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Biological Journal of the Linnean Society, 2012, 106, 70–80. With 3 figures
Mandibular shape correlates of tooth fracture in extant
Carnivora: implications to inferring feeding behaviour
of Pleistocene predators
CARLO MELORO*
Hull York Medical School, The University of Hull, Loxley Building, Cottingham Road, Hull
HU6 7RX, UK
Received 22 September 2011; revised 11 November 2011; accepted for publication 11 November 2011
bij_1843
70..80
Percentages of tooth fracture and mandible shape are robust predictors of feeding habits in Carnivora. If these
parameters co-vary above the species level, more robust palaeobiological inferences could be made on fossil species.
A test of association is presented between mandible shape and tooth fracture in a subset of extant carnivorans
together with large Pleistocene fossil predators from Rancho La Brea (Canis dirus, Panthera atrox, and Smilodon
fatalis). Partial least square (PLS) and comparative methods are employed to validate co-variation of these two
parameters in extant carnivorans. Association between mandible shape and percentage of tooth fracture is strongly
supported, even if both blocks of data exhibit a phylogenetic signal to a different degree. Dietary adaptations drive
shape/fracture co-variation in extant species, although no significant differences occur in the PLS scores between
carnivores and bone/hard food consumers. The fossil species project into PLS morphospace as outliers. Their
position suggests a unique feeding behaviour. The increase in the size of prey, together with consumption of skin
and hair from carcasses in a cold environment, might have generated unusual tooth breakage patterns in large
predators from Rancho La Brea. © 2012 The Linnean Society of London, Biological Journal of the Linnean
Society, 2012, 106, 70–80.
ADDITIONAL KEYWORDS: comparative methods – diet – geometric morphometrics – partial least square
– Rancho La Brea.
INTRODUCTION
Different bones of the vertebrate skeletons are built to
sustain different degrees of biomechanical stress
(Frost, 1964; Oxnard, 1993). The skulls of mammalian Carnivora have received particular attention in
this respect. Theoretical models suggest that skull
shape differences among carnivoran species depend
on adaptations to different mechanical requirements,
as related to distinct feeding behaviours (Wroe,
McHenry & Thomason, 2005; Slater, Dumont & Van
Valkenburgh, 2009; Slater et al., 2010; Wroe, 2010;
Figueirido et al., 2011; Tseng & Wang, 2011). Feeding
adaptations are even more evident in the mandible,
whose primary function is mastication (Herring,
1993). On the one hand, mandibles are optimally
designed for chewing, catching food, and for with*E-mail: [email protected]
70
standing the movement of prey during killing. On the
other hand, mandibles of closely-related species tend
to resemble each other in shape regardless of their
particular diet (Meloro et al., 2008; Piras et al., 2010;
Raia et al., 2010). The role of dentition in explaining
this process is crucial in Carnivora whose feeding
adaptations imply either reduction or development of
specific dental areas in the lower jaw.
Families of Carnivora are clearly distinct in their
mandible shape because of early morphological differentiation during their evolutionary history (Ewer,
1973; Holliday & Steppan, 2004; Van Valkenburgh,
2007; Meloro et al., 2008; Meloro & O’Higgins, 2011).
For example, Felidae and large Hyaenidae have a
reduced dentition in their lower jaw; their mandible is
designed for meat consumption; and little variation
occurs during their evolutionary history (with exceptions being the aardwolf Proteles cristata among
hyaenids, or sabertooth cats among felids). On the
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
MANDIBLES-FRACTURE
other hand, similarities in mandible shape occur
when the complete dental formula is retained thus
allowing them (with modifications) to cope with a
variety of food (e.g. Canidae and Viverridae; Meloro,
2011a, b; Meloro & O’Higgins, 2011). Consequently,
feeding adaptations become difficult to interpret in
extinct taxa even if external mandibular morphology
is an informative starting point to make palaeobiological inferences (Meloro, 2011a).
The quantification of tooth breakages is another
robust predictor of feeding habits in both extant
and fossil carnivorans (Van Valkenburgh, 1988a,
2009). Numerical models applied to the carnivorans of
Rancho La Brea show a strong competition among
large predators whose percentage of tooth fracture
was higher than in extant species (Van Valkenburgh
& Hertel, 1993). Percentages of tooth fracture are
calculated for both upper and lower jaw dentition
across different individuals of the same species. Tooth
fracture varies also among populations, although
feeding adaptation clearly causes interspecific differences (Van Valkenburgh, 2009). Consumers of hard
food such as bones or shells (hyenas, sea otter) tend to
break their teeth more often than meat eaters and
omnivores. Other biological correlates of tooth fracture incidence in Carnivora are ageing (specimens of
older age tend to exhibit high frequency of tooth
fractures) and nonfatal injuries. Pasitschniack-arts,
Taylor & Mech (1988) reported an individual arctic
wolf with a fractured upper carnassial caused by the
impact of a hoof of a large ungulate and suggested
that this kind of trauma is quite common in populations of grey wolf. However, Van Valkenburgh (2009:
76) clearly demonstrated that ‘diet appears to be the
fundamental factor determining rates of tooth fracture in carnivorans, and probably mammals, in
general’.
Because tooth fracture frequency and mandible
shape reflect the type of food consumed, we might
expect these two features to co-vary. This would lend
support to palaeobiological inferences made on either
one of these two factors.
In the present study, the hypothesis is tested that
mandibular shape and percentage of tooth fracture
correlates in extant Carnivora. Species with low percentage of tooth fracture are expected to exhibit a
mandible with a long premolar row, an elongated
molar crushing area, and a short coronoid area (i.e.
indicative of a relatively small area for the attachment of the temporalis) because they are all generalist feeders. On the other hand, species with high
percentage of tooth fracture (specialized predators
and hard object feeders) are expected to show a relatively thicker mandibular corpus, a shorter premolar
row, a more developed molar slicing area, and a
longer coronoid to provide a large area for the attach-
71
ment of the temporalis (Ewer, 1973; Van Valkenburgh, 2009; Meloro & O’Higgins, 2011; Meloro et al.,
2011). If this hypothesis is supported, it is expected
that the combination of these two features provide
indication of feeding habits in both extant and fossil
species. Consequently, the present study tests for the
effect of diet on the shape/fracture association and
includes in the analyses Pleistocene fossil species
from Rancho la Brea for which data are available.
