Heliconema longissimum (Ortlepp, 1923) (Nematoda: Physalopteridae) from Pisodonophis boro (Teleostei: Ophichthidae) in Thailand, with Remakks on the Taxonomy of the Proleptinae Schulz, 1927 (Moravec et al, 2007)
Syst Parasitol (2007) 66:73–80
DOI 10.1007/s11230-006-9066-2
ORIGINAL PAPER
Heliconema longissimum (Ortlepp, 1923) (Nematoda:
Physalopteridae) from Pisodonophis boro (Teleostei:
Ophichthidae) in Thailand, with remarks on the taxonomy
of the Proleptinae Schulz, 1927
Frantisek Moravec Æ Horst Taraschewski Æ
ˇ
Malinee Thairungroj Anantaphruti Æ
Wanna Maipanich Æ Thitiporn Laoprasert
Received: 19 January 2006 / Accepted: 11 April 2006 / Published online: 29 November 2006
Ó Springer Science+Business Media B.V. 2006
discussed, where a new delimitation of Proleptus
Abstract Physalopterid nematodes identified as
Dujardin, 1845, Heliconema Travassos, 1919 and
Heliconema longissimum (Ortlepp, 1923) were
Paraleptus Wu, 1927 is proposed based on the
collected from the stomach of rice-paddy eels
cephalic dentation. H. minnanensis [sic] Damin &
Pisodonophis boro (Hamilton) (Anguilliformes:
Heqing, 2001 is transferred to Paraleptus Wu,
Ophichthidae) from two brackish-water localities
1927 as P. minnanensis (Damin & Heqing, 2001)
(mangroves) in Thailand: one in Phan-Nga
n. comb. and Paraleptus chiloscyllii Yin & Zhang,
Province, southwestern Thailand, northeast of
1983 transferred by Damin & Heqing (2001) to
Phuket Island, and one in Ranong Province, near
Heliconema, is retained in Paraleptus. H. ahiri
the border with Myanmar. Study of the mor-
Karve, 1941 is considered a junior synonym of H.
phology of this hitherto insufficiently known
longissimum (Ortlepp, 1923). The present finding
nematode species, including its first SEM exami-
of H. longissimum in Pisodonophis boro repre-
nation, enabled a detailed redescription of
sents the first host record and the first record of
H. longissimum. Present taxonomic problems in
this nematode from Thailand.
the subfamily Proleptinae Schulz, 1927 are
F. Moravec (&)
Institute of Parasitology, Biological Centre, Academy
ˇ ´
of Sciences of the Czech Republic, Branisovska 31,
Introduction
ˇ ´ ˇ
370 05 Ceske Budejovice, Czech Republic
e-mail: moravec@paru.cas.cz
To date, there are generally few data on the
H. Taraschewski
helminth parasites of freshwater, brackish-water
¨
Abteilung Okologie und Parasitologie, Zoologisches
and marine fishes in Thailand (Sirikanchana,
¨
Institut der Universitat Karlsruhe (TH), Kaiserstrasse
1982; Sood, 1989) and no anguilliform fish of this
12, 76128 Karlsruhe, Germany
region has so far been examined for parasites.
M. T. Anantaphruti Æ W. Maipanich
During recent years, studies on the parasites of
Department of Helminthology, Faculty of Tropical
anguilliforms in different regions of the world
Medicine, Mahidol University, 420/6 Ratchawithi
have been of special interest to fish parasitolo-
Road, Ratchadewee, Bangkok 10400, Thailand
gists, particularly in the connection with questions
T. Laoprasert
of the origin and distribution of the highly
Department of Fisheries, Aquatic Animal Health
pathogenic swimbladder nematodes of the genus
Research Institute, Paholyothin Road, Chatuchak,
Anguillicola Yamaguti, 1935.
Bangkok 10900, Thailand
123
74 Syst Parasitol (2007) 66:73–80
Fig. 1 Heliconema longissimum (Ortlepp, 1923) from c
In March 2001, a collection of the metazoan
Pisodonophis boro. A,B, anterior end of body, lateral
parasites of four species of anguilliform fishes
and dorsoventral views; C, cephalic end, apical view
(eels), Anguilla bicolor McClelland, A. japonica (reconstructed from SEM micrograph); D, small (right)
Temminck & Schlegel, A. marmorata Quoy & spicule, lateral view; E, distal end of large (left) spicule,
lateral view; F, cephalic end of male, lateral view; G,
Gaimard and Pisonodophis boro (Hamilton) was
cephalic end of female, dorsoventral view; H, deirid,
made during a short stay by one of us (H.T.) in
lateral view; I, mature egg; J, region of vulva, lateral view;
F
Thailand. Results of the systematic evaluation of K, tail tip of male, subventral view; L, caudal end of gravid
nematode material from Anguilla bicolor have female, lateral view; M,N, posterior end of male, lateral
OO
and ventral views. Scale-bars in mm
been published by Moravec et al. (2006), whereas
those concerning nematodes found in P. boro are Karve, 1941; Notopteroides alatae Majumdar,
presented herein.
1965; Paraleptus komiyai Sood, 1970
Host: Rice-paddy eel Pisodonophis boro (Ham-
PR
Materials and methods
ilton) (Anguilliformes: Ophichthidae).
Site of infection: Stomach.
Eels were caught in fish traps by local fishermen.
Localities: Mangroves (brackish water) in Phan-
After their capture they were examined for par-
Nga Province, southwestern Thailand, northeast
asites within 24 h. All eels infected with physa-
of Phuket Island, and mangroves from Ranong
lopterids were the rice-paddy eel Pisodonophis
D Province, near the border with Myanmar.
boro (Hamilton), 15 specimens of which were
Infection: Phan-Nga: prevalence 60% (6 of 10 eels
examined (total body length 70–92 cm): 10 from
examined); intensity 2–33 (mean 19). Ranong:
mangroves (brackish water) in Phan-Nga Prov-
TE
prevalence: in 2 of 5 eels examined; intensity 1
ince, southwestern Thailand, northeast of Phuket
and 7.
Island, and five from mangroves in Ranong
Voucher material: Institute of Parasitology,
Province, near the border with Myanmar.
ˇ ´ ˇ
ASCR, in Ceske Budejovice (cat. no. N–862).
