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Warm spring and summer water
temperatures in small eutrophic lakes
of the Canadian prairies: potential
implications for phytoplankton
and zooplankton
ALAIN P. DUPUIS*† AND BRENDA J. HANN
DEPARTMENT OF BIOLOGICAL SCIENCES, UNIVERSITY OF MANITOBA, Z320 DUFF ROBLIN BLDG, WINNIPEG, MB, CANADA R3T
†
PRESENT ADDRESS: FISHERIES AND OCEANS CANADA, FRESHWATER INSTITUTE,
2N2
501 UNIVERSITY CRESCENT, WINNIPEG, MB, CANADA R3T 2N6
*CORRESPONDING AUTHOR: [email protected]
Received February 11, 2008; accepted in principle December 15, 2008; accepted for publication January 1, 2009; published online 24 January, 2009
Corresponding editor: Mark J. Gibbons
Shallow, polymictic lakes with low heat storage capacity are especially susceptible to warmer
spring conditions, predicted for a changing climate. In these lakes, atmosphere to water mass heat
transfer is efficient as a result of high wind exposures and large surface areas relative to volumes.
We examined effects of warmer water temperatures on phytoplankton and zooplankton abundance
and species composition in three small eutrophic lakes (5.2 – 14.9 ha) of the Canadian prairies in
Winnipeg, Manitoba, Canada, over two open-water seasons with contrasting spring weather conditions, i.e. 2005-a “normal” spring and 2006-a warm spring. Warmer spring and summer
water temperatures were associated with decreased water transparency, increased phytoplankton
biomass, increased relative filamentous cyanobacteria biomass and shifts in dominant genera from
Aphanizomenon to Anabaena and Planktothrix. Zooplankton responded strongly; abundance of
Daphnia (D. pulicaria, D. ambigua and D. parvula) decreased while rotifers, Skistodiaptomus
oregonensis and Bosmina longirostris increased in abundance. Of several factors influencing phytoplankton dynamics, total dissolved nutrients [nitrogen (N), phosphorus (P) and N:P] and water
column stability did not show important changes between years. In contrast, water temperature
[described as the metric degree-days (8C day)] was related to changes in phytoplankton and %
cyanobacteria biovolume. Daphniid abundance showed a significant negative relationship with an
increase in filamentous cyanobacteria biomass and, thus we suggest, was indirectly associated with
increased water temperatures.
I N T RO D U C T I O N
Warming air temperatures and changing climatic conditions have been linked to plankton population variability in both marine (Edwards and Richardson, 2004)
and freshwater (George and Taylor, 1995; Straile, 2000;
Winder and Schindler, 2004) ecosystems. Small shallow
lakes, in contrast to deep water-bodies, are especially
susceptible to warmer air temperatures (Adrian et al.,
1999; Gerten and Adrian, 2000). The seasonal period at
which changes occur may affect the magnitude of
impact on freshwater food webs. During spring, lakes
with small volume to surface area ratios efficiently transfer heat across the atmosphere – water interface leading
to water temperatures closely matching those of
ambient air (Carpenter et al., 1992). Downing et al.
(Downing et al., 2006) showed that small water-bodies
doi:10.1093/plankt/fbp001, available online at www.plankt.oxfordjournals.org
# The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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(,1 km2) predominate by surface area in a recent
survey of the world’s lakes and this may suggest that a
changing climate would have broad-ranging consequences for freshwater systems.
Long-term studies on shallow eutrophic lakes have
shown correlations between spring water temperatures
and the dynamics of phytoplankton and zooplankton
(Adrian et al., 1999; Gerten and Adrian, 2000; Benndorf
et al., 2001). For example, in Müggelsee, Germany, a
shallow eutrophic lake, warmer water temperatures in
late April and early May caused an earlier onset of the
spring daphniid peak and the clear-water phase (Gerten
and Adrian, 2000). Further, George and Hewitt
(George and Hewitt, 2006) demonstrated that interannual variations in temperature and wind speed not
only correlated with daphniid abundance but also with
an increased abundance of filamentous cyanobacteria.
Increased water temperatures have led to longer periods
of dominance of cyanobacteria in some eutrophic lakes;
hence, further research is needed to elucidate what
impact this might have on zooplankton populations,
particularly at the species level (Adrian and Deneke,
1996). Few studies have investigated impacts of warming
on small grazers such as rotifers that may be important
food-web components in years when larger daphniids
are lacking (Tirok and Gaedke, 2006).
This study examines the implications of a warm spring
and summer on plankton dynamics in three small
eutrophic lakes in the Canadian prairies (the Fort Whyte
lakes in Winnipeg, Manitoba, Canada). An increase in cyanobacteria biomass and a decline in large herbivorous zooplankton coincided with warmer spring temperatures in
2006 (+2.98C above the 30-year average) relative to that
experienced in 2005 (+0.98C above the 30-year average).
