Journal of Mammalogy, 82(4):1080–1091, 2001

CHROMOSOME STUDIES OF SEVEN SPECIES OF OLIGORYZOMYS

(RODENTIA: SIGMODONTINAE) FROM BRAZIL

JAQUELINE ANDRADES-MIRANDA, LUIZ F. B. OLIVEIRA, C. ANDRÉ V. LIMA-ROSA, ANDREA P. NUNES,

NILSON I. T. ZANCHIN, AND MARGARETE S. MATTEVI*

Departamento de Genética, Universidade Federal do Rio Grande do Sul, Caixa Postal 15053,
91501-970, Porto Alegre, Rio Grande do Sul, Brazil (JAM, CAVLR, NITZ, MSM)
Museu Nacional, Setor de Mastozoologia, Universidade Federal do Rio de Janeiro, 20940-040,
Rio de Janeiro, Brazil (LFBO)
Departamento de Zoologia, Museu Emilio Goeldi, Caixa Postal 399, Belém, Pará, Brazil (APN)

Karyotypes of 7 taxa of the rodent genus Oligoryzomys trapped in 33 localities from an

area ranging from 018N to 328S in Brazil were analyzed. Three species were trapped ex-
clusively in the Cerrado biome: O. stramineus, diploid number (2n) 5 52, fundamental
number (herein, number of autosomal arms; FN) 5 68; O. eliurus, 2n 5 62, with 2 fun-
damental numbers, FN 5 64 and 66; and Oligoryzomys sp., 2n 5 70, FN 5 74. In the
Amazon, we caught O. cf. messorius, 2n 5 56, FN 5 58, and O. microtis, 2n 5 66, FN
5 74. Oligoryzomys nigripes (2n 5 61, 62, FN 5 80–82) was trapped in 24 localities in
various biomes, and O. flavescens from several sites in southern Brazil presented the same
karyotypes as those already described at other sites. The C- and NOR-banding were per-
formed for all species, and the (T2AG3)n telomeric probe hybridized in situ to both the short
and long arms of all pairs of karyotypes of O. cf. messorius, O. eliurus, and Oligoryzomys
sp. An analysis performed with 11 microsatellite DNA heterologous primers improved
differentiation of O. nigripes from O. eliurus individuals, 2 species that presented 2n 5 62
and that were trapped at the same site.

Key words: Amazon, Cerrado, fluorescent in situ hybridization, karyotypes, Oligoryzomys, Sig-
modontinae

The South American rodent genus Oli-
goryzomys was described as a subgenus of
the genus Oryzomys of the Sigmodontinae
by Bangs (1900), thus joining a group of
species whose members were distinguished
by morphologic measurements. These
marker characters include, among others,
small body size, tail longer than head and
body, short and broad hind feet, small skull
but with a stout appearance, and rostrum
relatively broad and stocky (Carleton and
Musser 1989). These rodents are terrestrial,
nocturnal, and feed on seeds, fruits, and in-
sects, and some of the species can be ag-
ricultural pests or significant reservoirs of
* Correspondent: margarete.mattevi@ufrgs.br
hantavirus (Emmons and Feer 1990; Pow-
ers et al. 1999).
The genus Oligoryzomys is widely dis-
tributed, occupying Central and South
America from southern Mexico to Panama,
through French Guiana, Suriname, and
Guyana, western Venezuela, eastern and
southern Colombia, Ecuador, western Peru,
Chile, Bolivia, Paraguay, eastern and cen-
tral Argentina, and Brazil. The estimated
number of species varies from 1 (Hersh-
kovitz 1966), 12 (Honacki et al. 1982), 15
(Musser and Carleton 1993), 19 (Cabrera
1961), to 30 (Tate 1932). Both its status as
a genus and the relationships among its nu-
merous species have been controversial.
Currently, it is considered as a genus be-

1080
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS 1081

FIG. 1.—Collection sites (coordinates given in Appendix I): 1) Surumú, Roraima State (RR); 2)
Fazenda São Bento, Tartarugalzinho, Amapá State (AP); 3) including the localities: 40 km SW
Minaçú, 55 km N Niquelândia, 20 km NW Colinas do Sul, and 40 km NE Uruaçú; 4) Mambaı́, and
5) Ipameri, Caldas Novas, and Corumbaı́ba, Goiás State (GO); 6) Rio de Una, 10 km ESE São José,
Bahia State (BA); 7) Monte Verde, Espı́rito Santo State (ES); 8) Parque Nacional de Iguaçú, Paraná
State (PR); 9) Concórdia, and 10) Costa de Dentro, Santa Catarina Island, Santa Catarina State (SC);
11) Parque Estadual do Turvo, Derrubadas, 12) Nonoai, 13) Aratiba, 14) Aracuri Ecological Station,
Muitos Capões, 15) Ivaı́, Tupanciretã, 16) Caxias do Sul, 17) Tainhas, 18) Faxinal, Torres, 19) São
Francisco de Paula, 20) Riozinho, 21) Picada Verão and Alto Ferrabraz, Sapiranga, 22) Charqueadas,
23) including 2 localities: Rio Jacuı́, Eldorado do Sul, and Belém Novo, 24) Osório, 25) Tramandaı́
Lagoon, Tramandaı́, 26) Quintão, 27) northern Tapes Bay, Tapes, 28) Capão do Leão, Mostardas,
and 29) Taim Ecological Station, Rio Grande, Rio Grande do Sul State (RS).