The nematodes found were washed in physio-
EC
logical saline and then fixed in either boiling or cold
Description (Figs. 1, 2)
70% ethanol and preserved in 70% ethanol. For
light microscopical examination the nematodes
General. Body medium-sized, whitish, with thick
were cleared with glycerine. Drawings were made
transversely striated cuticle. Cephalic end roun-
with the aid of a Zeiss microscope drawing
RR
ded. Cuticle in cephalic region inflated to form
attachment. Specimens used for scanning electron
cephalic vesicle extending posteriorly to level of
microscopy (SEM) were post-fixed in 1% osmium
deirids. Oral aperture dorsoventrally elongate,
tetroxide, dehydrated through a graded alcohol
oval, rather large, surrounded by 2 massive,
series, critical point dried and sputter-coated with
rounded lateral pseudolabia; pseudolabium
gold; they were examined using a JSM-6300 scan-
CO
roughly rectangular in apical view (Fig. 2A),
ning electron microscope at an accelerating voltage
bearing 2 large submedian (dorsolateral and
of 15 kV. All measurements are in micrometres
ventrolateral) cephalic papillae and oval latero-
unless otherwise stated. The scientific names of
terminal depression; small lateral amphid situated
fishes are according to Froese and Pauly (2005).
at base of pseudolabium. Inner surface of each
UN
pseudolabium with elongate lateral mound bear-
ing marked triangular terminal lateral tooth
Family Physalopteridae Railliet, 1893
(internolateral tooth) and simple flat tooth at
Subfamily Proleptinae Schulz, 1927
each dorsoventral extremity; surface of each
pseudolabium forming 2 distinct small, narrow
Heliconema longissimum (Ortlepp, 1923)
submedian areas demarcated by grooves between
pseudolabium proper and inner lateral mould, in
Syns Physaloptera longissima Ortlepp, 1923;
apical view being broadest near lateral tooth and
Heliconema anguillae Yamaguti, 1935; H. ahiri
123
Syst Parasitol (2007) 66:73–80 75
123
76 Syst Parasitol (2007) 66:73–80
F
OO
PR
D
TE
EC
RR
Fig. 2 Heliconema longissimum (Ortlepp, 1923) from Pisodonophis boro, SEM micrographs. A, cephalic end, apical view;
CO
B, precloacal region of male, ventral view; C, posterior end of male, lateral view; D, tail of male, ventral view
gradually narrowing towards each dorsoventral Male (5 specimens). Length of body 23.50–
extremity (Fig. 2A); any series of denticles 27.00 mm, maximum width 530–612. Pseudolabia
absent. Buccal cavity short. Oesophagus divided 12–18 long. Cephalic vesicle 354–422 long, 218–
UN
into short, narrow anterior muscular portion 258 wide. Entire oesophagus 3.73–4.03 mm long,
and much longer, wide glandular portion. representing 14–17% of body length; muscular
Nerve-ring encircles muscular oesophagus pos- oesophagus 476–571 long, 68–95 wide; glandular
terior to its middle. Small simple deirids situ- oesophagus 3.16–3.50 mm long, 177–218 wide;
ated at level of nerve-ring. Excretory pore length ratio of parts of oesophagus 1:5.53–6.89.
slightly posterior to anterior end of glandular Nerve-ring, deirids and excretory pore 340–408,
oesophagus. Tail of both sexes with rounded 313–422 and 422–503, respectively, from anterior
tip. extremity. Caudal end spirally coiled, provided
123
Syst Parasitol (2007) 66:73–80 77
family Physalopteridae following the conception
with broad lateral alae supported by 4 twin pairs
of Chabaud (1975). However, mainly because of
of subventral pedunculate pre-anal papillae and 6
the many inadequate species descriptions of pro-
single pairs of subventral postanal papillae, of
leptines from fishes and occasionally the use of
which papillae of first 4 pairs are rather large and
unsuitable generic criteria, the taxonomy of this
pedunculate, and those of last 2 pairs are very
group, and especially regarding the delimitation
small and sessile; additional pair of rather small
of the genera, remains somewhat confused.
postanal sessile papillae situated ventrally at level
Within the Proleptinae, Chabaud (1975)
of first subventral postanal pair. Each caudal
recognised four genera, Proleptus Dujardin, 1845,
papilla surrounded by ring consisting of numerous
Heliconema Travassos, 1919, Paraleptus Wu, 1927
small cuticular, papilla-like protuberances (Fig. 2
and Bulbocephalus Rasheed, 1966, whereas the
B,D). Pair of minute phasmids present just pos-
morphologically similar Pseudoproleptus Khera,
terior to last pair of postanal papillae. Cloacal lips
1955, originally assigned to the Physalopteridae,
somewhat elevated. Ventral pre-cloacal surface
was listed in the habronematoid family Cystidi-
with about 17 longitudinal tesselated ridges (area
colidae Skryabin, 1946, as previoulsy suggested by
rugosa). Spicules unequal and dissimilar; left
Chabaud (1965).
spicule 520–734 long, with sharply pointed distal
Unfortunately, in the key to genera of Prolep-
tip and distal half (approximately) alate except
tinae given by Chabaud (1975), differential fea-
for conical tip; right spicule broader, boat-shaped,
tures, such as the position of the vulva and the
232–286 long, tapered towards distal tip. Length
length ratio of the spicules, are used, which, in our
ratio of spicules 1:1.82–3.16. Length of tail
opinion, are only of specific significance. For
381–422.
example, in different species of the cystidicolid
Female (5 gravid specimens). Length of body genus Spinitectus Fourment, 1883, the situation of
28.19–39.07 mm, maximum width 578–762. Pseu- the vulva is highly variable and may be near the
dolabia 12–18 long. Cephalic vesicle 422–435 anus (S. allaeri Campana-Rouget, 1961), at about
long, 231–340 wide. Entire oesophagus the middle of the body (S. multipapillatus Petter,
4.38–5.00 mm long, 13–16% of body length; 1987) or in the first third of the body length
muscular oesophagus 530–680 long, 82–122 wide; ˇ
(S. agonostomi Moravec & Barus, 1971). As
glandular oesophagus 3.85–4.38 mm long, pointed out by Threlfall and Carvajal (1984) in
218–340 wide; length ratio of parts of oesophagus Heliconema psammobatidus Threlfall and Carva-
1:5.66–7.26. Nerve-ring, deirids and excretory jal, 1984, and as observed in the present material,
pore 367–422, 408–435 and 544–585, respectively, the vulva may be somewhat pre-equatorial or
from anterior extremity. Rectum a hyaline tube. postequatorial within the same species. Regarding
Vulva situated 10.92–25.64 mm from anterior end the length ratio of spicules, this may be very var-
of body, at 39–66% of body length. Vagina iable within a genus, as previously mentioned by
narrow, muscular, initially directed anteriorly Sood (1970); for example, between different spe-
from vulva and then oriented posteriorly. Uteri cies of Rhabdochona Railliet, 1916, where the
containing numerous oval, thick-shelled, embry- spicules may be equally long (R. equispiculata
onated (larvated) eggs; eggs 75–81 · 42–48, with Moravec & Scholz, 1991) or very unequal (1:18–23
wall 5 thick. Tail short, 136–313 long, with roun- in R. kidderi texensis Moravec & Huffman, 1988);
ded tip; pair of small lateral phasmids present and a similar situation occurs within the camalla-
near tail tip. nid genus Procamallanus Baylis, 1923.
