Turkish Journal of Veterinary & Animal Sciences

Volume 43 Number 4 Article 14

1-1-2019

Morphometric analysis of the skulls of domestic cattle (Bos

taurus L.) and water buffalo (Bubalus bubalis L.) in Turkey
ERMİŞ ÖZKAN

ABU BAKAR SIDDIQ

KİFAYET OYA KAHVECİOĞLU

MUHSİN ÖZTÜRK

VEDAT ONAR

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Recommended Citation
ÖZKAN, ERMİŞ; SIDDIQ, ABU BAKAR; KAHVECİOĞLU, KİFAYET OYA; ÖZTÜRK, MUHSİN; and ONAR, VEDAT
(2019) "Morphometric analysis of the skulls of domestic cattle (Bos taurus L.) and water buffalo (Bubalus
bubalis L.) in Turkey," Turkish Journal of Veterinary & Animal Sciences: Vol. 43: No. 4, Article 14.
https://doi.org/10.3906/vet-1903-66
Available at: https://journals.tubitak.gov.tr/veterinary/vol43/iss4/14

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 Turkish Journal of Veterinary and Animal Sciences Turk J Vet Anim Sci
(2019) 43: 532-539
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© TÜBİTAK
Research Article doi:10.3906/vet-1903-66

Morphometric analysis of the skulls of domestic cattle (Bos taurus L.) and water buffalo
(Bubalus bubalis L.) in Turkey
1, 2 1 3 1
Ermiş ÖZKAN *, Abu Bakar SIDDIQ , Kifayet Oya KAHVECİOĞLU , Muhsin ÖZTÜRK , Vedat ONAR 
1
Department of Anatomy, Faculty of Veterinary Medicine, İstanbul University-Cerrahpaşa, İstanbul, Turkey
2
Department of Anthropology, Faculty of Letters, Mardin Artuklu University, Mardin, Turkey
3
Faculty of Health Science, İstanbul Esenyurt University, İstanbul, Turkey

Received: 22.03.2019 Accepted/Published Online: 05.07.2019 Final Version: 07.08.2019

Abstract: A total of 20 domestic cattle (Bos taurus L.) and 15 water buffalo (Bubalis bubalis L.) skulls were analyzed in this study. All of
the specimens belonged to female individuals. Using a total of 27 craniometric measurements from each of the skulls, 9 indices were
calculated. Although there were statistically significant differences between the linear measurements of the skulls of both species, while
calculating the indices with their ratios, the values of the measurements of the facial area were determinative in the craniology. Among
these indices, the facial index 1 value was statistically significant (P < 0.01) in the comparison of these two species. On the other hand,
while considering the orbit and foramen magnum measurements, in contrast with the transversal measurement, the height was more
determinant for their index and form.

Key words: Cattle, water buffalo, skull, morphometry, Turkey

1. Introduction morphometry has been a significant topic, not only for the
The measurement and documentation of cattle skulls study of individuals of the same species but also animals
has been of great importance in discussions about the from different species [7].
origin of cattle [1]. Rütimeyer’s work led to the beginning The tribe Bovini in the subfamily Bovinae was reported
of addressing the skull type, particularly in the study of to have three main genera [8]: Bos (domestic cattle),
evolutionary origin and classification of cattle [2]. However, Bubalis (water and swamp buffalo), and Syncerus (African
cattle classification according to skull measurements was buffalo) [8]. Morphologically and genetically, cattle breeds
first carried out by Wilckens [3] in 1876, inspired by the were described as two main types, respectively, as modern
works of Rütimeyer [4] and Nathusius [5] in 1867 and European cattle breeds as Primigenius and Indian cattle
1872, respectively [2]. breeds as Zebu [9]. On the other hand, buffalo were
The Linnaean taxonomy system, which mainly grouped into two main types, correspondingly, as African
emphasizes morphological differences, led to the wild buffalo and Asian buffalo. The domestic buffalo
categorization of cattle species based on their cranial were further divided into 2 groups as river buffalo and
shape, as well as the lengths and curves of their horns. In swamp buffalo [10–12]. However, the buffalo in Turkey
this classification system, therefore, the classification of are called Anatolian buffalo, and they originated from the
cattle skulls in an archaeological assemblage is likely to Mediterranean buffalo under the subgroup of river buffalo
be possible [2] since craniology has also been used for the [13].
identification and comparison of Bos species at prehistoric Although there is some information about the
sites [6]. craniology and craniometry of domestic cattle [6,14–19]
The origin of the craniometric study of cattle dates and some studies about the craniology of nondomesticated
back to the end of the 18th century [1]. However, it was bovine species [8,20,21], in general, there are scarce
reported that following this period, archaeozoologists data regarding this field. Moreover, it was observed that
gradually shifted their attention in domestic cattle studies these craniometric studies were based on the study by
[2]. Since the similarities and differences between the Duerst [22] and were mainly developed through these
species can only be revealed by comparative studies, skull measurements.
* Correspondence: [email protected]
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This work is licensed under a Creative Commons Attribution 4.0 International License.
 ÖZKAN et al. / Turk J Vet Anim Sci