longing to the Sigmodontinae (Carleton and
Musser 1989), and studies have been per-
formed on some aspects of the genetic
structure of the populations and relation-
ships of a few species (Chiappero et al.
1997; Dickerman and Yates 1995; Myers et
al. 1995; Patton et al. 1996). Karyologic
studies have helped to clarify systematics of
this complex group, which presents diploid
numbers (2n) from 44 found in the taxon
named as Oligoryzomys sp. 2 by Silva and
Yonenaga-Yassuda (1997) to 68 in the an-
imals considered as variant 1 of Oligory-
zomys longicaudatus by Gardner and Patton
(1976). We describe for the 1st time the
karyotypes of 3 species of this genus and 4
other species collected at 33 localities com-
prising the major part of the Brazilian range
of the genus.
MATERIALS AND METHODS
The sample included specimens of 7 taxa of
Oligoryzomys caught at 33 localities in an area
ranging from 018N to 328S in Brazil (Fig. 1; Ta-
ble 1). Skins and skulls of the individuals stud-
ied are deposited in the mammal collections of
the Museu Nacional, Rio de Janeiro (MN), and
the Universidade Federal da Paraiba, João Pes-
1082 JOURNAL OF MAMMALOGY Vol. 82, No. 4

TABLE 1.—Localities and number (n) of Oli- RESULTS AND DISCUSSION

goryzomys specimens analyzed. The 7 species analyzed displayed diploid
Species Localitiesa n numbers from 52 to 70. The diploid number
O. stramineus 4 7
of 70 that we found in Oligoryzomys sp. is
O. cf. messorius 1 4 the highest number reported to in the genus,
O. nigripes 5–11, 13–29 207 verified in 1 of the 3 undescribed karyo-
O. eliurus 3, 5 8 types we report in this paper (Table 2).
O. flavescens 10, 12, 17, 22, 26 59 Oligoryzomys stramineus.—Seven O.
O. microtis 2 6
Oligoryzomys sp. 3 21
stramineus (Tables 1 and 2) showed 2n 5
a
52, with 9 biarmed and 16 acrocentric au-
Numbers correspond to those in Fig. 1.
tosome pairs. The X chromosome was a
large submetacentric, between pairs 3 and
4 in size, and the Y chromosome was a me-
soa (UFPB). Voucher specimen numbers are
dium-sized metacentric. The C-bands (data
given in Appendix I.
not shown) were centromeric in the major-
Mitotic preparations were made employing the
technique of Baker et al. (1982). The C-, G-, and ity of the autosomes (but were absent in the
NOR-banding were performed following the 1st pair) and of the X chromosome. The Y
methods of Sumner (1972), Seabright (1971), and chromosome was entirely heterochromatic.
Howell and Black (1980), respectively. The fluo- The karyotype of O. stramineus could be
rescent in situ hybridization process with the telo- included in species group 3 (the first 2–4
meric sequence (T2AG3)n was applied to speci- pairs of similar size, according the classi-
mens of Oligoryzomys cf. messorius, O. eliurus, fication we made of the Oligoryzomys spe-
and Oligoryzomys sp., with the ‘‘all human telo- cies based in the size and shape of its pair
meres’’ probe (Oncor, Gaithersburg, Maryland) 1, see Table 3). That same Giemsa karyo-
stained with digoxygenin according to the man- type was reported by Bonvicino and Wek-
ufacturer’s protocol.
sler (1998:94, figure 2) in the type series of
Eleven sets of microsatellite DNA primers de-
O. stramineus, a new species that they de-
signed for Rattus (R12, R47, R65, R69, R75,
and R97—Serikawa et al. 1992) and Mus (M13,
scribed. Mambaı́ (Goiás State; Fig. 1), from
M23, and M49—Love et al. 1990; and ATP and which our sample came, was located inside
KRT—Santos et al. 1995) were amplified by the distribution area proposed for this spe-
heterologous polymerase chain reaction in O. cies (Cerrado of northern Goiás and Minas
eliurus and O. nigripes, as described in Lima- Gerais states and Caatinga of the states of
Rosa et al. (2000). Paraiba and Pernambuco).

TABLE 2.—Diploid number (2n) and autosomal arm fundamental number (FN), X- and Y-chro-
mosome morphologies, and NOR-band patterns of Oligoryzomys.

NOR
Species 2n FN X Y (pairs)
O. stramineus 52 68 SMa Mb
O. cf. messorius 56 58 SM SM 1
O. nigripes 61, 62 78, 80–82 M Ac
O. eliurus 62 64, 66 A/STd A/SM 1–3
O. flavescens 64–67 66–68 SM/M A
O. microtis 66 74 A A 2
Oligoryzomys sp. 70 74 A/ST A 2–5
a
Submetacentric.
b
Metacentric.
c Acrocentric.

d Subtelocentric.
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS 1083

TABLE 3.—Karyotyped species of Oligoryzomys grouped according to the size and shape of pair
1 (2n 5 diploid number; FN 5 fundamental number of autosomal arms).

