1

PHYTOPLANKTON BLOOM DYNAMICS IN A NITROGEN-LIMITED SUBTROPICAL LAKE

By

LINGHAN DONG

A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT

OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE

UNIVERSITY OF FLORIDA

2010

2

© 2010 Linghan Dong

3

To my Mom

4

ACKNOWLEDGMENTS

I thank my parents for supporting my writing mentally. I appreciate the academic

instruction from Dr. Edward Phlips, Dr. Mark Brenner and Dr. Karl Havens. Special

thanks are given to Dr. Mary Cichra for algal taxonomy training. I also appreciate the

help offered by people working in Phlips lab.

5

TABLE OF CONTENTS

ACKNOWLEDGMENTS ...................................................................................................... 4

page

LIST OF TABLES ................................................................................................................ 6

LIST OF FIGURES .............................................................................................................. 7

LIST OF ABBREVIATIONS ................................................................................................ 9

ABSTRACT........................................................................................................................ 10

CHAPTER

1 INTRODUCTION ........................................................................................................ 12

2 METHODS .................................................................................................................. 15

Site Description ........................................................................................................... 15 Sampling Regime ....................................................................................................... 15 Sampling Collection and Analysis .............................................................................. 16 Statistical Analysis ...................................................................................................... 17

3 RESULTS.................................................................................................................... 18

4 DISCUSSION .............................................................................................................. 44

Cyanobacterial Dominance ........................................................................................ 46 Succession Patterns ................................................................................................... 48

LIST OF REFERENCES ................................................................................................... 50

BIOGRAPHICAL SKETCH................................................................................................ 53

6

LIST OF TABLES

Table

page

3-1 Pearson’s correlation between day time total phytoplankton biovolume and different environmental variables, LAG and LEO.................................................. 43

3-2 Pearson’s correlation between nitrogen fixing cyanobacteria biovolume and nitrogen related chemical parameters, LAG and LEO .......................................... 43

7

LIST OF FIGURES

Figure

page

3-1 Map of Lake George .............................................................................................. 22

3-2 Rainfall in the Lake George Basin ......................................................................... 22

3-3 Day time water depths at LAG and LEO ............................................................... 23

3-4 Day time water temperature at LAG and LEO ...................................................... 23

3-5 Day time colored dissolved organic matter (CDOM) levels at LAG and LEO ...... 24

3-6 Day time water turbidity at LAG and LEO ............................................................. 24

3-7 Secchi depth at LAG and LEO............................................................................... 25

3-8 Day time total nitrogen concentrations at LAG and LEO ...................................... 25

3-9 Day time nitrate+nitrite (NOx) concentration at LAG and LEO ............................. 26

3-10 Day time ammonium concentrations at LAG and LEO ......................................... 26

3-11 Day time total phosphorus concentrations at LAG and LEO ................................ 27

3-12 Day time soluble reactive phosphorus (SRP) concentrations at LAG and LEO .. 27

3-13 Day time silica concentrations at LAG and LEO ................................................... 28

3-14 Day time phytoplankton biovolume at LAG and LEO. .......................................... 29

3-15 Day time cyanobacteria biovolume at LAG and LEO ........................................... 30

3-16 Relative biovolume of Cyanobacteria in phytoplankton community at LAG and LEO.................................................................................................................. 31

3-17 Relationship between biovolume of Cyanobacteria and total phytoplankton biovolume, LAG and LEO ...................................................................................... 32

3-18 Day time trends of diatom and cyanobacteria biovolume and silica concentrations, LAG and LEO ............................................................................... 33

3-19 Trends of biovolume of three groups of cyanobacteria: Anabaena spp.+Anabaenopsis spp.+Aphanizomenon spp.; Cylindrospermopsis sp.; other non-heterocystous cyanobacteria, LAG and LEO ...................................... 34

8

3-20 Trends of temperature and bivolume of three groups of cyanobacteria: Anabaena spp.+Anabaenopsis spp. +Aphanizomenon spp.; Cylindrospermopsis sp.; other non-heterocystous cyanobacteria, LAG and LEO ......................................................................................................................... 35

3-21 Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and total nitrogen concentrations, LAG and LEO ............................... 36

3-22 Trends of total phytoplankton biovolume and nitrate+nitrite (NOx) concentrations, LAG and LEO .............................................................................. 37

3-23 Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and ammonium concentrations, LAG and LEO................................... 38

3-24 Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and total phosphorus concentrations, LAG and LEO ......................... 39

3-25 Trends of total phytoplankton biovolume and soluble reactive phosphorus (SRP) concentration, LAG and LEO ...................................................................... 40

3-26 Ratios of estimated phytoplankton phosphorus and SRP to total phosphorus, LAG and LEO ......................................................................................................... 41

3-27 Ratio of estimated phytoplankton nitrogen and DIN to total nitrogen, LAG and LEO ......................................................................................................................... 42

9

LIST OF ABBREVIATIONS

DIN Dissolved inorganic nitrogen

NOx Nitrate and nitrite

SRP Soluble reactive phosphorus

TN Total nitrogen

TP Total phosphorus

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Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science

