J. Great Lakes Res. 33:156–169
Internat. Assoc. Great Lakes Res., 2007
Morphological and Ecological Differences Between Shallow- and
Deep-water Lake Trout in Lake Mistassini, Quebec
Mara S. Zimmerman1,*, Charles C. Krueger2, and Randy L. Eshenroder2
1Department
of Fisheries and Wildlife
Michigan State University
Lansing, Michigan 48823
2Great
Lakes Fishery Commission
2100 Commonwealth Blvd, Suite 100
Ann Arbor, Michigan 48105
ABSTRACT. Lake trout (Salvelinus namaycush) in Lake Mistassini, Quebec, were investigated to
determine whether they resembled the lean and siscowet morphotypes of Lake Superior and Great Slave
Lake. Lake trout caught in deep water were predicted to resemble the siscowet morphotype and to be better adapted for vertical migration (i.e., low percent buoyancy) than those caught in shallow water. The
research objectives were to 1) identify groups based on shape, and 2) determine whether shape was associated with other morphological traits (fin length, buoyancy, color), ecology (habitat depth, diet), and life
history (size at adulthood). Eighty-five lake trout were collected from three depth zones. At least two phenotypes exist in Lake Mistassini. A shallow-water form (< 50-m depth), identified by its streamlined
shape, was dark in color and high in percent buoyancy. A deep-water form (> 50-m depth), identified by
a deep anterior-body profile, was light in color and lower in percent buoyancy than the shallow-water
form. Absolute buoyancies were relatively high in both forms; therefore, the deep-water form did not
appear well-adapted for vertical migration. Opossum shrimp (Mysis relicta) were more frequent and
abundant in stomachs of deep-bodied trout. All deep-bodied trout (minimum 32-cm SL) had reached
adulthood, whereas immature streamlined individuals were as long as 49 cm in SL. The deep-bodied form
resembled humper lake trout, a lesser-known third morphotype from Lake Superior. A humper-like morphotype in Lake Mistassini, and the apparent absence of a siscowet-like morphotype, challenges the previously-held hypothesis that humpers resulted from an introgression of leans and siscowets.
INDEX WORDS:
Adaptation, buoyancy regulation, humper, lean, phenotypic diversity, siscowet.
For example, lake trout (Salvelinus namaycush)
phenotypic diversity in the Laurentian Great Lakes
once included shallow- and deep-water forms in
Lakes Superior, Michigan, Huron, and Erie (Brown
et al. 1981, Goodier 1981, Krueger and Ihssen
1995). However, this diversity was lost from Lakes
Michigan, Huron, and Erie during the past century.
Some of the original phenotypic diversity remains
in Lake Superior (maximum depth ~400 m) in
forms known as lean, humper, and siscowet lake
trout (Khan and Qadri 1970, Lawrie and Rahrer
1973, Moore and Bronte 2001).
The origin and maintenance of lake trout phenotypic diversity has been difficult to investigate due
to the loss of diversity from most of the Laurentian
Great Lakes and the highly disturbed nature of remaining communities. Therefore, recent lake trout
INTRODUCTION
An abundance of available niches is hypothesized
to have facilitated morphological divergence in fish
species colonizing recently deglaciated lakes (Skulason and Smith 1995, Smith and Skulason 1996).
In at least eight fish families, resource polymorphism is attributed to divergent selection in benthic
and pelagic habitats (Robinson and Wilson 1994,
Smith and Skulason 1996). A less-recognized ecological variable, habitat depth, is also associated
with the radiation of freshwater fishes (Eshenroder
et al. 1999, Turgeon et al. 1999, Power et al. 2005).
*Corresponding
author. E-mail: [email protected]
Address correspondence to Great Lakes Fishery Commission, 2100
Commonwealth Blvd., Suite 100, Ann Arbor, MI 48105-1563
156
Phenotypic Diversity of Lake Trout in Lake Mistassini
studies have been conducted on other large, deep
North American lakes. Descriptions of lake trout
communities in Great Bear (maximum depth ~450
m) and Great Slave (maximum depth ~600 m) lakes
have provided a broader perspective on the association of lake trout phenotypes with ecological variables such as habitat depth. In Great Slave Lake, for
example, a siscowet-like trout with high-fat-content
tissue recently was caught in deep-water habitats
more than 50 m in depth (Zimmerman et al. 2006).
In Great Bear Lake, deep-water forms have not
been identified; however, shallow-water trout are
exceptionally diverse in their morphology (Blackie
et al. 2003, Alfonso 2004). Further, inter-lake comparisons of large, deep lakes would provide a better
understanding of lake trout phenotypic diversity
and its association with deep-water habitat.
The siscowet phenotype from Lake Superior has
high-lipid tissue (Eschmeyer and Phillips 1965),
which may be an adaptation for buoyancy regulation in deep-water habitats (Thurston 1962, Henderson and Anderson 2002). The compressed swim
bladder of a vertically migrating fish, when the fish
has descended, is ineffective at regulating buoyancy
(Alexander 1972, 1993). High-lipid content lowers
the density of body tissue in water and, consequently, minimizes the energetic costs of swimming
with a compressed swim bladder (Henderson and
Anderson 2002). Diel vertical migrations have been
observed in siscowet predators (Hrabik et al. 2006,
Jensen et al. 2006) as well as in deep-water lacustrine prey such as bloater Coregonus hoyi (Eshenroder et al. 1998, TeWinkel and Fleischer 1999) and
opossum shrimp Mysis relicta (Beeton 1960, Bowers 1988). The ubiquity of a siscowet-like phenotype in large, deep North American lakes would
suggest that this form is best adapted to deep-water
living and to foraging on vertically migrating prey
such as deep-water coregonines.
A second deep-water form, the humper trout, is
far less abundant than siscowets in Lake Superior
(Peck 1975). Humpers have been considered to be
a “form” (Eschmeyer and Phillips 1965) or a “morphological variant” (Lawrie and Rahrer 1973, Burnham-Curtis and Bronte 1996) of the lean trout and
have been hypothesized to have resulted from the
introgression of lean and siscowet trout during a period of fluctuating water levels (Burnham-Curtis
1993, Burnham-Curtis and Smith 1994). If humperlike trout occur as distinct populations outside Lake
Superior in the absence of the siscowet form, the
existing hypothesis on their origin would need to be
reconsidered.
157
The purpose of this study was to quantitatively
describe the phenotypic diversity of lake trout in
Lake Mistassini, a large, deep lake (maximum
depth > 150 m) in central Quebec. The abundance
of deep-water habitat in this lake was proportionally comparable to other lakes where lake trout phenotypic diversity was known; however, this lake
was smaller in surface area (2,150 km2) than Lake
Superior (82,100 km2) or Great Slave Lake (28,568
km2) (Beeton 1984). Two hypotheses were tested in
this study. First, lake trout occupying deep-water
habitat are predicted to have lower percent buoyancy, and thus be better adapted for vertical migration, than those occupying shallow-water habitat.
