Biological Journal ofthe Linnean Socieg (1985), 25: 119-167. With 18 figures
Geographic variation in size and sexual
dimorphism of North American weasels
KATHERINE RALLS
Department of zoological Research, National zoological Park, Smithsonian
Institution, Washington, D.C. 20008, U.S.A.
AND
PAUL H. HARVEY*
School of Biological Sciences, University of Sussex, Falmer, Brighton BNl SQG, Sussex
Accepted for publication June 1984
Geographic variation in size (skull length) and sexual dimorphism in Mustela erminea, Mustela frenata
and Mustela nivalis in North America is described and analysed in relation to latitude, longitude,
climatic variables, and sympatry or allopatry of these species. Only erminea increases in size with
latitude; it does so regardless of the presence or absence offrenata or nivalis. Latitude is a better
predictor of size in erminea than available measures of climate, seasonality or prey size. There is no
evidence for character displacement between any pair of species. The sexes covary in size in frenata
and erminea, and probably in nivalis, although geographic variation i n sexual dimorphism occurs in
frenata and erminea. The principal cause of sexual dimorphism appears to be sexual selection for large
size in males rather than the high energetic requirements resulting from an elongate body shape.
However, prey size may constrain female size (and possibly also male size). Regional differences in
the abundance of prey during the growth of young weasels may affect adult size much more in
males than in females and contribute to geographic variation in sexual dimorphism.
- Mustela - size
geographic variation.
KEY WORDS:-Weasel
Bergmann’s Rule
-
-
sexual dimorphism - character displacement -
CONTENTS
Introduction . . . . . . . . . . . . . . .
Materials and methods.
. . . . . . . . . . . .
. . . . . . . . . . . . . . . . .
Results
. . . . . . . . . .
Distributions of the species.
General characteristics of the sample . . . . . . . .
Geographic variation in size and sexual dimorphism
. . . .
. . . . . . . . . .
Covariation between sexes.
Covariation between species . . . . . . . . . .
The influence of climate . . . . . . . . . . .
The influence of prey size . . . . . . . . . . .
Sexual dimorphism in mustelids in relation to body size and elongation
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*Current address: Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS.
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0024-4066/85/060119
+ 49 $03.00/0
0 1985 The Linnean
Society of London
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K. RALLS AND P. H. HARVEY
Discussion. . . . . . . . . . . . . . .
Behaviour, life history, and ecology of the three species . . .
Main patterns in size and sexual dimorphism in North America.
Factors influencing size and sexual dimorphism. . . . .
Acknowledgements
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References. . . . . . . . . . . . . . .
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INTRODUCTION
Three species of weasels occur in North America: Mustela erminea, the ermine
or stoat; Mustela frenata, the long-tailed weasel; and Mustela nivalis*, the least
weasel. M . erminea and nivalis have holarctic distributions but frenata is found
only in the New World.
In Alaska and much of Canada, erminea is sympatric with the smaller nivalis;
in the southern part of its range it is sympatric with the larger frenata (Fig. 1).
Both nivalis and frenata occur in the central portion of the most southern parts of
erminea’s range; frenata occurs alone beyond the southern limits of the ranges of
the other two species.
Erminea is one of the most variable North American mammals in size: an
average male of the subspecies arctica weighs four times as much as one of the
subspecies muricus (Hall, 1951). In general, the larger individuals belong to the
northern subspecies and the smaller to the southern subspecies. Frenata is also
quite variable in size, but nivalis shows comparatively little variation in size in
North America (Hall, 1951). Nivalis does, however, vary considerably in size in
Europe and the U.S.S.R (King, 1975a, 1980).
These mustelids comprise a series of related predators with different body
sizes but similar hunting strategies. Rosenzweig (1966) termed such a group a
“hunting set” and argued that differences in size are probably important in
enabling the species of such a set to coexist.
Both Rosenzweig (1968) and McNab (1971) undertook quantitative analyses
of size variation in North American weasels as part of multispecies surveys.
Rosenzweig was unable to account for much of the variation in erminea in terms
of either competition with other weasel species or the size of potential prey items
and concluded that latitude and mean annual temperature were the best
predictors of size in this species. McNab, however, concluded that competition
and prey size were the main determinants of size in all three species and
interpreted latitudinal size variation in erminea and nivalis in terms of latitudinal
variation in these factors. More recently, Simms (1979) has also argued that size
variation in erminea is a consequence of the size of available prey which may, in
some areas, be influenced by competitive interactions with both frenata and
nivalis.
Males are larger than females in all three species throughout their ranges.
Two principal hypotheses have been put forward to explain this sexual
dimorphism: the first proposes that size differences between the sexes function
primarily to reduce intersexual competition for food (Brown & Lasiewski, 1972;
Powell, 1979), while the second argues that, because weasels are polygynous,
*The taxonomy of the small, short-tailed weasels of Europe, Asia and North America has fluctuated over
time. Early descriptions list two species, nivalis and rixosa (Hall, 1951). However, Reichstein (1958) concluded
that rixosa was conspecific with nivalis, primarily on the basis of geographic variation in Europe. Hall (1981)
refers to the North American species as nivalis.
VARIATION IN N AMERICAN WEASELS
121
Figure 1 . Distribution of Mustela crminea (vertical lines), Mustela frenafa (horizontal lines) and
Mustela niualzs (circles) in North America (after Hall, 1981).
selection for increased male fighting ability has selected for increased male
weight (Erlinge, 1979; Moors, 1980). It has also been suggested that small size
in females may be favoured by the small size of prey burrows and the energetic
demands of reproduction (Erlinge, 1979; Simms, 1979; Powell, 1979; Moors,
1980; Powell & Leonard, 1983).
Both erminea and frenata show an amazing degree of geographic variation in
sexual dimorphism. In erminea, for example, the skull of the male averages 129%
heavier than that of the female in the subspecies richardsonii but only 33%
heavier in the subspecies anguinae (Hall, 1951). All three species are noteworthy
because they are extremely dimorphic for such small species in at least some
parts of their range: in general, species showing such extreme degrees of sexual
dimorphism tend to be large (Ralls, 1976).
The North American weasels are thus of unusual interest because of the great
variation in size and sexual dimorphism in two of them and the relative lack of
variation (within North America at least) in the third. The conclusions of
previous authors as to the causes of these phenomena are conflicting. The
principal purposes of this paper are to describe quantitatively variation in both
size and sexual dimorphism in more detail than previous studies, using much
larger sample sizes; to reassess the value of latitude, climate, prey species, and
the presence of other weasel species as predictors of size; and to further
understanding of the geographic variation in sexual dimorphism.
122
K. RALLS AND P. H. HARVEY
MATERIALS AND METHODS
Condylobasal skull length was used as a measure of size. Skull length has been
used as a measure of size in other mustelids (Hagmeier, 1958) and has several
advantages over other measures such as head plus body length or weight. Head
plus body length must be estimated from field measurements of total length and
tail length. Skull length can be measured precisely and enables the largest
possible sample size because the many ‘skull only’ specimens in museum
collections can be included. Examination of skulls also allows specimens to be
aged. Product-moment correlation coefficients between skull length and head
plus body length were calculated for both sexes of erminea using the average
values for subspecies given by Hall (1951): the two measures are highly
correlated (males: r = 0.97, N = 19; females: r = 0.98, N = 16). Few weight data
are available because weights are not usually recorded by field mammalogists.
Although weight is a useful measure of size when comparing species that cover a
broad range of sizes, it is often a poor measure for fine-grained comparison
within species or among very similar species because of its high variability
(Ralls, 1976). This is particularly true in weasels, where the weight of individual
animals varies considerably depending upon the time since the last meal,
reproductive condition, season, and other factors (King, 1975b).
The sample includes specimens from the following institutions: Acadian
University Museum; American Museum of Natural History; British Columbia
Provincial Museum; California Academy of Sciences; Carnegie Museum of
Natural History; Field Museum of Natural History; Harvard University,
Museum of Comparative Zoology; Los Angeles County Museum; Manitoba
Museum of Man and Nature; Milwaukee Public Museum; National Museum of
Natural History (U.S.A.); National Museum of Natural Sciences (Canada);
Nova Scotia Museum; Philadelphia Academy of Natural Sciences; Royal
Ontario Museum; San Diego Natural History Museum; University of Alaska
Museum; University of Alberta, Museum of Zoology; University of British
Columbia, Vertebrate Museum; University of California, Berkeley, Museum of
Vertebrate Zoology; University of Illinois; University of Kansas, Museum of
Natural History; University of Michigan, Museum of Zoology; University of
Minnesota, James Ford Bell Museum of Natural History; University of
Montana; University of Wisconsin, Madison, Zoological Museum; and
Universitetets Zoologiska Museum, Copenhagen, Denmark.
Specimens were aged according to the criteria of Hall (1951); only adult
specimens were measured. Condylobasal length of the skull was measured to the
nearest tenth of a millimetre with dial calipers. Most collecting sites were
located to degrees and minutes. Each site was scored as to whether or not it was
within the range of the other two species according to the maps in Hall (1981).
They were also initially scored with respect to the range of Mustela nigripes, the
black-footed ferret. However, the inclusion of this variable resulted in sample
sizes too small for practical use so it was not included in the analysis.
Only erminea occurred on islands. Specimens from islands in Canada’s
Northwest Territories, except for those from the Belcher Islands, were retained
in the sample (49 males and 23 females) but those from Alaskan and coastal
islands were excluded (152 males and 30 females). Primarily because of the
scarcity of specimens, the size offrenata below the southern limits of the United
States was not considered.
VARIATION IN N AMERICAN WEASELS
I23
Some parts of the range of each species in North America provided more data
than others. To minimize possible distortions from this cause, the data were
organized into a grid system centred at the intersections of odd-numbered
parallels and meridians and enclosing two-degree latitude-longitude blocks.
Mean skull length of each sex was calculated for each square from which one or
more specimens were available and assigned to the latitude and longitude at the
centre of the square.
Computer maps were prepared from the data for the square means by the
SYMAP program of Harvard University. This program is designed to produce a
smooth surface through a set of data points which portrays trends or patterns
which those points imply. The interpolation algorithm is complex but is
basically a weighted average of the slopes and values of nearby data points
(Shepard, 1970). In interpreting a SYMAP, one should recognize that it is
perfectly reliable-up to the accuracy of the data points-only at data points.
The wider the spacing of data points, and the greater the fluctuation in data
values from one datum point to its neighbours, the less reliable the SYMAP
becomes. SYMAPS are thus useful primarily for portraying general trends.
Statistical analyses used the means of the squares and both custom written
and SPSS programs (Nie et al., 1975). Statements that effects are significant
indicate that P < 0.05.
Francis and Avis James extracted the climatic data. Sources were as follows:
U.S.A. (except Alaska)-Air Ministry Meteorological Office, London ( 1958),
U.S. Department of Commerce (1965), and Albright (1939); Canada-Canada
Meterological Branch (1965); and Alaska-US. Weather Bureau (1959, 1965).
Simms (1979) has suggested that erminea feeds largely on voles, and that the
size of female erminea covaries geographically with the size of local vole species.
T o test this hypothesis, the geographical distribution and sizes of the various
vole species (27 species belonging to the genera: Clethrionomys, Phenacomys,
Microtus, Lagurus, Lemmus, Synaptomys and Dicrostonyx) were extracted from an
extensive literature by R. Hoffmann (pers. comm.). A list of the vole species in
each of the two-degree latitude-longitude squares for which we had skull lengths
of erminea was compiled. Most vole species show comparatively little
geographical variation in size but there may be considerable size variation
among the adults of a given species at a particular locality because voles
continue to grow throughout their lives (R. Hoffmann, pers. comm.). T o
determine the minimum, maximum, and median size of vole species present in
each square, we listed data on minimum and maximum zygomatic skull breadth
for each species. The minimum values and the maximum values in this list were
used to represent the possible size range for each species. The median for each
species was determined from these ranges; and the smallest, largest, and median
value of these species medians were used as estimates of minimum, maximum,
and median vole size values for each square.
