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A new insular species of the genus Bothrops is described from Ilha dos Franceses, a small island off the coast of Espírito Santo State, in southeastern Brazil. The new species differs from mainland populations of B. jararaca mainly by its small size, relative longer tail, relative smaller head length, and relative larger eyes. The new species is distinguished from B. alcatraz, B. insularis and B. otavioi by the higher number of ventral and subcaudal scales, relative longer tail and smaller head. The new species is highly abundant on the island, being nocturnal, semiarboreal, and feeding on small lizards and centipeds. Due its unique and restricted area of occurrence, declining quality of habitat, and constant use of the island for tourism, the new species may be considered as critically endangered.
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Accepted by P. Passos: 17 Feb. 2016; published: 4 Apr. 2016
ISSN 1175-5326 (print edition)
(online edition)
Copyright © 2016 Magnolia Press
Zootaxa 4097 (4): 511
Another new and threatened species of lancehead genus Bothrops
(Serpentes, Viperidae) from Ilha dos Franceses, Southeastern Brazil
Museu de Zoologia, Universidade de São Paulo, P.B. 42494, São Paulo 04218–970, São Paulo, Brazil
Departamento de Ecologia e Oceanografia, Universidade Federal do Espírito Santo, Vitória 29075–910, Espírito Santo, Brazil
ICMBIO, Reserva Biológica de Comboios. P.B. 105, CEP 29900-970, Linhares, Espírito Santo, Brazil
Departamento de Ciências Biológicas, Universidade Federal de São Paulo, Diadema 09972–270, São Paulo SP, Brazil
Corresponding author. E-mail:
A new insular species of the genus Bothrops is described from Ilha dos Franceses, a small island off the coast of Espírito
Santo State, in southeastern Brazil. The new species differs from mainland populations of B. jararaca mainly by its small
size, relative longer tail, relative smaller head length, and relative larger eyes. The new species is distinguished from B.
alcatraz, B. insularis and B. otavioi by the higher number of ventral and subcaudal scales, relative longer tail and smaller
head. The new species is highly abundant on the island, being nocturnal, semiarboreal, and feeding on small lizards and
centipeds. Due its unique and restricted area of occurrence, declining quality of habitat, and constant use of the island for
tourism, the new species may be considered as critically endangered.
Key words: Atlantic Forest, Bothrops, Conservation, Island rule, Heterochrony, taxonomy
Uma nova espécie insular de jararaca é descrita para a Ilha dos Franceses, localizada na costa do estado do Espírito Santo,
no sudeste do Brasil. A nova espécie difere das populações continentais de B. jararaca principalmente pelo menor tama-
nho, maior comprimento relativo de cauda, menor comprimento relativo da cabeça e olhos relativamente maiores. Dife-
rencia-se também de B. alcatraz, B. insularis e B. otavioi pelo maior número de escamas ventrais e subcaudais, maior com-
primento relativo de cauda e menor comprimento relativo de cabeça. A nova espécie é encontrada em grande abundância
na ilha, sendo noturna, semi arborícola, e se alimenta de pequenos lagartos e centopeias. Devido à sua reduzida área de
ocorrência, declínio da qualidade do habitat, e acesso constante de turistas à ilha, a nova espécie deve ser considerada
como criticamente ameaçada de extinção.
Palavras-chave: Mata Atlântica, Bothrops, Conservação, Regra das ilhas, Heterocronia, Taxonomia
Pitvipers diversity, morphology, and ecology are remarkable (Campbell & Lamar 2004). Approximately 230
species of crotalines are currently recognized, with at least 14 new species being described in the last four years
only (see Uetz & Hošek 2015). Bothrops is the most diverse genus within crotalines, including about 50 species
splitted into six different monophyletic groups: B. alternatus, B. atrox, B. jararaca, B. jararacussu, B. neuwiedi,
and B. taeniatus (Martins et al. 2001, 2002; Araújo & Martins 2006; Fenwick et al. 2009; Carrasco et al. 2012).
The genus is distributed from Central to South America, throughout several types of landscapes, including
rainforests and open habitats (Martins et al. 2002; Campbell & Lamar 2004).
Zootaxa 4097 (4) © 2016 Magnolia Press
The Bothrops jararaca complex comprising four known species: Bothrops jararaca (Wied, 1824), B. alcatraz
Marques, Martins & Sazima, 2002, B. insularis (Amaral, 1921), and B. otavioi Barbo, Grazziotin, Sazima, Martins
& Sawaya, 2012. The only mainland species, B. jararaca, is widespread throughout the Brazilian Atlantic forest,
from the northeastern highland forested enclaves of Bahia to the southern Atlantic forest of the state of Rio Grande
do Sul (Campbell & Lamar 1989; Martins et al. 2002), also occurring in disturbed environments such as borders of
forests and urbanized areas (Marques et al. 2009; Barbo et al. 2011). The latter three species are all endemic from
small continental islands of the Southeastern coast of Brazil (Ilha dos Alcatrazes, Ilha da Queimada Grande, and
Ilha da Vitória, respectively). Those islands correspond to emerging mountain picks with relatively high elevation
(more than 200 m above sea level; asl hereafter), located more than 20 km off the coast, and surrounded by
relatively deep waters (more than 30 m below sea level; hereafter bsl).
Recent studies have shown that the number of species for the group is probably underestimated (Grazziotin et
al. 2006; Barbo et al. 2012). Known mainland populations of B. jararaca possibly form a complex of species since
several highly genetically structured populations were identified by mitochondrial DNA analyses (Grazziotin et al.
2006). At the same time, the insular populations have shown several apparently fixed autapomorphic
morphological characters of coloration and scalation that distinguish them from their mainland relatives. These
unique morphotypes suggest the presence of distinct evolutionary trajectories that have not been hitherto
comprehensively studied throughout the entire distribution of the group (Marques et al. 2002).
Here, we describe a fifth species of the B. jararaca group from Ilha dos Franceses (maximum altitude 36 m
asl), a small island located less than five kilometers off the coast of the state of Espírito Santo and surrounded by
very shallow waters (less than 5 m bsl). The fact that this species lives in a small island easily accessible from the
shore makes it unique for ecological and evolutionary studies, but at the same time highly threatened and
dependent of governmental actions for its preservation.
Materials and methods
We examined 58 specimens of the new species, being five collected in the field by our team, nine photographed
and released in the field, and 44 previously available in scientific collections. We compared them with 154
specimens of Bothrops jararaca from mainland localities distributed throughout the states of Espírito Santo (n =
82), São Paulo (n = 30), Paraná (n = 23), Santa Catarina (n = 9), and Rio Grande do Sul (n = 10). We also compared
the new species with eight specimens of B. alcatraz, 26 B. insularis, and 31 B. otavioi. Because only a few
specimens of B. alcatraz were available for this analysis, we complemented its sample with data retrieved in
Marques et al. (2002), totaling 32 specimens. Additional specimens of B. insularis from literature and unpublished
data (Amaral 1921; K. Kasperoviczus, pers. com.) were also included in some analyses (n = 374). Specimens
examined are cited in the Appendix and institutional abbreviations follow Sabaj-Pérez (2015).
Linear morphometric analyses. Samples available for this analysis included a total of 260 males and 311
females (Table 1). We measured snout–vent length (SVL) and caudal length (CL) using a flexible ruler to the
nearest millimeter (mm). We also measured the head length (HL; from snout to extreme posterior portion of
mandible), with calipers to the nearest 0.01 mm. We determined the trunk length (TR) as SVL subtracting up the
HL. The relative tail length (RTL) corresponded to CL/SVL, whereas the relative head length (RHL) was obtained
by HL/TR. We counted ventral scales (from the first scale wider than long), intersupraocular scales (lines of
anterior, middle, and posterior scales between supraoculars), and interrictal scales (line of scales linking last
supralabials). Lateral scales of head were also counted: interoculabials (between upper 3–4
supralabials and
suboculars), circumorbitals (scales contacting eye), pre and postfoveals, temporals, and supra and infralabials.
