Habitat use by five species of sympatric pitvipers
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Herpetology Notes, volume 13: 951-960 (2020) (published online on 26 November 2020)
Habitat use by five species of sympatric pitvipers
(Bothrops, Crotalus) in a Brazilian savannah
Bruno Ferreto Fiorillo1,2,*, Alexandro M. Tozetti3, and Marcio Martins1
Abstract. Detailed information on habitat use allows for a better understanding of a species’ behaviour and spatial ecology
and provides basic information that may help with conservation assessments and in defining conservation actions. Here we
present data on habitat use and short-term movements of five sympatric pitvipers inhabiting a protected area of savannah in
southeastern Brazil. We conducted monthly surveys for two years, using road driving, visual searches, occasional encounters,
and relocations of animals equipped with PIT-tags, thread-bobbins, and radio-transmitters. The frequency of individuals of
Bothrops alternatus and B. itapetiningae was significantly higher than expected in campo sujo, B. moojeni was significantly
more frequent in gallery forest and wet field, B. pauloensis was significantly more frequent in campo cerrado, and Crotalus
durissus was significantly more frequent than expected in cerradão. All species are primarily terrestrial and commonly use
burrows in the ground as shelter. Most of the few recaptures of PIT-tagged individuals occurred within short distances from the
site of first capture, indicating sedentary habits for all species. Our results add to the information available about habitat use in
neotropical pitvipers and could contribute to the conservation of the studied species.
Keywords. Microhabitat, movement, PIT-tag, radio-tracking, thread bobbins, Cerrado
Introduction more accurate assessments of the conservation status of
species and more effective conservation actions (Maritz
The study of snake habitat use leads to a better
and Alexander, 2012).
understanding of their behavioural (e.g., feeding,
Finding snakes in the field, through visual searches
mating, seasonal, diel activity) and spatial ecology (e.g.,
or accidental encounters, provides useful information
home range, habitat use, movement patterns; Oliveira
on how species use their habitat, both at the scale of
and Martins, 2002; Tozetti and Martins, 2008; Sasa
vegetation types and of microhabitats (i.e., the substrates
et al., 2009; Maritz and Alexander, 2012). Although
used; Martins and Oliveira, 1998). Furthermore, mark-
essential to an understanding of snake ecology and
recapture studies and other tracking methods like thread
their role in ecosystems, such basic natural history
bobbins and radio-tracking have shown to be useful
information is still lacking for many species (e.g.,
when used in combination (Tozetti and Martins, 2007)
Sazima and Haddad, 1992; Sawaya et al., 2008; Barbo
and provide additional information on habitat use,
et al., 2011). Furthermore, this information can be
including movement patterns (Nogueira et al., 2003;
particularly helpful for conservation issues, allowing
Tozetti et al., 2009).
The Cerrado is the second largest neotropical
ecoregion, extending through approximately 2 million
square kilometres mostly in central Brazil (Strassburg et
al., 2017; Colli et al., 2020). It comprises mostly open
savannahs, but with a high environmental heterogeneity
1
Departamento de Ecologia, Instituto de Biociências, that includes at least six common vegetation types:
Universidade de São Paulo, 05508-090 São Paulo, SP, Brazil. campo sujo (grassy scrubland), campo cerrado (grassy
2
Programa de Pós-Graduação em Ecologia Aplicada, scrubland with scattered trees), cerrado sensu stricto
Universidade de São Paulo, Escola Superior de Agricultura
(dense savannah), cerradão (cerrado woodland), gallery
Luiz de Queiroz, 13418-900 Piracicaba, SP, Brazil.
3
Laboratório de Ecologia de Vertebrados Terrestres,
forest, and wet field (or wet grasslands and swamps;
Universidade do Vale do Rio dos Sinos, 93022-000 São Eiten, 1972; Furley and Ratter, 1998; Ribeiro and
Leopoldo, RS, Brazil. Walter, 1998). This environmental heterogeneity may
*
Corresponding author. E-mail: ferreto_74@hotmail.com influence the local distribution of snakes (e.g., Sawaya
952 Bruno Ferreto Fiorillo et al.
et al., 2008; Fiorillo, 2020), particularly pitvipers of the São Paulo, Brazil) were externally attached to the dorsal
genus Bothrops (Nogueira, 2001; Valdujo et al., 2002; region at the dorsolateral region of the posterior third
Nogueira et al., 2003). of the snake’s body using three strips (four centimetres
The Cerrado of south-eastern Brazil harbours five wide) of duct tape, long enough to encircle half of its
species of pitvipers: Bothrops alternatus Duméril et al., girth, as suggested by Tozetti and Martins (2007; Fig.
