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136
Can. J. Fish. Aquat. Sci. 57(Suppl. 2): 136–145 (2000) © 2000 NRC Canada
Pelagic and benthic algal responses in eastern
Canadian Boreal Shield lakes following harvesting
and wildfires
Dolors Planas, Mélanie Desrosiers, S-Raphaëlle Groulx, Serge Paquet, and
Richard Carignan
Abstract: Pelagic and benthic algal biomass and pelagic algal community structure were measured in Boreal Shield
lakes impacted by forest harvesting and wildfires (Haute-Mauricie, Québec). Sixteen reference lakes in which the wa
-
tershed has been unperturbed for at least 40 years, seven harvested lake watersheds (logged in 1995), and nine lake
watersheds burnt in 1995 were sampled for 3 years following harvesting or wildfires. From 1996 to 1998, repeated-
measures ANOVA showed significant effects between treatment and sampling years for pelagic chlorophyll a (Chl a)
and biomass, but for 1997–1998 benthic Chl a, repeated-measures ANOVA showed only significant treatment effects.
Chl a concentrations increased 1.4- to 3-fold in perturbed lakes as compared with reference lakes. Areal pelagic Chl a
(milligrams per square metre) was lower than estimated littoral Chl a in perturbed lakes. The pelagic algal community
was dominated by mixotrophic nanoflagellates in reference lakes. Watershed perturbation induced differential changes
in pelagic algal communities: mixotrophic nanoflagellates increased in harvested lakes and photoautotrophic diatoms in
burnt lakes. Considering only perturbed lakes, algal biomass was proportional to the fraction of the catchment area per
-
turbed divided by the surface area of lakes in the catchment.
Résumé : La biomasse des algues pélagiques et benthiques ainsi que la structure de la communauté pélagique ont été
mesurées dans 32 lacs de la forêt boréale (Haute-Mauricie, Québec) : seize lacs de référence non perturbés depuis au
moins 40 ans, sept lacs ont été perturbés par des coupes forestières (1995) et neuf lacs dont les bassins versants ont
subi des feux de forêt (1995). Pour la chlorophylle a (Chl a) et la biomasse pélagique (1996–1998), l’ANOVA en me-
sures répétées montre un effet significatif du traitement et de l’année alors que seul le traitement est significatif pour la
Chl a benthique (1997–1998). La concentration du Chl a augmente de 1,4 à 3 fois dans les lacs perturbés par rapport
aux lacs de référence. Dans les lacs perturbés, la Chl a pélagique par unité de surface (milligrammes par mètre carré)
est plus faible que la Chl a benthique. La communauté pélagique est dominée par les nanoflagellés mixotrophes dans
les lacs de référence. Cependant, les perturbations du bassin versant induisent des changements différentiels dans la
communauté d’algues pélagiques : les nanoflagellés mixotrophes augmentent dans les lacs de coupes alors que ce sont les
diatomées phototrophes qui augmentent lors d’un feu. Lorsque l’on considère uniquement les lacs perturbés, la biomasse
des algues est proportionnelle à la fraction du bassin versant perturbé divisée par la surface des lacs dans ce bassin.
Planas et al. 145
Introduction
Aquatic ecosystems and wetlands occupy almost a third of
the boreal ecoregion. More than 600 000 lakes larger than
4 ha are found in the Canadian Shield boreal region, south
of 52°N latitude and east of the Manitoba–Ontario border
(Minns et al. 1992). Timber harvesting in the Canadian bo
-
real forest has increased in the last two decades and con
-
cerns have been raised over its potential impact on aquatic
ecosystems. In the province of Québec, approximately 1%
of the boreal forest is harvested annually (Ministère Res
-
sources Naturelles Québec 1996).
The disturbances expected after logging are an increase in
the watershed export of suspended solids, base cations, nu
-
trients, and dissolved organic C (DOC) (e.g., Nicolson et al.
1982; Rask et al. 1998). In the boreal forest, similar distur
-
bances in watershed exports occur naturally, mainly follow
-
ing wildfires, which also increase flow, silt loads, and
chemical concentrations in waters (Bayley et al. 1992). As a
consequence of these perturbations, nutrients may increase
and light penetration may decrease, thereby modifying the
water quality and productivity of impacted watersheds (e. g.,
Wright 1976; Carignan et al. 2000).
Studies on the effects of forestry practices are more com
-
mon on running waters than on lakes (e.g., see Holopainen
Received September 2, 1999. Accepted April 28, 2000.
J15344
D. Planas,
1
M. Desrosiers, S-R. Groulx, and S. Paquet.
Groupe de Recherche Interuniversitaire en Limnologie
(GRIL), Département de Sciences Biologiques, Université du
Québec à Montréal, C.P. 8888, Succursale Centre-Ville,
Montréal, QC H3C 3P8, Canada.
R. Carignan. GRIL, Département de Sciences Biologiques,
Université de Montréal, C.P. 6128, Succursale Centre-Ville,
Montréal, QC H3C 3J7, Canada.
