at Parque Estadual da Serra do Tabuleiro

Herpetology Notes, volume 7: 11-15 (2014) (published online on 25 January 2014)
Reproduction of two exotic species of
Trachemys Agassiz, 1857 (Testudines, Emydidae)
at Parque Estadual da Serra do Tabuleiro,
state of Santa Catarina, southern Brazil
Marcos Adriano Tortato1, Raíssa Fries Bressan1,2* and Tobias Saraiva Kunz1,2
The genus Trachemys Agassiz, 1857 includes 15
species and is distributed from the mid-western United
States to southern South America (Seidel, 2002).
Trachemys scripta elegans (Wied, 1838) is native to
the west of the United States and occurs from the state
of Virginia until the north of Florida (Fritz and Havaš,
2007, van Djik et al., 2011). During the last decades,
hatchlings and juveniles of this species have been
extensively commercialized all over the world as pets,
therefore, established populations are known in several
countries (e.g. Ficetola, Monti and Padoa-Schioppa,
2002; Cadi et al., 2004; Bunnel, 2005; Shiau et al.,
2006; Perry et al., 2007; Pupins, 2007; Soorae, Quarqaz
and Gardner, 2008; O’Keeffe, 2009; Kitowski and
Pachol, 2009; Izquierdo et al., 2010), including Brazil
(Vieira and Costa, 2006; Ferronato et al., 2009; Bujes,
2011; Silva-Soares et al., 2011), where importation
and commercialization were forbidden in 1991 by the
federal environmental agency (IBAMA) (Souza et al.,
2007). Trachemys dorbigni (Duméril and Bibron, 1835)
is the southernmost species of the genus. It is present
in practically all Uruguayan territory (Cabrera, 1998;
Achaval and Olmos, 2007), in northeastern Argentina
– from the provinces of Misiones and Corrientes to the
La Plata River (Waller and Chebez, 1987; Cabrera,
1998; Alcalde et al., 2012) and in southern Brazil, in
the central-south portion of the state of Rio Grande do
Caipora Cooperativa, Avenida Desembargador Vitor Lima,
260, Sala 513 CEP 88040-400, Carvoeira, Florianópolis – SC,
Brasil.
2
Programa de Pós-Graduação em Biologia Animal, Laboratório
de Herpetologia, Departamento de Zoologia, Instituto de
Biociências, Universidade Federal do Rio Grande do Sul,
Brasil. Av. Bento Gonçalves, 9500, sala 109, Agronomia,
Porto Alegre-RS, Brasil, CEP 91509-900.
*Corresponding author: [email protected]
1
Sul reaching, by the coastal plain, the northeast region
of this state, close to the border with the state of Santa
Catarina (Lema and Ferreira, 1990; Lema, 1994; Santos
et al., 2005; Bujes, 2010; Alcalde et al., 2012).
Recently, Trachemys dorbigni was recorded in two
conservation units in southeast and south Brazil. An
adult female was found at the Parque Estadual Morro
do Diabo, southwest of the state of São Paulo, in the
Paraná River Basin (Zaher et al., 2009; Santos et al.,
2009). This record was attributed to introduction or
recent distribution expansion of the species (Santos et
al., 2009). In the west of the state of Santa Catarina,
the species was recorded at the Parque Estadual das
Araucárias, (Hartmann and Giassom, 2008). Since the
species’ occurrence in the southern Brazilian plateau is
very unlikely this specimen may also represents a case
of introduction. Hatchlings and juveniles of T. dorbigni
are also commercialized as pets in many Brazilian
states (Molina and Gomes, 1998a; Bujes and Verrastro,
2008).
Even though it is probably a native species of the
southern coastal plain of the state of Santa Catarina
(Bujes, 2010), T. dorbigni, as well as T. s. elegans,
was officially considered an invasive alien species by
this state’s environmental agency (CONSEMA, 2010),
because of its presence in regions outside its natural
range, specifically in the ombrophilous dense forest of
the eastern region of the state.
The Parque Estadual da Serra do Tabuleiro (PEST)
is located in the mid-east region of Santa Catarina
(Fig. 1). With 84.130 ha, it is the largest terrestrial
conservation unit in the state, and includes several
vegetation physiognomies of the Atlantic Forest Biome,
such as ombrophilous dense forest, cloud forest, mixed
ombrophilous forest (Araucaria forest), altitudinal
fields, restingas and mangroves (Ishy et al., 2009). The
coastal plain located at the eastern portion of the PEST,
known as Restinga da Baixada do Maciambu (RBM), is
adjacent to the Atlantic Ocean (27o50’ S; 48o50’ W), and
12
Marcos Adriano Tortato et al.
Figure 1. Map showing the location (black star) of the Restinga da Baixada do Maciambu and the Visitors Centre of the Parque
Estadual da Serra do Tabuleiro, State of Santa Catarina (SC), Brazil. RS = state of Rio Grande do Sul; PR = state of Paraná.
presents mainly grassland formations with shrubs and
scattered trees found in the driest areas over the sand
ridges. Extensive humid areas are found between sand
ridges, formed by perennial lakes connecting to marshes
during the rainy season. Cyperaceae and Tifaceae are
dominant families (Klein, 1981).