In order to examine predicted relationships between sexual dimorphism, body
size and elongation across the mustelids, data on head plus body length and
body weight for 26 species were taken from Gittleman (1984). The species were:
Mustela erminea, Mustela frenata, Mustela nivalis, Mustela altaica, Mustela sibirica,
Mustela lutreola, Mustela vison, Mustela putorius, Martes americana, Martes pennanti,
Martes zibellina, Gulo gulo, Ictonyx striatus, Poecilogale albinucha, Mellivora capensis,
Meles meles, Taxidea taxus, Mephitis mephitis, Spilogale putorius, Lutra lutra, Lutra
124
K.RALLS AND P. H. HARVEY
canadensis, Lutra enudis, Lutra maculicollis, Lutrogale perspicillata, Aonyx capensis and
Enhydra lutris.
RESULTS
Distributions of the species
The distributions of erminea, frenata, and nivalis according to Hall (1981) are
shown in Fig. 1. Mustela erminea ranges the furthest north and occurs alone in
three regions. Mustela nivalis overlaps much of erminea’s range. Mustela frenata is a
more southern species; it occurs alone over much of its range but overlaps occur
with one or both of the other species in the northern part of its range. For
erminea, but not for the other two species, we have found it convenient to cite
Hall’s (1951) subspecies names in the text when we are comparing our results
with those from other studies. Accordingly, Fig. 2 shows the distributions of
basilar skull length measures for the different erminea subspecies (taken from
Hall, 1951-note, Hall used basilar skull length, that is from the tip of the snout
to the foramen magnum, whereas our measure is the condylobasal skull length
which is longer because the condyles are also included).
Figure 2. Distribution of mainland Musfcla ermincu subspecies after Hall (1981). Numbers on the
figure refer to the following subspecies (average basilar skull lengths in mm for adult males from
Hall (1951) are given in parentheses): 1. M. c. ulusensls (37.5); 2. M. e. nrfica (42.5); 3. M. e. bangsi
(39.7); 4. M . c. cicognunii (35.7); 5. M . c. fullcndu (35.7); 6. M . c. gulosu (32.3-sample also contains
subadult males); 7. M. c. inuicfa (37.0); 8. M. c. muricu (30.6); 9. M. c. olympica (31.8);
10. M . e. poloris (41.3); 11. M . c. richurdsonii (40.9); 12. M.c. scmplei (37.5-sample also contains
subadult males); 13. M.c. strcufori (33.2).
VARIATION IN N AMERICAN WEASELS
I25
Table 1. Average size and other descriptive statistics for all species
Size (skull length, mm)
Sex and species
Mean
Var
S.E.
Skew
Kurt
C.V.
No. squares
Male erminea
Female erminea
Male erminea (tr.)
Female erminea (tr.)
Male frenata
Female frenata
Male nivalis
Female nivalir
42.50
36.79
43.07
37.15
48.98
43.56
32.02
29.90
10.30
6.34
3.55
3.29
5.19
9.20
2.93
1.52
0.20
0.19
0.17
0.16
0.17
0.26
0.24
0.19
-1.05
-0.15
0.20
0.87
0.05
0.71
0.17
-0.07
1.27
0.53
-0.55
0.37
0.25
0.41
0.60
-0.75
0.24
0.17
0.08
0.09
0.11
0.21
0.09
0.05
253
181
126
126
183
141
50
43
tr. = Data truncated by removal of small skulls as explained on page 131.
General characteristics of the sample
The sample consisted of 1541 male and 546 female erminea, 1146 male and 498
female frenata, and 137 male and 86 female nivalis. Reducing these data to the
means for two-degree squares resulted in the smaller sample sizes shown in
Table 1. The small sample size for nivalis and the unequal sex ratios reflect the
composition of museum collections. Male weasels are more readily trapped than
females: “the heavy mechanism and wide spacing of conventional traps select for
males, and, in addition, females may be more trap-shy” (King, 1 9 7 5 ~ ) The
.
data in Table 1 illustrate the well-known facts that frenata is the largest and
nivalis the smallest of the species, that males are larger than females in all three
species, and that nivalis is considerably less variable in size than the other two
species (Hall, 1951). The distributions of our samples for each sex of each species
mapped by 2” squares are shown in Fig. 3.
The average degrees of sexual dimorphism (measured as male skull length
divided by female skull length or as male skull length minus female skull length)
calculated from the sexual dimorphism values for the individual squares, agree
well with those calculated from the average values for male and female size
(Table 2). Erminea is the most dimorphic of the species, on the average, and
nivalis is much less dimorphic than the other two species.
Geographic variation in size and sexual dimorphism
Mustela erminea
Main patterns
Three broad geographic patterns are clear from the SYMAPS of male
(Fig. 4A) and female (Fig. 4B) size: ( 1 ) males are larger than females; (2) both
sexes tend to be larger towards the northern part of the range; (3) both sexes are
extremely small in much of the southwestern portion of the range. These
patterns agree well with the previous descriptions of Hall (1951).
Analyses of variance
The presence or absence of frenata and nivalis has been portrayed as a major
influence on the size of erminea (McNab, 1971). It has also been suggested that
size patterns shown by erminea in the east might be less clear or absent in the
126
K. RALLS AND P. H. HARVEY
A
Figure 3. 2" latitude-longitude squares for which data were available for A, male Mustela erminea; B,
female M . crminea; C, male M.frmala; D, female M.frenota; E, male M. nivalis, and F, female
M. nivalis.
127
VARIATION IN N AMERICAN WEASELS
west because of the extreme altitudinal variation in this region (McNab, 1971;
Simms, 1979). In order to investigate possible effects of other species and
longitude, we compiled the average size of male and female errninea (using single
values for each sex from each 2" square) in all possible combinations of the
presence and absence of the other species in both the east (of 105"W) and the
west (Table 3). Subjecting these data to a four-way analysis of variance resulted
in three significant main effects on size (Table 4): sex, presence or absence or
frenata, and presence or absence of nivalis. There were also two significant
interaction effects with longitude.
All of the significant effects can be understood in terms of the three main
patterns of size variation shown by the SYMAPS (Fig. 4A, B). Sex accounts for
Table 2. Average degree of sexual dimorphism and other descriptive statistics
for all species
Sexual dimorphism
Measure and species
From size
means
Mean
Var
S.E.
Skew
5.64
5.43
1.96
3.84
4.63
2.90
0.16
0.20
0.36
-0.65
-0.53
1.11
Male skull length/female skull length x 100
M . erminea
116
115
M . frenata
112
112
M . niualis
107
107
31.05
31.79
33.58
0.46
0.51
1.21
-0.42
-0.26
1.31
Kurt
C.V.
No. squares
0.59
0.28
5.87
0.68
0.85
1.48
146
122
23
0.70
-0.04
6.19
0.27
0.28
0.31
146
122
23
~~~
Male skull length-female skull length (mm)
M . erminea
M . frenata
M . niualis
5.71
5.42
2.12
128
K. RALLS AND P. H. HARVEY
129
VARIATION I N N AMERICAN WEASELS
Figure 4. Skull length variation in the three Mustela species across North America. Data are
incorporated into SYMAPS (see text) where different areas correspond to particular condylobasal
skull lengths. Arrows on contours point to areas of decreasing size and dotted lines demarcate
islands with similar size skulls. A, Male M. nminea. Size classes are I = < 34 mm; 2 = 34-37 mm;
3 = 37-40 mm; 4 = 40-43 mm; 5 = >43 mm. Based on data from squares indicated in Fig. 3A. B,
Female M . errninea. Size classes are I = < 34 mm; 2 = 34-37 mm; 3 = 37-40 mm; 4 = > 40 mm.
Bascd on data from squares indicated in Fig. 3B. C, Male M . frenata. Size classes are 1 = < 44 mm;
2 =44-47 mm; 3 = 47-50 mm; 4 = 50-53 mm; 5 = > 53 mm. Based on data from squares
indicated in Figure 3C. D, Female M . frenata. Size classes are 1 = < 41 mm; 2 = 41-44 mm;
3 = 44-47 mm; 4 = 47-50 mm; 5 = > 50 mm. Based on data from squares indicated in Fig. 3D. E,
Male M. niualis. Size classes are 1 = < 30 mm; 2 = 30-32 mm; 3 = > 32 mm. Based on data from
squares indicated in Fig. 3E. F, Female M. nivalis. Size classes are 1 = < 30 mm; 2 = > 30 mm.
Based on data from squares indicated in Fig. 3F.
Table 3. Size and slope of regression of size on latitude for male and female
erminea in relation to longitude and the presence or absence offrenata and niualis
Male
Species combination
Size (skull length, m m)
+frenata niualis
frenata - niualis
-frenata niualis
-frenata -niualis
+
+
+
Regression slope
+f r e n a ~ a+niualis
frenata - niualis
-frenata niualis
-frenata - niualis
+
+
East ( < 105")
42.12
41.25
42.76
43.74
0.1020
0.2466
0.1393
0.0445
Female
West ( 3105")
42.43
37.74
43.74
42. I 1
0.6259
0.4019
0.0336
0.2426
East
West
35.76
36.92
36.35
38.48
36.75
33.50
38.33
37.01
-0.0850
0.1998
0.0654
0.1423
1.oooo
0.3499
0.1522
0.1810
K. RALLS AND P. H. HARVEY
130
Table 4. Summary of analyses of variance on size and slope data for erminea
Size
Slope
Source
d.f
F
P
&=
d.f.
F
Sex
1,5
235.64
23.19
10.58
I .67
1.50
1.01
1.81
3.97
6.59
17.74
0.001
0.005
0.02
0.76
0.07
0.04
1,5
0.04
4.61
0.07
6.19
0.00
0.12
0.47
0.60
3.92
1.50
frenata
nivalis
Longitude
Sex x frenata
Sex x niualis
Sex x longitude
frenata x nivalis
frenata x longitude
niualis x longitude
0.05
0.009
Multiple rz = 0.88
P
&=
0.20
0.06
0.27
Multiple rz = 0.49
most of the variation (76%). This is because of pattern one (above): males are
larger than females. The second main effect is that erminea is smaller when frenata
is present. This results from pattern two: erminea is smaller in the south of its
range and frenata only occurs in this portion of its range (Fig. 1 ) . Although
erminea is smaller when frenata is present under every combination of conditions,
there is an interaction effect with longitude: erminea is smaller in the presence of
frenata in the west than in the east. This effect results from pattern three: erminea
is extremely small in the southwestern portion of its range. The third main effect
is that erminea tends to be smaller in the absence of nivalis. However, the
interaction effect of nivalis with longitude is stronger, in terms of F value, than
the main effect. This is because erminea is only consistently smaller when nivalis is
absent in the west. This effect also results from pattern three: nivalis is absent
from the southwestern portion of the range where erminea is very small.
Because erminea tends to be larger in the north of its range (Hall, 1951;
Rosenzweig, 1968; McNab, 1971; Fig. 4A, B ) , we compiled a table of the
regression slopes of size on latitude (Table 3) corresponding to the table of
average sizes. The importance of latitude was underscored by the fact that 15 of
the 16 slopes are positive. Both sexes of erminea tend to increase in size with
latitude in the east and the west, regardless of the presence or absence of other
species. A four-way analysis of variance (ANOVA) (Table 4) showed a
significant effect with longitude: slopes are steeper in the west. This effect results
from pattern three: the very small erminea in the southwest of the range, and also
possibly the relatively large erminea in the northwest of the range. There was no
effect of sex on slope.
The degree of sexual dimorphism, expressed as male size divided by female
size, shown by erminea in the same combinations of longitude and species
occurrence used for size and slope is shown in Table 5. A three-way ANOVA of
these data yielded no significant effects (Table 6). This suggests that males tend
to be larger than females by a constant amount throughout the range of the
species and is consistent with the lack of effect of sex in the slope analysis.
