327
RESEARCH NOTE / NOTA CIENTÍFICA
STRONGYLOIDES CRUZI (RHABDITIDA: STRONGYLOIDIDAE) IN OPHIODES STRIATUS
(SQUAMATA: ANGUIDAE) FROM BRAZIL: NEW HOST AND LOCALITY RECORDS WITH
TAXONOMIC COMMENTS ON STRONGYLOIDES OF LIZARDS
STRONGYLOIDES CRUZI (RHABDITIDA: STRONGYLOIDIDAE) EN OPHIODES STRIATUS
(SQUAMATA: ANGUIDAE) EN EL BRASIL: NUEVOS REGISTROS DE HUÉSPED Y
LOCALIDAD CON COMENTARIOS TAXONÓMICOS SOBRE STRONGYLOIDES DE LOS
LAGARTOS
Vitor Luís Tenório Mati, Hudson Alves Pinto & Alan Lane de Melo
Abstract
Keywords: Ophiodes striatus – reptile - Strongyloides cruzi - strongyloidiasis
Suggested citation: Mati, VLT, Pinto, HA & Melo, AL. 2013. Strongyloides cruzi (Rhabditida: Strongyloididae) in Ophiodes
striatus (Squamata: Anguidae) from Brazil: new host and locality records with taxonomic comments on Strongyloides of lizards.
Neotropical Helminthology, vol. 7, n°2, jul-dec, pp. 327 - 333.
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas
Gerais, Belo Horizonte, Minas Gerais, Brazil. C.P. 486, 30123-970.
E-mail: vitormati@yahoo.com.br
Neotrop. Helminthol., 7(2), 2013
2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
Strongyloides cruzi Rodrigues, 1968 was found in Ophiodes striatus (Spix, 1825) from Itabirito,
state of Minas Gerais, Brazil. The morphology of the nematodes obtained was briefly described
and compared with previous reports of Strongyloides spp. from lizards. Taxonomic comments
about these parasites are presented and a species of Strongyloides, a genus whose members have
rarely been reported in lizards, is for the first time observed in an anguid reptile.
Resumen
Palabras clave: Estrongiloidosis, Ophiodes striatus, reptil, Strongyloides cruzi.
Strongyloides cruzi Rodrigues, 1968 fue encontrado en Ophiodes striatus (Spix, 1825) en
Itabirito, estado de Minas Gerais, Brasil. La morfología de los nematodos obtenidos es descrita
brevemente y comparada con reportes previos de Strongyloides spp. en lagartos. Comentarios
taxonómicos sobre estos parásitos son presentados y una especie de Strongyloides, un género
cuyos integrantes rara veces se han observado en lagartos, es reportado por primera vez en un
reptil ánguido.
from Brazil, and a new location of occurrence of
the parasite are presented. Additionally,
taxonomic aspects correlated to Strongyloides
spp. of lizards, whose reports were scattered in
the literature, are discussed.
One golden specimen of anguid lizard from
Itabirito (20°15'10''S, 43°48'03''W),
metropolitan region of Belo Horizonte, state of
Minas Gerais, southeastern Brazil, was already
dead when it was sent to the laboratory,
identified as O. striatus (Peters & Donoso-
Barros, 1970; Hoogmoed & Gruber, 1983),
necropsied and after deposited in the collection
of the Department of Parasitology, UFMG
(DPIC 2414). Viscera were separated in Petri
dishes containing saline (0.85% NaCl) and
examined with aid of a stereomicroscope to
recover parasites which were fixed in 10%
formalin and then analyzed with aid of a light
microscope. Images were obtained using a Leica
ICC50 HD digital camera attached to the
microscope, and measurements were obtained
by analyzing the captured images using the
Leica Application Suite (LAZ EZ) software,
version 2.0. Taxonomic identification of the
parasites was based on morphological criteria
according different authors (Little, 1966a, b;
Rodrigues, 1968, 1970; Sharpilo, 1973; Roca &
Hornero, 1992; Vicente et al., 1993). Nematode
specimens were deposited in the same collection
(DPIC 6274).