Geometric
morphometrics
and
comparative
methods are employed to validate mandibular shape/
fracture relationship at the interspecific scale. Geometric morphometrics furnish an optimal solution
in quantifying and visualizing shape variation in
complex structures such as the mandible. Meloro
et al. (2008) validated patterns of association of
mandible shape with tooth sharpness and diet in
Carnivora (Meloro & Raia, 2010; Figueirido et al.,
2011; Meloro & O’Higgins, 2011). Meloro (2011a)
also presented a survey of mandible shape in large
Carnivora to predict feeding adaptations in PlioPleistocene taxa, supported by a high degree of
statistical accuracy.
Comparative methods become necessary when
hypotheses at an interspecific scale need to be validated (Garland, Bennett & Rezende, 2005). The
lower carnassial morphology of Carnivora exhibits a
strong phylogenetic signal (Meloro & Raia, 2010) as
does the mandible (Meloro et al., 2008, 2011;
Figueirido et al., 2010, 2011; Meloro, 2011a, b;
Meloro & O’Higgins, 2011). Yet, there is no evidence
of a phylogenetic signal in tooth fracture. Van Valkenburgh (1988a) showed that hyaenids differ from
felids and canids in tooth fracture frequency, even if
larger dataset supports extensive overlap between
carnivoran families (Van Valkenburgh, 2009). The
present study reports multiple approaches that
provide new insights into the underlying processes
moulding mandible shape and percentage of tooth
fracture in Carnivora.
MATERIAL AND METHODS
SAMPLE
One hundred ninety-six digital images of mandibles
were collected for 38 species of Carnivora (Table 1; see
also Supporting information, Table S1) for which
tooth fracture data were available from the literature
(Van Valkenburgh, 2009). The mandible sample was
assumed to be representative of interspecific variability. The number of specimens per species varied from
one (Panthera atrox, Canis dirus, and Urocyon littoralis) to 14 (Otocyon megalotis) (mean of 5.16) (Table 1).
Only mandibles of noncaptive individuals of both
sexes with no evident pathologies were selected.
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
72
C. MELORO
Table 1. Statistics for the mandibular sample of extant and fossil Carnivora
Family
Number of
species
Number of
Specimens
Minimum
(N)
Maximum
(N)
Mean number
of specimens/
species
Canidae
Felidae
Hyaenidae
Mephitidae
Mustelidae
Procyonidae
12
10
3
3
8
2
67
50
16
11
42
10
1
1
4
2
4
4
14
8
7
5
10
6
5.58
5.00
5.33
3.67
5.25
5.00
categories in Carnivora (Crusafont-Pairó & TruyolsSantonja, 1957; Van Valkenburgh, 1988b; Meloro,
2011a, b; Meloro & O’Higgins, 2011). Landmarks 7 to
11 cover the ascending ramus region. A measurement
error survey showed that these landmarks are repeatable with a good degree of accuracy (Meloro, 2011a).
GEOMETRIC
Figure 1. The position of landmarks on a mandible
outline of Canis lupus BMNH 34.6.28.47. 1–2, anteroposterior diameter of c1; 2–3, diastema length; 3–4, length of
the premolar row; 4–6, length of the molar row; 5, projection of the protocone cusp on the m1 baseline; thickness of
the mandibular corpus under the canine (2–14) and molar
row (4–13, 6–12) identified by the landmark projections
perpendicular to the line 1–6; 7, tip of the coronoid
process; 8–9, the maximum depth of the condylar process
(Processus condylaris); 10, most posterior extreme point
of angular process; 11, the ventral extreme of angular
process. Scale bar = 1.0 cm.
Fossil specimens were represented by casts housed at
the Natural History Museum of London and Royal
Museum of Scotland (see Supporting information,
Table S1). Those casts were already employed in a
previous study on mandible shape and did not present
any kind of shape or growth anomaly (Meloro, 2011a).
Digital photographs were collected with a Nikon
camera at a distance of 2 m in accordance with the
protocol described by Meloro et al. (2008), Meloro
(2011a, b), and Meloro & O’Higgins (2011). Fourteen
anatomical landmarks were digitized with TPSDIG,
version 2.09 (Rohlf, 2006a) as in Figure 1. Landmarks
from 1 to 6 were recorded at teeth alveoli, covering
the corpus mandibulae, together with landmarks 12
to 14. Landmark 5 was placed to distinguish the
slicing from the crushing molar region in the lower
dentition, which is relevant to discriminate feeding
MORPHOMETRICS
Shape variables were extracted from raw landmark
coordinates (on the x- and y-axes) by applying Generalized Procrustes Analysis (GPA; Rohlf & Slice,
1990). This algorithm aligns landmark configurations
to a common reference (the consensus) after removing
the effect of rotation, translation, and differences
in size among specimens. The new landmark coordinates were projected into the Kendall tangent space
(with respect to the consensus) and thin plate spline
decomposition method was applied to extract affine
(uniform; Uni) and non-affine (partial warps; PWs)
components of shape. PWs and Uni represent regional
variation of landmarks that can be visualized through
deformation grids. GPA was repeated for each species
separately to extract consensus coordinates, then the
species consensus coordinates were analyzed into a
common shape space re-performing the GPA.
Partial least square (PLS; Rohlf & Corti, 2000)
analysis was applied to detect possible correlation
between shape variables (both PWs and Uni) and the
tooth fracture data sensu Van Valkenburgh (2009). To
quantify tooth fracture data, only the percentage
of fracture quantified for Canines (C), premolars (P),
and carnassials (CR) was considered (Van Valkenburgh, 2009: 74). This way, only teeth covered by
the landmark configuration were included in the
analyses. The PLS extracts pairs of orthogonal latent
variables from the correlation matrices of each
block, using singular value decomposition. Each pair
of latent variables (singular warps; SW) maximize
the possible co-variation between the two blocks.
Because fossil taxa exhibit an unusual pattern of
tooth fracture (Van Valkenburgh, 1988a, 2009; Van
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
MANDIBLES-FRACTURE
Valkenburgh & Hertel, 1993), PLS was applied only
to test for the association between mandible shape
and tooth fracture in a subset of extant species
(N = 35). A nested analysis is also presented after
selecting specific ecological groups (diet categories,
sensu Van Valkenburgh, 2009: C, carnivorous; B/S,
bone or shell hard-object feeders; O/I, omnivorous
and/or insectivorous) that emerged from PLS plots
(Meloro, 2011a). Fossil taxa were projected in the SW
spaces to identify similarities (or dissimilarities) with
extant taxa in relation to mandible shape and percentage of tooth fracture. This procedure was
employed by Manfreda et al. (2006) in a study on the
association between locomotion and atlas shape in
primates. In that case, the aim was to detect whether
humans exhibit unusual atlas morphology compared
to other primates (Manfreda et al., 2006). GPA and
PLS analyses were performed using TPSPLS, version
1.18 (Rohlf, 2006b).