Relationships with latitude
The maps and analyses of variance indicated that both male and female size,
but not the degree of sexual dimorphism, increased significantly with latitude. A
VARIATION IN N AMERICAN WEASELS
131
Table 5. Sexual dimorphism and slope of
regression of sexual dimorphism on latitude in
erminea in relation to longitude and presence or
absence of other species
Species combination
East
West
Sexual dimorphism (male skull length/female skull length)
frmata nivalis
1.178
1.160
frenata -nivalis
1.115
1.132
-frenata nivalis
1.173
1.168
-frcnata -nivalis
1.140
1.134
+
+
+
+
Regression slope
frcnala nivalis
frcnata -nivalis
-frcnata nivalis
-frenata -nivalis
+
+
+
+
0.009
0.003
- 0.00 1
-0.003
-0.053
0.004
-0.001
0.0 13
more detailed picture of these relationships is provided by Figs 5A, B & 6A.
Both male and female size show a relationship with latitude that is non-linear
due to a group of squares with very small average skull length-below 39 mm
for males and 34 mm for females. With one exception, these points represent the
extremely small specimens from the southwestern portion of the range
(Fig. 4A, B). We excluded these points and calculated best-fit lines to the
remaining values for both sexes. Both lines have a slope of -0.13, supporting
the earlier indications that, on the average, there is a constant difference in size
between the sexes. However, the ratio of male to female size is not quite
independent of latitude. Sexual dimorphism measured as a difference (male
skull length minus female skull length) remains an average of 5.9 mm over the
latitudinal range from 80" to 35" N, whereas sexual dimorphism measured as a
ratio (100 x (male skull length divided by female skull length)) should increase
very slightly over the same ranges from 1 15 to 117.
Correlation coefficients of male size, female size, and sexual dimorphism with
latitude are given in Table 7. The correlation coefficients for the two measures
of sexual dimorphism do not differ significantly. Although both measures of
sexual dimorphism show a positive Spearman's correlation with latitude when
all data are included, this relationship disappears when the very small skulls are
excluded. Thus it is due to the small erminea in the southwestern portion of the
Table 6. Summary of analyses of variance on sexual dimorphism and slope data
for erminea
Sexual dimorphism
Source
Longitude
frenata
niualis
Longitude x frenata
Longitude x nivalis
frenala x niualis
d.f.
1 9 1
F
0.1 1
0.66
18.29
0.07
0.81
0.45
P
Slope
E2
d.f.
F
1,1
0.92
0.92
1.80
2.68
2.83
0.69
P
E2
I32
K. RALLS AND P. H. HARVEY
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(ON)
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55
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35
VARIATION IN N AMERICAN WEASELS
133
Table 7. Correlation coefficients of male size, female size, and sexual
dimorphism in erminea with latitude. Sample sizes between 100 and 300
Size (skull length)
Correlation coefficient
and data used
Spearman (all)
Pearson (all)
Spearman (tr)
Pearson (tr)
Sexual dimorphism
Male
Female
Male-female
Male/female
0.67
0.63
0.56
0.57
0.67
0.69
0.25
0.15
(0.12)
(0.01)
0.15
(0.05)
0.52
0.61
tr. = Data truncated by removal of small skulls as explained on page
( ) = not significant.
(0.03)
(0.10)
131
range, which are not only small but have a particularly low degree of sexual
dimorphism.
Regional variation in sexual dimorphism
As Hall (1951) pointed out, considerable variation in the degree of sexual
dimorphism does exist across North America but analyses showed no consistent
relationships between the degree of sexual dimorphism and latitude, longitude,
or the occurrence of other species.
Sexual dimorphism can be caused by variation in the size of either sex. For
example, a high degree of sexual dimorphism can result from males being
unusually large, females being unusually small, or both. To distinguish between
such effects, we mapped squares where sexual dimorphism was high
(100 x (male skull length divided by female skull length) greater than 120) or
low (less than 110) and those where male or female size was more than 3%
above or below that predicted by the regression of size on latitude (see
Table 8). Two areas are particularly obvious on the resulting map (Fig. 7): the
northwestern portion (A) where male size, female size, and sexual dimorphism
are all greater than expected, and the southwestern portion (C) where all three
variables are smaller than expected. In the extreme southeast there is an area
(E) with low sexual dimorphism because of small males and large females, and
in the middle of the southern portion one with high sexual dimorphism due to
large males (D). However, no clear pattern emerged over most of the
northcentral and northeastern portions of North America (B), possibly because
our sampling intensity was too low in relation to the scale of patterns in this
area.
Mustela frenata
Main patterns
The SYMAPS (Fig. 4C, D) suggested that frenata size was not related to
latitude. This is in agreement with previous reports (Hall, 1951; Rosenzweig,
1968; McNab, 1971).
Figure 5. Skull length variation as a function of latitude in the three Mustela species. Individual
points refer to average sizes of skulls from individual 2" squares (see text). Dots refer to data from a
single square and figures denote the number of squares at that latitude with the same average skull
length. A, Male M . errninea; B, Female M . erminea; C, Male M.frenata; D, Female M.frenata; E ,
Male M . nivalis; F, Female M . nivalis.
K. RALLS AND P. H. HARVEY
134
135
A
0
130
0
0
:
0
0
0
12c
0
IIC
0
0
Ioc
9c
O
0
0
0
10
I
1
60
40
Latitude
I05
-
:
(ON)
0
0 . 0
0
3
0 0
0
0
0
0
.
0
0
0
0
0
0
1
1
-I
95-
60
50
30
40
Latitude
(ON)
3
VARIATION IN N AMERICAN WEASELS
135
I30
C
0
0
0
oe
55-
120-
0
2
0
0
0
0
2
$
a
0 . 0
0
0
0
0
2
Latitude (ON)
Figure 6. Variation in sexual dimorphism of skull length as a function of latitude in the three
Muslela species. Constructed as Fig. 5. A, M . erminea; B, M . frenata; C, M . erminea.
Anabses of variance
The average size of male and female frenata in all possible combinations of the
presence or absence of erminea and nivalis in the east and the west is shown in
Table 9. A four-way ANOVA on these data yielded three significant effects: sex,
presence or absence of nivalis, and longitude, as well as three significant
interaction effects (Table 10). Sex accounted for most of the variance: males are
always larger than females. Mustela frenata is larger in the presence of nivalis
except in the east where erminea is absent; it is also larger in the west, and this
effect is greater when erminea is present.
Although the SYMAPS suggested that the size of frenata had no overall
relationship with latitude, an analysis of variance of the slopes shown in Table 9
showed that frenata did increase significantly in size with increasing latitude
Ta.ble 8. The number of squares in areas A to E on Fig. 7 with particularly large
or small skulls and high or low degrees of sexual dimorphism in erminea.
Latitudinal effects are removed (see text)
Area
A
B
C
D
E
Male (large/small)
2213
7/23
2/29
7/1
218
Female (large/small)
Sexual dimorphism
(highllow)
K. RALLS AND P. H. HARVEY
136
Figure 7. Areas classified in Table 8 by size and sexual dimorphism of Mustela erminea skull sizes
related to those expected for that latitude (see text). In area A male and female skulls are large and
sexual dimorphism is high; in area B male and female skulls tend to be small and sexual dimorphism
is slightly above average; in area C male and female skulls are small and sexual dimorphism is low;
in area D male skulls are large, females about average and sexual dimorphism is high; in area E
females tend to be large, males are small and sexual dimorphism is low.
when niualis was present (Table 10). M . frenata size also increased with latitude
when erminea was present but this effect was dependent on longitude.
An ANOVA on the data in Table 11 gave no significant results, indicating
that the degree of sexual dimorphism in frenata is not consistently related to
latitude, longitude, or the presence or absence of other species.
Relationships with latitude
Plots of male size against latitude (Fig. 5C) and the lack of significant
correlations (Table 12) confirmed that there was no relationship between these
Table 9. Size and slope of regression of size on latitude for male and female
frenata in relation to longitude and the presence or absence of erminea and nivalis
Male
Female
East ( < 105")
West ( 2 105")
East
West
Size (skull length, mm)
niualis erminea
niualis -crminea
- niualis erminea
- nivalis- erminea
48.96
48.63
48.26
50.63
5 I .28
49.61
48.09
48.71
43.19
42.61
41.87
45.54
47.93
(45.50)*
42.70
43.63
Regression slope
nivalis erminea
niuolis -erminea
- nivalis erminea
- niualis -erminca
0.161
0.106
0.086
-0.353
0.107
0.325
0.058
-0.045
0.596
0.318
0.659
-0.471
0.366
Species combination
+
+
+
+
+
+
+
+
* No data.
(
) * = only one datum point: no regression coefficient could be calculated.
*
0.098
0.099
VARIATION IN N AMERICAN WEASELS
137
Table 10. Summary of analyses of variance on size and slope datafrenata
Size
Source
d.f.
F
Sex
niualis
erminea
Longitude
Sex x niualis
Sex x erminea
Sex x longitude
niualis x erminea
niualis x longitude
erminea x longitude
1,4
288.99
10.65
0.86
9.30
0.96
0.03
4.03
24.96
29.47
9.46
Slope
P
E?
d.f.
F
0.001
0.74
0.04
0.01
0.04
1,4
4.07
8.24
6.55
0.06
0.38
1.24
0.34
4.97
0.03
8.00
0.03
0.04
0.009
0.007
0.04
Multiple r = 0.89
P
EZ
0.046
0.20
0.17
0.048
Multiple r = 0.50
variables. Although the correlation between female size and latitude was small,
it was significant (Table 12, Fig. 5D). There was no clear correlation between
sexual dimorphism and latitude (Fig. 6B, Table 12).
Regional variation in size and sexual dimorphism
To describe geographical patterns in size and sexual dimorphism, we mapped
squares where sexual dimorphism, male size and female size lay in the upper or
Table 11. Sexual dimorphism and slope of
regression of sexual dimorphism on latitude in
frenata in relation to longitude and presence or
absence of other species
Species combination
Sexual dimorphism
niualis + erminea
+ nivalis -erminea
- niualis erminea
- nivalis- erminea
+
1.140
1.145
1.156
1.113
+
Regression slope
niualis erminea
+ niualis - erminea
- nivalis + erminea
- niualis - erminea
+
East
+
-0.009
-0.008
-0.009
-0.001
West
1.081
(1.099)
1.127
1.084
-0.016
*
0.001
0.014
* N o data.
( ) = Only one square.
Table 12. Correlation coefficients of male size, female size, and sexual
dimorphism in frenata with latitude
Size (skull length)
Sexual dimorphism
Correlation coefficient
Male
Female
Male-female
Male/female
Spearman
Pearson
(0.04)
(0.06)
0.16
0.19
( - 0.04)
( -0.04)
(-0.06)
(-0.07)
(
6
) = Not significant.
K. RALLS AND P. H. HARVEY
i38
Figure 8. Areas classified in Table 13 by size and sexual dimorphism of Mustela frenala. In area A
male and female skull sizes are small and sexual dimorphism is low. I n area B male and female skull
sizes are large and sexual dimorphism is low. In area C male and female skulls are small and sexual
dimorphism is high.
lower 12.5% of each distribution. Three geographical areas (Fig. 8) were
demarcated by these extreme data (see Table 13): a western region with small
males, small females, and intermediate sexual dimorphism (A); a central region
with large males, very large females, and low sexual dimorphism (B); and an
eastern region with intermediate sized males, small females and high sexual
dimorphism (C). Average male size, female size, and sexual dimorphism for
each of these regions are given in Table 13.
Table 13. Female size, male size, and sexual dimorphism for frenata in the three
regions of North America shown in Fig. 8
Female size
Region
A
B
C
Male size
Mean skull
length (mm)
S.E.
X
41.88
46.29
41.50
0.24
0.29
0.30
51
49
42
Percentage of squares in
area with:
A
B
C
Small 0
(G40mm)
Large 9
(>48mm)
31
0
31
0
29
2
Mean skull
length (mm)
46.75
50.85
48.00
Sexual dimorphism
S.E.
