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Potential mechanisms of phenotypic divergence in
body size between Newfoundland and mainland
black bear populations
Shane P. Mahoney, John A. Virgl, and Kim Mawhinney
Abstract: Phenotypic variation in body size and degree of sexual size dimorphism of North American black bears
(Ursus americanus) was quantified for populations from New Brunswick, Quebec, Ontario, Maine, Alaska, and the
island of Newfoundland. Based on a model of island biogeography developed by Case, we predicted that body size
should be larger in Newfoundland bears than in mainland populations. The presence of few large predators and minimal competition between herbivore prey on Newfoundland allow an appropriate test of the model (i.e., food availability
for bears may differ between populations on the mainland and in Newfoundland). In addition, sexual-selection theory
predicts that the coevolution of polygyny and large size will be coupled with an increase in sexual size dimorphism.
Therefore, we also predicted that among the six populations, male body mass should scale hyperallometrically with
female body mass (i.e., slope > 1). Analysis of deterministic growth curves indicated that bears from Newfoundland
attained greater asymptotic body size than populations on the mainland, which supports our first prediction. On average,
the relative difference in asymptotic body mass between females from the island and mainland populations was 55%,
while the relative difference between males was 37%. However, we found that sexual size dimorphism did not increase
disproportionately with body mass among the six populations, which refuted our second prediction. We discuss a range
of abiotic and biotic selection pressures possibly responsible for larger body size in Newfoundland bears. We suggest
that the ability to exploit seasonally abundant and spatially dispersed dietary protein by female and male black bears
on the island has been and is still a primary environmental factor selecting for large body size in Newfoundland bears.
Although the relationship between sexual size dimorphism and body size is tenuous (slope ≤ 1), it does suggest that
(an)other adaptive mechanism(s), opposing sexual selection for extreme male size, explain(s) a large amount of the
variation in sexual size dimorphism among black bear populations.
Résumé : La variation phénotypique de la taille et de l’importance du1660
dimorphisme sexuel de la taille a été quantifiée
chez des populations nord-américaines d’Ours noirs (Ursus americanus) du Nouveau-Brunswick, du Québec, de
l’Ontario, du Maine, de l’Alaska et de Terre-Neuve. D’après un modèle de biogéographie insulaire élaboré par Case,
nous avons prédit que la taille des ours de Terre-Neuve devait être supérieure à celle des ours des populations continentales. La présence limitée de prédateurs de grande taille et la compétition minimale entre les proies herbivores à
Terre-Neuve sont des conditions appropriées pour tester le modèle (i.e., la disponibilité de la nourriture peut être différente chez les populations insulaires et les populations continentales). De plus, la théorie de la sélection sexuelle prédit
que la coévolution de la polygynie et d’une grande taille devait s’accompagner d’une augmentation de l’importance du
dimorphisme sexuel de la taille. Nous avons donc prédit en outre que, chez les six populations, la masse corporelle des
mâles devait être hyperallométrique par rapport à la masse des femelles (i.e., pente > 1). L’analyse des courbes de
croissance déterministes indique que les ours de Terre-Neuve atteignent une taille asymptotique supérieure à celle des
ours des populations continentales, ce qui vérifie notre première prédiction. En moyenne, la différence relative entre la
masse asymptotique des femelles insulaires et celle des femelles des populations continentales a été évaluée à 55 % et
la différence relative entre les mâles, à 37 %. Cependant, le dimorphisme sexuel de la taille n’a pas augmenté de façon
disproportionnée en fonction de la masse corporelle chez les six populations étudiées, ce qui infirme notre deuxième
prédiction. Nous examinons une série de pressions de sélection possibles, abiotiques aussi bien que biotiques, qui pourraient être responsables de la taille plus grande des ours de Terre-Neuve. Nous croyons que la capacité des ours mâles
et femelles d’exploiter des sources saisonnières abondantes et éparses de protéines alimentaires dans l’île a été et
demeure le facteur environnemental déterminant de la sélection en faveur d’une grande taille chez les ours de TerreNeuve. Bien que la relation entre le dimorphisme sexuel de la taille et la taille elle-même soit ténue (pente ≤ 1), elle
Received August 16, 2000. Accepted July 31, 2001. Published on the NRC Research Press Web site at http://cjz.nrc.ca on
September 7, 2001.
S.P. Mahoney. Wildlife Division, Department of Forest Resources and Agrifoods, P.O. Box 8700, Building 810, St. John’s,
NF A1B 4J6, Canada
John A. Virgl.1 Ecological Developmental and Statistical Analysis, 222 Haight Place, Saskatoon, SK S7H 4W2, Canada.
