Reproductive aspects of two Enyalius lizards from the Atlantic forest

Herpetology Notes, volume 7: 273-276 (2014) (published online on 25 April 2014)
Reproductive aspects of two Enyalius
lizards from the Atlantic forest in Southeastern Brazil
Serena Najara Migliore1,2, Henrique Bartolomeu Braz1 and Selma Maria Almeida-Santos1
The lizard genus Enyalius (Leiosauridae) currently
comprises nine species distributed mainly in the
Atlantic Forest domain of South America, and in the
Brazilian Amazon rainforest, Cerrado, and Caatinga
(Frost et al., 2001; Rodrigues et al., 2006; Uetz, 2013).
Species of Enyalius are insectivorous, diurnal, with
arboreal or semi-arboreal habits (Jackson, 1978; Vitt
et al., 1996; Zamprogno et al., 2001; Van Sluys et al.,
2004; Rautenberg and Laps, 2010; Barreto-Lima and
Sousa, 2011). Enyalius iheringii Boulenger, 1885 and
E. perditus Jackson, 1978 are two species endemic
to the Brazilian Atlantic forest in southeastern Brazil
(Jackson, 1978), whose natural history, especially
their reproductive aspects, is poorly known (Marques
and Sazima, 2004; Barreto-Lima and Sousa, 2006;
Rautenberg and Laps, 2010; Sturaro and Silva, 2010).
Herein, we provide novel information on reproductive
aspects of E. iheringii and E. perditus from São Paulo,
southeastern Brazil.
On 3 November 2012 at 11:10 h (mid-spring), a
couple of E. perditus (both with snout-vent length
between 120-130 mm, approximately) were found in
a copulation attempt, during a herpetofaunal survey in
a fragment of Atlantic Forest with approximately 52
km2 at Juquiazinho district, in Juquitiba, São Paulo (23.97203, -47.02294; datum=WGS84; 730 m a.s.l.),
south-eastern Brazil. The couple was on a tree trunk
about 1 m above ground. The male was biting the
female’s neck when suddenly both fell from the trunk
on the leaf litter. After the fall, the male remained on
Laboratório de Ecologia e Evolução, Instituto Butantan - Av.
Dr. Vital Brazil, 1500 – Butantã, São Paulo-SP, CEP 05503900.
2
Corresponding author:
[email protected]; [email protected]
1
the back of the female, biting her neck in an attempt to
immobilize her (Fig. 1). Both remained in this position
for about 30 seconds. After this, the female disengaged
from the male and escaped, followed by the male a few
seconds later. Effective copulation was not observed.
Courtship was previously reported for at least three
species of Enyalius. Vitt et al. (1996) reported a possible
courtship in field conditions for E. leechii (Boulenger,
1885), whereas Grantsau (1966) and Barreto-Lima and
Sousa (2006) reported courtship and mating in captive
conditions for E. catenatus and E. perditus. To our
knowledge, our observation was the first courtship
confirmed taken in field conditions for a species of
Enyalius. In both captive reports, male bit females
during attempted copulation. The pattern of courtship
behaviour observed in nature was similar to those taken
in captive conditions (Grantsau, 1966; Barreto-Lima
and Sousa, 2006).
The period of courtship (spring) was coincident with
the period of vitellogenesis and courtship/mating in
captivity previously reported for the species (BarretoLima and Souza, 2006; Sturaro and Silva, 2010;
Table 1). Coincidently, the same female involved in
this courtship/mating episode was observed in the
previous night. The individual was recognized for
being in process of shedding skin (Fig. 2), in addition
to the presence of a callosity in the tail. The shedding
process is associated with the mating season of lizards
and snakes (Mason and Gutzke, 1990; Marques et al.,
2009), and several authors have suggested that shedding
is part of the oestrus signal (Aldridge and Duvall,
2002). The proposed mechanism is that reproductive
pheromones released at the time of shedding stimulate
male courtship behaviour (Mason and Gutzke, 1990;
Mason, 1992). Additionally, this female showed some
light orange spots on the neck and throat during the
copulation attempt, similarly to the observed by Sturaro
and Silva (2010) in reproductive females, suggesting
that this feature is an important courtship stimulator for
274
Serena Najara Migliore et al.
Figure 1. Copulation attempt in Enyalius perditus (Juquiazinho, Juquitiba, São Paulo, Brazil). Notice the male (green individual)
biting female’s neck (brownish individual) in attempt to immobilize her.
males (Baird, 2004). Taken together, shedding process
and colour signal suggest that the female of E. perditus
was probably signalling her condition to the male.
Reproductive observations on Enyalius iheringii were
taken from a female (voucher specimen: IBSPCR 0425;
Instituto Butantan, São Paulo, Coleção de Referência)
collected on 3 March 2012, in the Serra do Mar State
Park, Ubatuba, São Paulo, southeastern Brazil. The
female measured 103 mm of snout-vent length (SVL)
and 203 mm of tail length (TL). It was kept in a cage
containing branches and leaf litter. On 2 April 2012, it
laid 18 eggs within the cage. Five eggs were infertile.
