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Systematic Parasitology 41: 1–8, 1998.
© 1998 Kluwer Academic Publishers. Printed in the Netherlands.
1
Taxonomic status of Pelichnibothrium speciosum Monticelli, 1889
(Cestoda: Tetraphyllidea), a mysterious parasite of Alepisaurus ferox
Lowe (Teleostei: Alepisauridae) and Prionace glauca (L.) (Euselachii:
Carcharinidae)
Tom
´
aš Scholz
1
, Louis Euzet
2
& František Moravec
1
1
Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovsk´a 31, 370 05
ˇ
Cesk´eBudˇejovice,
Czech Republic
2
Station M´editerran´eenne de l’Environment Littoral, 1, quai de la Daurade, 34200 S`ete, France
Accepted for publication 23rd February, 1998
Abstract
Comparison of freshly collected tetraphyllidean cestodes from a teleost fish, Alepisaurus ferox Lowe, from Japan
with types and vouchers of Pelichnibothrium speciosum Monticelli, 1889, described from the same host, and
specimens of Prionacestus bipartitus Mete & Euzet, 1996, from the spiral valve of a shark, Prionace glauca
(Linnaeus), from the Indian Ocean between Réunion and Madagascar, revealed their conspecificity. Consequently,
P. bipartitus is considered a junior synonym of P. speciosum and the genus Prionacestus Mete & Euzet, 1996 is
suppressed. The life-cycle of the parasite, which retains larval features and is considered to represent a neotenic
form, is discussed.
Introduction
During an examination of a teleost fish, Alepisaurus
ferox Lowe (Scopeliformes: Alepisauridae) from
Shimizu, Japan, tetraphyllidean cestodes were found
by one of the authors (FM). The evaluation of these
tapeworms revealed that they belonged to the species
Pelichnibothrium speciosum Monticelli, 1889, as re-
described by Yamaguti (1934) on the basis of spec-
imens from the shark Prionace glauca (Linnaeus)
(Selachii: Carcharinidae). Since there has been some
confusion as to the validity of this parasite (see Euzet,
1994; Mete & Euzet, 1996), its taxonomic status and
life-cycle are discussed in the present paper, based on
new material and the examination of type-specimens
of P. speciosum.
Materials and methods
Tapeworms were found in the stomach and mainly
in the intestine of a specimen of Alepisaurus ferox
measuring 100 cm in total length, collected from
Shimizu, Miho Peninsula, Shizuoka Prefecture, Japan
(35
◦
00
0
N; 138
◦
33
0
E), on 1 February 1997. They were
fixed in 4% formaldehyde, then washed in water and
70% ethanol and stained with either hydrochloric or
acetic carmines. All measurements in descriptions are
in micrometres unless otherwise stated.
The following specimens were studied (acronyms
of museums: The Natural History Museum, Lon-
don, UK – BMNH; Institute of Parasitology,
ˇ
Ceské
Bud
ˇ
ejovice, Czech Republic – IPCAS; Muséum
d’Histoire Naturelle, Paris, France – MHNP; Meguro
Parasitological Museum, Tokyo, Japan – MPM; Nat-
ural Science Museum, Tokyo, Japan – NSMT; US
National Parasite Collection, Beltsville, Maryland,
USA – USNPC): several fragments of a few spec-
imens of Pelichnibothrium speciosum (BMNH No.
1997.9.19.1)designated“? types” from Alepidosaurus
(= Alepisaurus) ferox, from Madeira, Atlantic Ocean;
2 voucher specimens (BMNH Nos 1975.6.25.1–20
and 1975.6.25.21–30) from A. ferox, from Miami
Beach, Florida, USA, and from South East coast of
Iceland; 2 specimens from A. ferox from New York
Bight, USA (R. Campbell private collection); 86 spec-
2
imens of P. speciosum (3 specimens – BMNH No.
1997.9.25.1–2, 1998.2.26.3–5; 13 mounted spec. and
55 spec. in vial – IPCAS No. C-268; 5 spec. –
MHNP No. 589 HF Tk 120–124; 3 spec. – MPM No.