1854, B. itapetiningae (Boulenger, 1907), B. moojeni 3A). Radio-transmitters (Axabixo® radio-telemetry
Hoge, 1966, B. pauloensis Amaral, 1925, and Crotalus with digital coding, São Paulo, Brazil) were attached
durissus Linnaeus, 1758 (Fig. 1; Araújo et al., 2010; in the same way as thread bobbins, with the antenna
Fiorillo, 2020). Three of these species are endemic to oriented backwards (see additional details in Tozetti
the Cerrado ecoregion (B. itapetiningae, B. moojeni, and Martins, 2007; Fig. 3B). Each snake received either
and B. pauloensis; Nogueira et al., 2019). Some of the a thread bobbing or a radio-transmitter, never both.
Cerrado pitvipers are known to be strongly associated Snakes that were to be fitted with both thread-bobbins
with specific habitats (Nogueira, 2001; Valdujo et al., or radio-transmitters were captured and taken to a
2002; Sawaya et al., 2008; Fiorillo, 2020), such as B. field laboratory, where they were measured, sexed and
moojeni, which is strongly associated with wet habitats weighed, before a device was attached. These individuals
(wet fields and gallery forests; Nogueira et al., 2003). were then released at the site of their capture, 1−3 days
Herein we provide information about habitat use and after capture. The use of external attachment methods
short-term movements of five species of pitvipers in a reduces stress inflicted to the animal and risk of death,
protected area of savannah (the Brazilian Cerrado) in preventing undesirable physiological consequences
south-eastern Brazil. (e.g., reabsorption of ovarian follicles) that could result
from surgical intervention (including anaesthesia;
Materials and Methods Graves and Duvall, 1993; Rudolph et al., 1998).
Our study was carried out in the Santa Bárbara Each animal bearing a radio-transmitter or a thread-
Ecological Station (SBES), located in Águas de Santa bobbin was relocated at least once a day, with the
Bárbara Municipality, São Paulo State, south-eastern exception of animals whose radio signal was lost (n =
Brazil (22.8159°S, 49.2204°W; elevation 600–680 m), 2 of radio-tracked animals; 40%). Locations include
which contains all six common Cerrado vegetation the occasion when animals were released in the field,
types (Fig. 2). There are also some disturbed areas, as well as those in which the snake was not visible.
including some commercial tree plantations (Pinus and Animals equipped with thread-bobbins were located
Eucalyptus). The average temperature during the coldest by tracking the thread trail, while signals from radio-
month is 18 °C and in the warmer months it exceeds transmitters were tracked with a portable radio-receiver
22 °C. The annual rainfall is 1000–1300 mm (Melo (Axabixo®, with digital coding). Most locations
and Durigan, 2011). Furthermore, all common pitviper provided visual contact with individuals and the place in
species that occur in the Cerrado of south-eastern Brazil which the animal was observed was marked by coloured
are found in this protected area. flagging. Geographical coordinates were taken at each
Surveys were conducted monthly for ten consecutive location. Individuals that were hidden in burrows in
days, corresponding to 240 days of fieldwork from the ground were photographed when possible (Fig.
August 2016 – July 2018. Data were gathered during 4A) or observed through an endoscopic inspection, 2-
searches conducted by car along roads and firebreaks m optic fibre cable attached to a cell phone, allowing
(road driving), visual searches in different vegetation the animals to be seen in their shelter (Fig. 4B). The
types, occasional encounters, and relocations of animals distance moved from the initial site (DMIS; Tozetti
captured and released after being equipped with three et al., 2009) of animals bearing radio-transmitters or
types of devices that allowed us to identify recaptures thread-bobbins were measured in a straight line using
(PIT-tags) and track the movements of individuals the software QGIS (QGIS Development Team, 2019).
