September 2002] HERPETOLOGICA 303

Herpetologica, 58(3), 2002, 303–312

q 2002 by The Herpetologists’ League, Inc.

A NEW INSULAR SPECIES OF PITVIPER FROM BRAZIL, WITH

COMMENTS ON EVOLUTIONARY BIOLOGY AND
CONSERVATION OF THE BOTHROPS JARARACA GROUP
(SERPENTES, VIPERIDAE)
OTAVIO A. V. MARQUES1, MARCIO MARTINS2,4, AND IVAN SAZIMA3
1
Laboratório de Herpetologia, Instituto Butantan, 05535-900 São Paulo SP, Brazil
2
Departamento de Ecologia, Instituto de Biociências, C. P. 11461, Universidade de São Paulo, 05422-970
São Paulo SP, Brazil
3
Departamento de Zoologia and Museu de História Natural, C. P. 6109, Universidade Estadual de
Campinas, 13083-970 Campinas SP, Brazil

ABSTRACT: We describe a new pitviper species, Bothrops alcatraz, of the Bothrops jararaca
group, from Alcatrazes Island, off the coast of São Paulo, southeastern Brazil. It differs from the
mainland coastal populations of B. jararaca in southeastern Brazil mostly by its darker coloration;
smaller size; lower number of ventrals, subcaudals, and infralabials; number and shape of anterior
cephalic scales; shape of hemipenis spines; intense coagulant activity of venom; and three specific
venom proteins. From Bothrops insularis, another island species from southeastern Brazil, the new
species differs mainly by its color pattern, smaller size, lower number of subcaudals in males, and
absence of hemiclitoris in females. Bothrops alcatraz presents some features that may be viewed as
paedomorphic within the B. jararaca group, such as small adult size, proportionally large eyes,
intense coagulant venom activity, and diet composed of centipedes and lizards. We postulate that
the dwarfism and characteristics of venom in B. alcatraz may be related to its diet (similar to that
of juveniles of the mainland B. jararaca). Bothrops alcatraz and B. insularis may have originated
through the isolation of populations of a B. jararaca-like ancestor on the Alcatrazes and Queimada
Grande islands, respectively. The new species is regarded as critically endangered due to its very
small area of occurrence and the declining quality of its habitat.
Key words: Bothrops alcatraz; Crotalinae; Evolution; Island endemics; Natural history; South-
eastern Brazil

THE SYSTEMATICS of snakes of the genus and Lamar, 1989; Hoge and Romano-
Bothrops is notoriously difficult (Campbell Hoge, 1981; Werman, 1992), although sev-
eral species groups have been recognized
4
CORRESPONDENCE: e-mail, jararaca@ib.usp.br recently (Cadle, 1992; Gutberlet, 1998;
304 HERPETOLOGICA [Vol. 58, No. 3

Salomão et al., 1997, 1999; Werman, and Museu de História Natural da Univ-
1992). The genus is probably paraphyletic ersidade Estadual de Campinas (ZUEC).
(see Gutberlet, 1998; Parkinson, 1999), For each snake, we measured the snout–
and comprises about 40 species including vent length (SVL) and tail length (TL) to
those previously allocated in Bothriopsis the nearest 1 mm with a flexible rule.
(Gutberlet, 1998; Parkinson, 1999; Salo- Head length (HL; from snout to extreme
mão et al., 1997, 1999; Vidal et al., 1999). posterior part of mandible) and eye di-
Members of two groups of Bothrops oc- ameter (ED) were measured with a caliper
cur on coastal islands on southeastern Bra- to the nearest 0.1 mm; to compare HL and
zil. Snakes related to Bothrops jararaca ED between species, we divided HL by
(Wied), including Bothrops insularis the ‘‘trunk’’ length (TR 5 SVL 2 HL) and
(Amaral), are known from several islands ED by HL. Mass (to the nearest 1 g) was
of various sizes and distances from the obtained with spring scales after draining
coast (up to about 35 km), ranging from the excess preservative liquid through ven-
Franceses Island off Espı́rito Santo (lati- tral incisions; to compare mass between
tude about 218 009 S) south to Santa Ca- species, we divided mass by total length
tarina Island (latitude about 278 309 S), (TTL). Description and scale counts follow
whereas Bothrops jararacussu (Lacerda) is Campbell (1985). We considered the first
more restricted in its distribution and oc- ventral as being the first scale wider than
curs mainly on larger islands close to the long. Additionally, we counted the anterior
coast of São Paulo (,1 km from the main- cephalic scales (i.e., the total number of
land; Amaral, 1921a; Duarte et al., 1995; cephalic scales, including the intersupra-
Luederwaldt and Fonseca, 1923; personal oculars) to the tip of the snout. Hemipen-
observation). Island populations of snakes ial ornamentation names follow Dowling
are good subjects for evolutionary studies, and Savage (1960). Color names follow
especially when compared to their gener- Kornerup and Wanscher (1961). Data for
ally widespread mainland relatives (e.g., B. insularis in Table 1 are from Amaral
Forsman, 1991; Schwaner, 1985). These (1921a). Data on microhabitat use, feed-
populations also deserve special attention ing, and reproduction were obtained dur-
for conservation as they generally occur ing fieldwork and by examining preserved
exclusively in very restricted areas (e.g., 43 specimens in museum collections.
ha in the case of B. insularis, Duarte et al., The population of pitvipers inhabiting
1995). Alcatrazes Island is well differentiated
The B. jararaca group comprises two from both populations of snakes occurring
species (Salomão et al., 1999), the wide- in Queimada Grande Island (B. insularis)
spread B. jararaca, probably a complex of and on adjacent mainland (B. jararaca).
several species (Salomão et al., 1997), and After carefully analyzing the morphologi-
the insular endemic B. insularis. The latter cal and ecological attributes of the Alca-
species is restricted to Queimada Grande trazes pitviper, we concluded that the Al-
Island, off the coast of São Paulo, south- catrazes Island population represents a
eastern Brazil (Campbell and Lamar, distinctive species that may be known as:
1989). Herein, we describe a second in-
sular pitviper species from Brazil, first col- Bothrops alcatraz sp. nov.
lected in 1914 and previously referred to Holotype.—IB 62545 (Fig. 1), male
the widespread species B. jararaca (e.g., from Alcatrazes Island (248 069 S, 458 429
Luederwaldt and Fonseca, 1923). W), São Sebastião, São Paulo State, Brazil,
15 December 1999, collected by O. A. V.
MATERIALS AND METHODS Marques, M. Martins, M. E. Oliveira, D.
We examined 24 specimens of the new N. Pereira and A. Martensen.
insular species and 39 specimens of B. ja- Paratypes.—Eighteen specimens, all
raraca from adjacent continental popula- from the type locality: MZUSP 1453, Oc-
tions of coastal São Paulo (Appendix I) in tober 1920, collected by H. Luederwaldt;
the collection of Instituto Butantan (IB) ZUEC 2224, male, 22 March 2000, col-
September 2002] HERPETOLOGICA 305

