Natural History Notes
(Beebee & Griffiths, 2000). Autumn mating has
been recorded in the wild, including in england
(Braithwaite et al., 1989; Bull, 2010), and this
phenomenon could explain females showing early
signs of gestation the following spring, but would
not account for advanced gestation, such as in the
female that is the subject of this note.
typically, following spring mating, birth occurs
three to five months later in August or September
(Beebee & Griffiths, 2000). records of individual
snakes breeding biennially have therefore generally
been attributed to the breeding year being followed
by a fallow (non-breeding) year, presumably
allowing females to build up reserves for the
following season. Gravid overwintering, delaying
birth until the year after mating, could also produce
a pattern of biennial reproduction.
the current observation raises questions of
whether overwintering in this state is common
in england or elsewhere in the northern part of
the species’ range in europe and whether it may
also occur in the adder Vipera berus, which also
gestates its young internally rather than laying eggs,
and also has a biennial pattern of reproduction.
Further work would be needed to answer these
questions, including the possible use of x-ray or
ultrasound examination to confirm gravid status,
and the use of data from elsewhere in england and
the species’ northern (e.g. Norway) and core (e.g.
central France, italy) range, to allow comparison.
Similar data could also be collected for adders. it
has been reported that adders show some degree
of true viviparity, i.e. that there is some direct
transfer of nutrition from mother to young during
their development within the female, but that
smooth snakes are ovoviviparous, i.e. the young
are entirely enclosed within egg membranes during
development and presumably therefore receive
less nutrition than adder embryos (e.g. Beebee &
Griffiths, 2000). if transfer of nutrition to adder
embryos is more efficient than in smooth snakes, it
could be suggested as contributing to the observed
difference in the species’ northern limits.
A more thorough study involving a larger
sample of biometric data is planned for the next
season, but in the meantime the author would be
pleased to receive any observations regarding the
possibility of gravid overwintering in smooth snake
36
Number 118 - Herpetological Bulletin [2011]
or adder, whether in support or against.
i am grateful to Amphibian and reptile
Conservation for licence accreditation to handle
smooth snakes. John Wilkinson, Chris reading
and Nick moulton provided helpful advice in the
preparation of this note.
reFerenCeS
Beebee, t.J.C. & Griffiths, r.A. (2000). Amphibians
and Reptiles. A Natural History of the British
Herpetofauna. London: HarperCollins.
Braithwaite, A.C., Buckley J., Corbett K.F., edgar,
P.W., Haslewood, e.S., Haslewood, G.A.d.,
Langton, t.e.S. & Whitaker, W.J. (1989). the
distribution in england of the smooth snake
(Coronella austriaca Laurenti). Herpetol. J. 1,
370-376.
Bull, d. (2009). Coronella austriaca Laurenti
(smooth snake). record of late summer mating
in the wild in southern england. Herpetol. Bull.
111, 36-38.
Spellerberg, i.F. & Phelps t.e. (1977). Biology,
general ecology and behaviour of the snake,
Coronella austriaca Laurenti. Biol. J. Linn. Soc.
9, 133-164.
Sumbitted by: WiLL AtKiNS, London
Essex and Hertfordshire Amphibian and
Reptile Trust (LEHART), 5 Roughdown Villas
Road, Hemel Hempstead HP3 0AX, UK.
lehartrust@hotmail.com.
COLOBODACTYLUS DALCYANUS (NCN):
reProduCtioN. Gymnophthalmid biology
is poorly known, being limited by the paucity of
specimens in collections and observations in nature
(rodrigues et al., 2007; Jared et al., 2009). the
gymnophthlamid genus Colobodactylus comprises
two species, C. taunayi and C. dalcyanus, which
occur throughout southeastern Atlantic rainforests
of south America. Colobodactylus dalcyanus is
a rare species known only from high altitudes (>
1000 m asl) in two localities; Serra da mantiqueira,
Brejo da Lapa in rio de Janeiro (Vanzolini &
ramos, 1977) and Campos do Jordão in the state
of São Paulo (manzani & Sazima, 1997). to the
Natural History Notes
best of our knowledge there is no information on
the biology of C. dalcyanus.
