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Changes in skull components of the squirrel monkey evoked by growth and nutrition An experimental study.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 81:535-543 11990)
Changes in Skull Components of the Squirrel Monkey Evoked by
Growth and Nutrition: An Experimental Study
&TOR M. PUCCIARELLI, VICENTE DRESSINO,
NIVEIRO
AND
MARIO H.
Laboratorio de Investigaciones Morfologicas, Catedra Illa de Anatomia.
Facultad de Ciencias Medicas, Universidad Nacional de La Plata,
La Plata, Buenos Aires, Argentina
KEY WORDS
Size and shape, Functional craniology, Cranial
growth, Malnutrition
ABSTRACT
Twenty weanling 6-month-old male squirrel monkeys were
allotted to the following treatments: 1) first control animals were killed at
weaning; 2) second control animals were killed when 24 months old; and 3)
malnourished animals were fed on a low-protein diet and killed at age 24
months. Lateral and vertical teleradiographies were taken. Growth of the
neurocranial and splanchnocranial components were measured by volumetric
(size estimators) and morphometric (shape estimators) indices. All facial
components grew. The neurocranial components showed a heterogeneous
behavior: The anteroneural component remained stable, and the increase of
the midneural component was compensated by a decrease in the posteroneural
component. Malnutrition affected the growths of 1)the craniofacial complex,
2) the splanchnocranium, and 3) the respiratory and midneural components.
Growth influenced skull shape through 1)increases of the splanchnocranium
and the midneural component relative to the neurocranium; 2) decreases ofthe
masticatory and optic components relative to the splanchnocranium, and 3)
decreases of the anteroneural and posteroneural components relative to the
neurocranium. Malnutrition influenced skull shape through the relationship
between the anteroneural component and the neurocranium. These results
confirmed the existence of functional interrelationships among the cranial
components. A new approach to craniological studies is suggested.
Present-day craniology may be thought of
as composed of a descriptive field wherein
human taxonomy is focused mainly on the
variation of the skull as a whole and an
analytical field that centers on ways that
variation take place. Actually, these fields
are complementary, and they might be considered as a unique descriptive-explicative
corpus of the “craniofacial unknown.” Cranial variation can be explained on the basis
of two fundamental concepts, one of which is
the theory of functional craniology (Klaauw,
1948-1952; Moss and Young, 1960); the
other evolved from experimentation in biological anthropology (Washburn and Detwiler, 1943; Moss, 1961; Pucciarelli, 1974).
From the point of view of functional craniology, the skull is viewed as a complex of
relatively but increasingly structured os@
1990 WILEY-IJSS, INC
seous components: individual bones can belong to different components and, conversely, different bones can make up a
particular component. The classical bone
unit was replaced by the concept of skeletal
unit (SKU), which is the “hard evidence” of
the variation of the functional matrix (FM);
together they make up a functional cranial
component (FCC) (Moss, 1973).
For the anthropobiologist, discretization
of crania in SKUs gives insight into the
evolution of the related soft tissues, even if
they are not actually present. Measurement
of each SKU permits the analytical description of the behavior of the craniofacial complex. According t o the experimental concept,
Received August 10,1988;accepted February 28,1989
536
H.M. PUCCIARELLI ET AL.
the dynamics of cranial variation is the result of the reciprocal interaction between
environmental factors and feedback responses of the FCC. The whole interaction,
when partitioned into single cause-effect relationships, can be disclosed by means of
“diachronical” studies of variables under
conditions of environmental uniformity
(Pucciarelli, 1974). This is the basis of the
so-called individualized study of variation.
According to Sirianni (19851, it is necessary to maximize the usefulness of animal
models in evaluating similarities to and differences from the human primate. The interpretation of experimental studies is constrained by the large taxonomic distance
between the experimental subject and the
object of study, which is always man for the
anthropobiologist. The shorter the taxonomic distance, the greater the power of the
experimental procedure; hence the most
meaningful inferences are drawn from studies of taxonomic levels common to both the
object and the subject. This is one of the
reasons why Saimiri was chosen for the
present research; the other was the architectural similarity with the genus Homo
(Ameghino,1909).