1
Author to whom all correspondence should be addressed.
e-mail: planas.dolores@uqam.ca
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and Huttunen 1992). The few previous studies on the conse
-
quences of forest harvesting on lakes have only considered
the response of pelagic organisms (Rask et al. 1998). How
-
ever, benthic algal communities can be responsible for a sig
-
nificant fraction of the primary production in lakes, either in
shallow systems or in deep oligotrophic lakes, and their im
-
portance in whole-lake metabolism is often neglected (Loeb
et al. 1983; Wetzel 1996). Furthermore, the littoral zone is
the main feeding area of many freshwater fish species.
The objectives of this study were to analyse changes in
biomass and community structure of phytoplankton in boreal
eastern Canadian Shield lakes disturbed by fire and harvest
-
ing and to compare the responses of pelagic and littoral al
-
gae with these disturbances.
Material and methods
The study area (-50 000 km
2
) is centered on Gouin Reservoir
(47°52
¢
–48°59
¢
N, 73°19
¢
–76°43
¢
W) (Fig. 1) at the transition zone
between the boreal mixed and the boreal conifer forest (see
Carignan et al. 2000). Thirty-two thermally stratified lakes were
selected on the basis of several criteria (Carignan et al. 2000). Ini
-
tially, the experimental design consisted of 16 lakes located within
unperturbed watersheds, defined as a watershed untouched by fire
or anthropogenic influences for a minimum of 40 years and, in
general, for more than 70 years (reference lakes, N in Fig. 1). Of
the harvested lakes, seven had approximately 9–73% of their wa-
tershed logged in 1995 (C in Fig. 1) and one was harvested twice,
once in 1995, and once in 1997 (C9 in Fig. 1). Nine lakes had 50–
100% of their watershed area severely burnt in 1995 (burnt lakes,
FP and FBP in Fig. 1).
Sampling
Phytoplankton were sampled three times per year, in spring
(within 2 weeks of ice-out), summer, and fall, from 1996 to 1998.
Duplicate integrated samples from the euphotic zone (depth of 1%
light penetration, between 2 and 5 m) were taken near the deepest
part of the lake. Benthic algae were sampled using artificial sub
-
strates (70-
mm
Teflon
®
mesh; D. Planas et al., unpublished data) in
reference lakes (four for the summers of 1997 and 1998 and six for
winter), burnt lakes (five in 1997 and 1998), and cut lakes (four for
the summers of 1997 and 1998 and six for winter). We used artifi
-
cial substrates to minimize the heterogeneity of communities and
to facilitate comparisons between systems. Benthic biomass as
chlorophyll a (Chl a) was measured at two to four stations per lake
on quadruplicate substrates placed at a depth of 1 m and left in the
field for 3 months during the summers of 1997 and 1998 (summer
benthic algae) and during 9 months from September 1998 to May
1999 (winter benthic algae).
Phytoplankton and benthic algal biomass measurements
Water samples for pelagic algae were transported to the labora
-
tory on ice and Chl a was concentrated within 12 h by filtering a
known amount of water (750–1000 mL) on Whatman GF/C filters.
The filters were immediately frozen and kept at –40°C until extrac
-
tion. Phytoplankton Chl a was extracted using hot 90% ethanol and
absorbance was measured spectrophotometrically, before and after
acidification (Sartory and Grobbelaar 1984). For measurements of
benthic algal Chl a, the Teflon
®
substrates were transported to the
laboratory on ice and kept frozen at –40°C until analysis. Chl a
was extracted directly from artificial substrates by immersing them
in hot 95% ethanol for 5 min.
A portion of the pelagic sample was preserved with acid Lugol
solution for taxonomic analyses. Algae were identified, measured,
and counted with an inverted interferential microscope. Phyto
-
plankton counts were converted to wet weight biomass (biomass)
using average species dimensions (mean of 40 cells) and corre
-
sponding geometric shapes and assuming a specific density of 1
(Lewis 1976). Species were assigned to one of three fractions ac
-
cording to the longest cell dimension: picoplankton, <2
mm
; nano
-
plankton, 2–20
mm
; microplankton, >20
mm
.
Data analyses
In order to compare the relative importance of pelagic and ben
-
thic algae, phytoplankton biomass per unit volume was trans
-
formed to unit area of photic zone as phytoplankton biomass
(milligrams per cubic metre) × photic zone depth (metres). The
benthic to pelagic biomass ratio was estimated as average benthic
biomass per lake (milligrams per square metre) × littoral area
(square metres)/average phytoplankton biomass per lake (milli
-
grams per square metre) × area of the pelagic euphotic zone
(square metres). The littoral area was defined as the surface area of
bottom sediments receiving more than 1% of the light extinction
coefficient (
e
PAR
). For benthic algae, we assumed that the biomass
at 1 m corresponded to maximum biomass, since the substrates
were at a fixed depth in all lakes. This coarse approach probably
underestimated benthic algal Chl a, since typical epilithic algal
profiles in oligotrophic Shield lakes show maximum Chl a concen
-
trations below the 10% surface incident light depth (D. Planas et
al., unpublished data), and artificial substrates after a 3-month col
-
onization period have, in general, lower algal biomass than natural
substrates (D. Planas et al., unpublished data). We could not ex
-
clude the possibility that our calculations overestimated benthic al-
gal biomass, since factors other than depth and irradiance also
regulate littoral algal biomass in lakes.