FIG. 1.—Bothrops alcatraz type locality and two specimens in situ. Alcatrazes Island photographed from a
nearby islet with two brown boobies in foreground (upper left); the Atlantic forest on Alcatrazes Island (upper
right); holotype (IB 62545), showing gaping behavior and seabird droppings on the head (lower left); male
(IB 62290) showing body proportions, dorsal pattern, and seabird droppings scattered on the adjacent ground
(lower right). Photos of the island by F. P. de Campos.

lected by M. Martins, R. Sawaya, M. E. Martins, M. E. Oliveira, D. N. Pereira,

Oliveira, D. N. Pereira, A. Martensen and and A. Martensen.
O. A. V. Marques; ZUEC 2225, female, 24 Referred specimens.—Six specimens
March 2000, collected by O. A. V. from the type locality: IB 13031 male, IB
Marques; IB 584 male, IB 585 female, IB 13126 male, and IB 13183 female, Feb-
586 female, IB 587 female, and IB 588 ruary 1950, Instituto Butantan expedition
female, June 1914, collected by A. A. Go- coll.; IB 55578 male, December 1992, W.
mes; IB 13032, female, February 1950, Langeani coll.; IB 55581 male, 24 January
collected by Instituto Butantan expedition; 1992, W. Langeani coll.; IB 56133 female,
IB 13135 female, 1950, collected by Insti- 1994, Instituto Butantan expedition coll.
tuto Butantan expedition; IB 16211 and IB Diagnosis.—The new species is super-
16212 both females, 7 January 1955, col- ficially similar to B. jararaca from coastal
lected by F. Witaker; IB 55579 male, 14 São Paulo, from which it may be distin-
December 1992, collected by W. Lan- guished by the following combination of
geani; IB 55580, female, April 1992, col- characters (B. jararaca in parentheses):
lected by M. Buononato; IB 55791 male, smaller adult size, mean male TTL 425.6
16 April 1994, collected by A. Eterovic; IB 6 32.5, range 365–462 mm (versus 801.6
57105, male, 2 December 1996, collected 6 107.6 mm, range 378–924 mm); mean
by S. Sant’anna; IB 57107, female, 17 June female TTL 455.7 6 41.4, range 365–505
1994, collected by Instituto Butantan ex- mm (versus 969.0 6 107.1, range 337–
pedition; IB 62238, female, 15 December 1080 mm); shorter tail, TL/SVL 0.161 6
1999, collected by O. A. V. Marques, M. 0.007 (0.168 6 0.009) in males, 0.138 6
306 HERPETOLOGICA [Vol. 58, No. 3

FIG. 2.—Heads of Bothrops alcatraz (paratypes IB 587 and IB 585, upper) and Bothrops jararaca (IB
57903 and IB 58130, lower) in dorsal view showing variation in scalation. Line 5 5 mm.

