Herpetology Notes, volume 7: 599-602 (2014) (published online on 25 October 2014)
First occurrence of Spirocamallanus sp. (Nematoda,
Camallanoidea) in a freshwater turtle, Hydromedusa tectifera
(Cope, 1869) (Testudines, Chelidae), from Brazil
Iara A. Novelli1*; Glenda F. Morton2; Israel T. Trindade2; Diego A. Neto-Silva and Fabiano M. Vieira3
Hydromedusa tectifera Cope, 1869 (Testudines,
Chelidae) is a freshwater turtle native of South America,
occurring in Argentina, Bolivia, Paraguay, Uruguay,
and Brazil (Ernst and Barbour, 1989; Fritz and Havaš,
2007). In Brazil, this species is distributed throughout
the states of São Paulo, Rio de Janeiro, Paraná, Santa
Catarina, Rio Grande do Sul, and Minas Gerais (Ernst
and Barbour, 1989; Fagundes and Bager, 2007; Fritz and
Havas, 2007). According to Souza (2005) all records of
H. tectifera in Brazil are from the Atlantic rainforest
biome. However, this species was also recorded in
the Pampa biome by Fagundes and Bager (2007) and
the Cerrado biome by Sousa and Novelli (2009). This
species feeds on leeches, annelids, gastropods, arachnids,
insects, fishes, and larval and adult of anurans (Bonino
et al., 2009; Cabrera, 1998).
Reports of the parasites of H. tectifera in Brazil are
scarce and restricted to parasitism by ectosymbiont
Platyhelminthes, Pentastomida, and Nematoda (e.g.,
Damborenea and Cannon, 2001; Junker et al., 2003;
Mascarenhas et al. 2013). Until the current study, the
Programa de Pós Graduação em Ciências Biológicas,
Comportamento e Biologia Animal, Universidade Federal de
Juiz de Fora, Rua José Lourenço Kelmer, Bairro Martelos,
Juiz de Fora, MG, CEP 36036-330, Brazil.
2
Centro Universitário de Lavras - UNILAVRAS, Lavras, MG,
Brazil.
3
Laboratório de Parasitologia de Peixes, Departamento de
Parasitologia Animal, Universidade Federal Rural do Rio de
Janeiro, Seropédica, RJ, Brazil.
*Corresponding author: [email protected]
1
only one report of nematodes parasitizing H. tectifera
from Brazil was made by Mascarenhas et al. (2013),
but these nematodes are not Spirocamallanus Olsen,
1952 (Camallanoidea, Camallanidae, Procamallaninae).
Therefore, the aim of this study is to report for the first
time the occurrence of nematodes Spirocamallanus sp.
in the small intestine of H. tectifera from Brazil.
We collected six nematodes in the small intestine
of a young female of H. tectifera (CRLZ no 331) that
was deposited in Coleção de Répteis do Laboratório
de Zoologia do Centro Universitário de Lavras –
UNILAVRAS. The host was originated from Cerrado
area at the Reserva Biológica Unilavras – Boqueirão
(21.346ºS, 44.990ºW, datum: WGS84), municipality of
Ingaí, Minas Gerais state, and was collected in January
2011. The host was identified according to Bonin et al.
(2006) and Ernst and Barbour (1989). The parasites were
fixed AFA (70% ethanol, 93 parts; 37% formalin, 5 parts;
glacial acetic acid, 2 parts) for 48 h, and preserved in 70%
ethanol with 5% glycerin. For light microscopy studies,
the nematodes were cleared in Amann’s lactophenol
(1: 1 : 2 : 1 phenol : lactic acid : glycerin : water).
Photomicrographs were made with Canon A3000IS
camera, with 12.1 megapixels of resolution, coupled to
the Olympus BX41 light microscope. Identification and
classification of nematodes to the generic level follows
Anderson et al. (2009) and Gibbons (2010). Voucher
specimens (CHIOC no 35950) were deposited in the
Instituto Oswaldo Cruz Helminthological Collection
(CHIOC), Rio de Janeiro, Brazil.
All nematodes were identified as Spirocamallanus
sp. (Figs. 1A-D), by having sclerotized bands of buccal
capsule in form of spiral (Fig. 1C) and the absence of
teeth at the base of buccal capsule (Anderson et al.,
2009). The morphological identification of species
of Spirocamallanus is only possible with study of
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Iara A. Novelli et al.
Figure 1. Spirocamallanus sp. (A) anterior region, (B) anterior region – detail of buccal capsule, (C) posterior region, tail (D)
posterior region, detail of tip of tail.
male specimens, and in the current study only female
nematodes were found. Therefore, it was not possible to
identify the species of this study.
Until the current study, in Brazil other five species of
nematodes of the family Camallanidae in freshwater
turtles are reported. Serpinema microcephalus (Dujardin,
1845) [= Cucullanus microcephalus Dujardin,
1845; Camallanus microcephalus (Dujardin, 1845);
Camallanus trispinosus (Leidy, 1851)] was the first
nematode Camallanidae reported in freshwater turtles
from Brazil, from specimens collected by the naturalist
Johann Natterer and identified by Diesing (1851). This
species was collected in the small intestine of specimens
of Peltocephalus dumerilianus (Schweigger, 1812)
(Testudines, Podocnemididae) (= Podocnemis tracaxa
Wagler, 1830) and Podocnemis expansa (Schweigger,
1812) (Testudines, Podocnemididae) in unspecified
locality in Brazil (Diesing, 1851; Ribeiro, 1940).
