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of the
FLORIDA STATE MUSEUM
Biological Sciences
Volume 34 1988 Numbers 3 and 4
BIOLOGY AND NATURAL HISTORY
OF BRAZILIAN ATLANTIC FOREST
SMALL MAMMALS
Gustavo A.B. da Fonseca
Maria Cecilia M. Kierulff
SMALL MAMMAL INVENTORIES
IN AN EASTERN BRAZILIAN PARK
Jody R. Stallings
UNIVERSITY OF FLORIDA
GAINESVILLE
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PREFACE
The contributions from Drs. Fonseca and Stallings, published in this issue
of the Bulletin, allow us a glimpse into a little-known biogeographic province
that is currently threatened. The Atlantic Rain Forest of Brazil has a unique
flora and fauna. Currently, it is isolated from the Amazonian tropical forest by
the drier zones comprising the catinga, cerrado, and the chaco. Endemism is
high in the Atlantic Rain Forest, and although plant communities have been
studied in recent years, studies on higher vertebrates have lagged. Indeed, the
last major study of small mammals in the area was published in 1944. Drs.
Fonseca and Stallings have made a major contribution to our understanding of
small mammals in this unique habitat.
The two studies complement one another. Fonseca concentrates on the
manner in which rainfall affects the timing of reproduction by pulsing the
primary productivity. He nicely demonstrates that in this tropical forest there
is a great deal of temporal variation in reproduction, activity, and feeding
habits within small mammal communities.
Stallings provides a great deal of basic data on the poorly known small
mammal fauna in this portion of the Atlantic Rain Forest. Especially valuable
are the quantitative data on measurements and weights. Of special interest in
both papers are the evaluations of trapping techniques. Trap success varied
widely depending on not only the nature of the habitat but whether sets were
made arboreally or terrestrially. It is also evident from the work by Stallings
that some habitat specialization is demonstrable. Grasslands yielded the
lowest species richness, whereas forests of intermediate disturbance had not
only high densities of some species but a greater species richness. Taken
together, these papers offer a valuable insight into a little-studied area of the
globe.
John F. Eisenberg
Ordway Professor of
Ecosystem Conservation
BIOLOGY AND NATURAL HISTORY OF BRAZILIAN
ATLANTIC FOREST SMALL MAMMALS
Gustavo A. B. da Fonseca and Maria Cecilia M. Kierulff*
ABSTRACT
During a 17-month study, 20 small mammal species were recorded in the forests of the
western slopes of the Brazilian Atlantic coastal region in the state of Minas Gerais. A trapping
effort of 57,120 trap nights resulted in 1366 captures of 692 individuals belonging to 8 marsupial
and 12 rodent species. Both terrestrial and arboreal traps were used.
The common opossum Didelphis marsupialis was the most frequently trapped small mammal,
followed by Marmosa incana. The spiny rat Proechimys setosus was the third most common small
mammal and the most abundant rodent species. One marsupial and five rodent species were
considered rare in this study, being represented in the sample by two or fewer individuals.
Population turnover at the traplines was high for all species, with most individuals only appearing
once in the total study sample.
Average body weight for the largest species, Didelphis marsupialis, was close to 1000 g, while
for the smallest species, Oryzomys nigripes, it was approximately 20 g. Sexual dimorphism was
common among marsupial species, but rare in rodents. Male marsupials, on average, tended to
be larger than females. Male Oryzomys trinitatis, on the other hand, were slightly smaller than
females.
Most marsupials are seasonal breeders, while rodents tend to reproduce throughout the year.
The western slopes of the Atlantic forest are characterized by a pronounced dry season, and
reproduction is concentrated in late dry and the early and midwet season. Seasonality of
marsupial reproduction was recognized not only by the presence of breeding males and females,
but also by juvenile recruitment into the population in subsequent months.
The vast majority of small mammal species have demonstrated a high degree of overlap in
substrate use. A large number of small mammals have some level of scansorial ability, even the
ones which are more frequently caught at the forest floor. It is also suspected that most species
have mixed diets. Therefore, potential competition for resources is a definite possibility.
* The senior author, Dr. Fonseca, is in the Departamento de Zoologia, Instituto de Ciencias Biologicas, Universidade Federal
de Minas Gerais, Belo Horizonte, M.G. 30000, Brazil.
da Fonseca, GA.B., and M.C.M. Kierulff. 1989. Biology and Natural History of Brazilian
Atlantic Forest Small Mammals. Bull. Florida State Mus., Biol. Sci. 34(3):99-152.
100 BULLETIN FLORIDA STATE MUSEUM 34(3)
RESUMO
Durante um period de 17 meses consecutivos de levantamento, vinte especies de pequenos
mamiferos foram registradas nas florestas da regiio ocidental da Mata Atlintica Brasileira, no
estado de Minas Gerais. Um esforqo de capture de 57.120 armadilhas-noite resultou em um total
de 1.366 captures de 692 individuos de oito espdcies de marsupiais e doze de roedores. Fez-se
uso tanto de armadilhas ferrestres quanto de arb6reas.
O gambd comum Didelphis marsupialis foi o pequeno mamffero mais frequentemente
capturado durante o estudo, seguido por Marmosa incana. 0 rato-de-espinho Proechimys setosus
foi a esp6cie mais comum de roedor capturada neste estudo. Uma especie de marsupial e cinco
de roedores foram consideradas raras, sendo representadas na amostra por, no miximo, dois
individuos. A rotatividade de individuos nas linhas de capture foi bastante alta para quase todas
as especies, sendo que a maioria dos individuos foram registrados uma s6 vez no total da amostra
deste estudo.
A mddia de peso corporal para a maior das esp6cies, Didelphis marsupialis, foi de
aproximadamente 1.000 gramas, sendo que para a menor esp6cie, Oryzomys nigripes, a media de
peso esteve pr6xima de 20 gramas. A maioria das esp6cies de marsupiais mostrou dimorfismo
sexual, uma caracteristica rara entire roedores. Os machos das especies de marsupials tendem a
ser, em m6dia, mais pesados e maiores do que as femeas. Por outro lado, os machos de Oryzomys
trinitatis sio um pouco menores do que as f6meas.
As atividades reprodutivas da maioria dos marsupiais sio sazonais, enquanto que os
roedores se reproduzem ao long de todo o ano. As encostas ocidentais da Mata Atlantica sio
caracterizadas por uma estagio seca pronunciada, e a reproducao de pequenos mamiferos estA
concentrada no final da estacio seca e no inicio e meio da estacio chuvosa. A ocorr8ncia de
reprodugSo sazonal em marsupials foi determinada pela observa~io de machos e femeas em
condidlo reprodutiva e pelo recrutamento de jovens na populacio em meses subsequentes.
A grande maioria das espdcies de pequenos mamiferos mostrou superposiqco no uso de
substratos para locomoFio, utilizando-se tanto de substratos arb6reos quanto do solo das matas.
Um grande numero de espdcies demonstra habilidade escansorial, mesmo aquelas que
locomovem-se mais frequentemente no solo. Suspeita-se tamb6m que a maioria dos pequenos
mamiferos possuem dietas mixtas, ocorrendo superposicio de varios itens alimenticios. Existe a
possibilidade, portanto, de ocorrencia de competicgo por recursos entire estas especies de
pequenos mamiferos.
TABLE OF CONTENTS
Introduction........................................................................................... ............................................ 101
A know ledgem ent .......................................................................................... ........................... ....... 102
M materials and M ethods................................................................................. ................................... 103
Study Sites....................................................................................... ....................................... 103
Clim ate.................................................................................................. ............... 106
T rapping ............................................................................................. ........... .................. 107
Results and Species A ccounts....................................................................... ........... ............... 108
D iscussion................................................................................................................................................. 125
Seasonality and Resource Use ............................................ ........... ............ 125
Life H history Patterns ....................................................................... ............... .............. 128
Population T urnover................................................................................................................... 129
Literature C ited....................................................................... ...................... .. ....................... 130
Appendix I .................................................................. 134
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 101
INTRODUCTION
The neotropical region encompasses some of the most threatened
ecosystems in the world, and yet the mammalian fauna of this area still
remains very poorly known (Mares and Genoways 1982). In South America,
the Brazilian Atlantic forest has been the vegetation formation subjected to the
highest rate of destruction, with less than 5% of the region retaining some
form of forest cover (Fonseca 1985a), and probably less than 1% in
undisturbed state (Mittermeier et al. 1982). Nonetheless, the few natural
history studies conducted on its fauna have indicated that species diversity is
quite high, with many faunal elements being unique to the region (Mello-
Leitao 1946; Muller 1973; Fonseca, unpublished data). The pioneer works of
Moojen (1952), Vieira (1955), and Cabrera (1957; 1961) provide a general data
base indicating that there are at least 129 species of non-volant mammals in the
Atlantic forest region, about 40% of which are endemic. Were the taxonomy
of most of the groups better understood, other species would probably be
described. There are at least 23 marsupial and 57 rodent species described for
the Atlantic forest, of which 39% and 53 %, respectively, are endemic to the
region.
Because of past and present habitat destruction, the fauna is increasingly
isolated into small patches, and many members of this unique ecosystem are
now endangered. This situation has been documented for the most
conspicuous elements of the mammalian fauna, the primates (Coimbra-Filho
and Mittermeier 1977; Mittermeier et al. 1982; Fonseca 1985b). Nonetheless,
the rich and highly endemic small mammal fauna of the Brazilian Atlantic
forest region has been the subject of very few long-term studies, especially
when compared to the Amazon region (e.g. Pine 1973; Lovejoy et al. 1984;
1986; Terborgh et al. 1984; Malcolm 1987) or the Cerrado (Alho 1981; Alho
et al. 1986; Fonseca and Redford 1984; Lacher et al., in press; Nitikman and
Mares 1987). The only detailed study of Atlantic forest small mammals is now
over 40-years-old (Davis 1946).
Historically, the Brazilian Atlantic forest extended from the coast to the
eastern and portions of the western slopes of the coastal mountains (Hueck
1972; Alonso 1977). This vegetation formation was originally distributed over
an area of approximately 700,000 square km. Where rainfall permits the
presence of tall, evergreens, this type of forest extends into the western slopes
of the coastal formation. Due to a rain shadow, the vegetation of the western
slopes, where this study was conducted, possesses a number of deciduous tree
species, which lose their leaves during the approximately 6 months of the dry
season. During the wet season, however, the forests of both the eastern and
western regions are physiognomically undistinguishable. In addition, the
BULLETIN FLORIDA STATE MUSEUM 34(3)
faunal elements are mostly the same, generally belonging to the same
biogeographical region (Muller 1973).
The objective of this study was to investigate several aspects of the biology
and natural history of eastern Brazilian non-volant small mammals. During a
17-months period, data on the general aspects of population dynamics,
breeding, substrate use and movement patterns of small mammals (marsupials
and rodents) were collected in six forest plots, at three main sites in the state of
Minas Gerais, Brazil. Morphometric data were also collected. The present
study was part of a larger research project on small mammal community
structure, in which it has been shown that primary forests are comparably
poorer in species richness and diversity when compared to secondary
vegetation in mid-stages of succession. In addition, it was also suggested that
predation may exert a high degree of influence on the patterns of community
composition and structure in the forest fragments of the Atlantic coastal region
of Brazil. Patterns of species composition, relative abundances, habitat
preferences, predation pressure and other community structure param are
presented in Fonseca (1988).
ACKNOWLEDGEMENTS
First we would like to thank John G. Robinson for his advice during planning, field work,
analysis and writing of this study. John Eisenberg, Larry Harris, Kent Redford, Nigel Smith,
Melvin Sunquist, and Charles Woods also provided valuable support. John Eisenberg and Oliver
Pearson improved the manuscript. This research also benefited from discussions with Drs.
Thomas Lacher and Michael Mares.
Russell A. Mittermeier supported our research by advocating our cause with the World
Wildlife Fund-US, which financed the most substantial part of the costs. Additional financial
support was provided by the Program for Studies in Tropical Conservation, of the University of
Florida, and by the Research Council of the Federal University of Minas Gerais, Brazil. The
National Research Council of Brazil (CNPq) awarded one of us (G. A. B. da Fonseca) a doctoral
fellowship.
Celio Valle encouraged the field work with his enthusiasm, vision, and eternal optimism.
Several people helped during field work. I would like to thank Ludmilla Aguiar, Ilmar Bastos,
Sonia Rigueira, Carlos Alberto Pinto, Ederson Machado (sometimes), Silverio Machado, Ney
Carnevalli, Luiz Fernando Mello, Gisela Herrmann, Jairo Vieira, Eduardo Veado, Eduardo
Sabato, Luiz Paulo Pinto, and Maria Cristina Alves. Our small mammal data from the Rio Doce
Park was partially collected by Jody Stallings and his crew (see Stallings 1989).
Mr. Feliciano Abdalla and Dr. Antonio Cupertino kindly allowed us to work on their farms
and provided housing. "Santinho" let us stay in his house at the expense of family problems, and
we are thankful to him. The State Forest Institute of Minas Gerais (IEF) provided us with
accommodations and gasoline at the Rio Doce State Park. We are very grateful to the staff of
the Park, especially Ademir Camara Lopes, Jose Lourenco Ladeira and Hermogenes Ferreira
Neto. M. Carleton, K. Creighton, L. Emmons, G. Musser, P. Myers, and J. Patton generously
identified the small mammal voucher specimens.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 103
MATERIALS AND METHODS
Study Sites
Small mammal communities of six forest plots, two at each of three sites in the state of
Minas Gerais, were the subject of this study (Fig. 1). At each site, a primary and a secondary
forest plot was selected. The objective was to cover the widest possible spectrum of habitats. A
set of three parallel transect trapping lines was established in each. The primary forest plots
showed vertical stratification, with an average canopy height of 19 m. Tall buttressed emergents
were a common occurrence (Fig. 2a). The herbaceous stratum was somewhat sparse, while the
midstory was generally well developed. The secondary forests, on the other hand, were mostly in
their mid-stages of succession (Fig. 2b). Average canopy height was approximately 12 m;
herbaceous cover was frequently extensive, with masses of tangled vines being a common
occurrence. Epiphytes and emergents were conspicuously absent from the secondary forests.
The first site was Fazenda Esmeralda, located in the county of Rio Casca (Fig. 1). The
farm is under extensive agricultural use, with very little remaining under forest cover. Located
Figure 1. Locations of study sites in the state of Minas Gerais' Brazilian Atlantic forest
(1= Fazenda Esmeralda; 2= Rio Doce State Park; 3= Fazenda Montes Claros).
BULLETIN FLORIDA STATE MUSEUM 34(3)
along the plains of the Rio Doce River, the farm was covered almost completely by pristine forest
as recently as 1964. Wood extracting rights were then sold to the largest steel industry of the
state of Minas Gerais and by 1970 most of the farm was deforested. Forest patches located on
the top of two hills were selected for the study, one with a 60 ha second growth, and the other
with 80 ha of primary forest, known locally as "Lagoa Fria."
The second site was the Rio Doce State Park (also treated in detail by Stallings 1988), which
has portions of its area within the county of Marlieria (Fig. 1). The park, with its 35,973 ha,
constitutes the largest continuous area under tropical forest in the state of Minas Gerais. It was
created in 1944 and has been under the jurisdiction of the Government of the state of Minas
Gerais since that time. Since the creation of the State of Minas Gerais Forest Institute (IEF) in
the late 1960s, the park has been under its administration. It has recently become one of the best
maintained and protected areas under the Brazilian State Parks system. Because of several
extensive fires in the 1960s, a considerable area of the park is second growth. One of these,
"Mata do Hotel," was selected as a study area. A pristine primary forest, known locally as
"Campolina," constituted the second patch selected for study within the Rio Doce Park.
Fazenda Montes Claros was selected as the third site for this study. It is a coffee and cattle
farm located within the counties of Ipanema and Caratinga (Fig. 1). The total area of the farm is
about 1200 ha, 860 ha of which remain under forest cover. A research station under the
administration of the Brazilian Foundation for Conservation of Nature (FBCN) and the Federal
University of Minas Gerais (UFMG) was established on the farm in 1983. A second growth
forest patch at Fazenda Montes Claros, known as "Jao," was selected, and another under primary
forest, "Matao," was also used.
~~~,,'1 q~ WY4Up i
Figure 2. (a) Secondary forest of Fazenda Esmeralda, one of the study sites. (b on facing page)
Buttressed tree characteristic of the primary forests that were surveyed in this study (photo by
Kent H. Redford); Jody Stallings is in the foreground.
104
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 105
bill
TCb: -
~~i^
BULLETIN FLORIDA STATE MUSEUM 34(3)
Climate
Climatological data were collected at all three sites, but because of the extreme similarity in
temperature and rainfall regimes among study sites, only information collected at Fazenda
Montes Claros are presented here.
Hueck (1972) states that rainfall for the western slopes of the Atlantic forest region is always
below 1600 mm annually. In some areas, it can achieve a little over 1000 mm. A climatogram of
Walter (1971), constructed with data collected at this study, can be found in Figure 3. During the
study period, the region experienced an unusually dry period; total rainfall for the first 12 months
of trapping was 850 mm, while for the last 12 months rainfall totaled 931 mm. Rainfall is highly
seasonal, being concentrated between the months of September and February (Fig. 3). Average
monthly precipitation for the rainy season was 128 mm, while dry season rainfall averaged only 30
mm monthly.
Mean minimum annual temperature during the study period was about 18 C, close to the
average for the region (Hueck 1972). Average daily differences between minimum and maximum
temperatures are quite constant throughout the year. Rainfall maxima coincide with the warmest
months of the year, while winters are usually very dry. For the purpose of this analysis, the dry
season is considered to occur between the months of March and August, and the wet season
between September and February.
MONTHLY RAINFALL (mm)
MEAN TEMPERATURE (
250
200
150
100
50
0
Jun Jul AugSe
S RAINFALL SURPLUS
0
DROUGHT
- ~130
15
0
)OctNovDecJanFebMar AprMayJun Jul AugSepOct
MONTHS
Figure 3. Climate diagram of Walter (1971), constructed using climatological data collected at
Fazenda Montes Claros between June 1985 and October 1986. The diagram indicates periods of
drought and water surplus. The dry season can be defined between the months of March and
August. Temperatures are given in C, and rainfall in mm.
C)
150
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 107
Trapping
Three transect lines 300 m long were established in each plot at each of the three sites.
