J-STAGE Advance published date: December 22, 2021

WESTERN NORTH PACIFIC KILLER WHALE CRANIUM GROWTHGROWTH-RELATED CHANGES IN CRANIUM OF
KILLER WHALES IN THE WESTERN NORTH PACIFIC
Megumi TAKAHASHI1*, Gen NAKAMURA2 and Hidehiro KATO1, 2
Institute of Cetacean Research, 4–5 Toyomi-cho, Chuo-ku, Tokyo 104–0055, JapanTokyo University of Marine Science and Technology, 4–5–7 Konan, Minato-ku, Tokyo 108–8477, Japan*Corresponding author: takahashi@cetacean.jp
12

Abstract
One of the crucial questions for using the skull morphology for classiﬁcation purposes incetaceans is whether the skull features have growth-dependent diﬀerences. This question wasaddressed by examining cranial specimens collected from killer whales in diﬀerent localitiesof the western North Paciﬁc. The present study is the ﬁrst to investigate developmental change
in the skull morphology of western North Paciﬁc killer whales. A total of 24 cranial measurement characters were examined from 22 animals collected between 1937 and 2011. Two kindsof analyses were conducted 1) the relationships between body length (BL) and cranium length(condylobasal length CBL), and 2) between CBL and each measurement character. For theseanalyses, an allometric equation was used. The relationship between BL and CBL showed anegative growth pattern, consistent with previous studies in delphinid species. The length ofthe lacrimal bone and the width of the internal nasal cavity showed isometric change. Therefore, these characters can be used as criteria for sex and/or species/subspecies classiﬁcation as
their proportions are free from relative change with respect to skull growth in CBL. Regarding
ontogenic growth, this study showed that the anteroposterior length of the temporal fossa, thezygomatic process and the space where the temporal muscle passes became proportionallylarger as their skull grows. The development and activity of temporal muscles would produce
these changes. On the morphometric features involved in the generation and modiﬁcation of
acoustic signals, this study found the following changes: the width of the posterior regions of
the rostrum and preorbital bone became wider; the ventral surface of the preorbital process
became thick and sturdy, and the maxillary crest became more apparent with the skull growth.
Therefore, these morphometric features might be used to characterize species/subspecies of
the killer whales, which have highly divergent foraging behavior and vocalization.
Key words:

killer whale, skull morphology, growth-related change, western North Paciﬁc.

Introduction
The skull is an anatomical feature that consistently and compellingly displays species-speciﬁc characteristics and is an essential tool to study morphological diﬀerentiation (Miyazaki, 1994). Hence, theskull size and shape can be essential as classiﬁcation criteria. Studies on small cetaceans showed thatthe shape and size of the skull could provide information on geographical distribution of the species,
intraspeciﬁc subpopulations with diﬀerent ecological characteristics such as feeding ecology andacoustic properties, and social behavior, e.g., Van Waerebeek (1993), Yoshida et al. (1995), Galatius
and Gol’din (2011), Costa et al. (2016). Kitchener et al. (1990) studied the skull morphology of false
killer whale Pseudorca crassidens from three ocean basins, Australia (n=34), Scotland (n=58), andSouth Africa (n=53), showing considerable divergence among localities, including sexual dimorphism in the skull morphology. They considered this helpful information for the conservation andCetacean Popul. Stud. (CPOPS), Full paper
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management of the species.
Comparative analyses of skull morphology require large sample sizes; however, the availabilityof samples and data for such studies is limited for most cetacean species, including the killer whales
Orcinus orca. Killer whales are distributed throughout all oceans and contiguous seas, from equatorial
regions to the polar pack-ice zones. Still, they are most numerous in coastal waters and cooler areas
where productivity is high (Rice, 1998). Their wildly divergent diet preferences, cultural practices,and external morphological characteristics seem incongruent with their current categorization as asingle taxon (Heyning and Dahlheim, 1988; Pitman and Ensor, 2003; Foote et al., 2009; Morin et al.,2010; Pitman et al., 2011). Resident, transient and oﬀshore killer whale ecotypes have been well characterized since the 1980s in the eastern North Paciﬁc (Bigg et al., 1990).
Further west of the North Paciﬁc, a report identiﬁed multiple killer whale subpopulations throughout the Aleutian Islands: one subpopulation in the eastern and one in the central Aleutian Islands, anda third subpopulation ranging from the western Aleutians to Kamchatka and the Kuril Islands, Russia (Parsons et al., 2013). Recent colonization/re-colonization of the western North Paciﬁc by small
groups of killer whales originating from the central/eastern North Paciﬁc has been suggested (Filatova
et al., 2018). Although the information on this species around Japan is limited, catch records between
1948 and 1957 indicated killer whales were distributed in the coastal waters oﬀ Japan from Hokkaido
to the Okinawan islands. Researches in diﬀerent oceans have revealed the existence of sympatric populations displaying morphological, dietary, and genetic diversiﬁcation e.g., in the Antarctic (Pitman
and Ensor, 2003; LeDuc et al., 2008) and the North Atlantic oceans (Foote et al., 2009, 2010; Morinet al., 2010). Currently, the taxonomic status of killer whales is undergoing scrutiny and possible revision (Krahn et al., 2004; LeDuc et al., 2008; Morin, 2010; Bruyn et al., 2013).
One important question for using the skull morphology for classiﬁcation purposes is whether theskull features have a nature of growth-dependent diﬀerences. In the present study, this question wasaddressed by examining cranial specimens of killer whales collected from diﬀerent localities in thewestern North Paciﬁc. This study is the ﬁrst one to investigate a developmental change in the skull
morphology of killer whales.