Specimens of minuscule nematodes were
collected from the large intestine of the O.
striatus necropsied. Measurements and the main
taxonomic traits of the parasites recovered in the
present study and data of Strongyloides from
lizards reported by other authors are presented in
Table 1. After morphological analysis the
parasite was identified as Strongyloides cruzi
Rodrigues, 1968 (Figs. 1-3, Table 1).
There is still a substantial deficit in knowledge of
helminths from Neotropical reptiles, and
considering existing information about parasites
from lizards, the number of species known to
parasitize these animals is proportionally lesser
than that of other reptiles (Ávila & Silva, 2010),
perhaps due to shortage of surveys of their
helminth fauna.
Among the South American species of lizards,
the Striped Worm Lizard Ophiodes striatus
(Spix, 1825) occurs in northern Argentina,
Paraguay, Uruguay and Brazil (Peters &
Donoso-Barros, 1970; Bérnils & Costa, 2012;
Cacciali & Scott, 2012). Ophiodes spp. present a
cylindrical and elongate body with hind limbs
only that are reduced and flap-like (Peters &
Donoso-Barros, 1970). The taxonomy of these
lizards is complicated and O. striatus may be a
species complex. Some authors based on
unpublished information have considered O.
fragilis (Raddi, 1820), for example, as other
valid species from Brazil (Gutsche et al., 2007;
Cacciali & Scott, 2012), and the color of
Ophiodes might be useful in the specific
identification (Lema, 2002).
Without doubt helminths from these lizards need
to be further studied, since only two species of
nematodes have been reported in anguid host in
the continent: Cyrtosomum sp. and
Physaloptera retusa Rudolphi, 1819 in O.
striatus from Brazil (Baker, 1987, Ávila & Silva,
2010; Ávila et al., 2010).
Strongyloides spp. have been recorded in
different reptile hosts worldwide, including the
species S. cruzi Rodrigues, 1968, S. ophiusensis
Roca & Hornero, 1992 and S. darevskyi
Sharpilo, 1976 described from lizards
(Rodrigues, 1968, 1970; Sharpilo, 1973, 1976;
Roca & Hornero, 1992; Khanum et al., 2002;
Murvanidze et al., 2008). Moreover,
unidentified Strongyloides have also been
reported in these reptiles (Perera et al., 2013).
In the present note, the first record of
Strongyloides in an anguid lizard, O. striatus
INTRODUCTION
Mati et al.
Strongyloides cruzi in Ophiodes striatus from Brazil.
MATERIAL AND METHODS
RESULTS
328
Neotrop. Helminthol., 7(2), 2013
third from the anterior end, similar to that was
described for S. darevskyi, however, in previous
reports (Rodrigues, 1968, 1970), and also in the
present study, the nerve ring of S. cruzi was not
observed.
As other species of Strongyloides of lizards, S.
cruzi differs from Strongyloides of snakes
mainly by smaller size of body and esophagus,
shorter distance between the mouth and vulva,
and, except in relation to S. natricis, Navarro &
Lluch, 1993, shape of ovaries (Pereira, 1929;
Singh, 1954; Little, 1966b; Navarro & Lluch,
1993; Santos et al., 2010). Furthermore,
Strongyloides spp. from snakes usually have the
tails more sharply pointed and a greater number
of eggs in uteri than the species from lizards. In
fact, tails of Strongyloides from these reptiles are
in general short and narrow posteriorly to the
anus terminating in a blunt moderately tip (Fig.
3).
Reports of Strongyloides spp. from lizards are
scarce and the present study, despite sampling
limitations, contribute to knowledge about these
nematodes from Neotropical reptiles, especially
when considering also the taxonomic comments
that were presented.
Until now, S. cruzi is the only representative of
the genus Strongyloides already recorded in
New World lizards, although this species has
been reported in Asian H. flaviviridis by
Khanum et al. (2002) that suggested a wide
distribution of the parasite. However, the
specificity of Strongyloides spp. to the host is
usually not limited to generic level of the host,
since a same species of Strongyloides has been
reported in different families of hosts (Little,
1966a, b). In the present study, the find of S.
cruzi in a new host species of the family
Anguidae for which hitherto there was no record
of parasitism by Strongyloides may also suggest
the existence of certain unspecificity of this
parasite to its lizard hosts.
