all sampling dates were pooled for statistical analysis. There was a tremendous difference
in the numbers of fish caught in the two marsh
types at Hog Islands, despite equal effort. In the
previous year, average fish per pit trap deployed in
Spartina marshes was 2.48, while in Phragmites habitat the average was 0.01 fish per pit trap (Able and
Hagan 2000); similar results were obtained in 1999
(Able and Hagan 2003).
The d13C value of F. heteroclitus in Phragmites
504
C. A. Currin et al.
TABLE 4. Mean C, N, and S isotope values of primary producers collected from Hog Island sites in summer 1999. Sites included
three dominated by Spartina alterniflora and three dominated by Phragmites australis. Only benthic microalgae were collected from
both marsh types. Mean values are provided with standard error and number of replicate samples in parentheses. Missing values are
indicated by a period. Sample types are explained in the text and match those symbols used in Fig. 4.
Sample Type/Marsh
Mean d13C
Mean d15N
Mean d34S
Benthic microalgae
Phragmites BMI-Pa
Spartina BMI-Sa
224.35 (0.20, 18)
221.73 (0.30, 23)
4.66 (0.15, 18)
3.87 (0.19, 23)
21.07 (0.65, 14)
0.29 (0.84, 23)
Phragmites australis
Leaves Pa
Flowers Pa
Detritus Pa
225.88 (0.12, 64)
226.76 (0.15, 17)
225.59 (0.31, 16)
5.55 (0.23, 64)
5.78 (0.35, 17)
4.49 (0.46, 16)
9.39 (0.94, 64)
5.79 (0.69, 17)
9.65 (0.77, 15)
Spartina alterniflora
Leaves Sa
Flower Sa
Detritus Sa
213.39 (0.15, 52)
212.52 (0.17, 8)
213.55 (0.40, 17)
4.71 (0.11, 52)
4.65 (0.17, 8)
4.10 (0.39, 17)
4.66 (0.73, 52)
2.50 (2.60, 8)
9.60 (1.55, 14)
Spartina cynosuroides
Leaves Sc
213.61 (0.12, 16)
4.91 (0.13, 16)
9.27 (0.66, 14)
Spartina patens
Leaves Sp
213.52 (0.40, 33)
4.81 (0.12, 33)
5.13 (0.91, 35)
Suspended particulate matter
SPM
227.94 (0.32, 20)
5.61 (0.09, 20)
2.49 (0.63, 18)
marshes was significantly depleted relative to fish
in Spartina marshes (Table 3). There was no significant difference between the d15N and d34S values of F. heteroclitus caught in Phragmites and Spartina marshes (Table 3). Regression analysis demonstrated that over the size range of fish caught in
the pit traps (8 to 22 mm), there was a significant
though weak correlation between length and d15N
and d34S values of F. heteroclitus (F2 5 10.83, p 5
0.0013, adj r2 5 0.0647; F2 5 12.29, p 5 0.0007,
adj r2 5 0.1062, respectively). There was no correlation between d13C and length (p . 0.05).
These results suggest that ontogenetic changes in
diet are small within this size range and not responsible for the isotopic differences observed between F. heteroclitus obtained from Phragmites and
Spartina sites.
Dual isotope plots were also prepared to examine the relationship between primary producers
and juvenile F. heteroclitus in the Hog Islands marshes. As before, primary producer end-member values are represented by boxes reflecting the mean
6 standard error in producers observed over the
course of the study. Boxes for P. australis and of S.
alterniflora include values obtained for leaves, flowers, and detritus. SPM d34S have been revised to
range between 116 to 118, as previously described.
The majority of F. heteroclitus data points are clustered over the BMI from Spartina sites (BMI-Sa)
along the C axis (Fig. 4). There are some values
heavier than the BMI-Sa sample, indicating some
incorporation of S. alterniflora C in the food web.
The heaviest F. heteroclitus value is still 6 per mil
depleted compared to S. alterniflora values, suggesting a small contribution. The d13C values of F.
heteroclitus are also consistent with a mixture of
about 75% Phragmites and 25% Spartina. N isotope
values are more consistent with a larger contribution by BMI, as the average Fundulus d15N value
(9.1) is about 5 per mil enriched from the average
BMI value (4.2), compared to an enrichment of
less than 4 per mil over the average d15N value of
5.3 for P. australis (Tables 3 and 4). As reported
above, the average enrichment in consumer d15N
values is 3.4 per mil per trophic level, and gut content analyses demonstrate that juvenile Fundulus
are primarily carnivores (Allen et al. 1994; Smith
et al. 2000; Teo and Able In press). The relatively
enriched d15N values of SPM also suggest that it is
not a major contributor to these fishes food web.
