17

5
THE QUEIMADA GRANDE ISLAND AND ITS
BIOLOGICAL TREASURE

The Golden Lancehead

Marcio Martins, Ricardo J. Sawaya,

Selma Almeida-​Santos, and Otavio A. V. Marques

Introduction
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Queimada Grande is a small island (43 ha) located 33 km off the
coast of São Paulo state, southeastern Brazil (Figure. 5.1), close to
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Itanhaém and Peruíbe. It is roughly 1.7 km long and up to 0.6 km
wide, with its long axis oriented from north to south. The max-
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imum elevation is 135 m at its southern portion (Martins et  al.

2008). Only the ridge of the island has flat or low sloping areas
in which it is easy to establish trails for moving around the island.
There are no beaches on the island, which is surrounded by cliffs
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and gently to strongly sloping wave-​cut platforms (Figures 5.1 and

5.2). When the sea is rough, it is virtually impossible to access the
island. The area of the continental shelf between the island and the
coast is relatively shallow, with a maximum depth of 45 m.
The island is covered mostly by low tropical rainforest (approx-
imately 25 ha; Figures 5.2 and 5.3) growing on shallow soils. The
canopy of this forest lies approximately 5–​8 m above the ground.
In addition to the areas covered by forests, there are areas of bare
rock (approximately 7 ha; see Figure 5.2b), areas of rock covered by
herbaceous vegetation (approximately 5 ha; see Figure 5.2a), and
a few disturbed areas (totaling approximately 6 ha; Martins et al.
2008) from which the forest was removed in the past and are now
covered by grasses and a few shrubs (the grassy areas in Figure 5.2c).
The largest of these disturbed, grassy areas covers approximately 5
ha at the northern portion of the island, whereas extensive areas of
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1 1 8   •  I s l a n d s a n d  S n a k e s

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Figure  5.1  Satellite image showing the southeastern coast of Brazil and the location
of Queimada Grande Island. The inset shows an aerial photograph of the island taken in
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2002. This is the only island where the Golden Lancehead occurs.

bare rock occur on the extreme southern portion of the island. Insofar as most
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of the disturbed areas face the open sea, they are under the effect of sea breezes
carrying salt. Thus, forest regeneration is very slow (see inset of Figure 5.1).
A complete regeneration of the forest in these areas may take many decades.
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Queimada Grande lies in a region characterized by a wet subtropical cli-

mate with no dry months, hot summers, and mild winters. In the hottest
period (October–​May), the mean temperature may reach 27°C, and during
the coldest period ( June–​September), the mean temperature can drop to
18°C. Annual rainfall averages 1,750 mm, with a drier period from June to
September (monthly rainfall <100 mm) and a wetter period from October to
May (averaging >200 mm of monthly rainfall; Martins et al. 2008).
At the beginning of the 20th century, the island was inhabited by “3 or
4 light-​house watchmen and 1 or 2 sailors” (Amaral 1921b:85). However,
the island has been uninhabited since 1926, and the lighthouse is now au-
tomated and maintained sporadically by the Brazilian Navy (Kasperoviczus
and Almeida-​Santos 2012). There is no source of fresh water on the island
besides rainfall (Amaral 1921b). The island is owned by the Brazilian gov-
ernment and has been a protected area since 1985 (Instituto Chico Mendes
de Conservação da Biodiversidade 2017). Its protected area category (Area
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Figure 5.2  Views of the forest perimeter illustrating areas of exposed rock mostly cov-
ered with forest (a), bare rock at the edge of the island (b), and disturbed grassy slopes
between patches of forest (c).
Source: Photographs by M. Martins.
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1 2 0   •  I s l a n d s a n d  S n a k e s

strongly sloping wave-​cut platforms.

Source: Photograph by M. Martins.
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Figure 5.3  View of the forest that covers most of the Queimada Grande Island and its
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of Relevant Ecological Interest) encompasses sites with extraordinary nat-
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ural features or those that harbor unique organisms, and it is intended to

maintain these natural ecosystems and regulate its use (Ministério do Meio
Ambiente 2011).
Many seabirds visit the island, including the Brown Booby (Sula
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leucogaster), which nests on the island (Figure 5.4; Macarrão 2010). In ad-
dition to seabirds, 56 non-​marine birds have been recorded for the island,
almost all of them migratory species that visit the island seasonally, mostly
for short periods (Figure 5.5; Macarrão 2010; Marques et al. 2012). Only two
passerine birds are known to be resident: the House Wren (Troglodytes aedon)
and the Bananaquit (Coereba flaveola; Marques et al. 2002a, 2012). In addi-
tion to the birds, two species of bats, two amphibians, three lizards (including
the introduced House Gecko, Hemidactylus mabouia), two amphisbaenians,
and two snakes make up the vertebrate fauna of the island (Marques et  al.
2002a). The Golden Lancehead (Bothrops insularis; Figure 5.6a) is one of
the two species of snakes that inhabit the Queimada Grande Island (Hoge
1950; Marques et al. 2002a). It is endemic to the island and was described as
a new species in 1921 (Amaral 1921a) by the Brazilian herpetologist Afrânio
do Amaral (1894–​1982), who worked at the Butantan Institute for many
decades.
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Figure 5.4  A Brown Booby (Sula leucogaster) with its chick.
Source: Photograph by M. Martins.
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Figure  5.5  Bothrops insularis eating a passerine bird (White-​crested Elaenia, Elaenia
chilensis) on a tree.
Source: Photograph by M. Martins.
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1 2 2   •  I s l a n d s a n d  S n a k e s

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Figure 5.6  (a) A young adult of the Golden Lancehead, Bothrops insularis, and (b) an
adult female of Bothrops jararaca, a mainland species that is closely related to the former.
Source: Photographs by M. Martins.

