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Diet and Feeding Success of Fast-Growing Yellow Perch
Larvae and Juveniles in Perturbed Boreal Lakes
a d a b c d
Véronique Leclerc , Pascal Sirois , Dolors Planas & Pierre Bérubé
a
Laboratoire des Sciences Aquatiques, Département des Sciences Fondamentales, Université
du Québec à Chicoutimi, 555 Boulevard de l’Université, Chicoutimi, Quebec, G7H 2B1,
Canada
b
Centre GÉOTOP, Université du Québec à Montréal, C.P. 8888, Succursale Centre-Ville,
Montreal, Quebec, H3C 3P8, Canada
c
Direction de la Recherche sur la Faune, Ministère des Ressources Naturelles et de la Faune,
880 Chemin Ste-Foy 2e étage, Quebec City, Quebec, G1S 4X4, Canada
d
Direction de l’Expertise sur la Faune et ses Habitats, Ministère des Ressources Naturelles
et de la Faune, 880 Chemin Ste-Foy 2e étage, Quebec City, Quebec, G1S 4X4, Canada
Available online: 22 Sep 2011
To cite this article: Véronique Leclerc, Pascal Sirois, Dolors Planas & Pierre Bérubé (2011): Diet and Feeding Success of Fast-
Growing Yellow Perch Larvae and Juveniles in Perturbed Boreal Lakes, Transactions of the American Fisheries Society, 140:5,
1193-1205
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connection with or arising out of the use of this material.Transactions of the American Fisheries Society 140:1193–1205, 2011
C American Fisheries Society 2011
ISSN: 0002-8487 print / 1548-8659 online
DOI: 10.1080/00028487.2011.607040
ARTICLE
Diet and Feeding Success of Fast-Growing Yellow Perch
Larvae and Juveniles in Perturbed Boreal Lakes
Véronique Leclerc*1 and Pascal Sirois
Laboratoire des Sciences Aquatiques, Département des Sciences Fondamentales,
Université du Québec à Chicoutimi, 555 Boulevard de l’Université,
Chicoutimi, Quebec G7H 2B1, Canada
Dolors Planas
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Centre GÉOTOP, Université du Québec à Montréal, C.P. 8888, Succursale Centre-Ville,
Montreal, Quebec H3C 3P8, Canada
Pierre Bérubé1
Direction de la Recherche sur la Faune, Ministère des Ressources Naturelles et de la Faune,
880 Chemin Ste-Foy 2e étage, Quebec City, Quebec G1S 4X4, Canada
Abstract
The principal objective of this study was to test the hypothesis that enhanced early growth of yellow perch Perca
flavescens in lakes affected by forest harvesting was related to favorable feeding conditions after the perturbation.
Yellow perch larvae and juveniles and their zooplankton prey were sampled three times in three unperturbed lakes
and in three perturbed lakes where forest harvesting had occurred in the catchment 2 years earlier. Univariate and
multivariate analyses of the diets of age-0 yellow perch from both treatments showed that fish in perturbed lakes
primarily preyed upon Daphnia spp. and Polyphemus pediculus, whereas fish in unperturbed lakes preyed upon
more diverse food items. Perturbed lakes showed higher dissolved organic carbon concentrations, algal biomass, and
Daphnia spp. abundance. The feeding success index (number of prey items in the stomach per millimeter of fish
length) and recent growth rates of age-0 yellow perch showed a significant type II functional relationship with the
abundance of Daphnia spp. We hypothesized that the increase in Daphnia spp. abundance and a darkening of water
color in perturbed lakes may have favored prey detection and growth for larval and juvenile yellow perch, thereby
affecting population recruitment.
Central hypotheses in fishery science assume that the avail- fact, according to the growth–mortality hypothesis, slow growth
ability of adequate prey during the larval stage can explain lowers the survival rates of larval fish by increasing their vul-
a large proportion of the recruitment variability in marine nerability to predators owing to their smaller size (Miller et al.
and freshwater fish populations (Hjort 1914; Anderson 1988; 1988) and lower ability to escape (Takasuka et al. 2003).
Houde 2008). Low prey abundance could lead to high mortal- Factors that are likely to influence prey availability in fresh-
ity rates directly through starvation (critical period hypothesis: water lakes could therefore affect larval fish feeding success
Hjort 1914) or indirectly through integrated processes affect- and growth and generate large variations in recruitment. Several
ing growth (growth–mortality hypothesis: Anderson 1988). In studies have reported that forest harvesting in lake catchments
*Corresponding author: veronique.leclerc@mrnf.gouv.qc.ca
1
Present address: Direction de l’Expertise sur la Faune et ses Habitats, Ministère des Ressources Naturelles et de la Faune, 880 Chemin Ste-Foy
2e étage, Quebec City, Quebec G1S 4X4, Canada.
