Aquatic Botany 104 (2013) 70–79
Contents lists available at SciVerse ScienceDirect
Aquatic Botany
journal homepage: www.elsevier.com/locate/aquabot
Changing eelgrass (Zostera marina L.) characteristics in a highly eutrophic
temperate coastal lagoon
Benjamin Fertig a,∗ , Michael J. Kennish a , Gregg P. Sakowicz b
a
b
Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901, USA
Rutgers University Marine Field Station, 800 Great Bay Boulevard, Tuckerton, NJ 08087, USA
a r t i c l e
i n f o
Article history:
Received 1 March 2011
Received in revised form 30 August 2012
Accepted 7 September 2012
Available online 21 September 2012
Keywords:
Seagrass decline
Zostera marina
Plant characteristics
Biotic indicators
Eutrophication
Barnegat Bay-Little Egg Harbor Estuary
a b s t r a c t
Previous investigations of eelgrass (Zostera marina L.) beds in the Barnegat Bay-Little Egg Harbor Estuary,
New Jersey (USA) revealed a significant decline in plant biomass associated with ongoing nitrogen enrichment of the system and declines in light availability. Here, we update trends in eelgrass characteristics
(aboveground and belowground biomass, shoot density, percent cover, blade length) for 2008–2010 and
compare these to previous datasets (2004–2006). Analysis of quadrat, core, and hand samples collected
at 120 transect stations in 4 disjunct eelgrass beds of the estuary showed a distinct, continued reduction
in Zostera biomass. In 2010, Z. marina biomass decreased to its lowest level ever recorded in the estuary (mean aboveground biomass = 7.7 g DW m−2 ; mean belowground biomass = 27.0 g DW m−2 ). Reduced
biomass and other characteristics indicated that eelgrass beds had not recovered from previous reductions observed 2004–2006. The rate of decline was related to nutrient loading and associated symptoms
of eutrophication. Additionally, the rate of degradation changed over time. The decline in plant parameters was evident in all of the eelgrass beds investigated, indicating that an estuary-wide stressor was
responsible.
© 2012 Elsevier B.V. All rights reserved.
1. Introduction
Eelgrass meadows have been declining in many estuaries
around the world as human population growth and development
increased in coastal watersheds (Orth et al., 2006; Short et al., 2006;
Duarte et al., 2009; Waycott et al., 2009). Nutrient and sediment
loading from the watersheds, together with habitat loss and alteration in the estuarine water bodies themselves, have significantly
impacted eelgrass subsystems (Larkum et al., 2006; Ralph et al.,
2006). Implications of degraded eelgrass areal cover include elimination of habitat for bay scallops (Argopecten irradians), hard clams
(Mercenaria mercenaria), and other species, and can be linked to
changes in ecosystem structure and function driven by bottom-up
effects.
Nitrogen over-enrichment is thought to cause significant disruption of ecosystem structure and function (Nixon, 1995; Nixon
et al., 2001; Kennish et al., 2007a) including promotion of nuisance
and toxic algal blooms (phytoplankton and macroalgae), seagrass
epiphytes, all of which reduce light availability (McGlathery et al.,
2007; Paerl et al., 2003, 2009). Light reductions have been linked
with lower shoot densities and biomass, reduced depth penetration, slower growth rates, stunted morphology, and higher
∗ Corresponding author. Tel.: +1 301 785 7614; fax: +1 732 932 8578.
E-mail address: [email protected] (B. Fertig).
0304-3770/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquabot.2012.09.004
mortalities (Lee et al., 2007; Ralph et al., 2007; Ochieng et al., 2010;
Olesen, 1996; Olesen and Sand Jensen, 1993).
Long-term symptoms of eutrophication in Barnegat Bay-Little
Egg Harbor Estuary include low dissolved oxygen (in the central
and northern segments), harmful algal blooms, declining eelgrass
populations, heavy epiphyte loading, macroalgae blooms, loss of
essential habitat (eelgrass and shellfish beds), and depleted harvestable bay scallop (A. irradians) and hard clam (M. mercenaria)
fisheries (Kennish et al., 2007b, 2008a, 2011). Indeed, there is a
significant positive relationship between water column total nitrogen concentration and total nitrogen loading by subwatershed
(Kennish and Fertig, 2012). There is growing concern that escalating
eutrophication will result in severe, long-term degradation of eelgrass populations (Duarte et al., 2009; Kennish et al., 2007a, 2010).
Bologna et al. (2000) documented significant losses of eelgrass in
the estuary from the mid-1970s to 2000, which may have reduced
the areal distribution of the beds by 30–60%, most significantly in
Little Egg Harbor.
If symptoms of eutrophication are indeed affecting eelgrass
populations in Barnegat Bay-Little Egg Harbor Estuary, then
changes in eelgrass characteristics should be observed over time,
potentially at different rates as ecological or physiological stress
changes. The objective of this study was to identify if (and if so,
how) seagrass condition in Barnegat Bay-Little Egg Harbor Estuary
responded over time to symptoms of eutrophication. This study
updates previously reported trends (Kennish, 2001a,b; Kennish
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
71
Unlike river dominated estuaries and coastal waters that drain
large, inter-jurisdictional watersheds (e.g. Billen and Garnier, 2007;
Howarth et al., 2011; Kemp et al., 2005; Radach and Patsch,
2007; Rabalais, 2002; Seitzinger et al., 2010), the small watershed
(1730 km2 ) of Barnegat Bay-Little Egg Harbor coastal lagoon estuary lies entirely in one state (New Jersey) and mainly receives
non-point nutrients (e.g. residential fertilizers) via both overland
and groundwater (Kennish, 2001a; Kennish and Townsend, 2007).
Point sources (wastewater treatment plants) from the watershed
discharge to the Atlantic Ocean (Kennish, 2001b).
Eelgrass beds form an essential habitat in the estuary and are an
important indicator of water and sediment quality conditions. Seagrass in Barnegat Bay-Little Egg Harbor Estuary consists of mixed
beds of eelgrass (Zostera marina L.) and widgeon grass (Ruppia maritima). Eelgrass comprises more than 95% of the seagrass habitat,
and it overwhelmingly predominates in the southern and central segments of the estuary from Tuckerton Creek to Toms River
(Kennish et al., 2010). Widgeon grass dominates the beds in the
northern segment of the estuary (Toms River to Metedeconk River),
which is characterized by lower salinities.
2.2. Sampling design
Fig. 1. Study area exhibiting 120 seagrass sampling stations along 12 transects in
the Barnegat Bay-Little Egg Harbor Estuary. Inset shows the location of the estuary
with respect to the State of New Jersey.
From Kennish et al. (2010).
et al., 2007a, 2008a, 2010, 2011, 2012) by comparing eelgrass characteristics in 2008–2010 vs. 2004–2006 with respect to increasing
eutrophication. Specifically, we investigated eelgrass biomass
(aboveground and belowground), shoot density, areal cover, and
blade length across the estuary as affected by nutrient loading.
