American Journal of Primatology 44:255–275 (1998)

Chromosome Diversity of the Genus Aotus

From Colombia
OLGA MARÍA TORRES,1* SANDRA ENCISO,2 FRANCISCO RUIZ,2 ELIZABETH SILVA,3
2
AND IVÁN YUNIS
1
Instituto de Genética, Universidad Nacional, Santafé de Bogotá, Colombia
2
Laboratorio de Inmunogenética, Instituto Nacional de Salud, Santafé de Bogotá, Colombia
3
Laboratorio de Genética, Instituto Nacional de Salud, Santafé de Bogotá, Colombia

Description of six Colombian karyomorphs is completed through an ex-

tensive cytogenetic characterization of 35 Aotus (owl monkeys) specimens.
The description of a new karyomorph for Colombian Aotus by chromo-
some on Q, G, R, and C, sequential banding is included. Pairs of
karyomorphs 2 and 3 and 6 and 9 with 2n of 54, and 50, respectively, as
well as karyomorphs 7 and 8 with 46 and 58 chromosomes were strongly
suspected to represent different species on the grounds of large karyo-
typic differences. A proposal for a chromosome nomenclature of Aotus
karyomorphs that aims to clarify Aotus taxonomy is presented which
achieves a precise correspondence of different banding patterns, based
on Q, G, R, and C sequential banding and chromosome measurements.
Although our contribution is not a universal nomenclature system, unique
criteria for chromosome denomination within Aotus karyomorphs are es-
tablished. Previous systems of chromosome nomenclature have not suc-
cessfully addressed the nomenclature of chromosomes of the same
karyotype. Am. J. Primatol. 44:255–275, 1998. © 1998 Wiley-Liss, Inc.

Key words: Cebidae; Aotus; cytotaxonomy; karyomorph; karyotype;

Colombian owl monkey

INTRODUCTION
Taxonomy of neotropical monkeys of the genus Aotus (owl monkeys) is com-
plicated due to the difficulty of differentiating species using morphological char-
acters, the diversity of chromosome numbers within the genus, and the
chromosome number polymorphism of several species.
Karyological data concerning the genus Aotus reveal many intra- and inter-
specific chromosomal variations, both numerical and structural. Cytogenetic stud-
ies carried out by conventional Giemsa staining and banding techniques show
chromosome diploid numbers ranging from 46–58 in 18 karyotypes that can be
assigned to general karyotypically defined taxa. Table I summarizes the results
of cytogenetic studies available to date, including ours.

Contract grant sponsor: Instituto Nacional de Salud; Contract grant sponsor: Universidad Nacional
de Colombia.

*Correspondence to: Olga María Torres, Instituto de Genética, Universidad Nacional de Colombia
Santafé de Bogotá, Colombia.

Received for publication 3 November 1996; revision accepted 9 November 1997.

© 1998 Wiley-Liss, Inc.

TABLE I. Summary of Karyological Data Reported for Aotus

According to
Species Hershkovitz [1983] Banding Techniquese Country
a b c d
Aotus Aotus Ph 2n KM K CM Q G C N RBG of origin Referencesf
A. lemurinus lemurinus B 56–55 1 VIII + + Panama 1,2,3
IX
256 / Torres et al.

A. trivirgatus griseimembra A. lemurinus griseimembra B 54–52 2 IIa + + + + + + Colombia 2,4,5,6,7

IV
A. trivirgatus trivirgatus A. brumbacki 50 6 + + Colombia 5
A. trivirgatus vociferans A. vociferans B 46 7 V + + Colombia 2,4,9,10,11
48–46 X Perú
XI Brazil
A. hershkovitizig 58 8h + + Colombia 7,8
h
A. sp 50 9h Colombia
A. trivirgatus trivirgatus A. nancymai A 54 3 I + + + Colombia 2,4,10,11
Perú
Brazil
A. trivirgatus nigriceps A. nigriceps C 52/51 4 VII + + + + + Perú 2,4,9,13
A. trivirgatus azarae A. azarae boliviensis D 50/49 5 VI + + + + Bolivia 2,4,9,14,15
A. trivirgatus Azarae A. azarae azarae D 50/49 + + + Argentina 16
A. infulatus D 50/49 10h + + Brazil 17
A. (Rondonia) D 50/59 Brazil 18
A. trivirgatus 50–54 + 19–28
a
Ph, phenotype as defined by Ma et al [1976].
b
2n, diploid number.
c
KM, karyomorph denomination as defined by Reumer and De Boer [1980].
d
K, karyotype denomination as defined by Ma et al [1976].
e
CM, chromosome measures. Q, Q bands; G, G bands;R, R bands; C, C bands; N, N bands, nucleolar organizer regions. RBG, R bands, late replication by bromodeoxiuridine
incorporation.
f
1, Ma et al. [1978]; 2, Ma [1981]; 3, Bogart [1978]; cited by Reumer and De Boer [1980]; 4, Ma et al. [1976]; 5, Yunis et al. [1977]; 6, Miller et al. [1977]; 7, Giraldo et al.
[1986]; 8, Giraldo et al. [1983]; 9, Reumer and De Boer [1980]; 10, Ma et al. [1985]; 11, Pieczarka et al. [1992]; 12, Dutrillaux and Couturier [1981]; 13, Ma et al. [1980]; 14,
Minezawa and Valdivia [1984]; 15, Cambefort and Moro [1978]; 16, Mudry et al. [1984]; 17, Pieczarka and Nagamachi [1988]; 18, Pieczarka et al. [1993]; 19, Chu and
Bender [1961]; 20, Chiarelli [1961]; 21, Egozcue [1971]; 22, Brumback et al. [1971]; 23, Brumback [1975a]; 25, Brumback [1975b]; 26, De Boer [1974]; 27, Koiffmann and
Saldanha [1974]; 28, Descailleaux et al. [1990].
g
Groves [1993].
h
This report.
 Chromosome Diversity of Colombian Aotus / 257

