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Previous studies exploring the rhythmic activity of sloths of the Bradypus genus in undisturbed forests revealed cathemeral patterns of activity. In the current study we wished to examine sloth behavior in a highly disturbed secondary forest habitat. We evaluated activity pattern, time budget and rhythmic activities of brown-throated three-toed sloths (B. variegatus) living in the border of a highly disturbed forest fragment in northeastern Brazil. Three adults (2 females and 1 male) and 2 infants were studied over 29 days. Observational data were collected in 15 min increments over the 24-h day in the following categories: resting, moving, travelling, eating and grooming. Time series data were subjected to X2 periodogram, Fourier (Fast Fourier Transformation, FFT), cosinor and CircWave circadian rhythm analysis, and revealed significant 24-h rhythms in all behaviors in most circumstances. Unlike sloths located in an undisturbed forest, this population exhibited primarily diurnal activity patterns of behavior, with the center of gravity for each behavior occurring in the middle of the day. Furthermore, several behaviors were expressed in a bimodal pattern, with a morning and a late afternoon peak of activity. These data suggest that with decreased predator presence and with a more ubiquitous food source, sloths adjust their temporal niche to daytime.
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Mammalian Biology
Zeitschrift für Säugetierkunde
ISSN 1616-5047
Mamm Biol
DOI 10.1007/s42991-020-00047-5
Activity pattern, budget and diurnal
rhythmicity of the brown-throated three-
toedsloth (Bradypus variegatus) in
northeastern Brazil
Diogo de Oliveira Bezerra, Leandro
Ricardo Rodrigues de Lucena, Giles
E.Duffield, Dominic J.Acri & Antonio
Rossano Mendes Pontes
1 23
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Vol.:(0123456789)
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Mammalian Biology
https://doi.org/10.1007/s42991-020-00047-5
ORIGINAL ARTICLE
Activity pattern, budget anddiurnal rhythmicity
ofthebrown‑throated three‑toedsloth (Bradypus variegatus)
innortheastern Brazil
DiogodeOliveiraBezerra1· LeandroRicardoRodriguesdeLucena2 · GilesE.Dueld3 · DominicJ.Acri3 ·
AntonioRossanoMendesPontes4,5
Received: 25 May 2020 / Accepted: 15 June 2020
© Deutsche Gesellschaft für Säugetierkunde 2020
Abstract
Previous studies exploring the rhythmic activity of sloths of the Bradypus genus in undisturbed forests revealed cathemeral
patterns of activity. In the current study we wished to examine sloth behavior in a highly disturbed secondary forest habitat.
We evaluated activity pattern, time budget and rhythmic activities of brown-throated three-toed sloths (B. variegatus) living in
the border of a highly disturbed forest fragment in northeastern Brazil. Three adults (2 females and 1 male) and 2 infants were
studied over 29days. Observational data were collected in 15min increments over the 24-h day in the following categories:
resting, moving, travelling, eating and grooming. Time series data were subjected to X2 periodogram, Fourier (Fast Fourier
Transformation, FFT), cosinor and CircWave circadian rhythm analysis, and revealed significant 24-h rhythms in all behaviors
in most circumstances. Unlike sloths located in an undisturbed forest, this population exhibited primarily diurnal activity
patterns of behavior, with the center of gravity for each behavior occurring in the middle of the day. Furthermore, several
behaviors were expressed in a bimodal pattern, with a morning and a late afternoon peak of activity. These data suggest that
with decreased predator presence and with a more ubiquitous food source, sloths adjust their temporal niche to daytime.
Keywords Bradypus variegatus· Circadian rhythm· Diurnal rhythm· Forest fragmentation· Sloth behavior· Time budget
Abbreviations
CG Center of gravity
FFT Fast Fourier Transformation
ZT Zeitgeber time
Handling editor: Emmanuel Serrano.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s4299 1-020-00047 -5) contains
supplementary material, which is available to authorized users.
* Antonio Rossano Mendes Pontes
mendespontes@gmail.com
Diogo de Oliveira Bezerra
d.bezerra@yahoo.com.br
Leandro Ricardo Rodrigues de Lucena
leandroricardo_est@yahoo.com.br
Giles E. Duffield
duffield.2@nd.edu
Dominic J. Acri
dacri@iu.edu
1 Centro de Ciências Biológicas, Departamento de Zoologia,
Universidade Federal de Pernambuco, R. Prof. Moraes Rego,
1235, Cidade Universitária, Recife, PECEP:50740-620,
Brazil
2 Departamento de Zootecnia, Universidade Federal Rural de
Pernambuco, Campus de Serra Talhada, Av. Gregório Ferraz
Nogueira, S/N, SerraTalhada, PernambucoCEP:66909-535,
Brazil
3 Department ofBiological Sciences andEck Institute
forGlobal Health, Galvin Life Science Center, University
ofNotre Dame, NotreDame, IN46556-0369, USA
4 Instituto Nacional de Pesquisas da Amazônia-INPA, Núcleo
de Pesquisas de Roraima-NPRR, Rua Coronel Pinto, 315,
Centro, BoaVista, RoraimaCEP:69301-150, Brazil
5 Present Address: Estrada de Aldeia, 12.948,
Cond. Luzanópolis, Aldeia,, Camaragibe,
PECEP:54789-000, Brazil
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Mammalian Biology
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Introduction
Sloths, Bradypus, are among the most lethargic species
in the world (Eisenberg 1978; Giné etal. 2015). They are
inactive during most of the time of their 24-h cycles, and
can rest in up to 90% of the time (Beebe 1926; Queiroz
1995; Chiarello 1998; Consentino 2004; Cassano 2006;
Urbano and Bosque 2007; Ginè etal. 2015)
They are cathemeral heterothermic animals that can be
active at any time of their 24-h cycle, which is dictated by
ambient temperature, food acquisition, competition, and
predation (Queiroz 1995; Chiarello 1998, 2008; Urbano
and Bosque 2007; Ginè etal. 2015), and exhibit a cir-
cadian rhythm (Duarte etal. 1982; Chiarello 1998; Ginè
etal. 2015).
Thus, in different regions they can be diurnal, pre-
dominantly diurnal, or nocturnal (Montgomery and Sun-
quist 1978; Pinder 1985; Queiroz 1995) and also be more
active in either warmer or colder periods of the 24-h cycle
(Urbano and Bosque 2007; Castro-Vasquez etal. 2010).
Depending on the environmental conditions they could
even present an ultradian rhythm (Ginè etal. 2015).
Bradypus variegatus can spend up to 85% of their 24-h
cycles resting (Queiroz 1995; Consentino 2004; Urbano
and Bosque 2007), and are cathemeral animals that can be
active at any time of the day or night (Sunquist and Mont-
gomery 1973; Montgomery and Sunquist 1978; Queiroz
1995; Carmo 2002; Consentino 2004; Urbano and Bosque
2007; Castro-Vasquez etal. 2010). They are almost com-
pletely folivorous and can feed during any time of the day
or night (Beebe 1926; Sunquist and Montgomery 1973;
Queiroz 1995; Chiarello 1998; Urbano and Bosque 2007;
Castro-Vasquez etal. 2010).
