JOURNAL OF CRUSTACEAN BIOLOGY, 21(1): 304–312, 2001
OVICIDES JULIEAE N. GEN., N. SP. (NEMERTEA: CARCINONEMERTIDAE)
ON XANTHID CRABS FROM THE GREAT BARRIER REEF, AUSTRALIA
Jeffrey D. Shields
Department of Environmental Sciences, Virginia Institute of Marine Science,
The College of William and Mary, Gloucester Point, Virginia 23062, U.S.A. (e-mail: [email protected])
A B S T R A C T
A new genus and species of symbiotic, semi-parasitic nemertean worm, Ovicides julieae n. gen.,
n. sp., is described from the xanthid crabs Chlorodiella nigra and C. xishaensis. The new genus
possesses accessory stylet pouches and exhibits simultaneous hermaphroditism, features new to the
family Carcinonemertidae. The new species has a relatively small anterior proboscis chamber and
small basis, yet it possesses the largest stylet to basis ratio (up to 0.650) reported for the family. It
also has a flame cell pattern of at least 2[(3+3)], which is different from those reported for two
other species. The worm occurred in a lightly granulated sheath on the abdominal sterna, pleopods,
and clutches of its host, but few adult worms were found. The species exhibited a high host specificity and was more frequently found on C. nigra than on C. xishaensis (7.5 vs. 0.4%, overall
prevalence, respectively). Worms were only found on female crabs, and worm intensity showed a
modest but significantly positive correlation with host size. Ovicides julieae represents the second
genus in the Carcinonemertidae, the fifth described carcinonemertid species from Australia, and
the eleventh described species in the family.
The Carcinonemertidae is a highly modified family of nemertean worms that specializes in eating the eggs of crustacean hosts.
The type genus and species, Carcinonemertes
carcinophila (Kölliker, 1845), was first described from the body of a crab from the
Mediterranean. It has since been reported
from a number of portunid hosts from Europe
and eastern North America (Humes, 1942; Vivarés, 1971; Comely and Ansell, 1989). Carcinonemertids are relatively widespread, having been reported from at least 58 species of
crabs in 13 families (but primarily portunids,
majids, and xanthids) and 2 species of panulirid lobsters (Humes, 1942; Wickham and
Kuris, 1985; Campbell et al., 1989). The
members of the family that live on portunids
and grapsids are host generalists, hence the
large host range; others are host specialists.
While Arthur Humes is recognized as one of
the foremost copepodologists, he made several important contributions to the biology of
the Carcinonemertidae. In 1942, Humes gave
the first ecological and taxonomic assessment
of the family. He made significant contributions to the biology of C. carcinophila (Kölliker, 1845), the type species, and C. epialti
Coe, 1902, and described C. coei Humes,
1942. His monograph laid the foundation for
ecological and taxonomic work in the fam-
ily. Earlier, Humes (1941) studied the reproductive organs of C. carcinophila, where he
recognized the importance of Takakura’s
(1910) description of the enlarged seminal
vesicle and provided a valuable translation
into English.
While the carcinonemertids are common
on a wide range of host species, most species
are rare or underreported. Species of Carcinonemertidae are difficult to identify because
they are often at low prevalences in host
populations (Wickham, 1986), typically inhabit ovigerous hosts and thus share seasonal
cycles in abundance (Shields, 1993), and certain characters (stylet length, flame cells,
blood vessels, etc.) are best observed on live
specimens. The Carcinonemertidae are probably under-represented; there are, no doubt,
many more to be found and described.
