Biological journal ofthe Linncan So&&
(1981), 16: 337-355. With 8 figures
Evolution of skull shape in carnivores
2. Additional modern carnivores
LEONARD B. RADINSKY
Anatomy Department, The University of Chicago,
Chicago, Illinois 60637, U.S.A.
Accepted f o r publication Septmbcr 1981
Fifteen functionally significant aspects of skull morphology were measured on skulls of 36 additional
species of carnivores to complete a survey of skull shape'in modern fissiped (land) carnivores that
includes most of the living genera. The measurements were transformed to dimensionless variables
based on the residuals from allometric equations, and were analysed singly and in a 10 variable
principal components analysis. An initial study of 62 species of viverrids, canids, mustelids and felids
had shown those families to be distinguished from each other by the functionally significant
measurements. However, among the additional 36 species, some procyonids, ursids and mustelids
display a range of diversity of skull morphology that overlaps that of the other families and diminishes
the potential value of the measurements as taxonomic characters. Intraspecific variation is presented
for 12 species, and is low enough to allow use ofsome features as species level diagnostic characters. The
lack of correlation between diet and functionally significant aspects of skull morphology among
omnivorous carnivores, and the absence of certain skull shapes among carnivores are discussed.
KEY WORDS:-Carnivora
-
skulls - functional craniology - morphometrics.
CONTENTS
Introduction . . . . . . . .
Materials and methods.
. . . . .
Results . . . . . . . . .
Discussion . . . . . . . . .
Significance for carnivore systematics .
Functional significance and biological role
Carnivore skull shape morphospace. .
Acknowledgements. . . . . . .
References. . . . . . . . .
Appendices . . . . . . . .
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337
338
340
345
345
349
350
351
351
352
INTRODUCTION
This paper is part of a study of changes in skull morphology that occurred in the
origin and evolution of the modern carnivore families. The Order Carnivora first
appeared around 60 million years ago (My), and its major evolutionary radiation,
which gave rise to most of the modern families, took place around 35-40 My. It is
hoped that a functionally oriented analysis of skull morphology will help provide
insights into factors involved in that radiation-why it took place when it did
337
00224066/81/080337+19 s02.00/0
0 1981 The Linnean Society of London
338
L. B. RADINSKY
(20-25 My after the origin of the Carnivora), and how early members of the
modern families were differentiated from each other with respect to ecological
niche.
The purpose of this paper is to complete a survey of skull shape among modern
land (fissiped) carnivores, to provide a background for analysis of the fossil
carnivores. A previous paper (Radinsky, 1981), analysed skull shape in 62 species
representing the four largest families of carnivores : viverrids, canids, mustelids and
felids. That study showed that functionally significant aspects of skull morphology
distinguished those four families from each other, and suggested that the
anatomical differences are related to differences in killing behaviour. The present
paper examines skull morphology in the smaller remaining families, procyonids,
ursids and hyaenids, and in the genera of viverrids and mustelids that were not
included in the first paper, to see to what degree modern procyonids, ursids and
hyaenids are also distinguished by functionally significant aspects of cranial
morphology, and if the distinctive features noted for viverrids and mustelids in the
first paper also characterize the remaining genera in those families. Finally, this
paper provides data on intraspecific variation in the cranial features under
investigation, to allow estimation of the significance of differences observed among
taxa at the species level.
MATERIALS AND METHODS
Sixty-two species of modern carnivores were covered in the first study, and this
paper examines 36 additional species (listed in Appendix l ) , for a total of 98
species, including representatives of most of the living genera of fissiped carnivores.
The original sample of viverrids was comprised mainly of viverrines and
herpestines, and the six additional species measured for this paper are mainly
paradoxurines and hemigalines. The original mustelid sample consisted primarily
of mustelines, and the 13 additional species covered in this paper are badgers,
skunks and otters. The seven species of procyonids, seven species of ursids, and
three species of hyaenids represent all of the living genera in those families.
Measurements of the 15 functionally significant aspects of cranial morphology
used in the previous paper (Radinsky, 1981), were taken on one randomly selected
skull of each of the 36 species. (See Appendix 2 for abbreviations, definitions and
justifications of these measurements.) Bulla volume could not be estimated from
external skull measurements of ursids and most of the mustelids, and so was
omitted for those families. To allow comparisons of skull shape among species of
different sizes while accounting for possible effects of allometry, all measurements
were converted to logarithms (base lo), and were transformed into dimensionless
variables based on the residuals from reduced major axis equations of each variable
u. skull length (SL) or jaw length (3L).For example, if log Y = log a + b log SL,
(which is equivalent to Y = a SLb) the transform of Yi=Yi/u $Lib. The
dimensionless transforms of each measurement are indicated by a ' following the
abbreviation. Thus, ZAW' is the transform of ZAW. For a fuller discussion of the
procedures used in transforming the measurements to dimensionless variables, and
for a list of the equations used for calculating the residuals, see Radinsky (1981).
The data from the additional species of viverrids and mustelids were added to
those of the original viverrid and mustelid samples, and for each transformed
EVOLUTION OF SKULL SHAPE IN CARNIVORES
339
variable, t-tests were used to see if the family means of the expanded viverrid and
mustelid samples still differed from each other and from the canid and felid family
means as they had in the original study (Radinsky, 1981;Table 1). The procyonid,
ursid and hyaenid samples each include relatively few species, and, for the first two
families, a relatively large amount of morphological diversity. Therefore, the
transformed variables of those families were not analysed by family means, but
rather were examined on the level of individual species.