Since Bradypus spp. adjust their activity cycles to
avoid and confuse predators (Pepin and Cargnelutti 1994;
Chiarello 1998), to enhance food acquisition, and avoid
climatic fluctuations (Glanz 1982; Roxburgh and Perrin
1994; Terborgh and Wright 1994), it should be expected
some dramatic changes in their behavior in the twenty-
first-century highly impacted scenarios where they occur,
such as the Atlantic forest of northeastern Brazil (Mendes
Pontes etal. 2016).
In most of the studies carried out to date in disturbed
sites that lost at least some of the sloth’s competitors and/or
predators, Bradypus spp. were found expressing cathemeral
activity patterns, and, in some cases, presenting a more pro-
nounced diurnal activity (Sunquist and Montgomery 1973;
Montgomery and Sunquist 1978; Chiarello 1998; Carmo
2002; Consentino 2004; Cassano 2006; Urbano and Bosque
2007; Castro-Vasquez etal. 2010; Giné etal. 2015).
In the previous studies carried out to date with B. var-
iegatus, which were in disturbed sites, they were almost
entirely folivorous (up to 99.4% of their diet comprised
leaves), and spent between 2.1 and 14.2% of their 24-h
cycle on feeding (Urbano and Bosque 2007; Castro-
Vasquez etal. 2010). During the dry season they used
more frequently the forest interior, whereas in the rainy
season they preferred forest border, where they had access
to higher amounts of their preferred feeding tree, the
pioneer Cecropia spp., in which they may depend upon
entirely (Goffart 1971; Urbano and Bosque 2007; Castro-
Vasquez etal. 2010). In the different disturbed scenarios
where they were studied, they could spend more time feed-
ing during the day or during the night (Urbano and Bosque
2007; Castro-Vasquez etal. 2010).
Although some generalizations can be made about sloths,
Bradypus spp. including B. variegatus, some environmental
and methodological constraints could make comparisons dif-
ficult. Some studies were carried out in tropical forests of
Central America, whereas some others were carried out in
the Amazonia, or even in the Atlantic forest of Brazil (Sun-
quist and Montgomery 1973; Montgomery and Sunquist
1978; Queiroz 1995; Chiarello 1998). For instance, some
of the studies were carried out in pristine forests whereas
some others were in impacted, or even highly impacted
areas, which may cause profound changes in the sloths ecol-
ogy and behavior (Pinder 1985; Urbano and Bosque 2007;
Castro-Vasquez etal. 2010).
Additionally, most studies did not follow the study ani-
mals systematically, or did not follow the individuals for
entire 24-h cycles, which may limit the interpretation of
results (Queiroz 1995), and which makes it difficult to deter-
mine synchrony among individuals or rhythmicity of specific
behaviors. Besides ambient temperature, top predators and
feeding competition are said to influence sloths ecology and
behavior (Pepin and Cargnelutti 1994; Chiarello 1998; Ginè
etal. 2015). However, due to a lack of control sites, vegeta-
tion studies and predator’s abundance, the importance of
these variables is poorly understood.
In this study we evaluated activity pattern, budget, and
diel rhythmicity of brown-throated three-toed sloths living
in the border of a highly disturbed forest fragment in north-
eastern Brazil. The environment was dominated by Cecropia
trees, was highly disturbed, and with half of the tree species
and mammals having gone extinct. This includes the other
strictly folivorous species, possible sloth’s competitor [e.g.
howler monkey) and natural predators such as medium-sized
and large cats, boas (Boa constrictor), and various birds of
prey]. Most importantly, nocturnal hunting, with and without
feral dogs, was very intense. In another study conducted in
the same area, we recorded 95 rifle shots during 35 nights,
but no hunting was detected during the daytime. Such human
related activity has had a devastating impact on the remain-
ing fauna (Freitas 2012). Although there has never been
any records of sloths being hunted, the presence of hunters,
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barking feral dogs, and rifle shots might be predicted to gen-
erate a protective response behavior especially on sloths with
recently born babies.
Thus, considering that their possible diurnal competi-
tors (e.g. howler monkeys), diurnal (e.g. birds of prey), and
nocturnal predators (e.g. medium-sized and large cats) are
extinct, the temporal window of sloth activity should be
expected to be wider (cathemeral habits) (see an explana-
tion in Giné etal. 2015), or maybe no effect is expected
because other proximal factors could be more determinant
(see Chiarello 1998). However, such human pressure during
the night is likely to constrain the sloths nocturnal activ-
ity. We therefore hypothesize that in this scenario the sloths
should adopt a primarily diurnal habit, and the individuals
would have a highly synchronous behavior, with predictable
onset and offset times for each activity described.
Material andmethods
Study area
The Atlantic forest of northeastern Brazil above the São
Francisco River has a comparatively longer history of human
exploitation (Salvador 1975; Gandavo 1980). It has lost 94%
of its forest cover, at the same time that 50% of all its tree
species went extinct (Silva and Tabarelli 2000; Oliveira
etal. 2004; Santos etal. 2008). Most fragments are smaller
than 10ha, are all isolated in a non-forested matrix, have
irregular shape, and are exposed to rampant human pres-
sure (Mendes Pontes etal. 2016). In this scenario, 51.2%
(n = 22) of medium-sized and large mammals (all large ones)
have gone extinct, including some species that disappeared
before description, or even before being depicted by the first
colonizers (e.g. rufous long-tailed spider monkey, or Franz
Post’s spider monkey, Ateles sp.) (Mendes Pontes etal. 2016,
2019).
The study was carried out in Aldeia forest (7°5500S
and 35°0128W), one of the largest urban forest remnants
in the metropolitan perimeter of the city of Recife, state of
Pernambuco. The Aldeia forest has a total area of 3000ha
of mostly secondary forest (CHESF 2004). Following the
classification of Oliveira and Fontes (2000), the vegetation
is formed by highly undulating lowland evergreen forests,
with canopy that ranges from 15 to 25m in height. Tem-
perature varies between 18 and 27, and annual rainfall,
between 1300 and 2400mm, with a wet season from March
to September (Veloso etal. 1991). Sunrise occurs between
05:45 and 06:00h, and sunset, between 17:45 and 18:00h.
The field site is not officially protected and experiences
a high degree of human interference. Hunting activity,
the presence of feral dogs, forest clearing, selective cut-
ting, intentional fires, bisection by roads such as the PE-27
motorway, and regular use by people and domestic animals
threaten the once-pristine environment. The study animals
which inhabited the highly disturbed southern forest bor-
der (7°5557.76S 35°0133.95W), formed almost exclu-
sively by species of Cecropia spp. (Cecropiaceae), and never
entered the forest interior (never entered more than a 100m
from the forest border).
After 1025km walked during the day, and 743km
walked during the night, within a total of 21 forest frag-
ments [very small (≤ 10ha), small (10.1–100ha), medium-
sized (100.1–1000ha), and large (> 1000ha; the largest is
only 3478.3ha)], located in four of the best-protected forest
archipelagos of the Atlantic forest of northeastern Brazil,
we concluded that the only possible diurnal competitor of B.
variegatus, Alouatta belzebul, was currently extinct (Mendes
Pontes etal. 2016). Also extinct were their nocturnal/cath-
emeral predators, the large and medium-sized cats, namely,
Panthera onca, Puma concolor, and Leopardus pardalis
(Mendes Pontes etal. 2016).