With conditions of warmer water temperatures we
expected an increase in phytoplankton and zooplankton
biomass however, alternative dynamics were possible.
Other factors associated with cyanobacterial prevalence
include high nitrogen (N) and phosphorus (P) concentrations (Downing et al., 2001), low N:P ratios (Schindler,
1977; Smith, 1983) and high water column stability
(Reynolds and Walsby, 1975) and may be more important
than the influence of relatively small increases in water
temperatures (+28C). For large herbivorous zooplankton,
warmer water temperatures could alter the importance of
bottom-up (food quality) and/or top-down (planktivory)
mechanisms. Our approach was to use commonly collected
limnological variables (temperature profiles, nitrogen and
phosphorus concentrations and plankton) sampled at a
high frequency over both a cooler (2005) and a warmer
(2006) open-water season to examine potential implications
for phytoplankton and zooplankton dynamics. Using our
data, we addressed the following objectives. (i) To identify
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and contrast changes in the plankton community between
a cooler and a warmer thermal regime. (ii) To present
potential explanations for the documented changes.
METHOD
Study site
The Fort Whyte lakes (498 49.0200 N, 978 13.4400 W)
situated in Winnipeg, Manitoba, Canada are a set of
five man-made lakes, constructed at 20-year intervals
starting in 1920 (Loadman, 1980). Inflows to the lakes
are restricted to spring runoff draining from adjacent
agricultural fields, mixed-grass bison pasture, deciduous
forest and urban developments. They are presently used
as an environmental education centre (www.fortwhyte.
org) and receive nutrient inputs from the on-site
primary treatment lagoon and from migrating Canada
geese in the fall. For the purpose of this study, Lakes 2,
3 and 4 were selected as suitable models for small
eutrophic lakes representative of many prairie waterbodies such as small lakes, large ponds, impoundments
and dugouts. These lakes have small surface areas (5.2–
14.9 ha), intermediate mean depths (4.5– 5.0 m) and a
gradient in nutrient concentrations, although they are
interconnected via narrow channels (Table I).
Spring conditions (April and May) in 2006 were
2.98C warmer compared to average conditions from
1971 to 2000 (Environment Canada, 2004). While
ice-off occurred on April 14 in both 2005 and 2006, air
Table I: Morphological and chemical
characteristics of the Fort Whyte lakes,
Winnipeg, Manitoba, Canada
Parameter
Lake 2
Lake 3
Morphometry
Surface area
5.18
9.38
(ha)
23.45
43.47
Total volume
(104 m3)
Mean depth (m)
4.5
4.6
Maximum
8.4
7.5
depth (m)
Chemistry
30.87 (22.39)
54.32
Chlorophyll a
(+SD) (mg L21)
Total nitrogen
95.44 (23.35)
142.50
(+SD) (mM)
Total
3.70 (1.57)
5.64
phosphorus
(+SD) (mM)
Alkalinity (+SD) 4768.75 (171.67) 4393.75
(meq L21)
Lake 4
14.91
74.14
5.0
8.3
(39.47)
84.88 (50.79)
(54.52)
171.31 (52.14)
(2.70)
6.97 (2.74)
(226.96) 4488.75 (185.51)
Chemistry data reported as mean (+SD) May–August values for 2005 –
06.
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temperatures in April and May remained on average
28C higher in 2006 compared to 2005. As a result,
spring and summer thermal profiles were altered substantially (Fig. 1). Across Lakes 2, 3 and 4, mean
May temperatures of the epilimnion increased from
10.3 to 11.48C in 2005 compared with 13.1 to 13.88C
in 2006, an average increase of 2.58C (Fig. 1). Summer
(June– August) water temperatures also increased in
Lakes 2, 3 and 4 in 2006 increasing from a mean epilimnetic temperature of 20.28C in 2005 compared with
21.4– 21.88C in 2006.
Data collection
All three lakes were sampled weekly in 2005 and twice
weekly in 2006, weather permitting, at the deepest
point of each lake. On each sampling date, water transparencies were measured with a Secchi disc and temperature profiles were collected at 1-m intervals with an
YSI multi-probe meter (Model 55). Water chemistry
samples were taken from just below the surface and
analysed for total dissolved nitrogen and total dissolved
phosphorus (TDN and TDP), total nitrogen and total
Fig. 1. Contour plots of temperature profiles (8C) from May to August at the Fort Whyte lakes 2 (A and B), 3 (C and D) and 4 (E and F)
during the years 2005 and 2006.
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phosphorus (TN and TP) as well as chlorophyll a (chl
a). Analyses were completed in the water analysis lab at
the Freshwater Institute, Department of Fisheries and
Ocean in Winnipeg, MB using standard methods
(Stainton et al., 1977).