0.011 (0.144 6 0.012) in females; longer three venom proteins with molecular
head, HL/TR 0.0053 6 0.0003 (0.0041 6 weights of 20, 40, and 60 kD, which do
0.0002) in males, 0.0055 6 0.0003 (0.0045 not occur in B. jararaca, and the intense
6 0.0010) in females; larger eyes, ED/HL coagulant activity of venom of adult B. al-
0.157 6 0.010 (0.149 6 0.010) in males, catraz (M. F. D. Furtado, personal com-
0.154 6 0.009 (0.126 6 0.022) in females; munication), a character that occurs only
32–50, 37.5 6 4.2, anterior cephalic scales in juvenile B. jararaca (Furtado et al.,
generally rounded and with no or feeble 1991). From B. insularis, the new species
keels (32–64, 47.0 6 8.2, generally elon- is easily distinguished by color pattern and
gate and distinctly keeled, Fig. 2); lower smaller size (Campbell and Lamar, 1989:
number of infralabials usually 10/10 (usu- Figs. 214 and 215), and lower number of
ally 11/11); lower number of ventrals, 173– subcaudals in males (47–54 versus 55–65,
186 (197–218); lower number of subcaudal respectively). An additional diagnostic
scales in males 47–58 (62–72) and in fe- character of B. insularis is presence of the
males 45–52 (53–68) (Table 1), and hem- hemiclitoris (cf. Ziegler and Böhme, 1997)
ipenis spines relatively slender (stouter in in females. Furthermore, Bothrops alca-
B. jararaca) (Fig. 3). Additional characters traz is known only from Alcatrazes Island,
that distinguish B. alcatraz from B. jara- whereas B. insularis is known only from
raca are the presence in the former of Queimada Grande Island, and B. jararaca
September 2002] HERPETOLOGICA 307

TABLE 1.—Comparison of selected characters of Bothrops alcatraz, coastal specimens of B. jararaca, and B.
insularis. Measurements in mm, number of individuals in parentheses.

B. alcatraz B. jararaca* B. insularis**

Snout–vent length males 365–462 (10) 378–996 (15) 393–788 (94)

Snout–vent length females 365–505 (14) 320–1080 (24) 332–882 (106)
Ventrals males 173–182 (10) 200–211 (15) 171–188 (94)
Ventrals females 175–186 (14) 197–218 (19) 176–195 (106)
Subcaudals males 47–54 (10) 62–72 (15) 55–65 (94)
Subcaudals females 45–52 (14) 53–68 (19) 48–59 (106)
Mid-body scale rows 22–26 (24) 21–27 (34) 23–25 (200)
Intersupraoculars 6–8 (24) 7–10 (34) 7–9 (203)
Anterior cephalics 31–48 (24) 31–64 (34) —
Infralabials 10/10 (19); 10/11 (4); 10/10 (6); 10/11 (5); —
9/10 (1) 9/11 (1); 11/11 (15);
11/12 (4); 12/12 (2);
12/10 (1)
Hemipenial spines stout slender —
Postorbital stripe present present absent or faint
* From coastal São Paulo.
** Data from Amaral (1921a).

is a widespread species in southeastern mm, comprising 16.1% of total length; HL

Brazil, both on the mainland and on some 22.6 mm; maximum head width 15.1 mm;
larger islands close to the coast (Campbell mass 53 g (preserved); rostral scute 3.6
and Lamar 1989, personal observation). mm wide and 3.8 mm high; nasals divided
Etymology.—The specific epithet is a anterior and posterior to nostril; loreal sin-
noun in apposition and refers to the local gle; 3/3 prefoveals; 1/1 subfoveals; 1/1
name of the frigate bird, Fregata magni- post-foveals; prelacunal contacting the sec-
ficens (Pelecaniformes), whose colonies on ond supralabial on the right side of the
the Alcatrazes Island give name to the type head, fused with it on the left side; 1/1
locality of the new species. We suggest the suboculars; 2/2 preoculars; 2/2 postoculars;
common name ‘‘Alcatrazes lancehead’’ for 9/8 supralabials; 10/10 infralabials, first
the new species. pair in contact posteriorly; mental longer
Description of holotype.—An adult male than broad, contacting the first three in-
(Fig. 1) preserved in ethanol with both fralabials on each side; five gulars between
hemipenes everted; SVL 448 mm; TL 72 chin shields and first ventral; six rows of
gulars separating first ventral from infral-
abials; three anterior internasals; 2/2 can-
thals; 5 posterior intercanthals; 6 intersu-
praoculars; 34 cephalic scales with no or
feeble keels from mid level of the inter-
supraoculars to the tip of snout (Fig. 2);
25-25-19 dorsals; 177 ventrals; anal scute
single; 57 subcaudals (proximal 54 divided
and distal three undivided); five small
scales on each side of the cloaca; tail spine
three times as long as adjacent subcaudals,
dorsal scales covering anterior half of tail
spine.
Dorsal scales 2.5 times as long as wide
anteriorly, becoming wider posteriorly,
FIG. 3.—Asulcate side of right hemipenes of Both-
rops alcatraz (paratype ZUEC 2225, left) an Bothrops
about 1.5 times as long as wide on tail; all
jararaca (IB 62478, right) showing ornamentation. dorsal scales strongly keeled; paraventral
Line 5 5 mm. row of scales smooth to very weakly keeled
308 HERPETOLOGICA [Vol. 58, No. 3

on posterior part of body, parasubcaudals Atlantic forest covering Alcatrazes Island