In addition to univariate analysis, the transformed variables were also examined
by a principal components analysis followed by varimax rotation. In the previous
paper, that multivariate technique was shown to separate the 62 species of
viverrids, canids, mustelids and felids into their respective families along the first
two rotated axes of a 15 variable analysis (Radinsky, 1981: Fig. 3). Equally good
separation of those families can be obtained along the first two rotated axes using
only the ten highest loading variables of that analysis (i.e. the variables most
important in determining the axes), and the ten variable analysis (Fig. 1 and Table
1) is used as a background for examining the 36 additional species in this paper.
Because the present paper includes consideration of differences at the species
r
F E L.
F A C 2 (27%)
Figure 1 . Factor scores of the original four family, 62 species sample on the first two rotated a x a
(FAC 1 and FAC 2) of the 10 variable principal components analysis. Polygons enclose all species of a
given family: solid circles represent mustelids (MUS) and canids (CAN); open circles represent
viverrids (VIV) and felids (FEL). See Table 1 for loadings of variables on those axes.
L. B. RADINSKY
3 40
Table 1. Loadings of transformed variables on first two rotated axes
ZAW
OCPW‘
TFL‘
TRL‘
JL’
BRV’
ORBA
MAT’
MFL‘
JXA’
nh‘ Variance
FAC 1
FAC 2
0.323
0.749
0.874
-0.915
-0.865
0.170
-0.201
0.856
0.827
0.898
0.902
0.248
0.165
-0.171
0.266
0.852
0.916
-0.181
0.270
0.172
53.07
27.03
level in addition to analysis of differences at the family level, intraspecific
variability of the transformed variables was examined. Intraspecific variation was
estimated from measurements taken on six randomly selected skulls of each of three
randomly selected species of each of the original four family samples (viverrids,
canids, mustelids and felids), for a total of 12 species (listed in Appendix 4), for
which intraspecific variation was measured.
RESULTS
The dimensionless variable transforms of the 36 additional species of modern
carnivores are summarized in Table 2, and their factor scores on the first two
rotated axes of the multivariate analysis are presented in Figs 2, 3 & 5. The
addition of the six new species of viverrids to the original viverrid sample results in
some small changes in means (by no more than two per cent), and in observed
ranges for some of the variables, and the factor scores of the new species are within
or close to the range of the original viverrid sample (see Fig. 2). The small
differences in mean values for the transformed variables of the enlarged viverrid
sample do not change the significance of differences from the canid, mustelid and
felid means noted in the original analysis (see Appendix 3).
The addition of the 13 new species of mustelids to the original mustelid sample
changes the means and observed ranges for most of the transformed variables, but
the differences that distinguished the original mustelid sample from that of the
viverrids, canids and felids still hold for the enlarged mustelid sample (see
Appendix 3), with the following minor changes: mean brain size (BRV’/3’)is now
significantly higher than that of the viverrids: mean condyle to carnassial distance
(COM1‘) is now significantly higher than that of the canids and felids as well as
that of the viverrids; and mean moment arm of temporalis (MAT’) is still
significantly higher than that of viverrids and canids, but no longer significantly
higher than that of the felids.
The biggest differences in skull shape among the new mustelids are seen in the
otters and some of the badgers. The otters Enhydru (Enh), Aottyx (Aon) and
Pteroneuru (Ptr) have unusualy high BRVlfl’, and Enhydru and Aonyx have relatively
wide skulls (ZAW’) (see Table 2). Those features result in high factor scores on the
second rotated axis (FAC 2) for those genera, and an extension of the mustelid
34 I
EVOLUTION OF SKULL SHAPE IN CARNIVORES
range in that area (see Fig. 3). Among the badgers, Arctonyx (Atx) has a relatively
short temporal fossa length (TFL’), low MAT’ and low jaw cross section area
(JXA1/4’); Myduus (Myd) has relatively low MAT’ and JXA114’; and Melogale
(Mgl) has relatively low MAT’ and long jaw length UL’). As a result of those
features, Arctonyx, Myduus and Melogale have relatively low factor scores on the first
axis (FAC l ) , and are located below the original mustelid range on that axis (see
Fig. 3). (Extremes of skull shape among mustelids are illustrated in Fig. 4.)
Among the three new families, the hyaenids fall within the viverrid range for
most transformed variables. A notable exception is COMl’, for which all three
genera of hyaenids fall below the observed range of not only the viverrids but also
all other carnivores except Ailuropodu (the giant panda). Relatively high ZAW’ in
Hjuenu (Hyn) and relatively high BRVlP, and orbit area (ORBAlP’) in Crocutu
place those genera outside of the viverrid range of factor scores along the second
axis (FAC 2) in the multivariate analysis (see Fig. 2).
The procyonids and ursids display a greater diversity in skull morphology than
do most of the other families (see Fig. 5). Among the procyonids, the lesser panda,
Ailurus (Ail), and the kinkajou, Potos (Pot), have relatively high values for most
-2.0
- 2.0
L
I
-1.0
1
I
0
I
I
I
1.0
I
2.0
1
I
3.0
F A C 2 (27%)
Figure 2. Factor scores of six additional species of vivemds ( 0 )and three species of hyaenids ( 0 )on
the first two rotated axes of the 62 species principal components analysis. Polygons represent the ranges
of factor scores of the 62 species sample shown in Fig. 1. Key to abbreviations of species names is in
Appendix 1 .