Taxonomic summary
Host: Ophiodes striatus (new host).
Locality: Itabirito, Metropolitan region of Belo
Horizonte, State of Minas Gerais, Brazil (new
locality).
Site of infection: Large intestine.
Intensity of infection: 3 specimens.
Other hosts and localities reported:
Hemidactylus mabouia (Moreau de Jonnès,
1818) (host type), Rio de Janeiro, Brazil
(Rodrigues, 1968, 1970); H. flaviviridis
Rüppell, 1835, Dhaka, Bangladesh (Khanum et
al., 2002).
Remarks: Strongyloides cruzi was described
from one single specimen of H. mabouia from
Brazil and differs from the species S.
ophiusensis and S. darevskyi reported in lizards
from Balearic Islands (Spain) and Transcaucasia
(Azerbaijan and Georgia), respectively, by its
longer and wider body, higher number of
intrauterine eggs (slightly shorter in size), longer
tail and distinct shapes of ovaries. In the
specimens of S. cruzi analysed, the anterior
ovary was spiraled twice around intestine and
posterior ovary presented one or one and half
spiral, and this shape of ovaries is in accordance
with the figure of the parasite provided by
Rodrigues (1970). The anterior ovary of S.
ophiusensis forms one spiral around the intestine
and the posterior ovary lies parallel to the organ
(Roca & Hornero, 1992). Ovaries of S. darevskyi
are oftentimes also spiraled, but details on their
shapes were not related in the description.
However, a posterior ovary with partial spiral is
noticeable based on the drawing of the parasite
(Sharpilo, 1973, 1976). Strongyloides
ophiusensis and S. darevskyi are more closely
related to each other than with S. cruzi and
additional morphological studies on these two
species are still desirable. However, the body of
S. ophiusensis is shorter and thinner than S.
darevskyi. Eggs of the former species are
narrower and can achieve greater length, the
nerve ring is to a shorter distance from the mouth
and the vulva is about three-fourth of the body
length from the anterior end (Sharpilo, 1973,
1976; Roca & Hornero, 1992). On the other
hand, the vulva of S. cruzi is located in the two-
DISCUSSION
329
Figures 1-3. Parasitic female of Strongyloides cruzi: (1) total view; (2) detail of vulva and intrauterine eggs, lateral view; (3) tail,
lateral view.
Table 1. Morphological data of Strongyloides cruzi found in Ophiodes striatus from Brazil and other Strongyloides
spp. of lizards reported by different authors. Abbreviations: NA: not available; L: length; W: width; A: anterior; P:
posterior.
Strongyloides cruzi S. ophiusensis S. darevskyi
Present study Rodrigues (1968) Rodrigues (1970) Roca & Hornero
(1992)
Sharpilo (1976)
(n = 3) (n = 3) (n = NA) (n = 26) (n = 10)
Body L 2,307 ± 162
(2,123-2,430)
1,630-2,910
1,630-3,220
1,140 ± 127
(880-1,456)
1,400-1,600
W 47 ± 4 (43-50)
40-90
40-90
28 ± 3 (23-34)
33-36
Esophagus L 637 ± 42 (589-667)
525-632
525-728
479 ± 50 (372-592) 460-600
Mouth to vulva L 1,496 ± 387
(1,403-1,575)
1,295-1,790
1,295-2,050
806 ± 76
(652-956)
920-1,050
Tail L 73 ± 3 (70-77)
74-81
72-81 51 ± 4 (42-58)
49-60
Shape of
ovaries
A Two spirals
NA
Spiraled (two spirals*)
One spiral
Spiraled
P One or one and half
spiral
NA
Spiraled (one and half
spiral*)
Parallel to the
intestine
(One half spiral*)
Intrauterine
eggs
N 5 ± 2 (2-7)
Few eggs
Few eggs
2
1-3
Eggs L
W
45 ± 4 (40-50)
30 ± 3 (26-33)
49-55
33-35
39-55
25-35
55 ± 5 (48-68)
28 ± 2 (18-26)
50-60
27-30
Locality Brazil
(Minas Gerais)
Brazil
(Rio de Janeiro)
Brazil
(Rio de Janeiro)
Spain
(Balearic Islands)
Azerbaijan and Georgia
Host Ophiodes striatus Hemidactylus
mabouia Hemidactylus
mabouia Podarcis pityusensis Darevskia saxicola
* Information about shape of ovaries based on figures presented by authors, since detailed descriptions have not been provided in the text of the respective studies.