Second, deep-water forms, if they exist, will likely
resemble the shape and buoyancy of siscowet trout
from Lake Superior. The research objectives were
to 1) identify lake trout groups based on shape, and
2) determine whether lake trout shape was associated with other morphological traits (fin length,
buoyancy, color), ecology (habitat depth, diet), and
life history (size of adulthood).
MATERIAL AND METHODS
Study Site
Lake Mistassini (50º40′N 73º20′W) is the largest
natural lake (2,150 km2) in the Province of Quebec
(Fig. 1) and is located east of all other lakes where
coexisting lake trout morphotypes are known. The
lake has east and west arms separated by a long island chain. Each arm has steep, rocky shorelines
and abundant deep-water habitat (> 50-m depths).
The food web includes typical lake trout prey such
as opossum shrimp (Dadswell 1974), cisco Coregonus artedi, and shortjaw cisco C. zenithicus. Representative Coregonus specimens are held in the
University of Michigan Museum of Zoology Fish
Division (C. artedi Cat. No. 247005, C. zenithicus
Cat. No. 247006). Sport fishing in Lake Mistassini
is supported by abundant lake trout, brook trout (S.
fontinalis), walleye (Sander vitreus), and northern
pike (Esox lucius) populations. Additional human
impact is minimized by a provincial wildlife reserve that surrounds most of the lake (Fraser and
Bernatchez 2005).
Field Procedures
Lake trout were caught with gill-nets set in the
east and west arms of Lake Mistassini during August 2003 (Fig. 1). Gill-net mesh sizes ranged from
64-114-mm stretch measure. Of the 12 gill-net sets,
158
FIG. 1.
Zimmerman et al.
Location of 12 sites where lake trout were collected from Lake Mistassini, Quebec.
four were in water depths of 0-50 m, five in 50–100
m, and three in 100–150 m. Sets were overnight
and approximated a 24-hour soak time. Depth strata
were established based on the known depths of lake
trout forms in Lake Superior (Moore and Bronte
2001, Bronte et al. 2003). The data collected in the
field from each individual included a full-body photograph, air weight, water weight with swim bladder deflated (for estimating buoyancy), sex, and
reproductive state. Stomachs were collected and
their contents fixed in 10% formalin.
The lateral image of each lake trout was captured
in a full-body photograph as described in Zimmerman et al. (2006). Digital-image files were used to
quantify color, fin lengths, and body shape. Percent
buoyancy was measured as water weight divided by
air weight (Zimmerman et al. 2006). Each fish was
suspended from a Pesola spring scale (Jennings
1989) with a hook and weighed to the nearest gram
in air and then in water. Prior to measuring water
weight, any remaining swim-bladder gas was expelled through a longitudinal incision. The buoyancy measure accounted for the differences in soft
and hard tissues that affect the specific gravity of
lake trout tissue (Alexander 1972). As lipids have
lower specific gravity than water, tissue with high
lipid content will have a low percent buoyancy.
All trout were assessed for sex and reproductive
state. Juvenile trout had undeveloped (i.e., immature) gonads. Adult trout were those whose gonads
either were greatly enlarged or were in a so-called
resting state from a previous spawning event. Resting females had discernable though small (< 1.0
mm in diameter) ova, whereas immature females
(with which they could be confused) had ova discernable only under magnification. Resting-stage
Phenotypic Diversity of Lake Trout in Lake Mistassini
159
males had testes that were slightly enlarged,
whereas the entire length of the testis was undeveloped in immature fish.
Measures of Color, Fins, Shape, and Diet
Brightness, one measure of body coloration, was
quantified from each image using a 255-unit gray
scale (0 = black, 255 = white) and ImageJ v. 1.32
software (http://rsb.info.nih.gov/ij). Brightness was
averaged for six measures from each lake trout’s
lateral image (cheek, three dorsal, two ventral)
based on a 40 × 40 pixel square of each region.
Lake trout were excluded from color analysis if
their body coloration became mottled or bleached
after collection.
Fin-length measurements (Fig. 2a) were identical
to those used by Zimmerman et al. (2006) on lake
trout from Great Slave Lake; comparable measures
from Lake Superior were not available. Body shape
was measured using 16 landmarks and four semilandmarks (Fig. 2b). The 16 landmarks were consistent with lake trout studies on Great Slave Lake
(Zimmerman et al. 2006) and Lake Superior
(Moore and Bronte 2001). The four semi-landmarks
described the belly curvature at 20, 30, 40, and 50%
standard length (SL) (Sampson et al. 1996, Langerhans et al. 2003). Although semi-landmarks are not
homologous, and thus less valuable than landmarks
for shape comparisons (Zelditch et al. 2004), they
were included because they described a variable region between the pectoral and pelvic fins where homologous landmarks do not exist.
The landmark-based geometric morphometric
method was used to quantify body shape (Bookstein 1991, Zelditch et al. 2004). This method calculated shape variables from digitized coordinates
(Zimmerman et al. 2006). To better approximate
homology, semi-landmarks were further adjusted by
“sliding” along the contour defined by the four
semi-landmarks and two landmarks representing
standard length (1 and 10, Fig. 2b) (Zelditch et al.
2004). Sliding minimized the Euclidean distance
between corresponding semi-landmarks (Sampson
et al. 1996). Lake trout were excluded from the
analysis if fins were bent or broken or if the body
was bent or otherwise distorted in the photographs.
The x,y coordinates that captured fin length and
body shape were digitized using tpsDIG software
(http://life.bio.sunysb.edu/morph). Fin lengths were
calculated using TMorphGen software, shape variables were calculated using CoordGen software,
and semi-landmarks were adjusted using SemiLand
FIG. 2. Fin lengths (a) and landmarks (b) used
to compare lake trout from Lake Mistassini.
Length (a) was measured from the insertion point
to the tip of the first fin ray for the dorsal (1), anal
(3), pelvic (4), and pectoral (5) fins. Caudal fin (2)
was measured as the longest dorsal ray. Landmarks (b) were anterior tip of the snout (1), posterior tip of the maxilla (2), center of the eye (3), top
of the cranium (4), posterior of neurocranium
above top of opercle (5), anterior insertion of dorsal fin (6), posterior insertion of dorsal fin (7),
anterior insertion of adipose fin (8), dorsal insertion of caudal fin (9), midpoint of hypural plate
(10), ventral insertion of caudal fin (11), posterior
insertion of anal fin (12), anterior insertion of
anal fin (13), insertion point of pelvic fin (14),
insertion point of pectoral fin (15), and connection between gill covers (16), and 17-20 are semilandmarks (*) representing belly curvature at 20,
30, 40, and 50% of lake trout standard length.
software. TMorphGen, CoordGen, and SemiLand
are part of a series of Integrated Morphometric Programs (IMP) produced in MatLab6 (Mathworks
2000) and used for morphometric analysis
(http://www2.canisius.edu/~sheets/morphsoft.html).