Species 2n FN Locality Referencesa

First pair 1.5 larger than pair 2; acrocentric
Oligoryzomys sp. 1 46 52 Brazil 1
O. cf. messorius 56 58 Brazil 2
O. longicaudatus 56 64, 66 Argentina 3
O. longicaudatusb 56 66 Chile 4–6
O. delicatusc 60 72 Venezuela 7
O. eliurus 62 64, 66 Brazil 2
O. aff. eliurus 62 64 Brazil 8
O. fornesi 62–66 64–68 Paraguay 9
O. flavescens 60–66 66–70 Uruguay 10, 11
O. flavescens 64–67 66–70 d 2, 3, 11–13
O. cf. flavescens 66, 68 68, 70 Argentina 3
O. microtis 66 74 Brazil 2
O. longicaudatus var. 1 68 74 Peru 14
Oligoryzomys sp. 70 74 Brazil 2
First pair 1.5 larger than pair 2; biarmed
Oligoryzomys sp. 2 44, 45 52, 53 Brazil 1
O. magellanicuse 54 66 Chile 5, 6
O. microtisf 64 66 Peru 13–15
First 2–4 pairs of similar sizes
O. stramineus 52 68 Brazil 16
O. fulvescens 54 68 Costa Rica 14
O. fulvescens 60 74 Mexico 17
O. chacoensis 58 74 Paraguay 9
O. cf. longicaudatus 58 74 Argentina 3
O. andinus 60 70 Peru 14
O. destructorg 60 76 Peru 14, 15
O. longicaudatus var. 3 62 74 Venezuela 14
O. nigripes/delticola 61, 62 78–82 h 2, 3, 9, 11, 16, 18
a
1) Silva and Yonenaga-Yassuda (1997); 2) this work; 3) Espinosa and Reig (1991); 4) Gallardo and González (1977); 5)
Gallardo and Patterson (1985); 6) Gallardo and Palma (1990); 7) Kiblisky (1969); 8) Furtado (1981); 9) Myers and Carleton
(1981); 10) Brum (1965); 11) Brum-Zorrilla et al. (1988); 12) Sbalqueiro et al. (1991); 13) Aniskin and Volobouev (1999); 14)
Gardner and Patton (1976); 15) Musser and Carleton (1993); 16) Bonvicino and Weksler (1998); 17) Haiduk et al. (1979); 18)
Yonenaga et al. (1976).
b Described as Oryzomys longicaudatus philippii.

c Synonymized as Oligoryzomys fulvescens by Musser and Carleton (1993).

d Brazil, Bolivia, and Argentina.

e Described as Oryzomys longicaudatus magellanicus.

f The karyotype was reported as Oryzomys longicaudatus variant 2.

g The karyotype was reported as Oryzomys longicaudatus variant 4.

h Brazil, Paraguay, Uruguay, and Argentina.

Oligoryzomys cf. messorius.—Amazonian autosomal arms). The X chromosome was

specimens of O. cf. messorius (Fig. 1; Table
1) had 56 chromosomes, a karyotype hith-
erto not described in the genus. The 1st pair
was a large acrocentric, 2 pairs were small
metacentrics, and the other 24 pairs were
medium to small acrocentrics, resulting in
a fundamental number (FN) 5 58 (FN is
used herein to designate only the number of
a large submetacentric (between pairs 1 and
2 in size), and the Y chromosome was a
large metacentric (Fig. 2a). The C-bands
(heterochromatic material) were centromer-
ic in most of the chromosomes, including
the 1st pair. The short arm of the X chro-
mosome and the entire Y chromosome were
heterochromatic (Fig. 3a). One pair dis-
1084 JOURNAL OF MAMMALOGY Vol. 82, No. 4

FIG. 2.—Giemsa-stained karyotypes of a) Oligoryzomys cf. messorius, diploid number (2n) 5 56,
fundamental number (FN) 5 58, male; b) O. eliurus, 2n 5 62, FN 5 66, female (in the square,
acrocentric X and Y chromosomes); and c) O. microtis, 2n 5 66, FN 5 74.

played NOR-bands in the short arms (Table and Carleton (1993). The species we stud-
2). ied in the Amazon presents 2n 5 56, FN 5
Oligoryzomys messorius was considered 58 and belonged to species group type 1 of
as a synonym of O. fulvescens by Musser the Oligoryzomys karyotypes, in which the
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS 1085

