![Map of Alberta, showing location of study lakes (inset): Reference Lake 1 (R1; 55820 0 N, 111864 0 W); Reference Lake 2 (R2; 55815 0 N, 111876 0 W); Experimental Lake (EXP; 55805 0 N, 111865 0 W); and Piche Lake (source [S] lake; 55803 0 N, 111860 0 W).](https://www.researchgate.net/profile/Paul-Venturelli/publication/240765573/figure/fig1/AS:349590298611715@1460360230159/Map-of-Alberta-showing-location-of-study-lakes-inset-Reference-Lake-1-R1-55820-0_Q320.jpg)
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Diet and Growth of Northern Pike in the Absence of Prey Fishes:
Initial Consequences for Persisting in Disturbance-Prone Lakes
PAUL A. VENTURELLI*
1
AND WILLIAM M. TONN
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
Abstract.—The northern pike Esox lucius is a renowned piscivore, but will prey opportunistically on
invertebrates (e.g., in small lakes of boreal Alberta, where winterkill can unexpectedly reduce or eliminate
prey fishes). We emulated such a disturbance by stocking a fishless lake with northern pike and then
monitored their diet and growth over two summers. Stomach content analysis revealed that stocked adults
responded to the sudden absence of prey fishes by specializing on energy-rich leeches (families
Glossiphoniidae and Erpobdellidae), whereas juvenile offspring consumed a broader mix of invertebrates.
Stable isotope analysis supported these results and indicated a relatively rapid drop in the trophic position of
stocked adults. Compared with growth of northern pike in regional lakes containing prey fishes, growth of
adults in the experimental lake was apparently compromised by a diet of invertebrates but growth of juveniles
was high. Although long-term dynamics of northern pike in these disturbance-prone lakes are undocumented,
our results suggest that northern pike are capable of adapting rapidly to the absence of prey fishes; however,
such a diet imposes a trophic bottleneck that can lead to stunting.
The northern pike Esox lucius is considered to be
piscivorous throughout most of its circumpolar range
(Casselman 1996). Indeed, the morphology and
behavior of northern pike are specialized for ambush-
ing fish prey from the cover of vegetation (Keast and
Webb 1966; Webb 1984; Bry 1996). Not surprisingly,
numerous studies have shown northern pike to
specialize on fish prey (Frost 1954; Franklin and
Smith 1963; Vander Zanden et al. 1997; and references
therein). Consumption of large fishes is particularly
important for growth (Hart and Connellan 1984; Diana
1987; Margenau 1995).
Despite the piscivorous nature of northern pike and
the advantage of piscivory for growth, predation on
invertebrates (invertivory) has b een documented,
particularly in naturally productive systems in north-
western North America. Periodic bouts of invertivory
among otherwise piscivorous northern pike up to 600
mm in length (Chapman et al. 1989; Chapman and
Mackay 1990; Sammons et al. 1994; Lorenzoni et al.
2002) have been at tributed to differences in the
seasonal availability of vertebrate and invertebrate
prey. In other systems, predation on macroinvertebrates
appears more consistent (e.g., Beaudoin et al. [1999]
identified invertebrate specialists in two populations of
otherwise piscivorous northern pike on the basis of
complementary stomach content analysis [SCA] and
stable isotope analysis [SIA]). Such trophic flexibility
(Gerking 1994) is probably advantageous because of
dynamic prey environments (Dill 1983). Disturbances
(e.g., winterkills) are common in many small, naturally
productive boreal lakes (Danylchuk and Tonn 2003).
However, because northern pike are more tolerant of
winter hypoxia than other large-bodied fishes on which
they feed (Magnuson and Karlen 1970; Casselman
1996), northern pike can be found in lakes void of
forage fishes (Robinson and Tonn 1989). Populations
of northern pike in these lakes probably persist, in part,
because of an opportunistic feeding strategy (Chapman
and Mackay 1990; Beaudoin et al. 1999). Indeed,
invertivory is most prevalent among adult northern
pike in allopatric lakes (lakes in which northern pike
occur in the absence of prey fishes; Beaudoin et al.
1999).
Unclear, however, is the initial dietary response of
northern pike to sudden allopatry, as would occur after
a major winterkill (Tonn et al. 2004). Also unknown is
the energetic cost of the response and how this cost
affects growth. Northern pike are opportunists, but they
are also relatively poor learners (Coble et al. 1985). An
abrupt dietary switch from large to small prey (e.g.,
from piscivory to invertivory) might reduce net energy
intake per unit time, at least initially (Schoener 1971;
Werner et al. 1981; Gerking 1994; Pazzia et al. 2002),
and translate into lower growth.