X
0.24
0.22
0.24
59
71
56
Expected Calculated from squares
(from means) mean
S.E.
N
1.12
1.10
1.16
Percentage of squares in
area with:
SmallJ
( C 4 6 mm)
46
1
13
Large J
( Q 52 mm)
0
37
0
1.12
1.09
1.16
46
33
38
0.007
0.006
0.010
Percentage of squares in
area with:
Low S.D.
( C 1.06)
high S.D.
( 21.20)
9
15
8
0
2
42
VARIATION IN N AMERICAN WEASELS
139
Table 14. Size and slope of regression of size on latitude for male and female
nivalis in relation to longitude and the presence or absence of erminea and frenata
Male
Species combination
East
West
East
West
+
+
32.441
32.067
30.267
30.25
(33.10)
32.52
30.08
30.71
29.10
29.10
29.70
29.68
+
+
-0.136
0.025
0.014
-0.500
-0.234
0.009
-0.043
Size (skull length, mm)
frenata erminea
+frenata -erminea
-frenata erminea
-frenata -erminea
Regression slope
+frenata erminea
+frenata -erminea
-frenata erminea
-frenata - erminea
+
Female
*
*
*
*
0.302
*
*
*
*
*
*
-0.129
*
* N o data.
( ) = Only one square.
Mustela nivalis
Main patterns
The SYMAPS showed no overall tendency for niualis to increase in size
towards the north, despite the presence of some large specimens in Alaska
(Fig. 4E, F).
Analyses of variance
Because of the very limited data on this species, it was not possible to carry
out analyses of variance similar to those for erminea and frenata. Average skull
size showed no consistent relationship with longitude and the presence or
absence of other species; it did not always increase with latitude (Table 14).
Although the data on sexual dimorphism were sparse, they suggested no
consistent influence of any of these variables (Table 15).
Relationsh$s with latitude
Female, but not always male size showed an overall negative correlation with
latitude (Fig. 5E, F, Table 16). Both measures of sexual dimorphism were
positively correlated with latitude (Fig. 6C, Table 16).
Table 15. Sexual dimorphism and slope of
regression of sexual dimorphism on latitude in
nivalis in relation to longitude and the
presence or absence of other species
Species combination
East
West
Sexual dimorphism (Male skull length/female skull length)
+frenata erminea
1.058
1.060
+frenata -erminea
1.058
(1.103)
-frenata + erminea
( I ,043)
1.103
-frenata -ermines
*
*
Regression slope
+frenata + erminea
0.004
-0.009
+frenata -erminea
0.006
*
-frenata erminea
*
0.013
-frenata -erminea
*
*
+
+
*No data.
( ) = Only one square.
K. RALLS AND P. H. HARVEY
140
Table 16. Correlation coefficients of male size, female size, and sexual
dimorphism in nivalis with latitude
Size (skull length)
Correlation coefficient
Spearman
Pearson
(
Sexual dimorphism
Male
Female
Male-female
Malelfemale
( -0.06)
-0.44
-0.38
0.37
0.54
0.42
0.55
(0.11)
) = Not significant.
Regional variation in size and sexual dimorphism
The small sample size made it impossible to identify areas of high and low
sexual dimorphism or areas where either sex was unusually large or small.
Covariation between sexes
Male and female size are significantly correlated in North American erminea
and frenata but not nivalis (Table 1 7 ) . The relationship between male and
female skull length in erminea andfrenata is illustrated in Fig. 9A, B. Although
frenata occurs only in the New World, both erminea and nivalis are holarctic in
distribution. Data on the size of erminea in Europe and the U.S.S.R., taken from
the literature, have been included in Fig. 9A; they correspond well to the trend
shown by the North American points, indicating that male and female size are
correlated throughout the range of the species, although the largest erminea occur
outside North America. Plotting data on nivalis (assuming that it is conspecific
with rixosa) throughout its range shows that male and female size tend to covary
in this species as well (Fig. 9C); the lack of a significant correlation between
these measures in the North American sample may be due to restricted size
range and small sample size from the species in this region.
Covariation between species
Allopatry and gmpatry.
The analysis of variance on erminea size showed that both sexes are smaller
when frenata is present and larger when nivalis is present (Table 4).There are at
least two possible ihterpretations of these results: ( 1 ) they are due to character
Table 17. Correlation coefficients between male and female size in all species
Correlation coefficient
Pearson
Species
enninea
erminea (tr.)
frenata
nivalis
Spearman
rP
N
P
0.74
0.59
0.63
0.09
146
126
122
23
<0.001
<0.001
<O.OOl
0.33
tr. = Data truncated by removal of small skulls as explained on page
rs
N
P
0.65
0.54
0.60
0.2I
146
126
122
23
< 0.00I
<0.001
131.
<0.001
0.17
VARIATION I N N AMERICAN WEASELS
141
A
45-
40 -
*-
30
35
40
45
Female skull length (mm)
Female skull length ( m m )
Female skull length (mm)
Figure 9. The relationship between male and female skull length in samples of the three Mustela
species. A, Mustela erminea from North America (a),U.S.S.R. (A)and Europe (m). Individual
points for the North American data are means of 2" squares. The points from U.S.S.R. and Europe
refer to different sampling localities; data were extracted from Fairley 1971, Fog 1969, Heptner &
Naumov 1967, King pers. comm., Kratchovil 1977a, Miller 1912, Petrov 1956, Reichstein 1958,
van Soest & van Bree 1970, van Soest et al. 1972 and Vershinin 1972. B, Mustelafrenata from North
America. Individual points are means of 2" squares. C, Mustela nivalis ( = M . rixosa) from North
America, U.S.S.R. and Europe. Individual points for the North American data are means of 2"
squares. The points from U.S.S.R. and Europe refer to different sampling localities; data were
extracted from Barbu 1968, Beaucourmu & Grulich 1968, Fog 1969, King 1977, Kratchovil 1977b,
Miller 1912, Morozova-Turova 1965, Reichstein 1958, Stroganov 1962.
displacement, and (2) they result from latitudinal effects (or those of variables
correlated with latitude) and their correlation with the presence or absence of
the other two species is coincidental. For example, the largerfrenala occurs only
in the south of erminea's range where erminea is small due to the latitudinal effect.
Several lines of evidence support the latter conclusion.
A
7 d
. *...,.....
.....
.
.
, ..
. *,.. . ..
*
0.
4
5
-
> !
:=
:
6
1).
>60°N
40
.. ...
35
- 2 3
I65
145
491
,
E
*.
5 4 5 2 :
-E
- .
P
-
2
I05
125
85
e.
,
>60"N
6561
..*,*+.*
............
. . . . ..**.'. . . . . ,.. ... .
. . ................
45-60°N 5
I
30
165
I
,
I
I
145
125
I05
85
I1
6561
I
E
t
a*.
40
321
165
49
- 100
x
&!
E951
165
130
$
E
E
1.
> 60W
0
35
a
,*
0 110'
I
145
I
I
I
125
105
85
'
.'
7:
I
6561
P
E
1
0
I
145
I
125
. I
105
I
85
I
6561
45
..,
35 32
-:
I
I
i
..
I
.*
I
I
I
. .*
.s
0.
..
Longitude
I
(OW)
1..
001
Longitude (OW)
Figure 10. Variation in skull length (A, male; B, female and C, skull length dimorphism) with longitude for Mustela eminea. The data are presented in three blocks of latitude:
> 60"N, 45-60"N and < 45"N. Data are averages for particular 2" squares. 8 Mustela nivalis absent, 4 Mustela frenata absent, 0 M . nivalis and M . frenata absent,
M.
nivalis and M . frenata present.
+
VARIATION IN N AMERICAN WEASELS
3
143
3
Figure I I . Variation in skull length of Mustela erminea in the southwestern portion of the species
range in North America. Data points are average skull lengths for 2" squares. The subspecies
recognized by Hall (1951) in this region are also indicated.
First, there is the analysis of variance on the slopes of the regression of erminea
size against latitude in the presence or the absence of the other species.
M . erminea increases in size with latitude regardless of the presence or absence of
the other species (Table 3); these species have no significant effects on the slope
of the regression (Table 4).
Second, plotting skull length against longitude in three latitudinal strips gave
similar results for both males (Fig. 10A) and females (Fig. 10B). Various species
combinations occur for any given skull length and neither size nor sexual
dimorphism (Fig. 1OC) is closely related to changes in species composition.
Third, a more detailed consideration of size variation of male erminea in the
southwestern part of the range is also informative. Hall (1951) describes two
small subspecies, streatori and muricus, and a larger subspecies, invicta, from this
region. Our data conform to this description (Fig. 1 1 ) . M . erminea's remarkable
size transitions in this area do not coincide with a change in species composition:
frenata is present and nivalis absent over most of this region.
Finally, we looked more closely at areas where species combinations changed.
There are three regions where a transition occurs between an area where erminea
occurs alone and one where it occurs together with nivalis: southeastern Canada,
the Northwest Territories, and southeastern Alaska and western Canada
(Fig. 1). We mapped male size at collecting localities in these regions.
Inspection of the map for southeastern Canada (Fig. 12) suggests that if any
difference in size exists between erminea in these two areas, the species might be
slightly larger where it occurs alone. The picture on the mainland agrees with
the analysis of variance and the SYMAP. *
I n the Northwest Territories, no consistent size difference appears between
* Hall 1951, states that erminea in Newfoundland are the same size as those on the neighbouring mainland
and refers them to the same subspecies, richardsonii; in fact, errninea in Newfoundland might be slightly larger
than those on the mainland.
144
K. RALLS AND P. H. HARVEY
Figure 12. Average skull lengths of male Mustela crminca in sampling localities with (shaded) and
without Mustela niualis in southeastern Canada. Localities with more than five skulls marked by a
triangle.
the two areas (Fig. 13). This region was divided between the eastern and
western samples in the ANOVA. Hall (1951) recognizes two subspecies in this
region: arctica, which is sympatric with nivalis over some of its range, and semplei,
which occurs alone. He states that arctica is larger than semplei. However, his
subspecies boundary does not coincide with the range limits of nivalis and his
arctica includes the very large erminea in Alaska. The pattern produced by the
SYMAP in this region is complex, with no consistent size trend across the range
limits of nivalis.
In southeastern Alaska and western Canada, the map is consistent with the
view that erminea are smaller where they occur alone but the data are too sparse
to be convincing (Fig. 14). Although the analysis of variance indicated that
Figure 13. Average skull lengths of male Musfcla crminca in sampling localities with (shaded) and
without Mustela niualis in the Northwest Territories. Localities with more than five skulls marked
with a triangle.
VARIATION IN N AMERICAN WEASELS
145
Figure 14. .4verage skull lengths of male Musfela errninea in sampling localities with (shaded) and
without Musfelu niualis in Alaska and Canada. Localities with more than five skulls marked with a
triangle.
western erminea are larger in the presence of nivalis, all the very large erminea in
Alaska, which are sympatric with nivalis, are included in our western sample.
Hall (1951) describes a transition in this area between the small alascensis and
the larger richardsonii; the SYMAP also suggests a trend towards larger
individuals as one moves west.
There are two regions in North America where a transition exists between an
area where erminea occurs alone and one where it occurs together with frenata:
southeastern Canada and the northeastern U.S.A., and southwestern Canada
and the northwestern U.S.A. (Fig. 1). Both the SYMAP and the locality map
(Fig. 15) suggest that erminea is indeed larger where it is found alone in the
eastern region. Hall (1951) shows a transition between the subspecies invicta and
the larger richardsonii in this region. However, erminea would also be expected to
be larger where it occurs alone, towards the north, because of the latitudinal
effect. In the western region (Fig. 16),the few data points available show little
or no consistent differences in size of erminea between the areas with and without
frenata.
