Activity Pattern of Brocket Deer (Genus Mazama)
in the Atlantic Forest: Does Sampling Design
Affect the Patterns?
Ana Carolina Srbek-Araujo1,2,3,4*, Tayná Seabra1 and Giovanna Colnago Cecanecchia1,2
1Laboratório de Ecologia e Conservação de Biodiversidade (LECBio), Universidade Vila Velha – UVV, Rua Comissário José Dantas de Melo, nº 21, Bairro Boa Vista, Vila Velha, Espírito Santo, Brazil
2Programa de Pós-graduação em Ecologia de Ecossistemas, Universidade Vila Velha – UVV, Brazil
3 Programa de Pós-graduação em Ciência Animal, Universidade Vila Velha – UVV, Brazil
4Instituto SerraDiCal de Pesquisa e Conservação, Belo Horizonte, Minas Gerais, Brazil
Submission: June 25, 2019; Published: September 19, 2019
*Corresponding author: Ana Carolina Srbek-Araujo, Laboratório de Ecologia e Conservação de Biodiversidade, Programa de Pós-graduação em Ecologia de Ecossistemas, Programa de Pós-graduação em Ciência Animal, Universidade Vila Velha, Vila Velha, Espírito Santo, Brazil
How to cite this article: Ana Carolina Srbek-Araujo, Tayná Seabra, Giovanna Colnago Cecanecchia. Activity Pattern of Brocket Deer (Genus Mazama) in the Atlantic Forest: Does Sampling Design Affect the Patterns? JOJ Wildl Biodivers. 2019: 1(2): 555560.
This study aimed to describe the activity pattern of Mazama spp. in an Atlantic Forest remnant in southeastern Brazil, and to test whether the sampling design can affect the recorded patterns. Data from 4 sampling periods were analyzed (June 2005 to February 2010), using different sampling designs, and these included camera trapping installed along internal unpaved roads or in the forest interior. The records of Mazama spp. were collected throughout the day, with no periods of inactivity, similarly to the results from other regions in South America, but differently from a previous study developed in the same sampled area. There was variation in the distribution of records throughout the day when the sampling periods/designs were compared, but the activity patterns were not statistically different when compared the 2 types of habitat sampled (internal roads and forest interior). Sampling design affect the activity pattern recorded for Mazama spp., which may be related to behavioral differences in response to spatial variations in habitat on a local/regional scale. We recommended the combined use of different sampling designs to better describe the activity pattern of species in camera trap studies, reinforcing that the risk of sample bias should be weighed during the study design.
The time of day in which a species is active is an expression of its circadian rhythm. This consists of approximately 24-h intervals associated with the light-dark cycle and is responsible for the regulation of biological processes . Biological rhythmicity is extremely important because it promotes an internal temporal organization in the physiology and behavior of living beings, and it enables them to synchronize with the external environment to anticipate and prepare for periodic environmental changes [2,3].
The methods used in studies on activity pattern include camera traps. However, despite the increasing use of this equipment in natural history studies of various taxa [4-6], differences related to sampling design, combined with differences in habitat use and species behavior, can affect the records obtained by this sampling method .
Brocket deer in the genus Mazama (Rafinesque, 1817) have a complex evolutionary
pattern, and the genus is represented by morphologically similar Neotropical species grouped in 2 main clades: the red brocket group and the gray brocket group . These deer occur from southern Mexico to northern Argentina, including practically the entire Brazilian territory . They are morphologically adapted to forest habitats, although they are also found in different vegetation types throughout their distribution, as such as Cerrado (the Brazilian Savanna), Caatinga (xeric shrubland and thorn forest) and open field formations, as well as capoeiras (secondary-growth forests in initial stages of regeneration) . There are 4 species of Mazama recognized for the Brazilian Atlantic Forest . Mazama americana (Erxleben, 1777) and Mazama gouazoubira (G. Fischer, 1814), which represent respectively the red and gray groups , are sympatric in the
southeast of the country.
Studies on activity pattern of M. americana and M.
gouazoubira are still scarce (if considering the wide geographic
distribution of these species), and in some cases, the available
data are conflicting [4,11-16]. It is thus necessary to investigate
the discrepancies between studies to better define the activity
patterns of these taxa, and to determine the environmental
factors that may influence the time of day in which Mazama spp.
are active, as well as check the sampling factors that may affect
the collection of records used in studies on activity patterns.
