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Andrades-Miranda - Chromosomes Studies of Seven Species of Oligoryzomys From Brazil
Transcript of Andrades-Miranda - Chromosomes Studies of Seven Species of Oligoryzomys From Brazil
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ANDRADES-MIRANDA ET AL.CHROMOSOMES OF OLIGORYZOMYS November 2001 1081
FIG. 1.Collection sites (coordinates given in Appendix I): 1) Surumu, Roraima State (RR); 2)
Fazenda Sao Bento, Tartarugalzinho, Amapa State (AP); 3) including the localities: 40 km SW
Minacu, 55 km N Niquelandia, 20 km NW Colinas do Sul, and 40 km NE Uruacu; 4) Mamba, and
5) Ipameri, Caldas Novas, and Corumbaba, Goias State (GO); 6) Rio de Una, 10 km ESE Sao Jose,
Bahia State (BA); 7) Monte Verde, Esprito Santo State (ES); 8) Parque Nacional de Iguacu, Parana
State (PR); 9) Concordia, 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 Capoes, 15) Iva, Tupancireta, 16) Caxias do Sul, 17) Tainhas, 18) Faxinal, Torres, 19) Sao
Francisco de Paula, 20) Riozinho, 21) Picada Verao and Alto Ferrabraz, Sapiranga, 22) Charqueadas,
23) including 2 localities: Rio Jacu, Eldorado do Sul, and Belem Novo, 24) Osorio, 25) Tramanda
Lagoon, Tramanda, 26) Quintao, 27) northern Tapes Bay, Tapes, 28) Capao do Leao, 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 ofthis 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 01N to 32S 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, Joao Pes-
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TABLE 1.Localities and number (n) of Oli-
goryzomys specimens analyzed.
Species Localitiesa n
O. stramineusO. cf. messorius
O. nigripes
O. eliurus
O. flavescens
O. microtis
Oligoryzomys sp.
41
511, 1329
3, 5
10, 12, 17, 22, 26
2
3
74
207
8
59
6
21
a Numbers correspond to those in Fig. 1.
TABLE 2.Diploid number (2n) and autosomal arm fundamental number (FN), X- and Y-chro-
mosome morphologies, and NOR-band patterns of Oligoryzomys.
Species 2n FN X Y
NOR
(pairs)
O. stramineus
O. cf. messorius
O. nigripes
O. eliurusO. flavescens
O. microtis
Oligoryzomys sp.
52
56
61, 62
626467
66
70
68
58
78, 8082
64, 666668
74
74
SMa
SM
M
A/STd
SM/M
A
A/ST
Mb
SM
Ac
A/SMA
A
A
1
13
2
25
a Submetacentric.b Metacentric.c Acrocentric.d Subtelocentric.
soa (UFPB). Voucher specimen numbers are
given in Appendix I.
Mitotic preparations were made employing the
technique of Baker et al. (1982). The C-, G-, and
NOR-banding were performed following themethods of Sumner (1972), Seabright (1971), and
Howell and Black (1980), respectively. The fluo-
rescent in situ hybridization process with the telo-
meric sequence (T2AG3)n was applied to speci-
mens of Oligoryzomys cf. messorius, O. eliurus,
and Oligoryzomys sp., with the all human telo-
meres probe (Oncor, Gaithersburg, Maryland)
stained with digoxygenin according to the man-
ufacturers protocol.
Eleven sets of microsatellite DNA primers de-
signed for Rattus (R12, R47, R65, R69, R75,
and R97Serikawa et al. 1992) and Mus (M13,
M23, and M49Love et al. 1990; and ATP and
KRTSantos et al. 1995) were amplified byheterologous polymerase chain reaction in O.
eliurus and O. nigripes, as described in Lima-
Rosa et al. (2000).
RESULTS AND DISCUSSION
The 7 species analyzed displayed diploid
numbers from 52 to 70. The diploid number
of 70 that we found in Oligoryzomys sp. is
the highest number reported to in the genus,
verified in 1 of the 3 undescribed karyo-
types we report in this paper (Table 2).
