41 - Association for the Sciences of Limnology and Oceanography

Notes
802
Limnol. Oceanogr., 4 l(4), 1996, 802-809
0 1996, by the American
Society of Limnology
and Oceanography,
Inc.
Interannual variability of a salt-marsh ecosystem
Abstract-Data from Great Sippewissett Salt Marsh are
used to gauge the extent of change of Spartina aZternzj7ora
marsh during periods of several to 22 yr. Our data all relate
to plant production: from aboveground, maximum plant
biomass measured over the entire period; from belowground, live root and rhizome biomass measured in
1974 and 1983, CO, evolution from the sediments for 7
yr, and pore-water concentrations of dissolved sulfide for
6 yr. All the measures indicated a relatively low degree of
interannual change in salt-marsh areas vegetated by talland short-form S. aZtern$ora.The similarity in both plant
and biogeochemical parameters between years is likely related to the regular, high-frequency tidal flooding of grass
stands. These interannual comparisons of each quantified
parameter support the contention that measurements made
in any single year can be applied to other years with suitable
precautions to account for seasonal cycles. Our data also
illustrate the importance of long time series for establishing
sound correlations in environmental
data.
Understanding the degree of interannual change in ecosystems is important for both ecological theory and the
practical study of ecosystems. In planning studies of ecosystem function and structure, it is generally necessary to
know the extent to which observations made in a given
year are applicable to those made in other years. Even in
relatively simple systems, it is often impossible to investigate all the necessary components simultaneously. The
construction of ecosystem models usually requires integration of diverse data sets collected over many years
(Kremer and Nixon 1978; Cammen et al. 1982). Studies
of succession require periods comparable to the life cycles
of the dominant organisms (Reiners 1992). As Krebs
(1991, p.7) pointed out:
All ecologists favor long-term studies. . . . But, like other
scientists, ecologists prefer to do experimental work. . . .
We must combine these two approaches to solve the major
ecological questions.
Unfortunately,
given the realities of ecological research,
interannual variations are often assumed to be small based
only upon available qualitative indicators such as species
composition.
In 25 yr of mostly experimental study of
Great Sippewissett Marsh (GSM), Falmouth, Massachusetts we have also collected quantitative, long-term data
that address the question of the degree of temporal change
in this salt-marsh ecosystem.
Our primary focus is to determine the level of interannual variation in basic parameters relating to the production
of individual
stands of
Spartina alterniflora. We
do not examine the spectrum of spatial variation
across
the marsh. One confounding feature in assessing temporal
trends of north-temperate marshes is the strong seasonal
variation in almost all major ecological parameters (Jass-
by and Powell 1990). We have attempted to circumvent
this problem
by analyzing
annual
cycles and using em-
pirically determined maxima.
Salt marshes subject to extreme changes in conditions,
such as large changes in salinity due to infrequent flooding
or extreme alterations in freshwater flows or high rates
of rise in relative sea level, can show significant interannual alterations in productivity.
Over longer periods,
the plant species composition in such marshes may also
change drastically. Even in marshes with relatively constant external forcing (primarily by tides), large interannual variations in plant production and community structure can be produced on scales of meters by periodic
accumulations of wrack (Pethick 1974; Hartman et al.
1983; Valiela et al. 1985). Our results from GSM are
representative of the more typical conditions of the larger
expanses of coastal marshes, where hydrologic conditions
are relatively constant and wrack accumulations are generally confined to the marsh-upland boundary-a
marsh
where, if there is “constancy”
among years, we should
find it. Our findings should be representative of coastal
marshes with regular flooding and moderate rates of sealevel rise.
Long-term biological data sets for which data quality
is known and consistent sampling has been conducted are
relatively scarce for coastal ecosystems (Wolfe et al. 1987).
We report on a series of such measurements made in short
and creekbank Spartina marsh. The assays all relate to
production of S. aZternz$ora, the dominant macrophyte
of regularly flooded intertidal salt marshes along the Atlantic coast. Measurements included aboveground plant
biomass (harvest and plant height), belowground live root
and rhizome biomass, and belowground CO2 evolution
and dissolved sulfide concentration. These parameters are
all aspects or results of the carbon cycle of the salt marsh.