The d34S values of F. heteroclitus are within the range
of values obtained for macrophytes, and 5 to 7 per
mil heavier than BMI values obtained from Hog
Islands marshes (see Discussion below).
Discussion
PRIMARY PRODUCER ISOTOPIC SIGNATURES
In this study we sought to determine whether
isotopic data substantiate hypotheses concerning
the role of estuarine primary producers in the
food web supporting F. heteroclitus in two tidal creek
systems. Before a consumer’s isotopic signature
can be attributed to a particular food web, the variability and uniqueness of the isotopic signature of
Brackish Marsh Food Webs
the primary producers themselves must be appraised. Within a tidal creek system, we found
marsh and elevation effects on a number of primary producers that could affect the interpretation of stable isotope data (Tables 1 and 4), and
sufficient variability and overlap between primary
producer end members to create some difficulty in
identifying unique end members (Figs. 3 and 4).
We found d13C values for BMI occupying the
marsh surface that were more depleted than those
reported from most other salt marsh studies (Tables 1 and 4; Currin et al. 1995). This represents
one of the few reports of BMI isotope values from
brackish marshes (Wainright et al. 2000; Weinstein
et al. 2000), and is a first report on the effects of
marsh type and elevation on the isotope values of
BMI from brackish marsh systems. At both Alloway
Creek and Hog Islands sites, the d13C value of BMI
obtained from P. australis marsh surface was 1 to
2.5 per mil lighter than BMI from the S. alterniflora
marsh surface. There was significantly lower BMI
biomass on the P. australis marsh surface (Fig. 1),
which was also observed by Wainright et al. (2000).
Given the taller canopy typical of P. australis marshes, we expected that BMI production would be lower than in S. alterniflora marshes. We also demonstrate for the first time a significant difference in
the C isotopic composition of BMI collected from
unvegetated mudflats than BMI collected from the
marsh surface; BMI from the marsh surface were
3 to 5 per mil depleted in d13C compared to BMI
from unvegetated creek banks and mudflats (Table
1). Depleted d13C values in BMI-marsh compared
to BMI-mudflat in Alloway Creek could be due to
a slower rate of primary production under conditions of reduced irradiance under the marsh canopy (Fogel et al. 1992) and due to fixation of 13C
depleted dissolved inorganic carbon (DIC) originating from the decomposition and respiration of
detrital C (Fogel et al. 1992; DesMarais and Canfield 1994). Both of these factors would result in
the incorporation of isotopically lighter C into microalgal biomass, and may also provide an explanation for the generally more depleted BMI d13C
values found in these brackish marsh systems with
significant P. australis marsh coverage. Previous isotopic studies examining marsh food webs have either not described exactly where within the marsh
the microalgal collections were made, or collected
BMI exclusively from creek banks (Peterson and
Howarth 1987), from the marsh surface (Sullivan
and Moncreiff 1990; Currin et al. 1995), pooled
results from creek banks and the marsh surface
(Wainright et al. 2000; Weinstein et al. 2000), or
used a range of literature values (Kneib et al. 1980;
Deegan and Garritt 1997). We demonstrate that
BMI communities from discrete marsh types (S. al-
505
terniflora versus P. australis) and elevations (marsh
surface versus creek bank-mudflat) can have distinct isotopic signatures, and suggest that future
efforts to assess the role of BMI in estuarine food
webs need to sample this community across a gradient of elevation and marsh types in order to attain an accurate BMI end member.
The d13C values we report for SPM (which serves
as a proxy for phytoplankton) range from 223.1
to 227.9, which is depleted relative to many other
published estuarine values for SPM (see Currin et
al. 1995). These values are similar to reports from
other brackish marsh-dominated or riverine-dominated systems (Deegan and Garritt 1997; Stribling
and Cornwell 1997; Chanton and Lewis 1999;
Wainright et al. 2000). This depletion is due to a
variety of factors, including changes in DIC concentration and d13C composition due to lowered
salinity (Chanton and Lewis 1999; Wainright et al.