Kim Mawhinney. Parks Canada, 1869 Upper Water Street, Halifax, NS B3J 1S9, Canada.
1
Corresponding author (e-mail: [email protected]).
Can. J. Zool. 79: 1650–1660 (2001)
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DOI: 10.1139/cjz-79-9-1650
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indique tout de même qu’un ou plusieurs autres mécanismes évolutifs qui s’opposent à la sélection sexuelle favorisant
le gigantisme des mâles expliquent une grande partie de la variation du dimorphisme sexuel de la taille chez les populations d’ours noirs.
[Traduit par la Rédaction]
Introduction
Mahoney et al.
Within mammalian species, body size typically varies across
latitudinal and longitudinal gradients (McNab 1971; Ralls
and Harvey 1985; Geist 1987; Brown 1995). Explanations
for the observed latitudinal pattern in body size include adaptations for temperature, primary productivity, seasonal unpredictability of food resources, and prey size. While the
classic correlation between increase in body size and decrease
in temperature (Bergmann’s rule) is controversial (Geist 1987),
a number of studies do support this hypothesis (McNab 1971;
Burnett 1983; Owen 1989; Quin et al. 1996). Alternatively,
Rosenzweig (1968) demonstrated that size in mammalian
carnivores was explained more by primary productivity than
by temperature, and suggested that highly productive environments should select for larger body size. Boyce (1979)
linked increasing latitude with primary productivity and seasonality, and predicted that variability in food resources
should select for longer fasting endurance, which is positively correlated with body size. Finally, given the relationship between maximum prey size and predator body size
(Schoener 1969; Vézina 1985), an increase in prey size with
latitude may also be coupled with an increase in predator
size (Ralls and Harvey 1985). All of these environmental
factors, operating through evolutionary time and space, have
likely contributed to the patterns of body-size variation in
species (Gould 1996).
Studies have also shown a link between body-size variation and biogeographical isolation, with insular populations
often being larger or smaller than mainland populations
(Foster 1964; Case 1978). While lagomorphs, ungulates, foxes,
raccoons, and snakes tend to be relatively smaller on islands,
other groups such as cricetid rodents, bears, and iguanid lizards display an increase in size relative to mainland populations. Based on optimal body size theory and predator–prey
dynamics, Case (1978) developed a model to predict the directional shift in body size among ecotype groups inhabiting
island and mainland environments. His primary assumptions
were that, in general, islands should (i) contain fewer predators on consumers, (ii) contain fewer consumer competitors,
and (iii) have a more benign climate. Given these conditions,
the increase in average food availability should be associated
with selection for increase in body size, provided that body
size is not overly constrained by other physical or biotic factors
(Case 1978). Although there were exceptions, Case found a
loose correlation between island gigantism and territorial
species and between island dwarfism and nonterritorial species.
Like the proposed latitudinal responses presented above,
island–mainland shifts (or phenotypic divergence) in body
size likely reflect current and (or) historical differences in
abiotic and biotic environmental selection pressures (Case
and Schwaner 1993; Brown 1995; Abrams 1996).
Across mammalian species there is a good correlation between the proportional difference in female and male sizes,
or the degree of sexual size dimorphism, and the type of
breeding system (Ralls 1977). For example, in monogamous
species, individuals are typically small to medium-sized, male
parental investment can be high, and there is little or no sexual
size dimorphism. Conversely, extreme polygyny is associated
with large body size, minimal male parental investment, and
a high degree of sexual size dimorphism. Comparative studies
that regress male body mass on female body mass among
primate species have generally shown that male body mass
scales hyperallometrically (i.e., slope > 1; Fairbairn and
Preziosi 1994) with female body mass (Clutton-Brock et al.
1977; Leutenegger 1978). Sexual selection for large body
size in males, and the associated advantage in terms of increased
mating opportunities, appears to be the primary mechanism
that explains the variation in sexual size dimorphism between monogamous and polygynous species (Fisher 1958;
Clutton-Brock et al. 1977; Ralls 1977; Leutenegger 1978).
Therefore, an increase in body size for polygynous species
should be correlated with an increase in the degree of sexual
size dimorphism. However, environmental factors, such as
spatial and temporal variation in availability of high-quality
food resources, availability of receptive females, and length
of the mating period, acting on both female and male body
size can constrain sexual selection for increasing size in
males (Fisher 1958; Clutton-Brock et al. 1977; Ralls 1977).
We investigated geographic variation in body size and sexual size dimorphism in North American black bears (Ursus
americanus) from five populations on the mainland and the
population on the island of Newfoundland. Bears on Newfoundland have coexisted with wolves (Canis lupus) and caribou (Rangifer tarandus) since the end of the Wisconsin ice
age, except during the last 80 years, when wolves have been
extirpated from the island (Dodds 1983). Moose (Alces alces),
which were introduced around the turn of the century (Pimlott
1953), are the only other large prey of Newfoundland bears.
