Journal of Water Resource and Protection, 2012, 4, 1029-1041 Published Online December 2012 (
Role of Suspended Sediments and Mixing in Reducing
Photoinhibition in the Bloom-Forming
Cyanobacterium Microcystis
Justin D. Chaffin, Thomas B. Bridgeman, Scott A. Heckathorn, Ann E. Krause
Lake Erie Center, Department Environmental Sciences, University of Toledo, Oregon, USA
Received October 2, 2012; revised November 4, 2012; accepted November 15, 2012
Toxic cyanobacterial blooms are becoming a global problem. Previous research of cyanobacterial bloom development
has examined how high nutrient concentrations promote cyanobacteria dominance, and how positive buoyancy provides
an ecological advantage over sinking phytoplankton. Tributaries responsible for loading nutrients into lakes often si-
multaneously contribute high concentrations of suspended sediments. High concentrations of suspended sediments may
also influence blooms by affecting the ambient light climate, reducing photodamage, and increasing the efficiency of
photosynthesis. We examined the effects of sediments and vertical mixing in potentially reducing photodamage to Mi-
crocystis by measuring photosynthetic parameters and pigment content of Microcystis in western Lake Erie during the
2008 bloom and in laboratory experiments. Photosynthetic efficiency increased with increasing sediment concentration
in the lake and laboratory experiment. Content of photo-protective carotenoid pigments per dry weight decreased with
increasing sediment concentrations, while the light-harvesting pigments, chl a and phycocyanin, increased with sedi-
ments. These results indicate that suspended sediments reduce photoinhibition for Microcystis. Further, photosynthetic
damage was higher when Microcystis was concentrated on the surface compared to a mixed water column. Measure-
ments of Microcystis abundance and light were also recorded, in addition to photosynthetic measurements. Greatest
Microcystis abundances in Lake Erie were recorded during light-limiting conditions, which offer Microcystis both
physiological and ecological benefits by reducing photoinhibition and increasing Microcystis’ advantage in light com-
petition via buoyancy. Efforts to reduce cyanobacterial blooms may include reducing suspended sediments loads in
combination with reducing nutrient loading.
Keywords: Chlorophyll Fluorescence; Cyanobacteria; Harmful Algae Bloom; Lake Erie; Microcystis; Suspended
1. Introduction
High biomasses of cyanobacteria, often called “blooms”,
are one of the foremost problems facing the protection of
water quality [1]. Cyanobacterial blooms are a concern
due to their toxins that affect aquatic animals, livestock,
and humans [2], and negatively impact local economies
[3]. Cyanobacterial blooms have become a global prob-
lem as a result of excess inputs of anthropogenic nutria-
ents [4]. Research devoted to the development of cyano-
bacterial blooms has been focused on high nutrient con-
centration, especially phosphorus (P) and nitrogen (N)
[5,6], low N-to-P ratios [7], water column stability [8,9],
global climate change [10,11], and Dreissena mussel
selective rejection [12]. Tributaries that are often respon-
sible for high nutrient concentrations in the adjacent wa-
ters of lakes may simultaneously contribute high concen-
trations of suspended sediments [13,14]. The impacts of
high suspended sediments on zooplankton, fish, and ben-
thic invertebrates is well known [15]. However, the ef-
fect of suspended sediments on cyanobacterial bloom
development, specifically Microcystis spp., is less under-
Suspended sediments increase the rate at which light is
attenuated with depth in aquatic ecosystems, as does high
phytoplankton abundance and dissolved organic com-
pounds [16]. Light attenuation affects photosynthesis as
phytoplankton acclimate to changes in light intensity in
time scales of seconds to days by altering their pigment
composition and photosynthetic rates [17]. High attenua-
tion results in less phytoplankton biomass due to light-
limited conditions [18], favoring cyanobacteria that can
regulate their vertical position in the water column and
remain in the photic zone. For example, the highly-
buoyant cyanobacterium Microcystis [9] can accumulate
opyright © 2012 SciRes. JWARP
high biomasses at the surface of a lake (often called a
“surface scum”) during periods of calm winds, no pre-
cipitation, and high atmospheric pressure [19]. Surface
scums can be exposed to high-light intensities for pro-
longed lengths of time, damaging photosynthetic ma-
chinery [20]. However, buoyancy only allows Microcys-
tis to form surface scums when the upward migration rate
exceeds the turbulent mixing of the water column [21].
Wind speeds greater than 3 m·s–1 will break up a surface
scum [19,22,23] and also circulate negatively buoyant
phytoplankton species into the photic zone, thus negating
the advantage of buoyancy regulation [9]. Previous re-
search has shown that vertical mixing of the water col-
umn provides relief from high-light intensities by circu-
lating Microcystis to deeper depths [24,25]. Furthermore,
river-generated sediment plumes increase phytoplankton
primary production [26]. However, there is currently a
poor understanding of how the interaction between mix-
ing of the water column and sediment plumes affects
Microcystis bloom formation.
