Estuaries
Vol. 28, No. 5, p. 750~60
October 2005
Reversal of Eutrophication Following Sewage Treatment
Upgrades in the New River Estuary, North Carolina
MICHAEL A. M A L L I N * , MATTHEW R. MCIVER, H E A T H E R A. W E L L S , DOUGLAS C. PARSONS, a n d
VIRGINIA L. J O H N S O N
Centerj~r Marine Science, University of North Carolina Wilmington, Wilmington, North Carolina 28409
ABSTRACT: T h e New River Estuary consists of a series of b r o a d shallow lagoons draining a catchment area of 1,436 k m 2,
located in Onslow County, N o l t h Carolina. During the 1980s a n d 1990s it was considered one of the most eutrophlc estuaries
in the southeastern U n i t e d States a n d s~aslained dense phytoplankton blooms, b o l t o m water anoxia a n d hypoxia, toxic
outbreaks of the dinoflagellate Pfiesteria, a n d fish kills. H i g h nulrient loading, especially of phosphorus (P), f r o m mtmicipal
a n d military sewage trealment plants was the principal cause leading to the eulrophlc conditions. Nulrient addition bioassay
experiments showed that additions of nitrogen (N) b u t n o t P consistently yielded significant increases in phytoplankton
p r o d u O i o n relative to conlrols. During 1998 the City of Jacksonville a n d the U.S. Marine Corps Base at Camp Lejeune
completely u p g r a d e d their sewage lrealment systems a n d achieved large improvements in nulrient removal, reducing point
source inputs of N a n d P to the estuary by approximately 57% a n d 71%, respectively. The sewage lrealment plant upgrades
led to significant es~uadne decreases in a m m o n i u m , ol~hophosphate, chlorophyll a, a n d turbidity concenlrations, a n d
subsequent increases in b o t t o m water dissolved oxygen (DO t a n d fight penelration. The large r e d u O i o n in phytoplankton
biomass led to a large reduction in labile phytoplankton carbon, likely an i m p o r t a n t source of biochemical oxygen d e m a n d in
this estuary. The u p p e r estuary stations experienced increases in average bottom water DO of 9.9 to 1.4 m g 1 1, representing
an i m p r o v e m e n t in benthic habitat f o r shellfish a n d other organisms. T h e reductions in fight attenuation a n d turbidity should
also improve the habitat conditions for growth of submersed aquatic vegetation, an i m p o r t a n t habitat for fish a n d shellfish.
Introduction
(Monbet 1992; Cloern 2001). D o c u m e n t e d recoveries from estuarine eutrophication have occurred
b u t r e m a i n few (Smith 1981; Brattberg 1986;
Johansson and Greening 2000). In this paper we
provide evidence of the reversal of eutrophication
and subsequent habitat i m p r o v e m e n t in a large
estualTf- fbllowing major nutrient reductions resulting from upgrades in sewage treatment.
T h e New River is a fifth-order blackwater stream
located entirely within Onslow County- on North
Carolina's Coastal Plain. It drains a catchment area
of approximately 1,436 k m 2 with an estimated
h u m a n population of 84,360 in 1998 (NCDENR
2001). T h e New River Estuary- consists of a series of
shallow (1-2 m ) , broad lagoons of mesohaline to
polyhaline salinities (Dame et al. 2000). T h e m o u t h
of the estuary- is constrained by barrier islands,
restricting flushing, a n d the channels require
frequent dredging to maintain a navigational depth.
Recent estimates p u t the m e d i a n flushing time at
64 d, as opposed to the m o r e rapidly flushed
(median 7 d) Cape Fear River EstualTf- 80 k m to
the south (Ensign et al. 2004). Much of the area
adjacent to the estuary- p r o p e r consists of the United
States M a r i n e Corps (USMC) Base at C a m p
Lejeune. T h e r e is one major municipality- in the
watershed, the City- of Jacksonville, located on
Wilson Bay-, the u p p e r m o s t portion of the New
River Estuary- (Fig. 1). Upstream of Jacksonville the
river primarily drains agricultural areas. Some areas
Eutrophication of estuarine systems has numerous deleterious consequences and is considered to
be a widespread problem by g o v e r n m e n t organizations and academic researchers (NRC 1993, 2000;
Bricker et al. 1999; D a m e et al. 2000; Anderson et al.
2002). Causes of eutrophication vary- a m o n g regions
and individual systems, but point source discharges
of nutrients from municipal and industrial sewage
treatment plants r e m a i n a widespread p r o b l e m
(NRC 1993, 2000). In industrialized nations, during
the second half of the 20th century- most raw sewage
discharges had been converted to primary- a n d
secondary- treated discharges, which led to improvements in estuarine water quality in terms of reduced
suspended sediments, biochemical oxygen d e m a n d
(BOD), a n d fecal bacterial loads (Albert 1987;
Grifflths 1987; Brosnan and O ' S h e a 1996). Secondary- treatment does not remove significant amounts
of nitrogen (N) from wastewater (NRC 1993), and
achieving significantly r e d u c e d nutrient output
from point sources can be expensive in terms of
infrasti~cture costs, and it requires considerable
political will and cooperation (NRC 1993). Yet malay
estuaries, especially shallow, poorlFflushed systems,
are sensitive to even m o d e s t n u t r i e n t inputs
* C o r r e s p o n d i n g author; tele: 910/962-2358; fax: 910/9622410; e-maih mailinm@uncw.edu
9 2005 Estuarine Research Federation
750
Reversal of Estuarine Eutrophication
A at 9
9
9
N
S
Fig. 1. Map of the sampling stations in the New River EstumT,
coastal North Carolina, showing location of major confined
animal facilities in the watershed.
are u n d e r traditional agriculture while some areas
contain n u m e r o u s c o n c e n t r a t e d animal feeding
operations (CAFO), particularly swine CAFOs. In
2000 there were 138 registered animal operations
with approximately 150,400 h e a d of swine and
868,000 head of poultry in the New River drainage
basin (NCDENR 2001). Wastes f r o m CAFO spills
and illegal discharges have also polluted this estuary
(Burkholder et al. 1997; Mallin 2000).
In a 1996 National Oceanic and Atmospheric
Administration survey this estuary was considered
one of the four most eutrophic estuaries in the
southeastern U.S. (NOAA 1996; Bricker et al. 1999).
