Disturbance in Georgia salt marshes: variation across
space and time
Shanze Li1,2 and Steven C. Pennings2,†
1State
Key Joint Laboratory of Environmental Simulation and Pollution Control, School of Environment, Beijing Normal University,
Beijing 100875 China
2Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204 USA
Citation: Li, S., and S. C. Pennings. 2016. Disturbance in Georgia salt marshes: variation across space and time.
Ecosphere 7(10):e01487. 10.1002/ecs2.1487
Abstract. We documented the frequency and effect on live biomass of five different types of disturbance
over 14 years in creekbank and mid-­marsh zones of eight salt marshes dominated by Spartina alterniflora in
Georgia, USA. Wrack (floating debris) and creekbank slumping were the most common disturbances at the
creekbank, and snails were the most common disturbance agent in the mid-­marsh. Disturbance frequency
varied among sites due to differences in plot elevation and landscape position. Wrack disturbance at the
creekbank was positively correlated with plot elevation, and both initial slumping and terminal slumping
of creekbank plots were negatively correlated with plot elevation. Wrack disturbance at the creekbank and
snail disturbance in the mid-­marsh were also most common at barrier island vs. interior marshes. Disturbance varied up to 14-­fold among years. Wrack disturbance at the creekbank was negatively correlated
with river discharge and sea level, and initial slumping of creekbank plots was also negatively correlated
with sea level. The different disturbance types varied in their effects on end-­of-­year standing plant biomass. At the creekbank, wrack disturbance reduced biomass in affected plots by ~46%, but slumping did
not affect biomass until the plot was totally lost. In the mid-­marsh, slumping and wrack were not important disturbances, but snail disturbance reduced biomass in affected plots by ~70%. In addition, abiotic
conditions (river discharge, maximum monthly temperature, sea level, and precipitation) strongly affected
year-­to-­year variation in biomass. Across the entire landscape, fewer than a quarter of the plots on average
were disturbed, and disturbance reduced overall standing biomass by ~18% in the creekbank zone and
~3% in the mid-­marsh zone. Our results indicate that wrack has fairly strong effects on end-­of-­year biomass at the creekbank. Overall, however, variation in abiotic conditions among years had stronger effects
on end-­of-­year standing biomass in both marsh zones than did disturbance.
Key words: climate; Long-Term Ecological Research; long-term monitoring; plant productivity; Spartina alterniflora.
Received 5 April 2016; revised 16 June 2016; accepted 21 June 2016. Corresponding Editor: D. P. C. Peters.
Copyright: © 2016 Li and Pennings. This is an open access article under the terms of the Creative Commons Attribution
License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
† E-mail: [email protected]
Introduction
et al. 2011), species composition (Shumway and
Bertness 1994, Platt et al. 2015), diversity (Strong
1977, Connell 1978), and biogeochemical cycling
(Bernhard et al. 2015). For logistical reasons,
many studies have investigated the effects of
disturbance at small spatial and short temporal
scales (Dayton 1971, Bertness and Ellison 1987,
Fischer et al. 2000), and we have a weaker understanding of how disturbance varies at the landscape level or over longer periods of time.
Natural disturbances play important roles in
many coastal ecological systems, including kelp
forests, coral reefs, mangroves, oyster reefs, and
sea grass beds (Short and Wyllie-­Echeverria 1996,
Kimbro and Grosholz 2006, Wilson et al. 2006,
Hoegh-­Guldberg et al. 2007, Reed et al. 2011, Guo
et al. 2013, Pickett and White 1985). Disturbance
can strongly affect primary production (Reed
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Li and Pennings
In coastal salt marshes, a variety of disturbances affect plant and animal communities
and ecosystem function (Valiela and Rietsma
1995, Silliman et al. 2005, McFarlin et al. 2015,
Reidenbaugh and Banta 2015). Common disturbances in salt marshes around the world
include deposition of floating wrack (Bertness
and Ellison 1987, Tolley and Christian 1999), ice
damage (Pennings and Bertness 2001), creekbank slumping (Pethick 1974), fire (Smith and
Kadlec 1985, Smith et al. 2013), and herbivory
or excavation by wildlife (Ellison 1987, Pennings
et al. 2009). By killing vegetation, providing
nutrients, and altering abiotic conditions, these
disturbances affect species composition and succession (Bertness and Ellison 1987, Bertness et al.