The objective of the present study was to describe the
activity pattern of Mazama spp. in an Atlantic Forest remnant
in southeastern Brazil, and to test whether the camera trap
sampling design can affect the recorded patterns.
The study was conducted at Reserva Natural Vale (RNV, Vale
Natural Reserve: 19°06’ - 19°18’ S and 39°45’ - 40°19’ W), which
is located between the municipalities of Linhares and Jaguaré,
in the north of the state of Espírito Santo, southeastern Brazil
(Figure 1). The RNV has an area of 22,711 ha and is adjacent to
the Reserva Biológica de Sooretama (RBS, Sooretama Biological
Reserve - 27,860 ha). Together with other 2 private reserves
(Recanto das Antas Private Natural Heritage Reserve – 2,212 ha,
and Mutum Preto Private Natural Heritage Reserve - 379 ha),
the RNV and RBS form a practically continuous block of native
vegetation (Linhares-Sooretama Block – more than 53,000 ha)
that represents approximately 11% of the current forested area
in the state of Espírito Santo (based on data available in ).
The Linhares-Sooretama Block is intersected by BR-101 Highway
in the southwest/northeast direction.
The RNV is composed by a mosaic of habitats, most of which
are covered by dense lowland forest (Tabuleiro forest) as well
as areas with less dense forest on sandy soils (Mussununga)
and occasional native grassland . The forest vegetation
in the RNV is classified as perennial seasonal forest . The
topography of the RNV is practically flat with tabular hills that
vary in altitude between 28 and 65 m . The climate in the
region is tropical with dry winters, i.e., type Aw according to the
Köppen classification system . The mean annual temperature
is 24.3 °C, and the mean annual rainfall is 1,215 ± 260 mm .
The RNV has an internal network of unpaved roads (Figure 1),
which are approximately 4 m wide and total 126 km in length,
allowing access to all parts of the reserve .
Data were collected during approximately 48 months of
sampling, which were distributed in 4 distinct sampling periods
using camera traps: Jun/2005 to Jun/2006 (Period 1), Jun/2006
to Aug/2007 (Period 2), Aug/2007 to Oct/2008 (Period 3), and
Jun/2009 to Feb/2010 (Period 4). CamTrakker game cameras
(CamTrak South Inc., USA) were used in the first sampling
period; and Tigrinus cameras (conventional model; Tigrinus
Equipamentos para Pesquisa, Brazil) were used in the other 3
Each sample period represented a distinct sample design, as
described below. In the first and fourth periods, the camera traps
were installed along internal unpaved roads; and in the second
and third periods, the equipment were installed out of roads,
in the interior of the forest (at 100-200 m, and 500 m from the
nearest internal road, respectively; Figure 1). In the first period, 30 sampling stations were selected that were distributed in
the north, south, and west subareas of the reserve (10 stations
in each subarea), and data were collected in the dry and rainy
seasons (2 consecutive months in each season/subarea). In
Period 2, 10 different sampling stations distributed throughout
the entire RNV were sampled. The same was done for Period 3. In
Period 4, 8 sampling stations were selected in the north subarea.
The camera traps were operated for 24 hours/day, and the
equipment was set to stamp the date and the time of the record
at each photograph. The solar time was used for the time of day
throughout the entire sampling period. The interval between
consecutive photos was set to 20 seconds. The camera traps were
fixed on tree trunks approximately 45 cm above the ground, and
checked every 30 days for cleaning, battery replacement and
to collect the photographic records. No bait was used to attract
At first, we selected good quality photographic records of
Mazama spp. to confirm the identification of the species present
in the RNV. The photographs were sent to the Cervidae Research
and Conservation Center (Núcleo de Pesquisa e Conservação
de Cervídeos - NUPECE, from Universidade Estadual Paulista -
UNESP) for identification by cervid specialists (José Maurício
Barbanti Duarte and Márcio Leite de Oliveira). A total of 56
photographic records were selected. Of these, 6 were identified
as M. americana; 4 as M. gouazoubira; 39 were identified as from
gray clade, but apparently different from M. gouazoubira; 3 were
identified as from red clade, but apparently different from M.
americana; 2 were classified as potential hybrids; and 2 did not
receive any identification (clade or species level). According to
Duarte et al. , the morphological similarity between the taxa
has caused numerous errors in the identification of Mazama
spp., and external morphometry by itself has low power in
species discrimination. Thus, given the difficulty in identifying
the species from most of the photographic records, even by
specialist researchers, and the existence of many doubtful
records, we chose to keep the data analysis at the genus level.