Suspended sediments and nutrient concentrations often
co-vary in nearshore zones. In this manuscript we isolate
the effects of suspended sediments from the effects of
nutrients on the photosynthetic status of Microcystis
blooms in western Lake Erie and in laboratory experi-
ments. In another report, Chaffin et al. [27], analyzed the
nutrient status of the samples collected for this manu-
script and showed that all were N-replete while the ma-
jority of samples had a moderate P deficiency. Sediments
are loaded into Lake Erie from the Maumee River at the
rate of 800 tonnes per day [14] and the concentrations of
suspended sediments decreases from nearshore to off-
shore [28], which makes western Lake Erie an ideal loca-
tion to study the effects of suspended sediments on Mi-
crocystis bloom development. Furthermore, the spatial
pattern of Microcystis blooms in western Lake Erie
closely aligns with the Maumee River sediment plume
[27]. We use physiological measurements (chlorophyll
fluorescence and pigment content) as tools to determine
Microcystis’s photosynthetic status in response to the
difference of light intensity between sediment plume
water and clear water, and between calm water and
mixed water. We hypothesized that Microcystis surface
scums will be more photo-inhibited than Microcystis in a
mixed water column. We also hypothesized that high
concentrations of suspended sediments not only give
buoyant Microcystis an ecological advantage for light
competition, but also create a more favorable light cli-
mate for photosynthesis, providing a physiological bene-
2. Materials and Methods
2.1. Study Site
The Maumee River drains a large (16,376 km2) agricul-
tural (87.8%) watershed [29] that empties into the west-
ern corner of Lake Erie (Figure 1). The high sediment
load from the river [14] results in a steep gradient of high
suspended sediments and nutrient concentrations from
the Maumee River mouth to offshore Western Lake Erie
[28]. Further, the shallowness of Maumee Bay (<2 m)
and the western basin (mean depth of 7.4 m) allows for
frequent wind-induced sediment re-suspension from the
lake bottom [30]. Although a persistent summer thermo-
cline does not develop in western Lake Erie, diurnal
stratification is common [31]. However on calm days
diurnal thermal stratification (1˚C difference between
surface to bottom water) can suppress water column
mixing [32]. Longer calm periods may lead to episodic
(>2˚C) thermal stratification for periods ranging from 2
to 10 days [33]. Microcystis has an ecological advantage
during the periods of stratification [9], but also is ex-
posed to high-light intensity that may cause photoinhibi-
Microcystis spp. blooms have become an annual oc-
currence in western Lake Erie in recent years [34]. The
spatial pattern of the blooms closely coincides with the
near-shore suspended sediment plume [27,28], which
suggests conditions in the plume promote Microcystis
blooms. In the sediment plumes total P can reach con-
centrations greater than 5 mol· L –1 and secchi disk
depths are less than 50 cm due to high suspended sedi-
ments [27].
The light attenuation coefficient (kd) was used as a
proxy for suspended sediments. Both suspended sedi-
ments and phytoplankton can influence the kd measure-
ments. In Maumee Bay and western Lake Erie, however,
suspended inorganic particles are the major factor in re-
ducing water clarity [28,30]. Past measurements of sus-
pended sediments (as non-volatile suspended solids
(NVSS)) at our sample sites indicate that suspended
sediments can be predicted from kd (NVSS mg·L–1 =
(12.936 × kd) 11.244; N = 52, p < 0.001, r2 = 0.87,
Bridgeman unpublished data). There was no relationship
between kd and chlorophyll a (p = 0.671, r2 = 0.004,
Bridgeman unpublished data). Therefore, we use kd as an
index of suspended sediment concentration.
2.2. Limnological Measurements and Microcystis
In this report, we refer to the Microcystis spp. community
collectively as Microcystis. Microcystis aeruginosa
makes up the majority of the Microcystis population in
Lake Erie, but other species may be present [35]. Collec-
tions and measurements were made at six sites along an
approximately 80 km route in western Lake Erie and in
Maumee Bay (Figure 1) on ten dates from 7 July to 25
September 2008, approximaely once every 14 days. All t
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Figure 1. Sample locations in western Lake Erie. Contour lines are 5 meters and 9 meters. Site GR1 is located near the end of
a dredged shipping channel.
collections and field measurements were recorded be-
tween 10:00 am to 3:00 pm on full-sun days. At each site,
Microcystis abundance was estimated by the biovolume
retained in vertical plankton tow samples using a 112 m
mesh net as a part of a long-term study of Microcystis
abundance in western Lake Erie [27]. For photosynthetic
and pigment content measurements to be made in the
laboratory, Microcystis was collected from the lake using
a 64 m net, which captures 99% of Microcystis cells
[27]. The Microcystis collected was stored in dark poly-
ethylene bottles at ambient lake temperature during
transportation back to the laboratory. Depending on sam-
ple location, two to six hours passed between collection
on the lake and laboratory analysis. Upon arriving at the
laboratory, Microcystis was separated from other plank-
ton via buoyancy separation in Imhoff cones [27] and
examined for the presence of other phytoplankton species
by microscopy. These separated net samples were nearly
100% Microcystis, with exception of a trace amount of
Anabaena 24 July and 6 August.
meters to 5 meters, or at quarter-meter intervals in highly
turbid water. Light attenuation coefficients of PAR (kd)
were calculated as the linear regression slope of the
natural log of PAR vs depth [16]. The depth of the photic
zone was determined as the depth where light intensity
was 1% of that surface light intensity. Vertical position
of phytoplankton and Microcystis was determined by chl
a and phycocyanin (PC) concentration from lake water
collected at surface, 1 m, 3 m, and 5 m using a Van Dorn
bottle (see methods below).