1992), and primary production (Pennings and
Richards 1998). Many of these studies emphasize higher marsh elevations that have higher
plant species richness. In addition, with a few
exceptions (Valiela and Rietsma 1995, Brewer
et al. 1998, Fischer et al. 2000), these studies were
conducted at single sites over one or two years.
Finally, few of these studies compared disturbance with other factors that might affect plant
productivity. Thus, despite considerable interest
in disturbance in coastal salt marshes, we lack an
understanding of how frequent disturbance is
across all marsh elevations, how it varies among
sites and over time, and what types of disturbance and abiotic variables (elevations, physical
locations, and climate) are most important in
affecting plant productivity. As a consequence,
we also do not know whether the interest in disturbance in coastal salt marshes reflects its ecological importance in this habitat compared to
other systems.
To address these issues, we examined disturbance to permanent plots over 14 years at eight
salt marshes in coastal Georgia, USA, that were
dominated by the grass Spartina alterniflora. We
tested the hypotheses that (1) the type and frequency of disturbance would vary among sites,
marsh zones, and years; (2) the frequency of
disturbance would vary as a function of abiotic
conditions including climate and sea level; (3)
different types of disturbance would have different effects on standing biomass in affected plots;
and (4) disturbance would be similar in importance to local climate and abiotic drivers in affecting variation in plant productivity.
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Fig. 1. Map of the study site. GCE-­LTER perma­
nent monitoring sites that were included in this study
are marked with filled circles. GCE 3 and 6 were coded
as barrier island sites; 2, 5, 9, and 10 as intermediate;
and 1 and 4 as mainland sites.
Methods
Our study area was within the domain of the
Georgia Coastal Ecosystems Long-­Term Eco­
logical Research (GCE-­LTER) program (http://
gce-lter.marsci.uga.edu/). The GCE-­LTER program includes 10 permanent sites (GCE1–10) that
inc­lude fresh, brackish, and salt marshes that are
dominated by the plant species Zizaniopsis miliacea, Spartina cynosuroides and Juncus roemerianus,
and Spartina alterniflora, respectively. Tides are
semidiurnal and mesotidal, with a range of
2–3 m. We focused on the eight sites where the
creekbank or marsh platform was dominated by
S. alterniflora (creekbank zones at GCE sites 1,
2–6, and 9–10; mid-­marsh zones at GCE sites 2–6
and 9–10, Fig. 1; Appendix S1: Fig. S1). At each
site, we located eight plots at the creekbank and
eight in the mid-­marsh. S. alterniflora height varies with elevation, and ecologists often distinguish “tall Spartina” (typically at the creekbank,
>100 cm tall), “medium Spartina” (50–99 cm tall),
and “short Spartina” (<50 cm tall) (Schalles et al.
2013). Using these criteria, mid-­marsh plots at
sites 2–4 would probably be categorized as short
Spartina, mid-­marsh plots at sites 5, 6, 9, and 10
would be categorized as medium Spartina, and
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Li and Pennings
creekbank plots at all the sites would be categorized as tall Spartina. Elevations of plots varied
among sites, but with considerable overlap
between sites due to variation among plots
within each site (Appendix S1: Table S5). We
elected not to include the various different types
of high marsh vegetation present at these sites in
our sampling design so as to maximize our ability to compare disturbance to a single dominant
vegetation type across as many sites as possible.
We measured shoot heights and flowering status
of S. alterniflora every October from 2000 to 2014
and used allometric relationships (Appendix S1:
Table S1) to estimate standing biomass (Więski
and Pennings 2013). Since 2000 was the first year
of the project, all plots were initially undisturbed,
so disturbances were recorded from 2001 to 2014.