First occurrence of Spirocamallanus sp. in a freshwater turtle from Brazil
Another four species of Camallanidae occurs in
freshwater turtles in Brazil. Serpinema amazonicus
(Ribeiro, 1940) (= Camallanus amazonicus Ribeiro,
1940) was described as of specimens collected in the
small intestine of P. expansa in the State of Pará , Brazil
(Ribeiro, 1940, Ivashkin et al., 1971; Vicente et al.,
1993). Serpinema monospiculatus Freitas & Dobbin Jr.,
1962 was described as a parasite of the small intestine
of Mesoclemmys tuberculata (Luederwaldt, 1926) [=
Batrachemys tuberculata (Luederwaldt, 1926)] from
the State of Pernambuco (Freitas and Dobbin Jr. 1962),
and subsequently also recorded in the small intestine
of Mesoclemmys nasuta (Schweigger, 1812) [=
Batrachemys nasuta (Schweigger, 1812)] and Phrynops
geoffroanus (Schweigger, 1812) from the state of
Pernambuco (Freitas and Dobbin Jr., 1971; Vicente
et al., 1993). Serpinema magathi (Sprehn, 1932) (=
Camallanus maghati Sprehn, 1932) was recorded in the
small intestine of Kinosternon scorpioides (Linnaeus,
1766) from the state of Pernambuco , Brazil (Freitas
and Dobbin Jr., 1971; Vicente et al., 1993). Camallanus
sp. was reported in Acanthochelys spixii (Duméril and
Bibron, 1835) (Chelidae) and H. tectifera from the
State of Rio Grande do Sul, Brazil (Mascarenhas et
al.,2013).
Regarding the record of parasites in species of
Hydromedusa Wagler, 1830 (Testudines, Chelidae)
from Brazil, the only records in H. tectifera are the
ectosymbiont Temnocephala brevicornis Monticelli,
1889 (Platyhelminthes, Temnocephalidae) in hosts
from the State of São Paulo (Pereira and Cuocolo, 1941;
Damborenea and Cannon, 2001), Temnocephala sp.
in hosts from the State of Rio Grande do Sul (Soares
et al., 2007), Diesingia megastoma (Diesing, 1836)
(Maxillopoda, Pentastomida) parasitizing lungs of H.
tectifera from the State of Paraná (Junker et al., 2003),
and Spiroxys contortus (Rudolphi, 1819) (Nematoda,
Gnathostomatidae) and Camallanus sp. (Nematoda,
Camallanidae) parasitic in H. tectifera of the State
of Rio Grande do Sul (Mascarenhas et al. 2013). In
Hydromedusa maximiliani (Mikan, 1825) are registered
T. brevicornis in hosts from São Paulo, Rio de Janeiro,
Minas Gerais and Espírito Santo states (Pereira and
Cuocolo, 1941; Damborenea and Cannon, 2001; Novelli
et al., 2009), and the description of Polystomoides
brasiliensis Vieira, Novelli, Sousa & Souzalima, 2008
(Monogenea, Polystomatidae), a parasite of mouth and
esophagus of hosts in the Minas Gerais state (Vieira et
al., 2008).
In other South American countries the reports of
601
nematodes in H. tectifera are restricted to Argentina.
However, the species of this nematodes were not
identified (Alcade et al. 2010; Mascarenhas et al.,
2013).
In Brazil, until the current study, Spirocamallanus
species are recorded only in fishes. Thus, this is the first
report of Spirocamallanus sp. in a freshwater turtle from
Brazil.
Acknowledgements. Iara A. Novelli was supported by a
Postdoctoral fellowship from CAPES/PNPD (Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior, Brazil/Programa
Nacional de Pós-doutorado). Israel T. Trindade was supported
by a scientific initiation fellowship from Fundação de Amparo
à Pesquisa do Estado de Minas Gerais (PROBIC/FAPEMIG).
Fabiano Matos Vieira was supported by a Postdoctoral fellowship
from FAPERJ/CAPES (Fundação Carlos Chagas Filho de
Amparo à Pesquisa do Estado do Rio de Janeiro). This work
was performed under a permit from the Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renováveis (SISBIO/
IBAMA) (Process number 14740-1).
References
Alcalde, L., Derocco, N.N., Rosset, S.D. (2010): Feeding in
syntopy: diet of Hydromedusa tectifera and Phrynops hilarii
(Chelidae). Chelonian Conservation and Biology 9: 33–44.
Anderson, R.C., Chabaud, A.G., Willmott, S. (2009): Keys to
the nematode parasites of vertebrates. Wallingford, CAB
International.
Bonin, F., Devaux, B., Dupre, A. (2006): Turtles of the World.
London, A and C Black Publishers.
