Journal of Plankton Research Vol.19 no.3 pp.319-342, 1997
Relationships between phytoplankton dynamics and the
availability of light and nutrients in a shallow sub-tropical lake
Edward J.Phlips, Mary Cichra, Karl Havens1, Charles Hanlon1, Susan Badylak,
Beate Rueter, Mike Randall and Phyllis Hansen
Department of Fisheries and Aquatic Sciences, University of Florida, 7922 NW
71st Street, Gainesville, FL 32653 and 'South Florida Water Management District,
3301 Gun Club Road, West Palm Beach, FL 331346-4680, USA
Abstract. The role of light and nutrient availability in controlling the abundance and structure of
phytoplankton populations was studied in Lake Okeechobee, a large eutrophic lake in south Florida,
USA. Measurements of selected environmental parameters at sampling sites within four ecologically
distinct regions of the lake were combined with direct experimental determinations of limiting levels
of light and nutrients for phytoplankton growth to determine spatial and temporal variations in the
relative roles of these limiting factors. Estimated mean light availability in the mixed layer, Im, was significantly lower in the turbid central region of the lake than in other regions. Correlations between /m
and phytoplankton standing CTops led to the conclusion that low light availability in the central region
of the lake, and to a lesser extent in other areas, restricts phytoplankton standing crops to levels below
the potential provided by the nutrients available. The results of the irradiance-growth experiments
confirmed the conclusions of the correlation analyses that phytoplankton growth is restricted by the
levels of light availability experienced during the winter and spring in the central region of the lake.
Bioassays indicated that nitrogen was the most frequently limiting nutrient for phytoplankton growth.
High rates of nitrogen fixation were frequently observed in the lake, along with correspondingly high
abundances of nitrogen-fixing cyanobacteria and nitrogen fixation activity. Elevated concentrations of
soluble inorganic nitrogen appeared to suppress both nitrogen fixation and the relative abundance of
nitrogen-fixing cyanobacteria.
Introduction
Discussions of bottom-up control of phytoplankton abundance and composition
in lakes frequently focus on a single dominant limiting factor. Phosphorus has
been identified as the principal limiting factor for primary production in many
temperate lakes (Schindler, 1978; Vollenweider and Kerekes, 1980; Tilzer, 1990),
while nitrogen has been identified as the main limiting factor in a number of tropical lakes (Toerien et al., 1975; Henry et al., 1985;Thornton, 1987; Rast et al., 1989).
The nature of limiting factors can vary spatially and temporally within individual
lakes. In Lake Okeechobee, a large sub-tropical system in Florida, empirical and
experimental evidence indicates that both light and nutrient availability may have
significant impacts on the abundance and structure of phytoplankton, but the relative importance of these factors varies over time and between regions in the lake
(Aldridge et al., 1995; Phlips et al, 1995b).
In a recent study of Lake Okeechobee, Aldridge et al. (1995) concluded that
nitrogen is the most commonly limiting nutrient for the growth of phytoplankton.
The existence of nitrogen-limiting conditions can affect both the structure and
dynamics of phytoplankton populations, including the promotion of taxa capable
of nitrogen fixation (Schindler, 1978; Flett et al, 1980; Findlay et al, 1994). Frequent and massive blooms of the nitrogen-fixing species Anabaena circinalis in
Lake Okeechobee (Jones, 1987; Havens, 1994) are indicative of nitrogen
© Oxford University Press
319
EJ.Phlips el aL
limitation. High abundances of nitrogen-fixing cyanobacteria, like Anabaena and
Aphanizomenon, have also been observed in numerous lakes around the world
(Reynolds and Walsby, 1975; Pearl, 1988). In Lake Okeechobee, these blooms
generally occur in the northern, western and southern regions of the lake, but
seldom in the central and eastern regions (Phlips et al, 1993,1995c; Havens, 1994).
Phlips et al. (1995a,b) hypothesized that, in the latter regions, resuspension of
light-attenuating muddy sediments causes light limitation of phytoplankton
standing crops, thereby preventing these populations from reaching the potential
biomasss provided by the prevailing available nutrients.
In temperate and high-latitude lakes, the role of light availability in controlling
phytoplankton standing crops is often viewed from a seasonal perspective (Tilzer,
1990). Low winter irradiances, combined with deep mixed layers, preclude the
development of high phytoplankton standing crops. Sub-tropical and tropical
environments are, however, subject to less seasonal variation in irradiance. In
some eutrophic lakes in the tropics, like Lake George (Ganf and Viner, 1973), high
phytoplankton standing crops are sustained throughout the year. This is not,
however, the case in lakes subject to high levels of non-algal solids in the water
column, i.e. tripton. For example, despite their tropical location and eutrophic
nutrient status, phytoplankton standing crops in Lakes Chapala (Limon et al,
1989) and Chad (Brylinsky and Mann, 1973) are unexpectedly low due to the
severe restriction of light availability in the mixed layer, caused by high concentrations of tripton. This situation appears to hold true for certain regions of Lake
Okeechobee.
Recent studies of Lake Okeechobee (Schelske, 1988; Phlips et al, 1993,1995b)
have stressed the importance of recognizing and understanding the causes of the
spatial and temporal heterogeneity that exists in the abundance and structure of
phytoplankton. Beyond the goal of better describing the basis for population
dynamics, this understanding is key to predicting the consequences of management strategies that alter nutrient loading and water flow within lake ecosystems.
Current evidence indicates that the impact of top-down (i.e. grazing) control on
phytoplankton populations in Lake Okeechobee is low (Havens et al, 1996a).
Like many eutrophic lakes in the sub-tropical environment of south Florida, the
zooplankton community is dominated by small-bodied rotifers (Crisman et al,
1995). While there appears to be a positive relationship between the abundance
of rotifers and phytoplankton (Crisman et al, 1995), the results of both empirical
(Beaver and Havens, 1996) and experimental (Havens et al, 1996b) studies indicate a minimal role for zooplankton in the control of phytoplankton dynamics.