Received September 16, 2010; accepted February 19, 2011
11931194 LECLERC ET AL.
can modify water quality and the limnoplankton community The general objective of the study was to test the hypothesis
structure (Carignan et al. 2000; Patoine et al. 2000; Planas that the enhanced growth rate of age-0 yellow perch in boreal
et al. 2000; Winkler et al. 2009). Recently, Leclerc et al. lakes affected by forest harvesting was attributable to favorable
(in press) showed that young-of-the-year (age-0) yellow perch feeding conditions after the perturbation. To reach this objective,
Perca flavescens exhibited higher growth rates and greater we first described and compared the diets of larval and juvenile
lengths at age during the larval stage (0–40 d posthatch) after yellow perch from perturbed and unperturbed lakes. We then
forest harvesting in lake catchments on the eastern Canadian Bo- compared the availability of the principal prey taxa in both lake
real Shield. These results suggested that modifications in water types. Finally, we investigated the influence of environmental
quality and limnoplankton community structure due to forestry conditions, such as prey abundance and water quality, on the
activities influenced the feeding success of age-0 yellow perch, feeding success index (number of prey items ingested per mil-
causing the changes in growth. The effect of forest harvesting on limeter of fish length) and the recent growth rate of age-0 yellow
fish populations is not well described, and very few studies have perch.
focused on the early life stages of fish. Moreover, the processes
by which forest harvesting may enhance yellow perch growth
during early life are still unknown. METHODS
The yellow perch is a well-studied and common forage fish Study sites and field sampling.—The study area, located in
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in North American waters. The early life stages of yellow the Canadian Boreal Shield ecoregion, was situated north of
perch are zooplanktivorous, feeding on copepods and clado- the 50th parallel (50◦ N) and approximately 60 km southeast of
cerans (Hansen and Wahl 1981; Post and McQueen 1988; Craig Lake Mistassini in the province of Quebec (Figure 1). Lakes in
2000). Yellow perch growth and recruitment are closely related this area are typically oligotrophic and shelter fish communities
to temperature (Glémet and Rodrı́guez 2007), prey availability that are mainly composed of northern pike Esox lucius, walleyes
(Abbey and Mackay 1991; Bremigan et al. 2003; Dettmers et al. Sander vitreus, white suckers Catostomus commersonii, burbot
2003), and environmental factors that control the visual environ- Lota lota, and yellow perch. This region is also characterized by
ment and feeding success (Hinshaw 1985; Arvola et al. 1996; spruce–moss landscapes that are exploited by the forest industry.
Richmond et al. 2004). Therefore, forest harvesting in lake Six headwater lakes were selected for this study (Figure 1;
catchments may affect recruitment success via changes in the for a detailed description of each lake, see Leclerc et al., in
prey community. press). All lakes were sampled in summer 2005. At the time of
FIGURE 1. Study area in the eastern Canadian Boreal Shield, showing the location of perturbed and unperturbed lakes.DIET AND FEEDING SUCCESS OF YELLOW PERCH 1195
sampling, three lakes were unperturbed sites (i.e., without any pelagic zone of each lake were conducted from 1 m off the bot-
perturbation in the drainage area). The three other lakes (here- tom to the surface; the sampling gear was a 53-µm-mesh net
after, perturbed lakes 1, 3, and 5; Figure 1) were perturbed by with a 25-cm-diameter mouth aperture. Three replicate hauls
forest harvesting that had occurred 2 years before; the percent- were performed in the littoral zone with the same sampling
age of drainage area that was affected by harvesting was 57% device, but the net was deployed along a 30-m transect at the
for perturbed lake 1, 51% for perturbed lake 3, and 34% for water surface on the 1-m isobath. The volume of water filtered
perturbed lake 5. Perturbed and unperturbed lakes had similar was measured with a flowmeter (General Oceanics). Zooplank-
geographical, morphological, physicochemical, and biological ton were anesthetized in carbonated water and preserved in 4%
characteristics based on measurements made before the pertur- buffered formaldehyde.
bation occurred (Leclerc et al., in press). Water quality and chlorophyll-a concentration (chl a) were
Larval and juvenile yellow perch and their zooplankton prey measured in all lakes on 8 August 2005. Measurements of tem-
were collected during three surveys in each lake: early July perature, Secchi depth, dissolved organic carbon (DOC) con-
(4–8 July 2005), mid-July (19–22 July 2005), and early August centration, and chl a were taken in the euphotic zone at the
(1–4 August 2005). Age-0 yellow perch display ontogenetic deepest point of each lake (see Winkler et al. 2009 for complete
shifts in habitat use. Early in the season, yellow perch hatch in methods).
the littoral zone and undergo a migration to the pelagic zone; Diet composition analyses.—Yellow perch from all samples
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upon reaching approximately 25 mm in length, they then return were sorted and measured. For each lake, stomach content analy-
to the littoral zone (Whiteside et al. 1985; Post and McQueen sis was performed on a random subsample of age-0 yellow perch
1988). Given these size-specific migrations, we used a sampling selected in proportion to the length frequency distributions ob-
plan designed to obtain a complete collection of all size-classes served for each survey (Table 1). The entire stomach contents
as suggested by Scharf et al. (2009). During the early July of 287 fish were examined under a stereoscopic microscope at
survey, fish sampling was conducted at six randomly located 50× magnification. All prey items were identified to the lowest
stations in the pelagic zone and six stations in the littoral zone taxonomic level possible (species in most cases). The devel-
to catch larvae, early juveniles, or both. The pelagic sampling opmental stage was noted for copepods (nauplii or copepodite
gear consisted of two push nets (500-µm mesh; mouth aperture stages CI–CVI) and immature insects (larvae, pupae, or adult).