Although their main diurnal predator, harpy eagle,
Harpia harpyja, is referred to as occurring in the Brazilian
Atlantic forest (Sick 1993; Souza and Borges 2004), it has
never been sighted in the Atlantic forest of northeastern Bra-
zil above the São Francisco River. Accordingly, H. harpyja
was never recorded during this study or in Mendes Pontes
etal. (2016). Collared forest-falcon, Micrastur semitorqua-
tus, crested caracara, Polyborus plancus (Falconidae), the
road-side hawk, Buteo magnirostris (Accipitridae), and the
sparrow hawk, Falco sparverius (Falconidae) are likely to
be too small to predate on these sloths.
Captures andradio‑tracking
Between 10 and 14 August 2004 three wild brown-throated
three-toed sloths, B. variegatus, were opportunistically
located along 200m of forest border, and captured by hand,
immobilized, but were not anaesthetized. They were released
only a few minutes after capture to avoid stress and bias in
the observations.
Two adult female sloths (BV-1 and BV-3), and one adult
male (BV-2) were fitted with TW-3 rubber-coated cable-tie
radio-collars (Biotrack Ltd., Wareham, UK; ~ 60g, which
is < 2% of all the animals body weight) insitu and subse-
quently released in the same tree where they had been cap-
tured. No licenses were required by the Brazilian authori-
ties since the species was not threatened and the area was
privately owned and not legally protected. We followed the
Guidelines for the Capture, Handling and Care of Mammals,
as approved by the American Society of Mammalogists,
1998 (https ://www.mamma lsoci e ty.org/uploa ds/commi ttee_
files /ACUC1 998.pdf). After release, we waited for 2weeks
until the behavioral observations started. The radio-collars
were removed from the individuals at the end of the study.
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The behavioral activities of each target individual were
systematically recorded with the help of a RX-80 Mariner
receiver and flexible directional Yagi antennae, with the help
of a powerful spotlight and using a 10 × 42 Leica binoculars,
via instantaneous scan sampling method (Altmann 1974),
recording the first performed behavior every 15-min. No
missing values exist. The instantaneous scans were taken
every time an alarm clock went off. The behavior of each
animal was classified as resting (when the study animal was
motionless); moving (when engaged in horizontal or vertical
movements of the body that not resulting in changing places
or following any specific direction); travelling (when mov-
ing from one previous place to another and/or following any
specific direction); feeding (taking to the mouth and chewing
and/or swallowing any food item, or browsing and/or han-
dling food); and autogrooming (when scratching or groom-
ing their own body). No allogrooming was ever recorded.
Over a period of 29days between August 2004 and Janu-
ary 2005, the same observer followed the three adult sloths
(one at each observation night; no nights were consecu-
tive) for 24-h periods (the smallest continuous measure of
time was 24h) for a total of 696h, and recorded a total of
2800 behavioral records. During the observational period
two infants were born, one to female BV-1 (F-1), and one
to female BV-3 (F-2), and they were also followed (at the
same time that their mothers), totaling 336h of observations,
comprising 1344 observational records. This summed up
to 1032h of observation and 4144 observational records
(Table1).
Data analysis
Averages of time budgeted for each behavior over the course
of each 24-h period was calculated for each animal at each
day. This allowed comparisons of average percentage of time
spent in each activity by each individual, and also between
individuals. Data did not fit a normal distribution (Kol-
mogorov–Smirnov test), and therefore it was subjected to
a nonparametric Kruskal–Wallis one-way analysis of vari-
ance corrected for ties. When the p < 0.05, Dunn’s multiple
comparisons were performed.
Regarding the two infants, comparisons of average per-
centage of time spent in each activity by each individual was
also evaluated by the nonparametric Kruskal–Wallis one-
way analysis of variance corrected for ties, whereas to com-
pare between individuals, a Mann–Whitney test was used.
For the purposes of testing for circadian/diel and ultra-
dian rhythmicity in the five behavior categories, the data
representing entire 24-h durations of data collection for indi-
vidual sloths were concatenated, providing for 9–11days of
activity (adults) and 5–9days (infants). Data were viewed
in actogram format, and temporal data were subjected to
X2 periodogram and Fourier (Fast Fourier Transformation,
FFT) analyses using the Clocklab software (Actrimetrics,
Wilmette, IL) (Duffield etal. 2009). The period length of
rhythms scored as significant at p < 0.001 in the range of
10–30h was determined using the periodogram analysis.
Cosinor (one sine wave) and related Circwave analysis (one
sine wave with up to two additional harmonics) were also
used to test for 24-h sinusoidal patterns of rhythmicity using
CircWave v1.4 software by fitting a Fourier curve to the
data, and producing R2 and center of gravity values (https
://www.hutla b.nl, https ://www.euclo ck.org) (Van der Veen
etal. 2008; Zhou etal. 2014). Data were first arranged into
2-h bins, thereby allowing for a minimum of 0 and maximum
of 8 events per time interval. The p values reported are the
result of an F test from the software. Percentage activity dur-
ing day (Zeitgeber time 12 (ZT12) to ZT0; 06h00 to 18h00),
and percentage activity during the night (ZT0–ZT12;
18h00–06h00) were calculated from the 5–11days of activ-
ity. Zeitgeber time 0 marks the approximate onset of daytime
(06:00h); and ZT12 marks sunset and the approximate onset
of night (18:00h).
Results
Activity budget
Our 24-h period observations (100% of success rate of
recorded scans) revealed that the three individuals rested
for a mean of 74.9% of their time, and that the females
(BV-1 and BV-3) rested significantly more than the male
(BV-2) (Kruskal–Wallis test H = 13.42, df = 2, p < 0.0001).
Conversely, females moved (H = 14.93, df = 2, p < 0.0001),
and autogroomed (H = 10.57, df = 2, p = 0.005) significantly
Table 1 Sample size for the brown-throated three-toed sloths in the
Atlantic forest of northeastern Brazil
Bold values indicate Total
Individual Period No. of days of hours ∑ of
behavioral
observations
BV-1 Aug–Dec 2004 11 264 1056
BV-2 Aug 2004–Jan
2005
10 240 960
BV-3 Sept 2004–Jan
2005
8 192 784
29 696 2800
F-1 Sept–Dec 2004 9 216 864
F-2 Nov 2004–Jan
2005
5 120 480
14 336 1344
1032 4144
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less than the male (Table2). No differences were detected in
travelling or eating among the three individuals (Table2).
The activity budget was dominated by resting followed
by moving for all animals, although the percentages of
the other behavioral categories varied among the indi-
viduals (Table2). Both females, BV-1 (H = 32.23, df = 4,
p < 0.0001), and BV-3 (H = 25.38, df = 4, p < 0.0001), as well
as male BV-2 (H = 34.77, df = 4, p < 0.0001) rested more
than performed any other of the studied behaviors (Table3).
Although no other significant differences were detected
among the other behaviors in female BV-1 and BV-3, male
BV-2 was recorded moving significantly more than travelling
(p = 0.027) and eating (p = 0.03).