Statistical analyses were performed on log
10
-transformed data
when necessary using SAS 6.14 and JMP 3.2.5 statistical packages
(SAS institute Inc., Cary, N.C.). For pelagic Chl a and biomass and
for summer benthic Chl a, univariate repeated-measures ANOVA
(RMA) were applied to examine changes in Chl a and biomass
measurements over time (1996, 1997, and 1998 for pelagic algae
and 1997 and 1998 for benthic algae) for each treatment (refer-
ence, burnt, and harvested). One-way ANOVA was performed on
wintering benthic Chl a (1998–1999). When an effect was signifi
-
cant, a Dunnett one-tailed t test was applied to compare reference
and treated lakes. Differences among treatments and among years
were tested using Tukey’s honestly significant difference test for
multiple comparisons. The t tests were used for benthic data (two
years sampled) and for pelagic and benthic comparisons.
Multiple regressions were performed with a stepwise variable
selection (p < 0.05 as an entering and keeping level) using Mal
-
low’s Cp as a model selection criterion, and colinearity between
variables was accounted for by using a variance inflation factor.
Normality of the predicted–observed residuals was verified with a
Shapiro-Wilk W test. Correlations between phytoplankton taxon
and physical and chemical variables were calculated using the
Pearson product-moment pairwise method. Finally, we used
ANCOVA (covariance on intercept and heterogeneity of slopes for
regression coefficients) to test if the regression relationships be
-
tween Chl a and total P (TP) (data from Carignan et al. 2000) and
the ratio of Chl a to TP and
e
PAR
(data from Carignan et al. 2000)
were different among groups of perturbed lakes.
Results
Response of pelagic algal biomass
RMA on pelagic Chl a and biomass concentrations
showed significant effects between treatments (burnt and
harvested lakes with more than 10% catchment perturbed)
and years (within treatments). The interaction term was sig
-
nificant for Chl a, indicating that temporal changes are de
-
© 2000 NRC Canada
Planas et al. 137
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© 2000 NRC Canada
138 Can. J. Fish. Aquat. Sci. Vol. 57(Suppl. 2), 2000
Fig. 1. Location of the 32 study lakes in the Haute-Mauricie (Québec). N, reference lakes; FP and FBP, burnt lakes; C, harvested lakes (cut in 1995). The circles mark the
lakes in which benthic algae were sampled.
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pendent on lake watershed treatment (Table 1). Over the 3-
year period, perturbed lakes had higher mean Chl a and bio
-
mass than reference lakes (p < 0.05, Dunnett’s test) (Figs. 2
and 3). Regardless of treatment, 1996 had higher Chl a and
biomass than 1998 (p < 0.05, Tukey’s test) and values in
1997 were intermediate (p > 0.05) between 1996 and 1998.
A comparison within years found higher Chl a and biomass
in perturbed lakes as compared with reference lakes in 1996
(p < 0.05), and these differences persisted only in burnt
lakes for 1997 and 1998. Burnt lakes had higher Chl a in
1997 than in 1998 (p < 0.05, Tukey’s test).
A highly significant relationship (r
2
= 0.69, p < 0.0001)
was found between pelagic algal Chl a and biomass when
data for all years and treatments were combined. However,
when regressions were performed by treatment, the strongest
relationship was found in burnt lakes (r
2
= 0.66, p < 0.0001)
and the weakest in harvested lakes (r
2
= 0.40, p < 0.002).
The relationship was also weak in reference lakes (r
2
= 0.42,
p < 0.0001) (Fig. 4). ANCOVA indicated nonsignificant dif
-
ferences between slopes (p > 0.05) and intercepts (p > 0.05)
among treatments.
Phytoplankton communities were dominated by the
nanoplankton fraction, which represented between 76 and
91% of the total biomass. Nanoplankton increased in burnt
and harvested lakes 1 year after perturbation and, in compar
-
ison with reference and harvested lakes, remained high 2
and 3 years after perturbation in burnt lakes (p < 0.05). In
harvested and reference lakes, nanoplankton biomass tended
to decrease from 1996 to 1997 (p < 0.05). Picoplankton bio
-
mass represented between 3 and 13% of the total biomass
© 2000 NRC Canada
Planas et al. 139
Type III SS df Fp> F
Phytoplankton Chl a
Treatments 0.48 2 13.33 0.0001
Years 0.07 2 11.01 0.0001
Treatments × years 0.06 4 4.77 0.0022
Wet weight biomass
Treatments 2.36 2 17.08 0.0001
Years 0.33 2 10.9 0.0001
Treatments × years 0.11 4 1.83 0.1384
Summer benthic Chl a
Treatments 0.72 2 6.25 0.0174
Years 0.04 1 0.04 0.1119
Treatments × years 0.02 2 0.02 0.5636
Winter benthic Chl a
Treatments 2.44 112 18.36 <0.0001
Table 1. Results of univariate RMA for phytoplankton Chl a
(mg·m
–3
), wet weight biomass (mg·m
–3
), and summer benthic
Chl a (mg·m
–2
, 3-month colonization) and one-way ANOVA for
winter benthic Chl a (mg·m
–2
, 9-month colonization).