Bonino, M.F., Lescano, J.N., Haro, J.G., Leynaud, G. C. (2009):
Diet of Hydromedusa tectifera (Testudines-Chelidae) in a
mountain stream of Córdoba province, Argentina. AmphibiaReptilia 30: 545–554
Cabrera, M.R., Haro, J.G., Monguillot, J.C. (1986): Presencia
de Hydromedusa tectifera y Phrynops hilarii (TestudinesChelidae) en la Provincia de Córdoba. Academia Nacional de
Ciencias, Miscelánea 73: 1–10.
Damborenea, M.C., Cannon, L.R.G. (2001): On neotropical
Temnocephala (Platyhelminthes). Jounal of Natural History 35:
1103–1118.
Diesing, K.M. (1851): Systema Helminthum, Vol. II. Vindobonae,
Wilhelmum Braumüller.
Ernst, C.H., Barbour, R.W. (1989): Turtles of the world.
Smithsonian Institution Press, Washington.
Fagundes, C.K., Bager, A. (2007): Ecologia reprodutiva de
Hydromedusa tecifera (Testudines: Chelidae) no sul do Brasil.
Biota Neotropica 7: 179–184.
Freitas, J.F.T., Dobbin Jr., J.E. (1962): Novo nematódeo
camalanídeo parasito de quelônio. Atas da Sociedade de
Biologia do Rio de Janeiro 6: 5–7.
Freitas, J.F.T., Dobbin Jr., J.E. (1971): Contribuição ao
conhecimento da fauna helmintológica de quelônios no Estado
de Pernambuco, Brasil. Memórias do Instituto Oswaldo Cruz
602
Iara A. Novelli et al.
69: 33–39.
Fritz, U., Havas, P. (2007): Checklist of Chelonians of the World.
Vertebrate Zoology 57: 149–368.
Gibbons, L.M. (2010): Keys to the Nematode parasites of
Vertebrates. Supplementary Volume. Wallingford, CAB
International.
Ivashkin, V.M., Sobolev, A.A., Khromova, L.A. (1971):
Camallanata of Animals and Man and the Diseases Caused
by Them. Osnovy nematodologii 22. Moscow, Nauka (In
Russian.)
Junker, K., Riley, J., Boomker, J. (2003): Redescription of Diesingia
megastoma (Diesing, 1836) Sambon, 1922, a pentastomid
parasite from the South American terrapin Hydromedusa
tectifera Cope. Systematic Parasitology 56: 211–218.
Lema, T., Ferreira, M.T.S. (1990): Contribuição ao conhecimento
dos Testudines do Rio Grande do Sul (Brasil) – Lista sistemática
comentada (Reptilia). Acta Biologica Leopoldensia 12: 125–
164.
Mascarenhas, C.S., Souza, J.D., Coimbra, M.A.A., Müller, G.
(2013): Nematode parasites of Chelidae (Testudines) from
Southern Brazil. Parasitology Research 112: 3365–3368.
Novelli, I.A., Sousa, B.M., Carvalho, A.R., Bessa, E.C.A., SouzaLima, S. (2009): Ocorrência de Temnocephala brevicornis
Monticelli, 1889 (Platyhelminthes, Temnocephalidae) associada
a Hydromedusa maximiliani (Mikan, 1820) (Testudines,
Chelidae) em Juiz de Fora, Minas Gerais, Brasil. Revista
Brasileira de Zoociências 11: 175–179.
Pereira, C., Cuocolo, R. (1941): Estudos sobre Temnocephalidae
Monticelli, 1899, com estabelecimento de dois novos gêneros
australianos e descrição de duas novas espécies neotropicais.
Arquivos do Instituto Biologico 12: 101–127.
Ribeiro, D.J. (1940): Pesquisas helmintológicas realisadas no
Estado do Pará; VIII - Camallanus amazonicus n. sp. parasito de
Podocnemis expansa (Schw.). Memórias do Instituto Oswaldo
Cruz 35: 723–727.
Soares, J.F., Oliveira, C.B., Silva, A.S., Souza C.P., Monteiro,
S.G. (2007): Temnocefalídeo em tartaruga de água doce,
Hydromedusa tectifera, da região central do Rio Grande do Sul.
Ciência Rural 37: 901–903.
Sousa, B.M., Novelli, I.A. (2009): Reptilia, Testudines, Chelidae:
Hydromedusa tectifera: Distribution extension in Brazil. Check
List 5: 396–398.
Souza, F.L. (2005): The Brazilian Snake-necked Turtle,
Hydromedusa maximiliani. Reptilia 40: 47–51.
Vicente, J.J., Rodrigues, H.O., Gomes, D., Pinto, R.M. (1993):
Nematóides do Brasil. Parte III: Nematóides de Répteis. Revista
Brasileira de Zoologia 10: 19–168.
Vieira, F.M., Novelli, I.A., Sousa, B.M., SouzaLima, S. (2008):
A new species of Polystomoides Ward, 1917 (Monogenea:
Polystomatidae) from freshwater chelonians (Testudines:
Chelidae) in Brazil. Journal of Parasitology 94: 626–630.
Accepted by Mirco Solé
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in a freshwater turtle, Hydromedusa tectifera