Post-natal Development in the Linear and Tric Morphometrics of the ...

Anat.Histol.Embryol.31, 232–236 (2002)
Ó 2002 Blackwell Verlag, Berlin
ISSN 0340–2096
Department of Medical Microbiology, Faculty of Science, King Saud University, Bureidah, AlQassim, Kingdom
of Saudi Arabia
Post-natal Development in the Linear and Tric Morphometrics of the Camelidae
Skull
O. Al-Sagair 1 * and S.A.ElMougy 2
1 2
Addresses of authors: Department of Medical Microbiology, Faculty of Science, and Department of Veterinary Medicine,
Faculty of Agriculture and Veterinary Medicine, King Saud University, Bureidah, AlQassim, Kingdom of Saudi Arabia;
*Corresponding author: e-mail: salehsce@hotmail.com
With 3 figures and 4 tables Received November, 2001; accepted for publication January, 2002
Summary
The craniometric measurements in addition to the skull, cranial
and facial indices undertaken in the immature and mature male
Camelus dromedarius of the Malha phenotype (black) were: the
skull length (35.99 cm), maximum width of neurocranium
(11.33 cm), cranial length (15.45 cm), maximum zygomatic
width (14.81 cm), viscerocranial length (20.55 cm), skull index
(41.13), cranial index (73.70), facial index (72.31), cranial volume
(231.73 ml) and skull weight (795.70 g) were measured in
the immature camels.In the mature camels, the skulls gave the
following measurements: the skull length (50.53 cm), maximum
width of neurocranium (15.96 cm), cranial length (21.93 cm),
maximum zygomatic width (22.75 cm), viscerocranial length
(28.60 cm), skull index (45.06), cranial index (72.99), facial
index (79.83), cranial volume (310.80 ml) and skull weight
(2598.31 g). The results of a total of 30 skulls of immature and
mature Malha camel revealed that all the measurements
increased with age whereas the cranial index was the only
parameter for which a decreased value was recorded.The
anterior basicranial angle averaged about 203 in the immature
animal to increase to an insignificant value of 204 in the mature
camel skull.Similarly, the posterior basicranial angle did not
exhibit a significant difference between the immature and
mature values, which ranged between 110 and 112 , respectively.
Introduction
Detailed information about the growth of the skull is available
for only a small proportion of the many thousands of known
mammalian species (Huang, 1987; Aiumlamai et al., 1992;
Sivachelvan et al., 1996; Bulnes et al., 1998). Therefore, this
investigation was carried out to reveal and evaluate the pattern
of the skull growth during post-natal life in one of the camel
phenotypes prevailing in the AlQassim area in Saudi Arabia, the
Malha.Parallel with growth, the farther the values are from the
mean value, the higher the risk of coming across skull defects in
the growing animal.A correlation exists between the shape of
the skull and an increase in the risk of nasal cancer (Wilson and
Olson, 1985; Reif et al., 1998). Thus, the obtained data may be
of veterinary clinical use in investigating the correlation between
several skull defects and/or diseases and the shape of the skull.
This endeavour was aimed at measuring the changes in the
craniometric dimensions in the skull of the one-humped camel
(Camelus dromedarius) during the immature and the mature
stages.
Materials and Methods
A total of 30 skulls of male Malha camel, which were divided
into two groups, were used in the present investigation.Group
1 comprised 15 camel skulls between the age of 2 and 3 years
(immature) and group 2 comprised 15 camel skulls between the
age of 6 and 7 years (mature).The skulls were macerated
according to the procedure of Simoens et al.(1994) and Onar
et al.(1997).The positions of certain points and markers on
the skull were determined in making linear measurements with
a Vernier calliper.The craniometric measurements for 10
different regions of the skull were made using the methods
outlined by Zietzschmann (1943), Sisson (1975), Driesch
(1976), The and Trouth (1976), Nickel et al.(1977), Brehm
et al.(1985), Regedon et al.(1991), Evans and Christensen
(1993), Yildiz et al.(1993), Simoens et al.(1994), Onar et al.
(1997) and Onar (1999).