IDENTIFIABLE
FACTORS
Covariation between mandible shape and tooth fracture could be influenced by common factors. Parametric and nonparametric multivariate analysis of
variance (MANOVA) (using PAST, version 2.4;
Hammer, Harper & Ryan, 2001) were employed to
test for differences in PLS scores as a result of diet
(categories in Van Valkenburgh, 2009). This study
also tested for an association between SWs and mandibular size (as quantified by centroid size of
landmark configuration) with nonparametric correlation. Because of statistical non-independence of
inter-specific data, comparative methods (Garland,
Bennett & Rezende, 2005) were applied to take the
phylogenetic effects into account. A K-statistic was
employed to detect a phylogenetic signal in SW
scores and tooth fracture data (Blomberg, Garland &
Ives, 2003). The K-statistic varies between 0 (no phylogenetic signal in the data, such as with a star
phylogeny) to 1 or even more (1 = data fit a Brownian
motion model of evolution).
The phylogenetic tree for the 35 extant species of
Carnivora was pruned using MESQUITE (Maddison
& Maddison, 2009) from the Bininda-Emonds, Gittleman & Purvis (1999) phylogeny. It includes time of
divergence in million of years calibrated from the
fossil record (see Supporting information, Fig. S1).
The software PDAP (Garland et al., 1993; Garland,
Midford & Ives, 1999; Garland & Ives, 2000) and
PHYSYG (Blomberg et al., 2003) were used to
manipulate the tree and to test for significance of the
phylogenetic signal. Then, phylogenetic generalized
least square (PGLS) analysis (Rohlf, 2001, 2006c) was
applied to validate the PLS analyses, and to verify the
effect of diet and size on SW scores. PGLS was
73
employed to validate the association between SWs
including phylogenetic co-variance matrix as an error
term in the regression model with SW shape as x and
SW fracture data as y (Meloro et al., 2011). PGLS
analysis was repeated to test for an association
between diet or size (as x) and specific SW (as y). This
procedure provided the same results as performing
correlation tests between independent contrasts of
paired SWs. PGLS analyses were conducted with
NTSYS, version 2.21c (Rohlf, 1986–2009).
RESULTS
OVERALL
SAMPLE
PLS analysis supports a strong correlation between
the percentage of tooth fractures and mandible shape
in extant Carnivora. The analysis for 35 extant
species extracts three pairs of SW vectors of which
the first explains 81.98% of covariance, the second
explains 15.35%, and the third explains 2.65%. The
correlation coefficient for the first pair of SW is high
(r = 0.728) and significantly larger than expected by
9999 random permutations (P = 0.0001). On the
second SW, the correlation is lower (r = 0.568) but still
significant (P = 0.0001). With the third pair of axes,
the correlation is nonsignificant. Along the first pair
of SWs, a high degree of overlap occurs between
Canidae and Felidae, whereas members of Mephitidae, Hyaenidae, and Mustelidae appear distinct
(Fig. 2A). The omnivores/insectivores (O/I) show more
negative SW scores on both axes (shape and tooth
fracture) compared to carnivores and B/S (Fig. 2A).
The hard food feeders (B/S) fall within the range of
variability of carnivores, even if only hyaenids occupy
a discrete portion of the morphospace. Diet categories
are significantly different along the first two pairs of
SWs (nonparametric MANOVA F = 8.979; P < 0.0001),
even though the pairwise comparisons show no difference between carnivores and bone/shell feeders in
SW scores (P = 0.7824).
On the negative scores of SW1, species exhibit a low
percentage of fractures, a mandible with elongated
crushing molar area, and a curved and posteriorly
thick corpus (Fig. 2B). Positive scores are occupied by
species with higher percentage of tooth fractures (particularly the premolars), whose mandibular corpus is
less curved, and exhibit a longer diastema and a
shorter crushing molar area. The ascending ramus is
elongated posteriorly because of the shift of the
condylar process landmark (Fig. 2B).
When fossil taxa are projected in the SW1 space,
they all exhibit positive scores and cluster within the
range of C and B/S groups, with the exception of the
sabertooth cat Smilodon (Fig. 2A). Canis dirus is
within Canidae and Felidae with SW1 scores very
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
74
C. MELORO
Figure 2. Plot of the first pair of Singular Warps (SW)
representing mandibular shape block (x-axis) and tooth
fracture data block (y-axis) for 38 species of Carnivora.
A, species are labelled for families. In the smaller plot taxa
are labelled for diet. O/I, omnivores/insectivores are grey
diamonds; C, carnivores are white diamonds; B/S bone
shell consumers are black diamonds. Fossil species are
projected. B, profile plot for tooth fracture data and deformation grids of mandibular shape data associated with
SW1. The left side represents the extreme negative scores,
and the right side represents the positive scores. On the
profile plot: C, % Canine; P, % Premolar; CR, % Carnassial.
close to that of the tiger (Panthera tigris), whereas
P. atrox clusters within Canidae because of very
high SW1 fracture scores that resembles the grey
wolf (Canis lupus) and the island fox (U. littoralis)
(Fig. 2A). Smilodon fatalis exhibits a high positive
score for mandible shape and clusters much greater
than the range of extant hyaenids (Fig. 2A).
The effect of centroid size on SW1 (only extant taxa)
is significant for both shape and fracture data,
although no association occurs with either one of the
SW2 axes (Table 2).
NESTED
ANALYSIS
Because of the clear separation between carnivores
and bone/shell feeders from the omnivore/insectivores
in the SW1 plot (Fig. 2A), PLS was repeated on the 28
extant species belonging to the former two categories.
