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Bucephalidae (Platyhelminthes: Digenea) of Plectropomus (Serranidae: Epinephelinae) in the tropical Pacific

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  • Western Australia Department of Primary Industries and Regional Development

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We examined four species of Plectropomus Oken, 1817 (Serranidae: Epinephelinae), Plectropomus areolatus (Rüppell), Plectropomus laevis (Lacepède), Plectropomus leopardus (Lacepède) and Plectropomus maculatus (Bloch) from sites off Heron Island and Lizard Island on the Great Barrier Reef, Australia (GBR), and the Gambier Islands, French Polynesia. Three new species of Neidhartia Nagaty, 1937, five new species of Prosorhynchus Odhner, 1905, and one previously described species, Prosorhynchus freitasi Nagaty, 1937, are characterised. The three species of Neidhartia, Neidhartia haywardi n. sp., Neidhartia plectropomi n. sp. and Neidhartia tyleri n. sp. are readily distinguishable morphologically. Two of the six species of Prosorhynchus (Prosorhynchus lesteri n. sp. and Prosorhynchus wrightae n. sp.) are easily distinguished from their other congeners by morphology but the other four species (P. freitasi, Prosorhynchus heronensis n. sp., Prosorhynchus munozae n. sp. and Prosorhynchus plectropomi n. sp.) are generally similar in morphology and were only distinguished initially by comparing their ITS2 rRNA sequences. Three additional taxa, one from the GBR and two from French Polynesia, were recognised as distinct on the basis that their ITS2 rRNA sequences differed from those of the new taxa described here; these species remain unnamed for the present. Inter-specific divergence observed within these genera in the ITS2 rRNA ranged from 10 to 42 base pairs (4-16 %) for species of Neidhartia and 2-57 base pairs (3-21 %) for species of Prosorhynchus. Inter-generic divergences were 42-55 base pairs (17-21 %). No intraspecific variation in the ITS2 rRNA region was observed for any of the six species for which multiple sequence replicates were obtained. Phylogenetic analysis of 12 operational taxa from Plectropomus together with sequences of three other species from epinepheline serranids demonstrated that Neidhartia and Prosorhynchus were reciprocally monophyletic with the exception that P. wrightae n. sp. fell either within or basal to the Neidhartia species. The richness of bucephalids in species of Plectropomus appears to be exceptional within the Serranidae relative to that observed in other serranid genera in the tropical Indo-West Pacific.
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Parasitology Research
Founded as Zeitschrift für
Parasitenkunde
ISSN 0932-0113
Volume 112
Number 7
Parasitol Res (2013) 112:2561-2584
DOI 10.1007/s00436-013-3423-2
Bucephalidae (Platyhelminthes: Digenea) of
Plectropomus (Serranidae: Epinephelinae)
in the tropical Pacific
Nathan J.Bott, Terrence L.Miller &
Thomas H.Cribb
1 23
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ORIGINAL PAPER
Bucephalidae (Platyhelminthes: Digenea) of Plectropomus
(Serranidae: Epinephelinae) in the tropical Pacific
Nathan J. Bott &Terrence L. Miller &Thomas H. Cribb
Received: 25 November 2012 /Accepted: 4 April 2013 / Published online: 1 June 2013
#Springer-Verlag Berlin Heidelberg 2013
Abstract We examined four species of Plectropomus
Oken, 1817 (Serranidae: Epinephelinae), Plectropomus
areolatus (Rüppell), Plectropomus laevis (Lacepède),
Plectropomus leopardus (Lacepède) and Plectropomus
maculatus (Bloch) from sites off Heron Island and Lizard
Island on the Great Barrier Reef, Australia (GBR), and the
Gambier Islands, French Polynesia. Three new species of
Neidhartia Nagaty, 1937, five new species of Prosorhynchus
Odhner, 1905, and one previously described species,
Prosorhynchus freitasi Nagaty, 1937, are characterised.
