Biologia

https://doi.org/10.2478/s11756-020-00523-w

ORIGINAL ARTICLE

Diverging temporal and thermal niche dimensions favor syntopy

of Tropidurus hispidus and Tropidurus semitaeniatus
(Squamata: Tropiduridae)
Thiago Maia-Carneiro 1 & Carlos Frederico Duarte Rocha 1

Received: 15 December 2019 / Accepted: 20 May 2020

# Institute of Zoology, Slovak Academy of Sciences 2020

Abstract
Divergences in ecological niche dimensions favor the coexistence of species in syntopy. Supposedly, closely related species face
stronger pressures to differ in dimensions of niches. Integration among temporal, spatial and thermal niche dimensions is relevant
for lizards because it allows proper regulation of body temperatures, which has consequences for their physiology and ecology.
Here, we investigated temporal (daily activity) and thermal (body and microhabitat temperatures) niche dimensions and ther-
moregulation of Tropidurus hispidus and T. semitaeniatus. We hypothesized that divergences of niche dimensions would favor
their local coexistences (syntopy). Tropidurus hispidus and T. semitaeniatus had similar lengths of daily activity cycles, but
differed in movement rates along the day (start of the activities; hours of activity peaks; periods of greater inactivity). Activity
rates and body temperatures of the lizards reflected phylogeny and thermal conditions. For both species, microhabitat temper-
atures and sunlight were sources for thermoregulation. Tropidurus semitaeniatus used warmer microhabitats than T. hispidus, but
the species had similar body temperatures. Body sizes did not influence body temperatures, presumably because of effective
behavioral thermoregulation allowing maintenance of body temperatures under appropriate ranges. Levels of active or passive
thermoregulation varied depending of the thermal source (air and substrate temperatures). To thermoregulate, lizards raised up or
brought down their bodies and increased or decreased levels of body flattening over substrates and shuttled across microhabitats
with different temperatures and levels of sunlight. Along the day, T. hispidus used mainly partially shaded microhabitats and
T. semitaeniatus used mostly full sunlight. Temporal and thermal niche dimensions of T. hispidus and T. semitaeniatus differed in
ways that favor their syntopy.

Keywords Body temperature . Daily activity . Microhabitat use . Niche overlap . Thermal ecology . Thermoregulation

Introduction
Divergences of ecological niche dimensions favor species’
local coexistences (syntopy) (Pianka 1969, 1973, 1993), and
closely related ones supposedly face stronger pressures to dif-
fer in such dimensions. Besides, integration among temporal,
spatial, and thermal niche dimensions is relevant for lizards
because it allows proper regulation of body temperatures even
when activity and microhabitat use are constrained by thermal
* Thiago Maia-Carneiro
tmaiacarneiro@gmail.com
1
Laboratório de Ecologia de Vertebrados, Departamento de Ecologia,
Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier
524, CEP 20550-013 Rio de Janeiro, Brazil
conditions (Van Sluys 1992; Hatano et al. 2001; Ribeiro et al.
2009; Maia-Carneiro et al. 2017a). In the face of variability of
microhabitat temperatures along the day, lizards maintain ap-
propriated processing of physiological and ecological func-
tions through behavior (Vitt and Carvalho 1995; Vitt et al.
1996; Maia-Carneiro et al. 2012, 2017a), which reflects phy-
logenetic factors (evolutionary kinship) (Bogert 1949; Rocha
et al. 2009; Grigg and Buckley 2013) as well as effects from
thermal conditions (Adolph and Porter 1993; Rocha et al.
2009; Maia-Carneiro et al. 2012). To avoid pronounced body
temperature alterations due to intrinsic (e.g., body size –
Garrick 2008; Maia-Carneiro and Rocha 2013a) and extrinsic
factors (e.g., microhabitat temperatures – Vitt and Carvalho
1995; Vitt et al. 1996; Rocha et al. 2009; Maia-Carneiro and
Rocha 2013b), lizards thermoregulate integrating perceptions
from temporal, spatial, and thermal niche dimensions.