The Queimada Grande Island is one among many small land-​bridge

islands that occur throughout the coastal regions of southeastern Brazil.
Distinct populations of lanceheads have been described from four of these
islands (Amaral 1921a; Marques et  al. 2002b; Barbo et  al. 2012, 2016),
and other new populations may be found in the future. Like Queimada
Grande Island, most of these small islands are uninhabited, with restricted
access by laypeople because they are part of protected areas. However, ex-
cept for the Golden Lancehead, the biology of these populations is still
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Queimada Grande Island and the Golden Lancehead  •  123

relatively poorly known, although all of them are considered threatened

with extinction.

The Origin of the Golden Lancehead

In the adjacent mainland, the most common species of lancehead is the
Jararaca Lancehead, Bothrops jararaca (Figure 5.6b), which is very close phy-
logenetically to the Golden Lancehead and to other island pit vipers from
southeastern Brazil—​inferred from morphological and molecular similarities
(Grazziotin et al. 2006; Fenwick et al. 2009; Carrasco et al. 2012; Alencar
et al. 2016). The distribution of the Jararaca Lancehead occupies more than
2,000 km of the Brazilian coast (from Bahia to Rio Grande do Sul states)
and extends inland to the interior of the continent and central Argentina

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(Campbell and Lamar 2004). Based on the close affinities of the Golden and
Jararaca Lanceheads, we have proposed the following scenario for the origin
of the former.
During the many glaciations that occurred during the Pleistocene, roughly
2.6  million to 12,000  years ago, marked variations in sea level occurred
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throughout the world. The Brazilian continental shelf was no exception
(Martin et al. 1986). For instance, at the peak of the last glacial maximum ap-
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proximately 26,000 to 21,000 years ago, the sea level at the coast of Tropical
America was approximately 120 m below the present sea level (Peltier and
Fairbanks 2006). During these low sea levels, most of the continental shelf of
Brazil became exposed and was probably covered by the lowland rainforests
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that characterize the coast of southeastern Brazil today. In our model, we as-
sume that the populations of the Jararaca Lancehead were widespread on this
exposed portion of the continental shelf, where the Queimada Grande Island
was completely exposed and consisted of a forest-​covered mountain in the
middle of this generally flat area. As the sea level rose toward the next inter-
glacial period of the present time, the island became completely isolated by
seawater approximately 11,000 years ago, and the populations of plants and
animals that inhabited the forests on this mountain became isolated from
those on the mainland (Rodrigues 1990).
Based on the small size of Queimada Grande Island, we assume that many
of the animals trapped by the rising sea level became extinct since the iso-
lation of the island (a process called faunal relaxation; see Chapter  1, this
volume). For example, there is currently no terrestrial mammal on the island,
although many occur on the adjacent mainland. Similarly, a small area of
forest on the adjacent mainland tends to have approximately 20–​25 species of
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1 2 4   •  I s l a n d s a n d  S n a k e s

snakes, 30–​4 0 frogs, and 5–​7 lizards (Marques and Sazima 2004; Hartmann
et al. 2009a, 2009b). Only 2 species of snakes, 3 lizards, 2 amphisbaenians,
and 2 frogs are recorded from the Queimada Grande Island (Marques et al.
2002a). Thus, the present biota of the Queimada Grande Island is a small
fraction of the biota that occurred in the exposed continental shelf during the
last glacial period. One of the remnant vertebrate populations that persisted
on the island is the Golden Lancehead, which has differentiated in mor-
phology and habits since its complete isolation. We have no evidence for mi-
gration of lanceheads to or from the island during 20 years of fieldwork. Many
other insular snake populations that occur on other land-​bridge islands like
Queimada Grande quite possibly originated in a similar manner (Marques
et al. 2002b; Barbo et al. 2012).

The Biology of the Golden Lancehead

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Since isolation of the Golden Lancehead on the Queimada Grande Island, the
morphology and biology of these snakes have changed in many different ways.
It is a moderate-​sized lancehead, with males attaining a maximum total length
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of 912 mm and females 1,093 mm (Guimarães et al. 2010). Compared to the
closely related, mainland species, B. jararaca, the Golden Lancehead is shorter
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(females of the former may attain up to 1,500 mm), slightly more slender, and
has a longer tail (Martins et al. 2001; Wüster et al. 2005). All these differences
may reflect the more arboreal habits of the Golden Lancehead (Figure 5.7). In
addition to these morphological differences, the color of B. insularis is quite
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different from that of neighboring populations of B.  jararaca (see Figure