These transects were as parallel to each other as possible and separated by 100 m. Each transect
line possessed 16 trapping stations 20 m apart. Traps were placed in suitable locations within a
3.5 meter radius measured around center of station. A squirrel-size Tomahawk live trap (one-
door folding trap, size 203, Tomahawk Live Trap Co., Tomahawk, WI) was placed on the ground
at each station. At every other station, a second Tomahawk trap of the same size was wired
either to a branch or vine at heights from 1 m to 4 m high. In addition to these traps, every other
station possessed a mouse-sized collapsible Sherman trap (H. B. Sherman Traps, Inc.,
Tallahassee, FL), with alternation of ground and tree traps. Moreover, the two outermost
transect lines had, at every other station, a large 80 x 30 x 30 cm wire home-crafted live trap.
Therefore, each outer line possessed 16 ground Tomahawk traps, 8 tree-bound Tomahawk traps,
4 ground and 4 tree-bound Sherman traps, and 8 ground large wire traps. The total for each
outer line was 40 traps. The mid-line did not have large traps, but a total of 24 Tomahawk and 8
Sherman traps. In summary, each forest plot had 48 trap stations disposed into 3 transects of 16
stations each, and a total of 112 permanent based traps. With the exception of Sherman traps, all
traps were closed at the end of each five-night trapping session and left in place. Sherman traps
were removed, washed, and replaced each month.
Trapping took place between June 1985 and October 1986, i.e. for 17 consecutive months.
Each forest plot was trapped for five consecutive nights every month. During the course of the
study, a total of 9520 trap nights was accumulated for each plot. Therefore, trapping effort for all
six forest plots together totaled 57,120 trap nights.
Fresh pineapples, oatmeal, and a cotton ball soaked with a commercial codfish oil solution
were used as baits. Traps were checked every morning for captures and for adequacy of bait,
which was replaced as needed.
For each individual, the following information was recorded:
1. Species. If not readily identifiable, the individual was preserved for later taxonomic
identification. The only individuals that were consistently prepared as skins and skulls
were representatives of Oryzomys trinitatis and Oryzomys nigripes. Specimens of the
former species show a high degree of variability in skin color and pattern and were
considered, during field work, as belonging to more than one species. Whenever
possible, animals that died in the traps were also preserved. Moreover, live trapping
and snap-trapping were conducted on other locations within the same forest type for
preparation of voucher specimens and determination of stomach contents. Taxonomic
identification of voucher specimens was provided through the kindness of the following
specialists: Drs. M. Carleton, K Creighton, L. Emmons, G. Musser, P. Myers, and J.
Patton.
2. Location in grid.
3. Individual identification. If already tagged with metal fish tags (fish and small animal
tag, size 1, National Band and Tag Co., Newport, KY), the animal was promptly
released; otherwise the animal was tagged. Individuals with positive taxonomic
identification were released at the same station where captured.
4. Sex.
5. Weight.
6. Body length.
7. Tail length.
8. Ear length.
9. Hind foot length.
10. Reproductive condition. Female rodents were checked for perforated vaginas. I also
noticed whether individuals were pregnant (in late stages) or lactating. Male rodents
were considered in breeding condition if testes were descended. Female marsupials
were considered in breeding condition if neonates were found in either pouch or
attached to nipples, or if the nipple area showed signs of recent nursing by previous
litter. Male marsupials with testes of reduced size were considered pre-pubertal, while
BULLETIN FLORIDA STATE MUSEUM 34(3)
for some species (Metachirus nudicaudatus, Marmosa incana, Marmosa cinerea,
Marmosa agilis, and Philander opossum) abdominal or sternal scent gland activity
indicated breeding condition. We also recorded any pouch young old enough to be
sexed.
11. Behavior upon release.
Analysis of variance (Procedure GLM: PC-SAS, SAS Institute, Cary, NC) was used to test
the null hypothesis of absence of sexual dimorphism, using the following morphological
characters: weight, body length, tail length, hind foot length, and ear length. Kruskal-Wallis tests
were performed to test for differences in persistence times in traplines among sexes.
Since the number of arboreal traps in each set of three traplines (N=36; 32 %) was different
from that of terrestrial ones (N=76; 68 %), analysis of differential trapping success of arboreal
versus terrestrial traps was conducted with corrections to account for the differential probability
of trapping in the different strata. Where sample size permitted, chi-square tests were performed
to test the null hypothesis of lack of difference in substrate use among sexes. For this analysis, all
proportions were arc-sin transformed (Sohkal and Rohlf 1981).
RESULTS AND SPECIES ACCOUNTS
During the course of this study, a total of 692 individuals of 8 marsupial and
11 rodent species were caught 1366 times in all six forest plots (Table 1).
Table 1. Trapping results for all six forest plots together during 17 months of trapping.
Number of Total Number of
Species First Captures Captures
Caluromys philander 6 7
Didelphis marsupialis 144 404
Marmosa agilis 7 11
Marmosa cinerea 43 120
Marmosa incana 127 220
Marmosa microtarsus 1 1
Metachirus nudicaudatus 105 156
Philander opossum 14 29
Abrawayomys ruschi 1 1
Akodon cursor 29 53
Nectomys squamipes 10 14
Oryzomys capitol 1 2
Oryzomys nigripes 5 5
Oryzomys subflavus 1 1
Oryzomys trinitatis 84 99
Oxymycterus roberti 2 2
Rhipidomys mastacalis 1 1
Echimys sp. 1 1
Proechimys setosus 110 239
TOTAL 692 1366
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 109
One individual of the species Monodelphis americana was trapped on one of
the auxiliary lines at the primary forest of Fazenda Montes Claros. Mean
trapping success, averaged over 17 months of trapping at all sites, was 2.4 %.
For most species, trapping success was much higher during the cold, dry
months, dropping sharply around October with the onset of rains.
Caluromys philander. Woolly opossums (Fig. 4) were only registered for
the Rio Doce State Park. Although occasionally trapped on the ground, this
species is mostly arboreal (Davis 1947; Nowak and Paradiso 1983). In this
study, only one individual was captured on the ground. Upon release, all
individuals climbed into canopies, disappearing from sight at heights of about
10 m. Both the small number of arboreal traps (32%) relative to terrestrial
ones, and the absence of traps in higher strata of the forest may have
accounted for the low trapping success for this species. Only three males and
three females were captured during the course of the study. One female was
recaptured once. Morphometric data on these individuals are presented in
Appendix 1A.
Didelphis marsupialis. Opossums occurred at all sites and represented the
most common small mammal species captured in the majority of forest plots.
This is a generalist species, found in all habitat types (Hunsaker 1977; Miles et
al. 1981; Alho et al. 1986). Adult males were significantly heavier than females
(Appendix 1B). Hind feet were also sexually dimorphic. Other biometric
param did not vary between sexes.
Opossums have been previously described as being mainly terrestrial,
although they are able to climb opportunely while foraging (Miles et al. 1981).
These generalizations were confirmed here. Overall, 73% of D. marsupialis
captures were from terrestrial traps, while 93% of individuals released also
remained on the ground. However, young opossums tend to use aerial
substrate more often than adults. Approximately 23% of the individuals
released (11 out of 37) climbed into trees and/or onto vines. The same result
was obtained by Davis (1947). There were no significant differences in
substrate use between adult males and females.
A total of 79 males and 64 females was captured 196 and 204 times,
respectively, with sex ratios of both number of individuals and total captures
deviating very little from 1:1. Based upon recaptures, males did not persist for
long periods on averaging 1.74 months. Females stayed within the traplines an
average of 2.6 months, but this difference is not significant (p= 0.14). Record
persistence times were achieved by one female and one male, which were
recorded for a total of 12 months. Fleming (1972) found similar low
persistence times for Didelphis marsupialis in Panama. If the conclusions of
Sunquist et al. (1987) with D. marsupialis from Venezuela are extrapolated to
BULLETIN FLORIDA STATE MUSEUM 34(3)
frl
Figure 4. Adult Caluromys philander captured at the Rio Doce State Park.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 111
the present study, the low persistence times can probably be attributed to high
mortality rates rather than to dispersal.
The distance traveled between successive captures were not significantly
different between males and females. The overall mean was 143.4 m
(maximum =400 m), slightly higher than the figure given by Fleming (1972).
However, similar to grid trapping methods, traplines underestimate actual
distances traveled in a night, which Sunquist et al. (1987) found, using radio
transmitters, to average one kilometer.
Even though trapping success during the first three months of study was
very high, population levels, as reflected by the number of captures, did not
appear to vary between dry and rainy seasons (Appendix 1B). Reproductive
activity, on the other hand, was highly seasonal, with most females breeding
just prior and well into the rainy season. The number of juveniles recorded
also followed this same pattern (Appendix 1B). Two females were recorded as
having two consecutive litters, the first in August, and the second in October.
The same has been observed in Brazil by Collins (1973 in Nowak and Paradiso
1983). The occurrence of two consecutive litters has also been reported
elsewhere for D. marsupialis in Colombia (Tyndale-Biscoe and Mackenzie
1976) and southeastern Brazil (Davis 1946).
An interesting result was the decrease in opossum abundances during the
second year's late dry season, especially in the small forest plots. Smaller plots
are where D. marsupialis was found to be most abundant during the first year
of trapping, and capture success was much lower than for the previous year
(Appendix 1B). The reason for this apparent population crash is not yet clear,
but may be due to a reduction in food resources that occurred as a result of a
severe dry season. Although the reduction in abundance was observed across
all plots, smaller forests experienced the highest decrease, lending support to
this hypothesis, since populations inhabiting smaller plots should be more
susceptible to a decrease in food resources.
Average litter size of pouch young was 8.6, with a M:F sex ratio of 1.7:1.0,
highly skewed towards males (Appendix 1B). Overall, two-thirds of females
produced male-biased litters. This average litter size is much higher than those
obtained in Colombia by Tyndale-Biscoe and Mackenzie (1976) or by Fleming
(1973) in Panama. Both studies reported averages of approximately 6.5 young.
In addition, these studies found that sex ratios of pouch young did not differ
from a 1:1 ratio. Austad and Sunquist (1986) were able to experimentally
induce male-biased sex ratios in D. marsupialis by providing dietary
supplementation. Therefore, relative to the sites studied by Fleming (1973)
and Tyndale-Biscoe and Mackenzie (1976), the forests sampled in the present
research may be more productive for common opossums, which may have
resulted in the observed skewed sex ratios.
BULLETIN FLORIDA STATE MUSEUM 34(3)
Marmosa agilis. This small arboreal marsupial (Fig. 5) can be fairly
common in gallery forests of the Cerrado region (Nitikman and Mares 1987),
but was infrequently caught in this study. The first individual of the species
was recorded only after 12 months of trapping. In total, three males and four
females were caught 11 times in two forest plots. Of the 11 captures, 10 (91
%) were in traps placed on trees or vines, which is a capture rate on arboreal
traps similar to that obtained by Nitikman and Mares (1987). Alho et al.
(1986) also found M. agilis to be preferentially arboreal in gallery forest
habitat.
Except for two males and one female, which were recorded in traplines for
two months, no other animal was recaptured in subsequent trapping sessions.
The only individual for which data on movement between trapping stations
were obtained traveled 40 m in consecutive nights, a figure very close to that
determined by Nitikman and Mares (1987). Biometric data on M. agilis are
presented in Appendix 1C.
Mannosa cinerea. This species (Fig. 6) is one of the largest within the
genus (Nowak and Paradiso 1983) and was fairly common at the Rio Doce
Park, but was conspicuously absent from both Fazenda Montes Claros and
Fazenda Esmeralda. Most individuals were captured during the cold, dry
months (Appendix 1D), with trapping success during the rainy season being
fairly low. Lactating females, on the other hand, were only trapped during the
rainy season, indicating that the high trapping success of the following months
reflected the addition of recently born young into the population.
A total of 8 males and 35 females was caught 120 times (Table 1), making it
the species with the highest recapture rate in this study (31% for males and
37% for females). While sex ratio for first captures was 1.6:1.0, total captures
approximated a 1.0:1.0 ratio. This might indicate that females are captured
more frequently than males, which may be due to the fact that males are more
transient than females (chi-square=5.17; df=l, p<0.02) and averaged only
about 1.8 months in traplines. Females, on the other hand, persisted in the
areas for an average of 3.8 months. The longest tenancy in traplines was also
by a female that was recorded present for 14 months. In addition, males also
traveled farther between successive captures than females (males =142 m,
maximum:380 m; females =80 m, maximum:180 m), which also supports the
contention that transient males are a frequent occurrence.
On average, adult males were found to be slightly heavier than females.
However, the species did not show sexual dimorphism for any biometric
parameter measured (Appendix 1D). Although trapped frequently on the
ground, M. cinerea appeared to be primarily arboreal, especially the females
(Appendix 1D). The behavior upon release also revealed that, while 56% of
the males remained on the ground, only 27% of the females displayed a similar
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS
*~ :~.
L
Figure 5. Marmosa agilis, recorded in Fazenda Esmeralda and Fazenda Montes Claros (Photo by
Kent H. Redford).
BULLETIN FLORIDA STATE MUSEUM 34(3)
behavior. Terborgh et al. (1984) list M. cinerea as being able to exploit several
forest strata, from understory to canopy. Miles et al. (1981) determined M.
cinerea to be mostly arboreal, with all nests also located above ground.
Mannosa incana. This was the second most frequently caught species in
this study (Fig. 7). It was present in all six forest plots sampled. We captured
80 males and 44 females a total of 220 times. Three individuals escaped before
their sex could be determined. Sex ratio for first captures was 1.8:1.0, and
2.9:1.0 for all captures. Males also persisted on the traplines more than
females (chi-square=8.1, df=l, p<0.005), on average 1.9 and 1.2 months,
respectively. Therefore, in contrast with M. cinerea, M. incana males appear to
be more sedentary than females. M. incana males traveled an average of 64.7
m between successive captures (maximum=200 m), while the only female
recaptured in the same trapping session traveled 40 m.
Figure 6. Marmosa cinerea, recorded only at the Rio Doce State Park.
114
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 115
Mannosa incana adult males were sexually dimorphic for all morphometric
characters measured, with males being, on average, 20% heavier than adult
females (Appendix 1E). Body length of males was also 14% larger than of
females. Adult females also lack the sternal gland, which is functional in males
during the breeding season.
As with M. cinerea, trapping success increased markedly with the end of the
rainy season (Appendix 1E). This population growth is accounted for by the
increase in the number of juveniles trapped (Appendix 1E). The hypothesis
that increased trapping success is due to juvenile recruitment is further
supported by the observation that the occurrence of breeding males and
especially breeding females is tied tightly to mid to late rainy season (Appendix
1E).
Mannosa incana can be characterized as a scansorial species, as its use of
arboreal and terrestrial traps was approximately evenly split (Appendix 1E).
Figure 7. Marmosa incana, trapped at all study sites.
BULLETIN FLORIDA STATE MUSEUM 34(3)
The same result was obtained by using behavior upon release as a measure of
differential substrate use. Approximately 53% of individuals released climbed
trees or vines, while 47% remained on the ground. There were no statistical
differences in substrate use between males and females (chi- square= 3.19;
p > 0.05).
Marmosa incanq appears highly insectivorous. Three stomachs analyzed in
this study contained only insects, mostly belonging to the orders Coleoptera
and Orthoptera. Nowak and Paradiso (1983) reported that most members of
the genus Marmosa are insect and fruit eaters, although vertebrates are also
occasionally consumed.
Mannosa microtarsus. During the last month of the survey, October 1986,
an adult male of this species was caught in an arboreal trap in the secondary
forest of the Rio Doce Park. The species was previously described as being
quite abundant in both secondary and primary forests of the Atlantic forest
region (Davis 1947). Marmosa microtarsus is similar in morphology to
Mannosa agilis, and it is usually difficult to distinguish them. Morphometric
data from this individual are as follows: weight =31 g; body length =106 mm;
tail length = 148 mm; ear length = 14 mm; hind foot = 17 mm.
Metachirus nudicaudatus. This relatively large-bodied terrestrial didelphid
(Fig. 8) was the third most common marsupial species trapped in this study
(Table 1). The brown four-eyed opossum was present in all six forest plots
surveyed. A total of 60 males and 45 females were caught 88 and 68 times,
respectively. The sex ratio for first captures was equal to that of recaptures
(1.3:1.0). Adult males were, on average, larger than females, with most
biometric param measured proving sexually dimorphic (Appendix 1F). Males
were, on average, 25% heavier than adult females.
Even though the species was relatively common throughout the year, a
trapping success peak was observed following the rainy season (Appendix 1F).
This peak probably coincides with the onset of breeding in mid rainy season
and the beginning of the dry months. Both lactating females and males with
functional abdominal glands were frequently caught at this time (Appendix
1F). Metachirus nudicaudatus may also be able to produce a second litter in
the same year. One female had a litter in March and the second in October.
The number of pouch young ranged from 5 to 9, with an average of 7.2 young
(Appendix 1F). For the two females in which young were old enough to be
sexed, there was a biased sex ratio towards females.
Nowak and Paradiso (1983) regard brown four-eyed opossums as being
arboreal, but the species caught in an arboreal trap was only once in 156
captures. Furthermore, only once was an individual observed to use aerial
substrate upon being released. In fact, the large and non-graspable hind feet
and clumsy behavior on above ground support do suggest a complete
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 117
terrestrial life for the species. Using a spool-line device, Miles et al. (1981)
also found Metachirus nudicaudatus to be completely terrestrial. Terborgh et
al. (1984) also regard gray four-eyed opossums as a species confined to the
ground.
Male and female brown four-eyed opossums did not differ in persistence
times in traplines, with both sex classes averaging 1.7 months. Two males and
two females were also recorded in traplines over a nine-month period.
Distances traveled between successive trapping were among the lowest for
marsupials, averaging 36.7 m (maximum =120 m; N=6) for males and 40 m
(maximum= 80 m; N=7) for females.
Monodelphis americana. Short-tailed opossums have a fairly wide
distribution in Brazil (Streilein 1982). Only one female was caught in an
auxiliary line established in the primary forest at Fazenda Montes Claros, for
Figure 8. Metachirus nudicaudatus, trapped at all study sites.
BULLETIN FLORIDA STATE MUSEUM 34(3)
Figure 9. Philander opossum, captured at all sites, except at the Rio Doce State Park.
the purpose of collecting voucher specimens. The capture site did not differ
physiognomically from the regular traplines, and therefore the species might
also occur consistently at this site. However, it is felt that trapping methods
were not proper to adequately represent the species. Its small body size and
foraging habits on the forest litter may have accounted for its low
representation in the sample (Davis 1947). The biometric data on this
individual are as follows: weight = 19 g; body length = 92 mm; tail length =
46 mm; hindfoot = 16 mm; ear length = 13 mm. Comparisons with data
provided by Nowak and Paradiso (1983) indicate that this individual was
probably a juvenile.