Each year when standing biomass was estimated in the plots, we also recorded disturbances due to wrack (floating debris, usually
consisting of the stems of dead plants), creekbank slumping (the collapse of the creekbank
toward the bottom of the creek), or aggregations
of snails in each plot. The decision to mark a
plot as disturbed was based on clear evidence
of the purported disturbance agent. For example, we recorded plots as disturbed by wrack if
we found abundant wrack in the plot or broken
plant stems indicative of plants having been
crushed by wrack. We recorded plots as slumping (initial slump) based on crevices in the marsh
or displaced plot stakes indicating that the plot
was sliding into the creek. We also recorded
plots as slumping (terminal slump) if the plot
stakes had slipped beyond the lower distribution limit of intertidal vegetation (in these cases,
we scored standing biomass as zero and established a replacement plot at higher elevations in
the same general location). Finally, we recorded
plots as disturbed by snails if we observed high
densities of snails in the plot (>~250/m2) coupled
with visual observation of snail grazing damage
to plants (Silliman and Zieman 2001, Schalles
et al. 2013). Thus, we did not score plots as disturbed if the plots contained small amounts of
wrack or normal densities of snails without evidence of damage to vegetation, and we might
have missed disturbances that happened earlier in the growing season if plants had mostly
recovered and the evidence of the disturbance
had disappeared.
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We qualitatively compared the frequency of
different types of disturbance among years, sites,
and marsh zones from 2001 to 2014. To determine how disturbance affected the fall standing
biomass of S. alterniflora, we compared biomass
of plots experiencing the more common types
of disturbances at the creekbank (wrack disturbance, initial slump, terminal slump, both wrack
disturbance and initial slump, and no disturbance) and in the mid-­marsh (wrack disturbance,
snail disturbance, and no disturbance) using one-­
way analysis of variance (ANOVA) with all years
combined. Data were ln(x + 1)-­transformed before
analysis to improve homogeneity of variance.
We collected data on six factors that might
affect disturbance and plant biomass (site, elevation of each plot, temperature, precipitation,
sea level, and river discharge) from GCE-­LTER
data sets or public sources. We used maximum
temperature instead of mean temperature as a
predictor because maximum temperature was
previously shown to be a better predictor of plant
biomass (Więski and Pennings 2013). Site locations, elevation of each plot, temperature, precipitation, and river discharge are accessible on the
GCE-­LTER Web site (http://gce-lter.marsci.uga.
edu/portal/monitoring.htm). Sea level is available on the Web site of National Oceanographic
and Atmospheric Administration (8670870 Fort
Pulaski, Georgia, http://www.noaa.gov/). Data
sources are described more fully in Appendix S1:
Tables S2–S5. Predictors that varied during each
year (river discharge, sea level, precipitation, and
maximum temperature) were averaged over the
growing season (April–September) to provide
a single value per year. We addressed the contributions of abiotic (landscape location, plot
elevation) or climate factors (sea level and river
discharge) in predicting disturbance frequency
using stepwise logistic regression. We started
with a full model and sequentially removed
terms with P > 0.25 at each step.
We examined the importance of the six environmental factors in combination with disturbance type (wrack disturbance, snail disturbance,
initial slump, and terminal slump) on plant biomass using analyses of covariance (ANCOVAs)
for the creekbank and mid-­marsh zones separately. Plots (8 zone−1 year−1 site−1) were used
as the unit of replication. In the creekbank zone
(n = 1015), we modeled S. alterniflora biomass
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Li and Pennings
Fig. 2. (A) Variation in Spartina alterniflora fall standing biomass, all sites combined. (B–H) Frequency of
different disturbances in creekbank and mid-­marsh zones.
Results
as the dependent variable, with wrack disturbance, initial slump, terminal slump, and site as
fixed factors, and plot elevation, river discharge,
sea level, precipitation, and maximum monthly
temperature as covariates (no creekbank plots
were disturbed by snails). In the mid-­marsh zone
(n = 837), we modeled S. alterniflora biomass as
the dependent variable, with snail disturbance
and site as fixed factors (mid-­marsh plots did
not experience slumping disturbance, and wrack
disturbance was rare, n = 6), and plot elevation,
river discharge, sea level, precipitation, and maximum temperature as covariates. Plot elevation
and sea level were removed from the mid-­marsh
model because they were not significant (Abdala-­
Roberts and Mooney 2014). All statistical analyses
were performed in SPSS 22 (Allen et al. 2014).
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Standing biomass of Spartina alterniflora was
~2.6 times higher in the creekbank vs. the mid-­
marsh zone (Fig. 2A). Standing biomass varied
~threefold among years in the creekbank zone
and ~twofold among years in the mid-­marsh
zone.