Materials and methods
Samples
The list of samples used in the present study is shown in Table 1. Skull samples of killer whales
were available from diﬀerent museums, aquariums and other institutions in Japan. Killer whales werefrom diﬀerent localities of the Paciﬁc coast of Japan, the Okhotsk Sea, and around the Okinawan Islands. A total of 22 skulls of killer whales (seven females, eight males, and seven individuals with nosex information) were available. Body length information was available for 14 whales.
Morphometric feature
Cranial measurements are given in Table 2. Crania were measured in a straight line using an anthropometer to the nearest 0.1 cm. We did not include the mandible bone in this study because it was lostin several individuals. A total of 24 measurements was used in the statistical analysis (Table 2, Fig. 1).
Most of those measurements have been used previously in taxonomic and population identity studies
of Delphinidae species (Perrin, 1975; Kitchener et al., 1990). In this study the measurements wereidentiﬁed using the preﬁx ‘Vx’ (see Table 2). The body length and sex information were obtained fromeach museum, aquarium or university storing a specimen when possible. The observation of genitalorgans determined sex.

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Fig. 1. Killer whale Orcinus orca cranial measurement points. A: Dorsal view of the cranium, B: ventral view,
C: lateral view, and D: posterior view. Measurement points were determined following Perrin (1975) andKitchener et al. (1990) and are abbreviated according to Table 2.

Statistical analysis
The relationships between body length and skull length, and between skull length and each length
measurement were examined using the following allometric equation:y = βxα(1)

where x is body/skull length, y is skull length/each length measurement, β is the intercept of the lineon the y-axis, and α is the slope of the line, also known as the allometric coeﬃcient. The allometriccoeﬃcients (α) at each measurement site were examined using a t-test for classiﬁcation of three different growth patterns: positive allometry (α signiﬁcantly greater than 1), isometric allometry, andnegative allometry (α signiﬁcantly smaller than 1). Analyses by sex were not conducted because of thelimited number of whales with identiﬁed gender. Although the range of sampling years was vast, we
treated them as one sample collection because of the limited number of specimens available.

Results
Relationship between body length (BL) and skull length (condylobasal length CBL)
The relationship between BL and CBL (Fig. 1) was examined in a subset of 14 killer whale samples
for which body length data were available. The BLs in these whales ranged from 218 cm to 785 cm,
which had CBLs of 43.8 cm and 121.7 cm, respectively (samples No. 15 and 8, respectively in Table 1). The CBL showed a negative growth pattern (y=−0.37x0.78, P<0.001) (Fig. 2), indicating that
CBL growth is relatively slower than that of BL.
Relationship between skull length (CBL) and other cranial measurements
Table 2 shows the results of the allometric analyses for the relationship between CBL and each cranial measurement (see also Appendix).
Skull width, rostral length and width
Four of the ﬁve skull width characters (V5, V6, V12, and V13 in Fig. 1 and Table 2) showed a positive growth pattern, though the width at the tip of the antorbital process of the maxilla (V18) was isometric. The rostral width characters (V2–4 and V19) also exhibited positive allometry with the growthof CBL (Table 2). These results showed the braincase becoming relatively shorter, the rostral length
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Table 1. List of specimens of the killer whales from western North Paciﬁc examined in this study, by sex, age,and locality of sampling. Body length (BL) and skull (condylobasal) length (CBL) are also shown.
Sample
no.

Sex

BL
(cm)

CBL
(cm)

Age

LocationYearobtained

Sample ID

Sample holder

1
2
3

F
F
F

547
600
654

98.5
99.2
108.6

—
17*
29*

East China Sea, Okinawa
Nemuro Strait, Rausu
Nemuro Strait, Rausu

1988
2005
2005

M67 (nago-B)
kaitaku-AKW6
rakuno-AKW9

4

F

614

103.8

—

2008

1.2.7

5

F

589

99.7

>28**

2011

Taiji-6

6

F

563

98.3

13*

Paciﬁc Ocean,Kii Peninsula, Taiji
Paciﬁc Ocean,Kii Peninsula, Taiji
Nemuro Strait, Rausu

Nago Museum
Hokkaido Museum
Rakuno Gakuen
University
Port of Nagoya Public
Aquarium
Taiji Whale Museum