Philander opossum. Gray four-eyed opossums (Fig. 9) were trapped in all
forest plots, except at the Rio Doce Park. Fourteen individuals were caught
during the course of this study. The occurrence of this large didelphid
marsupial is apparently tied to the presence of standing or running water
(Davis 1947; Handley 1976; Nowak and Paradiso 1983; Alho et al. 1986). As
only a few transects occurred close to streams, this may explain the low
trapping success for this species. As with other species, trapping success was
much higher during the dry season (Appendix 1G).
While only three individual females were recorded, these had a much
higher recapture rate; 11 males were caught 17 times, while 3 females were
captured in 12 different occasions. The longest persistence times on the
traplines were 4 and 5 months, achieved by two adult females.
All females caught were lactating, and two still had pouch young. Nowak
and Paradiso (1983), based on several studies, concluded that P. opossum
breeds seasonally. However, the small sample size of the present study does
not allow any conclusions as to seasonality of reproduction. One female had
pouch young in February, while the remaining were caught lactating in August
and September. Each had 5 young attached to the nipples. The figure given by
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 119
Davis (1947) in the Atlantic forest was an average number of pouch young of
4.5, with a maximum of seven, while litter sizes in Nicaragua were found to be
slightly larger (Phillips and Jones 1965). For one litter which sex could be
determined, there were four female and one male young.
Even though the small sample size precluded statistical analysis of sexual
dimorphism, adult males were on average over 30% heavier than females
(Appendix 1G). As noticed by Nowak and Paradiso (1983), in this study the
species also proved to be primarily terrestrial with only 17% of captures in
arboreal traps, and 7% of individuals climbing trees after being released.
Based on field observations, however, it is felt that gray four-eyed opossums
are able, if needed, to efficiently use arboreal substrate. The same was
suggested by Miles et al. (1981) and Crespo (1982).
Abrawayomys ruschi. This rare monotypic murid rodent, endemic to the
Atlantic forest of eastern Brazil, is only known through its type specimen,
collected in the state of Espirito Santo (Nowak and Paradiso 1983). A single
adult male, with descended testes, was collected at the secondary forest of the
Rio Doce State Park in January 1986, for which measurements are as follows:
weight=63 g; body=128 mm; tail length=146 mm; hind foot=31 mm; ear
length= 20 mm.
Akodon cursor. The genus Akodon comprises over 40 species, and A.
cursor is among the largest. Sexual dimorphism is lacking in A. cursor
(Appendix 1H), although males weighed more than females in another study
(Nitikman and Mares 1987). This species occurred frequently in the Rio Doce
Park secondary forest, but also was caught occasionally at other sites, especially
in some auxiliary lines that were located in humid grasslands. Within the
traplines, a total of 29 individuals was caught 53 times (Table 1), 27 of which
were trapped at the Rio Doce Park. Sex ratios for first captures and all
captures were, respectively, 2.3:1.0 and 3.4:1.0.
Akodon cursor was previously described as being completely terrestrial
(Crespo 1982; Alho et al. 1986; Nitikman and Mares 1987). However, the
species demonstrated scansorial ability in this study, with approximately one-
third of trapping success being obtained at arboreal traps.
A distinct peak in population density was found between May and July.
Very few individuals were recorded during the rainy season (Appendix 1H).
This was attributed to recruitment of young into the population just at the end
of the wet and in the dry season. This conclusion is supported by the
observation that the number of males with descended testes closely follows that
of trapping success, and coincides with mid dry season (Appendix 1H).
Gestation and subsequent weaning are close to five weeks (Nowak and
BULLETIN FLORIDA STATE MUSEUM 34(3)
Paradise 1983), and the influence of reproduction activity on population
density was readily noticeable in terms of increased trapping success.
Akodon cursor appears to be primarily insectivorous. Individuals trapped in
both grasslands and forests had high amounts of insects in their stomachs,
which possibly indicates that insects are a part of their diets in all habitats. The
species also makes use of seeds, fruits, and vegetative parts, especially those of
the Graminae (Appendix 1H).
Akodon cursor turnover rates appear very high, with 78% of individuals only
being recorded during one trapping session. Maximum persistence was
achieved by two individuals, but for only three and four months. The two
individuals for which data on travel distances were available, moved 20 and 40
m between successive captures.
Nectomys squamipes. This semi-aquatic rat occasionally was trapped in the
vicinities of small streams or flooded areas within forests. Alho et al. (1986)
obtained 93% of all the captures of N. squamipes in the Cerrado region on
flooded areas. A few individuals in the present study were found over 500 m
from any source of water, suggesting that the species occasionally may exploit
non-aquatic habitats. The three stomachs analyzed contained only vegetative
material, two exclusively fruit pulp.
Nectomys squamipes is a fairly large-bodied rodent, with males attaining
over 250 g (Appendix 1I). A total of eight males and one female was recorded
in tree plots, one at each of the study sites. Another individual escaped before
sex could be determined. All but one individual was caught during the mid dry
season, i.e. between May and August.
Although adapted for semi-aquatic life, N. squamipes were trapped 38% of
the times in arboreal traps. Two males persisted in the areas for three and
four months, respectively.
Oryzomys capitol. A widespread habitat generalist, this rodent is
extensively distributed in South America (Handley 1976). It is possibly mostly
terrestrial, and in the Cerrado region was found more commonly at dense
forests (Alho et al. 1986; Nitikman and Mares 1987). However, it was a rare
species in the forests sampled in this study and was represented by only one
male and one female at the Rio Doce Park, both caught in September 1986.
All captures were on ground traps. The measurements of these individuals
are, respectively: weight =60 and 63 g; body length =122 and 132 mm; tail
length =115 and 129 mm; hind foot= 32 and 34 mm; ear length =22 and 21
mm.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 121
Oryzomys nigripes. This small cricetid rodent commonly occurred at
auxiliary traplines located in grasslands, and it has wide distribution among
Cerrado habitats (Alho et al. 1986; Nitikman and Mares 1987). It was,
however, relatively uncommon in forests. Only five individuals, two males and
three females, were caught in forest traplines. All trappings were done in mid
to late rainy season, i.e. between January and April. Two of these captures
were on arboreal traps, although it is felt that the species is certainly more
terrestrial and/or scansorial, as it was also observed by Crespo (1982). Alho
and Pereira (1985) in Cerrado gallery forests and Veiga-Borgeaud (1982) in
the Atlantic forest region determined that Oryzomys nigripes (=eliurus) makes
extensive use of low shrubs, with nests located about 1 meter from ground.
Stomach contents revealed high frequency of insects, complemented by
fruit, seeds and leafy material (Appendix 1J). Barlow (1969 in Dalby 1975),
and Crespo (1982) also found insects as part of 0. nigripes' diet, even though in
lower proportions. Biometric data are presented in Appendix 1J.
Reproduction occurs throughout the year, albeit it may increase in
frequency at some periods. Two females, one caught in February and the
other in August, both had four fetuses, coinciding with two major reproductive
peaks observed by Veiga-Borgeaud (1982). A third female, trapped in April,
had five implanted fetuses.
Oryzomys subflavus. Only one female of this otherwise fairly common
Cerrado species (Melo 1977; Alho and Pereira 1985; Alho et al. 1986) was
caught in an arboreal trap in the forest traplines. The measurements of this
individual are as follows: weight =92 g; body length= 165 mm; tail length= 173
mm; hind foot = 34 mm; ear length= 25 mm.
Oryzomys trinitatis (=concolor). This cricetid (Fig. 10) was the most
frequent rodent found in the forests sampled, being present at all sites. It is
widely distributed, from Costa Rica to Paraguay (Nowak and Paradiso 1983),
and found mostly in forested habitats (Alho and Pereira 1985; Nitikman and
Mares 1987). A total of 84 individuals was captured 99 times (Table 1). Due
to coat color variation, most individuals were prepared as skins. Therefore,
recapture figures underestimate true recapture rates. Sex ratios at first
captures were 1.35:1.00. In contrast to other small mammal species observed
in this study, females were slightly heavier and longer than males. Other
biometric param were found not to be significantly dimorphic (Appendix 1K).
The species appears to be mostly arboreal. Approximately 74% of males
and 62% of females were captured in arboreal traps (Appendix 1K). This
figure is very close to that observed by Nitikman and Mares (1987) in a gallery
forest of Central Brazil. Males and females did not differ in degree of
arboreality (chi-square=2.40; df=l; p>0.05). Since most individuals were
prepared as voucher specimens, sample size was too small to evaluate the
122 BULLETIN FLORIDA STATE MUSEUM 34(3)
k1 .
;h'l. i.#
~- .e~
IkI\
p.. ~
A
Figure 10. Oryzomys trinitatis, captured at all study sites.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 123
differential use of substrate by analyzing behavior upon release. However, the
few individuals that were released demonstrated climbing ability. Even though
relatively uncommon in the forests of Manu National Park in Peru, Oryzomys
trinitatis (=concolor) was listed by Terborgh et al. (1984) as being able to use
most all forest strata, from the understory to canopy.
Although there were variations in trapping success on a monthly basis,
there does not seem to exist any season characterized by high population, in
contrast to most other species (Appendix 1K). This might be a consequence of
the absence of seasonal breeding. Reproduction seems to take place
throughout the year, as breeding males and females were captured in 14 out of
17 months of study (Appendix 1K).
The two stomachs available for analysis indicated a high degree of
insectivory. The stomach contents of an individual were 100% insects, while a
second had 48% unidentified insects and coleoptera larvae, and 52% fruit pulp.
Oxymyctenrs roberti. This genus includes semi-fossorial cricetids. The
genus is represented in these forests by only one juvenile male and one adult
female of the species roberti (Table 1). Members of this genus are mostly
insectivorous (Borchert and Hansen 1983; Redford 1984); two stomachs
analyzed in the present study yielded 100% insects, especially Coleoptera
larvae and ants. Species of the genus Oxymycterus are more commonly found
in grasslands and inundated savannas (Borchert and Hansen 1983; Fonseca
and Redford 1984; Redford 1984), a habit which can account for the rarity of
the species in the forests of this study. Biometric data for the male and female
are, respectively: weight=57 and 85 g; body length= 124 and 245 mm; tail
length= 111 and 112 mm; hind foot =27 and 30 mm.
Rhipidomys mastacalis. This arboreal rat (Fig. 11) was only caught once in
this study, in the month of September. It is found mostly in moist, forested
habitats (Davis 1947; Dietz 1983; Fonseca and Redford 1984; Alho et al. 1986),
even though it can also invade households (Nowak and Paradiso 1983; J.
Stallings, pers. comm.). The adult male measurements are as follows:
weight=72 g; body length =137 mm; tail length =161 mm; hind foot =27 mm;
ear length = 18 mm.
Echimys sp. Members of this genus are entirely arboreal (Hershkovitz
1969). This may explain the low success in recording this species in the forests
sampled. It is possible that it preferentially occupies higher canopy strata.
Davis (1947) never trapped Echimys below 5 m, while Miles et al. (1981) found
nests of Echimys chrysunrs in tree cavities located at the canopy level.
Only one adult male was caught on the primary forest of Fazenda Montes
Claros in July 1986, in an arboreal trap. The voucher specimen could not yet
be identified beyond genus, but may possibly either be Echimys brasiliensis
BULLETIN FLORIDA STATE MUSEUM 34(3)
Figure 11. Rhipidomys mastacalis, a rare species in the forests trapped in this study.
(sensu Moojen 1952) or a species which has not been described (L. Emmons,
pers. comm.). This specimen had the following measurements: weight= 225 g;
body length =215 mm; tail length =205 mm; hind foot =38 mm; ear length= 14
mm.
Proechimys setosus. Spiny rats were the third most abundant small
mammal in this study (Table 1). Only opossums surpassed P. setosus in
number of recaptures. Even though species of the genus Proechimys were also
found to be quite common in other studies in the Atlantic forest (Davis 1947;
Carvalho 1965; Avila-Pires and Gouvea 1977; Botelho and Linardi 1980; Miles
et al. 1981; Fonseca et al. 1987), in the Cerrado (Fonseca and Redford 1984;
Alho et al. 1986) and in the Amazon region (Bishop 1974; Emmons 1982; 1984;
Terborgh et al. 1984; Malcolm 1987), spiny rats were surprisingly absent from
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 125
the Rio Doce Park traplines. This can possibly be attributed to higher
predation rates by mammalian carnivores, owls and other predators at the Rio
Doce Park (see Fonseca 1988). The park has a larger and richer carnivore
fauna which exert a larger impact upon P. setosus populations than the
comparatively depauperated predator community of the smaller forest plots.
Sex ratios of first captures deviated little from a 1:1 sex ratio, with 56 male
and 49 female individuals being trapped. Five individuals escaped before their
sex could be determined. Females were recaptured at a slightly higher rate
than males, yielding a sex ratio for all captures of 0.83:1.00.
Although spiny rats were caught in all 17 months of the study, a distinct mid
to late dry season peak in trapping success was notable (Appendix 1L). This
may result from the increase in the recruitment rate of juveniles into the
population at this time (Appendix 1L). However, reproduction does not seem
to be strictly seasonal, as it was also observed by Bishop (1974) in Mato
Grosso, Brazil. Pregnant and lactating females were present in all trapping
sessions, although an increase in the frequency of breeding individuals could be
observed both in mid rainy season and in mid dry season (Appendix 1L). A
few females had two litters in the same year, coinciding with the
abovementioned breeding peaks.
There is no sexual dimorphism in this species of spiny rat, as none of the
morphological characters measured significantly differ between sexes
(Appendix 1L). Proechimys setosus is entirely terrestrial, lacking any scansorial
ability. All 239 spiny rat captures were conducted in terrestrial traps. Analysis
of stomach contents indicate that spiny rats are primarily frugivorous, but also
make opportune use of insects and seeds (Appendix 1L). Emmons (1982)
found Proechimys to be highly frugivorous, with insects being frequent in
stomach samples.
Although, on average, females persisted in traplines more than males
(respectively, 2.7 and 2.0 months), there were no significant differences
between sexes (chi-square=0.58, df= 1, p>0.05). The records for persistence
times were obtained by two females who stayed, respectively, 10 and 12 months
within traplines. Males and females also did not differ in mean traveled
distances between successive captures with, respectively, 98.7 (maximum = 220
m) and 87.5 m (maximum =240 m).
DISCUSSION
Seasonality and Resource Use
One of the most striking phenomena common to several small mammals of
the western slopes of the Atlantic forest is the occurrence of seasonal
BULLETIN FLORIDA STATE MUSEUM 34(3)
reproduction. With the exception of the two most abundant rodents (Oryzomys
trinitatis and Proechimys setosus), all four species with sufficient sample size to
allow analysis proved to concentrate breeding in the late dry season and into
the early to mid wet season. These were all marsupials. The evidence for
these patterns derive from both the increase in trapping success starting in late
wet season, represented mostly by the addition of juveniles, as well as the
observation of adults in breeding condition just previous to that period.
Furthermore, the number of first-time captures of all small mammals is
significantly and negatively correlated with average monthly precipitation
(r =0.55; p <0.02), which indicates that recently weaned juveniles are recruited
into the population at the end of the rains. Akodon cursor is also a seasonal
breeder, but unlike marsupials its reproduction is concentrated in the dry
season.
Davis (1946) and Laemmert et al. (1946) observed a pattern of cyclic
reproduction among several Brazilian Atlantic forest small mammal species.
Breeding was concentrated in the late dry winter and in the wet summer
months, albeit less marked than in the present study. The possible reason for
this may be that both these studies were in the eastern side of the Brazilian
coastal mountains, where the dry season is shorter and less severe (Hueck
1972). These two studies have also revealed the lack of seasonality for some
rodent species, especially ones from the genus Proechimys, which probably
breed year-round throughout its range.
A large number of African rodents seem also to closely tie the onset of
reproductive activities to just before the end of the wet season (Delany 1986).
Cerrado species appear to be equally divided between seasonal and year-round
breeders (Dietz 1983; Alho 1982; Alho and Pereira 1985). In Panama, over
50% of mammals are seasonal breeders (Fleming 1973), although reproduction
is concentrated in the three months of the dry season, which results in most
young being weaned at the beginning of the rains.
Other things being equal, reproductive output and juvenile survival of small
mammals would be maximized if reproduction occurred when the environment
is best in terms of resource availability (Fleming 1975). In fluctuating
environments the energetic costs of pregnancy and lactation, coupled with the
needs of adequate resources for newly weaned young, should pose constraints
on the timing of reproduction. Lee and Cockburn (1985) state that all tropical
didelphids are seasonal breeders, and the timing of reproduction is linked with
availability of food. Marsupial food resources, in turn, are tied to the
fluctuation in rainfall regimes of seasonal environments (Charles-Dominique
1983). Information on small mammal diets in this study are not sufficient to
provide an accurate and longitudinal picture of diet composition. However, it
is important to notice that all but the semi-aquatic Nectomys squamipes were
observed to consume insects in variable quantities. All didelphid marsupials
appear to be predominantly insectivorous (Nowak and Paradiso 1983), and
126
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 127
even large-bodied species, such as Didelphis marsupialis and Philander
opossum, depend heavily on insect prey (Charles-Dominque 1983). Metachints
nudicaudatus, Marmosa spp., and Caluromys philander have also been listed as
being consumers of ants and termites (Redford 1987), although the latter
species may rely more heavily on fruits (Atramentowicz 1982).
Results of studies on insect population fluctuations in the neotropics vary
(see Elton 1975; Bigger 1976; Janzen and Schoener 1968; Janzen 1973; Wolda
1978), but most authors agree that samples obtained in wet season months are
larger than comparable ones collected during the dry months (Davis 1946;
Wolda 1978; Smythe 1982; Charles-Dominique 1983). Therefore, the trends of
this study certainly support the notion that small mammal reproduction,
especially that of marsupials, is influenced by availability of insect prey.
However, until the variation in the cycles of prey populations across the year
are described, explaining timing of reproduction of small mammals as a
consequence of abundance of insect prey in the late wet to early rainy season
will remain speculative.