1.71
1.89
1.54
1.39
1.59
1.60
1.67
1.45
1.58
215
1.59
1.63
1.89
Additional mustelids
At%
1.24
Tax
1.29
Me1
1.20
1.13
Mgl
Con
1.31
1.31
MPh
1.35
SPl
1.02
MYd
Sul
1.11
Enh
157
pa
1.22
Lut
1.28
Aon
1.43
1.29
151
150
1.54
1.02
1.17
1.15
0.98
1.21
1.13
1.14
0.69
0.84
1.06
1.13
1.05
1.34
1.16
0.92
OCPW' 'IlW"
1.18
1.10
0.97
1.11
1.08
1.23
ZAW'
Additional vivenids
CYn
1.04
p"g
1.11
Hem
0.99
Par
1.18
1.1 1
451
Arc
1.15
Specit3
1.23
1.32
1.31
1.00
1.07
1.06
1.12
1.18
1.06
1.04
1.11
1.32
0.87
1.00
1.07
0.95
1.05
1.02
1.02
TFL'
1.00
0.94
0.91
0.97
0.92
0.91
0.98
0.86
0.90
0.84
0.81
0.87
0.89
1.10
0.89
1.08
0.98
0.94
0.89
'
I
"
0.94
0.98
0.96
1.02
0.99
0.98
0.99
0.97
0.97
0.92
0.87
0.91
0.98
1.06
1.06
1.02
1.01
1.10
1.03
JL'
1.13
1.25
1.20
1.01
1.12
0.96
1.04
1.13
1.07
1.59
1.42
1.18
1.41
1.01
1.03
0.99
1.02
1.07
0.89
0.95
0.81
1.00
0.99
O M
1.13
0.H
0.67
1.02
1.04
0.88
0.93
0.84
0.80
0.78
0.83
0.84
0.74
0.84
1.00
0.92
0.87
0.87
0.99
0.97
1.09
131
1.26
1.05
1.a
1.23
1.25
1.19
1.30
1.40
1.26
1.22
1.10
0.99
0.88
0.85
0.92
0.82
0.89
1.09
1.08
1.16
1.08
1.22
123
1.13
1.14
1.13
1.11
1.13
1.13
1.18
1.14
095
1.09
1.13
1.12
a92
1.15
1.45
1.54
1.50
1.60.
os3
0.85
1.42
1.26
1.12
1.24
1.41
1.27
1.22
0.90
1.27
1.26
1.13
0.88
BRV~P'BULV'P~ORBA~P~
o c p H COMI' MAT'
Table 2. Transformed variables of 36 additional carnivorans*
1.05
0.99
1.14
1.01
1.06
1.27
1.35
1.24
0.89
0.96
la
1.08
0.19
1.18
om
0.93
1.10
0.97
1.20
MAM'
0.91
1.10
1.02
1.11
0.96
1.10
1.07
0.93
1.M
0.99
1.02
1.06
1.01
0.85
1.09
0.90
1.03
1.22
1.15
MFL'
1.16
1.53
1.21
1.31
1.33
091
1.31
1.13
1.06
1.15
I .29
1.18
o.!w
1.06
0.98
0.87
1.12
1.OO
1.07
JXAV.
13.62
11.95
10.95
8.54
8.23
7.77
5.19
8.67
7.51
13.29
15.14
10.92
8.59
10.94
11.64
10.60
10.41
9.41
13.06
SL
35
P
r
W
P
N
1.73
1.13
1.37
1.37
1.05
1.22
1.58
Ursids
He1
MIS
Sel
TlT
Thl
UrS
APa
1.32
1.22
1.38
1.15
1.26
1.19
1.34
1.61
1.47
1.24
1.43
1.82
205
1.28
1.17
1.03
1.78
0.74
1.18
1.10
a75
0.85
1.54
1.32
1.66
1.08
0.93
1.36
1.32
1.29
1.12
1.02
0.85
1.19
0.93
1.06
1.12
0.98
0.98
1.18
1.04
1.29
0.89
0.88
1.26
0.97
1.13
1.07
1.oo
0.89
0.82
0.78
0.93
0.93
0.84
0.92
1.14
1.07
1.11
1.18
1.06
0.89
1.08
1.03
0.97
0.99
1.06
I31
0.96
1.09
1.06
1.19
1.04
1.28
1.58
1.18
131
135
1.24
1.33
1.09
1.14
1.38
1.07
1.27
1.30
0.96
0.94
0.97
1.01
0.87
1.04
1.08
1.10
1.03
1.07
1.06
1.08
1.13
1.26
1.33
0.83
oa2
0.89
1.20
0.73
oa7
0.88
1.03
1.15
1.10
0.99
0.99
0.94
0.93
1.02
0.99
0.94
0.75
1.13
1.09
1.12
0.85
1.13
1.01
0.97
1.16
0.92
1.07
0.95
0.89
1.15
0.95
0.85
1.07
1.08
1.01
1.06
1.12
1.22
0.95
1.07
030
0.84
0.85
0.87
1.01
0.98
1.04
1.04
1.02
1.02
1.10
1.16
1.01
1.02
1.16
1.08
1.14
oai
1.08
1.23
1.46
1.09
1.17
1.31
1.23
1.27
1.53
1.29
1.25
1.39
0.69
oai
1.29
1.64
1.01
1.16
0.99
1.04
1.13
1.05
0.89
1.58
1.33
0.86
0.77
2.65
0.99
1.01
0.87
1.03
1.87
0.95
0.84
0.89
1.15
0.87
0.91
0.90
0.95
0.92
0.94
0.89
1.11
0.74
0.82
1.15
0.98
1.02
1.32
1.28
1.12
1.48
1.02
1.16
1.21
1.08
1.00
1.39
1.31
1.51
1.13
0.86
1.41
1.01
1.16
23.00
24.40
12.62
23.20
29.71
25.65
22.89
34.75
25.29
25.68
12.04
10.27
11.00
10.75
8.02
8.61
7.34
Boldface numbers denote relatively high or low values: for viverrids and hyaenids, values that fall outside of the observed range of the original viverrid sample; for mustelids,
values that Bll outside of the observed range of the original mustelid sample; and for pmyonids and ursids, values that fall above or below the highest or lowest (respectively)
family means of the vivemd, canid, mustelid and felid samples (see Appendix 3).