Mati et al.
Strongyloides cruzi in Ophiodes striatus from Brazil.
330
Neotrop. Helminthol., 7(2), 2013
In helminthological surveys performed in
lizards, many of them with a substantial number
of animals sampled, species of Strongyloides
have not been found (Lewin, 1990, 1992a, b;
Fontes et al., 2003; Goldberg et al., 2006, 2007;
Adeoye & Ogunbanwo, 2007; Ávila et al., 2010,
2011; Ávila & Silva, 2011; Albuquerque et al.,
2012) indicating that the parasite may be rare in
this host group. In fact, the prevalence of
infection of Podarcis pityusensis (Boscá, 1883)
with S. ophiusensis was 1.2% and the mean
intensity was 9.7 (Roca & Hornero, 1992). In
relation to S. cruzi from H. flaviviridis the mean
prevalence and intensity were 5.8 and 4.6 ± 2.5,
respectively (Khanum et al., 2002). Due to this
low intensity of infection and the consequent
difficulty in diagnosis of the infection, a
molecular screening of Strongyloides in lacertid
lizards has recently been proposed (Perera et al.,
2013). However, higher prevalences of S.
darevskyi (up to 75%) with variable intensity of
infection (1-55) were found in some populations
of Darevskia spp. from Transcaucasia (Sharpilo,
1973, 1976). In addition to the type host D.
saxicola (Eversmann, 1884), this author
reported S. darevskyi in D. armeniaca (Méhely,
1909), D. rostombekovi (Darevsky, 1957) and D.
rudis (Bedriaga, 1886).
In the present study new locality and host for S.
cruzi are reported. No record of parasitism by
any species of Rhabditida, not only of
Strongyloides, had so far been carried out for O.
striatus. The diversity of potential hosts and
distribution of S. cruzi are likely underestimated
and studies aiming to elucidated new interaction
between Neotropical lizards and their parasites
are still necessary.
To Miss Ana Paula M. Oliveira from our library
and researchers worldwide for their kindness in
helping us with bibliographies, especially the
book and manuscript by Sharpilo.
ACKNOWLEDGMENTS
BIBLIOGRAPHIC REFERENCES
Adeoye, GO & Ogunbanwo, OO. 2007.
Albuquerque, S, Ávila, RW & Bernarde, PS.
2012.
Ávila, RW & Silva, RJ. 2010.
Ávila, RW & Silva, RJ. 2011.
Ávila, RW, Cardoso, MW, Oda, FH & Silva, RJ.
2011.
Ávila, RW, Souza, FL & Silva, RJ. 2010.
Baker, MR. 1987.
Bérnils, RS & Costa, HC. 2012.
Cacciali, P & Scott, NJ. 2012.
Fontes, AF, Vicente, JJ, Kiefer, MC & Sluys,
Helminth parasites of the African lizard
Agama agama (Squamata: Agamidae), in
Lagos, Nigeria. Revista de Biologia
Tropical, vol. 55, pp. 417-425.
Occurrence of helminths in lizards
(Reptilia: Squamata) at lower Moa river
forest, Cruzeiro do Sul, Acre, Brazil.
Comparative Parasitology, vol. 79, pp. 64-
67. Checklist of
h e l m i n t h s f ro m l i z a rd s a n d
amphisbaenians (Reptilia, Squamata) of
South America. Journal of Venomous
Animals and Toxins including Tropical
Diseases, vol. 16, pp. 543-572.
