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Controlling harmful cyanobacterial blooms ina hyper-eutrophic lake (Lake Taihu, China): The needfor a dual nutrient (N & P) management strategy
Hans W. Paerl a,*, Hai Xu b, Mark J. McCarthy c,d, Guangwei Zhu b, Boqiang Qin b,Yiping Li e, Wayne S. Gardner d
aUniversity of North Carolina at Chapel Hill, Institute of Marine Sciences, 3431 Arendell Street, Morehead City, NC 28557, USAb State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences,
73 East Beijing Road, Nanjing 210008, PR ChinacUniversite du Quebec a Montreal, Departement des sciences biologiques, Montreal, Quebec H3C 3P8, CanadadUniversity of Texas at Austin, Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, USAeDepartment of Environmental Science and Engineering, Hohai University, 1 Xikan Road, Nanjing 210098, PR China
a r t i c l e i n f o
Article history:
Received 16 February 2010
Received in revised form
26 August 2010
Accepted 14 September 2010
Available online 29 September 2010
Keywords:
Eutrophication
Nitrogen
Phosphorus
Cyanobacteria
China
Nutrient management
a b s t r a c t
Harmful cyanobacterial blooms, reflecting advanced eutrophication, are spreading globally
and threaten the sustainability of freshwater ecosystems. Increasingly, non-nitrogen (N2)-
fixing cyanobacteria (e.g.,Microcystis) dominate such blooms, indicating that both excessive
nitrogen (N) and phosphorus (P) loads may be responsible for their proliferation. Tradi-
tionally, watershed nutrient management efforts to control these blooms have focused on
reducing P inputs. However, N loading has increased dramatically in many watersheds,
promoting blooms of non-N2 fixers, and altering lake nutrient budgets and cycling char-
acteristics. We examined this proliferating water quality problem in Lake Taihu, China’s
3rd largest freshwater lake. This shallow, hyper-eutrophic lake has changed from bloom-
free to bloom-plagued conditions over the past 3 decades. Toxic Microcystis spp. blooms
threaten the use of the lake for drinking water, fisheries and recreational purposes.
Nutrient addition bioassays indicated that the lake shifts from P limitation in wintere
spring to N limitation in cyanobacteria-dominated summer and fall months. Combined N
and P additions led to maximum stimulation of growth. Despite summer N limitation and P
availability, non-N2 fixing blooms prevailed. Nitrogen cycling studies, combined with N
input estimates, indicate that Microcystis thrives on both newly supplied and previously-
loaded N sources to maintain its dominance. Denitrification did not relieve the lake of
excessive N inputs. Results point to the need to reduce both N and P inputs for long-term
eutrophication and cyanobacterial bloom control in this hyper-eutrophic system.
ª 2010 Elsevier Ltd. All rights reserved.
1. Introduction
Harmful (toxic, food web-disrupting) cyanobacterial blooms
(CyanoHABs) are a troubling indicator of advanced
eutrophication. These blooms are increasing worldwide and
represent a serious threat to drinking water supplies, and the
ecological and economic sustainability of our largest fresh-
water ecosystems (Reynolds, 1987; Paerl, 1988; Carmichael,
* Corresponding author. Tel.: þ1 252 726 6841; fax: þ1 252 726 2426.E-mail address: [email protected] (H.W. Paerl).
Avai lab le a t www.sc iencedi rec t .com
journa l homepage : www.e lsev ie r . com/ loca te /wat res
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3
0043-1354/$ e see front matter ª 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.watres.2010.09.018
Author's personal copy
2001; Huisman et al., 2005). Examples include Lake Erie (North
America), LakeWinnipeg, Canada, Lake Victoria, the largest of
the African rift lakes, Lakes Biwa and Kasimagaura, Japan’s
largest lakes, and Lake Taihu, the 3rd largest freshwater lake
in China. Anthropogenic nutrient over-enrichment of these
and smaller lakes and reservoirs has been linked to CyanoHAB
proliferation (Paerl et al., 2001; Huisman et al., 2005). Nitrogen
(N) and phosphorus (P) are the key nutrients of concern
(Likens, 1972; Schindler, 1977; Paerl, 2008). Inputs of both
nutrients to natural waters have increased dramatically in the
post-World War II era. A central question facing water
researchers and managers is; which nutrient(s) control Cya-
noHAB production and proliferation in impacted systems?
The answer to this question is of immense ecological and
economic importance, because it dictates the strategies and
costs involved in mitigating this serious water quality
problem.
Phosphorus has been implicated traditionally as having
a central role in the control of freshwater primary production
(Likens, 1972) and CyanoHAB bloom formation (Paerl, 1988,
2008). This conclusion is particularly relevant to nitrogen
(N2) fixing CyanoHABs, since they may satisfy their own N
requirements (Smith, 1983, 1990). As a result, P input restric-
tions have been implemented widely since the 1960s. These
reductions have slowed eutrophication rates and reduced
algal bloom potentials (Schindler, 1977). However, nutrient
loading dynamics have changed considerably since the 1960s.
Agricultural, urban and industrial nutrient sources have
accelerated rapidly (Vitousek et al., 1997; Galloway and
Cowling, 2002). These sources are treated more effectively
for removal of P than N before being discharged, leading to
higher N than P loading to already nutrient-stressed water
bodies (Paerl, 1997; Rabalais, 2002; Boyer et al., 2004). Excessive
N loads have promoted non-N2 fixing CyanoHABs, including
expanding blooms of the toxin producing, colonial, surface-
dwelling (buoyant) cyanoHABMicrocystis, and the filamentous
genera Lyngbya (non-N2 fixing strains) and Oscillatoria (Paerl,
2008, 2009).
A severely impacted large lake system is Taihu (meaning
“great lake” in Mandarin), with an area of 2338 km2 and
a volume of 4.4 billion m3 (Pu and Yan, 1998; Qin et al., 2007,
2010). This shallow (mean depth 1.9 m) polymictic lake is
located in the Yangtze River delta; themost rapidly developing
region in China (Fig. 1). Approximately 40 million people live
within the Taihu watershed. The Taihu Basin accounts for
only 0.4% of China’s land area, but the region accounts for 11%
of its Gross Domestic Product (Qin et al., 2007). The lake is
a key drinking water, fishing and tourism resource for the
region. However, it also serves as a waste repository for urban,
agricultural and industrial segments of the local economy
(Guo, 2007; Qin et al., 2007). Consequently, Taihu has experi-
enced accelerating eutrophication over the past 3 decades
(Qin et al., 2007, 2010). During this period, it has changed from
a mesotrophic, diatom-dominated lake to hyper-eutrophic,
cyanobacteria-dominated system, with Microcystis blooms
now occurring regularly throughout much of the lake (Chen
et al., 2003a,b) (Fig. 1). These blooms have caused environ-
mental, economic and societal problems, including a threat to
potable water supplies for approximately 10 million
consumers (Guo, 2007).