T h e New River Estuary hosted massive phytoplankton blooms, incidents of bottom-water hypoxia and
anoxia, and fish kills caused by low dissolved oxygen
(DO) incidents and toxic Pfiesteria outbreaks (Burkholder et al. 1997; Mallin et al. 2000; Glasgow et al.
2001; N C D W Q 2005). T h e m o r p h o l o g y of this
system, a series of b r o a d shallow lagoons that are
p o o r l y flushed, tends to retain n u t r i e n t s a n d
encourage algal b l o o m f o r m a t i o n (Mallin et al.
2000; Ensign et al. 2004). In 1988 the N o r t h
Carolina Division of Environmental M a n a g e m e n t
751
declared the New River as nutrient-sensitive waters,
so n o new wastewater discharges were to be
p e r m i t t e d into Wilson Bay (Holder personal communication).
A set of n u t r i e n t addition bioassays was perf o r m e d to assess the nutrients that were m o s t
stimulator-/ to p h y t o p l a n k t o n p r o d u c t i o n (using
&lanastrum capricornutum monocultures) in three
locations near Morgan Bay in J u n e 1989 (NCDEHNR
1990). In those e x p e r i m e n t s n i t r o g e n (N) was
d e t e r m i n e d to be the limiting nutrient. Phosphorus
(P) was a b u n d a n t in this estuary due to p o i n t
source inputs f r o m the 45 permitted point source
discharges involving b o t h civilian a n d military
wastewater facilities in the c a t c h m e n t (NCDEHNR
1990). In 1990 the total N and P loads to the
u p p e r estuary (from Morgan Bay upstream) were
estimated at 498,747 and 124,254 kg yr ], respectively
( N C D E H N R 1990). P o i n t s o u r c e d i s c h a r g e s
accounted for 65% of the total P load and 49%
of the total N load to the estuary (NCDEHNR
1990).
Prior to upgrades the Jacksonville and Marine
C o r p s sewage t r e a t m e n t plants s u f f e r e d f r o m
f r e q u e n t p r o b l e m s and inefficiently treated discharges. In the late 1980s estimated total N load
to Wilson Bay f r o m the Jacksonville discharge was
145,570 k g y r ] and estimated total P load was
54,380 kg yr ] (NCDEHNR 1990). In 1995 the City
of Jacksonville b e g a n construction of a new 6
million gallon per day (MGD) wastewater t r e a t m e n t
facility on 2,511 ha of land 15 km outside the
city, and effluent discharge was r e m o v e d f r o m
Wilson Bay in M a r c h 1998. T h e new facility
consists of primary settling and secondary aeration
in large lagoons, f r o m which chlorinated effluent is
sprayed alternatively over 8 zones each consisting of
104 h a of pine forest (Holder personal c o m m u n i cation).
T h e USMC previously o p e r a t e d 7 t r e a t m e n t
plants with a c o m b i n e d flow of 7.4 MGD. Plankton
samples collected in the estuary in 1994-1995
showed significantly higher abundances of nontoxic
Pfiesteria stages present at the sewage t r e a t m e n t
plant outfalls c o m p a r e d with control areas of no
outfalls (Burkholder and Glasgow 1997, Fig. 12).
These outfalls likely served as nutrient-rich reservoirs for potentially toxic h a r m f u l algae. In November 1998 the wastewater that previously flowed into
those plants was consolidated into a single new
15 MGD capacity p l a n t that features biological
n u t r i e n t removal. T h e discharge enters the estuary
n e a r Channel Marker 39 in Farnell Bay (Fig. 1).
T o t a l USMC N l o a d i n g has d e c r e a s e d f r o m
113,500 kg yr ] to 54,480 kg yr ] and total P has
decreased f r o m 18,160 k g y r ] to approximately
2,270 kg yr ] (Ashton personal c o m m u n i c a t i o n ) .
752
M . A . Mallin et al.
T h e objectives of this research were to spatiallyand temporally assess water quality- conditions in the
New River Estuary-, determine the nutrients most
limiting to phytoplankton production, and to assess
t h e effect o f the wastewater t r e a t m e n t p l a n t
upgrades on concentrations of nutrients, chlorophyll a (chl a), DO, a n d o t h e r water qualityparametm~ in both Wilson Bay- and the New River
Estuary- as a whole.
Methods
SAMPLINGAREA
Sampling was initiated in N o v e m b e r 1994 at
several stations and was continued at approximately
monthly intmwals. I n J u l y 1995 a swine waste lagoon
breached, p o u r i n g 1.43 • 107 1 of swine waste into
the New River, which reached the estuary- located
35 k m downstream of the spill (Burkholder et al.
1997). T h e h o g spill sent a large load of a m m o n i u m
and P into the u p p e r estuary-, and caused algal
blooms that persisted ~br 3 m o (Burkholder et al.
1997). To avoid potential skewing of the nutrient
and chl a data by this event we used (~br the pointsource comparison) only data collected b e g i n n i n g
with N o v e m b e r 1995, 6 m o after the spill a n d
after its water column and sediment effects had
passed (Burkholder et al. 1997). Eight stations have
b e e n routinely s a m p l e d since N o v e m b e r 1995
(Fig. 1).
T h e hydrology of the New River Estuary- lends
itself well to algal bloom ~brmation. This system
consists of a series of broad shallow lagoons linked
together by narrow channels (Fig. 1). Six of the
eight sampling stations were located at n u m b e r e d
channel markers (M52, M47, M39, M31, M18, and
M15). Wilson Bay (Station WB) ~eeds into Morgan
Bay (sampled at Station M47) through a channel
sampled at Station M52. Several tributaries including Southwest, Northeast, a n d Wallace Creeks,
draining Camp Lejeune and parts of Jacksonville
also ~eed into Morgan Bay-. Channel Marker 39
represents the region in Farnell Bay nearest the
previous and present treated sewage discharge fi-om
the main wastewater treatment plant on C a m p
Lejeune; this area also receives drainage fi-om
French's Creek. Downstream of Farnell Bay lies
Stones Bay (sampled at Station M31), part of which
previously (until March 1997) received drainage
fi-om a smaller sewage treatment plant located near
a rifle range. Station 172 lies in a narrow channel
separating Stones Bay fi-om C o m t h o u s e Bay and the
lower New River Estuary-. Courthouse Bay previously
(until July 1996) received inputs fi-om a small
sewage treatment plant. T h e lower portion of the
estuary- (Stations M18 and M15) is the best flushed
part of the system, as it adjoins the Atlantic
Intracoastal Waterway and receives some exchange
with the Atlantic O c e a n near Topsail Island (Fig. 1).