(thread bobbins and radio-transmitters). The minimum distance moved per day (MDMD) was
PIT-tags (Trovan® ID 100 Implantable Transponder, calculated by dividing DMIS by the number of days
Alltags, Botucatu, São Paulo, Brazil) were implanted the snake was tracked. This latter number represents
by making diminutive cuts on the ventrolateral region the period from the release of the snake with a thread-
of the snakes through which the tags were inserted. bobbing or a transmitter until the thread-bobbing ended
Thread-bobbins (~170 m long; Hiltex® Ltda., Itatiba, or was detached or the transmitter was detached. As
Habitat use by five species of sympatric pitvipers in a Brazilian savannah 953 Figure 1. Individuals of the five species of pitvipers found at the Santa Bárbara Ecological Station. All pictures depict individuals as they were found in the field. (A) Bothrops alternatus found in the morning on an unpaved road crossing an area of campo sujo. (B) B. itapetiningae found in the morning in an area of campo sujo. (C) B. moojeni found at night in a wet field close to a gallery forest in an area of campo cerrado. (D) B. pauloensis found at night in an area of campo sujo. (E) Crotalus durissus found on an unpaved road crossing an area of cerrado sensu stricto. (F) C. durissus found in the morning in a cerradão (note leaf litter covering the ground). in some situations, observations were done between wet field, and disturbed areas), we used a contingency different field trips, this number may be used to estimate table analysis with a chi-square test (Monte Carlo only the minimum distance moved per day. method with 5000 simulations). Adjusted residuals were To test for possible associations of pitviper species used to visually describe the results of this test. These with different vegetation types (campo sujo, campo analyses were made with XLStat (Addinsoft, 2019). cerrado, cerrado sensu stricto, cerradão, gallery forest, Considering all methods together, sampling effort was
954 Bruno Ferreto Fiorillo et al.
Figure 2. Natural vegetation types of Santa Bárbara Ecological Station. (A) Campo sujo (grassy scrubland). (B) Campo cerrado
(grassy scrubland with scattered trees). (C) Cerrado sensu stricto (dense savanna). (D) Cerradão (cerrado woodland). (E) Gallery
forest. (F) Wet field.
relatively homogeneous in different vegetation types Results
(e.g., although visual search was more frequent in
During our two-year survey we found a total of 124
more open vegetation, most of the roads used in road
individuals of five species of pitvipers. Among these,
sampling cross more dense vegetation types), especially
a combined 77% were Bothrops pauloensis (n = 56) or
considering the extent of the cover of each vegetation
Crotalus durissus (n = 40; Table 1). Using data obtained
type in the study area (gallery forests, for instance, cover
through all sampling methods, we found variation
only a small area and was likewise sampled less often).
in the apparent abundances (number of captures)
of species in different vegetation types (Table 1).
Habitat use by five species of sympatric pitvipers in a Brazilian savannah 955
Table 1. Pitviper records for each vegetation type at the Santa Bárbara Ecological Station and surroundings.
Table 1. Pitviper records for each vegetation type at the Santa Bárbara Ecological Station and surroundings.
Species Campo Campo Cerrado Cerradão Gallery Wet field Disturbed TOTAL
sujo cerrado sensu stricto forest areas
Bothrops alternatus 6 1 0 0 0 0 2 9
Bothrops itapetiningae 3 1 0 0 0 0 0 4
Bothrops moojeni 0 1 1 1 7 2 3 15
Bothrops pauloensis 10 36 4 1 0 1 4 56
Crotalus durissus 2 6 5 12 1 1 13 40
Considering all vegetation types (Fig. 2), B. alternatus frequent in cerradão (P = 0.003), gallery forest (P =
and B. itapetiningae were found only in open savannahs 0.008), and disturbed areas (P = 0.008), and C. durissus
(campo sujo and campo cerrado), B. pauloensis mainly was significantly more frequent than expected in
in open savannahs (campo sujo and campo cerrado), but cerradão (P = 0.0001) and disturbed areas (P = 0.005),
also in cerrado sensu stricto, B. moojeni mostly in wet and less frequent in campo sujo (P = 0.01) and campo
areas (gallery forests and wet fields), and C. durissus cerrado (P = 0.001) (Fig. 5). Finally, all species except
in all natural vegetation types plus disturbed areas B. itapetiningae were found in disturbed areas (Table 1),
(Table 1). The contingency table analysis using data in especially C. durissus (13 out of 40 individuals).