In spite of extensive research of the genus Aotus, systematic and phyloge-

netic studies cannot take full advantage of karyotypical information, for cytoge-
netic studies have often been rather superficial, incomplete, and in some instances
disconnected from taxonomic relationships. Furthermore, much confusion arises
on the chromosome nomenclature of those karyological types.
Taxonomy of the genus Aotus has been highly controversial. Aotus, regarded
as a single species with allopatric subspecies [Hershkovitz, 1949; Hernandez-
Comacho & Cooper, 1975], may actually be comprised of a heterogeneous assem-
blage of karyotypically different animals [Ma et al., 1978; Ma, 1981]. It remains
to be explained why phenotypic similarities occur between groups, while cytoge-
netically distinct forms are found in the same geographical areas.
A taxonomic review of this genus [Hershkovitz, 1983] proposes that nine sepa-
rate species and four subspecies can be defined on the basis of variation of pel-
age coloration, karyotype, and geographic origin. These species belong to two
main groups: the gray-neck group north of the Amazon River and the red-neck
group south of the Amazon River. However, more recent data challenge this view
[Pieczarka et al., 1993].
Ford [1994] recognized only two species of the gray-neck group and five spe-
cies of the red-neck group, based on multivariate analysis of two data sets: cra-
nial and pelage features.
Cytogenetic characterization of Colombian owl monkeys from different loca-
tions may help clarify taxonomic relationships. We propose a chromosome no-
menclature for each karyomorph of the genus. Using this proposed nomenclature,
our results show six karyomorphs north of the Amazon River. The term
karyomorph (KM) is used here according to the definition of Reumer and De
Boer [1980].

METHODS
Animals
This study covers 35 owl monkeys form different geographical areas of Co-
lombia shown in Figure 1. Twenty-two specimens were fully characterized,
whereas information was supplemented on 13 specimens which had been reported
previously [Yunis et al., 1977; Giraldo et al, 1983]. Identification, place of cap-
ture, and sex of specimens are presented in Table II as well as the animal fate
and current location. Some animals are housed at Bioterio Central Instituto
Nacional de Salud (BINS), Centro de Rehabilitación World Society for the Pro-
tection of Animals (WSPA), and Centro Experimental de Primates (CEP)
(Universidad del Valle/Zoológico de Cali/Instituto Nacional de Salud). The skin
and skulls of several specimens were preserved and catalogued at Instituto de
Ciencias Naturales (ICN), Museo de Historia Natural Universidad Nacional de
Colombia, and at Instituto Humboldt (IU) (Instituto Nacional de los Recursos
Naturales Renovables y del Ambiente [INDERENA]).

Cytogenetics
Whole blood samples were cultured according to a modification of the method
of Moorhead et al. [1960] using RPMI 1640 culture medium supplemented with
20% fetal bovine serum. Phytohaemagglutinin P (Difco, Detroit, MI), a crude
extract of lectin from Vicia fava seeds (Favin), or pure Favin (Sigma, St. Louis,
MO) was used as a mitogen. Favin crude extract gave the best results.
258 / Torres et al.

Fig. 1. Colombian map showing the regions of karyomorphs location. 2, KM2, Costa Altantica; 3, KM3,
Amazonas; 6, KM6, Meta; 7, KM7, Caquetá; 8, KM8, Boyacá; 9, KM9, Quindío.

The Favin crude extract was prepared in our laboratory according to Arango
and Moreno [1977]. Favin was used at 5–20 µg/ml in a constant volume of whole
blood of 0.04 ml/ml. Incubations were carried out at 36.5°C for 63–79 hours.
Colcemid (Sigma) (1 µg/ml) was added 40 min before harvesting. Four cultures
were performed for each specimen, two of them for late DNA replication patterns
(RBH-FPG) after a 5-bromodeoxyuridine (BrdU) (50 µg/ml) terminal pulse treat-
ment during the last 5 and 7 h [Willard & Latt, 1976].
Air-dried slides were prepared by conventional methods. Chromosomes were
banded with quinacrine dichloride for QFQ identification [Caspersson et al., 1970].
Giemsa solid staining or banding techniques were carried out on slides that had
been Q-banded. Banding techniques included general and regional banding. The
general banding techniques were R banding RHG [Sehested, 1974], G banding
GTG [Seabright, 1971], and R late replication banding (RBH-FPG) [Willard &
Latt, 1976; Goto et al., 1975]. Regional banding techniques were C banding CBG
modified [Arrighi & Hsu, 1971; Sumner, 1972] and Ag staining NOR [Goodpasture
& Bloom, 1975]. Photographs were taken of each metaphase stained by Q band-
ing and of the same metaphase stained by the others (R, G, C, Ag banding) or
solid staining methods. Double karyotypes were prepared by cutting out prints
of the same metaphase stained simultaneously by two methods.
 Chromosome Diversity of Colombian Aotus / 259
TABLE II. Aotus Specimens Studied