Across all years and disturbance types, the frequency of disturbance was ~eight times higher in
the creekbank zone than in the mid-­marsh zone
(Fig. 2B). Disturbance varied ~fivefold among
years in the creekbank zone and ~11-­fold among
years in the mid-­marsh zone.
The frequency of different types of disturbance
varied between zones, among sites, and among
years. The most common disturbances in the
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Li and Pennings
creekbank were wrack, which affected about
15% of plots, and slumping, which affected about
16% of plots, with initial slumping and terminal
slumping equally common (Fig. 2C). The most
common disturbance in the mid-­marsh was
snails, which affected about 4% of the plots overall (Fig. 2D). The four disturbance types varied
in different ways among sites (Fig. 2C, D) and
years, with wrack and snail disturbance most
important early in the study period, and terminal slumping most important late in the study
period (Fig. 2E–H).
Wrack disturbance at the creekbank was more
common at barrier island sites than at sites further inland (Fig. 3A) and was also affected positively by plot elevation, negatively by river
discharge, and negatively by sea level (Table 1;
Appendix S1: Fig. S2A–C). Initial slumping at
the creekbank was affected negatively by plot
elevation and negatively by sea level (Table 1;
Appendix S1: Fig. S2D, E). Terminal slumping
at the creekbank was affected negatively by plot
elevation (Table 1; Appendix S1: Fig. S2F). Snail
disturbance in the mid-­marsh was more common
at barrier island sites than at sites further inland
(Fig. 3B) and was negatively affected by plot elevation (Table 1; Appendix S1: Fig. S2G).
Spartina alterniflora biomass was reduced by
~46% in creekbank plots experiencing wrack
disturbance compared to undisturbed plots
(Fig. 4A). Initial slumping had no effect on biomass, but terminal slumping resulted in total
biomass loss. In the mid-­marsh zone, wrack disturbance did not affect standing biomass, but
snail disturbance reduced biomass by ~70% in
affected plots (Fig. 4B).
We multiplied the frequency of disturbance
by its effect on standing biomass in affected
plots to calculate the total effect of disturbance
on S. alterniflora biomass at the landscape
level (Table 2). Depending on the site, wrack
Fig. 3. (A) Variation of wrack disturbance
frequency among different landscape locations at the
creekbank zone and (B) variation of snail disturbance
frequency among different landscape locations at the
mid-­marsh zone.
disturbance reduced biomass in the creekbank
zone by 3–15%, loss of creekbank plots due to
terminal slump reduced biomass by 2–16%, and
snails reduced biomass in the mid-­marsh zone
by 1–7%. On average, across all sites, years, and
types of disturbance, disturbance reduced biomass by ~18% in the creekbank zone and ~3% in
the mid-­marsh zone.
Both disturbance and abiotic drivers helped
explain variation in S. alterniflora biomass.
Creekbank biomass was negatively affected by
wrack disturbance, terminal slumping, maximum
Table 1. Logistic regression relationships between disturbances and abiotic drivers.
Creekbank
Mid-­marsh
Abiotic driver
Wrack
Initial slump
Terminal slump
Snails
Plot elevation
River discharge
Sea level
Landscape location
0.546 (P < 0.05)
−0.004 (P < 0.0001)
−6.303 (P < 0.01)
0.462 (P < 0.01)
−0.733 (P < 0.05)
−1.207 (P < 0.001)
−5.994 (P < 0.01)
−7.611 (P < 0.01)
1.691 (P < 0.001)
Note: Values are regression coefficients and P-values; only significant predictors are shown.
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Li and Pennings
among marsh zones, sites, and years. Overall,
plant biomass in these salt marshes was more
strongly affected by abiotic drivers than by disturbance, in contrast to some other ecological systems where productivity is strongly dependent
on disturbance (Reed et al. 2011).