= 50 cm in diameter) deployed on each side of the boat. Push The following keys were used for identification: Edmondson
nets were deployed at the lake surface for 10 min at a constant (1959) for general identification, Smith and Fernando (1978)
speed of 2 km/h between 2100 and 0200 hours; this time period and Czaika (1982) for copepods, Hebert and Finston (1996,
was selected because pelagic-phase yellow perch feed at night 1997) for Daphnia spp., and Merritt and Cummins (1996) for
in surface waters to avoid predation (Cucin and Faber 1985; immature insects. Developmental stages of copepods were de-
Post and McQueen 1988). The littoral sampling gear consisted termined by using the criteria of Czaika (1982). Incomplete or
of a beach seine (4 m long; 1 m deep; 500-µm mesh) deployed digested organisms and immature copepods that could not be ac-
over a 30-m transect between 1400 and 1900 hours, the time at curately identified to the species level were assigned to species
which yellow perch feed in littoral habitats (Post and McQueen that were present in the stomach in proportion to their relative
1988). During the mid-July and early August surveys, fish were abundance (Robert et al. 2008). This procedure was applied to
sampled in the littoral zone only. Once captured, sampled fish less than 2% of all prey items.
were immediately immersed in a 100-mg/L solution of tricaine Subsampled fish were grouped into six length-classes (stan-
methanesulfonate (MS-222) for 2–4 min to prevent stomach dard length in 5-mm increments; Table 2). The smallest length-
content regurgitation before the fish were preserved in 95% class was underrepresented in perturbed lakes, and the largest
ethanol. The ethanol was replaced within 24 h to avoid alcohol length-class was not represented in unperturbed lakes. We
dilution and otolith damage (Butler 1992). used fish in the three length-classes that were common to the
The zooplankton community was sampled during each sur- two lake treatments (15–20, 20–25, and 25–30 mm) for most
vey in the pelagic and littoral zones. Three vertical hauls in the analyses.
TABLE 1. Number of yellow perch used in feeding and growth analyses for each sampling survey period in perturbed (pert.) and unperturbed (unpert.) lakes of
the Canadian Boreal Shield.
Sampling survey Pert. 1 Pert. 3 Pert. 5 Unpert. 1 Unpert. 3 Unpert. 4 Total
Early Jul 35 21 18 18 3 13 108
Mid-Jul 26 19 15 23 0 23 106
Early Aug 19 9 15 10 0 20 73
Total 80 49 48 51 3 56 2871196 LECLERC ET AL.
TABLE 2. Diet composition by lake treatment and yellow perch length-class, expressed as the mean percent numeric contributions of the different prey taxa to
the diets of fish with at least one prey item in their stomachs (dash = zero; na = data not available). Feeding statistics are also provided. Fish from the 35–40-mm
length-class were not captured in unperturbed lakes.
Perturbed lakes: fish length- Unperturbed lakes: fish length-
class (mm) class (mm)
Prey taxon Stagea 10–15 15–20 20–25 25–30 30–35 35–40 10–15 15–20 20–25 25–30 30–35
Rotifera na – 0.09 – 0.02 0.02 2.08 3.67 2.67 – –
Copepoda
Nauplii na 10.12 0.43 0.26 – – – 0.32 4.63 5.96 –
Calanoida
Leptodiaptomus minutus CI–CV na 10.25 11.70 3.31 1.00 3.08 – 3.33 0.93 0.05 –
CVI na 10.46 14.65 2.94 0.85 1.04 31.19 5.23 2.64 3.08 1.32
Skistodiaptomus oregonensis CVI na – – – – 0.12 – – – – –
Epischura lacustris CI–CV na 0.61 0.34 0.17 0.12 – – – 1.00 0.47 –
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CVI na 12.97 0.83 4.04 5.07 0.01 12.47 5.54 1.67 3.22 –
Cyclopoida
Cyclops scutifer CVI na – – – – – 2.92 1.90 – 0.03 –
Mesocyclops edax CI–CV na – – 0.24 0.11 – – – – – –
CVI na – 0.12 0.09 1.51 0.01 4.46 – – 0.05 –
Microcyclops varicans CVI na – – – – – – – – 0.37 –
