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Communal egg-laying and nest-sites of the Goo-eater Snake, Sibynomorphus mikanii (Dipsadidae, Dipsadinae) in southeastern Brazil

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26 Number 106 - Herpetological Bulletin [2008]
Communal egg-laying and nest-sites of the Goo-eater Snake,
Sibynomorphus mikanii (Dipsadidae, Dipsadinae) in southeastern
Brazil
HENRIQUE B. P. BRAZ1, 3, 4, FRANCISCO L. FRANCO2
and SELMA M. ALMEIDA-SANTOS1
1 Laboratório de Ecologia e Evolução, Instituto Butantan, 05503-900, São Paulo SP, Brasil
2 Laboratório de Herpetologia, Instituto Butantan, 05503-900, São Paulo SP, Brasil
3 Programa de Pós-graduação Interunidades em Biotecnologia, Universidade de São Paulo, SP, Brasil
4 Corresponding author: hbraz@butantan.gov.br
FOR oviparous reptiles without parental
behaviour, female nest-site selection plays a
significant role in the evolution of life histories
(Resetarits, 1996; Shine, 2004). Nevertheless,
nest-sites and oviposition modes of neotropical
snakes are relatively unknown, mostly because
mothers are so successful at hiding their eggs that
nests are rarely found in nature. Additionally,
much emphasis has been placed on life history
components such as body size, number and size of
offspring, and age at maturity (Stearns, 1992;
Resetarits, 1996).
Snakes oviposit under rocks, logs or any other
surface cover, in preformed subterranean chambers
(Packard & Packard, 1988) and within nests of
other animals such as alligators (Hall & Meier,
1993), ants and termites (Riley et al., 1985). With
regard to oviposition modes, snakes oviposit both
in solitary and communal nests (Vaz-Ferreira et
al., 1970; Graves & Duvall, 1995; Blouin-Demers
et al., 2004).
Communal oviposition is a widespread
phenomenon and occurs when several females,
conspecifics or not, share the same nest cavity to
deposit their eggs (Graves & Duvall, 1995).
Among neotropical species, reports of nest-sites
and communal nests are scarce and are mostly
related to colder climates (e.g. Vaz-Ferreira et al.,
1970; Cadle & Chuna, 1995). Recently,
Albuquerque & Ferrarezzi (2004) reported one
communal nest for the neotropical colubrid snake
Sibynomorphus mikanii in an anthropized area in
southeastern Brazil. Herein we describe another
three nest-sites, nesting areas and oviposition
modes of the goo-eater snake S. mikanii in
southeastern Brazil.
Sibynomorphus mikanii is a dipsadine snake
that feeds on slugs (Laporta-Ferreira et al., 1986;
Oliveira, 2001) and is distributed in Central,
Atlantic and Meridional Brazilian uplands in
cerrado and tropical forest areas (Franco, 1994).
Females oviposit from September (early spring) to
February (mid-summer) and clutch size varies
from three to 10 eggs, averaging 5.9 (Oliveira,
2001).
On 5 February 2007, 41 eggs and 11 empty
shells (Fig. 1c) were found together inside a hole,
20 cm below ground surface, at the edge of a
degraded wood inside Instituto Butantan (IBSP),
São Paulo city, Brazil. The nest (hereafter nest #1)
was situated 17 m away from the wood and 9 m
away from the backyard of a house on a slightly
steep slope (Fig. 1a). A small hole (50 mm
diameter), at the side of the nest may have
provided access for the snakes (Fig. 1b).
Temperature at the same depth around the nest
averaged 27.3°C (range = 27-28°C). Four empty
shells contained fluids indicating recent hatchings
whereas seven were completely desiccated. Two
dead hatchlings were found near the nest (± 1 m
away). Nest #2 and #3 were discovered by a
farmer in two different spots, in a 5000 m2 house
backyard, in Vargem city, Brazil. Nest #2 was
discovered under dry grass accumulated after
ground weeding and contained nine eggs. Nest #3
was found 30 m away from nest #2 under a large
Figure 1. (A) Diagrammatic vertical section of the terrain surrounding nest #1; (B) view of the destroyed nest and
its likely entrance; (C) Eggs of Sibynomorphus mikanii found within nest #1.
Herpetological Bulletin [2008] - Number 106 27
rock (30 x 60 x 15 cm) and had a total of 12 eggs.