Identification Current location

a
Cultb Place of capture Sex KMc 2n Numberd Dead Alive
2 67
008–72 Bolivar Tiquisio F 53 5 INDERENA
060–74 Bolivar Tiquisio M 54 5 INDERENA
062–74 Bolivar Tiquisio M 54 5 INDERENA
064–74 Bolivar Tiquisio M 54 5 INDERENA
065–74 Bolivar Tiquisio F 52 5 INDERENA
066–77 N. Santander (unknown) F 54 3 U. SALLE
067–77 N. Santander (unknown) M 54 3 U. SALLE
F1.4 056–94 Sucre B8 × A57 F 54 3 INC 14020
F1.59 001–94 Sucre A62 × A71 M 54 2 BINS
F1.15 086–94 Sucre A86 × A67 M 54 3 BINS
F1.74 085–94 Sucre A88 × A21 F 53 2 BINS
F1.43 058–94 Sucre D48 × D47 M 53 2 BINS
642 021–95 (Unknown) F 52 5 WSPA
B.1 002–94 Sucre (San Marcos) M 54 2 BINS
B.4 013–94 Sucre (San Marcos) F 52 5 BINS
D.36 003–94 Sucre (San Marcos) F 53 4 BINS
D.70 004–94 Sucre (San Marcos) F 54 4 ICN14022
F1.63 011–95 Sucre (unknown) M 54 2 ICN 14016
F1.136 057–94 Sucre B16 × A53 F 54 2 ICN 14017
3 19
A1 014–05 Amazonas (Leticia) M 54 3 BINS
A2 015–95 Amazonas (Leticia) F 54 5 ICN 14019
A3 088–94 Amazonas (Leticia) M 54 3 BINS
A4 089–94 Amazonas (Leticia) F 54 3 BINS
A5 080–94 Amazonas (Leticia) M 54 5 BINS
6 25
039–73 Meta (Villavicencio) F 50 5 IH 0354
040–73 Meta (Villavicencio) F 50 5 IH 2806
V66 009–94 (Unknown) F 50 5 CEP
728 020–95 (Unknown) M 50 5 WSPA
905 022–95 (Unknown) M 50 5 WSPA
7 10
V32 010-94 Caquetá (unknown) F 46 10 CEP
8 15
L1 080–82 Boyacá (Pajarito) M 58 6 Lost
L2 084–83 Boyacá (Pajarito) F 58 3 ICN 8880
L3 089–83 Boyacá (Pajarito) M 58 4 Lost
L4 081–82 Boyacá (Pajarito) F 58 2 IH 4140
9 10
Q2 079–94 Quindio (unknown) F 50 10 ICN 14023
a
Identification number of specimen.
b
Identification number of kidney or blood culture-year.
c
Karyomorph. Located as shown in Figure 1.
d
Number of karyotypes scored from each animal and karyomorph.

Chromosome measurements were made on two to ten Giemsa karyotypes

(Table II) from each animal by two independent observers using a graduated magni-
fying glass (0.1 mm). In order to balance the known inter- and intraindividual vari-
ability, we made chromosome length measurements on at least ten karyotypes (Table
II) from each karyomorph. Average chromosome lengths are reported.
260 / Torres et al.

Chromosome length is expressed as the percentage of the X-containing hap-

loid complement length (% TCL). The arm ratio is the length of the long arm
divided by the length of the short arm (q/p).
The karyotypes were ordered on the basis of chromosome measurements (size
and centromeric position) and the heterochromatic nature of the short arm, as
suggested by Miller et al., [1977], with Tjio and Levan’s [1956] ranges. The auto-
somes were classified in three groups defined according to the mean values of
arm ratio and arranged in a decreasing size order within each group as follows:
metacentric arm ratio, 1–1.9; submetacentric plus subtelocentric arm ratio, 2–4.9;
acrocentric plus telocentric arm ratio, >5. All chromosomes with whole heterochro-
matic short arms were included in the third group independently of arm ratio.
For the nomenclature proposed herein, each chromosome is defined by its
banding patterns in addition to its size and morphology. Each karyotype was
arranged with three major morphological groups clearly defined. C banding lets
us easily distinguish whole heterochromatic short arm chromosomes which are
responsible for the major interindividual variability in Aotus chromosomes. Each
group was ordered by decreasing chromosome size.

RESULTS
Phenotypes
The specimens from Amazonas belong to the red-neck group, whereas those
from Costa Atlántica, Meta, Caquetá, Boyacá, and Quindío belong to the gray-
neck species group. Following the classification proposed by Hershkovitz [1983],
specimens from Costa Atlántica, Meta, Caquetá and Amazonas would be named
Aotus lemurinus griseimembra, Aotus brumbacki, Aotus vociferans, and Aotus
nancymai, respectively.
Following phenotypic descriptions from Ma et al. [1976], specimens from Costa
Atlántica would belong to phenotype B and those from Amazonas to phenotype
A; the specimen from Quindío, those from Meta, and the four from Boyacá could
not be assigned to either group. Salient phenotypic characters of the unassigned
specimens are as follows.
The specimen from Quindío (Fig. 2) shows some peculiar features: the linear
marks on the forehead are wide and well defined, while lateral ones run forward
from the top of the head going down like a semicircle at the cheek level, and the
commissure. The neck is dark gray, except for a yellowish tuft present at the
throat level. The abdominal and thoracic ventral regions are covered by long
light yellowish fur, which is more evident at the order line which separates the
agouti color from the ventral area. A distinctive characteristic for this specimen
is that the pattern reaches the wrist on the forelimbs and the ankle on the
hindlimbs, in contrast with phenotypes A and B, in which the pattern reaches
only the elbow and knee or halfway, respectively. In the specimens from Meta,
the ventral color also extends as far as the elbows and knees to the inside of the
arms and legs, and the hair color is pale orange. The gray-neck specimens from
Boyacá show a rather dull yellow hair color in the limbs’ underside reaching the
elbows and knees; the hair coat is long and soft [Espinal et al., 1984].