rubellus
Acanthocyclops capillatus CI–CV na – – – – – – – – 0.14 –
CVI na – – – – 0.01 – – 0.02 0.45 –
Acanthocyclops vernalis CI–CV na – 0.05 – 0.09 0.37 – 0.33 0.09 0.41 –
CVI na – 0.11 – 0.32 1.40 2.23 0.29 1.28 2.48 –
Eucyclops agilis CI–CV na – – – 0.25 0.02 – 0.08 1.17 2.24 –
CVI na – – – 0.27 0.17 – 0.32 1.74 8.46 –
Macrocyclops albidus CI–CV na – – 0.95 0.26 0.50 – – – – –
CVI na – – 0.01 0.56 1.42 – – 0.47 0.03 –
Tropocyclops prasinus CI–CV na 1.97 0.49 – – 0.35 – – 0.47 1.33 –
mexicanus CVI na 0.57 3.12 – 0.19 0.73 – – 5.38 7.58 –
Cladocera
Leptodoridae
Leptodora kindtii na 1.57 0.13 – 0.12 – – – – – –
Sididae
Latona setifera na – – – 0.03 0.06 – 9.29 13.27 4.14 –
Sida crystallina na 0.75 0.48 0.21 0.48 – – 14.34 7.95 1.59 –
Diaphanosoma spp. na – – 3.44 2.40 1.28 – – – – –
Holopedidae
Holopedium gibberum na 1.00 0.96 0.01 – – – 11.96 7.94 10.01 0.36
Daphnidae
Daphnia longiremis complexb na – 18.06 13.08 12.24 14.08 7.37 6.79 0.06 – –
Daphnia pulex complexc na 0.29 22.42 12.27 24.49 28.76 – – – – –
Ceriodaphnia reticulata na – – – 2.00 0.23 – – 0.04 – –
Bosminidae
Bosmina spp. na 1.36 2.74 7.50 6.93 1.44 37.28 14.19 12.32 5.92 22.37
Macrothricidae
Acantholeberis curvirostris na – – – 0.54 2.28 – 0.08 0.05 0.02 –
Ophryoxus gracilis na – – – 10.69 11.60 – – 1.94 3.30 –
Parophryoxus tubulatus na – – – 0.12 0.11 – – – – –
(Continued on next page)DIET AND FEEDING SUCCESS OF YELLOW PERCH 1197
TABLE 2. Continued.
Perturbed lakes: fish length- Unperturbed lakes: fish length-
class (mm) class (mm)
Prey taxon Stagea 10–15 15–20 20–25 25–30 30–35 35–40 10–15 15–20 20–25 25–30 30–35
Chydoridae
Acroperus harpae na – 0.21 0.48 0.59 2.52 – 1.17 7.30 2.19 1.09
Alona affinis na – – – 0.42 0.51 – – 0.71 0.07 –
Alona costata na – – – 0.18 0.11 – – – – 1.82
Alona quadrangularis na – – 0.07 – – – 0.63 0.05 0.78 –
Alona rustica na – – 0.07 0.03 0.08 – 1.45 1.24 0.09 –
Chydorus sphaericus na – 0.02 – 0.07 0.16 – 0.44 2.23 0.76 –
Eurycercus spp. na – – – 1.34 1.22 – – 0.05 0.03 –
Rhynchotalona falcata na – – 0.03 0.10 0.03 – – 8.69 22.47 72.22
Other chydoridsd na – 0.09 0.24 0.38 – – – 0.58 0.62 –
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Polyphemidae
Polyphemus pediculus na 47.64 22.45 47.84 22.05 5.84 – 17.93 9.51 2.53 0.36
Insecta
Hemiptera
Corixidae Corixinae Larva na – – – 0.45 1.46 – – 0.10 0.63 –
Diptera Larva na – – 2.07 2.13 10.95 – 0.40 1.21 3.94 0.36
Diptera Pupa na – 0.42 0.42 1.16 2.17 – – 0.28 1.38 –
Other insects Larva na 0.22 – – 0.11 0.69 – – 0.12 0.14 –
Amphipoda
Hyalella azteca na – – – 0.22 1.25 – – 0.03 1.23 –
Other invertebratese na 0.22 0.09 0.26 0.11 3.92 – 0.32 0.17 1.81 0.10
Prey categories
Pelagic zooplankton na 98.81 98.69 92.71 78.48 59.58 100 71.88 54.04 54.81 24.41
Vegetation-associated na 0.75 0.80 4.54 17.35 19.96 – 27.40 44.05 36.06 75.23
zooplankton
Benthic macroinvertebrates na 0.44 0.51 2.75 4.17 20.46 – 0.72 1.91 9.13 0.36
Feeding statistics
Number of fish analyzed 1 20 43 29 46 38 18 20 48 22 2
Number of fish with ≥ 1 prey 0 19 42 28 45 31 8 15 46 22 2
Feeding incidence (%) 0 95 98 97 98 82 44 75 96 100 100
Mean number of prey 0 33.8 47.1 132.3 98.9 101.4 19.6 19.0 61.6 49.0 87.5
a
Developmental stage is shown for copepods (CI–CVI) and immature insects (larvae and pupae).
b
Daphnia longiremis complex includes D. longiremis, D. dubia, D. galeata mendotae, and D. rosea.
c
Daphnia pulex complex includes D. pulex, D. middendorffiana, D. catawba, D. pulicaria, and D. minnehaha.
d
Other chydorids include Alonella excisa, Camptocercus rectirostris, Chydorus bicornutus, Chydorus piger, Graptoleberis testudinaria, and Pleuroxus procurvus.
e
Other invertebrate taxa include Acariformes, Collembola, Harpacticoida, adult Insecta, Oligochaeta, and Ostracoda.