In our opinion, the delimitation of genera
within the Proleptinae, which are objectively
Discussion determined by their type species, should be based
on the cephalic features. It has already been
The general morphology of nematode specimens suggested by Chitwood and Wehr (1934) that the
of the present material shows that they belong to morphological structure of the cephalic region
the physalopterid subfamily Proleptinae of the should be used as an important character in the
123
78 Syst Parasitol (2007) 66:73–80
minnanensis [sic] Damin & Heqing, 2001 should
classification of spiruroid nematodes. In physa-
be transferred to Paraleptus as P. minnanensis
lopterids, Chabaud (1975) regarded the cephalic
(Damin & Heqing, 2001) n. comb.; and P. chil-
dentation, which corresponds to a great extent
oscyllii Yin & Zhang, 1983, transferred by
with a distribution in one or another group of
Damin and Heqing (2001) to Heliconema, should
hosts, to be a valuable character.
be retained in Paraleptus.
Of the four above-mentioned genera of the
F
The morphology of the present material from
Proleptinae, Bulbocephalus is easily distinguished
Pisodonophis boro shows that they belong to a
by the unusual structure of its cephalic end
OO
species of Heliconema, which is supported by their
(presence of protrusible oesophageal lobes, re-
eel host. At present this genus includes the fol-
duced pseudolabia, absence of cephalic collar-
lowing 13 species, which are listed chronologically:
ette). The characters of the remaining three
H. heliconema Travassos, 1919 (type-species); H.
genera are rather similar and, in fact, there are
longissimum (Ortlepp, 1923); H. brevispiculum
frequent confusions in assigning different species
Baylis, 1934; H. ahiri Karve, 1941; H. urolophi
to these genera. In our opinion, there is a need to
PR
re-diagnose them on the basis of a detailed study (Johnston & Mawson, 1951); H. baylisi Ogden,
of the cephalic structures of their type-species, all 1969; H. hamiltonii Bilqees & Khanum, 1970; H.
of which are inadequately described in this re- serpens Fusco & Palmieri, 1980; H. izecksohni
spect. Until a relevant revision is made, we sug- Fabio, 1982; H. psammobatidus Threlfall &
gest distinguishing these three genera on the basis Carvajal, 1984; H. kherai Gupta & Duggal, 1989;
D
of their cephalic dentation: H. brooksi Crites & Overstreet, 1991; and H.
savala Akram, 1996. Of these, H. hamiltonii, H.
Proleptus: Each pseudolabium with a single
izecksohni and H. urolophi should be considered
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internolateral tooth; outer rim of buccal cavity wall
species inquirendae (Crites and Overstreet 1991;
with a circumoral row of minute denticles (serra-
Moravec 1998).
tions). [These denticles were found in all three
The taxonomy of Heliconema spp. is compli-
Proleptus spp. studied by SEM and are apparently
cated by the fact that some morphological
a generic feature – see Specian, Ubelaker, & Dai-
EC
structures are difficult to observe under the light
´
ley, 1975; Moravec, Van As, & Dykova, 2002.].
microscope and, therefore, some species are
Mainly parasites of elasmobranchs.
evidently inadequately described. Moreover,
Heliconema: Internal border of each pseudolabi-
Fusco and Palmieri (1980) started to use the
um with an internolateral tooth only and usually
numbers of ventral precloacal tesselated longi-
RR
with a simple tooth at each dorsoventral extrem-
tudinal ridges (area rugosa) as the principle
ity. Mostly parasites of teleosts, particularly an-
differentiating feature between the species,
guilliforms.
which was followed by some subsequent authors.
Paraleptus: Internal border of each pseudolabium
However, in our opinion, this feature is quite
with a series of larger denticles in addition to the
unreliable, because the number of such ridges is
CO
internolateral tooth. Mainly parasites of elasmo-
rather variable within a species and depends
branchs.
partly on the body size and age of the worm, as
In having many denticles in the buccal cavity, has been observed in some other spirurine
Proleptus and Paraleptus appear to be more nematodes (e.g. Rhabdochona spp.), where these
closely related to each other than to Heliconema, may even be absent in younger specimens
UN
as reflected by their common principle hosts (Moravec, 1972).
(elasmobranchs). However, it is necessary to The present specimens can easily be distin-
note that the cephalic structures of most pro- guished by the length ratio of their spicules (1:1.8–
leptine species have not yet been studied in de- 3.2) from H. heliconema (1:12.7–20.0), H. brooksi
tail (preferably by SEM) and, accordingly, their (average 1:10.6), H. psammobatidus (1:4.1–4.3)
present generic allocations may not be correct. and H. baylisi (1:1.1–1.4), whereas H. brevispicu-
With respect to the above delimitation of the lum differs in possessing conspicuously large
genera, the recently described Heliconema papillae in the last two postanal pairs. H. serpens,
123
Syst Parasitol (2007) 66:73–80 79
described from a snake in Malaysia, allegedly has Heliconema longissimum (reported as Physa-
only four pairs of postanal papillae and a spicule loptera longissima) was first recorded by Ortlepp
ratio averaging 1:1.7. (1923) from ‘‘snakes’’ in Australia, but, as men-
The general morphology, including the length tioned by Ogden (1969) and some previous au-
ratio of the spicules, of the present specimens thors, the host (snakes) of the type-material is
corresponds, more or less, to the existing doubtful. Later, it was recorded from the eels
descriptions of H. longissimum (see Ortlepp, Anguilla bengalensis, A. japonica Temminck &
1923; Yamaguti, 1935; Ogden, 1969; Sood, 1970; Schlegel, A. mossambica (Peters) and A. pekin-
De et al., 1978; De, 1988), except for some details ensis (a probable synonym of A. japonica) (An-
in the structure of mouth and the number and guilliformes: Anguillidae) and from the swamp-
arrangement of the postanal papillae. However, eel Mastacembelus armatus (Synbranchiformes:
this species was not previously studied by SEM, Synbranchidae) in China, Japan, India and South
and some details are hardly visible under the light Africa (Li, 1934; Yamaguti, 1935; Karve, 1941;
microscope. Ogden, 1969; Sood, 1970; De et al,. 1978; De,
The differences mainly concern the postanal 1988; Taraschewski, Boomker, Knopf, & Mora-
papillae: while Ogden (1969) described six pairs vec, 2005). The present finding represents new
of these papillae, De, Ghosh, and Majumdar host and geographical records.
(1978) illustrated seven pairs (including phas-
Acknowledgements Thanks are due to the staff of the
mids), and it is worth noting that a group formed
Department of Helminthology, Faculty of Tropical Medi-
by the two last pairs of minute papillae and a pair cine, Mahidol University, Bangkok, to Dr Somboon Lao-
of phasmids is extremely difficult to observe. prasert, Chief of the Ranong Coastal Aquaculture Station,
However, De et al. (1978) did not find the pair of Ratchakrut, Muang and to Dr Supranee Chinabut,
Director of the Aquatic Animal Health Research Institute,
small sessile ventral papillae just posterior to the
Kasetsart University, Bangkok, for various forms of sup-
cloaca at the level of the first pair of postanal port, such as transport and/or accommodation. We also
pedunculate papillae. But such papillae were thank the staff of the Laboratory of Electron Microscopy
ˇ
illustrated in this species (reported as Paraleptus ´ ˇ
at the Institute of Parasitology, ASCR, Ceske Budejovice,
´ ´
for their technical assistance and Mrs Irena Husakova of
komiyai Sood, 1970) by Sood (1970), who, con-
the Department of Helminthology of the same Institute for
versely, failed to observe the last two pairs of her help with the preparation of the illustrations. The au-
minute papillae. The pair of sessile ventral thors are very grateful to Dr David I. Gibson, Natural
papillae located just posterior to the cloaca, as History Museum, London for revising the English and his
help with the literature. This study was supported by grant
confirmed by our SEM observations, has not yet
no. 524/06/0170 from the Grant Agency of the Czech
been reported for any other Heliconema species. Republic, Research Centre ‘‘Ichthyoparasitology’’
Because of this, the present material is considered (LC522) and a research project of the Institute of Parasi-
to be H. longissimum. tology, ASCR (no. Z60220518).
