Neotrop. Helminthol., 6(2), 2012
2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
Abstract
The coypu (Myocastor coypus Molina, 1782) has been reported as the definitive host of Hippocrepis
fuelleborni in Argentina and Uruguay; and Hippocrepis myocastoris Babero, Cabello & Kinoed, 1979
in Chile. Specimens of M. coypus (n = 4) from the State of Rio Grande do Sul, in Brazil, were received
from donations and necropsied in the laboratory. Digeneans were identified as H. fuelleborni due to
the presence of ventral papillae, oblique testes and eggs with no polar filaments. The prevalence of H.
fuelleborni was 25%, with a mean intensity of infection of 12 helminths/ host. The infection of M.
coypus by H. fuelleborni probably occurred as a result of the ingestion of aquatic plants with
metacercariae. This is the first report of H. fuelleborni parasitizing M. coypus in the State of Rio
Grande do Sul, Brazil.
Keywords: coypu - digeneans - Hippocrepis - Neotropic Region - taxonomy.
Resumo
Palavras-chave: ratão-do-banhado - Região Neotropical - taxonomia.digenéticos - Hippocrepis -
Para o ratão-do-banhado (Myocastor coypus Molina,1782) foram registradas Hippocrepis fuelleborni
na Argentina e Uruguai; e Hippocrepis myocastoris Babero, Cabello &
Kinoed, 1979 no Chile. Espécimes de M. coypus (n = 4) provenientes do Estado do Rio Grande do Sul,
Brasil, foram doados e necropsiados em laboratório. Digenéticos foram identificados como H.
fuelleborni por apresentarem papilas ventrais, testículos em diagonal e ovos sem filamentos polares. A
prevalência de H. fuelleborni foi 25%, com intensidade média de infecção de 12 helmintos/
hospedeiro. Provavelmente a infecção de H. fuelleborni em M. coypus ocorreu com a ingestão de
vegetação aquática com metacercárias. Este é o primeiro registro de H. fuelleborni parasitando M.
coypus no Estado do Rio Grande do Sul, Brasil.
Travassos & Vogelsang, 1930
Suggested citation: Rocha, AGS, Gallas, M & Silveira, EF. 2012. Hippocrepis fuelleborni (Digenea, Notocotylidae) parasitizing
Myocastor coypus (Rodentia, Myocastoridae) in Southern Brazil. Neotropical Helminthology, vol. 6, N°2, pp. 185 - 190.
1Departamento de Biologia, Museu de Ciências Naturais, Universidade Luterana do Brasil. 92425-900, Canoas, Rio Grande do Sul, Brasil
2Bolsista PROICT/ULBRA.
anagabrieladasilvarocha@yahoo.com.br
185
HIPPOCREPIS FUELLEBORNI (DIGENEA, NOTOCOTYLIDAE) PARASITIZING MYOCASTOR
COYPUS (RODENTIA, MYOCASTORIDAE) IN SOUTHERN BRAZIL
HIPPOCREPIS FUELLEBORNI (DIGENEA, NOTOCOTYLIDAE) PARASITANDO MYOCASTOR
COYPUS (RODENTIA, MYOCASTORIDAE) NO SUL DO BRASIL
1,2 1 1
Ana Gabriela da S. Rocha ; Moisés Gallas & Eliane F. da Silveira
Rocha AGA et al.
Hippocrepis fuelleborni in Myocastor coypus
The genus Hippocrepis was proposed by
Travassos (1922) to accommodate the species
Monostomum hippocrepis Diesing, 1850. To date,
three species have been described in this genus:
Hippocrepis hippocrepis (Diesing, 1850)
Travassos, 1922; Hippocrepis fuelleborni
Travassos & Vogelsang, 1930 and Hippocrepis
myocastoris Babero, Cabello & Kinoed, 1979.