Fig. 2. Average summer means ± SE of pelagic algal Chl a for
reference (open bars, n = 16), harvested (grey bars, n = 7), and
burnt lakes (black bars, n = 9). Different letters indicate mean
differences (p < 0.05, ANOVA) within sets of lakes.
Fig. 3. Annual average total biomass of pelagic algae taxa. R,
reference lakes (n = 16); H, harvested lakes (n = 7); B, burnt
lakes (n = 9).
Fig. 4. Regression plot between pelagic algal Chl a concentra
-
tions and pelagic algal biomass (wet weight) for reference lakes
(circles), harvested lakes (diamonds), and burnt lakes (squares)
(log(Chl a) = –0.745±0.085 + 0.389±0.027log(biomass); r
2
=
0.69, p < 0.0001, n = 96). The dotted line, dashed line, and
solid line indicate the linear fit for reference, harvested, and
burnt lakes, respectively.
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and was higher in reference than in harvested and burnt
lakes (p < 0.05). In reference lakes, picoplankton increased
between 1996 and 1998 (p < 0.05). Microplankton biomass
represented between 8 and 18% of the total biomass increase
in harvested lakes in 1997 and was higher than in reference
and burnt lakes (p < 0.05).
The dominant communities in the nanoplankton fractions
were Chrysophyceae and Cryptophyta taxa. This association
is characteristic of oligotrophic boreal lakes (Kling and
Holgrem 1972; Willén et al. 1990). Cyanobacteria communi-
ties, the most important taxa within the picoplankton frac
-
tion, were dominated by small chroococcales, which were
abundant in terms of numbers but of minor importance when
converted to biomass. Cyanobacteria species found in our
study are typical of temperate, nutrient-poor, dark waters
and are abundant in eastern Canadian Shield lakes in the
middle of summer, often associated with small green chloro
-
coccales (D. Planas et al., unpublished data). Harvesting
barely changed the phytoplankton community composition
in lakes; some taxa increased, such as Chrysophyceae,
Cryptophyceae, and dinoflagellates, or decreased, as was the
case for cyanobacteria. More drastic changes in community
composition were measured in burnt lakes 1 year after per
-
turbation; diatoms became the dominant taxa and Crypto
-
phyceae also increased in these perturbed lakes (Fig. 3).
Response of benthic algal biomass
In the littoral zone, algal communities also had higher Chl
a in perturbed lakes compared with reference lakes. RMA on
benthic summer Chl a showed only significant treatment ef
-
fects (Table 1). Among perturbed lakes, burnt lakes had the
highest concentrations of Chl a (p = 0.0025) (Fig. 5). For
both years, Chl a concentrations were threefold higher in
burnt lakes than in reference lakes, and in 1997, burnt lakes
had twofold higher Chl a concentrations than harvested
lakes (data not shown). A one-way ANOVA on wintering
benthic algae also showed differences among treatments
(p < 0.0001) (Table 1). Mean wintering algal Chl a concen
-
trations in lakes impacted by harvesting (23.30 mg·m
–2
) and
wildfire (29.06 mg·m
–2
) were higher than in reference lakes
(14.57 mg·m
–2
), but the difference between harvested and
burnt lakes was not significant (p < 0.05, Tukey’s test) (Ta
-
ble 1). In 1998, mean Chl a concentrations in the littoral
zone were higher in winter than in summer, for any treat
-
ment (reference, p = 0.0008; harvested, p = 0.0001; burnt,
p = 0.0014; t test).
Biomass budget
In the subset of 16 lakes for which littoral algae were
sampled, the comparison of littoral versus pelagic algal bio
-
mass (Chl a) per unit area of photic zone was estimated
from the average summer biomass of 1997 and 1998 com
-
bined. When both communities were compared, differences
were only found in perturbed lakes in which littoral Chl a
was higher than pelagic Chl a (Fig. 5). The means of the ra
-
tios of benthic to pelagic algal biomass were 1.31 in refer
-
ence lakes, 2.56 in harvested lakes, and 2.74 in burnt lakes
(Fig. 5).