Figure 3. Plot of the first pair of Singular Warps (SW)
representing mandibular shape block (x-axis) and tooth
fracture data block (y-axis) for 28 species of carnivores and
B/S (bone shell) that includes Hyaenidae, Canis lupus, and
Enhydra lutris. A, families and fossil taxa are projected. B,
profile plot for tooth fracture data and deformation grids of
mandibular shape data associated with SW 1. The left side
represents the extreme negative scores, and the right side
represents the positive scores. On the profile plot: C, %
Canine; P, % Premolar; CR, % Carnassial.
Three pairs of SWs are extracted, although only
the first shows a very high significant correlation
(r = 0.904, P < 0.0001 after 9999 randomizations). The
first pair of SW explains 76.15% of covariance,
whereas the second (nonsignificant) explains 20.72%.
The strong association between the first pair of axis
shows that Mustelidae are clearly distinct in the SW
scores from the other families (Fig. 3A). They occupy
negative scores of SW1 (Fig. 3A) being characterized
by a small percentage of fractured premolars but
higher canine fracture and a curved mandible with
long crushing area (Fig. 3B). On positive scores felids,
hyaenids, and canids show higher premolar and carnassial tooth fracture in relation to a straighter mandible with a longer slicing area (Fig. 3A). The diet
signal is mixed in this plot because the sea otter
Enhydra lutris (a B/S) clusters with other mustelids,
whereas the grey wolf is closer to bone cracking
hyenas (Fig. 3A). A nonparametric permutation test
showed nonsignificant separation between C and B/S
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
MANDIBLES-FRACTURE
75
Table 2. Spearman nonparametric r-values (below diagonal) and probability values (above) for correlation between Ln
centroid size (CS) and Singular Warps (SW) 1 and 2
Ln_CS
SW1_Sh
SW2_Sh
SW1_Fr
SW2_Fr
Ln_CS
SW1_Sh
SW2_Sh
SW1_Fr
SW2_Fr
1.0
0.69613
-0.09328
0.54675
0.066676
3.43 ¥ 10–6
1.0
-0.02563
0.75602
0.16299
0.59404
0.88379
1.0
0.061502
0.54619
0.000678
1.51 ¥ 10–7
0.72561
1.0
0.60315
0.70353
0.34952
0.000688
0.000126
1.0
Significant values are shown in bold.
Table 3. K-statistics and probability values for phylogenetic signal in different variables for both the overall
(N = 35) and the nested sample (N = 28)
N = 35
C
PM
CR
Ln CS
SW1 shape
SW1 fracture
SW2 shape
SW2 fracture
N = 28
K
P
K
P
0.24553
0.43108
0.15348
0.90907
1.3862
0.2774
0.5563
0.2924
0.01902
< 0.0001
0.47648
< 0.0001
< 0.0001
0.0050
< 0.0001
0.0110
0.18475
0.37992
0.13406
0.81130
1.1767
0.5950
–
–
0.12613
0.00100
0.48448
< 0.0001
< 0.0001
< 0.0001
–
–
C, % canine; PM, % premolar; CR, % carnassial; Ln CS,
natural log-transformed centroid size (CS); SW, Singular
Warp.
based on SW1 scores (Mahalanobis distance = 0.054,
P = 0.8529).
The projection of fossil taxa shows that they are
all outliers in the SW1 plot because of a high percentage of canine fractures associated with negative
scores of SW1 (Fig. 3A, vertical axis). Canis dirus is
the only fossil species with SW scores close to the
lower limit of other extant canids (the side-striped
jackal Canis adustus). Panthera atrox has a shape
score similar to felids but resembles mustelids in
the fracture SW1 score. Smilodon fatalis is similar
in fracture score to some felids like the cheetah
(Acinonyx jubatus) and the jaguar (Panthera onca)
but its shape is very distinct (Fig. 3A). In this
nested sample, mandibular size shows a significant
positive association only with SW1 fracture scores
(rspearman = 0.44, P = 0.019).
PHYLOGENETIC
SIGNAL AND COMPARATIVE TESTS
In Table 3, the K-statistic and probability values are
reported for SW scores including the raw data for
percentage of tooth fracture. All exhibit a significant
phylogenetic signal, with the exception of the percentage of carnassial tooth fracture in both overall and
nested samples, and the percentage of canine fracture
only for the nested sample (N = 28).
Centroid size and SW scores of mandible shape
exhibit a very high phylogenetic signal. On the other
hand, SW scores of tooth fractures have a low but
significant signal. The association between the first
pair of SWs is supported also when phylogeny is
taken into account (PGLS when N = 35, r = 0.408,
FS = 6.60, P = 0.015; with N = 28, r = 0.502, FS = 8.74,
P = 0.006). However, the correlation between the
second pair of SW in the overall sample is not significant (P = 0.81). Nonsignificance also applies to the
association between centroid size and SW1 axes
(P > 0.2) in all cases. On the other hand, diet is still a
significant factor on discriminating the overall sample
for both pairs of SW scores (FS = 6.1975, P < 0.0001)
but not when only carnivores and B/S are analyzed
(FS = 1.435, P = 0.257).
DISCUSSION
EXTANT CARNIVORA
The association between mandibular shape and percentage of tooth fracture is robust in Carnivora and it
is not influenced by phylogeny or by size (whose effect
disappears when phylogeny is taken into account).
Carnivory and hard food consumption are the main
adaptations that drive this association. This is apparent in the SW plot of all species (Fig. 2A) where
omnivores and insectivores clearly occupy a separate
region of the morphospace. They all belong to the
suborder Caniformia (see Supporting information,
Table S1) and are adapted to chewing by means of a
large crushing molar area. This adaptation allows
omnivores/insectivores to distribute masticatory
stress to the posterior area of the mandible, so that
the corpus shape thickens below this region. Even
herbivorous carnivorans show similar mandibular
morphology (Figueirido et al., 2010, 2011; Meloro,
2011a).
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
76
C. MELORO
At the opposite extreme, carnivores and hard
object feeders show a high percentage of fractures
for all the teeth and they are characterized by a
mandible with a more developed molar slicing area.
The enlargement or reduction of molar slicing/
crushing area is a fundamental correlate of carnivoran feeding ecology (Van Valkenburgh, 1988b;
Meloro, 2011a, b; Meloro & O’Higgins, 2011) and
relates well to the percentage of tooth fracture.
However, PLS analyses show that carnivory and
hard object feeding are not mutually exclusive.