The yellow perch diet was first characterized in terms of the residuals (Quinn and Keough 2002). The total number of in-
total number of ingested prey. Three-way partly nested analysis gested prey was tested over all 15–30-mm yellow perch (n =
of variance (ANOVA) was used to compare the total number 182).
of ingested prey. Sources of variation were lake treatment (per- Zooplankton species assemblages in the yellow perch diet
turbed and unperturbed; fixed factor), individual lakes (lakes were compared with three different multivariate procedures.
nested within treatment; random factor), length-class (15–20, First, the ANOVA model described in the previous para-
20–25, and 25–30 mm; fixed factor), and their interactions. Data graph was used to test for differences in ingested prey as-
were log10 transformed to achieve normality and homoscedas- semblages. This analysis was done with a permutational multi-
ticity, as indicated by visual examination of the distribution of variate ANOVA (PERMANOVA; Anderson 2001). The model1198 LECLERC ET AL.
had the same sources of variation as described above but used The functional relationships between prey abundance and
4,999 permutations to determine the test statistics. The PER- yellow perch feeding success and recent growth rate were based
MANOVA was performed on the Bray–Curtis similarity matrix on a type II functional response (Holling 1959) and were as-
of standardized abundance data (Bray and Curtis 1957). Second, sessed with Ivlev’s (1961) function,
zooplankton species assemblages in the diet were illustrated by
a nonmetric multidimensional scaling (NMDS) ordination on y = a(1 − exp−bx ),
standardized abundance data with the Bray–Curtis similarity
measure. Third, similarity of percentages (SIMPER) analyses where y is predator response (i.e., feeding success or recent
(Clarke and Warwick 2001) were conducted on the Bray–Curtis growth rate), x is prey abundance, a is the maximum predator
similarity matrix of standardized abundance data to determine response, and b is the coefficient relating the change in prey
the principal prey taxa consumed by fish in both treatments and abundance to the predator response. The regression model was
to identify, if necessary, the species involved in the diet dissim- fitted with SigmaPlot version 10.0.
ilarity illustrated in the NMDS analysis. Fish (15–30 mm) with Recent growth rates of yellow perch were compared between
empty stomachs were not considered in multivariate analyses; perturbed and unperturbed lakes by using one-way ANOVA
we only used fish with at least one prey item in the stomach (lake treatment: perturbed and unperturbed; fixed factor). The
(n = 172). replication unit was individual lakes; the mean recent growth
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Prey field analyses.—Zooplanktonic organisms from pelagic rates of fish captured in the same sampling survey were av-
and littoral samples (n = 100) were subsampled by use of eraged. The unbalanced number of sampling surveys between
a pipette with a 4-mm opening. Organisms were enumer- lakes prevented the use of the same statistical test used for the
ated, staged, and identified to the lowest taxonomic level nested models.
possible—usually species—with the aforementioned keys. Other environmental variables, such as water temperature,
The abundance of yellow perch prey taxa in perturbed and Secchi depth, DOC, and chl a, were compared by means of two-
unperturbed lakes was compared with three-way partly nested way partly nested ANOVA with lake treatment and individual
ANOVA by using zooplankton samples from both littoral and lakes (nested in the treatment factor) as sources of variation.
pelagic habitats as replicates. Sources of variation were lake
treatment (perturbed and unperturbed; fixed factor), individual RESULTS
lakes (lakes nested within treatment; random factor), survey
(early July, mid-July, and early August; fixed factor), and their Diet Composition
interactions. Data were log10 (x + 1) transformed to achieve The diet of age-0 yellow perch in all length-classes (10–
normality and homoscedasticity. In addition to univariate analy- 40 mm) was mainly composed of zooplankton (Table 2). For the
ses, complete zooplankton assemblages were compared between three length-classes between 15 and 30 mm, age-0 yellow perch
lake treatments with a three-way partly nested PERMANOVA in perturbed lakes preyed predominantly on Polyphemus pedicu-
on log10 (x + 1)-transformed data with the same sources of lus, Daphnia spp., and Leptodiaptomus minutus stages CI–CVI,
variation as mentioned for univariate analyses of zooplankton whereas Bosmina spp., Rhynchotalona falcata, Latona setifera,
data. Holopedium gibberum, P. pediculus, and Sida crystallina were
Feeding success and recent growth analyses.—A length- the most abundant food items consumed by larvae and juveniles
independent feeding success index for age-0 yellow perch was in unperturbed lakes (Table 2). Cladoceran species represented
estimated as the number of prey ingested per millimeter of fish more than 50% of the prey ingested by 15–30-mm yellow perch
length (i.e., ingested prey items/mm). This index accounts for in perturbed and unperturbed lakes (Table 2). However, pelagic
the fact that larger fish have higher stomach volume and could species (e.g., Daphnia spp. and P. pediculus) were preferred in
ingest a higher number of prey items, considering that all an- perturbed lakes, whereas a significant percentage (>25%) of
alyzed fish predominantly preyed upon zooplankton. Recent cladoceran species consumed in unperturbed lakes were asso-
growth rate was measured by means of otolith microstructure ciated with aquatic vegetation (e.g., Sididae and Chydoridae;
analysis as described by Leclerc et al. (in press). Briefly, lapil- Table 2). In both lake types, age-0 yellow perch ingested lower
lar otoliths were removed, mounted on a microscope slide with proportions of pelagic zooplankton and higher proportions of
thermoplastic glue, and polished with 3- or 5-µm lapping film. vegetation-associated zooplankton and benthic macroinverte-
Daily increments were counted and measured with an image brates as they grew (Figure 2).
