Transcript CULTURAL EUTROPHICATION OF THREE MIDWEST URBAN RESERVOIRS: THE ROLE OF NITROGEN LIMITATION IN DETERMINING PHYTOPLANKTON COMMUNITIES Pascual, D.

CULTURAL EUTROPHICATION OF THREE MIDWEST URBAN RESERVOIRS:
THE ROLE OF NITROGEN LIMITATION IN DETERMINING PHYTOPLANKTON COMMUNITIES
Pascual, D. L., University of Michigan School of Public Health & Indiana University-Purdue University, (UM) Ann Arbor & (IUPUI) Indianapolis, USA
Johengen, T. H., University of Michigan, Ann Arbor, USA
Filippelli, G. M., Indiana University – Purdue University, Indianapolis, USA
Tedesco, L. P., Indiana University – Purdue University, Indianapolis, USA
Moran, D., Veolia Water, Indianapolis, LLC,1 USA
ABSTRACT:
The cultural eutrophication of three Midwest urban reservoirs has resulted in impaired water quality. Nutrient loading to these reservoirs has resulted in the formation of nuisance algal blooms, including possible toxin-producing and/or taste and odor causing,
heterocyst-forming blue-green algae such as Anabaena, Aphanizomenon, and Cylindrospermopsis. However, while eutrophication models tend to utilize a single parameter, namely P, to predict potential algal standing stocks, data from three Midwest urban
reservoirs showed that N was equally important in determining phytoplankton productivity and more important in determining phytoplankton succession from diatoms and greens to heterocyst-forming blue-green algae. Analysis of monthly nutrient concentrations
(Total P, NO3-, NH4+) taken from 1998 – 2000 for two southeastern Michigan reservoirs, Ford Lake and Bellville Lake, and weekly nutrient data taken from 1976 – 1996 and bi-weekly data collected in 2003 for Eagle Creek Reservoir, Indiana showed consistent
annual trends of NO3- + NH4+ depletion and P abundance from mid- to late summer, suggesting that phytoplankton production became seasonally N-limited in these reservoirs. Data from Eagle Creek Reservoir indicated that N concentrations were more strongly
dependent on watershed inputs than was P, a trend not supported by Ford and Bellville Lake data sets.
INTRODUCTION:
Since Vollenweider first developed input-output models to
describe the relationship between phosphorus and
eutrophication, empirical models have been employed as a way
to understand how a single parameter can work to affect
ecological changes such as changes in phytoplankton biomass
(e.g. Dillon and Rigler, 1974). However, understanding the
change from a diverse phytoplankton community to a specific
nuisance algal bloom, i.e. heterocyst-forming (HC) blue-green
algae capable of producing toxins and/or taste and odor
causing compounds (e.g. MIB (2-methylisoborneol) and
geosmin), requires a complex model which uses several
parameters founded in mechanistic theory. These mechanismbased parameters include physical conditions necessary for
nuisance algal growth, nutrient or chemical dynamics which
promote nuisance algal growth, and biotic stresses, such as
resource competition, which work to select specific nuisance
algae for exponential growth (e.g. Sterner, 1989 and Tilman et
al., 1982). Therefore, a mechanistic understanding of nuisance
algal bloom formation could be used to predict phytoplankton
abundance and seasonal phytoplankton succession to nuisance
algae, specifically, HC blue-greens (Fig. 1).

METHODS:
 Nutrient data from three eutrophic Midwest, urban
reservoirs of similar morphology were analyzed for trends in
[Combined N] (NH3-N + NH4-N) and [Total P].
 Nutrient and phytoplankton data from 3 stations in Ford
Lake (1998-2000) and 3 stations in Eagle Creek Reservoir
(ECR) (2003) were pooled then analyzed for empirical
relationships between nutrient concentrations and
phytoplankton growth as measured by [chlorophyll a] (Ford
Lake) and phytoplankton counts (ECR). (See maps.)
 2003 ECR nutrient and phytoplankton data were then
analyzed in the context of the proposed model.

1998-2000: Mean Monthly [Total P]
1976 - 1987 & 2003: Mean Monthly [Total P]
Ford Lake
Belleville Lake
140
2003
1980 - 1987
325
1976 - 1987
A
B
275
100
225
80
175
[Total P] (ug/L)
[Total P] (ug/L)
120
60
40
125
75
20
25
0
-25
-20
F
M
A
M
J
J
A
S
O
1998-2000: Mean Monthly [NO 3- + NH4+]
N
D
J
F
M
A
M
J
J
A
S
O
1976 - 1996 & 2003: Mean Montlhy [NO 3- + NH4+]
Ford Lake
A
N
D
B
Warm temperatures
High incident solar radiation
+ Quiescent water column
Deep Photic Zone
C
N Si
N
Si
P
Growth of specific algae in lake
C N
Si Silica Limiting
Growth of all algae in lake
Diatoms
Greens
C
P
N
P
Nitrogen Limiting
Growth of all algae in lake
Given P abundance, HC bluegreen algae will likely dominate
as they are able to fix
atmospheric N2.