FIELD AND LABORATORYMETHODS
Sampling was conducted approximately monthly
fi-om N o v e m b e r 1995 through August 2002, during
ebb tide. Field parameters (water temperature, pH,
D O , turbidity, salinity-, a n d conductivity) were
m e a s u r e d at each site using a YSI 6920 Multiparameter Water Quality- Sonde linked to a YSI 610D
display- unit. YSI Model 85 and 55 D O meters were
also u s e d on occasion. T h e i n s m a m e n t s were
calibrated prior to each sampling trip to ensure
accurate measurements. T h e light attenuation coefficient k was determined fi-om data collected on
site using vertical profiles obtained by a Li-Cor LI1000 integrator interfaced with a Li-Cor LI-193S
spherical q u a n t u m sensor. When field conditions
indicated a potential algal b l o o m in progress
(elevated p H or supersaturated D O concentrations)
whole water samples were taken ~br qualitative
phytoplankton identifications, accomplished in the
laboratory- using an Olympus BX50 phase contrast
microscope. Potentially harmfill algal specimens
(primarily Pfiesteria-like mganisms) were sent to
Dr. J. M. Burkholder at N o r t h Carolina State
University- ~br identification using electron microscopy.
For nitrate + nitrite (hereafter referred to as
nitrate) and orthophosphate assessment, 3 replicate
acid-washed 125-ml bottles were placed c. 10 cm
below the surface, rinsed, filled, capped, and stored
on ice until processing. In the laboratory- the
triplicate samples were filtered simultaneously
t h r o u g h 25 m m G e l m a n A / E glass fiber filters
(nominal pore size 1.0 ~tm) using a mani~bld with
3 fimnels. T h e pooled filtrate was stored fi-ozen
until analysis. Nitrate and orthophosphate were
analyzed using Technicon and Bran and Luebbe
AutoAnalyzers ~bllowing U.S. EPA protocols. San,ples ~br a m m o n i u m were collected in duplicate,
presmwed with phenol in the field, stored on ice,
and analyzed in the laboratory- according to the
methods of Parsons et al. (1984). Triplicate samples
~br silicate (hereafter, Si) were collected on site, and
reactive Si was measured using the m e t h o d described in Parsons et al. (1984).
Chl a concentrations were determined fi-om the
filters used ~br filtering samples ~br nitrate and
orthophosphate analyses. All filters were wrapped
individually in a l u m i n u m ~bil, placed in an airtight
container with desiccant, and stored in a freezer.
During the analytical process the glass fiber filters
were separately i m m e r s e d in 10 ml of 90% acetone.
T h e acetone was allowed to extract the chlorophyll
fi-om the material ~br 18-24 h. T h e extracted
Reversal of Estuarine Eutrophication
material was analyzed for chl a concentration using
a Turner AU-10 fluorometer (Welschmeyer 1994).
753
August, September, and N o v e m b e r 1995; and
February, March, April, May-, and J u n e 1996.
NUTRIENT LIMITATIONBIOASSAYEXPERIMENTS
STATISTICALANALYSIS
We tested the hypothesis that N is the key limiting
nutrient in the New River EstualTf-. The basis of these
experiments was to add the suspected limiting
nutrient in excess to replicated estuarine water
samples and determine if the phytoplankton community- in the samples showed a positive response
(i.e., chlorophyll or carbon [C] uptake increase).
Other possible limiting nutrients (treatments) were
tested as well, with a replicated set of control
samples incubated to serve as a baseline. The
specific design was as follows: water was collected
at Station 172 in 25-1 carboys, returned to the
laboratoi% and dispensed into 4-1 cubitainers (3 1
per cubitainer). Nutrient treatments were added
as follows (expressed as final concentration): no
additions (controls), orthophosphate alone (100 ~tg
1 1 or 3.2~tM as P), nitrate alone (200~tgl ~ or
14.3 ~tM as N), combination (200 ~tg 1 a nitrate and
100 ~tg 1 1 o r t h o p h o s p h a t e ) , a n d silica a l o n e
(200 ~tg 1 a or 7.1 ~tM as Si). All treatments were
conducted in triplicate. After nutrient addition
a 10 ~tCi aliquot of 14C-NaHCOs was added to each
cubitainer to allow measurement of photosynthetic
a4C assimilation as an estimate of algal growth
(Rudek et al. 1991; Fisher et al. 1992).
Cubitainers were floated on circulating ponds at
the University- of North Carolina Wilmington at
ambient seawater temperatures. The cubitalners
were covered by 2 layers of neutral density- screening
to allow solar irradiance penetration of about 30%
of that reaching the water surface, to prevent
photostress to the phytoplankton (Mallin and Paerl
1992). The cubitalners were kept in motion by
constant circular agitation of the p o n d water using
a submerged bilge pump. The cubitalners were
sampled daily for 3 d for ~4C uptake as follows: a 50ml aliquot was filtered through Whatman 934 AH
glass fiber filters. Filters were fumed with hydrochloric acid vapors for 30 min to remove abiotically
precipitated a4C, dried, and treated with Ecolume
scintillation cocktail. Carbon uptake (a4C activity-)
was assayed on a Wallac LKB 1214 Rackbeta liquid
scintillation counter. The cubitainers were also
sampled daily for chl a content (50-ml samples
measured by the fluorometlTf- method of Parsons et
al. 1984) and analyzed as above.
To minimize bottle effects we restricted the
length of the bioassays to 3 d. This length of time
was chosen to be appropriate for m e a n i n g f u l
statistical comparisons based o n our previous
estuarine bioassay experiences. Nutrient limitation
bioassays were c o n d u c t e d d u r i n g August a n d
November 1994; February-, April, May-, June, July,
Statistical analysis of n u t r i e n t limitation test
results was performed using the Statistical Analysis
System (SAS) procedure of analysis of variance
(ANOVA). This test uses the means and standard
deviations of the response data (chlorophyll concentrations and 14C uptake) and determines if there
exists a significant difference (p < 0.05) between
the response means of the various nutrient treatments. We used the meal, responses for each
cubitalner over the 3-d tests for the analyses. If
a difference in response means exists among the
treatments, the ANOVA test is fbllowed by treatm e n t ranking by the least significant difference
(LSD) procedure (Day- and Q u i n n 1989).