De et al. (1978) and De (1988) synonymised
two species, Paraleptus komiyai Sood, 1970 and
Notopteroides alatae Majumdar, 1965, both de-
References
´`
scribed from Mastacembelus armatus (Lacepede)
in India, with H. longissimum. But Sood (1989) ´
Chabaud, A. G. (1965). Classe des nematodes. Sous-classe
had considered the former as probably belonging des Secernentea (=Phasmidia auct.). Ordre des
to H. ahiri, a species described by Karve (1941) ´ ´
Spirurida. In P.-P. Grasse (Ed.), Traite de Zoologie,
´ ´
Tome 4, fasc. III. Nemathelminthes (Nematodes,
from Anguilla bengalensis (Gray) in India, which
´ `
Gordiaces), Rotiferes, Gastrotriches, Kinorhynques
allegedly differs from H. longissimum in having (pp. 1025–1151, 1187–1200). Paris: Masson et Cie.
three pairs of minute papillae (apparently Chabaud, A. G. (1975). Keys to genera of the order
including phasmids) near the tail tip (the tail was Spirurida. Part 1. Camallanoidea, Dracunculoidea,
Gnathostomatoidea, Physalopteroidea, Rictularioidea
observed only in lateral view). However, because
and Thelazioidea. In R. C. Anderson, A. G. Chabaud,
such papillae are also present in H. longissimum, & S. Willmott (Eds.), CIH keys to the nematode par-
we consider H. ahiri a junior synonym of asites of vertebrates. No. 3(1) (pp. 27). Farnham
H. longissimum. Royal: Commonwealth Agricultural Bureaux.
123
80 Syst Parasitol (2007) 66:73–80
Chitwood, B. G., & Wehr, E. E. (1934). The value of ce- allanus (Spirocamallanus) anguillae sp. n. (Camallani-
phalic structures as characters in nematode classifica- dae) and some other nematodes from the Indonesian
tion, with special reference to the superfamily shortfin eel Anguilla bicolor in Thailand. Parasitology
¨
Spiruroidea. Zeitschrift fur Parasitenkunde, 7, 273–335. Research, in press
Crites, J. L., & Overstreet, R. M. (1991). Heliconema ´
Moravec, F., Van As, J. G., Dykova, I. (2002). Proleptus
brooksi n. sp. (Nematoda: Physalopteridae) from the obtusus Dujardin, 1845 (Nematoda: Physalopteridae)
ophichthid eel Ophichthus gomesi in the Gulf of from the puffadder shyshark Haploblepharus edwar-
Mexico. Journal of Parasitology, 77, 42–50. dsii (Sciliorhinidae) from off South Africa. Systematic
F
Damin, L., & Heqing, H. (2001). Heliconema minnanensis Parasitology, 53, 169–173.
n. sp. (Physalopteroidea: Physalopteridae) and Ogden, C. G. (1969). A revision of the genus Heliconema
OO
Raphidascaris trichiuri (Yin et Zhang) n. comb. Travassos, 1919, Physalopteridae (Nematoda). Jour-
(Ascaridoidea: Anisakidae) in marine fishes. Journal nal of Natural History, 3, 423–431.
of Parasitology, 87, 1090–1094. Ortlepp, R. J. (1923). The nematode genus Physaloptera
De, N. C. (1988). Remarks on the validity of the species Rud. Proceedings of the Zoological Society of London,
Notopteroides alatae Majumdar, 1965. Folia Parasito- 999–1107.
logica, 35, 281–284. Sirikanchana, P. (1982). Check list of parasites of fishes in
De, N. C., Ghosh, M., & Majumdar, G. (1978). Records of Thailand. Notes from Faculty of Fisheries, Kasetsart
PR
some little known nematodes from Indian fishes. Folia University, Bangkok, 10, 1–11.
Parasitologica, 25, 317–322. Sood, M. L. (1970). On Paraleptus komiyai n. sp.
Froese, R., & Pauly, D. (Eds.). (2005). FishBase. World (Physalopteridae Leiper, 1908: Nematoda) from a
Wide Web electronic publication. www.fishbase.org, fresh water fish, Mastacembelus armatus from Luc-
version 12/2005. know, India. Japanese Journal of Parasitology, 19,
Fusco, A. C., & Palmieri, J. R. (1980). Heliconema serpens 437–439.
sp. n. (Nematoda: Physalopteridae) and Camallanides Sood, M. L. (1989). Fish nematodes. New Delhi–Ludhiana:
D
malayensis sp. n. (Nematoda: Camallanidae) from Kalyani Publishers, pp. 452–228.
Cerberus rhynchops (Schneider) (Reptilia: Colubri- Specian, R. D., Ubelaker, J. E., & Dailey, M. D. (1975).
dae) in Malaysia. Proceedings of the Helminthological Neoleptus gen. n. and a revision of the genus Proleptus
TE
Society of Washington, 47, 72–79. Dujardin, 1845. Proceedings of the Helminthological
Karve, J. N. (1941). Some parasitic nematodes of fishes. I. Society of Washington, 42, 14–21.
Journal of the University of Bombay, New Series, 10B, Taraschewski, H., Boomker, J., Knopf, K., & Moravec, F.
9–42. (2005) Anguillicola papernai (Nematoda: Anguilli-
Li, H. C. (1934). Report on a collection of parasitic nem- colidae) and other helminths parasitizing the African
atodes, mainly from North China. Part 2. Spiruroidea. longfin eel Anguilla mossambica. Diseases of Aquatic
EC
Transactions of the American Microscopical Society, Organisms, 63, 185–195.
53, 174–195. Threlfall, W., & Carvajal, J. (1984). Heliconema psam-
Moravec, F. (1972). General characterization of the nem- mobatidus sp. n. (Nematoda: Physalopteridae) from a
atode genus Rhabdochona with a review of the South skate, Psammobatis lima (Chondrichthyes: Rajidae),
American species. Acta Societatis Zoologicae Bohe- taken in Chile. Proceedings of the Helminthological
RR
moslovacae, 36, 29–46. Society of Washington, 51, 208–211.
Moravec, F. (1998). Nematodes of freshwater fishes of the Yamaguti, S. (1935) Studies on the helminth fauna of Ja-
Neotropical Region. Prague: Academia, 464 pp. pan. Part 9. I. Nematodes of fishes. Japanese Journal
Moravec, F., Taraschewski, H., Thairungroj Anantaphruti, of Zoology, 6, 337–386.