In this study, we emulated sudden allopatry caused
by winterkill by stocking piscivorous northern pike
into a fishless lake, while simultaneously monitoring
other populations in lakes containing prey fishes, to
* Corresponding author: paul.venturelli@utoronto.ca
1
Present address: Department of Ecology and Evolutionary
Biology, University of Toronto, 25 Harbord Street, Toronto,
Ontario M5S 3G5, Canada.
Received September 20, 2005; accepted May 26, 2006
Published online November 9, 2006
1512
Transactions of the American Fisheries Society 135:1512–1522, 2006
Ó Copyright by the American Fisheries Society 2006
DOI: 10.1577/T05-228.1
[Article]
determine the (1) initial dietary response of the stocked
northern pike and their juvenile offspring and (2)
consequences for growth of adult northern pike and
their offspring. This research is particularly relevant,
given the increasing prevalence of anthropogenic
disturbances (e.g., forestry and oil and gas exploration)
in the boreal region (Timoney 2003). These distur-
bances not only increase the accessibility of small,
remote lakes to fishers and other recreational users but
might also affect the frequency or severity of winterkill
(Devito et al. 2000; Schindler 2001) and, therefore, the
dynamics of both predators and prey (Tonn et al. 2004;
Venturelli and Tonn 2005). Effective management of
these developing fisheries requires, in part, that we
understand how disturbance-mediated patterns in diet
and growth affect the dynamics of populations of
northern pike.
Methods
Experimental design.—Our experiment was con-
ducted in three small, shallow, naturally eutrophic
lakes in a remote region of the mixed-wood boreal
forest of nor theas t Albe rta (Fi gure 1) . The two
reference lakes in this study, R1 (103.5 ha in area, 8
m in maximum depth) and R2 (61.6 ha, 4.5 m), were
dominated by northern pike and yellow perch Perca
flavescens. The experimental lake (EXP; 13 ha, 5.2 m)
had been fishless for at least 6 years after a suspected
winterkill (W.M.T. and coworkers, unpublished data).
During summer 2000 (May–August), we conducted
monthly monitoring of (1) diet and growth of northern
pike (in the reference lakes only, details below) and (2)
abundance and biomass of macroinvertebrates in the
1.0–1.5-m depth zone of each lake (see Venturelli and
Tonn 2005 for details). In May 2001, we collected
northern pike (N ¼ 355; mean total length [TL] 6 SE ¼
587 6 2.5 mm; mean mass 6 SE ¼ 1,148 6 12 g)
from nearby Piche Lake (518 ha, 18 m), which also
contained the following species: yellow perch, walleye
Sander vitreus, white sucker Catostomus commersoni,
brook stickleback Culaea inconstans, and various
cyprinids; we then introduced northern pike from this
lake into EXP to achieve a biomass density of
approximately 35 kg/ha. Northern pike were individ-
ually tagged with plastic anch or ta gs. Sam pling
continued in the three study lakes throughout 2001
and 2002. To prevent winterkill of northern pike in
EXP, we visited the lake twice per month (December
2001–March 2002) to clear the ice of snow and aerate
the water with compressed air (Venturelli and Tonn
2005).
Stable isotope analysis.—Stable isotope analysis is a
means of describing the trophic structure of food webs
by comparing isotopic signatures of constituent
organisms (Post 2002). In this study, we used stable
isotopic ratios of ca rbon (
13
C/
12
C) and nitrogen
(
15
N/
14
N) to compare the trophic positions of northern
pike in EXP and the source lake.
Samples for SIA were collected in 2002 from EXP
(late July) and Piche Lake (early August). Lymnaeid
snails, amphipods (Gammarus lacustris and Hyallela
azteca), and erpobdellid leeches (hereafter, ‘‘ leeches’’ )
were handpicked or netted from littoral habitats and
kept alive for 24 h to allow for evacuation of gut
contents. We captured northern pike and yellow perch
with gill nets and hook and line. Blood was collected
from the caudal vein of adults. White muscle tissue was
FIGURE 1.—Map of Alberta, showing location of study lakes
(inset): Reference Lake 1 (R1; 55820
0
N, 111864
0
W); Refer-
ence Lake 2 (R2; 55815
0
N, 111876
0
W); Experimental Lake
(EXP; 55805
0
N, 111865
0
W); and Piche Lake (source [S] lake;
55803
0
N, 111860
0
W).