5.6b). As the name implies, the Golden Lancehead has a predominantly pale
yellowish brown dorsum with slightly darker post-​orbital stripe and blotches
that may have variable shapes (see Figure 5.6a). The tip of the tail is black
throughout life, in contrast with B. jararaca, in which only juveniles have dif-
ferently colored tail tips. The venter is cream. When coiled on high branches
of the forest trees, the pale ventral body makes individuals very easy to spot by
researchers on the ground (Figure 5.8). Curiously, when kept in captivity, the
Golden Lancehead becomes generally darker in color.
In 1959, Belgian zoologist Alphonse Richard Hoge (who also worked
at Butantan) and collaborators recorded the occurrence of several females
of B.  insularis bearing a structure similar to the hemipenis of male snakes.
Hoge and collaborators called these females “intersexes” (Hoge et al. 1959).
They also described the finding of a single hermaphrodite individual bearing
active gonads of males and females. Our recent studies have shown that the
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the ground.
Source: Photograph by M. Martins.
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Figure  5.7  Bothrops insularis moving on forest vegetation approximately 1 m above
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Figure 5.8  A Golden Lancehead, Bothrops insularis, resting on a branch of a tree ap-

proximately 4 m above the ground, with the light-​colored ventral body exposed and seen
from the ground.
Source: Photograph by M. Martins.
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1 2 6   •  I s l a n d s a n d  S n a k e s

population of Golden Lancehead consists of males and intersexual females

because all females that have been sampled on the island have a hemipenis—​
almost always smaller than those of males and sometimes malformed
(Kasperoviczus 2009). It remains uncertain whether the hemipenis of the in-
tersexual females has some present function.
The seasonal timing of reproduction of the Golden Lancehead is similar
to that of the mainland Jararaca Lancehead as well as to that of other species
of the genus Bothrops. We have observed males searching for females, as well
as courtship, at the end of the wet period and at the onset of the “dry” period
(i.e., June and July), especially during the latter time (Figure 5.9). Accordingly,
the highest number of moving males has been observed at this time of the
year:  During one of the field trips to the island in July, almost half of the
males (40%, n = 24) were crawling (at other periods, it is uncommon to find

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snakes crawling). One male was observed moving toward a female on a tree,
apparently having followed the female’s scent trail. The female initially was
climbing, then rested on a branch, and the male approached. The mating pe-
riod of the Golden Lancehead seems to be relatively more delayed and longer
than that observed for other snakes of the genus Bothrops, in which mating
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usually occurs from March to July (Marques et al. 2013).
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Figure 5.9  Courtship in a pair of Bothrops insularis crawling on leaf litter of the forest
floor. The male snake is on the top.
Source: Photograph by M. Martins.
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Queimada Grande Island and the Golden Lancehead  •  127

Apparently, the Golden Lancehead also reproduces by facultative par-

thenogenesis (Almeida-​Santos and Salomão 2002). Females with ovarian
follicles in vitellogenesis occur from March to December. Ovulation and
fertilization occur at the end of the dry period and the onset of the wet pe-
riod (September), and gravid females are found from October to April. The
number of vitellogenic follicles (mean = 8; range, 3–​20) is fewer than that of
B. jararaca (mean = 19; range, 11–​36), but this might reflect differences in
body size, insofar as fecundity is usually strongly correlated with body size
in snakes. However, the Golden Lancehead usually exhibits a high incidence
of atretic follicles (approximately 45% of females produce unfertilized eggs),
which was never observed in females of the Jararaca Lancehead. Litter size
recorded in captive females of B. insularis ranged from 3 to 10. The gestation
period may extend from 4 to 5 months, and the recruitment of newborns is

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restricted to a warmer period from February to March. The body size of the
newborns (mean = 220 mm) is similar to those of other species of the genus
Bothrops, including B. jararaca (Marques et al. 2013).
A peculiar aspect of the reproduction of the Golden Lancehead is the repro-
ductive frequency, which is highly variable from year to year. Approximately
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half the females of the Jararaca Lancehead reproduce annually, whereas the
frequency of reproductive females in the Golden Lancehead is variable and
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usually lower (0–​50%; see Chapter 9, this volume). Annual variation in food
supply might be responsible for the great year-​to-​year variation in reproduc-
tive frequency in the Golden Lancehead (Marques et al. 2013). This insular
pit viper feeds upon migratory passerine birds (discussed later), and the year-​
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to-​year variation in the numbers of these birds has been recorded in coastal
areas from southeastern Brazil (Marques et al. 2012).
The Golden Lancehead is found almost exclusively in forested areas
(Martins et  al. 2008). The use of open areas for basking, a common ther-
moregulatory behavior for other snakes, is largely avoided, probably due to
foraging constraints, increased risks of predation, and dehydration caused
by the very windy conditions of these sites (Bovo et  al. 2012). Compared
to the Jararaca Lancehead, the Golden Lancehead has become more arbo-
real in habits. In the former, juveniles are commonly found on low vegeta-
tion, ambushing frogs, whereas adults are predominantly terrestrial (Sazima
1992; Marques and Sazima 2004). In the Golden Lancehead, both juveniles
and adults are frequently found on vegetation up to 5 m above the ground.
Contrary to the Jararaca Lancehead, juveniles of the Golden Lancehead are
difficult to find during both diurnal and nocturnal visual searches. We still
do not know why this happens. Juveniles of the Golden Lancehead could use
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1 2 8   •  I s l a n d s a n d  S n a k e s

predominantly visually inaccessible microhabitats, such as canopy or under-

ground substrates (the ground on the island is covered by tangled roots and
rocks). Indeed, Amaral (1921b) reported that newborns “immediately seek
a hiding place under dry leaves or under moss found on the ground” (p. 87).
However, the low number of viable vitellogenic follicles as well as the low
frequency of reproductive females suggest that low sampling of juveniles of
the Golden Lancehead may be due to low rate of recruitment of newborns
(Marques et  al. 2013). Future radio-​tracking studies would be helpful to
clarify this issue.
Instead of being mainly nocturnal, as in the Jararaca Lancehead, adults
of the Golden Lancehead are primarily diurnal. This shift in the timing of
activity in adults may reflect the typical diurnal habits of their avian prey, in
contrast to the predominantly nocturnal activity of small mammals that con-