Relative to the number of different large predators and herbivores on the mainland, the presence of few large predators
and minimal competition between herbivore prey on Newfoundland meet the assumptions of the island biogeographical
model described above (i.e., Case 1978) and allow an appropriate test of the model. Thus, based on the model developed
by Case (1978) and the territorial behaviour of black bears,
we first predicted that female and male black bears from
Newfoundland would be larger than mainland populations.
Furthermore, because black bears are polygynous and exhibit almost no male parental investment (except gamete
contribution), we used sexual-selection theory to predict that
sexual size dimorphism should increase hyperallometrically
with body size among populations.
Materials and methods
Animal collection and morphometrics
Morphometric data were collected from black bear populations
inhabiting six geographic areas in North America: Alaska, Ontario,
Quebec, New Brunswick, Newfoundland, and Maine. More
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Can. J. Zool. Vol. 79, 2001
Table 1. Capture methods and periods for black bears from six geographically separate
populations in North America.
Newfoundland
New Brunswick
Ontario
Quebec
Alaska
Maine
Capture method
Capture period
Hunting/livetrapping
Hunting
Livetrapping
Hunting
Hunting/livetrapping
Hunting/livetrapping
1985–1993
1989–1991
1989–1991
1983–1987
1977–1985
1979–1991
specifically, the Alaska measurements were obtained from bears
captured within the areas of Moose Pens and Fingers Lake, and
Ontario data were collected from individuals captured in the Chapleau
area (northern Ontario). All bears from Quebec were captured within
the La Vérendrye Wildlife Reserve (southwestern Quebec) and individuals from Maine were captured within the counties of Spectacle
Pond, Stacyville, and Bradford. Studies involved a mixture of capture methods and capture periods (Table 1). We acknowledge that
differences in capture methods may have influenced the results to
some degree, but we assume that whether hunting or trapping was
used is incidental to the observed patterns of growth and adult size
among populations.
Measured variables included body mass, total body length, chest
girth, and neck girth (except for Alaska and New Brunswick bears).
Body mass was measured to the nearest 1 kg. Total body length, or
contour length, was measured from the tip of the nose to the tip of
the tail. Chest girth, or heart girth, was recorded as the circumference of the body immediately posterior to the shoulders. Neck
girth represents the circumference of the neck directly behind the
jaw. All length and girth measurements were recorded to the nearest 1 cm with a flexible steel tape.
Age determination and categorization
Age of bears at first capture, except young of the year, was determined from an extracted premolar and by counting cementum
annuli (Willey 1974). Age of recaptured bears was determined by
back-dating to the initial capture date. For all bears age was adjusted to the month of capture. For example, assuming that the parturition period is in January (Alt 1983), a 2-year-old individual
captured in August was recorded as being approximately 2.67 (2 +
8/12 months) years of age. Similarly, young of the year captured in
April were 0.33 years old. We assumed that this adjustment would
minimize biases associated with gross changes in nutrient-reserve
mass (fat and protein) that occur in black bears between hibernation periods.
Postnatal growth
Geometric growth was analyzed using the following three growth
models:
[1]
M(t) = A·[1 – 1/3 e–K(t–I)]3
[2]
M(t) = A·e–e–K(t–I)
[3]
M(t) = A·[e–K(t–I) + 1]–1
where M(t) is body mass, total body length, or chest girth at age t,
A is asymptotic mass or size, K is the growth-rate constant (year–1),
and I is age (years) at the inflection point. Equations 1, 2, and 3
represent the von Bertalanffy, Gompertz, and logistic growth curves,
respectively, (Zullinger et al. 1984).
Data for individuals from each geographic area were fitted to
growth models, separately for each sex, using the Gauss–Newton
method (PROC NLIN; SAS Institute Inc. 1990). Parameter estimates (mean ± 1 SE) were generated after convergence was met,
(May–November)
(May–June, October)
(May–August)
(June–July)
(January–December)
(January–December)
and the residual sum of squares (SSres) and coefficient of determination (r2) were also calculated.
Statistical analyses
To assess the fit of each growth model to the data, a one-way
analysis of variance was used to examine SSres for body mass, and
the shapes of the curves were visually assessed (Zullinger et al.
1984). Following selection of the model, total body length and
chest girth were then fitted to the same equation. Parameter estimates among populations were judged to differ significantly if the
standard errors did not overlap.
For descriptive purposes, means and standard deviations of neck
girth were also calculated among age-classes (i.e., 0, 1, 2,…, ≥10).