To date, only 10 species of Carcinonemertidae have been described: C. carcinophila
(Kölliker, 1845), from an unidentified crab,
later found on Callinectes sapidus Rathbun,
1896, and other Atlantic portunids (Humes,
1942; Comely and Ansell, 1989) [two subspecies are recognized, C. c. carcinophila
(Kölliker, 1845) and C. c. imminuta Humes,
1942]; C. epialti Coe, 1902, from Pugettia
productus (Randall, 1840), but more common
on Eastern Pacific grapsids (Kuris, 1978; Roe,
304
SHIELDS: A NEW CARCINONEMERTID FROM XANTHID CRABS
1979); C. mitsukurii Takakura, 1910, from
Eriocheir japonicus de Haan, 1935, and many
different portunids including Portunus pelagicus (Linnaeus, 1758) (see Humes, 1942;
Shields and Wood, 1993); C. coei Humes,
1942, from Charybdis natator (Herbst, 1794);
C. errans Wickham, 1978, from Cancer magister Dana, 1852; C. regicides Shields, Wickham, and Kuris, 1989, from the Alaskan red
king crab, Paralithodes camtschaticus (Tilesius, 1815) and the Tanner crab, Chionoecetes
bairdi Rathbun, 1924; C. australiensis Campbell, Gibson, and Evans, 1989, from Panulirus cygnus George, 1962; C. humesi Gibson and Jones, 1990, from Naxia aurita (Latreille, 1825); C. wickhami Shields and Kuris,
1990, from the spiny lobster Panulirus interruptus (Randall, 1840); and C. pinnotheridophila McDermott and Gibson, 1993,
from the pea crab Pinnixa chaetopterana
Stimpson, 1860. Three of these species are reported from Australia, with an undescribed
form from Tasmania (Bell and Hickman,
1985). Two other egg predators, Pseudocarcinonemertes homari Fleming and Gibson,
1981, and Alaxinus oclairi Gibson, Wickham,
and Kuris, 1990, have uncertain systematic
affinities and are probably not members of the
Carcinonemertidae.
A new genus and new species of Carcinonemertidae is described. The worm is
placed in a new genus because it possesses
accessory stylet pouches, and because of the
simultaneous presence of mature ovaries and
testes (simultaneous hermaphroditism) in individuals. It is a new species based on the
small body size, the small size of the apical
proboscis chamber and basis, and the large
stylet to basis ratio. The worm is clearly a
monostiliferous hoplonemertean with otherwise typical carcinonemertid characters.
MATERIALS AND METHODS
The crab hosts, Chlorodiella nigra (Forskål, 1775) and
C. xishaensis Chen and Lan, 1978, were collected from
various locations near Heron Island and Wistari Reef
(Capricorn Section of the Great Barrier Reef), and near
Lizard Island (Central Section of the Great Barrier Reef).
Collections were made under the auspices of the Great
Barrier Reef Marine Park Authority: GBRMPA permits
G89/428, G90/383, G91/500, G92/499. Coral rubble and
small patches of dead coral (Acropora spp. and Pocillopora spp.) were collected by hand using snorkel and
SCUBA on reef flats, rubble fields, subtidal reef crests
and slopes. Crabs were carefully removed from coral rubble which had been gently broken apart with a hammer.
Several crabs were held in flowing-sea-water aquaria for
further observations.
305
Basic parameters of the crab populations, including
size as carapace width (CW), sex, and reproductive condition of females (e.g., ovigerous vs. non-ovigerous) were
recorded. Crabs were then examined with a stereomicroscope for nemerteans. The carapace of each crab was removed and the branchial chamber was examined for
worms. In some cases, gills and eggs were examined with
a compound microscope.
Worms were fixed in 5% Formalin-sea water, dehydrated in alcohol, embedded in paraffin, and sectioned at
5 or 6 µm. Measurements were made on living and sectioned worms with an ocular micrometer in a compound
microscope. All measurements are in micrometers unless
otherwise stated, with mean (range) shown.
RESULTS
Ovicides julieae, n. gen. et n. sp.
Figs. 1–3
Adult (Holotype: single specimen observed
alive, fixed and serially sectioned).—Body
slender, light pink to orange in color, delicate;
found in tough, thick, parchment-like sheath.
Sheath finely granular, slightly longer than
worm. Worm measured alive ranged
2,275–2,450 µm long by 175–210 µm wide.
Motility primarily mucociliary movement.
Two conspicuous ocelli 7 or 8 µm long, located 51–68 µm from tip of head. Distance
between ocelli 24–34 µm. Proboscis apparatus dorsomedial to foregut. Anterior proboscis
chamber 15 µm long. Stylet bulb 34–41 µm
long by 35 µm wide. Basis small, granular
in appearance, 20 µm long. Single stylet on
basis, 13 µm long. Stylet to basis ratio, 0.650.
Four stylets in accessory stylet pouches subjacent to stylet bulb; stylets 10 µm long. Middle proboscis chamber 21 µm in diameter,
granular in appearance. Posterior proboscis
chamber not measured in living specimen.