Physical and chemical variables influencing algal Chl a
Pelagic algal Chl a could be predicted by TP, which ex-
plained 48% of the partial variance, followed by
e
PAR
and
dissolved inorganic N (DIN = NO
3
+NO
2
+NH
4
) (data
from Carignan et al. 2000), which explained 6 and 4% of the
variance, respectively (Table 2). The same variables entered
into the biomass regression model, but the predictive power
in this model was slightly weaker for TP, but not for
e
PAR
and DIN, than contribute slightly more to the total variance
(Table 2). The relationship between TP and Chl a in per-
turbed lakes is shown in Fig. 6A, and for the same set of
lakes, the relationship between the ratio of Chl a to TP and
e
PAR
is shown in Fig. 6B.
Catchment characteristics as well as the area of cut or
burnt watershed that predicted the physical and chemical
water changes in our lakes (Carignan et al. 1999), also pre
-
dicted changes in pelagic biomass (Fig. 7). For phyto
-
plankton biomass, the fraction of the watershed perturbed
over the sum of lake surface areas in the watershed ex
-
plained 57% of the variance in Chl a.
TP was the best predictor of benthic algal Chl a concen
-
trations in summer, explaining 34% of the variance, fol
-
lowed by NO
3
and DOC, which accounted for 17 and 11%
of the variance, respectively (Table 2). TP as well as DOC
also showed a relationship with winter benthic algal Chl a,
but total N (TN) explained a stronger percentage of the vari
-
ance (Table 2).
Variables influencing algal taxon composition
In general, correlations between phytoplankton taxon
composition and environmental variables were significant,
although correlation coefficients were low. Cryptophyta and
Bacillariophyceae (diatoms) showed weak positive correla
-
tions with TP (r
2
= 0.29, p = 0.0038 and r
2
= 0.34, p =
0.0007, respectively). Bacillariophyta was also correlated
with DIN (r
2
= 0.5070, p < 0.0001) and Cryptophyta with
e
PAR
(r
2
= 0.3998, p = 0.0001). Chrysophyceae, cyano
-
bacteria, and Chlorophyceae showed weakly negative rela
-
© 2000 NRC Canada
140 Can. J. Fish. Aquat. Sci. Vol. 57(Suppl. 2), 2000
Fig. 5. Average summer means ± SE of benthic algal (solid bars)
and pelagic algal (open bars) Chl a concentrations per unit area
in reference and perturbed lakes. Different letters indicate mean
differences (p < 0.05; t test) within sets of lakes.
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tionships with nutrients, including both TP (r
2
= –0.20, p =
0.0472, r
2
= –0.42, p < 0.0001, and r
2
= –0.22, p = 0.0289,
respectively) and DIN (r
2
= –0.39, p = 0.0001, r
2
= –0.21,
p = 0.0417, and r
2
= –0.22, p = 0.0344, respectively). The
negative correlations of these taxa with water column nutri-
ents suggests that they were not directly controlled by nutri-
ents.
Discussion
Algal responses to watershed perturbations
Phytoplankton biomass (Chl a and biomass) as well as the
dominant taxa in the reference lakes of our study region
were characteristic of pristine oligotrophic Canadian Shield
lakes (Armstrong and Schindler 1971; Kling and Holgrem
1972). Within perturbed watersheds, and particularly in
burnt lakes, volumetric biomass increased to mesotrophic
levels (Chl a > 3 mg·m
–3
, biomass > 3000 mg wet weight·
m
–3
) with maximum Chl a concentrations greater than
5 mg·m
–3
. Moreover, increases in taxa such as diatoms,
which are more characteristic of boreal enriched environ
-
ments (Eloranta 1986), only occurred in burnt lakes. Benthic
algal biomass responses to watershed perturbations followed
the same pattern as for phytoplankton; the response was,
however, magnified relative to the pelagic community, par
-
ticularly in burnt lakes. In burnt lakes, benthic algal Chl a as
high as 100 mg·m
–2
was measured 2 years after perturbation,
while in references lakes, the highest Chl a measured was
approximately 30 mg·m
–2
. Other studies have also reported
considerable increases in benthic algal biomass following
boreal forest disturbance ranging from 21- to 46-fold in
rivers and from two to fourfold in lakes compared with ref
-
erence systems (Holopainen and Huttunen 1992; Rask et al.
1998). In our study, benthic algal Chl a in the perturbed
lakes was only two to three times higher than in the refer
-
ence lakes and is thus comparable with boreal lake
responses (Rask et al. 1998).
Even 3 years after perturbations, algal communities in the
lakes may not have reached a steady state. Long-term re-
sponses to disturbances have been reported in aquatic eco-
systems following watershed perturbations, such as wildfires
(Wright 1976; Minshall et al. 1997). During our 3-year
study, the greatest response was measured in the second year
following disturbances, and the sign of the response was dif-
ferent in relation to the type of disturbance. Biomass in
-
creased and major taxa shifts were observed in burnt lakes,
whereas biomass decreased in harvested lakes. These inter
-
annual differential changes in algal biomass and (or) species
composition in lakes with perturbed watersheds could be ex
-
plained by variability in chemical fluxes and light penetra
-
tion. Higher runoff was measured in 1997 compared with
1996 and 1998 in the region of the Gouin Reservoir
(Lamontagne et al. 2000). Nutrient loading was equivalent in
both types of perturbations for 1996 and 1998, and it was
50% higher than in reference lakes. The increase in P load
-
ing in 1997 was 25% higher in burnt lakes than in harvested
lakes (S. Lamontagne, GRIL, Université de Montréal, C.P.