noticeably keeled; paraventrals about twice (semi-arboreal habits are characteristic
as wide as adjacent dorsal scales; posterior within the B. jararaca group: see Martins
cephalic scales strongly keeled and longer et al., 2002); the holotype was found on
than wide; anterior cephalic scales round- the rocks of the wall of an old building
ed, smooth to weakly keeled; temporal (Fig. 1). Two individuals were resting by
scales keeled; internasals, canthals, and su- day, one within a decomposing palm trunk
praoculars smooth; scale row dorsal to su- and the other under a fallen palm leaf. Of
pralabials weakly keeled. 12 prey found in the guts of B. alcatraz,
Everted hemipenis subcylindrical, bi- nine were otostigmine centipedes (Otos-
lobed, extending to seventh subcaudal tigmus sp.) and three were lizards (two in-
scale; bifurcation of sulcus spermaticus at troduced gekkonid lizards, Hemidactylus
level of first subcaudal; sulcus extending to mabouia, and one scincid, Mabuya ma-
tip of each lobe; bifurcation of lobes at lev- crorhyncha). Centipedes and H. mabouia
el of second subcaudal scale; small to large are common on the low portions of tree
ossified spines assymetrically distributed and palm trunks, as well as on the walls of
on hemipenis extending from level of first old buildings. Most specimens of B. alca-
subcaudal; largest spines about the same traz were found under seabird (Sula leu-
length as adjacent subcaudal scales; lobes cogaster and Fregata magnificens) roosts
covered with high retiform ridges forming on the canopy of the low forest, where
papillate calyces (Fig. 3). large amounts of guano accumulate on the
Dorsum of head (in preservative) leaf litter (individuals of B. alcatraz are of-
brownish gray with diffuse dark olive- ten found with bird droppings splashed
brown markings. A prominent dark olive- over their body, Fig. 1). Cockroaches and
brown postorbital stripe extending from centipedes (which probably prey on the
behind the eye to below the angle of the former) are abundant on and around the
jaw, encroaching upon the posterior three guano. This is the only species of Bothrops
supralabials on the right side of head and known to feed mostly, if not exclusively, on
the posterior two scales on the left side; ectothermic prey (Martins et al., 2001).
this stripe bordered dorsally by a diffuse This prey type and the venom properties
pale brown zone. Canthal region and su- of B. alcatraz probably are related, as a
pralabials uniform gray. Iris grayish yellow relationship was found between the diet
with darker flecking. Body brown gray and venom composition for some Both-
with a series of 14 large, pale gray-edged, rops species and/or ontogenetic phases
dark olive-brown trapezoidal markings on (Andrade and Abe, 1999; Andrade et al.,
each side, with their apices on the verte- 1996; Furtado et al., 1991; M.F.D. Furta-
bral line; trapezoidal markings arranged do, personal communication). Curiously,
opposite each other, or partly or complete- despite preying on lizards, neither juve-
ly juxtaposed; the pale borders of dark niles (n 5 3) nor adults have whitish or
markings diffuse (Fig. 1). Tail dark brown otherwise conspicuous tail tips, a feature
dorsally. Venter pale yellowish gray with ir- present in all species of Bothrops known
regular brown blotching to flecking be- to prey on lizards or frogs, which are lured
coming more concentrated on tail. by the snake’s tail movements (Martins et
Distribution.—Known only from Alca- al., 2001).
trazes Island (1.35 km2), the largest of four Other snake species recorded on Alca-
small islands of Alcatrazes Archipelago trazes Island are two colubrids, Dipsas al-
(Fig. 1), approximately 35 km from the bifrons and Siphlophis pulcher, and an el-
coast of São Paulo (Vanzolini, 1973), apid, Micrurus corallinus, which also oc-
southeastern Brazil, with an elevational cur in the mainland Atlantic forest of
range of 3–266 m above sea level. southeastern Brazil (Peters and Orejas-Mi-
Natural history.—We found the new randa, 1970). Species of Dipsas are arbo-
species active both on the ground (n 5 6) real but may forage on the ground and
and on low vegetation (n 5 5) within the prey on slugs and snails. Siphlophis pulch-
September 2002] HERPETOLOGICA 309