Statistical tests were performed in R (R Core Team 2013). Adults and juveniles were analyzed separately due
to possible bias in RTL and RHL throughout ontogeny. Males and females from Ilha dos Franceses were
considered adults when the specimen was longer than 450 mm SVL and 540 mm SVL, respectively (see Natural
History Section below). Males from the mainland population of the state of EspíritoSanto were considered adults
when they were longer than 610 mm SVL, while adult females were longer than 740 mm SVL (K. Kasperoviczus,
pers. comm.). We tested for the normality and homoscedasticity of samples using Kolmogorov-Smirnov and
Bartlett tests, respectively. We used Student’s t tests for morphological comparisons, when normal distributions
assumption applied (p-value > 0.05), with RTL and RHL as dependent variables. For non normal distributions we
applied Kruskal-Wallis' test.
Zootaxa 4097 (4) © 2016 Magnolia Press
Geometric morphometric analysis. Samples available for this analysis included a total of 78 males and 84
females from the mainland populations of B. jararaca (N = 134) and Ilha dos Franceses (N = 28). Only the right
side of the head of each specimen was photographed with a camera Nikon D700 coupled to an AF-S VR Micro-
Nikkor 105 mm f/2.8G IF-ED lenses, fixed in a copystand with a standardized distance from the camera body of
550 mm. Images were digitalized with landmarks type I (Bookstein 1991) using tpsDig2 software (Rohlf 2005).
Sixteen landmarks were recognized in the right plane. Landmarks 1 to 5 refer to the region of the eye, 6 to 8 to the
loreal pit, 9 and 10 to the rostral region, and 11 to 16 to the mouth. (Fig. 1). We performed a Canonical Variate
Analyses (CVA) separately for mature males and females, with MorphoJ (Klingenberg 2011) and R (R CoreTeam
2013) softwares. The CVA was performed with the residuals of the regression between the shape and centroid size
aiming to correct the allometric differences.
Our morphological comparisons using linear morphometrics identified a set of characters that distinguished the
population of Ilha dos Franceses from the mainland populations of B. jararaca and from all three insular species of
the group (B. alcatraz, B. insularis, and B. otavioi). We further identified significant shape differences between the
population from Ilha dos Franceses and the mainland populations of B. jararaca by performing a landmark-based
geometric morphometric analysis of head shape in a total of 162 specimens. Results from our analyses are provided
Linear morphometric analyses
Our linear morphometric analyses distinguished the population of Ilha dos Franceses from the three insular species
of the group and the closest mainland population of B. jararaca.
The population from Ilha dos Franceses showed the following differences to the closest population of B.
jararaca from mainland Espírito Santo (Table 1): smaller adult size in males (H = 30.29, p < 0.001) and in females
(H = 29.14, p < 0.001); lower number of ventral scales in males (t = -2.803, df = 54.92, p = 0.006) and lower
numbers of subcaudals in females (H = 3.43, p = 0.064); relatively longer tail (TL/SVL) in males (t = 2.9075, df =
42.98, p = 0.006); relatively smaller heads (HL/TR) in males (t = 2.525, df = 38.223, p = 0.01).
The population from Ilha dos Franceses differed from Bothrops alcatraz by the following morphometric
characteristics (Table 1): larger adult size in males; higher number of ventral scales in males and females; higher
number of subcaudals in males and in females; relatively longer tail in males and in females; relatively smaller
head in males. We did not present statistical comparisons because all vouchers of B. alcatraz were lost in 2010
during the fire of herpetological collection of Instituto Butantan. Therefore, comparisons of measurments and
counts were made using data available in Marques et al. (2002).
The population from Ilha dos Franceses differed from Bothrops otavioi by the following morphometric
characteristics (Table 1): larger adult size in males (H = 14.819, p = 0.0001), and in females (H = 7.286, p = 0.007);
higher number of ventrals in males and females; higher number of subcaudals in males and females; relatively
smaller head in males (H = 15.418, p < 0.001), and females (H = 12.265, p <0.001).
Finally, the population from Ilha dos Franceses differed from Bothrops insularis mainly by its grayish-
brownish coloration vs. pale or yellowish in B. insularis; smaller adult size in males (t = -3.266, df = 27.362, p =
0.003), and females (H
= 21.452, p < 0.001); higher number of ventral scales in males (H
= 52.744, p < 0.001), and
females (H
= 58.064, p < 0.001); higher number of subcaudal scales in males (H = 49.145, p < 0.001), and females
(H = 44.829, p < 0.001); relatively smaller tail in males (H
= 13.28, p = 0.0002), and females (H
= 4.504, p = 0.03);
relatively smaller head in males (H
= 37.606, p < 0.001), and females (H
= 39.917, p < 0.001).
Zootaxa 4097 (4) © 2016 Magnolia Press
alcatrazDQGB. insularisZHUHREWDLQHGLQ0DUTXHVet alDQG$PDUDO
Bothrops sazimai VSQRYBothrops jararaca
PDLQODQG(VStULWR6DQWRBothrops alcatraz*Bothrops insularis**Bothrops otavioi
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Zootaxa 4097 (4) © 2016 Magnolia Press
7$%/(&RQWLQXHG    
Bothrops sazimai VSQRYBothrops jararaca
PDLQODQG(VStULWR6DQWRBothrops alcatraz*Bothrops insularis**Bothrops otavioi
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Geometric morphometric analysis
Our geometric morphometric analysis identified significant shape differences between the population of Ilha dos
Franceses and the remaining mainland populations of Bothrops jararaca distributed throughout the range of the
species. Indeed, the points of dispersion in the CVA did not overlap in insular and mainland populations, with the
ellipses of 95% confidence intervals overlapping only marginally in males (Fig. 1). The first canonical axes of CVA
explained 67.6% and 86.1% of variation for males and females, respectively. When compared with mainland
populations of B. jararaca, specimens of Ilha dos Franceses presented shorter distances between landmarks 11 to
16 and longer distances between landmarks 1–2 and 15 (Fig. 1), indicating a smaller head length and higher head
height at the level of the eyes, respectively. Landmarks 1–5 were distributed farther away from each other in
specimens of Ilha dos Franceses, instead of closer to each other as in all mainland populations, reflecting the larger
eyes in the new species. Landmarks 2–3, and 9 showed that canthals and the tip of the snout were projected
downward in the population of Ilha dos Franceses, whereas mainland populations had a snout projected upward.
Specimens from Ilha dos Franceses also differed from the mainland populations of B. jararaca in respect to their
rostral region that appeared to be sunk (landmarks 9 to11), and the modified size of their loreal pit that were nearer
to the nostril (landmarks 6–7 relative to 9) (Fig. 1).
In synthesis, our quantitative analyses (linear and geometrical) allowed us to recognize the population from
Ilha dos Franceses as a new species, described below.
Bothrops sazimai sp. nov.
Figs. 2–4
Bothrops jararaca—Campbell & Lamar, 2004. Venomous Reptiles of the Western Hemisphere. Vol. 1, 1–476:391. (in part).
Holotype. An adult male, MZUSP 22228, collected by our team on May 14, 2013, at Ilha dos Franceses
(20°55'36"S, 40°45'15"W), municipality of Itapemirim, Itaoca beach, state of Espírito Santo, Brazil (Figs. 2–3).