There are studies covering the cranial
anatomy and the craniology of the squirrel
monkey (reviewed by Osman Hill, 1960;
Thorn, 1965; Kaack et al., 1979; Oxnard,
1983; Thorington, 1985; Ayres, 1985). A
functional interpretation of cranial variation
is lacking. The object of the present work is 1)
to study the postweaning craniofacial
growth patterns of the male squirrel monkey
on the basis of its SKUs; 2) to measure the
effect of a low-protein diet on 1)and 3) to
assess the analytical value of volumetric and
morphometric indices for each SKU.
MATERIALS AND METHODS
Twenty weanling male Saimiri sciureus
(Cebidae) born in captivity were allotted to
three groups: 1)first control (Cl), in which
five animals were killed a t weaning (6
months old), 2) second control ((321, in which
six animals were fed ad libitum on a control
diet (Table 1J from weaning to 24 months of
age and then killed; and 3) malnourished
(Ml), in which nine animals were fed ad
libitum on a low-protein diet (Table 1)and
treated as in (2).
The skulls were cleaned and the following
points marked with 0.3-mm diameter copper
filaments: nasion, bregma, sphenoccipital,
sphenoethmoidal, maxilopalatal, maxilopremaxillary, and sphenofrontal. The skulls
were oriented with a craniostat, and lateral
and superior teleradiographies were taken
from 1.2 m above the skull. The length (L),
width (W), and height (H) of each of the
following components were measured on the
radiographies (Fig. 1): craniofacial (CF)
complex: 1) CFL rhinion-lambda length, 2)
CFW eurion-eurion width, 3) CFH gnationbregma height; splanchnocranium (F)4) FL
gonion-rhinion length, 5) FW width of the
postorbital constriction, 6) FH height from
gnation to orbitofrontal angle; neurocranium (N): 7) NL nasion-lambda length, 8)
NW neurocranial width, passing through basion, 9j NH basion-bregma height; facial
components: masticatory (MI: 10)ML length
from gnation to incisive point, 11)MW gonion-gonion width, 12)MH height from gnation to nasal-alveolar point; respiratory (R):
TABLE I . Percent comDosition of control and low-urotein diets
Control diet
Component
Soybean meal
Wheat meal
Rice meal
Wheat bran
Corn starch
Sugar
Skimmed milk
Egg
Margarine
Vitamin mixture
Salt mixture
Water
Total
Low-protein diet
Amount ( g )
Protein
content
Amount (9)
Protein
con tent
28.0
14.7
3.3
5.6
3.0
3.5
10.6
7.0
4.2
1.4
1.4
17.3
100.0
13.0
1.8
0.3
1.0
0.0
0.0
3.7
0.2
0.0
0.0
0.0
0.0
20.0
1.5
14.7
8.2
5.6
30.0
3.5
2.1
1.3
7.9
1.4
1.4
22.4
100.0
0.6
1.8
0.8
1.0
0.0
0.0
0.7
0.1
0.0
0.0
0.0
0.0
5.0
SKULL CHANGES IN THE SQUIRREL MONKEY
537
A
C
B
Fig. 1. Photoradiographs of a skull of a male juvenile
squirrel monkey. A Lateral view. 1,craniofacial length;
3, craniofacial height; 4, facial length; 6, facial height; 7,
neural length; 9, neural height; 10, masticatory length;
12, masticatory height. B: Lateral view. 13, respiratory
length, 15, respiratory height; 18,optic height, 19,anter-
oneural length; 21, anteroneural height; 22, midneural
length; 24, midneural height; 25, posteroneural length;
27, posteroneural height. C: Vertical view. 2, craniofacial; 5, facial; 8, neural; 11, masticatory; 14, respiratory
widths; 16, optic length; 17, optic; 20, anteroneural; 23,
midneural; 26, posteroneural widths.