Cytogenetics
Eight different karyotypes were identified among the 35 specimens, which
were distributed in six karyomorphs: 2, 3, 6, 7, 8, and 9. Chromosomal struc-
tures of those karyomorphs are shown in Table III.
 Chromosome Diversity of Colombian Aotus / 261

Fig. 2. Aotus phenotype from Quindío (karyomorph 9, KM9, 2n = 50).

Chromosome relative length and arm ratio measurements from karyomorphs

studied are shown in Table IV. Chromosome numbers are unique for each
karyomorph. Numbers were assigned to a chromosome as a result of its length,
morphology, and sequencing banding patterns; consequently, a number does not
represent the same chromosome in different karyomorphs.
Every chromosome in the karyomorphs analyzed showed constitutive hetero-
chromatin (C banding) at pericentromeric regions, but only some chromosomes
have a completely heterochromatic short arm, which sometimes is absent from
the homologous chromosome. Variations in the amount of heterochromatin be-
tween homologous chromosomes and among specimens were observed (data not
shown). At least three classes of constitutive heterochromatin were present. 1)
C-positive–Q-brilliant (Fig. 8, chromosome 5, for example), 2) C-positive–Q-pale
(Fig. 7, chromosome 13, for example), and 3) C-negative–Q-brilliant (Fig. 6, chro-
mosome 3, for example).
All specimens studied showed a metacentric chromosome with an achromatic
region in q, the marker chromosome characteristic of the Aotus genus [Egozcue
et al., 1969]. No specimen showed consistent CBG-positive staining in this re-
gion, except occasionally in a few cells, and this positive band, significantly lighter
(Fig. 3), could represent NOR activity. This observation occurred in all
karyomorphs studied.
262 / Torres et al.
TABLE III. Chromosomal Structure of Colombian Karyomorphs Studied

Pairs of autosomes Sex chromosomes

Mb Sb Ab
Karyomorph 2na 1–1.9c 2–4.9c >5c X RLd Y RLd

2 54/52 5/6 5 16/14 Mb 5.5 Mb 0.8

3 54 9 2 15 M 5.1 M 0.6
6 50 5 5 14 M 5.1 M 0.9
7 46 7 5 10 M 5.4 NDe —
8 58 4 4 20 M 5.3 M 1.4
9 50 9 3 12 M 5.0 NDe —
a
2n, diploid number.
b
Chromosome morphology: M, metacentric; S, submetacentric; A, acrocentric.
c
Range of arm ratio (q/p).
d
RL, relative length expressed as % TCL. Total X-containing haploid complement length.
e
ND, not determined (since only females were studied).