The aboveground biomass results extend for more than
two decades while underground biomass data are from
1974 and 1983. CO, efflux and sulfide concentrations
were measured for 6 yr. Much of the plant biomass data
is calculated from plant height measurements made once
a year in early autumn, and these measurements are proportional to maximum standing crop. Seasonal studies of
the patterns of growth and decay of Spartina have been
presented previously (Valiela et al. 1975, 1976; Howes et
al. 1984). Measurements of CO2 and sulfide were made
at intervals through the active season to encompass seasonal variations, which are mostly temperature controlled
(Kaplan et al. 1977; Howes et al. 1985a), and comparisons were made of the maxima in each year.
All the marsh parameters were measured at GSM, which
our group has studied since 1970. The marsh sites include
the two 3 lo-m2 experimental control sites for our fertilization studies (Valiela et al. 1975) as well as other comparable “short Spartina” sites. These sites are occupied
Notes
by S. alterniflora of -30 cm in height. The sites are
intertidal, normally flooded l-2 times per day, are ~2 m
from the nearest creekbank, and have highly reduced sediments and poor drainage (Howes et al. 1986). Additional
measures of maximum plant height and biomass came
from “creekbank marsh” -S. alterniflora growing on the
banks of the tidal creeks from the control (N = 2) and
fertilized plots (N = 12). The data for creekbank Spartina
height are comparable to the control data because fertilization has no effect on the biomass of creekbank Spartina
(Valiela et al. 1978). The data for aboveground biomass
of S. aherniflora are from calculated total living and dead
biomass from an empirically
derived relationship
between the harvested dry weight and measurement of the
10 tallest nonflowering plants in a sample and from harvested dry weight (60°C) of the maximum standing crop
of living and dead biomass produced that year.
Measurements were made on duplicate, randomly
placed 0.1 -m2 quadrats taken within each marsh type in
each plot. The relationship between measured and calculated biomass was determined by weekly sampling
through the 1983 growing season to find the maximum
biomass and plant height (within samples). A linear regression gave an adequate estimate of biomass for Spar-
tina:
gm-2
803
goor,
800
,
-
,
,
,
,
,
,
A
,
,
Short
,
,
,
Spartina
/
,
,
,
,
,7
alterniflora
600
0)
'6
500
PO
h
4
400
300
0 control
-overall
2
mean
01 “““““““““‘1’
71
2000
73
,
75
,
,
77
,
,
(
79
(
,
81
,
B
83
,
,
Tall
,
85
,
,
Spartina
87
,
,
69
,
,
91
,
I
I
alterniflora
El
a
control
0l”“““““““““‘I
71
73
75
77
/
DlOtS
79
81
83
85
87
69
91
Year
= 93.6 + 11.6 x cm
where cm is the average height of the 10 tallest nonflowering plants in the sample (r2 = 0.83, N = 105). A smaller
set of measurements from earlier years did not show a
significantly different relationship (data not shown). We
also have periodic comparisons of harvested and calculated maximum biomass throughout the two decades. A
paired t-test of these Spartina data from creekbank (P =
0.6, N = 23) and short-form (I’ = 0.3, N = 40) marsh
areas indicated no significant difference between harvest
and calculated biomass numbers. The relation between
maximum biomass and total grass productivity
in GSM
was discussed by Valiela et al. (1975) and for other marshes by Roman and Daiber (1984), Shew et al. (198 l), and
Kaswadji et al. (1990).
We sampled for living roots and rhizomes with 6.5cm-diameter cores to depths >20 cm, below which there
was no living plant tissue (Valiela et al. 1976). Roots and
rhizomes were separated by hand, dried, and weighed,
and their carbon content was measured with a PerkinElmer CHN elemental analyzer. The 1983 data are from
triplicate cores.
CO2 losses through the sediment surface were measured
with field and laboratory techniques in which cores and
bell jars were used to isolate sediment samples and collect
gases for analysis by gas chromatography
(Howes et al.
1985a). These data do not include plant respiration except for root respiration that did not take place through
aerenchyma. Data at each sampling are from three marsh
sites, with 3-6 cores taken per site. Sulfide concentrations
were measured with pore-water sippers. Samples were
fixed in the field and handled and analyzed according to
Howes et al. (1985 b) to prevent errors due to sulfide loss
or oxidation. Precipitation data are from the University
,
Fig. 1. Maximum aboveground biomass of Spartina alternifora at Great Sippewissett Marsh. A. Short S. alterniflora in
control plots. B. Tall S. alterniflora from control plots and from
experimentally
fertilized
plots.
of Massachusetts Cranberry Experiment Station at the
head of Buzzards Bay, -20 km north of the study marsh.