13) RL length from nasal-alveolar point to
the posterior nasal spine, 14) RW width between both palatal diastema, 15) RH height
from nasion to maxilopalatal suture; optic
(0):16) OL length from optic foramen to
biectoconchial width, 17) OW biectoconchial
width, 18) OH height from the orbitofrontal
angle to the orbitobasal angle; neurocranial
components: anterior (NA): 19) ANL length
from nasion to optic foramen to frontal inflexion height, 20) ANW neurocranial width
passing through the optic foramen, 21) ANH
height from optic foramen to the frontal
inflexion; mid (MN), 22) MNL length from
optic foramen to frontal inflexion to vermion-bregma line, 23) MNW neurocranial
width passing through the posterior borders
of the occipital condyles, 24) MNH sphenoccipital-bregma height; posterior (PN), 25)
PNL length from vermion-bregma line to
lambda, 26) PNW neurocranial width, passing through vermion, 27) PNH height from
vermion to parietal inflexion.
Volumetric and morphometric indices
were derived from the measurements (Table
2). The volumetric indices estimate size
538
H.M. PUCCIARELLI ET AL.
TABLE 2. Volumetric and morphometric indices derived f r o m the measurements
Index name
Index formula
Volumetric indices
craniofacial
facial
neurocranial
masticatory
respiratory
optic
anterior neural
middle neural
posterior neural
Morphometric indices
neurofacial
mastifacial
rcspifacial
optifacial
anteroneural
midneural
nosteroneural
CFI: (CFL X CFW X CFH)/10,000
FI: (FL X FW X FH)/1,000
NI: (NL X NW X NH)/1,000
MI: (ML X MW X MH)/1,000
RI: (RL X RW X HH)/100
0 1 : (OT, X OW X OH)/100
NAI.(ANLx ANW x A N H ) / ~ , O O O
NMI: (MNL X MNW X MNH)/1,000
NPI: (PNL X PNW X PNH)/1,000
NFI: (FI/NI) X 100
MFI:(MI/FI) X 100
RFI: (RI/FI) X 100
OFI: (OUFI) X 10
ANI: (NAIINI) X 100
MNI: (NMIINI) X 100
PNI: (NPI/NI) X 100
20
10
5
0
CFI
Fl
NI
MI
Fig. 2. Relative differences in means (RELDIF) for
volumetric indices between first and second controls
(first bar) and between second controls and malnourished animals (second bar). Black, P < 0.001; squared, P
< 0.01; hatched, P < 0.05; white, nonsignificant differ-
RI
Of
NAI
NMI
N PI
ence. CFI, craniofacial; FI, facial; NI, neurocranial; MI,
masticatory; RI, respiratory; 01, optic; NAI, anterior
neural; NMI, middle neural;_NPI,qosteriorneural, indices. RELDIF: lOO(X, - X,)/(X, + X2].
539
SKULL CHANGES IN THE SQUIRREL MONKEY
changes and are expressed in arbitrary
units; morphometric indices estimate shape
changes by the relative growth between components. The degrees of radiographic magnification (MgI) and distortion (DsI) also were
calculated:
MgI = 50 (C x D) - {A x B)/(C X D); DsI =
lOOV:(A/B) - (CAI))'. where A = CRL measured 'on the skull, B' = CRH measured on
the skull, C = CRL measured on Rx, and D =
CRH measured on Rx.
Because of the small sample size, size and
shape changes could not be discriminated by
multivariate analysis. Data were subjected
to analysis of variance (ANOVA), and means
were compared by Tukey tests when ANOVA
F values were significant ( P < 0.051.
~
RESULTS
Radiographic magnification and distortion values were, respectively, 4.5% and
0.9% for the first control; 4.7%and 1.3%for
the second control; and 4.9%and 0.9%for the
malnourished groups. Those indices were
nonsignificant (F: 0.49 and 0.56, respectively).
Volumetric indices
Relative differences among treatments
are shown in Figure 2. Between C1 and C 2 ,
there were highly significant differences in
the facial, masticatory, respiratory, optic,
and middle neural indices; there was a significant difference in the craniofacial index
20
.5
.o
1.
10
15
NFI
MFI
RFI
Fig. 3. Relative differences between means
(RELDIF) for the morphometric indices, between first
and second controls (first bar) and between second controls and malnourished (second bar). Black, P < 0.001;
squared, P < 0.01; hatched, P < 0.05; white, nonsignifi-
OF1
AN1
MNI
PN I
cant difference. NFI, neurofacial; MFI, mastifacial; RFI,
respifacial; OFI, optifacial; ANI, anteroneural; MNI,
midnegralLPN1, posteroneural, indices. RELDIF: 100
(XI - X&X, + X2).