Stomach data included prey identity and prey
abundance. Identification of diet items was made to
the lowest taxonomic level possible based on the
condition of partially digested prey. For the purpose
of analysis, prey were classified as terrestrial insect,
aquatic invertebrate, or fish. Fish were combined
160
Zimmerman et al.
into a single category for analysis because the digested state of most prey fish obscured an accurate
identification to the genera level and thus lowered
the sample size for statistical comparison.
Identification of Lake Trout Phenotype Groups
An unweighted-pair-group method with arithmetic mean (UPGMA) cluster analysis based on
shape variables was inspected for groups (Objective
1; MVSP v. 3.1, Kovach Computing Services 2003).
Prior to analysis, shape variables were adjusted to a
common size (using Standard6, a program in the
IMP series). Shape variables were partial warp
scores that have the correct number of degrees of
freedom for multivariate tests (Zelditch et al. 2004).
Groupings identified in the cluster analysis were
evaluated with a canonical variate analysis (CVA).
Robustness of the groups was evaluated with a jackknifing procedure that randomly removed 10% of
the sample, recalculated the canonical function, reassigned individuals to groups based on the recalculated function, and computed the rate of correctly
classified individuals over 500 trials (Nolte and
Sheets 2005). The CVA was performed using
CVAGen, a program in the IMP series.
Phenotypic Measures Associated with
Lake Trout Shape
Two approaches, univariate and multivariate,
were used to describe how shape was associated
with other phenotypic measures (Objective 2). The
univariate approach, through a series of parametric
and nonparametric tests, provided an empirical description of differences between identified shape
groups. The multivariate approach, a two-block partial-least-squares analysis (2B-PLS), identified
whether and how shape covaried with multiple
measures of phenotype (Rohlf and Corti 2000,
Ruber and Adams 2001).
Lake trout groups, identified in the cluster analysis based on shape measures, were tested for differences in buoyancy, coloration, fin lengths, capture
depth, diet, and reproductive maturity. These measures were selected because they were known to
differ among co-existing shallow- and deep-water
morphotypes in Lake Superior and Great Slave
Lake. An analysis of covariance (ANCOVA) tested
whether buoyancy and brightness differed between
groups. A multivariate analysis of covariance
(MANCOVA) tested whether fin lengths (dorsal,
caudal, anal, pelvic, and pectoral) differed between
groups. Group and sex were the explanatory factors
and standard length was the covariate in these
analyses. Fin and standard lengths were log10 transformed prior to analysis. Except where noted in the
results, models met the assumption of homogeneous slopes. Significant multivariate effects were
interpreted from standardized-canonical-function
coefficients derived from a discriminant function
analysis. A G-test of independence determined
whether lake trout groups differed in depth distribution and in the number of empty versus full stomachs. Separate G-tests for goodness-of-fit tested
whether the presence of terrestrial insect, aquatic
invertebrate, and fish prey differed between forms.
Separate Mann-Whitney U tests determined
whether the abundance of terrestrial insects, aquatic
invertebrates, and fish differed between groups. A
G-test of independence examined whether the distribution of juvenile and adult trout differed between groups, and a two-way analysis of variance
(ANOVA) tested whether size (SL) of adult lake
trout differed between groups or sexes.
Two two-block partial-least-squares analyses
were performed. The first analysis tested the covariation of shape with buoyancy, brightness, and
capture depth. The second analysis tested the covariation between shape and fin lengths. In both
analyses, Block 1 included shape variables standardized to a common centroid size. In the first
analysis, Block 2 included buoyancy, brightness,
and capture-depth measures. In the second analysis,
Block 2 included all five fin lengths. Block 2 measures were size-adjusted (except capture depth) and
standardized to a z-distribution. Size-adjusted measures were the residuals from each measure regressed on SL (fin lengths and SL were log 10
transformed prior to the regression). The 2B-PLS
calculated vector pairs that best explained the covariation between the two blocks and that were described based on the weighting of each contributing
variable (similar to interpretation of principal component axes). Permutation tests determined whether
the identified vector pairs explained more covariance between blocks than expected by chance and
whether the existing correlations within identified
vector pairs were less likely to occur than random.
The 2B-PLS analysis was conducted with PLSMaker, a program in the IMP series.
Unless specifically mentioned, statistical analyses were performed using SPSS 12.0 (SPSS 2003).
Results were considered significant when p < 0.05.
Phenotypic Diversity of Lake Trout in Lake Mistassini
161
FIG. 3. Dendrogram produced by a UPGMA cluster analysis based on shape
variables calculated for Lake Mistassini lake trout. Each terminal line represents
an individual fish. Outlines were drawn from vector plots of the first canonical
axis, which discriminated between Groups 1 and 2. Shapes were standardized to 42cm standard length. Images are representative lake trout from each group.
RESULTS
A total of 85 lake trout were analyzed from the
12 gill-nets set in the three depth zones (Mean, 10
trout/set). Forty-nine lake trout, ranging in length
from 28 to 71-cm SL (Mean ± 1 SD, 45.2 ± 6.9),
were caught in the 0-50-m depth stratum. Twentyseven lake trout, ranging in length from 34 to 45cm SL (Mean ± 1 SD, 39.6 ± 3.1), were caught in
the 50-100-m depth stratum. In the 100-150-m
depth stratum, nine trout were caught and ranged in
length from 32 to 43-cm SL (Mean ± 1 SD, 37.9 ±
3.9). Two individuals were length outliers (> 3 standard deviations from the mean) and at least 12-cm
longer than any other trout collected. These individuals were removed from the statistical analyses because they biased the size-adjustment procedure
and consequently affected other results of this
study.
Groupings of Lake Trout Phenotypes
Two major groups were identified from the
UPGMA cluster analysis (Fig. 3). Group 1 had a
streamlined body profile, a long upper jaw, and an
eye positioned centrally on the head. Group 2 had a
deep anterior-body profile, a narrow caudal peduncle, a short upper jaw, and an eye positioned dorsally high on the head (Canonical variate 1: λ =
0.18, χ2 = 109, df = 36, P < 0.001). The canonical
function discriminating the groups correctly classified 100% of individuals originally assigned to
Group 1 and 98% of those originally assigned to
Zimmerman et al.
162
Group 2. Eight-six percent of individuals were correctly classified when a jack-knifing procedure was
applied to the canonical function. Representatives
of the deep-bodied form were placed in the University of Michigan Museum of Zoology (Cat. No.
247004).
Phenotypic Measures Associated with
Lake Trout Shape
Brightness differed between forms (F1,47 = 19.6,
P < 0.001). On average, a 42-cm SL lake trout of
the deep-bodied (Group 2) form was 45% lighter in
color than the streamlined (Group 1) form (Table
1). Brightness did not differ between males and females in either group (F1,47 = 0.6, P = 0.4), and the
interaction between sex and form was not significant (F1,47 = 0.8, P = 0.4). Within each form, body
coloration darkened with length (F1,47 = 13.3, P =
0.001).
