Neotrop. Helminthol., 6(1), 2012
2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
STOMACHICOLA LYCENGRAULIDIS N. SP. (DIGENEA, HEMIURIDAE), PARASITE OF THE
ATLANTIC SABRETOOTH ANCHOVY LYCENGRAULIS GROSSIDENS (CLUPEIFORMES,
ENGRAULIDAE)
STOMACHICOLA LYCENGRAULIDIS N. SP. (DIGENEA, HEMIURIDAE), PARÁSITA DE
LA ANCHOA DE RÍO LYCENGRAULIS GROSSIDENS (CLUPEIFORMES, ENGRAULIDAE)
Ruben Daniel Tanzola & Silvana Seguel
Laboratorio de Patología de Organismos Acuáticos- Dep. Biología, Bioquímica y Farmacia, Universidad Nacional del Sur,
San Juan 670 (8000) Bahía Blanca, Argentina. E-mail: rtanzola@uns.edu.ar
Suggested citation: Tanzola, RD & Seguel, S. 2012. Stomachicola lycengraulidis n. sp. (Digenea, Hemiuridae), parasite of the
atlantic sabretooth anchovy Lycengraulis grossidens (Clupeiformes, Engraulidae). Neotropical Helminthology, vol. 6, nº1, pp.
59 -66.
59
Abstract
This paper describes and illustrates a new species of digenetic trematode, parasitic in the stomach of
the sabretooth anchovy Lycengraulis grossidens (Agassiz, 1829) from the Bahía Blanca estuary and
the Paraná River, Argentina, designated as Stomachicola lycengraulidis n.sp. The new taxon differs
from S. bayagbonai and S. singhi congeneric species from the Gulf of Guinea and Indian Ocean
respectively, mainly in the body size, the structure of the reproductive system, the development of the
ecsoma and the sinus sac. It differs from the first one mainly in the presence of two frontal
protuberances at the level of the preoral lobe, which are absent in the specimens studied here. Also in
general terms, S. bayagbonai is comprised of slightly larger individuals, with larger pharynx, testicles
and ovary. And it differs from S. singhi by their smaller duct and hermaphroditic sac and for having a
well developed seminal receptacle, which is absent in the Bay of Bengal specimens. When comparing
the relative size of the ecsoma, we found significant differences among both of the populations of
digeneans examined, the worms collected in the Paraná River was more developed than those from the
Bahia Blanca estuary. The host, L. grossidens, migrates to the Paraná river in winter and spring and
then, from December to March it makes a trophic migration towards the sea and is found all along the
Atlantic coast of Buenos Aires province. For this reason, it is here hypothesized that the relative
development of the tail, is affected by environmental conditions, such as pH and osmolarity of the
stomach, salinity and/or water temperature.
Key words: Anchovy - Digenea - Lycengraulis - Stomachicola.
Tanzola & Seguel
Stomachicola lycengraulidis parasite of Lycengraulis
Yamaguti (1934) considered that the proposal of
a new genus named Stomachicola was justified
due to the relative size of the ecsoma
(approximately 90% of the total length), the
extension of the pars prostatica and the
development of the seminal receptacle of some
hemiurids. Later, several Indian workers raised
numerous parasites of the stomach of teleostean
fishes to species level, mainly from the Pacific
and Indian oceans. However, most of these were
later considered junior synonyms of the type
species S. muraenesocis Yamaguti, 1934
(Bilqees, 1971; Hafeezullah, 1980; Gupta &
Gupta, 1991). Tanzola & Guagliardo (2000)
recorded individuals belonging to Stomachicola,
as components of low prevalence in the helminth
fauna of the Argentine Conger, Conger
orbignianus Valenciennes, 1847, from the Bahia
INTRODUCTION
Blanca estuary, but the authors did not specify
their taxonomical status. This paper describes
and illustrates a new species from the stomach of
the sabretooth anchovy Lycengraulis grossidens
(Agassiz, 1829) and its designation as
Stomachicola lycengraulidis n. sp. is proposed.