Disturbance was more common at the creekbank than in the mid-­marsh. Many previous
studies of salt marsh disturbance have focused on
the importance of wrack disturbance in the high
marsh, where floating wrack can be deposited by
spring tides, remain in place for weeks, and affect
vegetation composition (Bertness et al. 1992). Both
Bertness and Ellison (1987), working in Rhode
Island, and Valiela and Rietsma (1995), working
in Massachusetts, found wrack disturbance to be
greatest in the high marsh. Both studies, moreover,
concluded that wrack disturbance in the low marsh
did not strongly affect plant community composition because wrack was relatively rare, wrack
patches were regularly moved by high tides, and
plant species richness was low. Although uninteresting from a community ecology point of view,
creekbank disturbance by wrack may nevertheless strongly affect plant biomass. We found much
higher rates of wrack disturbance at the creekbank
than in the mid-­marsh. Creekbank plots often had
Fig. 4. Biomass of Spartina alterniflora plots experi­ modest rather than heavy mats of wrack at the
encing different disturbances in creekbank and mid-­ time that we sampled the plots, suggesting that
marsh zones (all years and sites combined). Data are the heavy mat of wrack that initially disturbed
means ± 1 SE (n = 149, 51, 74, 14, and 727 for wrack the plot had since been largely transported elsedisturbance, initial slump, terminal slump, wrack + where, consistent with the view of past workers
initial slump, and no disturbance plots, respectively, in that wrack in the low marsh is relatively transient.
the creekbank zone, and n = 6, 29, and 802 for wrack Nevertheless, the tall stems of S. alterniflora along
disturbance, snail disturbance, and no disturbance the creekbank are vulnerable to breaking when
plots, respectively, in the mid-­marsh). Bars not shar­ crushed by mats of wrack, even if the wrack mat
ing a letter are significantly different from one another persists in a given location for only a single low
(P < 0.05).
tide. Thus, even if wrack does not persist long at
any single location along the creekbank and does
monthly temperature, and plot elevation and not affect species composition, it may nevertheless
positively affected by river discharge, sea level, have strong effects on standing biomass and proand precipitation (Table 3). Plant biomass in the ductivity. Moreover, if wrack mats at the creekmid-­marsh zone was negatively correlated with bank move around frequently, the cumulative
snail disturbance and maximum monthly tem- disturbance to the creekbank zone may be much
perature and positively correlated with local pre- greater than that suggested by a snapshot survey
cipitation and river discharge (Table 3).
of wrack abundance at any one time.
Other disturbance types also varied with
Discussion
marsh zone. Because the mid-­marsh is almost
flat, slumping did not occur in the mid-­marsh
We found that type, frequency, and importance zone. In contrast, snail disturbance was only
of disturbance varied strongly and predictably observed in the mid-­marsh, because predators
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Table 2. Effects of wrack, initial slump, terminal slump, and snail disturbances on standing biomass of
Spartina ­alterniflora in creekbank and mid-­marsh zones, respectively.
Creekbank
Mid-­marsh
Site
Wrack
Initial slump
Terminal slump
Total
Snails
Site 1
Site 2
Site 3
Site 4
Site 5
Site 6
Site 9
Site 10
8.66
6.60
14.85
3.30
6.60
9.08
8.66
10.73
2.43
2.43
0.30
0.76
0.91
1.67
1.67
0.30
11.61
16.07
2.68
6.25
2.68
12.50
12.50
1.79
22.70
25.10
17.83
10.31
10.19
23.25
22.83
12.82
ND
0.00
7.49
3.74
0.00
5.62
0.00
1.25
Notes: Data are percentage reductions in biomass at each zone at each site by the various disturbances. Only results for statistically significant disturbances are shown. ND = no data because this zone at site 1 is not dominated by S. alterniflora.
varying ~12-­fold, initial slumping varying ~eightfold, terminal slumping varying ~18-­fold, and
snail disturbance varying ~sixfold among sites.
Variation among sites is probably largely due
to differences in plot elevation and to landscape
position. Wrack disturbance at the creekbank
was positively correlated with plot elevation,
probably because wrack was more likely to be
stranded in plots that were higher in the intertidal frame. Both initial slumping and terminal slumping at the creekbank were negatively
correlated with plot elevation, perhaps simply
reflecting the fact that lower elevation plots are
the closest to the creeks. Finally, snail disturbance
in the mid-­marsh was negatively correlated with
plot elevation; however, this correlation had a
very poor fit and was highly influenced by a relatively small number of plots at three or four sites
(Fig. S2G), and we therefore do not place a high
level of confidence in this result.
typically limit snails at the creekbank to densities below those at which snails harm vegetation
(Silliman and Bertness 2002).