Helminths of
lizards (Reptilia: Squamata) from Mato
Grosso state, Brazil. Comparative
Parasitology, vol. 78, pp. 129-139.
Helminths from lizards (Reptilia:
Squamata) at the Cerrado of Goiás state,
Brazil. Comparative Parasitology, vol. 78,
pp. 120-128.
Helminths from seven species of lizards
(Reptilia: Squamata) at the Cerrado of
Mato Grosso do Sul State, Brazil.
Comparative Parasitology, vol. 77, pp. 67-
71. Synopsis of the Nematoda
parasitic in amphibians and reptiles.
Memorial University of Newfoundland,
Occasional Papers in Biology, vol. 11, pp.
1- 325. Répteis
brasileiros: lista de espécies. Versão
2012.2. Sociedade Brasileira de
Herpetologia, accessed in May 13, 2013,
<http://www.sbherpetologia.org.br>
Revisión del
género Ophiodes de Paraguay
(Squamata: Anguidae). Boletín de la
a
Sociedad Zoológica del Uruguay, 2
época, vol. 21, pp. 1-8.
331
MV. 2003.
Goldberg, SR, Bursey, CR, Caldwell, JP, Vitt, L
& Costa, GC. 2007.
Goldberg, SR, Bursey, CR & Vitt, LJ. 2006.
Gutsche, A, Kwet, A, Kucharzewski, C &
Hallermann, J. 2007.
Hoogmoed, MS & Gruber, U. 1983.
Khanum, H, Sultana, R, Alam, MS & Zaman,
RF. 2002.
Lema, T. 2002.
Lewin, J. 1990.
Lewin, J. 1992a.
Parasitism by helminths in
Eurolophosaurus nanuzae (Lacertilia:
Tropiduridae) in an area of rocky outcrops
in Minas Gerais State, Southeastern
Brazil. Journal of Herpetology, vol. 37,
pp. 736-741.
Gastrointestinal
helminths from six species of frogs and
three species of lizards, sympatric in Pará
state, Brazil. Comparative Parasitology,
vol. 74, pp. 327-342.
Helminths of the Brown-eared anole,
Norops fuscoauratus (Squamata,
Polychrotidae), from Brazil and Ecuador,
South America. Phyllomedusa, vol. 5, pp.
83-86.
Historical
collections of amphibians and reptiles
from Brazil by Wilhelm Ehrhardt,
deposited at the Zoological Museum of the
University of Hamburg. Mitteilungen aus
dem Hamburgischen Zoologischen
Museum und Institut, vol. 104, pp. 175-
194. Spix and
Wagler type specimens of reptiles and
amphibians in the Natural History
Museum in Munich (Germany) and
Leiden (The Netherlands). Spixiana, vol.
9 (Suppl.), pp. 319-415.
Endoparasitic helminth
infection in Hemidactylus flaviviridis
(Ruppel, 1835). University Journal of
Zoology, Rajshahi University, vol. 21, pp.
17-19. Os répteis do Rio Grande do Sul:
atuais e fósseis, biogeografia e ofidismo.
EDIPUCRS, Porto Alegre.
Parasitic worms in a slowworm
(Anguis fragilis L.) population from the
Bieszczady Mountains (Poland). Acta
Parasitologica Polonica, vol. 35, pp. 207-
215. Parasites of Lacerta vivipara
Jacquin, 1787 in Poland. Acta
Parasitologica, vol. 37, pp. 79-82.
Lewin, J. 1992b.
Little, MD. 1966a.
Little, MD. 1966b.
Murvanidze, L, Lomidze, T, Nikolaishvili, K &
Jankarashvili, E. 2008.
Navarro, P & Lluch, J. 1993.
Pereira, C. 1929.
Perera, A, Maia, JP, Jorge, F & Harris DJ. 2013.
Peters, JA & Donoso-Barros, R. 1970.
Roca, V & Hornero, MJ. 1992.
Rodrigues, HO. 1968.