The skull, cranial and facial indices were calculated as
described by Brehm et al.(1985), Evans and Christensen
(1993), Yildiz et al.(1993) and Simoens et al.(1994).Also, the
cranial volume of each skull was calculated using the methods
of Sandhu and Dhingra (1986), Saber (1989) and Onar (1999).
Duncan’s (1955) test was used to analyse the data derived from
the two groups and the method of Snedecor and Cochran
(1980) was used for the correlation test of the morphometric
values using the general linear models (GLM) procedures of
the Statistical Analyses System (SAS, 1996).
Definitions of the measuring points on the cranium (Figs 1and 2)
Inion (I): central surface point on the external occipital
protuberance.Nasion (N): junction on the median plane of
the right and left nasofrontal sutures.Prosthion (P): anterior
end of the inter-incisive suture, located between the roots of
the upper central incisor teeth.Euryon (E): the most lateral
point of the brain case.Zygion (Z): the most lateral point of
the zygomatic arch.
Measurement of the cranium (Figs 1and 2)
The following measurements were made: skull length (inion–
prosthion), maximum zygomatic width (zygion–zygion),
cranial length (inion–nasion), maximum width of the neurocranium
(euryon–euryon), viscerocranial length (nasion–
prosthion), skull index (maximum zygomatic width 100/
skull length), cranial index (maximum width of neurocranium
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Post-natal Development of the Camelidae Skull 233
Fig.1. Measurments of the camel skull (dorsal view): inion (I), nasion
(N), prosthion (P), zygion (Z), skull length (1), cranial length (2)
viscerocranial length (3), maximum width of neurocranium (4) and
maximum zygomatic width (5).
100/cranial length), facial index (maximum zygomatic width
100/viscerocranial length), cranial volume and skull weight.
The measurement of the cranial volume was commenced by
plugging the foramina opening into the cranial cavity with
fresh Plasticine.The cavity was then filled with fine-quality rice
seeds to the level of the distal border of the foramen magnum.
When the cranial cavity was filled with rice seeds via the
foramen magnum, the space immediately cranial to the
tentorium cerebelli osseum was also filled.The contents were
emptied and measured in a measuring cylinder calibrated in
millilitres.
Linear and angular dimensions of the cranial base (Fig 3)
The cranial base, as traditionally defined in growth studies of
the mammalian skull, consists (in the median plane) of a
segment, termed the basicranial axis, stretching from the
pituitary region to the ventral (anterior) margin of the foramen
magnum, an anterior extension from the pituitary region to the
junction of the frontal and nasal bones, and a posterior
extension from the ventral to the dorsal margin of the foramen
magnum (Moore, 1981).
Fig.2. Measurments of the camel skull (lateral view): inion (I),
prosthion (p), nasion (N), skull length (1), viscerocranial length (2) and
cranial length (3).
Fig.3. Sagittal sections of the skull of camel to show linear and
angular dimensions of cranial base.E ¼ endobasion; N ¼ nasion; O ¼
opisthion; PP ¼ pituitarty point.The anterior and posterior basicranial
angles are shown by dashed lines.
Statistical analysis
Changes in the craniometric measurements within and between
age groups were statistically evaluated by the least-squares
analysis of variance using the GLM procedures of the
statistical analysis system (SAS, 1996).
Results
The craniometric measurements and the cranial volume
increased significantly with age.The results recorded in Table
1 reveal that the skull, cranial and viscerocranial lengths,
neurocranium and the maximum zygomatic widths, increased
significantly with age.Although the skull and facial indices
increased, the cranial index insignificantly decreased in value
with age.
The results of the correlation analyses of the features
examined in the immature and mature animals are recorded in
Table 2.
There was a strongly positive correlation among the skull,
viscerocranial lengths, cranial and the maximum zygomatic
width in the immature and mature animals.
The maximum width of the neurocranium showed a strong
significant positive correlation with all of the measurements in
both the immature and mature groups of camels.
The skull and facial indices in the immature and mature
camels were found to have a positive correlation with the
maximum zygomatic width and the skull, cranial and viscerocranial
lengths in the immature and mature animals.The
cranial index was found to have a negative correlation with all
of the craniometric measurements with the exception of the
viscerocranial length, which was insignificantly positive.
However, a similar comparison in the immature and mature
groups of camels showed that the cranial index had a weak
negative significant correlation with the cranial length.