Microcystis and other non-N-fixing cyanobacteria are
effective competitors for reduced N forms, especially ammo-
nium (NH4þ) (Kappers, 1980; Blomqvist et al., 1994), which is
rapidly regenerated in the water column and sediments of
these shallow systems. Cyanobacteria capable of N2 fixation
can also assimilate NH4þ when available. For example, Shel-
burne Pond in Vermont was dominated by N2 fixers, but
characterized by low rates of N fixation (<9% of total N uptake)
and NOx uptake (<5%), but high acquisition rates of NH4þ
(82e98%) in summer (Ferber et al., 2004). Thus, the presence of
N2 fixers does not ensure that N2 fixation is a significant N
source; regenerated NH4þ may be a key N source for sustaining
blooms, even among N2 fixing groups.
Although Microcystis blooms dominate, heterocystous,
filamentous genera capable of N2 fixation (Anabaena, Aphani-
zomenon) are also present in the water column and as over-
wintering cells in the sediments of Taihu. The N2 fixing genera
increase in numeric importance toward the lake center, i.e.,
away from shoreline locations, although they remain sub-
dominant toMicrocystis (Chen et al., 2003a,b).While N2 fixation
rates have not been measured in the lake, these observations
Fig. 1 e Upper: Satellite (MODIS) image of Lake Taihu, the
nearby cities of Wuxi (N), Souzhou (E), and Shanghai (E),
near the mouth of the Yangtze River on 7 June, 2007, when
a massive cyanobacterial (Microcystis spp.) bloom that
covered almost the entire lake (image courtesy NASA).
Lower: Photograph of a Microcystis bloom on the north side
of the lake on 24 October, 2009 (photograph by H. Paerl).
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 31974
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suggest that N2 fixing conditions may increase from the lake’s
shorelines to its open waters, as hypothesized by McCarthy
et al. (2007). These observations also suggest that nutrient
availability and limitations may vary spatially in the lake.
Temporal differences may also be important because water-
shed N and P inputs exhibit seasonal patterns (Qin et al., 2007,
2010; Xu et al., 2010).
The fact that both N2 fixing and non-N2 fixing cyanoHABs
coexist in hyper-eutrophic Taihu has raised questions as to
whether N, P or both N and P inputs should be reduced to
control blooms. Based on research in other lakes, primary
production and bloom formation may be controlled by both N
and P inputs, either contemporaneously or sequentially, with
different individual nutrients being limiting at different times
of the year (Dodds et al., 1989; Elser et al., 2007; Havens et al.,
2001; Kronvang et al., 2005; Jeppesen et al., 2007; North et al.,
2007; Lewis and Wurtsbaugh, 2008; Ozkan et al., 2009; Xu
et al., 2010). These findings have been challenged recently,
based on the premise that lake eutrophication cannot be
controlled by reducing N inputs (Schindler et al., 2008). This
conclusion relies on the observation that many systems
exhibiting advanced eutrophication also contain significant
N2 fixing cyanoHAB populations, and the assumption that N
fixed by these populations can meet ecosystem N require-
ments. However, diverse studies show that only a fraction,
usually far less than 50% of ecosystem-level N demands, is
met by N2 fixation (Howarth et al., 1988; Paerl, 1990; Lewis and
Wurtsbaugh, 2008). In fact, a recent re-examination of
Schindler et al.’s (2008) data on P-fertilized Lake 227 indicates
that N2 fixation does not meet ecosystem N demands (Scott
and McCarthy, 2010). In other cases, N2 fixation rates are
very low and supply little new N, even when N fixing cyano-
bacteria are dominant (Ferber et al., 2004). Furthermore,
factors in addition to stoichiometric N:P ratios (Smith, 1983,
1990) control this energy-demanding process in aquatic
ecosystems (Howarth et al., 1988; Paerl, 1990; Forbes et al.,
2008). Reversing eutrophication and reducing CyanoHABs in
a range of lakes have required either reduction of only P
(Schindler, 1977) or both N and P inputs (Kronvang et al., 2005;
Jeppesen et al., 2007). Hence, nutrient reduction strategies
appear system-specific.
We examined effects of individual and combined N and P
additions on phytoplankton growth (based on chlorophyll
a concentrations) in Taihu, using short-term (up to 6 days)
nutrient addition bioassays incubated under natural light and
temperature conditions. These bioassays provide a rapid
assessment of nutrient limitation characteristics, i.e., imme-
diate growth responses, rather than predicting long-term
phytoplankton succession patterns (Paerl and Bowles, 1987;
Piehler et al., 2009). We also evaluated NH4þ regeneration and
potential uptake rates within the context of dominance by
non-N2 fixing cyanoHABs.
2. Methods and materials
2.1. Location and field sites
Lake Taihu is located approximately 150 kmwest of Shanghai;
with the lake center coordinates at 31�100000N, 120�90000E. The
Taihu drainage basin is 36,500 km2 (Fig. 2). The lake has more
than 30 input sources, ranging from rivers to small streams
andman-made drainage canals. Water exits the southeastern
corner of Lake Taihu via the Taipu River, which drains through
Shanghai into the East China Sea (Figs. 1 and 2).
Field monitoring and bioassay water collection sites were
located in one of the northern bays, Meiliang Bay (Inner Bay,
Outer Bay), and the lake proper (Main Lake) (Fig. 2). Other lake
sites sampled included the least bloom-impacted eastern
regions of the lake (ELT stations) (Fig. 2). Meiliang Bay was
chosen as a focal point because it is the site of recurring and
intensifying Microcystis spp. blooms (Chen et al., 2003a,b; Qin
et al., 2007). Meiliang Bay receives freshwater inputs from
the Liangxi and Zhihu Gang rivers, which drain untreated
wastewater from factories, residential and agricultural areas.
The named rivers in Fig. 2 contribute more than 85% of the
lake’s freshwater inflow.