Oligoryzomys stramineus.Seven O.
stramineus (Tables 1 and 2) showed 2n
52, with 9 biarmed and 16 acrocentric au-
tosome pairs. The X chromosome was a
large submetacentric, between pairs 3 and
4 in size, and the Y chromosome was a me-
dium-sized metacentric. The C-bands (data
not shown) were centromeric in the major-
ity of the autosomes (but were absent in the
1st pair) and of the X chromosome. The Ychromosome was entirely heterochromatic.
The karyotype of O. stramineus could be
included in species group 3 (the first 24
pairs of similar size, according the classi-
fication we made of the Oligoryzomys spe-
cies based in the size and shape of its pair
1, see Table 3). That same Giemsa karyo-
type was reported by Bonvicino and Wek-
sler (1998:94, figure 2) in the type series of
O. stramineus, a new species that they de-
scribed. Mamba (Goias State; Fig. 1), from
which our sample came, was located inside
the distribution area proposed for this spe-cies (Cerrado of northern Goias and Minas
Gerais states and Caatinga of the states of
Paraiba and Pernambuco).
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ANDRADES-MIRANDA ET AL.CHROMOSOMES OF OLIGORYZOMYS November 2001 1083
TABLE 3.Karyotyped species of Oligoryzomys grouped according to the size and shape of pair
1 (2n diploid number; FN fundamental number of autosomal arms).
Species 2n FN Locality Referencesa
First pair 1.5 larger than pair 2; acrocentricOligoryzomys sp. 1
O. cf. messorius
O. longicaudatus
O. longicaudatusb
O. delicatusc
O. eliurus
O. aff. eliurus
O. fornesi
O. flavescens
O. flavescens
O. cf. flavescens
O. microtis
O. longicaudatus var. 1
Oligoryzomys sp.
46
56
56
56
60
62
62
6266
6066
6467
66, 68
66
68
70
52
58
64, 66
66
72
64, 66
64
6468
6670
6670
68, 70
74
74
74
Brazil
Brazil
Argentina
Chile
Venezuela
Brazil
Brazil
Paraguay
Uruguayd
Argentina
Brazil
Peru
Brazil
1
2
3
4 6
7
2
8
9
10, 11
2, 3, 1113
3
2
14
2
First pair 1.5 larger than pair 2; biarmed
Oligoryzomys sp. 2
O. magellanicuse
O. microtisf
44, 45
54
64
52, 53
66
66
Brazil
Chile
Peru
1
5, 6
1315
First 24 pairs of similar sizes
O. stramineus
O. fulvescens
O. fulvescens
O. chacoensis
O. cf. longicaudatus
O. andinus
O. destructorg
O. longicaudatus var. 3
O. nigripes/delticola
52
54
60
58
58
60
60
62
61, 62
68
68
74
74
74
70
76
74
7882
Brazil
Costa Rica
Mexico
Paraguay
Argentina
Peru
Peru
Venezuelah
16
14
17
9
3
14
14, 15
14
2, 3, 9, 11, 16, 18
a 1) Silva and Yonenaga-Yassuda (1997); 2) this work; 3) Espinosa and Reig (1991); 4) Gallardo and Gonzalez (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
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) 58 (FN is
used herein to designate only the number of
autosomal arms). The X chromosome was
a large submetacentric (between pairs 1 and
2 in size), and the Y chromosome was alarge 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-
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FIG. 2.Giemsa-stained karyotypes of a) Oligoryzomys cf. messorius, diploid number (2n) 56,
fundamental number (FN)
58, male; b) O. eliurus, 2n
62, FN
66, female (in the square,acrocentric X and Y chromosomes); and c) O. microtis, 2n 66, FN 74.
played NOR-bands in the short arms (Table
2).
Oligoryzomys messorius was considered
as a synonym of O. fulvescens by Musser
and Carleton (1993). The species we stud-
ied in the Amazon presents 2n 56, FN
58 and belonged to species group type 1 of
the Oligoryzomys karyotypes, in which the
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ANDRADES-MIRANDA ET AL.CHROMOSOMES OF OLIGORYZOMYS November 2001 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.
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1st pair is 1.5 larger than pair 2 (Table 3).