A positive correlation between the facial index and the
maximum width of the neurocranium was found in the
immature and mature camels.
The correlation between the skull and facial indices in both
groups was positive and strong.The correlation between the
cranial and facial indices was weakly significant in the
immature and mature camels.

234 O. Al-Sagair and S. A. ElMougy
Table 2.Correlation analysis of the skull measurements of the immature and mature Malha (black) camels (Camelus dromedarius)
Skull
length
(cm)
Viscerocranial
length
(cm)
Cranial
length
(cm)
In both the immature and mature camels, the cranial volume
generally indicated a significant positive correlation with the
skull measurements, but there was a weak negative correlation
between the cranial volume and the skull, cranial and facial
indices.In neither of the camels, immature and mature, was
this significant.
The skull weight showed a negative correlation with the
cranial index only in the immature camel, whereas in the
mature camels the skull weight evidenced a positive correlation
with the skull and facial indices in addition to all of the other
craniometric measurements.
The results of the correlation analysis between the immature
camels, as recorded in Table 3, reveal a strongly positive
correlation between the craniometric measurements, with one
exception.The cranial index had an insignificant negative
correlation with all craniometric parameters except with the
facial index where it had a weak negative significant correlation
and an insignificant positive correlation with the viscerocranial
length.
The results of the correlation analysis between the mature
camels, as recorded in Table 4, reveal that the only strong
significant correlation values were between the viscerocranial
length and the skull length, viscerocranial length and the facial
Maximum width Maximum
of neurocranium zygomatic
(cm) width (cm)
Skull
weight
(g)
Skull
index
Cranial
index
Facial
index
Cranial
volume
(ml)
Skull length (cm) 0.965*** 0.946*** 0.967*** 0.963*** 0.952*** 0.549*** 0.181 0.448* 0.900***
Viscerocranial
length (cm)
0.965*** 0.828*** 0.906*** 0.912*** 0.893*** 0.484** 0.006 0.271 0.856***
Cranial length (cm) 0.946*** 0.828*** 0.948*** 0.926*** 0.932*** 0.577*** 0.395* 0.624*** 0.867***
Maximum width of
neurocranium (cm)
0.967*** 0.906*** 0.948*** 0.960*** 0.967*** 0.624*** 0.087 0.549** 0.912***
Maximum zygomatic
width (cm)
0.963*** 0.917*** 0.926*** 0.960*** 0.931*** 0.751*** 0.135 0.628*** 0.900***
Skull weight (g) 0.952*** 0.893*** 0.932*** 0.967*** 0.931*** 0.576*** 0.128 0.509** 0.905***
Skull index 0.549** 0.484* 0.577*** 0.624*** 0.751*** 0.576*** 0.003 0.880*** 0.594***
Cranial index 0.181 0.006 0.395* 0.087 0.135 0.128 0.003 0.358* 0.083
Facial index 0.448* 0.271 0.624*** 0.549** 0.628*** 0.509** 0.880*** 0.358* 0.503**
Cranial volume (ml) 0.900*** 0.856*** 0.867*** 0.912*** 0.900*** 0.905*** 0.594*** 0.083 0.503**
*P < 0:05.
**P < 0:01.
***P < 0:001.
Immature Mature
Mean SE Mean SE
Skull length (cm) 35.99 b 0.44 50.53 a 0.44
Maximum width of neurocranium(cm) 11.33 b 0.11 15.96 a 0.11
Cranial length (cm) 15.45 b 0.34 21.93 a 0.34
Maximum zygomatic width (cm) 14.81 b 0.24 22.75 a 0.24
Viscerocranial length (cm) 20.55 b 0.42 28.60 a 0.42
Skull index 41.13 b 0.61 45.06 a 0.61
Cranial index 73.70 a 1.17 72.99 a 1.17
Facial index 72.31 b 1.56 79.83 a 1.56
Cranial volume (ml) 231.73 b 4.22 310.80 a 4.22
Skull weight (g) 795.70 b 70.33 2598.31 a 70.33
SE standard error of mean.
P < 0:001 for all parameters.The difference between the mean values of measurements is statistically
significant.
a;b Means with the same letter are not significantly different.
