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Dental development in the cotton ear marmoset (Callithrix jacchus).

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Dental Development in the Cotton Ear Marmoset
(Callithrix jacchus) '
GARY W. JOHNSTON, SAMUEL DREIZEN AND BARNET M. LEVY
University of Texas Dental Science Institute at Houston,
Houston, Texas 77025
The dental development of the cotton ear marmoset (Callithrix jacchus) was determined from gross and radiographic examinations of 40 colony born
specimens to provide a biological yardstick for estimating the age of wild caught young
animals. In this species 4 deciduous teeth (Idl) erupt during the first week;
4 (Ida) during the second week; 12 (Cd, Mdl, Mds) during the third week and 4
(Mdr) during the fourth week of age. Four permanent teeth ( M I ) are visible on oral
Mz, 11, 12,
examination at 3 to 4 months: 8 (MI, M2) at 4 to 6 months; 12 to 20 (MI,
Pm3) at 7 to 8 months; 24 to 28 (MI, Mz,11, IP, P m , Pmz, Pml) at 8 to 11
months and the full complement of 32 at 11 to 12 months of age. The stage of mixed
dentition extends from age 112 to 340 days. There is a close correspondence in the age
related eruption pattern in each quadrant with no significant difference between males
and females.
ABSTRACT
Marmosets are South American primates
of the suborder Anthropoidea, family Callithricidae, native to the Amazon basin and
Eastern Brazil. Small size (200 to 500 gm)
and comparatively low purchase, care and
housing costs have favored their use in
many areas of biomedical research. They
breed well in captivity following acclimatization, have a gestation period of approximately 140 days and usually give birth to
biovular twins. Weaning is complete by
three months of age and physical maturity
is attained in 12 to 18 months. Their estimated life span is 15 years.
In the wild, marmosets are highly arboreal, diurnal and omnivorous subsisting
on a diet of fruits, tender vegetation, seeds,
seed pods, insects, bird eggs and nestlings.
They live in family groups of three to seven
with the father and older offspring participating actively in the care of the young.
The husbandry requirements for the successful breeding and maintenance of marmosets in a laboratory environment have
been detailed by Levy and Artecona ('64)
and by Hampton, Hampton and Landwehr
('66).
Criteria for definitively identifying the
age of wild caught marmosets are lacking.
Immature animals are conventionally classified as infant, juvenile and subadult on
the basis of appearance, size and weight.
AM. J. PHYs. ANTHROP.,33: 41-48.
The purpose of this study was to develop a
method for more accurately ageing young
cotton ear marmosets (Callithrix jacchus)
by ( a ) delineating the pattern of dental
development from animals of known birth
date and by (b) collating the readily detectable dental maturity indicators with chronological age.
MATERIALS AND METHODS
Postmortem dental radiographs of 40
(21 male and 19 female) cotton ear marmosets were available for study. The age
at death ranged from 2 to 390 days. All
animals had been delivered at term by
mothers in the breeding colony of the University of Texas Dental Science Institute.
They had been born in hanging wire cages
in a room maintained at 80°F and a relative humidity of 6 0 % . The parents had received a diet containing adequate amounts
of all of the presently known nutritional
requirements of the species (Diet 82-7.
Theracon, Inc., Topeka, Kansas). Only animals which had been sacrificed or died
within 24 hours following an acute illness
or accident were included in the investigational series.
1 This study was supported by grants from the National Institute of Dental Research, National Institutes
of Health (DE-02232)and from the Medical Research
Foundation of Texas.'
41
42
G. W. JOHNSTON, S. DREIZEN AND B. M. LEVY
The radiographs were prepared from
heads removed at necropsy, fixed in 10%
neutral formalin and sawed midsagittally
following fixation. Grenz ray roentgenograms of each side were made on three and
one-quarter by four inches Kodak projector
slide plates of medium contrast emulsion.
The target film distance was 16 cm, exposure time five minutes, and the machine
settings 4 ma and 10 KV (Model VI. X-Ray
Mfg. Corp. of America, Great Neck, New
York). After processing, the radiographs
were examined at X 3 magnification with
a Bausch and Lomb Model BVB 73 stereomicroscope fitted with a fluorescent illuminator for the stage of crown and root formation and the eruption status of the deciduous and permanent teeth. Gingival eruption was distinguished from alveolar eruption by inspection of the gross specimens
using the stereomicroscope and a metallic
probe. A tooth was considered erupted
when part of the crown had pierced the
gingiva.