Phytoplankton samples were collected just below the
surface using glass scintillation vials (20 mL) and were
preserved with Lugol’s solution and stored in the dark. In
2006, an integrated epilimnetic phytoplankton sample
was also collected by combining water samples taken at
1-m intervals throughout the epilimnion for comparison
with the subsurface samples. Our analysis showed that,
on average, the estimation of the phytoplankton biomass
in subsurface samples was within 13% of that estimated
for the integrated epilimnion samples. To maintain consistent methods between years, only the subsurface
samples were further analysed. On each sampling date,
integrated zooplankton samples were taken through the
epilimnion to the surface using a 25 cm diameter
Wisconsin zooplankton net with a 73 mm mesh size at
similar periods during the day, i.e. between 9:00 and
11:00 am. A 73 mm mesh size was used in an effort to
maximize net efficiency (to prevent clogging under conditions of high algal biomass) and minimize loss of small
zooplankton passing through the net. As a result, the
abundance of small rotifers (,73 mm) was likely underestimated. Zooplankton samples were preserved with 95%
ethanol. In our study, we define the epilimnion as the
upper layer with ,18C difference per meter. A change
of .18C per meter was defined as the thermocline and
the hypolimnion is the layer from the thermocline to the
bottom. When the water-column was isothermal, a 3-m
integrated depth was sampled.
Data processing
Two water-column stability estimates were calculated
for each sampling date in 2005 and 2006, the Schmidt
stability index (S) and the density gradient between the
epilimnion and the hypolimnion. This was estimated to
test the possibility that changes in water-column stability
were related to the observed dynamics in cyanobacteria
biomass. S (g cm21) describes the amount of work
required to mix the entire water column to a uniform
density (Robertson and Imberger, 1994).
S ¼ A1
o
X
ðz zÞðrz r ÞAz Dz
r ¼ V1
X
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ðVz rz Þ
where Az is the lake area (m2) and rz is the density
(g cm23), both at depth z (m). z* represents the depth
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where the mean density is found, and r* is that density.
V represents volume (m3). One-meter depth intervals
(Dz) were used for the calculations. The second
measure of water-column stability was determined by
calculating the difference in mean density between the
epilimnion and the hypolimnion. This was calculated to
determine the possibility of mixing between the layers.
Water density values were based on theoretical relationships between water temperature (8C) and density of
water (g mL21).
A measure of cumulative daily temperatures, degreedays (DD, 8C day) was estimated for each day during
the open-water season (May – August) above a given
threshold temperature (TTh) (Neuheimer and Taggart,
2007). Within an appropriate physiological range,
ectotherm growth and development are temperaturedependent. Therefore, degree-days can be used to relate
temperature to organism developmental time.
Degree-days are calculated using the formula:
DDðnÞ ¼
X
ðTi TTh Þ†Dd; Ti TTh
Relevant threshold temperature (TTh) is given as 48C,
found during isothermal conditions following ice-off. Ti
is the mean daily temperature and Dd is a day.
Average daily epilimnetic water temperatures were
estimated based on linear interpolations of local air
temperatures on measured water temperatures for each
lake. A dynamic linear model was used to estimate
daily epilimnetic temperatures (Kjellman et al., 2003):
WTt ¼ a þ WTt1 þ b ðATt1 WTt1 Þ
Daily water temperatures (WTt) were estimated based
on air temperatures (ATt) recorded at time t from a nearby
Environment Canada weather station (Richardson
International Airport, 498 55.2000 N, 978 13.8000 W). The
minimum sum of squares between measured and estimated water temperature were used to estimate parameters a and b. Linear regressions were performed
relating predicted values to observed values to determine
the suitability of the model in estimating daily epilimnetic
temperatures. As a result, the dynamic model gave reasonably good estimates of daily epilimnetic temperatures
(linear regressions: Lake 2, observed ¼ (22.532 1027)
+1.000(predicted), F1,43 ¼ 55.757, P , 0.001, r 2 ¼ 0.565;
Lake 3, observed=(22.162 1027) + 1.000(predicted),
F1,43 ¼ 38.523, P , 0.001, r 2 ¼ 0.571; Lake 4,
observed ¼ (22.057 1028) + 1.000(predicted), F1,43 ¼
77.949, P , 0.001, r 2 ¼ 0.644).
Zooplankton were identified to species using taxonomic keys developed for Daphnia (Hebert, 1995) and
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for other cladocerans and copepods (Pennak, 1989).
Rotifers were counted only as a group; however, dominant species were identified (Chengalath et al., 1971).
For zooplankton, a minimum of 100 animals per subsample were counted. Phytoplankton were classified by
cell size based on longest linear dimensions.
Filamentous cyanobacteria were identified to genus
(Findlay and Kling, 1979). Phytoplankton cell counts
were made using the Utermöhl inverted-microscope
technique. For phytoplankton, a single subsample was
counted. Biovolumes were estimated by approximating
cell dimensions to nearest geometrical shapes (Rott,
1981).