Paratypes. Fourteen specimens: IBSP 86673 (female), IBSP 86674–75 (males), MBML 3319 (male with
hemipenis prepared), MBML 3320–21 (females), MBML 3322 (male), MBML 3323 (female), MZUSP 22229
(male), MZUSP 22230 (female), MZUSP 22231 (male), MZUSP 22232 (female), ZUEC 3383 (male), ZUEC 3384
Diagnosis. Bothrops sazimai is distinguished from other species of B. jararaca group by the following
combination of characters: (1) larger eyes; (2) shorter and higher head; (3) slender body; (4) relative longer tail; (5)
dorsum predominantly grayish and/or brownish; (6) venter creamish white, speckled in gray; (7) postorbital stripes
with the same color of lateral saddles; (8) usually two postoculars; (9) 22–25 interictals; (10) 20–24 anterior
dorsals; (11) 20–23 midbody dorsals; (12) 198–214 ventrals in females, 193–206 in males; (13) 54–65 subcaudals
in females, 62–70 in males.
Bothrops sazimai differs from the mainland populations of B. jararaca by its smaller adult size (SVL), relative
longer tail (RTL), slender body, and larger eyes (Fig. 1; Table 1). The new species can be easily distinguished from
the other three species of the B. jararaca group (B. alcatraz, B. insularis, and B. otavioi) by a higher number of
ventrals and subcaudals (Table 1). It further differs from B. insularis by its grayish or brownish ground color
pattern, smaller length of adults, relative smaller head, and relative smaller tail. The new species is also
distinguished from B. alcatraz and B. otavioi, by its larger adult size, presence of conspicuous yellowish tail tip in
juveniles, and additionally from the latter species by the presence of two postoculars and higher number of
intersupraocular scales (Table 1).
Description of the holotype. Adult male; total length 738 mm; SVL 630 mm; TL 108 mm (17% of total
length); TR 604.1 mm; head length 25.9 mm (0.49% of trunk); head width 14.9 mm; mass 52.3 g (after draining
preservative). Rostral 2.9 mm wide, 4.2 mm high; nasal divided anterior and posterior to nostril; loreal trapezial
and single; prefoveals 2/2; postfoveals 2/2; prelacunal fused with second supralabial forming lacunolabial on both
sides; preoculars 2/2; postoculars 2/2; supralabials 8/8; interoculabials 3/2; circumorbitals 6/6; temporals 5/6;
infralabials 10/10, first three pairs contacting chin shields; four gulars between chin shields and first ventral scales;
six rows of gulars separating first ventral scales from 8
infralabial; canthals 2/2; five anterior intercanthals; four
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FIGURE 1. Canonical analysis of females (A) and males (B) of Bothrops jararaca species group. Limits of variation in head
shape were defined by 95% confidence ellipses and computed by parametric bootstrap. Blue = population from Ilha dos
Franceses; Red = population of B. jararaca from mainland portions of the state of Espírito Santo; Green = other mainland
populations of B. jararaca, from the states of São Paulo, Paraná, Santa Catarina, and Rio Grande do Sul.
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FIGURE 2. Dorsal (A), lateral (B), and ventral (C) views of head of the holotype of Bothrops sazimai (MZUSP 22228). Scale
bar = 10 mm.
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FIGURE 3. Dorsal (above) and ventral (below) views of the holotype of Bothrops sazimai (MZUSP 22228). Scale bar = 20
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FIGURE 4. Active specimens of Bothrops sazimai at night in different macrohabitats on the island. Over fallen trunks and
twigs (A); coiled over trees (B) (MZUSP 22230); two individuals close to one another and moving on the ground (C); on the
rocks near the sea (D); coiled on the ground (MZUSP 22232) (E). Photographs by R. Sawaya (A, E), R. Zorzal (B), F. Barbo
(C), and T. Portillo (D).
posterior intercanthals; rows of anterior, central and posterior intersupraoculars 7/7/12; interrictals 22; dorsals
reducting posteriorly 21/21/17; ventrals 196; cloacal plate single; divided subcaudals 64. Posterior cephalic scales
longer than wide and strongly keeled; intersupralabials scales weakly keeled; temporal scales keeled; internasals,
canthals, and supraoculars smooth.
Coloration in life was grayish on dorsal surface with 15/14 lateral trapezoidal markings (saddles) irregularly
defined, dark brown-gray with well-defined borders, weakly pale-grayish edged, opposite and alternate to each
other in middle of dorsum; dorsum of head grayish, spotted with two small well-defined dark blotches between
occipital–temporal portion and neck (Figs. 2–3); postorbital stripe is dark brown, bordered below by a thin white
line. Extends from behind eye, covering superior portion of 6
, 7
and 8
supralabials, up to three scales long
behind rictual region and three scales downwards to ventral direction; gular region mostly whitish-creamish, with
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infralabials and symphysial speckled of gray; venter mostly whitish anteriorly, speckled in gray posteriorly and
covering cloacal plate; tail grayish dorsally, covered with small dark gray lateral blotches, with subcaudals
speckled in ventral plan.
Variation (Table 1). Dorsum of head can vary from entirely brownish or grayish, with or without brownish
stripes and blotches between supraoculars and the neck. Second supralabial fused with prelacunal forming the
lacunolabial (n = 23), partially fused (n = 6), or separated (n = 6). Besides differences in pholidosis, adult males
have longer tail than females (Table 1; H
= 15.55, p < 0.001).
Hemipenis (n = 8). There is no evident variation in hemipenial morphology regarding shape and
ornamentation. Fully everted and maximally expanded organ moderately bilobed, subcylindrical, and bicapitate;
small and medium ossified spines covering proximal region of hemipenis; hemipenial body and intralobular region
asymmetrically covered by spinules on proximal portion, and medium and large spines on median and distal
portions on both sulcate and asulcate sides of organ; ossified spinules bordering sulcus spermaticus up to
capitulum, excepting croach; border of proximal calyces forming capitulum spinulate; sulcus spermaticus
bifurcating at level of croach and extending to tips of lobes (Fig. 5).
FIGURE 5. Sulcate (left) and asulcate (right) views of the hemipenis of B. sazimai (MBML 3319 paratype). Scale bar = 5 mm.
Distribution. The new species is known only from the type-locality, Ilha dos Franceses, (Fig. 6). This island
has about 15 ha with maximum elevation of 36 m asl covered by secondary Atlantic forest remnants (Ferreira et al.
2007), and located 3.6 Km eastwards from Itaoca beach (Fig. 7).
Natural History. Bothrops sazimai is abundant in Ilha dos Franceses as we have found approximately two
snakes per hour-person by visual search. The beginning of daily activity was observed in late afternoon. Specimens
were observed coiled (n = 13), moving (n = 8) or stationary (n = 4), on the ground (n = 15), as well as in lower
portions of shrubs and trees (n = 9) (Fig. 4). Except for the five collected individuals (holotype and four paratypes),
all snakes were observed and/or photographed and released in the field. Juveniles and adults of the new species
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feed on ectothermic prey. Twenty-six out of 58 individuals examined in scientific collections had prey remnants in
their stomach and gut contents, including lizards (Gymnodactylus darwinii and Hemidactylus mabouia, n = 14),
centipedes Scolopendromorpha (n = 6), and a conspecific snake (n = 1). Youngs have yellowish tail-tip (n = 13),
suggesting caudal-luring behavior (see Andrade et al. 2010; Sazima 1991). The smallest mature male with enlarged
testes and opaque efferent ducts had 451 mm SVL, whereas the smallest mature females with follicles or embryos
in the oviduct measured 551 mm SVL (K. Kasperoviczus, pers. com.).
FIGURE 6. Coastal region of the state of Espírito Santo (above), with the Ilha dos Franceses (below), the type locality of
Bothrops sazimai. Legend of states: Bahia (BA); Espírito Santo (ES), Minas Gerais (MG), and Rio de Janeiro (RJ).