It was argued, in a study on the craniology of domestic The morphometric measurements (Figures 1A–1H)
cattle breeds [6] that the results were quite variable, obtained in this study are presented below:
especially regarding the horn length of Bos taurus, and 1. Total length (TL): acrocranion-prosthion
there was a possibility of finding intraspecies differences. 2. Condylobasal length (CBL): aboral border of the
One of the Indian breeds, Zebu, was reported to possess a occipital condyles-prosthion
very long and narrow skull with a narrow protuberantia 3. Basal length (BL): basion-prosthion
intercornualis in the aboral part of the frontal region, 4. Short skull length (SSL): basion-premolare
particularly in the region between the horns [23]. The 5. Premolare-prosthion (PP)
osteology of the Savannah buffalo was reported as not 6. Viscerocranium length (VCL): nasion-prosthion
similar to that of domestic cattle, Egyptian water buffalo, 7. Median frontal length (MFL): acrocranion-nasion
or Asian water buffalo [8]. The swamp buffalo was reported 8. Greatest length of the nasals (GLN): nasion-rhinion
to have a long skull with the effect of the width on its skull 9. Lateral facial length (LFL): ectorbitale-prosthion
shape [20]. 10. Dental length (DL): postdentale-prosthion
On the other hand, despite having a different cranium, 11. Lateral length of the premaxilla (LLP):
Neolithic cattle were recognized as an archetype of nasointermaxillare-prosthion
domestic cattle, assuming that the cattle cranium remained 12. Greatest inner length of the orbit (GILO):
relatively unchanged over time [2]. However, it was also ectorbitale-entorbitale
reported that the absolute size was variable among cattle 13. Greatest inner height of the orbit (GIHO)
craniums and the lowest coefficient of variation was found 14. Greatest mastoid breadth (GMB): otion-otion
for basal length [6]. 15. Greatest breadth of the occipital condyles (GBOC)
For the postnatal ontogeny of cattle, two basic indices 16. Greatest breadth at the bases of the paraoccipital
have been used in the estimation of the changes in the skull processes (GBPP)
ratios: the frontal and facial indices, which were reported 17. Greatest breadth of the foramen magnum (GBFM)
to have been used as a common denominator, showing 18. Height of the foramen magnum (HFM): basion-
significant changes in the maximum width (Ect-Ect), opisthion
median frontal length (MFL) (Op-N), and viscerocranium 19. Least occipital breadth (LOB): distance between the
length (VL) ratios of the skull compared to their mutual most medial points of the aboral borders of the temporal
values [24]. However, there was an effect of the sex of the grooves
individual on some skull dimensions, such as the width 20. Least frontal breadth (LFB): breadth of the
and height measurements, which commonly tended to be narrowest part of the frontal aboral of the orbits
larger in bulls, while the length measurements were the 21. Greatest breadth of the skull (GBS): ectorbitale-
same in both sexes [6,14]. ectorbitale
Originating from the river buffalo, and unlike the 22. Least breadth between the orbits (LBO): entorbitale-
swamp buffalo, Anatolian buffalo are raised mainly for entorbitale
milk production. It was also reported that these buffalo 23. Facial breadth (FB): across the facial tuberosities
are genetically different from the swamp buffalo [25]. They 24. Breadth across the premaxillae on the oral
are widely found animals [10] and have a unique genotype protuberances (BPOP)
adapted to the ecological conditions of Anatolia [26]. By 25. Greatest palatal breadth (GPB): measured across
comparing the basic craniometric characteristics, this the outer borders of the alveoli
study attempts to illustrate the similarities and differences 26. Greatest height of the occipital region (GHOR):
between the skull morphometry of domestic cattle (Bos basion-highest point of the intercornual ridge in the
taurus) and Anatolian buffalo (Bos bubalis). median plane
27. Least height of the occipital region (LHOR):
2. Materials and methods opisthion-highest point of the intercornual ridge in the
The skulls of 20 cattle (Bos taurus L.) and 15 buffalo median plane
(Bubalis bubalis L.), aged between 3 and 7 years, were A total of 9 indices were calculated using the obtained
used as samples in this study. All of the skulls belonged to morphometric measurements. The index calculations were
female individuals. The specimens are currently available based on a comparison of both the data obtained from
in the collection of the Department of Anatomy, Faculty these two species and the data available in the literature.
of Veterinary Medicine, İstanbul University-Cerrahpaşa, The calculated indices in this study are presented
Turkey. A total of 27 morphometric measurements were below:
taken from each of the skull samples based on the method Skull index = GBS / TL × 100
of von den Driesch [27] using a 0.5-mm digital caliper. Facial index 1 = FB / VCL × 100

