Sexual dimorphism in
development and venom production of the insular threatened pit viper Bothrops insularis (Serpentes:Viperidae) of QueimadaGrande Island, Brazil
Silvia
Regina Travaglia-Cardoso 1, André Zelanis 2& Maria de Fátima Domingues Furtado 3
1,3 Laboratório
de Herpetologia, Instituto Butantan - SP, Av. Vital Brazil, 1500, 05503-900,
São Paulo-SP, Brazil
2 Laboratório
Especial de Toxinologia Aplicada (CAT/CEPID), Instituto Butantan-SP, Brazil
Email: 1 silviacardoso@butantan.gov.br, 2 azelanis@butantan.gov.br, 3 fatifurtado@butantan.gov.br
Date of publication (online): 26 September 2010
Date of publication (print): 26 September 2010
ISSN 0974-7907 (online) | 0974-7893 (print)
Editor: Aaron Bauer
Manuscript
details:
Ms #
o2369
Received
22 December 2009
Final
received 20 August 2010
Finally
accepted 23 August 2010
Citation: Travaglia-Cardoso, S.R., A. Zelanis &
M.de.F.D. Furtado (2010).
Sexual dimorphism in development and venom production of the insular threatened
pit viper Bothrops insularis (Serpentes: Viperidae)
of Queimada Grande Island, Brazil. Journal of Threatened Taxa 2(10): 1177-1184.
Copyright: © Silvia Regina Travaglia-Cardoso, André Zelanis
& Maria de Fátima Domingues Furtado 2010. Creative Commons Attribution 3.0 UnportedLicense. JoTT allows unrestricted use of this article
in any medium for non-profit purposes, reproduction and distribution by
providing adequate credit to the authors and the source of publication.
Author
Details: Silvia R. Travaglia-Cardoso is a researcher from the Herpetology Laboratory,
at Butantan Institute, São Paulo, Brazil. She is
currently a PhD student in USP. Her main research field is the reproduction and
maintenance of snakes in captivity.
André Zelanis is a PhD student at
Center for Applied Toxinology (CAT/CEPID) at Butantan Institute, São Paulo,
Brazil. His main research field is the variability found in the venom proteome
of South American snakes.
Maria de Fátima Domingues Furtado is a researcher from the Herpetology Laboratory,
at Butantan Institute, São Paulo, Brazil. She has
performed her PhD in Physiology at Biosciences Institute at São Paulo
University. Her main research is the venoms of snakes and the biological
variability.
Author
Contribution: SRTC -
maintaining the snakes in captivity, biometrical data measurement, venom
extraction, discussion of the results and writing the paper. AZ - biometrical data
measurement, discussion of the results and writing the paper. MdeFDF - experimental design, discussion of the results and writing the
paper.
Acknowledgement: Fundação de Amparo à Pesquisa do Estado de
São Paulo - FAPESP(grant # 06/60486-0).
Abstract: Bothrops insularis is a
threatened snake endemic to Queimada Grande Island,
southern coast of São Paulo, Brazil, and the occurrence of sexual abnormalities
in females (females with functional ovaries and rudimentary hemipenis)
has been reported in this population. To
date there are few data regarding developmental features of this particular
species. The aim of this study was to
follow some developmental features in specimens maintained in captivity for
seven years in the Herpetology Laboratory at Instituto Butantan, São Paulo, Brazil. We verified a pronounced sexual dimorphism in
development and venom production in the specimens analyzed. In this regard,
females showed greater length, mass and amount of venom in comparison to males. Our results suggest a possible niche partitioning
between the sexes that reduces (or minimizes) intraspecificdisharmonic interactions (eg. competition) on their small
living area (Queimada Grande Island). Taken together, our data suggest that males
and females probably are divergent in their diets, with females feeding
preferentially on endothermic prey (such as migratory birds), while males
maintain the juvenile diet (with the major items being ectothermicprey).