*See Appendix 1 for full species names, and Appendix 2 for explanations of variables.
Prt
Hyaenids
Hyn
CrO
1.12
1.17
1.06
1.51
1.27
1.40
1.13
1.61
1.28
1.36
1.75
1.48
1.41
1.64
Procyonids
Pro
Ail
Nsa
Nsl
Pot
Bsc
Bsn
w
e
w
f
2
z
c
(
m
9
w
8
$
2
L. B. RADINSKY
344
F E L.
-2.0
-2.0
,
I
-1.0
1
I
I
0
I
I
1.0
1
2.0
I
1
3.0
F A C 2 (27%)
Figure 3. Factor scores of 13 additional species of mustelids on the h t two rotated axes of the 62
species principal components analysis. Polygons represent the ranges of factor scores of the 62 species
sample shown in Fig. 1. Key to abbreviations of species names is in Appendix 1.
transformed variables, excluding JL’ and tooth row length (TRL’), which results
in their placement in the upper right quadrant of the factor score plots in Fig. 5.
Potos is also unusual in having an extremely expanded angular process, which is
reflected in the highest moment arm of masseter (MAM’) of any carnivore (see
Fig. 6). The coatimundi, Nasuu (Nas), has relatively high JL’ and TRL’ values,
and, together with the little coati, Naruellu (Nsl), has relatively low values for
several other variables, which places those two procyonid genera in the lower left
quadrant of the factor score plot (Fig. 5). Extremes of procyonid skull shape are
illustrated in Fig. 6.
Among the ursids, the Malayan sun bear, Helurctos (Hel), and the giant panda,
Ailuropodu (Apa), stand out with relatively high values for many transformed
variables, which places them in the upper right quadrant of the factor score plots of
Fig. 5. Helurctos has the highest ZAW’ and second-highest occipital plate width
(OCPW’) (after Enhydra) of the 98 species measured in this study. Extremes of
ursid skull shape are illustrated in Fig. 7.
Intraspecific variation in transformed variables is summarized in Appendix 4 &
Fig. 8. As expected, in general intraspecific variation is less than interspecific
variation with families, with the only exceptions in viverrid TRL’ and felid
EVOLUTION OF SKULL SHAPE IN CARNIVORES
345
Figure 4. Extremes ofdiversity in skull shape in modern mustelids. All drawn to same scale. See text for
discussion.
masseteric fossa length (MFL’) and JXAU4’. The intraspecific standard deviations
presented in Appendix 4 allow assessment of the significance of differences in
transformed variables seen among species listed in Table 2, and the visual display
of intraspecific variation in factor scores presented in Fig. 8 allows assessment of the
significance of differences in placement of species on the factor score plots in Figs 2,
3 & 5.
DISCUSSION
Signijcance for carnivore systematics
The previous study (Radinsky, 1981), showed that 62 species of viverrids,
canids, mustelids and felids could be grouped into their respective families on the
basis of functionally significant aspects of skull morphology. Those families are
currently defined primarily on the basis of middle ear region and basicranial
L. B. RADINSKY
946
2.1
MUS.
-
I.(
c*
8
tc)
Ln
v
-
I
VIV.
0
a
LL
-I.
- 2.1
-
.o
1
I
-1.0
I
I
0
I
I
I
1.0
I
2 .o
I
I
3.0
F A C 2 (27%)
Figure 5. Factor scores of procyonids ( 0 )and unids ( 0 )on the first two rotated axes of the 62 species
principal components analysis. Polygons represent the ranges of factor scores of the 62 species sample
shown in Fig. 1. Key to abbreviations of species names is in Appendix I .
anatomy (Hunt, 1974; Tedford, 1976), and it was hoped that the functionally
significant aspects of skull morphology might provide additional characters for
carnivore family diagnoses. The present study shows that additional species of
viverrids fall largely within the range of morphology seen in the original viverrid
sample, but that among mustelids, some species of badgers and otters fall far
outside of the range of morphology of the original (mainly musteline) mustelid
sample. The previous study had shown mustelids to be distinguished from viverrids
by features of skull morphology reflecting relatively short, robust jaws and
relatively large, powerful jaw muscles (variables important in determining
FAC 1-see Fig. 1, Table 1). However, three of the badgers-Melogale, Myduur
and Arctonyx-fall well within the viverrid range in those variables. Thus, although
mustelid and viverrid family means are still significantly different from each other
for many of the variables (see Appendix 3), there is now so much overlap that these
features cannot be considered useful systematic characters for family level
diagnoses.