Table 1 showed a significant association between species Of the 75 individuals equipped with PIT-tags (B.
and vegetation types (χ2 = 36.4, df = 24, P < 0.0001; alternatus, n = 4; B. moojeni, n = 11; B. pauloensis, n =
Fig. 5). The frequency of individuals of B. alternatus and 33; C. durissus, n = 27), only four were recaptured. One
B. itapetiningae was significantly higher than expected PIT-tagged individual of B. moojeni was recaptured
in campo sujo (P = 0.001 and P = 0.015, respectively), three times in the same place (a gallery forest adjacent to
B. moojeni was significantly more frequent in gallery an artificial pond near the SBES headquarters) between
forest (P = 0.0001) and less frequent in campo cerrado March 2016 and February 2018, with less than 20 m
(P = 0.01), B. pauloensis was significantly more between release and last recapture. We also recaptured
frequent in campo cerrado (P = 0.0001) and less three individuals of B. pauloensis. One of them was
Figure 3. Detail of individuals of Crotalus durissus (A) and Bothrops pauloensis (B) with a thread bobbin and a radio-transmitter,
respectively. Both tracking devices are attached to the dorsolateral region with transparent silver duct tape.956 Bruno Ferreto Fiorillo et al. Figure 4. An individual of Bothrops pauloensis in a shallow termite mound (A) and an individual of B. alternatus observed through an endoscopic camera in a burrow in the ground. Note that the individual in (A) has a radio-transmitter attached and that the duct tape is beginning to detach from the skin of the snake. recaptured about 400 m from the site of capture, 34 days campo cerrado and recaptured about 100 m away from later, in campo sujo. Another individual first captured in site of capture 107 days later. an area of campo cerrado was recaptured 37 days later, Of the 21 individuals equipped with thread-bobbins about 15 m from the first site, after the area had been (B. alternatus, n = 1; B. moojeni, n = 3; C. durissus, completely burned. A third individual was captured in n = 12) and radio-transmitters (B. alternatus, n = 2; B. Figure 5. Adjusted residuals of a contingency table analysis used to test for associations between pit viper species and vegetation types at the Santa Bárbara Ecological Station. Red bars indicate significant positive or negative associations while grey bars indicate no association.
Habitat use by five species of sympatric pitvipers in a Brazilian savannah 957
Table 2. Individuals monitored with thread bobbins and radio-transmitters. Locations include the occasion when animals where
released in the field, as well as those in which the snake was not visible. CC: campo cerrado; CD: cerradão; CS: campo sujo;
DMIS: distance in a straight line from the capture site; F: female; GF: gallery forest; M: male; MDMD: minimum distance moved
Tableper
2. Individuals Pinus sp.
day; PF:monitored withplantation; RT:
thread bobbins andRadio-tracking; SS: cerrado
radio-transmitters. Locations includesensu stricto;
the occasion SVL:
when snout–vent
animals length;
where released in the TB:
field, Thread-bobbin;
as well as those in which
the snake was not visible. CC: campo cerrado; CD: cerradão; CS: campo sujo; DMIS: distance in a straight line from the capture site; F: female; GF: gallery forest; M: male;
WF: wet field.
MDMD: minimum distance moved per day; PF: Pinus sp. plantation; RT: Radio-tracking; SS: cerrado sensu stricto; SVL: snout–vent length; TB: Thread-bobbin; WF: wet
field.