2.2. Nutrient inputs to Lake Taihu
Data were obtained from the Taihu Basin Authority, Ministry
of Water Resources, China, for 30 primary tributaries from
2000 to 2005, includingmonthly flow discharge and TN and TP
concentrations, to estimate N and P loads discharged to the
lake (Fig. 2). These tributaries with 30 monitoring stations
accounted for approximately 85% of the total runoff input to
the lake (Qin et al., 2007). TN or TP load for each month was
calculated by the following formula:
Fi ¼ 2:592$X30
j¼1
Cij$Qij (1)
where Fi is TN or TP load for ithmonth (i¼ 1e12) inmetric tons,
Cijis the TN or TP concentration for ithmonth and jth tributary
( j¼1e30) inmg/L.Qij is theflowdischarge for ithmonthand jth
tributary ( j¼1e30) inm3/s. 2.592 is the factor for convertingg/s
to ton/mo. Spring, summer, autumn and winter in this paper
represent MarcheMay, JuneeAugust, SeptembereNovember,
and DecembereFebruary, respectively.
We estimated historic changes in atmospheric N loads to
the lake based on data derived from regional atmospheric
deposition models (Lelieveld and Dentener, 2000) and direct
measurements (Zhai et al., 2009).
2.3. Lake environmental measurements
Monthly samples for nutrients, chlorophyll a, and phyto-
plankton identification and enumeration were collected at the
Meiliang Bay and Main Lake locations (Fig. 2). Water samples
for nutrient addition bioassays were collected at the Inner Bay
location. For logistical reasons, the bioassays were incubated
at a lake location near the Taihu Laboratory for Lake
Ecosystem Research (TLLER), Nanjing Institute of Geography
and Limnology, Chinese Academy of Sciences (Fig. 2).
Monthly physical, chemical, and biological parameters,
including surface water temperature, dissolved oxygen, pH,
and electrical conductivity, were measured using a Yellow
Springs Instruments (YSI) 6600multi-sensor sonde. Integrated
water sampleswere taken using a 2-m long, 0.1-mwide plastic
tube with a 1-way valve.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3 1975
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2.4. Nutrient analyses
Water samples were analyzed for total nitrogen (TN), total
dissolved nitrogen (TDN), dissolved inorganic nitrogen (DIN;
ammonium (NH4þ) þ nitrate (NO3
�) þ nitrite (NO2�)), total phos-
phorus (TP), total dissolved phosphorus (TDP), and dissolved
inorganic phosphorus (DIP). DIP was determined using the
molybdenum bluemethod (APHA, 1995). NH4þ was determined
using the indophenol bluemethod, andNO3� andNO2
�with the
cadmium reduction method (APHA, 1995). TP, TDP, TN, and
TDNweredeterminedusing a combined persulphate digestion
(Ebina et al., 1983), followed by spectrophotometric analysis as
for DIP and NO3�. Particulate nitrogen (PN) was obtained by
subtracting TDN from TN, and particulate phosphorus (PP) by
subtracting TDP fromTP. Analytical errorswere determined as
the average % coefficients of variation of triplicates. Average
errors for PP and PN were 6.3% and 5% respectively.
2.5. Biological measurements
Phytoplankton samples were preserved with Lugol’s iodine
solution (2% final conc.) and settled for 48 h. Phytoplankton
species were identified and counted according to Hu et al.
(1980). Chlorophyll a (Chl a) concentrations were determined
spectrophotometrically, following extraction in 90% hot
ethanol (Papista et al., 2002).
2.6. Nutrient limitation bioassay experiments
In situ nutrient addition bioassays were performed seasonally
in 2008e2009 on “inner bay” water (Fig. 2) to examine nutrient
limitation of the natural phytoplankton community. Water
samples were collected from 0.2 m below the surface using
0.01 N HCl-washed and then lake water-rinsed 20 L poly-
ethylene carboys. Water was screened through 200 mm mesh
to remove large zooplankton and dispensed into acid (0.01 HCl)
and then lake water washed 1-L polyethylene Cubitainers
(HedwinCo.). Cubitainers are chemically inert, unbreakableand
transparent (80% PAR transmittance). The methodology and
deployment for Cubitainer bioassays followed Paerl and Bowles
(1987). At the start of each experiment (To), water sampleswere
analyzed for Chl a and nutrients. Three treatments were con-
ducted, in addition to a control (no nutrient additions): (1) N
addition (þN) (2) P addition (þP) (3) N and P addition (þNP).
Fig. 2 e Map of Lake Taihu. The lake’s largest tributaries are named. The Taipu River is the main river discharging water
from the lake. The Wangyu River periodically delivers Yangtze River water to the lake (see Fig. 1 for the location of the
Yangtze River relative to Taihu). Sampling locations are indicated, as is the Taihu Laboratory for Lake Ecosystem Research
(TLLER). Insert shows the location of Taihu in the PR China.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 31976
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Nitrogen was added as KNO3, reflecting the dominant form of
inorganic N in Taihu. NH4Cl was also used as an N source in
summer 2009 to compare phytoplankton growth responses to
different N forms. Phosphoruswas added as K2HPO4$3H2O. The
final concentration of N was 2.00mg N/L, and the final concen-
tration of P was 0.50 mg P/L. These concentrations approxi-
mated the values of these nutrient forms in the lake during
maximumdischarge periods (Pu andYan, 1998; Qin et al., 2007).
All treatments were conducted in triplicate. Following
nutrient additions, Cubitainers were incubated in situ near
the surface for 4 or 6 days by placing them in a floating
frame suspended off a pier at TLLER (Fig. 2). This approach
provided natural light, temperature and surface wave action
conditions. One layer of neutral density screening was
placed over the frame to prevent photoinhibition during the
incubations. Following deployment, Cubitainers were sub-
sampled at 2e3 d intervals for Chl a and nutrient
concentrations.
2.7. Water column NH4þ regeneration and potential
uptake rates
Water column NH4þ regeneration and potential uptake rates
in Taihu, as described in McCarthy et al. (2007), were con-
ducted to provide insights into consequences of unmitigated
N discharges into Taihu. Previously published water column
N cycling rates were determined in late summer 2002 from
four sites in northern Taihu (McCarthy et al., 2007). The N
and P addition bioassays described in the present study
were conducted on water collected at sites corresponding to
“inner bay” and “main lake” in McCarthy et al. (2007). Water
column NH4þ recycling rates also were determined at the
main lake station and four sites in East Lake Taihu (ELT) in
January 2004 and all northern Taihu and ELT locations in
May 2004 (Fig. 2). The ELT sites were located in the south-
eastern portion of the lake, near the outflow of the lake into
the Taipu River. Methodological details are provided in
McCarthy et al. (2007).
Briefly, water samples were amended with saturating
levels of 15NH4þ and incubated at ambient temperature and
light for w24 h. Total NH4þ concentration and isotope ratios
were determined using high performance liquid chromatog-
raphy (HPLC; Gardner et al., 1995), and regeneration and
potential uptake rates were calculated using the isotope
dilution technique (Blackburn, 1979; Caperon et al., 1979).