Keywords: Bothrops insularis, insular species, sexual
dimorphism, venom production.
For figures, images & tables -- click here
Introduction
Sexual dimorphism is an important morphological
feature among snakes, often related to differences in ecology and behavior
between males and females in many families (Shine 1994), including differences
in vulnerability to predation, choice of prey items, and reproductive success
(Shine 1994). Sexual dimorphism may vary in intensity during an animal’s
ontogeny (Beaupre et al. 1998) and may appear in neonates or only be expressed
after sexual maturity (King et al. 1999). In snakes sexual dimorphism may be apparent in such characteristics as
length and mass of the body (Shine 1990; Forsman1991; Madsen & Shine 1993; King et al. 1999; Bertona& Chiaraviglio 2003), tail length (King et al.
1999) length and shape of the head (Shine 1990; King et al. 1999;
Rodriguez-Robles 2002). These morphometric variations are usually related to sexual and
ontogenetic variations in diet and may strongly influence the snake’s
reproductive strategies (Vanzolini 1986; Mushinsky 1987; Shine 1988; Sazima1992; Marques et al. 2002; Shine et al. 2002; Shine 2003).
Bothrops insularis (Image 1) is a Critically Endangered snake endemic to QueimadaGrande Island, southern coast of São Paulo State, Brazil (Marques et al.
2004). This species was first described
by Afrânio do Amaral (Amaral 1921) as having peculiar characteristics such as a
semi-arboreal habit, and both diurnal and nocturnal activity. The diet is composed of migratory birds and
occasionally lizards. Chilopods are food items of juvenile snakes (Hoge et al. 1959; Martins et al. 2002). Hoge et al. (1959) showed sexual abnormalities within the B. insularis population, with true females, true males and
intersexes all occurring. Intersexes are genetically females, with functional
ovaries, but with a unilateral or bilateral non-functional hemipenis(Hoge et al. 1959). According to cytogenetic studies made by Beçaket al. (1990) this phenomenon could be due either to inbreeding or to
mutations. Recently, studies concerning
several aspects of the reproductive biology of B. insularis showed that both females and intersexes have hemipenis retractor muscles, and now are designated as
“females” (Kasperoviczus 2009).
To date, studies on this species mainly have
dealt with biological/ecolocical characteristics (Hoge et al. 1959; De Biasi et al.
1986; Federsoni et al. 1986 a,b;
Duarte et al. 1995; Martins et al. 2002; Duarte & Garrubo2003), systematics (Salomãoet al. 1999; Martins et al. 2001; Wuster et al.
2005), with few data available on reproductive strategies (Almeida-Santos &Salomão 2002) or sexual dimorphism (Hoge et al. 1959), and none related to developmental
characteristics. The lack of such data
denotes the importance of studies on this species, which has been designated as
Critically Endangered (CR) in the IUCN Red List of Threatened Species (Marques
et al 2004). Martins et al. (2008),
showed a decrease in the population size of B. insularis at Queimada Grande
Island, a main factor reinforcing the need for conservation efforts. This work provides biological data on sexual
dimorphism in the development and venom production of B. insularis specimens in captivity.
Materials and methods
Queimada Grande Island is located approximately 34km
from the southern coastline of São Paulo State (24029’S & 46041’W). It has been proposed that this island was
isolated from the mainland about 11,000 years ago, after the last glaciation and elevation of sea level during the late
Pleistocene (Vanzolini 1973). The Island is not inhabited by humans and
comprises a total area of 430,000m2, with the highest
point at 200m. There are no sandy
beaches and the vegetation is of the general Atlantic Forest pattern, with
grasslands and bushy areas (Hoge 1959; Vanzolini 1973). The
density of snakes is one of the highest in the world; the species represented
are the endemic pit viper Bothrops insularis (Amaral 1921; Hoge et al. 1959; Duarte et al. 1995) and Dipsas albifrons cavalheiroi (Duarte et al. 1995).