We tested the hypothesis that there were no
significant differences in parameter concentrations
before and after sewage treatment upgrades for
individual upper and middle estuaiTf- stations and
for the New River Estuary- as a whole. To account for
seasonality in nutrient runoff and phytoplankton
productivity we compared data for Wilson Bay
collected between November 1995 and March
1998 to data collected between November 1998
and March 2002. For all other stations and the New
River Estuary- as awhole (the means of all 8 stations)
we compared data collected between November
1995 and October 1998 to data collected between
November 1998 and October 2002.
Before statistical analyses the data sets were tested
for normality- using the Shapiro-Wilk test. Water
temperature, salinity-, and DO data sets were
normally distributed; nutrients, chl a, turbidity-,
and hydrological vaiiables required log-transfbrmation before statistical analyses were performed.
Differences between parameters befbre and after
sewage treatment upgrades were tested using the
two-sample t-test with a significance level of p
0.05. Statistical analyses were performed using the
SAS (Schlotzhauer and Littell 1997).
To help ascertain the relationship among nutrient sources, hydrology, and estuarine responses we
perfbrmed correlation analyses among nutrient and
chl a concentrations, river discharge, and local
rainfall data. Correlations were performed using
individual stations and the combined New River
Estuary- stations. New River discharge data were
obtained from the U.S. Geological Sui~zey, Raleigh,
North Carolina, office website http://nc.water.usgs.
gov/. We tested both day-of:sampling discharge and
average discharge for the 7-d period preceding
sampling. Local rainfall data were obtained from
the USMC at Camp Lejeune, measured at a station
near Stones Bay (Fig. 1). We used total rainfall in
754
M . A . Mallin et al.
TABLE1. Nutrient and chlorophyll a concentrations (gg 1 ~) by station for the New RiverEstuary, 1995-2002,as mean (+ SD) and range.
Station
Ammonium
Wilson Bay
79.4 (134.1)
1.0-656.0
32.2 (60.6)
1.0-340.0
20.4 (38.5)
1.0-238.0
15.4 (32.0)
1.0-227.0
15.4 (30.7)
1.0-231.0
17.8 (33.5)
1.0-224.0
17.6 (31.7)
2.0-230.0
14.6 (27.2)
1.0-204.0
M52
M47
M39
M31
172
M18
M15
Nitzate
Or tlaophosphabe
171.6 (202.6)
1.0-701.0
46.5 (83.9)
1.0-403.0
22.4 (56.1)
1.0-300.0
10.0 (27.8)
1.0-161.0
5.5 (16.4)
1.0-128.0
5.0 (13.2)
1.0-100.0
4.4 (10.2)
1.0-73.0
4.1 (7.1)
1.0-43.0
the 24-h p e r i o d p r e c e d i n g sampling and total
rainfall in the 72-h p e r i o d p r e c e d i n g sampling fbr
the correlation analyses.
Results
WATER QUALITYPATTERNSIN THE NEW RIVER ESTUARY
N u t r i e n t and chl a concentrations were highest in
Wilson Bay- and decreased downstream in order of
M52, M47, M39, and M31 (Table 1). Sharp maxima
in a m m o n i u m and nitrate were evident in u p p e r
stations (Table 1), especially p r i o r to t r e a t m e n t
p l a n t upgrades (Fig. 2). Phytoplankton blooms
could be extremely dense, with chl a concentrations
exceeding 180 gg 1 1 at times in the u p p e r 3 stations
(Table 1, Fig. 2). Substantial algal blooms o c c u r r e d
as far downstream as M39 in Farnell Bay-. Qualitative
examinations of phytoplankton samples indicated
that the blooms primarily consisted of diatoms
(especially Thalassiosira spp., Nitzs&ia closterium,
and Skeletonema costatum), dinoflagellates (especially
Heterocapsa triquetra, Prorocentrum minimum, a n d
Katodinium rotundatum), and various cryptomonads.
During blooms of other taxa elevated numbers of
Pfaesteria spp. were periodically noted (during some
fish kills this estuary- had tested positive for both
toxic Pfiesteria piscicida and P. shumwayae; Glasgow et
al. 2001). P. minimum has displayed toxicity- to
finfish or shellfish elsewhere (Burkholder 1998),
but has not caused fish kills in the New River
Estuary-.
Bottom-water hypoxia was a p r o b l e m in the u p p e r
estuary- (Fig. 2). Long-term average surface DO
concentrations at stations WB, M52, M47, and M39
r a n g e d fi-om 8.9 to 9.2 mg 1 1. Long-term average
bottom DO concentrations at WB, M52, M47, and
M39 were 5.8, 6.7, 7.3 and 7.6 mg 1 1, respectively.
Over the course of the study we measured severe
hypoxia (defined as DO < 2.0 mg 1 1) in Wilson Bay-
47.0 (48.0)
1.5-321.0
22.1 (28.3)
1.0-127.0
14.4 (18.2)
1.0-87.9
9.0 (13.9)
1.0-73.2
6.5 (10.2)
1.0-81.0
6.2 (9.6)
1.0-79.0
5.7 (7.4)
1.0-59.0
5.3 (6.4)
1.0-51.0
Silicate
1829.2 (1015.6)
43.1-6538.8
1298.7 (814.1)
88.4-4181.2
1154.9 (767.8)
62.0-4192.7
993.7 (702.2)
18.5-3717.4
874.0 (693.6)
7.0-3662.5
729.1 (570.3)
30.8-2572.6
540.8 (475.1)
15.8-1980.1
388.2 (442.3)
5.3-2320.9
Qlalorophy]l a
40.8 (64.4)
1.0-379.3
25.1 (35.2)
1.0-189.4
16.9 (24.8)
1.0-193.1
12.9 (13.3)
1.9-73.0
7.3 (5.6)
1.4-32.0
5.6 (4.4)
1.0-24.8
4.1 (2.7)
1.0-13.4
3.3 (2.0)
1.0-10.1
bottom waters on 9 occasions. Severe hypoxia was
m e a s u r e d 5 times at M52 and 2 times each at M47
and M39; severe hypoxia was not e n c o u n t e r e d in
bottom waters fi-om M31 downstream to the estuarym o u t h at M15.