FIG. 3.—The C-bands of a) Oligoryzomys cf. messorius, male; b) O. eliurus, male (in the square,
pair of sex chromosomes of a female); c) O. microtis (the X and Y chromosomes are below the
letters); and d) Oligoryzomys sp.
1086 JOURNAL OF MAMMALOGY
1st pair is 1.5 larger than pair 2 (Table 3).
However, O. fulvescens is chromosomally
quite distinct, presenting 2n 5 54, FN 5 68
in Costa Rica (Gardner and Patton 1976)
and 2n 5 60, FN 5 74 in Mexico (Haiduk
et al. 1979), and these karyotypes are in-
cluded in species group 3 (the first 2–4
pairs of similar size; see Table 3). The taxon
messorius was reported by Thomas (1901)
in the Kanuku Mountains, Guyana, about
150 km from the locality where we col-
lected our sample (Surumú, Roraima State;
Fig. 1). This geographic vicinity, allied to
the chromosome distinctiveness from ful-
vescens, suggests that the taxon of Surumú
may be cf. messorius.
Oligoryzomys nigripes.—We found 2n 5
62 in specimens of O. nigripes from several
places in the states of Bahia, Goiás, Espı́rito
Santo, Paraná, Santa Catarina, and Rio
Grande do Sul (Fig. 1). That karyotype pre-
sented FN 5 78, 80, 81, and 82. That var-
iation was due to pericentric inversions oc-
curring in pairs 3 and 4 (acrocentrics or
submetacentrics, with all combinations of
heterozygous and homozygous individuals;
Tables 1 and 2). Pair 2 was always biarmed,
but an inversion made it either subtelocen-
tric or submetacentric. The X chromosome
was a large metacentric, submetacentric, or
subtelocentric, and the Y chromosome, also
polymorphic, was a small acrocentric, a
medium metacentric, or a large submeta-
centric. The 2n 5 61 karyotype correspond-
ed to an XO female (Table 2). The C-bands
(data not shown) were pericentromeric and
seen only in some medium and small pairs.
The C-band was always absent in the 1st
pair. The short arm of the X chromosome
and the long arm of the Y chromosome
were heterochromatic. That same karyo-
type, with 2n 5 62 and the pericentric in-
version systems, was reported in specimens
from Paraguay by Myers and Carleton
(1981:16, figure 5) and from the states of
São Paulo and Rio de Janeiro, Brazil (Al-
meida and Yonenaga-Yassuda 1991); this
karyotype also was described in individuals
referred to as O. delticola from Uruguay
Vol. 82, No. 4
(Brum-Zorrilla et al. 1988) and Argentina
(Espinosa and Reig 1991). O. nigripes Ol-
fers, 1818 (an older name than delticola)
inhabits eastern Paraguay and northern Ar-
gentina, and O. delticola Thomas, 1917
presents a complementary distribution to it,
occurring in east-central Argentina, Uru-
guay, and southern Brazil (Musser and
Carleton 1993). These 2 taxa apparently
constitute a unique cytotaxonomic entity
(2n 5 62, FN 5 78–82), which we found
occupying a broad area of South America,
extending from northern Argentina to Par-
aguay and from Uruguay and southern Bra-
zil to the east on the coast to 158S (Southern
Bahia) and to the west to the Cerrado biome
in central Brazil.
Oligoryzomys eliurus.—The individuals
of O. eliurus, another species with 2n 5 62,
were collected at 4 localities of the Cerrado
biome (Fig. 1; Table 1). Two autosomal
conditions, FN 5 64 and 66, were ob-
served, both with a large acrocentric pair, a
medium submetacentric pair, a large poly-
morphic X chromosome (acrocentric or
subtelocentric), and a small acrocentric Y
chromosome. The FN 5 64 karyotype pre-
sented 27 acrocentric pairs of medium to
small sizes, and a medium metacentric pair.
The karyotype with FN 5 66 has 26 acro-
centric pairs of medium to small size and 2
pairs of small metacentrics; the Y chromo-
some was a submetacentric (Fig. 2b; Table
2). The C-bands occurred in the centromer-
ic regions of the majority of the autosomes
but were absent in the 1st pair. In the X
chromosome, the C-band (centromeric) var-
ied in size, and the Y chromosome proved
to be entirely heterochromatic (Fig. 3b).
The NORs were located in the short arms
of 1–3 pairs (Table 2).
From a chromosomal standpoint, 3 spe-
cies of Oligoryzomys presented 2n 5 62
and a low FN to 2n ratio: in Brazil in the
Cerrado (FN 5 64, 66—this work) and
Caatinga (FN 5 64, referred to as O. aff.
eliurus by Furtado 1981) biomes and in
Paraguay (FN 5 64, named O. fornesi by