Since Lake Taihu is shallow and well-mixed, rates were
extrapolated to the whole water column to estimate a total
internal N load from water column recycling processes.
2.8. Statistical analyses
Differences in the growth responses between various treat-
ments were analyzed by one-way ANOVA. Post Hoc Multiple
Comparisons of treatment means were performed by Tukey’s
least significant difference procedure. Untransformed data in
all cases satisfied assumptions of normality and homosce-
dasticity. Statistical analysis was performed using the SPSS
13.0 statistical package for personal computers, and the level
of significance used was at p < 0.05 for all tests.
3. Results and discussion
3.1. Nutrient inputs and concentrations
Seasonal and annual surface water TN and TP loads to Taihu
during 2000e2005 indicate that the lake received high
amounts of N and P on a year-round basis, with N loads being
higher, relative to P, in the winter (Fig. 3). Ratios (by weight) of
TN to TP loading range from w22 to over 29, indicating rela-
tively N enriched conditions on an annual basis. Lowest N:P
loading ratios occur in summertime, whereas highest ratios
occur in winterespring.
The Taihu basin has, over the past 3 decades, experienced
dramatic increases in population and urbanization (Qin et al.,
2007; Guo, 2007). The high N:P loading reflects the combined
effects of population growth, changes in land use, including
increasing agricultural, and urban and rural wastewater
discharge. These changes and the emphasis of P over N
control in wastewater treatment (Wang andWang, 2009) have
led to increases in N:P loading from cities. In addition,
reflecting a worldwide pattern (Galloway and Cowling, 2002),
chemical N fertilizer use has increased in agricultural regions
Fig. 3 e Upper: Seasonal total nitrogen (TN) loading to Lake
Taihu from its tributaries, covering a period from 2000 to
2005, inmetric tons of N. Lower: Seasonal total phosphorus
(TP) loading, in metric tons of P, to Lake Taihu from its
tributaries, from 2000 to 2005.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3 1977
Author's personal copy
of the Taihu watershed, leading to N relative to P enrichment.
Lastly, atmospheric deposition, which is enriched in N relative
to P (Zhai et al., 2009), is an increasing source of N, accounting
for approximately 30% of the external N loading to the lake.
Atmospheric N inputs are estimated to have undergone a 25-
fold increase over the past 150 years, and this trend has
accelerated during the past 3 decades (Lelieveld and Dentener,
2000) (Supplementary material 1: S-1).
Recent increases in TN and TP loading can be seen as
trends in TN and TP concentrations in the lake (mid-lake
location) (Fig. 4). Increases were evident between the mid
1980s and 2000, a period of rapid population growth and
urbanization in the Taihu watershed (Qin et al., 2007; Guo,
2007). They may have leveled off since the early 2000,
possibly a result of persistent droughts (Qin et al., 2007, 2010),
diversion of sewage from the cities of Wuxi and Suzhou to
waterways draining to the East China Sea, and usage of the
Wangyu River canal, which exchanges water between Taihu
and the Yangtze River. The decreases TN loading may have
resulted from a reduction in pollutant input from the water-
shed in 1998. However, at the end of 1998, a pollutant emission
reduction movement (the so called “zero point action”)
launched by the government throughout the entire water-
shed, did not persist over time.
Both TN and TP, as well as DIN and DIP concentrations,
showed strong seasonal variation in Taihu. Maximum TN and
DIN values occurred in winter and spring, whereas minimum
values were observed in summer and autumn during the 2-yr
period (Fig. 5). In contrast, TP and DIP values showed an inverse
pattern,withwinterhaving lowvaluesandsummerhighvalues.
DIN patterns closely tracked TN over time (Fig. 5). Overall, TN
values were higher in Meiliang Bay than in the lake proper,
reflecting large external loads and elevated internal loading.
3.2. Nutrient addition bioassays
The in situ nutrient addition bioassays showed stimulation of
algal biomass production (as Chl a) in response to individual
and combined N and P additions, indicating that nutrient
enrichment enhanced algal growth and bloom potentials.
Nutrient limitation showed strong repeated seasonal patterns
in 2008 and 2009, although different degrees of algal biomass
stimulation were observed between the two years (Fig. 6). P
limitation prevailed in winter and spring, while N limitation
occurred in summer and fall. In most instances, algal growth
responses to N and P additions exceeded those observed with
0.00
0.05
0.10
0.15
0.20
0.25
0.30
1987
1989
1991
1993
1995
1997
1999
2001
2003
2005
2007
2009
Year
TP
(mg/
L)
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
TN
(m
g/L
)
TP TN
Fig. 4 e Annual average TN and TP concentrations, as mg/L
of each element, in Lake Tahu. Data are from the Main Lake
station.
Fig. 5 e Patterns of TN, DIN, TP and DIP, as mg/L of each element, at Inner Bay and Main Lake locations during 2008e2009.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 31978
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N and P alone (Fig. 6). This “synergistic” N and P effect was
most pronounced in summer and fall, when algal growth
rates, and hence nutrient demands, were highest.
Nutrient limitation patterns followed inverse concentra-
tion patterns of dissolved inorganic N (DIN) and P (DIP). DIN
concentrations were high during winter and spring, reflecting
high N inputs, while DIP concentrations were at their lowest
levels (Fig. 5). As a result, DIP proved to be the limiting nutrient
at this time. Then, DIN decreased rapidly as growth and bloom
conditions improved in late spring and summer with
increased light levels and temperatures. In contrast, DIP
concentrations remained quite high and actually increased
during summer bloom periods. The summer DIP increases
may relate to elevated pH conditions (due to photosynthetic
CO2 demand by blooms), which can enhance DIP release from
the sediments (Andersen, 1975; Xu et al., 2010). Further,
Microcystis can store P during sedimentary phases and
assimilate N in larger proportion to P during bloom phases
(Ahn et al., 2002). This uneven nutrient assimilation pattern
can lead to decreases in N:P and enhance N limitation. It
appears that DIN availability during this period determines
the magnitudes and duration of booms.
The availability of iron (Fe), a nutrient required for photo-
synthetic growth and N2 fixation, may have played an addi-
tional role in controlling phytoplankton production. However,
when Fe (as EDTA-chelated and non-chelated Feþ2) was added
alone and in combination with N and P to Inner Bay and open
lake water samples during summer 2009, no significant
stimulatory (or inhibitory) effects of Fe were observed (not
shown).