Our 24-h period observations showed also that the two
infants rested for a mean of 79% of their time, and that there
was no statistically significant inter-individual difference
in the percentage of time spent resting (Mann–Whitney
test U = 17.5, p = 0.518). No significant differences were
detected in the percentage of time spent moving (U = 17,
p = 0.452), travelling (U = 15.5, p = 0.275), eating (U = 12,
p = 0.156), or autogrooming (U = 13, p = 0.158).
The activity budget of the infants was dominated by rest-
ing, which was followed, in order of magnitude, by mov-
ing, eating, travelling, and autogrooming (Table4). Both
infants, BV1 Infant (X2 = 36.017, df = 4, p < 0.0001), and
BV3 Infant (X2 = 21.311, df = 4, p < 0.0001), rested and
moved more than they performed any other of the studied
behaviors (Table5).
Activity pattern
The sloths were found to be primarily diurnal, with the
majority of activity on most 24-h days occurring during the
hours of daylight (Fig.1a–e). However, on some days, activ-
ity in the moving and travelling categories were observed
during parts of the night, as early as 01:00h and as late
as 22:00h (Fig.1b, c). Eating was the only activity that
never started before dawn, even though its bouts continued
Table 2 A comparison of the mean percentage of time (± SD) spent on each behavioral category among brown-throated three-toed sloth indi-
viduals during the 24-h periods in the Atlantic forest of northeastern Brazil
*Statistically significant
Individual n (days) Resting (%) Moving (%) Travelling (%) Eating (%) Auto-grooming (%)
BV-1 11 80.19 (± 4.02) 5.90 (± 2.34) 3.36 (± 1.43) 3.18 (± 2.18) 3.36 (± 2.06)
BV-2 10 69.4 (± 6.36) 10.70 (± 2.71) 4.80 (± 2.44) 3.40 (± 2.72) 7.7 (5.46)
BV-3 879.5 (± 4.07) 5.25 (± 1.16) 4.75 (± 2.38) 4.38 (± 2.32) 2.13 (± 1.45)
Overall 29 74.9 (± 8.64) 7.3 (± 2.98) 4.3 (0.82) 3.65 (± 0.64) 4.40 (± 2.93)
K–Wallis (H) 13.42 14.94 2.6 1.47 10.57
df 2 2 2 2 2
p< 0.0001 < 0.0001 0.272 0.479 0.005
N96 96 96 96 96
Multiple comparisons BV-1 × BV-2 (< 0.0001)* BV-1 × BV-2 (< 0.0001)* NS NS BV-1 × BV-2 (= 0.025)*
BV-1 × BV-3 (= 0.953) BV-1 × BV-3 (= 0.803) BV-1 × BV-3 (= 0.734)
BV-2 × BV-3 (= 0.001)* BV-2 × BV-3 (< 0.0001)* BV-2 × BV-3 (= 0.007)*
Table 3 Multiple comparisons
of the mean percentage of
time spent on each behavioral
category by each brown-
throated three-toed sloth
individual during the 24-h
periods in the Atlantic forest of
northeastern Brazil
* Statistically significant
Behavioral categories BV-1 BV- 2 BV-3
Resting×moving < 0.0001* < 0.0001* < 0.0001*
Resting×travelling < 0.0001* < 0.0001* < 0.0001*
Resting×eating < 0.0001* < 0.0001* < 0.0001*
Resting×auto-grooming < 0.0001* < 0.0001* < 0.0001*
Moving×travelling 0.152 0.027* 0.994
Moving×eating 0.107 0.003* 0.955
Moving×auto-grooming 0.152 0.522 0.112
Travelling×eating 1 0.947 0.998
Travelling×auto-grooming 1 0.555 0.241
Eating×auto-grooming 1 0.179 0.387
Kruskal–Wallis 32.23 (< 0.0001) 34.77 (< 0.0001) 25.38 (< 0.0001)
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throughout the day and infrequently at night until around
21:00h (Fig.1d). Generally, the observed animals were
more diurnal, with the highest peaks of activity around
07:00h and 16:00h.
Throughout the study period both the females BV1 and
BV3, and the male BV2 were invariably inactive between
22:00 and 01:00h. The only exception over this period was
some occasional autogrooming, likely triggered by some
external stimulus, such as ticks and mosquitoes (Fig.1a–e).
Adults exhibited a highly cyclic pattern of activity, always
starting their activity bouts at the same time, and also a
biphasic pattern of activity, with moving, travelling, eating,
and autogrooming presenting at least one peak in the morn-
ing and one in the afternoon (Fig.1a–e). The same pattern
was also detected among the infants (Fig.1a–e).
Throughout the study period both F1 and F2 infants were
invariably inactive between 19:00 and 05:00h, presenting an
even more markedly diurnal activity rhythm. They started
to move, travel, and eat sometime between sunrise and
07:00h, although these activity bouts continued to occur
until 19:00h (Fig.1a–e).
When we analyze each observational day separately for
each of the sloths, for each of the three adult individuals,
we detect variability in the time of the day and frequency
with which the daily activities occur for the three individuals
(Figs.2a–k, 3a–h, 4a–j). For instance, BV-1 (Fig. 2a–k)
could be recorded feeding at 18:00h in day one (Fig.2a),
around 11:00h in day three (Fig.2c), at 8:00h in the morn-
ing in day five (Fig.2e), or at 16:00h in the afternoon in day
10 (Fig.2j). The same can be said of the daily activities of
the infants (Fig.2a–k; Fig.3a–h). Additionally, their activi-
ties did not always overlap with that of their mothers. For
instance, the infant could be moving when his mother was
feeding or resting (Fig.2c).
When these data were arranged according to day versus
night occurrence, most behaviors showed distinct partition-
ing to the daytime (Fig.5). In the example data from sloth
BV-1, this is most noticeable with grooming at 100% day
activity, while eating 80% occurred during the day. Rest-
ing occurred primarily during the night, at 60%. This broad
pattern of primarily daytime portioning of activity was
observed for all animals, but with some variation within each
specific behavior category. Average proportions across all
five animals reveal a highly conserved temporal portioning:
resting (day 40 ± 7%: night 60 ± 11%; mean ± SE), moving
(87 ± 16%: 13 ± 4%), travelling (78 ± 15%: 22 ± 7%), eating
(95 ± 18%: 5 ± 4%) and grooming (94 ± 18%: 6 ± 4%) (Fig.5;
Suppl. Mat. S1–S4).
Circadian/diel andultradian rhythmicity
To objectively test for rhythmic patterns of behavior, con-
catenated data from individual sloths were subjected to
X2-squared periodogram analysis and FFT. Representa-
tive actograms for each of the five behaviors are shown for
BV1 (Fig.6), BV2, BV3 and the two infants (Suppl. Mat.
S5–S8). In most cases significant rhythmicity with ~ 24-h
period length (20–27h; p < 0.001) were detected for each of
the five recorded behaviors in both adult and infant animals
(Table6; Fig.7a, b). Only in BV-2 and BV-3 were behaviors
not found to be significantly rhythmic, specifically moving
and travelling.
Resting behavior consistently provided the most robust
measure of activity, as measured by the amplitude and power
axes of the periodogram and FFT analyses respectively, act-
ing as objective measures of the relative strength of each
rhythm. Example analysis is shown for moving behavior for
BV1 (Fig.7c, d).
