349
Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FIRST REPORT FROM THE STATE OF RIO GRANDE DO SUL, BRAZIL ON
CYLICOSPIRURA (CYLICOSPIRURA) FELINEUS (CHANDLER, 1925) SANDGROUND, 1932
(NEMATODA, SPIROCERCIDAE) IN LEOPARDUS GEOFFROYI D'ORBIGNY & GERVAIS, 1844
(CARNIVORA, FELIDAE)
CYLICOSPIRURA (CYLICOSPIRURA) FELINEUS (CHANDLER, 1925) SANDGROUND, 1932
(NEMATODA, SPIROCERCIDAE) EM LEOPARDUS GEOFFROYI D'ORBIGNY & GERVAIS,
1844 (CARNIVORA, FELIDAE): PRIMEIRO REGISTRO PARA O ESTADO DO RIO GRANDE
DO SUL, BRASIL
1 1 2
Moisés Gallas ; Eliane Fraga da Silveira & Eduardo Périco
1 Laboratório de Zoologia de Invertebrados, Museu de Ciências Naturais, Universidade Luterana do Brasil. 92425-900, Canoas, RS, Brasil.
mgallas88@gmail.com
2 Laboratório de Ecologia, Museu de Ciências Naturais, Centro Universitário UNIVATES. 95900-000, Lajeado, RS, Brasil.
Resumo
Palavras-chave: felídeos - gato-do-mato-grande - helmintofauna - nematoide - Região Neotropical - taxonomia.
Para a Região Neotropical, a única espécie de Cylicospirura registrada para felídeos silvestres foi
Cylicospirura (Cylicospirura) subaequalis no Paraguai e Brasil. Durante 2007 e 2009, espécimes
atropelados de Leopardus geoffroyi (n = 6) foram doados para necropsia. Nematoides encontrados
no estômago foram identificados como Cylicospirura (Cylicospirura) felineus pela presença de
seis dentes trífidos, vulva anterior à junção do esôfago com intestino e, tamanho dos espículos. A
prevalência de C. (C.) felineus em L. geoffroyi foi 16,7%. Não foram observadas lesões causadas
pelos nematoides no hospedeiro infectado, como registrado em outros estudos. Este é o primeiro
registro de C. (C.) felineus para a Região Neotropical (Estado do Rio Grande do Sul, Brasil) e, L.
geoffroyi como novo hospedeiro.
Suggested citation Gallas, M, da Silveira, EF & Périco, E. 2014. Cylicospirura (Cylicospirura) felineus (Chandler, 1925)
Sandground, 1932 (Nematoda, Spirocercidae) in Leopardus geoffroyi D'orbigny & Gervais, 1844 (Carnivora, Felidae): first
report from the State of Rio Grande do Sul, Brazil. Neotropical Helminthology, vol. 8, n°2, jul-dec, pp. 349-355.
Abstract
Keywords: felines - Geoffroy's Cat - helminth fauna – nematode - Neotropical Region - taxonomy.
In the Neotropical Region, the only species of Cylicospirura reported so far in felines is
Cylicospirura (Cylicospirura) subaequalis in Paraguay and Brazil. Between 2007 and 2009,
roadkilled specimens of Leopardus geoffroyi (n = 6) were donated for necropsy. Nematodes found
in the stomach of one individual were identified as Cylicospirura (Cylicospirura) felineus by the
presence of six large tricuspid teeth, a vulva anterior to the junction of the esophagus and intestine,
and the size of the spicules. The prevalence of C. (C.) felineus in L. geoffroyi was 16.7%. No
lesions caused by the nematodes were found in the infected feline, as reported in other studies.
This is the first report of C. (C.) felineus in the Neotropical Region (State of Rio Grande do Sul,
Brazil) and L. geoffroyi represents a new host.
Gallaset al.
Cylicospirura felineus in Leopardus
The genus Cylicospirura was originally
proposed to accommodate the species
Spiroptera subaequalis Molin, 1860, due the
differences found in the morphology of the
buccal capsule (Vevers, 1922). Three subgenera
were subsequently proposed by Chabaud
(1975): Cylicospirura Vevers, 1922 (parasites of
carnivores), Gastronodus Singh, 1934 (parasites
of insectivores) and Skrjabinocercina
Matschulsky, 1952 (parasites of rodents),
although this arrangement was not accepted by
Junker et al. (2013) who elevated all these taxa
to the genus level.
Chandler (1925) described Spirocerca felineus
Chandler, 1925 from specimens removed from
cysts collected from the stomach of domestic
cats in India. This nematode was subsequently
transferred to the genus Cylicospirura, based on
the examination of specimens collected from
Felis bengalensis (= Prionailurus bengalensis
Kerr, 1792) in Indochina by Sandground (1932).
Cylicospirura (Cylicospirura) subaequalis
(Molin, 1860) Vevers, 1922, and Cylicospirura
(Cylicospirura) felineus (Chandler, 1925)
Sandground, 1932 have all been considered to be
synonymous, although Pence et al. (1978) and
Waid & Pence (1988) consider them to be valid
species.