Parallel microscopic determinations of phytoplankton
biomass agreed with chlorophyll a results (Xu et al., 2010),
confirming that Chl a was a good indicator of phytoplankton
biomass response in the bioassays. Additional total particu-
late organic carbon measurements made on the bioassays
confirmed that Chl a responses reflected true increases in
phytoplankton biomass.
Microcystis spp. remained the dominant bloom-forming
cyanobacteria during the summer-fall bloom periods of both
years, despite chronic N limitation. These N limited periods
should have provided optimal conditions for N2 fixing genera
(i.e., Anabaena, Aphanizomenon) to become dominant (Smith,
1983, 1990; Schindler et al., 2008), but this situation did not
develop, even though DIP remained plentiful (Figs. 4 and 5).
Possible explanations for this result include; (1) superior ability
of Microcystis spp. to compete for NH4þ and P from sediments
(Kappers,1980)andwatercolumnregeneration (Blomqvistetal.,
1994), and (2) mutually-beneficial bacterialecyanobacterial
interactions in the “phycosphere” of Microcystis spp. colonies,
which can enhance nutrient cycling and growth of “host”
Microcystis populations (Paerl and Pinckney, 1996).
Bioassays illustrated thatMicrocystis spp. competed for DIN
effectively, especially for NH4þ. Per amount of N added,
ammonium stimulated significantly more algal biomass
formation than nitrate (Fig. 7). The extent to which natural
Microcystis populations dominated the absolute uptake of NH4þ
was not determined, but phytoplankton biomass was domi-
nated (>80%) by Microcystis in bioassays. This mechanism
helps explain the persistence of Microcystis during periods of
low DIN concentrations. In addition, Microcystis’ ability to
Fig. 6 e Phytoplankton biomass (chlorophyll a) responses
in bioassays conducted in May, July, October, and
December 2008 and May, July and October 2009. Water
samples for bioassays were collected from the surface at
the Inner Bay location in Meiliang Bay. Initial chlorophyll
a content is shown. Responses were for 3-day incubations
in spring, summer, and fall, 6-day incubations in winter
2008, and 2-day incubations in spring, summer, and fall
2009. Mean values are shown. Error bars represent ±1SD of
triplicate samples. Differences between treatments are
shown based on ANOVA post hoc tests (a > b > c;
p < 0.05).
Fig. 7 e Phytoplankton biomass (chlorophyll a) responses
to various nitrogen sources, each added at 2.00 mg N/L, in
bioassays conducted in August 2009, using Inner Bay
water from Meiliang Bay. Response is 2-day chlorophyll
a average. Error bars represent ±1SD of triplicate samples.
Differences between treatments are shown based on
ANOVA post hoc tests (a > b > c; p < 0.05).
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3 1979
Author's personal copy
adjust its vertical position by buoyancy compensation
(Reynolds, 1987) may enable exploitation of the entire water
column, taking advantage of regenerated as well as exter-
nally-supplied (atmospheric, surface runoff) N sources.
The results indicate that inputs of both nutrients should be
reduced to control bloom formation and magnitude. Algal
biomass production may be controlled by P availability in the
spring, while N availability may determine the magnitude,
spatial extent and duration of the bloom during summer-fall
when the bloom potential is highest. Nutrient co-limitation
was observed during all periods; i.e., combined enrichment
with N and P led to higher magnitudes of biomass formation
than either N or P alone. This result suggests that N and P
supplies are closely balanced with regard to the requirements
for supporting and promoting eutrophication and bloom
formation.
3.3. Water column NH4þ regeneration and potential
uptake
Water column NH4þ regeneration and potential uptake rates
showed seasonal and spatial differences (S-1). In January, light
uptake rates were significantly lower ( p < 0.01; ANOVA) than
those in September (main lake) and May (main lake and ELT
sites). In northern Taihu, only the inner bay had a seasonal
difference in regeneration rates, although the difference was
large (0.89 mmol N/L h in May versus 0.19 mmol N/L h in
September). In ELT, uptake and regeneration rates were lower
than the Meiliang Bay sites, but this pattern was expected
since ELT is dominated by submerged aquatic vegetation
(SAV) rather than phytoplankton.
To scale regeneration rates and to compare with external
loads, sites were first regrouped based on location within the
lake. Lake Taihu has a surface area of 2338 km2, but Meiliang
Bay and ELT account for only 100 and 131 km2, respectively, of
the total surface area. The outer bay site was located at the
interface between Meiliang Bay and the main lake and is
15e20 km from river discharges. Thus, this site was grouped
with the main lake station. After regrouping the sampling
sites, volumetric regeneration rates (see S-1) were converted
to areal rates using water depth and extrapolated based on
surface area of the appropriate lake region.
Extrapolatedwater columnNH4þ regeneration rates suggest
that 3.77� 107 kg N/yr are regenerated as NH4þ in Meiliang Bay,
where the most severe Microcystis blooms occur. Despite
actual regeneration rates being an order ofmagnitude lower in
the main lake than Meiliang Bay, the large surface area of the
central basin results in 6.57 � 107 kg N/yr regenerated as NH4þ.
As expected, ELT plays a minor role in total N recycling in the
water column (0.13 � 107 kg N/yr). The sum of these annual
regeneration estimates is about 400% of total estimated N
loading to the lake (2.5 � 107 kg N/yr; James et al., 2009).
However, these estimates include only N regenerated as NH4þ.
No estimates of the NH4þ proportion of the total N load are
known, but the proportion is presumably small relative to
oxidized (i.e., NO3�) and organic N forms. Internal N cycling is
important for the maintenance and species succession of
cyanobacteria blooms in Taihu, especially as it pertains to
Microcystis spp. (McCarthy et al., 2007). Atmospheric deposi-
tion is a significant additional source of bioavailable N in the
lake (Zhai et al., 2009) (S-2). For example, NH4þ and NO3
-con-
centrations of a rainwater sample collected in May 2004 were
370 and 146 mM, respectively (McCarthy and Gardner, unpub-
lished data).
Direct denitrification measurements in Meiliang Bay and
the main lake in late summer 2002 (McCarthy et al., 2007)
and Meiliang Bay, the main lake, and ELT from January to
May 2004 (McCarthy and Gardner, unpublished data) were
extrapolated to estimate a lake-wide denitrification rate.