Proboscis sheath not observed, greatly reduced. Foregut ellipsoidal 62 µm long by 32
µm wide; laterally displaced; at level of posterior proboscis chamber. Anterior blood vessel in a simple loop over esophagus. Worm
hermaphroditic, with ovaries found in medial
field and testes found in posterolateral field.
Ovaries 38–43 µm in diameter, with 3 or 4
ova developing within. Ovaries arranged in
alternating lateral bands. Ovarian pore indistinct but present in histological sections. Eggs
observed but not measured. Testes observed
histologically, 27 (25–32) µm in diameter.
Takakura’s duct may be present but not observed.
Large Juveniles or Regressed Adults (Observations from 13 live specimens from Heron
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
Fig. 1. Ovicides julieae. Composite drawn from live observations on holotype and juveniles.
Island).—Similar in gross morphology to
holotype. Regressed adults difficult to distinguish. Worms 1,745 (790–3,528) µm long by
239 (100–504) µm wide; delicate; found in
tough, thick, parchment-like casement. Ocelli
located 54 (38–75) µm from tip of head. Distance between ocelli 49 (38–72) µm. Proboscis apparatus dorsal or slightly lateral with
foregut. Anterior proboscis chamber 14
(10–18) µm long. Stylet bulb 40 (30–55) µm
long by 32 (28–39) µm wide. Basis small,
20 (15–25) µm long by 8 µm wide. Single
stylet on basis, 10 (6–13) µm long. Stylet to
basis ratio, 0.400–0.667. Zero to 4 stylets in
2 accessory stylet pouches subjacent to stylet
bulb. Middle proboscis chamber 24 (13–39)
µm in diameter, granular in appearance. Posterior proboscis chamber 30 (25–33) µm long
by 17 (13–20) µm wide. Proboscis sheath
greatly reduced. Anterior portion of lateral
blood vessels fuse in simple loop dorsal to
esophagus. Flame cells located laterally at
level of dorsal ganglia and proboscis chambers; tentative flame cell pattern 2[(3+3)].
Taxonomic Summary
Type Host and Site of Infestation.—On the
sterna, pleopods, or in the egg masses of the
xanthid crab Chlorodiella nigra (Forskål,
1775), rarely on C. xishaensis Chen and Lan,
1978 (2 infested hosts, 16 February 1992).
Worms were never found on the gills or
branchial chambers of the host crabs.
Type Locality.—Australia; Great Barrier
Reef; Lizard Island (approx. 14°40′S,
145°27′E); in patches of dead coral (Acropora and Pocillopora spp.) and coral rubble;
at depths of 1–5 m.
Date of Collection.—Holotype: 24 April
1991. Juveniles also found at Heron Island
(approx. 23°27′S, 151°57′E) and nearby Wistari Reef; in patches of dead corals and coral
rubble; at depths of 1–5 m. Juveniles first collected 15 November 1989, repeatedly found
on sampling trips through 1992.
Holotype.—Hermaphroditic adult (QM#
G218108) deposited in the Invertebrate Zo-
SHIELDS: A NEW CARCINONEMERTID FROM XANTHID CRABS
307
Fig. 2. Ovicides julieae, from live specimens. (A) Anterior of holotype showing basis (B) and stylet (S), bar = 20
µm; (B) Anterior of juvenile worm with accessory stylet pouch showing several accessory stylets (arrows), bar = 30
µm; inset from same juvenile from squash preparation, bar = 10 µm; (C) Parchment-like sheath of juvenile worm
(Sh), bar = 100 µm; (D) Detail of parchment-like sheath, bar = 5 µm.
ology Collection, Queensland Museum, P.O.
Box 300, South Brisbane, 4101, Australia.
Additional material: Juveniles in situ on host
(QM# GL12718).
Etymology.—The generic name, ovi- (egg,
Latin) and -cides (killer, Latin) refers to the
predatory habit of members of the family. The
gender of the genus is masculine. The species
is named after my wife, Julie, for her help in
collecting the host crabs.
Diagnosis
Ovicides n. gen.—Hoplonemertea, Monostilifera, Carcinonemertidae. Adults with 2 accessory stylet pouches containing zero to
many accessory stylets, anterior proboscis
chamber small. Proboscis reduced in size.