540
H.M. PUCCIARELLI ET AL.
and nonsignificant differences in the neurocranial and anterior neural indices. The posterior neural index decreased significantly.
The sizes of the facial and middle neural
indices in C2 were greater (P < 0.01) than in
M1. Differences were not so marked (P <
0.05) in the craniofacial, neurocranial, and
respiratory indices. Masticatory, optic, and
anterior neural and posterior neural indices
did not differ.
T A B L E 3. Mean ( X ) and standard devsation (SO)
for the indices and measurements
Index/
measurement
Volumetric
Craniofacial
Facial
Neurocranial
Masticatory
Respiratory
Optic
Anterior neural
Middle neural
Posterior neural
Morphometric
Neurofacial
Mastifacial
Respifacial
Optifacial
Anteroneural
Midneural
Posteroneural
Lengths
Craniofacial
Facial
Neurocranial
Masticatory
Respiratory
Optic
Anteroneural
Midneural
Posteroneural
Widths
Craniofacial
Facial
Neurocranial
Masticatory
Respiratory
Optic
Anteroneural
Midneural
Posteroneural
Heights
Craniofacial
Facial
Neurocranial
Masticatory
Respiratory
Optic
Anteroneural
Midneural
Posteroneural
First
control
_
_
- _
X
SL)
Second
control
___
X
SD
Malnourished
-~
~
X
SD
2.0
14.2
47.6
67.8
15.3
31.5
56.8
12.1
32.9
9.5
0.9
2.5
5.5
1.0
3.0
4.5
1.4
2.5
1.5
12.9
40.5
59.8
14.1
26.8
52.4
12.5
26.8
8.7
0.9
3.0
5.6
1.2
3.0
4.9
1.0
1.7
2.4
51.2
36.1
65.8
13.9
20.4
41.7
18.4
7.6
2.8
9.1
1.4
1.7
1.9
3.1
70.5
32.2
66.3
12.0
17.8
48.7
14.0
5.5
2.2
7.3
1.0
0.8
4.2
1.9
68.2
34.8
66.0
12.9
21.0
45.1
14.3
6.3
2.4
4.0
0.6
1.4
2.3
2.8
59.8
31.2
51 8
27.9
14.4
13.0
13.0
23.1
15.2
1.4
0.8
1.2
0.8
1.0
0.3
1.1
0.7
1.1
61.6
34.8
53.4
32.4
17.0
13.7
11.8
27.3
13.6
2.9
0.8
1.4
1.2
0.3
1.2
1.0
0.7
1.4
61.4
33.2
51.1
31.6
16.5
13.5
13.1
24.7
13.7
2.3
1.2
1.8
1.1
1.0
1.1
0.9
1.2
1.6
38.5
31.3
36.6
24.4
8.8
27.4
34.8
36.0
33.0
1.4
2.1
0.9
0.8
0.7
0.8
1.4
1.3
2.0
38.7
38.0
37.5
26.3
9.8
31.2
34.7
37.3
33.1
1.0
1.1
1.2
0.5
0.5
0.7
1.8
1.3
2.7
37.0
35.2
35.7
25.3
9.7
28.8
33.1
35.1
30.9
0.9
1.1
0.8
1.3
0.3
0.9
1.2
0.8
2.4
54.6
32.2
32.6
16.6
16.3
12.2
27.9
31.0
22.5
1.1
1.8
1.2
1.0
1.4
0.7
0.7
0.7
1.2
59.4
36.0
33.8
18.0
18.9
13.3
29.5
32.3
21.0
1.7
0.7
1.1
0.6
0.9
0.4
0.5
1.1
0.9
57.0
34.7
32.7
17.6
16.8
13.5
28.7
30.9
20.0
1.5
1.0
15
0.8
0.8
0.7
0.6
1.4
2.1
12.6
31.6
621
11.3
20.7
43.4
12.6
25.8
11.4
0.8
4.4
5.0
1.0
2.8
3.3
1.7
1.5
Morphometric indices
Between-group relative differences are
shown in Figure 3. Between C1 and C2, there
were highly significant differences in the
neurofacial and midneural indices; significant differences in the mastifacial, optifacial, anteroneural and posteroneural indices; and nonsignificant difference in the
respifacial index.