Each age-class included bears captured within a calender year (i.e.,
January–December). For example, young of the year were placed
in age-class 0. Because of the limited neck-girth values for bears
older than 10 years, all individuals ≥10 years of age were pooled
for each sex.
The relationship between sexual size dimorphism and body mass
among populations was analyzed by least squares regression of
log10(male body mass) on log10(female body mass), where male
and female masses were asymptotic estimates obtained from growth
curves. This represents an appropriate test of the allometric relationship between male and female body masses (Clutton-Brock et
al. 1977; Leutenegger 1978; Fairbairn and Preziosi 1994). Correlating the ratio of male to female body masses with average body
mass is not recommended, owing to the mathematical interdependence between dependent and independent variables (see Fairbairn
and Preziosi 1994). We specifically tested the hypothesis that the
relationship between male and female body masses among populations would be hyperallometric (i.e., slope > 1). All statistical
analyses were performed with the SAS statistical package for
microcomputers (version 6.0; SAS Institute Inc. 1990).
Results
Selection of a growth model
Analysis of variance indicated that the moderate amounts
of unexplained variance (SSres) associated with each growth
equation for female and male black bears were very similar
among models (F[2,33] = 0.01, P > 0.50). However, the shape
of the fitted curve varied enough among the models to generate differences in parameter estimates. For example, the
von Bertalanffy model produced the largest estimates of asymptotic mass, while the logistic model generated the highest estimates of growth rate (see also Zullinger et al. 1984).
The Gompertz model typically produced parameter estimates
that fell between estimates for the von Bertalanffy and logistic equations. We decided to use the middle values generated
by the Gompertz model to estimate asymptotic body sizes
and growth rates among black bear populations.
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Table 2. Estimates (mean ± 1 SE) of sex-specific asymptotic body mass (A, kg), growth-rate constant
(K, year–1), and age at the inflection point (I, years) for black bears from six geographically separate populations in North America.
Females
Males
A
Newfoundland
New Brunswick
Ontario
Quebec
Alaska
Maine
Mean
101.1
67.1
67.3
54.8
68.4
65.8
K
±
±
±
±
±
±
9.6
2.4
3.1
1.4
1.8
1.0
70.7 ± 6.4
0.302
0.514
0.431
0.593
0.603
0.526
I
±
±
±
±
±
±
0.096
0.104
0.081
0.071
0.063
0.021
0.494 ± 0.045
1.9
1.1
2.1
1.9
1.6
2.1
A
±
±
±
±
±
±
0.4
0.3
0.3
0.1
0.1
0.1
1.8 ± 0.2
178.6
145.5
147.9
118.2
129.0
116.2
K
±
±
±
±
±
±
9.7
11.8
8.6
8.2
4.5
2.4
139.3 ± 9.5
0.313
0.305
0.253
0.337
0.418
0.522
I
±
±
±
±
±
±
0.045
0.050
0.036
0.048
0.042
0.021
0.356 ± 0.038
3.2
2.7
3.9
3.2
2.6
2.4
±
±
±
±
±
±
0.3
0.3
0.3
0.3
0.1
0.1
3.0 ± 0.2
Note: Parameters were estimated from the Gompertz model.
Phenotypic variation in body size and growth rate
Estimates of asymptotic body mass indicated that female
and male black bears from Newfoundland were significantly
larger than individuals from mainland populations, which
supports our first prediction (Table 2). The average difference
in asymptotic mass between female bears from the island
(101 kg) and mainland populations (65 kg) was approximately
55%, while the difference between males from the island
(179 kg) and mainland populations (131 kg) was approximately 37%.
Among mainland populations, asymptotic estimates of body
mass were less variable for females than for males (Table 2).
For example, female bears from New Brunswick, Ontario,
Alaska, and Maine did not differ in mass, but females from
these four populations were significantly larger than females
from Quebec. In contrast, asymptotic masses of male bears
from Ontario and New Brunswick were similar, and males
from these two populations were significantly larger than
males from Quebec, Alaska, and Maine. In addition, males
from Alaska were larger than males from Maine but similar
in size to those from Quebec (Table 2).
For all populations, age at the inflection point for females
(1.8 ± 0.2 years; mean ± 1 SE) was less than for males (3.0 ±
0.2 years), and the variation in inflection point among populations for each sex was moderate (Table 2). For example,
age at the inflection point ranged from 1.1 years for females
from New Brunswick to 2.1 years for females from Ontario
and Maine. For males, age at the inflection point ranged
from 2.4 years for Maine bears to 3.9 years for Ontario
bears. Age at the inflection point for Newfoundland females
and males was 1.9 and 3.2 years, respectively.