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FIGURE 7. Aerial view of Ilha dos Franceses (A); forest remnants in the light-house area (B); vegetation on rocks of the tide
zone (C); dense vegetation predominant in island (D); view of Ilha dos Franceses from Itaoca Beach (E). Photographs by
Google Earth Pro (A), F. Barbo (B, C, D), and R. Sawaya (E).
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Etymology. The specific epithet sazimai represents a patronymic name dedicated to the friend and professor
Ivan Sazima, for his invaluable contribution to the study of natural history and conservation of Brazilian fauna, and
for his inspiring and pioneering field studies on Bothrops jararaca. Professor Ivan advised and mentored various
generations of students and researchers that presently work with diverse systems and organisms, including snakes,
amphibians, fishes, mammals, birds, and plants. He published hundreds of scientific contributions, among articles,
book chapters, and educational texts. We suggest the standard English name “Franceses island-Lancehead” for the
new species.
Lanceheads of the Bothrops jararaca species group have been collected in continental islands along the Brazilian
coast since the 1910's. These were initially determined as B. jararaca due to their general morphological
similarities. An exception at that time was Bothrops insularis, which was described as a distinct species due to its
outstanding differences in coloration and ecological attributes when compared to the remaining species of the B.
jararaca complex (Amaral 1921). In the past few decades, studies on natural history and ecology within this group
of Lanceheads allowed to refine our understanding of its hidden ecological diversity (Martins et al. 2008; Andrade
et al. 2010; Marques et al. 2012, 2013; Guimarães et al. 2014). However, the taxonomic status of several isolated
populations of B. jararaca remains poorly understood (but see Marques et al. 2002; Barbo et al. 2012). Recent
studies showed that two additional insular populations, previously recognized as belonging to B. jararaca, are
actually distinct species (Marques et al. 2002; Barbo et al. 2012). Bothrops sazimai represents the fourth island
endemic to be described for the group.
Island species usually show different patterns of body size and growth regime when compared to their related
mainland species (Foster 1964). Van Valen (1973) termed the phenomenon related to gigantism and dwarfism in
insular populations of mammals as the island rule (see also Lomolino 2005, 2012). According to this rule, large
mainland species become dwarf on islands and small mainland species become giant on islands. Some studies have
demonstrated that snakes also follow this rule, a phenomenon that could be triggered by reduced prey availability
and/or reduced prey size (Case 1978; Keogh et al. 2005), as suggested by the diet alteration hypothesis sensu
Boback (2003). The diet alteration hypothesis, related to island dwarfism in snakes, could explain the distinct body
size patterns observed in the insular members of the B. jararaca complex. All three island species of the group
present change on diet, because none of those islands retain natural populations of small mammals, the main prey
item of adult B. jararaca (Sazima 1992).
Bothrops insularis does not have any tendency to dwarfism or gigantism, and its diet resembles that of
mainland populations, with juveniles feeding upon ectothermic prey whereas adults became bird specialists,
shifting their diet towards the largest prey available in the island. Bothrops insularis also shows some variation in
body form that is apparently related to its more arboreal habits (see Martins et al. 2001). Bothrops alcatraz and B.
otavioi, on the other hand, are considered dwarf forms within the B. jararaca complex, the former feeding mainly
on centipedes, but also on lizards, while the latter preys upon frogs (Marques et al. 2002; Barbo et al. 2012).
Although Bothrops sazimai is larger than B. alcatraz and B. otavioi, it is definitely smaller than B. insularis and the
mainland populations of B. jararaca, and is considered here another dwarf form that feeds on ectothermic prey
(lizards, centipedes, and conspecific snakes). These three dwarf forms show a body form similar to that of young
mainland specimens of B. jararaca that also feed exclusively on ectothermic prey. We could then consider this
repeated and parallel evolution of dwarf forms as an evidence of the diet alteration hypothesis, and one possible
causal mechanism related to the well-known island rule pattern.
We observed a significant number of specimens (n = 13) of Bothrops sazimai in the field that were coiled on
the soil with their head directed to the base of tree trunks in which a large number of centipedes and small lizards
could also be observed. Since prey-type selection is known to have a strong effect on the evolution of head size
(Vanhooydonck et al. 2007), we consider that the overall larger eyes and more ventrally directed and shorter nostril
of B. sazimai (Fig. 1) may represent adaptations to this specific microhabitat and prey items. Small ectothermic
prey could be probably more effectively detected and subjugated by snakes with larger eyes and smaller heads,
with more anteriorly positioned sensorial organs. Although most field observations related to foraging B. sazimai
were made on specimens located on the ground, it is likely that the species also forages on the trees since nine
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specimens were observed at 1.5–2 meters above the ground, inside the forest. Additionally, B. sazimai shows a
relatively longer tail length when compared to B. alcatraz and B. otavioi, a feature that is associated to arboreal
habits. Finally, the two lizards that are preyed by B. sazimai are arboreal species, and are the dominant prey found
in gut contents of preserved specimens.
Marine oscillations of the Brazilian coast are already known and mapped, with the intervals of time of
retractions and transgressions well defined (Martin et al. 1986). The islands of Alcatrazes, Queimada Grande, and
are located about 35 to 40 km off the coast of the state of São Paulo, whose depths varying between 40–60
m. During the Pleistocene, between 12,000–10,000 ya, the sea level was ca. 60 m lower (Martin et al. 1986),
indicating that these islands and the mainland were connected in this period. These pleistocenic oscillations of sea
level are the most acceptable hypothesis for separation between the mainland B. jararaca-like ancestor and these
closely related island species (see Rohling et al. 1998). For B. sazimai this process has probably occurred more
recently when comparing to the islands mentioned above.
Due to the short distance between the mainland and Ilha dos Franceses (ca. 4 km), and the relatively low depth
of the sea in this region (ca. 4 m), island and mainland should be probably connected during the medium Holocene
(ca. 3,800–4,000 ya; Martin et al. 1986; Massad et al. 1996), when the sea level was ca. 4–6 m lower than observed
nowadays. Even so, this short time could be enough to promote some notable modifications in morphology and
ecology of the new species. These modifications could be produced by a strong genetic drift derived from the
genetic bottleneck caused by the insularization process, or instead by a strong selection driven by the restrictions of
the insular environment (absence of small mammals, population density, etc.). Alternatively, other factors as
heterochrony or more specifically allometry can be playing an important role in shaping the morphology of B.
sazimai. We claim that a more detailed study on this subject is needed to better understand the evolutionary process
involved in such speciation events.
The probable recent isolation of Bothrops sazimai (ca. 3,800–4,000) in Ilha dos Franceses—suggested by the
cycles of the marine oscillations of the Brazilian coast—can bring different sort of problems for the methods of
species delimitation based on the coalescent process (Maddison & Knowles 2006; Knowles & Carstens 2007). As
shown by Grazziotion et al. (2006) and Barbo et al. (2012) there is no genetic difference between the insular
species of the B. jararaca group and the mainland populations of B. jararaca. These authors also shown that B.
insularis, B. alcatraz and B. otavioi are nested within the B. jararaca mitochondrial lineages, presenting the same
mitochondrial haplotype found in the mainland B. jararaca. This mitochondrial DNA pattern indicates the
existence of shallow polymorphism among these species and suggests that the incomplete lineage sorting is
producing discrepancies between the gene tree and the species tree (Edwards 2008). Therefore, even not providing
genetic data for B. sazimai, we argue that the species probably does not present reciprocal monophyly in relation to
the mainland populations of B. jararaca. Based on the results of Grazziotin et al. (2006) and Barbo et al. (2012) we
also claim that sequencing a handful of loci will not offer sufficient molecular evidence for helping in the
delimitation of this species. Consequently, we based the description on morphological characters and the unique
combination of characters states (Davis & Nixon 1992) that makes B. sazimai diagnosable.