2.3. Photosynthetic Parameters of Lake Samples
In this section, we made photosynthetic measurements
aboard the research vessel and collected samples for ad-
ditional photosynthetic measurements to be made in the
laboratory. Photosynthetic efficiency was measured as
the quantum yield of photosystem II (PSII) electron
transport (Φet). PSII is often the weak link of photosyn-
thetic electron transport, as it is most vulnerable to
light-induced damage, i.e. photoinhibition [36]. Φet natu-
rally decreases with increased light intensity, but de-
creases in Φet at a given light intensity indicate either
damage to PSII or post PSII electron transport, or photo-
protective down-regulation of electron transport [37]. Φet
is proportional to carbon fixation at a given light level
[38]. Onboard, Φet of the whole phytoplankton commu-
nity was measured on phytoplankton collected at the
surface and at 1 m depth for sample dates after 24 July
—when Microcystis was present. Water was collected
Vertical profiles of water temperature, pH, and dis-
solved oxygen were recorded using a YSI #6600 probe
(Yellow Springs Instruments, Yellow Springs, OH, USA).
Wind speed and direction were measured approximately
2 m above the surface of the water using a hand-held
anemometer (Kestrel #1000, Birmingham, MI, USA)
integrated over 15 seconds. Underwater photon flux den-
sity PAR (Li-Cor # LI - 188B with spherical sensor,
Lincoln, NE, USA) was recorded at every half-meter
from surface to 2 meters and at every one-meter from 2
using a Van Dorn bottle, transferred to dark polyethylene
bottles, and immediately filtered through Whatman GF/C
filters or Fisher Brand G4 filters (1.2 µm pore sizes) [39]
using low vacuum pressure (<10 cm Hg). Approximately
20 to 50 mL of water was used per filter. Filtering and
measuring of Φet took place in the boat’s cabin to avoid
direct sunlight. The Φet of phytoplankton was determined
within 60 seconds from collection, using an OS1-FL Opti-
Sciences modulated fluorometer (Hudson, NH, USA).
In the laboratory, light-response (PI) curves and the
maximal PSII quantum yield (Fv/Fm) measurements were
made with Microcystis collected from the lake. PI curves
were generated by measuring Φet at nine light intensities
from 20 to 1640 µmol photons m–2·s–1 using a Walz
fluorometer (model PAM 101/103, Effeltrich, Germany)
and light pulse provided by a Schott flash lamp (model
KL1500, Elmsford, NY, USA) [40,41]. The relative
electron transport rate (rETR) was calculated from Φet
and light intensity [42]: rETR = Φet × PAR × absorbance
constant, PAR is the light intensity, and 0.85 was as-
sumed to be the absorbance constant. The PI curve data
were fit to the equation of Zhang et al. [43], and then the
maximum rETR (rETRmax) was calculated. Fv/Fm was
determined on separate samples that had been dark-ac-
climated for 30 minutes [42]. Decreases in dark Fv/Fm
indicate damage to PSII. Even though the fluorometers
used here were designed for plants, they have been used
for cyanobacteria and have been shown to positively
correlate with net photosynthesis of cyanobacteria [40].
For further description of the chlorophyll fluorescence
parameters, please see Schreiber et al. [42], Campbell et
al. [40], or Maxwell and Johnson [36].
2.4. Pigment Content of Lake Samples
To determine the ability of Microcystis to alter photo-
synthetic pigment content (also to assist in interrupting
the photosynthetic fluorescence data, see Discussion), chl
a, PC, and total carotenoid content were determined on
Microcystis collected from the lake. Microcystis was
separated in Imhoff cones (as above), concentrated, and
then stored at –80˚C until analysis. Photosynthetic pig-
ments were extracted from still-frozen Microcystis. Chl a
and total carotenoid were extracted in dimethyl sulfoxide
heated to 70˚C for 45 minutes, then centrifuged at 21,000
g for 10 minutes to remove debris. Chl a and total caro-
tenoid were calculated from absorbance read using a UV -
1650 PC Shimadzu (Columbia, MD, USA) spectropho-
tometer [44]. Total carotenoid are presented relative to
chl a. PC was extracted in 0.1 M sodium phosphate
buffer pH 6.8 [45] with cells lysed by sonication (Bran-
sonic #1510, Danbury, CT, USA) in an ice bath for 15
minutes. Samples were incubated at 4˚C for 60 minutes
and then centrifuged for 10 minutes at 4600 g. PC fluo-
rescence was recorded in a 10 - AU Turner Design
fluorometer (Sunnyvale, CA, USA) with P/N 10 - 305
filters. PC was quantified using a standard curve of C-PC
standards. Pigment content was corrected for dry weight
(mg of pigment per g of dry weight tissue) determined by
drying tissue until a constant weight at 70˚C. Dry weight
was constant after 24 hours.
2.5. Laboratory Experiment
Suspended sediment concentration and nutrients often
co-vary, and each may potentially affect photosynthesis.
Water column mixing might also generate suspended
sediments in shallow lakes, possibly producing another
interaction effect. To isolate the effects of suspended
sediments, nutrients, and mixing, a 2 × 2 × 2 × 2 factorial
experiment was used to test the effects of nutrient con-
centration (low and high nutrients), suspended sediments
(low and high), mixing (mixed or non-mixing), and sam-
ple depth (surface and at depth) on photosynthetic effi-
ciency and pigments. All six treatment combinations
(nutrient × suspended sediments × mixing) were ran-
domized between trials and samples were collected from
both depth in each trial. The experiment was replicated in
three independent trials, with each treatment combination
in each trial. Experimental tanks were constructed of 61
× 9 × 90 cm (36.5 L) polyethylene bins. Experiments
were conducted in a greenhouse and exposed to natural
sunlight (up to 1500 µmol photons m–2·s–1) at ambient
temperature (25˚C - 28˚C).