Indeed, no significant differences occur in all PLS
analyses between these two feeding categories. They
clearly challenge carnivoran ecomorphology so that,
when only carnivores and hard object feeders are
analyzed, the association between SW becomes
stronger (Fig. 3A). Such a differentiation in SW morphospace is related to the loading of tooth fracture
vector (Fig. 3B): predatory mustelids and the sea
otter (negative SW1 scores) are characterized by a
relatively higher canine fracture percentage compared to canids, hyaenids, and felids, and their
mandible is more curved and thicker below the
molar slicing/crushing area (Fig. 3B). Mustelids
show a well developed molar crushing area, allowing
them to occupy a disparate range of feeding niches
(including omnivory or insectivory).
They have also a thicker corpus below the canine
area, possibly related to higher physical stress in this
region. Such high stress indicates an adaptation to
killing very large prey (Ewer, 1973; Christiansen &
Wroe, 2007): species such as Mustela erminea exhibit
17% of canines being fractured, almost doubling the
grey wolf or the leopard (Panthera pardus), with
9.8%.
Canids, felids, and hyenas show a higher percentage of fractures in premolars and carnassials. Their
mandibles are less curved in the corpus area,
possess a diastema, and have a relatively longer
blade in the carnassial. The coronoid is also projected posteriorly, providing a larger area of attachment for the temporalis relative to the masseter
(Figs 2B, 3B). As expected, this mandibular design
relates to a predaceous lifestyle (Meloro &
O’Higgins, 2011; Meloro et al., 2011). It is also interesting to note that the highest positive fracture
score is exhibited by the least carnivorous predatory
canids: the red fox (Vulpes vulpes) and the island fox
(U. littoralis). In these species, the rate of premolars
fracture is unusually high compared to that of
larger canids. Possibly, the specialization for
hunting on small rodents supplemented with eggs
and vegetable matter challenges foxes’ feeding
behaviour, whose contact with unexpected kinds of
food material is more likely to occur than in the
large predators (Van Valkenburgh, 2009). Addition-
ally, foxes eat the entire body of small rodents
(including skeletons), increasing the risk of contacting small bones with their anterior teeth.
Felids and hyaenids share similar scores in both
fracture and mandibular shape vectors because of
their long carnassial blade. However, they also cluster
with the phylogenetically distant large canids
because of the low phylogenetic signal in fracture
data (Table 2). Killing large prey is an ecomorphological challenge that constrains all predatory carnivorans to cope with high stress in the mandible as
a result of prey holding (Biknevicius & Van Valkenburgh, 1996; Meloro et al., 2011). The SW vectors
show that predatory canids, felids, and hyaenids cope
with higher stress on the anterior canine area differently from mustelids.
The similarity in SW scores of the grey wolf,
hyenas, and the tiger does not support a distinct
ecomorphological adaptation for bone consumption. A
study by Van Valkenburgh (1996) on free-ranging
African carnivores might help to explain this pattern.
Both the African wild dog (Lycaon pictus, which occupies the central plot area in Figs 2A, 3A) and hyenas
consume more bone than felids. This is achieved
differently because Lycaon relies more on carnassials
and post carnassials to crack bones, whereas hyenas
use their premolars (Van Valkenburgh, 1996). Dentition again appears to constrain mandibular morphology in adapting differently to bone consumption
(Werdelin, 1996; Tseng & Binder, 2010). It is noteworthy that premolars are also involved in skin,
muscle, and bone processing (Van Valkenburgh,
1996).
Clearly, if adaptation to carnivory and hard object
feeding favours a functional association between percentage of tooth fracture and mandibular shape,
processes related to developing dentition constrain
masticatory function so that a phylogenetic signal
also occurs in PLS morphospace (Figs 2A, 3A,
Table 3). Previous studies on carnivoran mandible
and dentition showed that ecomorphological differentiation occurred very early in the history of Carnivora
(Meloro et al., 2008; Meloro & Raia, 2010; Meloro &
O’Higgins, 2011), so that members of the same families tend to resemble each other. This applies also
to mandibular shape correlates of tooth fracture
percentage. Interestingly, a significant phylogenetic
signal occurs in some tooth fracture percentage variables (percent of canines, premolars; Table 3), suggesting that they need to be interpreted with caution
and treated statistically using comparative methods.
The PGLS models support an adaptive response of
the mandible shape to feeding stress. Dentition constrains the methods of chewing, although it does not
prevent adaptation to distinct feeding habits taking
place in Carnivora.
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
MANDIBLES-FRACTURE
PLEISTOCENE
FOSSILS
The projection of fossil species in PLS plots suggests
that some of them might show similar variability to
extant taxa (Fig. 2A). Mandibular shape of C. dirus
resembles the living canids, and the North American
lion P. atrox is similar to extant felids (Anyonge &
Baker, 2006; Christiansen & Harris, 2009; Meloro,
2011a). However, the SW plot (Fig. 2A) shows a
reversed pattern, clearly as a result of the unusual
tooth fracture data exhibited by those species. Smilodon fatalis appears distinct in both traits, confirming
its unique morphological adaptations (Andersson,
Norman & Werdelin, 2011; Christiansen, 2008; Slater
& Van Valkenburgh, 2008; Meloro, 2011a). When only
carnivores and hard object feeders are analyzed, all the
three Pleistocene taxa are outliers (Fig. 3A). Competition for carcasses might have been stronger in these
highly carnivorous species, generating higher stress
during feeding (Van Valkenburgh & Hertel, 1993;
Binder, Thompson & Van Valkenburgh, 2002; Van
Valkenburgh, 2009), although why their mandibles did
not evolve to match this condition remains unknown.
Canis dirus possibly follows ecomorphological
variation of extant taxa, even if its canine tooth
fracture frequency is very high compared to extant
canids (generating a low score on SW1 fracture in
Fig. 3A). The pattern for P. atrox is even more
unusual because its canine fracture frequency is
similar to that of mustelids. Canines could be
involved in muscle and bone mastication but Van
Valkenburgh (1996) showed that they are more often
used to manage skin and to open the carcass of dead
prey. The convergence in tooth fracture of these Pleistocene fossils with mustelids suggests that the stress
in prey holding could also explain their feeding
behaviour. Both C. dirus and P. atrox were capable of
killing prey larger than themselves at Rancho La
Brea (Coltrain et al., 2004; Carbone et al., 2009;
Meloro, 2011a) and this factor alone might explain
the unusually high percentage of canine fracture. A
specialization of killing large Pleistocene herbivores
might have increased the risk of canine fracture
during predation considering the larger size of ruminants in the Ice Age (Raia, Meloro & Barbera, 2007;
Pushkina & Raia, 2008). Additionally, a study by
Anyonge & Baker (2006) supported the strong similarity in craniofacial morphology between C. dirus
and C. lupus. Tooth fracture pattern should also be
expected to be similar, although this is not the case.