Fruits and seeds were the other frequent items present in the stomachs of
small mammals in this study, although it is felt that rodents may depend more
heavily on these resources than the more insectivorous marsupials. If the
number of trees with fruits can serve as a measure of food resource availability
for small mammals, the timing of reproduction of most small mammal species
seems to track that of resources. In the Brazilian Atlantic forest
asynchronously fruiting trees may be found at every month of the year (Davis
1946). Nonetheless, fruit production of several plant species of seasonal
neotropical environments has been shown to be influenced by precipitation,
usually peaking just prior to the start of the rainy season (Foster 1982; Smythe
et al. 1982; Charles-Dominique 1983). A second peak in fruit productivity can
also be present at the end of the rainy season (Davis 1946). A preliminary
study conducted in the Rio Doce Park (CETEC 1981) also indicated that there
are tree species flowering and fruiting throughout the year, and also that there
is a slight peak in the number of fruiting species in September and October, i.e.
in early rainy season.
I expected marsupials, which use invertebrates to a larger extent than
rodents, to display a higher degree of seasonality due the more fluctuating
nature of their food resources. This was observed in the present study.
Rodents, on the other hand, can probably rely on resources which are more
seasonably stable in the Atlantic forest, such as fruits, seeds, and leaf tissue,
and thus can reproduce throughout the year. The two most common rodents,
Proechimys setosus and Oryzomys trinitatis, do not show seasonality in their
reproductive patterns. Since they also have been shown to use and during
some periods heavily rely on insects, the consequent larger resource spectrum
should place lower limits on the reproduction of rodent species.
BULLETIN FLORIDA STATE MUSEUM 34(3)
While some small mammals may exploit resources on the forest floor, most
of the tropical forest productivity is located above ground (Eisenberg and
Thorington 1973). Therefore, even for primarily terrestrial species, some level
of scansorial ability should prove advantageous. There was a high degree of
overlap in substrate use among small mammal species in this study. Twelve
species are shown to use both aerial and ground substrate regularly, even
though their relative degrees of arboreality varied. Among marsupials, only
Metachirus nudicaudatus was confined to the ground level of the forest. Only 4
of 11 rodent species can be safely classified as terrestrial, while the remaining
are at least marginally arboreal. This is consistent with descriptions of other
neotropical small mammal fauna, where the majority of species show some
level of climbing ability (see August 1984; Fonseca et al. 1987; Nitikman and
Mares 1987).
It should be stressed that these findings do not imply that arboreality is the
dominant mode of life among Atlantic forest small mammals. Of the species
caught in the present study, only Caluromys philander, Marmosa cinerea,
Mannosa agilis, Oryzomys trinitatis, Rhipidomys mastacalis, and Echimys sp.
can be regarded as predominantly arboreal. It does, however, indicate the
widespread ability of a greater fraction of the community in exploring a tri-
dimensional environment. This may be especially important during certain
periods of the year. Charles-Dominique (1983) provided data indicating that
the insect faunas of the canopy and of the undergrowth can fluctuate
asynchronously with each other. Therefore, if a particular food resource is
undergoing a period of seasonal shortage, those species with versatile habits
would be at an advantage. It has been demonstrated before that in the highly
seasonal savanna region of central Brazil gallery forests play an important role
in maintaining overall mammalian species diversity (Fonseca and Redford
1984) and become crucial during periods of stress. Part of the reason for this
may be linked to the higher productivity of the tri-dimensional gallery forest
environment, when compared, during periods of moisture deficit, to that of the
cerrado savannas.
Life History Patterns
While the occurrence of pouch litters with skewed sex ratios in neotropical
marsupial species has not often been reported, it was interesting to find
Didelphis marsupialis with litters having a predominance of males. Skewed sex
ratios have only been achieved experimentally under a regime of diet
supplementation, a procedure which does not always produce the predicted
male bias outcome (Austad and Sunquist 1986). Therefore, it is important that
future investigations address this question. The female-biased sex ratio
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 129
obtained for Metachirus nudicaudatus pouch young is not based on a large
enough sample size and therefore remains inconclusive.
Three out of four marsupial species, for which sample size was large
enough to allow statistical inference, proved sexually dimorphic. Male
Didelphis marsupialis also has been found to be larger than females elsewhere
in South America (O'Connell 1979). Other Marmosa species also have larger
and heavier males (Nowak and Paradiso 1983), the same being true for
Philander opossum. No references have been found to indicate size differences
for Metachirus nudicaudatus, except for the present study. While larger males
usually have been associated with polygynous species in which males strongly
compete for females (Rails 1976), there was no evidence of territorial defense
by any of the marsupials studied here. However, this does not necessarily
preclude males from actively competing for females at overlapping ranges.
Fierce fighting for estrous females has been observed elsewhere in Didelphis
marsupialis (Austad and Sunquist 1986). Since marsupial breeding in this
study was usually confined to a certain season, the potential for male-male
competition for estrous females is likely.
Rodents, on the other hand, are seldom dimorphic (see Eisenberg
1981), especially the smaller species. In only one species, Oryzomys trinitatis,
could a size difference be found in this study. In this instance, however,
females proved to be larger on average than males. This could be attributed to
extra energetic demand placed on pregnant and lactating females, a cost non-
existent for males who do not provide parental care (see Rails 1976).
Moreover, since rodent young do not undergo, unlike marsupials, a teat
attachment phase, female placental mammals may increase litter size above
that of the teats. The increase in rodent litter sizes may be achieved if the
female is larger and better nourished. Marsupial litter sizes, on the other
hand, due to the obligatory teat attachment phase, are constrained by the
number of teats. Furthermore, marsupials can spontaneously terminate
lactation, or more often in smaller species reduce litter size if energetically
stressed (Lee and Cockburn 1985). Young are also born after a very short
gestation period, making the reproductive investment minimal. For these
reasons no added security would be achieved by genetically fixed propensity for
larger marsupial females.
Population Turnover
Although the area sampled by traplines was not enough to represent the
home range of several species, especially the larger ones, the reduced
persistence time of the average small mammal individual was nonetheless
striking. Average persistence times ranged from 1.2 months for male Marmosa
BULLETIN FLORIDA STATE MUSEUM 34(3)
incana to a maximum of 3.8 months for Marmosa cinerea females, with most
species remaining in traplines within the range of 1.7 to 2.7 months. While it is
reasonable to assume that some of the disappearances can be attributed to
home range shifts (see Nitikman and Mares 1987) and/or juvenile migration
and dispersal (Lidicker 1975), predation might also play an important role in
increasing turnover, rates among tropical small mammals. Monthly turnover
rate for the small cricetid rodent Akodon cursor approached 80% in this study.
Several authors have suggested that predators might cause variations in local
abundances (August 1983), and sometimes they do take a large percentage of
small mammal standing biomass (Hershkovitz 1969; Pearson 1985; Emmons
1987; Sunquist et al. 1987). Predation in traps was observed in this study on
several occasions and it is felt that it may play a major role in the structure of
these communities (Fonseca 1988).
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BULLETIN FLORIDA STATE MUSEUM 34(3)
APPENDIX I -- A-L.
A. CALUROMYS PHILANDER
Biometric data for three males and three females of Caluromys philander. Weight is given in
gms, and other body measurements in mm.
MALE FEMALE
Mean St.Dev. Mean St.Dev.
Weight 171.3 57.6 180.5 40.5
Body length 210.7 30.0 206.8 11.4
Tail length 301.0 25.9 298.8 20.7
Hind Foot 36.3 2.5 36.3 2.6
Ear length 33.3 1.5 30.5 1.9
B. DIDELPHIS MARS UPIALIS
Biometric data for adult male and female Didelphis marsupialis. Weight is given in gms, and
other body measurements in mm. N= number of individuals, St. Dev.= Standard Deviation. P
refers to p-value associated with analysis of variance for sexual dimorphism
(n.s. =p >0.05;, =p <0.05; **=p<0.01; ,.=p <0.001).
MALE FEMALE
Mean St.Dev. N Mean St.Dev. N P
Weight 1,024.0 361.4 63 946.0 157.0 34 **
Body length 354.0 40.4 63 354.0 29.7 34 n.s.
Tail length 348.5 30.9 62 349.6 27.4 31 n.s.
Hind Foot 58.1 3.9 62 56.1 4.3 34 **
Ear length 51.2 4.2 62 50.0 3.6 34 n.s.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 135
Litter sizes and sex ratios of Didelphis marsupialis pouch young.
Number of Number of Total Sex Ratio
ID Number Female Young Male Young Young M:F
0076
0088
0055
0072
0087
0126*
0156
0162*
0067
0192
0193
0209
0072*
0081
0220
0251
0257
0258
0274
0209**
0278
0281
0227
0480
14/10
42P
11/12
Means
2.0:1.0
1.7:1.0
3.5:1.0
1.3:1.0
1.0:1.0
1.0:1.0
3.5:1.0
2.5:1.0
1.0:1.0
1.7:1.0
*Females were in poor condition, with multiple injuries.
used in calculating means.
**Second consecutive litter.
Therefore, their litter sizes were not
BULLETIN FLORIDA STATE MUSEUM 34(3)
100l
80
o i i i i I I I I I I I
Jun Jul AugSepOctNovDecJanFebMar AprMayJun Jul AugSepOct
I Number of Captures M Rainy Season Limits
Figure 12. Number of captures of Didelphis marsupialis according to monthly trapping period.
Straight lines enclose boundaries of rainy season (September to February).
Jun Jul AugSepOct NovDec Jan Feb Mar Apr May Jun Jul AugSepOct
SiBreeding Females i Number of Juveniles -X- Mean Rainfall (mm)
Figure 13. Number of breeding females and juveniles of Didelphis marsupialis, according to
monthly trapping period. Data points in line represent mean daily rainfall (in mm).
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 137
C. MARMOSA AGILIS
Biometric data for four males and one female Mannosa agilis. Weight is given in gms, and other
body measurements in mm.
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N
Weight 29.5 11.3 4 25.0 1
Body length 109.3 13.2 4 99.0 1
Tail length 155.3 7.1 4 151.0 1
Hind Foot 18.3 1.5 4 17.0 1
Ear length 20.5 0.6 4 21.0 1
D. MARMOSA CINEREA
Biometric data for adult male and female Marmosa cinerea. Weight is given in gms, and other
body measurements in mm. P refers to p-value associated with analysis of variance for sexual
dimorphism (n.s. =p >0.05; *=p<0.05; **=p<0.01; ***=p<0.001).
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 117.3 29.4 24 99.7 16.7 11 n.s.
Body length 176.1 20.0 24 177.1 20.5 11 n.s.
Tail length 258.9 26.0 24 261.7 17.9 11 n.s.
Hind Foot 28.9 3.9 24 28.0 3.1 11 n.s.
Ear length 30.4 2.8 24 29.7 2.1 11 n.s.
BULLETIN FLORIDA STATE MUSEUM 34(3)
20-
15-
10-
5-
Jun Jul AugSepOctNovDecJanFebMar AprMayJun Jul AugSepOct
I Number of Captures Rainy Season Limits
Figure 14. Number of captures of Marmosa cinerea according to monthly trapping period.
Straight lines enclose boundaries of rainy season (September to February).
70 (
/
Differential Trapping Success (in %)
Males
Females
M Terrestrial Traps = Arboreal Traps
Figure 15. Differential trapping success (in percentages) of Marmosa cinerea in arboreal and
terrestrial traps.
1, b
1 --- ------ --,-- ; ---
5K.
' ' '
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 139
E. MARMOSA INCANA
Biometric data for adult male and female Marmosa incana. Weight is given in gms, and other
body measurements in mm. P refers to p-value associated with analysis of variance for sexual
dimorphism (n.s. =p> 0.05; =p <0.05; ** =p <0.01; ***=p <0.001).
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 82.3 23.6 62 68.4 23.1 23 **
Body length 150.5 18.0 62 141.0 15.5 23 *
Tail length 203.9 18.2 62 191.2 18.2 23 ***
Hind Foot 23.4 2.0 61 21.5 3.9 23 **
Ear length 28.1 2.4 61 26.5 3.0 23 ***
50
40
30
20
10
, l
Jun Jul AugSepOct NovDec Jan FebMar Apr May Jun Jul AugSepOct
= Number of Captures M Rainy Season Limits
Figure 16. Number of captures of Marmosa incana according to monthly trapping period.
Straight lines enclose boundaries of rainy season (September to February).
I I I
/
;
BULLETIN FLORIDA STATE MUSEUM 34(3)
Jun Jul AugSepOctNovDecJanFebMarAprMayJun Jul AugSepOct
I Number of Juveniles -- Mean Rainfall (mm)
Figure 17. Number of juveniles ofMarmosa incana according to monthly trapping period. Data
points in line represent mean daily rainfall (in mm).
Jun Jul AugSepOct NovDec Jan Feb Mar Apr May Jun Jul AugSepOct
3 Breeding Males = Breeding Females Mean Rainfall (mm)
Figure 18. Number of breeding males and females of Marmosa incana according to monthly
trapping period. Data points in line represent mean daily rainfall (in mm).
I
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS
Differential Trapping Success (in %)
Males Females
M Terrestrial Traps
SArboreal Traps
Figure 19. Differential trapping success (in percentages) of Marmosa incana in arboreal and
terrestrial traps.
F. METACHIRUS NUDICAUDATUS
Biometric data for adult male and female Metachirus nudicaudatus. Weight is given in gms, and
other body measurements in mm. P refers to p-value associated with analysis of variance for
sexual dimorphism (n.s. =p >0.05; =p <0.05; ** =p <0.01; *** =p <0.001).
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 352.7 94.0 51 280.8 57.1 33 **
Body length 252.0 28.7 51 232.1 25.4 32
Tail length 324.1 30.5 51 315.9 34.0 31 n.s.
Hind Foot 44.9 3.1 51 42.3 3.3 32 *
Ear length 37.4 3.9 50 36.5 2.9 32 n.s.
BULLETIN FLORIDA STATE MUSEUM 34(3)
Litter sizes and sex ratios of Metachirus nudicaudatus pouch young.
Number of Number of Total Sex Ratio
ID Number Female Young Male Young Young M:F
271 9 -
322 5 -
338 8
346 3 2 5 0.7:1.0
338* 6 3 9 0.5:1.0
Means 7.2 0.6:1.0
* Second consecutive litter.
20
15
10
5
0 I I I I I lI-f ISB 1 II
Jun Jul AugSepOctNovDecJanFebMar AprMayJun Jul AugSepOct
] Number of Captures = Rainy Season Limits
Figure 20. Number of captures of Metachirus nudicaudatus according to monthly trapping
period. Straight lines enclose boundaries of rainy season (September to February).
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 143
10
8-
4 -
2-
Jun Jul AugSepOctNovDecJanFebMarAprMayJun Jul AugSepOct
2 Breeding Males = Breeding Females -8- Mean Raintall (mm)
Figure 21. Number of breeding males and females of Metachirus nudicaudatus according to
trapping period. Data points in line represent mean daily rainfall (in mm).
G. PHILANDER OPOSSUM
Biometric data for seven males and three females of gray four-eyed opossum, Philander opossum.
Weight is given in gms, and other body measurements in mm.
MALE FEMALE
Mean St. Dev. Mean St. Dev.
Weight 394.9 98.7 295.0 39.7
Body length 282.0 51.3 285.0 48.2
Tail length 325.5 21.6 295.0 18.0
Hind Foot 45.3 2.6 40.3 4.0
Ear length 32.7 3.0 29.3 3.1
BULLETIN FLORIDA STATE MUSEUM 34(3)
12 -'
10
8
6
4
2 -
Jun Jul AugSepOctNovDecJanFebMar AprMayJun Jul AugSepOct
SNumber of Captures M Rainy Season Limits
Figure 22. Number of captures of Philander opossum according to monthly trapping period.
Straight line encloses boundaries of rainy season (September to February).
H. AKODON CURSOR
Biometric data for adult Akodon cursor. Weight is given in gms, and other body measurements in
mm. P refers to p-value associated with analysis of variance for sexual dimorphism (n.s. =p> 0.05;
*=p<0.05; "=p<0.01; =**=p<0.001).
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 48.1 8.1 14 45.5 6.8 8 n.s.
Body length 107.8 10.1 13 103.0 14.3 8 n.s.
Tail length 98.8 9.9 12 94.9 10.4 8 n.s.
Hind Foot 26.9 1.3 13 25.9 1.3 8 n.s.
Ear length 18.1 1.6 14 18.8 0.9 8 n.s.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 145
Stomach contents of fourAkodon cursor.
PERCENTAGE OF
ID Number Insects Leafy Material Seeds Fruits
CEM1/10* 33 33 0 33
47P** 100 0 0 0
101P* 100"* 0 0 0
106P* 96*** 0 4 0
* Forest traplines.
** Grasslands.
*** Coleoptera and ants.
Jun Jul AugSepOctNovDecJanFebMar AprMayJun Jul AugSepOct
I I Number of Captures M Rainy Season Limits
Figure 23. Number of captures ofAkodon cursor according to monthly trapping period. Straight
line encloses boundaries of rainy season (September to February).
BULLETIN FLORIDA STATE MUSEUM 34(3)
Jun Jul AugSepOctNovDecJanFebMarAprMayJun Jul AugSepOct
E Breeding Males E- Mean Rainfall (mm)
Figure 24. Number of males of Akodon cursor with descended testes according to monthly
trapping period. Data points in line represent mean daily rainfall (in mm).
I. NECTOMYS SQUAMIPES
Biometric data for five males and one female Nectomys squamipes. Weight is given in gms, and
other body measurements in mm.
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N
Weight 197.0 67.0 5 165 1
Body length 188.4 19.9 5 190 1
Tail length 207.8 24.9 5 210 1
Hind Foot 50.0 2.8 5 50 1
Ear length 22.0 2.2 5 22 1
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 147
J. ORYZOMYS NIGRIPES
Stomach contents of Oryzomys nigripes.
PERCENTAGE OF
ID Number Insects Fruit Leafy Material Seeds
105P 100 0 0 0
56P 20 0 0 80
CEM3 6 90 4 0
CEM2 30 12 58 0
Biometric data for two males and three females of Oryzomys nigripes. Weight is given in gms, and
other body measurements in mm.
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N
Weight 19.5 0.7 2 18.3 2.9 3
Body length 87.5 0.7 2 83.0 5.3 3
Tail length 126.0 4.2 2 116.8 6.1 3
Hind Foot 23.5 0.7 2 24.0 1.0 3
Ear length 16.0 0.0 2 17.3 0.6 3
BULLETIN FLORIDA STATE MUSEUM 34(3)
K. ORYZOMYS TRINITATUS
Biometric data for adult male and female Oryzomys trinitatis. Weight is given in gms, and other
body measurements in mm. P refers to p-value associated with analysis of variance for sexual
dimorphism (n.s.=p>0.05; *=p<0.05; ** =p<0.01; ***=p<0.001)
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 63.2 8.2 35 70.0 10.9 28 **
Body length 129.1 8.8 35 136.4 8.1 28 ***
Tail length 152.3 10.2 35 159.4 18.2 27 n.s.