Of the new families examined in this study, hyaenids are distinguished only by
their very low COM1’ values, which are lower in Hyaena and Crocutu than in any
other carnivores in the study. The procyonids include relatively few taxa but are
EVOLUTION OF SKULL SHAPE IN CARNIVORES
341
Figure 6. Extremes ofdiversity in skull shape in modern procyonids. All drawn to same scale. See text
for discussion.
extremely diverse in skull morphology. Most species have relatively small auditory
but in other features procyonids overlap broadly with several
bullae (BULV1’3’),
other families. At one extreme, the coatimundis (Nusuu and Nusueflu) resemble
canids in their long TRL and JL, and at the other extreme, the lesser panda
(Ailurus) and the kinkajou (Potos) are similar to felids in having relatively hi h
ZAW’ and BRV’l3’values, and to mustelids in having high MAT and JXA !/4,
values. Ursids like procyonids, include relatively few taxa but a large degree of
diversity in skull morphology. At one extreme, the polar bear (Thulurctos) and sloth
bear (Melursus) are similar to viverrids in many aspects of skull shape, and at the
other extreme, the giant panda (Ailuropodu) and Malayan sun bear (Helurctos)
overlap the high end of mustelid and felid ranges in several transformed variables.
The diversity in skull morphology displayed by the procyonids, ursids and some
L.B. RADINSKY
348
6
cm
6 cm
Figure 7. Extremes of diversity in skull shape in modem unids, drawn to diflercnt scales. See text for
discussion.
of the more unusual mustelids, is such that the original pattern of separation into
family groups seen in the 62 species analysis (Fig. 1) is obscured with the addition
of the new species (Figs 3, 5 ; Table 2, Appendix 3). The four large families
(viverrids, canids, mustelids and felids) still differ in mean values of several of the
transformed variables, but there is so much overlap across families that the
characters cannot be considered useful for systematics at the family level. Further,
the procyonids and ursids are so diverse (for the small number of taxa involved),
that it is not even meaningful to characterize them by family means for the
transformed variables. However, while these characters are not distinctive at the
family level, the amount of intraspecific variation in the transformed variables is
low enough that in many cases some of them can be used to distinguish species
within families (cf. Table 2, Appendix 4).
349
EVOLUTION O F SKULL SHAPE IN CARNIVORES
9
8
\ 7 I
\
I
-2.0
-2.0
1
I
/
I
-1.0
?
4
I
0
I
I
I
1.0
I
2.0
I
I
3.0
F A C 2 (27%)
Figure 8. Intraspecific variation in factor scores of 12 species of modem carnivores on the first two
rotated axes of the 62 species principal components analysis. Polygons represent the ranges of factor
scores of the 62 species sample shown in Fig. 1. The circles represent species means, and the vertical
and horizontal lines representftwo standard deviations (95% limits) on the FAC 1 and FAC 2 axes
respectively. See Appendix 4 for list of species (indicated by numbers 1-12), and for the data upon
which this graph is based.
Functional signijcance and biological role
The previous study (Radinsky, 1981) proposed the functional hypothesis that
high loading FAC 1 variables reflect bite strength, and the biological role
hypothesis that differences in bite strength are correlated with differences in killing
behaviour. The present study covers mainly omnivorous carnivores, and if the
functional hypothesis that FAC 1 variables reflect bite strength is correct, there is a
surprising lack of correlation between inferred bite strength and diet.
Among the ursids, Ailuropoda has been considered to represent an extreme of
cranial modification for powerful chewing (Sicher, 1944; Davis, 1964), and its
skull morphology was inferred to be an adaptation for chewing hard bamboo
(which comprises an important part of its diet). However, Helurctos is even more
derived (specialized) than Ailuropoda in cranial features related to strong jaws and
powerful jaw muscles, and yet there are no unusually hard food items reported as
important components of its omnivorous diet (Walker, 1964). Among the
procyonids, the apparently powerful jaw apparatus of Aibrus may be causally
350
L.B. RADINSKY
related to the reported presence of acorns as an important food item in its diet
(Walker, 1964), but there are no obvious dietary correlates that account for the
distribution of other procyonid species along the FAC 1 axis, from Nusua at one
extreme to Potos at the other. Similarly, among the mustelids there are no obvious
differences in reported diets to account for the differences in skull morphology
among the omnivorous skunks and badgers, from Arctotip at one extreme to
7 m i d e a and Mephitis at the other. Finally, among the hyaenids, the skull
morphology of Proteles, the aardwolf, suggests a weaker bite than in the hyaenas,
Hyaena and Crocuta (see TFL’ and MAT’ in Table 2), but would not lead one to
suspect that Proteles subsists largely on a diet of termites.
The lack of correlation between diet and aspects of skull morphology related to
bite strength may be accounted for by three kinds of explanations. First, the
functional hypothesis that FAC 1 variables reflect bite strength may be too
narrow : perhaps additional aspects of functional significance are involved also.