RESULTS OF NUTRIENT ADDITION
BIOASSAYEXPERIMENTS
Phytoplankton p r o d u c t i o n as 14C was stimulated
by additions of nitrate and the N + P combination
on 13 out of 15 e x p e r i m e n t s (Table 2). Chl
a p r o d u c t i o n also was stimulated on 14 out of 15
experiments. P alone was stimulatoi T only- in April
1995 and February- 1996, when inorganic N : P
ratios were well above 30. Si proved to be a limiting
n u t r i e n t in April 1995 just after a diatom bloom.
While Si c o n c e n t r a t i o n s averaged 650 ~tg 1 1 at
Station 172 t h r o u g h o u t the bioassay study, concentrations fell to undetectable levels in late April when
the bioassay was performed. T h e N : P ratios d u r i n g
most experiments were below the Redfleld ratio of
16, likely owing to the P c o n t r i b u t i o n s fi-om
wastewater discharges. N was the primax T n u t r i e n t
limiting phytoplankton p r o d u c t i o n in the New River
Estuary-, essentially year-round.
EFFECT OF SEWAGE TREATMENTUPGRADES
Wilso~ Bay
A m m o n i u m concentrations in Wilson Bay- decreased by 81% fbllowing sewage t r e a t m e n t upgrades, a highly significant decrease (p
0.0001).
Nitrate concentrations decreased 28%, which was
statistically nonsignificant (Fig. 2, TaMe 3). D u r i n g
this p e r i o d the average chl a biomass decreased
fi-om 76.7 to 20.9 ~tg 1 z, a highly significant decrease (Fig. 2, Table 3). O r t h o p h o s p h a t e concentrations showed a significant 49% decrease fbllowi n g sewage t r e a t m e n t i m p r o v e m e n t s (Fig. 2,
Reversal of Estuarine Eutrophication
800
400
+Before
T A B L E 2. R e s u l t s o f 1 9 9 4 - 1 9 9 6 n u t r i e n t a d d i t i o n b i o a s s a y
experiments
showing nutrient
treatments
y i e l d i n g ~4C a n d
c h l o r o p h y l l a r e s p o n s e s s i g n i f i c a n t l y (p < 0 . 0 5 ) g r e a t e r t h a n
control. Test water was from Station 172, New River Esmary. na
means not available.
e . . . A~er
200
y~ax
1994
1995
4OO
E
200
1O0
0
Cq
~
9 ~
755
9ra
1996
400
~1 200
MontJa
14C response
August
November
February
April
May
June
July
August
September
November
February
March
April
May
June
Clalorophyll
a response
N, N+P
N, N+P
N, N+P
N+P, Si
N, N+P
N, N+P
N, N+P
N, N+P
N, N+P
N, N+P
N, P, N+P
N, N+P
N, N+P
N, N+P
N, N+P
N, P, N+P, Si
N, N+P
N, N+P
N, N+P
N, N+P
N, N+P
N, N+P
N, P, N+P
N, N+P
N, N+P
N, N+P
N, N+P
Inorganic N : P
rno] ax ratio
na
na
9.3
49.7
49.6
9.5
1.8
7.6
18.1
2.2
37.2
5.3
8.5
4.7
1.5
8 ~00
80
g
e
o
16
2
0k..
~
~
-*.,,'~
.............
~
~'. . . . . . . . . . . . . . .
bOJF~I~MJJA~Ot,DJF~/~MJ,ASO'OJF~ANUJASONDJFM~J ,ASQ,~ F~MJ,A $ C N W ~
1996
1997
1998
1999
2000
:~. . . . . . . .
& ~
~
2001
2002
F i g . 2. C h a n g e s i n a m m o n i u m ,
nitrate, orthophosphate,
c h l o r o p h y l l a, l i g h t a t t e n u a t i o n , a n d b o t t o m d i s s o l v e d o x y g e n
b e f o r e a n d a f t e r s e w a g e t r e a t m e n t u p g r a d e s i n W i l s o n Bay.
Table 3). Average bottom water DO concentrations
increased 0.9 mg 1 1 (not statistically significant due
to high variability). Befbre the upgrades severe
bottom-water hypoxia was measured on 4 of 27
occasions; severe hypoxia still occurred after sewage
upgrades, but at a slightly lesser fi-equency, with 5
out of 45 measurements yielding DO less than
2.0 mg 1 1. The sewage treatment improvements
improved water clarity, as light attenuation showed
a significant decrease of 27% and turbidity showed
a significant decrease of 41% (Fig. 2, Table 3).
Some of the turbidity in Wilson Bay-was likely due to
phytoplankton biomass, as there was a positive (r
0.334, p
0.017) correlation between turbidity and
chl a.
Station M52
Station M52, located where the narrow channel
into Wilson Bay- opens into the estuary- proper
(Fig. 1), showed slight but nonsignificant decreases
in a m m o n i u m and nitrate, but statistically significant decreases in orthophosphate (average of 26.318.3 g g P 1 1), chl a (42.8-10.1 g g 1 1), l i g h t
attenuation coefficient k (2.3-1.7 m 1), and turbidity (11.2-6.1 NTU). There also was a statistically
significant increase in average bottom water DO
concentration (6.0-7.4 mg 1 1). Due to its location
this station would be affected by improvements in
b o t h the Jacksonville and USMC wastewater treatm e n t systems.
Mainstem Estuary Stations
Station M47 in Morgan Bay- showed highly
significant (p
0.0001) decreases in average chl
a (27.8-8.2 gg 1 1) and turbidity (8.1-4.7 NTU), but
changes in nutrient concentrations were not statistically significant. There was an increase in average
b o t t o m water DO c o n c e n t r a t i o n fi-om 7.1 to
7.7 mg 1 1 at this site, a l t h o u g h this was n o t
statistically significant. Stations located fbrther
downstream did not show decreases in nutrient
concentrations or increases in average bottom water
DO concentrations. Highly- significant (p
0.0001)
decreases in chl a occurred at stations M39 and
M31, and turbidity showed a significant (p
0.02)
decrease at M39.
New River Estuary as a Whole
An, m o n i u m concentrations fbr the entire estuary(means of 8 stations) decreased approximately- 41%
fbllowing sewage treatment upgrades (nonsignificant, Fig. 3, Table 4). Nitrate decreased on average
26% and orthophosphate decreased just slightly,
about 21% (both nonsignificant). These reductions
in nutrients translated to an approximate 69%,
756
M . A . Mallin et al.