Crown formation was rated as cusp or
incisal tip present, cusp fully formed and
crown completed; root formation as initial,
partial or entire; eruption as impending,
partial or complete. Both gross and radiographic examinations were used to establish the sequence and time of eruption of
the deciduous and permanent dentition.
Ink line drawings and photographs of representative radiographs were made to depict the most noteworthy age related
sequential changes in the dental developmental pattern.
at the contact points, a feature repeated in
all deciduous molars and all permanent
teeth. Each of the upper deciduous molars
is morphologically distinct. Md, is shaped
like the canine, Md, like a two cusped premolar and Md, like a three cusped molar.
All buccal cusps are sharply exaggerated.
There is a progressive increase in crown circumference from Md, through Md,.
The lower deciduous teeth form a V
shaped arch. In each quadrant the six
crowns are paired into three distinct configurations. Idi and Id, are chisel shaped,
rectangular in labial view, narrow and of
approximately equal height and width. Cd
and Md, are cone shzped and Md, and Md,
are molariform with two large buccal and
two small lingual cusps. Md, is the largest
tooth in the lower deciduous arch. All deciduous anterior teeth have one root, upper
molars three roots and lower molars two
roots. There are no distinguishable sex differences in the deciduous dentition.
The permanent upper incisors have short
crowns and project slightly forward and
outward. I, is broader mesiodistally and
more spatulate than I,. The upper canines
are tusk-like and extend well below the occlusal plane of the other teeth. They are
separated from I, by a large diastema and
their size and height are much greater in
males than in females. The three upper premolars are unequal in size, widened buccolingually and bicuspid contoured with a
well formed buccal and diminutive lingual
cusp. The upper M, is a large tricuspid
tooth with two high buccal and a single low
lingual cusp. M, has a similar configuraOBSERVATIONS
tion but is smaller and rounder.
Thirteen of the specimens had a decidThe crowns of the permanent lower inuous, 23 a mixed and 3 a permanent den- cisors slant forward and are almost as long
tition. The deciduous dental formula was as the adjoining canines. They are narrow
I 2 / 2 , C 1/1, M 3/3; the permanent for- mesiodistally and broad labiolingually. The
mula I 2 / 2 , C 1/1, Pm 3/3, M 2/2. One incisal edge of I, is slightly convex. Each
animal also had a lower permanent third lower canine is fusiform in shape and has
molar.
a prominent cingulum on the lingual surAnatomically, the deciduous upper in- face. The lower Pml has a very high pointed
cisors are centrally placed in front of the buccal cusp and a rudimentary lingual
maxilla. Idl and Id, are spade shaped with equivalent resembling the adjacent canine
sloping concave lingual surfaces. Id, is in appearance. Pm2 and Pm, are obliquely
distinguished by a small midcrown tuber- oval with a prominent buccal and a miniacle on the distal surface. The upper decid- ture lingual cusp. Buccal cusp height diuous canines are conical and come to a minishes progressively from Pm, through
point at the occlusal line. Both proximal Pm,. The permanent lower molars are
surfaces are expanded into small tubercles quadrangular in outline and have two well
43
DENTAL DEVELOPMENT IN CALLITHRIX JACCHUS
formed buccal and two lesser lingual cusps
separated by a cruciate sulcus. As in the
upper arch M, is smaller and more rounded
than M,. All permanent anterior and premolar teeth have one root; lower molars
two roots and upper molars three roots.
For each of the parameters measured in
the deciduous and permanent dentition
the mean age values in each sex for each
quadrant were essentially identical. The
deciduous eruption sequence was Idl >
Id, > (Cd = Md, = Md,) > Md,. Average
ages of eruption ranged from 2.5 days
(Id,) through 9.3 days (Id$), 21.0 days
(Cd, Mdl, Md,) to 27.5 days (Md,).
The minimum ages of appearance of
radiographic evidence of crown formation,
root formation, crown eruption and root
completion for each of the permanent teeth
are shown in figure 1. Calcification of the
permanent crown began at 12 days in MI,
22 days in I,, 37 days in I,, C and Pmt,
44 days in Pm, and M, and 52 days in Pma.
Crown completion and initiation of root
400
a-
formation were first seen at 37 days in MI,
112 days in I, and M2,116 days in Iz, 136
days in Pms, 138 days in Pm, and Pmz and
244 days in C. The age and eruption sequence of the permanent teeth were 112
days for M1, 138 days for M2, 160 days
for 11,244 days for Iz and Pms, 288 days
for Pm, and 340 days for C and Pml. Root
formation was complete at 152 days in
M,, 244 days in M2,348 days in 11,370 days
in Pm, and Pms, 377 days in Iz and 390
days in C and Pm,. The time required for
complete development of the permanent
teeth ranged from 140 days for MI to 353
days for C and Pml.