M., Maipanich, W., & Laoprasert, T. (2006). Procam-
CO
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123
DOI 10.1007/s11230-006-9066-2
ORIGINAL PAPER
Heliconema longissimum (Ortlepp, 1923) (Nematoda:
Physalopteridae) from Pisodonophis boro (Teleostei:
Ophichthidae) in Thailand, with remarks on the taxonomy
of the Proleptinae Schulz, 1927
Frantisek Moravec Æ Horst Taraschewski Æ
ˇ
Malinee Thairungroj Anantaphruti Æ
Wanna Maipanich Æ Thitiporn Laoprasert
Received: 19 January 2006 / Accepted: 11 April 2006 / Published online: 29 November 2006
Ó Springer Science+Business Media B.V. 2006
discussed, where a new delimitation of Proleptus
Abstract Physalopterid nematodes identified as
Dujardin, 1845, Heliconema Travassos, 1919 and
Heliconema longissimum (Ortlepp, 1923) were
Paraleptus Wu, 1927 is proposed based on the
collected from the stomach of rice-paddy eels
cephalic dentation. H. minnanensis [sic] Damin &
Pisodonophis boro (Hamilton) (Anguilliformes:
Heqing, 2001 is transferred to Paraleptus Wu,
Ophichthidae) from two brackish-water localities
1927 as P. minnanensis (Damin & Heqing, 2001)
(mangroves) in Thailand: one in Phan-Nga
n. comb. and Paraleptus chiloscyllii Yin & Zhang,
Province, southwestern Thailand, northeast of
1983 transferred by Damin & Heqing (2001) to
Phuket Island, and one in Ranong Province, near
Heliconema, is retained in Paraleptus. H. ahiri
the border with Myanmar. Study of the mor-
Karve, 1941 is considered a junior synonym of H.
phology of this hitherto insufficiently known
longissimum (Ortlepp, 1923). The present finding
nematode species, including its first SEM exami-
of H. longissimum in Pisodonophis boro repre-
nation, enabled a detailed redescription of
sents the first host record and the first record of
H. longissimum. Present taxonomic problems in
this nematode from Thailand.
the subfamily Proleptinae Schulz, 1927 are
F. Moravec (&)
Institute of Parasitology, Biological Centre, Academy
ˇ ´
of Sciences of the Czech Republic, Branisovska 31,
Introduction
ˇ ´ ˇ
370 05 Ceske Budejovice, Czech Republic
e-mail: moravec@paru.cas.cz
To date, there are generally few data on the
H. Taraschewski
helminth parasites of freshwater, brackish-water
¨
Abteilung Okologie und Parasitologie, Zoologisches
and marine fishes in Thailand (Sirikanchana,
¨
Institut der Universitat Karlsruhe (TH), Kaiserstrasse
1982; Sood, 1989) and no anguilliform fish of this
12, 76128 Karlsruhe, Germany
region has so far been examined for parasites.
M. T. Anantaphruti Æ W. Maipanich
During recent years, studies on the parasites of
Department of Helminthology, Faculty of Tropical
anguilliforms in different regions of the world
Medicine, Mahidol University, 420/6 Ratchawithi
have been of special interest to fish parasitolo-
Road, Ratchadewee, Bangkok 10400, Thailand
gists, particularly in the connection with questions
T. Laoprasert
of the origin and distribution of the highly
Department of Fisheries, Aquatic Animal Health
pathogenic swimbladder nematodes of the genus
Research Institute, Paholyothin Road, Chatuchak,
Anguillicola Yamaguti, 1935.
Bangkok 10900, Thailand
123
74 Syst Parasitol (2007) 66:73–80
Fig. 1 Heliconema longissimum (Ortlepp, 1923) from c
In March 2001, a collection of the metazoan
Pisodonophis boro. A,B, anterior end of body, lateral
parasites of four species of anguilliform fishes
and dorsoventral views; C, cephalic end, apical view
(eels), Anguilla bicolor McClelland, A. japonica (reconstructed from SEM micrograph); D, small (right)
Temminck & Schlegel, A. marmorata Quoy & spicule, lateral view; E, distal end of large (left) spicule,
lateral view; F, cephalic end of male, lateral view; G,
Gaimard and Pisonodophis boro (Hamilton) was
cephalic end of female, dorsoventral view; H, deirid,
made during a short stay by one of us (H.T.) in
lateral view; I, mature egg; J, region of vulva, lateral view;
F
Thailand. Results of the systematic evaluation of K, tail tip of male, subventral view; L, caudal end of gravid
nematode material from Anguilla bicolor have female, lateral view; M,N, posterior end of male, lateral
OO
and ventral views. Scale-bars in mm
been published by Moravec et al. (2006), whereas
those concerning nematodes found in P. boro are Karve, 1941; Notopteroides alatae Majumdar,
presented herein.
1965; Paraleptus komiyai Sood, 1970
Host: Rice-paddy eel Pisodonophis boro (Ham-
PR
Materials and methods
ilton) (Anguilliformes: Ophichthidae).
Site of infection: Stomach.
Eels were caught in fish traps by local fishermen.
Localities: Mangroves (brackish water) in Phan-
After their capture they were examined for par-
Nga Province, southwestern Thailand, northeast
asites within 24 h. All eels infected with physa-
of Phuket Island, and mangroves from Ranong
lopterids were the rice-paddy eel Pisodonophis
D Province, near the border with Myanmar.
boro (Hamilton), 15 specimens of which were
Infection: Phan-Nga: prevalence 60% (6 of 10 eels
examined (total body length 70–92 cm): 10 from
examined); intensity 2–33 (mean 19). Ranong:
mangroves (brackish water) in Phan-Nga Prov-
TE
prevalence: in 2 of 5 eels examined; intensity 1
ince, southwestern Thailand, northeast of Phuket
and 7.
Island, and five from mangroves in Ranong
Voucher material: Institute of Parasitology,
Province, near the border with Myanmar.
ˇ ´ ˇ
ASCR, in Ceske Budejovice (cat. no. N–862).