PHYTOPLANKTON BLOOM DYNAMICS IIN A NITROGEN-LIMITED SUBTROPICAL

LAKE

By

Linghan Dong

August 2010

Chair: Edward Phlips Major: Interdisciplinary Ecology

The focus of this study was Lake George, a eutrophic lake in Florida, which has

experienced major algal blooms for decades. Phytoplankton blooms in the lake are

typically dominated by cyanobacteria. The goal of the study was to examine the

dynamics of a major bloom event within the context of variations in physical, chemical

and biological conditions. A temporally intensive sampling regime was used to reveal

successional patterns in phytoplankton composition and abundance at scales

appropriate to the growth of phytoplankton. Two major bloom periods were observed

over the study period. The first bloom was dominated by a mix of diatoms and several

nitrogen-fixing species of cyanobacteria, including Anabaena spp., Aphanizomenon

spp. and Anabaenopsis spp. The second, and larger, bloom was dominated by the

nitrogen-fixing cyanobacterium Cylindrospermopsis sp. These observations

demonstrate the importance of nitrogen fixation in supplying the nitrogen needed to

support primary production in the lake. Statistical correlation analyses showed

relationships between phytoplankton structure and environmental factors, emphasizing

the impact of bioavailable nitrogen concentrations, Si concentrations and temperature.

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The results of this research hav significant implications for future efforts to manage the

ecology of Lake George, in an effort to prevent the continued proliferation and

intensification of cyanobacterial blooms.

12

CHAPTER 1 INTRODUCTION

One common symptom of eutrophication in aquatic systems is algal blooms. Many

ecosystems around the world are experiencing increased rates of eutrophication due to

rapid agricultural and industrial development, population expansion and urbanization

(Paerl and Huisman, 2009). The essential role of nutrient load in eutrophication has

focused attention on the relative importance of different macronutrients in controlling

phytoplankton productivity, with nitrogen and phosphorus generally receiving the most

attention. One long standing paradigm is that phosphorus is more often limiting in lakes

than nitrogen (Einsele, 1941; Schindler, 1977; Schindler et al., 2008; Vollenweider,

1971; Vollenweider and Kerekes, 1982). Evidence for the importance of phosphorus

includes stoichiometric relationships between nitrogen and phosphorus (Hutchinson,

1957; Pearsall, 1930) and the correlation between total phosphorus (TP) and

chlorophyll-a (Chl-a) (Dillon and Rigler, 1974; Sakamoto, 1966). The importance of

phosphorus limitation has been further supported through whole lake fertilization

experiments by Schindler (Schindler, 1974; Schindler, 1977). Despite the evidence for

the role of phosphorus as a limiting factor, other researchers have shown that nitrogen

availability also impacts phytoplankton dynamics in many freshwater ecosystems (Lewis

Jr and Wurtsbaugh, 2008; Paerl and Huisman, 2009). For instance, many tropical and

subtropical lakes have low N: P ratios, an indicator of nitrogen limitation (Ryding and

Rast, 1989). The results of nutrient limitations bioassay experiments also support the

existence of nitrogen limitation in phosphorus-rich eutrophic lakes in Florida, such as

Lake Okeechoobee (Aldridge et al., 1995; Phlips et al., 1997), Lake Griffin (Phlips et al.,

2004) and Lake George (Piehler et al., 2009) . In these Florida lakes, nitrogen-fixing

13

cyanobacteria are often prominent members of the phytoplankton community, a

response to nitrogen limitation. Questions remain about whether nitrogen fixation can

provide sufficient nitrogen input to phosphorus enriched ecosystems to ultimately induce

phosphorus limitation of phytoplankton growth and biomass, making nitrogen limitation

a short-term phenomenon, ultimately leading to phosphorus limitation in the long term. If

so, management of nitrogen input to lakes would not aid in the reduction of trophic state

(Schindler et al., 2008). Some, however, argue that nitrogen fixation cannot fully make

up for nitrogen limitation in many ecosystems due to physical, biological and chemical

limitations on the process (Lewis Jr and Wurtsbaugh, 2008; Paerl and Huisman, 2009),

leading to the conclusion that it is important to consider both nitrogen and phosphorus

loads in management efforts. The goal of this study was to examine the dynamics of

phytoplankton bloom events in a lake subject to nitrogen-limiting conditions, and follow

the dynamics of key physical and chemical parameters, in an effort to evaluate the

response of the phytoplankton community.