Buoyancy differed between forms (F1,51 = 4.8, P
= 0.03). However, this difference was slight and the
range of buoyancies represented in each group
overlapped substantially (Group 1 = 4.2–7.1%,
Group 2 = 4.5–6.5%). On average, a 42-cm lake
trout of the deep-bodied form was just 0.3% lighter
(i.e., % buoyancy was lower) than a similar-sized
streamlined form (Table 1). Buoyancy of males and
females did not differ in either group (F1,51 = 2.1, P
= 0.2), and the interaction between sex and form
was not significant (F 1,51 = 0.7, P = 0.9). Within
each form, percent buoyancy increased with length
(F1,51 = 11.4, P = 0.001).
Size-adjusted fin lengths differed between the
two lake trout groups (F5,62 = 4.5, P = 0.002) and
sex (F5,62 = 4.6, P = 0.001). The function that discriminated between forms was heavily weighted by
TABLE 1. Phenotypic differences between the
streamlined (Group 1) and deep-bodied (Group 2)
forms of lake trout in Lake Mistassini. Brightness,
buoyancy, caudal fin, and anal fin measures are
calculated for a 42-cm SL lake trout. Data are
means (± 1 S.E.).
Measure
Brightness
Buoyancy
Caudal fin
Anal fin
Depth (m)
Adult size (cm SL)
Group 1
(streamlined)
85.2 (6.2)
5.7 (0.1)
8.0 (0.1)
5.8 (0.1)
38.8 (3.5)
43.3 (0.8)
Group 2
(deep-bodied)
123.5 (3.4)
5.4 (0.1)
7.7 (0.1)
5.9 (0.1)
72.3 (4.3)
41.3 (0.7)
the caudal fin (1.48), which was longer in the
streamlined form, and by the anal fin (-0.82), which
was longer in the deep-bodied form (Wilks λ =
0.76, χ2 = 18, df = 5, P = 0.003). The magnitude of
difference was small; caudal and anal fins differed
less than 0.3 cm between streamlined and deepbodied trout (Table 1). In comparison to the caudal
and anal fins, group differences were minimally influenced by dorsal, pelvic, and pectoral fin lengths;
standardized-canonical-function coefficients were
–0.50, –0.35, and 0.26 respectively. Fin lengths
were size-adjusted prior to analysis because the relationships between fin and standard length differed
for male and female trout (sex by SL interaction:
F5,58 = 5.9, P < 0.001). Small males had shorter fins
than similar-sized females and large males had
longer fins than large females. Fin lengths were
equivalent (slopes intersected) at approximately 42
cm (SL). The size-adjustment was performed using
residuals from the regression of each fin length versus standard length calculated separately for male
and female trout. Residuals from these regressions
were added to the predicted fin lengths of a 42-cm
lake trout (Reist 1985).
The deep-bodied form occupied deeper habitats
than the streamlined form (Table 1). The streamlined form (Group 1) represented a higher proportion of those caught in the 0–50-m depth stratum
whereas the deep-bodied form (Group 2) represented a higher proportion of those caught in the
50–100-m and the 100–150-m depth strata (Fig. 4,
G = 24.4, df = 2, P < 0.001).
Opossum shrimp occurred more frequently (G =
4.07, df = 1, P = 0.04) and were more abundant
(U = 161, P = 0.007) in the stomachs of the deepbodied than in the stomachs of streamlined lake
trout (Fig. 5). Terrestrial insects did not differ between forms in percent occurrence (G = 2.47,
df = 1, P = 0.12) or abundance (U = 204, P = 0.06).
Similarly, fish prey did not differ in occurrence
(G = 0.73, df = 1, P = 0.39) or abundance (U = 237,
P = 0.34) in the stomachs of the two lake trout
forms. Empty stomachs were more common in the
streamlined (35%) than the deep-bodied (11%)
form (G = 4.87, df = 1, P = 0.03). Of particular
note, terrestrial insects were found in the stomachs
of 13 deep-bodied trout; ten of which were caught
in water deeper than 80 m. Terrestrial insects in the
diet included Hymenoptera and Coleoptera. Aquatic
invertebrates in the diet were primarily opossum
shrimp; one stomach also contained Ephemeroptera
nymphs. Fish prey included sculpins (Cottidae),
Phenotypic Diversity of Lake Trout in Lake Mistassini
FIG. 4. Relative abundance of lake trout forms
in three depth strata in Lake Mistassini. Graph
shows the proportion of each form caught in each
depth strata. The streamlined (Group 1) and deepbodied (Group 2) forms were identified by a
UPGMA cluster analysis (see Fig. 3).
sticklebacks (Pungitius pungitius), ciscoes (Coregonus spp.), and charr (Salvelinus spp.).
Catch of the streamlined form included proportionally more juveniles (i.e., immature) than the
deep-bodied form (Fig. 6, G = 14.2, df = 1, P <
0.001) even though the size ranges for deep-bodied
(34–51-cm SL) and streamlined (28-53-cm SL) lake
trout caught in the gillnets were similar. Of the ten
juveniles in the streamlined group, the longest was
49 cm (SL). All lake trout in the deep-bodied group
163
FIG. 6. Reproductive status of lake trout in three
length categories. Streamlined (Group 1) and
deep-bodied (Group 2) forms are plotted separately. Graph shows the proportion of adult to
total fish in each length category.
were adults, including the 34-cm smallest individual. On average, lake trout in the deep-bodied group
(all adults) were 2-cm shorter than adults in the
streamlined group (F1,70 = 4.6, P = 0.04, Table 1).
Length did not differ between adult male and female trout in either group (F1,70 = 0.1, P = 0.8), and
no interaction existed between sex and group (F1,70
= 3.1, P = 0.08). Of note, length comparisons did
not include the two outlier lake trout which were
both longer than 65 cm (SL).
Covariation of shape with brightness, buoyancy,
and depth was explained by a single vector pair
FIG. 5. Frequency of occurrence (a) and abundance (b) of prey items in
the stomachs of streamlined (Group 1) and deep-bodied (Group 2) lake
trout.
164
Zimmerman et al.
size for this 2B-PLS analysis was limited to 36 lake
trout due to available color data. Despite this limitation, a bimodal distribution was evident in the
shape scores derived from the x-axis of the vector
pair (Fig. 7b).
The majority of covariation (51%) of shape with
fin lengths was explained by a single vector pair,
which was not significant (permutation test: P =
0.3).