We hypothesize that much of the heterogeneity in the structure and dynamics
of phytoplankton populations in Lake Okeechobee is attributable to fundamental
regional and seasonal differences in the nature of bottom-up controlling factors.
The goal of this study was to measure selected light- and nutrient-related variables
from four ecologically distinct regions in Lake Okeechobee (Phlips et al, 1993),
and simultaneously to carry out direct experimental bioassays of light and nutrient limitation of phytoplankton growth, in order to establish a spatially and temporally integrated view of bottom-up control of phytoplankton structure and
abundance. We also carried out nitrogen fixation assays and microscopic analysis
320
Phytoplankton dynamics and light availability
of phytoplankton composition to describe spatial and temporal patterns of phytoplankton structure and function further. This suite of information was used to
explore the validity of our hypothesis.
Method
Site description
This research was carried out in Lake Okeechobee, a large (1730 km2) and shallow
(mean depth <3 m) lake located in the sub-tropical environment of south-central
Florida, USA (Beaver et al., 1981). Shallow mean depths, combined with large
area and wind fetch, make this lake predominantly polymictic (Herdendorf, 1990).
Lake Okeechobee has been classified as eutrophic (Stoermer et al, 1992) and is
characterized by ecologically distinct regions (Figure 1) (Phlips et al., 1993),
including: (i) a large central region characterized by muddy bottom sediments, a
turbid water column and the deepest water column (>4m) in the lake; (ii) a northern region characterized by muddy sediments, major inflows of nutrient-rich
water and intermediate depth (3-4 m); (iii) a western perimeter region with firm
sediments and frequent blooms of phytoplankton; (iv) a littoral fringe region
along the western and southern boundaries of the lake, containing significant
populations of submerged aquatic vegetation (Zimba et al., 1995); (v) an extensive
littoral community encompassing -20% of the lake's total area. The high turbidity observed at the central site is in large part a product of high concentrations of
non-algal suspended solids in the water column (Phlips et al., 1995c), caused by
resuspension of muddy flocculent sediments (Figure 1).
Sampling
Four pelagic sites (north, central, south and west) in Lake Okeechobee were
sampled weekly from May 1994 to April 1995 (Figure 1). The locations of the sampling stations were based on the four ecologically distinct regions within the lake's
open-water habitat discussed in the previous section. One sampling site was
selected in each region. Water was collected using a 4 cm diameter PVC tube that
evenly sampling water from the surface to 0.1 m from the bottom. Samples were
dispensed into duplicate dark containers, one containing Lugol's preservative,
packed on ice and transported to the laboratory in Lakeport, Florida, for initial
processing. Unpreserved water was filtered for chlorophyll onto 0.5 |xm porosity
glass fiber filters on the day of sampling, placed in a sealed container with desiccant, and frozen.
Other parameters measured included Secchi disk depth, surface and subsurface photosynthetically active radiation (PAR) using Li-cor Quantum 2ir PAR
cosine light sensors. Mean light availability (per day) in the mixed layer, Im, was
estimated using the formula /m = [lJ{K^Zm)\[\ - e-WCZ-)], where Zm is the depth
of the mixed layer (m), Io is the mean daily surface irradiance (mol photons day 1 )
and Kt is the light extinction coefficient (nr 1 ) (Stefan et al., 1976). Zm was assumed
to be equal to station depth due to the generally polymictic character of the lake.
Io was obtained from literature values of mean daily irradiance for 27°N latitude.
321
E J.Phlips et aL
PEAT
LITTORAL
LJ SAND
MUD
ROCK
OkMchob**
Taylor Creak
I
KtalmnwaRlvw ^ f ^ /
Nubbin. 8tough
Indian PreJrto
Canal
B
North
Station
(104)
Hamay Pond
C
Cantar
Station
(204)
Witt
Station
(513)
Zones
Northern
Nearshore
Littoral
Central
Western
Fig. L (A) Sediment types in Lake Okeechobee (top) (Reddy el aL, per. comm.) and (B) geographical boundaries of ecologically distinct zones (Phlips et aL, 1993) and locations of four sampling stations
used in this study (bottom).
322
Pbytoplankton dynamics and light availability
The range of / m used was based on two levels of incident irradiance: (i) average
incident light including the estimated effect of cloud cover (i.e. /m AVE) (Oswald
and Gataas, 1957) and (ii) maximum incident irradiance assuming clear weather
conditions (i.e. Im MAX).
Phytoplankton enumeration
Water samples were settled in 19 mm diameter cylindrical chambers. Phytoplankton cells were identified and counted at 400 X and 100 X with a Nikon
phase-contrast inverted microscope. At 400 X, counts were completed upon
reaching 100 cells of a single dominant taxon, but a minimum of 30 ocular micrometer grids were counted. Large-celled taxa (>30 u.m maximal linear dimension)
were enumerated by a complete count of the settling chamber of 100 X.
Picoplankton were enumerated with fluorescence microscopy using filtered
samples (0.2 u.m pore Nuclepore). Samples were counted with a Nikon microscope equipped with fluorescence.
Many studies of phytoplankton in lakes use chlorophyll a concentrations as a
measure of standing crop and trophic state (Carlson, 1977; Rast et al., 1989). Based
on chlorophyll a concentrations observed in other studies (Havens, 1994; Phlips et
al, 1994,1995c; Aumen, 1995), Lake Okeechobee is a eutrophic system. In this
study, we used cellular biovolume as the principal measure of phytoplankton
abundance. Biovolume conversions for each taxon were determined using replicated measurements of taxa along with the closest geometric shape(s) and the
appropriate volumetric formulae. A recent 5 year study of phytoplankton in Lake
Okeechobee (Cichra et al, 1995) provided biovolume conversion estimates for
most of the taxa observed. These conversions included adjustments for seasonal
and inter-annual variations in the size of cells. When new taxa were encountered,
a minimum of 10 cells were measured to obtain volume estimates.