Although the Q- and G-banding patterns were usually similar remarkable

differences were the variable heterochromatic Q-bright bands at the ends of the
short arms and several interstitial bright bands, usually C-positive but not al-
ways G-positive.
The R-banding patterns from bromodeoxiuridine terminal treatment (RBH-
FPG) did not represent in all cases the reverse of the G-banding patterns (GTG);
several chromosomes showed some similar and corresponding R-positive and G-
positive bands. Good quality R bands (RHG) were not usually obtained, and opti-
mal conditions could be reproduced only in isolated cases.
Karyomorph 2. This karyomorph was defined from three different diploid
numbers, 54, 53, and 52 [Reumer and De Boer, 1980], corresponding to the karyo-
types II, III, and IV of Ma et al. [1976]. We observed it in specimens from the
Costa Atlántica. Following the criteria of Hershkowitz [1983], we feel these speci-
mens correspond to Aotus lemurinus griseimembra. Figure 4a shows a QFQ karyo-
type, which has five pairs each of metacentric and submetacentric chromosomes
and 16 pairs of acrocentric ones. The chromosome numbering was determined
according to our proposed criteria. Bright heterochromatic terminal bands were
observed in chromosomes 1p, 2p, 5p, 6p, 7p, 8p, 9p, and 10p; all of them were
heteromorphic. Figure 4b shows a composite karyotype representing the haploid
set with G, R, and C banding. The X chromosome was metacentric as in other
karyomorphs, and the Y chromosome, the smallest metacentric chromosome,
showed interindividual morphologic variations due to the resolution level.
Karyomorph 3. This karyomorph exhibits a 2n = 54 [Reumer & De Boer,
1980]; it is equivalent to the karyotype I of Ma et al. [1976]. We observed it in
the specimens from Amazonas. Following the criteria of Hershkovitz [1983], we
feel these specimens correspond to Aotus nancymai. Figure 5a shows a QFQ karyo-
type. It has nine pairs of metacentric, two pairs of submetacentric, and 15 pairs
of acrocentric chromosomes; however, herein the chromosome numbering changes
according to our proposed criteria. Terminal bright heterochromatic bands were
observed in chromosomes 12p, 13p, 15p, 17p, and 24p. Figure 5b shows a com-
posite karyotype representing the haploid set with G, R, and C banding. Except
for whole heterochromatic short arms (chromosomes 12, 13, 14, 15, 17, 18, and
24), no terminal or iterstitial constitutive heterochromatin was observed in the
specimens carrying this karyomorph. The centromeric heterochromatin of chro-
mosomes 1, 3, 4, and 6 showed heteromorphisms. The Y chromosome, the small-
TABLE IV. Chromosome Measurements From Colombian Karyomorphs Studied*
Karyomorph 2 Karyomorph 3 Karyomorph 6 Karyomorph 7 Karyomorph 8 Karyomorph 9
% TCL Arm ratio % TCL Arm ratio % TCL Arm ratio % TCL Arm ratio % TCL Arm ratio % TCL Arm ratio
Chromo- Chromo- Chromo- Chromo- Chromo- Chromo-
some x s x s some x s x s some x s x s some x s x s some x s x s some x s x s
1 5,5 0,31 1,4 0,14 1 8,8 0,34 1,0 0,05 1 6,4 0,30 1,5 0,13 1 8,9 0,36 1,2 0,08 1 3,8 0,10 1,2 0,08 1 9,2 0,52 1,2 0,09
2 4,2 0,18 1,9 0,29 2 8,3 0,45 1,1 0,08 2 5,7 0,22 1,2 0,08 2 6,6 0,33 1,7 0,17 2 3,6 0,18 1,2 0,12 2 8,5 0,44 1,2 0,08
3 3,8 0,29 1,3 0,23 3 5,5 0,30 1,3 0,14 3 4,3 0,34 1,9 0,23 3 5,9 0,22 1,1 0,11 3 3,2 0,22 1,1 0,15 3 5,4 0,32 1,3 0,19
4 3,3 0,17 1,1 0,14 4 4,0 0,23 1,9 0,18 4 4,0 0,14 1,4 0,15 4 5,1 0,37 1,0 0,09 4 2,6 0,13 1,1 0,04 4 5,0 0,41 1,2 0,11
5 2,4 0,17 1,0 0,07 5 3,7 0,27 1,7 0,20 5 3,7 0,22 1,4 0,14 5 4,4 0,20 1,6 0,20 5 6,1 0,22 2,5 0,23 5 4,4 0,24 1,6 0,21
6 5,9 0,40 3,4 0,58 6 3,7 0,20 1,4 0,28 6 5,9 0,39 3,5 0,79 6 4,2 0,22 1,6 0,23 6 5,0 0,18 2,7 0,28 6 3,9 0,33 1,6 0,35
7 5,3 0,20 3,5 0,35 7 3,7 0,28 1,2 0,21 7 5,0 0,30 2,8 0,34 7 3,8 0,28 1,3 0,17 7 4,8 0,19 2,3 0,22 7 3,8 0,26 1,9 0,29
8 5,2 0,19 3,3 0,43 8 3,3 0,27 1,1 0,15 8 4,5 0,18 3,2 0,36 8 6,0 0.19 3,9 0,65 8 4,2 0.08 2,8 0,26 8 3,7 0,20 1,2 0,14
9 4,6 0,24 3,2 0,27 9 2,3 0,25 1,9 0,42 9 4,2 0,23 2,3 0,60 9 4,9 0,30 3,1 0,20 9 4,9 0,18 69,2 30,78 9 3,3 0,41 1,1 0,11
10 4,2 0,31 3,2 0,30 10 5,5 0,56 4,5 0,90 10 3,9 0,25 3,4 0,53 10 4,5 0,19 3,3 0,70 10 4,4 0,11 3,0 0,21 10 5,7 0,28 3,4 0,49
11 4,5 0,21 6,6 1,57 11 3,8 0,30 3,2 0,50 11 5,7 0,29 8,0 2,20 11 4,1 0,32 3,9 0,95 11 4,3 0,14 26,3 17,14 11 4,0 0,29 3,3 0,49
12 4,5 0,25 54,7 27,96 12 4,8 0,16 4,7 0,67 12 4,8 0,28 12,3 8,66 12 3,7 0,33 2,7 0,31 12 3,9 0,20 14,6 11,64 12 3,4 0,28 3,3 0,31
13 4,4 0,35 8,2 12,64 13 3,9 0,39 4,2 0,82 13 3,9 0,24 12,7 7,06 13 5,9 0,31 5,8 1,54 13 3,6 0,15 21,1 8,78 13 4,5 0,46 6,1 1,60
14 3,9 0,22 6,1 1,40 14 3,5 0,29 6,0 1,52 14 3,9 0,23 4,0 0,71 14 4,2 0,19 2,7 0,48 14 3,4 0,14 15,4 14,73 14 4,3 0,30 7,6 2,50
15 3,9 0,19 6,5 3,41 15 3,3 0,17 4,7 1,62 15 3,6 0,25 14,4 11,05 15 3,4 0,18 19,9 10,43 15 3,2 0,11 27,0 19,22 15 4,0 0,39 6,3 1,85
16 3,4 0,19 14,5 16,74 16 3,2 0,20 20,1 21,20 16 3,5 0,30 10,7 9,59 16 3,3 0,20 29,5 14,59 16 3,1 0,09 31,8 15,42 16 3,8 0,31 6,6 2,47
17 3,3 0,26 37,3 22,33 17 3,0 0,20 6,0 1,46 17 3,4 0,21 12,7 7,80 17 3,2 0,18 17,8 9,83 17 3,1 0,10 25,3 20,73 17 2,9 0,36 5,2 2,42
18 3,2 0,26 18,5 14,08 18 2,9 0,29 5,1 4,68 18 2,9 0,28 15,2 6,37 18 2,6 0,15 19,9 10,57 18 3,1 0,19 2,3 0,28 18 2,7 0,22 6,8 2,80
19 2,7 0,24 18,8 16,02 19 2,8 0,89 9,5 7,24 19 2,9 0,21 15,0 11,46 19 2,5 0,25 21,0 10,72 19 3,0 0,20 26,4 19,31 19 2,6 0,29 11,6 4,42
20 2,6 0,33 24,3 18,08 20 2,7 0,22 6,1 2,77 20 2,7 0,30 14,3 10,84 20 2,5 0,22 17,9 8,89 20 2,7 0,14 19,7 11,64 20 2,4 0,27 12,5 5,87
21 2,6 0,21 21,4 16,62 21 2,6 0,18 6,5 5,38 21 2,6 0,22 15,5 11,72 21 2,5 0,19 12,5 10,01 21 2,7 0,16 24,3 15,44 21 2,3 0,27 15,3 7,32
22 2,5 0,24 26,4 16,90 22 2,5 0,14 5,7 2,48 22 2,6 0,28 15,2 11,75 22 2,4 0,22 14,9 6,04 22 2,7 0,28 28,1 13,51 22 2,1 0,26 14,6 5,41
23 2,4 0,40 22,8 16,89 23 2,1 0,16 7,0 3,89 23 2,5 0,30 21,7 13,39 X 5,4 0,45 1,3 0,08 23 2,5 0,12 15,4 9,37 23 1,6 0,18 8,0 2,76
24 2,2 0,09 28,3 14,44 24 2,1 0,29 3,1 1,01 24 2,4 0,25 13,2 8,15 24 2,4 0,17 17,1 10,76 24 1,5 0,15 11,4 3,35
25 2,2 0,17 27,9 11,26 25 1,8 0,19 12,3 8,78 X 5,1 0,29 1,2 0,12 25 2,3 0,16 20,3 11,80 X 5,0 0,32 1,2 0,14
26 1,8 0,15 25,6 9,19 26 1,2 0,20 9,2 7,15 Y 0,9 0,12 1,1 0,14 16 2,2 0,14 17,8 9,84
X 5,2 0,26 1,3 0.09 X 5,1 0,19 1,3 0,10 27 2,1 0,12 16,8 4,91
Y 0,8 0,14 1,1 0,09 Y 0,6 0,32 1,1 0,53 28 1,8 0,15 7,8 7,49
X 5,3 0,10 1,3 0,08
Y 1,4 0,16 1,2 0,14