er is arboreal and may also forage on the islands and there is no evidence that they
ground preying on lizards (including M. previously occurred there. Thus, from a
macrorhyncha and H. mabouia). Micrurus semiarboreal, dietary generalist ancestor
corallinus is fossorial and feeds on am- (Martins et al., 2001), two distinct evolu-
phisbaenians and other elongate reptile tionary routes seem to have been taken by
prey (Marques and Sazima, 1997; Sazima, these two insular species. As a result of the
1989; Sazima and Argôlo, 1994; personal absence of small mammals on the islands,
observation). Thus, only S. pulcher over- adult B. insularis relied heavily on migrant
laps with B. alcatraz in food requirements. passerine birds (approximately 85% of
The smallest mature male (with opaque their current diet; Martins et al., 2001),
efferent ducts and enlarged testes) of B. became more arboreal (Martins et al.,
alcatraz was 365 mm SVL and the smallest 2001), and evolved a venom that kills birds
mature female (with oviductal embryos) more effectively (Amaral, 1921b; Cogo et
was 477 mm SVL; males and females of al., 1993). On the other hand, adults of B.
B. jararaca attain sexual maturity at about alcatraz retained two characters of juve-
650 and 750 mm SVL, respectively (Ja- niles, a diet based on ectotherms (present
neiro-Cinquini et al., 1993; Sazima, 1992). study) and venom composition (M.F.D.
Thus, individuals of Bothrops alcatraz at- Furtado, personal communication). The
tain sexual maturity at a much smaller size isolation of populations of the B. jararaca-
than individuals of B. jararaca. A female like ancestor on coastal islands of south-
of B. alcatraz collected in December con- eastern Brazil may have occurred during
tained one oviductal embryo and one atre- one or more of the several oscillations of
sic vitellogenic follicle. The embryo was sea level during the Pleistocene (Martin et
fully-developed (SVL 130 mm, TL 27 al., 1986), the last of these occurring about
mm). Another female collected in January 11,000 yr ago (Rodrigues, 1990).
contained two atresic vitellogenic follicles, The main prey of the two insular species
apparently not ovulated. These data indi- (birds and centipedes) occur in the diet of
cate that the period of juvenile recruit- almost all generalist species of Bothrops,
ment in B. alcatraz may be similar to those including B. jararaca, although in much
of most species of Bothrops, in which par- lower frequencies (Martins et al., 2001),
turition occurs generally between January and were likely already present in the diet
and May (Almeida-Santos and Salomão, of their B. jararaca-like ancestor. Thus,
2001; personal observation). Fecundity in feeding mostly on ectothermic prey by B.
B. alcatraz may be low due to its small alcatraz and on birds by B. insularis may
body size, a trend recorded for several be considered as exaptations. A compre-
snake species (e.g., Shine, 1994). Another hensive study of the phylogeny and habits
island species, B. insularis, also shows a of the jararaca group, including other is-
low fecundity (litters of 2–10 and a high land populations along the coast of south-
frequency of atresic eggs: Hoge et al., eastern and southern Brazil, would pro-
1959). vide useful tools for evaluating the hypoth-
eses above.
DISCUSSION In general, resources on islands are in
Available data on the natural history of short supply, especially on small islands,
the three species of the B. jararaca group and this may explain why mammals sel-
(see Sazima, 1992; Martins et al., 2001) dom colonize these isolated habitats
suggest to us the following scenarios for (McNab, 1994). On the other hand, ecto-
diversification within this group. Two pop- therms require lower levels of resource
ulations of a B. jararaca-like ancestor be- use and several reptiles are successful is-
came isolated in the past (see below) on land colonizers (e.g., Case, 1983; Hasega-
Queimada Grande and Alcatrazes islands. wa and Morigushi, 1989). Well known ex-
Small mammals, the main prey of adult B. amples of successful island colonizers
jararaca (and of most Bothrops; Martins et among pitvipers include four species of
al., 2001), do not presently occur on these Bothrops in the Caribbean and in south-
310 HERPETOLOGICA [Vol. 58, No. 3