Second, the biological role hypothesis that the observed dietary differences among
modern carnivores will be causally related to differences in bite strength may be
incorrect. Bite strength may be correlated with other biological roles, such as
intraspecific combat or defence. Third, other factors besides strictly adaptational
ones may be involved in determining differences in skull shape among modern
carnivores (see Gould & Lewontin, 1979, for a discussion of such factors).
Carnivore skull shape morphospuce
The first two rotated axes of the multivariate analysis can be considered as
framing a view into a 10-dimensional morphospace that describes skull shape in
modern carnivores based on the variabIes listed in Table 1. The original four
family analysis (Fig. 1) shows mustelids, viverrids and canids spread out along the
first axis (FAC 1), determined primarily by variables reflecting relatively short,
robust jaws and relatively large powerful jaw muscles at the mustelid end of the
axis. Felids are segregated out on the second axis (FAC 2), determined primarily
by relatively great skull width (ZAW) and large sensory capsules (ORBA and
BRV) .
The additional carnivore species covered by the present study fill in much of the
empty morphospace of the first analysis. Hyaenids and various species of
procyonids and ursids are located in the space between the original four family
ranges (see Figs 2, 5), overlappifig the viverrid range on FAC 1 and the canid
range along FAC 2. Otters and a few procyonid and ursid specks fall in the upper
right quadrant, overlapping the mustelid range on FAC 1 and thefelid range on
FAC 2 (see Figs 3, 5).
The only region of the FAC 1-FAG 2 morphospace that is not filled by modern
carnivores is the lower right quadrant, which would be occupied by species with
relatively long, slender jaws, long tooth rows, and short temporal fossae, like
canids, and relatively wide skulls with relativeiy large sensory capsules, like felids.
The absence of modern species with those skull shape characteristics may in part
be an artifact of how the original measdrements are transformed into dimensionless
variables. Long jaws and long tooth rbw lengths add to skull length, and the
variables that determine FAC 2-ZAW, ORBA and BRV-are transformed by
regression against skull length. In other wofds, species with lbnger JL and TRL
EVOLUTION OF SKULL SHAPE IN CARNIVORES
35 1
will have longer SL, and, for the same sized ZAW and sensory capsules, those
species will have lower ZAW, ORBA’” and BRV’’3’than species with shorter SL.
This problem of potential bias introduced by the process of transforming the
measurements into dimensionless variables is discussed more hlly in the previous
paper (Radinsky, 1981), particularly with respect to sensory capsules.
On the other hand, the absence of species in the lower right quadrant of the
FAC 1-FAC 2 morphospace may also reflect, at least in part, biomechanical
constraints on carnivore skull shape. Relative zygomatic arch width (ZAW’) is an
important determiner of FAC 2, and to the degree that ZAW reflects size ofjaw
musculature, one would expect high ZAW’ to be associated with high values in
other variables related to bite strength, and the latter would place species high on
FAC 1. Thus one would not expect to find carnivore species with both high ZAW’
and low TFL’, MAT’ and JXAW, and this may in part account for the absence of
species in the lower right quandrant of the FAC 1 v. FAC 2 factor score plot.
The pattern of distribution of modern carnivore species in the FAC 1-FAC 2
morphospace raises additional questions with respect to the evolution of diversity
of skull morphology among carnivores. For example, why are there no short-faced
canids or long-jawed mustelids or felids. Or, why are the felids so conservative (i.e.
limited in diversity) with respect to FAC 1 variables compared to the other
families? The distributional patterns seen in Figs 1, 2, 3 & 5 may reflect
biomechanical constraints on skull shape in the various carnivore families, but
before that is assumed, the fossil representatives of those families should be
surveyed, to see if they conform to the ranges of their modern relatives. Then, to
approach the question of why a given family group has a particular range of skull
morphology, more detailed biomechanical analyses of the functional significance
of the morphology, and more extensive behavioral-ecological analyses of its
biological roles must be carried out, to gain more understanding of the observed
patterns. Work in those two areas is currently in progress.
ACKNOWLEDGEMENTS
For help and advice on this study, I am grateful to the people acknowledged in
the previous paper (Radinsky, 1981). I thank S. Arnold for additional advice on
statistics, and S. Emerson for critical comments on the manuscript. Measurements
were taken on skulls from the Department of Mammalogy of the Field Museum of
Natural History, Chicago, and I thank the curators of that collection for access to
those materials. This work was supported in part by a grant from the National
Science Foundation, DEB-7901584.
REFERENCES
DAVIS, D. D., 1964. The giant panda. A morphological study of evolutionary mechanisms. Fieldinma: (oologuul
Memoirs, 3: 1-339.
GOULD, S. J. & LEWONTIN, R. C., 1979. The spandrels of San Marco and the Panglossian paradigm: a
critique of the adaptationist programme. Proceedings o f h Ryul Sock& of London (B), 205: 581-598.
HUNT, R. M. 1974., The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore
evolution. Journal of Morphology, 143: 21-76.
RADINSKY, L. B., 1981. Evolution of skull shape in carnivores. 1. Representative modern carnivores. Biologuul
journal of the Linncun Socicg, 15: 369-388.
L. B. RADINSKY
352
SICHER, H., 1944. Masticatory apparatus in the giant panda and the bears. Fialdiana: @logical SniCs, 29:
61-73.