Blue-Greens
Given Si abundance, diatoms will
likely dominate as they are better
competitors for N and P than
greens and blue-greens.
Diatoms
Bloom formation of HC blue-green algae
C Si
Blooms can lead to a
shading effect, thereby,
limiting the growth other
competing algae.
HC blue-greens such as Anabaena are
known taste and odor causing algae.
Blue-Greens
Greens
Given P and Si
abundance, HC
blue-green algae,
which can fix
atmospheric N2,
and diatoms,
which are better
competitors than
green algae for
scarce N when Si
is abundant, will
likely dominate.
High rates of N assimilation
effectively deplete N.
N
P
Nitrogen Limiting
Figure 1: Mechanistic model based on resource competition for limiting nutrients, describing seasonal phytoplankton succession to HC blue-green algae and
possible MIB and geosmin production. A diagrams a successional pattern in which green algae dominate during mid-summer; B shows a successional
pattern in which green algae are never able to become a significant portion of the phytoplankton community because Si abundance allows for high rates of
N assimilation by diatoms which leads to N-limited phytoplankton growth, a condition in which HC blue-greens are ideally suited to thrive.
STUDY SITES:
Both Ford Lake and Eagle Creek Reservoir have been documented as experiencing mid- to late Summer blooms of HC bluegreen algae: Ford Lake having yearly Aphanizomenon blooms and Eagle Creek Reservoir having a mixed bloom including
Anabaena, Aphanizomenon, and Cylindrospermopsis.

Ford Lake, Michigan
Belleville Lake, Michigan
Eagle Creek Reservoir, Indiana
Impoundment of the Huron River
Created in 1932
Area: 3.25 km2
Volume: 15,151,000 m3
Impoundment of the Huron River
Created in 1924
Area: 5.14 km2
Volume: 21,923,000 m3
Impoundment of Big Eagle Creek
Created in 1967
Area: 5.01 km2
Volume: 20,820,000 m3
(Tedesco et al., 2003)
Eutrophic
Eutrophic
2003
1990 - 1996
Belleville Lake
Warm temperatures
High incident solar radiation
+ Quiescent water column
Deep Photic Zone
C
P
Eutrophic
-75
J
HYPOTHESES:
 Small urban reservoirs undergo a transition from nitrogen rich, P-limited growth conditions to nitrogen poor, P-abundant
growth conditions.
 Given sufficient physical conditions for growth (i.e., water temperatures > 25 °C, abundant incident solar radiation, and
quiescent water,) , this transition in the nutritive environment spurs the growth of nuisance algal blooms of heterocystforming blue-green genera such as Anabaena, Aphanizomenon, and Cylindrospermopsis.
1980 - 1989
5
2.5
C
2.0
R2 = 0.5241
R2 = 0.5241
1976 - 1979
D
4.5
4
3.5
[NO3- + NH4+] (mg/L)
[NO3- + NH4+] (ug/L)
1.5
1.0
0.5
RESULTS:
 All three reservoirs showed that surface water [Tot P]
remained constant or slightly increased from June to October:
Ford and Bellville Lake [Tot P] showed no significant change at
=0.10; ECR [Tot P] increase was significant at =0.05 (Fig.
2A and 2B) .
 All three reservoirs showed that surface water [Combined N]
(NO3-N + NH4-N) significantly decreased from June to August
(Ford and Belleville Lakes at =0.10 and ECR at =0.05) (Fig.
2C and 2D).
 Historical mean monthly discharge from the major tributary to
ECR correlated more strongly to [Combined N] (R2 = 0.8892)
than to [Total P] (R2 = 0.1151) from April to October (Fig. 2H,
2D, and 2B): [Total P] significantly increased (=0.05) as
stream discharge from Big Eagle Creek was decreasing (Fig.
2H and 2B). This was not seen in Ford Lake data sets, which
showed that neither N or P correlated well with Huron River
discharge (Fig. 2G, 2C, and 2A).
 1998 – 2000 Ford and Belleville Lake molar N:P (NO3-N +
NH4-N to Total P), as well as ECR’s 1980-1987 molar N:P
(NO3-N + NH4-N to Total P) and 2003 molar N:P (TKN-N +
NO3-N to Total P) significantly decreased (= 0.10 and 0.5,
respectively) from mid- to late Summer (Fig. 2E and 2F).
