Climate Change Impacts on Zooplankton Species Richness in the

Experimental Lakes Area, Canada

Saket Agrawal
Kelley Robbins-Thompson
Vanessa Waller
Received: December 1, 2016
Introduction
Over the past several decades,
limnologists have studied the effect of climate
change on the Boreal Shield Lakes of the
Experimental Lakes Area (ELA) in Ontario,
Canada. With mean annual temperatures
expected to increase 2 to 3 degrees C over the
next 50 years, scientists are interested in how
such changes may affect ecological conditions
(Arnott et al. 2003). In general, lakes are
considered effective sentinels for climate
change because they are sensitive to climate,
respond rapidly to change, and integrate
information about changes in the catchment
(Adrian et al. 2009).
Specifically, limnologists are interested
in phytoplankton and zooplankton as indicators
of how lakes respond to a changing climate. For
instance, Rusak et al. (2002) have noted that
"zooplankton are increasingly being used as
ecological indicators and to set recovery targets
for lake ecosystem restoration. Climate change
indicators have been shown to affect species
richness and abundance, respectively, for both
phytoplankton (Findlay et al. 2001) and
zooplankton (Rusak et al. 2002) in boreal lakes.
Findlay et al. (2001) found that phytoplankton
species richness increased in response to climate
change signals, but studies on changes in
zooplankton richness in response to climate are
difficult to find (M. Paterson, pers. comm.
2016). Rusak et al. (2002) studied zooplankton
in boreal lakes, but focused on zooplankton

abundance rather than species richness. Our

study combined elements of the methodology of
Findlay et al. and Rusak et al., by analyzing how
and to what extent zooplankton species richness
changes in response to climate signals. To
address the question of spatial and temporal
coherence among similar lakes, we examined
similarities among climate change indicators
across two lakes, and we included time as a
factor in our model for zooplankton richness.
Similar studies of biological indicators
have included elements of coherence analysis.
Coherence analysis is a term used in the
literature to describe either temporal
coherence or spatial coherence. Temporal
coherence is defined as the tendency for lakes to
behave similarly around the same time (Rusak
et al. 2002). In other words, temporal coherence
means that lakes change in similar ways with
respect to time, even if lakes are located in
different areas. Spatial coherence refers to the
tendency of lakes in similar areas to behave in
similar ways (Rusak et al. 2002). One of our
goals was to do a basic analysis of temporal and
spatial coherence for two lakes. Our lakes are
located in close proximity to one another (see
Appendix map); therefore, our study seeks to
assess whether temporal or spatial differences
can be detected at a finer scale.
Our null hypotheses were that 1) there
would be no difference in mean annual climate
change indicators between L373 and L442, and
2) there would be no significant effects of any
climate change indicators, or time, on
zooplankton richness for either lake. Our
alternative hypotheses were that 1) there would
be significant differences, in terms of climate
indicators, between lakes, and 2) climate change
variables and/or time variables would be
significant predictors of zooplankton richness
changes over the period of interest.

Methods

zooplankton: crustacea. We chose crustacea

because we considered rotifers to be less
important within the context of our study due to
their small body size (M. Paterson, pers. comm.
2016).

Study Area and Biological Measurements: Our

lakes are located in the Experimental Lakes
Area (ELA) in Ontario, Canada. We studied two
lakes: Lake 373 (L373) and Lake 442 (L442),
both of which are close enough spatially (see
Appendix map) to represent an interesting
spatial coherence analysis. According to ELA,
each lake is similar in terms of depth,
stratification, and trophic system, and both lakes
are free from artificial manipulation; both are
considered reference lakes, in contrast to
many lake sites at ELA that undergo
experimental manipulations.
We obtained zooplankton data from
ELA for each lake, and each lake's data was
obtained using the same methodology,
according to ELA (M. Paterson, pers. comm.
2016). For simplicity, we focused our analysis
on data recorded from the epilimnion of the two
lakes; the only caveat is that zooplankton
richness data were recorded using vertical haul
nets, as zooplankton migrate vertically through
the water column (M. Paterson, pers. comm.
2016). Nevertheless, epilimnion-level changes
are likely to affect zooplankton community
dynamics as a whole.
We chose epilimnion depth, water
clarity, and dissolved organic carbon (DOC) as
climate signal variables because of their use as
climate indicators in the literature. Epilimnion
depth is the depth of the topmost strata of water,
and an increase in epilimnion depth is
considered an indication of climatic warming
(Adrian et al. 2009). Increases in DOC are also
associated with climatic warming, and are
related to multiple lake ecosystem properties,
such as water transparency and lake metabolism
(Adrian et al. 2009). Water clarity, measured
using a secchi disk, is also related to climate
effects, and we expected clarity to be negatively
correlated to DOC (see Courture et al. 2015, M.
Paterson, pers. comm. 2016).
To simplify our analysis, we studied
species richness for a certain type of