2005

7

F

550

99.8

—

Okinawan Island, Japan

1994

AMP-R20AKW2
SUM071

8
9
10
11

M
M
M
M

785
700
704
660

121.7
110.7
118.2
107.9

—
—
—
—

1957
1988
2010
1978

Suma-K01
M66 (nago-A)
SNH10057
Taiji-2

12

M

—

122.0

—

1937

13

M

690

120.6

—

KPMNF1002979
Taiji-1

Kanagawa Prefectural
Museum of Natural History
Taiji Whale Museum

14

M

410

85.1

—

Seto Inland Sea, Hyogo
East China Sea, Okinawa
Soya Strait, Wakkanai
Paciﬁc Ocean,Kii Peninsula, Taiji
Okhotsk, Sakhalin Island,
Gulf of Patience
Paciﬁc Ocean,Kii Peninsula, Taiji
Boso Peninsula, Japan

Ashoro Museum ofPaleontology
Okinawa Churashima
Foundation
Suma Aqualife Park
Nago Museum
Okhotsk Museum Esashi
Taiji Whale Museum

O-15

15

M

218

43.8

—

Boso Peninsula, Japan

16

Uk

—

96.5

—

17

Uk

—

96.2

—

18

Uk

—

104.2

—

Toyokoro-cho,
Hokkaido, Japan
Taiki-cho,
Hokkaido, Japan
Japan

19
20
21
22

Uk
Uk
Uk
Uk

—
—
—
—

106.8
104.9
103.4
104.6

—
—
—
—

Kii Peninsula, JapanKii Peninsula, JapanKii Peninsula, Japan
Okinawan Island, Japan

Tobayama’s CetaceanCollection/TUMSAT***
Tobayama’s CetaceanCollection/TUMSAT***
Ashoro Museum ofPaleontology
Ashoro Museum ofPaleontology
Institute of Cetacean
Research
Taiji Whale Museum
Taiji Whale Museum
Taiji Whale Museum
Okinawa Churashima
Foundation

1966

O-11
2005

AMP-R26

2005

AMP-R27
ICR-001
Taiji-3
Taiji-4
Taiji-5
Okinawa-1*: Age information quoted from Amano et al. (2011).
**: Rearing period.
***: Tokyo University of Marine Science and Technology.

(V1) somewhat longer, and the braincase width relatively more comprehensive (Fig. 3). The zygomatic process of the squamosal bone became laterally more protrusive with CBL growth, in qualitative
observation, as the space where the temporal muscle passes (the ventrolateral opening of the temporal
fossa) was getting more enlarged compared to those of the newborn calf (Fig. 4).
BraincaseIn this study, the braincase was deﬁned as the regions directly covering the brain, including thefrontal, maxilla, premaxilla, ethmoid, sphenoid, squamosal, parietal, interparietal and occipital bones(Uekusa et al., 2018). The measurements indirectly describing the braincase size (V22, V23, and V24)
showed negative allometry or isometry, though the length of squamosal (V14), which is not directly

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Table 2.

Relative growth coeﬃcients and growth patterns of each killer whale skull region.

RegionSiteno.

Measurement characternBased oncondylobasal
Plength (CBL) value†αlnβ

Relative
Adj. R
growthsquarepattern

Skull width

V13 Greatest width of skull
V5
Greatest preorbital width
V6
Least supraorbital width
V12 Greatest width of maxillaries
V18 Width at tip of anterior process of maxilla

22
22
22
21
21

1.13
1.18
1.24
1.34
1.31

−1.04
−1.44
−1.75
−2.19
−2.14

**
**
**
**
0.075

positive
positive
positive
positiveisometry

0.99
0.97
0.98
0.91
0.76

Rostral length
and width

V1
V2
V3

22
22
21

1.13
1.28
1.35

−1.23
−2.49
−2.78

*
**
**

positive
positive
positive

0.98
0.98
0.89

22
20

1.59
1.91

−4.93
−5.81

**
**

positive
positive

0.91
0.93

Greatest parietal width at the posterior section of 21
the frontal
V23 Greatest occipital width within temporal fossa
20
V24 Height of skull
11
V14 Length of zygomatic process of squamosal (right) 22

0.75

0.14

*

negative

0.75

0.95
1.15
1.28

−0.76
−1.52
−2.95

0.795
0.458
**

isometry
isometry
positive

0.54
0.79
0.98

V8

22

1.20

−2.01

**

positive

0.97

21

1.07

−1.91

0.744

isometry

0.57

20

1.35

−3.37

*

positive

0.87

21

1.40

−3.60

0.054

isometry

0.72

Braincase

Temporal fossa

Length of rostrum
Width of rostrum at baseWidth of rostrum at 60 mm anterior to the base of
rostrum
V4
Width of premaxillaries at midlength of rostrum
V19 Width of rostrum at 3/4 length, measured fromposterior end
V22

Greatest length of right temporal fossa, measured
to external margin of raised suture
V9Greatest width of right temporal fossa at right angles to greatest length
V15 Anteroposterior diameter of the ventrolateral
opening of the right temporal fossa
V16 Lateral diameter of the ventrolateral opening of
the right temporal fossa

Nasal area

V7
V20
V21

Greatest width of external nares
21
Greatest width of internal nares
20
Distance from foremost end of junction between 19
nasals to hindmost point of margin of supraoccipital crest

0.85
0.95
0.76

−1.27
−1.52
−1.19

0.398
0.32
0.08

isometry
isometry
isometry

0.55
0.95
0.65

Orbital region

V10

Length of right orbit from apex of preorbital pro- 22
cess of frontal to apex of postorbital process
Length of antorbital process of right lacrimal
22
The antorbital process thickness: the distance 21
from the ventral surface of the lacrimal to thedorsal surface of the maxilla (right-side)

0.53

0.08

**

negative

0.70

1.17
1.84

−3.12
−5.90

0.307
**

isometry
positive

0.72
0.79

V11
V17

: The signiﬁcance of deviation of each relative coeﬃcient from a value of 1 (*: P<0.05, **: P<0.01).