 Ford Lake’s surface [Total P] was moderately positively
correlated to [chlorophyll a] using a linear regression (R2 =
0.5740) (Fig. 4A)
 ECR’s surface [Total P] was moderately positively related to
total phytoplankton concentrations as natural units/mL using a
linear regression (R2 = 0.4875) (Fig. 4B).
 Ford Lake’s surface [Combined N] was moderately correlated
to [chl a] using an exponential decay regression (R2 = 0.5241)
(Fig. 4C).
 ECR’s surface [Total N] (TKN+NO3-N) was weakly related to
total phytoplankton concentrations using an exponential decay
model (R2 = 0.3849) (Fig. 4D).
 Ford Lake’s molar surface N:P (NO3-N + NH4-N to Total P) was
strongly correlated to [chl a] using an exponential decay
model (R2 = 0.7089) (Fig. 4E).
 ECR’s surface molar N:P (TKN-N+ NO3-N to Total P) was
moderately related to total phytoplankton counts using an
exponential decay model (R2 = 0.5635) (Fig. 4F).
 In July and September, 2003, ECR reached N:P minima of
27N:1P and 9N:1P, respectively (Fig. 3F).
 ECR’s 2003 phytoplankton community structure was
dominated by diatoms throughout the year with HC bluegreens making up a large portion (34%) of the community on
July 23 (Fig. 3). (Phytoplankton growth was disrupted by
treatment with algaecide on April 30, June 11, July 25, and
October 16).

3
2.5
100
1.5
0.0
2003 Eagle Creek Reservoir [Total P] vs [Phytoplankton]
2003 Ford Lake [Total P] vs [Chlorophyll a]
2
A
70000
B
1
[Chlorophyll a] (g/L)
0
-1.0
J
F
M
A
M
J
J
A
S
O
N
J
D
F
M
A
M
J
J
A
S
O
N
Eagle Creek Reservoir: N-to-P Ratios
D
1980-1987
250
E
60000
80
0.5
2003
F
200
[Phytoplankton] (natural units)
-0.5
60
40
20
R2 = 0.5740
50000
40000
30000
20000
R2 = 0.4875
10000
N:P
150
0
0
100
0
20
40
50
1998 - 2000 Monthly Mean Streamflow
(USGS Gage #04174500, Huron River)
G
M
A
M
J
A
S
O
N
D
1976 - 1987 Monthly Mean Streamflow
(USGS Gage #03353200, Eagle Creek)
H
25
J
USGS DOQQ 1998
N
0
IMAGIS 2002
500 Meters
7
20
5
m 3 /s
m 3 /s
15
10
4
3
2
5
1
0
0
J
F
M
A
M
J
J
A
S
O
N
J
D
F
M
A
M
J
J
A
S
O
N
D
Figure 2: Mean monthly N, P, and N:P for Ford Lake, Belleville Lake, and
ECR. 2003 ECR N:P are in timescale (F). Stream discharge for Huron River
upstream of its inflow to Ford Lake and for Big Eagle Creek upstream of its
inflow to ECR. Dashed lines corresponding to nutrient concentrations
represent ±2 St.Dev. Horizontal red lines represent molar sestonic 22N:1P,
Healy and Hendzel (1980) threshold for N-limited phytoplankton growth (E
and F).
45000
40000
natural units/mL
35000
30000
25000
5000
Total
Chrysophyta
Chlorophyta
Euglenophyta
Non-HC Forming
HC Forming
/1
/2
0
03
03
/2
0
9/
10
10
/2
0
03
03
8/
13
/2
0
7/
28
/2
0
03
03
7/
23
03
/2
0
7/
2/
20
/2
0
03
6/
12
6/
11
/2
0
03
0
5/
29
100
Figure 3: 2003 ECR phytoplankton populations and community structure
from May 29 – October 1, 2003.
Acknowledgements:
Veolia Water Indianapolis, LLC White River Analytical Labs, especially D. Peterson.
Center for Earth and Environmental Science
L. Shrake, Project Coordinator
B.E. Hall, Systems Engineer
160
0
50
100
150
200
250
300
[Total P] (mg/L)
2003 Eagle Creek Reservoir [Total N] vs [Phytoplankton]
C
70000
80
D
60000
60
40
R2 = 0.5241
20
50000
40000
30000
R2 = 0.3849
20000
10000
0
0
0
2
4
6
8
10
0.0
0.5
1.0
1.5
[NO3-N + NH4-N] (mg/L)
100
2.0
2.5
3.0
3.5
4.0
[Total N] (mg/L)
2003 Eagle Creek Reservoir N:P vs [Phytoplankton]
2003 Ford Lake: N-toP Ratios vs [Chlorophyll a]
E
70000
F
60000
80
60
40
R2 = 0.7089
20
50000
40000
30000
R2 = 0.5635
20000
10000
0
0
0
100
200
300
N:P
10000
•
•
DISCUSSION AND CONCLUSIONS:
All three reservoirs showed an annual trend of N depletion and P abundance during mid- to late Summer.