TABLE 3. Changes in Wilson Bay water quality--pre versus post sewage treatment upgrades, November 1995-March 1998 versus
November 1998-March ~00~, as mean ( + SD). Nutrient and chlorophyll a data as btg 1 ~, turbidity as NTU, dissolved oxygen data as mg 1
light attenuation as k ~. * Indicates significant (p < 0.05) change; ** indicates highly significant (p < 0.01) change.
pazamemr
Ammonium
Nitrate
Orthophosphate
Turbidity
Chlorophyll a
Bottom dissolved oxygen
Light attenuation
]De-upgrades
168.4
~35.8
67.~
15.0
76.7
5.5
3.3
0995
1998)
Post upgrades
(187.8)
(~33.0)
(64.4)
(8.3)
(94.3)
(3.0)
(1.0)
h i g h l y s i g n i f i c a n t (p
0.0001) d e c r e a s e in chl
a (Fig. 3). T u r b i d i t y s h o w e d a n e s t u a r y - w i d e
s i g n i f i c a n t d e c r e a s e as well, a n d a v e r a g e b o t t o m
water DO showed a nonsignificant increase of
0.2 m g 1 ~ ( T a b l e 4). F o l l o w i n g t h e 1998 sewage
t r e a t m e n t i m p r o v e m e n t s t h e N o r t h C a r o l i n a Division o f M a r i n e Fisheries was a b l e to r e o p e n 122 h a
o f s h e l l f i s h i n g waters p r e v i o u s l y c l o s e d d u e to
e l e v a t e d fecal c o l i f b r m b a c t e r i a l o a d i n g .
3~.0
170.9
34.5
8.9
18.8
6.4
~.4
% change
(36.1)
(185.8)
(3~.4)
(4.5)
(14.8)
(3.3)
(0.7)
81%**
~8%
49%**
41%**
75%**
+16%
~7%**
t i o n b e t w e e n local rainfall a n d o r t h o p h o s p h a t e , b u t
n o t N variables ( T a b l e 7).
Discussion
Decomposing phytoplankton can be an import a n t s o u r c e o f B O D in coastal w a t e r b o d i e s p r o n e to
algal b l o o m s (NRC 1 9 9 3 ) . I n a n u m b e r o f lakes,
rivers, a n d estuaries in N o r t h C a r o l i n a ( M a l l i n et al.
2005) and elsewhere (Heiskary and Markus 2001)
HYDROLOGICAL FORCING AND NUTRIENT SOURCES
W h e r e a s a m m o n i u m a n d o r t h o p h o s p h a t e dec r e a s e d c o n s i d e r a b l y in W i l s o n Bay- a n d various
stations in t h e u p p e r N e w River Estuary-, n i t r a t e
d e c r e a s e d o n l y slightly o r n o t at all. W e p e r f o r m e d
c o r r e l a t i o n analyses to h e l p assess n u t r i e n t sources
t h a t may- b e a s s o c i a t e d w i t h h y d r o l o g i c a l variables
(i.e., r i v e r d i s c h a r g e a n d l o c a l rain~M1). M o s t
n u t r i e n t variables t e s t e d w e r e positively c o r r e l a t e d
with river d i s c h a r g e a n d n e g a t i v e l y c o r r e l a t e d with
salinity- in W i l s o n Bay- a n d M 5 2 ( T a b l e 5). N i t r a t e
s h o w e d a p a r t i c u l a r l y s t r o n g c o r r e l a t i o n with river
d i s c h a r g e . T h i s i n d i c a t e s t h a t u p s t r e a m sources play
a n i m p o r t a n t post-sewage t r e a t m e n t u p g r a d e r o l e in
n u t r i e n t delivery to t h e estuary. T h e r e was a w e a k
inverse c o r r e l a t i o n b e t w e e n r i v e r d i s c h a r g e a n d chl
a, i n d i c a t i n g t h a t h i g h flow (river-like o r lotic)
physical c o n d i t i o n s are n o t immediately- c o n d u c i v e
to p h y t o p l a n k t o n b l o o m ~bm~ation. L o c a l rainfall,
m e a s u r e d n e a r S t o n e ' s Bay- (Fig. 1), was weakly
c o r r e l a t e d with n i t r a t e at M52 a n d weakly c o r r e l a t e d
with o r t h o p h o s p h a t e at b o t h u p p e r stations, ind i c a t i n g t h a t l o c a l i z e d ~nanoff is p r o b a b l y a m i n o r
n u t r i e n t s o u r c e to t h e u p p e r estuary- ( T a b l e 5).
T h e M o r g a n Bay- a n d F a r n e l l Bay- stations ( M 4 7
and M39) generally showed strong correlations
between river discharge and nitrate but much
w e a k e r c o r r e l a t i o n s with a m m o n i u m a n d n o n e with
Si ( T a b l e 6). L o c a l rainfM1 was weakly c o r r e l a t e d
with o r t h o p h o s p h a t e c o n c e n t r a t i o n s at M 4 7 a n d
M 3 9 as well. T h r o u g h o u t t h e estuary t h e r e w e r e
s t r o n g c o r r e l a t i o n s b e t w e e n river d i s c h a r g e a n d
nitrate and weaker correlations between river
discharge and ammonium
and orthophosphate
( T a b l e 7). T h e r e was also a n estuary-wide correla-
(1998~2002)
25O
g
aoo~
~
z
150t
~
o
:
1~176
I
Before
:~
9 o. 9 A~er
ca
100
D-
60
f
80
a:
O
2
40
3O
~
*0
co o~a%9
00 $
~Dj r M ~ ~Ag0N00 ~,l~a J JASONDJ r ~
1996
1997
J J~ SO.C J ~
1998
0oo8o0 o 6 c~ce
J JA SO~0J ~
1999
%.~ao
,4%ooa~
J J ~ SOlD J ~AU J J~ ~ m ~ ~.l~a J JAS
2000
2001
2002
Fig. B. Changes in ammonium, nitrate, orthophosphate,
chlorophyll a, and light attenuation before and after sewage
treatment upgrades in the New River Estuary, means of eight
stations.