The three species of Neidhartia,Neidhartia haywardi n.
sp., Neidhartia plectropomi n. sp. and Neidhartia tyleri n.
sp. are readily distinguishable morphologically. Two of the
six species of Prosorhynchus (Prosorhynchus lesteri n. sp.
and Prosorhynchus wrightae n. sp.) are easily distinguished
from their other congeners by morphology but the other
four species (P. freitasi,Prosorhynchus heronensis n. sp.,
Prosorhynchus munozae n. sp. and Prosorhynchus plectropomi
n. sp.) are generally similar in morphology and were only
distinguished initially by comparing their ITS2 rRNA se-
quences. Three additional taxa, one from the GBR and two
from French Polynesia, were recognised as distinct on the basis
that their ITS2 rRNA sequences differed from those of the new
taxa described here; these species remain unnamed for the
present. Inter-specific divergence observed within these genera
intheITS2rRNArangedfrom10to42basepairs(416 %) for
species of Neidhartia and 257 base pairs (321 %) for species
of Prosorhynchus. Inter-generic divergences were 4255 base
pairs (1721 %). No intraspecific variation in the ITS2 rRNA
region was observed for any of the six species for which
multiple sequence replicates were obtained. Phylogenetic anal-
ysis of 12 operational taxa from Plectropomus together with
sequences of three other species from epinepheline serranids
demonstrated that Neidhartia and Prosorhynchus were recip-
rocally monophyletic with the exception that P. w ri g h t a e n. sp.
fell either within or basal to the Neidhartia species. The richness
of bucephalids in species of Plectropomus appears to be excep-
tional within the Serranidae relative to that observed in other
serranid genera in the tropical Indo-West Pacific.
Introduction
The Serranidae is a relatively large family of predominately
marine (although some species do enter freshwater) fish in
tropical and temperate waters worldwide. The family current-
ly comprises over 475 species in three subfamilies, the
Serraninae, Anthiinae and Epinephelinae (Nelson 2006).
Heemstra and Randall (1993) recognised 159 species in the
Epinephelinae which occurs in both the Atlantic and Indo-
Pacific. Within the Epinephelinae, Plectropomus Oken, 1817,
comprises seven species, all restricted to the Indo-Pacific and
mainly found associated with coral reefs (Heemstra and
Randall 1993; Randall et al. 1997). Species of Plectropomus
are highly prized food and angling fish and are becoming
significant components of aquaculture industries in some re-
gions (Welch et al. 2008). Species of this genus are ambush
predators, whose diets are dominated by fish but also include
cephalopods and crustaceans (Heemstra and Randall 1993).
Five of the seven Plectropomus spp. are found on the Great
Barrier Reef, Australia (GBR); Plectropomus punctatus is
only known from the western Indian Ocean and
N. J. Bott :T. H. Cribb
School of Biological Sciences, The University of Queensland,
Brisbane, QLD 4072, Australia
T. L. Miller
School of Marine and Tropical Biology, James Cook University,
PO Box 6811, Cairns, QLD 4870, Australia
Present Address:
N. J. Bott (*)
Aquatic Sciences, South Australian Research and Development
Institute, PO Box 120, Henley Beach, SA 5022, Australia
e-mail: nathan.bott@sa.gov.au
Parasitol Res (2013) 112:25612584
DOI 10.1007/s00436-013-3423-2
Author's personal copy
Plectropomus pessuliferus has an erratic distribution not in-
cluding the GBR (Heemstra and Randall 1993).
The primarily piscivorous nature of their diet exposes
species of Plectropomus toinfectionbydigeneantrematodes
of the family Bucephalidae Poche, 1907, which utilise teleosts
as second intermediate hosts (Matthews 1973;Matthews
1974;Stunkard1976). To date, four named bucephalids and
one unidentified species have been reported from two species
of Plectropomus;Pseudoprosorhynchus hainanensis Shen,
1990; Prosorhynchus freitasi Nagaty, 1937; Prosorhynchus
thapari Manter, 1953; Prosorhnychus sp. and Rhipidocotyle
calvivesiculatum Ku and Shen, 1975 (Ku and Shen 1975;
Manter 1953;Nagaty1937; Shen 1990).