This rate ranged from 7360 kg N/km2 per year when esti-
mated by net N2 flux to 26,700 kg N/km2 per year when
estimated using 15NO3� addition assays. Both estimates were
obtained from continuous-flow incubations of intact sedi-
ment cores. Rates from 15NO3� additions should be qualified
as potential rates, whereas rates from net N2 flux would
include any N2 fixing activities, which were not significant in
sediments of this lake (McCarthy et al., 2007). Therefore, net
N2 flux represents the best estimate of denitrification and
accounts for 66.2% of external N loading. This N loss via
denitrification would not account for the N recycled in the
water column. In late summer, Meiliang Bay and main lake
sediments are an N source to the water column (McCarthy
et al., 2007). Sediments also are an N source in ELT and the
main lake in January and May (McCarthy and Gardner,
unpublished data). However, sediments in Meiliang Bay were
a strong N sink in January and May. These patterns suggest
that late summer cyanobacteria blooms rely, in part, on
nutrients released from sediments (McCarthy et al., 2007).
Depth averaged water column NH4þ regeneration rates for the
shallow water column imply that water column regeneration
supplies a greater amount of N (5-fold more on an areal
basis) than sediments for cyanobacterial assimilation in the
summer (McCarthy et al., 2007).
In addition to the importance that total N loads play in
determining rates of eutrophication, the supply rates and
ratios of various N forms help structure microalgal commu-
nities mediating freshwater primary production (Paerl, 1988;
McCarthy et al., 2007, 2009). For example, the ratio of NH4þ to
oxidized N was related to the proportion of cyanobacteria
comprising the total phytoplankton community of Lake
Okeechobee, FL, USA (McCarthy et al., 2009). While non-N2
fixing cyanobacteria, such as Microcystis, compete effectively
for reduced N (Blomqvist et al., 1994), N2 fixing cyanobacteria
also assimilate ammonium preferentially if it is available
(Ferber et al., 2004). Ammonium and other reduced N forms,
such as dissolved free amino acids, are more available than
oxidized N forms (nitrate and nitrite) to bacteria (Vallino et al.,
1996) and cyanobacteria because less energy is required to
incorporate and assimilate the former (Syrett, 1981; Gardner
et al., 2004; Flores and Herrero, 2005).
These issues were not addressed in recent studies sug-
gesting that eutrophication cannot be controlled by reducing
N inputs (e.g., Schindler et al., 2008; Wang and Wang, 2009).
The assumption that N2 fixing genera will replace non-N2
fixing genera like Microcystis when N is limiting and P is
sufficient could not be confirmed in Taihu. Furthermore, our
observation that Taihu does not fit the proposed “P only”
management paradigm of Schindler et al. (2008) is not unique.
Numerous other lakes, reservoirs, rivers and fjords worldwide
exhibit N and P co-limitation, either simultaneously or in
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 31980
Author's personal copy
seasonally-shifting patterns (Dodds et al., 1989; Elser et al.,
2007; Forbes et al., 2008; Scott et al., 2008; North et al., 2007;
Lewis and Wurtsbaugh, 2008; Conley et al., 2009; Xu et al.,
2010; Abell et al., 2010).
4. Conclusions
Nutrient loading analyses, nutrient addition bioassays and
nutrient cycling studies provide the basis for recommending
that N control be included, along with the previously
prescribed P control (Chen et al., 2003a,b; Wang and Wang,
2009), as a nutrient management strategy for Taihu. Denitri-
fication rates, while high relative to other lakes, are lower than
estimates of N loading and therefore would not mitigate high
N loads. Also, late summer cyanobacterial blooms are main-
tained primarily by water column N regeneration. Recycling
produces NH4þ available to non-N-fixing cyanobacterial
blooms (Microcystis), regardless of the N form discharged into
the lake.
The fact thatMicrocystis spp. were not replaced by N2 fixing
cyanobacterial bloom species during N limited, but P sufficient
summer periods is evidence that predictions of succession
from non-N2 to N2 fixing taxa based on N:P stoichiometry
(Smith, 1990; Schindler et al., 2008) may not apply to hyper-
eutrophic lakes. Excess inputs of both N and P, combined with
internal cycling of these nutrients, may overwhelm the ability
of a single nutrient to control increasing eutrophication and
bloom intensification in Lake Taihu and other large lakes
experiencing such blooms (e.g., Lake Erie, Lake Okeechobee,
Lake Victoria).
P input reductions are an important component of eutro-
phication management in large lakes and reservoirs.
However, failure to control N inputs may result in continued
serious eutrophication problems caused by non-N2 fixing
cyanobacterial blooms.
Acknowledgements
We thank the TLLER, the Taihu Basin Authority, and the
Chinese Ministry of Water Resources for providing water
quality data, and XiaodongWang, Linlin Cai, Jingchen Xue, Lu
Zhang and Longyuan Yang for assistance with sampling and
chemical analyses and Guangbai Cui and Yong Pang for data
collection. This research was supported by the Chinese
Academy of Sciences (Contract: KXCX1-YW-14), the Ministry
of Science and Technology of China (Contract: 2009ZX07101-
013), the Chinese National Science Foundation (Contract:
40825004, 40730529, 51009049), Fundamental Research Funds
for the Central Universities (China), the US Environmental
Protection Agency (Project 83335101-0), and US National
Science Foundation (CBET Program) Project 0826819.
Appendix. Supplementary data
Supplementary data related to this article can be found online
at doi:10.1016/j.watres.2010.09.018
r e f e r e n c e s
Abell, J.M., Ozkundakci, D., Hamilton, D.P., 2010. Nitrogen andphosphorus limitation of phytoplankton growth in NewZealand lakes: implications for eutrophication control.Ecosystems. doi:10.1007/s10021-010-9367-9.
Ahn, C.-Y., Chung, A.-S., Oh, H.-M., 2002. Rainfall, phycocyanin,and N:P ratios related to cyanobacterial blooms in a Koreanlarge reservoir. Hydrobiologia 474, 117e124.
Andersen, J.M., 1975. Influence of pH on release of phosphorusfrom lake sediments. Archiv fur Hydrobiologie 76, 411e419.
APHA., 1995. Standard Methods for the Examination of Water andWastewater, nineteenth ed. American Public HealthAssociation, American Water Works Association, WaterEnvironment Federation.
Blackburn, T.H., 1979. Method for measuring rates of NH4þ
turnover in anoxic marine sediments, using a 15NeNH4þ
dilution technique. Applied & Environmental Microbiology 37,760e765.
Blomqvist, P., Pettersson, A., Hyenstrand, P., 1994.Ammoniumenitrogen: a key regulatory factor causingdominance of non-nitrogen-fixing cyanobacteria in aquaticsystems. Archives of Hydrobiology 132 (2), 141e164.
