Short Communication
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9322–9326
New distribution records of Mesoclemmys vanderhaegei
(Testudines: Chelidae) from southeastern Brazil, including
observations on reproduction
ISSN 0974-7907 (Online)
ISSN 0974-7893 (Print)
Fábio Mafei 1, Bruno Tayar Marinho do Nascimento 2, Guilherme Marson Moya 3 &
Reginaldo José Donatelli 4
OPEN ACCESS
1,3,4
Universidade Estadual Paulista “Júlio de Mesquita Filho”, Faculdade de Ciências, Departamento de Ciências
Biológicas, Avenida Engenheiro Luiz Edmundo Carrijo Coube, 14-01, CEP 17033-360, Bauru, SP, Brazil.
3
Insituto Pró-Terra, Rua Nicolau Piragine, 253, Chácara Bela Vista, CEP 17209070 Jaú, SP, Brazil.
1
mafei.fabio@gmail.com (corresponding author), 2 tayarbio@gmail.com, 3 guimmoya@hotmail.com,
4
rjdonat@fc.unesp.br
Abstract: Mesoclemmys vanderhaegei is a poorly known freshwater
turtle widely distributed in central South America, where it occurs in
Argenina, Paraguay, Brazil, and probably Bolivia. It is considered “Near
Threatened” by the IUCN Red List and “Data Deicient” by other local
lists. Herein, we present new records and data on the reproducive
biology of Mesoclemmys vanderhaegei in southeastern Brazil.
Keywords: Cerrado, chelonians, repiles, South America.
Brazil has a great diversity of chelonians, including
ive species of sea turtles, 29 species of freshwater turtles
and two species of terrestrial tortoises (Costa & Bérnils
2015). Chelidae is the richest family in species with 20
representaives of seven genera (Acanthochelys, Chelus,
Hydromedusa, Mesoclemmys, Phrynops, Platemys and
Rhinemys; Costa & Bérnils 2015). Among the eight
species in the Mesoclemmys genus, M. vanderhaegei
(Toad-headed Turtle) is a medium-sized freshwater
turtle, which has a carapace length of approximately
250mm and inhabits shallow water bodies with dense
aquaic vegetaion (Marques et al. 2014). It is a
poorly known freshwater turtle widely distributed in
central South America, where it occurs in the Amazon,
Tocanins, Paraguay, Paraná, and Uruguay River basins
in associaion with open formaions (Souza 2005) in the
countries of Argenina, Paraguay, Brazil, and probably
Bolivia (Marques et al. 2014). In Brazil, this species has
been recorded in the states of Tocanins, Goiás, Distrito
Federal, Mato Grosso, Mato Grosso do Sul, Minas Gerais
and São Paulo, inhabiing Cerrado areas, but there is
only one record in the Atlanic Rainforest area in the
state of São Paulo (Bour & Pauler 1987).
Mesoclemmys vanderhaegei is considered “Near
Threatened” by the IUCN Red List (Tortoise & Freshwater
Turtle Specialist Group 1996). In the List of Brazilian
Fauna Threatened with Exincion, this species was
already classiied as “Data Deicient” (Machado et al.
2005), but is now categorized as “Least Concern” (Vogt
et al. 2015). The same category is presented in the
List of Fauna Species of Minas Gerais State, in which
this species was evaluated as “Data Deicient” in 2007
(Biodiversitas 2007), but is currently not listed. This
species is also present in the List of Endangered Fauna
of São Paulo State in the category of “Data Deicient”
(São Paulo 2014), while in Paraguay it is considered
DOI: htp://dx.doi.org/10.11609/jot.2643.8.11.9322-9326 | ZooBank: urn:lsid:zoobank.org:pub:C87AEA20-9175-448E-A6AE-2DDBC1BADAB1
Editor: Anonymity requested.
Date of publicaion: 26 September 2016 (online & print)
Manuscript details: Ms # 2643 | Received 24 March 2016 | Final received 08 September 2016 | Finally accepted 10 September 2016
Citaion: Mafei, F., B.T.M. do Nascimento, G.M. Moya & R.J. Donatelli (2016). New distribuion records of Mesoclemmys vanderhaegei (Testudines: Chelidae) from
southeastern Brazil, including observaions on reproducion. Journal of Threatened Taxa 8(11): 9322–9326; htp://dx.doi.org/10.11609/jot.2643.8.11.9322-9326
Copyright: © Mafei et al. 2016. Creaive Commons Atribuion 4.0 Internaional License. JoTT allows unrestricted use of this aricle in any medium, reproducion
and distribuion by providing adequate credit to the authors and the source of publicaion.