19723; 2 spec. – NSMT Nos Pl-5024 and Pl-5025;
3 spec. – USNPC No. 87728; 2 spec. in second au-
thor’s collection) from A. ferox, from Shimizu, Japan;
several vouchers of Prionacestus bipartitus (second
author’s collection) from Prionace glauca, from In-
dian Ocean between Réunion and Madagascar. One
of the few specimens of Monticelli (syntypes) from
A. ferox listed above (BMNH No. 1997.9.19.1) was
stained with hydrochloric carmine and mounted as a
permanent preparation.
Results
Comparison of tapeworms from Alepisaurus ferox
from Japan with type and voucher specimens of
Pelichnibothrium speciosum Monticelli, 1899, as well
as vouchers of Prionacestus bipartitus Mete & Euzet,
1996 from Prionace glauca, revealed their conspeci-
ficity. Therefore, P. bipartitus is considered a junior
synonym of P. speciosum. Considering previous con-
fusion concerning the taxonomic status of both taxa,
an amended description of P. speciosum is presented
(Figures 1–4). This description is based on measure-
ments of only 10 specimens from Japan, because it
was difficult to obtain specimens suitable for mor-
phological evaluation due to the presence of strongly
plicated strobila (Figure 1A).
Pelichnibothrium speciosum Monticelli, 1899
Amended description
Based on material from Alepisaurus ferox (measure-
ments of the only stained and mounted syntype in
parentheses). Tapeworms of very variable size, 12–
185 mm long (one specimen from New York 330 mm
long), consisting of 3 parts (Figure 1A): scolex,
strobila separated from scolex by very short neck,
and bladder (“tail” of Yamaguti, 1934; “vésicule
postérieure” of Mete & Euzet, 1996). Scolex (Figures
1B,2) oval, 1.34–2.25 (1.38) mm long by 1.42–2.03
(1.40) mm wide, with 4 bothridia (2 ventral and 2
dorsal) and spherical apical sucker (Figure 1C). Both-
ridia slightly tapered anteriorly, 1.26–1.95 mm long
by 568–974 wide (contracted and deformed in syn-
type), with anteriorly situated accessory suckers (Fig-
ure 1D) measuring 266–320 (256–264) × 280–376
(264–296); apical sucker 176–240 (168) × 192–240
(208), smaller than bothridial suckers [ratio 1: 1.17–
1.48 (1.44)]. Neck very short, indistinctly separated
from strobila, 0.93–1.32 mm wide (contracted in syn-
type). Scolex, including bothridial cavity and cavity
of bothridial sucker, and neck densely covered with
hair-like microtriches (Figure 1E–G).
Strobila (Figure 1A) strongly plicated, consist-
ing of 14–250 (30) short, wide proglottides (Figure
3). No mature (with spermatozoa in vas deferens)
or gravid (with eggs in uterus) proglottides present
even in largest specimens. Anterior 10–25 proglot-
tides exhibit only primordia of genitalia (vas deferens
and vagina) which appear almost immediately pos-
terior to scolex (Figure 2). Subsequent proglottides,
including last which measure 2.44–5.08 (2.64–3.25)
mm wide by 365–670(609–711) long, remain at same
state of maturity, although genitalia are more devel-
oped. Longitudinal musculature well developed, with
conspicuous median band of muscular fibres. Testes
occupying 2 lateral fields which are not confluent
medially, but reach posterior to margin of proglottis
(Figure 3). Testes 39–114 (81–116) × 31–81 (52–80),
very numerous (>400), lying in 3–4 layers; approx.
200–230 testes on poral side, even more on aporal
side. External vas deferens forms numerous small
loops which reach to mid-line of proglottis and cross
vaginalcanal at level of median margin of poral testic-
ular field (Figure 3); no spermatozoa observed within
vas deferens. Internal vas deferens straight. Cirrus-sac
thick-walled, elongate, 448–770 (464–640) long by
86–125 (80–138) wide; genital pore post-equatorial,
irregularly alternating.