In North America, C. (C.) felineus has been
reported in two host species: Felis rufus (= Lynx
rufus Schreber, 1777) in United States (Pence et
al., 1978; Tiekotter, 1985; Waid & Pence, 1988;
Ferguson et al., 2011) and Felis canadensis (=
Lynx canadensis Kerr, 1792) in Canada (Pence
et al., 1978; Smith et al., 1986). Domestic and
wild felines in Asia, Africa, and Oceania have
also been reported as hosts of C. (C.) felineus
(Yamaguti, 1961; Ferguson et al., 2011; Junker
et al., 2006, 2013).
However, there are few data on the distribution
of the Cylicospirura species in South America
(Junker et al., 2006). In Paraguay, Junker et al.
(2006) recorded C. (C.) subaequalis parasitizing
Herpailurus yaguarondi (= Puma yagouaroundi
É. Geoffroy Saint-Hilaire, 1803), while in
Brazil, Yamaguti (1961) recorded the species in
Felis concolor (= Puma concolor Linnaeus,
1771) and Felis mellivora (= P. yagouaroundi ?).
The present study reports the occurrence of C.
(C.) felineus for the first time in the Neotropical
Region (State of Rio Grande do Sul, Brazil), and
Leopardus geoffroyi d'Orbigny & Gervais, 1844
as new host.
Six roadkilled specimens of L. geoffroyi were
collected during the monitoring of the road
system in the State of Rio Grande do Sul, Brazil
between 2007 and 2009. The felines were
donated to the 'Laboratório de Zoologia dos
Invertebrados' of the 'Museu de Ciências
Naturais da ULBRA'. The collection and
transportation of the specimens was conducted
according to normative ruling no. 154 of March
1st, 2007, chapter VI, article 26 (Ibama, 2007).
The nematodes found in these specimens were
fixed in A.F.A. (glacial acetic acid, formalin and
ethanol) at 65º C, and the helminths were
mounted temporally with Amann's lactophenol
for the visualization and measurement of
morphological characters (Humason, 1972;
Amato & Amato, 2010).
All measurements are given in micrometers
(μm) unless otherwise indicated. The range of
values (minimum–maximum) are presented for
the eggs, together with the mean, standard
deviation, and number of eggs measured
between parentheses. Ecological terminology
followed Bush et al. (1997). The drawings were
produced using a drawtube attached to the
microscope. The systematic and identification of
the parasite was based on Chabaud (2009), and
that of the host following Wozencraft (2005). A
representative specimen of the host was
deposited in the 'Coleção de Vertebrados' of the
'Museu de Ciências Naturais da ULBRA'
(MCNU), Canoas, Brazil; and voucher
specimens of the helminths were deposited in
the 'Coleção Helmintológica' of the 'Museu de
Ciências Naturais da ULBRA' (CHMU).
INTRODUCTION
MATERIALS AND METHODS
350
Neotrop. Helminthol., 8(2), 2014
Cylicospirura (Cylicospirura) felineus
(Chandler, 1925) Sandground, 1932.
(Figures 1 and 2)
Description based on two specimens, clarified in
lactophenol. Spirocercidae, Spirocercinae.
Nematodes of small size, spiraled body and
cuticle with transversal striations. Anterior
region with buccal capsule sclerotized with six
large tricuspid teeth. Esophagus with muscular
and glandular portions.
Male (n = 1). Body 331.92 wide. Glandular
esophagus 138.3 wide. Spicules dissimilar, the
smallest with distal extremity blunt tipped,
measuring 0.3 mm long; and the largest with
distal extremity acicular, 1.39 mm long.
Gubernaculum 46.1 long and 27.66 wide.
Caudal alae present. Four pairs of precloacal
pedunculated papillae, two pairs of poscloacal
pedunculated papillae and five pairs of
poscloacal sessile papillae next to the tip of tail.
Cloaca 147.52 from posterior extremity.
Female (n = 1). Body 13.91 mm long, 0.33 mm
wide in the glandular esophagus region. Buccal
capsule 73.76 long, 110.64 wide. Cephalic
papillae not observed. Muscular esophagus 0.39
mm long, 55.32 wide; glandular esophagus 1.46
mm long, 0.13 mm wide. Nerve ring 0.30 mm
from anterior extremity. Excretory pore 0.46
mm from anterior extremity. Vulva 2.99 mm
RESULTS
Figure 1. Incomplete diagram of Cylicospirura
(Cylicospirura) felineus (Chandler, 1925) Sandground, 1932:
Male posterior extremity showing long (l) and short (s)
spicule, gubernaculum (g), pedunculated papillae (pep),
sessile papillae (sep) and caudal alae (ca). Scale bar = 100 μm.
Figure 2. Incomplete diagram of Cylicospirura
(Cylicospirura) felineus (Chandler, 1925) Sandground, 1932:
Female anterior extremity with buccal capsule (bc), muscular
esophagus (me), glandular esophagus (ge), nerve ring (n),
excretory pore (e), vulva (v), eggs (eg) and intestine (in). Scale
bar = 100 μm.
351
Gallaset al.