Four turtle species are known to exist in the RBM: the
chelid turtles Phrynops hilarii (Duméril and Bibron,
1835) (Tortato, 2007) and Hydromedusa tectifera Cope,
1869 (M. Tortato, pers. obs.) and the exotic emydids T.
s. elegans (Wied, 1838) (Tortato, 2007; this study), and
T. dorbigni (this study), as well as some specimens of
the introduced tortoise, Chelonoidis carbonaria (Spix,
1824) (M. Tortato, pers. obs.). At least P. hilarii is
known to nest in this area (Tortato, 2007).
In September and October 2006, three T. dorbigni
females were recorded nesting in the RBM (fig. 2A).
Two records occurred on September 17th, between 9 and
11 a.m.; the first nest was 12 cm deep and contained
nine eggs; the second nest, located 30 cm away from the
first, was 16 cm deep and contained 10 eggs. Both were
above the maximum water level, 1.5 m away from a dry
water channel and approximately 140 m away from a
perennial pond. On October 18th, around 1 p.m., the third
nesting female was found on a sand ridge covered by
low vegetation (grasslands). This female laid five eggs
in a 15 cm deep nest. It was cloudy and rainy in both
days when T. dorbigni nesting was recorded. Females
of this species may lay at least two clutches per year
as was verified by Vanzolini (1997) and corroborated
by Molina and Gomes (1998b) and Bager, Freitas
and Krause (2007). Clutch size recorded at the Taim
Ecological Station, Rio Grande do Sul state, varied from
six to 19 eggs (Bager, Freitas and Krause, 2007), while
Fagundes, Bager and Cechin (2010) recorded a clutch
size varying from four to 15 eggs.
On October 20th a tegu lizard (Tupinambis merianae)
was observed digging and preying on eggs from the
second nest. Lizards of the genus Tupinambis are well
known predators of vertebrates’ eggs, including turtles
(e.g. Krause, Gomes and Leyser, 1982; Gonçalves,
Cechin and Bager, 2007; Tortato, 2007; Salera-Jr.,
Malvasio and Portelinha, 2009; Schneider, Ferrara
and Vogt, 2009; Fagundes, Bager and Cechin, 2010;
Schneider et al., 2011).
Reproduction of two exotic species of Trachemys Agassiz, 1857
The nesting activity of T. dorbigni observed in the
PEST occurred at the beginning of the species egglaying season, known to extend from September to
February (Krause, Gomes and Leyser, 1982; Bager,
Freitas and Krause, 2007; Gonçalves, Cechin and
Bager, 2007; Fagundes, Bager and Cechin, 2010). The
occurrence of nesting during rainy days may be a way to
prevent desiccation of eggs or the elevation of females’
body temperature (Moll and Legler, 1971).
On September 1st 2006, three Trachemys hatchlings
were observed; one was being predated by a burrowing
owl (Athene cunicularia) and the other two were in a pond
13
about 50 m away from the T. dorbigni nesting site. Of
these, one was collected (maximum carapace length 39
mm; fig. 2B-C), identified as T. s. elegans, and deposited
in the Collection of Reptiles of the Departamento de
Ecologia e Zoologia of the Universidade Federal de
Santa Catarina, Santa Catarina, Brazil (CHUFSC 866).
Considering that they were found in late winter, it is
possible that these hatchlings had overwintered in the
nest (see Bager, Fagundes and Piedras, 2007). The
collected individual already presented a completely
unfolded shell and a partially closed umbilical scar.
Figure 2. Trachemys spp. recorded in the PEST. 2A) Female T. dorbigni photographed after nesting (nest 02); 2B) Dorsal view
of the T. s. elegans hatchling (CHUFSC 866); 2C) Ventral view of the same hatchling.
14
The establishment of reproductive populations of
T. scripta in the European Union is related to warmer
climates and higher precipitation (Ficetola, Thuiller and
Padoa-Schioppa, 2009) and its establishment risk was
evaluated as moderate (Kopecky, Kalous and Patoka,
2013). There is no data about the establishment of
reproductive T. scripta populations in Brazil, and the
same is true for T. dorbigni populations out of its natural
range. Field observations indicate that T. dorbigni is
more abundant than T. scripta in the PEST. If these were
reproductive populations, as our data suggest, T. dorbigni
could be favored by the resemblance and geographic
proximity to its natural range of distribution.
Acknowledgements. The authors would like to thank the
Fundação do Meio Ambiente of the state of Santa Catarina
(FATMA), the staff of the Visitors Centre of the Parque Estadual
da Serra do Tabuleiro, Alex Bager and Silvia Ziller for their
help and information provided. We would like to specially thank
Flavio de Barros Molina for the valuable contributions and for
reviewing the manuscript.
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Accepted by Mirco Solé