The nematodes found were washed in physio-
EC
logical saline and then fixed in either boiling or cold
Description (Figs. 1, 2)
70% ethanol and preserved in 70% ethanol. For
light microscopical examination the nematodes
General. Body medium-sized, whitish, with thick
were cleared with glycerine. Drawings were made
transversely striated cuticle. Cephalic end roun-
with the aid of a Zeiss microscope drawing
RR
ded. Cuticle in cephalic region inflated to form
attachment. Specimens used for scanning electron
cephalic vesicle extending posteriorly to level of
microscopy (SEM) were post-fixed in 1% osmium
deirids. Oral aperture dorsoventrally elongate,
tetroxide, dehydrated through a graded alcohol
oval, rather large, surrounded by 2 massive,
series, critical point dried and sputter-coated with
rounded lateral pseudolabia; pseudolabium
gold; they were examined using a JSM-6300 scan-
CO
roughly rectangular in apical view (Fig. 2A),
ning electron microscope at an accelerating voltage
bearing 2 large submedian (dorsolateral and
of 15 kV. All measurements are in micrometres
ventrolateral) cephalic papillae and oval latero-
unless otherwise stated. The scientific names of
terminal depression; small lateral amphid situated
fishes are according to Froese and Pauly (2005).
at base of pseudolabium. Inner surface of each
UN
pseudolabium with elongate lateral mound bear-
ing marked triangular terminal lateral tooth
Family Physalopteridae Railliet, 1893
(internolateral tooth) and simple flat tooth at
Subfamily Proleptinae Schulz, 1927
each dorsoventral extremity; surface of each
pseudolabium forming 2 distinct small, narrow
Heliconema longissimum (Ortlepp, 1923)
submedian areas demarcated by grooves between
pseudolabium proper and inner lateral mould, in
Syns Physaloptera longissima Ortlepp, 1923;
apical view being broadest near lateral tooth and
Heliconema anguillae Yamaguti, 1935; H. ahiri
123
Syst Parasitol (2007) 66:73–80 75
123
76 Syst Parasitol (2007) 66:73–80
F
OO
PR
D
TE
EC
RR
Fig. 2 Heliconema longissimum (Ortlepp, 1923) from Pisodonophis boro, SEM micrographs. A, cephalic end, apical view;
CO
B, precloacal region of male, ventral view; C, posterior end of male, lateral view; D, tail of male, ventral view
gradually narrowing towards each dorsoventral Male (5 specimens). Length of body 23.50–
extremity (Fig. 2A); any series of denticles 27.00 mm, maximum width 530–612. Pseudolabia
absent. Buccal cavity short. Oesophagus divided 12–18 long. Cephalic vesicle 354–422 long, 218–
UN
into short, narrow anterior muscular portion 258 wide. Entire oesophagus 3.73–4.03 mm long,
and much longer, wide glandular portion. representing 14–17% of body length; muscular
Nerve-ring encircles muscular oesophagus pos- oesophagus 476–571 long, 68–95 wide; glandular
terior to its middle. Small simple deirids situ- oesophagus 3.16–3.50 mm long, 177–218 wide;
ated at level of nerve-ring. Excretory pore length ratio of parts of oesophagus 1:5.53–6.89.
slightly posterior to anterior end of glandular Nerve-ring, deirids and excretory pore 340–408,
oesophagus. Tail of both sexes with rounded 313–422 and 422–503, respectively, from anterior
tip. extremity. Caudal end spirally coiled, provided
123
Syst Parasitol (2007) 66:73–80 77
family Physalopteridae following the conception
with broad lateral alae supported by 4 twin pairs
of Chabaud (1975). However, mainly because of
of subventral pedunculate pre-anal papillae and 6
the many inadequate species descriptions of pro-
single pairs of subventral postanal papillae, of
leptines from fishes and occasionally the use of
which papillae of first 4 pairs are rather large and
unsuitable generic criteria, the taxonomy of this
pedunculate, and those of last 2 pairs are very
group, and especially regarding the delimitation
small and sessile; additional pair of rather small
of the genera, remains somewhat confused.
postanal sessile papillae situated ventrally at level
Within the Proleptinae, Chabaud (1975)
of first subventral postanal pair. Each caudal
recognised four genera, Proleptus Dujardin, 1845,
papilla surrounded by ring consisting of numerous
Heliconema Travassos, 1919, Paraleptus Wu, 1927
small cuticular, papilla-like protuberances (Fig. 2
and Bulbocephalus Rasheed, 1966, whereas the
B,D). Pair of minute phasmids present just pos-
morphologically similar Pseudoproleptus Khera,
terior to last pair of postanal papillae. Cloacal lips
1955, originally assigned to the Physalopteridae,
somewhat elevated. Ventral pre-cloacal surface
was listed in the habronematoid family Cystidi-
with about 17 longitudinal tesselated ridges (area
colidae Skryabin, 1946, as previoulsy suggested by
rugosa). Spicules unequal and dissimilar; left
Chabaud (1965).
spicule 520–734 long, with sharply pointed distal
Unfortunately, in the key to genera of Prolep-
tip and distal half (approximately) alate except
tinae given by Chabaud (1975), differential fea-
for conical tip; right spicule broader, boat-shaped,
tures, such as the position of the vulva and the
232–286 long, tapered towards distal tip. Length
length ratio of the spicules, are used, which, in our
ratio of spicules 1:1.82–3.16. Length of tail
opinion, are only of specific significance. For
381–422.
example, in different species of the cystidicolid
Female (5 gravid specimens). Length of body genus Spinitectus Fourment, 1883, the situation of
28.19–39.07 mm, maximum width 578–762. Pseu- the vulva is highly variable and may be near the
dolabia 12–18 long. Cephalic vesicle 422–435 anus (S. allaeri Campana-Rouget, 1961), at about
long, 231–340 wide. Entire oesophagus the middle of the body (S. multipapillatus Petter,
4.38–5.00 mm long, 13–16% of body length; 1987) or in the first third of the body length
muscular oesophagus 530–680 long, 82–122 wide; ˇ
(S. agonostomi Moravec & Barus, 1971). As
glandular oesophagus 3.85–4.38 mm long, pointed out by Threlfall and Carvajal (1984) in
218–340 wide; length ratio of parts of oesophagus Heliconema psammobatidus Threlfall and Carva-
1:5.66–7.26. Nerve-ring, deirids and excretory jal, 1984, and as observed in the present material,
pore 367–422, 408–435 and 544–585, respectively, the vulva may be somewhat pre-equatorial or
from anterior extremity. Rectum a hyaline tube. postequatorial within the same species. Regarding
Vulva situated 10.92–25.64 mm from anterior end the length ratio of spicules, this may be very var-
of body, at 39–66% of body length. Vagina iable within a genus, as previously mentioned by
narrow, muscular, initially directed anteriorly Sood (1970); for example, between different spe-
from vulva and then oriented posteriorly. Uteri cies of Rhabdochona Railliet, 1916, where the
containing numerous oval, thick-shelled, embry- spicules may be equally long (R. equispiculata
onated (larvated) eggs; eggs 75–81 · 42–48, with Moravec & Scholz, 1991) or very unequal (1:18–23
wall 5 thick. Tail short, 136–313 long, with roun- in R. kidderi texensis Moravec & Huffman, 1988);
ded tip; pair of small lateral phasmids present and a similar situation occurs within the camalla-
near tail tip. nid genus Procamallanus Baylis, 1923.
In our opinion, the delimitation of genera
within the Proleptinae, which are objectively
Discussion determined by their type species, should be based
on the cephalic features. It has already been
The general morphology of nematode specimens suggested by Chitwood and Wehr (1934) that the
of the present material shows that they belong to morphological structure of the cephalic region
the physalopterid subfamily Proleptinae of the should be used as an important character in the
123
78 Syst Parasitol (2007) 66:73–80
minnanensis [sic] Damin & Heqing, 2001 should
classification of spiruroid nematodes. In physa-
be transferred to Paraleptus as P. minnanensis
lopterids, Chabaud (1975) regarded the cephalic
(Damin & Heqing, 2001) n. comb.; and P. chil-
dentation, which corresponds to a great extent
oscyllii Yin & Zhang, 1983, transferred by
with a distribution in one or another group of
Damin and Heqing (2001) to Heliconema, should
hosts, to be a valuable character.
be retained in Paraleptus.