1999), the potential fixation of recycled DIC (CO2)
resulting from the microbial respiration of detritus
(Fogel et al. 1992), and the potential incorporation of d13C-depleted Phragmites detritus into SPM
(Wainright et al. 2000). In this study, the depleted
d13C values of benthic and planktonic microalgae
move the algal end members closer to the P. australis end member (Figs. 3 and 4).
This shift in algal d13C values that co-occurs with
the increased presence of P. australis means that
discriminating between microalgal and P. australis
contribution to food webs is difficult using C isotopes alone. There was also significant overlap in
reported N and S isotope values between these primary producer groups, and a large amount of variability in the d34S values of macrophytes from
these brackish marshes (Tables 1 and 4). The reported d34S values of SPM, and to a lesser degree
BMI, are subject to contamination with inorganic
S, so that the actual d34S value for microalgal-derived organic S is most likely within the 5 to 20 per
mil range. The d34S ratios of S. alterniflora in polyhaline marshes is also variable (Peterson et al.
1985; Peterson and Howarth 1987), but the average value of 0.5 reported for S. alterniflora from a
number of previous studies (Currin et al. 1995) is
about 10 per mil lower than that reported here.
Stribling et al. (1998) found an inverse relationship between salinity and S. alterniflora d34S values,
and a similar inverse relationship has been reported between salinity and the d34S values of sulfate
in tidal creek water (Peterson and Howarth 1987;
Stribling et al. 1998). Reported d34S values for sulfate in oligohaline (, 2‰) tidal creeks range
from 22.5 to 23.5, while d34S values for porewater
sulfide in these systems can range from –21 to 110
(Peterson et al. 1986; Peterson and Howarth
1987). Variable primary producer d34S values result
506
C. A. Currin et al.
from differential utilization of these inorganic S
sources. Phytoplankton use primarily sulfate in the
water column, while rooted macrophytes and BMI
use both porewater and water column sources of
inorganic S, resulting in more depleted and variable d34S signals. The variation may be particularly
large in brackish systems, where seasonal sulfate
depletion can create unusual excursions in the inorganic S isotope ratios (Stribling et al. 1998). The
net result of these factors in the tidal creeks we
examined was that macrophyte d34S values fell in
between the average value of SPM and BMI, and
exhibited sufficient variability that there was often
an overlap in the mean 6 standard error boxes
representing the end-member values of primary
producers (Figs. 3 and 4). This reduces the usefulness of S isotopes in determining the sources of
primary production used by consumers in brackish
marsh systems.
EVIDENCE FOR ONTOGENETIC AND SEASONAL
CHANGES IN FUNDULUS DIET
N isotope ratios are often of more value in determining trophic position than in distinguishing
primary producer contributions to food webs. An
increase in one trophic level is associated with an
approximate 2 to 4 per mil increase in d15N, with
an average trophic level enrichment of 3.4 per mil
(Peterson and Howarth 1987; Post 2002). We
found significant positive relationships between F.
heteroclitus d15N values and length in fish collected
from both Alloway Creek and Hog Islands sites
(Fig. 2, Table 2), suggesting that there was some
increase in trophic position as fish grew. F. heteroclitus d15N values were 5 to 7 per mil greater than
primary producer d15N values, indicating that these
fish were feeding approximately two trophic levels
above primary producers. Gut content analyses of
F. heteroclitus have shown that a significant portion
of ingested material consists of algae and detrital
material (Kneib et al. 1980; Allen et al. 1994), and
that the proportion of algae and detritus to animal
prey items increases when fish become larger than
25 mm (Smith et al. 2000). The change in d15N
values we observed were similar to those seen by
Griffin and Valiela (2001) for F. heteroclitus from
Massachusetts, and the slopes of the regression
lines in both that study and ours indicated an increase of 0.5 to 1 trophic level as fish grew from
30 to 100 mm. It seems likely that algae and detritus are incidentally consumed by larger F. heteroclitus targeting invertebrate prey. As pointed out by
Kneib (2000), even if the detrital material is largely
unassimilated, F. heteroclitus can serve in the trophic
relay of macrophyte production by ingesting material while grazing on the marsh surface at high
tide, and then defecating into tidal creeks and
channels during low tide. This pattern of F. heteroclitus primarily feeding on the marsh surface during high tide has been found in numerous studies
(Weisburg and Lotrich 1982; Allen et al. 1994).