2. Materials and methods
2.1. Study area
Barnegat Bay-Little Egg Harbor, located along the central New
Jersey coastline (USA), is a highly eutrophic coastal lagoon (Kennish,
2007a,b, 2009; Kennish et al., 2007a,b). Barnegat Bay and Little
Egg Harbor are back-bay basins that form an irregular contiguous
lagoonal system ∼70 km long, 2–6 km wide, and mean 1.5 m deep
(Fig. 1). Together they have a net surface area of 280 km2 and a volume of 3.54 × 108 m3 (Kennish, 2001a,b). The adjoining Barnegat
Bay watershed covers an area of 1730 km2 . A total of ∼575,000
people now inhabit the surrounding watershed year-round, with
highest densities in the northern region. Similar to many coastal
lagoons in the mid-Atlantic region, the Barnegat Bay-Little Egg
Harbor Estuary is affected by a burgeoning human population in
adjoining coastal watershed areas (Kennish, 2009). The population
expands to 1.2 million people during the summer tourist season
when nutrient enrichment also peaks. With population growth
in the watershed expected to increase from the current number
of ∼575,000 year-round residents (>1.2 million people during the
summer tourist season) to ∼850,000 people projected at buildout
(∼50% increase in year-round residents), anthropogenic pressures
will continue to mount, including impervious cover and other land
surface alteration in the watershed, which will also partition habitats, leading to a greater input of nutrients and other pollutants to
the estuary. A north-to-south gradient of decreasing human population density and development occurs in the watershed, as does
a north-to-south gradient of decreasing nutrient loading in the
estuary (Hunchak-Kariouk and Nicholson, 2001; Seitzinger et al.,
2001; Wieben and Baker, 2009).
Quadrat, core, and hand sampling was conducted over the June
to November period in 2008–2010 targeting the same eelgrass beds
and transects sampled in Barnegat Bay (∼1550 ha) and Little Egg
Harbor (∼1700 ha) during the 2004–2006 period (Kennish et al.,
2008a,b, 2010). Specifically, sampling during 2004–2010 was conducted along 12 transects in four disjunct eelgrass beds, and each
transect consisted of 10 sampling stations (Fig. 1). Each station was
permanently located with a Differential Global Positioning System
(Trimble® GeoXTTM handheld unit). Note that transects 1–6 were
sampled in 2004, transects 7–12 were sampled in 2005, and transects 1–12 were sampled in 2006 and 2008–2010. Sampling efforts
were based on the SeagrassNet monitoring and sampling protocols
of Short et al. (2002). The main modification of methods was establishing transects perpendicular to shore rather than parallel, to
identify differences along a clearly defined depth gradient. Eelgrass
samples were collected during each of 3 time periods (June–July,
August–September, and October–November) in all years. The following eelgrass characteristics were recorded on all sampling dates
at each sampling station: aboveground and belowground biomass,
shoot density, blade length, and areal cover.
2.3. Quadrat sampling
Based on the field sampling methods of Short et al. (2002), a
0.25-m2 metal quadrat was haphazardly tossed at the sampling
stations to obtain measurements of eelgrass and macroalgae areal
cover. A diver estimated the percentage of the quadrat covered by
eelgrass and macroalgae in increments of 5 along a scale of 0–100.
For macroalgae, areal cover of 60–70% was considered ‘Pre-Bloom’,
70–80% was considered ‘Early Bloom’, and >80% was considered
‘Full Bloom’ conditions, according to methods of Kennish et al.
(2011). The diver then visually inspected the eelgrass bed within
the quadrat for occurrence of grazing, boat scarring, macroalgae,
epiphytic loading, wasting disease, bay scallops, and hard clams.
Each sampling station was also imaged using a digital camera to
validate the diver observations. Subsequently, 5 replicate eelgrass
blades were collected from within the quadrat, and blade lengths
were measured.
2.4. Core sampling
Coring methods also followed those of Short et al. (2002)
using a 10-cm diameter PVC coring device to collect the eelgrass
72
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
samples within the quadrat, with care taken not to cut or damage
the aboveground plant tissues. The diver-deployed corer extended
deep enough in the sediments to extract all belowground fractions
(roots and rhizomes). Each core was placed in a 3-mm × 5-mm
mesh bag and rinsed to separate plant material from the sediment.
After removing the eelgrass from the mesh bag, the sample was
placed in a labeled bag and stored on ice in a closed container prior
to transport to the Rutgers University Marine Field Station (RUMFS)
in Tuckerton for laboratory analysis.
2.5. Laboratory analysis
In the laboratory, the eelgrass samples were carefully sorted and
separated into aboveground (shoots) and belowground (roots and
rhizomes) components. The density of eelgrass shoots was then
determined. The aboveground and belowground fractions were
subsequently oven dried at 50–60 ◦ C for a minimum of 48 h. The dry
weight biomass (g DW m−2 ) of each fraction was then measured to
the third decimal place.
2.6. Physical and chemical measurements
Physical and chemical measurements made in Barnegat BayLittle Egg Harbor Estuary during 2004–2010 were compared to eelgrass characteristics to quantify changes in eelgrass characteristics
in relation to changes in water quality condition (e.g. eutrophication). Water temperature, salinity, dissolved oxygen, pH, and depth
were recorded each sampling time (June/July, August/September,
and October/November of 2004–2006, 2008–2010) at each station
prior to biotic sampling at each station. These data were collected at a uniform depth (∼10 cm) above the sediment–water
interface using either a handheld YSI 600 XL datasonde coupled
with a handheld YSI 650 MDS display unit, an automated YSI
6600 unit (equipped with a turbidity probe), or a YSI 600 XLM
automated datalogger. Secchi depth was subsequently recorded.
Water samples (N = 72) were also collected at all 12 transects in
2008 to determine nutrient concentrations. Laboratory analysis
of the nutrients followed standard methods, with samples analyzed using a Lachat QuikChem FIA+ ® autoanalyzer. Additional
physical and chemical measurements in Barnegat Bay-Little Egg
Harbor Estuary (61 stations throughout the estuary) were extracted
from long-term (1989–2011) quarterly water quality monitoring data available from the U.S. Environmental Protection Agency
(http://www.epa.gov/storet/dbtop.html).
2.7. Statistical analysis
Temporal and spatial changes were tested across all 120 stations
with three-way ANOVA (transects, years, and sampling periods
were class variables) for each water quality metric (salinity, temperature, dissolved oxygen concentration, and pH) and eelgrass
characteristic (aboveground biomass, belowground biomass, shoot
density, blade length, and areal cover by Zostera). Unless otherwise noted, the cutoff for statistical significance was p < 0.05.
Effects of physical and chemical variables on Z. marina characteristics were determined with multivariate analysis (MANOVA, Proc
GLM, SAS Inc.) to test (1) overall effects, (2) differences between
transects, and (3) differences between Little Egg Harbor (transects
1–6) and Barnegat Bay (transects 7–12). A principal component
analysis was conducted on the multivariate regression predicted
values through redundancy analysis (Proc Transreg, tstandard=z,
method=redundancy, SAS Inc.) with the physical and chemical
variables as independent variables and Z. marina characteristics
as dependent variables to test for covariance and collinearity
between physical/chemical variables and Z. marina characteristics. Coefficients for predicting independent variables from the
Table 1
Mean (standard deviation) water temperature, salinity, dissolved oxygen, pH, and
Secchi depth at survey stations in Barnegat Bay-Little Egg Harbor Estuary during
sampling periods in 2008, 2009, and 2010.