In sum, the locality maps of erminea size in boundary areas do not provide
evidence for the character displacement hypothesis. In one area the size
difference seems to be the opposite from that predicted by this hypothesis; in
two areas there appears to be no size difference across the boundary of another
species’ range; in one area the data are consistent with a difference in the
predicted direction but are too sparse to be convincing; and in the one area
where there is a fairly clear size difference in the predicted direction it is also
predicted by the latitudinal hypothesis.
The data on the other two species also provide little support for the character
displacement hypothesis, as the presence or absence of congeners do not have
consistent effects. Some areas of large frenata occur both towards the north
K. RALLS AND P. H. HARVEY
146
401
74
.
.
60
Figure 15. Average skull lengths of male Mwtcla crminea in sampling localities with (shaded) and
without Mwtela frenata in the eastern U.S.A. Localities with more than five skulls marked with a
triangle.
where errninea is present and towards the south where it is absent (Fig. 4C,
4D). The analysis of variance confirms that there is no effect of erminea on frenata
size (Table 10). It does suggest an effect of nivalis but this is not consistent, since
it is lacking in the east when erminea is absent (Table 9).
The character displacement hypothesis predicts that nivalis should be larger in
the absence of errninea. This is difficult to test because errninea is present
Figure 16. Average skull lengths of male Mustela enninca in sampling localities with (shaded) and
without Mwtclafrenata in the western U.S.A. and Canada. Localities with more than five skulls
marked with a triangle.
VARIATION IN N AMERICAN WEASELS
147
Table 18. Correlation coefficients between size (skull length) of female frenata
and male erminea and between female erminea and male nivalis
Correlation
Pearson
Pair
Female frenatamale erminea
Female ermincamale niualis
Spearman
TP
x
P
rs
N
P
0.20
73
0.04
0.20
73
0.05
0.19
23
0.20
0.27
23
0.12
throughout so much of nivalis' range (Fig. 1). The small sample size for nivalis
made it impossible to perform an analysis of variance. However, in the absence
of erminea, male nivalis are slightly smaller in the east and female nivalis are
slightly larger in both the east and the west (Table 14). Both male and female
nivalis are larger in the absence of frenata in the west but not in the east
(Table 14).
Couariation in v m p a t y
In a pair of sexually dimorphic species such as weasels, the larger sex of the
smaller species and the smaller sex of the larger species are the closest in size and
should be the closest competitors. If the character displacement hypothesis is
true, one would expect these pairs to covary in size. Although a significant
correlation exists between the size of male erminea and femalefrenata (Table 18),
plotting the data shows that it is entirely due to the very small erminea and
frenata which occur in the southwestern portion of erminea's range (Fig. 17). The
size of female erminea and male nivalis are not significantly correlated (Table 18).
.. .. .. .. .
...; .: ..:..i . .
8
[I
..
..
* "
351
30
8 . .
I
*:.
. .
..
.
I
1
Figure 17. The relationship between male Mustela erminea skull length and female Mustela frenata
skull lengths. Data are average lengths from different 2" squares where samples of both species were
available.
I48
K. RALLS AND P. H. HARVEY
Correlations between the extent of sexual dimorphism, measured both as male
skull length minus female skull length and male skull length divided by female
skull length, in pairs of species are given in Table 19. There were few significant
correlations. Sexual dimorphism in erminea, measured as male skull length minus
female skull length, did show a significant negative relationship with sexual
dimorphism in frenata with both Pearson’s and Spearman’s coefficients. Again,
however, this appeared to be due mainly to the very small individuals in the
southwestern portion of erminea’s range, because the correlation decreased in
magnitude and became non-significant when these were excluded.
The inzuence of climate
Introduction and methods
Because climate has been shown to be correlated with size in some other
mammalian species (see Clutton-Brock & Harvey, 1983) and because of the
likelihood that the correlation of size with latitude in erminea reflects climatic
influences, we explored the relationship between size in all species and a variety
of climatic measures such as wind, sun, precipitation, solar radiation, and wet
and dry bulb temperature. Average values for most of these measures were
available for January, April, July, October, and the entire year.
Our procedure was investigative: we sought correlations between skull length
or sexual dimorphism with these climatic measures. Coefficients of variation of
the various climatic measures across months were included as measures of
seasonality because the latter has been suggested as a general source of
increasing size with latitude (Boyce, 1978, 1979). Both Spearman’s Rank
Coefficient and Pearson’s Product Moment Coefficients were calculated. The
former reveal increasing or decreasing functional relationships while the latter
also measure deviations from linearity (Feller, 1957). Differences between the
two coefficients thus suggest the presence of non-linear relationships. Only the
Spearman’s coefficients are presented. Analysing the erminea data as the
truncated sample (see page 131), removed one source of non-linearity: that
between latitude and skull length in this species. Correlations were calculated
for both measures of sexual dimorphism but only those for male skull length
divided by female skull length are presented because those for male skull length
minus female skull length were very similar.
The results of the analyses are given in Tables 20 and 21. Correlations
between size and sexual dimorphism with latitude and longitude are also shown
for comparison. Only the highest of the monthly correlations are shown; the
months are indicated in parentheses. Non-significant relationships (P> 0.1, onetailed) are enclosed in parentheses. However, we do not give much credence to
statistical significance here because values for contiguous squares are unlikely to
be independent. In the following account we draw attention to the largest
absolute correlations with size and sexual dimorphism in each species.
Size
As expected, differences between the Spearman’s and Pearson’s (not shown)
coefficients indicated numerous non-linear relationships between the climatic
measures and skull length in erminea when the full data set was used, while use of
the truncated set produced correspondence between the two coefficients. Dry
Table 19. Correlation coefficients between sexual dimorphism in skull length in species pairs in the same twodegree squares
Pearson’s
frmata
Spearman’s
frenata
nivalis
nivalis
rs
x
P
rs
x
P
Sexual dimorphism measured as male skull length minus female skull length
enninea
-0.22
48
0.06
0.41
13
0.08
erminea (tr.)
-0.05
31
0.39
0.40
12
0.10
frenata
-0.27
15
0.17
-0.17
-0.03
48
31
0.13
0.43
0.60
0.56
-0.19
13
12
15
0.02
0.03
0.25
Sexual dimorphism measured as male skull length divided by female skull length
erminea
-0.31
48
0.02
0.32
13
0.14
erminea (tr.)
-0.21
31
0.13
0.30
12
0.17
frenah
-0.28
15
0.16
-0.28
-0.17
48
31
0.03
0.19
0.41
0.32
-0.29
13
12
15
0.08
0.15
0.15
‘P
N
P
rP
x
P
e
0
01
Table 20. Correlations of size (skull length) with climatic variables for all species. The highest correlation within each category
is underlined
mninea (tr.)
mninea
Male
Latitude
Longitude
0.67
Male
0.67
(0.17)
0.31
Climate
Wind (m/h)
Sun (h/month)
Precipitation (in)
Solar radiation
(Langley's/day)
Dry bulb T"F
Wet bulb T"F
-0.69 (AL)
-0.49 (AP)
Seasonality
Wind
Sun
Precipitation
Solar radiation
Dry bulb T"F
Wet bulb T"F
-0.24
0.46
-0.33
(0.05)
0.32
0.5 1
0.35
-0.26
-0.54
-0.24
Female
(AL)
(OC)
(JA)
(OC)
0.37
-0.28
-0.42
-0.45
0.56
0.32
(AL)
(JU)
(JA)
(JU)
0.24
-0.19
-0.62
0.31
-0.64 (AL)
-0.38 (AP)
( -0.11)
(-0.07)
-0.45
(-0.12)
(0.13)
0.35
(AL)
(JU)
(JA)
(AL)
-0.68 (AL)
(-0.12)
(-0.15)
-0.18
(-0.06)
0.33
JA =January, AP = April, JU =July, O C = October; AL
( ) = non-significant.
Q a
= ALL
niualis
frmlo
Female
Male
Fernale
0.52
0.23
(0.04)
(-0.04)
0.28
-
(-0.09) UU)
-0.24 UU)
-0.35 UU)
-0.27 UU)
-0.35 (AL)
(-0.08) (AP)
(0.02)
-0.20
a
( -0.05)
(-0.12)
(0.00)
(average for year).
0.26
0.15
-0.20
0.19
Male
0.16
(OC)
-0.12
0.14
-0.33
0.20
UA)
UA)
UA)
( -0.06)
UA)
UA)
(AP)
(AL)
(-0.05) UA)
0.15 UU)
(-0.10) UA)
(0.11) (AP)
(0.05)
(-0.16)
0.18
-0.19
(0.03)
(0.04)
-0.13
(-0.081
'
0.18'
(-0.07)
0.12
(-0.06)
(0.02)
(0.16) (JU)
0.50 (JA)
(-0.20) (AL)
-0.28 (JU)
0.29 (JA)
(0.14) (AL)
( - 0.07)
-0.43
0.56
-0.41
( -0.17)
( -0.02)
Female
--0.44
F
-0.23
(-0.12)
-0.35
0.40
-0.33
UA)
(AP)
UU)
UU)
0.41 (OC)
0.54 (AL)
(0.1 1)
-0.42
(0.02)
-0.40
-0.28
-0.36
>
Z
U
151
VARIATION IN N AMERICAN WEASELS
Table 2 1. Correlations of sexual dimorphism (male skull length/f'emale skull
length) with climatic variables for all species. The highest correlation within
each category is underlined. Units and abbreviations as in Table 20
erminea
Latitude
Longitude
Climate
Wind
Sun
Precipitation
Solar radiation
Dry bulb T"F
Wet bulb T"F
Season
Wind
Sun
Precipitation
Solar radiation
Dry bulb T"F
Wet bulb T"F
0.15
(0.02)
0.31 (OC)
-0.26 (OC)
-0.39 (JA)
(0.11 UA)
-0.50 (AL)
-0.48 (AL)
-0.24
( -0.06)
(-0.07)
( -0.05)
0.35
0.40
-
errninea (tr.)
(0.03)
(0.07)
0.25 UU)
-0.24 (OC)
-0.34 CJA)
0.26 (AL)
-0.44 (AL)
-0.45 (AL)
(-0.14)
( -0.05)
(0.01)
(-0.08)
0.34
0.40
-
frenata
( -0.06)
- 0.31
0.32 (AL)
-0.18 UU)
0.41 (AP)
-0.28 (AL)
0.11 UA)
0. I 7 (OC)
0.24
(0.02)
[ -0.03)
(0.05)
-0.19
(0.04)
niualis
0.42
0.48
-0.34 UA)
0.66 (AP)
-0.74 (AL)
(0.21) (OC)
-0.70 (OC)
-0.75 (IA)
-0.41
(0.21)
(0.30)
(0.02)
0.46
0.56
-
bulb temperature is negatively correlated with size to about the same extent
that latitude is positively correlated except in the truncated female sample.
Precipitation shows a similar negative correlation with size. Wet bulb
temperature seasonality is well correlated with male size and precipitation
seasonality with female size. However, these correlations are smaller than those
of size with latitude. This does not, of course, imply that size changes in response
to latitude per se, merely that the climatic measures used were less reliable
predictors of size than latitude.
There are no strong correlations betweenfrenata size and any of the climatic
measures: the highest correlation is 0.33. Wind speed is positively correlated
with male size and precipitation is negatively correlated with female size. There
are no seasonality effects.
Female nivalis show a negative correlation between size and latitude. The
highest values for this species are the positive correlations between solar
radiation and male size, precipitation seasonality and male size, and wet bulb
temperature and female size.
Sexual dimorphism
Both dry and wet bulb temperature are negatively correlated with sexual
dimorphism in erminea, as is precipitation. The temperature relationship
accounts for about 20% of the variance in sexual dimorphism. Sexual
dimorphism is positively related to temperature seasonality, the correlation with
wet bulb temperature being slightly higher than with dry bulb temperature.
Sexual dimorphism in frenata is positively correlated with precipitation; this
relationship accounts for about 15% of the variance.