Several studies have suggested that microalgae
may be more important in estuarine food webs in
the spring, when macrophyte detritus is less available and marsh canopies are not fully developed,
allowing greater light penetration to the sediment
surface and potentially greater BMI production
(Wainright et al. 2000; Angradi et al. 2001). If such
a change were to occur, it may be evident in S isotopes, as the end-member values for macrophyte
detritus are enriched by 4 to 10 per mil compared
to BMI values (Tables 1 and 4). In Alloway Creek,
we did not observe a significant increase in the d34S
values of F. heteroclitus between June and August.
This observation is perhaps confounded by the fact
that much smaller fish were sampled in August. We
did observe a significant increase in d34S values
with increase in length at both the Hog Islands and
Alloway Creek Spartina sites (Table 2, Results section). This observation is consistent with a greater
contribution of macrophyte detritus into the F. heteroclitus food web as the fish grows. The concurrent
increase of d15N with the increase in length suggests that the greater role of macrophyte detritus
in the food web of larger fish is due to indirect,
rather than direct assimilation of detritus. Small
fish (, 25 mm) appear to be cleaner eaters compared to larger fish, capable of picking off such
microalgal grazers as copepods and polychaetes
(Smith et al. 2000). Larger fish not only ingest
more detrital material directly, but by feeding
deeper in the sediment may ingest more subsurface deposit-feeders, which use detritus to a greater
extent than surface deposit-feeders (Lopez and
Levinton 1987). Larger fish, and fish feeding later
in the summer, may incorporate a larger amount
of macrophyte production into their food web.
FOOD WEBS SUPPORTING FUNDULUS PRODUCTION IN
BRACKISH MARSHES
The difference in stable isotope signatures between F. heteroclitus using Phragmites, Spartina, and
restored marshes within the same creek system
provided strong support for the conclusion that juvenile and adult Fundulus spp. exhibit significant
side fidelity (Lotrich 1975; Talley 2000; Teo and
Able In press). The isotopic signatures of F. heteroclitus in the Alloway Creek system, where fish from
Phragmites marshes were approximately 2 per mil
depleted in C and 2 per mil enriched in S compared to fish from Spartina or restored marshes, is
consistent with several interpretations: a greater
contribution of P. australis to the food web, a greater contribution of SPM in Phragmites marsh food
Brackish Marsh Food Webs
webs, and a change in the isotopic composition of
BMI that provides a significant proportion of the
fishes’ food web support in all marsh types. Given
the reduced microalgal biomass in Phragmites
marshes, it is likely a combination of these factors.
Recently hatched F. heteroclitus in the Hog Islands
system also demonstrated site-specific isotopic signatures, consistent with the evidence from markrecapture studies that fish ,20 mm spend the majority of their time on the marsh surface (Able unpublished data). The fact that juvenile F. heteroclitus
occupying Spartina marsh in the Hog Islands system were 6 to 10 per mil depleted in 13C compared
to S. alterniflora suggest a very small role for S. alterniflora detritus in the food webs supporting recently hatched fish. As before, the question is
whether the depleted C signal in F. heteroclitus is
due to incorporation of P. australis detritus (P. australis occupies .80% of the marsh surface in the
Hog Islands area, Windham and Lathrop 1999),
BMI biomass, or SPM into the food web. Note that
at Hog Islands, the d15N values of recently hatched
fish were consistent with a primary producer with
a d15N value of 3–4 per mil (Fig. 4), which is closer
to the value of BMI than other primary producers.
The S isotopes for F. heteroclitus at Hog Islands were
enriched compared to BMI from Hog Islands
marshes, however, and indicate a potential significant contribution of P. australis detritus in this food
web. If BMI samples were even slightly contaminated by the presence of d34S depleted pyrite or
sediments, which have d34S values ranging from
220 to 210 (Peterson et al. 1986; Peterson and
Howarth 1987), thereby skewing the d34S value in
a negative direction, then a hypothesis that BMI
are one of the main components of the F. heteroclitus food web becomes more viable. SPM C and S
isotope values were both far enough removed from
recently hatched F. heteroclitus that it could represent at most 40% of the food web support, although the real contribution is probably much
less. The known food preference of many F. heteroclitus prey items (Allen et al. 1994; Smith et al.