Water and air temperatures and solar radiation are from
Woods Hole, at the other end of the bay, -7 km south
of the marsh. Monthly mean sea-level data are from the
NOAA database for the tide station at Woods Hole. We
used deviations from the 60-yr trend averaged from June
to August.
Aboveground, maximum living and dead biomass in
our short Spartina plots varied from 383 to 523 g m-2
in control stand 1, similar to the range for control stand
2 (342-5 10 g me2) (Fig. 1A). There was no significant
trend to the time series in either stand; even adjacent
years showed no significant (P < 0.05) autocorrelation.
Control 1 produced - 8.5% more biomass than control
2 -a statistically but probably not biogeochemically
significant difference considering that most of the Spartina
production passes through the detritus pathway. The coefficients of variation, 10% for control 1 and 9% for control 2, were not significantly different (P < 0.05, T-test)
from each other.
S. alterniflora production, plant height and density, is
controlled principally by nitrogen supply (Valiela et al.
1978). Nitrogen supply in marshes with high organic sediment is controlled principally by sediment redox (Morris
1980; Howes et al. 198 l), which is controlled by air entry
into the sediment as a result of drainage and(or) evapo-
Notes
804
7200
I
I
I
I3
fl 7150
3ii
4
4
P
0
2
A
-Q
6950
M
.r(
$
6900
I
I
I
I
I
I
I
0 June, July, August
I
I
-
I
I
l
I
I
l
l
,
l
89
90
1930 to 1990 trend
7100
7050
7000
6850
71
I
I
I
I
I
I
I
72
73
74
75
76
77
78
I
79
I
I
I
I
80
81
82
83
I
I,
84
85
86
l
,
87
88
Year
Fig. 2. Mean monthly tides at Woods Hole plotted relative to datum of 1972. The values
for June-August are highlighted with circles. The solid line is the regression on mean annual
levels from 1930 to 1990.
transpiration (Howes et al. 1986). Low sediment redox
in salt marshes results primarily from the accumulation
of dissolved sulfide produced by microbial sulfate reduction in the surficial sediments. Other factors also affect
a00
32
“:
E!
w
Radiation,
700
- 700
600
28
500
- 650
011
0V
400
'fi
24-
7
600
300
2
i a00
“:
El
1600
w
1400
I
I
.----
I
I
I
I
I1
May to July
I
I
I
I,
rain
1
I
I
I
I
I
35
-80
30
- 70
0 Biomass
25
2z
1200
-
I50 fl
- 50
E!
20
15 $4oj
1000
:
a00
!i
.A
P
600
1*
400
rl
200
- 30 r,
10
t -
6 mean
OLI”“““““““I~I
'7
1 ‘73
‘75
5
sea level
- 20
-10
JO
‘77
‘79
‘81
‘83
‘85
‘87
‘89
‘91”
Fig. 3. Top- maximum aboveground biomasses (mean of
two sites) plotted with June-August solar radiation at ground
level, and June-August mean air and water temperatures. Bottom - mean maximum aboveground biomass for unfertilized
creekbank marsh (mean of two sites) plotted with May-July
rainfall and mean sea-level deviations from the 1930-l 990 trend
for June to August.
plant production (e.g. salinity, Nestler 1977; Morris et al.
1990). The net result of all these factors is that short
Spartina is stunted by a high water table leading to low
redox from sulfide accumulation that reduces nitrogen
uptake; creekbank stands approach potential growth maxima as controlled by initial nitrogen supply, light, and
temperature. We compared variations in aboveground
height in tall and short stands of S. alterniflora with meteorological data (precipitation,
air and water temperatures, and incident solar radiation) and with variations
in local sea level during the two decades of study. These
comparisons were first made on individual
study plots
and then on the means of replicate plots using the number
of years to derive the degrees of freedom in the analyses.