this note provides the first observations of
C. dalcyanus reproduction. Notes were taken
during a herpetological survey of Campos do
Jordão State Park during spring, 15-18 october
2005. Additional observations were made in a
laboratory. Specimens were obtained 1940 m
asl in a forest near a small stream surrounded by
“Campus montanus” environment (iBGe, 1992)
(22o43’01.3’’S; 45o27’43.3’’W). the climate was
18oC and 55% rH.
reptiles and possibly evolved independently in
several lineages (Shine, 1988; Greene et al., 2006).
the behaviour described herein for C. dalcyanus
has also been observed for Leposoma puk (m. dixo,
pers. comm.). this suggests that parental care may
be more common among gymnophthalmids than
expected.
the two eggs laid in captivity were
subsequently fixed at different day intervals to
provide embryological data. developmental
stages of the embryos were established by an
approximation with the developmental table for
Figure 1. Colobodactylus dalcyanus
female (mZuSP 95598).
Figure 2. embryos of Colobodactylus dalcyanus from
female mZuSP 95603. a) embryo mZuSP 99608 at
stage 36 (dufare & Hubert, 1961). b) embryo mZuSP
99609 at stage 40. Scale bar = 1.0 mm.
Four female C. dalcyanus with eggs in their
oviducts were collected during this survey. two
of them were preserved (mZuSP 95601, 95602)
while the remaining two specimens (mZuSP
95598, 95603) were kept alive and transferred to the
laboratory where they laid eggs. All four specimens
retained two eggs, one in each oviduct, fitting the
clutch size pattern of two eggs recorded for most
Gymnophthalmidae (Pianka & Vitt, 2003). one
female (mZuSP 95598) (Fig. 1) was found under
leaf litter, curled around its laid eggs. this female
did not show any defensive behaviour. When
disturbed it reacted by moving the body without
loosening the curl around the eggs and remained
inactive when left in-situ. A second female (mZuSP
95603) was collected by pitfall trap from the same
forest area and laid two eggs in a plastic container.
this specimen was transferred with the eggs to a
terrarium covered with the litter vegetation from
its capture area. After approximately one hour
the female curled around the eggs and kept this
position for 30 hours.
these two records suggest initial parental care
of eggs by C. dalcyanus. Parental care is rare in
Lacerta vivipara (dufaure & Hubert, 1961). the
first egg was opened 32 days after oviposition and
revealed an embryo (mZuSP 99608; SVL= 12,6
mm) in stage 36. digits were already differentiated
but the interdigital membrane was still in the
process of being absorbed (Fig. 2a). the second
egg was opened after 56 days and revealed an
embryo (mZuSP 99609; SVL = 26.7 mm)
in stage 40 (Fig. 2b). According to dufare &
Hubert (1961), stage 40 is one of the latest
stages before hatchling, being characterised
by pigmented scales, closed parietal fontanel
and the presence of an egg tooth. the presence
of an embryo with 56 days pre-hatchling
morphology indicates a period of embryological
development of approximately 60 days, under
controlled conditions.
We thank Vanessa K. Verdade, miguel t.
rodrigues, Giovanna G. montingelli and Paola
Sanches martinez for their critical reading of
previous versions of this contribution and itamar A.
martins and Álvaro F. B. Junqueira for assistance
Herpetological Bulletin [2011] - Number 118
37
Natural History Notes
in field work. We are also grateful to iBAmA
for providing the research permit (No. 148/2005
CGFAu/LiC, 02001.007052/2001). this work
was funded by Fundação de Amparo à Pesquisa do
estado de São Paulo (FAPeSP) through a thematic
Project (02/136024) to HZ.
reFerenCeS
dufaure, J.P. & Hubert, J. (1961). table de
développement du lézard vivipare: Lacerta
(Zootoca) vivipara Jacquin. Arch. Anat. Micr.
Morph. Exp. 50, 309-328.
Greene, H.W., rodríguez, J.J.S. & Powell, B.J.
(2006). Parental behavior in anguid lizards. S.