2000), as determined by a variety of techniques, is
BMI (Creach et al. 1997; Buffan-Dubau and Carman 2000; Sullivan and Currin 2000). Based on
these results, and our interpretation of the stable
isotope results, we believe that BMI were a significant component of the food web supporting F. heteroclitus in these brackish marshes, especially recently hatched fish occupying pools on the marsh
surface. The 2 per mil difference in d13C between
Fundulus occupying the nearly adjacent Phragmites
and Spartina marshes we sampled is consistent with
less reliance on BMI and greater reliance on P. australis production in P. australis-dominated marshes.
TROPHIC SUPPORT OF FUNDULUS
SALT MARSHES
IN
507
RESTORED
This study presents a snapshot view of the recovery of trophic function in restored S. alterniflora
marshes in the Alloway Creek system. The mean
d13C value of F. heteroclitus from restored marshes
was intermediate between values of fish from naturally occurring S. alterniflora marshes and nearby
areas invaded by P. australis. F. heteroclitus from restored marshes had more depleted average d15N
values than fish from the unrestored marshes and
d34S values that were significantly depleted compared to fish collected from Phragmites marshes
(Table 3). We hypothesized that BMI may play a
greater role in the food web supporting fish production in restored marshes, as the decreased canopy may permit greater BMI biomass and production (Piehler et al. 1998). BMI biomass at the restored marsh sites was always greater than in Phragmites marshes, sometimes significantly so (Fig. 1),
and the stable isotopic data support the hypothesis
of greater BMI incorporation in the food web, although alternative combinations of SPM and
marsh macrophytes cannot be ruled out. F. heteroclitus using restored marsh habitat exhibited both
a wider range and greater standard error in isotope values than fish from the other marsh systems
(Fig. 3, Table 3). This may be due to either a greater variety of food sources available in restored
marshes or less site fidelity in fish collected from
restored marshes. When used across greater spatial
and temporal scales of marsh restoration, stable
isotope analysis may be a useful metric in assessing
the recovery trajectory of restored marsh systems
(Talley 2000; Weinstein et al. 2000).
ASSESSING THE ROLE OF MACROPHYTE AND
MICROALGAL PRODUCTION IN ESTUARINE
FOOD WEBS
A literature review of published stable isotope
studies where d13C values are available for BMI,
SPM, dominant macrophyte vegetation, and Fundulus spp., revealed that Fundulus mean d13C values
track BMI and SPM more closely than changes in
dominant macrophyte vegetation (Fig. 5). Sites in
Fig. 5 are ordered by increasing Fundulus d13C values. Data are from the Atlantic, Gulf, and West
Coasts of the U.S. Although salinity values were not
available for all sites, sites from brackish water environments have the most depleted SPM values,
and the most enriched SPM values were from polyhaline sites, so that there is a general trend of
increasing salinity along the x axis in Fig. 5. Fish
data represent F. heteroclitus, with the exception of
data from Mississippi (MS; F. majalis), and Tijuana
Estuary and Mission Bay (TJE and MB; Fundulus
508
C. A. Currin et al.
Fig. 5. Plot of published mean d13C values for benthic microalgae (BMI), suspended particulate matter (SPM), Phragmites
australis (Phragmites), Spartina spp., and Fundulus spp. from a
variety of sites. Data are plotted in ascending order of mean
d13C Fundulus values. Sites and appropriate references are as
follows: HI-Pa, Hog Islands Phragmites (this study); AC-Pa, Alloway Creek Phragmites (Wainright et al. 2000); HI-Sa, Hog Islands
Spartina (this study); AC-Pa Alloway Creek Phragmites ( June, this
study); AC-Pa, Alloway Creek Phragmites (August, this study); ACSa, Alloway Creek Spartina ( June, this study); AC-Sa, Alloway
Creek Spartina (August, this study); MS, Mississippi Graveline
Marsh (Sullivan and Moncreiff 1990); TJE, Tijuana Estuary
(Kwak and Zedler 1997); MHC, Mad Horse Creek (Wainright
et al. 2000); MB, Mission Bay California (Talley 2000); GA, Sapelo Island, Georgia (Peterson and Howarth 1987); and NC,
Port Marsh North Carolina (Currin et al. 1995).
parvipinnis). S. alterniflora is replaced by S. foliosa
at TJE and MB. Figure 5 illustrates that across this
wide spectrum of sites, Fundulus d13C values remain
closer to BMI (within 2.2 per mil) than any other
primary producer, with the exception of at AC-Pa
(Wainright et al. 2000). BMI values in Wainright et
al. (2000) were pooled samples from creek banks
and marsh surface, which might explain this discrepancy. S. alterniflora d13C values, which fall within the narrow range indicated on Fig. 5, were between 2.1 and 6.6 per mil enriched relative to Fundulus d13C values from S. alterniflora-dominated
sites. P. australis also exhibited little site-to-site variation, and is 3.4 to 5.9 per mil depleted compared
to F. heteroclitus collected from Phragmites marshes.