Tropidurus hispidus (Spix, 1825) (Squamata, Tropiduridae)
is found in different countries of South America (Rodrigues
1987, 1988; Avila-Pires 1995; Carvalho 2013) and
Tropidurus semitaeniatus (Spix, 1825) (Squamata,
Tropiduridae) in some regions of Brazil (Carvalho 2013).
Tropidurus hispidus inhabit Amazonian savanna enclaves,
Atlantic Forest, Cerrado, and Caatinga (Rodrigues 1987,
1988; Avila-Pires 1995; Carvalho 2013), whereas
T. semitaeniatus live in rock outcrops in Caatinga Biomes,
in transitional zones towards the Atlantic Forest, and at alti-
tudes 1000 m above sea level in campos rupestres (rock
fields) (Carvalho 2013). Tropidurus hispidus and
T. semitaeniatus are respectively in the taxonomic groups
T. torquatus and T. semitaeniatus (Frost et al. 2001); never-
theless, as congeneric species, they share similarities regard-
ing components of the niches and differ in them when in
syntopy (Vitt 1995; Ribeiro and Freire 2010). Tropidurus
hispidus and T. semitaeniatus live side-by-side on rock out-
crops in northeastern Brazil, giving an opportunity to investi-
gate how divergences of ecological niche dimensions do allow
better coexistences. In spite of issues related to two-species
comparative studies (Garland and Adolph 1994), even with-
out using tools to control effects from phylogeny, between-
species comparisons reveal niche dimension divergences that
mirror effectively ecological differences that relate to chal-
lenges for coexistence. Ergo, here, we investigate components
of temporal (activity time) and thermal (body and microhabi-
tat temperatures – which vary across time and space) niche
dimensions and thermoregulation of T. hispidus and
T. semitaeniatus, looking for possible interspecific diver-
gences that would favor their syntopy.
Materials and methods
Study area
Fieldwork was carried out on rock outcrops in Igatu, municipal-
ity of Andaraí, state of Bahia, northeastern Brazil (12º53’ S,
41º19’ W), in the surroundings of the Parque Nacional da
Chapada Diamantina (a Conservation Unity for nature protec-
tion). The Chapada Diamantina is located in the central portion
of Bahia and is characterized by a plateau of rock outcrops dating
from the Mesoproterozoic Era (Delgado et al. 1994). Rocky
outcrops are xeric environments with elevated levels of drainage
and constant exposure to solar radiation. Nevertheless, in general,
particular altitudinal conditions in Chapada Diamantina sustain a
mesothermic climate of the type Cwb of Köppen (1923), with
mean annual temperatures below 22 ºC (Rocha et al. 2005;
Alvares et al. 2013). Some locations may have annual rainfall
lower than 700 mm, which represents the driest Cwb location in
Brazil (Alvares et al. 2013). Although mainly rock outcrops
dominate the area, some parts of the habitat have sand soils,
Biologia
sometimes covered by undergrowth, herbaceous, and shrubby
vegetations, and small trees.
Data collection
Data were collected by TMC in January and February 2013
through visual encounter surveys (VES - Crump and Scott
1994) limited by time (30 min). We avoided influences from
seasonal variations on the parameters investigated by concen-
trating the samplings in a same season. The VES consisted of
slow walks across the study area searching for lizards on
ground, plants, and rocks. To investigate the daily activity
cycles of T. hispidus and T. semitaeniatus, we conducted the
VES each hour between 05:00 and 19:00, covering fourteen
hour intervals of the day. Capture attempts with noose or by
hand were made whenever a lizard was sighted. We estimated
the activity cycle based on the number of individuals of each
species found active at different hour intervals along the day.
Each individual captured was identified by painting on its
body and by toe clipping to eliminate pseudo-replication. For
each lizard captured, we recorded body temperature using a
quick-reading cloacal thermometer Miller and Weber with
precision of 0.2 ºC. The microhabitat temperatures used by
the lizards were also measured using the Miller and Weber
thermometer − air temperature (Ta) 1 cm above the site where
the lizard was first sighted and substrate temperature (Ts) on
the same site. The snout-vent length (SVL) and the body mass
of the lizards were measured respectively with a Mitutoyo
caliper (precision of 0.01 mm) and with spring scales
Pesola (precision of 0.25 g for individuals up to 30 g
and of 1.0 g for those heavier than 30 g). Additionally, we
recorded light levels on microhabitats used by the lizards
when first sighted−shade; filtered sunlight (mosaic of light
and shade); full sunlight (direct exposure to sun radiation).
Analytical procedures
To evaluate the temporal overlap between T. hispidus and
T. semitaeniatus, we compared the daily activity of these
species through the Pianka’s niche overlap index Ojk = Σ
pij pik / √ Σ (pij2) (pik2), where, pij and pik are the propor-
tions of individuals of the species j and k found active at
each hourly interval i during the searches (Pianka 1973).
We compared the overlap of temporal niche dimensions
observed to those expected from 1000 simulations using
null models (randomization algorithm 3, meaning niche
breadth retained and zero states reshuffled and resource
states equiprobable - for more details see Winemiller and
Pianka 1990). This procedure allows to evaluate if the
temporal overlap differed from random distributions (sim-
ulations). Additionally, to compare between species the
number of individuals recorded as active at each period
Biologia
of hour surveyed, we performed a two-independent-
samples Kolmogorov-Smirnov test (Zar 1999).
To analyse if Tb, Ta, and Ts differed between species,
we made pairwise comparisons using Mann-Whitney U
tests (Zar 1999). To evaluate the use of each thermal
source for thermoregulation, we performed Spearman’s
non-parametric correlations (Zar 1999) with data of
body and microhabitat temperatures. To evaluate the
relevance of SVL and body mass for Tb, we performed
Spearman’s non-parametric correlations. Moreover, to
know if interspecific differences of body size (SVL
and body mass) were associated with microhabitat tem-
peratures, we pooled data of both species and performed
Spearman’s non-parametric correlations.
To test for intraspecific differences between Tb and
microhabitat temperatures and between Ta and Ts, we
performed Friedman tests followed by Wilcoxon signed
rank tests for pairwise comparisons. Levels of behavior-
al thermoregulation of each species were estimated
through differences between activity body temperatures
and microhabitat temperatures (ΔT), where ΔTa = (Tb –
Ta) and ΔTs = (Tb – Ts) (Vrcibradic and Rocha 1998;
Kiefer et al. 2007; Sousa and Freire 2011; Maia-
Carneiro and Rocha 2013b). We considered lizards as
active thermoregulators if Tb did not reflect precisely
microhabitat temperatures (Vrcibradic and Rocha 1998;
Kiefer et al. 2007; Maia-Carneiro and Rocha 2013b).
Conversely, we considered lizards as passive thermoreg-
ulators if Tb was quite similar to microhabitat tempera-
tures (Vrcibradic and Rocha 1998; Kiefer et al. 2007;
Maia-Carneiro and Rocha 2013b). Therefore, the greater
the absolute values of ΔTa and ΔTs, the greater the level
of active thermoregulation regarding the respective mi-
crohabitat temperatures (Vrcibradic and Rocha 1998;
Kiefer et al. 2007; Sousa and Freire 2011; Maia-
Carneiro and Rocha 2013b).
To assess interspecific and intraspecific differences of
ΔTa and ΔTs, we made Mann-Whitney U tests. To eval-
uate associations between ΔTa and Ta and between ΔTs
and Ts, we performed Spearman’s non-parametric corre-
lations for each species. The levels of passive or active
thermoregulation were also estimated by calculating the
percentages of negative values of ΔTa and ΔTs, which
show the frequencies that body temperatures were lower
than microhabitat temperatures (Vrcibradic and Rocha
1998; Kiefer et al. 2007; Sousa and Freire 2011; Maia-
Carneiro and Rocha 2013b). Values closer to zero indi-
cate little level of behavioral thermoregulation and high
values suggest active thermoregulation. Suitable interpre-
tations of estimates of behavioral thermoregulation
through ΔT and percentages of negative values rely on
the knowledge of body temperatures and which are the
main thermal sources for thermoregulation and on the
evaluation of differences between microhabitat tempera-
tures. Data were presented for each species as number of
observations (n) and arithmetic means ± 1 standard devi-
ation (SD).
Results
Temporal niche dimensions
The daily activity cycles of T. hispidus (n = 104) and
T. semitaeniatus (n = 143) extended along the whole day-
light period and had a bimodal pattern (Fig. 1). The first
active T. hispidus were sighted near 05:00 and their num-
ber increased until achieve the first peak between 12:00
and 14:00. Between 14:00 and 15:00 the number of indi-
viduals declined, and from 15:00 to 16:00 their movement
rate increased again and reached the second peak. From
16:00, the number of individuals tended to decrease and
the activity ended around 19:00 (Fig. 1a). Tropidurus
semitaeniatus started its activity near 06:00, achieving
the first peak between 10:00 and 12:00. From 12:00 to
14:00, the number of active individuals declined, and an-
other peak was reached between 14:00 and 17:00.
Tropidurus semitaeniatus ended their daily activity
around 19:00 (Fig. 1b). The decrease in the activity of
both species supposedly occurred due to high environ-
mental temperatures around midday. However, the micro-
habitat temperatures of T. semitaeniatus tended to be
higher during its second peak of activity than when it
was less active, the period that coincided with the first
peak of activity of T. hispidus, and the second peak of
activity of T. semitaeniatus included periods of decreased
movement of T. hispidus, suggesting that competitive in-
t e r f er e n ce m a y h a v e i n f l u e nc e d t h e a c t i vi t y o f
T. semitaeniatus. The overlap index (Oij) revealed a tem-
poral niche overlap of 0.886 between species, whereas the
mean value of the simulated index was 0.800 (variance =
0.00239). The level of overlap of temporal niche dimen-
sions observed was greater than expected (p = 0.039). The
daily activity differed interspecifically (Kolmogorov-
Smirnov, Dmax = 0.500, p = 0.038).
Thermal niche dimensions
The Tb of T. hispidus and T. semitaeniatus averaged, respec-
tively, 34.3 ± 2.5 ºC (range: 26.6 − 37.8 ºC, n = 51; Table 1)
and 34.8 ± 2.4 ºC (range: 27.6 − 38.6 ºC, n = 143; Table 1).
The body temperatures of individuals varied along the the day,
having relatively lower values at early mornings and late af-
ternoons when individuals of both species respectively started
and ended their daily activity cycles (Fig. 2). From the