The Hippocrepis species are helminth parasites of
rodents that occur in South America: H.
hippocrepis has been reported in the capybara,
Hydrochaeris hidrochaeris Linnaeus, 1766
(Travassos, 1922; Boero & Boehringer, 1967;
Kohn & Pereira, 1970; Lombardero & Moriena,
1973; Rodriguez et al., 1975; Tabes, 1980; Mones
& Martínez, 1982; Hoffmann et al., 1986; Costa &
Catto, 1994; Casas et al., 1995; Sutton et al., 1997;
Bonuti et al., 2002; Salas & Herrera, 2004; Sinkoc
et al., 2009), whereas H. fuelleborni and H.
myocastoris have been reported in the coypu,
Myocastor coypus Molina, 1782 (Travassos &
Vogelsang, 1930; Boero & Boehringer, 1967;
Kohn & Pereira, 1970; Ostrowski de Núñez, 1976;
Babero et al., 1979; Flores et al., 2007).
Dubois (1962) apud Kohn & Pereira (1970)
proposed that H. fuelleborni was a synonym of H.
hippocrepis, considering that the species does not
presented valid diagnostic characters. Kohn &
Pereira (1970) redescribed H. hippocrepis and H.
fuelleborni as valid taxa. However, the
redescription of the later species was based in the
original description, due the condition of the
specimen obtained by the authors.
The life cycle of Hippocrepis is known only for H.
fuelleborni, for which planorbid snails
(Biomphalaria peregrina Orbigny, 1835) are
considered to be intermediate hosts (Ostrowski de
Núñez, 1976). The definitive hosts are aquatic
animals which ingest waterside plants hosting
metacercariae. In the present study H. fuelleborni
is reported in M. coypus from the State of Rio
Grande do Sul, Brazil.
INTRODUCTION
Four specimens of M. coypus were obtained in Rio
Grande do Sul, RS, Brazil, between 2008 and 2010.
All four animals were victims of roadkill, and were
donated to the “Laboratório de Zoologia dos
Invertebrados” do “Museu de Ciências Naturais da
ULBRA” (MCNU) in Canoas, Brazil. The
collection and transportation of the specimens was
conducted according to normative ruling no. 154 of
March 1st, 2007, chapter VI, article 26. The
digeneans found were fixed in A.F.A., stained with
Delafield's hematoxylin, and mounted in Canada
balsam (Amato & Amato, 2010). Measurements
are given in micrometers (µm) unless otherwise
indicated. Means, standard deviations, and the
number of specimens are shown in this order in
parentheses after the range of values. Ecological
terms were used according to Bush et al. (1997).
Drawings were made using a drawing tube
attached to a microscope. A representative
specimen of the host was deposited in the “Coleção
de Mamíferos” do “Museu de Ciências Natuais da
ULBRA” (MCNU), Canoas, Brazil, while a
voucher specimen of the trematode was deposited
in the “Coleção Helmintológica do Instituto
Oswaldo Cruz” (CHIOC), Rio de Janeiro, Brazil.
Hippocrepis fuelleborni Travassos & Vogelsang,
1930
Figs 1–5.
Description based on 10 specimens mounted in
toto. Digenea, Notocotylidae. Body elongated,
4.74-8.05 mm (6.09, 1.07, n = 10) long, 0.64-1.22
mm (1.00, 0.19, n = 10) wide (Figs 1 and 2). Oral
sucker subterminal, 299-529 (426.78, 68.14, n = 9)
long, 276-460 (393.55, 58, n = 9) wide with two
lateral projections 92.2-230.5 (149.57, 40.39, n =
9) wide, on each side (Figs 1 and 2). Pharynx
absent, esophagus 165.96-230.5 (189.01, 24.56, n
= 6) long, 27.66-55.32 (39.59, 9.52, n = 6) wide,
with small diverticula, opening through a cecum.
Cecum fused posteriorly, between the testes (Fig.
1). Ventral sucker absent. Ventral papillae present
from the genital pore to posterior extremity,
arranged irregulary in longitudinal rows with a
diameter of 36.88-92.2 (58.08, 17.41, n = 20) (Fig.
2). Genital pore postbifurcal 0.60-1.04 mm (0.85,
186
MATERIAL AND METHODS
RESULTS
Neotrop. Helminthol., 6(2), 2012
0.12, n = 9) from anterior extremity (Figs 1 and 2).