Parameter
Sampling period
June–July
August–September
October–November
Temperature ( C)
2008
23.4 (3.6)
2009
21.8 (1.0)
2010
23.4 (2.3)
24.0 (1.1)
25.8 (1.2)
25.6 (1.6)
19.08 (2.2)
14.55 (2.7)
16.48 (1.8)
Salinity (ppt)
2008
2009
2010
26.4 (3.4)
27.5 (0.6)
26.9 (4.2)
28.2 (2.7)
26.0 (4.1)
29.3 (2.5)
26.17 (5.6)
26.72 (3.9)
27.95 (3.0)
Dissolved oxygen (mg L−1 )
2008
7.3 (1.1)
2009
8.3 (1.3)
2010
8.4 (1.1)
6.6 (1.0)
7.9 (7.3)
7.1 (1.0)
7.27 (1.1)
9.74 (8.5)
9.36 (0.7)
pH
2008
2009
2010
8.1 (0.2)
8.0 (0.2)
8.2 (0.2)
8.0 (0.3)
7.9 (0.2)
8.0 (0.1)
8.00 (0.2)
8.00 (0.2)
8.08 (0.1)
Secchi depth (m)
2008
1.2 (0.3)
2009
1.3 (0.3)
2010
1.2 (0.3)
1.1 (0.2)
1.1 (0.3)
1.0 (0.2)
1.28 (0.4)
1.35 (0.2)
1.19 (0.3)
◦
redundancy variables are plotted on top of the scores for the redundancy axes. Differences in the frequency of macroalgal blooms
between 2004–2006 and 2008–2010 were tested with chi square
analysis (Proc Freq, SAS Inc.) by bloom condition (‘Early Bloom’:
percent cover 70–80%, ‘Full Bloom’: percent cover > 80%).
We hypothesize that as symptoms of eutrophication (i.e.
concentrations of total nitrogen, chlorophyll a, and dissolved oxygen) increase, eelgrass characteristics (i.e. biomass) will become
degraded (i.e. have decreased values).
3. Results
3.1. Physical and chemical conditions
Strong seasonality was observed, as is generally the case for temperate Zostera beds, and a significant sampling period effect was
generally obvious for physical and chemical conditions (Table 1).
The contribution of seasonality to variance in seagrass was separated out (Table 2) so that the remaining effect of other factors
(year, transect) could be examined. Sampling period explained 68%
of the variance associated with temperature, but spatial location
(transect) explained 68% of the variance associated with salinity
(due to proximity to Toms River and the inlets which provide freshwater input and oceanic exchange, respectively). Most variance of
dissolved oxygen (82%) and pH (73%) was not explained by either
spatial or temporal effects (Table 2). Dissolved oxygen concentrations were generally above 5.0 mg L−1 .
3.2. Eelgrass characteristics
3.2.1. Eelgrass biomass
Eelgrass biomass declined consistently during both 2004–2006
and 2008–2010 periods and overall from 2004 to 2010, and biomass
in 2010 was the lowest recorded for Barnegat Bay-Little Egg Harbor
(Fig. 2). Aboveground and belowground biomass declined significantly (p < 0.01, Table 2) from 2008 to 2009 to 2010 (Fig. 2). Within
years, only belowground biomass declined over June to November
in 2008 (main effect, p < 0.01, Table 2), but both aboveground and
belowground eelgrass biomass decreased over time in 2009 (main
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Table 2
Three-way ANOVA testing effect of Year, Sampling Period, and Transect and their
interactions on temperature, salinity, dissolved oxygen, pH, and Z. marina aboveground biomass, belowground biomass, shoot density, blade height, and areal cover.
Degrees of freedom (df), percent sum of squares (% SS), and p value (p < 0.05 in bold)
are reported.
Variable
Water quality
Temperature
Salinity
Effect
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Dissolved oxygen
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
pH
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Z. marina
Aboveground
biomass
Belowground
biomass
Shoot density
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
df
% SS
2
2
11
4
22
22
44
2
68
1
6
4
10
7
963
2
2
2
11
4
22
22
38
4
3
68
2
3
3
2
916
19
2
2
11
4
22
22
38
2
2
3
0
3
3
6
914
82
2
2
11
4
22
22
38
1
1
5
0
5
5
8
913
73
2
2
11
4
22
22
44
6
1
8
0
6
3
3
854
75
2
2
11
4
22
22
44
4
2
11
0
4
3
4
854
72
2
2
11
4
22
22
44
3
0
6
3
12
7
8
639
64
Table 2 (Continued)
Variable
Effect
Blade height
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
Areal cover
Year
Sampling Period
Transect
Year × Sampling Period
Transect × Year
Transect × Sampling Period
Transect × Year × Sampling
Period
Error
p
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
0.0002
<0.0001
0.0019
0.9072
0.0251
0.1557
0.0113
0.0027
0.0007
<0.0001
0.1923
<0.0001
<0.0001
<0.0001
<0.0001
0.0024
<0.0001
0.2673
<0.0001
0.0766
0.9112
<0.0001
<0.0001
<0.0001
0.3377
0.0013
0.0112
0.3993
<0.0001
0.3468
<0.0001
<0.0001
<0.0001
<0.0001
0.0038
73
df
% SS
2
2
11
4
22
22
41
9
1
34
3
6
2
3
455
36
2
2
11
4
22
22
44
1
2
11
2
6
3
3
971
73
p
<0.0001
0.0352
<0.0001
<0.0001
<0.0001
0.1299
0.5694
0.0041
<0.0001
<0.0001
<0.0001
<0.0001
0.0044
0.7285
effect, p < 0.01, Table 2). Belowground biomass was higher than
aboveground biomass (ANOVA, p < 0.01, Fig. 2). Eelgrass biomass
was generally low along transects 1, 2 (southern segment) and 12
(central segment) and consistently high along transects 5, 9, and
11 (Fig. 1). The spatial factor (transect) explained 8% of variance
for aboveground biomass and 11% of variance for belowground
biomass, both of which were higher than for any other factor
(Table 2).
The rate of decline in aboveground and belowground eelgrass biomass was significantly sharper during 2004–2006
than in 2008–2010. Regression analysis indicated a slope
of −23.8 g m−2 yr−1 (intercept = 47,765, R2 = 0.14, p < 0.01) during 2004–2006 and −8.7 g m−2 yr−1 (intercept = 17,496, R2 = 0.04,
p < 0.01) during 2008–2010. A t-test comparing these slopes
showed a significant difference (t = −6.13, p < 0.01), indicating that
the decline slowed significantly in the latter three years, as can be
seen in Fig. 3d–i. In contrast, the slopes for belowground biomass
did not differ (t = 0.25, p = 0.80) though the decline continued
(slope = −17.0 during 2004–2006 and −18.4 during 2008–2010).
3.2.2. Eelgrass shoot density
Though biomass declined from 2004 to 2010, the number
of shoots (a proxy for individuals in the population) generally
increased from 2004 (189 shoots) to 2010 (596 shoots). Timing of peak mean eelgrass shoot density (August–September in
2008, June–July in 2009) coincided with peak biomass (aboveground in 2008, both aboveground and belowground in 2009).
Shoot density was much lower during the summer-fall period in
2009 than in 2008 (Table 3). The highest amount of variation (12%)
was explained by the significant interaction (three-way ANOVA,
p < 0.01) transect × year (Table 2).
3.2.3. Eelgrass blade length
Transect explained 34% of the variation (Table 2) in eelgrass blade length. Though only explaining 9% of the variation,
mean lengths of eelgrass blades generally decreased from 2008
(30.8 ± 13.1 cm) to 2009 (22.7 ± 12.1 cm) to 2010 (21.6 ± 12.2 cm)
(Tables 2 and 3). By comparison, in 2004 the mean blade lengths
of eelgrass were 34.0 ± 10.9 cm in June–July, 32.2 ± 7.2 cm in
August–September, and 31.8 ± 8.4 cm in October–November, and
during 2005 the mean blade lengths of eelgrass amounted to
32.7 ± 17.6 cm in June–July, 25.9 ± 14.9 cm in August–September,
and 28.5 ± 14.7 cm in October–November. Somewhat lower mean
blade length measurements were recorded in the heavily impacted
year of 2006 during June–July (19.4 cm), August–September
(18.7 cm), and October–November (18.6 cm).
