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Activity pattern of Atlantic Forest small arboreal mammals as revealed by

camera traps
Luiz Gustavo R. Oliveira­Santos, Marcos A. Tortato and Maurício E. Graipel

Journal of Tropical Ecology / Volume 24 / Issue 05 / September 2008, pp 563 ­ 567

DOI: 10.1017/S0266467408005324, Published online: 08 September 2008

Link to this article: http://journals.cambridge.org/abstract_S0266467408005324

How to cite this article:

Luiz Gustavo R. Oliveira­Santos, Marcos A. Tortato and Maurício E. Graipel (2008). Activity pattern of Atlantic Forest small
arboreal mammals as revealed by camera traps. Journal of Tropical Ecology, 24, pp 563­567 doi:10.1017/
S0266467408005324

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Journal of Tropical Ecology (2008) 24:563–567. Copyright © 2008 Cambridge University Press
doi:10.1017/S0266467408005324 Printed in the United Kingdom

SHORT COMMUNICATION
Activity pattern of Atlantic Forest small arboreal mammals as revealed
by camera traps

Luiz Gustavo R. Oliveira-Santos∗,1 , Marcos A. Tortato† and Maurı́cio E. Graipel‡

∗ Programa de Pós-graduação em Ecologia e Conservação, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Mato Grosso do Sul, Brazil
† Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biologia, Universidade Federal do Paraná, Brazil
‡ Departamento de Ecologia e Zoologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Brazil
(Accepted 23 July 2008)

Key Words: arboreal, canopy, Didelphis albiventris, Juliomys pictites, marsupial, Micoureus paraguayanus, niche, rodent,
scansorial

Even though the great majority of the biomass and
diversity of mammals in tropical forests inhabit the
canopy (Eisenberg & Thorington 1973), most knowledge
of this group is based on forest-floor samples (Lowman &
Moffett 1993). Studies that include trapping efforts in the
canopy are becoming increasingly common (Grelle 2003,
Lambert et al. 2005, Malcolm 1995, Patton et al. 2000,
Vieira & Monteiro-Filho 2003, Voss et al. 2001), but
aspects on the ecology of arboreal small mammals still
remain poorly understood. Many species of non-flying
mammals co-occur in the canopy and, thus, are expected
to use niche dimensions differently to permit coexistence
(Cameron et al. 1979). Despite the difficulties of access
to and in understanding the three-dimensional use of the
arboreal strata by the different species (Emmons 1995),
some studies have demonstrated that the differential use
of the habitat (Cunha & Vieira 2002, Gentile & Fernandez
1999), of food items (Cáceres et al. 2002, Santori et al.
1995) or both (Leite et al. 1996, Mauffrey & Catzeflis
2003), include strategies involved in the division of
resources.
Few studies in Brazil have shown the importance of
the activity period on the division of the niche (Graipel
et al. 2003). However, the time of activity may be one of
the most relevant strategies for the coexistence of species
(Schoener 1974). Knowledge of circadian activities of
small mammals is normally granted by means of simple
classifications, such as those of diurnal and nocturnal
activity patterns (Olmos 1991). The objectives of this
study were (1) to describe the period of activity of the
1Corresponding author, at Vila Ipiranga, Campo Grande MS, Brazil.
Email: gu_tapirus@hotmail.com
white-eared opossum (Didelphis albiventris), the long-
furred woolly mouse opossum (Micoureus paraguayanus),
and the lesser Wilfred’s mouse (Juliomys pictipes), which
occupied the arboreal strata of the Atlantic Forest; (2)
to analyse the strategies in the partitioning of resources
among D. albiventris and M. paraguayanus; and (3) to
discuss the innovative use of camera-traps directed to
suspended platforms in studies about the activity of
arboreal and scansorial species.
The study was carried out in the Serra do Tabuleiro
State Park (STSP) in the State of Santa Catarina, in
southern Brazil (27◦ 40 S, 48◦ 49 W). The predominant
climate of the region is mesothermal humid, with annual
temperature average of 19 ◦ C. The mean annual rainfall is
1600 mm, the wettest month being February (270 mm),
and the driest, June (68 mm). The camera-traps and
platforms were installed in two physiognomically distinct
areas of the Atlantic Forest, one in dense ombrophilous
forest and the other in coastal sand-plain forest (Klein
1981). The ombrophilous forest was located in the
municipality of Santo Amaro da Imperatriz, northern
region of the STSP, at 200 m asl. Its vegetation was in
an advanced stage of regeneration (logging stopped 60 y
ago), with its canopy at 20 m. The coastal sand-plain forest
was located in the municipality of Palhoça, on the eastern
sector of the STSP. This coastal forest is characterized by a
canopy that varies around 5 m, with Psidium, Arecastrum,
Cauna, Diodia as predominant tree genera, and a dense
shrub understorey composed mainly of species of Cordia,
Clusia, Miconia and Tibouchina. During the study period,
local sunrise was from 06h15 to 07h00 and local sunset
from 17h30 to 18h30.
Eight suspended platforms were built and used from
March to June 2005: three in the dense ombrophilous
forest and five in the coastal sand-plain forest. The
564 LUIZ GUSTAVO R. OLIVEIRA-SANTOS, MARCOS A. TORTATO AND MAURÍCIO E. GRAIPEL