To avoid double counting of records in the same capture
event, only the first record of Mazama spp. was considered
valid when there was more than one photo of the genus within a
period of 1 hour at each sampling station (= independent record;
). To compare the number of independent records obtained
in each sampling period/design according to differences in the
effective sampling effort, the capture success of Mazama spp. in
each sampling period was calculated by dividing the number of
valid records by the sampling effort and multiplying the result
by 100 [7, 21]. The sampling effort was calculated by multiplying
the number of camera traps by the number of effective sampling
days (the total time between the first and last records in each
sampling period, considering all sampling stations) .
Because the clade represents the main predictor of the activity
in the genus Mazama (see Discussion for details), we classified
the records into records obtained at night (18:00h-05:59h) and
in the daytime period (06:00h-17:59h).
To describe the activity pattern, the independent records of
Mazama spp. were grouped into 1-hour intervals for a total of
24 daily intervals. The overall data (grouping of all records), the
data from each sampling period/design, and the data from each
type of habitat sampled (internal roads - grouping of Periods 1
and 4; and forest interior - grouping of Periods 2 and 3) were
considered. The Mardia-Watson-Wheeler test was used to
assess whether there were differences in the daily distribution
pattern of Mazama app. records. This test considers the time
of each photographic record (independent inputs) and, based
on the grouping of the data to be compared, draws random
samples to determine whether the circular distribution of the
data is identical to that of the original samples . Initially,
the 4 sample periods/designs were compared simultaneously
(multisample) and then pairs of periods were compared with
each other and with the overall pattern (pairwise). The same test
was used to compare the types of habitat sampled (pairwise).
The analyses were conducted using the program Oriana (version
4.0; ) and the level of significance was 5% (p-value < 0.05).
To represent the activity pattern graphically, rose diagrams
and line graphs were used. To prepare the line graphs, 1-hour
intervals and the percentage of records obtained in each interval
were considered. Percentages were used so that any differences
related to the absolute number of records did not affect the
visual comparison of the activity patterns recorded. The activity
peak was defined when the percentage of captures in any given
hour was 50% greater than the hour with the greatest percent of
A total of 1,029 independent records of Mazama spp.
were obtained during the study period, and the records were
differently distributed among the sampling periods/designs.
The Period 3 had the highest capture success, followed by
Period 2 (Table 1). About 74.1% of all records were obtained
in the daytime period, and the highest proportion of records in
this period was also observed when considering each sampling
period separately (69.6 to 90.9%; Table 1).
Records of Mazama spp. were obtained throughout the day
(24 hours, with no periods of inactivity), and the genus was more
active between 05:00h and 18:00h (Figure 2). There was a first
peak in activity early in the morning, which extends until midafternoon,
between 05:00h h and 15:00 h, and a second peak
late, at 17:00-18:00 h, in the evening (Table 2; Figure 2).
Considering the overall pattern and each sampling period/
design separately, the activity pattern of Mazama spp. varied in
relation to the hours with the highest activity and/or the number
of activity peaks during the day (Table 2). The daily distribution
pattern of Mazama spp. records differed significantly between
the sampling periods/designs (W = 22.957, P < 0.001). The
pairwise comparisons revealed significant differences between
overall × Period 2, overall × Period 4, Period 2 × Period 3, Period
2 × Period 4, and Period 3 × Period 4 (Table 3; Figure 3).
When the sampled habitats were analyzed separately, the
proportion of records associated with the first and second
activity peaks differed, with the first peak being more expressive
for unpaved roads, and the second peak for forest interior
(Figures 4 and 5). However, the daily distribution pattern of
Mazama spp. records was similar between internal unpaved
roads and the forest interior (W = 3.011; P = 0.222).