Between M1 and C2, the anteroneural
index was the only one that differed significantly between those groups. The rest of the
comparisons were nonsignificant.
Measurements
Mean values and standard deviations are
shown in Table 3 and multiple comparisons
among means in Table 4. In C2 the facial,
masticatory, respiratory, and midneural
widths and lengths, as well as the craniofacial, facial, respiratory, and anteroneural
heights were significantly greater than in
C1. Also, the masticatory and optic heights
in C2 were significantly greater than those
in C l .
Between C2 and M1, the midneural length
and the facial, neurocranial, and midneural
widths, and respiratory height were highly
T A B L E 4. Mvasuremrnts uihrclz presented significant
differences between groups
Tukey tests
Measurements
Lengths
Facial
Neurocranial
Masticatory
Respiratory
Midneural
Widths
Craniofacial
Facial
Neurocranial
Masticatory
Respiratory
Midneural
Heights
Craniofacial
Facial
Masticatory
Respiratory
Optic
Anteroneural
*P<OO6
**P< 0 01
***P< o.om
Control (1)control (2)
8.8***
Control (2)rnalnourishcd
n.s.
10.3***
7.0***
10.8***
4.1*
3.8'
ns.
ns.
7.1***
ns.
11.1***
ns.
4.7**
4.8**
10.8***
4.1*
5.0**
5.0**
n.s.
n.s.
7.1***
7.8***
7.4***
4.4*
6.0**
4.2*
6.5***
4.2*
n.s.
ns.
52**
n.s.
n.s.
SKULL CHANGES IN THE SQUIRREL MONKEY
greater in the former group. The facial and
neurocranial lengths and the craniofacial
width and height were significantly greater
in C2 than in M1.
DISCUSSION
The craniofacial complex showed a growth
intermediate between the splanchnocranium, which grew actively, and the neurocranium, which remained stable. The
marked facial increase reproduced the general trend observed in primate growth between late suckling and early postweaning
periods (Schultz, 1962).In the rat the masticatory component is also the most active for
the facial growth (Pucciarelli, 1981).
Similar growth patterns have been described in several primate genera (Schultz,
19621, particularly in Macaca mulatta (Enlow, 1966; Duterloo and Enlow, 1970; Elgoyhenet al., 1972;Michejdaet al., 19791,M.
nemestrina (Orloski, 1982; Sirianni et al.,
19821, and M . fascicularis (Nanda et al.,
1987). These results are relevant for the
present study because the similar cranial
proportions observed in both the cercopithecid and platirhine monkeys (Petit-Maire,
1971) lead to a morphological convergence
between both taxonomic groups (Biegert,
1963).
The facial components differed only in
terms of quantitative growth (Fig. 2). Therefore, the splanchnocranium can be considered a “continuum complex of growth.” Differences found for facial growth in M .
mulatta (Enlow, 1966) can be explained on
this experimental basis. The foregoing masticatory-respiratory behavior means (Du
Brul and Laskin, 1961) a limitation to the
principle of functional ‘independence among
cranial components. That restriction accrues
from the topographic neighbourhood between the masticatory and respiratory components. The masticatory component can influence growth of the respiratory component
(and vice versa) through the maxilopalatal
bony plate, the lower table of which is the
roof of the oral cavity, and its upper table is
the floor of the nasal cavity.
Both anteroposterior and transverse
growths are necessarily constrained by the
relative plasticity of the maxilopalatal
diploe. Part of the growth of each SKU can be
explained by a kind of “carryover”effect, i.e.,
a residual mechanical strain resulting from
the linkage between those components. This
process, which is different from allometric
541
growth, gives experimental support to the
well-known principle of functional interdependence among cranial components
(Klaauw, 1948-1952).