Funding: Duratex S.A. and FUNDIBIO.
Conlict of Interest: The authors declare no compeing interests.
Acknowledgements: Thanks to Duratex and Fundibio by the inance of the study in Estrela do Sul, Insituto Florestal de São Paulo for permission to research
in Águas de Santa Barbara, Decio Tadeu for helping in ield work, Virginia Bernardes and Chrisine Strussmann for the available literature, Fernanda Magno for
English translaion, and Flávio K. Ubaid for map.
LOGOs
9322
Mafei et al.
New records of Mesoclemmys vanderhaegei from southeastern Brazil
“Insuiciently Known” (Prado et al. 2012).
Despite its wide occurrence, there are few known
records of M. vanderhaegei in southeastern Brazil
(Bour & Pauler 1987; Souza et al. 2000; Silveira et al.
2009; Marques et al. 2013; Mendonça et al. 2013) and
studies are needed on the geographical distribuion and
populaion dynamics of this species (Vogt et al. 2015).
In this context, we present new records and addiional
data on the reproducive biology of Mesoclemmys
vanderhaegei.
Materials and Methods
An inventory of the herpetofauna was made at two
sites of Cerrado biome areas in southeastern Brazil, the
basin of Paraná River. At the irst site, ield visits were
conducted monthly in 2011 and 2012 in Águas de Santa
Barbara municipality, São Paulo State, totaling 24 visits.
The observaions were made in a small pond (60 x 60 m)
in the Ecological Staion of Santa Barbara (22048’50”S &
49014’11”W, alitude 620m). The pond is located in the
open area and its border is formed by grass and emergent
vegetaion. The water is crystal clear; the maximum
depth is 3 m; the low is slow and the water surface has
loaing macrophytes (Image 1). At the second site, ield
visits were conducted bimonthly between October 2014
and February 2016 in Estrela do Sul municipality, Minas
Gerais State, totaling nine visits. The observaions were
made in a small pond (35x45m) at Nova Monte Carmelo
Farm, Estrela do Sul municipality, Minas Gerais State
(18045’9”S & 47051’52”W, alitude 941m). This pond is
close to a crystal-clear stream in an open Cerrado area
(Image 2). At this site, a funnel trap (Bury et al. 2012)
was used during two days only in the third ield visit. The
captured individuals were marked based on the method
of Cagle (1939).
The chelonians were recorded according to the
permits SISBIO 30833-1 and 46085-1. The specimens
were ideniied according to Rueda-Almonacid et al.
(2007).
Results and Discussion
On 13 October 2011, a couple of Mesoclemmys
vanderhaegei (Images 3, 4 and 5) was manually captured
in Águas de Santa Bárbara. We collected and deposited
voucher specimens in the Herpetological Collecion
at the University of São Paulo, “Museu de Zoologia da
Universidade de São Paulo” (Numbers MZUSP T 4396 and
4397). On 16 October 2012 another adult individual was
seen in the same pond. Both records were obtained at
night (about 20:00 hr) while the animals were foraging.
On 27 February 2015 a female of Mesoclemmys
© Fábio Mafei
Image 1. Habitat of Mesoclemmys vanderhaegei observed at
the Ecological Staion of Santa Barbara, Águas de Santa Bárbara
municipality, state of São Paulo, southeastern Brazil
© Fábio Mafei
Image 2. Habitat of Mesoclemmys vanderhaegei at the Nova
Monte Carmelo Farm, municipality of Estrela do Sul, Minas Gerais,
southeastern Brazil
vanderhaegei (Image 6) in Estrela do Sul was captured
by using the “funnel trap” and kept in a plasic box at
the study base. The individual measured 206mm of
carapace length and 134mm of carapace width. On
the next day, the female laid seven eggs that had the
following measures (L x W mm, weight): Egg 1 - 23.7x18.9
mm, 9.1g; Egg 2 - 21.3x19.1 mm, 8.5g; Egg 3 - 22.3x18.9
mm, 8.1g; Egg 4 - 22.7x19.8 mm, 8.7g; Egg 5 - 23.9x19.3
mm, 9.3g; Egg 6 - 22.9x19.4 mm, 8.7g; Egg 7 - 22.3x17.9
mm, 7.5g. The eggs were incubated, but did not result
in hatchlings.