Hind Foot 30.4 4.1 35 29.1 2.0 28 n.s.
Ear length 18.6 3.0 35 19.0 1.8 28 n.s.
Differential Trapping Success (in %)
Males Females
S Terrestrial Traps I Arboreal Traps
Figure 25. Differential trapping success of male and female Oryzomys trinitatis in arboreal and
terrestrial traps.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 149
16
14
12 -
Figure 26. Number of captures of Oryzomys trinitatis according to monthly trapping period.
Straight line encloses boundaries of rainy season (September to February).
10
8-
6-
4-
2
0
Jun Jul AugSepOct NovDecJan FebMar AprMayJun Jul AugSepOct
B reeding Males of ap Breeding Females ean Rainfall (mm)
Figure 26. Number of captureeding male and female Oyzomys trinitatis according to monthly trapping period.
trapping period. Data points in ine represent mean daily(September to February).
10-
8-
6-
4-
2-
0
Jun Jul AugSepOct NovDec Jan Feb Mar Apr May Jun Jul AugSepOct
M Breeding Males = Breeding Females E3 Mean Rainfall (mm)
Figure 27. Number of breeding male and female Oryzomys trinitatis according to monthly
trapping period. Data points in line represent mean daily rainfall (in mm).
BULLETIN FLORIDA STATE MUSEUM 34(3)
L. PROECHIMYS SETOSUS
Biometric data for adult male and female Proechimys setosus. Weight is given in gms, and other
body measurements in mm. P refers to p-value associated with analysis of variance for sexual
dimorphism (n.s.=p>0.05;*=p<0.05; **=p<0.01; ***=p<0.001).
MALE FEMALE
Mean St. Dev. N Mean St. Dev. N P
Weight 270.7 36.2 43 259.6 43.4 41 n.s.
Body length 200.2 14.2 42 196.5 18.9 40 n.s.
Tail length 212.3 13.9 39 208.3 15.4 39 n.s.
Hind Foot 51.2 2.1 43 50.7 4.6 40 n.s.
Ear length 29.2 2.1 43 30.6 2.8 40 n.s.
Analysis of seven stomachs of Proechimys setosus.
PERCENTAGE OF
ID Number Fruit Insects Seeds
39P 81 0 19
93P 64 36 0
95P 100 0 0
90P 0 100* 0
91P 100 0 0
92P 100 0 0
79P 47 0 53
* Termites and Coleoptera larvae.
FONSECA & KIERULFF: BRAZILIAN ATLANTIC FOREST SMALL MAMMALS 151
40
30-
20-
10-
Jun Jul AugSepOctNovDecJanFebMarAprMayJun Jul AugSepOct
SI Number of Captures M Rainy Season Limits
Figure 28. Number of captures of Proechimys setosus according to monthly trapping period.
Straight line encloses boundaries of rainy season (September to February).
Jun Jul AugSepOct NovDec Jan Feb Mar Apr May Jun Jul AugSepOct
SI Number of Juveniles 3 Mean Rainfall (mm)
Figure 29. Number of Proechimys setosus juveniles according to monthly trapping period. Data
points in line represent mean daily rainfall (in mm).
BULLETIN FLORIDA STATE MUSEUM 34(3)
16
14
12
10
8
6-
4
2
Jun Jul Aug SepOct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
E Breeding Males ] Breeding Females -E- Mean Rainfall (mm)
Figure 30. Number of breeding male and female Proechimys setosus according to monthly
trapping period. Data points in line represent mean daily rainfall (in mm).
SMALL MAMMAL INVENTORIES
IN AN EASTERN BRAZILIAN PARK
Jody R. Stallings
BULLETIN FLORIDA STATE MUSEUM 34(4)
Plate 1 A. Didelphid marsupials (Didelphis marsupialis [top] and Metachirus nudicaudatus
[bottom]) captured in Rio Doce State Forestry Park, Minas Gerais, Brazil (photographs by
author).
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES 155
Plate 1 B. Didelphid marsupials (Marmosa cinerea [top] and Caluromys philander [bottom])
captured in Rio Doce State Forestry Park, Minas Gerais, Brasil (photographs by author).
BULLETIN FLORIDA STATE MUSEUM 34(4)
Plate 2 A. Cricetid rodents (Oryzomys subflavus [top] and Abrawayaomys ruschii [bottom])
captured in Rio Doce State Forestry Park, Minas Gerais, Brazil (photographs by author).
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Plate 2 B. Cricetid rodents (Rhipidomys mastacalis [top] and Akodon cursor [bottom]) captured
in Rio Doce State Forestry Park, Minas Gerais, Brazil (photographs by author).
SMALL MAMMAL INVENTORIES
IN AN EASTERN BRAZILIAN PARK
Jody R. Stallings*
ABSTRACT
Small mammal inventories were conducted between September 1985 and February 1987 in
native forest, exotic forest, and open field habitats in a state forestry park in southeastern Brazil.
In 40,490 trap nights, 17 species of non-volant small mammals were captured. This small
mammal fauna was composed of 6 species of didelphid marsupials and 11 species of rodents.
Open field habitats were dominated, in terms of species richness and relative abundance, by
rodents. One species, Akodon cursor, represented 85% of the captures in this habitat type.
Forested habitats, both native and exotic, were composed of more species of rodents, but higher
relative densities of didelphid marsupials. Didelphid marsupials Metachimrs nudicaudatus,
Marmosa incana, and M. cinerea were the three most common and ubiquitous forest-dwelling
species captured during the inventory. Exotic Eucalyptus forests with native species subcanopy
help to maintain the species diversity of small mammals in a landscape greatly altered by human
activities.
RESUMO
Inventarios de pequenos mamiferos foram realizados entire Setembro de 1985 e Fevereiro de
1987 em habitats de florestas native, exotica e campo situados no Parque Estadual da Floresta do
Rio Doce no Estado de Minas Gerais, Brasil. Em 40.490 armadilhas-noite, foram capturadas 17
esp6cies de pequenos mamiferos terrestres e arb6reos. EstA fauna de pequenos mamiferos
compreendeu 6 esp6cies de marsupiais didelfideos e 11 esp6cies de roedores. Os habitats de
campo foram dominados em terms de esp6cies e relative abundancia, pelos roedores. Uma
especie, Akodon cursor, representou 85% das captures neste tipo de habitat. Os habitats de
floresta, tanto native como exotica, apresentou um maior numero de esp6cies de roedores, porem
com uma maior diversidade relative de marsupiais didelfideos. Os marsupials didelfideos
Metachirus nudicaudatus, Marmosa incana, e M. cinerea foram as tres especies mais comuns
capturadas durante o inventario, no habitat florestal. As florestas exoticas de Eucalyptus, com
um sub-bosque de especies nativas, auxiliam na manutenqao da diversidade de esp6cies de
pequenos mamiferos num ambiente grandemente alterado pela aqao antropica.
* The author is in the Departamento de Zoologia, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais,
Belo Horizonte, M.G. 30000, Brazil. He was formerly a Post Doctoral Associate in the Department of Wildlife and Range
Sciences, School of Forest Resources and Conservation, University of Florida.
Stallings, J. R. 1989. Small Mammal Inventories in an Eastern Brazilian Park. Bull. Florida
State Mus., Biol. Sci. 34(4):153-200.
BULLETIN FLORIDA STATE MUSEUM 34(4)
TABLE OF CONTENTS
Introduction........................................................................................ ........................................... 160
Acknowledgements........................ ................ ............ 161
Study Site.................................................................................................................... ............... .... 162
M ethods................................................................................................................. .................... .... 163
Results ......................................................... 168
Species A accounts ............................................................................................................... ..... 173
D iscussion............................................................................... .......................... ........................ 180
L literature C ited .................................................................................... ........................................ 184
T ables......................................................... .................................................................................. 187
A appendix 1................................................................. .................................... ........... 194
INTRODUCTION
Despite the country's great size, few studies have been conducted on small
mammal communities in Brazil. Most published reports on Brazilian
mammals are preliminary species lists (e.g. Avila-Pires and Gouvea 1977) or
inventories (e.g. Moojen 1952; Vieira 1955). Some Brazilian studies have
focused on densities (Emmons 1984), others on abiotic effects on small
mammals (Borchert and Hansen 1983; Peterson in press). Still others have
addressed such applied subjects as plantation effects (Dietz et al. 1975) and
public health needs or mammals that carry human diseases (e.g. Laemment et
al. 1946; Botelho and Linardi 1980; Dias 1982).
Recently, work in Brazil using mark-release techniques has addressed the
use of space, longevity, diversity, and social habits of small mammals (see Alho
1982). As Alho (1982) indicated, most of these studies were concentrated in
the xerophitic Cerrado and Caatinga habitats (e.g. Lacher 1981; Mares et al.
1981; Fonseca and Redford 1985; Redford and Fonseca 1986; Nitikman and
Mares 1987; Streilein 1982). Fewer studies have been carried out in humid
forest. Carvalho (1965) live-trapped small mammals in a tropical humid forest
in Sao Paulo, and J. Malcolm (pers. comm.) conducted similar studies in
another such forest near Manaus, Amazonia. Fonseca (1988) worked on small
mammals in a range of forested habitats in eastern Minas Gerais.
The Brazilian Atlantic forest has a highly diverse flora and fauna, with many
endemic species of trees (Mori et al. 1981), reptiles (Miiller 1973), and birds
(Haffer 1974). In-depth mammal inventories in the region are lacking. The
mammalian fauna is poorly known. Mittermeier et al. (1982) and Kinzey
(1982) reported on the high level of diversity and endemism found in the
primates of the region. Preliminary species lists for non-volant mammals in
this region also suggest very high diversity and endemism (Moojen 1952; Vieira
1955; Cabrera 1957, 1961; Honacki et al. 1982). For this paper, a preliminary
analysis was conducted of the non-volant mammal species that probably occur
in the Atlantic Forest region. These data indicate that for the region there are
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
at least 130 species, 54 of which (42%) are endemic. Didelphid marsupials and
rodents account for 78% of the endemic species and 82% of the endemic
genera.
The purpose of this paper is to report the results of intensive inventories of
small mammals in the tropical humid Rio Doce State Forestry Park, Minas
Gerais, Brazil. These inventories were part of a larger overall project
concentrating on small mammal communities in the Brazilian Atlantic Forest.
Gustavo A. B. da Fonseca concentrated his efforts on the effect of habitat size
and disturbance on small mammal species diversity in eastern Minas Gerais
state. The small mammal biology and natural history observations from his
research are presented in Fonseca and Kierulff (This volume). I investigated
the effect of forest fire on small mammal communities in the Rio Doce State
Forestry Park, eastern Minas Gerais state. In-depth small mammal inventories
are lacking from this Park. Gastal (1982) and Avila-Pires (1978) reported
preliminary results from intermittent small mammal inventories in this
sanctuary.
ACKNOWLEDGEMENTS
Foremost, I thank John Robinson, my Ph. D. committee chairman, for his continued support
throughout the various phases of this project and for his suggestion to work on small mammals in
Brazil. Dr. Robinson, along with John Eisenberg, Mel Sunquist, Wayne Marion, S. David Webb,
and Oliver Pearson made constructive comments on the manuscript. John Robinson and Kent
Redford were instrumental in helping me design and implement the project. L. Aguiar, L. P. de
Souza Silva, and E. Sabato helped collect the field data. J. Ladeira, H. Silva-Neto, and A. Lopes
solved daily logistical problems in the Park. Housing in the Park was provided by the Instituto
Estadual de Florestas. G. Fonseca, C. Valle, and I. Santos helped me obtain my visa to work in
Brazil and offered laboratory space in the Federal University of Minas Gerais. This project was
funded by an Organization of American States Fellowship and by the Program for Studies in
Tropical Conservation. Gustavo and Ana Fonseca opened their doors to me and my family, and
we will always be grateful for the assistance that they provided in helping us become acclimated
to Brazil. This is contribution No. 35 from the Program for Studies in Tropical Conservation.
STUDY SITE
Small mammal trapping was carried out in the Rio Doce State Forestry
Park (1948'18" and 19o29'24" south latitude and 42038'30" and 4228'18" west
longitude). The Park was created in 1944 at the request of Dom Helvecio, the
bishop of the region (Gilhaus 1986). The State Forestry Institute of the state
of Minas Gerais is the present administrative body.
The climate of the Park is classified as tropical humid (Gilhaus 1986) with a
seasonal pulse of precipitation from November through February and a
pronounced dry season from June through August. Average annual rainfall for
BULLETIN FLORIDA STATE MUSEUM 34(4)
a 20-year period (CETEC 1981) was 1480 mm, although the rainfall recorded
during the study year was considerably less (Fig. 1). Mean annual temperature
averaged 22C (CETEC 1981), and mean minimum monthly temperatures
varied greatly throughout the year (Fig. 2).
The Park boundaries on the north and the east are two rivers, the Rio
Piracicaba and the ARio Doce, respectively (Fig. 3). The southern and western
boundaries abut plantations of Eucalyptus spp.
The altitude in the Park varies from 230 m to 515 m. CETEC (1981)
reported that 21% of the Park is composed of plains, 40% undulating to
strongly undulating hills, and 34% strongly undulating hills to mountainous
terrain. The predominant terrain derives from dissection of fluvial plains
(Gilhaus 1986).
A unique feature of the Park is the system of lakes in the Rio Doce Valley.
Approximately 40 lakes and numerous marshes within the Park's boundaries
were formed by damming the drainage river of the Rio Doce watershed (Saijo
and Tundisi 1985). The marshes are the result of the sedimentation of
previous lakes.
The vegetation of the park is classified as tropical semi-deciduous (Gilhaus
1986). Most of the emergent trees lose their leaves during the cool dry
months. Forest fire has been a major threat to the vegetation and the wildlife
in the park because of the litter that accumulates during the dry season. In
1964 and 1967, major fires burned approximately 30% of the park (Lopes 1982;
Silva-Neto 1984).
METHODS
Habitats Studied
Small mammals were live-trapped in four habitat types within the Park and
in an exotic habitat type near the Park boundary. Five forested and five
open/field habitats have been described for the Park by Gilhaus (1986). These
are related to the four habitats that were sampled in the park (Table 1). I
trapped in five sites within the native forested habitat category. Two of the
sites, Rio Doce/Campolina (RD/C) and Rio Doce/Turvo (RD/T), were
primary forests and corresponded to the Gilhaus (1986) classification of Tall
Primary Forest with Epiphytes. All of the forested and open/field habitats
have been altered to some extent by fire, with the exception of the Tall Primary
Forest with Epiphytes. With respect to this study, two sites, Rio Doce/Hotel
(RD/H) and Rio Doce/Misturado (RD/M) were altered by forest fire in 1967
and burned in an intermediate fashion which produced a forest mosaic of
short, secondary, and tall forest. This habitat type corresponded to the
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
MONTHLY RAINFALL (MM) MEAN TEMPERATURE (C)
4N'mr. 4
MONTHLY RAINFALL (MM)
MEAN TEMPERATURE (C)
0 SURPLUS 20 3 SURPLUS 20
20 AU2(0
200 0 DEFICIT 80 2. OO DEFICIT o
60 60
100 40 100 40
20 20
0 0 0
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
MONTHS MONTHS
Figure 1. Walter and Leith climatic diagrams characterizing precipitation surplus and deficit per
month in Rio Doce State Forestry Park, Minas Gerais, Brazil. Y axis is monthly rainfall in mm
and Y axis in mean temperature ("C). A = data collected for a 20-year period (1954-1974), and B
= data collected during present study.
TEMPERATURE (C)
0 1
NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
MONTHS
MEAN MAXIMUM TEMP -- MEAN MINIMUM TEMP
Figure 2. Temperature graph demonstrating the pronounced decrease in minimum temperature
during June, July, and August in the Rio Doce State Forestry Park, Minas Gerais, Brazil.
MTA FROM 1..4-1974
QT1 FROM tBB6-1B8
BULLETIN FLORIDA STATE MUSEUM 34(4)
RIO -190 29'
PIRACIC BA
ATLANTIC
FOREST
PFERD
RIO
DOCE
PFERD
R I0 TURVO
0 4KM
S-- 190 48'
Figure 3. Map of Rio Doce State Forestry Park, Minas Gerais, Brazil. Rivers Piracicaba and
Doce form the northern and southern boundaries of the Park respectively. Trapping sites are
indicated by circled letters: E = eucalypt forest with native species subcanopy (RD/E); B = wet
meadow habitat (RD/B); F = homogeneous short secondary forest (RD/F); M = mosaic habitat
of secondary and primary forest (RD/M); H = mosaic habitat of secondary and primary forest
(RD/H); T = primary forest habitat (RD/T); C = primary forest habitat (RD/C).
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Medium to Tall Forest with Bamboos and Graminoids. The remaining native
forest site, Rio Doce/Fogo (RD/F), was burned completely to the ground in
1967, and the resulting vegetation type corresponded to the Medium Secondary
Forest with Bamboos and Graminoids.
The wet meadow habitat, Rio Doce/Brejo (RD/B), corresponded to both
the Low Woodland and Low Tree and Scrub Tallgrass Savanna classified by
Gilhaus (1986). This habitat type occurs between the edge of permanent
marshes and secondary forest. Grasses were the dominant vegetative cover
and were introduced in the region as food for cattle.
The eucalypt forest with native subcanopy habitat, Rio Doce/Eucalypt
(RD/E), was planted with Eucalyptus saligna in 1954 after the original
vegetative cover was removed. The eucalypt forest was harvested selectively in
1964 and again in 1971. However, the eucalypt forest was never clear-cut and
the native species were allowed to regenerate, largely through coppicing, and
developed into a complex native subcanopy. The result was a homogeneous
eucalypt upper canopy and a native species subcanopy or "mata suja." Tall
exotic grasses covered the ground. Emergent eucalypt trees reached 20 m in
height.
Mammal Trapping
Small mammals were snap trapped in order to obtain voucher specimens, as
well as dietary and reproductive information. Such trapping was carried out
exclusively in wet meadow and secondary successional habitats. All specimens
were either preserved in 10% formalin or made into museum study skins with
corresponding complete skulls. I also made study skins of individuals of
species of uncertain taxonomic status that were live-trapped in habitats other
than those where snap trapping was carried out.