Sexual dimorphism in nivalis is positively correlated with both latitude and
longitude: each accounts for about 20% of the variance. Several climatic
variables show strong relationships with sexual dimorphism: both wet and dry
bulb temperature are negatively correlated, as is precipitation, while solar
K . RALLS AND P. H. HARVEY
152
radiation is positively correlated. Each of these measures accounts for about
50% of the variance in sexual dimorphism. Temperature seasonality is positively
correlated with sexual dimorphism but accounts for only about 30% of the
variance.
The influence of
prv size
The prey size hypothesis, which argues that geographic variation in some
particular component of prey size determines variation in weasel size, is difficult
to falsify because it has been stated in very general terms. We chose to
concentrate our efforts on erminea because Fitzgerald (1977) and Simms (1979)
have suggested that it is a vole specialist.
We first attempted to obtain evidence against the hypothesis by determining
whether or not structures related to feeding increased in size with latitude along
with skull length. This analysis was prompted by Barnett’s (1977) finding that
in grey squirrels, Sciurus carolinensis, skull length increased in size with latitude
while the size of several structures related to feeding did not. He interpreted this
as a reflection of the relatively constant size of the principal nuts eaten by this
species throughout its range. In erminea, however, the size of the structures
related to feeding is highly correlated with skull length and both increase with
latitude in much the same way (Table 22), so we were unable to rule out the
prey-size hypothesis by this analysis.
If a cline in prey size is indeed the cause of erminea’s tendency towards larger
size in the north, then the average size of vole species should increase with
latitude and vole species should be very small in the southwest portion of
Table 22. Correlations of skull measurements in male erminea with latitude and
each other. Based on a sample of 48 skulls, eight from each of the 3 mm
categories shown in Fig. 4
Skull measures
“Feeding measures”
1
Latitude
Skull measures
I
2
3
4
5
6
7
8
9
2
“Non-feeding measures”
8
9’
10
3
4
5
6
7
0.794 0.809
0.787
0.832
0.818
0.800
0.750
0.776
0.981
0.940
0.945
0.967
0.964
0.931
0.970
0.978
0.964
0.974
0.986
0.971
0.937
0.961
0.953
0.944
0.944
0.925
0.940
0.947
0.940
0.964 0.736 0.941
0.931 0.711 0.926
0.910 0.698 0.914
0.934 0.705 0.929
0.915 0.691 0.918
0.991 0.748 0.978
0.914 0.747 0.924
0.750 0.983
0.739
0.421
0.780
* This measurement proved difficult to make accurately which probably accounts for the low correlations
between it and other measures.
Measurements were taken as follows: 1, length of lower jaw from condyle to anteriormost point of canine; 2,
length of anterior half of skull from posterior-most point of last molar to anterior edge of base of incisors; 3,
length of upper carnassial; 4,width across upper canines at base; 5, width at posteriormost point of carnassials;
6,total skull length from condyle to anterior edge of base incisors; 7, width at condyles; 8, posterior half of
skull, measurement 6 minus measurement 2; 9, width at mastoid processes; 10, length from condyle to base
of orbit.
153
VARIATION IN N AMERICAN WEASELS
Table 23. Correlation coefficients (r,,) of vole size with latitude and of erminia
size with vole size and latitude
Vole size (skull width)
Minimum
Median
Maximum
Latitude
No. of squares
0.396
0.727
0.586
-
302
0. I44
0.342
0.397
0.539
0.314
0.283
0.634
0.668
266
195
Latitude
Erminea
(skull size)
Male
Female
erminea's range. Vole size does increase with latitude and vole size is also
correlated with erminea size (Table 23). However, as with our measures of
climatic variation, latitude is a better predictor of errninea size than any of our
vole size measures.
Although erminea size thus appears to be related to vole size throughout its
range in North America, a plot of female erminea size against median vole size
(our most highly correlated measures) suggest this relationship may not be a
close one (Fig. 18) and the southwestern area of very small erminea could not be
defined in terms of the vole species present.
Sexual dimorphism in mustelids in relation to body size and elongation
Existing analyses of the possible relationships between sexual dimorphism in
mustelids and body size (Moors, 1980) and the degree of elongation (Powell,
1979) are confounded by (1) including the same variables on both axes, and (2)
equal weighting of points that represent different taxonomic levels. We therefore
examined these relationships across genera within the family Mustelidae and
across species within the genus Mustela using both regression and reduced major
5 40-
i
e
c
3 38-
.*
.*
t
n
0
36Ql
=E
e
LL
34-
32t
I
30
13
..
:.I.
I
I!
14
15
I
I
I
I
I6
17
18
19
Median vole skull width (mml
I
20
I
Figure 18. The relationship between female Murfcla ermanea skull length and the estimated median
skull length of the median sized vole species across 2" squares for which data on both variables are
available.
154
K. RALLS AND P. H. HARVEY
Table 24. Relationships between sexual dimorphism and body size and degree
of elongation across genera in the family Mustelidae and across species within
the genus Mustela. Data for 14 genera and 26 species were taken from Gittleman
(1984). Generic points are means of values for the species within the genus.
Relationships across genera of mustelids are identified by capital letters; those
within the genus Mustela by small ones. L = head plus body length, W = body
weight, SD(W) = dW/$?W, SD(L) = dL/$?L.Null hypothesis for t-test is that
the observed slope equals the expected slope
Variables Cy,x)
Correlation
coefficient (r)
Slope ( b )
Expected
slope
d.f.
t value
for slopes
A
a
0.996***
0.992***
0.936
0.960
1.000
1 .ooo
12
6
2.59*
0.79
B
0.947***
0.926***
0.987
0.868
I .ooo
1.000
12
6
0.14
0.91
b
-0.581*
-0.199
C
C
D
d
0.281
0.165
E
e
0.923***
0.625
0.314
0.183
0.333
0.333
12
6
0.508
1.600
F
f
0.954***
0.443
0.239
0.134
0.333
0.333
12
6
1.52
1.79
G
0.281
0.165
g
*P<0.05;***P < 0.001.
axis analysis. The latter is generally preferable when the variables cannot be
identified as dependent or independent on the basis of the distribution of error
(Harvey & Mace, 1982). However, in the present case, correlations between
pairs of variables were so high that the results of the two types of analysis were
very similar and only the results of the regression analysis are shown in
Table 24.
If sexual dimorphism changes with body size, then a plot of log (male size)
against log (female size) should have a slope significantly different from one.
Sexual dimorphism tends to decrease with increasing body size across genera of
mustelids using weight as a measure of size but not using head plus body length
(Table 24). Sexual dimorphism is not significantly related to body size within
the genus Mustela using either measure (Table 24), though sample sizes are very
much smaller. Correlations between sexual dimorphism and the two size
measures give a similar picture (Table 24).
For animals of the same general shape, length is proportional to the cube root
of weight, that is,
or
length = k x
log (length) = log (k)+0.33 (log (weight))
where k is a constant. If the degree of body elongation varies with body size,
then a plot of log (length) against log (weight) should have a slope significantly
VARIATION IN N AMERICAN WEASELS
155
different from 0.33. The degree of elongation does not vary with body size across
genera of mustelids in either males or females or within the genus Mustela
(Table 24). Again, the small intrageneric sample size allows only weak inference
from the statistical test.
Sexual dimorphism is not correlated with the degree of elongation (calculated
from body weights and lengths averaged from the two sexes) either across
genera or across species within the genus Mustela (Table 24).
DISCUSSION
The results presented in this paper must, ultimately, be interpreted in terms of
the life history, behaviour and ecology of weasels. Thus, we briefly review these
topics, concentrating our attention on results that are relevant to our later
discussion. We then present a summary of our results on variation in size and
sexual dimorphism of the three North American species. Taken together, the
review and summary permit an examination of the possible effects of climate,
sympatry, and allopatry on size and sexual dimorphism in these species, and of
prey size on erminea size. There has been previous discussion of the effects of
these factors as well as others, such as habitat type and the degree of polygyny,
on weasel morphology. Our data do not provide information on the latter
topics. However, in the light of our correlational evidence, we shall comment on
various hypotheses and point out profitable areas for future research.
Behaviour, lqe history, and ecology of the three species
Feeding and population regulation
All three species are predators which hunt mainly for rodents, lagomorphs
and birds. There is now sufficient evidence for the generalization that the larger
species, and the larger sex within a species, feeds disproportionately on larger
prey (see Anon, 1976; Simms, 1979 for reviews). Most dietary studies have been
on European populations, but these are not readily translatable across the
Atlantic because erminea in North America are appreciably smaller than
elsewhere (see Fig. 9A), because frenata is restricted to North America, and
because prey species differ between the two continents. Nevertheless, we shall
mention some of the more informative European studies before considering the
situation in North America.
Day’s (1968) study compared the diets of nivalis and erminea in the U.K. and
differences were impressive: voles and mice comprise more of niualis’ diet than
erminea’s (57% compared with 23%) and the position is reversed for the larger
birds and lagomorphs (33% compared with 61%). Although a variety of prey
may be taken by individuals through the year, Day reported that 91% of the
two species’ gut contents contained specimens of only a single prey type.
The birds and lagomorphs taken by nivalis were almost all taken by males.
Such feeding niche differences between the sexes, which have also been recorded
in erminea (see, for example, Erlinge, 1979), tend to become emphasized as prey
become increasingly scarce (Anon, 1976; Erlinge, 1979). Female erminea tend to
do more hunting of small prey in burrows than do males (Teplov, 1948; Erlinge,
1977a) although this is not true in all localities: for example, Fitzgerald (1977)
found that both sexes of the small erminea from the Sierra Nevada mountains in
California are subnivean (beneath snow cover) vole feeders.
I56
K. RALLS AND P. H. HARVEY
The more carnivorous members of the order Carnivora have larger homerange sizes and lower population densities than the others (Gittleman &
Harvey, 1982; Gittleman, 1984) and this provides circumstantial evidence that
populations are regulated in size by their food supplies. Other indirect evidence
for food as a population regulating factor comes from the reduction of erminea
populations following the introduction of myxomatosis which drastically
reduced the U.K. rabbit population Ueffries & Pendlebury, 1968; Craster,
1970; Hewson, 1972), and from the reduction of niualis populations when small
rodents became scarce Ueffries & Pendlebury, 1968; Craster, 1970).
Interactions between niualis and erminea have rarely been recorded in the wild.
It is, of course, possible that they compete for the same food sources, in which
case the larger erminea is likely to be more successful at direct or interference
competition (King & Moors, 1979) while niualis should be able to hunt smaller
prey into restricted spaces such as prey burrows. However, there is a dearth of
evidence combined with much speculation (e.g. King & Moors, 1979) about
interactions between the two species in Europe.
Erminea is sometimes considered to be a vole specialist in North America
(Fitzgerald, 1977; Simms, 1979), and Simms even claims that female erminea are
optimally sized vole predators which show parallel geographical variation in size
with their prey so that they can chase voles down burrows. The data on which
Simms’ speculations are based are scant and not totally convincing, but he may
be correct.*
The two major dietary studies in North America both involve erminea and
frenata. Fitzgerald (1977) studied the two species in the Sierra Nevada (across an
area containing the very small erminea (Fig. 1 l ) ) , and concluded that during the
winter both species feed mainly on voles (Microtus montanus) in the subnivean
space. Erminea seemed particularly dependent on voles as food because, when
vole population density was low, a higher proportion of the population was
removed by erminea. Simms’ (1979) study in southern Ontario also pointed to
the importance of voles (Microtus pennsyluanicus) as erminea’s staple diet; even in
areas where Peromyscus species were common, erminea preyed primarily on voles.
From a series of tunnel trials, Simms concluded that, in the areas where they
were found, there were no subnivean spaces or vole tunnels that female erminea
could not penetrate. Frenata, however, had a much more varied diet, feeding in
part on larger prey such as rabbits and birds.?