6128, Montreal, QC H3C 3J7, Canada, personal communica
-
tion). However, the large difference in chemical loading be
-
tween harvested and burnt lakes was a result of the large
increase in DOC (50–80%) in harvested watersheds, which
was not observed in burnt watersheds (S. Lamontagne,
GRIL, Université de Montréal, C.P. 6128, Montreal, QC
H3C 3J7, Canada, personal communication). Higher DOC
concentrations in harvested lakes strongly influenced light
penetration in our study lakes (Carignan et al. 2000). Thus,
low light transmission could explain, for any year, the small
response of algal biomass in harvested lakes as compared
with burnt lakes, and this in spite of similar nutrient load
-
ings. Moreover, light differences between treatments could
© 2000 NRC Canada
Planas et al. 141
(a)log
10
(Chl a) = –0.168±0.061 + 0.700±0.090log(TP) – 0.322±0.113log(
e
PAR
) + 0.074±0.022log(DIN)
r
2
partial
0.48 0.06 0.04
SSE=0.75 r
2
adjusted
= 0.565 F = 42.1 p < 0.0001 n =96
(b)log
10
(biomass a) = 1.951±0.139 + 1.270±0.204log(TP) – 0.925±0.255log(
e
PAR
) + 0.220±0.053log(DIN)
r
2
partial
0.31 0.10 0.07
SSE=2.85 r
2
adjusted
= 0.489 F = 31.3 p < 0.0001 n =96
(c) log
10
(Chl a) = –0.414±0.320 + 0.650±0.320log(TP) + 0.169±0.068log(NO
3
) + 0.847±0.517log(DOC)
r
2
partial
0.34 0.17 0.11
SSE=0.62 r
2
adjusted
= 0.568 F = 11.9 p < 0.0001 n =26
(d)log
10
(Chl a) = –0.109±0.288 + 1.320±0.275log(TP)
SSE=0.16 r
2
= 0.622 p = 0.0003 n =16
(e) log
10
(Chl a) = –3.414±0.856 + 1.931±0.353log(TN)
SSE=0.15 r
2
= 0.681 p < 0.0001 n =16
(f)log
10
(Chl a) = 0.095±0.225 + 1.407±0.303log(DOC)
SSE=0.16 r
2
= 0.606 p = 0.0004 n =16
Note: Physical and chemical data from Carignan et al. (2000). p = p > F; biomass is wet weight;
e
PAR
is the available
radiation light extinction coefficient.
Table 2. Multiple or simple regression models of yearly averages of algal biomass and physical and chemical
variables of lakes (independent variables): (a) phytoplankton Chl a,(b) phytoplankton wet weight biomass,
(c) summer benthic algal Chl a, and (d–f) winter benthic algal Chl a.
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explain the lack of difference in pelagic algal Chl a per unit
area between treatments. Low light, when nutrients are
available, could limit algal primary production and hence
biomass (Petersen et al. 1997). For a similar increase in nu
-
trients in perturbed lakes, differences in
e
PAR
could also ex
-
plain differences in the algal taxa responses, which are
discussed below.
Relationship between algal responses and physical and
chemical lake characteristics
TP was the best predictor of pelagic algal biomass in the
study lakes. For a given P concentration, lakes in burnt wa
-
tersheds produced more Chl a per unit TP than harvested
lakes. It is well known that P limits phytoplankton produc
-
tion in boreal Canadian Shield lakes (Schindler 1974) and,
as mentioned before, watershed perturbation in our study in
-
creased TP export by twofold as compared with references
lakes (Lamontagne et al. 2000). Nitrogen also seemed to
have had some control on pelagic algal biomass responses. It
is known that N plus P additions yielded the greatest bio
-
mass response as compared with additions of one or the
other alone (Axler et al. 1994). Thus, in our burnt lakes, in-
creases in P and N loading increased algal biomass per unit
volume. Harvesting increased TP concentration but not inor-
ganic N concentrations (Carignan et al. 2000), and thus,
lower N could explain the lower algal biomass in harvested
lakes as compared with burnt lakes. However, lower light
penetration could also explain the lower Chl a concentra-
tions per unit biomass in harvested lakes in relation to burnt
lakes.