De-chlorinated water was used for this experiment.
Mixing of the chamber was achieved using powerhead
pumps (Aquatic gardens #601, San Diego CA, USA), so
that the intake hose was placed at the bottom of the
chamber and outflow just beneath the surface. Suspended
sediments and nutrient treatments were chosen to reflect
conditions in Maumee Bay (high sediments and high
nutrients) and the center of the western basin (low sedi-
ments and low nutrients). Sieved (400 µm) Lake Erie
top-layer (0 - 2 cm) sediments were added to bring the
high sediment level to 30 NTU and low sediment level
was 1 NTU. After sediments were added, sodium nitrate
and sodium phosphate were added to bring the initial
concentration up to 215 mol N L–1 and 4.85 mol P L–1
for the high nutrient and 43 mol N L–1 and 0.97 mol P
L–1 for the low nutrient treatment, which reflect Maumee
Bay and offshore western basin, respectively [27]. All
other nutrients were at half concentration of the WC me-
dium [46] and were the same among all experimental
treatments. Cultures of Microcystis with a know chl a
level were added so that each chamber had an initial chl
a of 2.5 µg·L–1. Microcystis that was intended for the
experiment were grown in separate liquid cultures with
the nutrient concentration of the low treatment level for
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two weeks before use in the experiment, to insure that
internal phosphorus storage did not take place. This Mi-
crocystis was collected from Lake Erie during 2008 and
cultured in laboratory.
Once treatments were set up and Microcystis added, 96
hours were allowed for growth. Following the 96 hours,
samples were collected at the surface and at a depth of 70
cm. At 70 cm, light levels in the low-sediment treatment
were approximately 20% of surface light (measured just
beneath water surface). In the high-sediment treatment,
light levels at 70 cm were <0.5% of the surface irradi-
ance. At the end of the incubation period, 100 mL of wa-
ter containing phytoplankton was filtered onto GF/F fil-
ters and Φet was measured within 60 seconds after collec-
tion. Separate samples were dark-acclimated for 30 min-
utes and Fv/Fm was determined. Φet and Fv/Fm were de-
termined on filters as above. Chl a and total carotenoid
concentration were determined on the filters as above.
Photosynthetic measurements and light levels were re-
corded between 12:00 pm and 2:00 pm on sunny days.
2.6. Data Analysis
Past studies of cyanobacteria surface scum formation [19]
classified the presence or absence of a surface scum
based on visual observations of cyanobacterial colonies
at the surface. In this study, we attempt to determine if a
surface scum is present or absent based on quantitative
measurements of wind speed, water temperature profiles,
and phytoplankton vertical position (Table 1). Water
temperature profiles are often used to separate the epili-
mnion from the hypolimnion; however, western Lake
Erie usually lacks thermal stratification. The concentra-
tion of photosynthetic pigments (chl a and PC) at the
surface relative to 1 meter allows determination of how
much of the phytoplankton is concentrated at the surface
(hence a surface scum). PC concentration gives insights
to how much of the chl a is due to Microcystis. Samples
that were collected when Microcystis was concentrated at
the surface (low wind speed, high ratio of surface:1 me-
ter pigment concentration) were classified as a “surface
scum”, while samples collected when Microcystis was
circulated down to deeper depths (high wind speeds, low
ratios of surface:1 meter pigments) were classified as
To determine the effects of suspended sediments, ver-
tical mixing of the water column, and depth on the
phytoplankton community in situ Φet (n = 59), ANCOVA
models were used to tests for the effects of depth (0 me-
ter, 1 meter), mixing (surface scum or mixed), and sus-
pended sediments (kd, range: 0.44 to 4.83 m–1) on Φet.
Statistics were computed using PROC REG of the statis-
tical software SAS (v. 9.1, Cary, NC, USA) by con-
verting our categorical factors (depth, mixing) into indi-
cator variables [47] and kd was the covariate. Signifi-
cance was determined with
= 0.05 for all tests.
The effect of suspended sediments on photosynthetic
parameters measured from the PI curve, Fv/Fm, and pig-
ments (chl a, PC, total carotenoid:chl a) was analyzed
using linear regressions vs kd. Surface scums and mixed
samples were analyzed separately because ANCOVA
test for parallel slopes indicated that slopes were not par-
allel for all parameters, hence not appropriate for AN-
COVA test.
For the laboratory experiment, four-way ANOVAs
were performed to test for the effect of mixing (mixed or
calm), sediments (high or low), nutrients (high or low),
and sample depth (surface and at depth) on Φet, Fv/Fm,
and total carotenoid:chl a. Tukey HSD test was per-
formed for multiple comparisons. PROC GLM of SAS
was used [47].
Table 1. Classification of “surface scum” or “mixed” conditions based on wind speed, chlorophyll (chl) a, and phycocyanin
(PC) profiles. Surface:1 meter is the ratio of chl a or PC measured at the surface relative to chl a or PC measured at 1 meter.