* It is, however, unlikely that Simms is wholly correct when he claims that European erminea too are vole
specialists, feeding on the water vole, Arvicola terresfris, and that this accounts for the larger size of erminea in
Europe. Many feeding and gut content analyses from various parts of western Europe, including the British
mainland where erminea is particularly large, reveal that it is not a vole specialist, even less a water vole
specialist (Day, 1968; Anon, 1976; Erlinge, 1979; King & Moors, 1979). However, recent work in southern
Sweden reveals a clear preference by male (but not female) erminea for water voles (Erlinge, 1981) and Klimov
(1940) states that water voles are also a major food supply of erminea in Western Siberia.
tSimms (1979) also considered that food availability limits the distribution of the mustelids. The northern
limit offrenata is, he argued, set by snow cover: beyond their northern range subnivean spaces are too small for
frenata to hunt successfully and above the snow they are outcompeted by larger and more arboreal mustelids.
However, Gamble (l981), showed that the distribution limits used by Simms were incorrect. Incorporating
additional distribution records, he concluded that snow cover was not a barrier to frenah. Simms also
hypothesized that interference competition favours frenafa in some areas of sympatry with erminea, as well as
limiting the southward spread of mninea. Niualis supposedly ranges south because of its higher reproductive
potential (see below). Simms’ hypotheses are interesting and merit further testing. The possibility of
competition restricting sympatry offrenata and mninea is underscored by the fact that “a straight line drawn
from southern Peru to northern Greenland reveals a linear overlap of only 9.7% for M. erminea and 6.8% lor
M.frenafa” (Simms, 1979).
VARIATION IN N AMERICAN WEASELS
157
Breeding ecology and l$e history
It seems likely that most mustelids have the same basic pattern of territoriality
(Powell, 1979), although of the three species under discussion only erminea and
nivalis have been studied in any detail. In the summary below, data are from
direct or telemetric observations of wild animals in Europe, except for Erlinge’s
(1977b) results on an enclosed population in southern Sweden.
For most of the year a proportion of the males and all the females hold
territories (Lockie, 1966; King, 1975b; Erlinge, 1977a). Male territories are
larger than female territories and contain roughly two to five contiguous female
territories (King, 1975b; Erlinge, 1977a). Territoriality is intrasexual for the
most part so that females defend their territories against other females while
males defend theirs against other males (King, 1975b; Erlinge, 1977a). Outside
the breeding season, males are dominant to females and have reasonably free
access to female territories, but in the latter stages of pregnancy and when the
female has very small young, dominance relationships are reversed and females
defend their territories against males as well as other females (Lockie, 1966;
Erlinge, 197713). Intrasexually, established animals are probably dominant to
transients, although among the males (but not the females) age and weight also
seem to influence dominance (Erlinge, 1977b). Indeed, recent work in southern
Sweden (M. Sandell, pers. comm.) suggests that some older males (2 years and
above) may abandon their own territories in the breeding season and roam
through those of subordinate younger males (one year old), mating with
receptive females. Territories may break down in winter after which time young
males disperse to breed away from their natural area while young females
remain to set up territories the following spring.
There is one important difference in breeding ecology between nivalis and the
other two species. Mustela nivalis females mature in the year of their birth and
young born early in the season can produce a litter later that summer (see King
& Moors, 1979); the gestation period is 36 days and adult females can produce
two litters a year (Heidt et al., 1979; King & Moors, 1979). M . erminea and
frenata, however, have delayed implantation so that they can produce only one
litter a year (Wright, 1942, 1948; Rowlands, 1972; Muller, 1970). Five-week-old
pre-weaned erminea can have fertile matings (Muller, 1970) so mother and
daughter may be mated by the same male-the mother in late spring and the
daughter in early summer (Erlinge, 1977a). Male erminea do not mate until the
year after their birth (Erlinge, 1977a). Mothers raise their young without help
from males (Powell, 1979; Erlinge, 1979). Given the annual breakdown of
territories, the movement patterns of the males (M. Sandell and S. Erlinge,
pers. comm.), and the high mortality rates of both sexes (Kopein, 1967; Erlinge,
1977a), it is unlikely that young females are mated by their fathers but this must
remain a possibility.
Main patterns in size and sexual dimorphism in North America
In order of increasing size, the species are nivalis, erminea, and frenata. In each
species the male is larger than the female and, whether sexual dimorphism is
measured as a size ratio or an absolute size difference between the sexes, erminea
is slightly more dimorphic than frenata on the average, but nivalis is much less
158
K. RALLS AND P. H. HARVEY
sexually dimorphic than the other two species. The results are in general
agreement with the descriptions in Hall (1951).
Mustela erminea
The species increases in size with latitude, so it is largest in Alaska and follows
Bergmann’s Rule. Previous workers have also found this trend (Hall, 1951;
Rosenzweig, 1968). The size (measured as a length) increase with latitude is
roughly linear except for a n area in the southwest of the species’ range where
both sexes are extremely small. There are no obvious ecological, geographical,
or climatic correlates which might be used to explain why erminea is so small in
this area.
The sexes covary in size so that the size of one sex is generally a good
predictor of the size of the other, in spite of the geographical variation in sexual
dimorphism. We find it useful to interpret these variations in terms of the
expected size of each sex, that is, whether the males and/or the females in a
particular area are larger or smaller than would be expected from the
relationship of size with latitude.
Latitude seems a very good predictor of body size, and none of the climatic
variables used, which include measures of temperature, precipitation, wind,
sunlight, and seasonality, is a significantly better predictor of body size than is
latitude. Rosenzweig (1968) was also unable to find a climatic variable which
was a better predictor of size than latitude. The median size of the vole species
present increases with latitude and vole size is correlated with erminea size. Once
~.
-predictor of erminea size than is vole size.
again, however, latitude is a better
Changes in the size of errninea do not appear to be correlated with the presence
or absence of frenata or nivalis, contrary to the claims of McNab (1971), nor do
these species covary in size or sexual dimorphism with erminea.
Mustela frenata
Unlike erminea, frenata does not increase in size with latitude. This agrees with
previous work (Hall, 1951; Rosenzweig, 1968; McNab, 1971). We can find no
clear pattern of change in size or sexual dimorphism with the presence or
absence of erminea and nivalis, nor does the species covary in size or sexual
dimorphism with either of these species when sympatric. There are no clear
climatic correlates of body size in frenata; this agrees with the results of
Rosenzweig ( 1968).
As in erminea, the sexes covary in size. However, there are three broad areas
with different degrees of sexual dimorphism: in the west sexual dimorphism is
intermediate and both sexes are small; in the east sexual dimorphism is high and
females are small; and in the middle of the range sexual dimorphism is small
and while males are large, females are very large.
Although climatic variables account for as much as about ‘20% of the
variation in sexual dimorphism, given the regional variation and consequent
non-independence inherent in the data, we conclude that climate is not a very
useful predictor of sexual dimorphism.
Mustela nivalis
Our sample size for nivalis is relatively small compared with those for erminea
and frenata, although larger than that used in previous studies.
VARIATION IN N AMERICAN WEASELS
159
The species does not increase in size with latitude, contrary to the claim of
McNab (1971) that it did so when frenata was absent. Female size actually shows
a negative correlation with latitude. However, given the small sample size and
probable non-independence of adjacent squares coupled with fairly large
variation in size, this result may be an artifact. Rosenzweig (1968) found that
both male and female size were negatively correlated with latitude, but his
sample sizes were even smaller than ours. Although we found some correlations
with climatic variables, the small sample size allows no clear conclusions to be
drawn.
We can find no evidence for the presence or absence of frenata or erminea
correlating with changes in size or sexual dimorphism in nivalis. Similarly, there is no
apparent covariation between frenata or erminea and nivalis body size or sexual
dimorphism when it is sympatric with either of the other two species. Again, we
caution that small sample sizes may mask any pattern.
The sexes do not significantly covary in size within North America but this
may be a consequence of the small variation in size range in our data-when
samples from Europe and the U.S.S.R. are included, clear covariation is
apparent .
Factors inJuencing size and sexual dimorphism
Size
Bergmann’s Rule: Mustela frenata does not increase in size with latitude in North
America. Mustela nivalis does not increase in size with latitude in either North
America or over most of Europe (Kratochvil, 1977a, b); in fact the species
decreases in size with latitude in Sweden (Stolt, 1981). Mustela erminea shows a
striking conformance with Bergmann’s Rule in North America but not in
Ireland (Fairly, 1981) or the U.S.S.R. (Petrov, 1962). It is difficult for most
general explanations of Bergmann’s Rule to account for these facts. McNab
(1971) provided a possible explanation with his claim that “a positive
correlation of size and latitude is usually found in small carnivores beyond the
northern limits of the larger species of the same set”. However, our data do not
substantiate his claim, although weasels were one of his main examples (see the
section on character displacement below).
Although Bergmann’s (1847) original explanation of this type of pattern is
now discredited, several alternative hypotheses have been suggested. These are
reviewed in Pyke (1978) and Clutton-Brock & Harvey (1983). One explanation
of Bergmann’s Rule is proposed by Boyce (1979) who points out that
environments become more seasonal at higher latitudes. Perhaps larger animals
are able to survive periods of food scarcity in seasonal environments. We found
no evidence to support this hypothesis even with respect to erminea in North
America: latitude is a better predictor of size than seasonality in any climatic
variable. McNab (1971) believed that erminea’s increase in size with latitude was
due to a corresponding cline in the size of its prey, but he presented no data on
prey size. We found that the size of vole species does increase with latitude. Vole
size also correlates with erminea size. However, latitude is the best predictor of
both vole size and erminea size. Furthermore, the relationship between vole size
and erminea size does not appear to be a close one and we could detect no
relationship between vole size and the southwestern area with very small erminea.
160
K. RALLS AND P. H. HARVEY
We are unable to reach firm conclusions about causal relationships based on
these correlations. Although we cannot falsify the prey-size hypothesis, we are
also unable to present really convincing evidence in its favour. This may be
because our vole-size measures, although perhaps the best possible with the data
available from the literature, are still too crude. Two potential prey-size
averages at various geographical points were calculated by Rosenzweig ( 1968):
the mean size of all species likely to be eaten by any weasel species and that of
those likely to be eaten by each individual weasel species. Neither average was a
good predictor of weasel body size but Rosenzweig was hesitant to say that prey
size was of no possible consequence because of the “somewhat arbitrary and
artificial nature of these variables”. This problem is likely to plague future
studies of prey size: exactly what aspect of prey size should be best correlated
with predator size? Our vole-size measures are probably more appropriate
measures of prey size than are Rosenzweig’s, but other measures might be even
more suitable (such as the size of the most common prey species or some other
species eaten mainly during the most critical season or in years when prey are
scarce).
Character displacement: McNab (197 1) claimed that erminea increased in size with
latitude only in the absence of the larger frenata. His study was justly criticized
by Grant (1972) who commented: “The evidence for character displacement is
no more than suggestive. . , the data are inadequate. . . In the graphs relating
body size to latitude. . . the lines drawn are biased towards showing [expected]
change in body size. More detailed study is required to substantiate the
character displacement hypothesis”. Our more detailed study completely failed
to support this hypothesis: erminea increases in size with latitude regardless of the
presence or absence of either frenata or nivalis and several analyses showed no
evidence of character displacement.
These results lead us to be wary of statements about weasel size that invoke
character displacement either in North America or elsewhere. For example,
Hutchinson (1959) and Williamson (1972) point out that erminea is smaller in
Ireland, where it occurs alone, than on the British mainland, where nivalis is also
present. Both authors view the difference as tentative evidence for character
displacement. However, it is now apparent that erminea from the south of
Ireland are similar in size to those on the British mainland-it is only in the
north of Ireland that erminea is so small (Fairly, 1981).Similarly, King & Moors
(1979) argue that erminea is usually smaller in western North America than in
Britain because the largerfrenata is present in western North America and that,
since nivalis is absent, erminea occupies its niche. However, we can identify other
areas in North America where large erminea are found in the presence of frenata
(e.g. parts of British Columbia and Alberta) and other areas where small erminea
are found with nivalis (e.g. in northern Saskatchewan).