Variation in asymptotic body mass and age at the inflection
point were correlated with sex-specific and among-population
differences in growth rate. For mainland populations, females reached asymptotic mass at approximately 7–8 years
of age (Fig. 1). In contrast, females from Newfoundland did
not reach asymptotic mass until they were 12 years of age.
Thus, although females from Newfoundland had a significantly slower growth rate than females from mainland populations, they spent more time growing and attained a greater
asymptotic size (Table 2). Relative to females, age at asymptotic mass and growth rate for males were more variable
among populations (Fig. 1, Table 2). Males from Alaska and
Maine attained asymptotic mass at 10–11 years of age and
exhibited the highest growth rates, while males from the
other populations, including Newfoundland, reached asymptotic mass at 14–16 years of age and had lower growth rates.
Except for populations from Newfoundland and Maine, the
growth rate of male bears was significantly lower than that
of females (Table 2).
Analysis of other correlates of body size generated similar
patterns, although the results were more equivocal. Bears
from Newfoundland did not consistently exhibit the extreme
estimates of asymptotic size, but they were invariably larger
than the average for all populations. For example, asymptotic total body length was greatest for female bears from
Newfoundland and Ontario, followed by Alaska (Fig. 2).
Total body lengths of females from New Brunswick, Quebec,
and Maine were similar. Male bears from Ontario attained
the largest total body length, followed by Newfoundland and
Alaska (Table 3). Total body length for males from New
Brunswick was greater than that for males from Maine but
similar to that for males from Quebec. Asymptotic chest
girth in females from Newfoundland was significantly larger
than in females from mainland populations (Table 4). Among
mainland populations, chest girth in females was largest for
bears from Alaska, followed by those from Ontario, New
Brunswick, Maine, and Quebec. Chest girth in males from
Newfoundland, New Brunswick, Ontario, and Alaska was
larger than in males from Quebec and Maine (Table 4). Mean
neck girth for bears older than 7 years of age, particularly
females, was also largest for the population from Newfoundland, followed by Ontario, Quebec, and Maine (Table 5). As
with body mass, the growth-rate constants obtained for total
body length and chest girth were significantly higher for females than for males, except in populations from Newfoundland and Maine (Tables 3 and 4).
Sexual size dimorphism
Using the asymptotic values obtained from each population, a regression of male body mass on female body mass
generated a significant relationship (F[1,5] = 10.86, P = 0.03,
r2 = 0.73). However, the slope (0.69) of the relationship was
not statistically different from 1 (F = 2.18, P = 0.21), indicating that male body mass did not increase hyperallometrically
with female body mass (Fig. 3). Although our estimate of
the allometric exponent (slope) must be tempered by our low
sample size, it does suggest a trend towards a decrease in
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Fig. 1. Geometric growth in body mass for female (䉱) and male (䉭) black bears (Ursus americanus) from different populations in
North America. Predicted curves were calculated from the Gompertz model.
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Fig. 2. Geometric growth in total body length for female (䉱) and male (䉭) black bears from different populations in North America.
Predicted curves were calculated from the Gompertz model.
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Table 3. Estimates (mean ± 1 SE) of sex-specific asymptotic total body length (A, cm) and
growth-rate constant (K, year–1) for black bears from six geographically separate populations in North America.
Females
Males
A
K
Newfoundland
New Brunswick
Ontario
Quebec
Alaska
Maine
164.9
145.6
162.0
146.1
157.6
147.5
±
±
±
±
±
±
3.5
1.3
2.0
1.7
1.8
0.7
Mean
154.0 ± 3.5
A
0.479
0.688
0.487
0.874
0.653
0.901
±
±
±
±
±
±
0.088
0.101
0.046
0.118
0.074
0.022
0.676 ± 0.073
183.2
170.3
192.7
168.9
181.1
164.4
K
±
±
±
±
±
±
3.0
2.5
4.2
3.4
2.4
1.1
176.7 ± 4.4
0.560
0.496
0.335
0.479
0.490
0.906
±
±
±
±
±
±
0.060
0.051
0.048
0.048
0.047
0.024
0.542 ± 0.075
Note: Parameters were estimated from the Gompertz model.
Table 4. Estimates (mean ± 1 SE) of sex-specific asymptotic chest girth (A, cm) and
growth-rate constant (K, year–1) for black bears from six geographically separate populations in North America.