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stitute the principal prey of adult B. jararaca. On the other hand, juveniles of
the Golden Lancehead are found mostly at night, as in B. jararaca.
As observed in many populations of snakes inhabiting islands, the Golden
Lancehead is exceptionally common at the Queimada Grande Island. We sus-
pect that approximately 4,000 snakes occurred in the forests of the island in
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the mid-​1990s (see the section titled Threats and Conservation). Thus, the
density of snakes at that time might have been close to 160 snakes per hec-
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tare of forest. This is one of the highest densities of snakes recorded in the
world. A study aimed to estimate the population size through direct counts
inside sampling plots showed that the density of the Golden Lancehead varies
markedly along the north–​south axis, with a peak on the higher area at the
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southern end of the island. In this small area—​informally named the “Garden
of Eden” by Harry W. Greene—​up to 15 snakes can be seen at a time on the
forest floor and on tree branches (see Chapters 6–​9, this volume). This excep-
tionally high density of snakes suggests there is a relatively low predation pres-
sure at the island compared with mainland habitats of B. jararaca. However,
at least six potential predators have been observed on the island:  The
Guira Cuckoo (Guira guira) is resident; two species of caracara (Milvago
chimachima and Caracara plancus) are regular visitors; and Roadside Hawks
(Rupornis magnirostris), Peregrine Falcons (Falco peregrinus), and Burrowing
Owls (Athene cunicularia) appear occasionally at the island (Macarrão 2010).
Compared to its sister species, the diet of juveniles of the Golden
Lancehead has not changed after isolation. Thus, juveniles display a diet based
on frogs, lizards, centipedes, and sometimes snakes, as also occurs in juveniles
of the Jararaca Lancehead (Martins et al. 2002; see Chapter 9, this volume).
Adults, on the other hand, changed from a diet based almost exclusively on
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Queimada Grande Island and the Golden Lancehead  •  129

small mammals (birds are very rare prey in the diet of the Jararaca Lancehead)
to a diet based almost exclusively on birds (Martins et al. 2002; Marques et al.
2012; see Chapters 6 and 8, this volume). Thus, the absence of small mammals
did not impede the persistence of the ancestral population of the Golden
Lancehead on Queimada Grande Island, and the habit of eating occasional
birds, observed in the Jararaca Lancehead, may have facilitated the dietary
shift that is observed in adults.
With the help of ornithologists, we now know that 56 species of birds (ex-
cluding seabirds) can be seen on the island during the course of a year. Most
of these birds are migratory and spend only a few days at a time on the island
(Macarrão 2010). Examination of the gut contents of 47 adults of the Golden
Lancehead showed that relatively few of these species are actually used as
food by the snake (Marques et al. 2012). Most common food items include

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the small White-​crested Elaenia, Elaenia chilensis (see Figure 5.5), and the
Yellow-​legged Thrush, Turdus flavipes. On the mainland, the thrush occurs in
the highlands during the rainy season of the austral spring and summer, but it
migrates to lowland areas along the coast during the austral winter (Develey
2004; Alves 2007). Some of these migrating individuals reach the Queimada
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Grande Island (Macarrão 2010). The White-​crested Elaenia migrates from
southern to northern South America, appearing on the southeastern coast of
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Brazil at the end of summer and the onset of autumn (Marini and Cavalcanti
1990; Pacheco and Gonzaga 1994). Both species were among the most abun-
dant passerine birds during the period they spent on the island (Macarrão
2010; Marques et al. 2012). Based on a sample of almost 500 snakes that we
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found during visual searches, we learned that the way adult vipers use the
available substrates during a given time is closely associated with the habits of
the migratory avian prey that are simultaneously present on the island. When
avian prey is found mainly on trees (e.g., White-​crested Elaenia), the snakes
are predominantly arboreal, whereas when avian prey is more frequently
found on the ground, the snakes are largely terrestrial (Marques et al. 2012).
On some occasions, up to 4 snakes can be found near the fallen fruits of the
common Jerivá Palm (Syagrus romanzoffiana). These yellow fruits attract
fruit flies, which in turn attract thrushes that are eaten by the snakes.
Interestingly, the two resident species of passerine birds, the House
Wren (T. aedon) and the Bananaquit (C. flaveola), were never found in the
gut contents of the Golden Lancehead, although both are among the spe-
cies observed more frequently at the island (Marques et al. 2012). Indeed, the
former species is the most common bird on the island, making up approxi-
mately 50% of all bird records. We have evidence that the House Wren is able
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1 3 0   •  I s l a n d s a n d  S n a k e s

to avoid predation by the pit viper. In one instance, a wren foraging on the
ground suddenly stopped moving, stared at a coiled lancehead, and made a
long turn apparently to avoid getting closer to the snake.
Our field data indicate that adults of the Golden Lancehead feed mainly
in late summer and early autumn, when the White-​crested Elaenia is the
most abundant bird prey on the island, and, to a lesser extent, in the winter,
when the Yellow-​legged Thrush fills a similar role (Marques et al. 2012). The
remaining times of the year may well constitute periods of fasting for adult
vipers because during these times no migratory birds are found in large num-
bers on the island. Indeed, the relatively low reproductive frequency recorded
for this insular lancehead, compared to its sister species B. jararaca, may re-
flect these extended periods of low food supply.
Using the tail as a lure is believed to occur in most species of neotro­pical