Values greater than 1 indicate that phytoplankton is concentrated at the surface. PC:Chl a is the ratio of PC to Chl a aver-
aged across all six sites and depths. Values are averages (±SE) across 6 sample sites.
July 24 August 6 August 12 August 21 September 1 September 25
Surface Scum
Mixed Present Present Mixed Mixed Present
Wind Speed
(m·s–1) 3.83 ± 0.38 1.28 ± 0.30 1.62 ± 0.25 3.90 ± 0.19 3.62 ± 0.29 1.73 ± 0.43
Surface Chl a
(g·L–1) 15.42 ± 10.4 38.47 ± 18.2 28.52 ± 15.6 15.24 ± 2.9 31.80 ± 2.1 227.17 ± 176.0
Surface Chl a:1 m
Chl a 1.00 ± 0.05 1.81 ± 0.61 3.02 ± 1.96 0.99 ± 0.03 1.07 ± 0.07 6.95 ± 4.99
Surface PC
(g·L–1) 0.38 ± 0.2 35.25 ± 18.1 46.47 ± 39.9 14.63 ± 5.4 22.67 ± 3.5 89.04 ± 66.2
Surface PC:1 m PC 1.38 ± 0.21 5.31 ± 2.63 9.70 ± 8.11 1.51 ± 0.08 1.04 ± 0.08 17.41 ± 11.35
PC:Chl a 0.03 ± 0.01 0.47 ± 0.17 0.97 ± 0.45 0.67 ± 0.15 0.66 ± 0.07 0.33 ± 0.09
3. Results
3.1. Lake Properties
Figure 2 displays Microcystis abundance, light availabil-
ity, and water temperature in western Lake Erie during
2008. Microcystis was absent from net tows until 24 July,
and during this time the photic depth to lake depth ratio
was greater than 0.5, indicating a high-light environment.
Between 12 August and 21 August Microcystis bio-
volume retained in nets increased nearly four-fold and
remained high for the rest of the summer. On 21 August
through rest of summer, the photic depth to lake depth
ratio was less than 0.2. Water temperature was between
22˚C and 26˚C during the Microcystis bloom. Dissolved
oxygen (DO) ranged from 7.6 to 10.2 (mg·L–1) and pH
from 8.0 to 8.6 from measurements at 1 meter depth at all
sites and dates. DO and pH did not vary with depth ex-
cept on 6 August when there was a 1.1 mg·L–1 difference
in DO and 0.5 in pH between surface and near sediments
at stratified sites. kd was relatively low from June to mid
August at all sites except MB20– the site closest to the
Maumee River (Figure 3). Much higher kd was recorded
following mid August. On each sample date, there was a
general pattern with highest kd measured in Maumee Bay
(sites MB20 and MB18), and lower kd further from shore
(sites GR1 and 4P).
Thermal stratification was only observed on 6 August,
with 2˚C difference between the surface and bottom wa-
ters. Wind speed, chl a, and PC concentration were used
to classify each sample date as surface scum or mixed
Figure 2. Light availability as photic depth/lake depth
(dashed line; filled circles), temperature (dotted line; open
triangles) and Microcystis biovolume (bold line; open squa-
res) in western Lake Erie during 2008. Arrows represent
sample dates with mixed conditions. The horizontal dashed
line with no symbols corresponds to 0.16, the value that
indicates light limitation of phytoplankton biomass [18].
Values are the mean (±SE) of six sites.
Figure 3. Light attenuation coefficients (kd) recorded in
western Lake Erie at 6 locations during summer 2008. Site
MB20 was not sampled on 21 August.
(Table 1). Microcystis was concentrated as a surface
scum on 6 August, 12 August, and 25 September. On
these dates, wind speeds were less than 1.73 m·s–1, which
allowed Microcystis to float and become concentrated on
the surface as indicated by high surface chl a - 1 meter
chl a ratios. Therefore, 6 August, 12 August, and 25
September were classified as “surface scum” dates. Wind
speeds greater then 3.62 m·s–1 on 24 July, 21 August, and
1 September resulted in the Microcystis mixing down to
deeper depths preventing a surface scum. Surface chl a
and PC concentrations were nearly identical to chl a and
PC concentrations measured at 1 meter and half-water-
column-depth. 24 July, 21 August, and 1 September were
classified at “mixed” dates because Microcystis was not
concentrated at the surface. The low PC:Chl a ratio on 24
July would indicate that Microcystis was not the domi-
nant phytoplankton on this date, however, large Micro-
cystis colonies were visible and abundant enough on 24
July to collect with plankton net for measurements to be
made in the laboratory.
3.2. Photosynthetic Parameters of Lake Samples
Φet increased linearly with increasing kd (p < 0.0001) for
samples collected from both the surface and 1 meter
(Figure 4). Φet was greater at 1 meter than surface, due
to lower light intensity at 1 meter. Mixing did not have a
significant effect on Φet (p = 0.345), however, mixing
increased Φet at higher kd values compared to scum sam-
ples. Interactions were not significant (p = 0.551).