Our results with respect to character displacement are part of a general
failure to confirm this phenomenon. Re-examination of the classical cases of
supposed character displacement has failed to substantiate earlier claims (Grant,
1972, 1975; Harvey et al., 1983). Strong et u1. (1979) concluded that there were
only two known instances where morphological differences between two species
showed the pattern predicted by the character displacement hypothesis, one
between a pair of congeneric skinks (Huey & Pianka, 1974; Huey et al., 1974)
and the other between two snail species (Fenchel, 1975). Although recent work
VARIATION IN N AMERICAN WEASELS
161
casts some doubt on the snail example (Levinton, 1982) other authors have
suggested some additional possible instances (Fuentes & Jaksic, 1979; Patterson,
1981; Perrin, in press).
Covariance between the sexes: The factors producing the major geographic trends
in body size appear to be similar for both sexes as male and female size covary
within each species. Moors’ (1980) claim that “the optimum sizes of males and
females are likely to vary independently” is thus incorrect, although particular
selective pressures expected to affect primarily one sex may contribute to the
geographical variation in sexual dimorphism.
Sexual dimorphism
Reasons f o r sexual dimorphism: We have already mentioned the major hypotheses
suggested to explain the fact that male weasels are larger than females. Here we
assess the evidence that allows us to distinguish between the two major
hypotheses (the reduction of intersexual competition for food, and intrasexual
selection favouring larger body size in males).
Brown & Lasiewski (1972) point out that weasels have sacrificed metabolic
efficiency by evolving an elongate body shape which enables them to enter
confined spaces in search of prey. They argue that the increased energy needs
arising from this body shape increased intersexual competition for food, which
in turn led to the evolution of sexual dimorphism in body size. O u r data on
erminea size and vole size provide no support for this hypothesis. The degree of
sexual dimorphism in erminea, measured as male size divided by female size, is
not correlated with the number of vole species present per square ( r = 0.153,
N = 160), and the degree of sexual dimorphism, measured as male size minus
female size, is not correlated with the size range of vole species, measured as
maximum vole size minus minimum vole size, per square (vole skull width:
r = 0.084, N = 160). Differences in the diet of male and female weasels have
been documented and these tend to become emphasized as prey become scarce
(see above). Different feeding niches between the sexes may, however, be a
result rather than a cause of dimorphism.
Furthermore, we believe the reasoning behind the Brown and Lasiewski
hypothesis is unsound. The increased energy needs of an elongate weasel would
be expected to be accompanied by increased hunting efficiency and, possibly,
decreased population density. Since, as discussed previously, the population
density of weasels appears to be limited by their food supply, we see no reason
why an elongate weasel should necessarily suffer increased competition for food.
Brown and Lasiewski’s hypothesis has been criticized on other grounds by
Erlinge (1979) and Moors (1980). Erlinge points out that since males are larger
than females in all solitary mustelids, this form of dimorphism is not especially
tied to the evolution of an elongate body shape. H e also points out that
increased sexual dimorphism might increase rather than decrease intersexual
competition for food. We concur with two of Moor’s criticisms: the hypothesis
does not predict that males rather than females should be the larger sex and
large mustelids sometimes eat very small prey. However, his claim that the
benefits of reducing intersexual competition are obvious because “the continued
survival of the species depends on one sex not being able to outcompete the
other” invokes group selection (sensu Wynne-Edwards, 1962), and his statement
that larger weasels have more available prey is unsubstantiated.
162
K. RALLS AND P. H . HARVEY
Brown and Lasiewski’s hypothesis predicts that elongate mustelids should be
more dimorphic than less elongate species of equal body weight. Powell (1979)
plotted data on a variety of mustelid species and concluded that this was true.
However, his analysis was confounded by equal weighting of points representing
different taxonomic levels and by the inclusion of the same variables on both
axes. Our reanalysis, eliminating these problems and based on a larger number
of species, showed that sexual dimorphism is not correlated with the degree of
elongation either across genera of mustelids or across species within the genus
Mustela.
The hypothesis also predicts that weasels should display more intense
intrasexual than intersexual territoriality. This is generally true but many nonelongate mammal species have a similar social system.
Weasels are known to be polygynous, so competition between males for access
to females would be expected to lead to large size in males relative to females.
Indeed, monogamous species in the order Carnivora tend to be less sexually
dimorphic than polygynous species (Gittleman, 1984). However, the question
here, we feel, is whether sexual selection alone is sufficient to account for the
degree of sexual dimorphism exhibited in weasels or whether selection for small
body size in females also contributes.
Three selective pressures for small size in females have been proposed: the
small size of prey burrows (Moors, 1980; Erlinge, 1979; Simms, 1979); the
advantages of early sexual maturity (Erlinge, 1979); and the ability of a small
female to channel more energy into reproduction because of her own reduced
needs (Moors, 1980; Powell, 1979; Powell & Leonard, 1983).
The burrow size suggestion is plausible: males tend to feed on larger prey
than females and female erminea at least tend to do more hunting in burrows
than males do. However, really convincing evidence in support of this
hypothesis is lacking. Simms’ (1979) data are from only five areas and the prey
species in two of those areas are substantially larger than the female erminea (in
terms of “minimum passable diameter”) and so cannot be considered a
reasonable constraint on weasel size. Our data are consistent with this idea as
vole size was more highly correlated with female than with male erminea size. It
may also be advantageous for females to reach sexual maturity rapidly.
However, the notion that small females are favoured because of their own
reduced energy needs is more suspect: this would be true if smaller and larger
females were equally efficient hunters, which may not be the case. Moors (1980)
has calculated that a typical male-sized female nivalis would need to catch an
extra 0.5 vole per day merely to supply her own increased metabolic needs. In a
similar vein, Powell & Leonard (1983) calculate that it would be difficult for a
female fisher, Martes pennanti, with young to obtain the additional
300-500 kJ/day necessary were she the size of the larger male fisher. Both
calculations are presented as evidence for selection favouring small females
which are able to channel the excess energy into reproduction. However, this is
not necessarily true. If the hunting efficiencies of males and females were the
same, we suggest that a more profitable way of viewing the size differences
would be to seek the selective pressures which have operated to make males so
large and energetically inefficient. Since nothing is known about the relationship
between weasel size and hunting efficiency, further speculation is pointless.
Geographical variation in sexual dimorphism: We doubt that variations in
VARIATION IN N AMERICAN WEASELS
I63
the degree of sexual dimorphism are due to variations in energy needs as we
doubt that increased energy needs necessarily lead to increased sexual
dimorphism. Furthermore, the patterns of sexual dimorphism in the North
American weasels do little to support this hypothesis. The larger two species are
both more dimorphic than the smallest, which has the greatest surface to
volume ratio. Only nivalis, which shows the least variation in dimorphism and is
the least dimorphic species in North America, becomes more dimorphic with
increasing latitude. Even here latitude accounts for only a small proportion of a
small effect: about 25% of the relatively small degree of variation in sexual
dimorphism.
We found no evidence that variation in the degree of sexual dimorphism
might be due to character displacement in size resulting from competition
between weasel species in areas of sympatry. The sizes of the pairs likely to
compete most strongly, (1) female frenata and male erminea, and (2) female
erminea and male nivalis, do not covary.
While it is possible that females tend to be optimally sized predators suited to
the prevailing prey in each geographical region, it seems unlikely that factors
constraining female size are the major cause of extreme sexual dimorphism, as
small female size is not necessarily associated with high sexual dimorphism (see
Figs 7, 8). Female size variation could only control geographic variation in
dimorphism if the geographic variance in female size was greater than that in
male size. This is true only forfrenata (Table 1).
Geographic variation in size probably results from the interaction of local
environmental conditions and genetic differences among populations. For
example, James (1983) exchanged eggs of red-winged blackbird (Agelaius
thoeniceus) populations differing in nestling development, and found that the
locality in which the young birds were raised accounted for a significant
proportion of the differences in nestling development between the populations.
We suspect that variation in the abundance of prey when young males are
growing most rapidly may be a major cause of geographic variation in sexual
dimorphism in weasels. Theoretically, males should be as large as possible at a
given locality as large size would be an advantage in inter-male competition.
Males may often fail to attain the maximum growth potential, however, if
abundant food is not available during their period of growth. Data on several
mammalian species show that adult male size is more severely reduced than
adult female size if food resources are restricted during the normal period of
rapid growth (Widdowson, 1976; Wolanski, 1979). An indication that this may
also be true in weasels is provided by the nivalis litter raised in captivity with
unlimited food by East & Lockie (1964). The captive females attained a body
weight of 85 g, compared with a typical 60 g for wild females from the same
population, while the single captive male was a massive 300 g compared to the
usual 130 g for wild males. Raising more captive litters might be quite
informative on this point. The extent to which males are larger than females
may also depend in part on their efficiency at catching the prey species for
which females are more or less the optimal sized predator. If these suggestions
are true, then in areas where sexual dimorphism is high, males should have
more food available during the growing season than in areas where dimorphism
is low. Furthermore, because of the species differences in diet, we should not be
surprised that sexual dimorphism does not correlate between species.
I64
K. RALLS AND P. H. HARVEY
Powell' (1979) recognized that the attainment of maximum size in male
mustelids could be constrained by lack of abundant food resources and provided
a supporting example in fishers, Martes pennanti. Fifteen years after fishers were
introduced into an area where a food supply (porcupines) was unexploited by
other predators, males averaged significantly heavier than the original males but
females did not (Powell & Brander, 1977). There is also some evidence that size
in other mammals may be constrained by available food. Robinson (1979)
found that body size in springboks, Antidorcas marsupialis, from 10 locations was
highly correlated with the winter dietary protein in the rumens of both sexes.
Prairie dogs, Cynomys, have become more dimorphic over time in the U.S.A. and
Pizzimenti (1981) has suggested that increased forage due to human agriculture
was one possible cause.
Less abundant prey at some critical period of the year, though not necessarily
when the young are growing, would also tend to increase female territory size.
Conventional interpretations of sexual selection would suggest reduced malemale competition, and hence reduced male size, because of the reduction in the
environmental potential for extreme polygyny (Ralls, 1977; Emlen & Oring,
1977).
In summary, we suggest that fruitful lines for further investigation will involve
searching for the factors which influence male and female size in weasels. Female
size may be correlated with an appropriate measure of prey size. Male size
covaries with female size and, therefore, may also be partly related to prey size.
However, males are larger than females, probably as a consequence of
intrasexual selection. The extent to which males are larger than females may
depend on the environmental potential for polygyny (and hence female territory
size which will be larger in areas where prey are least abundant) and on the
amount of food available during the period of rapid growth of young males.
While the different patterns of geographic variation in size and sexual
dimorphism exhibited by three such similar species makes us wary of simplistic
generalizations between species, the fact that large-scale geographic patterns are
discernible lends hope for relatively simple explanations for them.
ACKNOWLEDGEMENTS
We thank: the many museum curators and technicians who helped us locate
specimens during visits to their institutions or who loaned their specimens;
Robert Hoffmann, Francis James, and Richard Thorington, Jr, for their
encouragement and advice, particularly during the early stages of this project;
Robert Hoffmann for compiling the vole data; Francis and Avis James for
extracting the climatic data; Dante Piacesi and Ken McCormick for the initial
computer processing of the weasel data; Lee-Ann Hayek and Maureen
Anderson for some initial statistical analyses; Louis Valenti for producing the
original SYMAPS; Carolyn King for locating several European and U.S.S.R.
literature references; and Sam Erlinge, John Gittleman, Lawrence Heany,
Carolyn King, Devra Kleiman and Mikael Sandell for their helpful comments
on our draft manuscript. Michael Regen, David Campbell, and the Staff of the
Geography and Map Division, Library of Congress, were especially helpful in
determining the latitude and longitude of many obscure collection localities.
Jonathan Ballou and Martyn Stenning helped to prepare some of the figures.
VARIATION I N N AMERICAN WEASELS
165
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