Table 4 A comparison of the mean percentage of time (± SD) spent on each behavioral category among brown-throated three-toed sloth infants
during the 24-h periods in the Atlantic forest of northeastern Brazil
Individual n (days) Resting (%) Moving (%) Travelling (%) Eating (%) Auto-grooming (%)
F-1 9 81 (± 4.12) 10 (± 3.04) 1 (± 0.67) 3 (± 0.71) 1 (± 0.37)
F-2 5 77.2 (± 7.39) 12.6 (± 5.59) 1.4 (± 0.93) 4.6 (± 0.75) 0.2 (± 0.2)
Overall 14 79.1 (± 2.69) 11.3 (± 1.84) 1.2 (± 0.28) 3.8 (± 1.13) 0.6 (± 0.57)
Table 5 Multiple comparisons of the mean percentage of time spent
on each behavioral category by each brown-throated three-toed sloth
infant during the 24-h periods in the Atlantic forest of northeastern
Brazil
* Statistically significant
Behavioral categories BV-1 Infant BV-3 Infant
Resting×moving < 0.0001* < 0.0001*
Resting×travelling < 0.0001* < 0.0001*
Resting×eating < 0.0001* < 0.0001*
Resting×auto-grooming < 0.0001* < 0.0001*
Moving×travelling < 0.0001* 0.005*
Moving×eating < 0.0001* 0.057*
Moving×auto-grooming < 0.0001* 0.002*
Travelling×eating 0.518 0.767
Travelling×auto-grooming 1 0.992
Eating×auto-grooming 0.518 0.508
Kruskal–Wallis 36.017 (< 0.0001) 21.311 (< 0.0001)
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When the data were subjected to cosinor analysis (using
a single sine wave) or CircWave analysis (using multiple
harmonics), significant 24-h rhythmicity was observed, and
the center of gravity for each behavior (except resting) was
determined to occur during the daytime between ZT4 and
ZT8, i.e. 10:00h and 14:00h (Table6; Fig.7c, d).
The advantage of CircWave analysis is that it allows for
more precise determination of multicomponent rhythms, and
as such some behaviors allowed fitting of several harmonics
revealing two distinct bouts of activity, one during the morn-
ing, the other during late afternoon (Fig.7d). This bimodal
pattern of behavior can also be seen in the actogram for
BV-1 moving, and especially so for eating. In addition to
rhythms with a circadian period length, ultradian rhythms
of 16–18h were detected for BV-2 and BV-3 adults in rest-
ing, eating and grooming behaviors, as well as for infant F1
in eating.
Discussion
General considerations
Bradypus spp. are heterothermic animals, with low and
labile body temperature (Giné etal. 2015). To adapt to their
folivorous and arboreal habit, they have a low metabolism
and low percentage of body muscle mass (Kredel 1928;
Goffart 1971; McNab 1978). Because of these metabolic
constraints, their activity patterns, budget, and rhythm are
a function of the oscillations of ambient temperature (Brit-
ton and Kline 1939; Giné etal. 2015). In most studies car-
ried out to date, Bradypus spp. have been observed as active
mostly during the day and the night, and have been consid-
ered cathemeral creatures (Queiroz 1995; Chiarello 1998,
2008; Giné etal. 2015). In cases in which competitors and/or
predators were absent, however, sloths apparently adopted a
pronounced diurnal feeding habit (Consentino 2004).
Interestingly, none of these studies considered the effects
that the various forms of human impacts present would have
on the ecology and behavior of the sloths, despite the poten-
tial impacts that they might exert on the species (Mendes
Pontes etal. 2007, 2016; Pinheiro and Mendes Pontes 2015).
Furthermore, it has been postulated that colder or hotter sea-
sons, altitudinal, or latitudinal range, or montane or low-
land forests with colder or hotter ambient temperatures are
the best predictors of sloth activity (Chiarello 1998, 2008;
Urbani and Bosque 2007; Giné etal. 2015).
Besides having to adjust to the oscillations of ambient
temperature, sloths are likely to modify their behavior to
avoid predators and competitors, to locate food, and to assist
in the process of digestion, as with other mammals (Donati
and Borgognini 2006; Halle 2006; Eising etal. 2014). The
importance of these variables should change completely in
(a) Resng
(b) Moving
(c) Travelling
0
20
40
60
80
100
18:00-18:45
19:00-19:45
20:00-20:45
21:00-21:45
22:00-22:45
23:00-23:45
00:00-00:45
01:00-01:45
02:00-02:45
03:00-03:45
04:00-04:45
05:00-05:45
06:00-06:45
07:00-07:45
08:00-08:45
09:00-09:45
10:00-10:45
11:00-11:45
12:00-12:45
13:00-13:45
14:00-14:45
15:00-15:45
16:00-16:45
17:00-17:45
%
Females BV-1 and BV-3Male BV-2Infants
0
5
10
15
20
25
30
35
40
45
18:00-18:45
19:00-19:45
20:00-20:45
21:00-21:45
22:00-22:45
23:00-23:45
00:00-00:45
01:00-01:45
02:00-02:45
03:00-03:45
04:00-04:45
05:00-05:45
06:00-06:45
07:00-07:45
08:00-08:45
09:00-09:45
10:00-10:45
11:00-11:45
12:00-12:45
13:00-13:45
14:00-14:45
15:00-15:45
16:00-16:45
17:00-17:45
%
Females BV-1 and BV-3Male BV-2Infants
0
3
6
9
12
15
18
21
18:00-18:45
19:00-19:45
20:00-20:45
21:00-21:45
22:00-22:45
23:00-23:45
00:00-00:45
01:00-01:45
02:00-02:45
03:00-03:45
04:00-04:45
05:00-05:45
06:00-06:45
07:00-07:45
08:00-08:45
09:00-09:45
10:00-10:45
11:00-11:45
12:00-12:45
13:00-13:45
14:00-14:45
15:00-15:45
16:00-16:45
17:00-17:45
%
Females BV-1 and BV-3Male BV-2Infants
(d) Eang
(e) Autogrooming
0
3
6
9
12
15
18
21
24
18:00-18:45
19:00-19:45
20:00-20:45
21:00-21:45
22:00-22:45
23:00-23:45
00:00-00:45
01:00-01:45
02:00-02:45
03:00-03:45
04:00-04:45
05:00-05:45
06:00-06:45
07:00-07:45
08:00-08:45
09:00-09:45
10:00-10:45
11:00-11:45
12:00-12:45
13:00-13:45
14:00-14:45
15:00-15:45
16:00-16:45
17:00-17:45
%
Females BV-1 and BV-3Male BV-2Infants
0
5
10
15
20
25
30
18:00-18:4
5
19:00-19:4
5
20:00-20:4
5
21:00-21:4
5
22:00-22:4
5
23:00-23:4
5
00:00-00:4
5
01:00-01:4
5
02:00-02:4
5
03:00-03:4
5
04:00-04:4
5
05:00-05:45
06:00-06:4
5
07:00-07:4
5
08:00-08:45
09:00-09:4
5
10:00-10:4
5
11:00-11:4
5
12:00-12:45
13:00-13:45
14:00-
14:45
15:00-
15:45
16:00-
16:45
17:00-17:4
5
%
Females BV-1 and BV-3Male BV-2Infants
Fig. 1 Percentage of time three adult and two infants brown-throated
three-toed sloths (Bradypus variegatus) spent in a resting, b moving, c
travelling, d eating, and e autogrooming, during 24-h periods in a remnant
of the Atlantic forest of northeastern Brazil
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highly disturbed sites, such as in the Atlantic forest in this
study. At these disturbed sites, competitors and predators
have become extinct, forest structures have changed (e.g.
canopy discontinuity, selective cut, among others), and
tree species diversity has been reduced (Silva and Tabarelli
2000; Tabarelli etal. 2004; Santos etal. 2008), all of which
would be predicted to impact sloth behavior. For instance,
the Atlantic Forest of northeastern Brazil has lost more
than 50% of the total tree species (Silva and Tabarelli 2000;
Oliveira etal. 2004; Santos etal. 2008), which may change
dramatically the structure of the forest as well as the avail-
ability of feeding trees.