Visual inspection of Fig. 1A suggests a correlation between the variations in short Spartina biomass in the two
plots, especially during the early 1980s. If a relation between environmental
conditions and biomass is to be
found, it should be most evident during those years. We
examined a number of environmental factors summed or
averaged over various time periods during the growing
season to see whether there was any clear indication of
such a relationship. The tide data (Fig. 2) illustrate both
the smaller variability in monthly average levels in summer compared with the entire year and the difference
between measuring monthly deviations from the rising
long-term mean vs. the absolute datum. Of the possible
correlations with peak Spartina biomass from either a
logical consideration or visual inspection of the data, the
most likely were monthly (June-August) mean tidal deviations from the mean long-term trend (June-August
solar radiation, air temperature, and water temperature)
and May-July rainfall (Fig. 3). These factors were chosen
because Spartina grows in air but is regularly flooded by
tides, so air and water temperatures affect it, as does
805
Notes
Table 1. Regression statistics for tall (creekbank) and short (inland) Spartina alterniflora maximum
environmental
factors 197 l-l 99 1.
Tall
Mean sea level, Jun-Aug
Air (“C), Jun-Aug
Solar radiation, Jun-Aug
Water (“C), Jun-Aug
Rain, May-Jul
aboveground
biomass and
Short
Sign of
relation
r2
PC
Sign of
relation
r2
P-c
+
0.296
0.020
0.050
0.018
0.044
0.07
0.71
0.44
0.66
0.46
+
+
-
0.105
0.079
0.000
0.022
0.00 1
0.10
0.22
0.40
0.52
0.87
sunlight. Tidal deviations affect sediment oxidation. Rain
dilutes the salinity of surface marsh sediments, and Spartina grows better at lower salinities. Rain is distributed
fairly uniformly throughout the year on average (average
annual total during the study period was 1,229 mm). We
tried both annual and growing season precipitation.
We first analyzed only the 198 1-1991 decade because
these data covered the period during which most of the
other carbon cycle parameters were measured. Within
this subset of data, we could predict 64% (adjusted r2,
stepwise multiple regression) of the variability
in mean
maximum standing crop biomass of the two plots from
average water temperatures during the growing season (P
= 0.01) and June through August total radiation (P =
O.OOS),both positive correlations. Upon obtaining these
results, we expanded the analysis to include the environmental data from the previous decade. When we analyzed
the full 22 yr, the multiple regression model was not
significant (adjusted r2 = -3%). None of the analyses
done separately on either one of the plots for the entire
period showed any significant correlations with the environmental variables (Table 1). It is possible that controlling factors changed over the study period or that the
significant correlations found in the first analysis were
simply spurious (i.e. when enough correlations are tried
a posterior-i, some will eventually show a significant correlation merely by chance).
For creekbank marsh, we have data from both control
and fertilized plots (Fig. 1B) for the 15 yr from 1977 to
1992. As with the short grass areas, there were no significant temporal trends or autocorrelations among years.
In addition, we found no differences between the control
and the fertilized plots except for a slightly greater variability in the control plots (control C.V. = 16%; fertilized
C.V. = 11%). Unlike the more inland marsh, creekbank
marsh does not show a consistent increase in biomass
with fertilization (Valiela et al. 1978). The smaller interannual variability of maximum biomass suggested in the
data from the fertilized vs. control creekbank stands is
consistent with the hypothesis that adding nitrogen reduces one source of variation by assuring that nitrogen
uptake by the plants can remain at the physiologically
maximum level, manifesting itself as less variable biomass accumulation (Valiela et al. 1975, 1978). Correlation analysis performed over the 15-yr period on the
creekbank data from the control plots revealed a margin-
ally significant negative correlation between deviations
in mean sea-level rise and maximum standing crop (P =
0.067, r = 0.55).
The 1974 root and rhizome biomass data were reported
in dry weight units by Valiela et al. ( 1976); we converted
these data to carbon using the oven-dried root and rhizome material archived for carbon analysis. Carbon is a
more accurate estimator of production than dry weight,
and the seasonal picture is more clearly defined. The standard errors for the 1983 dry weights averaged -45% of
the means (data not shown) compared with the carbon
values, which had standard errors that averaged 2 1% of
the means. This difference is likely due to inorganic material (e.g. iron), which remains associated with the roots
and which, because of its relatively high density, increases
the variability observed in dry weight. The seasonality of
root and rhizome biomass was similar in 1974 and 1983,
and biomass was slightly (not statistically
significant)
higher in 1983 (870 vs. 1,020 g m-2 respectively). Aboveground biomass varied in the opposite direction (50 1 vs.