In the wet meadow habitat, live trapping started in February 1986 and
continued at monthly intervals through January 1987. I used two parallel
trapping lines in this habitat. Each line was 280 m in length and subdivided
into 20 trap stations separated by 15 m. All traps were placed on the ground,
with even numbered stations having only one Sherman live trap, while odd
numbered stations had one Sherman and one locally made small wire live trap.
Bait was identical to that used in the homogeneous eucalypt forest.
In the eucalypt forest with native subcanopy and the native forested habitats,
the trapping design was identical. In each area, I cut three parallel lines 300 m
in length through the forest; 16 trapping stations were placed along the line
separated by 20 m. I used Sherman live traps and locally made small (15 X 15
X 30 cm) and large (25 X 30 X 60 cm) wire live traps. All traps were placed
within 3.5 m of the trapping post. All trapping posts had a terrestrial small live
trap. Odd numbered trapping posts had a small wire live trap placed in a tree
BULLETIN FLORIDA STATE MUSEUM 34(4)
or bush. Mean arboreal live trap height was 1.2 m. Odd numbered trapping
posts had a Sherman live trap alternating between arboreal and terrestrial
positions. The exterior trapping lines were identical with respect to number,
kind, and placement of traps. I did not use the large live traps on the interior
line. Aside from the large live traps, the exterior and interior lines were equal
in trap number. However, the positions of the Sherman and small live wire
traps were reversed for the interior line. The Sherman live traps were
introduced into each of the forested habitats after the study was well underway
in an attempt to sample smaller bodied species. I placed Shermans in two of
the native forested sites in January 1986 and introduced Shermans in the
remaining forested sites in May of the same year.
I also experimented with traps that were placed in the canopy by a pulley
and platform device. This method was similar to that developed by Malcolm
(pers. comm.) for use in the Brazilian Amazon. Mean trap height was 11.2 m.
I used these arboreal traps to sample the canopy dwelling small mammals.
Traps were located at trapping posts along the established lines. I selected
trees that were to have arboreal platforms in a subjective manner. I placed
traps in trees that I thought had a high degree of canopy connectivity and
upper stratum vine density. I spread 42 arboreal platforms across four native
forested sites. The primary forest sites, RD/C and RD/T, and one of the
mosaic sites, RD/H, each had 12 arboreal traps, 4 traps per line. The other
mosaic site, RD/M, had only 6 traps, because I did not believe that there was
sufficient upper strata development to support canopy dwelling species.
Arboreal canopy trapping started in June 1986 and continued through October
1986. I followed the same schedule in canopy trapping as I had used for
terrestrial and arboreal trapping.
I used dry oatmeal, pineapple chunks, and cotton balls soaked with cod-liver
oil for bait. Traps were set during the day and remained open for five
consecutive nights each month for one calendar year.
Calculations
A first capture was defined as the first occasion that an individual was
trapped and marked. The first capture plus subsequent captures of each
individual were considered total captures. Minimum known alive (MKA) was
the number of individuals actually captured during a particular month whether
the capture was the first capture or a recapture from an earlier session.
Trapping success of small mammals was calculated in the following manner.
The number of traps was multiplied by the number of nights the traps were
baited and armed per site per month to determine the number of trap nights.
Trapping success was the number of first captures, MKA, or total captures of
all species divided by the number of trap nights and expressed in percentages.
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
For example, if 100 individuals were trapped during 1000 trap nights, the
trapping success would be (100/1000) X 100 = 10%. Recapture indices were
calculated by dividing total captures by first captures; thus indicating the
average number of times an individual of each species was captured.
I recorded the following information from each small mammal captured:
date, location on trapping line, position of trap, species, sex, whether a juvenile
or adult, its reproductive condition, general condition, external parasitic load
on a relative scale, and behavior upon release. I also recorded standard body
measurements for each individual: body length, tail, ear, hind foot, and mass.
Numbered metal eartags were placed in the left pinna of each individual upon
the initial trapping of the individual. In general, there was very little evidence
of tag loss. Individuals eartagged from open/field habitat tended to have
higher occurrence of tag loss compared to individuals in forested habitats.
My taxonomic determinations, when in doubt, were checked by taxonomists
specializing in various small mammal groups. Voucher specimens were
distributed to the following people: cricetid rodents and marsupials (genus
Mannosa) were sent to Dr. Phil Myers, University of Michigan; rodents of the
subgenus Oecomys to Dr. Guy Musser, American Museum of Natural History,
and to Dr. Mike Carleton, U.S. National Museum of Natural History.
I used body measurements, mass, reproductive condition, and pelage
characteristics to determine the age class (juvenile or adult) of each captured
individual. An individual was considered an adult if it was reproductively
active. Female rodents were considered reproductively active if they (1) had a
perforated vulva, (2) were pregnant, or (3) were lactating. Marsupial females
were considered reproductively active if they (1) were lactating or (2) had
young attached to the teat field. Male rodents were considered reproductively
active if the testes were descended. I could not determine the reproductive
status of male marsupials as the testes are permanently descended. However,
the activity state of the sternal gland in marsupials can indicate the
reproductive time of year. Initially, I used the overall condition and relative
size of each individual of each sex to assign age classes. Later, I compared my
initial classification with the body measurements and mass. Body
measurements and weights were sorted for each sex of each species and
plotted according to size. I then assigned a body measurement value as the
threshold for separating juvenile and adult age classes. These age classes were
then compared to the initial age classes that were assigned in the field.
I used the General Linear Program (PC-SAS) ANOVA to test for the
equivalence of adult body measurements and mass means between sexes for
each species. This analysis enabled me to determine the extent of sexual
dimorphism for the external characters. Statistical significance was set at <
0.05.
Feeding categories were determined by stomach content analysis (Charles-
Dominique et al. 1981) and from the literature. I relied heavily on information
gleaned from the literature on food preferences of small neotropical mammals.
BULLETIN FLORIDA STATE MUSEUM 34(4)
The use of vertical space (i.e. terrestrial, scansorial, or arboreal) of each
species was determined from three data sets. For each species, I compared the
proportion of captures in trees to that of captures on the ground. There were
more terrestrial than arboreal traps, and this bias was corrected by adjusting
the number of total trapping opportunities. For this adjustment, I divided the
number of arboreal total captures by the total arboreal opportunities (or total
arboreal trap nights). The same was done for terrestrial total captures.
Results of these two divisions were summed, and each respective result (e.g.
arboreal) was divided into the sum. The result generated adjusted percentage
success of arboreal and terrestrial captures. The sum of total captures was
multiplied by the adjusted percentage in order to generate adjusted number of
captures per trapping stratum (on the ground or in arborescent vegetation).
These adjustments also were made for each species at each site as well as
pooled adjustments across all sites. I tested the null hypothesis that there was
no difference in the proportion of arboreal and terrestrial captures for each
species across all habitats as well as within each trapping site. Prior to using
Student's t-test, I adjusted the proportions by an arc-sin transformation. I then
compared the proportion of arboreal and terrestrial responses upon release for
each species across all habitat types. These adjustments were made for all
species in each habitat type.
I used Student's t-tests to test the null hypothesis that there was no
difference in the locomotory response upon release of each species. These two
data sets were then compared to determine if there were any differences
between where an individual was captured and its locomotory behavior upon
release across all habitat types. These tests also were performed for each
habitat sampled. A species was considered to be arboreal if that species was
found to have a high proportion of arboreal captures and a high proportion of
arboreal behavior upon release. The opposite would be true for a terrestrial
species. A species would be scansorial if there were no significant differences
in the proportion of spatial captures and no significant differences in the
proportion of behaviors exhibited upon release. I then compared my results
obtained from the trapping data to the available literature for each species.
RESULTS
Trapping Results
Tables 2, 3, and 4 present the capture results by species for the three habitat
types: native forested, eucalypt with native species subcanopy, and wet meadow
habitats, respectively. As a group, marsupials represented 79.2% of the first
and 83.3% of the total captures in native forested sites and 67.7% and 82.9% in
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
eucalypt forest with native species subcanopy. Rodents represented 97.3% and
98.4% of the first and total captures in the wet meadow habitat.
In the native forested habitat, Marmosa cinerea represented over 40% of
the marsupial captures (Table 2), while in the eucalypt forest this species
represented more than 58% of the marsupial captures (Table 3). Akodon
cursor was the major contributor to the rodent captures in all three habitats.
This species only represented about 7% of the total captures in the native
forested habitat, but 40% of the rodent captures. In the eucalypt forest, A.
cursor represented about 16% of the total captures and 93% of the rodent
captures (Table 3). This rodent was the dominant species captured in the wet
meadow habitat, representing about 85% of both the total and of the rodent
captures.
In both the native and eucalypt forested habitats, marsupials in general
were recaptured at a high rate. Didelphis marsupialis and Marmosa
microtarsus both showed low recapture rates and reflect the small sample size.
Especially noteworthy was the relatively high recapture rate of Marmosa
cinerea (Tables 2 and 3). No individuals of other species, neither rodent nor
marsupial, were recaptured as frequently as individuals of this species. In the
native forested habitat, individuals of M. cinerea were recaptured on the
average 3.1 times, while in the eucalypt forest the average recapture rate for
individuals of this species was 7.7 times.
Akodon cursor was the only rodent that had a relatively high number of
captures and recaptures (Tables 3 and 4). This species had a recapture rate of
1.6 and 3.0 in the eucalypt and wet meadow habitats, respectively.
Trapping Success
Table 5 presents the trapping success by habitat type. Trapping success was
calculated for small mammals in the native forested habitat. The platform
trapping data were excluded. It must be kept in mind that the sampling effort
in each general habitat category was different; however, comparisons of
trapping success are the result of the number of captures relative to the
number of trapping opportunities or nights. Overall, the wet meadow habitat
yielded the highest trapping success (18.8%).
Figure 4 compares the progression of trapping success in the native forest
habitat (without the platform data), the wet meadow habitat, and the eucalypt
forest with subcanopy habitat. Although these three habitats have unequal
sampling effort and trapping design, they were sampled for a one-year period
and show important temporal trends. From the overall gross comparison
portrayed in Figure 4 and the percent trapping success presented in Table 5, in
BULLETIN FLORIDA STATE MUSEUM 34(4)
PERCENT SUCCESS
O I I I I I I I I I I
NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
MONTHS
EUCALYPT -- WET MEADOW -- NATIVE FOREST
Figure 4. Comparison of the trapping success of small mammals in three general habitat types:
eucalypt forest with native species subcanopy, wet meadow habitat, and native forest habitat in
the Rio Doce State Forestry Park, Minas Gerais, Brazil.
NUMBER OF CAPTURES
NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
MONTHS
TOTAL CAPTURES -- MKA CAPTURES -- FIRST CAPTURES
Figure 5. Small mammal capture curves for all native forested trapping sites in Rio Doce State
Forestry Park, Minas Gerais, Brazil. Capture curves include total captures, minimum known
alive (MKA), and first captures.
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
NUMBER OF CAPTURES
NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
MONTHS
TOTAL CAPTURES -- MKA CAPTURES -*-FIRST CAPTURES
Figure 6. Small mammal capture curves for eucalypt forest with a native species subcanopy near
the Rio Doce State Forestry Park, Minas Gerais, Brazil. Capture curves include total captures,
minimum known alive (MKA), and first captures.
NUMBER OF CAPTURES
NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
MONTHS
TOTAL CAPTURES -- MKA CAPTURES -- FIRST CAPTURES
Figure 7. Small mammal capture curves for wet meadow habitat in Rio Doce State Forestry
Park, Minas Gerais, Brazil. Capture curves include total captures, minimum known alive (MKA),
and first captures.
BULLETIN FLORIDA STATE MUSEUM 34(4)
contrast to the wet meadow habitat, it appears that the forested habitats, both
native and exotic, were quite similar in overall percent success and monthly
trapping success. The wet meadow trapping success fluctuated greatly
throughout time, from a high approaching 45% in March and April, to a crash
lower than 10% in May, October, and November.
I plotted the total captures, minimum known alive, and first captures
through time for each of the three habitats. Figure 5 presents the capture
curves for the native forested habitat. Capture rate was relatively low and
stable from November through April, with a noticeable increase in June, July,
and the early part of August. After the first of August, capture rate dropped
back to the levels observed prior to the increase. Figures 6 and 7 compare the
capture rate of small mammals in the eucalypt forest and the wet meadow
habitat, respectively. The highest number of captures at any one time in the
wet meadow habitat was double the highest in the eucalypt forest. However,
the trends were similar. Both habitats showed two pronounced peaks in their
respective capture curves that corresponded to the same months throughout
the year. There was a peak in February, March, and April followed by a crash,
and another peak in June, July, and August followed by another crash.
Trap Types
Overall, trapping success was higher in terrestrial traps than in arboreal
ones (Table 6). Caution should be used in these comparisons as the number of
trap nights are unequal; almost three times the number of terrestrial trap
nights as the number of arboreal ones. However, I feel that some degree of
comparison can be drawn from this analysis based upon the number of
captures relative to the number of trap nights.
Trapping success by trap type varied considerably (Table 6). Small
terrestrial Sherman live traps were the most successful (9.1%), medium
terrestrial traps represented the trap with the greatest number of captures and
trapping opportunities, and large terrestrial live traps were relatively
unproductive.
Arboreal trap type success varied. Small arboreal Shermans were the least
productive arboreal trap type (1.8% success). The arboreal platform traps had
a success rate of 6.3%.
Table 7 reports the number of total captures of each species and the
number of captures per trap type. Odd numbered traps represent terrestrial
traps, and even numbered ones represent arboreal traps. In general, the
number of captures per species in terrestrial and arboreal traps represented
the general use of space for each species. For marsupials, Didelphis
marsupialis and Metachirus nudicaudatus were captured principally in
terrestrial medium live traps (3MT), while Mannosa incana was captured in all
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
trap types except for the large terrestrial and arboreal platform traps.
Marmosa cinerea was captured in all trap types except the large terrestrial
traps. Caluromys philander was trapped principally in arboreal medium live
traps and arboreal platform traps. The sample size for rodents was too small
to allow for clear trapping trends. Akodon cursor is the clear exception. The
small terrestrial Sherman live trap was most effective for this species. This was
mostly a consequence of approximately 80% of all Akodon captures being
made in the wet meadow habitat. Oryzomys subflavus was trapped principally
in terrestrial small Shermans and medium live traps.
SPECIES ACCOUNTS
The small mammal fauna of the park consisted of 6 species of marsupials
and 11 species of rodents. The following accounts present the essential
observations regarding the autecology of each species. Additional natural
history observations of many of these same species are presented by Fonseca
and Kierulff (This volume). The diet, use of vertical space, and habitat
requirements are presented in Table 8 for each species captured during the
study.
SUBCLASS MARSUPIALIA
Family Didelphidae
Didelphis marsupialis Linne (1758)
(Plate 1A)
The black-eared opossum ranges widely in South America from the Isthmus
of Panama to southern Brazil. This species occurs sympatrically with D.
albiventris throughout much of its range (Streilein 1982). In the Rio Doce
Valley, however, D. marsupialis inhabits moister habitats, while D. albiventris
occurs in the cerrado vegetation (Valle and Varejao 1981). A. Gardner (pers.
comm.) suggested that the form of D. marsupialis found in eastern Brazil is
distinct and should be referred to as D. azarae. This species inhabits brush and
forested habitats (Alho 1982; Nowak and Paradiso 1983). Miles et al. (1981)
found this species to be nocturnal, with a preference for nesting in tree cavities.
This species was captured in all forested habitats in the park. Adult body
measurements did not indicate sexual dimorphism (Appendix 1). Females
have a well developed pouch. This species is terrestrial. There was a
significant percentage of terrestrial captures (Table 9) and terrestrial behavior
BULLETIN FLORIDA STATE MUSEUM 34(4)
upon release (Table 10). Several juvenile individuals and one adult were
observed to climb readily. Charles-Dominique (1983) reported that this
species exploits the lower stratum in forests, but can climb. It is basically an
opportunistic feeder and feeds upon fruit and animal matter (Charles-
Dominique 1983).
Metachirus nudicaudatus Geoffroy (1803)
(Plate 1A)
The brown four-eyed opossum has a geographical distribution similar to
that of D. marsupialis except that it is not found over much of Venezuela nor
in northeastern Brazil (Streilein 1982). M. nudicaudatus can be confused with
Philander opossum as both have pale spots above the eyes. In addition, there is
considerable confusion over the taxonomy of the two species. Nowak and
Paradise (1983) classified this species as Philander nudicaudatus and Philander
opossum as Metachirops opossum. I agreed with Honacki et al. (1982) and
followed their classification. This species was captured in all forested habitats
(Table 11). Metachirus nudicaudatus is sexually dimorphic in its mass and hind
foot measurements (Appendix 1). Females do not have a pouch. This species
is strongly terrestrial, rarely caught in arboreal traps (Table 9), and rarely
climbs upon release (Table 10). Miles et al. (1981) found this species to be
nocturnal and construct nests on the forest floor or in ground hollows. There
are very little data on the feeding habits of this species due to the small
numbers that have been reported to be trapped. Preliminary data indicate that
this species is an insectivore-omnivore (Robinson and Redford 1986) or
frugivore-omnivore (Hunsaker 1977).
Marmosa incana (Lund 1840)
This mouse opossum is endemic to the Brazilian Atlantic Rainforest
(Streilein 1982). M. incana occurs in both secondary and primary forest
habitat. This species is small in size (adults average weight = 62 g) and
strongly sexually dimorphic in body size and color. Males tended to have
larger ears and hind feet (Appendix 1) while females tend to have a more rose
colored venter and less pronounced face mask (P. Myers, pers. litt.). Females
do not have a true pouch. This species tended to use both the ground and
arborescent vegetation. I classify the spatial adaptation of this species as
scansorial. There was no significant difference in the proportion of terrestrial
and arboreal captures (Table 9, p > 0.90, df= 169), however; individuals tended
to remain on the ground upon release (Table 10,p < 0.001, df= 145). No data
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
exist on the feeding category of this species. Other species of Marmosa which
have similar body mass are classified as insectivore-omnivores. Stomach
content analysis (n= 3) showed 100% insects from two orders, Coleoptera and
Orthoptera (Table 12). I classify this species as an insectivore-omnivore based
on the relationship found between body mass and dietary classification
(Robinson and Redford 1986).