Analytical methods
Water samples were analyzed for chlorophyll a (corrected for pheophytin), total
phosphorus (TP), total nitrogen (TN), nitrate and soluble reactive phosphorus
(SRP). Total nitrogen was determined using nitrogen methods for flow injection
autoanalyzers [United States Environmental Protection Agency (USEPA), 1987].
Total phosphorus was determined after the persulfate digestion method (USEPA,
1979). Nitrate and SRP concentrations were determined using Hach (1992) procedures for low-range concentrations on the same day as water sampling. Chlorophyll a concentrations were determined from filtered samples by extraction with
90% acetone, grinding with a tissue grinder and standard spectrophotometric
analysis (American Public Health Association, 1989).
Nutrient limitation bioassays
The experimental design was based on methods described by Aldridge et al
(1995). Assays were carried out under laboratory conditions in 500 ml Erlenmeyer
323
E J.Phlips el al
flasks with 300 ml of whole lake water. Treatments (in triplicate) were control (no
additions),N addition (400 (xgN r>),2N addition (800 u.g N H),P addition (40 u.g
P I-1) and an N + P (N + P) (400 u.g N r 1 + 40 |xg P I"1). Nitrogen was added as
KNO3 and P was added as K2HPO4. Incubations were carried out in temperaturecontrolled water baths with bottom illumination. Incubation temperatures were
set at ambient lake temperatures recorded on each sampling date. Light intensity
was fixed at 120 jiE irr 2 s"1. The photoperiod was 12/12 (dark/light) h from
October through March and 11/13 (dark/light) h from April through September.
Algal biomass was estimated by in vivo fluorescence of chlorophyll a (IVF) using
a Turner Designs Model 10 fluorometer with 1 cm diameter tubes.
A nutrient was considered limiting when no growth occurred in the control and
addition of that nutrient stimulated algal growth. When algal growth occurred in
the control, it was concluded that neither nitrogen nor phosphorus was limiting
and that some component of the phytoplankton community was growing at the
time of sampling or some controlled variable, such as light, was more optimal
under the assay conditions than in the natural environment. Grazers were not
removed from the whole water used in the bioassays. Owing to the short time
frame and strict control and uniformity of all variables other than nutrient concentrations, it was assumed that grazing pressure would be relatively uniform
between treatment groups. A similar assumption was made in light limitation
bioassays.
In all of the assays, the 24 h response identified the limiting nutrient. Responses
at subsequent sampling, 72 and 96 h, confirmed the limiting nutrient classification
at 24 h. Thus, the 24 h response was used to assign primary limiting nutrient classifications.
Light limitation bioassays
Natural water samples collected from the four sampling sites described above
were incubated under a range of four daily irradiance levels (0.7,2.1,4.2 and 8.4
mol photons nr 2 day-1) compared to maximum daily surface irradiance in the
summer of 50 mol photons nr 2 day"1. The photoperiod was 12/12 (dark/light) h
from October through March and 11/13 (dark/light) h from April through September. Triplicate flasks (500 ml) containing 300 ml of water collected at the sampling sites were set up at each irradiance level. Each flask was injected with
N-KNO3 (400 (xg I"1) and P-K2HPO4 (40 |Ag I'1) to avoid nutrient limitation. Temperature was maintained at that observed at the time of sampling. Sub-samples
were taken from each flask at time = 0,24 h, 72 h and 120 h. Each sample was analyzed for chlorophyll a concentration using fluorescence and spectrophotometric
techniques. Growth rates used in the analyses represent the change in chlorophyll
between 24 and 72 h of incubation. The range of initial chlorophyll a concentrations in the whole water samples used in the bioassays varied between sampling
sites: north 7-75, central 8-28, south 5-70 and west 11-70 mg nr 3 . Up to 2-3 doublings were observed during the incubation periods.
The growth rates were plotted against the respective values for daily irradiance.
The growth versus irradiance curves were used in conjunction with values
324
Phytoplankton dynamics and light availability
for mean light availability in the mixed layer (/m), calculated from field
measurements, to generate the percent of maximum growth sustainable by the
light available in situ.
Nitrogen fixation assays
Nitrogen fixation potential was measured using the acetylene reduction method
(Hardy et ai, 1968; Taylor, 1983). Water samples collected in the field during the
early morning were returned to the field laboratory within 2 h of collection, and
immediately prepared for acetylene reduction analysis. Each incubation flask
contained 25 ml of station water and 5 ml of head space. The incubation flasks
were sealed with rubber stoppers and were injected with acetylene gas at time
zero. Thefinalconcentration of acetylene was 10% of the volume of the gas phase.
Acetylene reduction assays were performed in triplicate for each of the four sites
in the light and dark, in an incubation bath set at the station temperature
measured at the time of collection. Light flux was set at 60-70 (junol photons nr 2
s"1. Light and dark rates of acetylene reduction were based on 3-4 h incubation
periods. At the end of the incubation period, 0.5 ml aliquots of the gas phases of
each flask were injected into a Carle Instruments Model 311 gas chromatograph
equipped with a 2 m Hayesep A (mesh 60/80) column and flame ionization detector. Ethylene production, i.e. acetylene reduction, was determined from peak
heights, using ethylene standard curves.
Data analysis
Statistical Analysis Systems (SAS) statistical program for personal computers
(SAS Institute, Inc., 1989) was used to carry out general linear models procedures
and Tukey's multiple range test. A significance level of P < 0.05 was used to
compare mean values.
Results
General limnological characteristics
Annual mean depths at the four sampling locations in Lake Okeechobee were 2.1
(range 1.3-2.7), 3.4 (2.6-4.0), 3.8 (3.0-4.4) and 4.6 (3.8-5.2) m for the south, west,
north and central sites, respectively. Water temperatures varied over a relatively
narrow range during the year with mean seasonal values of 18,23,26 and 29°C for
winter, spring, fall and summer, respectively. Water temperatures during the year
ranged from 14.1 to 30.5°C. Water clarity, in terms of Secchi depth, was significantly less at the central site (annual mean Secchi depth of 0.29 m) than at the
other three sites in the study (west site 0.49, north site 0.55 and south site 0.75 m).