†

related to the braincase size, showed positive allometry (Table 2). According to qualitative observations, the parietal bones in the newborn calf’s temporal crest were laterally curved convex in posteriorview, and the greatest parietal width within the temporal fossa was wide as long as the greatest widthof the skull (Fig. 3). However, the temporal surface of the parietal bones concavely curved with CBL
growth and development of the temporal crest.
Temporal fossa
The anteroposterior length (V8) and the dorsoventral width (V9) of the temporal fossa showed
positive allometry and isometry, respectively (Table 2). Hence, the temporal fossa size became relaCetacean Popul. Stud. (CPOPS), Full paper
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Fig. 2. Relationship between body length and condylobasal length (CBL). Black and white circles indicate
males and females, respectively. The solid line indicates the prediction line from allometry analysis.

tively broader with CBL growth (i.e., horizontally with a long, elliptic shape) (Fig. 4). In qualitative
observations, the dorsal and lateral views of the skulls showed that the posterior ends of the temporal
crest are located far anterior to the posterior end of the occipital condyles in the newborn calf (Fig. 3).
However, along with the growth of the CBL, the posterior ends of the temporal crest were extended ina posterior direction, and the crest of the temporal fossa clearly developed, becoming thick and conspicuously ridged.
The anteroposterior diameter (V15) and the lateral diameter (V16) of the ventrolateral opening border of the temporal fossa showed positive allometry and isometry, respectively. These growth patterns
represented an extension of the space where the temporal muscle passes (Fig. 4). The posterior viewof the skull clearly showed the development of the temporal crests and an exoccipital and squamosal
extension with CBL growth (Fig. 3).

Fig. 3. Dorsal (upper) and posterior (lower) view of four male killer whale crania. Condylobasal length (CBL)and width of these crania scaled to the actual length.

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Fig. 4. Ventral (upper), diagonally right rear (middle) and lateral (lower) views of the newborn calf and adultkiller whale cranium. Orange arrows show the measurement points of the ventrolateral opening border of thetemporal fossa, which consists of the zygomatic process of the squamosal bone posteriorly and the postorbital
process of the frontal bone anteriorly (V15 and V16 in Table 2 and Fig. 1). Orange shades cover the estimatedarea where the temporal muscle is attached.

Nasal area
The width of the nares (V7 and V20) and the anterior junction of nasal to posterior margin of supraoccipital crest length (V21) displayed isometry (Table 2). According to qualitative observations,the adult animals’ nasal and surrounding areas (frontal, parietal, and occipital bones) were particularly
protruded in a dorsal direction, which diﬀered from those of the newborn calf (Fig. 4). Frontal and intraparietal bones were hardly visible as they were covered by maxillary and supraoccipital bones.
Orbital region
The orbit length from the apex of the preorbital process of the frontal bone to the apex of the
postorbital process, represented by V10, exhibited negative allometry (Table 2). The antorbital process
thickness deﬁned as the distance from the ventral surface of the lacrimal to the dorsal surface of themaxilla (V17) indicated positive allometry (Table 2). The relative length of the antorbital process of
the lacrimal bone (V11) showed isometry with CBL growth, and it was thick and sturdy throughout
the growth of a newborn into an adult whale (Fig. 4). The surface of the antorbital process, represented by the maxilla bone, remarkably developed in a dorsal direction.