analysis system at 400–1,000× magnification. Standard length The feeding incidence (percentage of fish with at least one
at age was back-calculated by means of the biological inter- prey item in their stomachs) of 15–30-mm age-0 yellow perch
cept method (Campana 1990) based on a laboratory-derived ranged from 95% to 98% in perturbed lakes and from 75%
measure of length at hatching (7.53 mm) and the individual ob- to 100% in unperturbed lakes and did not differ significantly
served otolith radius at hatching (Leclerc et al., in press). Recent between treatments (χ2 = 1.79, P = 0.1812; Table 2). The
growth rate was calculated as the average growth rate (mm/d) mean number of prey ingested by age-0 yellow perch within
that occurred during the 3 d before capture. this size range tended to increase with length-class, but theDIET AND FEEDING SUCCESS OF YELLOW PERCH 1199
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FIGURE 2. Diet composition (% of prey items) for yellow perch of three length-classes (15–20, 20–25, and 25–30 mm standard length) in (a) perturbed lakes
and (b) unperturbed lakes.
increase was only marginally significant (length-class: F 2, 12.9 variations within treatments (lake treatment: F 1, 3 = 2.63, P =
= 3.24, P = 0.0725; Figure 3). Even though the mean number 0.2032; Figure 3).
of prey appeared to be higher for fish in perturbed lakes, the The NMDS analysis showed a clear separation of species
difference between treatments was not significant owing to large assemblages in the diets of 15–30-mm age-0 yellow perch be-
tween perturbed and unperturbed lakes (Figure 4). The PER-
MANOVA indicated that species assemblages of ingested prey
were significantly different between lake treatments (Table 3).
The SIMPER analysis showed that the ingested prey assem-
blages were more homogeneous among fish in perturbed lakes,
as the average similarity was 25.3% compared with 12.3% in
unperturbed lakes. The ingested prey species assemblages were
92.8% dissimilar between fish in the two treatments. Together,
P. pediculus, Daphnia spp., Bosmina spp., and Leptodiaptomus
minutus stage CVI accounted for 48.6% of the dissimilarity
in diet species assemblages between lake treatments (Table 4).
These prey taxa were more abundant in the age-0 yellow perch
diets from perturbed lakes, except for Bosmina spp., which were
consumed more by fish in unperturbed lakes (Tables 2, 4).
Prey Field
In total, 39 zooplankton taxa were identified in perturbed
lakes and 31 zooplankton taxa were identified in unperturbed
lakes. Copepod species numerically dominated the zooplank-
ton community, making up on average 85% and 90% of
the samples in perturbed and unperturbed lakes, respectively.
FIGURE 3. Number of prey ingested (mean + SE) by yellow perch of three Among the prey taxa listed in Table 4 that were responsible
length-classes (15–20, 20–25, and 25–30 mm standard length) in perturbed and for the difference in age-0 yellow perch diets between lake
unperturbed lakes. treatments, only Daphnia spp. showed a significant difference1200 LECLERC ET AL.
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FIGURE 4. Nonmetric multidimensional scaling results, illustrating variations
in prey assemblages (standardized data) ingested by three yellow perch length-
classes (15–20, 20–25, and 25–30 mm standard length) from perturbed (pert.)
and unperturbed (unpert.) lakes. Results of the corresponding permutational
multivariate ANOVA are given in Table 3.
FIGURE 5. Daphnia spp. abundance (individuals [ind.]/L; mean + SE) mea-
sured in perturbed and unperturbed lakes during three surveys. Each bar repre-
in abundance between lake types: they were more abundant
sents the average abundance in the littoral and pelagic zones combined for the
in perturbed lakes than in unperturbed lakes throughout the three lakes in the corresponding treatment.
sampling surveys (lake treatment: F 1, 4 = 8.63, P = 0.0420;
Figure 5). There was no significant difference in the prey
species assemblages between perturbed and unperturbed lakes in Table 4 were not significant except for Daphnia spp. (Figure
(lake treatment: pseudo-F 1, 4 = 1.26, PMonte Carlo = 0.2912) 6). An Ivlev function that incorporated Daphnia spp. abundance
despite the lower Daphnia spp. abundance in unperturbed as the independent variable explained 29% of the variability in
lakes. yellow perch feeding success on Daphnia spp. (F 1, 14 = 5.73,
P = 0.0312) and 47% of the variability in recent growth rate
Feeding Success and Growth of Age-0 Yellow Perch in (F 2, 13 = 5.84, P = 0.0155; Figure 6). The maximum recent
Relation to Biotic and Abiotic Environmental Factors growth rate was reached at a Daphnia spp. abundance of approx-
Relationships between the feeding success or recent growth imately 0.23 individuals/L, whereas maximum feeding success
rate of age-0 yellow perch and the abundance of prey taxa listed was not reached even at the maximum observed abundance of
Daphnia spp. (0.62 individuals/L; Figure 6). On average, fish
TABLE 3. Results of three-way partly nested permutational multivariate in perturbed lakes exhibited a higher mean feeding success on
ANOVA on standardized data testing the effect of lake treatment (TR), lake Daphnia spp. than did fish in unperturbed lakes (lake treatment:
nested in the treatment factor (LA[TR]), yellow perch length-class (LC), and F 1, 4 = 12.10, P = 0.0254). In addition, fish in perturbed lakes
their interactions on the assemblages of ingested prey taxa (MS = mean square). had a higher mean recent growth rate than fish in unperturbed
Taxonomic resolution is as described in Table 2. Significant P-values are shown
lakes (lake treatment: F 1, 4 = 21.64, P = 0.0096; Figure 6).