NORTHERN PIKE DIET AND GROWTH 1513
used in SIA of yellow perch and young-of-the-year
(age-0) northern pike. Samples were frozen in the field
and transported to the laboratory. We removed
inorganic car bon fro m tha wed ma croinver tebrate
samples by soaking them in 1 M HCl for 24 h (or
until bubbles no longer appeared). Each specimen was
then air dried for approximately 48 h, homogenized
with a mortar and pestle, weighed to 1.0 6 0.1 mg, and
sealed in a 5- 3 8-mm tin capsule. We used composite,
taxon-within-lake samples when individual specimens
did not meet the target mass.
Up to five replicate samples of each taxon were
analyzed at the National Water Research Institute,
Saskatoon, by means of an online, continuous-flow,
isotope-ratio mass spectrometer calibrated to reference
standards (Pee Dee belemnite limestone and atmo-
spheric nitrogen). Isotope ratios are expressed in delta
(d) notation as parts per thousand (%) deviation from
standard with the formula
d
13
Cord
15
N ¼½ðR
sample
R
standard
Þ=R
standard
3 1; 000;
where R ¼
13
C/
12
Cor
15
N/
14
N (Gearing 1991).
Trophic position (k) of northern pike in Piche Lake
was calculated as
k
p
¼ k
s
þðd
15
N
p
d
15
N
s
Þ=3:4;
following Post (2002), where subscripts p and s refer to
northern pike and a baseline invertebrate herbivore
(here, snails), respectively . We calculated trophic
position of northern pike in EXP by means of a
modified version of this equation (a two-end-member
mixing model; Post 2002) to account for ambiguity in
the baseline nitrogen in this system, vegetative (snails)
versus detrital (amphipods).
Stomach content analysis.—We used multimesh gill
nets (45.5 m long 3 1.5 m deep; bar mesh sizes of 6.25,
8, 10, 12.5, 16.5, 22, 25, 30, 33, 43, 50, 60, and 75
mm) to collect up to 20 stomach samples per month
(May–August of 2000–2002) from northern pike in the
littoral zones of R1 and R2. Samples were collected in
late morning or early afternoon and limited to recently
captured northern pike to minimize errors associated
with the digestion or regurgitation of prey. Using a
nonlethal flushing technique similar to Light et al.
(1983), a maximum of 20 stomach samples per month
were also obtained from adult northern pike angled in
EXP (2001 and 2002). The better than 97% efficiency
of prey removal reported by Light et al. (1983) was
supported in this study by preliminary data on northern
pike from the reference lakes. Age-0 northern pike
were captured in EXP in 2002 with overnight and
daytime sets of Gee minnow traps and fyke nets. Due
to the difficulty in applying the flushing technique to
small fish (Hyslop 1980), age-0 northern pike were
sacrificed and their stomachs dissected. Diet samples
were preserved in a 10% solution of formalin, and prey
were later identified to the lowest practical taxonomic
level. Each taxon was then enumerated, individuals
were measured, and their dry mass was estimated by
means of length–dry mass regressions (see Venturelli
and Tonn 2005 for details).
Stomach content analyses were limited to those prey
taxa that occurred in more than one stomach sample
from any lake over the duration of the study. Frequency
of occurrence and percentage composition of prey taxa
by number and dry mass were used to determine the
relative importance (George and Hadley 1979) of prey
taxa to adult (.450 mm TL) and juvenile (,330 mm
TL) northern pike in each lake and year. Relative
importance for R1 and R2 was averaged further to
obtain overall reference means against which to
compare results from EXP.
The average energy content (EC) of adult and
juvenile diets was calculated as
EC ¼
X
n
j¼1
ðm
j
3 e
j
Þ;
where m
j
¼the proportion, by dry mass, of prey type j in
the diet and e
j
¼ the energy density of prey type j (Table
1). To estimate the potential for within-lake competition
between adults and juveniles and to compare diets
between lakes, we measured diet overlap by means of
the simplified Morisita index (C
H
; Krebs 1989):
C
H
¼ ð2 3
X
n
i¼1
p
ij
3 p
ik
Þ=ð
X
n
i¼1
p
2
ij
þ
X
n
i¼1
p
2
ik
Þ;
TABLE 1.—Caloric density of prey taxa consumed by adult
and juvenile northern pike in northeast Alberta lakes. Values
represent the mean of a range in some cases. The caloric
density of fish prey was calculated by averaging values for
adult and juvenile yellow perch.
Prey taxon Energy density (cal/mg dry mass)
Hirudinids 5.67
a
Snails 4.34
a
Amphipods 4.07
a
Ephemeropterans 5.69
a
Anisopterans 4.07
b
Zygopterans 5.35
b
Hemipterans 4.82
b
Trichopterans 5.00
b
Coleopterans 5.37
b
Dipterans 4.93
a
Cladocerans 5.46
a
Anurans 1.64
b
Fishes 4.86
a
a
Hanson et al. (1997).
b
Cummins and Wuychuck (1971).