Here, we report on a survey of the bucephalid fauna of four
species of Plectropomus,Plectropomus areolatus (Rüppell),
Plectropomus laevis (Lacepède), Plectropomus leopardus
(Lacepède) and Plectropomus maculatus (Bloch) collected
principally from sites off Heron Island (southern GBR),
Lizard Island (northern GBR) and from two individual fish
from the Gambier Islands, French Polynesia. A combined
morphological and molecular approach incorporating data
from the second internal transcribed spacer (ITS2) ribosomal
RNA region are used to explore the complex of bucephalid
species associated with Plectropomus from these localities.
We also report new host and locality records as well as
molecular data for some of the bucephalids reported by Bott
&Cribb(2009) from other serranid genera from off the GBR.
Materials and methods
Specimen collection
Fishes were collected by baited line or spear from the following
localities: Heron Island (23°27S; 151°55E) in the southern
GBR, Queensland, Australia, Lizard Island (14°40S; 154°28
E) in the northern GBR, Queensland, Australia and the
Gambier Islands (23°12S; 134°51W), French Polynesia. Fish
were euthanased upon capture by severing the nerve chord. The
entire digestive tract was removed and separated into stomach,
pyloric caeca, intestine and rectum. Each individual section was
then opened in vertebrate saline, washed and examined under a
stereo microscope using the methods of Cribb and Bray (2010).
Parasites were killed in near boiling vertebrate saline and fixed
in 5 % formalin or 100 % ethanol for molecular analysis.
Morphological analysis
Specimens were rinsed in water before being over-stained in
Mayers haematoxylin, destained in 0.5 % hydrochloric acid
and neutralised in 0.5 % ammonia solution. The worms were
then dehydrated through a graded series of ethanol, cleared in
methyl salicylate and mounted in Canada balsam. Specimens
were examined with an Olympus BH-2 compound micro-
scope, and drawn with the aid of a drawing tube.
Measurements were taken with an eyepiece micrometre. All
measurements are given in micrometres.
Molecular analysis
Genomic DNA was extracted from ethanol preserved worms
using the extraction method described by Kleeman and
Adlard (2000) or using a Qiagen DNeasy Kit (Qiagen Inc.,
Valencia, California) according to the manufacturers
instructions.
The second internal transcribed spacer RNA region (ITS2) for
the new species of Bucephalidae reported here and for additional
prosorhynchine taxa described by Bott and Cribb (2009)was
amplified via polymerase chain reaction (PCR) amplifications
(20 μl) using 1.6 μlofMgCl
2
(25 mM), 2 μl of PCR reaction
buffer (Promega) (10×), 0.8 μl of dNTPs (5 mM), 0.75 μlof
primer [forward primer 3S (5- GGT ACC GGT TCA CGT
GGC TAG TG - 3)orGA1(5- AGA ACA TCG ACA TCT
TGA AC - 3) and reverse primer, ITS2.2 (5- CCT GGT TAG
TTT CTT TTC CTC CGC - 3)] (10 pmol), 0.25 μlTaq
polymerase (PROMEGA, Madison, U.S.A.) (5 units/μl), 1
2μl of DNA template (5100 ng), made up to 20 μlwith
millipore H
2
O and run on a Minicycler (MJ Research, supplied
by Bresatec, Watertown, U.S.A). The following thermocycling
conditions were used: 4-min denaturation hold at 95 °C, 2 min at
45 °C, 90 s at 72 °C, 4 cycles of 45 s at 95 °C, 45 s at 50 °C and
90 s at 72 °C; then 25 cycles of 20 s at 95 °C, 20 s at 52 °C and
90 s at 72 °C and 5-min extension hold at 72 °C.
Amplified DNA was purified using Qiagen®
QIAquickPCR purification kit according to manufac-
turers protocol. Cycle sequencing was conducted using
the same primers utilised for PCR amplification on the
purified DNA products at the Australian Genome Research
Facility in Brisbane, Australia. The resulting sequences
were edited and contigs constructed using Sequencher
TM
(GeneCodes Corp. ver. 3.5) or Geneious Proversion 5.4
software (Biomatters Ltd.). GenBank accession numbers for
the new and undescribed species sequenced here are pro-
vided in the taxonomic summaries below.