Boyer, E.W., Howarth, R.W., Galloway, J.N., Dentener, F.J.,Cleveland, C., Asner, G.P., Greene, P., Vorosmarty, C., 2004.Current nitrogen inputs to world regions. In: Mosier, A.R.,Syers, J.K., Freney, J.R. (Eds.), Agriculture and the NitrogenCycle. Island Press, Washington, DC, pp. 221e230. SCOPE #65.
Caperon, J., Schell, D., Hirota, J., Laws, E., 1979. Ammoniumexcretion rates in Kaneohe Bay, Hawaii, measured by a 15Nisotope dilution technique. Marine Biology 54, 33e40.
Carmichael, W.W., 2001. Health effects of toxin producingcyanobacteria: the cyanoHABs. Human and Ecological RiskAssessessment 7, 1393e1407.
Chen, Y.W., Qin, B.Q., Teubner, K., Dokulil, M.T., 2003a. Long-termdynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China.Journal of Plankton Research 25, 445e453.
Chen, Y.W., Fan, C.X., Teubner, K., Dokulil, M., 2003b. Changes ofnutrients and phytoplankton chlorophyll-a in a large shallowlake, Taihu, China: an 8-year investigation. Hydrobiologia 506,273e279.
Conley, D.J., Paerl, H.W., Howarth, R.W., Boesch, D.F.,Seitzinger, S.P., Havens, K.E., Lancelot, C., Likens, G.E., 2009.Controlling eutrophication: nitrogen and phosphorus. Science323, 1014e1015.
Dodds, W.K., Johnson, K.R., Priscu, J.C., 1989. Simultaneousnitrogen and phosphorus deficiency in naturalphytoplankton assemblages: theory, empirical evidence andimplications for lake management. Lake and ReservoirManagement 5, 21e26.
Ebina, J., Tsutsui, T., Shirai, T., 1983. Simultaneous determinationof total nitrogen and total phosphorus in water usingperoxodisulfate oxidation. Water Research 17, 1721e1726.
Elser, J.J., Bracken, M.E.S., Cleland, E.E., Gruner, D.S., Harpole, W.S.,Hillebrand, H., Bgai, J.T., Seabloom, E.W., Shurin, J.B., Smith, J.E.,2007. Global analysis of nitrogen and phosphorus limitation ofprimary producers in freshwater, marine and terrestrialecosystems. Ecololgy Letters 10, 1124e1134.
Ferber, L.R., Levine, S.N., Lini, A., Livingston, G.P., 2004. Docyanobacteria dominate in eutrophic lakes because they fixatmospheric nitrogen? Freshwater Biology 49, 690e708.
Flores, E., Herrero, A., 2005. Nitrogen assimilation and nitrogencontrol in cyanobacteria. Biochemical Society Transactions 33(1), 164e167.
Forbes, M.G., Doyle, R.D., Scott, J.D., Stanley, J.K., Huang, H.,Brooks, B.W., 2008. Physical factors control phytoplankton
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3 1981
Author's personal copy
production and nitrogen fixation in eight Texas reservoirs.Ecosystems 11, 1181e1197.
Galloway, J.N., Cowling, E.B., 2002. Reactive nitrogen and theworld: 200 years of change. Ambio 16 (2), 64e71.
Gardner, W.S., Bootsma, H.A., Evans, C., St. John, P.A., 1995.Improved chromatographic analysis of 15N:14N ratios inammonium or nitrate for isotopic addition experiments.Marine Chemistry 48, 271e282.
Gardner, W.S., Lavrentyev, P.J., Cavaletto, J.F., McCarthy, M.J.,Eadie, B.J., Johengen, T.H., Cotner, J.B., 2004. The distributionand dynamics of nitrogen and microbial plankton in southernLake Michigan during spring transition 1999e2000. Journal ofGeophysical Research 109, 1e16.
Guo, L., 2007. Doing battle with the green monster of Lake Taihu.Science 317, 1166.
Havens, K.E., Fukushima, T., Xie, O.P., Iwakuma, T., James, R.T.,Takamura, N., Hanazato, T., Yamamoto, T., 2001. Nutrientdynamics and the eutrophication of shallow lakesKasumigaura (Japan), Donghu (PR China), and Okeechobee(USA). Environmental Pollution 111 (2), 262e272.
Howarth, R.W., Marino, R., Lane, J., Cole, J.J., 1988. Nitrogenfixation rates in freshwater, estuarine, and marineecosystems. Limnology and Oceanography 33, 669e687.
Hu, H., Li, Y., Wei, Y., Zhu, H., Shi, Z., 1980. Freshwater Algae inChina. Shanghai Science and Technology Press, Shanghai (inChinese).
Huisman, J.M., Matthijs, H.C.P., Visser, P.M., 2005. HarmfulCyanobacteria. Springer Aquatic Ecology Series 3. Springer,Dordrecht, The Netherlands, p. 243.
James, R.T., Havens, K., Zhu, G., Qin, B., 2009. Comparativeanalysis of nutrients, chlorophyll and transparency in twolarge shallow lakes (Lake Taihu, PR China and LakeOkeechobee, USA). Hydrobiologia 627, 211e231.
Jeppesen, E., Søndergaard, M., Meerhoff, M., Lauridsen, T.L.,Jensen, J.P., 2007. Shallow lake restoration by nutrient loadingreductiondsome recent findings and challenges ahead.Hydrobiologia 584, 239e252.
Kappers, F.I., 1980. The cyanobacterium Microcystis aeruginosa kg.and the nitrogen cycle of the hypertrophic Lake Brielle (TheNetherlands), pp. 37e43. In: Barica, J., Mur, L. (Eds.),Hypertrophic Ecosystems Dr. W. Junk (The Hague, TheNetherlands).
Kronvang, B., Jeppesen, E., Conley, D.J., Søndergaard, M.,Larsen, S.E., Ovesen, N.B., Carstensen, J., 2005. Nutrientpressures and ecological responses to nutrient loadingreductions in Danish streams, lakes and coastal waters.Journal of Hydrology 304, 274e288.
Lelieveld, J., Dentener, F., 2000. What controls troposphericozone? Journal of Geophysical Research 105, 3531e3551.
Lewis Jr., W.M., Wurtsbaugh, W.A., 2008. Control of lacustrinephytoplankton by nutrients: erosion of the phosphorusparadigm. Internationale Revue der gesamten Hydrobiologieund Hydrographie 93, 446e465.
Likens, G.E., 1972. In: Nutrients and Eutrophication Americ. Soc.Limnol. Oceanogr. Special Symp. 1.