1514 VENTURELLI AND TONN
where p
ij
and p
ik
¼ the proportion of prey type i in diet j
and k, respectively. We estimated diet breadth (DB;
macroinvertebrate prey only) in the experimental and
reference lakes as
DB ¼
X
n
j¼1
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
ðp
j
3 a
j
Þ
q
;
where p
j
¼the proportion of prey type j in the diet and a
j
¼ the proportion of prey type j in the environment
(Krebs 1989). The frequencies of empty adult and
juvenile s tomachs were averag ed for each year
according to lake type (EXP or reference). We
employed the two-tailed Fisher’s exact test to test the
null hypothesis that empty stomachs were equally
frequent in EXP and the reference lakes.
Estimated and observed growth of northern pike.—
Cleithra collected from up to 100 northern pike per lake
in July of each year (2000–2002) from gill-net surveys
conducted in R1 and R2 were used by Dr. Peter Aku
(Alberta Conservation Association) to develop lake-
specific regression equations relating length of cleithra
(anterior radius [AR]) to TL of northern pike. For R1,
TL ¼ 10:627 3 AR 0:159ðR
2
¼ 0:9831; n ¼ 141Þ;
and for R2,
TL ¼ 10:842 3 AR 0:472ðR
2
¼ 0:9792; n ¼ 111Þ:
Radius length was measured from the origin to the
posterior edge of each annulus (A) along the AR with a
digi tal caliper interfaced with a computer. Back-
calculated length at age for individual fish was
obtained by substituting A for AR in the regression
equations. We combined these data with similar data
from R1 and R2 in 1996 and 1997 (P. Aku and
W.M.T., unpublished data) to determine a length-at-
age profile for the reference lakes. For each age in this
profile, we then calculated the percentage increase in
TL. Age-specific growth rates were similarly devel-
oped from approximately 300 northern pike from three
allopatric populations sampled in this region in 1996
and 1997 (P. Aku and W.M.T., unpublished data).
Based on the length-at-age profile of northern pike
from the reference lakes, we estimated that northern
pike introduced into EXP ranged in age from 4 to 8
years. Growth of these i ndividuals 1 year after
introduction was measured directly with recapture data
from May 2002 (n ¼ 54) and was expressed as
percentage increase in TL. We then compared annual
growth in EXP to the average growth increment of
northern pike of ages 4–8 in regional lakes with and
without prey fishes. Length at age 1 for juveniles in
EXP (measured in early July 2003) was similarly
compared with estimated length at age 1 for juveniles
in reference and allopatric lakes. Statistical tests were
not used in either comparison because values were
obtained with dissimilar methods (i.e., measured from
individuals in EXP, but estimated from populations in
other lakes).
Results
Diets of Northern Pike
Based on SIA, adult northern pike in Piche Lake
were positioned at the top of the food web (Figure 2a).
The long-term diet of these northern pike consisted of
yellow perch and, given their low d
13
C signature,
probably other unsampled pelagic fishes (see France
1995). This diet corresponded to a trophic position of
4.7. In EXP, isotopic signatures of adult and age-0
northern pike were similar (Figure 2b) and suggested
that these northern pike were also the top predators in
this food web. The trophic position of northern pike in
EXP was estimated at only 3.9.
Stomach content analysis identified leeches (Erpob-
FIGURE 2.—Scatterplots of stable carbon (d
13
C; %) and
stable nitrogen (d
15
N; %) isotopic signatures of northern pike,
yellow perch, and macroinvertebrates in northeast Alberta
lakes, (a) Piche Lake and (b) the experimental lake, sampled
during late July and early August 2002.
NORTHERN PIKE DIET AND GROWTH 1515
dellidae) as the dominant prey of adult northern pike
from EXP in 2001 and 2002 (Figure 3). Of secondary
importance was the amphipod G. lacustris, along with
coleopterans and dipterans. Although G. lacustris
became more important (and leeches less so) in 2002,
both EC (Table 2) and overlap (Table 3) of the 2001
and 2002 diets were high. In 2002, diets of age-0
northern pike in EXP were dominated by G. lacustris;
secondary prey were zygopterans, chironomids, and
two families of leeches (Glossiphoniidae and Erpob-
dellidae; Figure 4). These diets contained less energy
per unit mass and were broader than diets of adults
(Table 2). Overlap of juvenile and adult diets in EXP in
2002 was moderate (Table 3).
The amphipod, G. lacustris, was the dominant prey
in the reference lakes; fishes, leeches, and larval
trichopterans were of secondary importance (Figure
3). This diet contrasted sharply with that of adults in
EXP in 2001, but less so in EXP in 2002 (Table 3).