Island endemics are unique entities, evolving apart from mainland populations under different time and
evolutionary scenarios. Bothrops alcatraz and B. insularis were included in IUCN red-lists (see Marques et al.
2004a,b), and were included in a pioneering initiative of protection proposed by the governmental institution
ICMBio. This program was developed exclusively for the study of threatened species, and aimed to provide
detailed information on their natural history, ecology and population dynamics that would be used in management
and conservation strategies. In our opinion, such program should be extended to B. sazimai that faces potential
threats due to the short distance of the Ilha dos Franceses to the shore, and the presence of a small beach, which
encourage a constant transit of tourists into the island. The continuous flux of visitation results in uncontrolled
littering and even occasional fires, increasing the risk of pollution and destruction of significant portions of the
island. Those threats could affect drastically or even drive to extinction this unique insular species.
The encounter rate of Bothrops sazimai is about 15 snakes per day of visual search, and could be compared to
the one observed in Ilha da Queimada Grande for B. insularis (between 15 and 33 snakes a day; Martins et al.
2008), thus representing a second case of highly unusual density of an insular Lancehead population along the
Brazilian coast. According to IUCN’s definitions (CR B1a,b [iii]), B. sazimai falls in the criterion of a "critically
endangered species" since it is endemic to an area with less than 100 km
(0,15 km
, Figs. 6–7). Therefore,
Brazilian government should define a protected area that would encompass Ilha dos Franceses. The new species
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could be included in the next future to the global and national red lists as Critically Endangered as well as in ex-situ
conservation actions.
We are grateful to K. Kasperoviczus for providing reproductive data for the new species and B. insularis, to G.
Sanches (MZUSP) and J. Paulo (MBML) for their support in respective collections, and to H.T. Pinheiro, T.E.
Simon (in memorian), C. Neto, T. Guedes, J.T. Portillo, and R. Zorzal for their help in the field. FEB and FGG
benefitted from a post-doctoral fellowship from the Fundação de Amparo à Pesquisa do Estado de São Paulo
(FAPESP grant numbers 2012/09156-0 and 2012/08661-3, respectively). This research was supported by grants
from Fundação de Amparo à Pesquisa do Estado de São Paulo (BIOTA/FAPESP 2011/50206-9 and FAPESP 2008/
54472-2) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 565046/2010-1, 303545/
2010-0) to HZ and (CNPq 305911/2012-0) to RJS. RJS also thanks FADA-UNIFESP for financial support. This
research was carried out in strict accordance with federal laws in Brazil. Collecting permits of holotype and four of
paratypes were provided by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio; Permit
numbers 14858–2 and 42270–1).
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APPENDIX. Material examined.
Countries are given in bold capitals, states in upper capitals, municipalities in italics, and localities in plain text.
Bothrops alcatraz (n = 8). BRAZIL: SÃO PAULO: São Sebastião, Ilha dos Alcatrazes (IBSP 13031, 13126, 13183,
55578, 56133, 61853; MZUSP 1453, 21640).
Bothrops insularis (n = 26). BRAZIL: SÃO PAULO: Itanhaém: Ilha da Queimada Grande (IBSP 666, 683, 686, 1731,
1857, 1866, 1871, 1881, 1888, 1890, 1892, 1900, 1911, 1925, 1928–29, 1932, 1939, 1944, 1946, 1967–68, 1970, 1975, 1984,
Bothrops jararaca (n = 154). BRAZIL: ESPÍRITO SANTO: Alfredo Chaves: Vila Nova Maravilha (MBML 1921);
Anchieta (MBML 2272); Aracruz (MBML 468); Cariacica: Pitanga (MBML 1918); Domingos Martins: São Paulinho do
Aracê (MBML 1716); Fundão (MBML 502); Guarapari (MBML 2005); Sítio Modesto, Lameirão (MBML 1769); Ibiraçu:
Fazenda Morro das Palmas, Picuan (MBML 2900); Ibitirama: Pedra Rocha, Parque Estadual do Caparaó (MBML 1770, 1777,
1779); Itarana: Barra do Sossego (MBML 1691), Centro (MBML 716), Córrego Penedo (MBML 2101), Limoeiro de Santo
Antônio (MBML 2850); Linhares (MBML 1788; MZUSP 4448), Reserva Biológica de Sooretama (MBML 2124, 2127),
Reserva Florestal da CVRD (MZUSP 5865; ZUEC 1788); Marechal Floriano (MBML 732), Sítio Amarildo (MBML 1985),
Sítio Três Marias (MBML 733–35, 752, 791–94, 1791), Sítio Zamprogno (MBML 1771, 1790); Nanuque (MZUSP 4459);
PARNA Caparaó: (MZUSP 14401); Santa Leopoldina (MZUSP 1491; ZUEC 1189–90), Encantado (MBML 280), Rio da Prata
(MBML 341, 346), Santo Antônio (MBML 381–83, 417, 458); Santa Maria de Jetibá (MBML 156; MZUSP 13171), Baixo
Rio Posmauser (MBML 1980), Rio Nove (MBML 397, 429, 451–53); Santa Teresa: (MZUSP 5114), Aparecidinha (MBML
49, 1281, 2015), road to Santa Lucia (MBML 485), Goiapaba Açu (MBML 865–66), Museu Biológico Mello Leitão (MBML
469), Patrimônio de Santo Antônio (MBML 446, 474), Rio Bonito (MBML 1233–34, 1138), São Lourenço (MBML 85, 563),
Sítio Duas Águas, Valão de São Pedro (MBML 720), Sítio Max Loureiro Penha (MBML 497); Vale de São Pedro (MBML
2848), Valsugana Velha (MBML 1277); Serra: Centro Industrial de Vitória (ZUEC 543), Lagoa Humaitá, Carapebus (MBML
1925), Sítio Gasparini, Carapebus (MBML 550, 1776, 1926–27); Vila Velha: Barra do Jacu (MBML 2014); Vitória (MBML
1772), Fonte Grande (MBML 2215), Restinga do Camburi (MBML 1917), Viveiro de Mudas da CST (MBML 1916);
PARANÁ: Castro (UFRGS 1377); Colônia Ouro Verde (UFRGS 1845); Cruz Machado (UFRGS 1694); Mallet (UFRGS
1640); Moreira Sales (UFRGS 1769); Palmas (UFRGS 1367, 1632); Porto União (UFRGS 1828); Porto União da Vitória
(UFRGS 1687–88, 1697, 1699, 1739, 1825, 1837); Rio Azul (UFRGS 1767); União da Vitória (UFRGS 1390, 1829, 1851,
1853); Valões (UFRGS 1827, 1849); Vera Guarani (UFRGS 1711); RIO GRANDE DO SUL: Campo Bom (UFRGS 219);
Canela (UFRGS 1764); Carlos Barbosa (UFRGS 1368); Caxias do Sul (UFRGS 1702); Erechim (UFRGS 1631); Gramado
(UFRGS 1373); Gravataí (UFRGS 1461); São Leopoldo (UFRGS 1463); Torres (UFRGS 1755); Viamão (UFRGS 1751); SÃO
PAULO: Bertioga (MZUSP 4637, 12382), Guaratuba (MZUSP 7324–25); Guarujá (MZUSP 3583–84); Iguape: Barra do
Ribeira (MZUSP 4062–63); Ilhabela (MZUSP 4054); Juquitiba (MZUSP 12770–71); Miracatu (MZUSP 12107); Mogi das
Cruzes (MZUSP 2265); Peruíbe (MZUSP 12852); Salesópolis: Estação Biológica de Boraceia (MZUSP 4466–68, 4883–84,
11576); Santo André: PNMN Paranapiacaba (MZUSP 17938); São José do Barreiro: Serra da Bocaina (MZUSP 4910); São
Miguel Arcanjo: Parque Estadual Carlos Botelho (MZUSP 15241–42, 17202); São Sebastião (MZUSP 1403–04), Barra do Una
(MZUSP 13167), Praia do Engenho (MZUSP 15137), Praia de Juquehy (MZUSP 12819); SANTA CATARINA: Canoinhas
Zootaxa 4097 (4) © 2016 Magnolia Press
(UFRGS 1846); Criciuma (UFRGS 1453); Garopaba (UFRGS 3487); Itaiopolis (UFRGS 1830); Lucerna (UFRGS 1710);
Porto Belo (UFRGS 239); São Bento do Sul (UFRGS 1884, 1895); São Domingos (UFRGS 6529).