One hundred and five L. grossidens (Teleostei,
Engraulidae), were examined. Ninety of them
were caught with nets during March 2007 and
March 2009 in the Bahía Blanca estuary (38º48' S
62º 16'W) and also15 fish from the Paraná river
(33°20'S 60º12'W) in November 2010. Some fish
were dissected fresh and the remainder were kept
in a freezer at - 20°C until necropsy. All worms
were collected in the lumen of the stomach. They
were slightly flattened between microscope
slides, fixed and preserved in 5% formalin for
MATERIALS AND METHODS
Resumen
En el presente trabajo se describe e ilustra una nueva especie, parásita del estómago de la anchoa de río
Lycengraulis grossidens (Agassiz, 1829) en el estuario de Bahía Blanca y el río Paraná, Argentina,
proponiendo su denominación como Stomachicola lycengraulidis n. sp. El nuevo taxón se diferencia
de sus congéneres del golfo de Guinea y océano Índico, S. bayagbonai y S. singhi, respectivamente,
principalmente en la estructura del aparato reproductor, el desarrollo del ecsoma y del saco del sinus.
De la primera de ellas se distingue principalmente por la presencia de dos protuberancias frontales a
nivel del lóbulo preoral, ausentes en los especímenes estudiados. Además en términos generales S.
bayagbonai comprende individuos ligeramente más grandes con faringe, testículos y ovarios de
mayor tamaño. Y se distingue de S. singhi por el ducto y saco hermafrodita más pequeños y poseer un
receptáculo seminal bien desarrollado, ausente en los especímenes de la Bahía de Bengala. Cuando se
comparó el tamaño relativo del ecsoma, se encontraron diferencias significativas entre ambas
poblaciones de digeneos examinadas, siendo que los especímenes colectados en el Río Paraná tenían
un mayor desarrollo que aquellos obtenidos en el estuario de Bahía Blanca. El hospedador, L.
grossidens, migra hacia el río Paraná en invierno y primavera y luego, desde diciembre a marzo,
realiza migraciones tróficas hacia el mar y se lo encuentra a todo lo largo de la costa de la Provincia de
Buenos Aires. Por esta razón, aquí se hipotetiza que el desarrollo de la cola es afectado por condiciones
ambientales, tales como el pH y la osmolaridad del estómago, así como la salinidad o temperatura del
agua.
Palabras clave: Anchoa - Digenea - Lycengraulis - Stomachicola.
60
Neotrop. Helminthol., 6(1), 2012
subsequent identification. They were stained
with Langeron's hydrochloric carmine, cleared
in clove oil and mounted in Canada balsam.
Drawings were made to scale with the aid of a
drawing tube. The prevalence and intensity of
infection (Bush et al., 1997) were calculated for
each of the sampling areas. A one-tailed t
Student test was carried out to compare the
lengths of the ecsoma in both populations of
hosts. In the present work the specimens come
from fish catch. They have not experimented
with live animals, not affected population
parameters of the host or provoked impacts on
the environment and human health or animal.
Stomachicola lycengraulidis n. sp.
(Figs. 2-4).
Description (based on 25 stained and mounted
specimens). Very elongated body. Smooth
tegument with delicate and little-defined folds.
Well developed ecsoma (=tail), half or 2/3 total
length. Rounded and subterminal oral sucker.
Spherical or subspherical acetabulum in the first
quarter of the body. The forebody is much shorter
than the hindbody. Subglobular pharynx. Short
oesophagus. Digestive caecae extend to the end
of the body, penetrating into the ecsoma.
They are separated and often overlap in the
testicular region or in the posterior region of the
ecsoma. The preovarian testicles are situated
obliquely and immediately after the seminal
vesicle. The saccular seminal vesicle has a thin
wall, elongated in the longitudinal direction of
the body. Very long, tubular and sinuous pars
prostatic, surrounded throughout by prostatic
glandular cells. Short tubular hermaphroditic
duct. The sinus sac and body of the sinus organ
are pyriform, permanent and muscular. The
genital atrium is large and usually contains eggs
in small clusters. The genital pore at the level of
the pharynx takes the form of a transversal slit,
posterior to the oral sucker. The oval to reniform
ovary is located immediately posterior to the
testicles. Conspicuous postovarian Mehlis'
gland. Seminal receptacle is large and postovaric.