ID Species Sex SVL Month Method Vegetation Days Number of DMIS MDMD Different
(mm) type locations (m) (m) field trips
498068 B. alternatus F 1070 Aug TB CS 43 18 52 1.2 Yes
500745 B. alternatus F 990 Sep RT CS 28 6 137 4.9 Yes
61C1A43 B. alternatus F 930 Jan RT CS/CC 11 5 47 4.3 No
505020 B. moojeni F 830 Oct TB PP/GF 1 2 65 65 No
501294* B. moojeni F 960 Sep/Oct TB GF 2 3 40 20 No
508549* B. moojeni F 1150 Nov TB WF/CC 2 2 175 87.5 No
498328* B. pauloensis F 580 Nov/Dec RT CS/CC 58 10 30 0.5 Yes
499441* B. pauloensis F 625 Oct RT CD/GF/SS 5 5 195 39 No
61C09D5 C. durissus M 988 Feb TB CS 1 5 130 130 No
499246 C. durissus F 830 Nov TB CS/CC 1 2 75 75 No
500193 C. durissus - 812 Feb TB CS/CC 1 2 150 150 No
497891 C. durissus F 700 Jan TB CC 2 2 80 40 No
501466 C. durissus M 725 Nov TB CC 1 2 80 80 No
504140* C. durissus F 940 Mar TB WF 2 3 75 37.5 No
506947 C. durissus M 939 Feb TB SS 1 2 125 125 No
504559 C. durissus M 845 May TB SS 1 2 90 90 No
501458 C. durissus M 660 Aug TB CD 2 3 30 30 No
507952 C. durissus F 750 Dec TB CD 1 2 98 98 No
610D402 C. durissus M 790 Mar TB CD 1 2 65 65 No
61C0387 C. durissus M 825 Mar TB CD/GF 1 2 70 70 No
61BFF4F* C. durissus M 900 Dec RT CS/CC 33 4 180 5.5 Yes
pauloensis, n = 2; C. durissus, n =1), almost all were transmitters, the mean distance moved from the initial
adults. Most tracking activity occurred in the wettest/ site (DMIS) was 78.7 ± 50.6 m for B. alternatus (n =
warmest months of the year (September–April) and 3; range 47–137 m), 93.3 ± 71.8 m for B. moojeni (n
monitoring time varied greatly depending on the = 3; range 40–175 m), 112.5 m for B. pauloensis (n =
method used and the species tracked (range 1–58 days; 2; range 30–195 m), and 96.0 ± 40.2 m for C. durissus
Table 2). The number of locations recorded for the same (n = 13; range 30–180 m; Table 2). The minimum
individual (including the occasion when the snake was distance moved per day (MDMD) was 1.2–4.9 m/d for
released) varied from 2–18 (Table 2). Both thread- B. alternatus (n = 3), 20.0–87.5 m/d for B. moojeni (n =
bobbin and radio tracking were terminated mostly 3), 0.5–39.0 m/d for B. pauloensis (n = 2), and 5.5–150
due to detachment of adhesive tape (n = 7; 77% of the m/d for C. durissus (n = 13; Table 2).
interruptions; see Fig. 3A), but also due to shedding (one During radio-tracking, the transmitter signal was
individual of B. alternatus and one of B. pauloensis; sometimes lost, probably due to the hiding place in
23% of interruptions). Thread-bobbins provided limited which the individual remained. In these cases, we found
information about total movement length because 14 the individuals several days after the last location,
out of 16 individuals monitored through this method which prevented the estimation of rates of daily
moved until the bobbin was empty, which took 1–2 movement. The five individuals monitored with radio-
days (excluding an individual of B. alternatus for which transmitters moved from 11–195 m (DMIS) and their
monitoring was performed between different field trips). MDMD varied from 0.5–39 m/day. Only one individual
Monitoring of the remaining specimen was interrupted of B. alternatus remained in the same vegetation type
by the detachment of adhesive tape. Considering during the entire period in which it was radio-tracked.
individuals with attached thread-bobbins and radio- The other individuals of this species, as well as one958 Bruno Ferreto Fiorillo et al.
B. pauloensis and one C. durissus, used two to three et al. (2008) found this species mainly in disturbed areas
vegetation types during monitoring (including cases of the surroundings of another cerrado area in São Paulo
where the monitoring was conducted on different field state (Itirapina Ecological Station). Thus, B. pauloensis
trips; Table 2). shows some degree of tolerance to disturbed areas but
Individuals of different species tracked, as well as apparently less than C. durissus. Although there is a
those found through visual searches and occasional wide habitat niche overlap among some species in our
encounters, were observed moving through the study area (e.g., B. alternatus, B. itapetiningae and B.
vegetation, sometimes using different strata (from pauloensis co-occurring in open habitats), interspecific
the ground to bushes ~1.5 m high) and even through competition is unlikely considering the relatively low
water bodies (two individuals of B. moojeni). They abundance of snakes and the apparent abundance of
were often observed sheltered in deep, narrow burrows resources (microhabitat, shelter, food; M. Martins and
(~10–15 cm opening diameter and up to 1 m deep; B.F. Fiorillo, pers. obs.).
two individuals of B. alternatus and one of each B. Our results regarding microhabitat use show that all the
itapetiningae, B. pauloensis, and C. durissus) and studied pitviper species often use subterranean burrows,
termite mounds (two individuals of B. pauloensis). We and the individual of B. pauloensis recaptured very close
also observed individuals in a foraging posture (see to a recently burned area suggest that these microhabitats
Oliveira and Martins, 2002) at night (one individual could function as efficient shelters against fire. Valdujo
of B. itapetiningae, one of B. moojeni and four of C. et al. (2002) suggest that besides being used as shelter
durissus), and even during the day (one individual of B. for fire protection, burrows may also (1) reduce the
itapetiningae and one of C. durissus). exposure to predators, (2) represent favourable foraging
sites, and (3) aid in thermoregulation (reducing heat loss
Discussion at night and providing a relatively stable microclimate).