Ovary tetra-lobed in cross-section, bi-lobed in
dorsoventral view, situated near posterior margin of
proglottis, with narrow ovarian isthmus; total length
0.87–1.77(1.32–1.62)mm; widthof ovarian lobes93–
208 (152–240). Vitelline follicles numerous, arranged
in 2 separate groups which partly surround internal
organs; follicles extend from lateral margins to mid-
dle third of proglottis, slightly overlapping testicular
fields medially (Figure 3). Vagina tubular, opening
into small genital atrium anterior to cirrus-sac; walls
of vaginal canal thickened near genital pore but no
distinct vaginal sphincter observed; vaginal canal di-
rected medially to reach mid-line of proglottis, then
turns posteriorly, crossing uterine sac and ovarian isth-
mus dorsally. Seminal receptacle small, elongate, situ-
3
Figure 1. Scanning electron photomicrographs of Pelichnibothrium speciosum from Alepisaurus ferox, Japan. A, entire worm; note boundary
between strobila (S) and tail (“vesicule cystique” – T) marked by an arrow; B, scolex; C, apical sucker; D, accessory suckers on bothridia; E–G,
filiform microtriches; interbothridial part of scolex (E), upper margin of bothridial sucker (F) and neck (G).
4
Figure 2. Scolex of Pelichnibothrium speciosum from Alepisaurus
ferox, Japan. Scale-bar in millimetres.
ated posterodorsal to ovarian isthmus. Mehlis’ gland
spherical. Uterus forms elongate, thick-walled sac,
curved porally, 256–408 (74–182) long by 128–660
(122–154) wide; uterine sac empty in all proglottides.
Osmoregulatory canals paired, with ventral pairs
wider than dorsal; canals cross individual proglot-
tides and continuing into bladder. Terminal proglottis
separated from bladder by more or less pronounced
constriction (Figure 1A).
Bladder vesicular, of variable size, very long in
largest specimens, 7–93 mm long (16 mm in syntype
and 138 mm in one specimen from New York) by
2.17–3.25(3.25)mmwide, with maximumwidthup to
6.50 mm in largest specimen (185 mm long); bladder
wider than strobila, slightly tapering towards posterior
end, containinglong,well-developedbundles of longi-
tudinal muscles and 2 pairs of osmoregulatory canals
situated near lateral margins and converging to open
via pore at tip.
Discussion
Monticelli (1889) described Pelichnibothrium specio-
sum from the intestine of the teleost fish Aleposaurus
(as Alepidosaurus) ferox from Madeira as a new
species. The original description was, however, very
superficial, as Monticelli (1889, p. 324) described
only the scolex morphology. Because of the absence
of any information about the strobilar morphology,
Braun (1894–1900) and Southwell (1925) doubted
the validity of the genus Pelichnibothrium Monticelli,
1889.
Several additional records of P. speciosum exist.
Yamaguti (1934) found a number of cestodes, some of
them possessinggravidproglottides, in the spiral valve
of the shark Prionace glauca (L.) collected from the
PacificOcean that he consideredto be conspecific with
P. speciosum. He provided a detailed description and
illustrations of mature proglottides, cross-sections and
a complete worm consisting of two parts: the anterior
part with the scolex and proglottides, and the posterior
part (bladder) lacking any internal organs (see figures
113–116 of Yamaguti, 1934). In 1952, Yamaguti re-
ported finding numerous mature, but not gravid P.
speciosum specimens from the shark P. glauca. Euzet
(1959) found one specimen of P. speciosum in the spi-
ral valve of thesame host, P. glauca fromSète, France;
this specimen was also immature. In addition, material
fromA. ferox examinedbythe presentauthors(BMNH
Nos 1975.6.25.1–20 and 1975.6.25.21–30) indicates
that P. speciosum is also present off the USA (Florida,
New York) and Iceland.
On the basis of some particular features of P. s pe -
ciosum (position of the bothridia, the presence of an
apical sucker and the tailed larva corresponding to a
plerocercoid),Yamaguti(1934) establisheda new sub-
family, the Pelichnibothriinae, to accommodate this
species. This subfamily, however, was not accepted by
subsequent workers, including Yamaguti (1959), and
P. speciosum was placed within the Phyllobothriinae
(see Wardle & McLeod, 1952; Schmidt, 1986). Euzet
(1994) assumed it to represent a phyllobothriid larva
(plerocercoid) of an unknown adult and included P.
speciosum in a section discussing genera that should
no longer be recognised.