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Discussion
Relationship between CBL and BL
The ratio of CBL to BL of killer whales declined with growth, and negative allometry was detected (Fig. 2). According to previous studies, the growth rate of some delphinid species’ skull decreases
with growth, and they stop growing when their BL reaches a plateau at a certain age (Perrin, 1975;
Ito and Miyazaki, 1990; Kitchener et al., 1990; Miyazaki and Amano, 1994). Therefore, the results ofthe present study agree with those previous studies. Diﬀerences in physical maturity of BL between
sexes are known in some whale species (e.g., short-ﬁnned pilot whale Globicephala macroryhnchus(Miyazaki, 1990), false killer whale Pseudorca crassidens (Baird, 2002; Ferreira et al., 2014)). Killer
whales exhibit a diﬀerence in size according to sex (adult males are longer than females). Sexual dimorphism (especially in external morphology) is evident in the killer whales. For example, profoundsexual dimorphism was observed in the dorsal ﬁn and ﬂipper size (males have larger structures)(Heyning and Dahlheim, 1988). Therefore it is expected that such sex diﬀerences in the relationshipbetween CBL and BL also occur in the killer whales, and future studies should consider comparisons
between females and males.
Utility of skull measurements as classiﬁcation criteria
Isometric changes in some particular skull measurements mean that such measurements can be employed as criteria for sex and/or species/subspecies classiﬁcation as they are not aﬀected by changes
in the skull size. While other measurements also showed an isometric character, the authors consider
that the best candidates to be used as taxonomical classiﬁcation criteria are the lacrimal bone length(V11) and the width of the internal nasal cavity (V20) because these measurements showed isometry(Table 2).
Lacrimal bone length (V11)
The proportion of V11 to the CBL did not change from newborn calf to adult, thus showing thatit might be helpful for sex prediction analysis in all age stages. A previous study that used only adultkiller whales from the western North Paciﬁc reported that the lacrimal bone length was useful for sex
prediction in this species (Takahashi et al., 2019). The study used linear discriminant analysis and a
Random forest algorithm. However, the authors recommended caution in interpreting their results as
the true sexual dimorphism for the population because the number of samples used in the study was
limited. The present study used a comparatively larger sample size, adding calf killer whales and gaining results to support this measurement character’s utility for classiﬁcation criteria: e.g., sex classiﬁcation. Kitchener et al. (1990) reported a signiﬁcant diﬀerence in this measurement between sexes in thefalse killer whale P. crassidens. This would be collateral evidence supporting our results. Therefore,
we conclude that the killer whale lacrimal bone length might be useful for sex prediction regardless of
specimen age.
Width of the internal nasal cavity (V20)
The width of the internal nasal cavity presented an isometry pattern with a high adjusted R squarevalue (>95%). This measurement character might be used as novel criterion to discriminate species
and subspecies of killer whales because 1) the measurement presented a low individual variance,and 2) the proportion of the measurement never changes with growth. Point 2) makes possible that allavailable samples can be used for discriminatory purposes. With larger sample sizes, this measurement
character might be helpful to discriminate between sexes as well.
Maturity and sex information are usually used in studies on taxonomy based on morphometry. The
body shape (not only the skull shape) of immature animals usually diﬀers from that of mature animals.
Such studies require a considerable number of samples to deal with several factors (e.g., sex, maturi-

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WESTERN NORTH PACIFIC KILLER WHALE CRANIUM GROWTHty). However, materials of this kind are hard to obtain in cetaceans. For this reason, the information on
growth-independent changes of some skull measurements in the present study is essential for future
taxonomical studies of the killer whales.
Eﬀect of ontogenetic growth on cranial shape
The allometry of the cranium of the killer whale was examined to clarify the eﬀects of size (i.e.,
ontogenic growth) on cranium shape. Only the width at the posterior section of the frontal bone (V22)
showed clearly negative allometry, although other features related to skull width (e.g., V13) showed
positive allometry. The analyses suggest that the upper maxillaries width (V12) indicates negative allometry while it represents the dorsal part of the braincase, i.e., it is restricted by the brain size. In contrast, the skull width (V13) and the horizontal diameter of temporal fossa proper (V16), which are notdetermined by brain size, showed positive allometry, creating space for the temporal muscle to pass.
In other words, the temporal muscle can be developed with CBL growth.
The temporal muscle is a fan-shaped muscle situated within the temporal fossa of the skull. The
primary function of this muscle is to produce the movements of the mandible at the temporomandibular joint and thus facilitate the act of mastication. In the case of cetaceans, the temporal muscle is also
known as one of the most developed muscles for mouth-closing (Seagars, 1982; Herring, 2007; Kimet al., 2018). A site of origin for the temporal muscle is the temporal fossa represented by V8 and V9
in our study. Although the width of the temporal fossa in a dorsoventral direction (V9) had no positive allometry, the length in an anteroposterior direction (V8) showed a high development with CBL
growth without being limited in a space produced by brain size. By qualitative observation, the posterior ends of these bones consisted of the temporal fossa extending in a posterior direction, over theposterior end of the braincase. These results indicate an extension of the surface and the crest where
the temporal muscle originates (Fig. 4). In addition, the results showed that the space where the temporal muscle passes were expanded with positive allometry and isometry (V15, 16; Fig. 4). Therefore,
the temporal fossa and temporal crest expansion may be caused by the development of muscle thickness. Especially, the posterior extension of the temporal crest might also increase the length of themuscle itself and increase the area of temporal muscle attachment. In the case of the bottlenose dolphin, the allometry of the temporal fossa implies the development of the temporal muscle with CBL
growth, and similar trends in the allometry of these characters between mature and immature specimens indicate that the development of temporal muscle occurs not only in ontogeny but also in larger
specimens among mature individuals (Kurihara and Oda, 2009). In other words, the feeding habit
aﬀects this morphological feature during both the immature and mature stages. This previous study
speculated that the same tendency might occur in the killer whales since they have a habit of catchingand shearing/biting prey (Ford, 2018). Therefore, if this tendency also occurs in mature killer whales
having diﬀerent feeding habits (i.e., ecotype), this morphological feature should be further examined
for a more sophisticated understanding and increased application in taxonomy.
Killer whale’s rostral length and width characteristics showed positive allometry in this study,
which appears to be related to the development of the feeding apparatus. Several studies using a sufﬁcient number of skull samples, e.g., bottlenose dolphin (Kurihara and Oda, 2009), baleen whales(Nakamura et al., 2012), have concluded that the positive allometry of rostral length is related to thefeeding apparatus, i.e., it reﬂects the growth for extension of the range for prey catching (Costa etal., 2016). For the rostral width, it might have been aﬀected by the development of the lateral rostral
muscles inserted at the lateral side at the rostrum. Mead and Fordyce (2009) concluded that the posterior areas of the rostrum (V2 and V3 in this study) and its attached rostral muscles are involved in thefeeding apparatus. Hence these features can reﬂect diﬀerences in feeding habits between populations.
In addition to the width of the rostrum, the present study results suggested that the width from theventral surface of the lacrimal bone (i.e., ventral surface) to the top of the maxillae bone showed positive allometry. Also, the surrounding area, i.e., the antorbital process of the maxillae bone and the
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preorbital process of the frontal bone, became thick, tough, sturdy, and the maxillary crest became
more remarkable with CBL growth. The posterior areas of the rostrum and the area surrounding theantorbital process of the maxilla are suggested that it is involved in the generation and modiﬁcation of
acoustic signals (Mead, 1975; Huggenberger et al., 2009). These portions are covered by the anterointernus muscle and M. maxillonasolabialis anteroexternus, relating the nasal apparatus structure (Huggenberger et al., 2009). Huggenberger et al. (2009) concluded that these muscles might exert a pulling
force on the connective tissue dorsal to the anterior nasofrontal sac and the rostral bursa cantantis. The
lateral region of the M. maxillonasolabialis anterointernus attaches to connective tissue dorsal to theangle and the inferior vestibulum and may control air movement and pressure in the angle and the nasofrontal sac.
Moreover, Cranford et al. (2011) concluded that all extant toothed whales generate sonar signals
using phonic lips and these muscles and tissues. In the killer whales, various and high-frequency
acoustic behaviors are known, and they can be considered as one of the survival strategies or habits by
population/ecotype (Miller and Bain, 2000; Deecke et al., 2005, 2011; Simon et al., 2006). Therefore,
the apparent developmental change in this area might be considered one of the crucial features of eachkiller whale population/ecotypes, and combining previous studies and our morphological report could
provide valuable evidence on taxonomic studies.
Acknowledgements