Myers and Carleton 1981). Musser and
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS
Carleton (1993) later suggested that the kar-
yotype of O. fornesi from Paraguay would
correspond to that of O. microtis. These 3
taxa share a large acrocentric pair 1, 26–27
medium to small acrocentric pairs, and 2 or
3 pairs of medium to small biarmed ele-
ments (Table 3). They also have the same
polymorphic X and Y chromomosomes. We
collected our sample in the Brazilian Cer-
rado, a region within the proposed distri-
bution of O. eliurus (central and southeast-
ern Brazil—Musser and Carleton 1993).
At 1 of the localities (Ipameri) of the
Cerrado where O. eliurus was trapped, it
was sympatric with O. nigripes. Myers and
Carleton (1981) proposed that these 2 taxa
were subspecifically distinct. Nevertheless,
the karyotype of O. eliurus is quite different
from that of O. nigripes. Although it bears
the same diploid number (62), O. eliurus
shows autosomal arm numbers of 64 and
66, smaller than the 78–82 presented by O.
nigripes. Furthermore, in previous studies,
we verified that heterologous amplifications
of some microsatellite DNA loci of Mus
and Rattus showed bands that were species-
specific in several oryzomyine taxa (Lima-
Rosa et al. 2000). We performed this anal-
ysis with 11 microsatellite DNA heterolo-
gous primers in 10 O. nigripes and 7 O.
eliurus specimens. We found that all of the
O. nigripes individuals presented a 192-
base pair band (amplified by primer R65 of
rat, designed by Serikawa et al. 1992). The
occurrence of this band in only this species,
not having been seen in the other species
of the Oligoryzomys genus including O. eli-
urus, reinforces the distinction between
these 2 species.
Oligoryzomys flavescens.—In O. flaves-
cens, 2n varied from 64 to 67 and FN from
66 to 72 because of the occurrence of a sys-
tem of 0–3 accessory chromosomes (B-
chromosomes; Table 2). The Giemsa-
stained and C-banded karyotype, the same
as that described by Sbalqueiro et al. (1991:
196, figures 2A and 2C), basically was
composed of a large acrocentric pair, 28
pairs of medium to small acrocentrics, and
1087
2 or 3 small biarmed pairs. The B chro-
mosomes were small submetacentrics to
metacentrics. The X chromosome was a
medium submetacentric (between pairs 1
and 2 in size), and the Y chromosome was
a polymorphic medium subtelocentric to
submetacentric or a small metacentric. That
same basic karyotype also was reported in
Argentina, Uruguay, Bolivia, and in several
localities in southern Brazil (Aniskin and
Volobouev 1999; Brum-Zorrilla et al. 1988;
Sbalqueiro et al. 1991; Vidal-Rioja et al.
1988). That karyotype also was the same as
that of O. fornesi with 2n 5 64–66, which
was collected in Paraguay by Myers and
Carleton (1981). O. fornesi was originally
described by Massoia (1973), who noted its
close relationship to O. flavescens. Later,
based on the chromosomal identity, Sbal-
queiro et al. (1991) considered flavescens
and fornesi to be in the same cytotaxonomic
group. We found O. flavescens with O. ni-
gripes at 4 sites in southern Brazil (locali-
ties 10, 17, 22, and 26; Fig. 1).
Oligoryzomys microtis.—The species O.
microtis, trapped in the Amazon biome (lo-
cality 2, Fig. 1), showed 2n 5 66 and FN
5 74. This species presented a large acro-
centric pair, 26 medium to small acrocen-
trics, and 5 biarmed pairs. The X chromo-
some was a medium acrocentric to subtel-
ocentric (between pairs 2 and 3 in size), and
the Y chromosome was a small acrocentric
(Fig. 2c). The C-bands occurred in the cen-
tromeric regions of the majority of the au-
tosomes but were absent in the 1st pair. In
the X chromosome, the C-band was centro-
meric, and the entire Y chromosome was
heterochromatic (Fig. 3c). The NORs were
located in the short arms of 2 pairs. O. mi-
crotis, whose type locality is the lower So-
limões River in the Brazilian Amazon, is
distributed throughout central Brazil, south
of the Solimões–Amazon rivers, and in the
contiguous lowlands of Peru, Bolivia, Par-
aguay, and Argentina (Musser and Carleton
1993). O. microtis includes 2 chromosome
constitutions, 2n 5 66, FN 5 74 in Brazil
(this report) and 2n 5 64, FN 5 66 in Peru
1088 JOURNAL OF MAMMALOGY Vol. 82, No. 4