Fig. 1 Number [frequency (%) a T. hispidus
above bars] of active individuals
of a Tropidurus hispidus (n =
104) and b Tropidurus
semitaeniatus (n = 143) at each
hourly interval throughout the day
in Igatu, municipality of Andaraí,
state of Bahia, northeastern Brazil
b T. semitaeniatus
morning, the body temperatures of T. hispidus and
T. semitaeniatus increased progressively and achieved greater
values between 10:00 and 16:00, then decreased continuously
until the end of their activities (Fig. 2).
The T b did not differ between T. hispidus and
T. semitaeniatus (Mann-Whitney U test, U = 3173.5, p =
0.169). Microhabitat temperatures were higher for
T. semitaeniatus than for T. hispidus (Ta: Mann-Whitney U
test, U = 2571.0, p = 0.002; Ts: Mann-Whitney U test, U =
2271.5, p < 0.0001; Table 1). The Tb of T. hispidus was pos-
itively correlated with Ta (Spearman’s correlation, rs = 0.588,
p < 0.0001, n = 51; Table 1; Fig. 3a) and with Ts (Spearman’s
correlation, rs = 0.697, p < 0.0001, n = 51; Table 1; Fig. 3b).
The same was observed for T. semitaeniatus both regarding Ta
(Spearman’s correlation, rs = 0.635, p < 0.0001, n = 143;
Table 1; Fig. 3c) and Ts (Spearman’s correlation, rs = 0.598,
p < 0.0001, n = 143; Table 1; Fig. 3d).
For T. hispidus, the Tb was not correlated with either SVL
(Spearman’s correlation, r s = 0.207, p = 0.146, n = 51;
Table 1) or body mass (Spearman’s correlation, rs = 0.222,
p = 0.118, n = 49; Table 1). Similar results for such correla-
tions also happened in T. semitaeniatus (SVL: Spearman’s
correlation, r s = 0.019, p = 0.822, n = 143; body mass:
Spearman’s correlation, r s = 0.066, p = 0.436, n = 142;
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Table 1). Considering inviduals of both species pooled, there
were negative correlations between SVL and Ta (Spearman’s
correlation, rs = – 0.172, p = 0.017, n = 194; Fig. 4a), SVL
and Ts (Spearman’s correlation, rs = – 0.205, p = 0.004,
n = 194; Fig. 4b), body mass and Ta (Spearman’s correla-
tion, rs = –0.163, p = 0.023, n = 194; Fig. 4c), and body
mass and Ts (Spearman’s correlation, rs = – 0.203, p =
0.005, n = 194; Fig. 4d).
Behavioral thermoregulation
The Tb, Ta, and Ts differed in T. hispidus (Friedman test, χ2 =
74.970, p < 0.0001; Table 1), with Tb higher than Ta (Wilcoxon
signed rank test, Z = – 6.184, p < 0.0001; Table 1) and Ts
(Wilcoxon signed rank test, Z = – 5.438, p < 0.0001; Table 1)
and Ts higher than Ta (Wilcoxon signed rank test, Z = – 5.661,
p < 0.0001; Table 1). The Tb, Ta, and Ts also differed in
T. semitaeniatus (Friedman test, χ2 = 207.954, p < 0.0001;
Table 1), with Tb higher than Ta (Wilcoxon signed rank test, Z
= – 10.142, p < 0.0001; Table 1) and Ts (Wilcoxon signed rank
test, Z = – 3.705, p < 0.0001; Table 1) and Ts higher than Ta
(Wilcoxon signed rank test, Z = – 10.342, p < 0.0001; Table 1).
Intraspecifically, both species had greater ΔTa than ΔTs
(T. hispidus: Mann-Whitney U test, U = 1700.0, p = 0.007;
Biologia