370 g m-2). In 1983 there was a deviation from the longterm mean sea-level trend (71 mm) that was near the
maximum observed during our 20-yr study period; the
1974 value was near the minimum (28 mm) (Figs. 2 and
3). These data suggest there might be a response to flooding frequency whereby more plant resources go into roots
with greater flooding. A flooding response is consistent
with the observation that the ratio of roots to shoots is
lower in the better drained creekbank marsh than in the
short Spartina marsh (Valiela et al. 1976) and with the
finding that the root: shoot ratio varies with nitrogen
availability (Morris 1980).
Because S. alterniflora, like most perennial grasses,
translocates and stores photosynthate during winter to
support initial growth the following spring, we examined
the relationship of each year’s aboveground growth relative to the previous year. No significant relationship was
observed for the 20 yr of study, possibly due to the relatively small amount of roots and rhizomes that overwinter in north-temperate
marshes (White and Howes
1994).
CO2 efflux data from the marsh surface were collected
for a period of 7 yr (Fig. 4). In each year, measurements
were made in August-September,
with seasonal measurements in some years to show the annual cycle. We
have not attempted to draw a curve through the points,
Notes
806
0.4
/
I
I
I
I
I
I
I
.... ..“. A
Mar
May
Jun
Jul
Aug
Sep
act
Nov
I
,
30
0
1978
E
0
v
1979
1980
E
u
v
0
1981
1982
n
1983
Dee
J
25
2
Jan
Fig. 4. CO, flux from the short Spartina marsh surface. For comparison, the mean water
temperature is shown by the curve. Each point represents the average of 4-8 replicates from
three different short Spartina alterniflora sites, C.V. < 10%.
but we do include a curve of mean water temperature
over most of the same period to illustrate the general
relationship (Fig. 4). The increasing CO, flux lagged behind temperature increase in spring, increased faster than
temperature as plant senescence began in late summer,
and dropped in proportion to temperature in autumn
(Howes et al. 1985a). In any one sampling, the variation
0
0
v
Jun
0
Aug
1
1963
1984
1985
v
0
n
1986
1989
1991
Dee
2
mM
3
Dissolved
4
5
6
Sulfide
Fig. 5. Sulfide concentrations (f SE) in short Spartina alternzjZoramarsh sediments measured during the 2 weeks around
1 September. 1983 datum is the mean of three sites on three
dates; 1984-three
sites, one date; 1985 -two sites, four dates;
1986-two sites, three dates; 1989 -three sites, one date; 199 lone site, one date. Inset gives seasonal changes for 1984 at four
depths (O-2 cm, l - 5 cm, V- 10 cm, v- 20 cm), showing that
the relative constancy between years is not a result of lack of
seasonal change.
in efflux was small (< 10%). Sampling was always at low
tide during the same stage of the lunar tidal cycle. It
appears that the composite seasonal cycle is relatively
constant regardless of the subsample of the data that comprises it.
Dissolved sulfide concentration
in marsh sediments
changes greatly through the seasons in relation to the
production of sulfide in the anoxic, belowground decomposition cycle (Valiela et al. 1976) and sulfide reoxidation
(Howes et al. 1984). We have most of an annual cycle in
short Spartina marsh for 1984 and analyses from the
period around 1 September in 1983, 1985, 1986, 1989,
and 199 1, which are not distinguishable statistically from
those for 1984 (Fig. 5). In salt marshes, there is a close
coupling between sediment conditions (nutrient uptake,
oxidation-reduction
potential, sulfide concentration, salinity) and plant production (Howes et al. 1986; Koch et
al. 1990; Morris and Haskin 1990). This coupling may
play a role in the relatively low interannual variation in
both aboveground plant biomass and dissolved sulfate
levels.
Overall, the correlations were weak between aboveground biomass of both short- and tall-form S. alterniJlora and various regional environmental variables: rainfall, air and water temperatures, solar radiation, and sealevel deviations from the 60-yr trend. In all cases, ~30%
of the interannual variation was described (Table 1). These
results seem to contrast with a detailed 5-yr study of a
South Carolina salt marsh, in which interannual differences in July and August absolute sea level were found
to be strongly and positively related to annual production
of Spartina (Morris and Haskin 1990; the regression in
our data was negative). The basis for the relationship is
believed to be that decreased flooding frequency results
in elevated interstitial salinities to the point where plant
growth is inhibited.