Table 1.Skull measurements of the
immature (n ¼ 30) and mature
(n ¼ 30) Malha (black) camels
(Camelus dromedarius)
index, cranial length and cranial index and between the
maximum zygomatic width and skull index.
In the present investigation, the OE angle, of the camel
skull, did not exceed the level of 112 in the mature animal
whereas during the immature stage it was 110 , which did not
reveal a significant difference.In addition, the PP angle
remained at an angle of 204 and did not change with growth.
Discussion
Because of the absence of any available information on the
craniometric measurements of the adult camel, it was a must
to involve the immature animal in our measurements and
thereafter compare with measurements on the mature camels.
An increase in the skull, cranial and viscerocranial lengths,
the neurocranium and the maximum zygomatic widths, the
cranial volume and the skull weight, and a decrease in the
skull, cranial and facial indices was found when the immature
camels reached maturity.
In addition, when the maximum zygomatic width and the
maximum width of the neurocranium, were compared with the
skull, cranial and viscerocranial lengths, the latter had a higher
increment rate with age.This showed that the skull of the

Post-natal Development of the Camelidae Skull 235
Table 3.Correlation analysis of the skull measurements of the immature Malha (black) camels (Camelus dromedarius)
Skull
length
(cm)
Viscerocranial
length
(cm)
Cranial
length
(cm)
Maximum width
of neurocranium
(cm)
Artiodactyla (Camelidae) took on a slightly long-nosed shape
as the animals grew older, whereas in the maximum zygomatic
width and the maximum width of the neurocranium, smaller
changes occurred.The change in the maximum width of the
neurocranium was even smaller with age.This was supported
by the fact that there was a low correlation between the
maximum width of the neurocranium and the skull, cranial
and viscerocranial lengths.
Both the determination of a strongly positive correlation
between the skull, cranial and viscerocranial lengths and
indices, and a decrease in indices with growth of the immature
camels reflected the development of an Artiodactyla-shaped
head.
Camels are considered to belong to the mammalian Artiodactyla
order and in the Camelidae group.In the present
study, the length–width index was 0.67 and 0.44 in the
immature and mature camels, respectively.Also, the ratio of
the total skull length to the maximum length between the two
zygomatic arches was 2.43 in the immature camels and 2.22 in
the mature ones, which indicates that as the camels grew, the
Maximum
zygomatic
width (cm)
Skull
weight
(g)
Skull
index
Cranial
index
Facial
index
Cranial
volume
(ml)
Skull length (cm) 0.965*** 0.946*** 0.967*** 0.963*** 0.952*** 0.549** 0.181 0.448* 0.900***
Viscerocranial
length (cm)
0.965*** 0.828*** 0.906*** 0.917*** 0.893*** 0.484** 0.006 0.271 0.856***
Cranial length (cm) 0.946*** 0.828*** 0.948*** 0.926*** 0.932*** 0.577*** 0.395 0.624*** 0.867***
Maximum width of
neurocranium (cm)
0.967*** 0.906*** 0.948*** 0.960*** 0.967*** 0.624*** 0.087 0.549** 0.912***
Maximum zygomatic
width (cm)
0.963*** 0.917*** 0.926*** 0.960*** 0.931*** 0.751*** 0.135 0.628*** 0.900***
Skull weight (g) 0.952*** 0.893*** 0.932*** 0.967*** 0.931*** 0.576*** 0.128 0.509** 0.905***
Skull index 0.549** 0.484** 0.577*** 0.624*** 0.751*** 0.576*** 0.003 0.880*** 0.594***
Cranial index 0.181 0.006 0.395 0.087 0.135 0.128 0.003 0.358* 0.083
Facial index 0.448* 0.271 0.624*** 0.549** 0.628*** 0.509* 0.880*** 0.358* 0.503**
Cranial volume (ml) 0.900*** 0.856*** 0.867*** 0.912*** 0.900*** 0.905*** 0.594*** 0.083 0.503**
*P < 0:05.