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Figure 1. Measurements of the cranium taken in this study. (A) Dorsal view of the cattle skull, (B) basal view of the cattle skull, (C)
lateral view of the cattle skull, (D) occipital view of the cattle skull, (E) occipital view of the water buffalo skull, (F) dorsal view of the
water buffalo skull, (G) basal view of the water buffalo skull, (H) lateral view of the water buffalo skull. Ak: Acrocranion, Ba: basion,
Ect: ectorbitale, Ent: entorbitale, N: nasion, Ni: nasointermaxillare, O: opisthion, Ot: otion, Rh: rhinion, P: prosthion, Pd: postdentale,
Pm: premolare.

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Facial index 2 = GBS / VCL × 100 the orbit of the cattle had a longitudinal oval structure.
Frontal index = GBS / MFL × 100 Significant correlations were also noticed between the
Basal index = GBS / BL × 100 correlation of the orbital index and the self-forming
Length-length index = MFL / VCL factors: positive with the height measurement, negative
Palatal index = GPB / DL × 100 with the transverse lengths, and varying between P < 0.05
Orbital index = GIHO / GILO × 100 and P < 0.01.
Foramen magnum index = HFM / GBFM × 100 With the exception of the LFB and greatest breadth
The mean values and standard deviations of all of the measurements of the foramen magnum, the other
craniometric measurements and indices were calculated neurocranium measurements of the skulls presented
using SPSS 21 (IBM Corp., Armonk, NY, USA). In addition, significant differences ranging from P < 0.05 to P < 0.01.
the values of both the cattle and buffalo were compared While measuring the LFB, one of the measurements from
using Student’s t-test in the same software program. the frontal region, no statistically significant difference
was found among the buffalo in contrast to a higher value
3. Results in the cattle. The foramen magnum had a more rounded
The cattle and buffalo skull measurements were evaluated in shape in the cattle, while it was more oval in the buffalo.
three different groups. The first group included the general However, only the difference between the height values of
skull and orbit measurements (Table 1), the second group the foramen magnum was statistically significant. This also
included the neurocranium measurements (Table 2), and showed the effect of height on the shape of the foramen
the third group included the viscerocranium measurements magnum in both species.
(Table 3). The orbit measurements were evaluated with the The differences between the mean values of both
general skull group because of its location at the border of species were insignificant in 4 of the 10 viscerocranial
the neurocranium and viscerocranium. measurements. These were the prosthion-premolare,
Except for the orbit, the differences between the mean DL, LLP, and breadth across the premaxillae on the oral
values of the general skull measurements were significant protuberance measurements, respectively. Except for these
(P < 0.01) for these species. However, the values were 4 particular measurements, the 6 other measurements had
higher in the cattle than in buffalo. higher values in the buffalo samples, but the differences
Almost the same value was found for the greatest were not statistically significant. The VCL was greater in
inner length measurement of the orbit among the cattle the cattle than in the buffalo. Since the VCL was longer,
and buffalo. The minimal difference between them was the facial region was longer than the neurocranium in the
statistically insignificant. However, the inner height cattle samples. It was also observed that the facial index 1
measurement of the orbit was observed to have a higher value was larger in cattle than in buffalo, and the difference
mean value in cattle (66.35 ± 4.83 mm). On the other between the mean values of both species was statistically
hand, the difference between the values in the buffalo was significant (Table 4).
statistically significant (P < 0.01). This further indicated Although the skull size in the cattle was larger than in
that the orbit of the buffalo was transverse oval, whereas the buffalo, the index values were almost the same in both