Data Preparation: All data manipulation and

analysis was completed using the open-source
software program R (R Core Team 2016). To
get comparable data across lakes and across
time periods, we used R to aggregate data by
day, month, and year. Although many years of
data were available for each lake, lack of
consistency among datasets meant that some
years were omitted from the dataset for the
purpose of comparison. Our dataset includes the
years 1989-2012, with some years omitted due
to lack of data for the years 1990 and 1993. We
obtained decimal values for species richness
through the aggregation process, so we rounded
our richness counts to the nearest whole number
for the purposes of using our data in Poisson
regression.
Statistical Tests: To test our hypotheses, we
used three statistical methods: Spearman
correlation to test the relationships among the
three climate variables; two-sample z-tests to
compare aggregated climate variable means
with respect to lake; and a Poisson regression to
assess the effects of climate change variables
(epilimnion depth, DOC, and water clarity) and
time variables (month, year, and seasonality) on
species richness for each lake.
To better understand how our predictor
variables were related, we began with Spearman
correlation analyses to assess whether predictor
variables (epilimnion depth, water clarity, and
DOC) were significantly correlated to each
other. Pearson correlation would have been
more desirable because it avoids the problem of
ranking (with ranking, equal values can be
confused), but because some explanatory
variables were not normal, even after
transformations, we decided to use the
Spearman method.

To test our first hypothesis, which deals

with the similarity between the two lakes, we
used two-sample z-tests to compare L373
aggregated mean predictor values to aggregated
mean predictor values for L442 (see Fig. 1). We
used z-tests rather than t-tests because although
not all three predictors were perfectly normally
distributed, transformations did not greatly
improve our distributions, and the large number
of observations per lake (about 100) was
considered adequate to account for the slight
departure from normality. Furthermore, t-tests
produced similar results to the z-tests.
To test our second hypothesis,
concerning the effect of climate change on
zooplankton, we used a Poisson regression
model. We chose Poisson regression because
our response variable (richness) is characterized
by count data (number of species observed), and
these counts were relatively small. We
developed a generalized linear model (GLM) of
the Poisson family to measure the effects of
each climate change indicator (epilimnion
depth, water clarity, and DOC), time
(seasonality), and lake number on zooplankton
species richness.
To select appropriate Poisson regression
models, we tested a variety of model iterations
using Akaikes Information Criterion (AIC).
Based on this test, along with a general
assessment of each models characteristics, we
selected the following models for comparison
(R=richness, S=water clarity measured by
secchi disk, E=epilimnion depth):

second model (in bold), as it had the lowest AIC

and at least one significant result. Diagnostics
for our chosen model did not indicate any
problems with residual clustering, lack of
normality, or outliers. Our model was slightly
underdispersed (dispersion ratio=0.3), but
because data was not overdispersed we decided
a quasipoisson was unnecessary. To account for
underdispersal, we experimented with a
generalized Poisson model (using the VGAM
package in R), but results were difficult to
interpret; therefore, we decided to use a GLM
from the Poisson family.
Results
Our Spearman correlation results show that
epilimnion depth and water clarity were
significantly negatively correlated, but only for
L373; all other correlations were not statistically
significant:
Lake 373
Epilimnion and clarity = 0.21 (pvalue=0.0234)
DOC and clarity = 0.0102 (p-value=0.9144)
DOC and epilimnion = 0.0324 (pvalue=0.734)
Lake 442

R~ S+E+DOC+factor(Lake)+factor(Season)

Epilimnion and clarity correlation = 0.127

(p-value=0.2109)

R~ S+DOC+factor(Lake)+factor(Season)

DOC and clarity = 0.1176 (p-value=0.2485)

R~ S+factor(Lake)+factor(Season)

DOC and epilimnion = 0.1883 (pvalue=0.0633).