However, O. fulvescens is chromosomally
quite distinct, presenting 2n 54, FN 68
in Costa Rica (Gardner and Patton 1976)
and 2n 60, FN 74 in Mexico (Haiduket al. 1979), and these karyotypes are in-
cluded in species group 3 (the first 24
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 (Surumu, Roraima State;
Fig. 1). This geographic vicinity, allied to
the chromosome distinctiveness from ful-
vescens, suggests that the taxon of Surumu
may be cf. messorius.
Oligoryzomys nigripes.We found 2n
62 in specimens of O. nigripes from several
places in the states of Bahia, Goias, Esprito
Santo, Parana, Santa Catarina, and Rio
Grande do Sul (Fig. 1). That karyotype pre-
sented FN 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, orsubtelocentric, and the Y chromosome, also
polymorphic, was a small acrocentric, a
medium metacentric, or a large submeta-
centric. The 2n 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 62 and the pericentric in-
version systems, was reported in specimensfrom Paraguay by Myers and Carleton
(1981:16, figure 5) and from the states of
Sao 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
(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, 1917presents 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 62, FN 7882), 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 15S (Southern
Bahia) and to the west to the Cerrado biome
in central Brazil.
Oligoryzomys eliurus.The individuals
of O. eliurus, another species with 2n 62,
were collected at 4 localities of the Cerrado
biome (Fig. 1; Table 1). Two autosomal
conditions, FN 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 64 karyotype pre-
sented 27 acrocentric pairs of medium to
small sizes, and a medium metacentric pair.
The karyotype with FN
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 13 pairs (Table 2).
From a chromosomal standpoint, 3 spe-
cies of Oligoryzomys presented 2n 62and a low FN to 2n ratio: in Brazil in the
Cerrado (FN 64, 66this work) and
Caatinga (FN 64, referred to as O. aff.
eliurus by Furtado 1981) biomes and in
Paraguay (FN 64, named O. fornesi by
Myers and Carleton 1981). Musser and
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ANDRADES-MIRANDA ET AL.CHROMOSOMES OF OLIGORYZOMYS November 2001 1087
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, 2627
medium to small acrocentric pairs, and 2 or3 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 BrazilMusser 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 ofO. 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 7882 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 03 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
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 wasa 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 6466, 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 66 and FN
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-
limoes River in the Brazilian Amazon, is
distributed throughout central Brazil, southof the SolimoesAmazon rivers, and in the
contiguous lowlands of Peru, Bolivia, Par-
aguay, and Argentina (Musser and Carleton
1993). O. microtis includes 2 chromosome
constitutions, 2n 66, FN 74 in Brazil
(this report) and 2n 64, FN 66 in Peru
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FIG. 4.Oligoryzomys sp., diploid number (2n) 70, fundamental number (FN) 74: a) con-
ventional stained karyotype; b) G-banding; and c) NOR-bearing chromosomes.
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ANDRADES-MIRANDA ET AL.CHROMOSOMES OF OLIGORYZOMYS November 2001 1089
(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 pair1, 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 70
and FN 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 Ychromosome 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 theystudied 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
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-
tfico e Tecnologico (CNPq), Financiadora de
Estudos e Projetos (FINEP), Fundacao de Am-
paro a 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. Hadrich
for technical support.
LITERATURE CITED
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ANISKIN, V. M., AND V. T. VOLOBOUEV. 1999. Compar-ative chromosome banding of two South-Americanspecies of rice rats of the genus Oligoryzomys (Ro-dentia, Sigmodontinae). Chromosome Research 7:557562.
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Santa Marta region of Colombia by W. W. BrownJr. Proceedings of the New England Zoology Club1:87102.
BONVICINO, C. R., AND M. W EKSLER. 1998. A new spe-cies of Oligoryzomys (Rodentia, Sigmodontinae)from n ortheastern and central Brazil. Zeistschrift furSaugetierkunde 63:90 103.
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Submitted 15 May 2000. Accepted 5 February 2001.
Associate Editor was Meredith J. Hamilton.