Fv/Fm of Microcystis was higher when collected when
the lake was vertically mixed compared to surface scum
(Figure 5(a)). kd did not affect Fv/Fm for either mixed (p
= 0.11; r2 = 0.196) or surface scum (p = 0.55; r2 = 0.028)
samples. rETRmax significantly (p = 0.0076; r2 = 0.460)
increased with kd when collected during mixing, but was
unaffected during surface scum (p = 0.40; r2 = 0.060)
Copyright © 2012 SciRes. JWARP
Figure 4. Photosynthetic efficiency (Φet) measured in west-
ern Lake Erie at the surface (thick lines, circles) and at 1
meter depth (thin lines, triangles), and either when surface
scum was present (solid lines, filled symbols) or mixed
(dashed lines, open symbols) as a function of light attenua-
(Figure 5(b)). rETRmax was greatest at light intensities
less than 1044 µmol photons m–2·s–1, thus high light
caused photoinhibition, especially at low kd. On average,
rETRmax for scum samples occurred at 348 µmol photons
m–2·s–1, while at 618 µmol photons m–2·s–1 for mixed
samples. The ability to maintain photosynthesis under
high-light intensity is presented as rETR measured at
1044 µmol photons m–2·s–1 (Figure 5(c)). Mixed samples
had rETR at 1044 µmol photons m–2·s–1 that significantly
(p = 0.0009; r
2 = 0.676) increased with increasing kd,
while surface scum Microcystis were not affected (p =
0.77; r2 = 0.007) by kd.
3.3. Pigment Content of Lake Samples
ANCOVA analysis revealed that sample location did not
significantly affect chl a (p = 0.81), PC (p = 0.12), and
total carotenoid:chl a (p = 0.28). Regressions analysis
revealed that the chl a linearly increased with increasing
kd (p = 0.0004, r2 = 0.513), and PC increased linearly
six-fold with increasing kd (p = 0.0003, r2 = 0.526) (Fig-
ures 6(a) and (b)). Total carotenoid:chl a decreased with
increasing kd (p = 0.0012, r2 = 0.450) (Figure 6(c)). Total
carotenoid content ranged from 2.11 mg·g–1 to 3.38
mg· g –1.
3.4. Labotory Experiment
The laboratory photosynthetic efficiency experiment
produced results similar to and consistent with the lake
study. Suspended sediments significantly (p < 0.0001)
increased Φet for each treatment combination of mixing
and depth (Figure 7(a)). Φet was significantly affected by
the depth*mixing interaction (p < 0.0001). Nutrients
Figure 5. Fv/Fm (a), maximum relative electron transport
rate (rETRmax; (b)), rETR at light intensity 1044 mol pho-
tons m–2·s–1 (c) from light response curves generated in the
laboratory from Microcystis collected in western Lake Erie,
as a function of in-lake light attenuation.
(high P and N vs low P and N) did not have a significant
effect on Φet, and no other interactions were present (p >
0.5). Tukey test showed that Φet was statistically greater
(p < 0.05) at depth than at the surface for the calm treat-
ment among both suspended sediments levels.
Fv/Fm was significantly affected only by suspended
sediments (p = 0.0004). Fv/Fm was greatest in the high-
sediment treatment (Figure 7(b)). Depth, mixing, nutria-
ents, or their interactions did not significantly affect
Fv/Fm (p > 0.1).
The total carotenoid:chl a ratio was only significantly
affected by suspended sediments (p = 0.0007). Total ca-
rotenoid:chl was 0.412 ± 0.018 in the low-sediment
treatment, and 0.318 ± 0.013 in the high-sediment treat-
ment. Total carotenoid:chl a was not affected by any
other factors or their interactions (p > 0.4).
Copyright © 2012 SciRes. JWARP
Figure 6. Chl a (a) and phycocyanin (b) content and the
ratio of total carotenoid to chl a (c) of Microcystis collected
in western Lake Erie as a function of light attenuation.
4. Discussion
4.1. Sediment Plumes and Moderate Mixing
Favor Microcystis
Our study conducted in western Lake Erie, which re-
ceives a heavy suspended sediment load from the Mau-
mee River [14] and lake bottom resuspension [30], dem-
onstrated how sediment plumes increase Microcystis
photosynthetic status relative to clear water. Tributaries
[13] and resuspension [48] also increase P concentration
of lakes, but here we isolate the effects of suspended
sediments and nutrients. Φet measured at the lake surface
increased with increasing suspended sediments in both
the lake study and laboratory experiment (Figures 4 and
7(a)), which indicates increased protection from high-
light intensities with increasing suspended sediment
concentration. The greater Φet measured at 1 meter is a
factor of light attenuation with depth, hence greater Φet.
The lake Φet samples were community measures, while
only Microcystis was used to the laboratory experiment,
Figure 7. In situ quantum yield of photosystem II electron
transport (et) of light-adapted samples (a), and Fv/Fm of
dark-adapted samples (b) of Lake Erie Microcystis grown in
laboratory conditions under natural sunlight intensities,
high or low suspended sediments, and mixing or calm wa-
yet they yielded similar results, because Microcystis
dominated the lake samples. Therefore, Microcystis (as
well as other phytoplankton) at the surface of a lake high
in suspended sediments will have greater photosynthetic
efficiency than Microcystis at the surface of a clear lake.
Microcystis is able to remain at or near the surface of
the lake, which provides a competitive advantage in
light-limiting conditions over negatively buoyant phyto-
plankton [9]. However, this advantage comes at a phy-
siological price. Surface Microcystis scums become
damaged, as indicated by the depressed Fv/Fm values
compared to mixed water column samples (Figure 5(a)).