Data analysis
Statistical analyses are separated into two parts: (i)
assessment of possible factors driving a shift towards
cyanobacteria dominance, and (ii) the effects of temperature on plankton abundance and composition. In
the first part, univariate paired t-tests were used to test
whether monthly means (May – August) of water
column stabilities, nutrient concentration (both TDN
and TDP) and TDN:TDP ratios differed between 2005
and 2006. Dissolved forms of N and P were selected for
analysis because they were assumed to be more readily
available for assimilation over the short-term (within a
month) in comparison to suspended forms.
The second part of the analysis investigated the
relationships between water temperature and plankton
abundance and composition using the metric, degreedays (DD, 8C day). Degree-day was related to phytoplankton biovolume estimates, to relative cyanobacteria
biovolume estimates and to daphniid abundance. These
relationships were examined by dividing the field season
into monthly intervals (May, June, July and August).
Lake-years were used as independent data points for
the analysis (3 lakes 2 years ¼ 6 data points). Mean
monthly values of biological parameters were regressed
by monthly degree-day values. In addition, simple
linear regressions were used to investigate effects of
water temperature on daphniid abundance by relating a
measure of food quality, % cyanobacteria, to daphniid
abundance. Unfortunately, the absence of planktivorous
fish data prevented us from investigating possible
relationships with zooplankton abundances. Normality
and homogeneity of residuals were verified using a
Shapiro – Wilk’s test for normality and visual checks of
residuals by predicted values plots for homogeneity.
Chlorophyll a and total phytoplankton biovolume were
log-transformed to normalize and homogenize
residuals. All statistical tests were performed in SAS
9.1.2.
R E S U LT S
Phytoplankton and zooplankton dynamics
Phytoplankton abundance and species composition
changed markedly between 2005 and 2006. Both
measures of phytoplankton biomass, chlorophyll a (mg
L21) and biovolume estimates (mm3 L21), indicate large
increases in 2006. In the present study, only biovolume
estimates were analysed in further detail as log(chl a)
and log(biovolume) estimates were strongly correlated
(Pearson: Lake 2, n ¼ 15, r ¼ 0.700, P ¼ 0.004; Lake 3,
n ¼ 8, r ¼ 0.809, P ¼ 0.015; Lake 4, n ¼ 15, r ¼ 0.693,
P ¼ 0.004). Across Lakes 2, 3 and 4, May– August
mean phytoplankton biovolume estimates ranged from
1.7 to 3.1 mm3 L21 in 2005 compared with 4.3 to
7.3 mm3 L21 in 2006 (Fig. 2). As a result, water transparency measured by Secchi disc declined substantially
from 2.9– 2.2 m to 0.6– 0.3 m between 2005 and 2006
(Fig. 2). Total phytoplankton biomass was negatively
correlated with Secchi depth (Pearson: Lake 2, n ¼ 22,
r ¼ 20.622, P ¼ 0.002; Lake 3, n ¼ 19, r ¼ 20.482,
P ¼ 0.037; Lake 4, n ¼ 15, r ¼ 20.770, P , 0.001).
Relative biomass of filamentous cyanobacteria increased
substantially from maximum open-water values of 28.2,
46.7 and 90.9% in 2005, increasing to 77.7, 90.1, 95.0%
in 2006, for Lakes 2, 3 and 4, respectively (Fig. 2). In
addition, phytoplankton succession progressed earlier in
2006. By mid-May in 2006, cyanobacteria already represented 11–15% of the total phytoplankton biomass. In
comparison, in 2005, cyanobacteria accounted for only
0.2–3% of the mid-May phytoplankton biomass (Fig. 2).
Dominant cyanobacteria taxa shifted from Aphanizomenon
spp. in 2005 to Anabaena spp. and Planktothrix spp. in 2006,
particularly from June to August (Fig. 3). Between 2005
and 2006, the relative importance of other phytoplankton
(omitting filamentous cyanobacteria) based on our size
classification did not change significantly (paired t-tests,
P . 0.2).
Major changes were observed in zooplankton communities between years. Across Lakes 2, 3 and 4, mean
May – August daphniid abundance decreased from
10.6 – 20.3 ind. L21 in 2005 to 0.5– 7.3 ind. L21 in
2006 (Fig. 4A – F). In 2005, Daphnia pulicaria and D.
ambigua dominated while D. parvula were observed nearly
exclusively in 2006. Mean May – August rotifer
(.73 mm in size) abundance increased to very high
values in all lakes ranging from 62.3 to 474.8 ind. L21
in 2005 compared with 3693.0 to 4112.5 ind. L21 in
2006 (Fig. 4). Populations that also increased between
2005 and 2006 are the calanoid copepod Skistodiaptomus
oregonensis (7.9 – 12.7 to 15.5– 41.7 ind. L21) and the
small cladoceran Bosmina longirostris (0 – 1.2 to 6.5– 21.0
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Fig. 2. Two-year (2005 and 2006) comparison of phytoplankton biovolume estimates (mm3 L21) and water transparency indicated in Secchi
depth (vertical bars, m) from May to August in Lakes 2, 3 and 4. Phytoplankton are classified by cell size except for filamentous cyanobacteria.
ind. L21) (Fig. 4). Cyclopoid copepods, dominated by
Diacyclops thomasi showed inconsistent changes between
years with a spring peak in 2005 but not in 2006 except
for Lake 4 (data not shown). Also, zooplankton predators, instars III and IV of Chaoborus flavicans, peaked in
summer except for Lake 2 in 2006. A single winter
sample taken February 15 in 2006, along with sampling
conducted continuously from 1977 to 1978 (Loadman,
1980), suggested that no cladocerans over-winter as
adults during the ice-covered conditions (data not
shown).