Secchi depths were greater in the summer and fall than in the spring and winter
at all four sampling sites, reflecting greater wind resuspension of sediments during
the winter/spring windy season in south Florida.
Annual mean TP concentrations were 50, 67, 81 and 97 mg nr 3 at the south,
west, north and central sites, respectively. Annual mean concentrations of SRP
325
E J.Phlips el aL
followed the same general spatial and temporal patterns as TP, but with greater
variance. The annual mean SRP concentration at the central site (32 mg m~3) was
over 6-fold higher than that at the south site (6 mg m~3) (Table I). Seasonal mean
SRP concentrations were significantly different at each site, except the central site
(Table I). The seasons with lowest SRP values varied by site, occurring in the
summer, spring and fall at the north, south and west sites, respectively (Table I).
Annual mean TN concentrations were not significantly different at the four
sampling sites, ranging from 1.29 g nr 3 at the north site to 1.37 g m~3 at the west
site. Annual mean nitrate concentrations were more variable than TN values,
being highest at the central site (204 mg nr 3 ) and lowest at the south site (64 mg
irr3) (Table I). Seasonal mean nitrate concentrations were significantly higher
during the winter and spring than summer or fall, except at the south site where
fall values were somewhat elevated (Table I).
Annual chlorophyll a concentrations were highest at the west site and lowest at
the central site (Table I). At the north, central and west sites, chlorophyll a concentrations were higher in the summer and fall than in the winter and spring
(Table I). At the south site, summer was the season of minimum chlorophyll a
concentration.
Spatial and temporal patterns of light availability
Annual mean light availability in the mixed layer, Im, was half as high at the central
site as at the north and west sites, and less than a fifth of the mean at the south site.
Annual mean values for Im AVE were 0.9,2.0,2.2 and 5.5 mol photons nr 2 day 1
for the central, north, west and south sites, respectively. Annual mean values for
Im MAX were 1.4, 3.0, 3.3 and 8.2 mol photons m~2 day 1 for the central, north,
west and south sites, respectively. Im values were subject to considerable temporal
Table L Annual and seasonal mean values for SRP, NO3 and chlorophyll a. Tukey's multiple range test
was used to test for significance between means. Seasonal means for each station with the same lowercase letter are not significantly different. Annual means with the same upper-case letter are not
significantly different
Station
Winter
Spring
Summer
Fall
Annual
16 B
29 A
1
SRP (mg nr- )
North
Central
South
West
NO3 (mg nr 3 )
North
Central
South
West
Chlorophyll a (mg nr 3 )
North
Central
South
West
326
21a
14 a
8a
19 a
35 a
26a
29 a
25a
6a
23a
2a
14 ab
8a
6a
5C
12 ab
4b
13 B
112 a
331a
173 a
367 a
23b
20b
77B
89 ba
72 a
10 b
2O5A
62 B
132 B
39 a
30A
21a
16 B
32 A
69a
97a
67 b
15 b
291a
225a
9b
17 b
21b
lib
48a
13 b
33 b
24 b
42 a
20 a
12 c
43 a
26 b
33 B
47 a
36A
Phytoplanklon dynamics and light arailability
variability (Figure 2) and were generally lower in the winter and spring than in the
summer and fall at all four sampling sites.
Spatial and temporal patterns of phytoplankton abundance and structure
The annual mean biovolume of the phytoplankton in Lake Okeechobee was
3.2 X 106 n,m3 ml 4 . Annual mean phytoplankton biovolume (Table II) was lowest
at the central site, 3-fold higher at the north site, and 7- to 8-fold higher at the south
and west sites.
Cyanobacteria were the overall dominant group at all four sites (Figure 2,Table
II). Seasonal mean biovolumes of total phytoplankton and cyanobacteria were
higher in the summer and fall than in the winter and spring at the north, central
and west sites (Table II). The largest difference between summer/fall and
winter/spring, nearly 4-fold, was observed at the central site. At the south site,
phytoplankton were least abundant in the summer (Table II).
Cyanobacteria were dominant in at least one of the four sampling sites during
the year (Table III). At the central site, small-celled cyanobacteria were consistently dominant, including small-diameter (2 u,m) Oscillatoria sp., Lyngbya contorta and Lyngbya limnetica (Table III). In the winter and spring, a 1-2 u.m
spherical cyanobacterium was the dominant phytoplankton species (Table III). At
the other three sites, larger nitrogen-fixing cyanobacteria shared dominance
status with the former cyanobacteria and at times with diatoms (Table III). Nitrogen-fixing species were particularly abundant in the summer and fall (Figure 3),
including Aphanizomenon sp., Cylindrospermopsis cuspis and Anabaena circinalis (Table III).
Diatoms were the next most abundant phytoplankton group after cyanobacteria. All other groups were only periodically present at significant levels,
including chlorophytes, cryptophytes, chrysophytes, euglenophytes and dinoflagellates. Annual mean diatom biovolumes were lowest at the north and central
sites (Table II). Annual mean diatom biovolumes were 3- to 8-fold higher at the
south and west sites than at the former two sites (Table II). Seasonal patterns of
diatom abundance were different between sites (Figure 4,Table II). At the central
site, where diatom abundances were relatively low, the species most commonly
encountered were small in size, e.g. Fragilaria construens (Table III).
Seasonal patterns of diatom abundance at the south and west sites were fundamentally different from those observed for cyanobacteria and total phytoplankton. Diatom biovolumes were higher in the winter and spring than in the
summer and fall, with a strong representation of both pennate and centric forms
(Table III).