Of the four above-mentioned genera of the
F
The morphology of the present material from
Proleptinae, Bulbocephalus is easily distinguished
Pisodonophis boro shows that they belong to a
by the unusual structure of its cephalic end
OO
species of Heliconema, which is supported by their
(presence of protrusible oesophageal lobes, re-
eel host. At present this genus includes the fol-
duced pseudolabia, absence of cephalic collar-
lowing 13 species, which are listed chronologically:
ette). The characters of the remaining three
H. heliconema Travassos, 1919 (type-species); H.
genera are rather similar and, in fact, there are
longissimum (Ortlepp, 1923); H. brevispiculum
frequent confusions in assigning different species
Baylis, 1934; H. ahiri Karve, 1941; H. urolophi
to these genera. In our opinion, there is a need to
PR
re-diagnose them on the basis of a detailed study (Johnston & Mawson, 1951); H. baylisi Ogden,
of the cephalic structures of their type-species, all 1969; H. hamiltonii Bilqees & Khanum, 1970; H.
of which are inadequately described in this re- serpens Fusco & Palmieri, 1980; H. izecksohni
spect. Until a relevant revision is made, we sug- Fabio, 1982; H. psammobatidus Threlfall &
gest distinguishing these three genera on the basis Carvajal, 1984; H. kherai Gupta & Duggal, 1989;
D
of their cephalic dentation: H. brooksi Crites & Overstreet, 1991; and H.
savala Akram, 1996. Of these, H. hamiltonii, H.
Proleptus: Each pseudolabium with a single
izecksohni and H. urolophi should be considered
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internolateral tooth; outer rim of buccal cavity wall
species inquirendae (Crites and Overstreet 1991;
with a circumoral row of minute denticles (serra-
Moravec 1998).
tions). [These denticles were found in all three
The taxonomy of Heliconema spp. is compli-
Proleptus spp. studied by SEM and are apparently
cated by the fact that some morphological
a generic feature – see Specian, Ubelaker, & Dai-
EC
structures are difficult to observe under the light
´
ley, 1975; Moravec, Van As, & Dykova, 2002.].
microscope and, therefore, some species are
Mainly parasites of elasmobranchs.
evidently inadequately described. Moreover,
Heliconema: Internal border of each pseudolabi-
Fusco and Palmieri (1980) started to use the
um with an internolateral tooth only and usually
numbers of ventral precloacal tesselated longi-
RR
with a simple tooth at each dorsoventral extrem-
tudinal ridges (area rugosa) as the principle
ity. Mostly parasites of teleosts, particularly an-
differentiating feature between the species,
guilliforms.
which was followed by some subsequent authors.
Paraleptus: Internal border of each pseudolabium
However, in our opinion, this feature is quite
with a series of larger denticles in addition to the
unreliable, because the number of such ridges is
CO
internolateral tooth. Mainly parasites of elasmo-
rather variable within a species and depends
branchs.
partly on the body size and age of the worm, as
In having many denticles in the buccal cavity, has been observed in some other spirurine
Proleptus and Paraleptus appear to be more nematodes (e.g. Rhabdochona spp.), where these
closely related to each other than to Heliconema, may even be absent in younger specimens
UN
as reflected by their common principle hosts (Moravec, 1972).
(elasmobranchs). However, it is necessary to The present specimens can easily be distin-
note that the cephalic structures of most pro- guished by the length ratio of their spicules (1:1.8–
leptine species have not yet been studied in de- 3.2) from H. heliconema (1:12.7–20.0), H. brooksi
tail (preferably by SEM) and, accordingly, their (average 1:10.6), H. psammobatidus (1:4.1–4.3)
present generic allocations may not be correct. and H. baylisi (1:1.1–1.4), whereas H. brevispicu-
With respect to the above delimitation of the lum differs in possessing conspicuously large
genera, the recently described Heliconema papillae in the last two postanal pairs. H. serpens,
123
Syst Parasitol (2007) 66:73–80 79
described from a snake in Malaysia, allegedly has Heliconema longissimum (reported as Physa-
only four pairs of postanal papillae and a spicule loptera longissima) was first recorded by Ortlepp
ratio averaging 1:1.7. (1923) from ‘‘snakes’’ in Australia, but, as men-
The general morphology, including the length tioned by Ogden (1969) and some previous au-
ratio of the spicules, of the present specimens thors, the host (snakes) of the type-material is
corresponds, more or less, to the existing doubtful. Later, it was recorded from the eels
descriptions of H. longissimum (see Ortlepp, Anguilla bengalensis, A. japonica Temminck &
1923; Yamaguti, 1935; Ogden, 1969; Sood, 1970; Schlegel, A. mossambica (Peters) and A. pekin-
De et al., 1978; De, 1988), except for some details ensis (a probable synonym of A. japonica) (An-
in the structure of mouth and the number and guilliformes: Anguillidae) and from the swamp-
arrangement of the postanal papillae. However, eel Mastacembelus armatus (Synbranchiformes:
this species was not previously studied by SEM, Synbranchidae) in China, Japan, India and South
and some details are hardly visible under the light Africa (Li, 1934; Yamaguti, 1935; Karve, 1941;
microscope. Ogden, 1969; Sood, 1970; De et al,. 1978; De,
The differences mainly concern the postanal 1988; Taraschewski, Boomker, Knopf, & Mora-
papillae: while Ogden (1969) described six pairs vec, 2005). The present finding represents new
of these papillae, De, Ghosh, and Majumdar host and geographical records.
(1978) illustrated seven pairs (including phas-
Acknowledgements Thanks are due to the staff of the
mids), and it is worth noting that a group formed
Department of Helminthology, Faculty of Tropical Medi-
by the two last pairs of minute papillae and a pair cine, Mahidol University, Bangkok, to Dr Somboon Lao-
of phasmids is extremely difficult to observe. prasert, Chief of the Ranong Coastal Aquaculture Station,
However, De et al. (1978) did not find the pair of Ratchakrut, Muang and to Dr Supranee Chinabut,
Director of the Aquatic Animal Health Research Institute,
small sessile ventral papillae just posterior to the
Kasetsart University, Bangkok, for various forms of sup-
cloaca at the level of the first pair of postanal port, such as transport and/or accommodation. We also
pedunculate papillae. But such papillae were thank the staff of the Laboratory of Electron Microscopy
ˇ
illustrated in this species (reported as Paraleptus ´ ˇ
at the Institute of Parasitology, ASCR, Ceske Budejovice,
´ ´
for their technical assistance and Mrs Irena Husakova of
komiyai Sood, 1970) by Sood (1970), who, con-
the Department of Helminthology of the same Institute for
versely, failed to observe the last two pairs of her help with the preparation of the illustrations. The au-
minute papillae. The pair of sessile ventral thors are very grateful to Dr David I. Gibson, Natural
papillae located just posterior to the cloaca, as History Museum, London for revising the English and his
help with the literature. This study was supported by grant
confirmed by our SEM observations, has not yet
no. 524/06/0170 from the Grant Agency of the Czech
been reported for any other Heliconema species. Republic, Research Centre ‘‘Ichthyoparasitology’’
Because of this, the present material is considered (LC522) and a research project of the Institute of Parasi-
to be H. longissimum. tology, ASCR (no. Z60220518).