This N scarcity compared to P occurred as phytoplankton production was increasing as seen exponential decay regressions.
This seems contrary to growth kinetics as decreasing the availability of a limiting nutrient should adversely affect phytoplankton
growth. However, Ford Lake (1998 – 2000) and ECR (2003) high phytoplankton biomass occurred when HC blue-green algae
(Anabaena and Aphanizomenon) were present in the water column.
2003 ECR data show a successional pattern that could be explained by Figure 1B, whereby high diatom (Asterionella,
Aulocoseira, Cyclotella, and Synedra) assimilation effectively depleted N. High N utilization compared to P by diatoms can be
significant: Asterionella’s N per cell mmol requirement is 100x greater than P (Lehman et. al., 1975). On July 23, when N:P
decreased below 22N:1P (Healy and Hendzel, 1980), a threshold for N-limited phytoplankton growth, the successional shift to
HC blue-green algae occurred. This mechanistic explanation was supported by the moderately strong empirical relationship
between N:P to phytoplankton counts. Variability in the model can be attributed to algaecide treatment in the reservoir which
disrupted phytoplankton population growth and acted to redistribute N in the water column, as well as the lack of taxa specific
thresholds for nitrogen limited growth: total phytoplankton counts represent many algal communities, whose growth limitation
and optimal growth conditions may occur at different N:P.
20000
15000
140
2003 Ford Lake [NO3-N + NH4-N] vs [Chlorophyll a]
N
Sample Sites
6
120
[Phytoplankton] (natural units)
500
F
100
[Total P] (g/L)
1000 Meters
0
J
80
[Phytoplankton] (natural units)
500
[Chlorophyll a] (g/L)
0
[Chlorophyll a] (g/L)
500
60
400
500
0
50
100
150
200
250
300
N:P
Figure 4: Empirical relationships between nutrients and phytoplankton biomass
In conclusion, data from three Midwest, urban reservoirs showed that N-to-P ratios could provide a better empirical model for
(Ford Lake - [chl a] and ECR – phytoplankton counts). Ford Lake (left) and ECR
predicting phytoplankton productivity in these systems than P or N alone. These reservoirs showed a stronger relationship
between phytoplankton growth and molar N-to-P ratios than to [P] or [N]. Furthermore, using resource competition theory, this (right).
model could also be used to predict phytoplankton succession to nuisance HC blue-green algae. As HC blue-green algae have
Works Cited:
Dillon, P.J., and Rigler, F., 1974. The phosphorus-chlorophyll relationship in lakes. Limnology and Oceanography. 19(5): 767-773.
an ecological advantage over non-N-fixing algae when N is limiting and P is abundant, they are ideally suited for exponential
Healy, F.P. and L.L. Hendzel. 1980. Physiological indicators of nutrient deficiency in lake phytoplankton. Can. J. Fish. Aquat Sci.
37: 442-453.
growth and bloom formation at low N:P. Therefore, rather than using P-only models to predict production in these systems,
Lehman, J.T., D.B. Botkin, and G.E. Likens. 1975. The assumptions and rationales of a computer model of phytoplankton
population dynamics. Limnology and Oceanography. 20(3) 343-364.
these reservoirs could be better modeled by utilizing N-to-P ratios and the mechanism by which HC blue-green algae would
Sterner, R.W. 1989. Resource competition during seasonal succession toward cyanobacteria. Ecology 70:229-245.
Tedesco, L.P., E.A. Atekwana, G. Filippelli, K. Licht, L.K. Shrake, B.E. Hall, D.L Pascual, J. Latimer, R. Raftis, D. Sapp, G. Lindsey,
become dominant. This data could then be applied to create long-term management models aimed at preventing the
R. Maness, D. Pershing, D. Peterson, K. Ozekin, C. Mysore, and M. Prevost. 2003. Water Quality and Nutrient Cycling in Three
Indiana Watersheds and Their Reservoirs: Eagle Creek/Eagle Creek Reservoir, Fall Creek/Geist Reservoir, and Cicero
occurrence of nuisance HC blue-green blooms in these eutrophic, urban reservoirs.

Creek/Morse Reservoir. Central Indiana Water Resources Partnership, CEES Publication 2003-01, IUPUI, Indianapolis, IN. 163
Ford and Belleville Lake research funded by a grant MDEQ (Michigan Department of Environmental Quality) and the University of Michigan
Eagle Creek Reservoir research funded by the CIWRP (Central Indiana Water Resource Partnership)
pp.
Tilman, D., S.S. Kilham and P. Kilham. 1982. Phytoplankton Community Ecology: The role of limiting nutrients. Annual Review of
Ecology and Systematics. 13: 349-372.