The braincase is usually considered as a
continuum. Because the midneural component grew significantly, the neural cavity
must be viewed as a nonhomogeneous complex made up of minor homogeneous functional components. Such neurocranial behavior of the Saimiri coincides with that of
the growing rat during ortocranialization
(Pucciarelli, 1978).The apparent stability of
the cerebral capsule was due to the compensatory decrease of the posteroneural component (Fig. 2). Moss (1960) regarded the neural mass, together with the basis, the vault,
and the organized fiber tracts of the dura
mater as integral parts of a biomechanical
entity. According to Popa (Moss and Young,
1960), five dorsobasilar junction regions
may be identified in the cerebral capsule of
humans by the insertion systems of oriented
fibers. Two are connected rostrally with the
sphenoid lesser wings and caudally with the
petrous crests of the temporals. Such insertion regions bound the midneural component, as described in the present work, and
consequently gave its particular growth behavior.
Nutrition affected the size and shape of
the growing primate skull, as was shown by
De Rousseau and Reichs (19871, who reported cranial and postcranial increments
because of improved alimentation of Macaca
from Cay0 Santiago. The malnourished animals (Fig. 2) showed an intermediate craniofacial decrease with regard to both major
components. Discretization made on each
major component revealed other effects of
malnutrition. The most active facial component-respiratory-was
affected to a lesser
extent than the midneural component (Fig.
2). This agrees with the decreased growth of
the endochondral tissue found for malnourished rhesus monkeys (Jha et al., 1968).
The concept of shape used in this paper
differs from that of classic craniology. Morphometric indices estimate relative tridimensional changes of growth between a particular SKU and its “logical continent” (e.g.,
the optifacial index) or between two components of the same functional hierarchy (e.g.,
the neurofacial index). Values of those indices cannot be assimilated to a particular
geometric shape, as is the case of the classical bidimensional indices (cepahlic, orbitary,
542
H.M. PUCCIARELLI ET AL.
etc.), because they reflect relative growth
differences instead of changes in superficial
areas.
Growth affected skull shape because of
two opposite trends: 1)the relative increase
of both the splanchnocranium and the midneural component relative to the neurocranium; and 2) the relative decrease of the
masticatory and optic components relative to
the splanchnocranium, as well as that of the
anteroneural and posteroneural components
relative to the neurocranium. The growth of
the respiratory component did not affect facial shape, because both grew to the same
degree (Fig. 3).
Nutrition affected the anteroneural component (Fig. 3). It did not grow (Fig. 21, but its
relative decrease in malnourished animals
counteracted the observed midneural expansion (Fig. 3).
Two fundamental facts may be highlighted: 1) All the facial components showed
a fairly homogeneous growth, and only one of
them reacted to malnutrition. At the same
time, all belonged to a higher component
(splanchnocranium), which is known to be
highly variable; and 2) the neural components showed a heterogeneous growth and
enhanced response to nutrition in at least
one. At the same time, they belonged to a
major component (neurocranium), which is
known to be highly stable.
These two facts have a special meaning for
anthropology: the worth of metric data depends closely on the choice of the measurements. In agreement with Andrews and
Williams (19731, it is preferable to group
craniofacial measurements in functionally
meaningful ways than to use too many functionally unrelated variables. In other words,
the higher the discretization of the SKUs,
the greater will be the approximation to real
continua. According to Moss (19731, neither
the shape nor the position of a particular
SKU reflects a genic activity, but they indirectly manifest a genic control of the functional matrices. The lack of a biological basis
for indiscriminated measurements (macromeasurements) may be the main reason
for the failure in correlating metric traits
with genic controlled features, e.g., some
discontinuous cranial traits.
CONCLUSIONS
Craniofacial behavior changes according
to the level of functional discretization of its
components. This fact gives enough experi-
mental evidence to justify use of truly functional criteria for developing a craniometry
on a sound biological basis. Macromeasurements encompass large components that distort the interpretation of data because of the
addition of multifactorial variations: nongenetic variation is largely added to genetical
variation. Conversely, the measurement of
functional components as small as possible
(highly discretized components) would provide some kind of genetic validity to craniological procedures.
ACKNOWLEDGMENTS
The authors are grateful to Ing. Agr.
Hector D. Ginzo (Centro de Ecofisiologia
Vegetal), Mrs. Maria C. Mune (Laboratorio
de Investigaciones Morfologicas), and to the
Centro Argentino de Primates (CAPRIM),
for their highly valuable assistance. This
study was supported by a grant from the
Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET).
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