It also may provide a humid retreat during dry weather
Habitat use.—The five species of pitvipers presented
and may function as a retreat where pre-ecdysis, post-
different habitat breadth (number of vegetation types
feeding, or pre-birthing females could shelter (Huey et
used), which varied from narrow habitat breadth in B.
al., 1989; Greene et al., 2003; Nogueira et al., 2003).
alternatus and B. itapetiningae (basically only two,
The data obtained through mark-recapture and tracking
very similar vegetation types) to wide habitat breadth in
methods indicate that pitvipers tend to move relatively
C. durissus (all vegetation types). Three of the studied
little in our study area. Indeed, some individuals were
species were more restricted to non-forest habitats (B.
recaptured very close to the sites of previous observation
alternatus, B. itapetiningae, and B. pauloensis), while
after relatively long periods (e.g., individuals of B.
the others often used forested habitats (B. moojeni and C.
moojeni and B. pauloensis observed more than a month
durissus). Previous studies also recorded B. alternatus,
later, after the first observation, less than 40 m from the
B. itapetiningae, and B. pauloensis in the open areas
capture site), even after the area had been burned (see
typical of the Cerrado ecoregion (Valdujo et al., 2002;
the example of B. pauloensis above). This indicates that
Sawaya et al., 2008; Nogueira et al., 2010; Leão et al.,
these species may use small areas for long periods, as
2014), while B. moojeni was found more frequently in
suggested by previous studies (Nogueira et al., 2003;
gallery forests and adjacent wet areas (Nogueira et al.,
Tozetti et al., 2009).
2003; Sawaya et al., 2008). Besides having the widest
Our results add to the information available about
habitat breadth, C. durissus was more often found in
habitat use by neotropical pitvipers (Oliveira and
disturbed areas than the other species. Although it uses
Martins, 2002; Valdujo et al., 2002; Nogueira et al.,
predominantly open and relatively dry habitats (e.g.,
2003; Tozetti and Martins, 2008; Sasa et al., 2009).
Sawaya et al., 2008; Tozetti and Martins, 2008), C.
Given that habitat use is critical information for
durissus presents great ecological plasticity and is often
assessing the conservation status of species, as well as
found in forest (Sawaya et al., 2008; Hartmann et al.,
for designing better conservation actions (Maritz and
2009; Benício, 2018) and disturbed areas (Bastos et al.,
Alexander, 2012), our results will certainly contribute
2005). On the other hand, B. pauloensis tended to be
to the conservation of the studied species.
less frequently found in disturbed areas. This species
is widely distributed across the Cerrado ecoregion Methodological issues.—Although the use of thread-
(Nogueira et al., 2019) and typically associated with open bobbins can be useful to study the movement of snakes
savannahs and grasslands (Valdujo et al., 2002). Sawaya in the wild, in most cases when we monitored individualsHabitat use by five species of sympatric pitvipers in a Brazilian savannah 959
using this method the snake moved to the end of the Universidade de São Paulo, Piracicaba, Brazil.
thread-bobbin within 24−48 hours. We wonder whether Furley, P.A., Ratter, J.A. (1998): Soil resources and plant
communities of the central Brazilian cerrado and their
the time, during which individuals were kept in captivity,
development. Journal of Biogeography 15: 97–108.
may have caused biases in daily movement rates for the
Graves, B.M., Duvall, D. (1993): Reproduction, rookery use, and
first few days after release, due to the adverse effects of thermoregulation in free-ranging, pregnant Crotalus v. viridis.
stress (see Mathies et al., 2001). Therefore, we suggest Journal of Herpetology 27: 33–41.
that the use of radio-tracking is more suitable for the Greene, H.W., May, P.G., Hardy, D.L., Sr., Sciturro, J.M., Farrel,
study of pitviper movement in the Brazilian Cerrado T.M. (2003): Parental behavior by vipers. In: Biology of Vipers,
than the use of thread-bobbins. Furthermore, although p. 179–205. Schuett, G. et al., Eds., Eagle Mountain, Utah, USA,
Eagle Mountain Publishing.