Data generated from PI curves further support the hy-
pothesis of photosynthetic damage to surface scums be-
cause rETRmax (Figure 5(b)) and the ability to handle
high-light intensity (Figure 5(c)) were not affected by kd
measured during sample collection. In contrast, the non-
damaged samples collected during mixing responded
with increasing rETRmax and increasing rETR at high-
light intensity with increasing kd. However, suspended
sediments increased Φet in the surface scum samples in
the lake study and laboratory experiment (Figures 4,
7(a)). Thus, the depressed surface Φet values recorded in
clear water during the lake study with low kd must be a
Copyright © 2012 SciRes. JWARP
result of photo-protective down-regulation, as opposed to
further damage, because Fv/Fm did not change with kd
(Figure 5(a)). In the lake and laboratory study, among
surface samples, Φet was greater in mixed-water condi-
tions when compared to calm waters with a surface scum
(Figures 4 and 7(a)). Surface scums in the calm water
would have a high average light exposure, while average
light exposure would be less in a mixed water column.
Mixing would transport surface Microcystis and other
phytoplankton downward, providing relief from high-
intensities of light, while upward-mixing exposes phyto-
plankton that were adapted to low-light levels at depth to
high-light intensities near the surface.
Vertical mixing, on the other hand, circulates Micro-
cystis throughout the water column, which decreases
exposure to high-light intensities preventing photosyn-
thetic damage. However Microcystis growth stops in
strongly-mixed waters [49,50], and the competitive edge
is shifted towards negatively buoyant phytoplankton [9].
Microcystis would benefit from moderate winds that
break up the surface scum, yet allow it to maintain a rela-
tively higher position in the upper water column than
competing species. Microcystis biovolume rapidly in-
creased between 12 August and 21 August (Figure 2).
During this time, the median mid-day wind speed meas-
ured at Toledo, Ohio was 2.23 m·s–1 (National Oceanic
and Atmospheric Administration, Data Station THRO1
9063085, Toledo, OH,
php?station=THRO1). This wind speed would provide
the ideal mixing condition for Microcystis, allowing the
buoyant Microcystis to maintain position in the upper
portion of the water column, but also prevent long-term
exposure to direct sunlight.
Reduced Fv/Fm indicates that photo-damage was ob-
served in Microcystis collected from the lake; however,
very little damage was seen in the laboratory experiment
(Figure 7(b)). This difference could be due to our inabil-
ity to replicate full-sunlight intensity in the laboratory. In
the lake, Microcystis was exposed to full sunlight that
exceeded 2000 μmol photons m–2·s–1 PAR at the surface,
while the maximum light intensity of the laboratory ex-
periment was around 1400 μmol photons m–2·s–1 PAR for
shorter periods of time. This suggests that Microcystis
may become light damaged at intensities between 1400
and 2000 μmol photons m–2·s–1 PAR. UV radiation
would also result in damage [39], and greenhouse glass
blocks most UV radiation, thus we would have had a
reduced UV effect in our experiment.
4.2. Microcystis Alters Pigment Content
Care needs to be taken when analyzing cyanobacteria
fluorescence data [40], because, unlike higher photosyn-
thetic organisms wherein fluorescence originates only
from chlorophyll, PC also provides fluorescence in cya-
nobacteria. Steady-state fluorescence of light-acclimated
and minimum fluorescence of dark-acclimated samples
increases with PC content, therefore lowering Φet and
Fv/Fm values even if PSII function is not inhibited [40].
We recorded higher PC content in turbid waters. If PSII
function was similar between clear water and turbid wa-
ter, we would expect decreased Φet and Fv/Fm in turbid
water due to higher PC content. This was not the case,
because Φet and Fv/Fm were greater in turbid water; thus,
our pigment data further support our fluorescence data.
Numerous laboratory studies have shown that cyano-
bacteria grown under different light intensities photoac-
climate by altering the amount of the light-harvesting
pigments and photo-protective pigments [17,51]. Photo-
acclimation among phytoplankton in deep stratified lakes
has also been shown [16,52]. The photosynthetic pigment
data presented here indicates that Microcystis alters its
pigment content in response to changes in water clarity
on spatial and temporal scales in Lake Erie (Figure 6).
These results have implications for using pigment con-
centration as a proxy for phytoplankton biomass, because
chl a and PC content vary with water clarity. Therefore
pigment concentration may be an inaccurate proxy for
algal biomass, especially when comparing turbid-near-
shore to less-turbid-offshore waters of large lakes. For
example, based on an analysis of PC content alone, the
Microcystis biomass in turbid Maumee Bay would likely
be overestimated by a factor of six relative to the clearer
open waters of the lake. Moreover, PC fluorescence is a
new tool to monitor lakes for potential toxin-producing
cyanobacteria blooms [53,54]. Chl a is less variable than
PC with water clarity, but could still result in an overes-
timation of algal biomass by a factor of two over the
range of water clarity conditions observed in our study.
On the other hand, researchers utilizing PC fluorescence
may overlook potential harmful blooms during the early
low-biomass stage of bloom development in clear lakes.