A subtropical eutrophic lake in Florida, Lake George, was the focus of the study

because of the existence of a long record for nutrient and phytoplankton composition

and a demonstrated history of cyanobacterial blooms under nitrogen-limiting conditions

(Piehler et al., 2009). Given its shallow depth and long water residence times, Lake

George falls into the category of a number of large phosphorus-rich lakes in Florida,

such as Lake Okeechoobee (Aldridge et al., 1995; Phlips et al., 1997), Lake Apopka

and Lake Griffin (Phlips et al., 2004), and in other subtropical regions around the world,

e.g., Lake Taihu and Donghu in China and Lake Kasumigaura in Japan (Havens et al.,

2001). Along with a historical record of intense cyanobacteria blooms, nitrogen limitation

14

seems to be an important factor in phytoplankton dynamics in Lake George (Piehler et

al., 2009). A temporally intensive sampling regime was employed in this study, to

provide a detailed view of the dynamics of blooms in Lake George.

Several hypotheses were examined in this study:

1. Large phosphorus loads to Lake George from the watershed are sufficient to support high algal biomass.

2. High phytoplankton biomass favors dominance of cyanobacteria.

3. Low bioavailable nitrogen load relative to bioavailable phosphorus load increases the potential for nitrogen limitation of algal growth, leading to prominence of nitrogen-fixing cyanobacteria.

4. Succession of phytoplankton species is correlated to shifts in key environmental conditions, including temperature, light flux and biologically available nitrogen, phosphorus and silica.

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CHAPTER 2 METHODS

Site Description

The St. Johns River is the longest blackwater river in Florida. It is unique for its low

elevation drop (8m) from its headwaters to mouth, resulting in low river flow rates (1-2

km day-1). The gentle slope of the river bed has resulted in the creation of many wide,

shallow pools, which are called “lakes” of the St. Johns River (Livingston, 1990). The

largest lake is Lake George, with an area of 18,934 ha (Piehler et al., 2009). Located

210 km from the river mouth, Lake George is the upstream lake, which is most

susceptible to tidal forces. Tidal forces and shallow river slope result in prolonged water

retention times in Lake George, which can exceed one month (Livingston, 1990).

The upper St. Johns River is the dominant source of water for Lake George. High

concentrations of nitrogen and phosphorus in the source water result in eutrophic

conditions in Lake George (Livingston, 1990). The rich nutrient supply, coupled with

long residence time, particularly in spring and summer (April-July) (Piehler et al., 2009),

provide conditions conducive to the formation of phytoplankton blooms (Phlips et al.,

2007).

Sampling Regime

Water samples were collected twice per week during the day time and once per

week at night from two sites, LAG and LEO, which are situated in the southern and

central region of the lake channel. Sampling was conducted from March 25th to June

23rd 2009. Biweekly sample collection was suspended from Mar 26th to April 14th and

from May 15th to 25th.

16

Sampling Collection and Analysis

Secchi depth was measured at every day-time sample collection. Parameters,

including temperature, conductivity, dissolved oxygen (DO), and pH, were measured by

Hydrolab probe from the water surface to just above the bottom at 0.5m intervals.

Five poles of depth-integrated samples were collected around the boat and then

combined in a plastic bucket. After complete agitation, lake water was transferred to

individual sample containers, 1000 ml brown plastic bottles for phytoplankton samples

and 100 ml white plastic bottles for water chemistry samples. Lugols-solution was used

for phytoplankton preservation, pipets for each bottle, followed by complete mixing.

Phytoplankton composition was determined using the Utermöhl method (Utermöhl,

1958). Lugol solution preserved samples were settled in 19mm inner diameter

cylindrical chambers. Phytoplankton cells were identified and counted at 400X and

100X with a Nikon phase contrast inverted microscope. At 400X, a minimum of 100

cells of a single taxon and 30 grids were counted. If 100 cells were not counted by 30

grids, up to a maximum of 100 grids were counted until one hundred cells of a single

taxon was reached. At 100X, a total bottom count was completed for taxa > 30 microns.

Biovolume (µm3 ml-1) is used as the primary measure phytoplankton biomass (Smayda,

1978).

Total nitrogen was colorimetrically determined using the persulfate digestion

method (APHA, 1989) with a Bran-Luebbe AutoAnalyzer. Nitrate, nitrite and ammonium

were colorimetrically determined using standard methods (APHA, 1989) with a Bran-

Luebbe AutoAnalyzer. Total phosphorus was colorimetrically determined using the

persulfate digestion method (APHA, 1989), with a Hitachi scanning spectrophotometer.

17

Soluble reactive phosphorus was colorimetrically determined using standard methods

(APHA, 1989) with a Hitachi scanning spectrophotometer. Chlorophyll a concentration

was colorimetrically determined after extraction of the filtered samples with 90% warm

ethanol (Sartory and Grobbelaar, 1984), with a Hitachi scanning spectrophotometer.

Water color was determined from filtered station water (0.7µm glass-fiber filter).

Samples were analyzed using platinum cobalt standards from protocols described in

Standard Methods (APHA, 1989) on a Hitachi scanning spectrophotometer. Turbidity

was determined with a La Motte turbidity meter.

Statistical Analysis

SAS 9.2 was used for Pearson’s Correlation Coefficient calculation. Graphs

showing trends and linear relationships were created by Microsoft Office Excel 2007.