Disturbance also varied among sites and across
the landscape. We know little about how disturbance varies among salt marsh sites, because
most previous studies focused only on one or a
few sites. Brewer et al. (1998) found variation in
disturbance among three salt marshes in Rhode
Island, but did not study enough sites to generalize their results. Fischer et al. (2000) studied
spatial variation in wrack disturbance in salt
marshes at Sapelo Island and found that it was
highly dependent on small-­scale aspects of creekbank morphology. Our plots were located along
relatively straight sections of creeks and did not
include sufficient variation in creekbank morphology to assess its importance. However, we
found considerable variation among sites in all
four disturbance types, with wrack disturbance
Table 3. ANCOVA table estimating effects of different disturbance and climate drivers on plant biomass in the
creekbank and mid-­marsh plots (n = 1015 and 837, respectively).
Creekbank (adjusted R2 = 0.47)
Source
Site
Wrack
Initial slump
Terminal slump
Plot elevation
Discharge
Max temp
Sea level
Precipitation
Mid-­marsh (adjusted R2 = 0.24)
F
P
Sign
35.30
50.08
12.32
302.35
11.22
42.59
42.56
8.54
12.81
<0.001
<0.001
<0.001
<0.001
0.001
<0.001
<0.001
0.004
<0.001
−
−
−
−
+
−
+
+
Source
F
P
Sign
Site
Snails
Discharge
Max Temp
Precipitation
23.66
34.01
11.82
16.74
5.64
<0.001
<0.001
0.001
<0.001
0.018
−
+
−
+
Note: Variables that were not significant were removed from the models.
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Wrack and snail disturbance also varied predictably across the landscape. Wrack disturbance was most common on barrier island sites,
likely because the net transport of wrack by
river flow is offshore. Snail disturbance was also
more common on barrier island sites than mainland marshes, likely because of increased larval
recruitment at sites closer to the ocean (B. R.
Silliman, personal communication). The overall
frequency of significant Littoraria irrorata snail
disturbance that we observed is consistent with
the study of Schalles et al. (2013), who estimated
that 4.5% of the marsh (all vegetation types on
the creek-­shed on the west side of Sapelo Island)
had snail densities >250/m2, but is lower than
one might expect from studies of the impact
that L. irrorata has on marsh vegetation in South
Atlantic salt marshes, which often report average snail densities of >300/m2 (Silliman and
Bertness 2002, Silliman and Bortolus 2003). It is
likely that this discrepancy is largely explained
by these studies working with L. irrorata where
it is most abundant in the short Spartina zone at
the upper reaches of the intertidal range dominated by S. alterniflora. In contrast, the majority of the mid-­marsh plots in this study were
located in medium Spartina, where snails are
considerably less abundant (77 vs. 237/m2 in
short Spartina, Schalles et al. 2013).
Finally, disturbance varied up to 14-­fold among
years, and different types of disturbance varied
out of synchrony with each other. Most previous
studies of disturbance in salt marshes have sampled over only one or a few years and therefore
are likely to poorly estimate the true frequency of
disturbance. Wrack disturbance at the creekbank
was negatively correlated with river discharge,
perhaps because wrack is transplanted offshore
during periods of high river discharge. Wrack
disturbance at the creekbank was also negatively
correlated with sea level, likely for the same
reason that it was positively correlated with
plot elevation. Both of these variables address
how deeply the marsh is flooded, with flooding greater in years of high sea level or at plots
located at low elevation. In both cases, wrack is
more likely to be transported over the creekbank
plots and into the remainder of the marsh or to be
exported from the marsh and out to sea.
Initial slumping of creekbanks was negatively
correlated with sea level, perhaps because periods
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of low sea level lead to increased pore water
drainage, and dewatered soils have a lower shear
strength (Gallage and Uchimura 2006). Terminal
slumping, however, was not correlated with sea
level. It is likely that terminal slumping, which
indicates that the slumping plot has reached elevations below which S. alterniflora can survive,
is a function of multiple additional variables,
such as creekbank steepness and wave exposure,
which were not measured in this study.
One caveat of our study is that we only scored
disturbances that were obvious in October when
we sampled the plots. Thus, we would have
missed disturbances that occurred early in the
growing season if the vegetation was largely
recovered, and we would have ignored small
disturbances that had only weak effects on the
vegetation. As our interest, however, was how
disturbance affected end-­of-­year standing biomass, neither of these would have had a large
effect on our results.