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pit vipers, whose juveniles have a whitish or yellowish tail tip and feed on small
lizards and/​or anurans (Martins et al. 2002). A darker color on the tip of the
tail (instead of the usual white or yellowish color) is rarely found but is espe-
cially evident in the Golden Lancehead (Figure 5.10). Tail luring was recently
recorded for a juvenile in nature, apparently directed to the frog Haddadus
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binotatus, which is a common species on the island (Andrade et  al. 2010).
Furthermore, the characteristic ambush posture, coiled with the conspicuous
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Figure 5.10  A young adult of Bothrops insularis coiled on the forest floor, with its dark
tail tip close to its head.
Source: Photograph by O. A. V. Marques.
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Queimada Grande Island and the Golden Lancehead  •  131

tail tip exposed close to the head (see Figure 5.10), suggests that adults of the
Golden Lancehead might use tail luring to attract birds. Birds attracted to the
lure may peck at a snake’s tail and suggestively the frequency of tail tip injuries
in adults of B. insularis (21%) is higher than that found in B. jararaca (7%;
Andrade et al. 2010).
A shift in the composition of venom has occurred in the Golden
Lancehead, probably as a consequence of a parallel shift in diet (Zelanis et al.
2008). Indeed, even the manner in which this snake deals with its prey has
changed. As a typical pit viper, when the Jararaca Lancehead preys on a small
mammal, it strikes the prey—​injecting venom with its anterior, movable
fangs—​releases it, and after a few seconds begins to follow the chemical track
left by the dying prey (Sazima 1992). This behavior presumably has evolved
in vipers as a way to avoid being bitten by the prey. When preying upon less

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dangerous prey, such as frogs or lizards, vipers frequently restrain the prey
after envenoming it. Adults of the Golden Lancehead restrain birds in their
mouth immediately after striking them (see Figure 5.5). Perhaps natural selec-
tion has favored this behavior as a way to avoid losing the bird when feeding
in aboveground vegetation. A falling or flying bird would leave no chemical
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track that could be followed. Interestingly, adults of the Golden Lancehead
strike and release exotic small mammals when they are offered to snakes in
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staged encounters in the field, indicating that the manner in which this snake
handles small mammals was retained, despite the fact that it does not feed on
them (Marques and Sazima 2009).
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Threats and Conservation
The Golden Lancehead is categorized as “Critically endangered” in three dif-
ferent red lists: the International Union for Conservation of Nature global
red list, the Brazilian red list, and the São Paulo State red list. The reasoning
for this classification in the global red list is based on this snake’s highly re-
stricted range in a single location and the “continuing decline in habitat
quality, as a result of removal of vegetation by people from the Brazilian Navy
who keep the lighthouse” (Marques et al. 2004). Our studies have shown that
the Golden Lancehead is highly dependent on forested areas (Martins et al.
2008; Bovo, et al. 2012), and removal of vegetation was indeed a significant
threat. Insofar as the removal of vegetation seems to have ceased, the recent
assessments of B. insularis are based on decline of the population (Martins
et al. 2008; Guimarães et al. 2014), instead of continuing decline in the quality
of habitat (Martins et al. 2008; Guimarães et al. 2014).
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Since its discovery in 1921 and until the early 1990s, many hundreds of
individuals of the Golden Lancehead were collected at the island and taken to
the Butantan Institute. For example, approximately 500 snakes were collected
by the lighthouse keeper from 1914 to 1920, and approximately 300 snakes
were collected by A. R. Hoge and collaborators from 1946 to 1957. Even in
the 1980s and early 1990s, more than 100 snakes were collected (Duarte et al.
1995). From the mid-​1990s to the present, very few individuals have been
removed from the island.
Based on the frequent encounter of snakes on the island, Hoge suggested
in the mid-​1970s that the population size of B. insularis was approximately
3,000–​4,000 individuals. In a study published in 2008 (Martins et al. 2008),
we estimated that the population size may be approximately 2,000. This
number was based on direct encounters with snakes inside 10 × 10 m plots

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carried out in 2002. We distributed 26 quadrat plots regularly in a trail that
crosses the island in the north–​south axis. In this same paper, we provided en-
counter rates obtained in a non-​systematic way during the previous 12 years.
We showed that these encounter rates decreased to half during this period,
indicating a significant decline in the population. Because we had evidence
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for the illegal removal of snakes from the island in the early 2000s, we sus-
pect that at least part of this decline is attributable to poaching. A  slight
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decreasing trend in population size was also detected in a study of population

dynamics published recently that used field data obtained from 2002 to 2010
(Guimarães et al. 2014).
Based on this information, there is an urgent need for enforcement to re-
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strain the illegal removal of snakes from the island as well as a monitoring
program to track future changes in the population size of B. insularis. This
would perhaps guarantee the future persistence of this interesting species on
Queimada Grande Island.
In addition to the in situ conservation program suggested previously, an
ex situ conservation program for the Golden Lancehead is underway at the
Butantan Institute. Captive breeding has the potential to play a pivotal role in
conserving threatened species, among others by maintaining a healthy popu-
lation. Ex situ programs usually have two phases. The first one aims to estab-
lish a reproductive population in captivity, and the second aims to keep snakes
in similar conditions as those of the island for an eventual reintroduction pro-
gram. The Butantan Institute is located in a small fragment of Atlantic Forest
inside the city of São Paulo, Brazil. Thus, it is possible to establish an isolated
forest area in order to house a small population of the Golden Lancehead.
31