*%TCL, relative length (% total chromosome length); x, means; s, standard deviation.

Chromosome Diversity of Colombian Aotus / 263
264 / Torres et al.

Fig. 3. Partial metaphases showing (a) Positive silver nucleolus organizing regions Ag-NORs from KM2
(2n = 54 and (b) QFQ and sequential CBG from KM3 (2n = 54). Arrows show positive C band in the second-
ary constriction or nucleolus organizing regions.

est metacentric chromosome, showed a late replication arm, but whether it cor-
responded to p or q could not be established.
Karyomorph 6. Recognized previously [Reumer & De Boer, 1980], this
karyomorph shows a 2n = 50 chromosomes. It was observed in specimens from
Meta. Following the criteria of Hershkovitz [1983], we feel these specimens cor-
respond to Aotus brumbacki. Figure 6a shows a QFQ karyotype, which has five
pairs each of metacentric and submetacentric chromosomes and 14 pairs of acro-
centric ones. Bright heterochromatic bands were observed in 1p, 2p, 3p, 6p, 7p,
8p, 10p, 11p, and 14q chromosomes (interstitial in the last one). However, these
bands were not C-positive in chromosomes 3, 8, and 10. Figure 6b shows a compos-
ite karyotype representing the haploid set with G, R, and G banding. In one of the
males studied, the Q-bright and C-positive interstitial heterochromatic band of chro-
mosome 14q was heteromorphic; this chromosome also had a heteromorphic whole
heterochromatic short arm. Chromosome 11p was also completely heterochromatic.
One male was heterozygous for a chromosome 13q paracentric inversion, centromere
proximal. Chromosome Y was the smallest metacentric chromosome.
Karyomorph 7. Recognized previously [Reumer & De Boer, 1980], this
karyomorph corresponds to karyotype V described by Ma et al. [1976]. With a 2n
= 46, it shows the lowest diploid number of the genus Aotus. We observed it is a
female specimen from Caquetá. Following the criteria of Hershkovitz [1983], we
 Chromosome Diversity of Colombian Aotus / 265

Fig. 4. Banding patterns from karyomorph KM 2 (2n = 54): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).
266 / Torres et al.

Fig. 5. Banding patterns from karyomorph KM 3 (2n = 54): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).
 Chromosome Diversity of Colombian Aotus / 267

Fig. 6. Banding patterns from karyomorph KM 6 (2n = 50): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).

feel this specimen corresponds to Aotus vociferans. Figure 7a shows a QFQ karyo-
type, which has seven pairs of metacentric, five pais of submetacentric, and ten
pairs of acrocentric chromosomes. Bright heterochromatic bands were observed
in chromosomes 2p, 5p, 8p, and 9p. These bands were also C-positive and hetero-
morphic. Figure 7b shows a composite karyotype representing the haploid set
with G, R, and C banding. The X chromosome was identified by its late replica-
268 / Torres et al.