McCarthy, M.J., Lavrentyev, P.L., Yang, L., Zhang, L., Chen, Y.,Qin, B., Gardner, W.S., 2007. Nitrogen dynamics relative tomicrobial food web structure in a subtropical, shallow, well-mixed, eutrophic lake (Taihu Lake, China). Hydrobiologia 581,195e207.
McCarthy, M.J., James, R.T., Chen, Y., East, T.L., Gardner, W.S.,2009. Nutrient ratios and phytoplankton community structurein the large, shallow, eutrophic, subtropical Lakes Okeechobee(Florida, USA) and Taihu (China). Limnology 10, 215e227.
North, R.L., Guildford, S.J., Smith, R.E.H., Havens, S.M., Twiss, M.R.,2007. Evidence for phosphorus, nitrogen, and iron colimitationof phytoplankton communities in Lake Erie. Limnology andOceanography 52, 315e328.
Ozkan, K., Jeppesen, E., Johansson, L.S., Beklioglu, M., 2009. Theresponse of periphyton and submerged macrophytes tonitrogen and phosphorus loading in shallow warm lakes:a mesocosm experiment. Freshwater Biology. doi:10.1111/j.1365e2427.2009.02297.x.
Paerl,H.W., 1990. Physiological ecologyandregulationofN2fixationin natural waters. Advances in Microbial Ecology 11, 305e344.
Paerl,H.W.,1988.Nuisancephytoplanktonbloomsincoastal,estuarine,and inlandwaters. Limnology and Oceanography 33, 823e847.
Paerl, H.W., 1997. Coastal eutrophication and harmful algalblooms: importance of atmospheric deposition andgroundwater as “new” nitrogen and other nutrient sources.Limnology and Oceanography 42, 1154e1165.
Paerl,H.W.,2008.Nutrientandotherenvironmentalcontrolsofharmfulcyanobacterial blooms along the freshwater-marine continuum.Advances in Experimental Medicine and Biology 619, 216e241.
Paerl, H.W., 2009. Controlling eutrophication along thefreshwateremarine continuum: dual nutrient (N and P)reductions are essential. Estuaries and Coasts 32, 593e601.
Paerl, H.W., Bowles, N.D., 1987. Dilution bioassays: theirapplication to assessments of nutrient limitation inhypereutrophic waters. Hydrobiologia 146, 265e273.
Paerl, H.W., Pinckney, J.L., 1996. Microbial consortia: their role inaquatic produc-tion and biogeochemical cycling. MicrobialEcology 31, 225e247.
Paerl, H.W., Fulton, R.S., Moisander, P.H., Dyble, J., 2001. Harmfulfreshwater algal blooms, with an emphasis on cyanobacteria.The Scientific World 1, 76e113.
Papista, E., Acs, E., Boeddi, B., 2002. Chlorophyll-a determinationwith ethanol e a critical test. Hydrobiologia 485, 191e198.
Piehler, M.F., Dyble, J., Moisander, P.H., Chapman, A.D.,Hendrickson, J., Paerl, H.W., 2009. Interactions betweennitrogen dynamics and the phytoplankton community in LakeGeorge, Florida, USA. Lake andReservoirManagement 25, 1e14.
Pu, P., Yan, J., 1998. Taihu Lake e a large shallow lake in the EastChina plain. Journal of Lake Sciences (China) 10 (suppl), 1e12.
Qin, B.Q.,Xu, P.Z.,Wu,Q.L., Luo, L.C., Zhang,Y.L., 2007. Environmentalissues of Lake Taihu, China. Hydrobiologia 581, 3e14.
Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H.W.,Carmichael, W.W., 2010. A drinking water crisis in Lake Taihu,China: linkage to climatic variability and lake management.Environmental Management 45, 105e112.
Rabalais, N.N., 2002. Nitrogen in aquatic ecosystems. Ambio 16(2), 102e112.
Reynolds, C.S., 1987. Cyanobacterial water blooms. Advances inBotanical Research 13, 67e143.
Schindler, D.W., 1977. The evolution of phosphorus limitation inlakes. Science 195, 260e262.
Schindler, D.W., Hecky, R.E., Findlay, D.L., Stainton, M.P.,Parker, B.R., Paterson, M., Beaty, K.G., Lyng, M., Kasian, S.E.M.,2008. Eutrophication of lakes cannot be controlled by reducingnitrogen input: results of a 37 year whole ecosystemexperiment. Proceedings of the National Academy of ScienceUSA 105, 11254e11258.
Scott, J.T., Doyle, R.D., Prochnow, S.J., White, J.D., 2008. Arewatershed and lacustrine controls on planktonic N2 fixationhierarchically structured? Ecological Applications 18,805e819.
Scott, J.T., McCarthy, M.J., 2010. Nitrogen fixation may not balancethe nitrogen pool in lakes over timescales relevant toeutrophication management. Limnology and Oceanography55, 1265e1270.
Smith, V.H., 1983. Low nitrogen to phosphorus ratios favordominance by blueegreen algae in lake phytoplankton.Science 221, 669e671.
Smith, V.H., 1990. Nitrogen, phosphorus, and nitrogen fixation inlacustrine and estuarine ecosystems. Limnology andOceanography 35, 1852e1859.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 31982
Author's personal copy
Syrett, P., 1981. Nitrogen metabolism in microalgae. Physiologicalbases of phytoplankton ecology. Canadian Journal of Fisheriesand Aquatic Science 210, 182e210.
Vallino, J.J., Hopkinson, C.S., Hobbie, J.E., 1996. Modeling bacterialutilization of dissolved organic matter: optimization replacesMonod growth kinetics. Limnology and Oceanography 41,1591e1609.
Vitousek, P.M., Mooney, H.A., Lubchenko, J., Mellilo, J.M., 1997.Human omination of earth’s ecosystem. Science 277,494e499.
Wang, H.J., Wang, H.Z., 2009. Mitigation of lake eutrophication:loosen nitrogen control and focus on phosphorus abatement.Progress in Natural Science 19, 1445e1451.
Xu, H., Paerl, H.W., Qin, B.Q., Zhu, G.W., Gao, G., 2010. Nitrogen andphosphorus inputs control phytoplankton growth in eutrophicLake Taihu, China. Limnology and Oceanography 55, 420e432.
Zhai, S., Yang, L., Hu, W., 2009. Observations of atmosphericnitrogen and phosphorus deposition during the period of algalbloom formation in Northern Lake Taihu, China.Environmental Management 44, 542e551.
wat e r r e s e a r c h 4 5 ( 2 0 1 1 ) 1 9 7 3e1 9 8 3 1983