Male reproductive system with cirrus-sac
elongated, 0.968-1.95 mm (1.42, 0.30, n = 10)
long, 0.16-0.29 mm (0.21, 0.04, n = 10) wide;
cirrus with small spines, 0.90-1.40 mm (1.13, 0.21,
n = 6) long (Figs 1 and 3). Internal seminal vesicle
295.04-645.4 (441.82, 104.7, n = 9) long, 101.42-
184.4 (132.6, 27.65, n = 9) wide. External seminal
vesicle beginning at the terminal portion of the
cirrus-sac and forming one or two coils ventrally
(Figs 1 and 3). Testes lobed, oblique, 460-805
(595.7, 112.91, n = 10) long, 368-644 (480.7,
89.04, n = 10) wide, with a variety of shapes (Figs
1, 2 and 5). Female reproductive system consisting
of metraterm well developed, parallel to the cirrus-
sac, 461-922 (699.2, 124.21, n = 10) long, 92-161
(124.73, 23.28, n = 10) wide (Figs 1 and 3). Uterus
with 17 to 24 transverse coils (Fig. 1). Ovary
pretesticular, 253-460 (315.1, 60.41, n = 10) long,
299-506 (407.1, 75.15, n = 10) wide (Fig. 1).
Mehlis' gland pre-ovarian, 115-207 (156.4, 26.11,
n = 10) long, 184-437 (278.3, 69.8, n = 10) wide;
vitelline follicles in two longitudinal rows (Fig. 1).
Eggs oval, with no polar filaments, 18.44-28.32
(23.08, 2.97, n = 20) long, 9.22-11.8 (9.86, 1.02, n
= 20) wide (Fig. 4).
Taxonomic summary:
Host: Myocastor coypus.
Host specimen deposited: MCNU 2536.
Site of infection: intestine.
Locality: Porto Alegre, State of Rio Grande do Sul,
Brazil.
Prevalence: 25%.
Mean intensity of infection: 12 helminths/ host.
Mean abundance of infection: 3 helminths/ host.
Voucher specimen deposited: CHIOC 37806.
The genus Hippocrepis includes tree species: H.
hippocrepis, H. fuelleborni and H. myocastoris. H.
fuelleborni can be distinguished from H.
myocastoris by the presence of ventral papillae,
oblique testes and eggs lacking polar filaments
(Flores et al., 2007). The specimens collected from
M. coypus in this study presented characters
consistent with the diagnosis of H. fuelleborni.
The specimens measured in the present study
presented relatively small cirrus (1.13 mm) in
comparison with the single specimen (2.9 mm)
measured by Travassos & Vogelsang (1930) and
Kohn & Pereira (1970). Boero & Boehringer
187
(1967) presented only length and width
measurements for the whole specimens, which
were similar to the values recorded in the present
study. The values recorded in the present study
were higher than those reported by Ostrowski de
Núnez (1976) for adults obtained by experimental
infection, which may have affected their size.
In their original description of the species H.
fuelleborni, Travassos & Vogelsang (1930)
referred to the presence of cirrus armed with
spines. This character was not mentioned in the
review of Kohn & Pereira (1970). Specimens with
cirrus armed with small, thin spines were observed
by Ostrowski de Núñez (1976). In the present
study, cirrus were observed with spines in
localized areas (proximal and distal extremities).
The spines are probably present along the full
length of the cirrus, but may not have been visible
do to tissue chromophilia.
The diagrams of H. fuelleborni presented by Boero
& Boehringer (1967) contain two errors – the
absence of lateral projections in the oral sucker and
the cecum separated and terminated on reaching
the testes. Kohn & Pereira (1970) subsequently
added details of the distal extremity of the cirrus
and the eggs, but they did not mention these errors.
In the present study, we provide a detailed
description and diagramation of the lateral
projections of the oral sucker and the morphology
of the cecum.
Based on the life cycle of H. fuelleborni described
by Ostrowski de Núñez (1976), the infection found
in the present study may be related to the ingestion
of aquatic vegetation with metacercariae by M.
coypus. The small sample obtained in the present
study prohibits a reliable ecological analysis of
infection patterns in M. coypus. Given this, a larger
number of H. fuelleborni specimens from a more
ample sample of M. coypus would be necessary for
a systematic evaluation of the levels of parasitism
in the host population.