18

CHAPTER 3 RESULTS

Several small peaks in rainfall in the Lake George (Figure 3-1) region were

recorded from March 29th through May 13th (Figure 3-2). A major rainfall event

occurred in late May, followed by smaller events in June.

Water depth remained stable around 3.0 m at LAG and 3.4 m at LEO until a near 1

m raise from May 16th to 20th (Figure 3-3). Water temperatures during the sampling

period increased gradually from 20 to near 30 ℃ from March 25th to May 10th at both

sites (Figure 3-4). Colored dissolved organic matter (CDOM) declined gradually from

100 PCU on March 25th to near 50 PCU on May 27th at both stations before increasing

again (Figure 3-5). The increase in CDOM was greater at LAG than LEO. Turbidity

ranged between 4 to 10 NTU at both stations (Figure 3-6), with several peaks in value.

Peaks in turbidity were higher at LAG than LEO. Secchi depth at both stations ranged

between 0.6 and 1.0 m (Figure 3-7). The deepest Secchi depths were observed in the

April and early May (Figure 3-7).

Total nitrogen (TN) concentration increased over the study period from 0.8 to over

1.2 mg L-1 at both stations. Peaks in TN concentration were generally higher at LEO

than LAG in the last half of the study period (Figure 8). Nitrate + nitrite concentration

(NOx) declined gradually from 0.014 mg L -1on March 25th to below 0.005 mg L-1 on

May 1st at both stations, before increasing in early June (Figure 3-9). The June

increase in NOx concentration was greater at LAG than LEO. Ammonium concentration

increased over the study period from near 0.05 mg L-1 to greater than 0.15 mg L-1 at

both LAG and LEO (Figure 3-10).

19

TP concentrations remained near 0.05 mg L-1 until June at both LAG and LEO,

before increasing substantially. LAG showed greater variability than LEO (Figure 3-11).

Soluble reactive phosphorus (SRP) concentrations remained near 0.010 mg L-1 at both

stations until June then increased substantially reaching 0.100 mg L-1 at LAG and 0.05

at LEO (Figure 3-12).

Silica concentrations showed a trend similar to SRP, remaining low concentrations

below or near 0.5 mg L-1 at both stations until a significant increase in late May (Figure

3-13).

Total phytoplankton biovolume at the two stations showed two peaks, a smaller

one in mid-April and larger one extending through most of May (Figure 3-14). At LEO

the second bloom period extended into early June and reached 50% higher biovolume

than the second bloom at LAG. During the first bloom period, the relative contributions

of cyanobacteria and diatoms to total biovolume were similar. However, the second

bloom period was dominated by cyanobacteria (Figure 3-14).

Within the cyanobacteria community, the first bloom period was dominated by the

nitrogen-fixing taxa Anabaena spp., Anabaenopsis spp. and Aphanizominon spp.

(Figure 3-15). During the second bloom period, the former taxa were initially important

but progressively gave way to increased dominance by another heterocystous

cyanobacterium, Cylindrospermopsis sp.and other non-nitrogen-fixing cyanobacteria,

particularly Oscillatoria spp. (Figure 3-15).

The relative contribution of cyanobacteria to total phytoplankton biovolume

increased significantly at both LAG and LEO from March 25th through April (Figure 3-

16). From the end of April through the beginning of June, cyanobacteria generally

20

represented over 80% of total phytoplankton biovolume. In June, cyanobacteria

dominance declined somewhat at LAG, but remained high at LEO (Figure 3-16).

For both stations, high linear regression was shown between biovolume of

cyanobacteria and total phytoplankton biovolume, with r2 above 0.95(Figure 3-17).

Diatoms showed a drop in biovolume immediately after the decrease of silica

concentrations in April and remained at low levels for the rest of the study period,

despite a sharp increase in silica concentrations at the beginning of June. (Figure 3-18)

Within the cyanobacteria assemblage, the major groups of taxa had distinct

temporal patterns of abundance. The heterocystous species Anabaena spp.,

Aphanizomenon spp. and Anabaenopsis spp. had two distinct peaks in abundance in

mid-April and early May at both stations (Figure 3-19). The biovolume of the

heterocystous species Cylindrospermopsis sp. increased dramatically in mid-May,

reaching peak levels in early June at both sites (Figure 3-19). Non-heterocystous

cyanobacteria, most prominently Oscillatoria spp. (Planktothrix spp.), gradually

increased in biovolume until June at both sites (Figure 3-19)

The emergence of Cylindrospermopsis sp. and crash of Anabaena spp.

+Aphanizomenon spp. +Anabaenopsis spp. group coincided with the maximum rate of

increase in temperature (Figure 3-20).

The relationship between temporal trends in phytoplankton biovolume and trends

in nutrient concentrations varied according to forms of nitrogen and phosphorus. Total

nitrogen concentrations increased coincident with increasing biovolume of both total

phytoplankton and nitrogen-fixing cyanobacteria until the dissipation of the second

bloom in June (Figure 3-21), which was accompanied by a decline in TN. By contrast,

21

NOx concentrations declined to near detection levels at both stations from March to the

end of May (Figure 3-22). Concentrations showed a sharp increase after the collapse of

the second phytoplankton bloom in June (Figure 3-22). Ammonium concentrations were

highly variable at both stations, but generally increased over the study period (Figure 3-

23).