Diets of adult northern pike from the reference lakes
contained consistently less energy but were broader
than those from EXP, although the latter broadened
theirdietin2002(Table2).Themeanannual
frequency of empty stomachs of adult northern pike
in EXP (13 of 43) was not significantly different than
that in the reference lakes (1 of 9; Fisher’s exact test: P
¼ 0.415). Diets of juveniles from the reference lakes
were similar to reference lake adults and EXP juveniles
in terms of composition of prey (Figure 4), EC and DB
(Table 2), and overlap (Table 3). The mean annual
frequency of empty stomachs of juvenile northern pike
in EXP (0 of 13) and the reference lakes (2 of 13) did
not differ (P ¼ 0.481).
Growth of Northern Pike
Annual percentage increase in TL of adult northern
pike in boreal Alberta lakes that contained prey fishes
was estimated from back-calculated length-at-age data
as being nearly 2.5 times as great as in regional
allopatric lakes (Figure 5a). Observed growth of adults
in EXP was only slightly higher than back-calculated
growth in allopatric lakes (5% versus 4%). Back-
calculated length at age of juvenile northern pike after
1 year in lakes with prey fishes (220 mm) was greater
than that in lakes without prey fishes (160 mm; Figure
5b). The largest first-year growth increment, however,
was the observed growth among juveniles in EXP,
which increased in length to almost 320 mm.
Discussion
Dietary Responses of Northern Pike to Invertebrate
Prey
The trophic level and d
13
C and d
15
N signatures of
the northern pike in Piche Lake were similar to those
FIGURE 3.—Relative importance of prey taxa in diets of
adult northern pike (.450 mm TL) collected from northeast
Alberta lakes (see Figure 1): (a) two reference lakes (average
of years and lakes), (b) the experimental lake in 2001, and (c)
the experimental lake in 2002. Sample size information
appears in Table 3. Taxa include anisopterans (Ani),
Chaoborus spp. (Cha), chironomids (Chi), coleopterans
(Col), dipteran pupae (Dip), erpobdellid leeches (Erp), fishes
(Fsh), gammarids (Gam), hemipterans (Hem), snails (Sna),
trichopterans (Tri), and ‘‘zygopterans (Zyg). Other (Oth)
indicates prey taxa with a relative importance less than 2.00
(reference lakes: adult frogs, anisopterans, chironomids,
dipteran pupae, and zygopterans; experimental lake 2001:
chironomids, dipteran pupae, and trichopterans; experimental
lake 2002: adult frogs, Chaoborus spp., and larval frogs).
1516
VENTURELLI AND TONN
reported for other large, piscivorous northern pike in
boreal Alberta (Beaudoin et al. 1999, 2001; Paszkow-
ski et al. 2004). This trophic level was, however, 0.8
positions higher than that of the northern pike from
Piche Lake after their introduction into the fishless
EXP. This change is consistent with results of Vander
Zanden et al. (1997) and Beaudoin et al. (2001), which
suggest that invertivorous populations of northern pike
feed 0.5–1.5 trophic positions below piscivorous
conspecifics (our calculations). Similarly, lake trout
Salvelinus namaycush dropped 0.6 trophic positions
over 10 years as they became planktivorous in response
to introduced competitors (Vander Zanden et al. 1999).
A potential source of error in our estimate of trophic
change was a difference in sources of energy as a
function of lake size. As lake size increases, external
(littoral) production becomes less important and
internal (pelagic) production more so (France 1995;
Post 2002). The lighter d
13
C signature of northern pike
relative to littoral consumers in Piche Lake is typical of
large lakes and suggests an additional unsampled
source of pelagic carbon. Since the d
15
N of primary
consumers increases with decreasing d
13
C (Vander
Zanden and Rasmussen 1999), our use of a littoral
d
15
N baseline might have overestimated the trophic
position of northern pike in Piche Lake. To correct for
this, we assumed a 4.6% d
13
C and þ1.6% d
15
N
difference for a pelagic baseline relative to a littoral
baseline (Vander Zanden and Rasmussen 1999) and
assumed that both habitats were represented equally in
diets of northern pike (but see Vadeboncoeur et al.
2002). We incorporated this pelagic baseline into our
estimate of trophic position by means of a two-end-
member mixing model (Post 2002). Results suggest
that northern pike in EXP might have dropped only 0.3
positions. On the other hand, rates of isotopic turnover
in the blood and muscle of fishes can be as long as 450
d (Herzka 2005) and are highly dependent on growth
(Harvey et al. 2002). Given that we sampled adult
northern pike in EXP roughly 400 d after introduction,
0.3 might represent a conservative estimate of change
in trophic position. Regardless, a 0.3–0.8 change is
substantial given the duration of our experiment, and
suggests that isotopic signatures of adults can respond
relatively rapidly to dramatic changes in diet, as would
result from disturbance events.