the use of external attachment methods reduces stress
Hartmann, P.A., Hartmann, M.T., Martins, M. (2009): Ecology and
associated with surgical intervention (Graves and
natural history of a snake assemblage at Núcleo Santa Virgínia,
Duvall, 1993; Rudolph et al., 1998), the use of adhesive Parque Estadual da Serra do Mar, southeastern Brazil. Biota
tape has its own limitations. Besides been limited to Neotropica 9: 173–184.
the time before the next shedding, in our study tracking Huey, R.B., Peterson, C.R., Arnold, S.J., Porter, W.R. (1989): Hot
with both thread-bobbin and radio-transmitters was rocks and not-so-hot rocks: retreat-site selection by garter snakes
interrupted mostly due to detachment of adhesive tape. and its thermal consequences. Ecology 70: 931–944.
Leão, S.M., Pelegrin, N., Nogueira, C., Brandão, R.A. (2014):
Thus, except when the study aims to track a high number
Natural history of Bothrops itapetiningae Boulenger, 1907
of snakes within short periods of time (Tozetti and (Serpentes: Viperidae: Crotalinae), an endemic species of the
Martins, 2007; Tozetti et al., 2009), internal implants Brazilian cerrado. Journal of Herpetology 48: 324–331.
would be more efficient (see Reinert, 1992). Maritz, B., Alexander, G.J. (2012): Dwarfs on the move: spatial
ecology of the world’s smallest viper, Bitis schneideri. Copeia
Acknowledgements. We thank Giordano Novak Rossi and 2012: 115–120.
Sandro Oliveira Neves for suggestions on earlier versions of Martins, M., Oliveira, M.E. (1998): Natural history of snakes
the manuscript. Fieldwork was conducted with the help of Jorge in forests of the Manaus region Central Amazonia Brazil.
Henry Maciel. This study was funded by the São Paulo State Herpetological Natural History 6: 78–150.
Research Foundation (FAPESP, grant # 2015/21259-8). Specimen Mathies, T., Felix, T.A., Lance, V.A. (2001): Effects of trapping
handling as well as mark-recapture and monitoring procedures and subsequent short-term confinement stress on plasma
were authorised by the Instituto Chico Mendes de Conservação corticosterone in the Brown Treesnake (Boiga irregularis) on
da Biodiversidade (ICMBio; SISBIO permit #50658-1) and Guam. General and Comparative Endocrinology 124: 106–114.
Comissão Técnico-Científica do Instituto Florestal (permit SMA Melo, A.C.G, Durigan, G. (2011): Plano de Manejo da Estação
#260108–011.518/2015). Ecológica de Santa Bárbara. Instituto Florestal, Secretaria
do Meio Ambiente de São Paulo. Available at: http://www.
References iflorestal.sp.gov.br/Plano_de_manejo/index.asp. Accessed on 1
September 2019.
Addinsoft (2019): XLStat. Version 2019.3.2. New York, USA, Nogueira, C. (2001): Ecologia histórica de Bothrops spp. (Serpentes:
Addinsoft. Viperidae: Crotalinae) simpátricas no Cerrado. Unpublished
Barbo, F.E., Marques, O.A.V., Sawaya, R.J. (2011): Diversity, MSc thesis, Universidade de São Paulo, Brazil.
natural history, and distribution of snakes in the municipality Nogueira C., Argôlo, A.J.S., Arzamendia, V., Azevedo, J.A., Barbo,
of São Paulo. South American Journal of Herpetology 6: 135– F.E., Bérnils, R.S., et al. (2019): Atlas of Brazilian Snakes:
160. Verified Point-Locality Maps to Mitigate the Wallacean Shortfall
Bastos, E.G.M., Araújo, A.F.B., Silva, H.R. (2005): Records of the in a Megadiverse Snake Fauna. South American Journal of
rattlesnakes Crotalus durissus terrificus (Laurenti) (Serpentes, Herpetology 14: 1–274.
Viperidae) in the state of Rio de Janeiro, Brazil: a possible case Nogueira, C., Sawaya, R.J., Martins, M. (2003): Ecology of the
of invasion facilitated by deforestation. Revista Brasileira de pitviper, Bothrops moojeni, in the Brazilian cerrado. Journal of
Zoologia 22: 812– 815. Herpetology 37: 653–659.