Table 1. Number of species captures, trapping efficiency in captures per trap-day (in parentheses) and sample effort by habitat.
Habitat
Order – Family Species Ombrophilous forest Coastal sand-plain forest
Rodentia – Cricetidae Juliomys pictites Osgood, 1933 28 (0.23) 0
Oligoryzomys nigripes Olfers, 1818 1 (0.01) 0
Oligoryzomys sp. 0 1 (0.01)
Oryzomys sp. 0 1 (0.01)
Didelphimorphia – Didelphidae Philander frenata Olfers, 1818 2 (0.02) 0
Didelphis aurita Wied-Neuwied, 1826 1 (0.02) 0
Didelphis albiventris Lund, 1840 0 26 (0.24)
Micoureus paraguayanus Thomas, 1905 12 (0.10) 90 (0.83)
Chiroptera – Phyllostomidae Sturnira lilum Geoffroy, 1810 24 (0.20) 0
Carnivora – Mustelidae Eira barbara Linnaeus, 1758 2 (0.02) 0
Carnivora – Procyonidae Nasua nasua Linnaeus, 1766 1 (0.01) 0
Sample effort
Number of camera stations 5 3
Trap-days by camera station 24 36
Total trap-days effort 120 108

platforms were 200–1000 m apart from each other, to
reduce the probability of recording the same individual
at two platforms. The platform comprised a rectangular
wooden platform of 35 × 25 × 2 cm and supported
by two 30-cm-long poles that were nailed to the trunk
between 3–6 m from the ground. Two camera-traps
(Tigrinus R
) in the coastal sand-plain forest and one in the
dense ombrophilous forest were used. The camera-traps
were switched to different platforms weekly, to minimize
conditioning of the animals to the attractiveness of the bait
and to increase the probability of another individual being
photographed. As such, each station was only re-sampled
at 11–21-d intervals. The camera-trap was fixed to an
adjacent tree (about 1 m away from the platform) and
fastened with a tie-down rubber strap to the trunk. It was
then directed to the wooden platform. The camera-trap
was positioned 20 cm above the platform and adjusted
with a branch, as necessary. Each trap was programmed
to work 24 h per day and to take shots at minimum
intervals of 30 min each. The camera was programmed
to record date and time of each photograph.
Banana slices with peanut butter were set on top of the
platforms as bait and replaced weekly. Since the bait was
totally consumed in between the third and fourth day of
the week throughout the whole experiment, only the first
four days were thus considered as the effective weekly
effort.
Additional data on D. albiventris, from a study
conducted from March to June 2006, which monitored 14
trapping stations with camera-traps on the coastal sand-
plain forest floor, were used. Identification of species was
based on the photographic records and on the knowledge
of species, gained in previous capture-mark-recapture
studies of small mammals on the floor and canopy of both
areas.
Photographs of the same species on each capturing
station with a minimal time-lapse of 1 h were considered
independent records, and the number of records made
every hour of the day was regarded as an index of
activity (Gómez et al. 2005). The period of activity was
only analysed for those species with more than 26
independent records. For the analysis of the circadian
activity patterns, circular statistics of the ORIANA 2.0
program was adopted. To compare the activity pattern
of D. albiventris and M. paraguayanus in the canopy, or
to compare the activity pattern of D. albiventris on the
floor to that of the canopy, the Watson’s test was used
(Zar 1996). Watson’s test is a non-parametric test that
verified differences on the distribution of two data groups
measured in a circular scale, such as circadian activity.
A robust alternative approach could use the camera
station as the replicate unit, to avoid pseudoreplication
from individuals. This approach was not used because of
the small sample size. However, our unpublished results
with live-traps indicated that 10–25 individuals of M.
paraguayanus and 10–20 individuals of D. albiventris could
be photographed in the coastal sand-plain forest.
We recorded eight species in the dense ombrophilous
forest and four species in the coastal sand-plain forest
(Table 1). Furthermore, in an effort of 480 traps-days
on the coastal sand-plain forest floor, only D. albiventris
were recorded (33 records). All recordings, except that of
N. nasua (16h59), were made from 18h00 to 06h00.
Micoureus paraguayanus, D. albiventris and J. pictipes
presented a strict nocturnal unimodal circadian activity
pattern (Figure 1). Juliomys pictipes presented constant
nocturnal activity (Figure 1a), whereas M. paraguayanus
and D. albiventris had their peak activity after sunset
(18h00), with gradual slowdown through the night
(Figure 1b, c). There were no significant differences
between the activity patterns of M. paraguayanus and
D. albiventris (U = 0.032, P = 0.57) in the canopy, nor
between the activities of D. albiventris in the canopy and
on the floor (U = 0.043, P = 0.32) (Figure 1c, d).
Small-mammal activity in the canopy 565