How important are disturbances vs. abiotic
factors in controlling end-­of-­year biomass of
salt marsh plants? Several previous studies have
examined the importance of abiotic factors in
mediating the productivity of salt marsh plants
(Morris et al. 1990, Więski and Pennings 2013). In
addition, several studies have looked at the effect
of disturbances on plant productivity at the plot
scale (Tolley and Christian 1999, Reidenbaugh
and Banta 2015). For example, Silliman and
Zieman (2001) found that snail grazing reduced
Spartina biomass by 51–66% (similar to our estimate of 70%). None of these previous studies
of disturbance in salt marshes, however, took a
landscape-­scale perspective, making it difficult
to scale their results up. And none of these past
studies integrated the importance of abiotic factors and disturbance.
We estimated the effect of disturbance at the
landscape scale by multiplying the frequency
of disturbance at each site with its overall effect
on standing biomass. This calculation suggested
that disturbance was of moderate importance
in mediating standing biomass at the landscape scale. On average, fewer than a quarter
of the plots were disturbed, and only some
disturbances (wrack and terminal slumping
at the creekbank and snails in the mid-­marsh)
strongly reduced standing biomass. The total
effect of disturbance was to reduce standing
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Li and Pennings
biomass by ~18% at the creekbank and ~3% in
the mid-­marsh. Although this is an important
effect, abiotic factors such as maximum temperature, river discharge, and sea level produce
much greater variation in end-­of-­year standing
biomass from year to year (Morris et al. 1990,
Więski and Pennings 2013). High temperatures
in salt marshes may reduce productivity if they
are beyond the thermal optimum for photosynthesis of Spartina (Giurgevich and Dunn 1982,
Więski and Pennings 2013). River discharge
and sea level affect productivity because they
mediate salinity of the pore water surrounding
the plant roots (Morris et al. 1990, Więski and
Pennings 2013). In comparison, disturbance is
not common enough across the landscape to
strongly affect standing biomass. Recovery of
S. alterniflora from disturbance depends on disturbance size, abiotic conditions, and top-­down
pressure (Angelini and Silliman 2012, Silliman
et al. 2013), all of which likely vary among sites
and years. Thus, not only disturbance but also
recovery is likely to be spatially and temporally
variable.
We are aware of few studies in other systems
that have explicitly contrasted the effects of abiotic factors and disturbance on primary production. One notable exception is a study of giant
kelp in California, where disturbance (storm
waves) overwhelmed bottom-­up (nutrient
availability) and top-­down (grazing pressure)
factors in determining net primary production
(Reed et al. 2011). Our study compared effects
of abiotic factors and disturbance on end-­of-­
year biomass, but did not explicitly consider
the role of consumers other than snails. A variety of herbivorous insects and crabs also affect
S. alterniflora biomass in southeastern Atlantic
salt marshes (Pennings et al. 2012) and so the
next step in understanding S. alterniflora productivity would be to integrate the effects of
these consumers.
In summary, our results indicate that disturbance in coastal salt marshes dominated by
S. alterniflora varies among marsh zones, plots,
sites, and years. Previous studies that have
focused on one or another type of disturbance,
often over a limited range of marsh elevations,
sites, or years, have been important in understanding the mechanisms by which disturbance
affects marsh structure and function. Our work
v www.esajournals.org
has begun to place these previous studies in a
broader context and has shown that while disturbance can be locally important in affecting
marsh productivity, abiotic drivers have a stronger effect on standing plant biomass across the
entire landscape.
Acknowledgments
This research was funded by the National Science
Foundation (OCE99-­82133, OCE06-­20959, OCE12-­
37140). Shanze Li was able to participate thanks to the
National Key Basic Research Program of China
(2013CB430406) and the China Scholarship Council.
We thank everyone who helped sample the permanent
plots over the years and thank Merryl Alber, Brian
Silliman, and Kazimerz Więski for helpful comments
on the manuscript. This work is a contribution of the
Georgia Coastal Ecosystems LTER program and contribution number 1051 of the University of Georgia
Marine Institute.
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Supporting Information
Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/
ecs2.1487/supinfo
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