Total phosphorus concentrations remained near 0.05 mg L-1 at both stations

through most of the study period until the dissipation of the second phytoplankton bloom

period in June (Figure 3-24), which was accompanied by a sharp increase in TP. TP

concentrations were more variable at LAG than at LEO. Soluble reactive phosphorus

concentrations remained near 0.010 mg L-1 at both stations from March to the end of

May and then increased substantially after the dissipation of the second phytoplankton

bloom in June (Figure 3-25).

Pearson’s correlation analyses showed that log phytoplankton biovolume was

significantly correlated to SRP, NOx, TN, Turbidity and TN: TP ratio at LAG. At LEO, log

biovolume was significantly correlated to NOx, TN, Turbidity and Secchi Depth (Table 3-

1). Correlations between nitrogen-fixing cyanobacteria biovolume and nitrogen

compounds were also examined (Table 3-2). At LAG, log nitrogen-fixing cyanobacteria

biovolume was negatively correlated with NH4 and NOx. At LEO, log nitrogen-fixing

cyanobacteria biovolume was negatively correlated with NOx and positively correlated

with TN (Table 3-2).

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Figure 3-1. Map of Lake George

Figure 3-2. Rainfall in the Lake George Basin

0

1

2

3

4

5

6

7

8

9

Rain

fall

(cm

)

23

Figure 3-3. Day time water depths at LAG and LEO

Figure 3-4. Day time water temperature at LAG and LEO

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

LEO

LAG

Wat

erde

pth

(m)

0

5

10

15

20

25

30

35

Tem

pera

ture

(℃)

LAG

LEO

24

Figure 3-5. Day time colored dissolved organic matter (CDOM) levels at LAG and LEO

Figure 3-6. Day time water turbidity at LAG and LEO

0

50

100

150

200

250

CDO

M(P

CU)

LAG

LEO

0

2

4

6

8

10

12

Turb

idity

(NTU

)

LAG

LEO

25

Figure 3-7. Secchi depth at LAG and LEO

Figure 3-8. Day time total nitrogen concentrations at LAG and LEO

0

0.2

0.4

0.6

0.8

1

1.2

Secc

hide

pth

(m) LAG

LEO

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

TN(m

g L-1

)

LAG

LEO

26

Figure 3-9. Day time nitrate+nitrite (NOx) concentration at LAG and LEO

Figure 3-10. Day time ammonium concentrations at LAG and LEO

0.00

0.01

0.02

0.03

0.04

0.05

0.06

NO

X(m

g L-1

)

LEO

LAG

0.00

0.05

0.10

0.15

0.20

0.25

NH

4(m

g L-1

)

LAGLEO

27

Figure 3-11. Day time total phosphorus concentrations at LAG and LEO

Figure 3-12. Day time soluble reactive phosphorus (SRP) concentrations at LAG and LEO

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

TP (m

g L-1

)

LEO

LAG

0.00

0.02

0.04

0.06

0.08

0.10

0.12

SRP

(mg

L-1) LAG

LEO

28

Figure 3-13. Day time silica concentrations at LAG and LEO

0

1

2

3

4

5

6

Si(m

g L-1

)

LAG

LEO

29

A

B

Figure 3-14. Day time phytoplankton biovolume at LAG (A) and LEO (B). The community is divided into four groups, cyanobacteria, diatoms, green algae and other phytoplankton taxa

0

2

4

6

8

10

12

14

16

18

Phyt

opla

nkto

n bi

ovol

ume

(106 µm

3m

l-1)

Other

Green

Diatoms

Cyanobacteria

LAG

0

2

4

6

8

10

12

14

16

18

Phyt

opla

nkto

n bi

ovol

ume

(106 µm

3 m

l-1)

Other

Green

Diatoms

Cyanobacteria

LEO

30

A

B

Figure 3-15. Day time cyanobacteria biovolume at LAG (A) and LEO (B). The cyanobacteria community is divided into four groups, Cylindrospermopsis sp.; Oscillatoria spp.; Anabaena spp.+ Anabaenopsis spp.+Aphanizomenon spp.; other cyanobacteria

0

2

4

6

8

10

12

14

Biov

olum

e (1

06 µm

3m

l-1)

Other Cyano

Ana+Aphan

Oscil

Cyl

LAG

0

2

4

6

8

10

12

14

Biov

olum

e (1

06 µm

3 m

l-1)

Other Cyano

Ana+Aphan

Oscil

Cyl

LEO

31

Figure 3-16. Relative biovolume of Cyanobacteria in phytoplankton community at LAG and LEO