The fact than N showed stronger relationships with ben-
thic rather than pelagic algal Chl a could be explained by the
differences in nutrient availability in the littoral as compared
with the pelagic zones. Phosphorus release from littoral
epilimnetic sediments could support benthic algal growth,
while pelagic algae rely on P dissolved in the water column
(Carlton and Wetzel 1988). While the export of N increased
in both harvested and burnt watersheds, N was primarily ex
-
ported as NO
3
in burnt lakes and probably as dissolved or
-
ganic N in harvested lakes (Lamontagne et al. 2000). Higher
NO
3
fluxes into the lakes could thereby help to explain the
higher algal benthic biomass in burnt lakes. The positive re
-
lationship between DOC and benthic algae biomass seen in
our study suggests that DOC could enhance littoral algal
growth, as was observed in an experimental study by Vine
-
brooke and Leavitt (1998). In our lakes, DOC regulates un
-
derwater spectral irradiance, but we do not know if it also
influences lake chemistry. DOC can complex metals and en
-
zymes that regulate P availability (Boavida and Wetzel
1998) or, conversely, can act as a source of labile organic
substrates, such as P and dissolved inorganic C (Moran and
Zepp 1997). DOC is also a vector for nutrients such as N
and P (Lamontagne et al. 2000). Although in our study, we
did not determine the proportion of nutrients that enter the
lake in the dissolved organic form, it is possible that in bo
-
real catchments, it is the more important form of nutrients
(Lamontagne et al. 2000). In our multiple regressions, P ex
-
© 2000 NRC Canada
142 Can. J. Fish. Aquat. Sci. Vol. 57(Suppl. 2), 2000
Fig. 6. (A) Relationship between 3-year average pelagic algal Chl a
in perturbed lakes (harvested (diamonds) and burnt (squares)) and TP
(log(Chl a) = –0.407±0.233 + 0.789±0.224log(TP); r
2
= 0.47, F =
12.38, p > F = 0.0034, n = 16). (B) Relationship between the Chl a/
TP ratio in perturbed lakes and
e
PAR
(Chl a/TP = 0.135±0.014 –
0.107±0.036log(
e
PAR
); r
2
= 0.38, F = 8.60, p > F = 0.0109, n = 16).
Fig. 7. Relationship (solid line) and 95% confidence intervals
(dotted lines) between phytoplankton Chl a in perturbed lakes
(harvested (diamonds) and burnt (squares)) and the fraction of
the watershed perturbed over the sum of lake surface areas in the
watershed (FA) (log(Chl a) = 0.412±0.036 + 0.024±0.006FA;
r
2
= 0.570, F = 18.53, p > F = 0.0007, n = 16).
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plained a greater percentage of benthic algal biomass in
summer as compared with winter. The wintering algae were
exposed to spring runoff, which contributes a high percent
-
age of the annual runoff in our lakes, as, in general, in tem
-
perate regions (Likens 1985). Thus, in spring, when UV
radiation is higher than in late summer, photolysis of DOC
could reactivate the alkaline phosphatase binding with
humic substances, thereby promoting P availability for litto
-
ral algae (Boavida and Wetzel 1998).
It has been observed that catchment variables can explain
the variability of Chl a almost as well as that of TP (Duarte
and Kalff 1989). In our study lakes, some of the easily mea
-
sured catchment characteristics, such as the area of cut or
burnt watershed, predict the physical and chemical changes
in our lakes (Carignan et al. 1999) as well as changes in pe
-
lagic biomass. The highest Chl a concentrations occurred in
burnt lakes (p = 0.001, t test), particularly in the FP region
where the 1995 wildfire hit more severely the lake’s shore
-
line. This relationship allowed for the prediction of either
lake water quality or the response of primary producers and
could be a useful tool for managers.
Changes in pelagic algal community associated with
environmental variables
Moderate enrichments, such as those observed in the per-
turbed lakes, may also explain increases or changes in algal
community taxa (Eloranta 1986; Willén et al. 1990). Diatom
increases in burnt lakes could be expected as a result of P
and, to a lesser extent, N augmentations in these lakes
(Jansson et al. 1996; Watson et al. 1997). Cryptophyta and
Chrysophyceae also increased in perturbed lakes, but these
increases cannot be explained by nutrients with which the
biomass of these two taxa were weakly or negatively corre-
lated. Weak correlations of these taxa or curvilinear re-
sponses with TP increases have been reported and attributed
to morphological diversity, differential herbivory, and mix
-
ing regime (Watson et al. 1997). In our study, the relatively
strong correlation of nutrients with diatoms and the weak or
absent relationship of nutrients with Cryptophyta and
Chrysophyceae cannot be explained by differential grazing
or mixing. Thus, in all taxa, the species present in our lakes
were edible, and no strong relationship was found between
phytoplankton and herbivorous zooplankton (Patoine et al.
2000), and the thermal characteristics of these lakes did not
differ (Carignan et al. 2000).
Dominance of Cryptophyta and Chrysophyceae, repre
-
senting almost 90% of the biomass, has been found in boreal
brown-water lakes (Kling and Holgrem 1972; Willén et al.