On 21 November 2015, a male individual was
manually captured in the same pond (Image 7). This
record was obtained at 21:00 hr and the animal was on
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9322–9326
9323
New records of Mesoclemmys vanderhaegei from southeastern Brazil
© Fábio Mafei
Image 3. A Couple of Mesoclemmys vanderhaegei observed at
the Ecological Staion of Santa Barbara, Águas de Santa Bárbara
municipality, state of São Paulo, southeastern Brazil
© Fábio Mafei
Image 5. Mesoclemmys vanderhaegei captured at the Ecological
Staion of Santa Barbara, Águas de Santa Bárbara municipality, state
of São Paulo, southeastern Brazil
the pond border. The individual measured 250mm of
carapace length and 160mm of carapace width. Both,
the female and the male were marked and returned to
the same capture site.
In the present study, a couple foraging was recorded
in October, corroboraing data of Rueda-Almonacid et
al. (2007) and Brito et al. (2009), who reported maing
in the spring and early summer, between September
and January. The clutch recorded in Estrela do Sul,
was observed in February, following the patern of the
species which has its spawning season in late summer
(Rueda-Almonacid et al. 2007). The recorded clutch size
(six eggs) it into the patern for this species, which is
6.5 eggs in nature (Rueda-Almonacid et al. 2007) and
6.4 eggs in capivity (Corazza & Molina 2004). The eggs
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Mafei et al.
© Fábio Mafei
Image 4. Female (let) and male (right) of Mesoclemmys
vanderhaegei observed at the Ecological Staion of Santa
Barbara, Águas de Santa Bárbara municipality, state of São Paulo,
southeastern Brazil
© Bruno Tayar Marinho do Nascimento
Image 6. Female of Mesoclemmys vanderhaegei observed at the
Nova Monte Carmelo Farm, municipality of Estrela do Sul, Minas
Gerais, southeastern Brazil.
© Bruno Tayar Marinho do Nascimento
Image 7. A Male of Mesoclemmys vanderhaegei observed at the
Nova Monte Carmelo Farm, municipality of Estrela do Sul, Minas
Gerais, southeastern Brazil.
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9322–9326
Mafei et al.
New records of Mesoclemmys vanderhaegei from southeastern Brazil
Figure 1. Map of distribuion of
Mesoclemmys vanderhaegei.
Records of Mendonça et al.
(2013) and Marques et al. (2014)
in yellow dots, and new records
in yellow squares.
had an average length of 22.7mm (± 0.9), and an average
width of 19.0mm (± 0.6) and mean weight of 8.6g (±0.6).
These are below the average values reported by Corazza
& Molina (2004): 34.1x26.9 mm, weight 14.4g. This
should be related to the female size. Wilkinson & Gibbons
(2005) reported that one of the factors contribuing to
the variability in egg size is the body size of the female.
Rueda-Almonacid et al. (2007) reported that the size
range of mature females of M. vanderhaegei is between
148mm and 285mm of carapace length, and the female
of this study showed an intermediate value (206mm).
However, Corazza & Molina (2004) did not observe any
staisically signiicant correlaion between the carapace
length of the female and the clutch size in capivity for
M. vanderhaegei.
In São Paulo State, this species was recorded at four
locaions. Souza et al. (2000) recorded the species in
Iirapina, ciing records in the ciies of Caieiras and São
Paulo (capital). Marques et al. (2013) recorded the
species in Angatuba. The present record is at 150km SW
from Iirapina and 100km NW from Angatuba (Fig. 1). In
Minas Gerais State, our record is the third in the state
and is at 200km SW from João Pinheiro (Silveira 2009)
and 450km W from Jaboicatubas (Mendonça et al.
2013). The records of Iirapina, Águas de Santa Barbara
and Jaboicatubas were in protected areas (Ecological
Staion of Iirapina, Ecological Staion of Santa Barbara
and Serra do Cipó Naional Park, respecively). The
records of Estrela do Sul and Angatuba (Marques et al.