Relationships between phytoplankton abundance and light availability
Positive empirical relationships between phytoplankton biomass (i.e. total phytoplankton biovolume) and 7m were evident at the central site (Figure 2). This observation was further manifested by the significant positive relationship between the
two variables; Ln(total phytoplankton biovolume) = 0.87Ln(/m MAX) + 12.98,
327
EJ.Phlips et at
M'J'JL
M'J'JL'AS'O'N D
1994
14
A S O N D J F M
1994
1995
D. Central Site
TOTAL
CYANO
DIAT
12
10
8
6
4
2
M J J L A S O N D
1994
J F M
1995
M J J L A S O N D
1994
1995
Date, Month/Year
Fig. 2. Mean irradiance in the mixed layer, mol photons nr 2 day-' (A, C, E, G) and biovolume, 106 (xm3
ml"1, of cyanobacteria, diatoms and total (B, D, F, H).
R2 - 0.50, P < 0.0001, n = 40. These observations indicate a role for light availability
as a limiting factor for phytoplankton growth and standing crop in the central
region of the lake. Significant positive relationships were also observed at the
328
Pbytoplankton dynamics and light availability
1994
14
F. South Site
I
14
12
12
II
10
8
2 8
o
!
1995
6
TOTAL
CYANO
j
M
j
4
11
H. West
rtl
Slte
it
A
2
MJJLASOND
1994
0
n 'i—rn
M J JL
1995
1994
1995
Date, Month/Year
Fig. 2. continued.
north and west sites, but the R2 values were lower, 0.35 and 0.33, respectively. At
the south site, there was a negative relationship between phytoplankton biovolume and Im.
329
E J.Phlips el aL
Table II. Annual and seasonal mean values for the biovolume of phytoplankton. TUkey's multiple
range test was used to test for significance between means. Seasonal means for each station with the
same lower-case letter are not significantly different. Annual means with the same upper-case letter
are not significantly different
Station
Winter
Spring
Summer
Fall
Annual
0.60
030
4.77
2.29
1.19
0.26
4.96
3.19
ab
b
ab
b
337 a
0.93 a
3.56 b
7.22 a
2.31
1.09
5.39
8.04
0.42 b
0.25 b
2.80 a
1.71 b
0.94
0.18
3.30
1.62
ab
b
a
b
2.85 a
0.70 a
3.21a
6.60 a
1.99 ab
0.89 a
4.15 a
7.31a
1.63
0.53
3.37
4.37
B
B
A
A
0.10 a
0.04 b
1.63 a
0.46 b
0.16
0.05
1.33
1.24
a
b
a
a
0.22
0.18
0.13
0.47
0.24
0.17
0.75
0.54
0.19
0.12
0.98
0.66
C
C
A
B
Total phytoplankton biovolume
(lOVm-'mH)
North
Central
South
West
Cyanobacterial biovolume
(lO'M.m'ml- 1 )
North
Central
South
West
b
b
ab
b
ab
a
a
a
1.96 B
0.68 C
4.71 A
5.23 A
Diatom biovolume
North
Central
South
West
a
a
b
b
a
a
ab
b
Light limitation bioassays
Phytoplankton growth yield was plotted against irradiance (mol photons nr 2
day 1 ) for 11 monthly light limitation bioassays at the four sampling sites. These
curves were compared with estimates of mean daily irradiance in the mixed layer
derived from on-site measurements of light attenuation. Estimates were obtained
for the percent of the maximum growth yield (i.e. light-saturated growth) achievable by the observed /m values (Figure 3). At the central site, eight of the 11 bioassays showed that the estimated ambient Im supported <25% of the maximum
growth. Only the August, September and October bioassays showed growth yields
>25% of maximum. In contrast, all 11 bioassays at the south site showed >25% of
maximum growth yields. At the north and west sites, there were significantly
reduced yields at ambient Im during the mid-winter to early spring months.
Nutrient limitation bioassays
Nitrogen was the most commonly limiting nutrient for the growth of phytoplankton samples collected from the lake (Figure 4). At the north site, nitrogen
was limiting in seven of 12 monthly bioassays (Figure 4). The remaining five
monthly bioassays (July, January, February, March and April 1) indicated the presence of both surplus nitrogen and phosphorus. At the central site, nine of 12
monthly assays showed a surplus of available nitrogen and phosphorus, while the
remaining monthly assays (August, September and October) showed nitrogen
limitation. At the south site, nitrogen was a primary limiting element in all
bioassays except for the April 1 sampling date. In addition, nine of 12 south site
330
1-2 jun sphere (C)
Lcontorta (C)
Econstruens (D)
1-2 (im sphere (C)
Oscillatoria 2 p.m (C)
Econstruens (D)
1-2 |im sphere (C)
Oscillatoria 2 MJH (C)
Pennate diatom 50 pjn
1-2 |im sphere (C)
Oscillatoria 2 (im (C)
Centric diatoms 10-20 jun
Aphamzomenon (CN)
Oscillatoria 2 p.m (C)
C.cuipfa(CN)
A.circinalis (CN)
Oscillatoria 2 jun (C)
1-2 jun sphere (C)
A.circinalis (CN)
Oscillatoria 2 pjn (C)
1-2 pjn sphere (C)
Ccuspis (CN)
1-2 pjn sphere (C)
Chroococcus (C)
Microcystis 2 (j.m (C)
Oscillatoria 2 |im (C)
Chroococcus (C)
Microcystis 5 (jum (C)
Oscillatoria 2 )un (C)
Chroococcus (C)
A.circinalis (CN)
Oscillatoria 2 jim (C)
A.clrcinalis (CN)
Aphaniiomenon (CN)
Centric diatom 10-20 |xm
Aphamzomenon (CN)
Oscillatoria 2 y.m (C)
Oscillatoria 2 pjn (C)
Centric diatom 10-20 |un
Ccuspis (CN)
Centric diatom 10-20 pjn
Oscillatoria 2 (im (C)
Aphamzomenon (CN)
Centric diatoms 10-24 jun
Econstruens (D)
South site
Lcontorta (C)
Oscillatoria 2 inn (C)
Econstruens (D)
Econstruens (D)
Centric diatom 10-20 |xm
L.contorta (C)
Econstruens (D)
Centric diatoms 10-20 pun
1-2 p.m sphere (C)
Centric diatoms 10-20 jira
1-2 n.m sphere (C)
L.contorta (C)
Oscillatoria 2 jun (C)
Ccuspis (CN)
Cgiganteus (C)
Llimnetica (C)
Oscillatoria 2 pun (C)
Ccujp/j (CN)
Oscillatoria 2 pjn (C)
A.circinalis (CN)
L.limnetica (C)
Oscillatoria 2 |xm (C)
A.circtnalis (CN)
Llimnetica (C)
Oscillatoria 2 \un (C)
Ccuspis (CN)
A.circinalis (CN)
Oscillatoria 2 ujn (C)
Ccuspis (CN)
Aphanizomenon (CN)
Oscillatoria 2 pjn (C)
Ccuspis (CN)
Aphanizomenon (CN)
Oscillatoria 2 (JLJBI (C)
West site
A.circinalis = Anabaena circinalis; Cgiganteus = Chroococcus giganteus; Ccuspis = Cyhndrospermopsis cuspis; Econstruens = Fragilana construens; L.contorta = Lynbgya
contorta; Llimnetica = Lyngbya limnetica; M.granulata = Melosira granulata.