eastern Brazil (Campbell and Lamar, 1989; (area of occupancy ,10 km2 and known
Duarte et al., 1995; our study), Agkistro- from a single locality) and B2c (continuing
don piscivorus in coastal Florida (Whar- decline observed in quality of habitat) of
ton, 1969), and several species of rattle- the IUCN Red List of Threatened Species
snakes (e.g., Case, 1983) in the New (IUCN, 2000, www.redlist.org). Bothrops
World, as well as Ovophis okinavensis insularis of Queimada Grande Island is
(Morigushi, 1989) and Gloydius shed- placed in the same category based on the
daoensis (Jian-Li, 1995) in Asia. The gen- same criteria (IUCN, 2000; see also Duar-
eralist habits of most pitvipers (Greene, te et al., 1995), and the same may apply
1992; Martins et al., 2001) may have great- to several other island populations of Both-
ly facilitated the colonization of islands by rops along the coast of southeastern Brazil,
species of Bothrops and other pitvipers. for which the taxonomic allocation remains
Although body size among species of is- uncertain. On the other hand, the coastal
land snakes is highly variable (e.g., Case, populations of B. jararaca are not under
1983; Schwaner, 1985), crotalines are gen- special threat at present, as most of the
erally smaller on islands (Case, 1983). Var- coastal Atlantic forest remnants in south-
iation in body size in insular snakes may eastern Brazil are included in protected
be a consequence of prey size and avail- areas (Kronka et al., 1993). Furthermore,
ability, as well as other factors such as B. jararaca is able to survive in disturbed
presence or absence of predators and habitats provided that some forest cover
competitors (Case, 1983; Hasegawa and remains (Sazima, 1992).
Morigushi, 1989; Kohno and Ota, 1991).
Both insular species of the B. jararaca RESUMO
group are smaller than their mainland rel- Uma espécie nova de viperı́deo, Both-
ative and have specialized diets. Compet- rops alcatraz, pertencente ao grupo jara-
itors and predators are apparently absent raca, é descrita da Ilha de Alcatrazes, si-
or rare on both islands (see above). Thus, tuada na costa de São Paulo no sudeste do
dwarfism in B. alcatraz (the smallest spe- Brasil. Esta espécie difere das populações
cies in the B. jararaca group) may be re- continentais da costa do sudeste do Brasil
lated to the small size of its prey (centi- pela coloração mais escura, menor taman-
pedes and small lizards). On the other ho, menor número de escamas ventrais,
hand, B. insularis feeds mostly on relative- subcaudais e infra-labiais, número e forma
ly large prey (birds), and thus smaller size das placas cefálicas anteriores e formato
in this latter species may be related mostly dos espinhos do hemipênis, além da inten-
to arboreal habits, as there seems to be an sa atividade coagulante e da presença de
upper body size limit (around 1 m) for ar- três proteı́nas especı́ficas do veneno. A es-
boreality in Bothrops (Lillywhite and pécie nova difere de Bothrops insularis,
Smits, 1992). outra espécie insular de jararaca do sud-
The Alcatrazes lancehead is restricted to este do Brasil, pelo padrão de coloração,
a small island off southeastern Brazil, menor tamanho, menor número de sub-
where it is relatively common, although caudais em machos e ausência de hemicli-
not as common as B. insularis on Quei- toris em fêmeas. Algumas caracterı́sticas
mada Grande Island (personal observa- de B. alcatraz, como o tamanho pequeno
tion). A cliff portion of the Alcatrazes Is- do adulto, os olhos proporcionalmente
land (Saco do Funil) has been used for tar- grandes, a intensa atividade coagulante do
get practice by cannons of the Brazilian veneno e a dieta composta por centopéias
Navy (F. P. de Campos, personal commu- e lagartos, podem ser interpretadas como
nication; personal observation). Should the pedomórficas dentro do grupo jararaca.
practice continue, it would impose a threat Sugerimos aqui que o pequeno tamanho e
for the Alcatrazes lancehead and other is- as caracterı́sticas do veneno de B. alcatraz
land endemics. Based on the information estejam relacionados à sua dieta (semel-
above, B. alcatraz is now included in the hante à dos juvenis de B. jararaca do con-
category Critically Endangered, criteria B1 tinente), o que pode ser resposta à difer-
September 2002] HERPETOLOGICA 311