FIG. 7. Covariation of lake trout shape with
brightness-buoyancy-depth as defined by a twoblock partial-least-squares analysis. Shape differences, represented on the x-axis (a), were illustrated by outlines that connected landmarks. The
brightness-buoyancy-depth axis (a) was heavily
weighted by brightness and depth variables. Each
point in (a) represents an individual. A histogram
of shape (b) represents seven equally-spaced intervals of increasing x-axis scores from the 2B-PLS
analysis. Graphs are coded by shape groups identified in a UPGMA cluster analysis (see Fig. 3).
(96%) and differed from that expected by chance
(permutation test: P < 0.001). Profiles with a deep
anterior body and narrow caudal peduncle were associated with light color, low percent buoyancy, and
deep water; whereas, streamlined body shapes were
associated with dark color, high percent buoyancy,
and shallow water (Fig. 7a, R = 0.64, permutation
test: P < 0.001). Intermediate shapes were also intermediate with respect to brightness-buoyancydepth scores. The brightness-buoyancy-depth block
was mostly weighted by brightness (0.51) and depth
(0.83) as compared to buoyancy (–0.23). Samples
DISCUSSION
Two lake trout phenotypes, one caught predominantly in shallow water and one in deep water, were
identified in Lake Mistassini. The shallow-water
form, identified by its streamlined shape, was dark
in color and high in buoyancy. The deep-water
form, identified by its deep anterior-body profile
and narrow caudal peduncle, was light in color and
lower in buoyancy. Maturity (i.e., adulthood) occurred at a smaller size for the deep-bodied than the
streamlined form. Lake trout shapes were bimodally distributed; those intermediate in shape
were also intermediate with respect to brightness,
buoyancy, and capture depth. Intermediate phenotypes may reflect incomplete differentiation among
forms, other undescribed forms, or environmental
influences on phenotypic expression (i.e., phenotypic plasticity).
The ecology of the two lake trout forms differed
based on capture depth and stomach contents. The
deep-bodied form, caught in deep water (> 50 m),
had a diet rich in opossum shrimp compared to the
streamlined form caught from shallow water. Diet
differences likely reflected differences in foraging
opportunity or in prey selectivity between the two
lake trout forms. Opossum shrimp are known to migrate vertically (Beeton and Bowers 1982). The disproportionate representation of this prey in the
stomachs of deep-bodied trout suggests that the
deep-bodied lake trout followed their migration
(i.e., increased foraging opportunity), or, if the
deep-bodied form does not migrate vertically, the
diet differences suggested that the deep-bodied
form foraged when the Mysis were descended and
near the bottom (i.e., increased prey selectivity).
Inter-lake Similarities in Phenotype
Buoyancy comparisons between forms were consistent with the hypothesis that low percent buoyancy would characterize lake trout associated with
deep-water habitat as compared to lake trout associ-
Phenotypic Diversity of Lake Trout in Lake Mistassini
ated with shallow-water habitat. Correlations
among buoyancy, body depth, and capture depth in
Lake Mistassini paralleled observations from Lake
Superior and Great Slave Lake; however, buoyancy
differences between Lake Mistassini forms were
slight. In Lake Superior, high-fat, deep-bodied siscowet trout were present in deeper water than lowfat, streamlined lean trout, and humper trout were
intermediate in fat content and depth (Eschmeyer
and Phillips 1965, Moore and Bronte 2001, Bronte
et al. 2003). A similar trend was reported from
Great Slave Lake; low-percent-buoyancy deepbodied trout were caught in deeper water than highpercent-buoyancy streamlined trout (Zimmerman et
al. 2006). The water-depth and body-shape association evident in all three lakes was also reported for
Lakes Michigan and Huron in the 19 th and early
20th centuries (Brown et al. 1981, Goodier 1981,
Eshenroder et al. 1995).
Buoyancy and fin length differences between the
shallow- and deep-water forms in Lake Mistassini
were slight in comparison with the differences observed in lake trout from Great Slave Lake (Zimmerman et al. 2006). The buoyancy difference
between streamlined and deep-bodied forms in
Great Slave Lake was 11 times larger in magnitude
than in Lake Mistassini. The lightest deep-bodied
individual in Great Slave Lake was almost neutrally
buoyant (buoyancy = 0.5%). In Lake Mistassini, the
lightest deep-bodied individual was negatively
buoyant (3.8%) and near the upper buoyancy limit
of the deep-water phenotype in Great Slave Lake.
The pectoral-fin length difference between streamlined and deep-bodied forms reported from Great
Slave Lake was not observed in Lake Mistassini.
Existing caudal and anal fin differences between
the Lake Mistassini forms were small enough in
magnitude that they were unlikely to influence
swimming performance.
The deep-bodied form in Lake Mistassini was not
well adapted for daily vertical migration behavior
in comparison to deep-water trout in Lake Superior
or Great Slave Lake. Low percent buoyancy, observed in Great Slave Lake and Lake Superior, and
long paired-fins, observed in Great Slave Lake, can
function as buoyancy aids when the swim bladder is
compressed after rapid descents (Henderson and
Anderson 2002). However, low percent buoyancy
(i.e., high lipid content) has a high energetic cost
and, in the absence of vertical migratory behavior,
buoyancy regulation is more efficiently accomplished by changes in swim bladder volume
(Alexander 1972, Henderson and Anderson 2002).
165
Based on tissue density and fin data, we expect that
the deep-bodied form in Lake Mistassini does not
undergo extensive vertical migrations, or, if it does,
its migrations are more energetically costly than
those of siscowets in Lake Superior or siscowet-like
trout in Great Slave Lake. Restriction of the deepbodied form to deep waters was further supported
by the lack of local traditional ecological knowledge regarding the existence of the deep-water form
(Andrew Coon, Kenny Longchamp, and Eric CoonCome, Council of the Cree Nation of Mistissini,
personal communications).
Given that morphological and buoyancy data
suggest the deep-bodied form was not well adapted
for vertical migration, the presence of terrestrial insects in their stomachs was perplexing. Terrestrial
insects might indicate surface feeding, and surface
feeding required vertical movements of greater than
80 m for most of the deep-bodied trout. Alternatively, deep-bodied trout may capture insects, after
sinking, at or near the lakebed. Further study of the
swimming movements and trophic position of the
lake trout forms in Lake Mistassini is needed to better understand the foraging behavior and the energetic trade-offs unique to these deep-water lake
trout.