Mete & Euzet (1996) found cestodes, morpho-
logically indistinguishable from those described by
Yamaguti (1934), in the same host, Prionace glauca,
from the Indian Ocean between Réunion and Mada-
gascar. These authors doubted the conspecificity of
Monticelli’s larval tapeworms, which were collected
5
Figure 3. Mature proglottis of Pelichnibothrium speciosum from Alepisaurus ferox, Japan. Testes only partly illustrated – actual number of
testes in a proglottis >400. Vitelline follicles are omitted on right side, except at median and lateral limits. Scale-bar in millimetres.
from a teleost, with adult tapeworms collected from
a shark. Thus, on the basis of the presence of gravid
proglottides, Mete & Euzet (1996) rejected the propo-
sition of Euzet (1994) that this taxon represents the
postlarva of an unknown adult cestode and erected a
new genus and species, Prionacestus bipartitus,for
this taxon. Mete & Euzet (1996) considered Yam-
aguti’s identification of tapeworms from P. glauca as
P. speciosum to be doubtful because it had been based
only on scolex morphology. These authors (Mete &
Euzet, 1996, p. 365–366)stated that “Il n’existe aucun
preuve que le grand plérocercoide trouvé dans l’in-
testin d’Alepidosaurus ferox soit le stade larvaire du
Cestode parasite de Prionace glauca.”
The present study, which includedthe examination
of Monticelli’s specimens (syntypes), showed that the
tapewormsfound inthe shark P.glauca areconspecific
with those from the teleost A. ferox (compare Mon-
ticelli, 1889, figures 13–14; Yamaguti, 1934, figures
113–116; Euzet, 1959, figure 238; Mete & Euzet,
1996, figures 1–3; the present paper). The only dif-
ference between the cestodes found by Mete & Euzet
(1996) and those found in Japan is that the former
contain gravid proglottides.
It seems evident that Yamaguti (1934) correctly
used the older name proposed by Monticelli (1889)
for a larval stage, in this case P. speciosum, for adults
considered to be conspecific with the larvae, which
is in accordance with the International Code of Zo-
ological Nomenclature (Article 17.2). Consequently,
Prionacestus bipartitus is synonymised with Pelichni-
bothrium speciosum herein and the genus Prionaces-
tus is suppressed.
Adults of Pelichnibothrium speciosum seem to be
specific parasites of Prionace glauca. The geographi-
cal distribution of P. speciosum is fairly extensive and
probably cosmopolitan, as records include the North
Atlantic Ocean (Madeira, Iceland, Canada, USA), in-
clusive of the Mediterranean Sea (France), the Indian
Ocean (Réunion) and the Pacific Ocean (Japan) (Mon-
ticelli, 1889; Yamaguti 1934; Euzet, 1959; Mete &
Euzet, 1996; present study).
The life-cycle of P. speciosum is poorly under-
stood and many questions remain to be addressed.
The occurrence of quite large specimens with fairly
well-developed genital organs but possessing appar-
ently larval features (bladder of a plerocercous larva,
functional apical sucker) in the intestinal lumen of the
teleost host seems to be the most peculiar feature of
this species.
The life-cycles of the Tetraphyllidea are supposed
to include two intermediate hosts: the first is a cope-
pod in which the procercoid develops; the second are
teleost fishes, crustaceans (decapods) or cephalopods;
and elasmobranchs serve as definitive hosts (Mudry &
Dailey; Williams & Jones, 1994). Teleosts, decapods
andcephalopodsprobablyalso serveas paratenichosts
(Euzet, 1959). In the second intermediate host, a ple-
rocercoid known as Scolex pleuronectis Müller, 1780
develops; it is typified in phyllobothriid genera by
its possession of a tail and an apical sucker which
serves in the attachment of the larva to the intestinal
wall of the host. It has been shown experimentally
(Euzet, 1959) that both the tail and apical sucker dis-
appear during their development in elasmobranchs. In
the intestine of A. ferox, tetraphyllidean larvae were
found alongside described maturing specimens of P.