a T. hispidus n = 51), which also occurred between ΔTs and Ts (Spearman’s

correlation, rs = – 0.354, p = 0.011, n = 51). Considering
T. semitaeniatus, ΔTa and ΔTs were negatively correlated, re-
spectively, with Ta (Spearman’s correlation, rs = – 0.628,
p < 0.0001, n = 143) and Ts (Spearman’s correlation, rs = –
0.240, p = 0.004, n = 143). Percentages of negative values of
T. hispidus were 3.9% for ΔTa and 7.8% for ΔTs, and for
T. semitaeniatus were 2.1% for ΔTa and 36.4% for ΔTs
(Table 2). Considering interspecific differences in ΔT,
T. hispidus had greater ΔTa (Mann-Whitney U test, U =
4420.5, p = 0.024, Fig. 5a) and ΔTs (Mann-Whitney U test,
U = 4327.5, p = 0.048, Fig. 5b) than T. semitaeniatus (Table 2).
Tropidurus hispidus were found predominantly in filtered
sunlight, whereas T. semitaeniatus were first sighted mainly in
microhabitats exposed to direct sunlight (Fig. 6). Between
07:00 and 11:00, T. hispidus were found mainly in full sun-
light (Fig. 6a). From 09:00, individuals of this species started
b T. semitaeniatus
to use shaded and filtered sunlight microhabitats (Fig. 6a).
During midday (12:00), there was a peak of these lizards using
shaded portions of the habitat (Fig. 6a). Tropidurus hispidus
occupied mainly filtered sunlight between 11:00 and 16:00
(Fig. 6a). T. semitaeniatus tended to use predominantly sunny
sites along the daily activity cycle (Fig. 6b). From 08:00,
individuals of this species started to use dappled sunlight,
and between 14:00 and 16:00 they frequently used microhab-
itats in shade (Fig. 6b).

Discussion

Temporal niche dimensions

Fig. 2 Body temperatures (ºC) of active individuals of a Tropidurus
hispidus (n = 51) and b Tropidurus semitaeniatus (n = 143) at each
hourly interval throughout the day in Igatu, municipality of Andaraí,
state of Bahia, northeastern Brazil
T. semitaeniatus: Mann-Whitney U test, U = 13562.0,
p < 0.0001; Table 2). For T. hispidus, ΔTa was negatively corre-
lated with Ta (Spearman’s correlation, rs = – 0.405, p = 0.003,
The daily activity cycles of T. hispidus and T. semitaeniatus
extended to as long as there was available sunlight. Overall,
due to thermal requirements for temperatures not too high
(e.g., in comparison to active foragers), sit-and-wait foragers
– as T. hispidus and T. semitaeniatus − tend to have longer
daily activity cycles because may be active during hours of
low environmental temperatures such as early mornings and
late afternoons (Bergallo and Rocha 1993; Hatano et al. 2001;

Table 1 Mean ± standard deviation (range and number of observations Tropidurus semitaeniatus sampled throughout the day in Igatu, munici-
within parentheses) of body, air, and substrate temperatures (all in ºC), pality of Andaraí, state of Bahia, northeastern Brazil
snout-vent length (mm), and body mass (g) of Tropidurus hispidus and

Variable Tropidurus hispidus Tropidurus semitaeniatus

Body temperature 34.3 ± 2.5 (26.6 − 37.8; n = 51) 34.8 ± 2.4 (27.6 − 38.6; n = 143)
Air temperature 30.1 ± 2.7 (24.4 − 36.6; n = 51) 31.4 ± 3.2 (23.4 − 38.0; n = 143)
Substrate temperature 31.6 ± 3.2 (26.0 − 43.2; n = 51) 33.9 ± 3.8 (25.0 − 43.6; n = 143)
Snout-vent length 91.2 ± 19.7 (46.4 − 124.9; n = 51) 59.1 ± 7.0 (39.1 − 75.7; n = 143)
Body mass 29.3 ± 18.9 (2.8 − 76.5; n = 49) 4.9 ± 1.8 (1.5 − 9.8; n = 142)

Fig. 3 Correlations between a a T. hispidus
body temperature (ºC) of active
Tropidurus hispidus and air
temperature (ºC), b their body
temperature and substrate
temperature (ºC), c body
temperature (ºC) of active
Tropidurus semitaeniatus and air
temperature (ºC), and d their body
temperature and substrate
temperature (ºC) in Igatu,
municipality of Andaraí, state of
Bahia, northeastern Brazil
c T. semitaeniatus
Filogonio et al. 2010). Although daily activity cycles of
Tropidurus vary according to thermal conditions (Ribeiro
et al. 2008; Filogonio et al. 2010; Veláquez and González
2010; Andrade et al. 2013), species of this genus tend to have
similar activity periods along the day − most part of the daylight
(Vitt and Zani 1998; González et al. 2004; Meira et al. 2007;
Pontes et al. 2008; Ribeiro et al. 2009; Filogonio et al. 2010;
Caldas et al. 2015; see also references in Table 3). The conser-
vatism regarding temporal niche dimensions in Tropidurus prob-
ably rely on phylogenetic factors since species of the genus show
similar daily activities despite of differences of thermal condi-
tions. Influences from ecological factors are supported by con-
tiguous progressions of movement rates and microhabitat tem-
peratures along the day, with individuals increasing activity with
increasing temperatures and decreasing it as temperatures de-
crease and on the fact that during periods of unfavorable thermal
conditions occur reduction of activity (Hatano et al. 2001;
Filogonio et al. 2010; this study).
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b T. hispidus
d T. semitaeniatus
Extensive daily activity cycles also occurred in
T. hispidus elsewhere in Brazil (Vitt 1995; Vitt and
Carvalho 1995; Vitt et al. 1996; Vitt and Zani 1998; Van
Sluys et al. 2004; Pontes et al. 2008; Ribeiro and Freire
2010; Andrade et al. 2013; Caldas et al. 2015) and in
Venezuela (González et al. 2004; Veláquez and González
2010). Likewise, T. semitaeniatus typically had wide daily
activity cycles (Vitt 1995; Ribeiro and Freire 2010; Caldas
et al. 2015; Gomes et al. 2015), but it was narrower in a
Caatinga population (from 08:00 to 15:00 − Andrade et al.
2013). Nevertheless, in Igatu, both species had slightly
extended daily activities. Interestingly, in an anthropic site
in Igatu, a T. hispidus was active around 20:30, when sun-
light was no longer available. The lizard was less than 0.5
m from an incandescent lamp apparently thermoregulating
through body postures, approaching, and distancing from
the heat source (i.e., the lamp). The lamp light was attrac-
tive for different types of arthropods that the lizard
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Fig. 4 Correlations between a snout-vent length (mm) and air tempera-
ture (ºC), b snout-vent length (mm) and substrate temperature (ºC), c
body mass (g) and air temperature (ºC) and d body mass (g) and substrate
captured easily. The discrepancy between potential and
realized activity periods may rely on decisions by lizards,
which might be partially shaped by local selective regimes
(see also Maurer et al. 2019). Although phylogeny seems
to contribute to temporal niche dimensions, as suggested
also here by the level of overlap of temporal niche dimen-
sions of T. hispidus and T. semitaeniatus observed being
greater than the expected, under favorable conditions such
as food supply and adequate heat sources for thermoregu-
lation, individuals may stay active.
Tropidurus hispidus and T. semitaeniatus decreased move-
ment rates around midday, presenting bimodal daily activity cy-
cles. Tropidurus reduce activity during hours of the day to avoid
excessively high environmental temperatures, but they also show
unimodal pattern of daily activity (Van Sluys 1992; Hatano et al.
2001; Pontes et al. 2008; Ribeiro et al. 2009; Filogonio et al.
2010; Veláquez and González 2010). These differences regard-
ing temporal niche dimensions commonly relate to availability of
thermal resources (Hatano et al. 2001; Ribeiro et al. 2008;
Filogonio et al. 2010). In Igatu, T. hispidus (see also Pontes
temperature (ºC) of Tropidurus hispidus and Tropidurus semitaeniatus in
Igatu, municipality of Andaraí, state of Bahia, northeastern Brazil
et al. 2008; Veláquez and González 2010; Andrade et al. 2013)
and T. semitaeniatus (see also Andrade et al. 2013) decreased
activity during the hottest hours of the day (respectively between
14:00 and 15:00 and between 12:00 and 14:00). By doing this,
lizards avoid high detrimental temperatures (which reached
around 50 ºC on sandy soils in Igatu - personal observation)
and risks of overheating and death (Mosauer 1936). Tropidurus
hispidus and T. semitaeniatus may have showed extended daily
activity in Igatu to compensate for costs associated with use of
refuges during hours of thermal restrictions (midday inactivity),
which might limit foraging and consequently maintenance,
growth, and reproduction (Sinervo et al. 2010). However, the
microhabitat temperatures of T. semitaeniatus tended to be higher
during its second peak of activity than when it was less active,
and the decrease of movement of T. semitaeniatus was during the
first peak of activity of T. hispidus (from 12:00 to 14:00) and the
second peak of activity of T. semitaeniatus included periods of
decreased movement of T. hispidus (from 14:00 to 15:00).
Therefore, interspecific interactions with larger-sized
T. hispidus may have influenced the activity of
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Table 2 Mean values and standard deviations (SD) for the absolute percentage of negative values (%) in Tropidurus hispidus and
differences (ΔT) between body temperature and air temperature (ΔTa, Tropidurus semitaeniatus sampled throughout the day in Igatu, munici-
ºC) and for the absolute difference between body temperature and sub- pality of Andaraí, state of Bahia, northeastern Brazil
strate temperature (ΔTs, ºC), range of the absolute differences, and