Queimada Grande Island and the Golden Lancehead  •  133

This isolated area would allow the snakes to move on vegetation and thus be
in a forest habitat similar to that on the island.
A captive breeding program of the Golden Lancehead has been oper-
ating on a regional level since 2010. The current living population consists of
31 adults and 23 juveniles born in captivity. By using noninvasive methods
(measurement of fecal metabolites), we intend to evaluate the variation of sex
steroids in the reproductive cycle in order to provide detailed knowledge of
reproductive endocrinology of this species, a necessary requirement for the
implementation of assisted reproduction techniques. Furthermore, we aim to
optimize the reproductive rates of the captive population by using methods
such as semen handling, extender composition, dilution and cooling rates,
and artificial insemination. We also believe that semen refrigeration is a nec-
essary step toward cryopreservation and future artificial fertilization with

SA
frozen semen. In addition, molecular characterization of each individual
based on microsatellite information will be performed in order to evaluate
genetic diversity and to manage putative parents, aiming to increase genetic
variability. We hope that in the near future, this ex situ population will pro-
vide healthy individuals for a reintroduction program in case the in situ con-
U
servation efforts are not enough to preserve this golden treasure.
P-

Perspectives for the Future
Since its description in the 1920s, the Golden Lancehead has attracted the
attention of many researchers, making it one of the most studied snakes in
OU

South America. However, there is still much to be learned about this in-
teresting island species. For instance, because it is relatively difficult, dan-
gerous, and expensive to get to Queimada Grande Island, previous studies
were focused on getting the most data possible during the short time of each
visit. Thus, aspects of the biology of the Golden Lancehead that can only be
studied during longer periods of time, such as behavior (e.g., behaviors related
to feeding, reproduction, and defense) and movement, are still virtually un-
known. Bothrops insularis is a member of an amazing small group of insular
snakes that rely heavily on migrating birds as food. The other species in this
group are the Shedao Pit Viper (Gloydius shedaoensis), from Shedao Island,
China (Li 1995; Sun et  al. 2001; Shine et  al. 2002), and the Milos Viper
(Macrovipera schweizeri), from Milos Island, Greece (Nilson et al. 1999; see
Chapter 8, this volume). Thus, this interesting biology appeared independ-
ently at least three times throughout the world. Knowing and preserving these
314

1 3 4   •  I s l a n d s a n d  S n a k e s

unique island vipers would allow future generations to enjoy these amazing
island treasures.

Acknowledgments
The writing of this chapter began in 2013 when MM was a Visiting Professor
at the Department of Biology, University of Florida, with a fellowship from
Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP; No.
2012/​15273-​0). MM also thanks FAPESP for grants during the writing of
the manuscript (Nos. 1/​50206-​9 and 2015/​21259-​8) and Conselho Nacional
de Desenvolvimento Científico e Tecnológico for research fellowships (Nos.
302953/​2012-​4 and 306961/​2015-​6).

SA
References
Alencar, L. R. V., T. B. Quental, F. G. Grazziotin, M. L. Alfaro, M. Martins, M. Venzon,
and H. Zaher. 2016. Diversification in vipers: Phylogenetic relationships, time of
divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution
U
105:50–​62.
Almeida-​Santos, S. M., and M. G. Salomão. 2002. Reproduction in neotropical pitvipers,
with emphasis on species of the genus Bothrops. In G. Schuett, M. Höggren, and
P-

H. W. Greene (Eds.), Biology of the Vipers. Eagle Mountain, UT: Eagle Mountain
Publishing, pp. 445–​4 62.
Alves, M.  A. S.  2007. Sistemas de migrações de aves em ambientes terrestres no
Brasil:  Exemplos, lacunas e propostas para o avanço do conhecimento. Revista
OU

Brasileira de Ornitologia 15:231–​238.

Amaral, A. 1921a. Contribution towards the knowledge of snakes in Brazil—​A : Part
I. Four new species of Brazilian snakes. Anexos das Memórias do Instituto Butantan
1:49–​81.
Amaral A. 1921b. Contribution towards the knowledge of snakes in Brazil—​A : Part
II. Biology of the new species, Lachesis insularis. Anexos das Memórias do Instituto
Butantan 1:83–​88.
Andrade, D. V., O. A. V. Marques, R. S. B. Gavira, F. E. Barbo, R. L. Zacariotti, and
I. Sazima. 2010. Tail luring by the golden lancehead (Bothrops insularis), an island
endemic snake from south-​eastern Brazil. South American Journal of Herpetology
5(3):175–​180.
Barbo, F. E., J. L. Gasparini, A. P. Almeida, H. Zaher, F. G. Grazziotin, R. B. Gusmão,
J. M. G. Ferrarini, and R. J. Sawaya. 2016. Another new and threatened species of
lancehead genus Bothrops (Serpentes, Viperidae) from Ilha dos Franceses, south-
eastern Brazil. Zootaxa 4097:511–​529.
Barbo, F. E., F. G. Grazziotin, I. Sazima, M. Martins, and R. J. Sawaya. 2012. A new
and threatened insular species of lancehead from southeastern Brazil. Herpetologica
68:418–​429.
315