April 1995
March 1995
February 1995
January 1995
December 1994
November 1994
October 1994
September 1994
August 1994
July 1994
Oscillatoria 2 tun (C)
C.aapls (CN)
Llimnetica (C)
Oscillatoria 2 jun (C)
A.circinalis (CN)
Aphaniiomenon (CN)
Oscillatoria 2 pjn (C)
Cciispis (CN)
Llimnetica (C)
Oscillatoria 2 \im (C)
Cciispis (CN)
A.circinalis (CN)
Oscillatoria 2 (im (C)
Pennate diatom 50 (j.m
Pennate diatom 75 |xm
1-2 (iin sphere (C)
Oscillatoria 2 (jjn (C)
L.contorta (C)
1-2 |xm sphere (C)
Oscillaloria 2 (im (C)
M.granulata (D)
1-2 tun sphere (C)
Oscillatoria 2 jun (C)
Pennate diatom 50 ixm
1-2 i±m sphere (C)
Oscillatoria 2 jun (C)
1-2 pjn sphere (C)
Oscillatoria 2 pjn (C)
Lcontorta (C)
1-2 ujn sphere (C)
M.granulata (D)
Oscillatoria 2 pjn (C)
Lcontorta (C)
Oscillatoria 2 y.m (C)
M.granulata (D)
Oscillatoria 2 pjn (C)
Lcontorta (C)
A.circinalis (CN)
Oscillatoria 2 |im (C)
A.cirdnalis (CN)
Llimnetica (C)
Oscillatoria 2 \tm (C)
L.contorta (C)
Econstruens (D)
1-2 inn sphere (C)
Oscillatoria 2 |xm (C)
Econstruens (D)
1-2 Mjn sphere (C)
Oscillatoria 2 ujn (C)
A.circinalis (CN)
Centric diatom 10-20 pjn
Oscillatoria 2 jun (C)
A.circinalis (CN)
Llimnetica (C)
Oscillatoria 2 ujn (C)
Llimnetica (C)
Rhaphidiopsis (C)
May 1994
June 1994
Central site
North site
Month
Table IIL Dominant phytoplankton taxa by sampling site and month. Only taxa that are at least 10% of total biovolume, on any given sampling date, within
each month are included. Taxa that represented over 25% of total biovolume are shown in bold. Taxa are listed in order of their highest percent contribution.
Group designations are: (C) cyanobacteria, (CN) nitrogen-fixing cyanobacteria, (D) diatoms and (G) green algae
a
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Fig. 3. Estimated percent of the maximum observed growth sustainable by the observed mean light
availability in the mixed layer on the day of sampling. The results of 11 monthly bioassays are shown.
Mean, solid and range, open bars.
332
Pbytoplankton dynamics and light availability
bioassays showed primary or secondary N + P co-limitation, indicating that the
amount of surplus phosphorus present was low. At the west site, nitrogen was the
primary limiting nutrient in eight of 12 bioassays. The remaining 4 months,
January-April 1, showed an initial surplus of both nitrogen and phosphorus.
Nitrogen fixation activity
Nitrogen fixation activity, measured as the areal rate of acetylene reduction, was
observed at all four sampling sites (Figure 4). Light-dependent activity was dominant in all samples, with dark rates of acetylene reduction consistently below 5%
of the light rate. At the north, south and west sites, nitrogen fixation activity was
highest in the early summer, late fall and winter. At the central site, nitrogen fixation activity was comparatively low and only present in the late summer and
early fall.
The biovolume of potentially nitrogen-fixing heterocystous cyanobacteria followed the same general temporal and spatial patterns as nitrogen fixation activity
(Figure 4). Nitrogen fixation activity was positively correlated to the biovolume
of heterocystous cyanobacteria; N2 fixation activity = 9.1 X 10~5 biovolume of heterocystous cyanobacteria + 25.45, R2 = 0.75, P < 0.0001,n = 140. Elevated levels of
nitrate in the water column were consistently associated with low or declining
nitrogen fixation activity and biovolume of heterocystous cyanobacteria (Figure
4). Significant negative Pearson correlation coefficients were obtained for the
relationships between nitrate concentrations and both the biovolume of heterocystous cyanobacteria (-0.56, P < 0.0001, n = 165) and nitrogen fixation activity
-0.47, P < 0.0001, n = 146).
Discussion
The results of this study support the hypothesis that regional differences in the
relative importance of light and nutrient availability strongly influence spatial and
temporal patterns observed in the abundance and composition of phytoplankton.
Regional differences were observed in the relationship between nutrient availability and phytoplankton abundance and composition. The strongest relationship
was in the littoral fringe region, and the weakest in the central region, where light
availability was the primary factor controlling phytoplankton abundance and
composition.
Light limitation
In the central region of Lake Okeechobee, which is subject to the highest levels of
tripton, phytoplankton abundance was positively related to light availability.