Marmosa cinerea Temminck (1824)
(Plate 1B)
M. cinerea has a disjunct geographical distribution in South America; it
occurs in northern Venezuela through the Guianas, and it occurs in the
Brazilian Atlantic Rainforest extending into Paraguay (Streilien 1982). M.
cinerea occurs in brush and forested habitat, ranging from secondary to
primary. This species is a large bodied Marmosa (Appendix 1, average
weight= 105 g) and is highly sexually dimorphic based on external body
measurements. Males tended to have larger body, tail, ear, and foot
(Appendix 1). Females do not have a pouch. This species is strongly arboreal
and exploits the high forest stratum (Miles et al. 1981; Charles-Dominique
1983). Miles et al. (1981) found this species to be nocturnal and to construct
open arboreal nests rather than use cavities. M. cinerea tended to be caught a
greater proportion of the time in arboreal traps (Table 9,p < 0.001, df=356)
and tended to exhibit arboreal rather than terrestrial behavior upon release
(Table 10, p < 0.001, df=303). This species is primarily an insectivore-
omnivore (Robinson and Redford 1986).
Marmosa microtarsus Wagner (1842)
This species is restricted to the Brazilian Atlantic Rainforest (Streilein
1982). M. microtarsus differs from its congener M. agilis by possessing a pure
colored white patch of hairs on the throat and chin (Tate 1933). There are
insufficient data in the literature to determine the spatial adaptation of this
species. I only recorded one capture during the study, in an intermediately
disturbed habitat (Table 11). However, the species has a long prehensile tail
and short wide feet which suggest an arboreal lifestyle. This species is
probably an insectivore-omnivore.
BULLETIN FLORIDA STATE MUSEUM 34(4)
Caluromys philander Linne (1758)
(Plate 1B)
This species has a disjunct geographical distribution with populations in
Venezuela, the Guianas and northern Brazil and in southeastern Brazil
(Streilein 1982). The woolly opossum is classified as a forest dwelling species
(Nowak and Paradiso 1983). This species was present in the eucalypt, mosaic,
and primary forested habitats (Table 10). Based upon the external body
measurements, there was no sexual dimorphism in adults (Appendix 1).
Females lack a true pouch. According to Charles-Dominique (1983) and Miles
et al. (1981), this species exploits the high forest stratum and is nocturnal. My
data (based on 51 captures) showed that there was a higher proportion of
arboreal captures (Table 9, p < 0.001, df= 49) and that this species tended to
climb more than remain on the ground upon release (Table 10, p < 0.05,
df=18). Fruit makes up a large portion of this species' diet (Charles-
Dominique 1983; Robinson and Redford 1986).
Suborder Eutheria
Order Rodentia
Oecomys (Oryzomys) trinitatus = (0. concolor) Wagner (1845)
This genus is in need of revision and the subgenus Oecomys is currently
being revised (P. Myers, pers. comm.). This species was previously called
Oryzomys concolor and was known, within Brazil, as an Amazonian species
(Alho 1982). However, Nitikman and Mares (1987) reported trapping this
species in gallery forest in the Brazilian cerrado. I captured this species in all
native forested habitats (Table 11). The species is not sexually dimorphic
(Appendix 1). Gyldenstolpe (1932) and Moojen (1952) stated that this species
is "more or less adapted for arboreal life." My data suggested that this rat is
scansorial; there were no significant differences in the proportion of terrestrial
and arboreal captures (Table 9,p > 0.10, df= 19) and no significant differences
in terrestrial and arboreal behavior upon release (Table 10, p > 0.20, df= 9).
Most species of the genus Oryzomys are frugivore-granivores (Robinson and
Redford 1986).
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Oryzomys subflavus Wagner (1842)
(Plate 2A)
This species is distributed throughout the Guianas, southeastern Brazil, and
eastern Paraguay (Honacki et al. 1982; Alho 1982). In Brazil, it occurs in the
cerrado, caatinga, and Atlantic Rainforest (Alho 1982). This species was
captured in wet meadow and heavily disturbed secondary habitat (Table 11).
There were no differences in body measurements between sexes in adult
individuals (Appendix 1). I classify this species as terrestrial. This species
tended to be captured more on the ground than in the trees (Table 9,p < 0.01,
df=46) and was never observed to climb upon release (Table 10). Stomach
content analysis (n = 1) showed 95% grass and 5% fruit (Table 12).
Oryzomys capitol Olfers (1818)
This species has a wide distribution throughout the neotropics and occurs in
a variety of habitats ranging from agricultural fields (Moojen 1952) to humid
forests (Alho 1982). Oryzomys capitol was primarily captured in humid forests
ranging from intermediate levels of disturbance to primary forests in the park
(Table 11). There were no significant differences in body measurements
between sexes for adults (Appendix 1). My capture and release data are in
accordance with Alho's (1982) terrestrial classification for this species. 0.
capitol tended to be caught more on the ground than in trees (Table 9, p <
0.05, df= 19) and tended to remain on the ground upon release (Table 10, p <
0.001, df= 11).
Oryzomys (Oligoryzomys) nigripes (eliurus) Wagner (1845)
This small-bodied rodent (Appendix 1) occurs in grassland, wet meadow,
and secondary forest habitat in northern Argentina, eastern Paraguay, southern
Brazil, and the Bolivian Beni (Honacki et al. 1982). In the Park, all captures
were made in the wet meadow habitat (Table 11). All captures were made on
the ground (n=4), however; the individuals climbed readily in captivity (pers.
obs.). The results from the stomach analysis (n=5) revealed a wide range of
foodstuffs (Table 12).
BULLETIN FLORIDA STATE MUSEUM 34(4)
Abrawayaomys ruschii Cunha and Cruz (1979)
(Plate 2A)
This species is only known from the type locality in Espirito Santo, eastern
Brazil. It is endemic to the Brazilian Atlantic Rainforest. The single capture
of this species was'recorded in an intermediately disturbed forest (Table 11).
There is very little information available regarding the ecology of this species,
and there are only three study skins found in museums (A. Gardner, pers.
comm.).
Rhipidomys mastacalis Lund (1840)
(Plate 2B)
Climbing mice range south from Margarita and Tobago islands to
Venezuela and Guianas to northeastern and east central Brazil (Honacki et al.
1982). This species was only captured in a relatively undisturbed primary
forest (Table 11). Sample size was too small to detect any differences between
terrestrial and arboreal captures and behavior upon release. However, as the
common name implies, this species climbs readily. I captured two individuals
in my house in the park, a commonly cited "exotic" habitat for this species
(Nowak and Paradiso 1983).
Nectomys squamipes Brants (1827)
The neotropical water rat occurs in aquatic habitats either in grasslands and
wet meadows or in forests. This species' distribution ranges from the Guianas
to Colombia to Peru and in Brazil, Paraguay, and northeastern Argentina
(Honacki et al. 1982). It tended to be caught more on the ground (Table 9, p
< 0.05, df= 17) and exhibited a significant tendency to remain on the ground
upon release (Table 10, p < 0.001, df= 10). Stomach content analysis (n=2)
showed 50% grass and stems and 50% fruit (Table 12).
Akodon cursor Winge (1887)
(Plate 2B)
This species occurs in several habitat types from southeastern and central
Brazil to Uruguay, Paraguay, and northern Argentina. The wet meadow
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
habitat in the park was the primary habitat to capture this species (Table 11).
A. cursor was formerly included in A. arviculoides (Honacki et al. 1982). This
species is sexually dimorphic in tail (p < 0.01) and body (p < 0.008) length
(Appendix 1). A. cursor is strongly terrestrial (Table 9 and Table 10). Analysis
of stomach contents (n=23) revealed a high proportion of insects, seeds and
fruit (Table 12).
Calomys laucha Olfers (1818)
This species occurs in grassland and wet meadows in southern Bolivia,
southeastern Brazil, Paraguay, central Argentina, and Uruguay. This species
was only captured in the wet meadow habitat in the Park (Table 11). The
results from one stomach sample revealed 100% seeds (Table 12).
Oxymycterus roberti Thomas (1901)
The burrowing mouse occurs in a variety of habitats but is usually
associated with moist substrate in open or brush habitats. This species was
captured in both wet meadow and secondary forest habitats in the Park (Table
11). This species is endemic to eastern Brazil. This semifossorial mouse is
described as an insectivore (Nowak and Paradisio 1983). Stomach analysis
(n=2) revealed 100% insects (Table 12).
Family Caviidae
Caviafulgida Wagler (1831)
This species of cavy is endemic to the open grasslands and wet meadows of
the Atlantic Rainforest of eastern Brazil (Honacki et al. 1982; Nowak and
Paradise 1983). I captured this species in grassland and wet meadow habitats
in the Park, however; it was not trapped in site RD/B. For this reason this
species does not appear in Table 11. Cavies are terrestrial and are herbivore-
grazers (Nowak and Paradiso 1983).
BULLETIN FLORIDA STATE MUSEUM 34(4)
Family Echimyidae
Euryzygomatomys spinosus Fischer (1814)
The single species of guiara is endemic to southeastern Brazil, Paraguay,
and northeastern Argentina (Honacki et al. 1982). I captured this species in
the wet meadow habitat (Table 11). This species inhabits open grasslands and
wet meadows, is considered terrestrial or semifossorial (Alho 1982), and is
most probably a herbivore-grazer.
DISCUSSION
The trapping success realized in this study for neotropical humid forests
falls within the range of observed success rates (Table 13). However, one
striking difference between this and other neotropical small mammal studies
was the high number of marsupial captures relative to rodent captures. All
reported studies show rodent biases and usually high captures of rodents
relative to marsupials. Only Emmons (1984) reported a marsupial to rodent
capture ratio approaching equality.
Trapping results from small mammal studies in southeastern Brazil varied
considerably with respect to marsupial and rodent biased captures. Only
Fonseca (pers. comm.) has reported marsupial biased trapping results from a
variety of native forest sites in eastern Minas Gerais. Avila-Pires (1978)
captured 245 rodents and 40 marsupials from the Rio Doce Park. Gastal
(1982) reported that five species of marsupials were captured in the Park but
gave no comparative data for rodents. Dias (1982) trapped more rodents than
marsupials in the Rio Doce Valley in Minas Gerais. Davis (1945) trapped 58
didelphid marsupials and 285 rodents in his study site in Rio de Janeiro.
Hunsaker (1977) stated that marsupials require considerable effort to trap.
Perhaps one explanation for the observed high marsupial capture rate could be
due to the habitat type found in the Park. Charles-Dominique (1983)
suggested that didelphid marsupials can reach high local densities in areas of
abundant food resources. He postulated that these species are r-strategists and
are adapted to the "unstable environment of secondary forests." There is very
little primary habitat in the Park relative to secondary habitat. Most of the
forest habitat in the Park has been altered by fire in the recent past. The
primary forest plots that I sampled yielded the lowest species richness and
absolute captures of didelphid marsupials relative to the other secondary
forested habitats (Stallings 1988). In Panama, Didelphis marsupialis tended to
occur at higher densities in primary forest, while Caluromys and Philander
were found at higher densities in secondary forest than primary forest
(Fleming 1972).
STALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Marsupials were recaptured with relative high frequency in this study,
especially Metachirus nudicaudatus, Mannosa incana, and Marmosa cinerea.
My recapture data on marsupials agreed with data reported by Fleming (1972,
1973), August (1984), and to some degree with that found by O'Connell (1979).
These data were not in accord with Hunsaker (1977), who stated that didelphid
marsupials are difficult to recapture. For example, individuals of Marmosa
cinerea were captured on the average 7.7 times in the eucalypt forest with
native subcanopy habitat. This high recapture rate could be an artifact of the
habitat. This trapping site was surrounded by habitat unsuitable for arboreal
species. In essence, this habitat was a forested island. On one side there was a
monoculture of Eucalyptus saligna with no subcanopy, on another a marsh
converted to a rice field, and the other two sides of the forest were bounded by
pasture. Also, the subcanopy offered more food and resting opportunities than
did the homogeneous eucalypt canopy. Perhaps the inability to move far
beyond the limits of the forest and the location of the optimal habitat within
the forest help explain the observed recapture rate.
Another obvious difference between this study and other inventories
conducted in neotropical native forests was the absence of echimyid rodents.
Species of the genus Proechimys are the most widespread taxa of the family
Echymidae in the neotropics (Hershkovitz 1969). These forest species are
terrestrial and usually appear on species lists from forest inventories. In
Panama, Proechimys was a common forest capture (Eisenberg and Thorington
1973; Glanz 1982). Handley (1976) reported Proechimys as a common species
in Venezuela. Emmons (1984) and Terborgh et al. (1986) reported captures of
Proechimys from forested sites in Peru and Ecuador.
There are several reports of Proechimys captures in Brazilian tropical moist
forests. Laemmert et al. (1946), Emmons (1984), Carvalho (1965), Miles et al.
(1981) and Malcolm (pers. comm.) reported Proechimys in their inventories
from the Brazilian Amazon. In the Atlantic Forest, Davis (1945) and Fonseca
(1988) reported two species of Proechimys from their studies in the states of
Rio de Janeiro and Minas Gerais, respectively. Dias (1982) trapped one
species of Proechimys in three study areas in the Rio Doce Valley. I did not
capture one individual of Proechimys from the Park in approximately 35,000
trap nights from 1985 to 1986, nor from an additional 30,000 trap nights from
1986 to 1987 (unpubl. data).
One explanation could be the presence of predators in the Park. Eisenberg
(1980) speculated that the abundance of rodents in some neotropical sites and
the paucity of rodents in other sites could be the result of the absence or
presence of top predators, respectively. Hershkovitz (1969) stated that species
of the genus Proechimys "are the basic source of protein for lowland predators
in the Brazilian subregion." The felid community in the Park is intact. All the
felids have been observed by field workers in the recent past. I saw spoor from
jaguar, puma, ocelot, Geoffroy's cat, and jaguarundi.
BULLETIN FLORIDA STATE MUSEUM 34(4)
The results from the wet meadow habitat were consistent with the literature
(Table 13). In every study, there were more rodent captures than marsupial
captures. In this study, Akodon cursor was the dominant species in terms of
absolute numbers and captures. O'Connell (1981) reported that
Zygodontomys, an ecological equivalent of Akodon, was the dominant rodent in
grass habitat in Venezuela and represented 85% of the total rodent captures.
However, one difference between this study and others was the observed high
trapping success. As can be observed from Table 10, Akodon cursor made up
85% of the captures and was largely responsible for the high trapping success.
One explanation for the high capture rate could be due to the shape and
amount of the available grass or wet meadow habitat in the Park. This habitat
type occurs particularly at the bases of hills and on the perimeter of the
swamps and lake edges. There are no vast areas of this habitat type in the
park, and these areas commonly take on a long and narrow shape following the
contour lines. There was a high degree of habitat specificity exhibited by the
species captured in this habitat. Grassland rodents can achieve high local
densities, and perhaps this fact, coupled with the populations being compressed
and compacted in narrow and small habitat, helps to explain the observed high
trapping success in the wet meadow habitat.
The eucalypt forest with native subcanopy habitat yielded surprising results.
I did not expect to find many small mammals in this habitat because of
"plantation effects." However, seven species of small mammals were captured,
five of which were marsupials. In fact, the marsupial/rodent capture ratio was
similar to that observed in the native forested habitat (Table 14). Dietz et al.
(1975) captured two species of terrestrial rodents, Oryzomys nigripes and
Akodon cursor, in homogeneous eucalypt forest with grass/bamboo
undergrowth. They reported a total of five species, only one of which was not
strictly terrestrial, in their two native forested habitats. The plantation habitats
in Dietz et al. (1975) and in this study are similar in that both treated eucalypt
plantations of similar age and that in both the terrestrial substrate was covered
by grass. The major difference was the native species subcanopy in this study.
I captured a relatively high number of terrestrial rodents and marsupials and a
high number of arboreal marsupials, but no arboreal rodents. The native
species subcanopy could be considered a secondary forest sere, if the emergent
eucalypt stratum was ignored. Charles-Dominique's (1983) hypothesis that
didelphid marsupial abundance increases in secondary habitat would explain
the high numbers of marsupials captured in this study.
The temporal capture results from the native forested habitat suggest that
seasonality is important with respect to the trappability of small mammals.
The trapping data show a pronounced peak in the total number of captures,
MKA, and first captures for the native forested habitat during the cool, dry
winter. Davis (1945) reported a similar trend and suggested that this was the
result of more younger individuals present in the trapping pool or because of a
paucity of natural food items during this time of year. My data do not support
ALLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
' the hypothesis that more younger individuals explain the pronounced increase;
rather it appears that food resource paucity results in the increase (unpubl.
data).
The eucalypt and wet meadow habitats both produced peaks in the cool, dry
winter and again in the late summer. These two habitats might have yielded
similar capture curves because they share a grass substrate. Akodon cursor was
an important component of both habitats and is an insectivore/omnivore that
is reported to use a high proportion of grass and grass seed in its diet (Nowak
and Paradiso 1983). Marmosa incana and Metachirus nudicaudatus are
insectivore/omnivores and frugivore/omnivores, respectively, and perhaps
track insect availability in grass substrate. The grass species did not produce
seeds until late May. Thus, perhaps the peak observed in February, March and
April can be explained by the lack of food for both rodents and marsupials.
The second peak, which occurred in June, July, and August, could also be
explained in terms of a decrease in food availability. Insect and fruit
availability are usually low during the hibernal period in seasonal neotropical
forests (e.g. Janzen and Schonener 1968). The marsupial species rely heavily
on these food resources. The results of a preliminary stomach content analysis
on Akodon, suggest that insects are important items in this species diet
(unpubl. data). Graminoids in this habitat were dry, and seeds were not as
readily available as they were during April and May.
Data analysis of trap type revealed that terrestrial small Sherman live traps
were very productive in the wet meadow habitat but yielded relatively few
captures in the forested habitats. Arboreal small Shermans were relatively
unproductive in the forested habitats. Large terrestrial live traps were
unproductive in the forested habitats. The most productive trap types in the
forested habitats were the medium sized terrestrial and arboreal traps and the
arboreal platform traps. Some individuals of species that are considered
terrestrial were captured in arboreal traps. Apparently these instances resulted
when low arboreal traps were easily accessible from the ground by either a vine
or log.
No additional species were added to the inventory list by using the arboreal
platform traps. However, these traps increased the capture frequency for the
highly arboreal marsupial Caluromys philander. In total, I recorded 49
captures for this species in both the eucalypt with native species subcanopy and
the native forested habitats. In the latter habitat, however, Caluromys was
captured only five times in the terrestrial and low arboreal traps, as compared
with 29 times in the arboreal platform traps. Clearly, the abundance of this
species would have been underestimated if arboreal traps had not been used.