Am. J. Herpetol. 1, 9-19.
iBGe- instituto Brasileiro de Geografia e estatística
(1992). manual técnico da Vegetação Brasileira.
1a edição, rio de Janeiro.
Jared C., Antoniazzi, m.m. & rodrigues, m.t.
(2009). reproductive behavior: Alexandresaurus
camacan. Herpetol. Rev. 40, 218-219.
manzani, P.r. & Sazima, i. (1997). Geographic
distribution:
Colobodactylus
dalcyanus.
Herpetol. Rev. 28, 95.
Pianka, e.r. & Vitt L.J. (2003). Lizards: Windows to
the Evolution of Diversity. Berkeley: university
of California Press.
rodrigues, m.t., Pellegrino, K.C.m., dixo, m.,
Verdade, V.K., Pavan, d., Argolo, A.J.S. &
Sites-Jr, J.W. (2007). A new genus of microteiid
lizard from the Atlantic forests of State of
Bahia, Brazil, with a new generic name for
Colobosaura mentalis, and a discussion of
relationships among the Heterodactylini
(Squamata, Gymnophthalmidae). Am. Mus.
Novit. 3565, 1-27.
São Paulo (estado). decreto estadual nº 53.494,
de 2 de outubro de 2008. Espécies de mamíferos,
aves, répteis, anfíbios e peixes de água doce
ameaçados de extinção no Estado de São Paulo.
diário oficial, Poder executivo SP, 3 de outubro
de 2008, Seção i, v. 118, 187, 1-10.
Shine, r. (1988). Parental care in reptiles. in:
Biology of Reptilia, Volume 16, Ecology B:
Defense and Life History. Gans C. & Huey, r.B.
(eds.). Pp. 275-239. New York.
Vanzolini, P.e. & ramos, A.m.m. (1979). A new
species of Colobodactylus, with notes on the
38
Number 118 - Herpetological Bulletin [2011]
distribution of a group of stranded microteiid
lizards (Sauria, teiidae). Pap. Avul. Zool. S.
Paulo 31, 123-144.
Submitted by: Pedro HeNriQue BerNArdo,
riCArdo Arturo GuerrA-FueNteS
and HuSSAm ZAHer Museu de Zoologia da
Universidade de São Paulo, Av. Nazaré, 481, CEP
04263-000, São Paulo, SP, Brazil. bernardoph@
gmail.com.
ODONTOPHRYNUS CARvALHOI (Carvalho’s
escuerzo): mALFormAtioN. Amphibians’
permeable skin, poorly protected eggs and embryos,
and biphasic life cycle make them particularly
sensitive to environmental change. the occurrence
of malformations in a few individuals is expected
in healthy populations and may be related to natural
mutations, developmental errors or predation
(Blaustein & Johnson, 2003). trematoda parasites,
uV radiation, environmental pollutants, and/or
the synergism between these variables may also
increase abnormalities among natural populations
(Loeffler et al., 2001; Kiesecker, 2002; Ankley et
al., 2004; Burton et al., 2008). the commonest
types of malformation in amphibians are the
absence of limbs or the presence of extra ones
(Ankley et al., 2004; meteyer, 2000). Abnormalities
in vital organs are less common and drastically
reduce chances of survival during the larval period
(Loeffler et al., 2001).
in this note, we report a case of anophthalmia
in Odontophrynus carvalhoi Savage and Cei, 1965,
an anuran species found in rainforests of eastern
Brazil. observations took place at Parque das
trilhas, municipality of Guaramiranga, state of
Ceará, northeast Brazil (04º16’S, 38º56’W; 880
m asl). the area comprised 70 ha of conserved
tropical rainforest that was continuous with
surrounding 1,584,836 ha of forest within an
area of environment protection under the State’s
responsibility. on 10 April 2009 at 11:15 an O.
carvalhoi (SVL 64.18 mm; 34 g) was found dead
near a small stream inside a conserved forested
area. upon inspection we found that the anuran’s
left eye was missing. there was a lack of scars
or sign of injury, suggesting this was a case of