Relationships between water temperature
and phytoplankton
Response of plankton abundance and composition to
changes in water temperature, observed from 2005 to
2006, was investigated using simple linear regression
models with degree-days as an explanatory variable.
Significant relationships were found between water
temperature and total phytoplankton biomass during
May and June, prior to cyanobacteria dominance
(Fig. 5A and B). Degree-days (8C day) explained 72 and
88% of the variability in total biovolume for the months
of May and June (Fig. 5A and B). July water temperatures were also significantly related to total phytoplankton biomass; however, this was primarily driven by
increasing prevalence of cyanobacteria.
Warmer water temperatures in 2006, indicated by
degree-days, were associated with greater relative cyanobacteria biomass in all lakes compared to 2005 (Fig. 5C
and D). Relative cyanobacteria biomass increased
quickly with degree-days, increasing by 36 and 26% in
July and August, respectively, for each 100 degree-days
(Fig. 5C and D). Degree-day explains 96 and 75% of
the variation in % cyanobacteria in July and August.
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Fig. 3. Two-year (2005 and 2006) comparison of relative abundances of dominant filamentous cyanobacteria genus, i.e. representing .95% of
total biomass, (Aphanizomenon spp., Planktothrix spp., Anabaena spp. and Limnothrix sp.) from biovolume estimates from May to August in
Lakes 2, 3 and 4. A star indicates no filamentous cyanobacteria in sample.
Alternative factors regulating cyanobacteria
Univariate paired t-tests were conducted to test for
difference in nutrient concentrations and water-column
stability between 2005 and 2006. Mean monthly nutrient concentrations were not significantly different
between years in the Fort Whyte lakes (Fig. 6D– I and
Table II). Thus, from 2005 to 2006, no important
influx of nutrients occurred that was common to all
three lakes at the same time. Several authors have
associated low N to P ratios with cyanobacteria dominance (Schindler, 1977; Smith, 1983). Between years,
only July and August showed significant differences in
TDN:TDP (Fig. 6J – L and Table II). Similarly, high
water-column stability can potentially favour dominance
of buoyancy-controlling cyanobacteria (Reynolds and
Walsby, 1975). Schmidt stability index (S, g cm21) did
not significantly vary between 2005 and 2006 (Fig. 6A–
C and Table II). We also calculated the density gradient
between the epilimnion and the hypolimnion in both
years. In July and August, the density gradient was significantly greater in 2006 compared to 2005 (Table II).
Relationships between water temperature
and daphniids
Monthly linear regressions between degree-days and
daphniid abundance were not significant (P . 0.05).
However, negative relationships between relative cyanobacteria biomass and daphniid abundance were significant for June and July (Fig. 7). In 2006, lower daphniid
abundance was associated with higher filamentous cyanobacteria biomass compared to 2005. Percent
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Fig. 4. Two-year (2005 and 2006) comparison of mean Daphnia spp. (ind. L21), Skistodiaptomus oregonensis (ind. L21), Bosmina longirostris (ind. L21)
and rotifer (103 ind. L21) population dynamics from May to August in Lakes 2, 3 and 4. Note the y-axis break for Lake 2 zooplankton
(A and B).
cyanobacteria explained most of the variation in
daphniid abundance in both June (r 2 ¼ 0.66) and July
(r 2 ¼ 0.71).
DISCUSSION
In the Fort Whyte lakes, changes in phytoplankton and
zooplankton population dynamics could have resulted
from a number of possible direct and indirect effects.
Some of the proposed factors explaining large increases
in cyanobacteria could be related to increased water
temperatures (Robarts and Zohary, 1987), grazing of
small phytoplankton species by herbivorous zooplankton (Lampert et al., 1986), increased nutrient concentrations (Downing et al., 2001), decreased nitrogen to
phosphorus ratios (Schindler, 1977; Smith, 1983) and
disruption of water-column stability (Reynolds and
Walsby, 1975). In addition, possible factors influencing a
decline in Daphnia and an increase in S. oregonensis,
B. longirostris and rotifers also include increased water
temperature, degrading food quality (e.g. increasing
prevalence of cyanobacteria), changes in planktivory
pressures and changes in vertical distribution. Although
many other mechanisms are possible and complex
interactions are likely, we focus our presentation on parameters that were measured using basic limnological
sampling methods (e.g. thermal profiles, Secchi transparency, zooplankton and phytoplankton abundance).