Bothrops otavioi (n = 31). BRAZIL: SÃO PAULO: Ilhabela municipality-archipelago: Ilha da Vitória (IBSP 18866–69,
18871–82, 78572 holotype); MZUSP 3949, 3951–52, 5577–85; ZUEC 3550–51).
Bothrops sazimai (n = 34). BRAZIL: ESPÍRITO SANTO: Itapemirim: Ilha dos Franceses: IBSP 86676–77 (females),
MBML 3318 (male with everted hemipenis), MBML 3324–25 (females), MBML 3326–27 (males), MZUSP 22285–87
(females), MZUSP 22288 (male with everted hemipenis), MZUSP 22289 (males), MZUSP 22290 (female), MZUSP 22291–92
(males), MZUSP 22293 (female), MZUSP 22294 (male with everted hemipenis), MZUSP 22295–96 (females), MZUSP 22297
(male), MZUSP 22298–99 (females), MZUSP 22300 (male), MZUSP 22534–39 (females), MZUSP 22540–43 (males),
MZUSP 22544 (female). The following nine specimens were only measured and photographed in the field, but not collected:
RJS 5001 (male), RJS 5002 (male), RJS 5003 (female), RJS 5004 (female), RJS 5007 (male), JMF 39 (male), JMF 40 (female),
JMF 42–43
... Carrasco et al., 2012), composed of 46 currently recognized species that inhabit a wide variety of ecosystems in Central and South America (Dal Vechio et al. 2021;Uetz et al., 2021). Nevertheless, insular diversity in Bothrops is mainly concentrated within the B. jararaca species group (Barbo et al., 2012(Barbo et al., , 2016Marques et al., 2002), which consists of five species, the mainland B. jararacaa common inhabitant of BAF (Sazima, 1992) and four insular species from the southeastern Brazilian coast. Three of these insular species occur in the state of São Paulo, as follows: B. alcatraz Marques et al., 2002, from Ilha dos Alcatrazes; B. insularis Amaral, 1921, from Ilha da Queimada Grande; and B. otavioi Barbo et al., 2012, from Ilha da Vit oria. ...
... Three of these insular species occur in the state of São Paulo, as follows: B. alcatraz Marques et al., 2002, from Ilha dos Alcatrazes; B. insularis Amaral, 1921, from Ilha da Queimada Grande; and B. otavioi Barbo et al., 2012, from Ilha da Vit oria. The fourth and most recently described species, B. sazimai Barbo et al., 2016, is endemic to Ilha dos Franceses, in the Brazilian state of Esp ırito Santo. Although several other insular populations of lanceheads occur on different islands in southern and southeastern Brazilian coast, they are commonly considered as falling within the phenotypic range described for the mainland B. jararaca without proper analysis of morphological distinctiveness (Cicchi et al., 2007). ...
... Previous research suggests that speciation events related to the origin of insular species of the Bothrops jararaca group were a direct consequence of the sea level oscillations during the Pleistocene/Holocene transition (Barbo et al., 2012(Barbo et al., , 2016Grazziotin et al., 2006;Marques et al., 2002). Considering the proposed scenario of extremely recent peripatric speciation on the Brazilian continental islandssmall insular populations recently isolated from a larger continental ancestral populationthe expected phylogenetic relationship among insular and continental populations is of insular species nested inside the mainland diversity due to incomplete lineage sorting (ILS) (Avise, 2000;Funk & Omland, 2003). ...
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Brazilian continental islands represent a natural laboratory to study speciation driven by recent phenotypic and genotypic divergence. The Bothrops jararaca species group is distributed in the Brazilian Atlantic Forest and on most of the Brazilian continental islands. The group is currently composed of the mainland common lancehead (B. jararaca) and four insular species (B. alcatraz, B. insularis, B. otavioi, and B. sazimai). Here, we evaluate mitochondrial DNA and morphological diversity of the B. jararaca species group and aim to provide additional evidence to understand insularization processes on the Brazilian coast. Our results, interpreted together with a comprehensive review of geomorphological data, provide a new conceptual framework for understanding the colonization process of the Brazilian continental islands. This framework suggests a history of multiple rounds of periodic isolation and reconnection between insular populations and their mainland relatives throughout the last 420,000 years. Furthermore, although some insular populations may have speciated prior to the last glacial maximum, other species likely diverged within the last 11,000 years. Additionally, the repeated evolution of size and dietary shift in the B. jararaca species group suggests a remarkable case of convergent adaptation. Our study provides evidence that the Bothrops from Ilha da Moela (Brazilian state of São Paulo) represents an undescribed species, presenting a distinct phenotype, and an exclusive history of isolation and adaptation. We describe this unique lancehead as a new species and we suggest it should be listed as critically endangered based on its endemicity to a small island that is severely impacted by constant and longstanding human presence.
... Experiments on naturally blind snakes or those partially deprived of vision have shown that biological traits and behaviors, such as body condition, prey capturing rate, and finding sexual partners are seldom affected by poor or lack of vision (Bonnet et al., 1999;Young & Morain, 2002), which indicate that the size of the eye per se may not undergo strong natural selection in adults. Additionally, Bothrops sazimai (Viperidae), an insular species closely related to B. jararaca, have relatively larger eyes than the B. jararaca population and are more efficient to detect their ectothermic prey, such as centipedes and lizards (Barbo et al., 2016). In this sense, eye size is probably more variable in juvenile B. jararaca, as ectothermic prey are more frequently found in their diet at this stage. ...
The common lancehead Bothrops jararaca is widespread in the Atlantic Forest in Brazil. The species is known to show a marked sexual dimorphism pattern, with the female being larger than the male. However, most efforts in clarifying morphological variation between the sexes are often focused on a single population. In this paper, we investigate how sexual dimorphism and ontogenetic trajectories vary among populations as well as the ontogenetic trajectories of B. jararaca. We analyzed 211 specimens from a coastal and a highland population and measured 17 morphological traits, including linear and meristic characteristics, and the analysis revealed a clear but variable effect of sex and population. Females were larger than males in all evaluated populations. Furthermore, females in the coastal population were generally smaller than in the highland population but had significantly more scales. Widespread species often experience differential environmental pressures even in terms of biotic and abiotic factors. We attribute the results found herein to specificities in prey availability and climatic conditions which affect the ontogenetic pattern between the sexes and the populations, resulting in specific sexual dimorphism patterns.
... Dorsal rows of anterior (one head length behind the head), middle, and posterior (one head length in front of the vent) portions of the body were counted. The evaluation of cephalic scales followed the scheme of Barbo et al. (2012Barbo et al. ( , 2016 for the B. jararaca group. We counted the intersupraoculars (anterior, middle, and posterior lines of scales between supraoculars), interrictals (line of scales above the head that link the last supralabials), and gulars (line of scales contacting posterior chin shields and first ventral). ...