Canis dirus shows a higher percentage of canine
fractures and lower of premolars (that are also comparatively bigger) versus hyenas and the grey wolf.
For P. atrox, the present study shows a similarity in
mandible shape/tooth fracture pattern only with
canids, felids (Fig. 2A), and mustelids (Fig. 3A), and
77
not with hyaenids. There is little support for a possible adaptation in bone consumption, except for the
fracture frequency similarity with the shell eater
E. lutris, whose dentition and mandible are completely distinct from that of bone consumers.
When considering S. fatalis, it is difficult to make
ecomorphological inferences because of its low bite
force and its unique morphology (Andersson et al.,
2011; McHenry et al., 2007). In the SW plots, Smilodon always shows SW fracture scores less than that of
hyenas and much closer to that of extant felids
(Figs 2A, 3A). Bone consumption also occurs in extant
lions (Domínguez-Rodrigo, 1999), although they chew
only thin ribs and long bone articular epiphyses.
Additionally, Anyonge (1996) provided strong evidence to support a low bone consumption rate in
Smilodon based on microwear.
The unusual trend in mandible shape and tooth
fracture for Pleistocene species appears to be more
indicative of a distinct hunting behaviour and carcass
consumption. The high percentage of canine fractures
supports the idea of higher stress in prey catching
and holding, together with higher (and possibly more
difficult) skin consumption.
Within this context, the environmental condition
should also be considered to provide an alternative
explanation for the fracture/shape pattern in Pleistocene fossils. Several studies indicate that tooth fracture might be facilitated by thermal stress or by
distinct environmental conditions (Brown, Jacobs &
Thompson, 1972; Clough, Kendall MacKenzie &
Broders, 2010 on moose, Alces alces). Similarly, Van
Valkenburgh (2009) found a higher percentage of tooth
fracture for Alaskan red foxes that rely extensively on
carcasses (possibly frozen). The late Pleistocene was a
particularly cold period, facilitating the freezing of
herbivore carcasses and a thickening of the hair and
skin in these species. Interestingly, Leonard et al.
(2007) found a very high percentage of tooth fracture in
eastern-Beringian wolves that could be explained by
increase in bone consumption. However, Stiner (1999)
provided similar evidence for cave bears (Ursus
deningeri) from Yarimburgaz cave of Turkey in the
Middle Pleistocene. The same study also reported an
unusually high percentage of canine fractures that
could not be explained by a peculiar diet.
More research is needed to clarify whether the
increase in tooth fractures in Pleistocene carnivorans
is a generalized phenomenon possibly related to distinct ecomorphologies of Pleistocene species, as well
as peculiar environmental conditions.
CONCLUSIONS
Mandibular shape and the percentage of tooth fracture can be interpreted together to obtain insights
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
78
C. MELORO
into the feeding behaviour of both extant and fossil
Carnivora. There is a strong association between
these two parameters, suggesting that carnivoran
mandibles are designed to sustain different degrees of
masticatory stress. In carnivorous and bone/shell consumers, this association is much stronger, although
the high phylogenetic signal in mandible shape is not
suggestive of convergence between bone consumers
and the specialist shell eater E. lutris. The projection
of Pleistocene species into the shape/fracture morphospace suggests that those taxa might have exhibited a unique feeding behaviour. Higher stress in
carcass feeding possibly occurred as a result of the
size of their favourite prey, the thicker skin and hair,
and the colder environmental conditions.
ACKNOWLEDGEMENTS
I am grateful to museum curators and staff for supporting my numerous visits for data collection. In
particular, I would like to thank P. Jenkins,
L. Tomsett, R. Portela-Miguez, A. Salvador, D. Hills,
J. J. Hooker, P. Brewer, and A. Currant (Natural
History Museum, London); E. Gilissen and W. Wendelen (Royal Museum for Central Africa, Tervuren,
Belgium); P. Agnelli (Museo Zoologico ‘La Specola’
Florence); M. Reilly and J. Liston (Huntherian
Museum and Art Gallery, University of Glasgow,
Glasgow); B. Sanchez, J. Morales, J. Cabarga, and
J. B. Rodriguez (Museo Nacional de Ciencias Naturales, Madrid); A. Kitchener (Royal Museum of
Scotland, Edinburgh); and D. Goujet, P. Tassy, and
C.Signe (Museum National d’Histoire Naturelle,
Paris). I thanks P. Piras and F. Lucci for sharing their
database of felids. This research was supported by
the European Community’s program ‘Structuring the
European Research Area’ under Synthesys at the
Museo Nacional de Ciencias Naturales (ES-TAF 858)
and Museum National d’Histoire Naturelle (FR-TAF
1680) for the project ‘The evolution of feeding habits
in extinct European carnivores’. The visit to the Royal
Museum for Central Africa was supported by the
project ‘Ecomorphology of extant African carnivores’
(BE-TAF 4901). I am indebted to P. Raia for providing
comments on an early version of this manuscript.
J. Allen and two anonymous reviewers considerably
improved the quality of this manuscript. This paper is
dedicated to M. Flinn who is facing the challenge of a
growing dentition.
REFERENCES
Andersson K, Norman D, Werdelin L. 2011. Sabretoothed
carnivores and the killing of large prey. PLoS ONE 10:
e24971.
Anyonge W. 1996. Microwear on canines and killing behaviour in large carnivores: saber function in Smilodon fatalis.
Journal of Mammalogy 77: 1059–1067.
Anyonge W, Baker A. 2006. Craniofacial morphology and
feeding behavior in Canis dirus, the extinct Pleistocene dire
wolf. Journal of Zoology 269: 309–316.
Biknevicius AR, Van Valkenburgh B. 1996. Design for
killing: craniodental adaptations of predators. In: Gittleman
JL, ed. Carnivore behavior, ecology and evolution, Vol. 2.
Ithaca, NY: Cornell University Press, 393–428.
Binder WJ, Thompson EN, Van Valkenburgh B. 2002.
Temporal variation in tooth fracture among Rancho La Brea
dire wolves. Journal of Vertebrate Paleontology 22: 423–
428.