Some minor variations in eruption sequence of the permanent teeth were found
in five (13.1 % ) of the specimens. They
consisted of delays in the eruption of upper
Pm, and lower Pma in a 244 day old female; lower Pm, in a 298 day old male; and
I, in a 348 day old male. In two females
(age 158 and 180 days) I1 erupted before
M*.
*-
d300
a-
c--
c/)
>
d
v
Lu
200
c3
*- *-
Q
IOC
0- 0C
~
TEETH
c3
I,
I2
C
Pm I
Pmz
Pm,
MI
M 2
M I N I M U M AGE SHOWING CUSP T I P F O R M I N G
M I N I M U M A G E SHOWING ROOT F O R M A T I O N B E G I N N I N G
c* M I N I M U M AGE SHOWING PERMANENT TOOTH ERUPTING
4 M I N I M U M AGE SHOWING ROOT F O R M A T I O N C O M P L E T E D
A-
G
USED T O I L L U S T R A T E DEVELOPMENTAL
PROGRESSION
Fig. 1 Minimum age of radiographic appearance of dental developmental indicators i n the marmoset (Callithrir iacchus). The letters A through G identify the age of the animals used in the preparation of the dental patterns shown in figure 3.
44
G . W. JOHNSTON, S . DREIZEN AND B. M. LEVY
(MI, M,, I,, Iz, Pma, Pme, Pml) at age 8 to
11 months and the full complement of 32
at age 11 to 12 months. The stage of mixed
dentition lasted from 112 to 340 days of
age (fig. 2).
Table 1 contains the distribution of
erupted deciduous and permanent teeth in
each marmoset arranged according to sex
and increasing chronological age. In each
sex four deciduous teeth (Idl) erupted
during the first postnatal week; four (Idz)
during the second week; 12 (Cd, Mdl, Mdz)
during the third week and four (Ma:,) during the fourth week. Four permanent teeth
(MI) emerged during the third to fourth
month and four (M,) during the fourth to
sixth month of age. The animals had 12 to
20 erupted permanent teeth (MI, Mz,11,
I,, Pm,) at age 7 to 8 months; 24 to 28
The salient features of postnatal odontogenesis in the cotton ear marmoset are depicted in figure 3. At birth the jaws contain the calcified crowns of the 20 deciduous teeth and the crypts of MI and Mz.
The
age related stages in the formation and migration of the succedaneous teeth are representative of the group. The migration
pathways of the permanent teeth follow a
TABLE 1
Distribution of erupted teeth in 40 marmosets
Age
Id1
Idt
Cd
Mdl
Mdz
Mdt
11
12
C
Pml
Pmz
Pms
MI
Ma
days
Males (21)
2
2
11
15
22
30
44
52
72
112
142
148
153
160
164
245
298
298
348 1
370
390
X
X
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
X
x
x
X
X
X
x
x
X
X
x
x
x
x
x
x
x
x
x
x
X
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Females (19)
9
20
36
113
134
136
136
138
146
157
158
180
198
204
244
244
287
288
377
1
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Animals with disturbances in eruption sequence.
X
X
x
x
X
X
X
x
x
X
X
X
x
x
x
x
x
x
x
x
x
x
X
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
45
DENTAL DEVELOPMENT IN CALLITHRIX JACCHUS
AGE R A N G E
S F R A D I O G R A P H I C EVIDENCE OF E R U P T I O N
OF M A R M O S E T
TEETH
d ' l
P
o
1
11
I2
C
I
MI
DECIDUOUS
M 2
I
M3
TEETH
1,
12
C
Pm,
Prn,
Pm,
MI
MZ
PERMANENT TEETH
Fig. 2 Age schedule and sequence of eruption of deciduous and permanent dentition in the marmoset (Callitkrix j a c c h u s ) .
forward, downward and lateral course in
the upper jaw and a forward, upward and
lateral course in the lower jaw as the face
grows and expands.
DISCUSSION
The dental development of the cotton ear
marmoset resembles that of the insectivorous primates as the permanent molars
are added to the dental arch before any of
the deciduous teeth are replaced by pennanent successors (Garn and Lewis, '63). A
distinguishing feature of the marmoset
permanent dentition is the presence of
three premolars and two molars in each
jaw quadrant in contrast to three premolars
and three molars in the other new world
monkeys and two premolars and three molars in the old world monkeys (James, '60).
The anomalous third molar found in one
specimen was the first encountered in
over 200 representatives of this species
examined in this laboratory.