Malcolm (per. comm.) obtained similar results with platform traps in Manaus.
Mannosa cinerea was also trapped with relatively high frequency in this trap
type. The use of arboreal platforms for trapping small mammals was first
described by Davis (1945) and Laemmert et al. (1946). Unfortunately, the
relative success of arboreal traps could not be determined from these studies.
BULLETIN FLORIDA STATE MUSEUM
It was surprising to find such a high frequency of Caluromys in the
eucalypt forest. Although this arboreal frugivore is quite common in native
forests, it was not expected in an exotic monoculture plantation. Presumably
its principal food resources came from the native species subcanopy. This
interpretation gains support from the fact that this species also was captured
in terrestrial and low arboreal traps, suggesting that this species regularly
moved down through the subcanopy.
The results of this small mammal inventory give substance to previous
impressions of a highly diverse and endemic Atlantic Forest fauna. These
results also demonstrate the important role that didelphid marsupials play in
the community structure of small mammals in one of the largest remaining
tracts of native Atlantic Forest in Brazil. Wet meadow habitat in this region
supports many rodents, although Akodon cursor dominates. Eucalypt forests
with native species subcanopy can play an important role in conserving small
mammal communities in a region greatly altered by monocultural
plantations.
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GS: BRAZILIAN SMALL MAMMAL INVENTORIES
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BULLETIN FLORIDA STATE MUSEUM 3
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464.
INGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Table 1. Forested and open/field habitats in the Rio Doce State Forestry Park, Minas Gerais,
Brazil. Habitats follow Gilhaus (1986).
Habitat Type
% Total
FORESTED HABITATS
Tall Primary Forest with Epiphytes 8.4
Tall Forest 30.0
Medium to tall Forest with Bamboos and Graminoids 30.6
Medium Secondary Forest with Bamboos and Graminoids 17.2
Low Secondary Forest 0.1
OPEN/FIELD HABITATS
Low Woodland 1.1
Low Tree and Scrub Tallgrass Savanna 0.6
Tallfern Field 0.1
Evergreen Tallgrass Field with Typha sp. 3.0
Partially Submerged Shortherb Field and Aquatic Habitat 8.9
100Z
Table 2. Capture results from native forested plots in Rio Doce State Forestry Park, Minas
Gerais, Brazil. RECAP INDEX= total captures/first captures, and represents the average
number of times that an individual of species X is captured. Numbers in parentheses represent
percent of contribution of capture per species per taxonomic group.
Total First Recap
Species Captures % Total Captures % Total Index
MARSUPIALS
Didelphis marsupialis 35 4.5 (5.4 32 7.89.9 1.1
Metachirus nudicaudatus 140 18.0 (21.6 91 22.3 (28.1 1.5
Marmosa incana 154 19.8 (23.8 90 22.1 (27.8 1.7
Marmosa cinerea 283 36.4 (43. 92 22.5 28.4 3.1
Marmosa microtarsus 1 0.1 0.2 1 0.2 0.3 1.0
Caluromys philander 34 0.4 5.3 18 4.4 5.5 1.9
7 32(0 24 79.4(100.0)
RODENTS
Nectomys squamipes 15 1.9 (11.5 9 2.2 (10. 1.7
Rhidpidomys mastacalis 7 0.9(5.4 3 0.73.6 2.3
Akodon cursor 52 6.7 40.0 27 6.6 2.1 1.9
Oecomys trinitatis 21 2.7 13.8 19 4.7 22.6 1.1
Oryzomys capitol 18 2.3 13.8 15 3.7 (17.9 1.2
Oryzomys subflavus 13 1.7 (10.0 7 1.7 8.3 1.9
Oxymycterus roberti 3 0.4 2.3 3 0.7 3.6 1.0
Abrawayomys ruschii 1 0.1 0.8 1 0.2 1.2 1.0
W30 16.( .0 m 20610
BULLETIN FLORIDA STATE MUSEUM
Table 3. Capture results from eucalypt forest with native forest subcanopy. RECAP INDEX=
total captures/first captures and represents the average number of times that an individual of
species X is captured. Numbers in parentheses represent percent of contribution of capture per
species per taxonomic group.
Total First Recap
Species Captures % Total Captures % Total Index
MARSUPIALS
Didelphis marsupialis 7 4.4 (5.3) 3 5.6 (8.3) 2.3
Metachirus nudicaudatus 18 11.4 13.7 9 16.7 25.0) 2.0
Marmosa incana 14 8.7 10.7) 8 14.8 22.2) 1.8
Marmosa cinerea 77 48.7 58.8 10 18.5 27.8) 7.7
Caluromysphilander 15 9.6 11.5 6 11.1 16.7 2.5
7 00 66.7(00
RODENTS
Akodon cursor 25 15.8(92.6) 16 29.6 (88.9) 1.6
Olyzomys capitol 2 1.4 7.4) 2 3.7 11.1 1.0
717.2(100.0) 33.3(100.0)
Table 4. Capture results from wet meadow site in Rio Doce State Forestry Park, Minas Gerais,
Brazil. RECAP INDEX= total captures/first captures and represents the average number of
times an individual of species X was captured. Numbers in parentheses represent percent
contribution of captures per species per taxonomic group.
Total First Recap
Species Captures % Total Captures % Total Index
MARSUPIALS
Marmosa incana 3 0.8(50.0) 2 1.3 50.0 1.5
Marmosa cinerea 1 0.3 (16.7) 1 0.7 (25.0 1.0
Caluromys philander 2 0.5 33.3) 1 0.7 (25.0 2.0
R5- 1.6(100.0) -7 2.7(100.0)
RODENTS
Nectomys squamipes 5 1.3 1.4 4 2.7 2. 1.3
Akodon cursor 315 84.5(85.8 105 70.0 (71.9 3.0
Oryzomys capitol 1 0.3 0.3 1 0.7(0. 1.0
Oryzonys subflavus 31 8.3 8.4 22 14.7 (15.1 1.4
Oryzomys nigripes 4 1.0 1.1 4 2.7 2. 1.0
Calomys laucha 4 1.0 1.1 4 2.7 2.7 1.0
Oxymycterus roberti 4 1.0 1.1 4 2.7 2.7 1.0
Eutyzygomatomys spinosus 2 0.5 0.5 2 1.3 1.4 1.0
73 98.4(100.0) 97.300
.LINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Table 5. Trapping success of small mammals calculated by habitat category in Rio Doce State
Forestry Park, Minas Gerais, Brazil.
Habitat Number of Number of
Category Trap Nights Captures % Success
Native forest (excluding platforms) 30,960 710 2.3
Native forest, platforms only 1,050 66 6.3
Wet meadow 1,980 373 18.8
Eucalypt forest w/native species
Subcanopy 6,000 158 2.6
Eucalypt forest w/no subcanopy 500 1 0.0
TOTALS 40,490 1,308
Table 6. Trapping success by trap type for all species in all habitat types. Trap types are
arranged according to trapping location: terrestrial or arboreal. Trap types are as follows:
1ST= small terrestrial Sherman live trap; 3MT= medium sized terrestrial live trap; 5LT= large
terrestrial live trap; 2SA= small arboreal Sherman live trap; 4MA= medium sized arboreal live
trap; 6PA= arboreal platform trap.
No. No. Percent
Trap Type Captures Trap Nights Success
TERRESTRIAL
1ST 370 4,080 9.1
3MT 553 18,000 3.1
5LT 42 5760 0.7
5 3.2
ARBOREAL
2SA 48 2,640 1.8
4MA 228 8,640 2.6
6PA 66 1050 6.3
0 2.8
BULLETIN FLORIDA STATE MUSEUM
Table 7. Trap response by species across all habitat types. Trap types are explained in Table 6.
Trap Types
Species Total 1ST 2SA 3MT 4MA 5LT 6AP
Didelphis marsupialis 42 0 0 24 2 15 1
Metachirus nudicaudatus 158 0 0 129 3 26 0
Marmosa incana 171 13 14 106 38 0 0
Marmosa cinerea 361 2 29 145 150 0 35
Caluromys philander 51 0 0 9 13 0 29
Marmosa microtarsus 1 0 0 0 1 0 0
Nectomys squamipes 19 4 0 13 1 1 0
Ripidomys mastacalis 7 0 0 3 3 0 1
Akodon cursor 392 312 2 78 0 0 0
Oecomys trinitatis 21 1 3 9 8 0 0
Oryzomys capitol 21 8 0 11 2 0 0
Oxymycterus roberti 10 7 0 3 0 0 0
Abrawayaomys ruschii 1 0 0 0 1 0 0
Oryzomys subflavus 44 18 0 20 6 0 0
Calomys laucha 2 2 0 0 0 0 0
Oryzomys nigripes 4 3 0 1 0 0 0
Euryzygomatomys spinosus 2 0 0 2 0 0 0
Totals ~T 7 M7 -4 "53 2 66
Percentages 28.3 3.7 42.3 17.4 3.2 5.0
Table 8. Ecological place of each species captured during this study in the Rio Doce State
Forestry Park. GM= grasslands and wet meadows, B= brushy areas, S= secondary forests, P=
primary forests, F= fossorial or semifossorial, SA= semiaquatic, T= terrestrial, S= scansorial,
A= arboreal, HG= herbivore-grazer; FG= frugivore-granivore; FO= frugivore-omnivore; 10=
insectivore-omnivore.
Spatial Dietary
Species Habitat Adaptation Classification
MARSUPIALS
Didelphis marsupialis B, S, P T, S FO
Metachirus nudicaudatus S, P T IO/FO
Marmosa incana* B, S, P S
M. cinerea B, S, P A IO
M. microtarsus* S, P A IO
Caluromys philander S, P A FO
RODENTS
Oecomys trinitatis S, P S FG
Oryzomys capitol S, P T FG
0. subflavus* GM, B, S T FG
0. nigipes* GM,B S FG
Akodon cursor* GM, B, S T IO
Calomys laucha GM, B T FG
Nectomys squamipes GM, B SA HG
Abrawayaomys ruschii* S T FG?
Oxymycterus roberti* GM, B, S F IO
Rlipidomys mastacalis S, P A FG
Cavia fulgida* GM, B T HG
Euryzygomatomys spinosus* GM, B F HG
* Taxa endemic to the Brazilian Atlantic rainforest or the eastern coastal area of South America.
190
LLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Table 9. Student's t-tests between adjusted and arcsin transformed percentages of terrestrial and
arboreal captures of small mammals in all forest types. NS = non significant.
% Terrestrial % Arboreal
Species Captures Captures V P <
Didelphis marsupialis 66.6 23.5 40 .001
Metachirus nudicaudatus 76.3 3.9 156 .001
Marmosa incana 43.9 46.1 169 NS
Marmosa cinerea 27.8 62.2 356 .001
Caluromys philander 16.3 73.8 49 .001
Nectomys squamipes 69.6 21.0 17 .050
Rhipidomys mastacalis 28.8 61.1 5 NS
Akodon cursor 83.5 6.3 390 .001
Oecomys trinitatis 31.2 58.8 19 NS
Oryzomys capitol 62.9 27.0 19 .050
Oryzomys subflavus 58.0 32.5 46 .010
Table 10. Results of Student's t-tests between terrestrial and arboreal behavior upon release of
small mammals captured in all habitats. NS= non significant. Species abbreviations are
explained in Table 8.
% Terrestrial % Arboreal
Species N Behavior N Behavior V T P <
DM 33 73.2 3 16.7 34 3.265 0.01
MN 150 80.7 4 9.1 152 4.934 0.001
MI 95 53.5 52 36.5 145 3.448 0.001
MC 11 10.8 294 78.9 303 7.743 0.001
CP 2 18.4 18 71.6 18 2.488 0.05
NS 12 90.0 0 0.0 10 10.882 0.001
RM 1 24.0 5 67.8 4 1.393 NS
AC 70 90.0 0 0.0 68 26.282 0.001
OT 9 64.8 2 25.3 9 1.763 NS
OC 13 90.0 0 0.0 11 11.326 0.001
OS 10 90.0 0 0.0 8 9.933 0.001
BULLETIN FLORIDA STATE MUSEUM
Table 11. Number of total captures and percent of total for each species (SPP.) per habitat type.
Numbers in parentheses represent the percentage of captures per species per habitat percentages
are rounded to the nearest whole number.
Habitat Types +
SPP* RD/F RD/H RD/M RD/T RD/C RD/E RD/B
DM 4(3 2(1 1(1 7(6 21 7
MI 25(18 75(27 2014 2822 6 14 3 (1)
MC 7452 71 26 649 383 31(35 77(49 1 (0
MM 0
CP 16 6 2 1) 13(10) 3 (3) 15(10) 2 (1
NS 6 2 9(6) 5(1)
RM 7(6)
AC 3(2) 46(17) 21 (1 25(16) 315(85)
OT 4(3) 8(3) 4 3(2) 2 (2)
OC 4 12(9) 2(2 2(1)
OS 12 (9) 1(0) 31
ON 4
OR (0) 2(1) 4
AR 1(0)
CL 4
ES 2(1)
142 276 142 128 89 158 373
RD/F= secondary habitat burned completely to the ground; RD/H= secondary habitat
burned in mosaic fashion; RD/M= secondary habitat burned in mosaic fashion; RD/T= primary
forest with little effect from forest fire; RD/C= primary forest; RD/E= eucalypt forest with
native species subcanopy; RD/B= wet meadow.
* DM= Didelphis marsupialis; MN= Metachirus nudicaudatus; MI= Marmosa incana; MC=
Marmosa cinerea' MM= Marmosa microtarsus; CP= Caluromys philander; NS= Nectomys
squamipes; RM= Rhipidomys mastacalis; AC= Akodon cursor; OT= Oecomys trinitatis; OC=
Oryzomys capitol; OS= Oryzomys subflavus; ON= Oryzomys nigripes; OR= Oxymycterus roberti;
AR= Abrawayaomys ruschii; CL = Calomys laucha; ES= Euryzygomatomys spinosus.
LLINGS: BRAZILIAN SMALL MAMMAL INVENTORIES
Table 12. Stomach content analysis of small mammals captured in Rio Doce State Forestry
Park, Minas Gerais, Brazil (N= number of stomachs analyzed).
Species % Fruit % Seeds % Grass % Insects
Marmosa incana (n=3) 100
Akodon cursor (n= 23) 19 19 8 52
Oryzomys subflavus (n = 1) 5 95
Oryzomys nigripes (n= 5) 34 11 21 34
Oxymycterus roberti (n = 2) 100
Calomys laucha (n = 1) 100
Nectomys squamipes (n = 2) 50 50
Table 13. Percent capture by taxonomic group, trapping success, and number of trap nights by
habitat type for this study compared to other neotropical field studies. % M= percent of total
marsupial captures; % R= percent of total rodent captures; % T.S.= percent trapping success; #
T.N. = number of trap nights.
Study Site % M % R % T.S. # T.N.
NATIVE FOREST
This study Brazil 83.2 16.8 2.3 30,960
Dietz et al. 1975 Brazil 9.3 90.7
Carvalho 1965 Brazil 0.3 99.7 3.6 10,080
Emmons 1984 Peru 48.0 52.0 6.9 2,987
Emmons 1984 Peru 7.0 4,390
Emmons 1984 Brazil -- --- 0.8 434
Dias 1982 Brazil 2.3 97.7 -
Nitikman and Mares 1987 Brazil 30.7 69.3 6.0 12,170
Laemment et al. 1946 Brazil 31.0 69.0 10.0 30,000
August 1984 Venezuela 25.0 75.0 0.9 30,269
Davis 1945 Brazil 17.0 83.0
Fleming 1972, 1973 Panama 19.0 81.0 16.0 24,732
O'Connell 1979 Venezuela 12.0 88.0 -
WET MEADOW/SAVANNA/PANTANAL
This study Brazil 2.0 98.0 18.8 1,980
August 1984 Venezuela 0.0 100.0 1.9 3,660
August 1984 Venezuela 25.0 75.0 0.1 4,400
Lacher and Alho, in press Brazil 0.0 100.0 4.2 3,582
Borchert and Hanson 1983 Brazil 0.0 100.0 3.5 4,173
O'Connell 1981 Venezuela 10.0 90.0 --- --
HOMOGENEOUS EUCALYPT FOREST
Dietz et al. 1975 Brazil 0.0 100.0 -
EUCALYPT FOREST WITH NATIVE SUBCANOPY
This study Brazil 83.0 17.0 2.6 6,000
BULLETIN FLORIDA STATE MUSEUM
Appendix 1. Standard body (mm) and mass (g) measurements for species of small mammals
captured in Rio Doce State Forestry Park, Minas Gerais, Brazil. Measurements are presented
for adults of both sexes. N=sample size, MIN=minimum measurement, MAX=maximum
measurement, MEAN + SD=arithmetic mean and one standard deviation. Significant
differences in measurements between sexes for each species are designated by (p < 0.05) and
* (p < 0.001).
N MIN MAX MEAN + SD
Didelphis marsupialis -- ADULTS, HINDFOOT > 51mm
MALES
MASS 9 578.00 1300.00 938.89 +295.32
BODY 9 292.00 415.00 354.78 + 39.98
TAIL 9 312.00 393.00 355.33 + 28.41
EAR 9 47.00 55.00 50.67 + 2.78
FOOT 9 51.00 63.00 57.89 + 4.20
FEMALES
MASS 8 568.00 1855.00 1158.62 +369.98
BODY 8 335.00 400.00 372.87 + 24.82
TAIL 8 345.00 400.00 377.25 + 18.01
EAR 8 46.00 58.00 51.37 + 3.93
FOOT 8 51.00 64.00 57.87 + 4.97
Metachirus nudicaudatus ADULTS, MASS > 90 g
MALES
MASS* 35 102.00 480.00 281.51 +117.00
BODY 35 170.00 300.00 233.89 + 36.76
TAIL 35 227.00 373.00 307.66 + 41.67
EAR 35 28.00 40.00 35.40 + 2.66
FOOT** 35 35.00 52.00 43.71 + 3.86
FEMALES
MASS 51 91.00 345.00 235.88 + 68.93
BODY 50 150.00 265.00 222.93 + 28.56
TAIL 51 178.00 363.00 297.96 + 43.19
EAR 50 31.00 43.00 35.72 + 2.62
FOOT 51 34.00 47.00 41.35 + 2.96
Marmosa incana -- ADULTS, MASS > 35 g
MALES
MASS 46 35.00 130.00 66.04 + 27.74
BODY 46 95.00 192.00 138.00 + 21.96
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