The genus Mazama was active over the entire 24 hours, with
more intense activity during the day, comprising a crepusculardiurnal
pattern in the RNV. Mazama activity over 24 hours,
considering either a single species or the combined records of
2 sympatric species (one from the red clade and another from
the gray clade) has also been observed in Ecuador , Peru ,
Bolivia [13,15], Argentina , and Brazil (Amazon, Pantanal,
and Atlantic Forest; ), but these results differ from those of
Ferreguetti et al.  based on data also collected in the RNV.
From the comparison of the results of previous studies
performed with M. americana and M. gouazoubira, we observe
that there are peculiarities in the activity time for the same
species of brocket deer between sites (intraspecific variations),
and the differences are related to the hours of more intense
activity and occasional periods of inactivity. These variations
may be attributed to differences in the photoperiod between
the sampled sites, which varies with latitude ; local effect of
altitude associated with topography on the incidence of solar
rays inside the vegetation at each study area ; differences
in the ambient temperature between regions [6, 23]; local
variations in the response to competition between Mazama
spp. ; the size of the studied remnants ; or changes in
the activity pattern in response to the presence of hunters .
Blake et al.  obtained records of M. americana during the day
and night and found an activity peak in the early morning and
another in the late afternoon. Di Bitetti et al.  and Gómez
 observed a similar pattern, although the first activity peak
occurred at the end of the night, and the species was less active
during the hottest hours of the day. Rivero et al.  recorded
more intense activity between sunset and sunrise and no records
in the early afternoon. Tobler et al.  obtained more records in
the late afternoon and throughout the night, with no records in
the hottest hours of the day. In Brazil, Oliveira et al.  recorded
more intense activity of M. americana at night, especially before
sunrise, in the Amazon, and attained a greater number of
records after sunset and during the night, in the Atlantic Forest.
Ferreguetti et al. , also in Atlantic Forest, obtained records
of M. americana only at night, with more intense activity after
midnight. For M. gouazoubira, Blake et al.  found greater activity during the day until sunset and inactivity at night. Rivero
et al.  and Tobler et al.  obtained records over 24 h, with
more intense activity in the early morning  or throughout the
diurnal period . In the Brazilian Pantanal, Oliveira et al. 
recorded more intense activity of M. gouazoubira early in the
morning and late at afternoon. In the Atlantic Forest, Ferreguetti
et al.  recorded the species only during the day, with activity
peak early in the morning and in the hottest hours of the day.
Ferreguetti et al.  classified M. americana as nocturnal
and M. gouazoubira as diurnal, with temporal segregation
between the 2 species, and 2 periods during the day with no
records of the genus (from 04:00h to 06:00h, and 17:00h to
20:00h). Although the species were not differentiated in the
present study, the gaps in records noted by Ferreguetti et al. 
were not observed, highlighting that some of the activity peaks
recorded here overlap the times without records in the previous
study. In addition, according to few records identified by cervid
specialists (see Materials and Methods for details), we recorded
M. americana at 17:21h, 18:20h, 18:52h, 22:31h, 00:05h and
02:10h (some of which correspond to the second gap identified
by Ferreguetti et al. ) while M. gouazoubira was recorded
by us at 08:08h, 08:29h, 09:36h and 14:52h in the RNV. The
gaps recorded by Ferreguetti et al.  also contrast with the
observed in other locations for the genus Mazama [4, 11,13-16].
The differences in the activity pattern of M. americana and M.
gouazoubira (interspecific variations) seem to be related to an
effect of phylogeny, and the clade represents the main predictor
of the activity of the species, with the red clade being more
nocturnal and the gray clade more diurnal . If this pattern
is also observed in the RNV, it is probable that our dataset
gathers a larger number of records of M. gouazoubira, the local
representative of the gray clade. This observation applies to
overall data, to the data from each sampling period/design and,
consequently, to each habitat sampled. Ferreguetti et al. 
also obtained a greater number of records of M. gouazoubira by
camera traps and transect surveys, suggesting that this species
may be more abundant in RNV than M. americana.
Although there was no difference in the activity pattern
between the sampled habitats in the present study, there was
difference between Periods 2 and 3, which included the forest
interior dataset. By contrast, the periods in which sampling
was conducted along unpaved roads did not differ. It is worth
noting that there was also a difference between the pattern
detected when the camera traps were only installed in the north
subarea (Period 4) and when the designs included sampling
throughout the entire RNV (Periods 2 and 3). These variations
in activity pattern should not be related to differences in the
proportion of records of the species/clades sampled, suggesting
that it is related to different behavioral responses of Mazama
spp. to spatial variations in habitat on a local/regional scale.