ente disponibilidade de tipos de presas na omous Reptiles of Latin America. Cornell Univer-
Ilha de Alcatrazes (especialmente a ausên- sity Press, Ithaca, New York, U.S.A.
CASE, T. J. 1983. The reptiles: ecology. Pp. 159–209.
cia de pequenos mamı́feros). Bothrops al- In T. J. Case and M. L. Cody (Eds.), Island Bio-
catraz e B. insularis podem ter se origi- geography in the Sea of Cortéz. University of Cal-
nado através do isolamento de populações ifornia Press, Berkeley, California, U.S.A.
ancestrais semelhantes a B. jararaca nas COGO, J. C., J. P. PRADO-FRANCESCHI, M. A. CRUZ-
HOFLING, A. P. CORRADO, AND M. A. RODRIGUES-
ilhas de Alcatrazes e Queimada Grande, SIMIONI. 1993. Effect of Bothrops insularis venom
respectivamente. A espécie nova é consi- on the mouse and chick nerve-muscle preparation.
derada como criticamente ameaçada de- Toxicon 31:1237–1247.
vido a sua pequena área de ocorrência e o DOWLING, H. G., AND J. M. SAVAGE. 1960. A guide
declı́nio da qualidade de habitat. to the snake hemipenis: a survey of basic structure
and systematic characteristics. Zoologica (New
Acknowledgments.—We thank J. A. Campbell, J. York) 45:17–28.
R. Mendelson III, and an anonymous referee for DUARTE, M. R., G. PUORTO, AND F. L. FRANCO.
helpful comments on the manuscript; H. Ferrarezzi 1995. A biological survey of the pitviper Bothrops
and F. L. Franco for useful comments throughout the insularis Amaral (Serpentes, Viperidae): an endem-
study; the Brazilian Navy for allowing access to Al- ic and threatened offshore island snake of south-
catrazes Island; M. E. Calleffo, A. Martensen, M. E. eastern Brazil. Studies on Neotropical Fauna and
Oliveira, D. N. Pereira, R. Sawaya, and the marines Environment 30:1–13.
for help in fieldwork; J. Cavalheiro, H. Ferrarezzi, V. FORSMAN, A. 1991. Adaptative variation in head size
J. Germano, and J. L. Oliveira for help in laboratory in Vipera berus L. populations. Biological Journal
work; F. P. de Campos and Projeto Alcatrazes for help of the Linnean Society 43:281–296.
during field trips; M. F. D. Furtado for information FURTADO, M. F. D., M. MARUYAMA, A. S. KAMIGUTI,
on venom of island species; W. Duleba and H. W. AND L. C. ANTONIO. 1991. Comparative study of
Greene for help with literature; F. P. de Campos for nine Bothrops snake venoms from adult female
photographs of Alcatrazes Island; D. N. Pereira for snakes and their offspring. Toxicon 29:219–226.
expertly finishing our line drawings. This study is part GREENE, H. W. 1992. The ecological and behavioral
of the project Natural History and Evolution of Both- context of pitviper evolution. Pp. 107–117. In J. A.
rops supported by FAPESP (1995/09642-5). Provi- Campbell and E. D. Brodie (Eds.), Biology of Pit-
dential fellowships were provided by the CNPq to O. vipers. Selva, Tyler, Texas, U.S.A.
A. V. Marques and I. Sazima. GUTBERLET, R. L. 1998. Phylogenetic Relationships
of New World Pitvipers (Squamata: Crotalinae) as
LITERATURE CITED Inferred from Gross Anatomy, Epidermal Micro-
ALMEIDA-SANTOS, S. M., AND M. G. SALOMÃO. 2001. structure, and Mithochondrial DNA. Ph.D. Disser-
Reproductive strategies in tropical pitvipers, genus tation, University of Texas at Arlington, Arlington,
Bothrops (Serpentes: Viperidae: Crotalinae). In Texas, U.S.A.
press. In G. Schuett, M. Höggren, and H. W. HASEGAWA M., AND H. MORIGUSHI. 1989. Geo-
Greene (Eds.), Biology of the Vipers. Eagle Moun- graphic variation in food habits, body size and life
tain Publishing, Eagle Mountain, Utah, U.S.A. history traits of the snakes on the Izu islands. Pp.
AMARAL, A. 1921a. Contribuição para o conhecimen- 414–432. In M. Matsui, T. Hikida, and R. C. Goris
to dos ophidios do Brasil. Parte I. Quatro novas (Eds.), Current Herpetology in East Asia: Proceed-
espécies de serpentes brasileiras. Anexos das Me- ings of the second Japan-China Herpetological
mórias do Instituto Butantan 1:1–37. Symposium, Kyoto, July 1988. Herpetological So-
. 1921b. Contribuição para o conhecimento ciety of Japan, Kyoto, Japan.
dos ophidios do Brasil. A. Parte II. Biologia da nova HOGE, A. R., H. E. BELLUOMINI, G. SCHREIBER,
espécie. Anexos das Memórias do Instituto Butan- AND A. M. PENHA. 1959. Sexual abnormalities in
tan 1:39–44. Bothrops insularis (Amaral, 1921). Memórias do
ANDRADE, D. V., AND A. S. ABE. 1999. Relationships Instituto Butantan 29:17–88.
of venom ontogeny and diet in Bothrops. Herpe- HOGE, A. R., AND S.A.R.W.L.D. ROMANO-HOGE.
tologica 55:200–204. 1981 (dated 1978/79). Sinopse das serpentes pe-
ANDRADE, D. V., A. S. ABE, AND M. C. DOS SANTOS. çonhentas do Brasil. Memórias do Instituto Butan-
1996. Is the venom related to diet and tail color tan 42/43:373–496.
during Bothrops moojeni ontogeny? Journal of JANEIRO-CINQUINI, T. R. F., F. F. LEINZ, AND E. C.
Herpetology 30:285–288. FARIAS. 1993. Ovarian cycle of the Bothrops jara-
CADLE, J. E. 1992. Phylogenetic relationships among raca. Memórias do Instituto Butantan 55:33–36.
vipers: immunological evidence. Pp. 41–48. In J. A. JIAN-LI, L. 1995. China Snake Island. Liaoning Sci-
Campbell and E. D. Brodie (Eds.), Biology of the ence and Technology Press, Liaoning, China.
Pitvipers. Selva, Tyler, Texas, U.S.A. KOHNO, H., AND H. OTA. 1991. Reptiles in seabird
CAMPBELL, J. A. 1985. A new species of highland colony: herpetofauna of Nakanokamishima Island
pitviper of the genus Bothrops from southern Mex- of the Yaeyama group, Ryukyu archipelago. Islands
ico. Journal of Herpetology 19:48–54. Studies in Okinawa 9:73–89.
CAMPBELL, J. A., AND W. W. LAMAR. 1989. The Ven- KORNERUP, A., AND J. H. WANSCHER. 1961. Tas-
312 HERPETOLOGICA [Vol. 58, No. 3