Phytoplankton abundance in this region was highest during the summer and fall
when light availability was highest, due to reduced tripton concentrations. This
contrasts with the littoral fringe region (e.g. south site) where phytoplankton were
least abundant in the summer, despite high light availability, indicating a limitation
of standing crop by a factor other than light availability.
333
EJ.Phlips et aL
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1995
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Cet ene r e d u c e d
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'"' h "' (A.C.E.G), biovoiume of heterocystous cyanobacteria
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In a recent study of the relationships between chlorophyll a and light availability in the mixed layer, /m, in Lake Okeechobee, Phlips et al. (1995a) hypothesized that there is a threshold between light limitation and light sufficiency at /m
values of 1.5-2 mol photons nr 2 day 1 . The threshold irradiance level suggested
for Lake Okeechobee coincides with the minimum irradiance value reported by
Tilzer (1990) for the onset of spring blooms of phytoplankton in Lake Constance
(i.e. 2 mol photons m~2 day"1). Hypotheses about light limitation thresholds have
been forwarded for other lakes, including Mt Bold Reservoir (Ganf, 1980; Oliver,
1981) and Lake Alexandria in Australia (Geddes, 1984). Im MAX values
observed in this study were below, or within, the threshold range in the winter and
spring at the north and central sites, and to a lesser degree at the west site (Figure
2). At the central site, lm MAX values were significantly below the threshold for
a large portion of the year (Figure 2), indicating an extended period of light limitation of phytoplankton growth and standing crop. This conclusion is supported
by the low phytoplankton biovolume observed at the latter site for much of the
sampling period.
Experimentally determined light-versus-growth relationships for natural
phytoplankton assemblages from Lake Okeechobee confirmed the conclusions
of correlation between / m and phytoplankton abundance. Light limitation bioassays showed that growth yields of phytoplankton from the central, and to a lesser
extent the west and north, sites were a small fraction of light-saturated yields at
the low light levels observed during winter and spring (Figure 3). The results of
concomitant nutrient limitation bioassays showed that winter and spring phytoplankton samples from these sites were not limited by nutrient availability
(Figure 4), further confirming the conclusion that low light availability was suppressing standing crops to levels below those sustainable by available nutrient
levels.
The importance of light limitation in Lake Okeechobee is also supported by
observations of cell-size distribution and pigment composition of phytoplankton
in different regions of the lake. As reported elsewhere (Phlips et al., 1996), chlorophyll a concentrations in phytoplankton cells (grams of chlorophyll per unit cellular biovolume) from light-limited regions of the lake (e.g. central site) were up to
10 times higher than values in phytoplankton from the south and west sites.
Winter/spring values were also higher than summer/fall values. Both of these
observations indicate strong shade adaptation (Kirk, 1994) in phytoplankton from
regions of the lake identified as light limited.
Regional differences in the taxonomic composition of phytoplankton further
manifest disparities in light availability. The central site was consistently dominated by small-celled species of cyanobacteria and diatoms, particularly the
former (Table III). This supports the concept that small cell size affords selective
advantages for phytoplankton under light-limiting conditions. It has been suggested that populations of small cells absorb incident irradiance more efficiently
than larger cells, i.e. 'sieve effect' (Tailing, 1971; Reynolds, 1984). In addition,
smaller cells have lower sinking rates than larger cells (except in the case of positively buoyant taxa), thereby allowing them to remain higher in the water column
near the source of incident irradiance (Reynolds, 1984).
336
Phytoplankton dynamics and light availability
In contrast to the frequently light-limited muddy bottom regions (e.g. north and
central sites) of Lake Okeechobee, the hard bottom western (e.g. west site) and
heavily vegetated littoral (e.g. south site) fringe regions normally exhibited /m
values greater than the 2 mol photons rcr2 s~' threshold for light limitation (Figure
2). Abundances of phytoplankton were significantly higher in the latter than the
former regions (Figure 2 and Table II). Greater light availability in the western
and littoral fringe regions is also indicated by the presence of high abundances of
nitrogen-fixing cyanobacteria and winter/spring increases in diatom populations.
Nitrogen-fixing cyanobacteria are known to require significant light energy to
sustain the energy-intensive process of nitrogen fixation.
Nutrient limitation
Another significant feature of Lake Okeechobee is high phosphorus levels resulting from both external and internal loading processes (Aumen, 1995; Olila and
Reddy, 1993). The frequent excess of phosphorus relative to nitrogen makes nitrogen the major limiting nutrient in the lake. In the littoral fringe regions of the
pelagic habitat, dense populations of submersed macrophytes, macroalgae and
epiphytes heighten competition for available nutrients in the water column
(Phlips era/., 1992), while at the same time increasing water clarity through stabilization of sediments.
The results of nutrient limitation bioassays supported the results of an earlier
study (Aldridge et ai, 1995) showing that nitrogen limitation predominates in
Lake Okeechobee, especially during the summer. Summer was the period of
lowest nitrate concentrations in the water column throughout the lake and bioassays confirmed that phytoplankton were limited by nitrogen during the summer
at all four sampling sites. SRP values in the water column did not, however, always
reflect the apparent surplus of bioavailable phosphorus indicated by bioassays.
This is in keeping with the observations of other researchers (Nalewajko and
Lean, 1980) that phytoplankton have the capacity to store surplus phosphorus.
The spatial and temporal patterns of nutrient limitation observed in bioassays
help to explain patterns of phytoplankton abundance and structure, particularly
in the two regions of the lake subject to the highest light availability, i.e. the south
and west sites. Midsummer was the period of minimum phytoplankton abundance
at the south site and reduced abundance at the west site (Figure 2). Bioassays
showed strong nitrogen or nitrogen/phosphorus co-limitation at these sites in
mid/late summer (Figure 4). The effects of nutrient limitation on phytoplankton
abundance appeared to be most severe in midsummer. Diatom abundances were
particularly low in the summer, after winter and spring peaks (Figure 2,Table II).
High cyanobacterial abundances were maintained through early summer, perhaps
indicative of the ability of nitrogen-fixing forms to overcome nitrogen limitation.