Females
A
Males
K
Newfoundland
New Brunswick
Ontario
Quebec
Alaska
Maine
98.1
82.8
83.6
76.9
86.8
80.8
±
±
±
±
±
±
3.5
1.4
1.5
1.9
1.4
0.6
Mean
84.9 ± 3.0
0.448
0.549
0.453
0.581
0.657
0.632
A
±
±
±
±
±
±
0.104
0.105
0.054
0.132
0.099
0.023
0.550 ± 0.034
119.7
115.0
117.0
99.5
116.3
97.3
K
±
±
±
±
±
±
3.4
4.4
5.2
3.4
3.5
1.1
110.4 ± 3.9
0.343
0.279
0.252
0.382
0.311
0.609
±
±
±
±
±
±
0.045
0.047
0.048
0.049
0.046
0.022
0.364 ± 0.050
Note: Parameters were estimated from the Gompertz model.
sexual size dimorphism with increase in body size among
populations.
Discussion
Adult female and male black bears from the island of Newfoundland were determined to be significantly larger than
bears from mainland populations. On average, the difference
in asymptotic body mass between females from the island
and mainland populations was 55%, while the difference between males was 37%. Although bears from Newfoundland
generally exhibited lower growth rates than mainland populations, females and, to a lesser degree, males spent more
time growing and attained asymptotic mass later than individuals from mainland populations. Less correlative measures
of body size, such as total body length and chest girth, generated more equivocal results, but asymptotes for Newfoundland bears were invariably among the largest. Therefore, the
results supported our prediction that Newfoundland black
bears would be larger than bears from the five mainland populations.
There are a number of potential environmental selection
pressures, which are not mutually exclusive, that could explain the observed phenotypic divergence in body size between Newfoundland and mainland bears. However, without
explicit statistical testing of the environmental selection pres2
sures that may be correlated with variation in body size
among populations, our explanations remain hypothetical. One
possible factor is the difference in spatial and temporal variation in food resources, particularly the availability of dietary
protein (Schoener 1969; Case 1978; Case and Schwaner 1993).
In this context, the island of Newfoundland may represent a
relatively unique foraging environment for North American
black bears. For example, caribou and black bears have coexisted on the island since the end of the Wisconsin ice age,
while moose were twice introduced around the turn of the
20th century (circa 1878 and 1904; Pimlott 1953). Thirteen
subpopulations of caribou inhabit Newfoundland and moose
have extensively colonized the island (the current estimate is
150 000) (Mahoney 20002). In accordance with Case’s
model (1978), minimal interspecific competition between
these herbivores creates the potential for an abundance of
caribou and moose calves that can provide a rich source of
protein for bears during the spring and early summer
(Mahoney 1986; Mahoney et al. 1990; Schwartz and
Franzmann 1991; Ballard 1992). Although hard mast crops are
unavailable on the island, early-successional forest stands and
wetland and “tundra” heath habitats can support an abundance of soft mast during the late summer and autumn
(Damman 1993). Furthermore, millions of capelin (Mallotus
villosus) spawn on accessible beaches in early summer and
are fed upon by bears, as are the large numbers of spawning
S.P. Mahoney. 2000. A synthesis and interpretation of the biology of woodland caribou on the island of Newfoundland. Vols. 1–15.
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5.4
4.8
5.0
6.2
6.1
5.7
4.7
5.9
3.7
5.9
9.9
±
±
±
±
±
±
±
±
±
±
±
19.2
31.3
42.7
47.4
54.7
56.1
58.9
58.8
61.8
62.0
63.7
Males
(199)
(122)
(80)
(66)
(45)
(51)
(37)
(23)
(22)
(11)
(38)
4.2
3.4
4.1
4.4
3.0
4.3
3.9
2.9
3.7
3.1
2.9
±
±
±
±
±
±
±
±
±
±
±
Females
18.6
28.8
35.3
38.7
41.0
42.4
43.0
44.7
46.6
44.7
46.7
±
±
±
±
±
±
±
±
±
±
±
± 3.2 (5)
± 4.0 (5)
(1)
± 3.5
± 4.4
± 3.7
± 2.4
± 3.4
± 7.0
± 1.5
±
±
±
±
±
14.7 (11)
3.9 (6)
6.2 (6)
6.9 (5)
8.8 (16)
19.0
30.0
36.6
42.2
42.0
45.6
44.6
46.3
nd
48.0
47.4
±
±
±
±
±
± 2.4 (4)
± 2.1 (5)
± 1.4 (2)
± 13.8 (2)
Note: Numbers in parentheses are sample sizes; nd, no data.