Seven sinuous vitellin tubules; three of them on
the right side and four on the left side. Vitellaria
extend up to the posterior testicle and penetrate
backward into the ecsoma. The uterus is mostly
postovaric and irregularly coiled. The degree of
penetration of the uterus into the ecsoma is
variable (in some specimens it is less than the
anterior third and in other parts reaches ¾ of the
tail). The eggs are small and oval in shape. The
morphometric data of 25 stained and mounted
specimens is summarized in Table I.
Taxonomical summary
Type host: Lycengraulis grossidens (Agassiz,
1829) (Teleostei; Engraulidae).
Additional host: Conger orbignianus
Valenciennes, 1837 (Teleostei; Anguilliformes).
Site of infection: Stomach.
Type locality: Bahía Blanca estuary (38º48'S
62º16'W).
Other localities: Paraná river (33º20'S 60º12'W).
Prevalence: Bahía Blanca estuary 22.22 %;
Paraná river 66.67%.
Mean intensity: Bahía Blanca estuary 1.3; Parana
river 4.3.
Etymology: The specific names refers to the
generic name of its type host.
Type material: Holotype accesion number=
MLP6442; paratype accession number=
MLP6443 (Colección de la División Zoología
Invertebrados, Museo de La Plata, Argentina).
RESULTS
61
Tanzola & Seguel
Stomachicola lycengraulidis parasite of Lycengraulis
Figure 2. Stomachicola lycengraulidis n.sp. (in toto).
Scale-bar= 1 mm.
Figure 4. S. lycengraulidis n.sp. Reproductive system
(schematic). Abbreviations as in fig. 3. and sv= seminal
vesicle, te= testicle, ov= ovary, sr= seminal receptacle,
vt= vitellaria. Scale-bar= 0.500 mm.
2
3
4
Figure 1. Sampling areas of the hosts, Lycengraulis
grossidens.
62
ss
so
mt
pp
ut
gp
eg
Figure 3. S. lycengraulidis n.sp. Genital terminalia
(detail). Abbreviations: gp= genital pore, eg= eggs in
the genital atrium, ss= sinus sac, so= sinus organ, mt=
metraterm, pp= pars prostatica, ut= uterus. Scale-bar=
0.250 mm.
DISCUSSION
Yamaguti (1934) raised the genus Stomachicola
designating S. muraenesocis as the type species, a
very common parasite of the stomach of
Muraenesox cinereus in the Inland Sea of Japan
and South China Sea. Manter (1947) transferred
the species Dinurus rubeus Linton (1910) and D.
magnus Manter (1931) to the genus
Stomachicola. Yamaguti (1971) in his synopsis of
trematode parasites of vertebrates recognized the
following species S. muraenesocis, S. rubeus and
S. magnus. However, later Sinclair et al. (1972)
considered S. rubea and S. magnum as junior
synonyms of S. muraenesocis. Bilqees (1971)
established three genera (with eight species)
parasites of marine fish in western Pakistan:
Cameronia (C. octovitellarii, C. pakistani);
Segmentatum (S. karachiensis, S. gadrii, S.
cinerensis and S. magnaesophagustum) and
Cestodera (C. gastrocecus, C. unicecus), but
Gibson (2002) considered these three genera
together with Linguastomachicola Srivastava &
Sahai, 1978 as junior synonyms of Stomachicola.
Hafeezullah (1980) had previously recognized
that the eight species described by Bilqees (1971)
conformed to the original description of S.
muraenesocis and that all of them should be
considered as junior synonyms. Stomachicola
mastacembeli Verma, 1973, S. polynemi Gupta &
Gupta 1974, S. lepturusi Gupta & Gupta 1974, S.
rauschi Gupta & Ahmad 1978 and S. singhi Gupta
& Ahmad 1978 were raised to designate parasites
of marine fish in the Indian Ocean. Siddiqi &
Hafeezullah (1975) described S. bayagbonai, a
parasite in the stomach of the Guinean pike
conger Phyllogramma regani Pellegrin 1934 (=
Cynoponticus ferox Costa 1846) in Nigeria. The
genera Pseudostomachicola Skrjabin &
Guschanskaja, 1954; Acerointestinecola Jahan,
1970 and Indostomachicola Gupta & Sharma,
1973 had been considered as junior synonyms of
Stomachicola Yamaguti, 1934 by Gibson & Bray
(1979). Gupta & Gupta (1991) reviewed the
genus Stomachicola and transferred S. lepturusi
and S. rauschi to Allostomachicola Yamaguti,
1958 and, in the same study, considered that S.