FIG. 4.—Oligoryzomys sp., diploid number (2n) 5 70, fundamental number (FN) 5 74: a) con-
ventional stained karyotype; b) G-banding; and c) NOR-bearing chromosomes.
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS
(Aniskin and Volobouev 1999). This last
karyotype also was described in Peru by
Gardner and Patton (1976) as O. longicau-
datus (variant 2). The main difference be-
tween these 2 cytotypes is a biarmed pair
1, a feature seen in individuals from Peru
that is absent in the Brazilian specimens.
Oligoryzomys sp.—Twenty-one speci-
mens of Oligoryzomys caught exclusively
in the Cerrado biome displayed 2n 5 70
and FN 5 74. The karyotype was com-
posed of a pair of large acrocentrics, 30
pairs of medium to small acrocentrics, 2
medium pairs of metacentrics, and a small
pair of metacentrics (Tables 1 and 2). The
X chromosome was a large subtelocentric
(between pairs 1 and 2 in size), and the Y
chromosome was a medium-sized subtelo-
centric (Giemsa staining, Fig. 4a; G-bands,
Fig. 4b). The C-bands were at the centro-
meres of the majority of the autosomes, in-
cluding the 1st pair, the 3 biarmed pairs,
and in the X chromosome. The Y chro-
mosome was entirely heterochromatic (Fig.
3d). This karyotype, which belonged to
species group type 1 (1st pair is 1.5 larger
than pair 2) has not been described previ-
ously for the genus Oligoryzomys and may
represent a new form or 1 of the several
forms included as synonyms in the current-
ly recognized species of central and western
Brazil.
The (T2AG3)n telomeric probes hybrid-
ized in situ in both the short and the long
arms of all pairs of chromosomes of the
species O. cf. messorius, O. eliurus, and
Oligoryzomys sp.; the hybridization signal
occurred with the same intensity in both
arms (data not shown). That band locali-
zation also was observed by Silva and
Yonenaga-Yassuda (1997) in the 2 unclas-
sified species of Oligoryzomys that they
studied with this technique.
The 26 taxa of genus Oligoryzomys kar-
yotyped to date are listed in Table 3. The
diploid numbers of the genus vary from 44
to 70, and 17 of the 26 taxa karyotyped
displayed a characteristic 1st pair, about
1089
50% larger than pair 2, with the majority
(12 of 17) being acrocentric.
Several authors found Oligoryzomys to
be a monophyletic genus (Carleton and
Musser 1989; Dickerman and Yates 1995;
Myers et al. 1995; Steppan 1995). But the
hierarchical relationships among its species
are controversial because the groups ar-
ranged by morphological characteristics
(Carleton and Musser 1989; Hershkovitz
1966; Myers and Carleton 1981; Olds and
Anderson 1987; Steppan 1995), polymor-
phism of proteins (Dickerman and Yates
1995), and polymorphism of DNA (Lima-
Rosa et al. 2000; Myers et al. 1995) differ.
The karyological data obtained in this work
and in the literature (Table 3) also assemble
the species of the genus in distinct groups.
ACKNOWLEDGMENTS
Conselho Nacional de Desenvolvimento Cien-
tı́fico e Tecnológico (CNPq), Financiadora de
Estudos e Projetos (FINEP), Fundação de Am-
paro à Pesquisa do Estado do Rio Grande do Sul
(FAPERGS), and Organization of the American
States (OAS) supported this study. We are grate-
ful to A. R. Langguth, D. A. Sana, J. L. P. Cor-
deiro, and J. R. Marinho for help in the field and
to L. S. Silva, B. A. Carvalho, and F. L. Hädrich
for technical support.
LITERATURE CITED
ALMEIDA, E. J. C., AND Y. YONENAGA-YASSUDA. 1991.
Pericentric inversion and sexual chromosome het-
eromorphisms in Oryzomys nigripes (Rodentia, Cri-
cetidae). Caryologia 44:63–73.
ANISKIN, V. M., AND V. T. VOLOBOUEV. 1999. Compar-
ative chromosome banding of two South-American
species of rice rats of the genus Oligoryzomys (Ro-
dentia, Sigmodontinae). Chromosome Research 7:
557–562.
BAKER, R. J., M. W. HAIDUK, L. W. ROBBINS, A. CAN-
DENA, AND B. F. KOOP. 1982. Chromosomal studies
of American bats and their systematic implications.
Pp. 303–327 in Mammalian biology in South Amer-
ica (M. A. Mares and H. H. Genoways, eds.). Spe-
cial Publications Series, Pymatuning Laboratory of
Ecology, University of Pittsburgh 6:1–539.
BANGS, O. 1900. List of the mammals collected in the
Santa Marta region of Colombia by W. W. Brown
Jr. Proceedings of the New England Zoology Club
1:87–102.
BONVICINO, C. R., AND M. WEKSLER. 1998. A new spe-
cies of Oligoryzomys (Rodentia, Sigmodontinae)
from northeastern and central Brazil. Zeistschrift für
Saügetierkunde 63:90–103.
1090 JOURNAL OF MAMMALOGY
BRUM, N. 1965. Investigaciones citogeneticas sobre al-
gunas especies de Cricetinae (Rodentia) del Uru-
guay. Annais II Congresso Latinoamericano de
Zoologia 2:315–320.
BRUM-ZORRILLA, N., T. G. FRONZA, R. WAINBERG, L.
VIDAL-RIOJA, AND N. ZWIRNER. 1988. Oryzomys fla-
vescens and O. delticola chromosomes (Rodentia,
Cricetidae) from Uruguay and Argentina. Caryolo-
gia 41:275–288.
CABRERA, A. 1961. Catalogo de los mamiferos de