**P < 0:01.
***P < 0:001.
Table 4.Correlation analysis of the skull measurements of the mature Malha (black) camels (Camelus dromedarius)
Skull
length
(cm)
Viscerocranial
length
(cm)
Cranial
length
(cm)
Maximum width
of neurocranium
(cm)
Maximum
zygomatic
width (cm)
Skull
weight
(g)
Skull
index
Cranial
index
Facial
index
Cranial
volume
(ml)
Skull length (cm) 0.692** 0.165 0.008 0.248 0.292 0.382 0.186 0.469 0.132
Viscerocranial length
(cm)
0.692** 0.598 0.347 0.212 0.033 0.225 0.470 0.758** 0.069
Cranial length (cm) 0.165 0.598 0.483 0.0152 0.369 0.117 0.849*** 0.516 0.052
Maximum width of
neurocranium (cm)
0.008 0.347 0.483 0.078 0.493 0.078 0.050 0.234 0.005
Maximum zygomatic
width (cm)
0.248 0.212 0.015 0.078 0.171 0.800*** 0.015 0.474 0.051
Skull weight (g) 0.292 0.033 0.369 0.493 0.171 0.348 0.130 0.110 0.336
Skull index 0.382 0.225 0.117 0.078 0.800*** 0.348 0.104 0.741 0.125
Cranial index 0.186 0.470 0.849*** 0.050 0.015 0.130 0.104 0.435 0.036
Facial index 0.469 0.758** 0.516 0.234 0.474 0.110 0.741 0.435 0.118
Cranial volume (ml) 0.132 0.069 0.052 0.005 0.051 0.336 0.125 0.036 0.118
**P < 0:01.
***P < 0:001.
ratio between skull length and maximum zygomatic width
decreased.
The cranial volume was found to increase in line with the
increments in other parameters reflected as a high correlation
in the immature and mature camels with a high correlation
with the indices.However, the relatively large changes with
age in these values compared to those taking place in the
skull, cranial and viscerocranial lengths showed that the
cranial cavity increased breadthwise, which meant that
the development of the skull was compatible with the
Artiodactyla type (Camelidae) and which is quite opposite to
what happens in the dolichocephalic-shaped head (Onar,
1999).In the dolichocephalic dogs, the skull takes on a longnosed
shape as the animals grow older, the cranial cavity
widened lengthwise with a strongly negative correlation
between the skull, cranial and viscerocranial lengths and
indices, and a decrease in indices with growth of the immature
dogs.
The growth changes in the linear dimensions of the
aforementioned segments of the cranial base and in the angles

236 O. Al-Sagair and S. A. ElMougy
between them record that the anterior basicranial angle
averaged about 203 in the immature animal increased
insignificantly to a value of 204 in the mature camel skull.
Similarly, the posterior basicranial angle did not exhibit a
significant difference between the immature and mature values,
which ranged between 110 and 112 , respectively.These linear
dimensions have been studied in several mammalian species.In
non-primates, the angle tends to increase during post-natal
growth to a value well in excess of 180 .In the rat, for
example, the anterior basicranial angle at maturity is of the
order of 240 (Moore, 1981).In the higher primates (Ceboidea,
Cercopithecoidea and the apes amongst the Hominoidea) the
anterior basicranial angle averages about 150 at the stage of
the milk dentition and, as in non-primates, continues to
increase throughout the growth period but to a much lesser
degree (Zuckerman, 1926; Ashton, 1957; Ashton et al., 1977).
Their result indicated that the anterior basicranial angle
remains below 180 throughout life.This difference is attributable
to the much enhanced growth of the primate brain
which is accommodated, anteriorly, by enlargement of the
braincase forwards above the facial skeleton.The primate
pattern, as well as the recorded results with the camel, can be
regarded as a tendency to retain the immature shape and
correlates with the observation, as already noted, that the
brain is large relative to the remainder of the head early in the
growth period.In prosimians, the degree of cranial flexion is
generally less than in anthropoid primates although the
anterior basicranial angle is still usually somewhat below
180 .It is of interest that in Daubentonia cranial flexion is
much greater than in other prosimians.Cartmill (1977) has
attributed this to the need to strengthen the skull, by
augmenting facial height, against the bending forces produced
during use of the incisor teeth (Daubentonia possesses rodentlike
incisors, which it uses in a powerful gnawing action).
The data obtained in this study using the correlations
amongst shape and dimension parameters for the brain and
the skull and the changes that occur with age may prove of
clinical usefulness to those clinically associated with the
camels.
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