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Here we describe a new species of Lancehead (Bothrops jabrensis sp. nov.) based on three individuals sampled from a previously unknown population from Pico do Jabre, an isolated and small Caatinga moist-forest enclave (CMFE) located in northeastern Brazil. Although this new species has an external morphology resembling those found in representatives of the Bothrops jararaca (Wied-Neuwied, 1824) species group, B. jabrensis can be diagnosed by a combination of meristic and color characters. Molecular phylogenetic analysis indicates the new species represents a unique and highly divergent lineage within Bothrops revealing the existence of a previously unknown phylogenetic lineage that has been evolving as an independent unit for more than 8 million years. Additionally, the estimated divergence time of this lineage conflicts with some proposed scenarios of historical processes associated with the evolution of CMFEs. Finally, the uniqueness of this species indicates its relevance for the maintenance of the phylogenetic diversity of Lanceheads in South America. Like other CMFEs, Pico do Jabre is consistently threatened by poaching, illegal fires, deforestation for agricultural purposes, and illegal logging. The restricted distribution of B. jabrensis, in a small and disturbed CMFE, strongly suggests that this species is critically endangered and is likely approaching extinction as a natural population.
... Finally, Hamdan et al. (2019) showed that the species previously known as Bothrops lojanus should be assigned to the genus Bothrocophias. Barbo et al. (2012Barbo et al. ( , 2016 described two island species of Bothrops, B. otavioi and B. sazimai, from Vitória Island, São Paulo State, and Ilha dos Franceses, Espírito Santo State, Brazil, respectively, using morphological and ecological data. mtDNA sequences show both species to be recent derivatives of the widespread mainland species B. jararaca. ...
... Venomous snakes in the genus Bothrops Wagler 1824 (family Viperidae) have been the focus of several phylogenetic and diversification studies over recent years (Wüster et al. 2008;Fenwick et al. 2009;Carrasco et al. 2012;Alencar et al. 2016), with an equally active taxonomy revelling unrecognised diversity at the species level (Ferrarezzi and Freire 2001;Marques et al. 2002;Da Silva and Rodrigues 2008;Folleco-Fernández 2010;Barbo et al. 2012Barbo et al. , 2016Carrasco et al. 2019;Timms et al. 2019). Despite these efforts, conflicting topologies, taxonomic uncertainty, and underestimation of species diversity persist (Machado et al. 2014;Dal Vechio et al. 2018. ...
Recent genetic studies have found unclear species boundaries and evidence of undescribed diversity in the poorly studied jararacussu species group within Bothrops. In this contribution, we investigate phenotypic and genetic diversity in the Amazonian snake Bothrops brazili to test previous assertions of unrecognised species diversity within this taxon. Our phylogenetic results and inferences of independently evolving lineages based on molecular data recover two divergent clades within B. brazili, one restricted to areas north and another to areas south of the Amazon River. Phylogenetic relationships between these lineages and other species in the jararacussu species group reveal B. brazili to be paraphyletic, with the northern clade inferred as sister to a clade composed of Atlantic Forest taxa (B. jararacussu, B. muriciensis, B. pirajai). External morphology (number of ventral and subcaudal scales) and colouration patterns (lateral trapezoidal marks) consistently separate the two lineages of B. brazili. We therefore recognise and describe the northern lineage as a new species of Bothrops, improving our knowledge of species diversity within a medically important clade of venomous South American snakes.
... Because sampling effort has been concentrated in the center-south of the Atlantic Forest (Figueiredo et al. 2017;Lima et al. 2017;Muylaert et al. 2017;Hasui et al. 2018;Vancine et al. 2018), it is not surprising that many newly described species were based on newly collected individuals from the northeast. (Buzzetti et al. 2013;Quintela et al. 2014Quintela et al. , 2017, coastal sandy plains (Tavares et al. 2011;Cardozo et al. 2018), and coastal islands (Barbo et al. 2012(Barbo et al. , 2016. ...
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The Atlantic Forest is a heterogeneous and complex vegetation mosaic caused by variety of climatic, geomorphological, and edaphic conditions. It has long been known that the Atlantic Forest has one of the most diversified biotas on the planet, presenting high levels of endemism. Here, we update the knowledge regarding terrestrial vertebrates occurring in the Atlantic Forest, focusing on endemic species and presenting its main spatial patterns of diversity. We also analyzed the main knowledge gaps associated with these species. We identified 2,645 species of Tetrapoda in the Atlantic Forest, being 719 species of amphibians, 517 species of reptiles, 1,025 species of birds, and 384 species of mammals. The uniqueness of its fauna is impressive even in a global scale, as 2.8% of the world’s Tetrapoda species occurs only in the Atlantic Forest. For reptiles, this percentage is 1.3%, while for both birds and mammals, it hovers around 1.9%, but for amphibians, it reaches an impressive 6.6%. Spatially, most groups exhibit their highest species richness at the core of the Atlantic Forest, and this pattern becomes more evident when only endemic species are considered. Even with all its impressive diversity, 157 new Tetrapoda species were described in the Atlantic Forest in the last decade, mostly from poorly sampled regions or environments. An increase of sampling effort on these regions might increase the number of species on this biome, which already is one of the most diverse in the world.
... According to Hausdorf (2002), "islands are considered areas of endemism in most empirical studies without an explicit analysis of distribution patterns", but this statement denotes problems in their conceptual definition, because the delimitation of such an area of endemism is based on the origin of species, if by vicariance or dispersal, and not on the occurrence of sympatric ranges. Thus, since Hausdorf (2002): "the delimitation of areas of endemism becomes problematic when dispersal occurs".Except for a few large lizards, reptiles in general are not able to disperse for long distances over the sea (~30 km), and therefore, the most plausible hypothesis of their occurrence in coastal islands is after allopatric speciation from vicariant events, after the rise of the sea level in the late Pleistocene, fragmenting coastal populations and generating insular biotas(Marques, Martins & Sazima, 2002;Barbo et al., 2012Barbo et al., , 2016. Two other island species of viperid snakes recorded in AF, Bothrops insularis and B. sazimai, were considered as 'noise components' in Biotic Element analysis as they are not found in sympatry with other AF endemics, probably because of the small size of our grid cells, that made their distribution distant and disjunct from other endemic snakes. ...
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Aim Vicariance has often been invoked to explain bioregionalization patterns in the Neotropics. Using a revised point locality data for endemic species, we aimed to test for the first time the predictions of the vicariance model in shaping biogeographical regions for endemic snakes in the Atlantic Forest (AF) megadiverse hotspot. Location South American Atlantic Forest. Taxon Snakes (Reptilia, Serpentes). Methods To identify the non‐random groups of co‐distributed species, we mapped 21,101 point locality records in a grid cell of 0.5° × 0.5° across the AF, and constructed a presence–absence matrix of endemic species. The two major predictions of vicariance model were tested by Biotic Elements (BE) analysis, searching for groups of significantly co‐distributed species (Biotic Elements) by comparing distances between observed and artificial random ranges, produced under null models from Monte Carlo simulations. We also tested for the occurrence of sister species in different Biotic Elements, and compared our results with previous bioregionalization schemes revealed by other organisms in the AF. Results We recorded 252 species of snakes in the Atlantic Forest, of which 79 (31%) are endemic to this domain. Biotic Elements analysis with endemic species revealed seven clusters of co‐distributed species (BEs) corresponding to biogeographical regions. The significant non‐random clusters of geographical ranges revealed in BE analysis, and the distribution of sister species in different BEs, validated both central predictions of the vicariance model. Main conclusions Snakes defined non‐random biogeographical regions in the Atlantic Forest, and these were congruent with previously identified areas based on other groups of organisms, indicating that general processes influenced geographical ranges across the region. Both central predictions of the vicariance model were valid, indicating that vicariant events must have been important in shaping non‐random clusters of co‐distributed snakes in this biodiversity hotspot, harbouring some of the richest snake faunas on the planet.