Previous reports of H. fuelleborni were derived
from specimens collected in Uruguay (Travassos
& Vogelsang, 1930), Argentina (Boero &
DISCUSSION
Figures 1–5 Incomplete diagrams of Hippocrepis fuelleborni. (1) Entire specimen showing oral sucker (s), lateral
projection (black arrowheads), esophagus (e), diverticula (de), cecum (c), genital pore (gp), cirrus (ci), cirrus pouch
(cp), internal seminal vesicle (isv), external seminal vesicle (esv), metraterm (m), uterus (u), Mehlis' gland (g), ovary
(o), vitelline follicles (vi) and testes (t). Bar = 500 µm. (2): Distribution pattern of the ventral papillae (p). Bar = 500
µm. (3): Detail of copulatory organs. Bar = 300 µm. (4): Ventral (left) and lateral (right) views of the eggs. Bar = 10
µm. (5): Variation in testes shape. Bar = 200 µm.
Rocha AGA et al.
Hippocrepis fuelleborni in Myocastor coypus
188
Neotrop. Helminthol., 6(2), 2012
189
Boehringer, 1967; Ostrowski de Núñez, 1976), and
Chile (Babero et al., 1979). Travassos et al. (1969)
considered that H. fuelleborni would probably also
occur in southern Brazil (Rio Grande do Sul) due to
the distribution of M. coypus in this region,
although this has only been confirmed in the
present study, which provides the first record of H.
fuelleborni from Rio Grande do Sul, Brazil.
We are grateful to PROICT/ULBRA for the
scholarship granted to the first author, and to
Verónica R. Flores (CONICET) for her help with
bibliography.
Casas, MC, Zalles, LM, Patrick, MJ & Dailey, M.
1995.
Costa, CA & Catto, JB. 1994.
Flores, VR, Brugni, N & Rauque, CA. 2007.
Hoffmann, RP, Fortes, E, Gutierres, VC &
Eberhard, AS. 1986.
Kohn, A & Pereira, RCS. 1970.
Lombardero, OJ & Moriena, RA. 1973.
Mones, A & Martínez, S. 1982.
Ostrowski de Núñez, M. 1976.
Rodriguez, HC, Brito, EC & Perea, FL. 1975.
Salas, V & Herrera, EA. 2004.
Sinkoc, AL, Brum, JGW & Muller, G. 2009.
Intestinal helminths of capybara
( H y d r o c h a e r i s ( H y d r o c h o e r u s )
hydrochaeris) from Bolivia. Journal of the
Helminthological Society of Washington,
vol. 62, pp. 87-88. Helmintos parasitos
de capivaras (Hydrochaeris hydrochaeris)
na sub-região da Nhecolândia, Pantanal-
sul-matogrossense. Revista Brasileira de
Biologia, vol. 51, pp. 39-48.
Redescription of Hippocrepis myocastoris
(Digenea: Notocotylidae) in the Coypu
M y o c a s t o r c o y p u s ( R o d e n t i a :
Myocastoridae) from Patagonia, Argentina.
Comparative parasitology, vol. 74, pp. 233-
236.
Ocorrência de
helmintos em capivaras (Hydrochoerus
hydrochoerus). Arquivos da Faculdade de
Veterinária da UFRGS, vol. 14, pp. 71-75.
Revisão do gênero
Hippocrepis Travassos, 1922, (Trematoda).
Memórias do Instituto Oswaldo Cruz, vol.
68, pp. 1-7. Nuevos
helmintos del carpincho (Hydrochoerus
hydrochaeris) para la Argentina. Revista de
Medicina Veterinária, vol. 53, pp. 265-269.
Estudios sobre la
familia Hydroeridae (Rodentia), XIII,
parasitosis y patologías de Hydrochoerus,
Brisson, 1762. Revista de la Facultad de
Humanidades y Ciencias, Serie ciencias
biológicas, vol. 1, pp. 297-329.