(1)
± 4.8
± 6.8
± 3.9
± 8.1
± 3.9
± 1.8
± 2.6
± 5.2
(7)
(4)
(7)
(11)
(7)
(7)
(3)
(8)
22.0
38.0
42.0
44.1
50.6
nd
52.0
66.0
62.3
73.4
69.4
± 4.2 (4)
Females
23.9
nd
42.5
39.6
48.6
47.1
51.6
50.5
51.7
48.2
51.6
± 4.4 (6)
± 5.6 (13)
± 4.1 (21)
± 4.2 (11)
± 0.9 (4)
± 6.0 (4)
(1)
(1)
± 2.1 (2)
(1)
± 10.7 (10)
28.9
40.0
48.2
48.7
55.0
59.3
60.3
74.0
76.5
74.5
72.6
Males
26.3
36.1
41.5
51.2
46.4
nd
48.6
50.0
59.3
nd
59.5
0
1
2
3
4
5
6
7
8
9
≥10
±
±
±
±
±
Females
Age
(years)
4.6 (2)
5.5 (6)
7.3 (10)
16.2 (5)
2.9 (5)
Males
4.0
3.6
3.3
5.2
5.7
(3)
(4)
(5)
(12)
(8)
Females
(7)
(9)
(11)
(7)
(10)
(8)
(3)
20.9
29.9
39.1
42.8
49.2
60.9
55.9
64.0
59.2
64.5
70.3
Males
1.2 (5)
3.0 (9)
4.9 (19)
4.1 (14)
2.6 (5)
14.8 (8)
7.9 (4)
5.7 (2)
7.5 (3)
0.7 (2)
6.5 (3)
Maine
Quebec
Ontario
Newfoundland
Table 5. Neck girths (mean ± 1 SD) of female and male black bears of different age-classes from Newfoundland, Ontario, Quebec, and Maine.
Atlantic salmon (Salmo salar) that provide North American
bear populations with high dietary energy and protein during the late summer and autumn (Welch et al. 1997; Jacoby
et al. 1999). In a recent study of brown bears, Ferguson and
McLoughlin (2000) also linked higher primary productivity
and the presence of anadromous fishes to larger mass of females in coastal bear populations relative to interior populations. Mainland black bear populations also have access to a
range of food items, but differences in the temporal continuity of dietary protein prior to each growth diapause (i.e., hibernation) may cause mainland populations to be relatively
more protein-limited than Newfoundland bears.
If the average seasonal availability of food is greater for
Newfoundland bears than for mainland populations, then being able to maximize the energy and protein acquired from
plants, caribou and moose calves, capelin, and salmon likely
requires that individuals travel efficiently from one locally
abundant food source to another. Although no work has been
done on body size and travel efficiency in bears, allometric
patterns predict that body size will be generally positively
correlated with cursorial development (e.g., larger lungs and
chest girth and longer limbs), which would enable individuals to move more efficiently over greater foraging distances
(Calder 1984; Schmidt-Nielsen 1994). Furthermore, while
black bears are omnivorous, they are also predatory, and for
solitary terrestrial carnivores there is a strong correlation between maximum prey size and predator body size (Schoener
1969; Vézina 1985). Thus, larger body size in Newfoundland black bears may be a phenotypic response allowing
them to take advantage of abundant but spatially dispersed
dietary protein, and conferring the ability to efficiently kill
large prey.
The shift in body size between Newfoundland and mainland black bear populations may also be linked to current
and (or) historic differences in the strength of interspecific
competition for prey (Abrams 1996; Losos 1996; McPeek
1996). During the past 80 years, black bears have been the
exclusive large carnivore on the island. Wolves were extirpated around 1920, and coyotes (Canis latrans) have been
present on the island only since 1985 (Larivière and Crête
1993). Again, in accordance with one of the assumptions of
Case’s model (Case 1978), limited competition with other
carnivores for large prey during the past 80 years or so may
also have influenced body size in Newfoundland black bears.
Whether or not phenotypic divergence in body size between Newfoundland and mainland black bear populations
is genetically linked remains to be determined. The Newfoundland black bear is currently recognized as a distinct
subspecies (Ursus americanus hamiltoni), based on differences
in skull size and shape (Cameron 1956). More recently,
Paetkau and Strobeck (1996) sequenced eight haplotypes
from black bear populations across North America but could
find no strong phylogenetic split between the Newfoundland
and mainland populations. Still, heritability of body morphology is typically high (approximately 0.50; Roff 1992),
and the larger size of Newfoundland bears could be partially
explained by genetic drift in a small isolated founder population (Paetkau and Strobeck 1996; Slatkin 1996; Lynch et al.
1997). During postglacial colonization of the island, a neutral or nonadaptive mutation in the gene complex regulating
body size may have provided the Newfoundland population
1657
(252)
(145)
(103)
(95)
(46)
(38)
(15)
(13)
(6)
(4)
(12)
Mahoney et al.
