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
          TE
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)
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