A full analysis of factors explaining patterns in planktonic succession and their relative importance has been
more thoroughly discussed in Sommer et al. (Sommer
et al., 1986) and Sommer (Sommer, 1989). In this study,
it remains impossible to isolate any given factor;
however, we believe there is enough evidence to discuss
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Fig. 5. Monthly relationships between degree-days (8C day) and phytoplankton biomass estimated as biovolume (mm3 m23) for May (A) and
June (B). (C) and (D) describe the monthly relationships between degree-days (8C day) and % filamentous cyanobacteria for July (C) and August
(D). In all figures, the dashed lines represent the 95% confidence interval.
the potential influence of some of the factors that were
monitored in this study.
Water temperature and phytoplankton
Water temperature is an important factor regulating
phytoplankton physiological rates (Rhee and Gotham,
1981). In 2006, a warm spring and summer in the Fort
Whyte lakes was correlated with increased total phytoplankton and relative cyanobacteria biomass. This is
consistent with long-term (.30 years) patterns observed
in several North American and European lakes where a
warming climate has been linked to earlier phytoplankton blooms (Weyhenmeyer et al., 1999; Gerten and
Adrian, 2000; Winder and Schindler, 2004), increased
total biomass (Schindler et al., 1990) and, in eutrophic
lakes, dominance of cyanobacteria (Adrian and Deneke,
1996). In nutrient-rich systems, empirical and experimental results suggest that increasing water temperatures are directly linked to changes in phytoplankton
species composition, showing an increasing proportion
of cyanobacteria taxa (Zhang and Prepas, 1996; De
Senerpont Domis et al., 2007). In fact, in some years,
warming temperatures have led to year-round cyanobacteria dominance (Adrian and Deneke, 1996).
In the Fort Whyte lakes, higher temperatures in
June – August were also associated with shifts in the
dominant cyanobacteria taxa, from Aphanizomenon in
2005 to Anabaena and Planktothrix in 2006. This may be
attributed to differences in competitive abilities among
species under different environmental conditions. We
suggest that direct effects of increased temperature did
not drive a taxonomic shift as A. flos-aquae growth rates
are greater than those of P. agardhii and P. redekei over a
range of temperatures (6 – 158C) without light limitation
(Gibson, 1985). Instead, decreased water transparency
associated with greater phytoplankton biomass and
elevated water temperatures in 2006 may have facilitated dominance of Planktothrix over Aphanizomenon.
Under conditions of lowered light intensities, several
laboratory experiments suggested greater photosynthetic
efficiency and growth rates in P. agardhii relative to
A. flos-aquae (Foy et al., 1976; Foy and Gibson, 1982)
resulting in superiority of the former in low-light
environments. Importantly, these shifts in cyanobacteria
species could have negative implications especially when
replacement taxa produce toxins and/or are of poorer
nutritional quality for zooplankton.
Alternative factors driving cyanobacteria
dominance
In the literature, increased nutrient loading and lowered
N:P ratios are often identified as the most important
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Fig. 6. Two-year comparison (2005 and 2006) of physical and chemical dynamics from May to August in Lakes 2, 3 and 4.
reason for increased cyanobacteria biomass (Downing
et al., 2001; Schindler et al., 2008). Between 2005 and
2006, we found no evidence that nitrogen or phosphorus concentrations differed and only in late summer
did we find significant difference in TDN:TDP ratios.
In this study, we do not believe that cyanobacteria
dynamics were related to TDN:TDP ratios as we
observed higher ratios in 2006 occurring after the
major changes in the phytoplankton community.
Another factor influencing the prevalence of cyanobacteria is water-column stability. Gas-vacuolation produced by some cyanobacteria could allow a competitive
advantage over other non-buoyant phytoplankton
under conditions of low mixing intensity (Reynolds and
Walsby, 1975; Visser et al., 1996). Overall water column
stabilities in the Fort Whyte lakes, measured by the
Schmidt stability index, did not change significantly
between years. In contrast, when comparing density
differences between epilimnetic and hypolimnetic water
volumes, density gradients were significantly greater in
July and August of 2006 compared to 2005. This may
suggest a partial explanation for greater cyanobacteria
biomass in 2006; however, important increases in cyanobacteria prevalence began prior to July in 2006 and
we did not observe changes in gas vacuolation in cyanobacteria between years.
An alternative explanation to consider is the potential
for zooplankton to control cyanobacteria biomass. In
the Fort Whyte lakes, it is also possible that grazing
pressures from large herbivorous zooplankton (i.e.