The authors thank Dr. Kazutoshi Arai, Mr. Hiromi Saeki, Dr. Hiroshi Katsumata, Dr. Etsuko Katsumata and the othermembers of the Kamogawa Sea World; Dr. Hiroshi Sawamura, Director of the Ashoro Museum of Paleontology; Mr. TairaUsui, Curator of the Okhotsk Museum of Art; Dr. Hajime Taru, Chief Curator of the Kanagawa Prefectural Museum of Natural History; Ms. Kiyomi Nakamura, Curator of the Kobe City Suma Marine Aquarium; Mr. Katsuki Hayashi, Director and
Ms. Tamaki Nakae, Curator of the Whale Museum, Taiji Town; Ms. Haruna Okabe and Dr. Nozomi Kobayashi and the othermembers of the Okinawa Churashima Foundation; Mr. Naofumi Murata, Curator of the Nago Museum; Mr. Makoto Soichi,
former Director, Nagoya Port Aquarium; Dr. Miki Mizushima, Curator, Hokkaido Museum; and Dr. Yoshikazu Sato, Professor, Rakunogakuen University and Dr. Takeharu Bando and Dr. Satoko Inoue of the Institute of Cetacean Research. Comments from anonymous reviewers signiﬁcantly improved this manuscript.

References
Baird, R. 2002. False killer whale (Pseudorca crassidens) pp. 411–412 In: Perrin, W.F., Würsig, B. and Thewissen, J.G.M.
(eds.). Encyclopedia of Marine Mammals, Second edition. Academic Press, San Diego, CA. 1352 pp.
Bigg, M.A., Olesiuk, P.F., Ellis, G.M., Ford, J.K.B. and Balcomb, K.C. 1990. Social organization and genealogy of resident
killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Rep. int. Whal. Commn.
(Special issue) 12: 383–405.
Costa, A.P.B., Rosel, P.E., Daura-Jorge, F.G. and Simões-Lopes, P.C. 2016. Oﬀshore and coastal common bottlenose dolphins of the western South Atlantic face-to-face: What the skull and the spine can tell us. Mar. Mamm. Sci. 32: 1433–
1457. doi: 10.1111/mms.12342.
Cranford, T.W., Elsberry, W.R., Van Bonn, W.G., Jeﬀress, J.A., Chaplin, M.S., Blackwood, D.J., Carder, D.A., Kamolnick,T., Todd, M.A. and Ridgway, S.H. 2011. Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): Evidence for two sonar Sources. J. Exp. Mar. Biol. Ecol. 407: 81–96. doi: 10.1016/j.jembe.
2011.07.010.
De Bruyn, P.J.N., Tosh, C.A. and Terauds, A. 2013. Killer whale ecotypes: is there a global model? Biol. Rev. 88: 62–80. doi:
10.1111/j.1469-185X.2012.00239.x.
Deecke, V.B., Ford, J.K.B. and Slater, P.J.B. 2005. The vocal behaviour of mammal-eating killer whales: Communicatingwith costly calls. Anim. Behav. 69: 395–405. doi: 10.1016/j.anbehav.2004.04.014.
Deecke, V.B., Nykänen, M., Foote, A.D. and Janik, V.M. 2011. Vocal behaviour and feeding ecology of killer whales Orcinus
orca around Shetland, UK. Aquat. Biol. 13: 79–88. doi: 10.3354/ab00353.
Ferreira, I., Kasuya, T., Marsh, H. and Best, P. 2014. False killer whales (Pseudorca crassidens) from Japan and South Africa: Diﬀerences in growth and reproduction. Mar. Mammal Sci. 30: 64–84. doi: 10.1111/mms.12021.
Filatova, O.A., Borisova, E.A., Meschersky, I.G., Logacheva, M.D., Kuzkina, N.V., Shpak, O.V., Morin, P.A. and Hoyt,
E. 2018. Colonizing the wild west: low diversity of complete mitochondrial genomes in western North Paciﬁc killer
whales suggests a founder eﬀect. J. Hered. 109: 735–743. doi: 10.1093/jhered/esy037.
Foote, A.D., Newton, J., Piertney, S.B., Willerslev, E. and Gilbert, M.T.P. 2009. Ecological, morphological and genetic