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Biomass (g dry weight m-2)
74
350
250
150
50
No Data
J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N
2004
2005
2006
2007
2008
2009
2010
Belowground biomass
Aboveground biomass
Fig. 2. Aboveground and belowground seagrass biomass values in the Barnegat Bay-Little Egg Harbor Estuary during the spring–fall sampling periods from 2004 to 2010
(except 2007).
eelgrass in 2009 decreased from 31 ± 36% in June–July to 27 ± 35%
in August–September, and then decreased greatly to 15 ± 19% in
October–November. Macroalgae ‘Early Blooms’ (70–80%) occurred
twice during 2004–2006 and 17 times during 2008–2010 (chi
square p < 0.01). Macroalgae ‘Full Blooms’ (>80%) occurred 12 times
during 2004–2006 and 24 times during 2008–2010 (chi square
p < 0.05, Fig. 4).
10
a)
6
4
2
0
0
200
400
Dissolved Oxygen (mg L-1)
8
Dissolved Oxygen (mg L-1)
Chlorophyll a (µg L-1)
3.2.4. Eelgrass and macroalgae areal cover
Transect explained 6% of the variation in eelgrass areal cover
(Table 2). The percent cover of eelgrass in 2008 was similar
to that observed in previous years of sampling (2004–2006).
In 2008, the percent cover of eelgrass was lowest in June–July
(22 ± 30%) and October–November (22 ± 31%), and highest in
August–September (30 ± 36%). By comparison, the percent cover of
10
b)
8
6
4
2
0
600
0
200
Total Nitrogen (µg L-1)
400
40
20
40
20
400
600
0
2
60
40
4
6
0
60
40
400
Shoot Density (shoots m-2)
2
600
4
6
8
10
i)
80
60
40
20
0
0
200
20
100
h)
80
0
0
40
Dissolved Oxygen (mg L-1)
20
20
f)
60
8
Biomass (g m-2)
Biomass (g m-2)
Biomass (g m-2)
100
80
8
80
-1
Total Nitrogen (µg L )
g)
4
6
2
Chlorophyll a (µg L-1)
Chlorophyll a (µg L )
-1
100
0
0
0
200
0
100
e)
60
0
0
2
600
Biomass (g m-2)
60
4
2008-2010
80
Biomass (g m-2)
Biomass (g m-2)
100
d)
80
6
Total Nitrogen (µg L-1)
2004-2006
100
c)
8
0
10
20
30
40
Areal Cover (%)
0
10
20
30
40
Light Availability (%)
2004-2006 2008-2010
Aboveground biomass
Belowground biomass
Fig. 3. Variation of water quality and biological metrics for 2004–2006 (circles) and 2008–2010 (triangles). Eelgrass biomass is divided into aboveground (black) and
belowground (white) components. Plots include chlorophyll a vs. total nitrogen (a), dissolved oxygen vs. total nitrogen (b), dissolved oxygen vs. chlorophyll a (c), eelgrass
biomass vs. total nitrogen (d), eelgrass biomass vs. chlorophyll a (e), eelgrass biomass vs. dissolved oxygen (f), eelgrass biomass vs. eelgrass shoot density (g), eelgrass biomass
vs. eelgrass areal percent cover (h), and eelgrass biomass vs. light availability (i).
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Table 3
Mean (standard deviation) shoot density, blade length, and percent areal cover of Z.
marina in Barnegat Bay-Little Egg Harbor Estuary, 2008–2010.
Sampling period
(months)
Shoot density
(shoots m−2 )
Blade length (cm)
Areal cover (%)
2008
June–July
August–September
October–November
242 (435)
414 (570)
264 (465)
29 (12)
22 (14)
31 (18)
22 (30)
30 (36)
22 (31)
2009
June–July
August–September
October–November
347 (536)
265 (407)
155 (325)
22 (13)
25 (12)
22 (11)
31 (36)
27 (35)
15 (19)
2010
June–July
August–September
October–November
665 (460)
377 (380)
440 (708)
22 (13)
20 (11)
23 (13)
28 (36)
21 (35)
9 (21)
3.3. Multivariate analyses of covariance and collinearity
Multivariate (MANOVA) tests of overall effects of physical
and chemical variables on Z. marina characteristics using the
Wilks’ Lambda criteria were statistically significant for temperature (F5,255 = 7.54, p < 0.01), salinity (F5,255 = 8.17, p < 0.01), dissolved
oxygen concentration (F5,255 = 3.96, p < 0.01), pH (F5,255 = 2.41,
p < 0.05), and Secchi depth (F5,255 = 6.21, p < 0.01). Follow up
multivariate comparisons using Wilks’ Lambda statistic indicated that there were significant differences between transects
(F55,1183.9 = 2.83, p < 0.01). Specifically, the average for Little Egg
Harbor was significantly different from the average for Barnegat
Bay (F5,255 = 5.03, p < 0.01). RDA indicated little separation between
transects (Fig. 5a), though transects 10, 11, and 12 tended to group
at the lower salinity, lower dissolved oxygen end of the spectrum.
Transects 7, 1, and 4 tended to be on the higher salinity end of
the spectrum (Fig. 5b), which corresponds to their proximity to the
inlets (Fig. 1). There is clearer temporal separation by both year
(Fig. 5b) and time period (Fig. 5c). Temperatures were lower and
salinity was higher in 2004 and 2010, while 2008 was warmer and
less saline. During October–November, dissolved oxygen and pH
are highest, while temperatures are cooler compared to other time
periods.
75
4. Discussion
Here, we present evidence that eelgrass condition in Barnegat
Bay has declined substantially (Fig. 2), that the rate of decline is
related to nutrient loading, algal shading, and associated symptoms
of eutrophication (Figs. 3–6), and finally that this degradation rate
has changed over time (Table 2). Trends in eelgrass characteristics presented here update previous studies in Barnegat Bay-Little
Egg Harbor Estuary, New Jersey, USA (Kennish et al., 2008a,b). The
current study focuses on a small set of plant characteristics and
thus is narrower than those that use suites of seagrass morphometrics (Duarte et al., 1994), Leslie table matrices (Uzeta et al., 2008),
or mortality estimates (Ebert et al., 2002) to derive demographic
histories and dynamics.