Table 1. Means of the general skull and orbit measurements.

Species Statistics TL CBL BL SSL GILO GIHO

Mean 529.52** 519.56** 486.24** 336.58** 60.34 NS
66.35**
N 20 20 20 20 20 20
Cattle SD 15.88 15.85 15.76 11.46 2.55 4.83
Minimum 499.73 485.73 454.96 317.26 56.51 59.96
Maximum 558.05 543.40 512.92 357.76 66.04 75.14
Mean 471.97** 482.34** 450.13** 295.23** 60.58 NS
57.49**
N 15 15 15 15 15 15
Water buffalo SD 45.77 45.93 44.99 28.06 6.88 4.32
Minimum 410.68 420.82 389.66 256.42 54.58 50.83
Maximum 528.40 541.75 505.15 332.63 75.47 68.98

NS
: Not significant, **: P < 0.01.

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Table 2. Means of the neurocranial part of the skull.

Species Statistics MFL GMB GBOC GBPP GBFM HFM LOB LFB GBS GHOR LHOR
Mean 233.49** 231.51** 113.28** 172.59** 42.74NS 38.87** 136.77** 169.95NS 228.93** 170.32* 131.32**
N 20 20 20 20 20 20 20 20 20 20 20
Cattle SD 12.06 11.25 5.68 8.14 2.97 2.23 12.70 9.56 10.16 7.45 7.32
Minimum 214.06 205.42 103.22 150.92 36.60 34.63 119.71 157.64 207.15 156.60 114.69
Maximum 255.86 245.54 129.92 184.63 50.27 42.56 159.93 185.37 243.74 184.66 144.93
Mean 213.89** 199.23** 98.41** 151.30** 40.78 NS
34.48** 101.38** 172.39 NS
202.80** 177.49* 168.36**
N 15 15 15 15 15 15 15 15 15 15 15
Water
SD 16.38 22.40 5.71 14.64 5.38 3.66 7.50 9.48 19.23 11.85 12.46
buffalo
Minimum 183.72 167.70 89.17 126.91 29.51 29.05 89.53 155.14 169.85 154.96 140.63
Maximum 239.13 226.75 107.78 174.61 56.21 45.09 115.52 191.49 228.00 191.70 184.53

: Not significant, *: P < 0.05, **: P < 0.01.

NS

Table 3. Means of the viscerocranial part of the skull.

Species Statistics VCL PP GLN LFL DL LLP LBO FB BPOP GPB

Mean 297.95* 151.12NS 199.88* 359.99* 284.70NS 160.25NS 177.14** 173.39** 92.04NS 148.41**
N 20 20 20 20 20 20 20 20 20 20
Cattle SD 15.04 8.46 13.08 29.76 12.70 12.20 8.10 8.45 4.99 5.92
Minimum 271.24 138.72 178.47 243.92 247.16 138.33 161.21 159.76 82.29 137.26
Maximum 326.77 168.73 229.74 389.13 306.43 184.42 191.25 190.22 102.50 157.71
Mean 273.45* 155.87NS 182.43* 333.09* 286.79NS 165.98NS 135.56** 133.36** 88.73NS 125.75**
N 15 15 15 15 15 15 15 15 15 15
Water
SD 37.38 17.60 24.58 34.67 32.76 26.45 16.28 17.84 23.64 16.40
buffalo
Minimum 229.20 133.37 143.28 284.93 230.49 133.45 107.44 106.60 26.29 103.61
Maximum 322.56 178.56 219.70 371.12 331.27 211.63 158.67 158.55 112.08 148.55

: Not significant, *: P < 0.05, **: P < 0.01.