Benício, R. (2018): Notes on habitat use of Crotalus durissus (South Nogueira, C., Colli, G.R., Costa, G.C., Machado, R.B. (2010):
American Rattlesnake). Herpetology Notes 11: 645–646. Diversidade de répteis Squamata e evolução do conhecimento
Colli, G.R., Vieira, C.R., Dianese, J.C. (2020): Biodiversity and faunístico no cerrado. In: Cerrado: Conhecimento Científico
conservation of the Cerrado: recent advances and old challenges. Quantitativo como Subsídio para Ações de Conservação, p. 333–
Biodiversity and Conservation 29: 1465–1475. 375. Diniz, I.R., Marinho-Filho, J., Machado, B.R., Cavalcanti,
Eiten, G. (1972): The Cerrado vegetational of Brazil. Botanical R.B., Eds., Brasília, Brazil, Editora UnB.
Review 38: 201–341. Nogueira, C., Sawaya, R.J., Martins, M. (2003): Ecology of the
Fiorillo, B.F. (2020): Diversity and effects of vegetation structure pitviper, Bothrops moojeni, in the Brazilian cerrado. Journal of
on squamates in a cerrado area in southeastern Brazil: subsidies Herpetology 37: 653–659.
for the management of protected areas. Unpublished PhD thesis, Oliveira, M.E., Martins, M. (2002): When and where to find a960 Bruno Ferreto Fiorillo et al.
pitviper: activity patterns and habitat use of the lancehead, sobre história natural. In: História Natural da Serra do Japi:
Bothrops atrox, in central Amazonia, Brazil. Herpetological Ecologia e Preservação de Uma Área Florestal no Sudeste do
Natural History 8: 101–110. Brasil, p. 212–236. Morellato, L.P.C., Ed., Campinas, Brazil,
QGIS Development Team (2019): QGIS Geographic Information Editora da Unicamp/FAPESP.
System. Open Source Geospatial Foundation Project. Available Strassburg, B.B.N., Brooks, T., Feltran-Barbieri, R., Iribarrem, A.,
at http://qgis.osgeo.org. Crouzeilles, R., Loyola, R., et al. (2017): Moment of truth for
Ribeiro, J.F., Walter, B.M.T. (1998): Fitofisionomias do bioma the Cerrado hotspot. Nature Ecology & Evolution 1: 1–3.
cerrado. In: Cerrado: Ambiente e Flora, p. 89–166. Sano, S.M., Tozetti, A.M., Martins, M. (2007): A technique for external radio-
Almeida, S.P., Eds., Planaltina, Brazil, Embrapa-CPAC. transmitter attachment and the use of thread-bobbins for studying
Reinert, H.K. (1992): Radiotelemetric field studies of pitvipers: snake movements. South American Journal of Herpetology 2:
data acquisition and analysis. In: Biology of Pitvipers, p. 185– 184–190.
197. Campbell, J.A., Brodie, E.D., Jr., Eds., Eagle Mountain, Tozetti, A.M., Martins, M. (2008): Habitat use by the South
Utah, USA, Eagle Mountain Publishing. American rattlesnake (Crotalus durissus) in southeastern Brazil.
Rudolph, D.C., Burgdorf, S.J., Schaeffer, R.R., Conner, R.N. Journal of Natural History 42: 1435–1444.
(1998): Snake mortality associated with late season radio- Tozetti, A.M., Vettorazzo, V., Martins, M. (2009): Short-term
transmitter implantation. Herpetological Review 29: 155–156. movements of the South American rattlesnake (Crotalus
Sasa, M., Wasko, D.K, Lamar, W.W. (2009): Natural history of the durissus) in south-eastern Brazil. Herpetological Journal 19:
terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. 201–206.
Toxicon 54: 904–922. Valdujo, P.H., Nogueira, C., Martins, M. (2002): Ecology of
Sawaya, R.J., Marques, O.A.V., Martins, M. (2008): Composition Bothrops neuwiedi pauloensis (Serpentes: Viperidae: Crotalinae)
and natural history of a cerrado snake assemblage at Itirapina, in the Brazilian cerrado. Journal of Herpetology 36: 169–176.
São Paulo State, southeastern Brazil. Biota Neotropica 8: 127–
149.
Sazima, I., Haddad, C.F.B. (1992): Répteis da Serra do Japi: notas
Accepted by Hinrich KaiserYou can also read