In this respect, the Mazama camera trapping data may have
been influenced by small differences within the same type
of habitat (such as the distance to the nearest internal road)
and/or regional peculiarities within the same remnant (such
as among the RNV subareas) highlighting that sampling was
always conducted in dense lowland forest. However, the sum
of the records from Periods 2 and 3 (forest interior) diluted the
local effect, resulting in a pattern like the data from Periods 1
and 4 combined (internal roads). Similarly, sampling along roads
throughout the entire RNV (Period 1) reduced the regional effect
(Period 4) so that the data were like those from the off-road
samplings (Periods 2 and 3).
The results of the present study corroborate those of Srbek-
Araujo & Chiarello , who indicated that sampling design
affects the collection of mammal records using camera traps,
reinforcing that the risk of sample bias should be weighed during
study design. According to the data presented here, the sampling
design may also result in different activity patterns for the same
species/taxa, which may be related to behavioral differences in
response to spatial variations in habitat on a local/regional scale.
Once the detection rate by camera traps is determined by the
level of activity of the species in a specific environment or habitat,
the capture rate will be proportional to their level of activity in
each place  and at each time of day . For this reason, the
integration of sample designs becomes more representative for
the characterization of the general activity pattern of the species,
encompassing the variation in the use of landscape components
(intensity of use) and the peculiarities in the pattern of use (time
of day, for example) of each element of the landscape. Indeed, the
integration of sampling periods diluted the differences between
sampling designs used here, highlighting that the types of
habitat sampled in the present study did not significantly affect
the recorded activity pattern of Mazama spp., which was similar
between the internal unpaved roads and the forest interior.
Regardless of the sampling design used, none of the activity
patterns observed for the genus Mazama in the present study
was like the pattern reported by Ferreguetti et al.  for the
same study area (considering the 2 species as a unit). It may be
due to differences in sampling design (location of camera traps,
for example), eventual inaccuracy in species identification,
and/or the randomization procedure proposed by Ferreguetti
et al.  to “correct” records that could not be identified
(uncertain identification). According to the authors, when the
identification was uncertain, they “randomized the unidentified
records using the proportion of each species found in the total
number of transect sightings and camera trap records” and
“the 2 species were recorded in similar proportions in the 2
sampling procedures” . This randomization procedure is
based on the identified records, so it is sensitive to accuracy
in species identification, which can generate biased results. In
addition, unidentified records are not necessarily distributed
between species in the same proportion as identified records
(or between transect sightings and camera trap records), which
may be influenced by the greater ease of identification of one cspecies over another, considering the quality of the photographic
records (e.g. light conditions, positioning/angle of the animal,
and proximity to the equipment), highlighting that the studied
species are very similar physically, with subtle diagnostic
Our results confirm that the genus Mazama is active
throughout 24-hour period, with no periods of inactivity, also
in southeastern Brazil, similarly, to results from other regions in
South America. Furthermore, we recommend the use of different
sampling designs to better determine the activity pattern of the
focal species in camera trap studies because details of the data
collection strategies can influence the data obtained and thus
affect the recorded patterns.
We would like to thank Hermano José Del Duque Júnior,
Eduardo de Rodrigues Coelho, Jesuíno Barreto, Braz Guerini
and José Simplício dos Santos for help with field activities.
JMBD and MLO (NUPECE) for help with species identification.
We also acknowledge financial support from Vale S.A. / Instituto
Ambiental Vale. GCC thanks Fundação de Amparo à Pesquisa
e Inovação do Espírito Santo (FAPES) for the postgraduate
scholarship. ACS-A is grateful to Fundação de Amparo à Pesquisa
e Inovação do Espírito Santo (FAPES 0607/2015 and FAPES
0510/2016), which sponsored the research of the Laboratório
de Ecologia e Conservação de Biodiversidade (LECBio)
Appendix 1: Brocket deer in the genus Mazama recorded in the Reserva Natural Vale, southeastern Brazil: M. americana (A),
M. gouazoubira (B), red clade (C and E), gray clade (D and F) and potential hybrid (G).
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