Rodrigues, HO. 1970.
Parasites of the sand lizard
(Lacerta agilis L.) in Poland. Acta
Parasitologica, vol. 37, pp. 19-24.
Comparative morphology of
six species of Strongyloides (Nematoda)
and redefinition of the genus. Journal of
Parasitology, vol. 52, pp. 69-84.
Seven new species of
Strongyloides (Nematoda) from
Louisiana. Journal of Parasitology, vol.
52, pp. 85-97.
The annotated list
of reptile helminths of Georgia.
Proceedings of the Institute of Zoology,
Tbilisi, vol. 23, pp. 54-61. Strongyloides
natricis sp. n. (Strongyloididae), un
nouveau nématode parasite de Natrix
maura (L. 1758) (Colubridae) en
Espagne. Annales de Parasitologie
Humaine et Comparée, vol. 68, pp. 136-
138. Strongyloides ophidiae n. sp.
Boletim Biológico, vol. 22, pp. 16-18.
Molecular screening of nematodes in
lacertid lizards from the Iberian
Peninsula and Balearic Islands using 18S
r R N A s e qu en c e s . J ou rn al o f
Helminthology, vol. 87, pp. 189-194.
Catalogue of the Neotropical Squamata
Part. II: Lizards and Amphisbaenians.
United States National Museum Bulletin,
297. Smithsonian Institution Press,
Washington. Strongyloides
ophiusensis sp. n. (Nematoda:
Strongyloididae), parasite of an insular
lizard, Podarcis pityusensis (Sauria:
Lacertidae). Folia Parasitologica, vol. 39,
pp. 369-373. Sobre nova espécie do
gênero "Strongyloides" Grassi, 1879
(Nematoda, Rhabdiasoidea). Atas da
Sociedade de Biologia do Rio de Janeiro,
vol. 12, pp. 31-32. Estudo da fauna
helmintológica de Hemidactylus mabouia
Mati et al.
Strongyloides cruzi in Ophiodes striatus from Brazil.
332
Neotrop. Helminthol., 7(2), 2013
(M. de J.) no Estado da Guanabara. Atas
da Sociedade de Biologia do Rio de
Janeiro, vol. 12 (Suppl.), pp. 15-23.
Morphological and molecular
characterization of Strongyloides
ophidiae (Nematoda, Strongyloididae).
Journal of Helminthology, vol. 84, pp.
136-142. First findings of
representatives from the genus
Strongyloides Grassi, 1879 (Nematoda,
Strongyloididae) in reptiles of Europe,
Transcaucasia and Middle Asia.
Dopovidi Akademiyi Nauk Ukrayins'koi
RSR, Seriya B, vol. 11, pp. 1047-1050. (in
Ukrainian). The parasitic helminths of
reptiles of fauna of USSR. Naukova
Dumka, Kiev. (in Russian).
Studies on the morphology and
life-history of Strongyloides mirzai n. sp.
Santos, KR, Carlos, BC, Paduan, KS, Kadri,
SM, Barrella, TH, Amarante, MR,
Ribolla, PE & Silva, RJ. 2010.
Sharpilo, VP. 1973.
Sharpilo, VP. 1976.
Singh, SN. 1954.
from snakes in India. Journal of
Helminthology, vol. 28, pp. 25-34.
Nematóides do Brasil.
Parte III: nematóides de répteis. Revista
Brasileira de Zoologia, vol.10, pp. 19-
168.
Vicente, JJ, Rodrigues, HO, Gomes, DC &
Pinto, RM. 1993.
Correspondence to author/ Autor para
correspondencia:
Vitor Luís Tenório Mati
Laboratório de Taxonomia e Biologia de
Invertebrados, Departamento de Parasitologia,
Instituto de Ciências Biológicas, Universidade
Federal de Minas Gerais, Belo Horizonte, Minas
Gerais, Brazil. C.P. 486, 30123-970.
E-mail / Correo electrónico:
vitormati@yahoo.com.br
Received May 15, 2013.
Accepted June 22, 2013.
333