0102030405060708090

100

% C

yano

bact

eria

Biov

olum

e

LAG

LEO

32

A

B

Figure 3-17. Relationship between biovolume of Cyanobacteria and total phytoplankton biovolume, LAG (A) and LEO (B)

y = 0.9707x - 901939R² = 0.9565

0

2

4

6

8

10

12

14

0 5 10 15

Cyan

obac

teri

a b

iovo

lum

e, 1

06 µm

3 ml-1

Phytoplankton biovolume, 106 µm3 ml-1

LAG

y = 0.971x - 928565R² = 0.9713

0

2

4

6

8

10

12

14

0 5 10 15

Cyan

obac

teri

a b

iovo

lum

e, 1

06 µm

3m

l-1

Phytoplankton biovolume, 106 µm3 ml-1

LEO

33

A

B

Figure 3-18. Day time trends of diatom and cyanobacteria biovolume and silica concentrations, LAG (A) and LEO (B)

0

1

2

3

4

5

6

0

2

4

6

8

10

12

14

Biov

olum

e, 1

06 µm

3m

l-1

Diatom

Cyanobacteria

Si

Si, mg L-1

LAG

0

1

2

3

4

5

6

0

2

4

6

8

10

12

14

Biov

olum

e, 1

06 µm

3m

l-1

Diatom

Cyanobacteria

Si

Si, mg L-1

LEO

34

A

B

Figure 3-19. Trends of biovolume of three groups of cyanobacteria: Anabaena spp.+Anabaenopsis spp.+Aphanizomenon spp.; Cylindrospermopsis sp.; other non-heterocystous cyanobacteria, LAG (A) and LEO (B)

0

2

4

6

8

10

12

Biov

olum

e (1

06 µm

3 m

l-1)

Ana+Aph

Cylindrospermopsis

Non Het

LAG

0

2

4

6

8

10

12

Biov

olum

e (1

06 µm

3 m

l-1)

Ana+Aph

Cylindrospermopsis

Non Het

LEO

35

A

B

Figure 3-20. Trends of temperature and bivolume of three groups of cyanobacteria: Anabaena spp.+Anabaenopsis spp. +Aphanizomenon spp.; Cylindrospermopsis sp.; other non-heterocystous cyanobacteria, LAG (A) and LEO (B)

0

5

10

15

20

25

30

35

0

2

4

6

8

10

12

Biov

olum

e, 1

06 µm

3m

l-1

Ana+Aph

Cylindrospermopsis

Non Het

Temperature

℃

LAG

0

5

10

15

20

25

30

35

0

2

4

6

8

10

12

Biov

olum

e, 1

06 µm

3m

l-1

Ana+Aph

Cylindrospermopsis

Non Het

Temperature

℃

LEO

36

A

B

Figure 3-21. Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and total nitrogen concentrations, LAG (A) and LEO (B)

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Figure 3-22. Trends of total phytoplankton biovolume and nitrate+nitrite (NOx) concentrations, LAG (A) and LEO (B)

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Figure 3-23. Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and ammonium concentrations, LAG (A) and LEO (B)

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Figure 3-24. Trends of total phytoplankton biovolume, nitrogen fixing cyanobacteria biovolume and total phosphorus concentrations, LAG (A) and LEO (B)

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Figure 3-25. Trends of total phytoplankton biovolume and soluble reactive phosphorus (SRP) concentration, LAG (A) and LEO (B)

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Figure 3-26. Ratios of estimated phytoplankton phosphorus and SRP to total phosphorus, LAG (A) and LEO (B)

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Figure 3-27. Ratio of estimated phytoplankton nitrogen and DIN to total nitrogen, LAG (A) and LEO (B)

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43

Table 3-1. Pearson’s correlation between day time total phytoplankton biovolume (log transformation of phytoplankton biovolume is used for the third column) and different environmental variables, LAG (top) and LEO (bottom)

LAG Correlation Correlation(log(biov)) SRP -0.45 (0.06) -0.48 (0.04) TP -0.45 (0.06) 0.11 (0.68) NH4 -0.12 (0.63) 0.40 (0.10) NOX -0.55 (0.02) -0.49 (0.04) TN 0.42 (0.08) 0.67 (0.002) DIN -0.23 (0.35) 0.30 (0.22) Turbidity 0.54 (0.02) 0.69 (0.002) Color -0.53 (0.02) -0.29 (0.24) TN/TP 0.45 ( 0.06) 0.53 ( 0.02) Secchi depth -0.04 (0.88) -0.01 (0.97) DO(top) 0.44 (0.09) 0.35 (0.19) DO(bottom) 0.28 (0.28) 0.23 (0.37) Temperature 0.16 (0.53) 0.15 (0.55) LEO Correlation Correlation(log(biov)) SRP 0.13 (0.61) 0.16 (0.54) TP 0.07 (0.79) 0.11 (0.68) NH4 0.32 (0.19) 0.40 (0.10) NOX -0.49 (0.04) -0.49 (0.04) TN 0.66 (0.003) 0.67 (0.002) DIN 0.23 (0.36) 0.30 (0.22) Turbidity 0.64 (0.004) 0.69 (0.002) Color -0.28 (0.26) -0.29 (0.24) TN/TP 0.44 (0.07) 0.44 (0.07) Secchi depth -0.50 (0.04) -0.54 (0.02) DO(top) 0.31 (0.22) 0.28 (0.28) DO(bottom) 0.22 (0.40) 0.10 (0.70) Temperature 0.28 (0.26) 0.37 (0.13) Table 3-2. Pearson’s correlation between nitrogen fixing cyanobacteria biovolume and