In the Atlantic forest of northeastern Brazil, where this
study was carried out, there is no continuous forest or con-
trol fragment and more than half of the tree species have
gone extinct (Silva and Tabarelli 2000; Oliveira etal. 2004;
Santos etal. 2008). All fragments are highly secondarized,
subject to border effect, have irregular shapes, and have
experienced some degree of human interference, such as
hunting, the presence of feral dogs, forest clearing, selective
cutting, or intentional fires, in addition to being bisected by
roads used by people and domestic animals (Mendes Pontes
etal. 2016). Therefore, we could not have control fragments
or control sloths to test hypotheses related to disturbed-
undisturbed sites, predator-absence effects, reproductive
status, gender differences, or food-density effects.
Although our sample size is comparatively smaller than
that of other studies, no measure of continuous time was
smaller than 24h. Thus, the atypical behavioral pattern
found here may offer evidence of some cause-consequences
of utmost importance for a better understanding of the spe-
cies in a highly modified, ever changing landscape.
Diel/circadian rhythmicity
Here we reveal that the adult and infant sloths exhibit dis-
tinct 24-h rhythmicity in all behaviors examined: resting,
moving, travelling, eating and grooming. Objective analy-
sis using Periodogram and FFA demonstrate clear rhythmic
activity with period lengths close to 24h. Visual inspec-
tion of the representative actograms reveal the occurrence
of rhythmicity. In some cases, ultradian rhythms of 16–18h
were also detected in addition to the rhythms of circadian
tau. Cosinor and Circwave analyses also support these find-
ings, and also place the center of gravity of the activity for
all behaviors except resting in the middle of the light/day
phase between ZT4 and ZT8. In several cases the behavior
is shown as a bimodal pattern with a distinct bout of activity
in the morning (between ZT0–4) and another during the late
afternoon (ZT8–12).
The proportion of time spent in each specific activity par-
titioned according to day or night clearly reveals the diur-
nal day active aspect of these rhythms. This is at 100% for
grooming through to 80% during the daytime for eating. The
least partitioned behavior would be resting, of which 40%
occurs during the daytime and 60% during the night.
These sloths inhabiting the disturbed Atlantic forest
exhibit circadian/diel rhythms of a diurnal/daytime active
nature, and with two distinct activity bouts, one during the
morning, one in the late afternoon.
Activity pattern
The studied brown-throated three-toed sloths are one of the
few living-dead species (Woodroffe and Ginsberg 1998) that
have survived a mass extinction without precedent in mod-
ern history (Silva and Tabarelli 2000; Mendes Pontes etal.
2016). The scenario in which this study site is inserted has
lost 50% of all tree species, 33% of all zoochorous trees, is
highly homogenized, secondarized, and has a highly discon-
tinuous canopy (Silva and Tabarelli 2000; Tabarelli etal.
2004; Santos etal. 2008).
Accordingly, approximately 50% of all medium-sized,
and all large mammals, have gone extinct, including all the
sloth’s competitors and predators (Silva Júnior and Mendes
Pontes 2008; Mendes Pontes etal. 2016). Other potential
predators of the sloths, such as medium-sized and large cats,
boas (Boa constrictor), and various birds of prey are also
extinct (Mendes Pontes and Soares 2005).
Although this scenario seems the worst possible from a
broad conservation perspective, it may have positively ben-
efitted the sloth population through a combination of fac-
tors. They no longer have to invest their time in avoiding
interspecific competition and predation, and, at the same
time, have access to an abundance of Cecropia spp. (Cecro-
piaceae) trees, which dominate the forest border. The lat-
ter, also contributes to reducing or preventing intraspecific
competition. This possibly facilitated the occurrence of a
synchronous activity pattern, in which all individuals started
and ended their activities roughly at approximately the same
time, as well as allowing them to be primarily day active.
Slater (1981) and Chiarello (1998) suggest that the lack
of synchrony between individual sloths could result from
’noise’ in the system and that it would not affect their sur-
vival. It should be beneficial only to those living in undis-
turbed sites, where it could help to confuse or avoid preda-
tors (Pepin and Cargnelutti 1994), or avoid competitors (as
in Queiroz 1995), but in a highly disturbed and depauperated
site, such as in this study, it should not be necessary. In the
Fig. 2 Daily activity budget throughout each of the observational
days ak for female BV-1 and her infant F1. Inner circle represents
adult behavior; outer circle represents infant behavior; Time incre-
ments are 15min. Time is reported in real clock time; day and night
are shown as outer light yellow and grey sections; %: Percentage of
each behavior in the daily sample
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case of Chiarello (1998), for instance, there was already a
tendency for the sloths to start feeding and moving at the
same time. Thus, a highly synchronized activity pattern of
the individuals that in turn, synchronize their activities with
ambient temperature (as in Giné etal. 2015), seems much
more plausible.
In this study, the diversity of food items was the lowest
possible and natural predators were absent. Then, the sloths
appeared to maximized food acquisition by exclusively
inhabiting the forest border where Cecropia spp. trees were
most abundant. Since they did not have to compete for this
abundant source, it should be easier for them to feed under
Fig. 3 Daily activity budget throughout each of the observational
days ah for female BV-3 and her infant F2. Inner circle represents
adult behavior; outer circle represents infant behavior; Time incre-
ments are 15min. Time is reported in real clock time; day and night
are shown as outer light yellow and grey sections; %: Percentage of
each behavior in the daily sample
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Fig. 4 Daily activity budget throughout each of the observational days aj for male BV-2. Time increments are 15min. Time is reported in real
clock time; day and night are shown as outer light yellow and grey sections; %: Percentage of each behavior in the daily sample
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the sunlight. This would suggest they would adopt a diurnal,
or primarily diurnal feeding habit, as was the case of sloth
behavior reported in Carmo (2002), and Consentino (2004).
Goffart (1971), Urbano and Bosque (2007), and Castro-
Vasquez etal. (2010) demonstrated that Cecropia spp. can
be an abundant and reliable source of food for sloths, and
that sloths can become dependent on them for their primary
food source. In the current study, the sloths appeared to be
dependent in that they inhabited exclusively the forest bor-
der, an area where Cecropia was found especially abundant.