Takakura’s duct may be present but not observed. Simultaneously hermaphroditic as
adults. Otherwise, with general features of the
Carcinonemertidae. In parchment-like sheaths
as juveniles and adults on pleopods, sterna,
and eggs of decapod crustaceans.
Ovicides julieae n. sp.—Adults small, up to
2.5 mm long, slender. Two accessory stylet
pouches present, containing zero to 4 accessory stylets each. Large stylet to basis ratio,
0.500–0.650. Found in finely granular, tough,
parchment-like sheath. Simultaneously hermaphroditic, but not observed in primary
breeding season. Ovarian pore indistinct but
present in histological sections. Ovaries present in alternating bands. Testes present in posterolateral field. Takakura’s duct may be present but not observed. Anterior portion of lateral blood vessels fuse in simple loop dorsal
to esophagus. Flame cells located lateral to
dorsal ganglion and lateral nerve, located in
a “field” between dorsal ganglion and proboscis chambers in a 2[(3+3)] arrangement.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
Fig. 3. Ovicides julieae. Serial sections of holotype: (A) medial section showing ovary (o), intestine (I), bar = 40
µm; (B) medial section showing ovarian pore (arrows), ovary (o), intestine (I), bar = 20 µm; (C) posterolateral section showing testis (T), intestine (I), and nearby gregarine infection (G), bar = 30 µm; (D) posterolateral section
showing testis (T), intestine (I), and portion of lateral nerve trunk (N), bar = 25 µm.
Found on Chlorodiella nigra and rarely on C.
xishaensis.
Remarks.—Ovicides julieae is one of the
smallest carcinonemertids yet described. It
can be distinguished from members of the
genus Carcinonemertes by the presence of the
accessory stylet pouches in adults, by its
small anterior proboscis chamber, and relatively small basis. It possesses distinct carcinonemertid characters: reduced proboscis,
short, poorly developed rhynchocoel, submuscular glands, and an absence of cerebral
organs and mid-dorsal vessel (Shields et al.,
1989; Gibson and Jones, 1990). However,
Takakura’s duct, an important character in the
family, was not observed in the holotype. Accessory stylet pouches have been observed
in other carcinonemertids, but none of these
forms have been described (see Wickham and
Kuris, 1988). Pseudocarcinonemertes homari
bears accessory stylet pouches and accessory
stylets, but it possesses cerebral organs and
a mid-dorsal vessel (Fleming and Gibson,
1981) and has been tentatively placed in the
Tetrastemmatidae by Uhazy et al. (1985).
Alaxinus oclairi possesses rudimentary stylet
pouches, but the presence of cerebral organs,
a mid-dorsal blood vessel, a muscular and
Fig. 4. Host size (carapace width) in relation to intensity
of infestation (worms per infected host). Intensity = 0.443
CW – 3.196; r = 0.355, P < 0.01, n = 77; open circles,
one host; stars, 2 hosts; boxes, more than 2 hosts with
corresponding intensity.
SHIELDS: A NEW CARCINONEMERTID FROM XANTHID CRABS
309
elongate rhynochoel, and the absence of submuscular glands place it outside the Carcinonemertidae (Gibson et al., 1990).
Ovicides julieae has the largest stylet to basis ratio of any described species of Carcinonemertidae (for ratios, see McDermott and
Gibson, 1993). It is the only described carcinonemertid to possess the capacity for simultaneous hermaphroditism. In addition, the
flame cell pattern, 2[(3+3)], is different from
those described for C. regicides 2[(1+1+1+1)]
and C. epialti 2[(2+2)] (Shields et al., 1989),
but few carcinonemertids have been examined while alive for flame cells. Carcinonemertes australiensis has ducts that may represent flame cells (Campbell et al., 1989), and
P. homari has ventrolateral nephridiopores on
the cephalic furrow (Uhazy et al., 1985).
Discussion
Ovicides julieae was only present on mature female crabs. Intensities ranged 1–15
with a mean of 3.1 ± 2.7 worms per infected
host (Fig. 4). Host size was significantly correlated with intensity (P < 0.01) even with the
removal of the potential outlier (r = 0.321, P
< 0.01). The worm was less abundant at
Lizard Island (C. nigra, 1.9% prevalence, n
= 7/374) than at Heron Island (C. nigra,
10.7% prevalence, n = 70/652) (Figs. 5, 6).