Sobre el ciclo de
vida biológico de Hippocrepis fuelleborni
Travassos y Vogelsang 1930 (Trematoda,
Notocotylidae). Physis, Sección B, vol. 35,
pp. 125-130.
Aspectos fisiológicos y sanitários del
chigüire. Cespedesia, vol. 4, pp. 15-44.
Intestinal
Helminths of Capybaras, Hidrochoerus
hydrochaeris, from Venezuela. Memórias do
Instituto Oswaldo Cruz, vol. 99, pp. 563-
566.
Gastrintestinal Helminths of Capybara
ACKNOWLEDGEMENTS
BIBLIOGRAPHIC REFERENCES
Amato, JFR & Amato, SB. 2010.
Babero, BB, Cabello, C & Kinoed, JE. 1979.
Bonuti, MR, Nascimento, AA, Mapelli, EB &
Ar a n t es , I G. 2 0 02 .
Boero, JJ & Boehringer, IK. 1967.
Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.
1997.
Técnicas gerais
para coleta e preparação de helmintos
endoparasitos de aves. In S Von Matter,
Straube, FC, Accordi, IA, Piacentini, VQ &
Cândido-Jr, JF. (eds.). Ornitologia e
Conservação: Ciência Aplicada, Técnicas
de Pesquisa e Levantamento. Technical
Books, Rio de Janeiro.
Helmintofauna de Chile. V. Nuevos
parasitos del coipo, Myocastor coypus
(Molina, 1782). Boletín Chileno de
Parasitología, vol. 34, pp. 26-31.
He l m i nt o s
g a s t r i n t e s t i n a i s d e c a p i v a r a s
(Hydrochoerus hydrochaeris) na sub-região
de Paiaguás, Pantanal do Mato Grosso do
Sul, Brasil. Semina: Ciências Agrárias, vol.
23, pp. 57-62. El parasitismo
de nuestra fauna autócton/Los parasitos del
Carpincho (Hydrochoerus hydrochoeris) y
del quiyá (Myocastor coypus), Revista de la
Facultad de Ciências Veterinárias, La Plata.
vol. 21, pp. 161-172.
Parasitology meets ecology on its
own terms: Margolis et al. revisited. Journal
of Parasitology, vol. 83, pp. 575-583.
Rocha AGA et al.
Hippocrepis fuelleborni in Myocastor coypus
Cruz, vol. 23, pp. 169-171.
Trematódeos do Brasil. Memórias do
Instituto Oswaldo Cruz, vol. 67, pp. 1-886.
Travassos, L, Freitas, JFT & Kohn, A. 1969.
(Hydrochoerus hydrochaeris, Linneus,
1766) in cattle breeding farm in the area of
the Ecological Reserve of Taim, Rio
Grande. Brazilian Archives of Biology and
Technology, vol. 52, pp. 327-333.
Los digeneos
Notocotyloidea de Hydrochaeris
hydrochaeris Linne (Rodentia) de
Argentina. Gayana Zoologia, vol. 61, pp.
23-31. Sobre uma coleção de helmintos
de chiguire (Hydrochoerus hydrochaeris)
de Venezuela. Revista Facultad Ciencias
Veterinaris U. C. V., vol. 28, pp. 19-47.
Informações sôbre a fauna
helmintológica de Mato Grosso. Fôlha
Médica, vol. 3, pp. 187-190. Pesquisas
Helmintológicas Realizadas em Hamburgo.
Sobre dois trematódeos parasitos de
mamíferos. Memórias do Instituto Oswaldo
Sutton, CA, Ostrowski de Núñez, M, Lunaschi, LI
& Allekotte, A. 1997.
Tabes, HM. 1980.
Travassos, L. 1922.
Travassos, L. & Vogelsang, E. 1930.
Co r res p on d enc e au t ho r / Aut o r pa ra
correspondencia:
Ana Gabriela da Silva Rocha
Departamento de Biologia, Museu de Ciências
Naturais, Universidade Luterana do Brasil, 92425-
900, Canoas, Rio Grande do Sul, Brasil.
E-mail/ correo electrónico:
anagabrieladasilvarocha@yahoo.com.br
Received July 2, 2012.
Accepted August 19, 2012.
190