Eelgrass biomass and areal cover generally decreased through
2010, but the decline in plant biomass, a key water quality indicator (Fig. 2, Burkholder et al., 2007; Moore, 2004, 2009; Duarte et al.,
2006; Lamote and Dunton, 2006; Moore and Short, 2006; Kennish
et al., 2008a,b, 2009, 2010), was most marked (Fig. 2). A general
decline in plant parameters (except blade length) was evident from
2008 to 2010 (Table 3) corresponding with temporal separation
(yearly and seasonally, Fig. 5) of environmental parameters suggests their importance to seagrass condition. Trends of eelgrass
characteristics indicated that eelgrass biomass (Figs. 2 and 3) had
yet to recover by 2010 from the decline of plant abundance and
biomass observed in 2006 (Kennish et al., 2009, 2010). However, the
rate of decline of eelgrass biomass during 2008–2010 was slower
than that of 2004–2006 (Fig. 2), perhaps because less was left to
be lost. Thus, biomass may be reaching a new, lower, steady state
(Beisner et al., 2003) though prediction of future condition is speculative at best, as it could either improve, as has been observed
subsequent to improvements in water quality or wasting disease
(Plus et al., 2003; Frederiksen et al., 2004), or it may be difficult to attain previously observed levels (e.g. Duarte et al., 2009;
Martin et al., 2010; Krause-Jensen et al., 2012). Though long-term
monitoring was not started early enough to observe the beginning of the initial decline prior to 2004, the pattern of biomass
decline with increasing nutrient concentrations (Fig. 3d) is similar to load-decline relationships described in the literature (Cloern,
2001; Nixon, 1995; Burkholder et al., 2007; Deegan, 2002; Tomasko
et al., 1996) and nitrogen concentrations in Barnegat Bay-Little Egg
Harbor are proportional with nitrogen loading from subwatersheds
(Fig. 6; Kennish and Fertig, 2012). Dissolved inorganic nitrogen
16
Early Bloom (70-79% cover)
14
Full Bloom (80-100% cover)
Frequency
12
10
8
6
4
2
0
No Data
J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N J-J A-S O-N
2004
2005
2006
2007
2008
2009
2010
Fig. 4. Frequency of macroalgae cover at ‘Early Bloom’ = 70–79%, and ‘Full Bloom’ = > 80% conditions. Frequencies observed during June–July (J-J), August–September (A-S),
and October–November (O-N) during 2004–2006 and 2008–2010. No data are available during 2007.
76
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Fig. 5. Redundancy analysis (RDA) with physical and chemical variables as independent variables and Z. marina characteristics as dependent variables. Redundancy scores are
plotted by (a) transect (1–12 indicated by color), (b) year (2004–2010 excepting 2007 by color), and (c) time period (June–July, August–September, and October–November
by color). Coefficients for predicting independent variables from the redundancy variables are plotted (gray lines). (For interpretation of the references to color in this figure
legend, the reader is referred to the web version of the article.)
concentration ranges measured in this study were consistent with
of those of Seitzinger et al. (2001), who recorded highest nitrogen concentrations in the northern estuary. The trend of eelgrass
decline has been estuary-wide, signaling a response to a broad scale
stressor that adversely affects plant condition across the system.
Vulnerability of eelgrass beds to nutrient loading may vary
across systems. Previous and current reductions in areal extent
of Z. marina beds (30–60%, Bologna et al., 2000; Table 3) were a
third of areal reductions observed in Waquoit Bay (80–100% bed
area, Hauxwell et al., 2003), but loading to Barnegat Bay-Little Egg
Harbor Estuary (2.5 kg N ha−1 yr−1 ; Wieben and Baker, 2009) was
4–8% that of Waquoit Bay (30–60 kg N ha−1 yr−1 ; Hauxwell et al.,
2003). The pattern of decline in Barnegat Bay-Little Egg Harbor
contrasts from that of Waquoit Bay in that shoot density and bed
area declined exponentially in Waquoit Bay, while in Barnegat BayLittle Egg Harbor it was biomass that declined exponentially while
shoot density did not change (or even increased), leading to an overall decline in biomass per shoot (Fig. 3). Long-term monitoring is
important in documenting broad changes, including recolonization
after complete die-offs (e.g. Plus et al., 2003). While we previously
reported that a ‘Nutrient Pollution Indicator’, defined by Lee et al.
(2004) as the ratio of Z. marina leaf nitrogen content (%N) to area
normalized leaf mass (mg dry wt cm−2 ), did not reliably indicate
estuarine eutrophic status or relate to nutrient loading from the
watershed (Kennish and Fertig, 2012), the more direct measurements of Z. marina characteristics reported here (e.g. biomass, shoot
density, etc.) responded spatially to changes in nutrient loading and
Table 4
Light availability (%) ± standard deviation in transects 1–6 (Little Egg Harbor) and
transects 7–12 (Barnegat Bay), 2004–2010.
Year
2004
2005
2006
2007
2008
2009
2010
Light availability (%)
Transects 1–6
Transects 7–12
9.6 ± 6.2
4.1 ± 3.9
7.0 ± 14.7
nd
5.6 ± 11.2
32.4 ± 7.7
31.9 ± 6.4
16.7 ± 17.1
21.8 ± 19.9
16.2 ± 18.7
nd
21.2 ± 7.8
24.1 ± 7.1
23.8 ± 7.4
symptoms associated with eutrophication (Figs. 3–5; Table 2). A
GIS spatial comparison analysis by Lathrop et al. (2001) suggested
a contraction of the eelgrass beds to shallow subtidal areas (<2 m)
during this 25-year time period due to diminished light availability in response to phytoplankton and macroalgal blooms, epiphytic
overgrowth, and other factors. However, Lathrop and Haag (Center for Remote Sensing and Spatial Analysis, Rutgers University,
personal communication, 2010), conducting more recent aerial
surveys (2003 and 2009) of eelgrass distribution in the estuary,
found an expansion of the bed boundaries by 69 ha during a time
span when biomass and other plant characteristics were dramatically declining. Short (2007) recently observed a similar pattern
of eelgrass distribution and plant characteristics in Great Bay Estuary, New Hampshire. Eelgrass beds appear to be thinning out, as
biomass shoot−1 declined from 2004 to 2010 (Fig. 3), and we speculate that this may decrease opportunities for future fertilization
and/or seed dispersal.
Since 2004, the condition of eelgrass beds in the estuary has
declined with increasing nitrogen loading from the Barnegat Bay
watershed (Figs. 2–3, Wieben and Baker, 2009) and associated
eutrophication (Fig. 6; Nixon, 1995; Seitzinger et al., 2001; Bricker
et al., 2007; Kennish et al., 2007a, 2010). Eelgrass degradation in
relation to eutrophication and algal shading in Barnegat Bay-Little
Egg Harbor (Fig. 3) also affects Great Bay Estuary, New Hampshire
(biomass, shoot density, canopy height, leaf area; Beem and Short,
2009), and Chincoteague Bay (seagrass coverage 2001–2004 by
Wazniak et al., 2007, seagrass coverage 2001–2007 by Orth et al.,
2010). System eutrophy (Figs. 3a–c and 4) and degradation of eelgrass characteristics in Barnegat Bay-Little Egg Harbor (Figs. 2 and 3,
Table 3; Kennish et al., 2007b, 2008a, 2010) have progressed in
concert with nutrient loading from surface water of the watershed
from 390,000 kg N yr−1 in 1998 (Hunchak-Kariouk and Nicholson,
2001) to 431,000 kg N yr−1 in 2008 (Wieben and Baker, 2009) and
watershed development (18% in 1972 to ∼33% in 2010, Lathrop and
Bognar, 2001; Richard G. Lathrop, Center for Remote Sensing and
Spatial Analysis, Rutgers University, 2010). Currently, 66% of the
total nitrogen load to the Barnegat Bay-Little Egg Harbor Estuary
derives from surface runoff of the watershed, up from 54% of the
total nitrogen load in 1998 (Wieben and Baker, 2009). The total
nitrogen load is expected to increase with increasing development
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
77
Fig. 6. Long-term total nitrogen concentrations for Barnegat Bay-Little Egg Harbor Estuary: 1989–2000 on top, 2001–2010 on bottom; June–July on the left, August–September
in center, and October–November on the right. Decadal means (symbols) are overlaid atop krig interpolation. Concentrations increase from green to red. (For interpretation
of the references to color in this figure legend, the reader is referred to the web version of the article.)
of the watershed, unless aggressive management actions are implemented. Yet projections indicate that impervious surface cover of
the Barnegat Bay watershed will increase to 12% of the land area at
buildout (Lathrop and Conway, 2001).