ΔT/Species n Mean ± SD Range % of negative values

ΔTa
Tropidurus hispidus 51 4.3 ± 2.3 0.2 − 10.2 3.9
Tropidurus semitaeniatus 143 3.5 ± 2.2 0 − 12.0 2.1
ΔTs
Tropidurus hispidus 51 3.0 ± 2.2 0 − 9.0 7.8
Tropidurus semitaeniatus 143 2.3 ± 1.9 0 − 9.4 36.4

T. semitaeniatus (see also Maia-Carneiro and Rocha 2015 and
Maia-Carneiro et al. 2017b for body size comparisons). This
hypothesis is supported by observations of agonistic interactions
among Tropidurus (Kohlsdorf et al. 2006; Passos et al. 2016),
including T. hispidus and T. semitaeniatus in Igatu. Differences
in the hours of peak and of reduction of the activities and in the
extensions of the activities seemed responsible for the statistical
difference between daily activity cycles.

Thermal niche dimensions

The Tb of T. hispidus and T. semitaeniatus varied throughout

Fig. 5 Differences of a ΔTa (ºC) and of b ΔTs (ºC) between Tropidurus
hispidus and Tropidurus semitaeniatus in Igatu, municipality of Andaraí,
state of Bahia, northeastern Brazil. Both ΔTa and ΔTs were greater in
T. hispidus than in T. semitaeniatus
the day and did not differ between the species. Comparisons of
Tb among Tropidurus revealed that they varied between 30 ºC
and 37.6 ºC and seemed affected by variations of thermal condi-
tions within and between localities (see Table 3 to access data of
Tb, Ta, and Ts of Tropidurus species as well as their respective
sources). Tropidurus hispidus had lower and higher mean body
temperatures in other localities comparing to Igatu (Table 3) and
the Tb of T. semitaeniatus in Igatu were comparatively lower
than in other populations (Vitt 1995; Ribeiro and Freire 2010;
Pelegrin et al. 2017). Similar to the effects of thermal environ-
ments on hourly activity rates of T. hispidus and T. semitaeniatus
in Igatu, daily variations of microhabitat temperatures also affect-
ed the Tb of these lizards. This was indicated by the contiguous
daily progressions of body and microhabitat temperatures, with
individuals achieving comparatively lower body temperatures in
the coldest hours of the day (early mornings and late afternoons)
and greater body temperatures when it was warmer.
The Tb of T. hispidus and T. semitaeniatus varied widely in
Igatu, which supposedly happened because they had broad
daily activity cycles, with individuals remaining active in pe-
riods of relatively low environmental temperatures, which did
not allow to achieve high body temperatures. Individuals
caught contributed to greater variations of Tb in Igatu, whereas
in other localities lizards were captured throughout the day in
intervals of comparatively lower thermal differences (see Vitt
1995; Vitt and Carvalho 1995; Vitt et al. 1996; Colli and Paiva
1997; Velásquez and González 2010). Nevertheless,
T. hispidus in the Brazilian state of Minas Gerais had wider
Tb variation than in Igatu and other localities despite of the
Biologia
Fig. 6 Number of active a a T. hispidus
Tropidurus hispidus (n = 44) and
b Tropidurus semitaeniatus (n =
121) individuals using different
thermal microhabitats (shade,
filtered sunlight, and full sun) at
each hourly interval throughout
the day in Igatu, municipality of
Andaraí, state of Bahia,
northeastern Brazil
b T. semitaeniatus
shorter time of daily activity (Van Sluys et al. 2004). Perhaps
lower environmental temperatures in Minas Gerais than in
Igatu and other localities restricted opportunities for thermo-
regulation by T. hispidus. Indeed, the Tb of these lizards
tended to vary more in populations exposed to more variable
microhabitat temperatures and less in sites where temperatures
were relatively more constant (Table 3). Therefore, thermal
conditions and extensions of daily activities (i.e., temporal
niche dimensions) relate to variations of lizards’ body
temperatures.
Tropidurus semitaeniatus showed warmer Ta and Ts than
T. hispidus, which may have different causes. Tropidurus
semitaeniatus may need higher microhabitat temperatures
compared to T. hispidus. The start of the activity of
T. semitaeniatus around an hour later in comparison to
T. hispidus might have occurred because of interspecific dif-
ferences with regard to thermal requirements. In this case, low
microhabitat temperatures in early mornings impeded
T. semitaeniatus of heating up to adequate levels, which re-
stricted their activity. Otherwise, as T. semitaeniatus lives in
rock walls in open habitats, temperatures of microhabitats
used by individuals are probably higher than those used by
T. hispidus generalist lizards, which does not imply that
T. semitaeniatus needs higher microhabitat temperatures.
However, overall, T. hispidus tended to use lower temperature
microhabitats than T. semitaeniatus (see Table 3).
Considering the importance of microhabitats as thermal re-
sources, T. hispidus may have excluded T. semitaeniatus from
rock sites with more suitable and mild temperatures, exposing
the later to inapropriate high temperatures. In Igatu, we ob-
served agonistic interactions with T. hispidus displacing
T. semitaeniatus from sites initially occupied (see also
Kohlsdorf et al. 2006; Passos et al. 2016), which concur to
the above hypothesis. Additional investigations are needed to
evaluate the causes of higher microhabitat temperatures of
T. semitaeniatus than of T. hispidus.
The use of warmer microhabitats in T. semitaeniatus than in
T. hispidus also may have happened because of differential
properties of thermal inertia of each species, with larger bodies
having greater capacity of heat conservation (Garrick 2008;
 Biologia