SPM d13C values are 2.1 to 6.6 per mil depleted
than Fundulus values, and follow the same general
trend as BMI and Fundulus.
The Fundulus values from Spartina marshes in
Fig. 5 could be explained by food webs composed
of a changing mixture of SPM and Spartina, or by
a significant contribution of BMI at all sites. Several
of these studies also included N and S isotopes to
further distinguish the food web, and Fundulus N
and S values have led several authors to conclude
that Spartina and BMI, rather than SPM, must be
the primary base of the Fundulus food web (Sullivan and Moncreiff 1990; Currin et al. 1995; Kwak
and Zedler 1997; Talley 2000). Figure 5 also illustrates that a mixture of P. australis and SPM cannot
provide the d13C value of Fundulus in P. australis-
dominated systems in brackish marshes, as Fundulus is several per mil enriched relative to both these
sources.
The annual primary production of P. australis is
estimated to be 400–800 g C m22, which is greater
than the estimated annual areal production rates
for phytoplankton, S. alterniflora, or BMI in estuarine ecosystems (Pinckney and Zingmark 1993;
Ibanez et al. 2000; Sullivan and Currin 2000). Decomposition rates of Phragmites leaves are similar
to those of other marsh macrophytes and demonstrate that a significant portion of P. australis C enters the microbial food web and can be transferred
to higher trophic levels (Warren et al. 2001). Given
the high rate of annual primary production and
the large areas dominated by P. australis, it is not
surprising to find that the isotopic signatures of
fish using marsh systems where P. australis occurs
exhibit an isotopic signature consistent with the incorporation of P. australis production into fishery
food webs (Wainright et al. 2000; Weinstein et al.
2000). In order to refine our estimates of the contribution of phytoplankton, BMI, and macrophyte
detritus in brackish marsh food webs, it will be necessary to employ additional techniques that will
provide a clear distinction between possible end
members. Approaches used elsewhere include isotope labeling experiments (Herman et al. 2000;
Hughes et al. 2000) and the use of molecular biomarkers in addition to stable isotopes.
This study suggests that BMI play a significant
role in the food web of F. heteroclitus occupying the
marsh surface, and that although F. heteroclitus .25
mm ingest considerable amounts of detritus and
algae, F. heteroclitus do not assimilate C and N from
these food sources to any significant degree and
are functionally at least two trophic levels above
primary producers throughout their life history.
Macrophyte detritus may play an increasing role in
the food web supporting larger fish, because of an
increase in the consumption of detritivores and
omnivores by larger, deeper-feeding F. heteroclitus.
Although we cannot definitively estimate the contribution of P. australis in the food web of F. heteroclitus, the evidence presented is consistent with an
increasing contribution of P. australis as the relative
abundance of P. australis increases within a tidal
creek system, concurrent with a reduction in BMI
biomass on the marsh surface. We note that in examinations of the role of marshes in estuarine food
webs, the term marsh production should include
all primary producers uniquely identified with the
marsh surface, including both macrophytes and
BMI communities.
ACKNOWLEDGMENTS
We thank T. Farley, A. Stelling, S. Brown, S. Hagan, K. Bosley,
and B. Lemasson for assistance in the field and laboratory. We
Brackish Marsh Food Webs
also appreciate the significant logistical support contributed by
the Rutgers Marine Field Station, the New Jersey Marine Science Consortium, the National Oceanic and Atmospheric Administration Center for Coastal Fisheries and Habitat Research,
and the Salem County Rutgers Cooperative Extension. This research was funded by the Marsh Ecology Research Program and
Public Service Enterprises Group. This is contribution no.
NJSG-03-518 of the New Jersey Sea Grant College Program and
contribution no. 2003-13 of Rutgers University Institute of Marine and Coastal Sciences.
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Great Bay Boulevard, Tuckerton, New Jersey 08087.
Received for consideration, March 25, 2002
Revised, October 20, 2002
Accepted for publication, November 11, 2002