Nutrient loading and symptoms of eutrophication (e.g.
increased nutrient and chlorophyll a concentrations) classically
impact seagrass through reductions in light availability (Burkholder
et al., 2007; Ralph et al., 2007; Lee et al., 2007). Decreases in overall light availability (Table 4) in Barnegat Bay-Little Egg Harbor
Estuary were contributed to increases in chlorophyll a (Fig. 3).
As chlorophyll a increases, Z. marina biomass (both aboveground
and belowground) increases until ∼5 ␮g L−1 chlorophyll a, beyond
which Z. marina biomass decreases (Fig. 3e). Yet chlorophyll a concentrations were much less than reported impacts on seagrass
elsewhere in the literature (Wazniak et al., 2007). Further, eelgrass
may be able to survive increases in turbidity by growing either up
or horizontally (Vermaat et al., 1997), but there is limited capacity
for this in Barnegat Bay-Little Egg Harbor due to shallow depths
and benthic substrate heterogeneity (Fig. 1; Psuty and Silveira,
2009). Observations of physical–chemical and nutrient parameters
(Table 1, Figs. 3 and 6) input into empirical-based relationships
and models (Kemp et al., 2004) indicate that estimated light
availability (Table 4) in 2004–2006 (12.6 ± 13.4% of surface irradiance) and 2008–2010 (23.2 ± 7.9% of surface irradiance) were
greater than the minimum light requirements (5–20% of surface
irradiance, Dennison et al., 1993), but generally less than optimal
light requirements for Z. marina (approaching 25% of incident radiation; Orth et al., 2006).
78
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Increased nitrogen in shallow water systems with adequate
water clarity can lead to the replacement of eelgrass plants by
opportunistic macroalgae (e.g. Ulva and Enteromorpha), filamentous epiphytic macroalgae, and benthic microalgae which require
lower light intensities for survival, thus outcompeting and shading
over the eelgrass, resulting in negative feedback (Hily et al., 2004;
McGlathery et al., 2007). Macroalgae blooms (mainly Ulva lactuca) were commonly observed in Barnegat Bay-Little Egg Harbor
(Kennish et al., 2011), increasing in frequency from 2004–2006 to
2008–2010 (Fig. 4) and thus diminishing light available to seagrass
leaves. Blooms of sheet-like macroalgae can contribute to transfer of nutrients to sediments (Boyer and Fong, 2005). Resulting
shifts in the composition of bottom-up controls also often resonates
through upper trophic levels of an estuarine ecosystem. Additionally, light attenuation associated with epiphytes (10% of eelgrass
biomass, Kennish et al., 2012), and detritus may be impacting Z.
marina in Barnegat Bay-Little Egg Harbor Estuary. The loss of eelgrass habitat due to light attenuation affects trophic structure by
reducing the abundance of herbivorous grazers that can control
algal overgrowth (Burkholder et al., 2007). The resulting increase
in algal epiphytes, therefore, may exacerbate eelgrass decline via
reduced top-down control (Heck and Valentine, 2007). We conclude that nutrient loading, algal shading, and eutrophication are
the primary drivers of change in eelgrass habitat of Barnegat BayLittle Egg Harbor Estuary.
Acknowledgments
This is Contribution No. 12-007 of the Institute of Marine and
Coastal Sciences, Rutgers University. Research grants to Michael J.
Kennish from the New Jersey Department of Environmental Protection, U.S. Environmental Protection Agency, Barnegat Bay National
Estuary Program, and NOAA’s National Estuarine Research Reserve
System Program are gratefully acknowledged.
References
Beem, N.T., Short, F.T., 2009. Subtidal eelgrass declines in the Great Bay Estuary, New
Hampshire and Maine, USA. Estuaries Coasts 32, 202–2005.
Beisner, B.E., Haydon, D.T., Cuddington, K., 2003. Alternative stable states in ecology.
Frontiers in Ecology and the Environment 1, 376–382.
Billen, G., Garnier, J., 2007. River basin nutrient delivery to the coastal sea: assessing
its potential to sustain new production of non-siliceous algae. Marine Chemistry
106, 148–160.
Bologna, P.A.X., Lathrop, R., Bowers, P.D., Able, K.W., 2000. Assessment of the health
and distribution of submerged aquatic vegetation from Little Egg Harbor, New
Jersey. Technical Report. Contribution #2000-11, Institute of Marine and Coastal
Sciences, Rutgers University, New Brunswick, New Jersey. 30 pp.
Boyer, K.E., Fong, P., 2005. Macroalgal-mediated transfers of water column nitrogen
to intertidal sediments and salt marsh plants. Journal of Experimental Marine
Biology and Ecology 321, 59–69.
Bricker, S.B., Longstaff, B., Dennison, W., Jones, A., Boicourt, K., Wicks, C., Woerner,
J., 2007. Effects of nutrient enrichment in the nation’s estuaries: a decade of
change. NOAA Technical Report. National Ocean Service, Special Projects Office
and National Centers for Coastal Ocean Science, Silver Spring, Maryland, USA.
Burkholder, J.M., Tomasko, D.A., Touchette, B.W., 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350, 46–72.
Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210, 223–253.
Deegan, L.A., 2002. Lessons learned: the effects of nutrient enrichment on the support of nekton by seagrass and salt marsh ecosystems. Estuaries 25, 727–742.
Dennison, W.C., Orth, R.J., Moore, K.A., Stevenson, J.C., Carter, V., Kollar, S., Bergstrom,
B.W., Batiuk, R.A., 1993. Assessing water quality with submerged aquatic vegetation. BioScience 43, 86–94.
Duarte, C.M., Fourqurean, J.W., Krause-Jensen, D., Olesen, B., 2006. Dynamics of
seagrass stability and change. In: Larkum, W.D., Orth, R.J., Duarte, C.M. (Eds.),
Biology, Ecology and Conservation. Springer, Dordrecht, pp. 271–294.
Duarte, C.M., Conley, D.J., Carstensen, J., Sánchez-Camacho, M., 2009. Return to neverland: shifting baselines affect eutrophication restoration targets. Estuaries
Coasts 32, 29–36.
Duarte, C.M., Marbá, N., Agawin, N., Cebrián, J., Enríquez, S., Fortes, M.D., Gallegos,
M.E., Merino, M., Oleson, B., Sand-Jensen, K., Uri, J., Vermaat, J., 1994. Reconstruction of seagrass dynamics: age determinations and associated tools for the
seagrass ecologist. Marine Ecology Progress Series 107, 195–209.
Ebert, T.A., Williams, S.L., Ewanchuk, P.J., 2002. Mortality estimates from age distribution: critique of a method used to study seagrass dynamics. Limnology and
Oceanography 47, 600–603.
Frederiksen, M., Krause-Jensen, D., Holmer, M., Laursen, J.S., 2004. Long-term
changes in area distribution of eelgrass (Zostera marina) in Danish coastal waters.
Aquatic Botany 78, 167–181.
Hauxwell, J., Cebrian, J., Valiela, I., 2003. Eelgrass Zostera marina loss in temperate estuaries: relationship to land-derived nitrogen loads and effect of light
limitation imposed by algae. Marine Ecology Progress Series 247, 59–73.
Heck Jr., K.L., Valentine, J.F., 2007. The primacy of top-down effects in shallow benthic
ecosystems. Estuaries Coasts 30, 371–381.