(a) Juliomys pictites (n = 28) (b) Micoureus paraguayanus (n = 90)

00:00 00:00

40 40
30 30

20 20

10 10

18:00 40 30 20 10 10 20 30 40 06:00 18:00 40 30 20 10 10 20 30 40 06:00

10 10

20 20

30 30
40 40

12:00 12:00

(c) Didelphis albiventris (canopy) (n = 26) (d) Didelphis albiventris (floor) (n = 33)
00:00 00:00

40 40
30 30

20 20

10 10

18:00 40 30 20 10 10 20 30 40 06:00 18:00 40 30 20 10 10 20 30 40 06:00

10 10

20 20

30 30
40 40

12:00 12:00

Figure 1. Activity pattern of small mammals in the canopy of the dense ombrophilous forest (a) and in the canopy (b, c) and floor (d) of the coastal
sand-plain forest. The bars indicate the proportion of recordings (%) made each hour of the day. n = the number of independent records.

The main differences in the richness and species
composition between the two studied areas are likely due
to the differences in the complexity and heterogeneity
of the habitat. The ombrophilous forest is a mature rain
forest, presenting high richness of small mammals and
some medium carnivores. In contrast, the coastal forest
presents a less complex and heterogeneous habitat, not
supporting a high richness of small mammals or medium
carnivores (Vieira & Monteiro-Filho 2003).
Micoureus paraguayanus and J. pictipes have arboreal
habits and D. albiventris is considered scansorial
(Fonseca et al. 1996). Didelphis albiventris has nocturnal-
crepuscular habits (Rossi et al. 2006), and studies with
D. marsupialis in captivity (McManus 1971) and with
D. aurita (Cáceres & Monteiro-Filho 2001) corroborate
that most activity occurs in the early hours of the
night. Micoureus paraguayanus is considered nocturnal
(Emmons 1997), and J. pictipes presented nocturnal
activity in the STSP. Activity pattern of small mammals
are shaped by intrinsic (endogenous or evolutionary
trait) or extrinsic factors (temperature, photoperiod, prey
availability or predation risk) (Aschoff 1966, Daan 1981).
In this case, we believe the general nocturnal activity
have been related to the evolutionary trait of arboreal
small mammals (Aschoff 1966, van Schaik & Griffiths
1996). However, the unimodal pattern observed in
the three studied species could be likely stimulated by
photoperiod. Indeed, in the case of the insectivorous
marsupials studied, the concentrated activity after dusk
could be related both to diminished predation risk
and to synchronize activity with the activity of insect
prey.
566 LUIZ GUSTAVO R. OLIVEIRA-SANTOS, MARCOS A. TORTATO AND MAURÍCIO E. GRAIPEL
Micoureus paraguayanus and D. albiventris presented a
similar arboreal habit and activity pattern in the coastal
sand-plain forest. Micoureus paraguayanus (Cáceres et al.
2002, Leite et al. 1996) and D. albiventris (Rossi et al.
2006) have an opportunistic insectivorous-omnivorous
diet and both species search for nesting sites and shelters
in the canopy (Delciellos et al. 2006, Moraes-Júnior &
Chiarello 2005). Despite similarity in the activity patterns
of both marsupials in the arboreal strata of the STSP,
D. albiventris was also recorded on the floor, whereas we
never recorded M. paraguayanus in this stratum. However,
some authors have reported M. paraguayanus as occurring
on the floor, mostly in the driest months, when there is less
availability of fruits in the canopy (Cáceres et al. 2002). In
the Amazonia Forest, M. demererae was captured mainly
in the understorey and canopy, while D. marsupialis was
captured equally on the floor, understorey and canopy
(Lambert et al. 2005). Similar results were found by Grelle
(2003) and Vieira & Monteiro-Filho (2003) that captured