184

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 175–188

WESTERN NORTH PACIFIC KILLER WHALE CRANIUM GROWTH
divergence of sympatric North Atlantic killer whale populations. Mol. Ecol. 18: 5207–5217. doi: 10.1111/j.1365294x.2009.04407.x.
Foote, A.D., Vilstrup, J.T., De Stephanis, R., Verborgh, P., Abel Nielsen, S.C., Deaville, R., Kleivane, L., Martín, V., Miller,
P.J., Oien, N., Pérez-Gil, M., Rasmussen, M., Reid, R.J., Robertson, K.M., Rogan, E., Similä, T., Tejedor, M.L., Vester,H., Víkingsson, G.A., Willerslev, E., Gilbert, M.T. and Piertney, S.B. 2010. Genetic diﬀerentiation among North Atlantic killer whale populations. Mol. Ecol. 20: 629–641. doi: 10.1111/j.1365-294X.2010.04957.x.
Ford, J.K.B. 2018. Killer whales Orcinus orca. pp. 531–537 In: Würsig, B. et al. (eds.) Encyclopedia of Marine Mammals,
Third edition. Academic Press & Elsevier, New York.
Galatius, A. and Gol’din, P.E. 2011. Geographic variation of skeletal ontogeny and skull shape in the harbour porpoise(Phocoena phocoena). Can. J. Zool. 89: 869–879. doi: 10.1139/z11-059.
Herring, S.W. 2007. Masticatory muscles and the skull: A comparative perspective. Arch. Oral Biol. 52: 296–299.
doi: 10.1016/j.archoralbio.2006.09.010.
Heyning, J.E. and Dahlheim, M.E. 1988. Orcinus orca. Mamm. Species 304: 1–9. doi: 10.2307/3504225.
Huggenberger, S., Rauschmann, M.A., Vogl, T.J. and Oelschläger, H.H.A. 2009. Functional morphology of the nasal complex in the harbor porpoise (Phocoena phocoena L.). Anat. Rec. 292: 902–920. doi: 10.1002/ar.20854.
Ito, H. and Miyazaki, N. 1990. Skeletal development of the striped dolphin (Stenella coeruleoalba) in Japanese Waters.
J. Mamm. Soc. Japan 14: 79–96. doi: 10.11238/jmammsocjapan1987.14.79.
Kim, S.E., Arzi, B., Garcia, T.C. and Verstraete, F.J.M. 2018. Bite forces and their measurement in dogs and cats. Front. Vet.
Sci. 5: 1–6. doi: 10.3389/fvets.2018.00076.
Kitchener, D.J., Ross, G.J.B. and Caputi, N. 1990. Variation in skull and external morphology in the false killer whale,
Pseudorca crassidens, from Australia, Scotland and South Africa. Mammalia. 54: 119–136. doi: 10.1515/
mamm.1990.54.1.119.
Krahn, M. M., Ford, M. J., Perrin, W. F., Wade, P. R., Angliss, R. P., Hanson, M. B., Taylor, B. L., Ylitalo, G. M., Dahlheim,
M. E., Stein, J. E. and Waples, R. S. 2004. Status review of Southern resident killer whales (Orcinus orca) under theendangered species Act. NOAA Tech. Memo. NMFS-NWFSC-62. 73 pp.
Kurihara, N. and Oda, S. 2009. Eﬀects of size on the skull shape of the bottlenose dolphin (Tursiops truncatus). Mammal
Study 34: 19–32. doi: 10.3106/041.034.0104.
LeDuc, R.G., Robertson, K.M. and Pitman, R.L. 2008. Mitochondrial sequence divergence among Antarctic killer whale ecotypes is consistent with multiple species. Biol. Lett. 4: 426–429. doi: 10.1098/rsbl.2008.0168.
Mead, J.G. 1975. Anatomy of the external nasal passages and facial comples in the Delphinidae (Mammalia: Cetacea).
Smithson. Contrib. Zool. 207: 1–72. doi: 10.5479/si.00810282.207.
Mead, J. G. and Fordyce, R. E. 2009. The Therian Skull: A Lexicon with Emphasis on the Odontocetes. Smithsonian Institution Scholarly Press, Washington D.C., USA. 249 pp. doi: 10.5479/si.00810282.627.
Miller, P.J.O. and Bain, D.E. 2000. Within-pod variation in the sound production of a pod of killer whales. Orcinus orca.
Anim. Behav. 60: 617–628. doi: 10.1006/anbe.2000.1503.
Miyazaki, N. 1994. Skull morphology of small cetacea. A consideration of taxonomic problems in the short-ﬁnned pilot
whale, Globicephala macrorhynchus, in Japanese waters. Honyurui Kagaku [Mammalian Science] 34(1): 31–42.
(In Japanese). doi: 10.11238/mammalianscience.34.31.
Miyazaki, N. and Amano, M. 1994. Skull morphology of two forms of short-ﬁnned pilot whales oﬀ the Paciﬁc coast ofJapan. Rep. int. Whal. Commn. 44: 499–507.
Morin, P.A., Archer, F.I., Foote, A.D., Vilstrup, J., Allen, E.E., Wade, P., Durban, J., Parsons, K., Pitman, R., Li, L., Bouffard, P., Nielsen, S.C.A., Rasmussen, M., Willerslev, E., Gilbert, M.T.P. and Harkins, T. 2010. Complete mitochondrial
genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res. 20: 908–
916. doi: 10.1101/gr.102954.109.
Nakamura, G., Kato, H. and Fujise, Y. 2012. Relative growth of the skull of the common minke whale Balaenoptera acutorostrata from the North Paciﬁc in comparison to other Balaenoptera species. Mammal Study 37: 105–112. doi:
10.3106/041.037.0201.
Parsons, K.M., Durban, J.W., Burdin, A.M., Burkanov, V.N., Pitman, R.L., Barlow, J., Barrett-Lennard, L.G., LeDuc, R.G.,
Robertson, K.M., Matkin, C.O. and Wade, P.R. 2013. Geographic patterns of genetic diﬀerentiation among killer
whales in the northern North Paciﬁc. J. Hered. 104: 737–754. doi: 10.1093/jhered/est037.
Perrin, W.F. 1975. Variation of spotted and spinner porpoises (genus Stenella) in the Eastern Paciﬁc and Hawaii. Bull.
Scripps Inst. Oceanogr. 22: 1–206.
Pitman, R.L., Durban, J.W., Greenfelder, M., Guinet, C., Jorgensen, M., Olson, P.A., Plana, J., Tixier, P. and Towers, J.R.
2011. Observations of a distinctive morphotype of killer whale (Orcinus orca), Type D, from subantarctic waters. Polar
Biol 34: 303–306. doi: 10.1007/s00300-010-0871-3.
Pitman, R.L. and Ensor, P. 2003. Three forms of killer whales (Orcinus orca) in Antarctic waters. J. Cetacean. Res. Manage.
5: 131–139.
Rice, D.W., 1998. Marine Mammals of the World. Systematics and Distribution. Soc. Mar. Mamm., Special Publication 4:
1–231.
Seagars, D.J. 1982. Jaw structure and functional mechanics of six delphinids (Cetacea: Odontoceti). [M.S. Thesis], San
Diego State University, San Diego, California. 179 pp.
Simon, M., Ugarte, F., Wahlberg, M. and Miller, L.A. 2006. Icelandic killer whales Orcinus orca use a pulsed call