The summer minima of phytoplankton abundance observed at the south and
west sites may be based on a number of co-existing conditions in Lake Okeechobee
during this season. Reduced wind velocities in the summer minimize resuspension
of meroplankton and potentially nutrient-laden sediments. Low wind energy also
limits horizontal transport of water, thereby restricting external inputs of nutrients
337
E J.Phlips el al
to limited regions. The principle that sedimentation of cells is a major factor in the
dynamics of pelagic diatom abundance (Knoechel and Kalff, 1978) is important to
consider. In a recent study of Lake Apopka, a shallow lake adjacent to Lake Okeechobee, Schelske et al. (1995) noted that the abundance of diatoms was positively
correlated to wind because of resuspension of meroplankton. This line of reasoning may also help to explain increases in diatom abundance in Lake Okeechobee
during the winter and spring, which are the seasons of highest wind mixing. In
regions of the lake subject to dense populations of submerged aquatic plants and
algae (i.e. the south site), wind mixing can further enhance pelagic diatom abundances by disruption of epiphytes, which are particularly abundant in Lake Okeechobee (Zimba, 1995). Conversely, during periods of low wind velocity, high
biomass and metabolism of submerged macrophytes, macroalgae and epiphytes
serve as a source of competition for available nutrients in the water column. The
latter is particularly relevant in the littoral fringe areas, like the south site, where
these populations are greatest (Phlips et al, 1992; Zimba, 1995; Zimba et al, 1995).
Light-dependent nitrogen fixation activity was observed in all but one of the
water samples where nitrogen was identified as the primary limiting nutrient for
phytoplankton growth (Figure 4). This indicates that nitrogen fixation activity is
stimulated by the nitrogen-limiting conditions common in Lake Okeechobee, and
helps to explain the major role of nitrogen-fixing cyanobacteria in Lake Okeechobee (Figure 4, Table III). Regression analysis showed a significant positive
relationship between the biovolume of potentially nitrogen-fixing heterocystous
cyanobacteria and the level of nitrogen fixation activity. This agrees with the
observations of Findlay et al. (1994) in a study of Canadian lake 227. At the same
time, there were negative correlations between nitrate concentrations and both
nitrogen fixation and the biovolume of nitrogen-fixing species (Figure 4). These
observations support the conclusions of a number of researchers (including Flett
et al., 1980; Smith, 1990; Findlay et al. ,1994) that low loading rates of nitrogen favor
the presence of nitrogen-fixing cyanobacteria. Conversely, the presence of significant amounts of soluble inorganic nitrogen in the water column appeared competitively to favor non-nitrogen-fixing species of phytoplankton.
The abundance of nitrogen-fixing cyanobacteria in Lake Okeechobee (Figure
4) is indicative of the importance of nitrogen fixation to the ecology of this ecosystem. This supports the conclusions of previous studies of Lake Okeechobee
(Phlips and Ihnat, 1995) and other aquatic ecosystems (Phlips, 1987; Howarth et
al, 1988; Findlay et al, 1994) that nitrogen fixation can play a major role in supporting primary production. The results of this study also indicate that the biovolume of nitrogen-fixing cyanobacteria provides a useful approximation of the
nitrogen fixation activity, and vice versa.
The basis for heterogeneity
Long-term maintenance of horizontal patchiness of phytoplankton communities
is most frequently associated with oceanic environments (Platt and Denman,
1980) and large lakes (Reynolds, 1984). At 1700 km2, Lake Okeechobee is
apparently large enough to permit the establishment of large-scale patchiness in
338
Phytoplanlcton dynamics and light aTaflabiHty
phytoplankton composition on a seasonal basis. Topographical, hydrological and
geological features of the lake, along with predominant meteorological patterns,
provide the foundation for persistent regional differences in the factors that
control phytoplankton abundance and structure.
One of the dominant geological features of Lake Okeechobee is the large area
of muddy sediments in the central, eastern and northern regions (Figure 1). The
wide distribution of muddy sediments (i.e. >50% of the open-water habitat), combined with generally polymictic conditions, result in high tripton concentrations
and low levels of light for phytoplankton growth, over large portions of the lake.
Within the region of muddy sediments, the area of greatest mixing depth, the
center of the lake (Figure 1), is subject to the most severe light limitation. This conclusion is supported by both empirical and experimental data from this study.
High winds encountered in the winter and spring seasons in South Florida
heighten the severity of light limitation by increasing tripton load in the water
column. This effect is more pronounced in regions of the lake characterized by
muddy flocculent sediments, i.e. the center and north (Phlips et ai, 1993,1995a).
Outside of the large region of muddy sediments, firmer sediment types prevail,
resulting in lower tripton concentrations. Since these areas are also characterized
by shallower mixing depths, light limitation gives way to nutrient limitation of
phytoplankton. The most severe nutrient limitation is experienced in the littoral
fringe regions where dense populations of benthic primary producers compete
with phytoplankton for available nutrients. Nutrient limitation in these regions is
most severe during the summer when wind-induced vertical and horizontal
mixing of water is at a minimum.
The region of transition between the predominantly light-limited central region
and nutrient-limited littoral fringe have historically been the site of frequent
phytoplankton blooms. The region between light and nutrient limitation has been
identified as a region of heightened productivity in estuarine ecosystems, e.g.
Georgia coastal estuary (Oertel and Dunstun, 1981). This transition region was
also the site of highest phytoplankton abundance in this study, indicating that
similar principles may apply to Lake Okeechobee.
Acknowledgements
We thank Claire Schelske and Frederick Aldridge for their review of this manuscript. We thank Ken Hall, Shanon Hall, Kristen McFarland, Mike Randall, Rema
Sakalas, Christine Wharton and Audrey Whitton for their participation in this
research. This research was funded by a grant from the South Florida Water
Management District, Contract C-52269. This paper is publication No. 4700 of the
Florida Agriculture Experimental Station Journal Series.
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Received on March 22,1996; accepted on October 10,1996
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