nitrogen related chemical parameters, LAG (top) and LEO (bottom) LAG Correlation Correlation(log(biov)) NH4 -0.11 (0.65) -0.47 (0.05) NOX -0.48 (0.05) -0.78 (0.0001) TN 0.44 (0.07) 0.10 (0.68) LEO Correlation Correlation(log(biov)) NH4 0.36 (0.14) 0.19 (0.45) NOX -0.44 (0.07) -0.61 (0.008) TN 0.71 (0.0009) 0.57 (0.01)

44

CHAPTER 4 DISCUSSION

High phytoplankton biomass was observed during our sampling period in Lake

George. Phytoplankton blooms are a regular wet season phenomenon in Lake George

(Phlips et al., 2000), as they are in many eutrophic lakes in subtropical and tropical

regions of the world (Havens et al., 2001). Both edaphic and anthropogenic factors

contribute to the high phosphorus loads that support blooms in Lake George

(Hendrickson et al., 2003). External nitrogen loads are relatively smaller than

phosphorus loads (Hendrickson et al., 2003). This is illustrated by the more than two-

fold increase in TP concentrations at LAG following the rainfall-induced increase in

water inputs from the upper St. Johns River to Lake George in late May, compared to

only a 30% increase in TN concentration. The consequences of the excess phosphorus

load are reflected in several structural and functional characteristics of the

phytoplankton community in Lake George.

One important functional feature is the common observation of nitrogen-limiting

conditions for phytoplankton growth in the lake (Piehler et al., 2009). The existence of

nitrogen-limiting conditions explains the important role that heterocystous cyanobacteria

play in the phytoplankton community of Lake George, as revealed in this study and in

previous studies (Piehler et al., 2009). As might be expected, the blooms of

heterocystous cyanobacteria have been shown to be associated with high rates of

nitrogen fixation (Doron, 2010). Nitrogen fixation rates observed during the summer of

2008 were sufficient to account for all of the deficits in nitrogen load to Lake George

estimated by nutrient load modeling carried out by the St. Johns River Water

Management District (Doron, 2010).

45

In terms of the potential for phosphorus limitation, SRP concentrations remained

relatively constant between 0.010 and 0.020 mg P L-1 through most of both bloom

periods, suggesting that phosphorus was not a limiting nutrient for phytoplankton

growth. In addition, the increasing ratio of estimated phytoplankton phosphorus to TP

showed that as phytoplankton biomass increased, more phosphorus was incorporated

into algal cells. Along with the trend of phytoplankton phosphorus to TP ratios, the ratios

of SRP to TP showed a similar increasing trend, which indicates a lack of phosphorus-

limitation of phytoplankton growth during the study period. Unfortunately, the bloom

observed during the study period was cut short by a freshwater flushing event

subsequent to high rainfall at the end of May. Without the disruption of the bloom

caused by dilution, phosphorus limitation might eventually have been observed. The

potential for periods of phosphorus limitation is indicated by the combination of high

phytoplankton phosphorus to TP and low SRP to TP ratios during some other major

bloom peaks observed over the historical data record (Phlips, unpublished data).

The results of this study also highlight the importance of rainfall conditions on

bloom dynamics. The influences of precipitation on phytoplankton dynamics are multi-

faceted and depend on the intensity, duration and timing of the events (Phlips et al.,

2007). Large rainfall events, such as the one observed in late May during this study,

substantially increased inputs of water to Lake George containing high phosphorus

concentration, but relatively low nitrogen levels. Such events cause a dilution of

phytoplankton biomass in the lake and displacement of the bloom water downstream

into the lower St. Johns River, thereby reducing water residence times in the lake and

river (Phlips et al., 2000; Phlips et al., 2007). More moderate rainfall events, as

46

observed in April, can introduce pulses of bioavailable nutrients to the lake, but do not

substantially reduce water residence time, allowing for a bloom response within the

lake.

Cyanobacterial Dominance

The phytoplankton blooms observed in Lake George during the study period were

dominated by cyanobacteria, which matches the historical record in the St. Johns River

System (Phlips et al., 2007). Strong correlations between cyanobacterial biomass and

total algal biomass have been observed in Florida lakes (Canfield et al., 1989). The

same pattern was found in Lake George. Strong linear regression relationships were

observed for both stations, with r2 values above 0.95. Several environmental conditions

in Lake George favor dominance by cyanobacteria. Factors that may be responsible for

the dominance of cyanobacteria at high phytoplankton biovolumes include their

preference for high temperature, ability to compete for inorganic carbon at high pH,

adaptability to environments with high light attenuation, and lack of requirement for

silica.