Distinctiveness of Lake Mistassini Forms
The size and brightness of the streamlined darkcolored form in Lake Mistassini were distinct from
lean-like trout occupying similar depth strata in
Lake Superior and Great Slave Lake. In size
(length), they were more similar to planktivorous
populations in inland lakes than to piscivorous lean
trout observed in large lakes (Martin 1966, Konkle
and Sprules 1986). An exception to this observation
were the two large lean-like trout (> 65-cm SL) removed from the statistical analyses as length outliers. Both of these trout had the robust appearance
of piscivorous trout found in the Great Lakes and
may represent a cannibalistic morph of the lean-like
trout (Martin and Olver 1980). The dark color of
the streamlined form, while not unique to Lake
Mistassini (Hallock 1877, Goode 1884, Koelz
1926, Gallagher 2002), was more difficult to interpret as numerous variables contribute to color variation in fishes. Background matching is a
well-recognized occurrence in fishes (van der Salm
et al. 2005) but not a likely explanation in Lake
Mistassini; the differences between forms were opposite from the theoretically expected light-in-shallow-water and dark-in-deep-water patterns that
166
Zimmerman et al.
were empirically reported for lake trout in Great
Slave Lake, NWT (Zimmerman et al. 2006) and for
Arctic charr (Salvelinus alpinus) in Gander Lake,
Newfoundland (O’Connell and Dempson 2002,
O’Connell et al. 2005). Color can be linked to reproductive behavior (Houde and Endler 1990,
McLennan 1996, Foote et al. 2004); however,
brightness did not differ between males and females
within the Lake Mistassini forms. Skin coloration
can also be affected by diet (Kalinowski et al.
2005), water chemistry (i.e., tannin staining), and/or
genetic make-up (Brooks and Endler 2001, Shikano
2005)—three possibilities that, with further study,
could provide explanations for the differences reported here.
The morphology and life history characteristics
of the deep-bodied form in Lake Mistassini were
more similar to humper trout from Lake Superior
than to siscowet-like phenotypes from Great Slave
Lake and Lake Superior. The small difference in
buoyancy between Lake Mistassini forms was similar to that between leans and humpers but not between leans and siscowets in Lake Superior
(Thurston 1962, Eschmeyer and Phillips 1965) or
between lean- and siscowet-like trout in Great
Slave Lake (Zimmerman et al. 2006). With their anteriorly distributed body depth and narrow caudal
peduncle, the deep-bodied form in Lake Mistassini
resembled the profile of humper trout in Lake Superior but did not resemble the deep head, mid-body,
and caudal profiles of siscowet trout in Lake Superior (Khan and Qadri 1970, Moore and Bronte
2001) and of siscowet-like trout in Great Slave
Lake (Zimmerman et al. 2006). Although the deepbodied form in Lake Mistassini lacked the thin abdominal wall that characterizes humper trout
(Lawrie and Rahrer 1973, Burnham-Curtis and
Bronte 1996, Moore and Bronte 2001), this feature
is not consistent across humper populations (Peck
1975). The “pot-belly” appearance of the Lake Mistassini deep-bodied form also was not characteristic
of Lake Superior humpers (Moore and Bronte
2001); in this respect, the deep-bodied form in Lake
Mistassini was distinctive in appearance. In terms
of life history, the deep-bodied form appeared to
mature at smaller sizes than did the streamlined
form. All deep-bodied individuals caught were capable of reproducing at a length of 32 cm (SL),
whereas immature streamlined individuals were as
long as 49 cm (SL). Small maturation size of the
deep-bodied form was similar to humper trout in
Lake Superior, which reach adulthood at shorter
lengths than lean and siscowet trout (Rahrer 1965,
Burnham-Curtis and Bronte 1996).
Origins of Sympatric Shallowand Deep-water Phenotypes
The availability of shallow- and deep-water
niches may be a key ecological variable contributing to lake trout phenotypic differentiation in Lake
Mistassini. Indeed, deep-water habitat is a feature
of all four lakes where lake trout phenotypes have
been observed. In comparison with Lake Superior,
Great Slave Lake, and Great Bear Lake, Lake Mistassini is young, shallow, and small in surface area
(Beeton 1984, Dyke and Priest 1987, Evans 2000).
As such, the presence of two sympatric phenotypes
in Lake Mistassini is important for understanding
the environment necessary for phenotypic differentiation to occur. A genetic basis for these different
phenotypes awaits further study, but is hypothesized based on the genetic distinctiveness of lean
and siscowet trout in Lake Superior (Burnham-Curtis and Smith 1994, Page et al. 2004) and on a
known genetic basis for two traits associated with
deep-water living—lipid content (Eschmeyer and
Phillips 1965) and swim-bladder gas retention
(Ihssen and Tait 1974). Ecological trade-offs contributing to phenotypic differentiation also await
further study. The competitive trade-off proposed
for high-lipid, vertically migrating siscowet-like
trout (Zimmerman et al. 2006) did not necessarily
apply to the deep-water phenotype in Lake Mistassini, which more closely resembled humper trout
whose ecology is poorly understood.
The existence of a humper-like phenotype in
Lake Mistassini challenges the hypothesis that the
humper form was produced from an introgression
of lean and siscowet forms (Burnham-Curtis 1993,
Burnham-Curtis and Smith 1994). If a siscowet-like
form never inhabited Lake Mistassini, the existing
deep-bodied form might either be the descendent of
a colonizing form (presumably the lean form), have
originated from dispersal after deglaciation of a
humper-like progenitor, or be one of two environmentally induced phenotypes in the lake (i.e., phenotypic plasticity). If siscowet-like trout have
historically inhabited or presently inhabit Lake
Mistassini, the form is either extinct or in low abundance. If siscowet-like trout were once present and
parallel introgression events occurred in Lake Superior and Lake Mistassini, the lakes differ remarkably in the long-term abundances of humper versus
siscowet phenotypes.
A humper-like phenotype is the dominant form in
Phenotypic Diversity of Lake Trout in Lake Mistassini
deep-water habitats in Lake Mistassini and their
abundance contrasts with Lake Superior and Great
Slave Lake where deep-water habitats are dominated by the siscowet phenotype. In Lake Superior,
humper trout occur in isolated populations on offshore humps similar to sea mounts. In Great Slave
Lake, a comparable humper-like phenotype was not
found in two survey years (2001 and 2002) of deepwater habitat (Zimmerman et al. 2006) indicating
that it is either absent or in low abundance and locally distributed in this lake as it is in Lake Superior. Based on available data, Lake Mistassini is
unique in that it demonstrates that, under certain
conditions, humper-like trout have the capacity to
be ecologically dominant in the deep waters of
large lakes.
ACKNOWLEDGMENTS
Michael Prince and Andrew Coon (Council of
the Cree Nation of Mistissini) assisted with permitting and study logistics. Kenny Longchamp and
Eric Coon-Come (Mistissini, Quebec) and Mark
Ebener (Chippewa/Ottawa Resource Authority) assisted with field work under demanding weather
conditions. Allison Niggemyer and Sean Sisler
helped with the diet analysis in laboratory space
provided by the Great Lakes Science Center
(USGS, Ann Arbor, MI). Julia Cameron and Kathleen Weesies (Michigan State University) constructed the map of sampling localities. H. David
Sheets (Canisius College) produced software used
for geometric morphometric analyses. Funding for
this research was provided by the Fishery Research
Program of the Great Lakes Fishery Commission.
REFERENCES
Alexander, R.M. 1972. The energetics of vertical migration by fishes. In The effects of pressure on living
organisms. Symposia of the Society for Experimental
Biology., eds. M.A. Sleigh and A.G. MacDonald, pp.