6
Figure 4. Tetraphyllidean larvae, presumably conspecific with Pelichnibothrium speciosum, from the intestine of Alepisaurus ferox.Note
presence of well-developed apical sucker (A–D) and accessory sucker on bothridia (E; lateral view). Scale-bars in millimetres.
7
speciosum. These larvae (total length 3.2–3.5 mm;
maximum width 500–550; Figure 4) have a scolex
possessing four sessile, oval bothridia with accessory
suckers situated anteriorly and a well-developed api-
cal sucker measuring 70–80 in diameter. The larvae
closely resemble in their morphologythe P. speciosum
specimens from the same fish, as describedabove, and
they may represent a transitional stage between ple-
rocercoids corresponding to S. pleuronectis and more
developed cestodes containing almost fully-formed
genital organs. However, this assumption needs to be
confirmed experimentally.
TheroleofA. ferox in the developmental cycle
of P. speciosum is yet to be resolved. It seems that
this teleost fish is a normal host of the parasite be-
cause there are many records of P. speciosum in A.
ferox and intensities of infection are often very high.
A. ferox may represent either the second intermediate
or paratenichost of the parasite. Since it is carnivorous
on fishes, cephalopods, tunicates and crustaceans, and
some specimensreach up to 2 metres in length (White-
head et al., 1984), it could easily become infected
with P. speciosum larval stages (procercoids or ple-
rocercoids) after consuming intermediate or paratenic
hosts. It remains to be proven whether this fish is actu-
ally involved in the transmission of the parasite to the
definitive host, P. glauca, which can prey upon small
A. ferox specimens. The consumption of A. ferox by
P. glauca is potentially possible because the former
is a pelagic fish, living from near the surface to be-
low 1,000 metres and sometimes approaching inshore
waters (Whitehead et al., 1984). Both hosts can also
exist sympatrically: A. ferox is probably cosmopolitan
and P. glauca also occurs in tropical to cool-temperate
waters everywhere (Whitehead et al., 1984). It cannot
beexcludedthat largeA. ferox specimensinfectedwith
P. speciosum represent a blind alley in the life-cycle of
this parasite. However,it is probable that even large A.
ferox specimens can represent a source of infection for
sharks which could bite the middle out of one without
ingesting the whole fish.
Yamaguti (1952) reported immature, but large
(lengthupto25cm)P. speciosum specimens from
the small intestine of two other species of teleostean
fishes, Lampris regia (Bonnaterre) and Thynnus thyn-
nus (L.) from Japan, but he did not providedescription
of these cestodes. Hence, the possibility that teleosts
other than A. ferox play a role in the life-cycle of P.
speciosum cannot be ruled out.
Tetraphyllidean larvae from the intestine of
salmonids (Oncorhynchus) from the River Amur in
the Russian Far-east, identified as P. speciosum (see
Dubinina, 1971), are likely to represent another phyl-
lobothriid species, because they differ distinctly from
P. speciosum with regard to the presence of the zone
of proglottis differentiationsituated far posterior to the
scolex (see figure 36 in Dubinina, 1971).
Acknowledgements
The authors are indebted to Dr Kazuya Nagasawa, In-
stitute of Fisheries, Shimizu, Japan, for support during
a stay of F.M. in Japan, and to Dr David I. Gibson
and Mrs. Eileen Harris, The Natural History Museum,
London, for loan of type and voucher specimens of
Pelichnibothrium speciosum. Thanks are also due to:
Prof. Janine Caira, University of Connecticut, Storrs,
USA for valuable comments; Dr Ronald A. Campbell,
University of Massachusetts Darmouth, North Dar-
mouth, USA, for helpful suggestions and the loan of
voucher specimens of P. speciosum; and to Mrs Mar-
tina Borovková and Miss Petra Eliášová, both Insti-
tute of Parasitology,
ˇ
Ceské Bud
ˇ
ejovice, for excellent
technical assistance and extreme patience in making
permanent preparations of P. speciosum and for the
preparation of SEM samples, respectively. Prof. An-
dré Raibaut, the Director of the Ecological Station of
the University of Montpellier II, France, is acknowl-
edged for enabling the short stay of one of the authors
(T.S.) at Sète, France; this stay and a part of this study
were financially supported by the Grant Agency of the
Czech Republic (project No. 508/95/0294).
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