R~S+factor(Lake)
Our two-sample z-tests show that the lakes are
significantly different from one another in terms
of all three climate variables: L373 has a deeper
mean epilimnion than L442 (Z=4.302, p-

The above models had similar AIC values

(first=887.5; second=886.09; third=886.4;
fourth=886.1), but we decided to choose the

value<0.001); L373 has lower DOC than L442

(Z= 31.09, p-value<0.001); and L373 has
greater water transparency than L442 (Z=11.37,
p-value<0.001).

Our Poisson model results show that water

clarity is the only variable that has a statistically
significant effect on species richness (pvalue=0.011, statistically significant at =
0.05). In our model, Lake 373 was our baseline
lake, and summer (Season 0) was our baseline
season. Season 0 represented summer (months
5-8), and Season 1 represented fall (months 911):

Fig 1: Comparisons of Climate Response by

Lake

Richness = 2.03 + 0.08*S + 0.09*DOC + 0.07*factor(Season1) + 0.09*factor(Lake 442)

We standardized our climate indicator
variables before developing our model so that
clarity (mean=5.1499 m, SD = 1.155 m) and
DOC (mean=450.3087 micromoles/L, SD =
117.95 micromoles/L) were in units of clarity
standard deviations and DOC standard
deviations, respectively. The model generated
the following results (note that only clarity was
a significant factor in our model):
(1) All else held equal, a one standard
deviation increase in clarity increases richness
by 0.0878 exponentiated; in other words,
richness is multiplied by 1.09, increasing by 9%
(Fig. 2).
(2) All else held equal, a one standard
deviation increase in DOC increases richness by
0.09 exponentiated; in other words, richness is
multiplied by 1.09, increasing by 9% (Fig. 2).
(3) All else held equal, a season shift
from summer (Season 0) to fall (Season 1)
decreases richness by 0.07 exponentiated; in
other words, richness is multiplied by 0.93,
decreasing by 7% (Fig. 2).
(4) All else held equal, if lake is changed
to 442 from 373, richness increases by 0.09
exponentiated; in other words, richness is
multiplied by 1.09, increasing by 9% (Fig. 2).

Fig. 2: Effect of Climate Signals and Time on Species Richness

Discussion and Limitations

Our z-test results suggest that we should
reject our first null hypothesis and accept the
alternative: that L373 differs from L442 with
respect to climate change response. Our Poisson
regression results suggest that we should reject
our second null hypothesis and accept the
alternative: that climate signals and/or time
variables will have a significant impact on
zooplankton richness. However, in the case of
our second hypothesis, it is important to note
that only one of our predictor variables was
significant.
Our lake comparison z-test results
suggest that L373 and L442 had different
responses to climate variables, despite being
located in the same region. This result would
appear to contradict the general assumption
expressed in Arnott et al. (2003), that lakes
within a region will experience similar
fluctuations in climate and therefore,
limnological variables strongly influenced by
climate will be expected to vary in a similar way
through time. However, Arnott et al. (2003)
also conclude that lake response can vary even
within a region, and our results confirm this
finding. It is likely that the observed difference
between our lakes is related to microclimate
effects. Although L373 and L442 are similar in
size, they have subtle morphological differences
that may contribute to the observed variation in
climate response.
Additionally, lakes have complex
internal feedback mechanisms that can
confound climate change effects (Adrian et al.
2009), which may help to explain the observed
difference. Further, lakes respond differently to
different climate signals: Weyhenmeyer (2008)
showed that lakes of different sizes may have
similar responses to climate signals acting via
the water surface, but lakes of different sizes
may respond differently to climate signals that
act via the watershed, such as mineral nutrient
concentrations. Our results suggest that climate
response in a single lake may not necessarily be