273–294. New York, New York: Academic Press.
——— . 1993. Buoyancy. In The physiology of fishes, ed.
D.H. Evans, pp. 75–97. Boca Raton, Florida: CRC
Press.
Alfonso, N.R. 2004. Evidence for two morphotypes of
lake charr, Salvelinus namaycush, from Great Bear
Lake, Northwest Territories, Canada. Env. Biol. Fish.
71:21–32.
Beeton, A.M. 1960. The vertical migration of Mysis
relicta in lakes Huron and Michigan. J. Fish. Res.
Board Can. 17:517–539.
——— . 1984. The world’s great lakes. J. Great Lakes
Res. 10:106–113.
167
——— , and Bowers, J.A. 1982. Vertical migration of
Mysis relicta Loven. Hydrobiologia 93:53–61.
Blackie, C.T., Weese, D.J., and Noakes, D.L.G. 2003.
Evidence for resource polymorphism in the lake charr
(Salvelinus namaycush) population of Great Bear
Lake, Northwest Territories, Canada. Ecoscience
10:509–514.
Bookstein, F.L. 1991. Morphometric tools for landmark
data. New York, New York: Cambridge University
Press.
Bowers, J.A. 1988. Diel vertical migration of the Opossum Shrimp Mysis relicta in Lake Superior—observations and sampling from the Johnson-Sea-Link II submersible. Bull. Mar. Sci. 43:730–738.
Bronte, C.R., Ebener, M.P., Schreiner, D.R., DeVault,
D.S., Petzold, M.M., Jensen, D.A., Richards, C., and
Lozano, S.J. 2003. Fish community change in Lake
Superior, 1970–2000. Can. J. Fish. Aquat. Sci.
60:1552–1574.
Brooks, R., and Endler, J.A. 2001. Direct and indirect
sexual selection and quantitative genetics of male
traits in guppies (Poecilia reticulata). Evolution
55:1002–1015.
Brown, E.H., Eck, G.W., Foster, N.R., Horrall, R.M.,
and Coberly, C.E. 1981. Historical evidence for discrete stocks of lake trout (Salvelinus namaycush) in
Lake Michigan. Can. J. Fish. Aquat. Sci.
38:1747–1758.
Burnham-Curtis, M.K. 1993. Intralacustrine speciation
of Salvelinus namaycush in Lake Superior: an investigation of genetic and morphological variation and
evolution of lake trout in the Laurentian Great Lakes.
Ph. D. dissertation. University of Michigan, Ann
Arbor, Michigan.
——— , and Bronte, C.R. 1996. Otoliths reveal a diverse
age structure for humper lake trout in Lake Superior.
Trans. Am. Fish. Soc. 125:844–851.
——— , and Smith, G.R. 1994. Osteological evidence of
genetic divergence of lake trout (Salvelinus namaycush) in Lake Superior. Copeia 1994:843–850.
Dadswell, M.J. 1974. Distribution, ecology, and postglacial dispersal of certain crustaceans and fishes in
eastern North America. National Museum of Canada,
Ottawa, Canada. Publications in Zoology, No. 11.
Dyke, A.S., and Priest, V.K. 1987. Late Wisconsinan
and Holocene history of the Laurentide ice sheet.
Geogr. Phys. Quat. 41:237–263.
Eschmeyer, P.H., and Phillips, A.M. 1965. Fat content of
the flesh of siscowets and lake trout from Lake Superior. Trans. Am. Fish. Soc. 94:62–74.
Eshenroder, R.L., Payne, N.R., Johnson, J.E., Bowen, C.,
and Ebener, M. P. 1995. Lake trout rehabilitation in
Lake Huron. J. Great Lakes Res. 21 (Suppl. 1):
108–127.
——— , Argyle, R.L., and TeWinkel, L.M. 1998. Evidence for buoyancy regulation as a speciation mecha-
168
Zimmerman et al.
nism in Great Lakes ciscoes. Arch. Hydrobiol. Sp.
Issues Adv. Limnol. 50:207–217.
——— , Sideleva, V.G., and Todd, T.N. 1999. Functional
convergence among pelagic sculpins of Lake Baikal
and deepwater ciscoes of the Great Lakes. J. Great
Lakes Res. 25:847–855.
Evans, M.S. 2000. The large lake ecosystems of northern
Canada. Aquat. Ecosystem Health Management
3:65–79.
Foote, C.J., Brown, G.S., and Hawryshyn, C.W. 2004.
Female colour and male choice in sockeye salmon:
implications for the phenotypic convergence of
anadromous and nonanadromous morphs. Anim.
Behav. 67:69–83.
Fraser, D.J., and Bernatchez, L. 2005. Adaptive migratory divergence among sympatric brook charr populations. Evolution 59:611–624.
Gallagher, C.P. 2002. Traditional knowledge and genetic
discimination of Lake Nipigon lake trout stocks. M.
Sc. thesis. University of Manitoba, Manotiba.
Goode, G.B. 1884. Section I. Natural history of useful
aquatic animals. U.S. Government Printing Office,
Washington, D.C.
Goodier, J.L. 1981. Native lake trout (Salvelinus namaycush) stocks in the Canadian waters of Lake Superior
prior to 1955. Can. J. Fish. Aquat. Sci. 38:1724–1737.
Hallock, C. 1877. The game animals, birds and fishes of
North America: their habits and various methods of
capture. New York, New York: “Forest and Stream”
Publishing Company.
Henderson, B.A., and Anderson, D.M. 2002. Phenotypic
differences in buoyancy and energetics of lean and
siscowet lake charr in Lake Superior. Environ. Biol.
Fishes 64:203–209.
Houde, A.E., and Endler, J.A. 1990. Correlated evolution
of female mating preferences and male color patterns
in the guppy Poecilia reticulata. Science
248:1405–1408.
Hrabik, T.R., Jensen, O.P., Martell, S.J.D., Walters, C.J.,
and Kitchell, J.F. 2006. Diel vertical migration in the
Lake Superior pelagic community. I. Changes in vertical migration of coregonids in response to varying
predation risk. Can. J. Fish. Aquat. Sci.
63:2286–2295.
Ihssen, P., and Tait, J.S. 1974. Genetic differences in
retention of swimbladder gas between two populations of lake trout (Salvelinus namaycush). J. Fish.
Res. Board Can. 31:1351–1354.
Jennings, M.R. 1989. Use of spring scales for weighing
live fish in the field. N. Am. J. Fish. Man. 9:509–511.
Jensen, O.P., Hrabik, T.R., Martell, S.J.D., Walters, C.J.,
and Kitchell, J.F. 2006. Diel vertical migration in the
Lake Superior pelagic community. II. Modeling tradeoffs at an intermediate trophic level. Can. J. Fish.
Aquat. Sci. 63:2296–2307.