TEDFORD, R. H.,1976. Relationship of pinnipeds to other carnivores (Mammalia). Sysrcmatic &h~,
25:
363-374.
WALKER, E. P., 1964. Mammals ofthe World.Baltimore: Johns Hopkins Prm.
APPENDICES
Appendix 1. Species measured and their abbreviations
~~~
Vivcnids
Cyn
Pag
Hem
Par
Agl
Arc
sui
Enh
Ptr
Lut
Aon
Cynogalebennetti
Paguma larvata
Hemigalus derbyanus
Paradoxurus zelonensis
Arctogalidea bivirgata
Arcfictis binhtrong
Procyonids
Pro
P n g v n cawiummrc
Ail
Ailuncs fulgens
N m a nasua
Nsa
N w l h olivacea
Nsl
PolosJIamls
Pot
Bassariscus astutus
BSC
Ban
Bassariyon allmi
Arctonyx collaris
Taxidea tam
Meles meles
Mehiale pnronahnn
Ursids
He1
Mls
Sel
Helarctos malayanus
Melursus ursinus
Seknarcl~slibeti
Conefihrc semisl&tus
TR
rremarclos m l u r
Mephitis nuphihi
Spilogale putorius
Mydaus
jauanensis
.
.
Suillotaxus marchei
Enhydra luhic
Phoneura brcyiliensis
Lutra lutra
Aonyx ciwea
Thl
Ul3
A P
rhalarctos mariiimus
Ursus americanus
Ailuropoda melanoha
Hyaenids
Hyaena brunnea
Hyn
cro
Crmtacronrta
Prt
Prolclcs
EVOLUTION O F SKULL SHAPE IN CARNIVORES
353
Appendix 2. Measurements
BRV
BULV
COMl
JL
JXA
MAM
MAT
MFL
OCPH
OCPW
ORBA
SL
TFL
TFW
TRL
ZAW
Brain volume, taken from endocranial capacity. Converted to BRV'p for comparisons with linear
dimensions.
Bulla volume, estimated from length, width and height measurements by the equation:
V = 0.5236 L x W XH (from V = 1/2(4/3nP).Converted to BULV'I3 for comparisons with h e a r
dimensions.
Condyle to MI, measured from the back of the mandibular condyle to the MI carnassial notch. A
measure of the moment arm of the resistance when biting at the carnassial.
Jaw length, measured from the back of the condyle to the front of the median incisor alveolus.
Resistance moment arm when biting with h n t teeth.
Jaw cross-section area, calculated as the second moment of area (I), an estimator of resistance to
bending. I = nabs/4, where a = 1/2 jaw width and b = 1/2 jaw height, measured beneath M I .
Converted to JXA'P for comparisons with linear dimensions.
Moment arm of masseter, measured from the dorsal surface of the condyle to the ventral border of
the angular process. An estimator of the moment arm of the superficial masseter.
Moment arm of temporalis, measured from the condyle to the apex of the coronoid pmess. An
estimator of the moment arm of a portion of the temporalis.
Masseteric fossa length, measured from the back of the condyle to the most anterior point of the
masseteric fossa. An estimator of the size of the deep maSSeter and of the moment arm of the deep
masseter.
Occipital height, measured from the medventral border of the foramen magnum to the dorsal rim
of the occiput.
Occipital width, measured at the widest point of the occiput, across the mastoids.
Orbit area, estimated from the circumference as measured around the orbital rim. A = C/12.5664,
derived from A = ntl and C = 2nr. An estimator of eye size. Converted to ORBA'P for
comparisons with linear dimensions.
Skull length, measured from the back of the occipital condyles to the anterior tip of the prmaxilla.
An estimator of body size with which most of the other measures are compared.
Temporal fossa length, measured from the most posterior point ofthe lambdoidal crest to the back
of the supraorbital process. An estimator of temporalis size.
Temporal fossa width, calculated by subtracting width at the postorbital constriction from width
across the zygomatic arches. An estimator of temporalis size.
Tooth row length, measured parallel to the palatal midline, from a point level with the back of the
last tooth to the front of the medial incisor alveolus.
Zygomatic arch width, measured across the widest portion of the zygomatic arches. Maximum
skull width, influenced by brain size and jaw muscle size.