Eggs were donated to IBSP on 1 March 2007,
some days after collection and by this time one
egg had hatched. In the laboratory, we counted
four fresh empty shells and 17 eggs (three
dehydrated and one parasitized by fungi). In both
backyards, dogs circulated freely over the nesting
areas. After the donation of the eggs, the farmer
found a dead hatchling of S. mikanii near nest #3.
Eggs were measured, weighed (Table 1), and
incubated in a laboratory at 27°C (temperature of
nest #1). Fungal infection precluded eight eggs
(19.5%) from nest #1 and five eggs (45.5%)
from nest #2 and #3 from hatching. Eggs were
dissected but we were unable to find or to identify
the embryos. One hatchling from nest #2 died half
emerged from the eggshell. Thus, 33 successful
hatchings from nest #1 occurred between 6
February and 16 April 2007, whereas from nest #
2 and #3 five occurred between 1 March and 31
May 2007. Hatchlings were measured, weighed,
and sexed by eversion of hemipenis (Table 1).
Based on mean clutch size of the species (5.9 eggs
[Oliveira, 2001]), we inferred that nearly seven to
nine different oviposition events may have occurred
in nest #1, one to two in nest #2, and two in nest
#3 in the current reproductive season. These
assumptions are strengthened if we take into
consideration hatching dates (seven in nest #1 and
three in nest #2 and #3). Although communal
oviposition in nest #1 and #3 is evident, there is
some doubt over nest #2 as it is quite possible that
one single female laid the nine eggs.
Nest-sites and nesting areas are described
for few species of neotropical snakes (e.g.
Vaz-Ferreira et al., 1970; Cadle & Chuna,
1995; Albuquerque & Ferrarezzi, 2004).
Despite the fact that some snakes dig a hole in the
soil to oviposit (e.g. Burger & Zappalorti, 1986),
most species apparently are unable to construct a
nest and rely on pre-existing sites for oviposition
(Packard & Packard, 1988). This seems to be the
case for S. mikanii (Albuquerque & Ferrarezzi,
2004; this study). Although eggs of nest #1 were
found inside a hole, it is unlikely that any female
of S. mikanii actually excavated it because the soil
was very compacted. Moreover, in the laboratory,
gravid S. mikanii tend to hide the eggs under the
Reproduction in Sibynomorphus mikanii
water bowl or under rocks instead of burying them
(H.B.P. Braz & S.M. Almeida-Santos, unpublished
data). In addition, other dipsadine snakes also
oviposit in pre-existing sites (Brandão & Vanzolini,
1985; Riley et al., 1985; Cadle & Chuna, 1995;
Greene, 1997).
Thermal conditions are often suggested as a
factor driving maternal choice of nest-site (Blouin-
Demers et al., 2004; Shine 2004) because
incubation temperature affects offspring
phenotypes (Deeming, 2004) and therefore may
influence organismal fitness (Elphick & Shine,
1998; Brown & Shine, 2004). Females frequently
oviposit in forest clearings (Fowler, 1966; Brodie
et al., 1969; Covacevich & Limpus, 1972;
Burger & Zappalorti, 1986; Albuquerque &
Ferrarezzi, 2004) and nests located in these areas
generally are hotter than nests located in shaded
areas because shading reduces insolation and
heating of the soil (Magnusson & Lima, 1984;
Shine et al., 2002). As well as nest #1, several
nests have also been found in slopes (e.g. Brodie
et al., 1969; Covacevich & Limpus, 1972; Burger,
1976; Albuquerque & Ferrarezzi, 2004; James &
Henderson 2004) and factors like direction and
slope influence the absorption of solar radiation
(Burger, 1976). Thus, mothers may have selected
these sites in seeking to maximize sunlight
exposure to accelerate embryonic development or
optimize phenotypic traits of the resulting
hatchlings. Therefore thermal conditions could
also be a major factor influencing communal
nesting behaviour. Temperatures in communal
nests are usually higher than in solitary ones (e.g.
Blouin-Demers et al., 2004) due to metabolic heat
generated by embryos (Burger, 1976; Ewert &
Nelson, 2003).