1990), and Cryptophyceae increases have been measured in
brooks of harvested watersheds (Holopainen and Huttunen
1992; Lepistö and Saura 1998). In our study, the negative re
-
lationship between nutrients and Chrysophyceae and light
penetration and Cryptophyta suggests that the species pres
-
ent in our lakes are capable of obtaining their energy via
means other than photoautotrophy, e.g., phagotrophy, hetero
-
trophy, or photoheterotrophy (Pick and Caron 1987). In Ca
-
nadian Shield lakes, stronger phagotrophic particle uptake
has been demonstrated in some Chrysophyceae species, and
phagocytosis was the dominant path for energy flow when
photosynthesis was light limited (Bird and Kalff 1987).
Mixotrophy has also been reported in Cryptophyta (Tranvik
et al. 1989). Thus, the different responses of taxa observed
in our study in relation to the type of perturbation, namely
the increase in photoautotrophic algae in burnt lakes but not
in harvested lakes, may be associated with differences in
light penetration.
Biomass budget
The littoral versus pelagic biomass (Chl a) per unit of sur
-
face area indicated a stronger response of littoral communi
-
ties to pertubations. Since no other studies investigating the
impact of watershed disturbance on lakes have simulta
-
neously measured the response of pelagic and benthic algae,
no comparisons with the literature were possible. However,
it is known that in humic oligotrophic lakes, phytoplankton
and benthic algae compete for nutrients (Hansson 1990).
Nutrient loading in the littoral zone is less diluted than in the
pelagic water column, and the efficiency of nutrient utiliza
-
tion, retention, and recycling is much greater among closely
aggregated benthic algal–microbial communities than in the
pelagic zone (Wetzel 1996). These littoral characteristics
lead to maximal resource utilization and productivity per ar
-
eal unit. In nine perturbed lakes, in which benthic algal bio
-
mass was measured, nutrients in the water column were
relatively abundant compared with unperturbed lakes, sug-
gesting that competition for nutrients between littoral and
pelagic zones was weaker in relation to reference lakes.
However, due to differences in the concentration of DOC,
the amount of light reaching the substrates differed between
treatments (Carignan et al. 2000), with 25% of surface
irradiance (
e
PAR
) in reference lakes, 14% in harvested lakes,
and 10% in burnt lakes. Low light penetration in perturbed
lakes could increase the Chl a content of cells (Ahlgren
1970), but mean Chl a per algal cell in phytoplankton was
equal in reference and harvested lakes. For benthic algae,
however, Chl a per unit cell was higher in burnt lakes (p <
0.05) than in harvested or reference lakes (D. Planas et al.,
unpublished data). Consequently, we cannot exclude the pos
-
sibility that higher Chl a concentrations in benthic algae in
burnt lakes are related to lower light conditions as compared
with reference lakes. For the burnt lakes in which benthic al
-
gae were studied, the 1997 and 1998 mean euphotic zone to
mixing depth ratio (Z
ph
/Z
mix
) was lower than 1 (Z
ph
/Z
mix
=
0.796 ± 0.106) and less (p < 0.05) than in the reference lakes
(Z
ph
/Z
mix
= 1.31 ± 0.101), while it was intermediate in har
-
vested lakes (Z
ph
/Z
mix
= 0.992 ± 0.106).
In conclusion, increases in nutrient loading as a conse
-
quence of watershed perturbation may modify algal biomass
and induce changes in the pelagic algal community struc
-
ture. The littoral algae showed a greater response to pertur
-
bations than pelagic algae. Responses were somewhat
different for lakes on harvested watersheds as compared with
lakes in burnt watersheds. Lack of riparian vegetation in
some burnt watersheds may explain why biomass and algal
composition responses were greater in burnt lakes than in
harvested lakes. Three years after perturbation, algal bio
-
mass may still have not reached a steady state. At present,
results indicate that TP is the main nutrient driving these
changes, although total pelagic productivity in the perturbed
lakes could be impaired by low light penetration. Changes in
species composition among perturbed lakes did not induce
the development of inedible algae in the pelagic zone. How
-
© 2000 NRC Canada
Planas et al. 143
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© 2000 NRC Canada
144 Can. J. Fish. Aquat. Sci. Vol. 57(Suppl. 2), 2000
ever, because N seems to play some role and if N export
decreases through time and P continues to leach from the
watershed, we can expect the development of toxic cyano
-
bacteria. Decreases in biomass associated with light limita
-
tion or changes in algal quality due to changes in N/P ratios
could negatively affect fish communities in these pristine
boreal lakes. Although we could not discount the influence
of natural interannual variability on our results because pre
-
perturbation data from these lakes were not available, our
study does indicate that simple empirical models incorporat
-
ing perturbation scenarios and variables such as lake area,
which is easily measured from maps, could be used in the
development of sustainable harvesting practices.
Acknowledgments
The project was supported by a research grant from the
Sustainable Forest Management Network of Centers of Ex
-
cellence and the Natural Sciences and Engineering Research
Council of Canada. The Ministry of Natural Resources of
Québec, Cartons Saint-Laurent, Donohue, and Kruger pro
-
vided land use information. We thank P. D’Arcy (Université
de Montréal) for coordination of the field activities and N.
Armstrong, S. Lamontagne, S. Montgomery, and C. Vis for
their valuable comments on the manuscript.
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