L. B. RADINSKY
354
Appendix 3. Means and observed ranges of transformed variables with amended
samples of viverrids and mustelids
Variable
ZAW'
OCPW'
TFW'
TFL
TRL'
JL'
BRV'P'
BULV1j3'
ORBA'/*'
OCPH
COMI'
MAT'
MAM'
MFL'
JXAl/4'
23 Viverrids
16 Canids
28 Mustelids
14 Felids
1.09
(0.92-1.33)
1.10
(0.8s1.25; 1.38)
1.07
(0.87-1.45)
1.04
(0.92- 1.25)
0.99
(0.89-1.10)
1.02
(0.94- 1.10)
1.03
(0.97-1.13)
0.98
(0.84-1.14)
0.94
(0.78- 1.17)
0.98
(0.82-1.27)
1.04
(0.92- 1.14)
1.13
(0.86-1.42)
I .07
(0.80; 0.W1.32)
1.02
(0.84-1.22)
1.07
(0.83-1.37)
1.17
(1.05-1.36)
1.11
(0.96-1.31)
1.01
(0.86-1.17)
068
(0.80-0.97)
1.16
(1.05-1.25)
1( I . W l . 13)
1.12
(0.99-1.28)
1.06
(0.89-1.16; 1.44)
1.07
(0.93-1.19)
1.oo
(0.89-1.21)
1.04
(0.94-1.1 1)
1.02
(0.89-1.1 7)
1.07
(0.86-1.26)
0.84
(0.73-0.98)
0.94
(0.81-1.13)
1.24
(1.02-1.43 ; 1.57)
152
( 1.3G.69)
1.36
( I .25-1.54)
1.25
(1.06-1.46)
1.12
(0.96-1.20)
0.M
(0.814-93)
0.99
(0.95-1.03)
1.29
( I. 15-1.41 )
1.29
(1.19-1.53)
158
( 1.21-1.89 ; 2.15)
1.14
(0.69; 0.82-1.54)
1.13
(0.87; 1.00-1.32)
Om
(0.761.OO)
w
(0.86- 1.02)
1.16
(0.92-1.42; 1.59)
1.04
(0.83-1.21; 1.62)t
0.83
(0.64-1.13)
1.19
(0.96-1.48)
1.11
(1.0E.23)
1.39
(0.85-1.68)
1.07
(0.79-1.35)
1.06
(0.88-1.26)
1.26
(0.91-1.58)
1.a
(1.2T.79)
1.15
1.02-1 29)
I .05
(0.98-1.15)
1.17
(1.05-1.29)
1.25
( 1.10-1.46)
1.14
(1.06-1.19)
1.25
(1.13-1.34)
*Means significantly different (99"/0level) from vivmid aample are indicated in boldface. Underlined boldface
means are also significantlydifferent from means between them and the viverrid sample mean. Semicolons denote
discontinuously high or low values in observed ranges.
?Sample unamended (no additions to original mustelid sample).
0.032
0.023
0.017
0.029
0.066
0.047
0.030
0.015
0.123
0.069
0.063
0.141
0.089
0.061
0.010
0.024
0.060
0.022
0.012
0.024
0.139
0.042
0.022
0.059
0.054
0.015
0.014
0.027
0.077
0.017
0.036
0.039
0.076
0.025
0.042
0.020
0.028
0.018
0.012
0.008
0.026
0.013
0.015
0.019
0.044
0.018
0.014
0.020
0.044
0.023
0.017
0.033
0.045
0.012
0.019
0.025
0.092
0.041
0.030
0.047
0.080
0.041
0.078
0.044
0.166
0.038
0.036
0.070
0.104
0.029
0.050
0.102
0.048
0.021
0.019
0.016
0.108
0.023
0.018
0.029
0.069
0.040
0.046
0.050
0.045
0.028
0.020
0.017
0.097
0.053
0.053
0.039
0.109
0.057
0.042
0.021
0.094
0.060
0.060
0.077
0.122
0.068
0.073
0.085
0.096
0.033
0.088
0.044
0.163
0.065
0.109
0.047
0.130
0.056
0.044
0.052
0.219
0.033
0.113
0.107
0.145
0.078
0.079
0.082
0.118
0.030
0.042
0.037
0.051
0.024
0.075
0.065
0.055
0.064
0.101
0.041
0.071
0.032
0.047
0.047
0.042
0.065
0.034
0.086
0.061
0.100
0.083
0.035
0.163
0.046
0.063
0.090
0.092
0.029
0.057
0.027
0.128
0.070
0.055
0.083
0.160
0.116
0.129
0.132
0.524
0.132
0.173
0.254
0.135
0.093
0.090
0.372
0.486
0.203
0.185
0.157
BRV’/3’ORBA’/20CPH’COMl’ M A T MAM’ MFL’ JXA*14’ FACl
0.032
0.015
0.008
0.011
JL‘
0.579
0.098
0.104
0.263
0.139
0.252
0.088
0.548
0.351
0.172
0.203
0.146
0.353
0.130
0.160
0.081
FAC2
* Intraspecific standard deviations calculated from six randomly selected individuals per species; intrafamily standard deviations calculated from the original samples of
viverrids, canids, mustelids and felids.
Numbers in parentheses after species names correspond to numbers in Fig. 8.
0.092
0.042
0.020
0.053
0.049
0.027
0.032
Felids (14 spp.)
Fcfis contolor (10)
Felis tigrim ( 1 1)
Fefis bmgaLcnsis (12)
0.086
0.060
0.019
0.032
0.032
0.137
0.033
0.046
0.072
0.178
0.038
0.050
0.102
0.076
0.025
0.033
0.037
Mustelids (15 spp)
Gulo gulo (7)
Grison cuju (8)
Must& frenu& (9)
0.080
0.043
0.048
0.012
0.022
0.019
0.102
0.055
0.091
0.031
0.021
0.028
0.077
0.047
0.048
0.024
Canids (16 spp.)
Lycuon pichrr (4)
Alopex lugopus (5)
F m m zndu (6)
0.031
0.031
0.014
0.024
0.088
0.015
0.017
0.016
0.162
0.084
0.070
0.108
0.136
0.052
0.034
0.047
0.113
0.025
0.047
0.049
Vivemds (17 spp.)
Viumu ribcthu ( 1)
Genet& tigrim (2)
Mungos mungos (3)
TFL’
ZAW’ OCPW TFW
TRL‘
Appendix 4. Intraspecific and intrafamily variation (in standard deviations) of transformed variables and factor scores*
v,
iEs
5