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 175–188

185

TAKAHASHI, NAKAMURA AND KATO
suitable for manipulating the schooling behaviour of herring Clupea harengus. Bioacoustics 16: 57–74. doi:
10.1080/09524622.2006.9753564.
Takahashi, M., Kato, H. and Kitakado, T. 2019. Sex prediction by machine learning methods for small sample sizes: A casestudy of cranial measurements of killer whales (Orcinus orca). Honyurui Kagaku [Mammalian Science] 59: 67–78. (InJapanese). doi: 10.11238/mammalianscience.59.67.
Van Waerebeek, K. 1993. Geographic variation and sexual dimorphism in the skull of the dusky dolphin, Lagenorhynchus
obscurus (Gray, 1828). Fish. Bull. (Wash. D. C.) 91: 754–774.
Yoshida, H., Shirakihara, K., Shirakihara, M. and Takemura, A. 1995. Geographic variation in the skull morphology of the
ﬁnless porpoise Neophocaena phocaenoides in Japanese waters. Fish. Sci. 61: 555–558.

Received: January 31, 2021
Accepted: August 5, 2021
Published online: December 22, 2021

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Appendix
Changes in the proportion of each measured character to the CBL of killer whales in the western
North Paciﬁc. Black, white, and gray indicate male, female, and sex-unknown, respectively. The solidline indicates the prediction line from allometry analyses. Skull morphometric feature measurements
are abbreviated according to Table 2.

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Appendix (Continued).

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