representative of climate response for an entire

region, so our results should not be extrapolated
to the entire ELA. Our results suggest that we
should use caution when extrapolating our
results to other lakes.
Our Poisson regression shows that in
general, zooplankton richness does not respond
strongly to climate signals. Only water clarity
represented a significant predictor of richness.
Given the non-significant (p-value=0.9144)
weak correlation ( = -0.0102) between clarity
and DOC for L373, it is not surprising that
clarity was significant while DOC was not; the
variables are not closely linked, either in terms
of correlation or within the context of the
Poisson regression.
Our model output, showing that
increases in water clarity tend to predict
increases in richness, is hard to interpret in the
context of the literature. Multi-decadal studies
of climate change impacts on boreal and
temperate lakes indicate that zooplankton
responses to climate warming are variable
across species. However, there is a notable trend
of zooplankton experiencing peak abundances
earlier and earlier in the spring season as
temperatures increase (Gerten and Adrian
2002). Early peaking can have significant
impacts on the trophic structure. Gerten and
Adrian (2002) assert, "it is important to
recognise that climate changes are likely to
generate complex, and possibly time-lagged,
direct and indirect responses in the entire food
web, and these responses are often nonlinear."
Limitations: In terms of data analysis, our
models have three major weaknesses. First, our
aggregation process meant that some data was
lost: our dataset of 300+ observations per lake
was reduced to a total of about 100 observations
per lake, once missing values were accounted
for. Our raw data was not entirely complete, as
some years (e.g. the year 1993) had no data for
one or more variables. Second, our data was
underdispersed; future research should examine
the data using a generalized Poisson model,

perhaps using the R package VGAM (see

discussion in Methods). Finally, we assumed =
0.05 would reflect anticipated effect size, but we
were unable to find evidence in the literature of
what would constitute an appropriate effect size
for this type of data.
Other limitations relate to the scale of
our study design. Most studies of climate
change effects on lake ecosystems study species
composition, and how different species move
through thermal layers as water changes. For
example, DeStasio et al. (1996) examined how
climate affected the percentage of daphnia, a
particular type of zooplankton, in terms of its
migration patterns through lake strata. Because
lake ecosystems are characterized by complex
trophic structures, climate altering zooplankton
predation (Jeppesen et al. 2009) and movement
through the water column (DeStasio et al.
1996), zooplankton may be best studied through
more complex experimental designs. Future
research should examine zooplankton ecology
not just in terms of one measure of species
richness (i.e. crustacean richness), but also in
terms of species composition; for example, does
one species increase more than others in
response to climate change?
Future research should also consider
alternate methods of assessing temporal
coherence. Rusak et al. (2002) assessed the ratio
of year-to-year zooplankton variance to total
zooplankton variance based on an ANOVA
model. They used this ratio to judge the
synchronicity of lake response with respect to
time. Future studies could incorporate this type
of coherence analysis, especially if a similar
ANOVA model were used.

Katherine Hurrell, Cooper Rosin, Matt Fuller,

and Bryan Brown.
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Acknowledgements: The authors wish to

acknowledge the scientists at ELA for providing
data and allowing us to learn from their
research. We would like to thank Mike Paterson
from ELA for his helpful guidance on our
project. We also wish to thank our statistics
professor Justin Kirkpatrick for his help with
statistical analysis technique, and our class TAs,

Jeppesen E, Kronvang B, Meerhoff M,

Sondergaard M, Hansen K, Andersen H,
Lauridsen T, Liboriussen L, Beklioglu
M, Ozen A, et al. 2009. Climate change

effects on runoff, catchment phosphorus

loading and lake ecological state, and
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38:19301941.
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environment for statistical computing.
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Rusak J, Yan ND, Somers K, Cottingham K,
Micheli F, Carpenter S, Frost T,
Paterson M, McQueen D. 2002.
Temporal, spatial, and taxanomic
patterns of curstacean zooplankton
variability in unmanipulated northtermperate lakes. Limnol. Oceanogr.
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small lakes? Hydrobiologia 599:105
110.

10

Appendix
Map: Lake Locations in ELA
Map of the Experimental Lakes Area (full map available at
https://www.iisd.org/ela/visitors/maps/). Each orthogonal square on the map represents one
square kilometer. Both L373 and L442 are shown in this section of the map, and both are located
on the left side of the roadway (solid red line).

11

Fig. A-1: Trends in Climate Signals with Time

The following graphs show general trends across time and seasons for our climate predictor
variables. Epi stands for epilimnion depth; Secchi stands for water clarity; Doc stands
for dissolved organic carbon (DOC). All values are standardized by the standard deviation of
each respective data type (see Methods).

12

13