Bininda-Emonds ORP, Gittleman JL, Purvis A. 1999.
Building large trees by combining phylogenetic information:
a complete phylogeny of the extant Carnivora (Mammalia).
Biological Review Cambridge Philosophical Society 74: 143–
175.
Blomberg SP, Garland T Jr, Ives AR. 2003. Testing for
phylogenetic signal in comparative data: behavioral traits
are more labile. Evolution 57: 717–745.
Brown WS, Jacobs HR, Thompson RE. 1972. Thermal
fatigue in teeth. Journal of Dental Research 51: 461–467.
Carbone C, Maddox T, Funston PJ, Mills MGL, Grether
GF, Van Valkenburgh B. 2009. Parallels between playbacks and Pleistocene tar seeps suggest sociality in an
extinct sabretooth cat, Smilodon. Biology Letters 5: 81–
85.
Christiansen P. 2008. Evolution of skull and mandible shape
in cats (Carnivora: Felidae). PLoS ONE 3: e2807.
Christiansen P, Harris JM. 2009. Craniomandibular morphology and phylogenetic affinities of Panthera atrox: implications for the evolution and paleobiology of the lion lineage.
Journal of Vertebrate Paleontology 29: 934–945.
Christiansen P, Wroe S. 2007. Bite forces and evolutionary
adaptations to feeding ecology in carnivores. Ecology 88:
347–358.
Clough MJ, Kendall MacKenzie CS, Broders HG. 2010.
The spatial variation of extreme tooth breakage in an herbivore and potential age structure effects. Annales Zoologici
Fennici 47: 261–271.
Coltrain JB, Harris JM, Cerling TE, Ehleringer JR,
Dearing M-D, Ward J, Allen J. 2004. Rancho La Brea
stable isotope biogeochemistry and its implications for the
palaeoecology of late Pleistocene, coastal southern California. Palaeogeography, Palaeoclimatology, Palaeoecology 205:
199–219.
Crusafont-Pairó M, Truyols-Santonja J. 1957. Estudios
masterométricos en la evolución Fisípedos. I. Los módulos
angulares a y b. II. Los parámetros lineales P, C, y T.
Boletino Instituto Geologico y Minero España 68: 1–140.
Domínguez-Rodrigo M. 1999. Flesh availability and bone
modifications in carcasses consumed by lions: palaeoecological relevance in hominid foraging patterns. Palaeogeography, Palaeoclimatology, Palaeoecology 149: 373–388.
Ewer RF. 1973. The carnivores. New York, NY: Cornell
University Press.
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
MANDIBLES-FRACTURE
Figueirido B, MacLeod N, Krieger J, De Renzi M, PérezClaros JA, Palmqvist P. 2011. Constraint and adaptation
in the evolution of carnivoran skull shape. Paleobiology 37:
490–518.
Figueirido B, Serrano-Alarcón FJ, Slater G, Palmqvist
P. 2010. Shape at the cross-roads: homoplasy and history in
the evolution of the carnivoran skull towards herbivory.
Journal of Evolutionary Biology 23: 2579–2594.
Frost HM. 1964. The laws of bone structure. Springfield, IL:
Charles C Thomas.
Garland T Jr, Bennett AF, Rezende EL. 2005. Phylogenetic approaches in comparative physiology. Journal of
Experimental Biology 208: 3015–3035.
Garland T Jr, Dickerman AW, Janis CM, Jones JA. 1993.
Phylogenetic analysis of covariance by computer simulation.
Systematic Biology 42: 265–292.
Garland T Jr, Ives AR. 2000. Using the past to predict the
present: confidence intervals for regression equations in
phylogenetic comparative methods. American Naturalist
155: 346–364.
Garland T Jr, Midford PE, Ives AR. 1999. An introduction
to phylogenetically based statistical methods, with a new
method for confidence intervals on ancestral states. American Zoologist 39: 374–388.
Hammer Ǿ, Harper DAT, Ryan PD. 2001. PAST: paleontological statistic software package for education and data
analysis. Palaeontologica Electronica 4: 1–9.
Herring SW. 1993. Functional morphology of mammalian
mastication. American Zoologist 33: 289–299.
Holliday JA, Steppan SJ. 2004. Evolution of hypercarnivory: the effect of specialization on morphological and
taxonomic diversity. Paleobiology 30: 108–128.
Leonard JA, Vilà C, Fox-Dobbs K, Koch PL, Wayne RK,
Van Valkenburgh B. 2007. Megafaunal extinctions and
the disappearance of a specialized wolf ecomorph. Current
Biology 17: 1146–1150.
Maddison WP, Maddison DR. 2009. Mesquite: a modular
system for evolutionary analysis, Version 2.72. Available at:
http://mesquiteproject.org
Manfreda E, Mitteroecker P, Bookstein FL, Schaefer K.
2006. Functional morphology of the first cervical vertebra in
humans and nonhuman primates. Anatomical Record. Part
B, New Anatomist 2898: 184–194.
McHenry C, Wroe S, Clausen PD, Moreno K, Cunningham E. 2007. Supermodeled sabercat, predatory behaviour
in Smilodon fatalis revealed by high-resolution 3D computer simulation. Proceedings of the National Academy of
Sciences of the United States of America 104: 16010–
16015.
Meloro C. 2011a. Feeding habits of Plio-Pleistocene large
carnivores as revealed by their mandibular geometry.
Journal of Vertebrate Paleontology 31: 428–446.
Meloro C. 2011b. Morphological disparity in Plio-Pleistocene
large carnivore guilds from Italian peninsula. Acta Palaeontologica Polonica 56: 33–44.
Meloro C, O’Higgins P. 2011. Ecological adaptations of
mandibular form in fissiped Carnivora. Journal of Mammalian Evolution 18: 185–200.
79
Meloro C, Raia P. 2010. Cats and dogs down the tree: the
tempo and mode of evolution in the lower carnassial of fossil
and living Carnivora. Evolutionary Biology 37: 177–186.
Meloro C, Raia P, Carotenuto F, Cobb SN. 2011. Phylogenetic signal, function and integration in the subunits of
the carnivoran mandible. Evolutionary Biology 38: 465–
475.
Meloro C, Raia P, Piras P, Barbera C, O’Higgins P. 2008.
The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zoological
Journal of Linnean Society 154: 832–845.