De et al. (1978) and De (1988) synonymised
two species, Paraleptus komiyai Sood, 1970 and
Notopteroides alatae Majumdar, 1965, both de-
References
´`
scribed from Mastacembelus armatus (Lacepede)
in India, with H. longissimum. But Sood (1989) ´
Chabaud, A. G. (1965). Classe des nematodes. Sous-classe
had considered the former as probably belonging des Secernentea (=Phasmidia auct.). Ordre des
to H. ahiri, a species described by Karve (1941) ´ ´
Spirurida. In P.-P. Grasse (Ed.), Traite de Zoologie,
´ ´
Tome 4, fasc. III. Nemathelminthes (Nematodes,
from Anguilla bengalensis (Gray) in India, which
´ `
Gordiaces), Rotiferes, Gastrotriches, Kinorhynques
allegedly differs from H. longissimum in having (pp. 1025–1151, 1187–1200). Paris: Masson et Cie.
three pairs of minute papillae (apparently Chabaud, A. G. (1975). Keys to genera of the order
including phasmids) near the tail tip (the tail was Spirurida. Part 1. Camallanoidea, Dracunculoidea,
Gnathostomatoidea, Physalopteroidea, Rictularioidea
observed only in lateral view). However, because
and Thelazioidea. In R. C. Anderson, A. G. Chabaud,
such papillae are also present in H. longissimum, & S. Willmott (Eds.), CIH keys to the nematode par-
we consider H. ahiri a junior synonym of asites of vertebrates. No. 3(1) (pp. 27). Farnham
H. longissimum. Royal: Commonwealth Agricultural Bureaux.
123
80 Syst Parasitol (2007) 66:73–80
Chitwood, B. G., & Wehr, E. E. (1934). The value of ce- allanus (Spirocamallanus) anguillae sp. n. (Camallani-
phalic structures as characters in nematode classifica- dae) and some other nematodes from the Indonesian
tion, with special reference to the superfamily shortfin eel Anguilla bicolor in Thailand. Parasitology
¨
Spiruroidea. Zeitschrift fur Parasitenkunde, 7, 273–335. Research, in press
Crites, J. L., & Overstreet, R. M. (1991). Heliconema ´
Moravec, F., Van As, J. G., Dykova, I. (2002). Proleptus
brooksi n. sp. (Nematoda: Physalopteridae) from the obtusus Dujardin, 1845 (Nematoda: Physalopteridae)
ophichthid eel Ophichthus gomesi in the Gulf of from the puffadder shyshark Haploblepharus edwar-
Mexico. Journal of Parasitology, 77, 42–50. dsii (Sciliorhinidae) from off South Africa. Systematic
F
Damin, L., & Heqing, H. (2001). Heliconema minnanensis Parasitology, 53, 169–173.
n. sp. (Physalopteroidea: Physalopteridae) and Ogden, C. G. (1969). A revision of the genus Heliconema
OO
Raphidascaris trichiuri (Yin et Zhang) n. comb. Travassos, 1919, Physalopteridae (Nematoda). Jour-
(Ascaridoidea: Anisakidae) in marine fishes. Journal nal of Natural History, 3, 423–431.
of Parasitology, 87, 1090–1094. Ortlepp, R. J. (1923). The nematode genus Physaloptera
De, N. C. (1988). Remarks on the validity of the species Rud. Proceedings of the Zoological Society of London,
Notopteroides alatae Majumdar, 1965. Folia Parasito- 999–1107.
logica, 35, 281–284. Sirikanchana, P. (1982). Check list of parasites of fishes in
De, N. C., Ghosh, M., & Majumdar, G. (1978). Records of Thailand. Notes from Faculty of Fisheries, Kasetsart
PR
some little known nematodes from Indian fishes. Folia University, Bangkok, 10, 1–11.
Parasitologica, 25, 317–322. Sood, M. L. (1970). On Paraleptus komiyai n. sp.
Froese, R., & Pauly, D. (Eds.). (2005). FishBase. World (Physalopteridae Leiper, 1908: Nematoda) from a
Wide Web electronic publication. www.fishbase.org, fresh water fish, Mastacembelus armatus from Luc-
version 12/2005. know, India. Japanese Journal of Parasitology, 19,
Fusco, A. C., & Palmieri, J. R. (1980). Heliconema serpens 437–439.
sp. n. (Nematoda: Physalopteridae) and Camallanides Sood, M. L. (1989). Fish nematodes. New Delhi–Ludhiana:
D
malayensis sp. n. (Nematoda: Camallanidae) from Kalyani Publishers, pp. 452–228.
Cerberus rhynchops (Schneider) (Reptilia: Colubri- Specian, R. D., Ubelaker, J. E., & Dailey, M. D. (1975).
dae) in Malaysia. Proceedings of the Helminthological Neoleptus gen. n. and a revision of the genus Proleptus
TE
Society of Washington, 47, 72–79. Dujardin, 1845. Proceedings of the Helminthological
Karve, J. N. (1941). Some parasitic nematodes of fishes. I. Society of Washington, 42, 14–21.
Journal of the University of Bombay, New Series, 10B, Taraschewski, H., Boomker, J., Knopf, K., & Moravec, F.
9–42. (2005) Anguillicola papernai (Nematoda: Anguilli-
Li, H. C. (1934). Report on a collection of parasitic nem- colidae) and other helminths parasitizing the African
atodes, mainly from North China. Part 2. Spiruroidea. longfin eel Anguilla mossambica. Diseases of Aquatic
EC
Transactions of the American Microscopical Society, Organisms, 63, 185–195.
53, 174–195. Threlfall, W., & Carvajal, J. (1984). Heliconema psam-
Moravec, F. (1972). General characterization of the nem- mobatidus sp. n. (Nematoda: Physalopteridae) from a
atode genus Rhabdochona with a review of the South skate, Psammobatis lima (Chondrichthyes: Rajidae),
American species. Acta Societatis Zoologicae Bohe- taken in Chile. Proceedings of the Helminthological
RR
moslovacae, 36, 29–46. Society of Washington, 51, 208–211.
Moravec, F. (1998). Nematodes of freshwater fishes of the Yamaguti, S. (1935) Studies on the helminth fauna of Ja-
Neotropical Region. Prague: Academia, 464 pp. pan. Part 9. I. Nematodes of fishes. Japanese Journal
Moravec, F., Taraschewski, H., Thairungroj Anantaphruti, of Zoology, 6, 337–386.
M., Maipanich, W., & Laoprasert, T. (2006). Procam-
CO
UN
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