According to SCA, adult northern pike adjusted to
allopatry by preying heavily on large leeches. Leeches
are not usually important in diets of northern pike
(Chapman and Mackay 1990; Sammons et al. 1994;
Beaudoin et al. 1999, 2001), probably owing to a
combination of their small size relative to prey fishes
and low availability in systems with fish. Leeches,
however, represent a large, easily digested, high-energy
alternative to other macroinvertebrates (Table 1). Given
that these leeches were abundant in EXP (Venturelli
and Tonn 2005), probably owing to the prolonged
absence of fish predators, the importance of leeches in
TABLE 2.—Mean sample size, total length (TL; mm), and diet characteristics of adult (.450 mm TL) and juvenile (,330 mm
TL) northern pike from the two reference lakes (REF; average of years [2001–2002] and lakes) and the experimental lake (EXP)
in northeast Alberta.
Lake
Sample size
(mean/year)
TL
Diet energy
(cal/mg dry mass)
Frequency of empty
stomachs/year Diet breadthMean 6 SE Range
Adults
REF 9 516 6 18.41 451–694 4.34 1 0.81
EXP (2001) 36 615 6 11.43 490–798 5.55 9 0.30
EXP (2002) 50 619 6 6.57 534–705 5.30 17 0.45
Juveniles
REF 13 273 6 6.36 147–329 4.34 2 0.90
EXP (2002) 13 123 6 11.23 73–195 4.85 0 0.79
TABLE 3.—Matrix of dietary overlap (Morisita index) between adult (.450 mm) and juvenile (,330 mm) northern pike from
two reference lakes (REF; average of years [2001–2002] and lakes) and the experimental lake (EXP) in northeast Alberta.
Life stage Lake
Adults Juveniles
REF EXP (2001) EXP (2002) REF EXP (2002)
Adults REF 1.000
EXP (2001) 0.23 1.000
EXP (2002) 0.40 0.93 1.000
Juveniles REF 0.95 0.12 0.21 1.000
EXP (2002) 0.84 0.24 0.44 0.91 1.000
NORTHERN PIKE DIET AND GROWTH 1517
diets of northern pike in 2001 and 2002 further
indicates that the stocked population adjusted rapidly
to allopatry with a diet that optimized energy intake per
unit time (Gerking 1994).
Examining the diet of northern pike in the two
reference lakes (both containing prey fishes) was
intended as a comparison of foraging strategies of
piscivorous and invertivorous northern pike. Surpris-
ingly, however, SCA indicated that adult northern pike
in R1 and R2 were largely invertivorous; they preyed
mostly on G. lacustris but also consumed other
macroinvertebrates and some fish. Diet data from
reference lakes were, nonetheless, valuable in evaluat-
ing the dietary response of northern pike in EXP. For
example, given that predators are predicted to become
specialists when high-ranking prey are abundant
(Schoener 1971; Werner and Hall 1974), the narrow
breadth of diet of adult northern pike in EXP relative to
the reference lakes further indicated that leeches were a
FIGURE 4.—Relative importance of prey taxa in diets of
juvenile northern pike (,330 mm TL) collected f rom
northeast Alberta lakes (see Figure 1): (a) two reference lakes
(average of years and lakes) and (b) the experimental lake in
2002. Sample size information appears in Table 3. Taxa
include anisopterans (Ani), Chaoborus spp. (Cha), chirono-
mids (Chi), cladocerans (Cla), coleopterans (Col), dipteran
pupae (Dip), ephemeropterans (Eph), erpobdellid leeches
(Erp), fishes (Fsh), gammarids (Gam), glossiphoniid leeches
(Glo), larval frogs (Laf), trichopterans (Tri), and zygopterans
(Zyg). Other (Oth) i ndicates prey taxa with a relative
importance less than 2.00 (reference lakes: coleopterans,
ephemeropterans, snails, and zygopterans).
FIGURE 5.—Observed (experimental lake; EXP) and back-
calculated growth in TL of (a) 4–8-year-old adult (.450 mm)
northern pike (mean percentage increase in TL) and (b)
juvenile northern pike (length at age 1). Growth is from
individuals for EXP, populations for regional lakes, and lake–
years for reference lakes (REF). Back-calculated growth in
regional lakes and REF includes data from P. Aku and W. M.
Tonn (unpublished; see Methods for details). Standard error
bars are for illustrative purposes only. Data were not used in
statistical analyses.