Queimada Grande Island and the Golden Lancehead  •  135

Bovo, R. P., O. A. V. Marques, and D. V. Andrade. 2012. When basking is not an op-
tion: Thermoregulation of a viperid snake endemic to a small island in the south
Atlantic of Brazil. Copeia 2012:408–​418.
Campbell, J.  A., and W.  W. Lamar. 2004. The Venomous Reptiles of the Western
Hemisphere. Ithaca, NY: Comstock (two vols.).
Carrasco, P. A., C. I. Mattoni, G. C. Leynaud, and G. J. Scrocchi. 2012. Morphology,
phylogeny and taxonomy of South American bothropoid pitvipers (Serpentes,
Viperidae). Zoologica Scripta 41:1–​15.
Develey, P. F. 2004. As aves da Estação Ecológica Juréia-​Itatins. In O. A. V. Marques and
W. Duleba (Eds.), Estação Ecológica Juréia-​Itatins: Ambiente Físico, Flora e Fauna.
Ribeirão Preto, Brazil: Holos Editora, pp. 278–​295.
Duarte, M. R., G. Puorto, and F. L. Franco. 1995. A biological survey of the pitviper
Bothrops insularis Amaral (Serpentes, Viperidae):  An endemic and threatened
offshore island snake of southeastern Brazil. Studies of Neotropical Fauna and
Environment 30:1–​13.

SA
Fenwick, A. M., R. L. Gutberlet, Jr., J. A. Evans, and C. L. Parkinson. 2009. Morphological
and molecular evidence for phylogeny and classification of South American
pitvipers, genera Bothrops, Bothriopsis, and Bothrocophias (Serpentes:  Viperidae).
Zoological Journal of the Linnean Society 156:617–​6 40.
U
Grazziotin, F. G., M. Monzel, S. Echeverrigaray, and S. L. Bonatto. 2006. Phylogeography
of the Bothrops jararaca complex (Serpentes: Viperidae): Past fragmentation and is-
land colonization in the Brazilian Atlantic Forest. Molecular Ecology 15:3969–​3982.
P-

Guimarães, M., R.  Munguía-​Steyer, P.  F. Doherty, Jr., M.  Martins, and R.  J. Sawaya.
2014. Population dynamics of the critically endangered golden lancehead pitviper,
Bothrops insularis:  Stability or decline? PLoS One 9(4):e95203. doi:10.1371/​
journal.pone.0095203
OU

Guimarães, M. R., R. P. Bovo, K. N. Kasperoviczus, and O. A. V. Marques. 2010. Bothrops
insularis (golden lancehead): Maximum length. Herpetological Review 41:89.
Hartmann, P.  A., M.  T. Hartmann, and M.  Martins. 2009a. Ecology of a snake as-
semblage in the Atlantic Forest of southeastern Brazil. Papéis Avulsos de Zoologia
49:343–​360.
Hartmann, P. A., M. T. Hartmann, and M. Martins. 2009b. Ecologia e história natural
de uma taxocenose de serpentes no Núcleo Santa Virgínia do Parque Estadual da
Serra do Mar, no sudeste do Brasil. Biota Neotropica 9:1–​12.
Hoge, A.  R. 1950. Notas erpetológicas:  7. Fauna erpetológica da Ilha da Queimada
Grande. Memórias do Instituto Butantan, 22:151–​172.
Hoge, A. R., H. E. Belluomini, G. Schreiber, and A. M. Penha. 1959. Sexual abnormalities
in Bothrops insularis. Memórias do Instituto Butantan 29:17–​88.
Instituto Chico Mendes de Conservação da Biodiversidade, Brazil. 2017. Unidades de
Conservação—​Marinho:  Arie Ilhas da Queimada Pequena e Queimada Grande.
Retrieved January 6, 2017 (http://​ www.icmbio.gov.br/​ portal/​
unidadesde­
conservacao/​biomas-​brasileiros/​marinho/​unidades- ​de- ​conservacao-​marinho/​
2248-​arie-​ilhas-​da-​queimada-​pequena-​e-​queimada-​grande).
316

1 3 6   •  I s l a n d s a n d  S n a k e s

Kasperoviczus, K.  N. 2009. Biologia Reprodutiva de Bothrops insularis da Ilha da

Queimada Grande de São Paulo. Unpublished MSc thesis, Universidade de São
Paulo, São Paulo, Brazil.
Kasperoviczus, K. N., and S. M. Almeida-​Santos. 2012. Instituto Butantan e a Jararaca-​
ilhoa:  Cem anos de história, mitos e ciência. Cadernos de História da Ciência
8:255–​269.
Li, J.-​L. 1995. China Snake Island. Dalian, China:  Liaoning Science and
Technology Press.
Macarrão, A. 2010. Avifauna da Ilha da Queimada Grande, SP: diversidade, estrutura
trófica e sazonalidade. Unpublished MSc thesis, Universidade Estadual Paulista,
São José do Rio Preto, Brazil.
Marini, M., and R. B. Cavalcanti. 1990. Migrações de Elaenia albiceps chilensis e Elaenia
chiriquensis albivertex (Aves: Tyrannidae). Boletim do Museu Paraense Emílio Goeldi
6:59–​67.
Marques, O. A. V., K. Kasperoviczus, and S. M. Almeida-​Santos. 2013. Reproductive