2013) were obtained in private eucalyptus farms. These
records in protected and private areas in the southeast
of Cerrado are important. Souza et al. (2000) indicated
that even small reserves may be important for the
conservaion of this species, since some populaions
survive and reproduce in small remnants. The Cerrado
biome is considered a global hotspot, which is a
priority area for conservaion characterized by a large
concentraion of endemic species, rich biodiversity and
high threat level (Myers et al. 2000). More than half of
the areas of this biome has been modiied by humans
and only 2.2% are protected areas (Klink & Machado
2005). Maintenance of the protected areas where this
species occurs, protecion of the remaining Cerrado
and consequent perpetuaion of the natural resident
subpopulaions of M. vanderhaegei are eicient acions
for the conservaion of this species (Vogt et al. 2015).
Although considered “Near Threatened” by the IUCN Red
List (Tortoise & Freshwater Turtle Specialist Group 1996),
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9322–9326
9325
New records of Mesoclemmys vanderhaegei from southeastern Brazil
Mesoclemmys vanderhaegei has a wide distribuion
and is abundant at some locaions (e.g.: Brito et al.
2009; Marques et al. 2013). More recently, in 2012, the
IUCN Tortoise and Freshwater Turtle Specialist Group
evaluated the species as either Data Deicient or Near
Threatened (Turtle Taxonomy Working Group, 2014).
Moreover, this species is tolerant of degraded areas
(Rueda-Almonacid et al. 2007). This report extends the
distribuion of Mesoclemmys vanderhaegei to the east
of São Paulo State and Minas Gerais State and proposes
that its threat category should be changed to “Least
Concern”. The last evaluaion by the IUCN (Tortoise &
Freshwater Turtle Specialist Group 1996) was made 20
years ago, from that period to the present, the number
of records of this species has increased signiicantly,
making necessary an update in the threat category.
References
Biodiversitas (2007). Revisão das listas das espécies da lora e da fauna
ameaçadas de exinção do estado de Minas Gerais. Relatório Final,
Volume 3 (Resultados: Lista Vermelha da Fauna de Minas Gerais).
Downloaded on 21 March 2016.
Bour, R. & I. Pauler (1987). Idenité de Phrynops vanderhaegei Bour,
1973, et des espèces aines. Mésogée 47: 3–23.
Brito, E.S., C. Strussmann & J.M.F. Penha (2009). Populaion structure
of Mesoclemmys vanderhaegei (Bour, 1973) (Testudines: Chelidae)
in the Cerrado of Chapada dos Guimarães, Mato Grosso, Brazil.
Biota Neotropica 9(4): 246–248.
Bury, R.B., D.T. Ashton, D.J. Germano, N.E. Karraker, D.A. Reese &
K.E. Schlick (2012). Sampling of Turtles: Trapping and Snorkeling.
Northwesfauna 7: 37–50.
Corazza, S.S. & F.B. Molina (2004). Biologia reproduiva e conservação
ex-situ de Bufocephala vanderhaegei (Testudines, Chelidae).
Arquivos do Insituto Biológico 71: 210–213.
Costa, H.C. & R.S. Bérnils (2015). Répteis brasileiros: Lista de espécies
2015. Herpetologia Brasileira 4(3): 74–84.
Klink, C.A. & R.B. Machado (2005). Conservaion of the Brazilian
Cerrado. Conservaion Biology 19: 707–713.
Machado, A.B.M, C.S. Marins & G.M. Drummond (2005). Lista da
Fauna Brasileira Ameaçada de Exinção: incluindo as espécies Quase
Ameaçadas e Deicientes em Dados. Belo Horizonte: Fundação
Biodiversitas, 160p.
Marques, T.S., S. Böhm, E.S. Brito, M.R. Cabrera & L.M. Verdade
(2014). Mesoclemmys vanderhaegei (Bour 1973) – Vanderhaege’s
Toad-headed Turtle, Karumbé-hy, pp. 083.1–083.8. In: Rhodin,
A.G.J., P.C.H. Pritchard, P.P. van Dijk, R.A. Saumure, K.A. Buhlmann,
J.B. Iverson & R.A. Mitermeier (eds.). Conservaion Biology of
Freshwater Turtles and Tortoises: A Compilaion Project of the IUCN/
SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian
Research Monographs 5(7); htp://dx.doi.org/10.3854/crm.5.083.
vanderhaegei.v1.2014
Mafei et al.
Marques, T.S., N.R.F. Lara, L.A.B. Bassei, B.O. Ferronato, A. Malvásio
& L.M. Verdade (2013). Populaion structure of Mesoclemmys
vanderhaegei (Testudines, Chelidae) in a silvicultural system in
southeastern Brazil. Herpetology Notes 6: 179–182.