APPENDIX I
Voucher specimens (Brazil).Oligoryzomys
stramineus: UFPB18241827, 1836, 1837(Mamba, GO, 1429S, 4606W); Oligoryzo-
mys cf. messorius: MN3775037753 (Surumu,
RR, between 03580427N and 6013
6116W); Oligoryzomys nigripes: MN37488
37500 (Ipameri, Caldas Novas, and Corumbaba,
GO, between 17411756S and 4828
4832W), MN37501 (Parque Estadual do Tur-
vo, Derrubadas, RS, between 272720S and
53405410W), MN3750237504 (Aratiba,
RS, 2723S, 5218W), MN3750537511 (Ar-
acuri Ecological Station, Muitos Capoes, RS,
2813S, 5110W), MN37512 (Iva, Tupancire-
ta, RS, 2857S, 5340W), MN37513 (Caxias
do Sul, RS, 2910S, 5110W), MN3751437528 (Tainhas, RS, 2916S, 5018W),
MN3752937531 (Sao Francisco de Paula, RS,
2927S, 5035W), MN3753237538 (Char-
queadas, RS, 2957S, 5137W), MN37539
37574 (Picada Verao and Alto Ferrabraz, Sapi-
ranga, RS, 2938S, 5100W), MN3757537578
(Riozinho, RS, 2938S, 5027W), MN37579
37604 (Faxinal, Torres, RS, 2920
S, 49
45
W),
MN37605 (Rio Jacu, Eldorado do Sul, RS,
3005S, 5136W), MN37606 (Belem Novo,
RS, 3008S, 5110W), MN3760737622 (Oso-
rio, RS, 2953S, 5016W), MN37623 (Traman-
da Lagoon, Tramanda, RS, 2959S, 5008W),
MN37624, MN37625 (Quintao, RS, 3020S,
5016W), MN3762637630 (northern Tapes
Bay, Tapes, RS, 3040S, 5123W), MN37631
37659 (Capao do Leao, Mostardas, RS, 3110S,
5056W), MN3766037682 (Taim Ecological
Station, Rio Grande, RS, 3232S, 5232W),
MN37683 (Costa de Dentro, Santa Catarina Is-
land, SC, 2746S, 4831W), MN3768437690
(Concordia, SC, 2714
S, 52
01
W), MN37691
37693 (Parque Nacional de Iguacu, PR, 2530S,
5430W), UFPB354, UFPB355, UFPB357361
( Mont e Ver de, ES, 1903S, 4157W),
UFPB428, UFPB429 (Rio de Una, 10 km ESE
Sao Jose, BA, 1506S, 3916W); Oligoryzomys
eliurus: MN35992 (55 km N Niquelandia, GO,
1428S, 4827W), MN36746 (40 km SW Min-
acu, GO, 1331S, 4813W), MN36928,
MN37258, MN37347 (40 km NE Uruacu, GO,
1431S, 4908W), MN3769437696 (Ipameri,
Caldas Nova, and Corumbaba, GO, between
17411756S and 48284832W); Oligory-
zomys flavescens: MN37697 (Nonoai, RS,
2725S, 5304W), MN3769837720 (Tainhas,RS, 2916S, 5018W), MN3772137747
(Ch arqu ea da s, R S, 2 957S, 5137W),
MN37748 (Quintao, RS, 3020S, 5016W),
MN37749 (Costa de Dentro, Santa Catarina Is-
land, SC, 2746S, 4831W); Oligoryzomys mi-
crotis: MN3775437759 (Fazenda Sao Bento,
Tartarugalzinho, AP, 0117N, 5048W); Oli-
goryzomys sp.: MN3 59 67, MN3 60 61 ,
MN36082, MN36083, MN36145, MN36147,
MN36161 (55 km N Niquelandia, GO, 1428S,
4827W), MN36220, MN36224, MN36234,
MN36242, MN36345, MN36356, MN36357,
MN36367, MN36426, MN36433, MN36438 (20
km NW Colinas do Sul, GO, 1409S, 4804W),MN36832 (40 km SW Minacu, GO, 1331S,
4813W), MN37282, MN37441 (40 km NE
Uruacu, GO, 1431S, 4908W).