NS

species and the minimal difference between them was not A positively significant correlation (Table 5) was
significant when evaluated according to the skull index. found between the facial index 1 and the FB. On the other
A negative correlation was observed between the skull hand, a low relationship was found between the VCLs. A
index and the TL. On the other hand, a positive correlation significance of P < 0.01 between the facial index 1 values of
was found between the skull index and GBS (Table 5). the two species was observed due to the fact that the facial
However, the level of both correlations was quite low and index was more effective than the VCL.
statistically insignificant. While observing the correlation between the factors
There were significant differences between the facial producing the basal index values in both species, the GBS
index 1 values of the cattle and buffalo (P < 0.01). The cattle value was statistically significant when compared to the
and buffalo had a ratio of 1.72 and 2.05 between the skull others.
length and FB, respectively. The facial region was narrower
when compared to the skull length in the buffalo. A similar 4. Discussion
situation was seen for the palatal index evaluated in the Since Rütimeyer’s work in 1867, scientific studies of
viscerocranial part. bovine skulls have been the center of attention for

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Table 4. Cranial indices of the cattle and water buffalo.

Foramen
Skull Facial Facial Frontal Basal Length Palatal Orbital
Species Statistics magnum
index index 1 index 2 index index index index index
index
Mean 43.23NS 58.28** 76.91NS 98.29NS 47.08** 0.786NS 52.20** 110.01** 91.31*
N 20 20 20 20 20 20 20 20 20
Cattle SD 1.50 3.27 2.96 6.79 1.43 0.060 2.60 7.24 7.68
Min 39.77 51.78 70.54 89.08 44.33 0.655 48.43 97.04 79.94
Max 45.97 66.90 81.48 113.87 50.48 0.868 59.21 122.82 108.63
Mean 43.01NS 48.88** 74.70NS 94.87NS 45.11** 0.791NS 43.82** 95.56** 85.03*
N 15 15 15 15 15 15 15 15 15
Water
SD 1.84 3.12 5.69 6.28 1.99 0.087 2.25 8.48 6.73
buffalo
Min 39.58 41.41 65.98 83.71 42.05 0.665 39.21 81.59 78.18
Max 46.04 52.58 84.74 106.73 48.31 0.957 47.48 105.05 104.61

NS
: Not significant, *: P < 0.05, **: P < 0.01, Min: minimum, Max: maximum.

Table 5. Correlation analysis between the indices and theirs factors.

TL GBS FB VCL MFL BL GPB DL GIHO GILO HFM GBFM

Skull index –0.090 NS

0.324 NS

Facial index 1 0.793** 0.174NS

Facial index 2 0.077 NS
–0.493**
Frontal index 0.590NS –0.197NS
Basal index 0.535** 0.088NS
Length-length index –0.723** 0.208NS
Palatal index 0.756** –0.116NS
Orbital index 0.737** –0.394*
Foramen magnum index 0.393* –0.442**

NS
: Not significant, *: P < 0.05, **: P < 0.01.

archaeozoologists. The documentation of craniometric this study. These two species have made great contributions
measurements concentrating on the origins of cattle has to humanity due to their economic value as suppliers of
also been of great importance in terms of ontogenetic meat, milk, leather, and fertilizer, as well as their supply of
studies [1]. However, there has been greater emphasis sheer physical labor [30] and an animal-based economy.
on craniological evaluations of domesticated bovid As a member of the tribe Bovini, the water buffalo
species [1,6,9,14–19,24] than on nondomesticated ones originated from the Indian river buffalo. It is a more
[8,21]. Whether they were carried out on domesticated resistant and adaptive species than cattle, in addition to
or nondomesticated species, it is indisputable that both being able to better benefit from pasture and forest pasture
interspecies and intraspecies studies have provided habitats [13]. Craniometric data have been revealed from
great contributions to the research on the origin and intraspecies studies on domestic cattle [1,6,7,9,14,15,31].
domestication of bovid species. The aspiration to classify However, although it has selective advantages, the skull
cattle skulls from archaeological assemblages was also the morphometry of the water buffalo has not thus far been
basis of this research [2]. Unlike the macroanatomy of the extended beyond macroanatomic evaluations [28,29].
skulls [28,29], the morphometric analysis of the skulls of It is also possible to access the craniometric data of the
two bovid species, i.e. cattle and buffalo, was carried out in swamp buffalo (B. bubalis carabenesis) [20], which is