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1658
Can. J. Zool. Vol. 79, 2001
Fig. 3. Allometric relationship between male and female body masses for black bears from six geographically separate populations in
North America. The slope of the relationship was greater than 0 (P = 0.03) but not significantly less than 1 (P = 0.21).
with the ability to respond to differences in protein availability,
prey size, and levels of interspecific competition. Alternatively, variation in body size among phylogenetically similar
black bear populations may largely reflect the norm of reaction
to these different environmental selection pressures (Roff
1992; Stearns 1992). We do not know the exact genetic and
environmental factors that led to the phenotypic divergence
in body size between the island and mainland populations,
but we believe that the ability of bears to efficiently exploit
seasonally abundant and spatially dispersed dietary protein
on Newfoundland has been and is still a primary factor.
As in other polygynous species, adult male black bears
are larger than adult females. For body mass, age at the inflection point in females occurred near weaning (i.e., mean
1.8 years), while geometric growth in males did not slow
down until they were approximately 3 years of age. Thus,
although the growth rate in male bears was less than or
equal to that in females, males spent more time growing and
achieved greater asymptotic body mass. Theoretically, the
larger size of male black bears could have evolved from
intrasexual competition for females and (or) the relaxation
of competition for food between females and males (i.e.,
competitive character displacement; Selander 1972; CluttonBrock et al. 1977; Shine 1989). For black bears, however,
the spatial and temporal availability of animal protein, and
phenology and dispersion of nutritious plant items, are expected to be similar for both sexes. This should minimize the
potential for strong niche separation, although whether or
not female and male bears differ in their propensity to prey
on ungulates remains unclear. We believe that sexual size dimorphism in bears has mostly evolved through intrasexual
selection in males for increased competitive abilities and
larger home ranges, which is associated with a polygynous
mating system (see also Bunnel and Tait 1981).
If sexual selection is the key factor explaining most of the
variation in adult body mass in black bears, then we would
expect that an increase in adult size would be associated
with an increase in sexual size dimorphism (Fisher 1958). In
other words, an increase in female mass should be accompanied by a disproportionate increase in male mass, which
would generate an allometric slope greater than 1 (i.e.,
hyperallometry; Fairbairn and Preziosi 1994). Therefore, we
predicted that the allometric relationship between male body
mass and female body mass in black bears should have an
exponent greater than 1. Although tenuous, our results did
not support this prediction, and we found a trend towards
decreasing sexual size dimorphism and increasing body size
among black bear populations (Fig. 3).
In a study on western bobcats (Lynx rufus), Dobson and
Wigginton (1996) also found a tendency for female body
size to increase disproportionately with male body size (i.e.,
slope = 0.85), but as in our results the exponent was not significantly less than 1. The allometric patterns exhibited by
both black bears and bobcats suggest that (an)other factor(s),
besides sexual selection, explain(s) a large amount of the
variation in male body size and the associated sexual size
dimorphism within these species. Because the evolution
of polygyny and large size appear to be quite inseparable
(Leutenegger 1978), we hypothesize that similar allometric
patterns to those for black bears and bobcats can be expected
within other species where the extent of polygyny is tempered
by local environmental conditions. Factors that constrain
polygyny, such as the feasibility of males monopolizing either food resources or females (which depends on the length
of the mating period and the spatial and temporal dispersion
of food or receptive females), will oppose sexual selection
for extreme size in males (Clutton-Brock and Harvey 1978).
Furthermore, these opposing processes may scale differently
among hierarchical levels (Wiens 1989), and population-level
responses to varying local environmental-selection pressures
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Mahoney et al.
may show different allometric patterns than species-level
associations (Ralls 1977; Leutenegger 1978; Fairbairn and
Preziosi 1994; McLoughlin and Ferguson 2000).
Acknowledgments
Our greatest appreciation is extended to the following people
and government agencies who provided body-morphology
data: D. Larsen, T. McCarthy, C. Schwartz, and T. Wettin
with the Department of Fish and Game, Alaska; K. Craig
with the Fish and Wildlife Branch, New Brunswick; M. Obbard
with the Wildlife Research Section, Ontario; H. Jolicoeur
with the Government of Quebec; L. Berchielli with the Wildlife Research Center, New York; and C. McLaughin with the
Department of Inland Fisheries and Wildlife, Maine. We are
heavily indebted to Mr. H. Abbott, who for nearly 10 years
gathered and assembled morphometric data on captured animals in Newfoundland. S. Larivière provided technical assistance during the production of the manuscript. We benefited
from the constructive comments of B. McLaren and two
anonymous reviewers. Funding for this project was provided
by the provincial government of Newfoundland and Labrador, which has continued its commitment to the development
of wildlife science.
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