Hily, C., Connan, S., Raffin, C., Wyllie-Echeverria, S., 2004. In vitro experimental
assessment of the grazing pressure of two gastropods on Zostera marina L. epiphytic algae. Aquatic Botany 78, 183–195.
Howarth, R.W., Chan, F., Conley, D.J., Garnier, J., Doney, S.C., Marino, R., Billen, G.,
2011. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate
estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment 9, 18–26.
Hunchak-Kariouk, K., Nicholson, R.S., 2001. Watershed contributions of nutrients
and other nonpoint source contaminants to the Barnegat Bay-Little Egg Harbor
Estuary. Journal of Coastal Research 32, 28–81 (Special Issue).
Kemp, W.M., Batiuk, R., Bartleson, R., Bergstrom, P., Carter, V., Gallegos, C.L., Hunley, W., Karrh, L., Koch, E.W., Landwehr, J.M., Moore, K.A., Murray, L., Naylor, M.,
Rybicki, N.B., Stevenson, J.C., Wilcox, D.J., 2004. Habitat requirements for submerged aquatic vegetation in Chesapeake Bay: water quality, light regime, and
physical-chemical factors. Estuaries 27, 363–377.
Kemp., W.M., Boynton, W.R., Adolf, J.E., Boesch, D.F., Boicourt, W.C., Brush, G., Cornwell, J.C., Fisher, T.R., Glibert, P.M., Hagy, J.D., Harding, L.W., Houde, E.D., Kimmel,
D.G., Miller, W.D., Newell, R.I.E., Roman, M.R., Smith, E.M., Stevenson, J.C., 2005.
Eutrophication of Chesapeake Bay: historical trends and ecological interactions.
Marine Ecology Progress Series 303, 1–29.
Kennish, M.J. (Ed.), 2001a. Barnegat Bay-Little Egg Harbor, New Jersey: estuary and
watershed assessment. Journal of Coastal Research 32, 280 pp. (Special Issue).
Kennish, M.J., 2001b. Characterization of the Barnegat Bay-Little Egg Harbor Estuary
and Watershed. Journal of Coastal Research 32, 3–12 (Special Issue).
Kennish, M.J., 2007. Barnegat Bay-Little Egg Harbor Estuary: ecosystem condition
and recommendations. Technical Report. Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey. 55 pp.
Kennish, M.J. (Ed.), 2007b. Eutrophication of estuarine and shallow coastal marine
systems. Ecological Applications 17 (5 Suppl.), 196 pp.
Kennish, M.J., 2009. Eutrophication of mid-Atlantic coastal bays. Bulletin of the New
Jersey Academy of Science 55, 5–12.
Kennish, M.J., Bricker, S.B., Dennison, W.C., Glibert, P.M., Livingston, R.J., Moore, K.A.,
Noble, R.T., Paerl, H.W., Ramstack, J.M., Seitzinger, S., Tomasko, D.A., Valiela, I.,
2007a. Barnegat Bay-Little Egg Harbor Estuary: case study of a highly eutrophic
coastal bay system. Ecological Applications 17 (5 Suppl.), S3–S16.
Kennish, M.J., Fertig, B., 2012. Application and assessment of a nutrient pollution
indicator using eelgrass (Zostera marina L.) in Barnegat Bay-Little Egg Harbor
Estuary, New Jersey. Aquatic Botany 96, 23–30.
Kennish, M.J., Fertig, B., Lathrop, R.G., 2012. Assessment of nutrient loading and
eutrophication in Barnegat Bay-Little Egg Harbor, New Jersey in support of nutrient management planning. Technical Report. Institute of Marine and Coastal
Sciences, Rutgers University, New Brunswick, New Jersey. 258 pp.
Kennish, M.J., Fertig, B., Sakowicz, G.P., 2011. Benthic macroalgal blooms as an indicator of system eutrophy in the Barngat Bay-Little Egg Harbor Estuary. Bulletin
of the New Jersey Academy of Science 56, 1–5.
Kennish, M.J., Haag, S.M., Sakowicz, G.P., 2007. Demographic investigation of SAV
in the Barnegat Bay-Little Egg Harbor Estuary with assessment of potential
impacts of benthic macroalgae and brown tides. Technical Report. Institute of
Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey.
366 pp.
Kennish, M.J., Haag, S.M., Sakowicz, G.P., 2008a. Seagrass demographic and spatial
habitat characterization in Little Egg Harbor, New Jersey, using fixed transects.
Journal of Coastal Research 55, 148–170 (Special Issue).
Kennish, M.J., Haag, S.M., Sakowicz, G.P., 2008b. Seagrass habitat characterization in
estuarine waters of the Jacques Cousteau National Estuarine Research Reserve
using underwater videographic imaging techniques. Journal of Coastal Research
55, 171–179 (Special Issue).
Kennish, M.J., Haag, S.M., Sakowicz, G.P., 2009. Assessment of eutrophication in the
Barnegat Bay-Little Egg Harbor System: use of SAV biotic indicators of estuarine condition. Technical Report. New Jersey Department of Environmental
Protection, Trenton, New Jersey. 73 pp.
Kennish, M.J., Haag, S.M., Sakowicz, G.P., 2010. Seagrass decline in New Jersey coastal
lagoons: a response to increasing eutrophication. In: Kennish, M.J., Paerl, H.W.
(Eds.), Coastal Lagoons: Critical Habitats of Environmental Change. Taylor and
Francis Publishers, Boca Raton, FL, pp. 167–201.
Kennish, M.J., Townsend, A.R., 2007. Nutrient enrichment and estuarine eutrophication. Ecological Applications 17 (5 Suppl.), S1–S2.
Krause-Jensen, D., Markager, S., Dalsgaard, T., 2012. Benthic and pelagic primary production in different nutrient regimes. Estuaries Coasts 35, 527–
545.
Lamote, M., Dunton, K.H., 2006. Effects of drift macroalgae and light attenuation
in chlorophyll fluorescence and sediment sulfides in the seagrass Thalassia testudinum. Journal of Experimental Marine Biology and Ecology 334, 174–186.
Larkum, W.D., Orth, R.J., Duarte, C.M. (Eds.), 2006. Seagrasses: Biology, Ecology and
Conservation. Springer, Dordrecht.
B. Fertig et al. / Aquatic Botany 104 (2013) 70–79
Lathrop, R.G., Bognar, J.A., 2001. Habitat loss and alteration in the Barnegat Bay
regions. Journal of Coastal Research 32, 212–228 (Special Issue).
Lathrop, R.G., Conway, T.M., 2001. A build-out analysis of the Barnegat Bay Watershed. CRSSA Technical Report 2001-02. Center for Remote Sensing and Spatial
Analysis, Rutgers University, New Brunswick, New Jersey.
Lathrop, R.G., Styles, R., Seitzinger, S., Bognar, J., 2001. Use of GIS mapping and modeling approaches to examine the spatial distribution of seagrasses in Barnegat
Bay, New Jersey. Estuaries 24, 904–916.
Lee, K.-S., Short, F.T., Burdick, D.M., 2004. Development of a nutrient pollution indicator using the seagrass, Zostera marina, along nutrient gradients in three New
England estuaries. Aquat. Bot 78, 197–216.
Lee, K.-S., Park, S.R., Kim, Y.K., 2007. Effects of irradiance, temperature, and nutrients
on growth dynamics of seagrasses: a review. Journal of Experimental Marine
Biology and Ecology 350, 144–175.