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morphologically and genetically a different subspecies of The visible morphology, as well as the length of the
the tribe Bovini [25]. However, because of the uncertainty horns, was different in both species. The statistical analyses
of the measurement points, it is not possible to use these in this study indicated changes in the viscerocranial part
data for a comparison with other Bovini species. of the skull, although it was thought that this difference
On the other hand, the length and shape of cattle horns commonly had an effect on the neurocranium due to
vary strongly [6], and their anatomical differences are also the frontal region of the skull. In particular, the width
obvious [28]. Therefore, examining and evaluating the measurements in the facial area showed a smaller value
horns was excluded in this study. The skull measurements when compared to both the skull and the VCL in the buffalo
in this study were evaluated within 3 distinct groups: samples. This also indicated that the buffalo skulls had a
general, viscerocranial, and neurocranial. Generally, two narrower structural feature with a longer viscerocranium.
indices (facial and frontal) are emphasized to predict Although it was argued that they had a longer skull shape
changes in skull ratios during the postnatal ontogenesis structure [20], the uncertainty of the reference points in
of cattle [24]. However, for a wider evaluation of the swamp buffalo created a limitation for their comparison
with the water buffalo, a different genotype [25] used in
comparison between the cattle and buffalo skulls, 9 index
this study.
calculations were produced. It has been argued that the
It was reported that the ox has a slightly dorsoventrally
GBS, MFL, and VCL ratios could be used as a common
flattened orbit, in which its transversal diameter is slightly
denominator of significant changes while predicting
larger than its height; however, the water buffalo was
changes in the skull ratios [24]. However, considering the
reported to usually have a circular foramen magnum
indices calculated in this study, it seems that this has no [29]. In this study, on the other hand, the transversal
significant contribution in the comparison of these two measurement of the orbit, which was the GILO, presented
species, because when the index values (e.g., skull, facial almost the same length in the two species, with a statistically
2, frontal indices) used in the GBS measurement of this insignificant difference between them. The basic difference
calculation are compared, the differences between them in the orbital measurements was only in the height. While
are not statistically significant (Table 4). the orbit had a greater height than its transverse length in
Although the GBS value had a positive correlation cattle skulls, a statistical difference was seen in the same
when compared with the TL, in the general skull rating measurements obtained from buffalo skulls. Contrary to
there was a low level and statistically insignificant the argument that the orbit was dorsoventrally flattened
relationship between them. Overall, the TL and GBS in cattle skulls [29], it was dorsoventrally elongated in this
linear measurements were larger in the cattle than in the study. In contrast, the orbit of the buffalo skulls was slightly
buffalo. This probably occurred because of the effect of dorsoventrally flattened when compared to the transversal
sex. However, the data obtained in this study were not length. This was also reflected in the index value. A
sufficient to reach a conclusion regarding this. The facial similar situation was also valid for the measurements of
index 1 presented the size of the changes in the facial area, the foramen magnum, since the height measurement was
although the proportional values of VCL and MFL were more determinative in its index value.
not significant in the comparison of the two species. There In conclusion, it can be argued that there are statistically
was a high positive correlation between the FB and facial significant differences between the linear measurements
index 1. This index value was lower in the buffalo and the of the skulls in both species. However, when the index
difference between the average values in the cattle was calculation was obtained by their ratios, the values of
significant (P < 0.01). This also showed that, compared to the measurements of the facial area were determinative
the skull length, the facial area was narrower in buffalo. in the craniology. For the orbit and foramen magnum
On the other hand, the GBS value was only effective on measurements, on the other hand, the measurement
the basal index calculation. This was probably related to of the altitude was seen as more determinative than the
the longitudinal curve of the skull. transversal measurement in their index and form.

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