1518
VENTURELLI AND TONN
high-ranking, abundant prey in EXP. The relatively
broad diets of northern pike in the reference lakes
suggests that leeches in these systems were relatively
unavailable, probably a result of predation. Indeed,
diets of northern pike in EXP in 2002 began to broaden
and converge upon the reference lake diet in response
to a reduced abund ance and biomass of leeches
(Venturelli and Tonn 2005).
Interestingly, the frequency of northern pike with
empty stomachs in the reference lakes was not
significantly different from that in EXP, but was more
than half of that observed previously in these systems
(Beaudoin et al. 1999). The proportion of empty
stomachs in a population of northern pike is inversely
related to the importance of invertivory (Diana 1979;
Chapman et al. 1989; Beaudoin et al. 1999), as
northern pike must consume small invertebrate prey
more frequently to meet their energy requirements
(Chapman et al. 1989). The prevalence of invertivory
and the correspo nding low frequ ency of empty
stomachs among adult northern pike in both reference
lakes suggest that the availability of fish prey was
limited. Although age-0 yellow perch appeared to be
abundant (P.A.V., unpublished data), this might have
been only a recent phenomenon because of winterkill
events in R1 (‘‘ L800’’ in Tonn et al. 2004) and R2
(W.M.T. and coworkers, unpublished data). Alterna-
tively, areas of dense macrophytes in these systems
might have provided refuge for yellow perch while
supplying adult northern pike with an abundance of
invertebrates (Diehl 1993).
Unlike adult northern pike, age-0 northern pike in
EXP did not specialize on leeches but exhibited a more
diverse diet that included the amphipod H. azteca,
zygopterans, and glossiphoniid leeches. This diet was,
however, similar to that of juveniles in another nearby
allopatric lake (C
H
¼ 0.9; Beaudoin et al. 1999; our
calculation) and our reference lakes. Juveniles in the
reference lakes might not have consumed more leeches
and fishes for the same reasons as adult northern pike
(see above). Equally plausible is that age-0 northern
pike were selecting from a larger range of prey types
and sizes than adults because (1) invertebrate taxa are
more likely to be detected by age-0 northern pike, (2)
net energy gain for small predators tends to vary less
with size of prey (Mittelbach 1981), and (3) age-0
northern pike selected shallow, densely vegetated (and
invertebra te-rich) habitats to avoid cannibalism
(Grimm and Klinge 1996).
Growth Response of Northern Pike to Invertebrate
Prey
Based on EC, diets of adult northern pike in EXP in
2001 and 2002 should have produced more growth
than the reference diet, which consisted primarily of G.
lacustris and to a less er extent, fish and other
macroinvertebrates. However, the observed grow th
rate of adult northern pike in EXP was low relative
to the reference lakes, suggesting that the sudden
switch from piscivory to invertivory had a negative
effect on growth and that invertivory is not ideal.
Indeed, the annual increase in TL of adult northern pike
in the reference lakes was about 10%, which compares
favorably with a mean of 8% using data from 82
circumpolar water bodies on three continents (Cassel-
man 1996; our calculation). In contrast, annual growth
of adults was 4% in our regional allopatric lakes and
5% in EXP . Stunted northern pike have been observed
after a prolonged absence of suitably sized prey
(Goeman and Spencer 1992; Margenau 1995); our
results suggest that invertivory compromises growth of
adults in as little as 1 year.
Given the prevalence of invertivory in the reference
lakes, it is curious that their adult northern pike
exhibited growth that was mor e indicative of a
piscivorous diet. Since piscivory is associated with a
relatively low percent daily ration and perhaps lower
costs associated with decreased activity (Pazzia et al.
2002), the n et en ergy gained by consuming the
occasional prey fish might be greater than expected
from a simple measure of the EC of a diet.
Furthermore, piscivory was more common in these
populations before recent winterkills (Beaudoin et al.
1999; Tonn et al. 2004; W.M.T. and coworkers,
unpublished data); thus, our estimated growth from
back-calculated length-at-age profiles would have
partly reflected this e arlier, mor e-pis civorous diet
(P.A.V., unpublished data). In addition, northern pike
in these lakes might have preyed more heavily on
fishes during the fall and winter, when densities of
macrophytes (and, therefore, prey refugia) would be
low relative to our sampling period (May–August).
Growth of northern pike during winter is possible
(Diana and Mackay 1979), but the relative importance
of prey fishes in diets during this period has yet to be
determined.
Similar to adults, estimated annual growth of
juveniles in the reference lakes (about 220 mm) was
comparable with the circumpolar average (about 200
mm; Casselman 1996), while the relatively slow
growth in regional allopatric lakes suggests that
elevated rates of growth are associated with an
ontogenetic transition to piscivory (Hunt and Carbine
1951). Surprisingly, observed growth in EXP exceeded
both the circumpolar average and reference estimates.