Communal nesting might be adaptive because
higher temperatures in nests enhance hatchling
phenotypes (Blouin-Demers et al., 2004). However,
studies on the thermal and hydric requirements of
S. mikanii embryos would be needed to test these
hypotheses. In parallel, egg aggregations also offer
other potential advantages such as protection
(Graves & Duvall, 1995; Jackson, 1998) and
predator satiation (Eckrich & Owens, 1995; Graves
& Duvall, 1995). If communal oviposition offers
such advantages to hatchlings (e.g. phenotype
improvement, predator satiation), why, then, would
one female oviposit in a solitary nest as is likely to
have occurred in nest #2? Blouin-Demers et al.
(2004) suggested that the disadvantages of solitary
nests may be compensated by lower risk of egg
parasitism by fungi. Additionally, in communal
nests availability of water is less than in solitary
nests (Marco et al., 2004; Radder & Shine, 2007).
This modifies hydric exchange between the eggs
and the environment and the consequences to
hatchling phenotypes may be more detrimental to
aggregated eggs (Marco et al., 2004). Thus it is
reasonable to suggest that there are trade-offs
between these two modes of egg-laying that result
in similar fitness payoffs (Blouin-Demers et al.,
2004).
In summary, there are two (but nonexclusive)
reasons for the occurrence of communal nesting
Measurements Nest #1 Nest #2 and #3
Eggs n = 41 n = 13
Length (mm) 27.9 ± 2.7 25.7 ± 3.0
Width (mm) 14.5 ± 2.0 12.6 ± 0.9
Mass (g) 3.5 ± 0.9 2.5 ± 0.4
Hatchlings n = 33 n = 5
SVL (mm) 171.8 ± 13.5 170.0 ± 5.8
TL (mm) 34.0 ± 4.7 29.4 ± 2.6
Mass (g) 2.3 ± 0.4 2.0 ± 0.5
Sex (male/female) 19/14 2/3
Table 1. Measurements of eggs and hatchlings of three natural nests of the Goo-eater Snake Sibynomorphus mikanii.
SVL = Snout-vent length; TL = Tail length.
Reproduction in Sibynomorphus mikanii
28 Number 106 - Herpetological Bulletin [2008]
behaviour: scarcity of suitable nesting sites (e.g.
optimum moisture and temperature; protection
against predators) or adaptive behaviour; that
increases reproductive success due to aggregation
in large clusters.
Our findings plus literature data indicate a
preference of gravid S. mikanii to nest communally
even when similar potential nest-sites were present
in nesting areas. We suggest that such widespread
behaviour might result from adaptation. However,
the adaptive significance of communal oviposition
remains unknown.
ACKNOWLEDGEMENTS
We thank D. A. C. Martins, and the staff of
Vigilância Sanitária de Vargem for the material
donation and information. J. C. Ferreira and A. C.
Barbosa for laboratory assistance. B. M. Graves
and D. W. Owens kindly provided references. This
study was supported by FAPESP (07/51977-3).
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30 Number 106 - Herpetological Bulletin [2008]
Reproduction in Sibynomorphus mikanii
... On the other hand, sexual divergences could be related to reproductive activities that, through natural selection, may impose selective pressures favoring the evolution of an expanded or modified trophic apparatus in one of the sexes (Shine, 1989;Camilleri and Shine, 1990). Observations on reproductive aspects indicate that females of D. mikanii nesting communally, such that multiple females share the same cavity for deposition of eggs (Albuquerque and Ferrarezzi, 2004;Braz et al., 2008). Although some snake species dig a hole in the soil to build their nests, this does not seem to be the case for D. mikanii (Burger and Zappalorti, 1986;Braz et al., 2008). ...
... Observations on reproductive aspects indicate that females of D. mikanii nesting communally, such that multiple females share the same cavity for deposition of eggs (Albuquerque and Ferrarezzi, 2004;Braz et al., 2008). Although some snake species dig a hole in the soil to build their nests, this does not seem to be the case for D. mikanii (Burger and Zappalorti, 1986;Braz et al., 2008). The cavities where communal nesting of this species have been observed presented highly compacted soil, suggesting that females used pre-existing cavities (Braz et al., 2008). ...
... Although some snake species dig a hole in the soil to build their nests, this does not seem to be the case for D. mikanii (Burger and Zappalorti, 1986;Braz et al., 2008). The cavities where communal nesting of this species have been observed presented highly compacted soil, suggesting that females used pre-existing cavities (Braz et al., 2008). Even if females of D. mikanii are unable actively to excavate soil, they probably select existing cavities with optimal thermal conditions and slope, given Ferrarezzi, 2004;Shine, 2004;Braz et al., 2008). ...
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