Daphnia) was stronger in 2005 leading to lower overall
biomass of total phytoplankton and cyanobacteria
biomass. This would then suggest that high cyanobacteria biomass in 2006 was an effect rather than a cause
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A. P. DUPUIS AND B. J. HANN
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WARM TEMPERATURES AND PLANKTON DYNAMICS
of low Daphnia abundance. Some experiments have
shown that even cyanobacterial filaments can be grazed
by large Daphnia (Epp, 1996).
Water temperature and shifts
in zooplankton community
Warmer water temperatures in the Fort Whyte lakes in
2006 did not lead to paralleled increase between
Table II: Results of univariate paired t-test
testing for differences between 2005 and
2006 monthly means for chemistry parameters
(TDN, TDP and TDN:TDP) and water
column stability estimates (Schmidt stability
index and density gradient between epilimnion
and hypolimnion), n ¼ 3
Month
Variable
T
P
May
TDN
TDP
TDN:TDP
Schmidt index
Epi.-Hypo. density
TDN
TDP
TDN:TDP
Schmidt index
Epi.-Hypo. density
TDN
TDP
TDN:TDP
Schmidt index
Epi.-Hypo. density
TDN
TDP
TDN:TDP
Schmidt index
Epi.-Hypo. density
2.25
0.90
20.12
20.23
22.45
2.09
4.06
20.70
22.87
23.39
20.34
1.84
212.70
0.12
25.80
1.08
2.25
212.13
20.37
26.02
0.15
0.46
0.92
0.84
0.13
0.17
0.056
0.56
0.10
0.08
0.77
0.21
0.006
0.92
0.03
0.39
0.15
0.007
0.74
0.03
June
July
August
gradient
gradient
gradient
gradient
Significant results (P , 0.05) are indicated in bold.
phytoplankton biomass and daphniid abundance.
Relationships between water temperature and daphniid
abundance were not significant. This is contrary to
some studies linking climate warming to changes in
plankton seasonal dynamics and abundance. In
European lakes, warming temperatures coincident with
the North Atlantic oscillation (NAO) were associated
with an earlier peak of both phytoplankton and Daphnia
(Straile, 2002). In some cases, higher water temperatures
were also linked to higher daphniid biomass (Straile,
2000).
Long-term studies of climate-related impacts on
plankton show a trend towards smaller zooplankton
species. In Heiligensee, Germany, a warming temperature trend was associated with a shift from D. galeata to
the smaller D. cucullata (Adrian and Deneke, 1996).
Similarly, in the Fort Whyte lakes, increased water
temperatures in 2006 were associated with small-bodied
D. parvula (adult size 1.0 mm) compared to high abundances of large-bodied D. pulicaria (adult size 2.2 mm)
and small-bodied D. ambigua (adult size 1.0 mm) in
2005. Concurrently in the Fort Whyte lakes, other small
zooplankton such as rotifers (albeit, species ,73 mm
are probably underestimated) and B. longirostris increased
to high densities in 2006. There have been several
examples of highly eutrophic lakes associated with small
size spectra in zooplankton community structure
(Gliwicz, 1977; Finlay et al., 2007). Our study further
suggests that warming temperatures could promote
shifts in zooplankton size spectra in moderately
eutrophic lakes such as the Fort Whyte lakes. This supports the arguments that climate change effects will
probably resemble symptoms of eutrophication in
shallow lakes (Mooij et al., 2005).
While increasing water temperatures may enhance
bottom-up and top-down factors in affecting the zooplankton community, we are unable to provide direct
Fig. 7. Monthly relationships between % filamentous cyanobacteria and daphniid abundance (ind. L21) for June (A) and July (B) with the 95%
confidence interval (dashed lines).
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support for either mechanism. In the Fort Whyte lakes,
daphniid food quality in 2006, expressed as % filamentous cyanobacteria, deteriorated with increasing temperatures and was negatively related to daphniid
abundance for the months of June and July. In accordance with this relationship, several authors have
suggested that the presence of filamentous cyanobacteria is generally associated with smaller species of
daphniid, i.e. ,1 mm body length (DeMott et al., 2001;
Ghadouani et al., 2003). Laboratory experiments have
shown that larger-sized daphniids are more negatively
affected by the presence of cyanobacterial filaments
than smaller-sized ones causing interference with
feeding appendages, high rejection rates, lowered filtering rates and decreased reproduction (Gliwicz, 1977;
Fulton and Paerl, 1987; Gliwicz, 1990). Furthermore,
recent studies have shown that changes in water viscosity, as a result of changing water temperature, can
negatively affect daphniid feeding efficiency (Abrusán,
2004; Bednarska and Dawidowicz, 2007). For D. pulicaria, decreasing water viscosity with increasing water
temperatures may allow greater water flow through
intersetular gaps of feeding appendages and thus,
increase the potential for clogging in the presence of
filaments (Abrusán, 2004).