Notes
Table 2. Interannual
Marsh.
807
statistics for the parameters measured during the 22 yr of study of Spartina alterniflora in Great Sippewissett
Short Spartina biomass (g m-“)
Creekbank biomass (g m-2)
Aug CO, production (mol m-2 d-l)
Aug sulfide concn at 5 cm (mM)
Belowground biomass (g C m-2)
N (v)
Mean
SD
C.V. (%)
Range of annual means
22
15
6
6
2
440
1,260
0.29
3.71
946
32
140
0.018
0.48
75
7.3
11.0
6.4
12.9
7.9
370-50 1
1,023-l ,623
0.27-0.32
2.94.5
872-1,021
There are, however, major differences between the South
Carolina and Massachusetts marshes that provide insight
into additional complexities in the relationship between
salt-marsh production and variations in meteorology or
sea-level rise. First, there was almost a 1O-cm interannual
sea-level variation in South Carolina compared with only
7 cm in Massachusetts. More important is that interstitial
salinities in GSM short S. alterniflora marsh are much
lower than in South Carolina and do not reach a level at
which salinity has an important inhibitory effect (Howes
et al. 1986). De Leeuw et al. (1990) reported a negative
correlation between aboveground production and rainfall
deficit that they believed was due to changes in soil conditions, but all of their synchronously varying communities were higher in the intertidal zone than ours and
flooded much less frequently. Therefore, one might expect
that the soil salinity and moisture content of their communities would show a much greater weather influence
than would be the case in our marsh. Furthermore, although we have seen an apparent “greening” of the marsh
following rain (Valiela et al. 1976), experimental watering
with freshwater did not increase aboveground biomass
(Valiela et al. 1982).
It appears that year-to-year changes in production in
more frequently flooded salt-marsh areas may be less
susceptible to variations in sea-level rise. The l-2 times
daily flooding of GSM may have removed the potential
for the salinity-sea-level
interaction that seems to mediate productivity
in the short Spartina marsh in South
Carolina. However, increased sea levels increase both the
flood duration and frequency. Because sediment oxidation in short Spartina marsh is generally controlled by
water-table excursion as controlled by the extent of water
removal between tides (Howes and Teal 1994; Howes et
al. 1986), increased flooding may negatively affect production by decreasing sediment oxidation. The best correlations of peak biomass of both tall- and short-form
Spartina were with sea-level deviations, with increasing
sea levels having a negative effect on biomass (Table 1).
As might be expected from the reliance of creekbank
sediment oxidation on pore-water drainage facilitating air
entry, the negative effect of increased sea levels was greater in creekbank than in inland grass areas.
S. alterniflora is generally restricted to the intertidal
zone, so large increases in flooding can result in conversion to open water and decreases to a shift in dominant
plant species. With moderate sea-level rise, areas vegetated by S. alternijlora maintain their elevation through
accretion of plant organic matter and trapped inorganic
particles. Although on average sea level is rising each year,
in any given year the average level may be higher or lower
than the previous year (Fig. 2). Thus, the effects of varying
sea levels over the long term should ordinarily be considered in terms of deviations from the long-term trend
as opposed to from a fixed datum, as was done by Morris
and Haskin (1990). At GSM during the study period, the
average sea-level rise has been -5 cm, similar to estimated marsh accretion (Orson and Howes 1992). The
effect is that sea level relative to marsh surface elevation
(on average) has been constant, whereas relative to a fixed
datum, both have risen.
Our other biogeochemical indicators are more closely
coupled to underground processes but still intimately connected with Spartina ecology. Aboveground production
supplies the organic matter that is translocated underground and forms the plant tissues in that part of the
system. When these tissues die, they become a part of the
peat, are removed from the marsh, or are decomposed
in place. Decomposition to CO2 accounts for at least 80%
of belowground production (Howes et al. 1985a). Most
of this decomposition occurs in the first year, so that while
COZ production is affected by production in previous
years, the effect is very small (Howes et al. 1985a; Valiela
et al. 1985; White and Howes 1994). Most of the sediment
is anoxic, so sulfate reduction accounts for a large part of
belowground decomposition.