Martin, P., Sébastien, D., Gilles, T., Isabelle, A., de Montaudouin, X., Emery, É., Claire,
N., Christophe, V., 2010. Long-term evolution (1988–2008) of Zostera spp. meadows in Arcachon Bay (Bay of Biscay). Estuarine, Coastal and Shelf Science 87,
357–366.
McGlathery, K.J., Sundbäck, K., Anderson, I.C., 2007. Eutrophication in shallow coastal
bays and lagoons: the role of plants in the coastal filter. Marine Ecology Progress
Series 348, 1–18.
Moore, K.A., 2004. Influence of seagrasses on water quality in shallow regions of the
lower Chesapeake Bay. Journal of Coastal Research 45, 162–178 (Special Issue).
Moore, K.A., 2009. Submerged aquatic vegetation of the York River. Journal of Coastal
Research 57, 50–58 (Special Issue).
Moore, K.A., Short, F.T., 2006. Zostera: biology, ecology and management. In: Larkum,
W.D., Orth, R.J., Duarte, C.M. (Eds.), Seagrasses: Biology, Ecology and Conservation. Springer, Dordrecht, pp. 361–386.
Nixon, S.W., 1995. Coastal eutrophication: a definition, social causes, and future
concerns. Ophelia 41, 199–220.
Nixon, S.W., Buckley, B., Granger, S., Bintz, J., 2001. Responses of very shallow marine
ecosystems to nutrient enrichment. Human and Ecological Risk Assessment 7,
1457–1481.
Ochieng, C.A., Short, F.T., Walker, D.I., 2010. Photosynthetic and morphological
responses of eelgrass (Zostera marina L.) to a gradient of light conditions. Journal
of Experimental Marine Biology and Ecology 382, 117–124.
Olesen, B., 1996. Regulation of light attenuation and eelgrass Zostera marina depth
distribution in a Danish embayment. Marine Ecology Progress Series 134,
187–194.
Olesen, B., Sand Jensen, K., 1993. Seasonal acclimatization of eelgrass Zostera marina
growth to light. Marine Ecology Progress Series 94, 91–99.
Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck Jr.,
K.L., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Olyarnik, S., Short, F.T., Waycott, M., Williams, S.L., 2006. A global crisis for seagrass ecosystems. BioScience
56, 987–996.
Orth, R.J., Marion, S.R., Moore, K.A., Wilcox, D.J., 2010. Eelgrass (Zostera marina L.)
in the Chesapeake Bay region of mid-Atlantic coast of the USA: challenges in
conservation and restoration. Estuaries Coasts 33, 139–150.
Paerl, H.W., Valdes, L.M., Pinckney, J.L., Piehler, M.F., Dyble, J., Moisander, P.H., 2003.
Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. BioScience 53, 953–964.
Paerl, H.W., Rossignol, K.L., Hall, S.N., Peierls, B.J., Wetz, M.S., 2009. Phytoplankton community indicators of short- and long-term ecological change in the
79
anthropogenically and climatically impacted Neuse River Estuary, North Carolina, USA. Estuaries Coasts, http://dx.doi.org/10.1007/s12237-009-9137-0.
Plus, M., Deslous-Paoli, J.-M., Dagault, F., 2003. Seagrass (Zostera marina L.) bed
recolonization after anoxia-induced full mortality. Aquatic Botany 77, 121–134.
Psuty, N.P., Silveira, T.M., 2009. Geomorphological evolution of estuaries: the
dynamic basis for morpho-sedimentary units in selected estuaries in the northeastern United States. Marine Fisheries Review 71, 34–45.
Rabalais, N.N., 2002. Nitrogen in aquatic ecosystems. Ambio 21, 102–112.
Radach, G., Patsch, J., 2007. Variability of continental riverine freshwater and nutrient inputs into the North Sea for the years 1977–2000 and its consequences for
the assessment of eutrophication. Estuaries Coasts 30, 66–81.
Ralph, P.J., Tomasko, D., Moore, K., Seddon, S., Macinnis-Ng, C.M.O., 2006. Human
impacts on seagrasses: eutrophication, sedimentation and contamination. In:
Larkum, W.D., Orth, R.J., Duarte, C.M. (Eds.), Seagrasses: Biology, Ecology and
Conservation. Springer, Dordrecht, pp. 567–593.
Ralph, P.J., Durako, M.J., Enríquez, S., Collier, C.J., Doblin, M.A., 2007. Impact of light
limitation on seagrasses. Journal of Experimental Marine Biology and Ecology
350, 176–193.
Seitzinger, S.P., Mayorga, E., Bouwman, A.F., Kroeze, C., Beusen, A.H.W., Billen, G.,
Van Drecht, G., Dumont, E., Fekete, B.M., Garnier, J., Harrison, J.A., 2010. Global
river nutrient export: a scenario analysis of past and future trends. Global Biogeochemical Cycles 24, GB0A08, http://dx.doi.org/10.1029/2009GB003587.
Seitzinger, S.P., Styles, R.M., Pilling, I.E., 2001. Benthic microalgal and phytoplankton
production in Barnegat Bay, New Jersey (USA): microcosm experiments and data
synthesis. Journal of Coastal Research 32, 144–162 (Special Issue).
Short, F.T., 2007. Eelgrass distribution in the Great Bay Estuary 2005. Technical
Report. University of New Hampshire, Durham, New Hampshire. 7 pp.
Short, F.T., McKenzie, L.J., Coles, R.G., Vidler, K.P., 2002. SeagrassNet Manual for
Scientific Monitoring of Seagrass Habitat. QDPI, QFS, Cairns, 56 pp.
Short, F.T., Koch, E.W., Creed, J.C., Magalhäes Fernandez, E., Gaeckle, J.L., 2006.
SeagrassNet monitoring across the Americas: case studies of seagrass decline.
Marine Ecology 27, 277–289.
Tomasko, D.A., Dawes, C.J., Hall, M.O., 1996. The effects of anthropogenic nutrient enrichment on turtle grass (Thalassia testudinum) in Sarasota Bay, Florida.
Estuaries 19, 448–456.
Uzeta, O.F., Arellano, E.S., Heras, H.E., 2008. Mortality rate estimation for eelgrass
Zostera marina (Potamogetonaceae) using projections from Leslie matrices.
Revista de Biologia Tropical 56, 1015–1022.
Vermaat, J.E., Agawin, N.S.R., Fortes, M.D., Uri, J.S., Duarte, C.M., Marba, N., Enriquez,
S., Van Vierssen, W., 1997. The capacity of seagrasses to survive increased turbidity and siltation: the significance of growth form and light use. Ambio 26,
499–504.
Waycott, M., Duarte, C.M., Carruthers, T.J.M., Orth, R.J., Dennison, W.C., Olyarnik,
S., Calladine, A., Fourqurean, J.W., Heck Jr., K.L., Hughes, A.R., Kendrick, G.A.,
Kenworthy, W.J., Short, F.T., Williams, S.L., 2009. Accelerating loss of seagrass
across the globe threatens coastal ecosystems. www.pnas.org/cgi/doi/10.1073/
pnas.0905620106
Wazniak, C.E., Hall, M.R., Carruthers, T.J.B., Sturgis, B., Dennison, W.C., Orth, R.J., 2007.
Linking water quality to living resources in a mid-Atlantic lagoon system, USA.
Ecological Applications 17 (5 Suppl.), S64–S78.
Wieben, C.M., Baker, R.J., 2009. Contributions of nitrogen to the Barnegat Bay-Little
Egg Harbor Estuary: updated loading estimates. U.S. Geological Survey. Technical Report. West Trenton, New Jersey.