Carotenoids have several functions, acting as light-
harvesting pigments and also as photo-protective mole-
cules [52]. Paerl et al. [55] observed a steady increase in
total carotenoid:chl a of Microcystis over a summer in
the Neuse River (North Carolina, USA) and attributed
the high carotenoid content to its survival near the sur-
face of lakes in high intensity sunlight. In contrast, we
measured a decrease in Microcystis’ carotenoid:chl a
ratio throughout the summer of 2008. Our results differ
from Paerl et al. [55] because the 2008 Lake Erie Micro-
cystis bloom first appeared during relatively clear water
conditions and needed more photo-protective carotenoid
pigments. After the water clarity decreased in mid-Au-
gust, the need for photo-protective pigments decreased
and the need for light-harvesting pigments would have
Copyright © 2012 SciRes. JWARP
4.3. Effect of Nutrients
In order for phytoplankton to acclimate to different light
intensities, nutrients, especially N, needs to be available
[56,57], mostly due to the N demand in the chl a and PC
molecules. In a parallel study, Chaffin et al. [27] as-
sessed Microcystis nutrient status via cellular N and P
content and ratios to carbon (C) and showed that all sam-
ples were N-replete and many of samples were moder-
ately deficient in P, but 30% of the Microcystis had no
nutrient deficiency. The content of chl a and PC ex-
plained 70% of the variation in the N content [27]. Thus,
Microcystis had sufficient N to meet the N demand re-
quired to produce chl a and PC in waters with high con-
centrations of suspended sediments.
Low nutrient concentrations can exacerbate the effect
that high-light has on photoinhibition [58]. Microcystis
cultured in low P concentrations will have decreased
rETR values of the PI curve [59]. Furthermore, low nu-
trient concentrations have been documented to decrease
phytoplankton Φet [60] and Fv/Fm [61] including Lake
Erie [62]. On the contrary, Harrison [63] showed the nu-
trient status of phytoplankton did not affect the Fv/Fm. In
our laboratory experiment nutrients did not affect Fv/Fm
or Φet , and furthermore, linear regression between Fv/Fm
and the N and P quota reported in Chaffin et al. [27] re-
sulted in non-significant relationships (p > 0.1). Our
finding that nutrients did not affect Fv/Fm differs with
Rattan et al. [62] who concluded nutrient deficiency
would decrease Fv/Fm. Rattan et al. [62] collected data in
Lake Erie during 2005 and reported that many of their
samples had C:N ratios that would indicate a moderate N
deficiency. We conducted our study during 2008 and
Microcystis did not have a N deficiency. Because nutria-
ent concentration did not affect Φet or Fv/Fm in both the
laboratory experiment and the 2008 lake samples, the
photoinhibition observed in clear water was not due to
lower nutrient concentration, but from lack of protective
suspended sediments.
4.4. Microcystis Abundance
The increase of suspended sediments during mid August
resulted in a light limited water column (Figure 2).
Lakes with higher concentrations of suspended sediments
often have lower total phytoplankton abundance due to
light limitation [4,64]. Microcystis would be less affected
by light limitation because of buoyancy regulation [65],
which was seen in our study because Microcystis ob-
tained high abundances during light limitation (Figure 2).
The data presented here suggest suspended sediments
favor Microcystis blooms, although other factors could
have contributed to the increase of Microcystis abun-
dance. Sediments and nutrients co-vary in our study site,
and the increase of sediments was accompanied by total
P concentrations that increased from 1.61 mol· L –1 to
2.91 mol· L –1 from July to September [27]. Stratification
is important to the success of Microcystis [9]. Low wind
speeds during the time Microcystis abundance rapidly
increased would have suppressed vertical mixing [32].
Seasonal succession patterns are not evident because
water temperature during 2008 was between 22˚C and
26˚C (Figure 2), and because the annual bloom can peak
at different times of the summer [27]. Non-quantified
factors such as grazers removing Microcystis’ compete-
tors [12,66] could also have influenced Microcystis abun-
dance patterns.
5. Conclusion
The negative impacts of suspended sediments on fish and
benthic macroinvertebrates are well known [15]. In this
report we show suspended sediments negatively affect
eutrophication by providing Microcystis a more favor-
able light climate for photosynthesis. Western Lake Erie
is usually turbid due to high suspended sediment loading
from the Maumee River [14,28]. Also, resuspension of
lake sediments [30], dredging of the shipping canal, and
open water disposal of those dredged sediments increase
turbidity. Although resuspension does not affect long-
term lake recovery following nutrient reductions [67],
resuspension or dredging during a Microcystis blooms
will acerbate that bloom. Thus, the effects of suspended
sediments should not be ignored when planning lake res-
toration. Because suspended sediments can be an impor-
tant factor in promoting buoyant cyanobacteria such as
Microcystis, future efforts to reduce blooms may include
components aimed at reducing suspended sediments
combined with reducing nutrient loading.
6. Acknowledgements
The authors would like to thank Dr. Sasmita Mishra for
laboratory assistance, Dr. Cyndee Gruden for use of their
lab’s sonicator, Dr. Mike McKay for a phycocyanin pro-
tocol, our team of undergraduates (Jesse Filbrun, Steve
Timmons, Catie Wukusick, and Janine Cannell) for as-
sistance collecting data in the field and setting up the
laboratory experiments. We thank anonymous reviewers
who provided helpful comments. This research was sup-
ported by the Ohio Sea Grant College Program, Project
R/ER 72, under Grant NA16RG2252 from the National
Sea Grant College Program, National Oceanic and At-
mospheric Administration and by funds provided by the
Lake Erie Commission, Lake Erie Protection Fund Pro-
ject #0-08. This is contribution number 2012-14 of the
Lake Erie Center.
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