The concentration of the
sulfide so produced is controlled by the balance between
production (highest during autumn when the grasses are
senescing and soil temperatures are still high) and consumption by oxidation (which brings the concentrations
down again in spring and early summer, Howes et al.
1984). By whatever pathway the plant parts decompose,
they produce COZ, which eventually passes to the atmosphere or is to a small extent reabsorbed by growing
plants. The production of CO2 is the best measure available to us of the integrated biological activity within the
marsh sediments (Howes et al. 1985a).
The concentrations of sulfide, the flux of CO2 to the
air, and the biomass of parts of living and dead plants
belowground all have annual cycles. The comparison values in a given year with the values at a similar point in
the annual cycle in other years gives a measure of temporal variability
(C.V. between years) within the saltmarsh system. For the data with measured annual cycles,
we used the data from the end of August to the beginning
of September for comparison. For sulfide, we chose the
5-cm-depth level, which is where the roots are most active. The variation at greater depths was slightly less and
808
Notes
-2% greater at the 2-m level, as might be expected because some oxygen penetrates to this depth (Howes et al.
1986). The C.V. is about + 10% (Table 2), equivalent to
the variability
between sites. The ranges of values are
considerably larger, especially for the creekbank marsh.
The variability
in short Spartina stands in GSM is
comparable to that found in the aboveground standing
crop measured in a Japanese IBP (Int. Biol. Program)
grassland for all species (11.2%), although the dominant
Miscanthus sinensis showed a C.V. of 15.9% (Shimada et
al. 1975). Variations in productivity
in terrestrial grasslands are strongly related to variations in rainfall (Figueroa and Davy 199 1; McNaughton
1985). Stability in
these systems is related to diversity, with the explanation
that with greater diversity, there are more likely to be
species present that can thrive during environmental perturbations and compensate for those competitors that
cannot (Tilman and Downing 1994). In contrast, regularly
flooded salt marshes, like GSM, are well watered and have
a low diversity of higher plants. These are “highly connected ecosystems” that need fewer species to be stable
and have more resilient populations and a more persistent
composition, but are more likely to lose species if one
species is removed (see Pimm 1984). The nature of the
short Spartina salt-marsh system is determined by the
regular tidal inundation it experiences and the resulting
salinity, high sulfide, and low redox conditions that limit
the plants that can thrive there to a single species.
We believe that the reproducibility
of the cycles described here for the periods during which they were studied demonstrates a degree of invariance within the short
Spartina part of the salt-marsh system that is driven by
regular tidal inundation and that justifies considering any
year comparable to another within the bounds of our
abilities to measure marsh processes. The variability
in
the plants is about the same as that in CO, and S2-, but
the degree to which this is the result of cause and effect
or simply of similar random variation is unknown. The
effects of interannual variations in aboveground biomass
(plant height) on consumers in the marsh, especially insects feeding directly on the standing plants, is potentially
significant and requires further study. Although we believe that the average variation (of the order of + 10%)
can be biologically significant, as an interannual variation
it is small relative to our ability to describe the biogeochemistry of this system at this level of long-term effort.
John M. Teal
Brian L. Howes
Woods Hole Oceanographic Institution
Woods Hole, Massachusetts 02543
Acknowledgments
We thank M. Taylor, D. Goehringer, S. Brown-Leger, R. Van
Etten, and N. Persson for field assistance and A. Gifford and
D. Gifford for use of their salt-marsh property. I. Valiela deserves special thanks for his active participation in earlier phases
of this research and for discussions since its beginning. The
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Submitted: 24 May 1994
Accepted: 7 November 1995
Amended: 14 February 1996
Errata
In the article by Chandy and Greene (July 1995: Vol. 40, No. 5), the regression equations (p. 950) for Pseudocalanus
and Acartia should ready = 0.141~ - 4.75 and y = 0.13x + 1.24, and the slopes from these regressions should read
y = 0.33x + 5.89 for P. newmani and y = 0.66x + 2.25 for A. Zongiremis. It thus follows (p. 953) that for the Acartia
experiments E = 0.33 h-l from the regression slope and for the Pseudocalanus experiments E = 0.66 h-l from the
regression slope.