Kalinowski, C.T., Robaina, L.E., Fernandez-Palacios,
H., Schuchardt, D., and Izquierdo, M.S. 2005. Effect
of different carotenoid sources and their dietary levels
on red porgy (Pagrus pagrus) growth and skin colour.
Aquaculture 244:223–231.
Khan, N.Y., and Qadri, S.U. 1970. Morphological differences in Lake Superior lake char. J. Fish. Res. Board
Can. 27:161–167.
Koelz, W. 1926. Fishing industry of the Great Lakes:
Appendix XI to the report of the U. S. Commissioner
of fisheries for 1925. Bureau of Fisheries, U. S.
Department of Commerce, Washington, D. C. Bureau
of Fisheries Document No. 1001.
Konkle, B.R., and Sprules, W.G. 1986. Planktivory by
stunted lake trout in an Ontario lake. Trans. Am. Fish.
Soc. 115:515–521.
Krueger, C.C., and Ihssen, P.E. 1995. Review of genetics
of lake trout in the Great Lakes: History, molecular
genetics, physiology, strain comparisons, and restoration management. J. Great Lakes Res. 21:348–363.
Langerhans, R.B., Layman, C.A., Langerhans, A.K., and
Dewitt, T.J. 2003. Habitat-associated morphological
divergence in two Neotropical fish species. Biol. J.
Linnean Soc. 80:689–698.
Lawrie, A.H., and Rahrer, J.H. 1973. Lake Superior: a
case history of the lake and its fisheries. Great Lakes
Fishery Commission, Ann Arbor, Michigan. Technical Report No. 19.
Martin, N.V. 1966. The significance of food habits in the
biology, exploitation, and management of Algonquin
Park, Ontario, lake trout. Trans. Am. Fish. Soc.
95:415–422.
——— , and Olver, C.H. 1980. The lake charr, Salvelinus
namaycush. In Charrs: salmonid fishes of the genus
Salvelinus, ed. E.K. Balon, pp. 205–277. The Hague,
The Netherlands: Dr. W. Junk Publishers.
Mathworks. 2000. Matlab v. 6.2. Natick, Massachusetts.
McLennan, D.A. 1996. Integrating phylogenetic and
experimental analyses: The evolution of male and
female nuptial coloration in the stickleback fishes
(Gasterosteidae). Syst. Biol. 45:261–277.
Moore, S.A., and Bronte, C.R. 2001. Delineation of sympatric morphotypes of lake trout in Lake Superior.
Trans. Am. Fish. Soc. 130:1233–1240.
Nolte, A.W., and Sheets, H.D. 2005. Shape based assignments tests suggest transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae). Frontiers in Zoology 2:11.
O’Connell, M.F., and Dempson, J.B. 2002. The biology
of Arctic charr, Salvelinus alpinus, of Gander Lake, a
large, deep, oligotrophic lake in Newfoundland,
Canada. Environ. Biol. Fishes 64:115–126.
——— , Dempson, J.B., and Power, M. 2005. Ecology
and trophic relationships of the fishes of Gander Lake,
a large, deep, oligotrophic lake in Newfoundland,
Canada. Int. Rev. Hydrobiol. 90:486–510.
Page, K.S., Scribner, K.T., and Burnham-Curtis, M.
2004. Genetic diversity of wild and hatchery lake
Phenotypic Diversity of Lake Trout in Lake Mistassini
trout populations: Relevance for management and
restoration in the Great Lakes. Trans. Am. Fish. Soc.
133:674–691.
Peck, J.W. 1975. Brief life history accounts of five commercial salmonid fishes in Lake Superior. Michigan
Department of Natural Resources Fisheries Division,
Lansing, Michigan. Research Report No. 1821.
Power, M., O’Connell, M.F., and Dempson, J.B. 2005.
Ecological segregation within and among Arctic char
morphotypes in Gander Lake, Newfoundland. Environ. Biol. Fishes 73:263–274.
Rahrer, J.F. 1965. Age, growth, maturity, and fecundity
of “humper” lake trout, Isle Royale, Lake Superior.
Trans. Am. Fish. Soc. 94:75–83.
Reist, J.D. 1985. An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Can. J. Zool. 63:1429–1439.
Robinson, B.W., and Wilson, D.S. 1994. Character
release and displacement in fishes: a neglected literature. Am. Nat. 144:596–627.
Rohlf, F.J., and Corti, M. 2000. Use of two-block partial
least-squares to study covariation in shape. Syst. Biol.
49:740–753.
Ruber, L., and Adams, D.C. 2001. Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. J. Evol. Biol. 14:325–332.
Sampson, P.D., Bookstein, F.L., Sheehan, F.H., and Bolson, E.L. 1996. Eigenshape analysis of left ventricular
outlines from constrast ventriculograms. In Advances
in morphometrics, L.F. Marcus, M. Corti, and A. Loy,
eds., pp. 211–233. New York, New York: Plenum.
Shikano, T. 2005. Marker-based estimation of heritability for body color variation in Japanese flounder Paralichthys olivaceus. Aquaculture 249:95–105.
169
Skulason, S., and Smith, T.B. 1995. Resource polymorphisms in vertebrates. Trends Ecol. Evol. 10:366–370.
Smith, T.B., and Skulason, S. 1996. Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu. Rev. Ecol. Syst. 27:111–133.
SPSS. 2003. v. 12.0 for Windows. SPSS Inc, Chicago,
Illinois.
TeWinkel, L.M., and Fleischer, G.W. 1999. Vertical
migration and nighttime distribution of adult bloaters in
Lake Michigan. Trans. Am. Fish. Soc. 128:459–474.
Thurston, C.E. 1962. Physical characteristics and chemical composition of two subspecies of lake trout. J.
Fish. Res. Board Can. 19:39–44.
Turgeon, J., Estoup, A., and Bernatchez, L. 1999. Species
flock in the North American Great Lakes: Molecular
ecology of Lake Nipigon Ciscoes (Teleostei: Coregonidae: Coregonus). Evolution 53:1857–1871.
van der Salm, A.L., Spanings, F.A.T., Gresnigt, R.,
Bonga, S.E.W., and Flik, G. 2005. Background adaptation and water acidification affect pigmentation and
stress physiology of tilapia, Oreochromis mossambicus. Gen. Comp. Endocrinol. 144:51–59.
Zelditch, M.L., Swiderski, D.L., Sheets, H.D., and Fink,
W.L. 2004. Geometric morphometrics for biologists:
a primer. New York, New York: Elsevier Academic
Press.
Zimmerman, M.S., Krueger, C.C., and Eshenroder, R.L.
2006. Phenotypic diversity of lake trout in Great Slave
Lake: differences in morphology, buoyancy, and habitat depth. Trans. Am. Fish. Soc. 135:1056–1067.
Submitted: 15 May 2006
Accepted: 6 December 2006
Editorial handling: Carol A. Stepien