Neotrop. Helminthol., 6(1), 2012
rubea, S. mastacembeli, S. polynemi, S. chauhani
and S. guptai, should be conspecific with S.
muraenesocis on account of the great variability
in shape and size of the internal organs.
For all these reasons, the genus Stomachicola
Yamaguti, 1934 would currently be comprised of
the following taxa: S. muraenesocis Yamaguti,
1934 (type species), S. bayagbonai Siddiqi &
Hafeezullah, 1975 and S. singhi Gupta & Ahmad
1978, whose comparative morphometric data are
shown in Table I.
Yamaguti (1934) gave no measurements in his
original description of the genus and made no
reference to the extent of the ecsoma. However his
iconography shows that the caudal organ occupies
approximately 90% of the total length of the body.
In the specimens subsequently examined by
Gupta & Gupta (1991) this appendix varies over a
wide range, comprising between 50% and 82% of
the body length. In the remaining species, the
caudal appendix represents approximately 75% in
S. bayagbonai and 80% in S. singhi. In our study,
specimens have shown less pronounced variation
in the development of the tail, constituting only
25% of the total length in some cases while others
reached 70%. When comparing the relative size of
the tail, we found highly significative differences
among both the populations of digenean
examined, the worms collected in the Paraná
River having a higher development than those
from the Bahia Blanca estuary (t Student= 3.236,
p=0.0019). The host, L. grossidens, migrates to
the Paraná river in winter and spring and then,
from December to March, makes a trophic
migration towards the sea and is found all along
the Atlantic coast of Buenos Aires province
(Cervigón et al., 1992). For this reason, here it is
hypothetized that the relative development of the
tail, which was considered a morphological
feature of taxonomic value by some authors, is
affected by environmental conditions, such as pH
and osmolarity of the stomach, the salinity and/or
water temperature. In this regard, Gibson & Bray
(1979) suggested that the ecsoma probably
functions as a feeding organ that could be
63
Tanzola & Seguel
Stomachicola lycengraulidis parasite of Lycengraulis
Table 1. Measurements of Stomachicola spp. from different sources (in mm).
References: * No stated in original publication.
Host
S. muraenesocis
Yamaguti
(1934)
S. muraenesocis
Gupta & Gupta
(1991)
S. bayagbonai
Siddiqi & Hafeezullah
(1975)
S. singhi
Gupta & Ahmad
(1978)