Reversal of Estuarine Eutrophication
757
TABLE 4. Changes in New River Esmary water quality (means of eight stations)--pre versus post sewage treatment upgrades, November
1995-October 1998 versus November 1998-October 2002, as mean (+ SD). Nutrient and chlorophyll a data as btg 1 ~, mrbidity as NTU,
dissolved oxygen data as mg 1 ~, and light attenuation data as k m ~. * Indicates significant (p < 0.05) change; ** indicates highly
significant (p < 0.01) change. DIN dissolved inorganic nitrogen; DIP dissolved inorganic phosphorus.
pazamemr
]De-upgrades (1995 1998)
Ammonium
Nitrate
Orthophosphate
Tm'bidity
DIN : DIP
34.3
39.2
16.4
10.3
12.6
5.7
23.4
7.3
1.8
Chlorophyll a
Bottom dissolved oxygen
Light attenuation
Postupgrades (1998 2002)
(47.2)
(49.8)
(12.7)
(5.5)
mean
median
(16.4)
(1.9)
(0.6)
c h l a h a s b e e n s t r o n g l y c o r r e l a t e d w i t h B O D . If we
c o n v e r t p h y t o p l a n k t o n c h l a b i o m a s s to p h y t o p l a n k ton carbon biomass using a rough conversion factor
o f 50 ( R i e m a n n et al. 1 9 8 9 ) , we s e e a n a v e r a g e
d e c r e a s e i n W i l s o n Bay- p h y t o p l a n k t o n C fl-om 3 . 8 3 5
to 1.045 m g C 1 1, o r a n a p p r o x i m a t e 7 3 % d e c r e a s e
in labile phytoplankton
C t h a t was p r e v i o u s l y
a v a i l a b l e as a s o u r c e o f B O D . T h e a m o u n t o f B O D
demanding material decreased considerably, contributing toward the increase in bottom water DO
(Fig. 2, T a b l e 3). M a x i m a l i m p r o v e m e n t may- t a k e
t i m e , b e c a u s e t h e o r g a n i c r e s i d u e t - o r e years o f
major algal blooms may contribute toward sediment
o x y g e n d e m a n d i n W i l s o n Bay-.
A n i m p o r t a n t secondary- r e s u l t o f t h e s e w a g e
treatment
upgrades
was the improvement
in
w a t e r clarity. S i g n i f i c a n t d e c r e a s e s i n t u r b i d i t y
and light attenuation were realized in the upper
e s t u a r y a n d t h e r e was a 2 2 % d e c r e a s e i n t h e
a v e r a g e l i g h t a t t e n u a t i o n c o e f f i c i e n t estuary-wide.
20.4
29.1
13.0
7.1
14.5
7.5
7.3
7.5
1.4
(28.8)
(35.8)
(15.1)
(2.6)
mean
median
(3.4)
(1.9)
(0.3)
% change
41%
26%
21%
31%**
+15%
+32%
69%*
+3%
22%
This should allow for improved submersed aquatic v e g e t a t i o n
(SAV) habitat, and the estuary
w o u l d b e n e f i t f r o m f u t u r e r e s t o r a t i o n efforts in
the form of SAV plantings. Since high light and low
nitrate conditions are required for SAV habitat,
r e s t o r a t i o n efforts may- o n l y b e f e a s i b l e i n t h e l o w e r
estuary-.
P h y t o p l a n k t o n b l o o m s d o c o n t i n u e to o c c u r in
t h e N e w R i v e r E s t u a r y a l t h o u g h w i t h m u c h less
f l - e q u e n c y a n d m a g n i t u d e t h a n i n years b e f o r e t h e
u p g r a d i n g o f s e w a g e t r e a t m e n t (Fig. 3). A v e r a g e
b o t t o m w a t e r D O c o n c e n t r a t i o n s h a v e i n c r e a s e d in
upper estuary stations and bottom-water maximal
DO concentrations
h a v e i n c r e a s e d as well, b u t
p e r i o d s o f s e v e r e b o t t o m w a t e r h y p o x i a still o c c u r
at t i m e s (Fig. 2) i n d i c a t i n g t h a t m o r e i m p r o v e m e n t
e f f o r t s a r e n e e d e d . P u l s e s o f n i t r a t e c o n t i n u e to
o c c u r i n W i l s o n Bay a n d s o m e o f t h e o t h e r u p p e r
estuary- s t a t i o n s (Figs. 2 a n d 3). N i t r a t e , a n d to
a lesser extent ammonium and orthophosphate, are
TABLE 5. Correlation coefficients between hydrological variables and nutrients for upper New River Estuary stations, 1998-2002. Flowday
river discharge on day of sample collection; Flow7 mean fiver discharge for week preceding sample collection; Rainday total rainfall
in 24-h period preceding sample day; and Rain3d total rainfall in 72-h period preceding sample day.
pazamemrs
Salinity
l~owday
l~ow7
0.371
0.0080
0.701
0.0001
0.324
0.0204
0.357
0.0009
0.688
0.0001
0.347
0.0127
0.357
0.0109
0.420
0.0050
0.649
0.0001
0.440
0.0032
0.616
0.0001
0.318
0.0356
Ralnday
Ralngd
Wilson Bay
Aininoniuin
Nitrate
Phosphate
Silicate
0.636
0.0001
0.386
0.0052
0.433
0.0017
0.334
0.0165
M52
AIilIi~oniuIn
Nitrate
Phosphate
Silicate
0.678
0.0001
0.411
0.0056
0.508
0.0005
0.298
0.0490
0.319
0.0349
758
M . A . Mallin et al.
TABLE 6. Correlation coefficients between hydrological variables and nutrients for mid to upper New River Estuary stations, 1998-2002.
Flowday river discharge on day of sample collection;Flow7
mean river discharge for weekpreceding sample collection; Rainday total
rainfall in 24-h period preceding sample day; and Rain3d total rainfall in 72-h period preceding sample day.
parameters
M47
Ammonium
Nitrate
Phosphate
Silicate
Sa/inlty
0.320
0.0360
0.505
0.0005
0.425
0.0040
0.443
0.0030
Iqowday
Iqow7
0.547
0.0001
0.416
0.0050
0.584
0.0001
0.327
0.0300
0.302
0.0464
0.371
0.0144
0.611
0.0001
0.299
0.0487
0.317
0.0361
M39
Ammonium
Nitrate
Phosphate
0.476
0.0011
0.311
0.0400
0.425
0.0040
significantly- c o r r e l a t e d with river d i s c h a r g e . I n p u t s
fi-om t h e u p p e r w a t e r s h e d appeal- to b e t h e c a u s e o f
t h e n u t r i e n t pulses t h a t o c c u r in t h e p o s t s e w a g e
t r e a t m e n t u p g r a d e p e r i o d . S t o r m w a t e r i x m o f f fi-om
t h e i m m e d i a t e vicinity- o f t h e estuary- a p p e a r s to b e
a minor source of nutrients.