The exceptional growth of age-0 northern pike in EXP
might reflect a lower degree of intraspecific competi-
NORTHERN PIKE DIET AND GROWTH 1519
tion relative to the reference lakes, a higher degree of
cannibalism than was indicated by our data, or both.
Conclusion
Winterkill is common in Alberta’s Boreal Plains
lakes (Danylchuk and Tonn 2003), and the sudden
reduction or elimination of prey fishes probably
contributes to the prevalence of invertivory by northern
pike in these systems (Beaudoin et al. 1999). After their
introduction into EXP, northern pike dropped in
trophic position and specialized on leeches, which
were abundant, re latively large, energy-ri ch prey.
Foraging lower in the food web can mean higher
energetic costs and slower rates of growth (Pazzia et al.
2002), however. Invertivory was more than adequate to
meet the energy requirements for juvenile growth but
limited the growth of adults. Therefore, disturbance-
induced invertivory will probably stunt populations in
small, boreal lakes by failing to support continued
growth of adults, despite high levels of primary
production in these habitats. Higher competition with
juvenile northern pike for a shared food resource
probably exacerbates the stunting of adults (Diana
1987). Data from the regional allopatric lakes suggest-
ed that such populations might remain chronically
stunted, perhaps as a result of a simple negative
feedback in which maximum achievable size is eroded
by an increasing scarcity of preferred invertebrate prey.
Chronic stunting as a result of competition for food has
even been observed in dense populations of piscivo-
rous northern pike and is difficult to reverse (Goeman
and Spencer 1992; Margenau 1995).
Effects of food web disturbances, such as winterkill,
on growth rates of northern pike can be complex. By
reducing the local population of invertivorous fish,
winterkill can eliminate optimal (fish) prey but can also
allow preferred macroinvertebrate prey taxa to recover
from predation (Tonn et al. 2004). These opposing
effects demonstrate the need for further research into
the relationship between invertivory and growth and
how this relationship varies with prolonged or periodic
disturbance and allopatry. For example, the paucity of
intercohort and intracohort cannibalism among inver-
tivorous northern pike in small, boreal lakes (Beaudoin
et al. 1999; this study) is inconsistent with data from
other systems (Smith and Reay 1991). Research is also
needed to address effects of invertivory and stunting on
the reproductive ecology and life history of northern
pike (Ylikarjula et al. 1999; Claessen et al. 2002).
Populations of northern pike in these small, once-
remote lakes were of little concern to managers 30
years ago. The increased (and increasing) prevalence of
local (e.g., resource exploration and extraction) and
regional (e.g., climate) disturbances (Schindler 2001;
Timoney 2003) has made effec tive management
strategies necessary. Developing and implementing
strategies that complement a lake’s natural disturbance
regime remains a challenge, however, because natural
disturbances are by nature unpredictable in both time
and space and because the long-term population
dynamics of northern pike in these systems have yet
to be determined. Until these issues are addressed, we
recommend that resource managers err on the side of
caution when implementing policies that will affect
directly populations of northern pike or their prey or
that will otherwise alter a lake’s natural disturbance
regime via changes in land use (Tonn et al. 2003) or the
quality and quantity of lake water (Danylchuk and
Tonn 2003).
Acknowledgments
We gratefully acknowledge S. Boss, I. Ludwig, I.
Lusebrink, K. Ostermann, R. Popowich, and numerous
volunteers for their hard work in t he field and
laboratory. Thanks also to K. Norris, University of
Alberta, for sampling juveniles in 2003, and P. Aku,
Alberta C onservation Association, for fastidi ousl y
aging our northern pike. P. Aku, D. Hayes, C.
Paszkowski, G. Scrimgeour, A. Wolfe, and anonymous
reviewers provided insightful comments on earlier
versions of this manuscript. Figure 1 was created with
help from D. Stoeher. In-kind support was provided
unselfishly by Lac La Biche District Fisheries manager
C. Davis and by staff at the Meanook Biological
Research Station, University of Alberta. Funding was
provided by grants and scholarships to P.A.V. from
Alberta Sport, Recreation, Parks and Wildlife Founda-
tion, Tran sCanada Pipelines, Alberta Conservation
Association, Canadian Circumpolar Institute, Mountain
Equipment Cooperative, Natural Sciences and Engi-
neering Research Council of Canada (NSERC),
Alberta–Pacific Forest Industries, and scholarships
through the Department of Biological Sciences,
University of Alberta, and the Government of Alberta.
Additional support was provided by an NSERC
research grant to W.M.T.
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