There have been only two reports of the
order of eruption of the deciduous teeth
in primates of the family Callithricidae. In
the white lipped tamarin, Saguinus nigri-
collis, the incisors and canines are present
at birth and are followed postnatally by
Mdl > Md, > Md, (Chase and Cooper, '69).
Serra ('52) listed the sequence in the genus Callithrix as Id, > Id, > Mdl > Md, >
Md, > C without making any distinction
as to species. In the colony born members
of the Callithrix jacchus included in this
study the deciduous canines emerged before the deciduous molars, eruption proceeding from Id, through Md, in a consecutive manner.
The eruption sequence of the permanent
teeth of the genus Callithrix has been
variously reported as MI > 1, > I, > Pm, >
Pm, > M, > C Pm, (Bennejeant, '36),
M, > M2 > I, > 1, > Pm? > Pmi > Pm2 >
C for uppers and Ml > I, > M, > I, > Pml
> Pml > Pm, > C for lowers (Steliscka,
'47) and either Mi > I1> M, > Pmj > I, >
Pma > Pm, > C, or MI > M2 > II > Pms >
I, > Pmz > Pml > C, or Mi > II > Mz >
Pmj > Pm2> It > Pml > C (Serra, '52).
Each of these sequences was derived from
gross and/or radiographic studies of defleshed skulls of unknown age. In the present series in which gingival penetration
46
G . W. JOHNSTON, S . DREIZEN AND B. M. LEVY
Fig. 3 Chronology of dental development in the marmoset ( C a l l i t h ~ i jxa c c h u s ) . A, 112 days; B, 160
days; C, 204 days; D, 244 days.
DENTAL DEVEI>OPMENT IN CALLlTHRlX JACCHUS
Figs. 3E-G
47
E, 288 days; F, 298 days; G , 370 days
rather than alveolar breakthrough was used
as the criterion of eruption in cotton ear
marmosets of known age the order was
M j > M I , > 1, > I, = Pm? > Pm2 > PmL =
C.
The analysis of the age-related roentgenograpically detectable dental developmental indicators was limited by the sample size and the availability of only a single
radiogram for each animal. Methods of
x-raying the dentition of live young animals
are presently being developed to permit a
longitudinal study of dental development in
the cotton ear marmoset. These involve the
use of a dental x-ray machine operating a t
10 m a and 70 KV and intraoral non-radiatizcd periapical dental films with a n exposure time of 0.5 second trimmed to fit the
siLe of the mouth.
The time staggered emergence of 24
deciduous and 32 permanent teeth in the
cotton ear marmoset during the first year
of life provides a large and informative
spectrum of useful age indicators. There is
sufficient consistency in the age and order
of eruption of the dentition in this species
to permit a fairly accurate assessment of
the relative chronological age of immature
48
G. W. JOHNSTON, S. DREIZEN AND B. M. LEVY
animals. The lack of a demonstrable sex
difference and the near proximity in the
eruption patterns of each quadrant permits
the use of a single general standard for
this purpose.
LITERATURE CITED
Bennejeant, C. 1936 Anomalies et Variations
Dentaires chez les Primates. P. Vallier, Clermont-Ferrand (Tese).
Chase, J. E., and R. W. Cooper 1969 Sangzcinus
nigricollis - physical growth and dental eruption in a small population of captive-born individuals. Am. J. Phys. Anthrop., 30: 111-116.
Garn, S. M., and A. B. Lewis 1963 Phylogenetic
and intra-specific variations i n tooth sequence
polymorphism In: Dental Anthropology. D. R.
Brothwell, ed. The Macmillan Company, New
York.
Hampton, J. K., Jr., S. H. Hanipton and B. T.
Landwehr 1966 Observations on a successful breeding colony of the marmoset, Oedipomfdas oedipus. Folia Primat., 4: 265-287.
James, W. W. 1960 The Jaws and Teeth oE
Primates. Pitman Medical Publishing Co. Ltd.,
London.
Levy, B. M., and J. Artecona 1964 The marmoset as an experimental animal i n biological research: care and maintenance. Laboratory Animal Care, 14: 2 C ~ 2 7 .
Serra, 0. D. 1952 A sequencia eruptiva dos
dentes definitivos nos simios platyrrhina e sua
interpretacao filogenetica. Anais da Faculdade
de Farmacia e Odontologia da Universidade de
Sao Paulo, 10: 215-296.
Steliscka, W’. 1947 Uzebienie naczelmych (The
dentition of primates). An. Universitatis
MariaeCurie-Sklodowska, 8: 183-276.
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