Before the upgrades the median inorganic N : P
ratio was well b e l o w t h e R e d f l e l d ratio o f 16 a n d t h e
m e a l , N : P ratio was s o m e w h a t b e l o w it. N : P ratios
well b e l o w 16 are g e n e r a l l y c o n s i d e r e d i n d i c a t i v e o f
N l i m i t a t i o n o f p h y t o p l a n k t o n growth. O u r experim e n t s ( T a b l e 2) i n d i c a t e d t h a t t h e N R E was strongly
N l i m i t e d b e f b r e wastewater t r e a t m e n t u p g r a d e s .
T h e p r e s e n t N : P ratios ( T a b l e 4) a r e s i m i l a r to
t h o s e b e f o r e sewage u p g r a d e s , so t h e system is still
N l i m i t e d , m e a n i n g N i n p u t s are likely to s t i m u l a t e
p h y t o p l a n k t o n growth. S i n c e r i v e r d i s c h a r g e at
p r e s e n t a p p e a r s to b e t h e p r i n c i p a l s o u r c e o f n i t r a t e
( T a b l e s 5, 6, a n d 7), we c o n c l u d e t h a t n i t r a t e p u l s e s
fi-om u p p e r w a t e r s h e d n o n p o i n t sources are likely
d r i v i n g t h e p r e s e n t algal b l o o m s . A n a n a l o g o u s
s i t u a t i o n o c c u r r e d in T a m p a Bay-, Florida, w h e r e t h e
w e l l - d o c u m e n t e d e s t u a r i n e i m p r o v e m e n t s , s u c h as
R~inday
R~ingd
algal b l o o m d e c r e a s e s a n d seagrass c o v e r increases,
w e r e r e v e r s e d f b r a p e r i o d in t h e late 1990s as
a result of increased nonpoint source N inputs
d u r i n g a p r o l o n g e d wet p e r i o d ( ] o h a n s s o n a n d
Greening 2000).
T o c o n t i n u e w a t e r quality- i m p r o v e m e n t s in t h e
N e w River it w o u l d b e p l x l d e n t to c o n c e n t r a t e o n
n o n p o i n t s o u r c e n u t r i e n t r e d u c t i o n , p a r t i c u l a r l y in
t h e u p p e r w a t e r s h e d . A m a j o r l a n d use in t h e u p p e r
N e w R i v e r w a t e r s h e d is i n d u s t r i a l i z e d l i v e s t o c k
p r o d u c t i o n , w i t h 138 r e g i s t e r e d C A F O s i n t h e
c a t c h m e n t (Fig. 1). T h e s e facilities c a n c o n t r i b u t e
n u t r i e n t i n p u t s to n e a r b y streams t h r o u g h l a g o o n
l e a k a g e , spraylield, ixmoff a n d s u b s u r f a c e d r a i n a g e ,
a c c i d e n t s , a n d illegal d i s c h a r g e s ( B u r k h o l d e r et al.
1997; M a l l i n 2 0 0 0 ) , a n d call c o n t r i b u t e a i r b o r n e
ammonium
to w a t e r b o d i e s as f a r as 80 k m
d o w n w i n d ( W a l k e r et al. 2 0 0 0 ) . Tactics t h a t c o u l d
r e d u c e n u t r i e n t e x p o r t fi-om t h e s e facilities i n c l u d e
installation of mixed-vegetation buffer zones along
a d j o i n i n g s t r e a m b e d s , constlxlction o f e n g i n e e r e d
w e t l a n d s to e n h a n c e d e n i t r i f i c a t i o n , a n d u s e o f
w a s t e w a t e r t r e a t m e n t systems to r e m o v e n u t r i e n t s
TABLE 7. Correlation coefficients between hydrological variables and nutrients for means of 8 New River Estuary stations, 1998-2002.
Flowday river discharge on day of sample collection;Flow7
mean river discharge for weekpreceding sample collection; Rainday total
rainfall in 24-h period preceding sample day; and Rain3d total rainfall in 72-h period preceding sample day.
parameters
Ammonium
Niu'ate
Phosphate
Silicate
Salinity
]~owday
]~ow7
0.264
0.0001
0.552
0.0001
0.501
0.0001
0.614
0.0001
0.316
0.0001
0.396
0.0008
0.137
0.0092
0.372
0.0001
0.459
0.0001
0.199
0.0001
R~Snday
R~Sngd
0.125
0.0130
0.117
0.0270
0.136
0.0104
0.204
0.0001
0.188
0.0001
Reversal of Estuarine Eutrophication
(i.e., biological nutrient removal). Since this estuaryis o n l y s l o w l y f l u s h e d a n d s u b j e c t t o s t r a t i f i c a t i o n
and potential
bottom
water hypoxia,
continued
efforts to reduce
nutrient
inputs
are especially
critical.
ACKNOWLEDGMENTS
F o r f u n d i n g we t h a n k the following sources: the University of
N o r t h Carolina Water Resources Research Institute (Project
#70136), the Center for Applied Aquatic Ecology at N o r t h
Carolina State University, the University of N o r t h Carolina at
Wilmington, a n d the U.S. Marine Coq)s at Camp Lejeune. For
facilitation we t h a n k Mr. Brynn Ashton, Mr. Scott Brewer, Dr.
J o A n n Burkholder, Dr. Lawrence Cahoon, Ms. Marian McPhaul,
Dr. James Merritt, a n d Mr. Rick Shiver. For field a n d laboratory
assistance we t h a n k Scott Ensign, Tara MacPher~on, Christian
Preziosi, Chris Shank, Ashley Skeen, and Ellen W a m b a c h a n d for
data analysis help we t h a n k Maverick Raber a n d Lisa Thatcher.
We t h a n k Holly Greening a n d two anonymous reviewers for
helpful manuscript comments.
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Received, February 18, 2005
Revised, rune 7, 2005
Accepted, rune 28, 2005