S. lycengraulidis n.sp.
Present study
Number of specimens
(not stated)
35
5
8
25
min
max
min
max
min
max
min max min max mean
Body length
---*
55
6.84
15.10 9.44
21.15 5.04 15.81 4.61 19.57 11.56
Body width
---
2.5
0.62
0.93
2.13
3.99
0.75 0.82 0.94 2.35 1.34
Ecsoma length
---
---
3.39
12.44 ---
---
---
--- 1.22 12.56 6.70
Oral sucker length
0.23
0.42
0.14
0.19
0.28
0.52
0.16 0.22 0.17 0.56 0.31
Oral sucker width
0.32
0.58
0.14
0.21
0.36
0.61
0.20 0.24 0.22 0.46 0.34
Ventral sucker length 0.70
1.36
0.44
0.59
0.85
1.14
0.56 0.60 0.49 1.19 0.82
Ventral sucker width 0.70
1.36
0.47
0.55
0.85
1.28
0.56 0.60 0.47 1.29 0.80
Sucker width ratio
---
---
1:2.5 1:3.36 1:2.4 ---
---
--- 1:1.71 1:2.89 1:2.5
Pharynx length
0.17
0.28
0.08
0.12
0.20
0.33
0.12 0.14 0.10 0.25 0.18
Pharynx width
0.17
0.28
0.08
0.13
0.20
0.33
0.11 0.13 0.10 0.25 0.17
Oesophagus
---
---
0.05
0.08
---
---
0.12 0.30 0.09 0.19 0.14
Anterior testis length 0.45
0.84
0.32
0.54
0.42
1.02
0.48 0.55 0.26 0.63 0.38
Anterior testis width 0.53
0.64
0.15
0.49
0.38
0.76
0.34 0.47 0.15 0.46 0.29
Posterior testis length 0.28
0.46
0.30
0.45
0.42
1.02
0.45 0.58 0.24 0.45 0.35
Posterior testis width 0.52
0.74
0.19
0.32
0.38
0.76
0.34 0.42 0.14 0.43 0.30
Pars prostatica length ---
---
1.15
2.21
---
---
0.82 1.63 1.95 3.60 2.46
Hermaphroditic duct ---
---
0.08
0.12
---
---
0.27 0.31 0.13 0.23 0.18
Seminal vesicle length ---
---
0.34
0.67
---
---
0.47 0.65 0.22 1.16 0.70
Seminal vesicle width ---
---
0.10
0.49
---
---
0.29 0.44 0.10 0.35 0.23
Ovary length
0.31
0.46
0.17
0.49
0.33
0.52
0.11 0.25 0.10 0.46 0.35
Ovary width
0.53
0.85
0.14
0.31
0.54
0.67
0.17 0.39 0.10 0.47 0.28
Egg length
0.017
0.022 0.007 0.021 0.017 0.019 0.015 0.020 0.013 0.018 0.016
Egg width 0.014 0.014 0.005 0.011 0.011 0.013 0.010 0.012 0.008 0.013 0.011
64
extruded under conditions of adequate pH and
osmolarity.
Specimens examined in this study differ from the
type material of S. muraenesocis Yamaguti 1934
mainly in the length of the ecsoma. However this
difference is not seen in the specimens described
by Gupta & Gupta (1991) as S. muraenesocis
from Congromuraena anago Temminck &
Schlegel, 1846, Symbranchus bengalensis
(McClelland 1844) (= Ophisternon bengalense)
and Amphipnous cuchia (Hamilton 1822)(=
Monopterus cuchia) from the Bay of Bengal,
Orissa, India. However, the pars prostatica,
seminal vesicle and hermaphroditic duct in the
parasite of L. grossidens are considerably more
developed than in S. muraenesocis. Unfortunately
these latter features of the reproductive system
were not taken into account in the original
description of S. bayagbonai in order for
comparisons to be made. However, a notable
feature in the last species is the presence of two
frontal protuberances at the level of the preoral
lobe, which are absent in the specimens studied
here. Also in general terms, S. bayagbonai is
comprised of slightly larger individuals, with
larger pharynx, testicles and ovary. Finally, the
hemiurids of the present study are distinguished
from S. singhi by their smaller duct and
hermaphroditic sac and for showing a well
developed seminal receptacle, which is absent in
the Bay of Bengal specimens.
For all these reasons, the parasitic helminths of
the stomach of Lycengraulis grossidens are
considered as representatives of a new species,
designated as Stomachicola lycengraulidis n. sp.
The authors wish to thank Dra. M.Ostrowski de
Núñez and Mg.Sc. Patricia Noguera for providing
part of the bibliography, Lic. Jorge Liotta for
sending samples from the Paraná river and Mg.Sc.
Rosemary Scoffield for her review of the English
version.
ACKNOWLEDGMENTS
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Author for correspondence / Autor para
correspondencia:
Ruben Daniel Tanzola
Laboratorio de Patología de Organismos
Acuáticos- Dep. Biología, Bioquímica y Farmacia,
Universidad Nacional del Sur, San Juan 670 (8000)
Bahía Blanca, Argentina.
E-mail/ correo electrónico:
rtanzola@uns.edu.ar
Received December 12, 2011.
Accepted February 16, 2012.
Tanzola & Seguel
Stomachicola lycengraulidis parasite of Lycengraulis
66