Oxnard CE. 1993. Bone and bones, architecture and stress,
fossils and osteoporosis. Journal of Biomechanic 26 (suppl.
1): 63–79.
Pasitschniack-arts M, Taylor ME, Mech LD. 1988. Note
on skeletal injuries in an adult arctic wolf. Arctic and Alpine
Research 20: 360–365.
Piras P, Maiorino L, Raia P, Marcolini F, Salvi D,
Vignoli L, Kotsakis T. 2010. Functional and phylogenetic
constraints in Rhinocerotinae craniodental morphology.
Evolutionary Ecology Research 12: 897–928.
Pushkina D, Raia P. 2008. Human influence on distribution
and extinctions of the late Pleistocene Eurasian megafauna.
Journal of Human Evolution 54: 769–782.
Raia P, Carotenuto F, Meloro C, Piras P, Pushkina D.
2010. The shape of contention: adaptation, history and
contingency in ungulate mandibles. Evolution 64–5: 1489–
1503.
Raia P, Meloro C, Barbera C. 2007. Incostancy in predator/
prey ratio in Quaternary large mammal communities
of Italy, with an appraisal of mechanisms. Quaternary
Research 67: 255–263.
Rohlf FJ. 1986–2009. NTSYSpc, Version 2.21c. New York,
NY: Exeter Software.
Rohlf FJ. 2001. Comparative methods for the analysis of
continuous variables: geometric interpretations. Evolution
55: 2143–2160.
Rohlf FJ. 2006a. A comment on phylogenetic correction.
Evolution 60: 1509–1515.
Rohlf FJ. 2006b. tpsDig, Version 2.10. Stony Brook, NY:
Department of Ecology and Evolution, State University of
New York.
Rohlf FJ. 2006c. tpsPLS, Version 1.18. Stony Brook, NY:
Department of Ecology and Evolution, State University of
New York.
Rohlf FJ, Corti M. 2000. Use of two-block partial least
squares to study covariation in shape. Systematic Biology
49: 740–753.
Rohlf FJ, Slice DE. 1990. Extensions of the Procrustes
method for the optimal superimposition of landmarks.
Systematic Zoology 39: 40–59.
Slater GJ, Dumont E, Van Valkenburgh B. 2009.
Implications of predatory specialization for cranial form and
function in canids. Journal of Zoology 278: 181–188.
Slater GJ, Figueirido B, Louis L, Yang P, Van Valkenburgh B. 2010. Biomechanical consequences of rapid
evolution in the polar bear lineage. PLoS ONE 5: e13870.
Slater GJ, Van Valkenburgh B. 2008. Long in the tooth:
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
80
C. MELORO
evolution of sabertooth at cranial shape. Paleobiology 34:
403–419.
Stiner MC. 1999. Cave bear ecology and interactions with
pleistocene humans. Ursus 11: 41–58.
Tseng ZJ, Binder WJ. 2010. Mandibular biomechanics of
Crocuta crocuta, Canis lupus, and the late Miocene Dinocrocuta gigantea (Carnivora, Mammalia). Zoological Journal of
the Linnean Society 158: 683–696.
Tseng ZJ, Wang X. 2011. Do convergent ecomorphs evolve
through convergent morphological pathways? Cranial
shape evolution in fossil hyaenids and borophagine canids
(Carnivora, Mammalia). Paleobiology 37: 470–489.
Van Valkenburgh B. 1988a. Incidence of tooth breakage
among large, predatory mammals. American Naturalist
131: 291–302.
Van Valkenburgh B. 1988b. Trophic diversity in past and
present guilds of large predatory mammals. Paleobiology
14: 155–173.
Van Valkenburgh B. 1996. Feeding behavior in free-ranging,
large African carnivores. Journal of Mammalogy 77: 240–
254.
Van Valkenburgh B. 2007. Déjà vu: the evolution of feeding
morphologies in the Carnivora. Integrative and Comparative
Biology 47: 147–163.
Van Valkenburgh B. 2009. Costs of carnivory: tooth fracture
in Pleistocene and recent carnivorans. Biological Journal of
the Linnean Society 96: 68–81.
Van Valkenburgh B, Hertel F. 1993. Tough times at La
Brea: tooth breakage in large carnivores of the Late
Pleistocene. Science 261: 456–459.
Werdelin L. 1996. Carnivoran ecomorphology: a phylogenetic
perspective. In: Gittleman JL, ed. Carnivore behavior,
ecology, and evolution, Vol. 2. New York, NY: Cornell
University Press, 582–624.
Wroe S. 2010. Cranial mechanics of mammalian carnivores:
recent advances using a finite element approach. In:
Goswami A, Friscia A, eds. Carnivoran evolution. New views
on phylogeny, form and function. Cambridge: Cambridge
University Press, 465–485.
Wroe S, McHenry C, Thomason J. 2005. Bite club: comparative bite force in big biting mammals and the prediction
of predatory behaviour in fossil taxa. Proceedings of the
Royal Society of London Series B, Biological Sciences 272:
619–625.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Figure S1. Phylogenetic tree of 35 extant Carnivora sensu Bininda-Emonds et al. (1999) Carnivora supertree.
Although six polytomies occur, this tree was favoured among other more updated topologies because it allows
a consideration of all the taxa presented in the present study with robust branch lengths in millions of years.
Table S1. List of specimens belonging to extant and fossil Carnivora included in the present study. Diet
categorization is given in parenthesis. Institutional abbreviations: B.M.N.H., British Museum of Natural
History. London, UK; H.M., Huntherian Museum and Art Gallery. University of Glasgow, Glasgow, Scotland,
UK; M.C.Z.R., Museo Civico di Zoologia. Roma, Italy; M.N.C.N., Museo Nacional de Ciencias Naturales, Madrid,
Spain; M.N.H.N., Muséum National d’Histoire Naturelle, Paris, France; M.Z.L.S., Museo Zoologico ‘La Specola’
Firenze, Italy; N.M.B., Naturhistorisches Museum Basel, Switzerland; RMCA, Royal Museum for Central
Africa, Tervuren, Belgium; R.M.S., Royal Museum of Scotland. Edinburgh, Scotland, UK; V.N.A., Museo di
Anatomia Veterinaria Università di Napoli; Z.S.M., Zoologische Staatssammlung München, Munich, Germany.
Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials
supplied by the authors. Any queries (other than missing material) should be directed to the corresponding
author for the article.
© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80