The remaining 13 eggs were measured, using a digital
calliper (to the nearest 0.1 mm) and weighed, using a
digital balance (to the nearest 0.01 g). Eggs averaged
15.0 ± 0.5 mm in length (range = 14.1–15.7 mm), 9.7 ±
0.7 mm in width (range = 8.8–11.2 mm), and 0.81 ± 0.10
g in mass (range = 0.70–1.05 g). After oviposition, the
female weighed 24.0 g. The relative clutch mass (RCM;
total clutch mass/maternal body mass after oviposition
+ total clutch mass; following Vitt and Price, 1982) was
0.378. Thirteen eggs were incubated. Eggs were housed
in a plastic container, half-buried with moistened
vermiculite, and maintained at room temperature
Table
1. Timing
of reproductive events recorded for Enyalius perditus and E. iheringii in the literature and present study.
Table
1.
Species
Courtship
Mating
Vitellogenesis
E. perditus
Spring
(Nov-Dec)1,5
Spring
(Nov-Dec)1
Spring
(Nov)2
E. iheringii
-
-
Spring
(Dec) and
Summer (Jan)4
Gravidity or
egg-laying
Spring
(Dec) and
summer (Jan)2
Corpus luteum
Hatching
Clutch size
Summer
(Feb and Mar)2
-
7-142
Winter
(Aug)5
10-183,4,5
Summer
(Jan and Feb) and
3,4,5
Autumn (Apr)
(1) Barreto-Lima and Sousa (2006); (2) Sturaro and Silva (2010); (3) Marques and Sazima (2004); (4) Rautenberg and Laps (2010); (5) Present study.
Reproductive aspects of two Enyalius lizards from the Atlantic forest
275
Figure 2. (A) The female Enyalius perditus observed one night before the copulation attempt. (B) Detail of the female’s head
highlighting the piece of skin in the head above the eye, indicating the process of shedding.
averaging 24° C. Eight eggs spoiled over incubation
period due to fungal contamination. Hatchings (n =
4) occurred between 23 and 28 August 2012, after an
incubation period ranging from 143 to 148 days. One egg
failed to hatch. This egg was dissected, and it contained
one full-term dead embryo with a malformation in the
tail. Hatchlings averaged 27.5 ± 3.5 mm SVL (range =
25–30 mm), 49.0 ± 8.5 mm TL (range = 43–55 mm),
and 0.77 ± 0.01 g (range = 0.76–0.78 g).
There are no data on RCM for other Enyalius but the
value observed here in E. iheringii is high and close
to the upper limit observed in other lizards (Vitt and
Price, 1982). In lizards, RCM and foraging modes
are associated. RCM tends to be relatively low within
species that forage actively, and relatively high within
species using the “sit-and-wait” foraging mode (Vitt and
Price, 1982). Since females of Enyalius species appears
to be “sit-and-wait” foragers (Sousa and Cruz, 2008;
Borges et al., 2013) and move shorter distances than
males (Barreto-Lima et al., 2013), the high RCM value
observed here in E. iheringii appears to be congruent
with such association.
Estimates on gravidity period and clutch size available
in the literature for Enyalius were largely obtained from
dissection of preserved females (Rand, 1982; Vitt et
al., 1996; Marques and Sazima, 2004; Rautenberg and
Laps, 2010; Sturaro and Silva, 2010). This is the first
report of egg size, incubation period, and hatchling size
of an Enyalius species. Gravid females of E. iheringii
were previously found in January and February
(Table 1) suggesting that the species presents some
reproductive seasonality (Marques and Sazima, 2004;
Rautenberg and Laps, 2010; R. Rautenberg, pers. com.).
Our observation of egg laying in April corroborates this
assumption but suggests that oviposition may be further
extended (at least to early autumn) than previously
thought. Considering the period of encounter of
gravid females of E. iheringii and our hatching report,
recruitment appears to occur from autumn to mid-winter
(Table 1).
The few information available for E. perditus and E.
iheringii impair broad comparisons between species and
definitive generalization on the timing of reproductive
events. However, taken together our data and literature
276
information indicate certain similarity between species,
at least on the timing of vitellogenesis and gravidity
(Table 1). However, gravidity period appears to extend
further (to early autumn) in E. iheringii. Detailed studies
are clearly needed to fully understand the reproductive
cycles of these species and test this assumption.
Acknowledgements. We thank M. T. Rodrigues, F. F. Curcio,
and V. J. Germano for taxonomic identification of the specimens,
and R. Recoder for the critical reading and comments on the
manuscript. We also thank R. Rautenberg, A. F. Barreto-Lima,
and B. Rocha for information on Enyalius specimens, and A.
Silveira for assistance with hatchlings. PAP (Programa de
Aprimoramento Profissional) provided a fellowship to S. N.
Migliore, and FAPESP (Fundação de Amparo à Pesquisa do
Estado de São Paulo) to H. B. Braz (grant no. 2009/54478-3).
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Accepted by Diogo Provete;
Managing Editor: Diogo Provete