Our study, however, does not rule out the alternative
that increasing water temperatures resulted in increased
planktivory. In spring, warming water temperatures are
directly related to larval fish growth to sizes capable of
feeding on large cladocerans and increasing predation
rate of adult planktivorous fish (Mehner, 2000; Hansson
et al., 2007). Also, feeding behaviour measured by attack
rate and swimming speed is positively related to water
temperature in some zooplanktivorous fishes (e.g. juvenile brook trout, Salvelinus fontinalis; Marchand et al.,
2002). Such studies suggest that warming water temperatures can increase the magnitude of and advance the
onset of planktivory by fish resulting in more intense
size-selective predation (Brooks and Dodson, 1965) and
declines in the abundance of large herbivorous zooplankton. These studies raise the possibility that warmer
conditions in the Fort Whyte lakes in 2006 resulted in
positive changes in zooplanktivory and caused a
restrained response in the spring development of a
population of large zooplankton grazers. Fish populations were not monitored during our study; therefore,
we cannot make clear conclusions about the impact of
planktivory.
Invertebrate planktivory can also impart important
top-down pressures on the zooplankton community. In
Bautzen Reservoir, Germany, Wagner and Benndorf
(Wagner and Benndorf, 2007) demonstrated that
warmer spring temperatures were related to an earlier
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onset of both young-of-the-year percid and Leptodora
kindtii predation on D. galeata. In another study, fishless
enclosures with Chaoborus resulted in decreased abundance of small-sized (Bosmina and rotifers) and mediumsized (Ceriodaphnia) zooplankton species (Lynch, 1979).
In contrast, Lynch (Lynch, 1979) showed that the presence of planktivorous fishes was associated with a
decreased abundance of the midge larvae. In Fort
Whyte lakes, a qualitative measure of Chaoborus flavicans
(daytime sampling and relatively small diameter net) did
not show changes in density of predatory instars III and
IV between 2005 and 2006 (data not shown). However,
without more data, we cannot exclude the alternative
explanation that changes in Chaoborus abundance were
related to inter-annual changes in zooplankton abundance and species composition. Further studies on the
potential impacts of climate change on plankton
dynamics will be needed to isolate the relative impacts
of bottom-up and top-down factors in the regulation of
zooplankton population and community composition.
It is also possible that the changes in zooplankton
community structure observed between years are related
to altered vertical migration behaviour. In zooplankton,
diel vertical migration has been shown to be related to
fish planktivory and light transparency (Lampert, 1993),
factors that could potentially be affected by warming
temperatures (De Stasio et al., 1996). In our study, zooplankton were only sampled within the epilimnion. As a
result, there is a possibility that some zooplankton were
not sampled if daytime habitat was deeper in 2006
compared to 2005. However, we believe that the
changes between years are so strong that they are unlikely to be an artefact of the sampling procedures. In
other words, we believe the patterns are valid, but that
the true whole water-column abundance of zooplankton
may have been underestimated in both years.
In summary, the present study suggests that a warmer
spring and summer could potentially trigger some
important changes in plankton population dynamics in
small eutrophic lakes. In the Fort Whyte lakes, warming
temperatures were related to substantial increases in
total phytoplankton biomass and relative importance of
filamentous cyanobacteria. As a result, water transparency decreased substantially and was related to shifts in
cyanobacteria species better adapted to low light conditions. Warmer spring and summer conditions were
also associated with strong responses in the zooplankton
community showing declines in daphniids and increases
in small-bodied zooplankton and a dominant calanoid
copepod. Taken together, our study suggests that
warming temperatures can have important implications
for phytoplankton– zooplankton interactions in small
eutrophic lakes.
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AC K N OW L E D G E M E N T S
Downing, J. A., Watson, S. B. and McCauley, E. (2001) Predicting cyanobacteria dominance in lakes. Can. J. Fish. Aquat. Sci., 58, 1905–1908.
We thank Michael Paterson and Mark Abrahams for
constructive comments and encouragement throughout
this study; Hedy Kling for providing guidance in phytoplankton taxonomy; Lynn Frazer for assistance with
zooplankton collection and identification and Fort
Whyte Alive for use of study site.
Downing, J. A., Prairie, Y. T., Cole, J. J. et al. (2006) The global abundance and size distribution of lakes, ponds, and impoundments.
Limnol. Oceanogr., 51, 2388– 2397.
Edwards, M. and Richardson, A. J. (2004) Impact of climate change
on marine pelagic phenology and trophic mismatch. Nature, 430,
881 –884.
Environment Canada. (2004) Canadian Climate Normals 1971–2000
for Winnipeg Richardson International Airport, Manitoba, Canada.
Environment Canada, National Climate Archive. Data Archives:
http://climate.weatheroffice.ec.gc.ca.
FUNDING
Financial support for this research was provided in part
by: National Sciences and Engineering Research
Council of Canada (NSERC) PGS M (A.P.D.),
University of Manitoba Graduate Fellowship (A.P.D.),
Fish Futures, Inc. (A.P.D.) and NSERC Discovery Grant
(B.J.H.).
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