Whether this was an artifact of seasonal sampling or a function of range was not clear.
Prevalences at Heron Island ranged from 5
to 41%, those at Lizard Island ranged from 0
to 15%. While seasonality was not examined,
the relatively high prevalences in the late austral summer months (February and March)
were suggestive of a summer peak in abundance.
Ovicides julieae was highly host specific.
It had an overall prevalence of 7.5%
(77/1,026) on Chlorodiella nigra vs. 0.4%
(2/471) on C. xishaensis. Numerous other
brachyuran and anomuran hosts (n > 6,300
individuals from approximately 160 species)
were examined from the same and nearby
habitats; none were found with this species of
nemertean (Shields, unpublished data).
Ovicides julieae was observed on ovigerous crabs, but mature worms were rare. Simultaneous hermaphroditism may be an adaptation to the rarity of adults and relatively
sparse distribution of the small populations.
Roe (1986) reported the common occurrence
of parthenogenesis in Carcinonemertes epi-
Fig. 5. Chlorodiella nigra from Heron Island, Great Barrier Reef, Australia. Size-frequency histogram of female
(above bar) and male (below bar) crabs during the different collection periods (mature adults, black; juveniles,
open; infested females, hatched). P = prevalence of females.
alti and C. errans. She found that both haploid and diploid larvae were produced and
later speculated on the ecological significance
of parthenogenesis (Roe, 1988). Hermaphroditism and parthenogenesis are clear examples of the semiparasitic adaptations present
in the family.
Most O. julieae were located on the sterna
or pleopods of the host. Five to six days after host oviposition, the worms migrated into
the clutch of the crab. Egg mortality from the
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
Humes (1942) reported a low prevalence of
C. c. carcinophila on males of Callinectes
sapidus. Such was not the case with O.
julieae, as no worms were found on males.
Lastly, a single, minute, presumably newly
settled juvenile was found ensheathed adjacent to a larger juvenile worm. The newly settled worm had a complete basis and stylet
with two completely formed accessory
stylets. Both were found on a non-ovigerous
female crab.
ACKNOWLEDGEMENTS
I thank Fiona Wood, Robert Gould, James Davis, Ted
Warren, Jim and Danielle Roberts, Sandra Whittingham,
and Julie and Jason Shields for their help in collecting
hosts and worms. Special thanks to Peter Davie at the
Queensland Museum for his identification of the crab
hosts, and to Profs. Colin Dobson and Bob (R. J. G.)
Lester for their gracious research support. Profs. Ray Gibson and Jon Norenburg provided useful comments. A University of Queensland Postdoctoral Fellowship, a Lizard
Island-United Airlines Travel Fellowship, and grants from
The University of Queensland (Special Projects Grant)
and the Australian Research Council (#A191940) made
this work possible. This is Contribution #2324 from the
Virginia Institute of Marine Science.
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Fig. 6. Chlorodiella nigra from Lizard Island, Great Barrier Reef, Australia. Size-frequency histogram of female
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open; infested females, hatched). P = prevalence of females.
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RECEIVED: 5 April 2000.
ACCEPTED: 10 June 2000.
ANNOUNCEMENT
The following application was published on 30 June 2000 in Vol. 57, Part 2 of the Bulletin of Zoological Nomenclature. Comment or advice on this application is invited for publication in the Bulletin and should be sent to the Executive Secretary (I.C.Z.N.), c/o The
Natural History Museum, Cromwell Road, London SW7 5BD, U.K. (e-mail:
[email protected]).
Case 3135. Scyllarus orientalis Lund, 1793 (currently Thenus orientalis; Crustacea, Decapoda): proposed designation of a neotype.
The following opinion was published on 30 June 2000 in Vol. 57, Part 22 of the Bulletin
of Zoological Nomenclature. Copies of this opinion can be obtained free of charge from the
Executive Secretary (I.C.Z.N.).
Opinion 1951. Spherillo Dana, 1852 (Crustacea, Isopoda): Spherillo vitiensis Dana, 1853,
designated as the type species.