Mendonça, S.H.S.T., A.L. Silveira, R.O.L. Salles & M.C.C. Secco (2013).
Quelônios do Parque Nacional da Serra do Cipó e da Área de
Proteção Ambiental Morro da Pedreira (Minas Gerais): composição
faunísica e uso de ambientes. Anais do VI Congresso Brasileiro de
Herpetologia, Salvador, Brasil.
Myers, N., R.A. Mitermeier, C.G. Mitermeier, G.A.B. Fonseca &
J. Kent (2000). Biodiversity hotspots for conservaion prioriies.
Nature 403: 853–858.
Prado, W.S., T. Waller, D.A. Albareda, M.R. Cabrera, E. Etchepare,
A.R. Giraudo, V.G. Carman, L. Prosdocimi & E. Richard (2012).
Categorización del estado de conservación de las tortugas de la
República Argenina. Cuadernos de Herpetología 26(1): 375–388.
Rueda-Almonacid, J.V., J.L. Carr, R.A. Mitermeier, A.J.V. RodríguezMahech, R.B. Mast, R.C. Vogt, A.G.J. Rhodin, J. Ossa-Velásquez, J.N.
Rueda & C.G. Mitermeier (2007). Las Tortugas y los Cocodrilianos de
los Países Andinos del Trópico. Bogotá: Conservación Internacional,
538pp.
São Paulo (2014). Decreto 60.133/2014. Declara as espécies da
fauna silvestre ameaçadas de exinção, as quase ameaçadas e
as deicientes de dados para avaliação no Estado de São Paulo
e dá providências correlatas. Diário Oicial Poder Execuivo Seção I, São Paulo, 124(27): 25. Downloaded on 21 March 2016.
http://www.al.sp.gov.br/repositorio/legislacao/decreto/2014/
decreto-60133-07.02.2014.html
Silveira, A.L (2009). Geographic distribuion. Mesoclemmys
vanderhaegei. Herpetological Review 40: 235–236.
Souza, F.L. (2005). Geographical distribuion paterns of South
American side-necked turtles (Chelidae), with emphasis on Brazilian
species. Revista Española de Herpetología 19: 33–46.
Souza, F.L., M. Marins & R.J. Sawaya (2000). A new record and
observaions of Vanderhaege’s toad-headed turtle Phrynops
vanderhaegei (Testudines, Chelidae) in SE Brazil. Bolein de la
Asociación Herpetológica Española 11: 85–88.
Tortoise & Freshwater Turtle Specialist Group (1996). Mesoclemmys
vanderhaegei. The IUCN Red List of Threatened Species 1996:
e.T17084A6797906. Downloaded on 21 March 2016; htp://dx.doi.
org/10.2305/IUCN.UK.1996.RLTS.T17084A6797906.en
Turtle Taxonomy Working Group [van Dijk, P.P., J.B. Iverson, A.G.J.
Rhodin, H.B. Shafer, & R. Bour]. (2014). Turtles of the world, 7th
ediion: annotated checklist of taxonomy, synonymy, distribuion
with maps, and conservaion status. Chelonian Research
Monographs 5(7): 000.329–479; htp://dx.doi.org/10.3854/
crm.5.000.checklist.v7.2014
Vogt, R.C., C.K. Fagundes, Y.S.L. Bataus, R.A.M. Balestra, F.R.W.
Baista, V.M. Uhlig, A.L. Silveira, A. Bager, A.M. Baistella, F.L.
Souza, G.M. Drummond, I.J. Reis, R. Bernhard, S.H.S.T. Mendonça
& V.L.F. Luz (2015). Avaliação do Risco de Exinção de Mesoclemmys
vanderhaegei (Bour, 1973) no Brasil. Processo de avaliação do risco
de exinção da fauna brasileira. ICMBio. Downloaded on 21 March
2016. htp://www.icmbio.gov.br/portal/faunabrasileira/estado-deconservacao/7440-repteis-mesoclemmys-vanderhaegei-tartrugacabeca-de-sapo
Wilkinson, L.R. & J.W. Gibbons (2005). Paterns of reproducive
allocaion: Clutch and egg size variaion in three freshwater turtles.
Copeia 2005(4): 868–879.
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