Fig. 7. Banding patterns from karyomorph KM 7 (2n = 46): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).

tion. The whole heterochromatic short arms of chromosomes 13 and 14 were het-
eromorphic. Chromosomes 2, 3, 5 and 6 show prominent centromeric bands.
Karyomorph 8. This karyomorph exhibits the highest diploid number of
the genus Aotus, 2n = 58 chromosomes. It was observed in four specimens from
Boyacá [Giraldo et al., 1983]. These specimens were considered Aotus hershkovitzi
by Groves [1993]. Figure 8a shows a QFQ karyotype, which presents four pairs
 Chromosome Diversity of Colombian Aotus / 269

Fig. 8. Banding patterns from karyomorph KM 8 (2n = 58): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).
270 / Torres et al.

each of metacentric and submetacentric chromosomes and 20 pairs of acrocentric

ones. Bright heterochromatic bands were observed, interstitial bands in the 20q
chromosome and terminal bands in chromosomes 2p, 5p, 6p, 7p, 8p, and 25q.
Two of four animals, a male and a female, presented a heteromorphic terminal
band in the Xp chromosome. Figure 8b shows a composite karyotype represent-
ing the haploid set with G, R, and C banding. Constitutive heterochromatin was
localized pericentromerically (in all chromosomes), terminally 10p, 4q, 5p, 6p,
7p, 8p, 25q, and Yq), and interstitially (20q, 27q). CBG heteromorphic bands were
observed (chromosomes 2, 3, 4, 5, 6, 7, 10, 18, 20, and 27), showing size varia-
tions, or sometimes were absent. The whole heterochromatic short arms of chro-
mosomes 10 and 18 do not have very late replication. Of the karyomorphs studied,
this karyomorph presented the longest Y chromosome, which was also the small-
est metacentric chromosome.
Karyomorph 9. This previously undescribed karyomorph exhibits a diploid
number of 50 chromosomes, with a chromosome constitution different from all
published Aotus karyotypes. It was observed in a female specimen from Quindío,
(Aotus sp.). Figure 9a shows a QFQ karyotype, which has nine pairs of metacen-
tric chromosomes, as well as three pairs of submetacentric and 12 pairs of acro-
centric ones. Intense fluorescent terminal bands were present in the 8p, 10p,
11p, 12p, 13p, 14p, and 15p chromosomes. For chromosomes 8, 13, 14, and 15,
these bands correspond to C-positive constitutive heterochromatin. Figure 9b
shows a composite karyotype representing the haploid set with G, R, and C band-
ing. As in other karyomorphs, the X chromosome was identified by its late repli-
cation and band pattern. Chromosomes 13q and 22q show interstitial C bands,
proximal to the centromere, while chromosomes 13–18 show heteromorphic whole
heterochromatic short arms. The centromeric heterochromatic band of chromo-
some 5p is also heteromorphic.
A comparison of chromosome nomenclature equivalence with previous reports
is presented in Table V.

DISCUSSION
The existence of six species of Aotus in Colombia is clearly possible from the
results presented here as well as from the comparisons of these karyomorphs
with those reported in the literature. We have identified eight karyotypes that
fit six different karyomorphs in Colombian Aotus based on chromosomal diver-
sity. Metacentric chromosomes ranged from four to nine pairs, submetacentrics
from two to five, and acrocentrics from 10–20.
To date, there is not a uniform system of cytogenetic nomenclature for the
genus. We intended to establish a uniform nomenclature system that follows
unique criteria for chromosome denomination in the karyomorphs studied. This
does not imply, however, that one particular chromosome maintains the same
denomination in different karyomorphs. This was not possible because of chro-
mosome diversity and the possibility of representing different species.
The major stumbling block for developing a single general standard number-
ing system for all karyomorphs observed was the great variability in chromo-
somal structure. For example, karyomorphs 2 and 3 have equal diploid numbers
of chromosomes and yet show differences that were impossible to consolidate
under the same numbering system. The same situation occurs for karyomorphs
6 and 9. Identical homologous chromosomes cannot conserve the same denomi-
nation in different karyomorphs without causing confusion regarding the rear-
ranged chromosomes. The equivalences for identical homologous chromosomes of
 Chromosome Diversity of Colombian Aotus / 271

Fig. 9. Banding patterns from karyomorph KM 9 (2n = 50): (a) Q banding and (b) G, R, and C banding
from a haploid set (including sex chromosomes).