Table 3 Means, standard deviations (SD), and ranges of body temperature (Tb; ºC), air temperature (Ta; ºC), and substrate temperature (Ts; ºC), locality
sampled, and source of information from studies with species of Tropidurus

Species Tb ± SD (range) Ta ± SD (range) Ts ± SD (range) Locality Source

T. etheridgei 35.8 ± 2.5 (28.0 − 43.7) 31.3 ± 2.6 (26.6 − 33.8) 31.7 ± 2.9 (25.5 − 38.4) Argentina Cruz et al. (1998)
T. helenae 34.67 ± 1.97 Caatinga Pelegrin et al. (2017)
T. hispidus 35.9 ± 0.13 (30.6 − 39.6) 31.8 ± 0.14 (26.8 − 36.4) 34.9 ± 0.15 (30.6 − 39.5) Caatinga Vitt (1995)
T. hispidus 34.4 ± 0.28 28.7 ± 0.16 30.8 ± 0.27 Amazon savanna Vitt and Carvalho (1995)
T. hispidus 34.1 (25.0 − 39.0) 28.9 ± 0.25 (23.2 − 35.2) 31.9 ± 0.36 (24.0 − 44.6) Amazon rainforest Vitt et al. (1996)
T. hispidus 35.98 ± 1.55 33.27 ± 1.85 34.67 ± 3.02 Amazon savanna Colli and Paiva (1997)
T. hispidus 32.2 ± 3.4 (23.8 − 36.4) 24.5 ± 2.0 (21.0 − 29.8) Rocky meadows Van Sluys et al. (2004)
T. hispidus 33.1 ± 2.2 Caatinga Ribeiro and Freire (2010)
T. hispidus 34.1 ± 2.5 Caatinga Ribeiro and Freire (2010)
T. hispidus 36.1 ± 1.07 (33.5 − 37.7) 30.63 31.05 Grove Velásquez and González (2010)
T. hispidus 35.27 ± 1.6 (32.6 − 37.8) 31.21 32.45 Grove Velásquez and González (2010)
T. hispidus 36.67 ± 2.36 Caatinga Pelegrin et al. (2017)
T. hispidus 34.23 ± 2.67 30.37 ± 2.59 31.98 ± 3.47 Caatinga Albuquerque et al. (2018)
T. hispidus 34.85 ± 2.75 30.42 ± 2.21 33.59 ± 3.92 Restinga Albuquerque et al. (2018)
T. hispidus 34.18 ± 2.62 29.56 ± 1.21 32.22 ± 2.86 Atlantic Forest Albuquerque et al. (2018)
T. hygomi 35.44 ± 2.57 Caatinga Kohlsdorf and Navas (2006)
T. hygomi 32.9 ± 2.0 (26.9 − 36.4) 31.4 ± 2.0 (26.3 − 35.3) 30.7 ± 2.0 (25.4 − 36.6) Restinga Vargens et al. (2008)
T. insulanus 34.52 ± 2.40 28.14 ± 2.53 30.01 ± 3.78 Cerrado Colli apud Kohlsdorf and
Navas (2006)
T. itambere 34.1 ± 2.02 (27.8 − 38.4) 26.3 ± 2.68 (19.0 − 32.0) Rock outcrop Van Sluys (1992)
T. itambere 34.06 ± 4.0 27.02 ± 2.67 30.13 ± 3.5 Amazon savanna Colli and Paiva (1997)
T. itambere 33.07 ± 2.84 (22.0 − 38.0) 25.72 ± 3.34 (14.7 − 34.8) 27.42 ± 4.21 (17.5 − 38.8) Cerrado Faria and Araujo (2004)
T. itambere 30.9 ± 2.73 Cerrado Kohlsdorf and Navas (2006)
T. montanus 31.7 ± 3.5 (25.8 − 38.2) 24.4 ± 3.1 (21.4 − 35.0) Rocky meadows Van Sluys et al. (2004)
T. montanus 34.7 Minas Gerais Kiefer et al. (2005)
T. oreadicus 35.8 ± 1.5 (32.0 38.1) Amazon Canga Rocha and Bergallo (1990)
T. oreadicus 32.9 ± 0.42 28.6 ± 0.29 30.4 ± 0.45 Rainforest Vitt (1993)
T. oreadicus 34.04 ± 3.47 28.68 ± 3.45 30.4 ± 3.67 Amazon savanna Colli and Paiva (1997)
T. oreadicus 33.48 ± 2.08 (22.0 − 38.0) 26.37 ± 2.81 (17.6 − 34.3) 28.03 ± 3.54 (19.3 − 39.4) Cerrado Faria and Araujo (2004)
T. psamonastes 37.55 ± 1.95 Caatinga Kohlsdorf and Navas (2006)
T. semitaeniatus 37.1 ± 0.15 (29.0 − 40.6) 32.1 ± 0.15 (20.7 − 36.8) 35.8 ± 0.15 (28.9 − 39.6) Caatinga Vitt (1995)
T. semitaeniatus 35.8 ± 1.7 Caatinga Ribeiro and Freire (2010)
T. semitaeniatus 34.4 ± 2.1 Caatinga Ribeiro and Freire (2010)
T. semitaeniatus 34.93 ± 1.87 Caatinga Pelegrin et al. (2017)
T. sp.1 35.7 ± 0.03 29.9 ± 0.21 31.5 ± 0.65 Rainforest Vitt (1993)
T. sp.2 36.2 ± 0.28 29.9 ± 0.24 Rainforest Vitt (1993)
T. sp.3 35.7 ± 0.5 25.9 ± 0.64 30.2 Rainforest Vitt (1993)
T. spinulosus 34.22 ± 1.83 (29.2 − 37.8) 29.33 ± 2.9 (24.3 − 34.5) 29.36 ± 3.54 (22.1 − 35.5) Argentina Cruz (1998)
T. spinulosus 30.3 (20 − 37.8) 31.4 27.7 Argentina Martori and Aun (1994)
T. torquatus 35.6 ± 1.9 Restinga Bergallo and Rocha (1993)
T. torquatus 35.3 ± 2.6 (25.6 − 40.2) 29.0 ± 3.3 − 30.3 ± 4.4** Restinga Teixeira-Filho et al. (1996)
T. torquatus 34.0 ± 0.4 29.3 ± 0.4 Open sandy habitat Gandolfi and Rocha (1998)
T. torquatus 34.8 ± 2.4 (28.6 − 39.0) Restinga Hatano et al. (2001)
T. torquatus 34.0 ± 3.7 (23.8 − 38.0) Abrolhos Rocha et al. (2002)
T. torquatus* 30.8 ± 4.5 − 36.2 ± 1.5 25.4 ± 3.1 − 32.4 ± 3.2 26.2 ± 3.2 − 35.1 ± 3.9 Restinga Kiefer et al. (2005)
T. torquatus 33.27 ± 2.15 Cerrado Kohlsdorf and Navas (2006)
T. torquatus 32.4 ± 2.7 28.3 ± 3.7 30.2 ± 4.5 Rock outcrop Ribeiro et al. (2008)
T. torquatus 30.4 ± 3.0 26.4 ± 3.1 28.5 ± 4.1 Rock outcrop Ribeiro et al. (2008)