Cylicospirura felineus in Leopardus
from anterior extremity. Embryonated eggs,
27.66–36.88 (33.2 ± 3.5; n = 10) long,
18.44–36.88 (19.64 ± 1.46; n = 10) wide. Anus
110.64 from posterior extremity.
Taxonomic summary:
Synonyms: Spirocerca subaequalis Seurat,
1913; Spirocerca felineus Chandler, 1925.
Host: Leopardus geoffroyi d'Orbigny & Gervais,
1844 – new host record.
Host specimen deposited: MCNU 1015.
Locality: Bagé, BR-293 (31º02'34”S,
54º32'15”W), RS, Brazil.
Site of infection: stomach.
Prevalence: 16.67%.
Mean abundance of infection: 0.33
helminth/host.
Voucher specimen of the helminth deposited:
CHMU 37-1-1-male; 37-1-2-female.
Nematodes found in the stomach of L. geoffroyi
were identified as C. (C.) felineus by the
presence of a buccal capsule with triphid teeth, a
vulva on the anterior junction of the esophagus
and intestine, and from the size of the spicules.
The measurements recorded in the present study
are close to the range reported by Pence et al.
(1978) and Junker et al. (2006). Chandler (1925)
reported much larger specimens from India,
however.
The presence of a papilla anterior to the cloacal
aperture was reported in C. (C.) felineus from
North America (Pence et al., 1978), although
this structure was not observed in the male
examined in the present study. In L. geoffroyi,
the nematodes were found in the stomach
unattached, although lesions caused by C. (C.)
felineus have been reported in a number of other
hosts (Pence et al., 1978; Watson et al., 1981;
Smith et al., 1986; Junker et al., 2006; Ferguson
et al., 2011).
The female reproductive system of C. (C.)
felineus was described as having vulva located
anterior in relation to the esophagus and
intestine junction and, ovejector directed
DISCUSSION
anteriorly until form a structure similar to a sac,
which bifurcates into two uterine branches
(Chandler, 1925). In their redescription of the
species, Pence et al. (1978) described the
ovejector as being directed towards the posterior
extremity. This was also the case in the female
examined in the present study, although one of
the uterine branches full of embryonated eggs
was directed to the anterior extremity, possibly
due to a fold in the tissue (Fig. 2).
To date, the nematode species reported
parasitizing L. geoffroyi are Gnathostoma
americ a num Travassos, 1925 in the
Municipality of Angra dos Reis, State of Rio de
Janeiro (Travassos, 1925; Vicente et al., 1997;
Vieira et al., 2008) and Toxocara cati (Schrank,
1788) Sprent, 1956 in the State of Rio Grande do
Sul (Gallas & Silveira, 2013). While Travassos
(1925) reported the occurrence of G.
americanum in Felis tigrina Linnaeus, 1758,
Vicente et al. (1997) and Vieira et al. (2008)
considered this host to be L. geoffroyi. However,
as the geographic distribution of L. geoffroyi in
Brazil is restricted to the southernmost State of
Rio Grande do Sul (Trigo et al., 2013), it seems
likely that the host may have actually been
Leopardus pardalis Linnaeus, 1758 or
Leopardus tigrinus Schreber, 1775, which are
both found in Rio de Janeiro. In the present
study, C. (C.) felineus was reported for the first
time in the Neotropical Region and L. geoffroyi
was confirmed as a new host of the species.
Ecological parameters available in the literature
(Table 1) were compared with data from the
present study, and suggest that the prevalence of
C. (C.) felineus is not related to the number of
hosts examined. The ample distribution of C.
(C.) felineus in North America, between Canada
(Alberta) and the southern United States
(western Texas) has been attributed the use of a
large variety of intermediate and paratenic host
species (Pence et al., 1978). The life cycles of
generalist nematodes that use a large variety of
intermediate or paratenic hosts may affect their
prevalence in different environments, due to the
variation in the distribution of these hosts. The
reduced prevalence of Cylicospirura may also
reflect the diet and rareness of their definitive
352
Neotrop. Helminthol., 8(2), 2014
hosts, for which few data on the helminth fauna
are available (Junker et al., 2013).
The occurrence of C. (C.) felineus in the
southern extreme of the Neotropical Region may
reflect an ample geographic distribution,
determined at least in part by the variability and
availability of intermediate or paratenic hosts.
The Geoffroy's Cat, L. geoffroyi, is currently
listed as near-threatened by the IUCN
(Lucherini et al., 2008) and as vulnerable in Rio
Grande do Sul (Indrusiak & Eizirik, 2003). The
examination of roadkilled specimens constitutes
an important resource of material for studies of
the helmith fauna of wild felines, contributing to
the understanding of the ecology of these felines
in the Neotropical Region and, as in the present
case, extending the geographic distribution of C.
(C.) felineus.
Research using animals killed on the roads
avoids the need to sacrifice the host and requires
no authorization. While these specimens may
also be utilized for the evaluation of ecological
aspects of the impact of roads on natural
populations and as indicators of the composition
of the local fauna, their usefulness is limited by
the generally small size of the sample.
ACKNOWLEDGEMENTS
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Table 1. Comparison of the ecological parameters of C. (C.) felineus in wild felines of different localities.
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