The Atlantic forest of northeastern Brazil has lost 98%
of its original forest (Silva Júnior and Mendes Pontes 2008;
Mendes Pontes etal. 2016), and no pristine, or control for-
est remains, making it difficult to know if brown-throated
three-toed sloths in totally preserved Atlantic forest sites
would still keep a primarily diurnal activity pattern. Queiroz
(1995), however, sheds light on this question in his assess-
ment of brown-throated three toed sloth behavior, studied in
a totally undisturbed site, with all competitors (e.g. howler
monkey, A. seniculus) and predators (e.g. harpy eagle, H.
harpija) present, and in an extremely rich vertebrate assem-
blage. Here sloths presented a cathemeral activity pattern.
Diurnality should therefore be an adaptive response to a
changing environment absent of predators.
Two other important variables could have triggered noc-
turnal inactivity in these sloths. Human impact through
uninterrupted and intense nocturnal hunting, with barking
feral dogs and frequent rifle shots, and the presence of vul-
nerable and dependent recently born babies, as suggested by
Castro-Vasquez etal. (2010).
Bradypus spp. have been recognized as essentially cath-
emeral (Chiarello 2008). Most of the studies carried out to
date with B. variegatus in protected areas (Queiroz 1995),
and in disturbed forests of the tropics have also revealed
cathemerality (Montgomery and Sunquist 1978; Consen-
tino 2004; Urbani and Bosque 2007; Castro-Vasquez etal.
2010). This suggests that ultimately shifting to a diurnal
activity pattern should benefit sloths in areas subjected to
very high human impact such as in this study. In fact, litera-
ture has shown that competition and predation, or a lack of
it, can contribute to adjustments to diel and circadian activity
patterns (Fenn and MacDonald 1995; Alanara etal. 2001),
which may be manifested through becoming more diurnal
(Lockard 1978).
This phenomenon of temporal niche switching of loco-
motor activity has been shown in various species of animal
(Hut etal. 2012). Laboratory experiments have shown that
nocturnal to diurnal switches can be induced by suppres-
sion of wheel-running behavior in rodents (Tachinardi etal.
2015), cold exposure during work-for-food protocols in
rodents (van der Vinne etal. 2014), and necessary balancing
of energetic demand in small mammals (van der Vinne etal.
2015). Other causes of temporal niche switching, however,
vary from reduced food intake to seasonal cues to predation
risks (Hut etal. 2012).
The same seems to hold true for B. torquatus, in which a
cathemeral activity pattern was recorded in disturbed sites
(Chiarello 1998; Carmo 2002; Cassano 2006; Giné etal.
2015). Another species, B. tridactylus, showed a cathemeral
activity pattern in a forest fragment in central Amazonia
(Carmo 2002).
Activity budget
As expected for an heterothermic, arboreal mammal, with
a highly folivorous diet and low metabolic rate (McNab
1963; Goffart 1971; Nagy and Montgomery 1980), living
in highly disturbed environments, the brown-throated three-
toed sloths in this study spent a large proportion of the 24-h
day at rest. An average of 74.9% of the adult sloth activ-
ity pattern was spent resting, with infants showing slightly
more at 79.1%. Although slightly higher, this is close to what
Urbani and Bosque (2007) and Castro-Vasquez etal. (2010)
found in similar conditions for adults (70.8% and 72.9%,
respectively).
The sloths in this study spent a long, continuous period
of time inactive in the middle of the night (and even a longer
period in the case of the infants), which, besides allowing
them to rest, may help in the slow process of digestion of
leaves acquired during the daytime. Giné etal. (2015) say
that resting for an entire day or night phase of the 24-h cycle
may be disadvantageous for sloths due to several potential
short-time requirements. For example, as they need postural
or spatial change for thermoregulation, digestion, a need to
stay vigilant to predators, and the need of food acquisition.
In the case of the current study, however, where competi-
tors and predators are absent, where sloths feed exclusively
Average proportion
BV1 proportions of day/night activity
100
80
60
40
20
0
RestingMovingTrave llingEatingGrooming
Fig. 5 Proportions of day and night activity for BV-1. Scored catego-
rized activity arranged according to the 12 h daylight or 12h dark/
night phase of the diel, with total activity = 100%. The majority of
activity in each category is almost entirely concentrated to the day-
time, except resting, which occurs slightly more during the night.
Data are mean ± SEM of activity scored per 24-h period over 11days
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0 8 16 0 8 16 0
12
10
8
6
4
2
Time (hour)
Days
0 8 16 0 8 16 0
12
10
8
6
4
2
Time (hour)
Days
0 8 16 0 16 0
12
10
8
6
4
2
Time (hour)
Days
0 8 16 0 8 16 0
12
10
8
6
4
2
Time (hour)
Days
0 8 16 0 8 16 0
12
10
8
6
4
2
Time (hour)
Days
(a)
(b)
(c) (d)
(e)
Resting
Moving
Travelling Eating
Grooming
Fig. 6 ae Activity records of each of the five behavior categories for
BV-1 are shown in double-plotted format. Each horizontal line rep-
resents a 48 h period, and the second 24 h period is plotted to the
right and below the first. Vertical bars represent the occurrence of a
behavioral observation. Data are concatenated allowing for 12days
of activity to be analyzed as a continuum. The timing of the light–
dark (diel) cycle is indicated by the white-and-black bars below the
records. Time is provided as local clock time. Distinct and robust
rhythms can be seen for all five behaviors, in which resting is concen-
trated in the night; and moving, travelling, eating and grooming are
almost entirely restricted to the daytime
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Table 6 Circadian/diel analysis of the brown-throated three-toed sloth in the Atlantic forest of Northeastern Brazil
Individual Behavior Significant periodogram
(p < 0.001)
FFT (cycle 0.042) Cosinor analysis Circwave analysis
Period length Amplitude Power F p R2CG F p R2CG No. Sin
BV-1 Resting 23.7 220 0.075 23.39 0.001 0.27 17.67 11.4 0.001 0.35 17.67 3
Moving 24.0 160 0.026 14.72 0.001 0.19 5.04 7.74 0.001 0.27 5.04 3
Travelling 20.7 120 0.015 6.07 0.003 0.08 5.73 NA
Eating 24.0 130 0.013 4.56 0.012 0.07 6.98 3.22 0.006 0.13 6.98 3
Grooming 24, 22 150, 125 0.018 11.88 0.001 0.16 5.59 4.75 0.001 0.19 5.59 3
BV-2 Resting 23,7 270 0.08 25.94 0.001 0.31 17.55 10.38 0.001 0.36 17.55 3
Moving 23,3 145 0.035 12.16 0.001 0.17 4.85 4.47 0.001 0.19 4.85 3
Travelling NA NA 0.022 5.43 0.006 0.09 3.68 2.51 0.025 0.12 3.68 3
Eating 24, 16.5 190, 120 0.017 5.97 0.003 0.09 7.39 3.38 0.004 0.15 7.39 3
Grooming 23.67, 16 145, 85 0.022 9.12 0.001 0.13 6.4 4.27 0.001 0.18 6.4 3
BV-3 Resting 23.7, 16 150, 90 0.05 9.05 0.001 0.15 20.65 6.06 0.001 0.26 20.65 3
Moving NA NA 0.019 8.16 0.001 0.13 7.65 4 0.001 0.19 7.65 3
Travelling NA NA 0.018 3.4 0.037, n.s 0.06 9.32 3.29 0.005 0.16 9.32 3
Eating 16, 24 125, 135 0.031 3.95 0.022 0.07 9.57 4.75 0.001 0.22 9.57 3
Grooming 26.5, 18.5 190, 110 0.0065 0.58 0.56, n.s 0.01 6 0.86 0.535 0.05 6 3
F1 Resting 24.3 225 0.05 20.37 0.001 0.28 18.69 10.28 0.001 0.38 18.69 3
Moving 24.0 180 0.045 19.36 0.001 0.27 6.4 9.65 0.001 0.36 6.4 3
Travelling 20.5, 26 105, 155 0.011 3.33 0.04 0.06 8.13 1.46 0.197, n.s 0.08 8.13 3
Eating 18, 24 110, 120 0.022 4.56 0.013 0.08 7.77 3 0.01 0.15 7.77 3
Grooming 24.3, 26 135, 140 0.009 3.79 0.026 0.07 4.86 1.98 0.076 0.11 4.86 3
F2 Resting 24.7 180 0.09 10.86 0.001 0.28 18.5 6.01 0.001 0.41 18.51 3
Moving 25.0 210 0.071 12.38 0.001 0.3 6.17 4.6 0.001 0.34 6.17 3
Travelling 25.0 200 0.014 0.64 0.532, n.s 0.02 4 0.76 0.604, n.s 0.079 4 3
Eating 23.5, 26.7 125, 140 0.033 2.14 0.127, n.s 0.07 8.3 2.85 0.018 0.24 8.3 3
Grooming 20.3 120 NA 1 0.375, n.s 0.04 1 1 0.438, n.s 0.1 1 3
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during the day, and where ambient temperature at night is
fairly warm, resting during the night phase of the 24-h cycle
should in fact be beneficial for them. Additionally, being
concealed over the night, when hunting is most intense (and
feral dogs and rifle shots can be heard throughout the entire
night), could be highly beneficial to these sloths, especially
for females with babies.