*Ranges of means and standard deviations from ten coastal populations. ** Range

Maia-Carneiro and Rocha 2013a). Such hypothesis was
strengthened by the correlations between body size (SVL and
body mass) and microhabitat temperatures (air and substrate),
with smaller T. semitaeniatus tending to occupy warmer micro-
habitats than larger T. hispidus. Large-sized lizards have
surface/volume ratios comparatively lower in comparison to
smaller ones, resulting in increased thermal inertia − slower
rates of heating up and cooling down, and lower susceptibility
to convective cooling (Porter and Gates 1969; Carothers et al.
1997; Garrick 2008; Maia-Carneiro and Rocha 2013b). Greater
thermal inertia and a consequent low heating rate would favor
large lizards with respect to the use of open environments,
Biologia
whereas small lizards could not be exposed to high tempera-
tures as long as large lizards (Porter and Gates 1969; Carothers
et al. 1997). However, in Igatu, the relative greater capacity of
heat retention by larger T. hispidus may have resulted in high
overheating risks. To prevent such risks, individuals may have
used colder microhabitats comparing to T. semitaeniatus. As
compared to smaller sizes, the greater thermal inertia due to
larger sizes allow to maintain more easily the body tempera-
tures and thus being exposed for longer periods to low environ-
mental temperatures.
The Tb of both T. hispidus and T. semitaeniatus were pos-
itively correlated to Ta and Ts, indicating that microhabitat and
body temperatures varied side-by-side along daily activities
and that individuals used these thermal resources for suitable
adjustment of body temperatures. Such associations are re-
ported for other species of the genus as well as for
T. hispidus and T. semitaeniatus (see references in Table 3).
Furthermore, for either T. hispidus and T. semitaeniatus and
other species of Tropidurus (e.g., Rocha and Bergallo 1990;
Teixeira-Filho et al. 1996; Vitt et al. 1996; Ribeiro et al. 2008),
besides air and substrate temperatures, the heat of direct solar
radiation (as indicated by the use of different sunlight levels
along the day) is relevant for regulation of body temperatures.
Behavioral thermoregulation
Tropidurus hispidus and T. semitaeniatus had higher Tb than
Ta and Ts, and despite interspecific differences regarding ther-
mal microhabitats, the Tb did not differ. The negative correla-
tions between ΔT and microhabitat temperatures suggested
that the lizards had smaller variations of body temperatures
comparing to microhabitat temperatures; the more the micro-
habitat temperatures increased the more they approximated to
ranges of body temperatures maintained by the individuals.
Tropidurus hispidus and T. semitaeniatus acquired heat also
through exposure to direct sunlight to increase body tempera-
tures, commonly above microhabitat temperatures. Together,
these data suggested that individuals did thermoregulate to
maintain body temperatures within suitable ranges along daily
activities. As other examples, T. semitaeniatus had higher
body temperatures, decreased the use of shade, and increased
the use of sunlight, during the season with colder microhabitat
temperatures; likewise, in the warmer season, T. hispidus used
mainly microhabitats with filtered sunlight and shade than
cloudy light and full sun, whereas in the colder season the
individuals remained similarly under different levels of expo-
sure to sunlight (Ribeiro and Freire 2010). Therefore, both
T. hispidus and T. semitaeniatus actively thermoregulate.
Tropidurus hispidus and T. semitaeniatus had Tb closer to Ts
than to Ta, warmer Ts than Ta, greater ΔTa than ΔTs, and greater
percentages of negative values for ΔTs than for ΔTa, which sug-
gested that substrates were more important heat sources than air
to increase their body temperatures. Supposedly, the air could not
provide enough heat to warm body temperatures up to suitable
levels. In a comparison among ten coastal populations of
Tropidurus torquatus Wied, 1820, lizards showed greater levels
of active thermoregulation in relation to substrate temperatures,
whereas high levels of passive thermoregulation were the most
common tendency regarding air temperatures (Kiefer et al.
2007). Since mean body temperatures of Tropidurus are often
higher than mean microhabitat temperatures and their mean sub-
strate temperatures are frequently greater than mean air temper-
atures (see Table 3), air temperatures seem to have minor impor-
tance for heat gain and these lizards actively use mainly warmer
substrates to raise up body temperatures (besides sunlight).
Nevertheless, the level of active or passive thermoregulation re-
garding microhabitat temperatures vary due to differences in the
relative importance of each thermal environment in a given oc-
casion (Kiefer et al. 2007; Maia-Carneiro and Rocha 2013b).
Considering that Tb did not differ between species and the
trend of the greater the microhabitat temperatures the lower the
ΔT, the greater values of ΔTa and ΔTs in T. hispidus comparing
to T. semitaeniatus reflected the lower values of Ta and Ts of
T. hispidus. As discussed above, these differences may relate to
thermoregulation, microhabitat use, agonistic interactions and/
or body sizes. Interspecific differences of ΔTa and ΔTs also
might indicate that T. hispidus showed more active thermoreg-
ulation than T. semitaeniatus (Vrcibradic and Rocha 1998;
Kiefer et al. 2007; Sousa and Freire 2011; Maia-Carneiro and
Rocha 2013b). Nevertheless, the greater percentages of nega-
tive values of T. semitaeniatus suggested a more active thermo-
regulation in this species. Overall, evaluation of data obtained
here together with those available in the literature suggests that
Tropidurus lizards thermoregulate actively.
As heliothermic animals, sun exposure is relevant for body
temperature regulation of T. hispidus and T. semitaeniatus,
however, the level of exposition varied between species.
Such as shown here, T. hispidus had lower microhabitat tem-
peratures than T. semitaeniatus, which seems to relate to the
tendency of T. hispidus to use mainly microhabitats with fil-
tered sunlight and of T. semitaeniatus to use mostly spots of
full sunlight. At early mornings, we sighted T. hispidus and
T. semitaeniatus mainly in microhabitats exposed to direct
sunlight to heat up, increasing body temperatures.
Individuals of these species started to use filtered sunlight
and shaded microhabitats according to the increase of envi-
ronmental temperatures. Tropidurus hispidus was mainly in
filtered sunlight microhabitats between 11:00 and 16:00, and
T. semitaeniatus tended to occupy full sunlight patches the
whole activity cycle. Tropidurus hispidus of other localities
also tended to use microhabitats with filtered sunlight or shade
(Vitt et al. 1996; Ribeiro and Freire 2010; Gomes et al. 2015),
nevertheless, in the Brazilian state of Roraima, they used
mainly microhabitats exposed to the sun (Vitt and Carvalho
1995). However, it was not specified if the category “Sun”
included full and filtered sunlight microhabitats or only one of