in bold italics.
For a given abundance of Daphnia spp., age-0 yellow perch in
Source of perturbed lakes always exhibited a higher feeding success and
variation df MS Pseudo-F PMonte Carlo faster recent growth than yellow perch in unperturbed lakes.
Chlorophyll a and DOC were significantly higher in per-
TR 1 20,699.0 2.2563 0.0394 turbed lakes than in unperturbed lakes (Table 5). Water trans-
LA(TR) 3 9,225.7 3.1056 0.0002 parency, as indicated by Secchi depth, tended to be lower in per-
LC 2 4,675.4 0.7778 0.7304 turbed lakes (P = 0.0546), suggesting that waters were darker
TR × LC 2 5,824.8 0.9690 0.4856 and more turbid in perturbed lakes than in unperturbed lakes (Ta-
LA(TR) × LC 6 7,121.5 2.3973 0.0002 ble 5). Water temperature did not differ significantly between
Residuals 157 2,970.7 lake treatments, even though more turbid water tends to absorb
Total 171 more sunlight than clear water.DIET AND FEEDING SUCCESS OF YELLOW PERCH 1201
TABLE 4. Results of similarity of percentages (i.e., SIMPER) analysis on standardized data, showing the major discriminating prey taxa in the diets of yellow
perch, their average abundance, average dissimilarity, and cumulative contribution to the dissimilarity between the assemblages of prey ingested by fish in perturbed
(pert.) and unperturbed (unpert.) lakes across fish length-classes (15–30 mm).
Average abundance (%)
Taxon Pert. Unpert. Average dissimilarity (%) Cumulative contribution (%)
Polyphemus pediculus 35.6 9.2 18.5 20.0
Daphnia pulex complex 14.4 0.0 7.2 27.7
Daphnia longiremis complex 13.1 1.3 6.8 35.1
Bosmina spp. 3.9 11.0 6.6 42.2
Leptodiaptomus minutus stage CVI 9.9 3.2 5.9 48.6
Rhynchotalona falcata 0.0 10.8 5.4 54.4
Latona setifera 0.0 10.1 5.1 59.8
Holopedium gibberum 0.9 9.2 4.7 64.9
Leptodiaptomus minutus stages CI–CV 8.6 1.1 4.7 69.9
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Sida crystallina 0.5 7.4 3.8 74.1
DISCUSSION prey taxa that were characteristic of the pelagic zone, as has been
Our results indicate that growth of age-0 yellow perch in lakes observed in studies on the ontogenetic migration and feeding of
affected by forest harvesting was largely influenced by feeding yellow perch (Whiteside et al. 1985; Post and McQueen 1988;
conditions. Perturbed lakes had higher Daphnia spp. abundance Dettmers et al. 2005). The observed combination of pelagic
and higher DOC concentrations than unperturbed lakes. We sug- and vegetation-associated zooplankton ingested by larger fish
gest that these changes in the biotic and abiotic environmental (>15 mm), which were all caught in the littoral zone, suggests
feeding conditions promoted yellow perch growth by offering a that they probably fed in different habitats. These results are
higher abundance of suitable prey that were more conspicuous, consistent with the observations of Post and McQueen (1988),
thereby lowering the energy costs allocated to foraging. Given who demonstrated that age-0 yellow perch (16–34 mm) migrate
the importance of growth for survival and recruitment of fish from offshore to nearshore at dawn and return at dusk, occupy-
populations, we therefore hypothesize that the perturbations in ing the nearshore zone throughout the day.
boreal lake catchments affect survival and recruitment of yel- The high taxonomic resolution of identified prey presented
low perch populations through changes in biotic and abiotic in this study demonstrates that despite the similar proportions
environmental conditions. of copepods, cladocerans, and macroinvertebrates in their diets,
fast-growing yellow perch from perturbed lakes fed primarily
Diet Composition of Fast- and Slow-Growing Larval on pelagic cladoceran species, such as Daphnia spp. and P.
and Juvenile Yellow Perch pediculus, whereas slow-growing yellow perch in unperturbed
In a recent investigation, we demonstrated that 2 years after lakes preyed on diverse food items. Many other studies have
forest harvesting occurred in lake catchments, the growth rate shown that age-0 yellow perch that feed on Daphnia tend to
of age-0 yellow perch from hatching to 40 d posthatch was 1.43 have higher growth rates (Hansen and Wahl 1981; Schael et al.