D. aurita mainly on the floor and M. paraguayanus was
sampled mainly at 2–12 m height in the Atlantic Rain
Forest.
A differentiated pattern of strata use has been also
shown with syntopic rodents in Amazonia (Mauffrey &
Catzeflis 2003) and with similar-sized marsupials and
rodents in the Atlantic Rain Forest (Vieira & Monteiro-
Filho 2003). Other studies suggested that the body mass
of South American marsupials is a limiting factor in
allowing arboreal movements (Cunha & Vieira 2002,
Delciellos & Vieira 2006). Therefore species of arboreal
small mammals, such as Micoureus spp. and Juliomys
spp., have lower body mass than scansorial species, such
as Didelphis spp. (Fonseca et al. 1996). Differences in
the spatial use of the strata, reported in the present
study, and in the size of the consumed items, normally
associated with the difference in body size of D. albiventris
(500–2750 g) and M. paraguayanus (58–132 g) (Rossi
et al. 2006), seem to be one of the most important
strategies in the resource partitioning between these
marsupials (Vieira 2006, Vieira & Monteiro-Filho 2003).
The majority of studies with camera-traps have dealt
with the activity period of ground-dwelling animals
(Gómez et al. 2005) or with population estimation of
species with natural markings (e.g. felines) (Karanth &
Nichols 1998). However, few studies used camera-traps
in the arboreal strata. Otani (2001) installed camera-
traps in the canopy to measure fig consumption by
primates, while Hirakawa (2005) tested the use of an
artificial attraction for bats. Studies of the activity of
small mammals are normally carried out with live-
traps. This methodology, when directed at the study of
activity patterns, demands constant checking of the traps,
which can alter the activities of animals (Bruseo & Barry
1995). When trap-checks are not made, a mathematical
correction is proposed in order to correct the gradual
reduction of capturability throughout the day (Graipel
et al. 2003). After each capture, there is a decrease in
capture probability, due to the reduction of available
traps and of individuals to be captured. Studies with
biased activity data, without repeated trap checks, may
confound the interpretation of activity and the capture
rates through time, without any form of correction
(Bruseo & Barry 1995).
With the use of camera-traps, checks and corrections
are not necessary, manipulation of the animal is avoided,
species are not selected by live-trap size, monitoring is
performed throughout the time of the study and many
species and individuals can be recorded by the same trap
during a sampling period. On the other hand, for the
majority of small mammals, species identification may
be difficult if not preceded by a study involving animal
capture. Furthermore, neither body and age variation
nor sex or reproductive conditions can be recorded.
Additionally, the bait might induce a potential bias, as
it increases the feeding time on the platform. In this
case, a sampling design that included many platforms,
short continuous sampling period in each platform and
long intervals between sampling period in each platform,
should decrease this bias effect. Finally, results presented
here suggest that the use of this innovative technique
with platforms at several heights may be a feasible way to
understand the temporal and spatial use of arboreal strata
by the different species.
ACKNOWLEDGEMENTS
We thank F. Bruggerman and T. T. Moreira for logistic
support and cooperation in the field, P. G. Crawshaw Jr.
and C. A. Zucco for commentaries on this manuscript.
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