them (Vitt and Carvalho 1995), which restricted comparisons.
With respect to T. semitaeniatus, in other populations it was
found predominantly in microhabitats with filtered sunlight
and full sun (Ribeiro and Freire 2010; Caldas et al. 2015;
Gomes et al. 2015).
To thermoregulate, Tropidurus hispidus and T. semitaeniatus
raised up or brought down their bodies and increased or de-
creased levels of body flattening over substrates and shuttled
across microhabitats with different temperatures and levels of
sunlight. Overall, lizards regulate body temperatures through be-
havior, modifying body postures and shuttling between thermal
environments (more or less windy; warm; cold; shade; sun)
(Rocha and Bergallo 1990; Vitt and Carvalho 1995; Teixeira-
Filho et al. 1996; Vitt et al. 1996; Cruz et al. 1998; Gandolfi and
Rocha 1998; Faria and Araujo 2004; Kiefer et al. 2007; Meira
et al. 2007; Rocha et al. 2009; Ribeiro and Freire 2010; Maia-
Carneiro and Rocha 2013b; Maia-Carneiro et al. 2012, 2017a).
At early mornings and late afternoons − mainly, it was common
to see T. hispidus and T. semitaeniatus flattened on rock surfaces
using the heat accumulated in the substrate to increase body
temperatures.
Concluding remarks
The life of congeners in syntopy is favored if each species
alternate inactivity periods and activity peaks and use micro-
habitats with different temperatures. In this case, intraspecific
particularities with respect to temporal and thermal niche di-
mensions would have conspicuous relevance for niche segre-
gation. Separation regarding activity times and use of thermal
microhabitats might guarantee better access to resources, such
as those needed for thermoregulation – e.g., microhabitat tem-
peratures, shade, and sunlight. Interspecific differences re-
garding body sizes of syntopic congeneric species are also
beneficial if they relate with differential use of thermal re-
sources. Levels of thermoregulation vary depending of intrin-
sic (e.g., thermal needs) and extrinsic (e.g., microhabitat tem-
peratures; opponents) factors, and behaviors are performed for
suitable regulation of body temperatures. As differences be-
tween congeneric species may be product of independent evo-
lutionary histories and not of their coexistence, future studies
might consider to investigate their ecological niches both in
syntopy and allopatry to evaluate for possible dimensional
changes. Nevertheless, we already know that the syntopy of
congeneric species is favored by interspecific divergences of
ecological niche dimensions.
Acknowledgements We thank Timothy Moulton for language revision.
We also thank the Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq), which provided grants for CFDR (processes nº
424473/2016-0 and 302974/2015-6), the Fundação Carlos Chagas Filho
de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) ,which
supported CFDR through Programa Cientistas do Nosso Estado (process
Biologia
nº E-26/202.920/2015 and E-26/202.803/2018) and the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the
FAPERJ for PhD grants for TMC.
Compliance with ethical standards
Authorization for scientific activities (number 34333-1) was given by the
Ministério do Meio Ambiente - MMA, Instituto Chico Mendes de
Conservação da Biodiversidade − ICMBio, Sistema de Autorização e
Informação em Biodiversidade – SISBIO.
Conflict of interest The authors state that there is no conflict of interest.
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