the different karyomorphs of the genus found in Colombia are reported by Torres
et al. [in press].
We did, however, develop a numbering system for each karyomorph or chromo-
some taxon in which each chromosome has a unique designation based on sequen-
tial banding patterns and chromosome measurements (size and morphology).
272 / Torres et al.
TABLE V. Aotus Karyomorph Found in Colombia: Chromosome Nomenclature
Equivalences With Previous Reports
Karyomorph
KM2 KM3 KM7 KM6
4b 9b 9b 4b 9b 4b 9b
TRa II 6b K2 (standard) TRa I 11b 12b (standard) TRa V 11b (standard) TRa 5b
25p
1 2 1 2 18q 1 2 2 1i 6/7 1 1 1 8/11 1 11
2 3 2 3 1 2 1 1 2i 8/11 2 2 2 9/25 2 5
3 4 3 4 2 3 3 3 4 4/15 3 3 3 4/15 3 12
4 5 4 5 3 4 4 4 6 4 4 4 21/22 4 13
5 6 5 6 4 5 5 5 5 5 5 5 1 5 1
6 7 6 7 5 6 6 6 8 3 6 7 7 20/27 6 2
7 8 7 9 6 7 7 7 7 2 7 8 8 2 7 3
8 9 8 8 7 8 8 8 9 8 10 10 10 8 4
9 12 9 12 10 9 10 10 23 9 12 12 6 9 10
10 11 10 13 12 10 11 11 3 5 10 11 11 12 10 6
11 10 12 10 9 11 14 14 11 12 11 13 13 3 11 14
12 13 11 1q 8 12 12 12 10 9 12 6 6 7 12 15
13 14 13 1p 11 13 13 13 13 13 9 9 13 16
14 15 14 11 16 14 16 18 15 14 17 17 14 19
15 16 15 14 13 15 15 17 16 18 15 15 15 15 18
16 17 16 15 17 16 19 19 12 16 16 16 16 17
17 18 17 16 14 17 18 15 14 17 14 14 14 17 20
18 19 19 17 15 18 17 9 18 18 21 20 18 22
19 21 20 19 19 19 23 21 19 19 18 19 19 21
20 23 23 20 22 22 17 20 22 21 20 23
21 24 21 21 20 21 20 23 21 21 19 18 21 8
22 22 22 20 21 22 21 16 20 22 20 22 22 9
23 20 18 23 23 23 9 20 22 23 7
24 26 24 22 22 24 24 24 24 25 24
25 25 25 24 26 25 25 25 25
26 27 26 25 27 26 26 26 26
X X X X X X X X X X X X X
Y Y Y Y Y Y Y
a
TR, this report.
b
References as cited in Table I: 4, Ma et al. [1976]; 5, Yunis et al. [1977]; 6, Miller et al. [1977]; 9, Reumer
and De Boer [1980]; 11, Pieczarka et al. [1992]; 12, Dutrillaux and Couturier [1981].

Previous nomenclature systems of Ma et al. [1976] and Reumer and De Boer

[1980] do not meet our analytical needs.
The nomenclature system of Ma et al. [1976] poses a few problems. First the
criterion for establishing the A and B chromosome groups does not define the
limits in arm ratio, and consequently there are mixtures of chromosomes with
euchromatic and heterochromatic short arms in the B group. Second, some de-
nominations are not represented in certain karyotypes, and thus the chromo-
some denomination does not keep a relationship with the diploid number. Finally,
it is difficult to distinguish a numeric polymorphism within one karyomorph from
the chromosome variation found in different karyomorphs.
Reumer and De Boer [1980] did not succeed in unifying the nomenclature
according to a standard karyotype for two reasons. First, their approach did not
take into account differences in karyotype structure (i.e., karyomorphs with similar
diploid numbers but qualitatively different chromosomes or karyotypes having a
 Chromosome Diversity of Colombian Aotus / 273

higher number than the standard karyotype), making it difficult to define some
karyomorphs. Second, the difficulty of identifying several chromosomes with
intrachromosomal rearrangements is not addressed. In this system, chromosomes
which have suffered inversion or other intrachromosome changes keep the same
denomination corresponding to the standard element; thus, fundamentally different
chromosomes have the same denomination. Although those chromosomes were de-
nominated as ‘‘variant chromosomes’’ ( a term that is theoretically incorrect, as the
authors themselves pointed out), this feature makes the nomenclature ambiguous.
Moreover, the authors recognize a weakness in their nomenclature when they find
one or two putative chromosome pairs in karyomorph 3 which are not present in
any other karyomorph.
It is well known that there are not direct relationships among banding pat-
terns. In independent studies with different chromosome identification methods,
one particular chromosome of the same established karyotype could have differ-
ent identity. For example, chromosome 2 (GTG) karyotype I of Ma et al., [1976]
does not correspond to chromosome 2 (RTBA) karyotype I of Dutrillaux and Cou-
turier [1981]. Such ambiguity can be solved by establishing a chromosome no-
menclature system based on sequential banding. In this proposal, chromosome
denomination is based on G, R, Q, and C sequential banding patterns and chro-
mosome measurements. Through this methodology, a precise correspondence of
different banding patterns is achieved.

CONCLUSIONS
1. Six different Aotus karyomorphs were found in Colombia. In order to elu-
cidate whether they represent different species, it is necessary to observe a larger
sample, both in the number of specimens and the number of regions.
2. It was not possible to generate a standard, single, cytogenetic nomencla-
ture for the genus Aotus because of the chromosomal differences of the observed
karyomorphs, but a nomenclature for each one of the recognized karyomorphs
would be effective.
3. The nomenclature system based on the sequential banding pattern size,
and morphology of the chromosomes proposed for each one of the six karyomorphs
accommodates all existing information to date.

ACKNOWLEDGMENTS
We are very grateful to the genetics group of the Instituto Nacional de Salud
for collaboration, to Camenza Murillo for the Favin extract preparation to Luis
Fernando Cadavid and Mario Contreras, who participated in the earlier part of
the work, to Gloria Pérez for her collaboration in the preparation and measure-
ment of karyotypes, to Cecilia Ramirez from the Instituto de Ciencias Naturales
for her collaboration in the preservation of the specimens, to Jorge Gardeazábal
from Zoológico de Cali, to Fernando Nassar and Juanita Roda from Centro de
Rehabilitación WSPA (World Society for the Protection of Animals) and to Tobias
Mojica, Ph.D., for his critical reading of the manuscript.
The work was supported by the Instituto Nacional de Salud and by the
Universidad Nacional de Colombia (OMT).

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