America del Sur. Revista del Museo Argentino de
Ciencias Naturales 4:1–732.
CARLETON, M. D., AND G. G. MUSSER. 1989. System-
atic studies of oryzomyine rodents (Muridae, Sig-
modontinae): a synopsis of Microryzomys. Bulletin
of the American Museum of Natural History 191:1–
83.
CHIAPPERO, M. B., G. E. CALDERÓN, AND C. N. GAR-
DENAL. 1997. Oligoryzomys flavescens (Rodentia,
Muridae): gene flow among populations from cen-
tral-eastern Argentina. Genetica 101:105–113.
DICKERMAN, A. W., AND T. L. YATES. 1995. System-
atics of Oligoryzomys: protein-electrophoretic anal-
yses. Journal of Mammalogy 76:172–188.
EMMONS, L. H., AND F. FEER. 1990. Neotropical rain-
forest mammals: a field guide. The University of
Chicago Press, Chicago, Illinois.
ESPINOSA, M. B., AND O. A. REIG. 1991. Cytogenetics
and karyosystematics of South American oryzomy-
ine rodents (Cricetidae, Sigmodontinae). III. Band-
ing karyotypes of Argentinian Oligoryzomys. Son-
derdruck aus Zeistschrift für Säugetierkunde 56:
306–317.
FURTADO, V. V. 1981. Diversidade cromossômica em
roedores das famı́lias Cricetidae e Cavidae de Per-
nambuco, Brasil. Ph.D. dissertation, Universidade
Federal do Rio Grande do Sul, Porto Alegre, Brazil.
GALLARDO, M. H., AND L. A. GONZÁLEZ. 1977. Sex
chromosome polymorphism in Oryzomys longicau-
datus philippii (Rodentia, Cricetidae). Experientia
33:312–314.
GALLARDO, M. H., AND E. PALMA. 1990. Systematics
of Oryzomys longicaudatus (Rodentia: Muridae) in
Chile. Journal of Mammalogy 71:333–342.
GALLARDO, M. H., AND B. D. PATTERSON. 1985. Chro-
mosomal differences between two nominal subspe-
cies of Oryzomys longicaudatus Bennett. Mamma-
lian Chromosomes Newsletter 25:49–53.
GARDNER, A. L., AND J. L. PATTON. 1976. Karyotypic
variation in chromosomal evolution in the Neotrop-
ical cricetine complex. Occasional Papers, Museum
of Zoology, Louisiana State University 49:1–48.
HAIDUK, M. W., J. BICKHAN, AND D. J. SCHMIDLY. 1979.
Karyotypes of six species of Oryzomys from Mexico
and Central America. Journal of Mammalogy 60:
610–615.
HERSHKOVITZ, P. 1966. South American swamp and
fossorial rats of the scapteromyine group (Criceti-
nae, Muridae) with comments on the glans penis in
murid taxonomy. Sonderdruck aus Zeistschrift für
Saügetierkunde 31:81–149.
HONACKI, J. H., K. E. KINHAN, AND J. W. KOEPPL (EDS.).
1982. Mammal species of the world: a taxonomic
and geographic reference. Association of Systemat-
ics Collections, University of Kansas, Lawrence.
Vol. 82, No. 4
HOWELL, W. M., AND D. A. BLACK. 1980. Controlled
silver-staining of nucleolar organizer regions with
protective colloidal developer: a 1-step method. Ex-
perientia 36:1014.
KIBLISKY, P. 1969. The chromosomes of two species
of the genus Oryzomys (Rodentia: Cricetidae). Ex-
perientia 25:1338–1339.
LIMA-ROSA, C. A. V., M. H. HUTZ, L. F. B. OLIVEIRA,
J. ANDRADES-MIRANDA, AND M. S. MATTEVI. 2000.
Heterologous amplification of microsatellite loci
from mouse and rat in oryzomyine and thomaso-
myine South American rodents. Biochemical Genet-
ics 38:97–108.
LOVE, J. M., A. M. KNIGHT, M. A. MCALEER, AND J.
A. TODD. 1990. Towards construction of a high res-
olution map of the mouse genome using PCR-ana-
lysed microsatellites. Nucleic Acids Research 18:
4123–4130.
MASSOIA, E. 1973. Descripción de Oryzomys fornesi,
nueva espécie y nuevos datos sobre algunas espécies
y subespécies argentinas del subgénero Oryzomys
(Oligoryzomys) (Mammalia–Rodentia–Cricetidae).
Revista de Investigaciones Agropecuarias, Instituto
Nacional de Tecnologı́a Agropecuaria, Serie 1, Biol-
ogı́a y Producción Animal 10:21–37.
MUSSER, G. G., AND M. D. CARLETON. 1993. Family
Muridae. Pp. 501–755 in Mammal species of the
world: a taxonomic and geographic reference. 2nd
ed. (D. E. Wilson and D. M. Reeder, eds.). Smith-
sonian Institution Press, Washington, D.C.
MYERS, P., AND M. D. CARLETON. 1981. The species of
Oryzomys (Oligoryzomys) in Paraguay and the iden-
tity of Azara’s ‘‘Rat sixième ou Rat à Tarse Noir.’’
Miscellaneous Publications, University of Michigan
161:1–41.
MYERS, P., B. LUNDRIGAN, AND P. K. TUCKER. 1995.
Molecular phylogenetics of oryzomyine rodents: the
genus Oligoryzomys. Molecular Phylogenetics and
Evolution 4:372–382.
OLDS, N., AND S. ANDERSON. 1987. Notes on Bolivian
mammals. 2. Taxonomy and distribution of rice rats
of the subgenus Oligoryzomys. Fieldiana: Zoology,
New Series 39:261–281.
PATTON, J. L., M. N. F. SILVA, AND J. R. MALCOLM.
1996. Hierarchical genetic structure and gene flow
in three sympatric species of Amazonian rodents.
Molecular Ecology 5:229–238.
POWERS, A. M., ET AL. 1999. Isolation and genetic
characterization of a hantavirus (Bunyaviridae: Han-
tavirus) from a rodent, Oligoryzomys microtis (Mu-
ridae), collected in northeastern Peru. American
Journal of Tropical Medicine and Hygiene 61:92–
98.
SANTOS, J., P. DE CASTRO, M. HERRANZ, AND J.