SA
ecology of the threatened pitviper Bothrops insularis from Queimada Grande
Island, southeast Brazil. Journal of Herpetology 47:393–​399.
Marques, O. A. V., M. Martins, P. F. Develey, A. Macarrão, and I. Sazima. 2012. The
golden lancehead (Serpentes: Viperidae) relies on two seasonally plentiful bird spe-
U
cies visiting its island habitat. Journal of Natural History 46:885–​895.
Marques, O. A. V., M. Martins, and I. Sazima. 2002a. A jararaca da Ilha da Queimada
Grande. Ciência Hoje 31:56–​59.
P-

Marques, O.  A. V., M.  Martins, and I.  Sazima. 2002b. A  new insular pitviper from
Brazil, with comments on the evolutionary biology and conservation of the
Bothrops jararaca group (Serpentes, Viperidae). Herpetologica 58:303–​312.
Marques, O.A.V., M. Martins, and I. Sazima. 2004. Bothrops insularis. The IUCN Red
OU

List of Threatened Species 2004:  e.T2917A9493475. Retrieved January 22, 2019.

http://​dx.doi.org/​10.2305/​IUCN.UK.2004.RLTS.T2917A9493475.en.
Marques, O. A. V., and I. Sazima. 2004. História natural dos répteis da Estação Ecológica
Juréia-​Itatins. In O. A. V. Marques and W. Duleba (Eds.), Estação Ecológica Juréia-​
Itatins:  Ambiente Físico, Flora e Fauna. Ribeirão Preto, Brazil:  Holos Editora,
pp. 257–​277.
Marques, O.  A. V., and I.  Sazima. 2009. Old habits die hard:  Mouse handling by a
pitviper species on a rodent-​free island. Amphibia–​Reptilia 30:435–​438.
Martin, L., N.  A. Mörner, J.  M. Flexor, and K.  Suguiu. 1986. Fundamentos e
reconstrução de antigos níveis marinhos do Quartenário. Boletim do Instituto de
Geociências, Publicação Especial 4:1–​161.
Martins, M., M. S. Araújo, R. J. Sawaya, and R. Nunes. 2001. Diversity and evolution
of macrohabitat use, body size and morphology in a monophyletic group of neotro­
pical pitvipers (Bothrops). Journal of Zoology 254:529–​538.
Martins, M., O.  A. V.  Marques, and I.  Sazima. 2002. Ecological and phylogenetic
correlates of feeding habits in neotropical pitvipers (genus Bothrops). In G.  W.
317

Queimada Grande Island and the Golden Lancehead  •  137

Schuett, M.  Höggren, M.  E. Douglas, and H.  W. Greene (Eds.), Biology of the
Vipers. Eagle Mountain, UT: Eagle Mountain Publishing, pp. 307–​328.
Martins, M., R. J. Sawaya, and O. A. V. Marques. 2008. A first estimate of the popula-
tion size of the critically endangered lancehead, Bothrops insularis. South American
Journal of Herpetology 3:168–​174.
Ministério do Meio Ambiente, Brazil. 2011. SNUC—​Sistema Nacional de Unidades de
Conservação da Natureza. Brasilia: Ministério do Meio Ambiente.
Nilson, G., C. Andrén, Y. Ioannidis, and M. Dimaki. 1999. Ecology and conservation
of the Milos viper, Macrovipera schweizeri (Werner, 1935). Amphibia–​Reptilia
20:355–​375.
Pacheco, J.  F., and L.  P. Gonzaga. 1994. Tiranídeos do estado do Rio de Janeiro
provenientes de regiões austrais da América do Sul. Notulas Faunisticas 63:1–​4.
Peltier, W. R., and R. G. Fairbanks. 2006. Global glacial ice volume and Last Glacial
Maximum duration from an extended Barbados sea level record. Quaternary Science
Reviews 25:3322–​3337.

SA
Rodrigues, M. T. 1990. Os lagartos da floresta Atlântica distribuição atual e pretérita e
suas implicações para estudos futuros. In II Simpósio sobre Ecossistemas da Costa Sul
Brasileira. Estrutura, Manejo e Função. São Paulo, Brazil: Academia de Ciências do
Estado de São Paulo, pp. 404–​410.
U
Sazima, I.  1992. Natural history of the jararaca pitviper, Bothrops jararaca, in south-
eastern Brazil. In J. A. Campbell and E. D. Brodie, Jr. (Eds.), Biology of the pitvipers.
Tyler, TX: Selva, pp. 199–​216.
P-

Shine, R., L.  X. Sun, M.  Kearney, and M.  Fitzgerald. 2002. Thermal correlates of
foraging-​site selection by Chinese pit-​vipers (Gloydius shedaoensis, Viperidae).
Journal of Thermal Biology 27:405–​412.
Sun, L. X., R. Shine, Z. Debi, and T. Zhengren. 2001. Biotic and abiotic influences on
OU

activity patterns of insular pit-​vipers (Gloydius shedaoensis, Viperidae) from north-​

eastern China. Biological Conservation 97:387–​398.
Wüster, W., M. R. Duarte, and M. G. Salomão. 2005. Morphological correlates of in-
cipient arboreality and ornithophagy in island pitvipers, and the phylogenetic posi-
tion of Bothrops insularis. Journal of Zoology 266:1–​10.
Zelanis, A., S. R. Travaglia-​Cardoso, and M. F. D. Furtado. 2008. Ontogenetic changes
in the venom of Bothrops insularis (Serpentes: Viperidae) and its biological impli-
cation. South American Journal of Herpetology 3:43–​50.