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Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called ‘island rule’ provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic meta-analysis to assess patterns and drivers of body size evolution across a global sample of paired island–mainland populations of terrestrial vertebrates. We show that ‘island rule’ effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions.
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Popular species names have always been based on human relationships with things around them, usually reflecting species' external morphology , behavior or even the habitat they inhabit. In Brazil, the high number of popular names, in many cases for the same species, makes it difficult to comprehensively recognize these names, hampering communication between everyone interested in reptiles. This study presents a compilation of the popular names for the species of reptiles occurring in Brazil based on literature data. We listed 1264 popular names, 25 for Amphisbaenia, 29 for Crocodylia, 137 for Testudines, 301 for "Lizards" and 772 for Snakes. All Testudines and
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Introduction, The existence of evolutionary trade-offs prevents simultaneous optimization of different functions that require opposing biomechanical or physiological adaptations (Stearns, 1992). Consequently, trade-offs likely play an important role in niche partitioning, in that species specialized in exploiting one type of niche (e.g. microhabitat) are expected to be less proficient at exploiting others. For instance, in Anolis lizards, a trade-off exists between sprint speed and sure-footedness because long limbs are required to move fast, whereas short limbs aid sure-footedness (Losos and Sinervo, 1989; Losos and Irschick, 1996). Accordingly, species that predominantly move on broad surfaces (i.e. trunk–ground ecomorph) specialize for speed and have long limbs, whereas species living on narrow substrates (i.e. twig ecomorph) are specialized in slower but secure movements. In a similar fashion, species specializing in different dietary niches may have diverged morphologically because the biomechanical demands on the feeding and/or locomotor apparatus are often not reconcilable within one phenotype. Clearly, the ability of a predator to exploit a certain prey type will depend on the functional characteristics of the prey (e.g. prey distribution, hardness, and escape response) and the performance of the feeding and locomotor system of the predator. For instance, in labrid fishes the amount of force potentially generated by the jaws trades off with the speed of jaw movement because of differences in the four-bar linkage system of the jaws and hyoid (long links aid high force outputs, but rapid movements are realized by short links) (Westneat, 1994, 1995). é Cambridge University Press 2007.
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Abstract It is a well-known phenomenon that islands can support populations of gigantic or dwarf forms of mainland conspecifics, but the variety of explanatory hypotheses for this phenomenon have been difficult to disentangle. The highly venomous Australian tiger snakes (genus Notechis) represent a well-known and extreme example of insular body size variation. They are of special interest because there are multiple populations of dwarfs and giants and the age of the islands and thus the age of the tiger snake populations are known from detailed sea level studies. Most are 5000–7000 years old and all are less than 10,000 years old. Here we discriminate between two competing hypotheses with a molecular phylogeography dataset comprising approximately 4800 bp of mtDNA and demonstrate that populations of island dwarfs and giants have evolved five times independently. In each case the closest relatives of the giant or dwarf populations are mainland tiger snakes, and in four of the five cases, the closest relatives are also the most geographically proximate mainland tiger snakes. Moreover, these body size shifts have evolved extremely rapidly and this is reflected in the genetic divergence between island body size variants and mainland snakes. Within south eastern Australia, where populations of island giants, populations of island dwarfs, and mainland tiger snakes all occur, the maximum genetic divergence is only 0.38%. Dwarf tiger snakes are restricted to prey items that are much smaller than the prey items of mainland tiger snakes and giant tiger snakes are restricted to seasonally available prey items that are up three times larger than the prey items of mainland tiger snakes. We support the hypotheses that these body size shifts are due to strong selection imposed by the size of available prey items, rather than shared evolutionary history, and our results are consistent with the notion that adaptive plasticity also has played an important role in body size shifts. We suggest that plasticity displayed early on in the occupation of these new islands provided the flexibility necessary as the island's available prey items became more depauperate, but once the size range of available prey items was reduced, strong natural selection followed by genetic assimilation worked to optimize snake body size. The rate of body size divergence in haldanes is similar for dwarfs (hg= 0.0010) and giants (hg= 0.0020- 0.0025) and is in line with other studies of rapid evolution. Our data provide strong evidence for rapid and repeated morphological divergence in the wild due to similar selective pressures acting in different directions.
The Quaternary Period has a very short duration in the Earth's history, but it is the most important because it represents the time interval in which we live. It is one of the most studied and known chapters or, perhaps, just for this, many are the doubts about the evolutionary history of the Earth during this period. Multiple aspects related to the "reconstruction of the ancient sea levels during the Quaternary" are here focused. The relative sea level fluctuations are produced by true variations of the sea level (eustasy) and by changes in the land level (tectonism and isostasy). So, sea level in a certain point of the coast is represented by an "instantaneous" resultant of complex interactions between the surfaces of ocean and continent. The changes of the relative sea levels are reconstructed through several evidence of these fluctuations, which must be recognized in time and space. To define their situation in space is necessary to know their present altitude in relation to their original altitude, that is, to determine their position in relation to the sea level during their formation or sedimentation. Their situation in time is determined by measuring the moment of their formation or sedimentation, using for this the dating methods (isotopic, archeological , etc.). When numerous ancient sea levels could be reconstructed, spreaded through a considerable time interval, is possible to delineate the sea level fluctuation curve for this period.
The insular body size trends for different vertebrate families are compared. Certain groups such as lagomorphs, bats, artiodactyls, elephants, foxes, raccoons, snakes, and teiid and lacertid lizards are habitually represented by relatively smaller forms on islands. On the other hand, cricetid rodents, iguanid lizards, tortoises, and bears often have races with larger body sizes on islands. Contrary to conventional niche theoretic concepts, in many instances knowledge of the body sizes of some of these animals' insular and mainland competitors does not help explain the difference in that species body size in the 2 places. To account for these divergent size changes I examine optimum body size models that use as the optimization criterion the net energy gained by an organism over a given time period. These models predict that increases in the mean amount of available food should lead to evolutionary increases in body size, but only if body size is not tightly constrained by additional physical or biotic factors: such additional factors might be important if a change in body size alters an animal's effectiveness in finding or handling preferred food items or increases competition with its neighbors. Next using arguments derived from simple non-age-structured 2 species predator-prey models, the availability of food for a given consumer species at equilibrium is compared in theoretical island and mainland situations. Because islands usually contain fewer competitors and the insular physical environment is often more moderate, food availability for colonists is initially expected to be high. On the other hand, as the population grows resources will become depleted. Further, the loss of many predator species on islands may allow consumer densities to increase to such an extent that at equilibrium food may become relatively more limiting for consumers on islands than on the mainland. Whether the supply to demand ratio (S:D) of consumers for their food is ultimately greater or lower will depend on the relative magnitude of these various factors. Within this framework, a necessary condition for island S:D ratios to be greater than on the mainland is that the consumers maintain individual feeding territories. For animals whose body sizes are not tightly bound within narrow limits by physical or competitive restraints, an increase in S:D should lead to an evolutionary increase in body size. Accordingly, a good association is found between the presence or absence of territoriality and the direction of the insular body size shift in a number of different vertebrate groups. Yet there are exceptions which fall into 2 categories: First, if a species' mainland predators preferentially take larger individuals, selection favoring small size may override selection based on optimizing energy input. Such may have been the case for the now extinct mainland relatives of certain giant relictual insular reptiles. Secondly, an animal's body size may be tightly constrained by physical or competitive factors. The body size of island foxes, rattlesnakes, and some lizards appears to be primarily adjusted to the competitive milieu along typical niche theoretic lines. That is, body size may be predicted quite well from knowing the size class of competitors which are absent from an island or from differences in the species' prey-size distribution between island and mainland sites.