FERNÁNDEZ-PIQUEIRAS. 1995. Eight new polymor-
phic microsatellites in mouse gene loci. Cytogenet-
ics and Cell Genetics 71:223–224.
SBALQUEIRO, I. J., M. S. MATTEVI, L. F. B. OLIVEIRA,
AND M. J. V. SOLANO. 1991. B chromosome system
in populations of Oryzomys flavescens (Rodentia,
Cricetidae) from southern Brazil. Acta Theriologica
36:193–199.
SEABRIGHT, M. 1971. A rapid banding technique for
human chromosomes. Lancet 2:971–972.
SERIKAWA, T., ET AL. 1992. Rat gene mapping using
November 2001 ANDRADES-MIRANDA ET AL.—CHROMOSOMES OF OLIGORYZOMYS
PCR-analyzed microsatellites. Genetics 131:701–
721.
SILVA, M. J. DE J., AND Y. YONENAGA-YASSUDA. 1997.
New karyotypes of two related species of Oligory-
zomys genus (Cricetidae, Rodentia) involving centric
fusion with loss of NORs and distribution of telo-
meric (TTAGGG)n sequences. Hereditas 121:217–
229.
STEPPAN, S. J. 1995. Revision of the tribe Phyllotini
(Rodentia: Sigmodontinae) with a phylogenetic hy-
pothesis for the Sigmodontinae. Fieldiana: Zoology,
New Series 80:1–112.
SUMNER, A. T. 1972. A simple technique for demon-
strating centromeric heterochromatin. Experimental
Cell Research 75:304–306.
TATE, G. H. H. 1932. The taxonomic history of the
South and Central American cricetid rodents of the
genus Oryzomys. Part 2: subgenera Oligoryzomys,
Thallomyscus and Melanomys. American Museum
Novitates 580:1–17.
THOMAS, O. 1901. On a collection of mammals from
the Kanuku Mountains, British Guiana. Annals and
Magazine of Natural History, Series 7 8:139–154.
VIDAL-RIOJA, L., T. G. FRONZA, R. WAINBERG, N.
BRUM-ZORRILLA, F. WALLACE, AND A. ZAMBELLI.
1988. C-banding pattern and satellite DNA locali-
zation on the chromosomes of Oryzomys flavescens
(Rodentia, Cricetidae). Caryologia 41:323–328.
YONENAGA, Y., O. FROTA-PESSOA, S. KASHARA, AND E.
J. C. ALMEIDA. 1976. Cytogenetic studies on Brazil-
ian rodents. Ciência e Cultura 28:202–211.
Submitted 15 May 2000. Accepted 5 February 2001.
Associate Editor was Meredith J. Hamilton.
APPENDIX I
Voucher specimens (Brazil).—Oligoryzomys
stramineus: UFPB1824–1827, 1836, 1837
(Mambaı́, GO, 148299S, 468069W); Oligoryzo-
mys cf. messorius: MN37750–37753 (Surumú,
RR, between 038589–048279N and 608139–
618169W); Oligoryzomys nigripes: MN37488–
37500 (Ipameri, Caldas Novas, and Corumbaı́ba,
GO, between 178419–178569S and 488289–
488329W), MN37501 (Parque Estadual do Tur-
vo, Derrubadas, RS, between 278–278209S and
538409–548109W), MN37502–37504 (Aratiba,
RS, 278239S, 528189W), MN37505–37511 (Ar-
acuri Ecological Station, Muitos Capões, RS,
288139S, 518109W), MN37512 (Ivaı́, Tupancire-
tã, RS, 288579S, 538409W), MN37513 (Caxias
do Sul, RS, 298109S, 518109W), MN37514–
37528 (Tainhas, RS, 298169S, 508189W),
MN37529–37531 (São Francisco de Paula, RS,
298279S, 508359W), MN37532–37538 (Char-
1091
queadas, RS, 298579S, 518379W), MN37539–
37574 (Picada Verão and Alto Ferrabraz, Sapi-
ranga, RS, 298389S, 518009W), MN37575–37578
(Riozinho, RS, 298389S, 508279W), MN37579–
37604 (Faxinal, Torres, RS, 298209S, 498459W),
MN37605 (Rio Jacuı́, Eldorado do Sul, RS,
308059S, 518369W), MN37606 (Belém Novo,
RS, 308089S, 518109W), MN37607–37622 (Osó-
rio, RS, 298539S, 508169W), MN37623 (Traman-
daı́ Lagoon, Tramandaı́, RS, 298599S, 508089W),
MN37624, MN37625 (Quintão, RS, 308209S,
508169W), MN37626–37630 (northern Tapes
Bay, Tapes, RS, 308409S, 518239W), MN37631–
37659 (Capão do Leão, Mostardas, RS, 318109S,
508569W), MN37660–37682 (Taim Ecological
Station, Rio Grande, RS, 328329S, 528329W),
MN37683 (Costa de Dentro, Santa Catarina Is-
land, SC, 278469S, 488319W), MN37684–37690
(Concórdia, SC, 278149S, 528019W), MN37691–
37693 (Parque Nacional de Iguaçu, PR, 258309S,
548309W), UFPB354, UFPB355, UFPB357–361
(Monte Verde, ES, 198039S, 418579W),
UFPB428, UFPB429 (Rio de Una, 10 km ESE
São José, BA, 158069S, 398169W); Oligoryzomys
eliurus: MN35992 (55 km N Niquelândia, GO,
148289S, 488279W), MN36746 (40 km SW Min-
açú, GO, 138319S, 488139W), MN36928,
MN37258, MN37347 (40 km NE Uruaçú, GO,
148319S, 498089W), MN37694–37696 (Ipameri,
Caldas Nova, and Corumbaı́ba, GO, between
178419–178569S and 488289–488329W); Oligory-
zomys flavescens: MN37697 (Nonoai, RS,
278259S, 538049W), MN37698–37720 (Tainhas,
RS, 298169S, 508189W), MN37721–37747
(Charqueadas, RS, 298579S, 518379W),
MN37748 (Quintão, RS, 308209S, 508169W),
MN37749 (Costa de Dentro, Santa Catarina Is-
land, SC, 278469S, 488319W); Oligoryzomys mi-
crotis: MN37754–37759 (Fazenda São Bento,
Tartarugalzinho, AP, 018179N, 508489W); Oli-
goryzomys sp.: MN35967, MN36061,
MN36082, MN36083, MN36145, MN36147,
MN36161 (55 km N Niquelândia, GO, 148289S,
488279W), MN36220, MN36224, MN36234,
MN36242, MN36345, MN36356, MN36357,
MN36367, MN36426, MN36433, MN36438 (20
km NW Colinas do Sul, GO, 148099S, 488049W),
MN36832 (40 km SW Minaçú, GO, 138319S,
488139W), MN37282, MN37441 (40 km NE
Uruaçú, GO, 148319S, 498089W).