While our sample size is too small to investigate sex-
specific differences in behavior observed in other studies
(Carmo 2002; Castro-Vasquez etal. 2010), we noted an
increase in activity in our male subject. Further studies are
needed to shed light on this question.
Conclusion
Brown-throated three-toed sloths living in a forest bor-
der in the highly impacted Atlantic forest of north-
eastern Brazil were found to be primarily diurnal and
exhibited a highly synchronous activity pattern. During
several days and of specific behaviors, bimodal patterns
of activity were observed. Sloths rested for most of their
time, fed exclusively during the day, and spent a long,
continuous period of time inactive during the night. We
hypothesize that this activity pattern and time budget is
an adaptive response to a modified, highly simplified and
0 4 8 12 16 20 24
-2
0
2
4
6
Zeitgeber Time (hours)
Moving
00.2 0.40.6 0.81
Frequency (cycles/hr)
0
0.01
0.02
0.03
Relative Power
0.042
10 12 14 16 18 20 22 24 26 28 30
Period (hours)
20
40
60
80
100
120
140
160
Amplitude
(a)
(d)
(b)
(c)
0 4 8 12 16 20 24
-2
0
2
4
6
Zeitgeber Time (hours)
Moving
Fig. 7 Temporal analysis of moving activity for BV-1. For peri-
odogram analysis (a), the ascending straight line represents a statis-
tical significance of p = 0.001. For Fourier analysis (b), a frequency
of 0.042 cycle/h corresponds to 1 cycle/24 h, which is donated by
the arrow head below the chart where statistical significant (statisti-
cal significance was determined by the Clocklab program). Cosinor
analysis (c) (p < 0.05, R2 = 0.19, center of gravity, CG = ZT5.04)
and Circwave analysis (d) (p < 0.05, R2 = 0.27, CG = ZT5.04) of
BV-1 moving activity. In the graphs, each dot represents the level
of activity for each animal in time-specific groups, the curve repre-
sents the best-fit Fourier curve, the Center of Gravity is represented
by the vertical bar, and the mean of the entire data set is represented
by the cross. All animals showed significant rhythmicity in all or
most behavior categories when analyzed using these four methods
(Table6). Each independent method scored BV-1 moving activity as
significantly rhythmic. A bimodal pattern for moving can be observed
with peak times of ZT2 and ZT10 (see also actogram analysis,
Fig.4b)
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Mammalian Biology
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homogenized environment, and that is deplete of predators
and competitors.
Acknowledgements We thank the head of the Condomínio Luzanópo-
lis for granting permission to carry out the research in its premises,
and Department of Zoology, Universidade Federal de Pernambuco for
provision of equipment for fieldwork.
Author contributions DOB: Collected and analyzed the data, and wrote
the article; LRRL: Analyzed the data; GED and DJA: Analyzed the
data and wrote the article; ARMP: Designed the experiment, analyzed
the data and wrote the article.
Funding This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Compliance with ethical standards
Conflict of interest We have no conflicts of interest/competing inter-
ests.
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... Indeed, there is evidence that birds must forage more in fragmented habitats (Saunders 1980, Redpath 1995, and that disturbances like logging and agriculture can alter the timing of daily activity for forest birds (Fonturbel et al. 2021). Moreover, fragmentation has markedly changed how many mammals structure their activity (Chaves et al. 2011, Mekonnen et al. 2017, Bezerra et al. 2020. Investigating how birds adjust their activity patterns in response to habitat fragmentation over the long-term can help to uncover important adaptations and mechanisms used to persist in in altered landscapes (Cornelius et al. 2017, Doherty andDriscoll 2018). ...
... Unlike many anthropogenically fragmented landscapes, the kīpuka system has stable populations of native birds (Flaspohler et al. 2010) and few anthropogenic stressors, enabling us to isolate the influence of fragmentation on activity patterns and to assess long-term ecological and evolutionary responses in activity strategies. We expected birds in the fragmented landscape to exhibit greater overall activity levels and more sustained activity throughout the day than those in the continuous landscape, as fragmentation often increases foraging time in mammals (Chaves et al. 2011, Mekonnen et al. 2017, Bezerra et al. 2020) and birds (Saunders 1980, Redpath 1995. Moreover, birds in the fragmented landscape will readily cross gaps but have smaller home ranges than birds in the continuous landscape (Paxton et al. unpubl.), ...
... Birds in the fragmented landscape exhibited earlier peak activity, higher activity levels during daylight hours, more sustained activity throughout the day, and a greater propensity for the constant busy bee strategy than those in the continuous forest. When fragmentation alters the availability and spatial distribution of food resources, animals often behaviorally adjust by either maximizing energy gain through intensified foraging, or by minimizing time and energetic requirements via decreased foraging and increased resting (Wong and Sicotte 2007, Boyle and Smith 2010, Chaves et al. 2011, Palma et al. 2011, Mekonnen et al. 2017, Bezerra et al. 2020). Although we did not directly measure foraging behavior, our observation that birds in the fragmented landscape exhibited higher activity levels and more sustained activity than those in the continuous forest is consistent with an energy maximization strategy. ...
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