times higher for fish from perturbed lakes compared with fish 1991). We therefore hypothesize that for age-0 yellow perch
from unperturbed lakes (Leclerc et al., in press). The results in lakes affected by forest harvesting, feeding on these two
of the present study support the hypothesis that the enhanced cladoceran taxa results in higher growth rates relative to fish
growth rate of age-0 yellow perch in perturbed lakes was related in unperturbed lakes, where a greater variety of prey types is
to favorable feeding conditions after the perturbation. consumed. The enhanced growth rate of age-0 yellow perch in
Several studies have described age-0 yellow perch diet com- perturbed lakes was related to the availability of Daphnia spp.
position, but few have determined diet to the species level but was also probably related to changes in the visual feeding
and none has employed a multivariate approach (Hansen and conditions due to forest harvesting.
Wahl 1981; Graeb et al. 2004; Fulford et al. 2006). Similar to
the findings of these studies, which were conducted on more Effects of Forest Harvesting on Prey Availability
southerly populations, our results show that age-0 yellow perch An inadequate prey supply may limit growth, lead to poor
(10–40 mm) in lakes on the northeastern Boreal Shield feed on nutritional condition, and increase the susceptibility of young
pelagic and vegetation-associated zooplankton prey—primarily fish to predation (Anderson 1988; Houde 2008). Therefore, zoo-
cladocerans. The smallest fish (1202 LECLERC ET AL.
TABLE 5. Physicochemical variables and algal biomass (mean with SD
shown in parentheses) in perturbed (pert.) and unperturbed (unpert.) lakes (DOC
= dissolved organic carbon; chl a = chlorophyll-a concentration). Results of
ANOVA testing the effect of lake treatment are shown. Significant P-values are
shown in bold italics.
Variable Pert. Unpert. F 1, 4 PDIET AND FEEDING SUCCESS OF YELLOW PERCH 1203
while other studies have not (Baumann et al. 2003; Takahashi foraging activity (Sirois and Dodson 2000; Utne-Palm 2002;
and Watanabe 2005) or have observed only a weak relationship Shoji et al. 2005). The enhancement of feeding with increasing
(Takasuka and Aoki 2006; Robert et al. 2009). In these previous contrast may be explained by the higher detection of prey and
studies, the finding of no prey preference might be related to the an increase in feeding activity caused by a lowered risk of pre-
low taxonomic resolution achieved in the identification of prey dation (Gregory and Northcote 1993; Utne-Palm 2002; Shoji
in the stomachs. In this study, we found a significant relationship and Tanaka 2006). Indeed, predators with a short visual field
between Daphnia spp. abundance and the feeding success and (e.g., planktivorous fish) could benefit from increased contrast,
recent growth rate of age-0 yellow perch. However, no func- whereas increased turbidity could negatively affect piscivorous
tional responses were found when we used a lower taxonomic fish by shortening their visual field (Gregory and Northcote
grouping, such as total zooplankton abundance or abundance of 1993; Utne-Palm 2002). Therefore, turbidity has a contradic-
zooplanktonic crustaceans, copepods, or cladocerans. The func- tory effect at different trophic levels or at different life stages,
tional response associated with Daphnia spp. abundance shows making the positive effect of turbidity on fish feeding contro-
the importance of a high taxonomic resolution of prey items, as versial.
was achieved in this study.
In the present study, we demonstrated that both feeding suc- ACKNOWLEDGMENTS
cess on Daphnia spp. and the recent growth rate of age-0 yellow
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We thank the field and laboratory teams, including Y. Bherer,
perch follow a type II functional response (Holling 1959) with J. Brassard, D. Cleary, A.-L. Fortin, C. Girard, A. Ménard, I.
Daphnia spp. abundance. Interestingly, for the same abundance Poirier, and A. Sanfaçon. We also thank Abitibi-Bowater for pro-
of Daphnia spp., fish in perturbed lakes generally had a higher viding land use information and field facilities. This research
feeding success on this taxon and a higher recent growth rate was supported by public funds from Fonds de la Recherche
than fish in unperturbed lakes. Stomach content analyses indi- Forestière du Saguenay–Lac-Saint-Jean, Fonds Québécois de
cated that for the same Daphnia spp. abundance in the environ- la Recherche sur la Nature et les Technologies, Ministère des
ment, fish in unperturbed lakes ingested other, smaller clado- Ressources Naturelles et de la Faune du Québec, and Consor-
ceran taxa, such as vegetation-associated members of Sididae tium de Recherche sur la Forêt Boréale Commerciale. V. Leclerc
and Chydoridae. The higher Daphnia spp. consumption and was funded by Fonds Québécois de la Recherche sur la Nature
higher recent growth rates for fish in perturbed lakes at a given et les Technologies, Université du Québec à Chicoutimi, and the
Daphnia spp. abundance suggest that perturbed lakes provided Fédération Québécoise des Chasseurs et des Pêcheurs.
a visual environment that favored predation on Daphnia spp.
Other researchers have demonstrated that for larval fish, feed-
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