chenlexikon der farben. Musterschmidt Verlag, SALOMÃO, M. G., W. WÜSTER, R. S. THORPE, AND
Zürich, Switzerland. BBBSP (Butantan-British Bothrops Systematics
KRONKA, F. J. N., C. K. MATSUKUMA, M. A. NALON, Project). 1999. MtDNA phylogeny of Neotropical
I. H. DEL CALI, M. ROSSI, I. F. A. MATOS, M. S. pitvipers of the genus Bothrops (Squamata: Ser-
SHIN-IKE, AND A. A. S. PONTINHAS. 1993. Inven- pentes: Viperidae). Kaupia: Darmstädter Beiträge
tário florestal do Estado de São Paulo. São Paulo, zur Naturgeschichte 8:127–134.
SMA/CINP/IF, São Paulo, Brazil. SAZIMA, I. 1989. Feeding behavior of the snail-eating
LILLYWHITE, H. B., AND A. W. SMITS. 1992. The car- snake, Dipsas indica. Journal of Herpetology 23:
diovascular adaptations of viperid snakes. Pp. 143– 464–466.
153. In J. A. Campbell and E. D. Brodie (Eds.), . 1992. Natural history of the jararaca pitviper,
Biology of the Pitvipers. Selva, Tyler, Texas. Bothrops jararaca, in southeastern Brazil. Pp. 199–
LUEDERWALDT, H., AND J. P. FONSECA. 1923. A Ilha 216. In J. A. Campbell and E. D. Brodie (Eds.),
de Alcatrazes. Revista do Museu Paulista 13:441– Biology of Pitvipers. Selva, Tyler, Texas, U.S.A.
512. SAZIMA, I., AND A. J. ARGÔLO. 1994. Siphlophis
MARQUES, O. A. V., AND I. SAZIMA. 1997. Diet and pulcher. Prey. Herpetological Review 25:126.
feeding behavior of the coral snake, Micrurus cor- SCHWANER, T. D. 1985. Population structure of black
allinus, from the Atlantic forest in Brazil. Herpe- tiger snakes, Notechis ater niger, on offshore islands
tological Natural History 5:88–91. of south Australia. Pp. 35–46. In G. Grigg, R.
MARTIN, L., N. A. MÖRNER, J. M. FLEXOR, AND K. Shine, and H. Ehmann (Eds.), Biology of Austra-
SUGUIO. 1986. Fundamentos e reconstrução de an- lian Frogs and Reptiles. Royal Zoological Society
tigos nı́veis marinhos do Quartenário. Boletim do of New South Wales, Chipping Norton, New South
Instituto de Geociências, Publicação Especial 4:1– Wales, Australia.
161. SHINE, R. 1994. Allometric patterns in the ecology of
MARTINS, M., O. A. V. MARQUES, AND I. SAZIMA. Australian snakes. Copeia 1994:851–867.
2001. Ecological and phylogenetic correlates of VANZOLINI, P. E. 1973. Distribution and differetiation
feeding habits in Neotropical pitvipers of the genus of animals along the coast and in continental is-
Bothrops. In press. In G. Schuett, M. Höggren, and lands of the state of S. Paulo, Brasil. I. Introduction
H. W. Greene (Eds.), Biology of the Vipers. Eagle to the area and problems. Papéis Avulsos de Zool-
Mountain Publishing, Eagle Mountain, Utah, ogia 26:281–294.
U.S.A. VIDAL, N., G. LECOINTRE, J. CHRISTOPHE, AND J. P.
MCNAB, B. K. 1994. Resource use and the survival GASC. 1999. What can mitochrondrial gene se-
of land and freshwater vertebrates on oceanic is- quences tell us about intergeneric relationships of
lands. American Naturalist 144:643–660. pitvipers? Kaupia: Darmstädter Beiträge zur Na-
MORIGUSHI, H. 1989. Preliminary observation on turgeschichte 8:107–112.
Trimeresurus okinavensis in the field. Pp. 393–400. WERMAN, S. D. 1992. Phylogenetic relationships of
In M. Matsui, T. Hikida, and R. C. Goris (Eds.), Central and South American pitvipers of the genus
Current Herpetology in East Asia: Proceedings of Bothrops (sensu lato): Cladistic analyses of bio-
the Second Japan-China Herpetological Sympo- chemical and anatomical characters. Pp. 21–40. In
sium, Kyoto, July 1988. Herpetological Society of J. A. Campbell and E. D. Brodie (Eds.), Biology of
Japan, Kyoto, Japan. the Pitvipers. Selva, Tyler, Texas, U.S.A.
WHARTON, C. H. 1969. The cottonmouth moccasin
PARKINSON, C. L. 1999. Molecular systematics and
on Sea Horse Key, Florida. Bulletin of the Florida
biogeographical history of pitvipers as determined
State Museum 14:227–272.
by mitochondrial ribosomal DNA sequences. Cop-
ZIEGLER, T., AND W. BÖHME. 1997. Genitalstruktu-
eia 1999:576–586.
ren und Paarungsbiologie bei squamaten Reptilien,
PETERS, J. A., AND B. OREJAS-MIRANDA. 1970. Cat-
speziell den Platynota, mit Bemerkungen zur Sys-
alogue of Neotropical Squamata. Part I. Snakes.
tematik. Mertensiella, Supplement zu Salamandra
United States National Museum Bulletin 297:1–
8:6–207.
347.
RODRIGUES, M. T. 1990. Os lagartos da floresta At- Accepted: 5 October 2001
lântica distribuição atual e pretérita e suas impli- Associate Editor: Joseph Mendelson III
cações para estudos futuros. Pp. 404–410. In II
Simpósio sobre ecossistemas da costa sul brasileira. APPENDIX I
estrutura, manejo e função. Academia de Ciências Specimens Examined
do Estado de São Paulo, São Paulo, Brazil. Bothrops jararaca Ubatuba (ZUEC 01051, 01052,
SALOMÃO, M. G., W. WÜSTER, R. S. THORPE, AND 01057, 01080, 01247, 01445, 01600, 01601, 01602);
BBBSP (Butantan-British Bothrops Systematics Peruibe, Estação Ecológica Juréia-Itatins (IB 57790,
Project). 1997. DNA evolution of South American 57792, 57866, 57871, 57953, 58002, 58014, 58088);
pit vipers of the genus Bothrops. Pp. 89–98. In R. Iguape, Estação Ecológica Juréia-Itatins (IB 55196,
S. Thorpe, W. Wüster, and A. Malhotra (Eds.), 57805, 57808, 57811, 57840, 57856, 57888, 57896,
Venomous Snakes: Ecology, Evolution and Snake- 57897, 57903, 57904, 57908, 57927, 57940, 57941,
bite. Claredon Press, Oxford, U.K. 57989, 58001, 58035, 58108, 58130, 58134, 58145).