Cyanobacteria generally exhibit optimal growth rates at higher temperatures than

many other phytoplankton groups, usually in excess of 25oC (Paerl and Huisman,

2009). Therefore, at high temperatures, cyanobacteria have a competitive advantage

over many eukaryotic phytoplankton species (De Senerpont Domis et al., 2007; Elliott et

al., 2006; Joehnk et al., 2007). In other words, as the growth rate of other groups

declines with temperatures greater than 25oC, cyanobacteria growth rates go up (Paerl

and Huisman, 2009). The temperature in Lake George increased over the study period,

which might favor the dominance of cyanobacteria. Since the temperature preferences

47

of the cyanobacteria and eukaryotic algae in Lake George are not known, it is difficult to

confirm this hypothesis.

Planktonic cyanobacteria grow at near optimal rates at high pHs (i.e. 7-9) (Kratz

and Myers, 1955). The high pH values (i.e., 8-9.5) observed during our study, reflect

high photosynthetic activity. At high pH, soluble CO2 in water is low, which places a

premium on the ability of algae to use bicarbonate as a source of carbon for

photosynthesis. The ability of many cyanobacteria to efficiently use bicarbonate has

been proposed as one explanation for the dominance of cyanobactria in eutrophic

ecosystems (Shapiro, 1973; Shapiro, 1990; Shapiro, 2007).

Secchi depths in Lake George are shallow, ranging from 0.6 to 1 m during the

study period. The largest contributers to light attenuation in Lake George are CDOM,

tripton (none algal suspended solids), and phytoplankton (Phlips et al., 2000). Based on

Secchi disk values, the depth of the euphotic zone in the lake is about half the depth of

the mixed-layer, indicating that light availability may contribute to the competition

between algal species and successional patterns. The ability of many planktonic

cyanobacteria to adjust their position in the water column using the regulation of gas

vesicles, represent a selective advantage in shallow euphotic zones (Oliver et al.,

2000), particularly during the summer when average wind intensities are relatively low in

Florida. In addition, low light flux also favors dominance of cyanobacteria, because of

their lower light requirements for growth compared to many other algal groups (Smith,

1986).

A possible reason for cyanobacteria dominance over diatoms in Lake George is

the potential for silica limitation. The drop in diatom biovolume observed immediately

48

after the decrease of silica concentrations was then followed by the sharp increase in

cyanobacteria biovolume, which might support this hypothesis.

Succession Patterns

Historical data for the lower St. Johns River ecosystem, including Lake George,

demonstrate recurring aspects of blooms includes: increases in diatom abundance in

the early spring followed by increasing dominance of cyanobacteria, with a succession

of cyanobacteria dominance from Anabaena spp., Anabaenopsis spp. and

Aphanizomenon spp. (A-Group) to Cylindrospermopsis sp. (C-Group) (Phlips et al.,

2007). The successional pattern has been observed in other ecosystems(Ryding and

Rast, 1989). Successional patterns can be controlled by allogenic factors, such as

nutrient supply, ambient temperature, light income, CO2 availability and turbulence, or

autogenic factors, such as physiological and life-history characteristics of individual

species.

In terms of nutrient supply, low concentration of dissolved inorganic nitrogen (DIN)

before the bloom events was undoubtedly a factor in the dominance of nitrogen fixing

cyanobacteria. Coincident with the increase in phytoplankton biomass during the

blooms, NH4 and TN concentrations increased, probably linked to the input of

atmospheric nitrogen to Lake George via nitrogen fixation (Doron, 2010).

The DIN: SRP ratio ranged from 2 to 12, with more than 50% of values falling

below 7, which is generally considered the threshold for distinguishing phosphorus from

nitrogen limitation. SRP concentration showed no evident change with the A-Group

peak, but an increase associated with the increase in C-Group biovolume. This might be

explained by the relatively high affinity phosphorus-uptake of Cylindrospermopsis, in

49

consort with its relatively low thresholds for phosphorus-uptake, high phosphorus-

storage capacity and its ability to mobilize internal P sources (Padisák, 1997).

The collapse of the A-Group and the significant increase in C-Group biomass were

both coincident with an evident increase in Secchi Depth, that is to say, an increase in

light penetration in water column. The increase in Secchi Depth might be an indicator of

calm conditions in the water column, with more bioavailable P settling to the bottom.

The different P uptake ability and buoyancy characteristics of these two groups could

contribute differently to their response to the changing environmental conditions, which

might be the reason for their alternating dominance.

The steady increase in temperature over the study period could be one factor

favoring the dominance of the C-Group over the A-Group. The former group became

increasingly dominant when water temperature exceeded 28 oC.

50

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53

BIOGRAPHICAL SKETCH

The author is originally from China, received her bachelor’s degree in biological

science from Nanjing Agricultural University in the summer of 2008. In the United

States, she received her master’s degree in interdisciplinary ecology from the University

of Florida in the summer of 2010.