Snakes and their maintenance in captivity
Gravid Bothrops insularis specimens were collected on Queimada Grande Island - SP and three clutches were
obtained. Snout vent length (SVL), tail length (TL), and
body mass was measured and sex determined. The animals were maintained at the Herpetology Laboratory of Instituto Butantan, São Paulo. They were placed in individual cages, in
rooms with controlled temperature (24 ± 3 0C). All the animals received mice (Mus musculus) and rats (Rattus norvegicus) for food, fortnightly, until 12 months of
age, and thereafter at monthly intervals. Mice of different weights were fed to
the snakes, according to the snakes’ length.
The small number of specimens used is because. B. insularis is difficult to obtain and to maintain in
captivity. This Critically Endangered snake has small litter sizes (mean 6.5) (Hoge et al. 1959). Nevertheless, the results demonstrated important ontogenetic and
individual shifts.
Biometric data and extraction of venom
Snout-vent length (SVL), tail length (TL) and mass
were obtained over intervals of three months at which time venom was extracted
from individiual snakes. All the correlation data were obtained taking
into account the multiple measurements on the same animal at different
ages. After extraction the venom was
lyophilized and weighted.
Results
Biometric data and development in captivity
Twelve animals (6 males and 6 females) from
three litters were born in summer (February and March). Masses of the neonates varied from 7.8 to 10
g, and SVL varied from 205 to 235 mm. Four animals that reached adulthood and which were analyzed in this
paper, were named “male”, “female 1”, “female 2” and “female 3”. The neonates did not show significant
differences of mass, SVL or TL. The
analysis of the specimens that reached adulthood showed that females had higher
SVL and mass than did males, although the latter had higher relative tail
length. The animals showed similar
patterns of growth (mass and length) up to two years of age, after which males
and females diverged (Fig. 1A). Females
showed an accelerated growth up to four years of age and they kept this pattern
until they reached their seventh year; on the other hand; the male continued to
grow up to four years of age but thereafter showed no significant changes in
body size. The patterns for mass were
similar, with females becoming heavier over time up to seven years but males
stabilizing weight after four years of age (Fig. 1B).
Taking into account the multiple measurements
on the same animal at different ages, neonates did not show any correlation
between TL and SVL or between TL and mass. On the other hand, among adults there was a strong correlation between
TL and SVL (r2 = 0.97 for males, and r2 = 0.96, r2 =
0.98 and r2 = 0.99, for females 1, 2 and 3, respectively) (Fig. 2A,
Table 1). Correlation between mass and
total length was found both for the male (r2 = 0.90), and for the
females (r2 = 0.85; 0.85 and 0.86, respectively) (Fig. 2B, Table 1).
Head length was not followed during animal’s
ontogeny, but in adults, females had larger relative length of the heads in
comparison to the male (females: 3.2 to 3.8% of body length and male 3.6% of
body length).
Venom yield
We verified significantly larger amounts of
venom produced by females in comparison to males of the same age. Venom yield
(here shown as the median per year) diverged between the sexes after two years
of age, with females having a higher production of venom in comparison to the
male. At the third year females’ venom
yield varied (73.9 to 94.3 mg) and the male’s yield was 34.1mg. This difference becomes increasingly
significant, until at the age of seven years female 2 showed a median venom
yield of 334.5mg, while that of the male was only 51.9 mg (Fig. 3). Taking into account the multiple measurements
on the same animal at different ages, venom yield and TL were correlated in
females (r2 = 0.81; r2 = 0.71 and r2 = 0.81),
but only weak so in the male (r2 = 0.33) (Fig.4A, Table
1). The same results were found in
relation to venom yield and body mass, in which a strong correlation was
observed for females (r2 = 0.90; r2 = 0.91 and r2 =
0.90), and a weak one for the male (r2 = 0.43) (Fig. 4B, Table 1).
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