Comparative molecular analyses
The partial ITS2 rRNA sequence data generated here and of
the species Bucephalus polymorphus,Dollfustrema hefeiensis
and Dollfustrema vaneyi obtained from GenBank were initial-
ly aligned using MUSCLE version 3.7 (Edgar 2004) with
ClustalW sequence weighting and UPGMA clustering for
iterations 1 and 2. The resultant alignments were refined by
eye using MESQUITE v. 2.75 (Maddison and Maddison
2009). After alignment of the ITS2 rRNA dataset was edited,
the ends of each fragment were trimmed to match the shortest
2562 Parasitol Res (2013) 112:25612584
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sequence in the alignment. Uncorrected ppairwise and total
nucleotide distance matrices were calculated using MEGA v.5
software (Tamura et al. 2011).
Minimum evolution analysis was conducted on the ITS2
only dataset using MEGA v.5 software. Nodal support for the
minimum evolution analysis of the ITS2 dataset was inferred by
bootstrap analysis using a heuristic search of 10,000 replicates.
Results
Combined morphological and molecular analyses indicate
that 12 species of prosorhynchine bucephalids were found in
the four species of Plectropomus examined here. One species
was recognised as previously described and eight of the spe-
cies are formally described as new here. The remaining three
putative species were recognised based on their significant
ITS2 rRNA sequence divergence relative to the other
bucephalids in this system and await further investigation
before they can be formally described. Molecular data are
presented for these undescribed operational taxonomic units
(OTUs) to illustrate the richness of the bucephalid fauna-
infecting species of Plectropomus. Table 1shows the preva-
lences of infection for the 14 species distinguished here. Most
host/locality combinations had too few examinations (<10) to
allow convincing prevalences to be detected. However, for the
host/locality combinations for which there were >10 exami-
nations, prevalences ranged from the minimum possible (1 of
12, 8.3 %) to over 80 %. The two most generally abundant
species in our samples were Neidhartia haywardi n. sp. and P.
freitasi which both had prevalences of over 60 % in P.
leopardus at both Heron and Lizard Islands. Prosorhynchus
heronensis n. sp. was by far the rarest species, being found in
only two of six P. laevis examined at Heron Island. In addition
to the species of Plectropomus,wehaveexamined26other
epinepheline species from six genera in the tropical Pacific
(Table 2) without finding any of the bucephalids reported here
from species of Plectropomus.
Descriptions
Bucephalidae Poche, 1907
Prosorhynchinae Odhner, 1905
Neidhartia Nagaty, 1937
Neidhartia tyleri n. sp.
Type-locality: Heron Island, Queensland Australia
(23°27S; 151°55E)
Other localities: Lizard Island, Queensland Australia
(14°40S; 154°28E)
Type host:P. leopardus (Lacepède) (Heron and Lizard
Islands)
Other hosts:P. laevis (Lacepède) (Heron Island), P.
maculatus (Bloch) (Heron Island)
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia Holotype: QM G 224925, Paratypes: QM G
224926 to 224935
GenBank accession numbers: ITS2 (JX415297)
Etymology: This species is named for Dr Gaines Tyler of
the University of Connecticut, U.S.A.
Description (Fig. 1ac) (measurements in Table 3)
Body elongate, widest at level of posterior testis.
Tegument spiny. Rhynchus large, muscular, able to be
retracted into body; posterior section highly glandular (see
Fig. 1b). Parenchymal gland ducts often prominent at ante-
rior margin of body, may superficially resemble circumoral
spines (see Fig. 1b). Mouth in posterior quarter of the body.
Pharynx muscular, ovoid; caecum short, sac like, extends
anteriorly, obscured by uterus in many specimens.
Testes tandem, ovoid, displaced dextrally. Cirrus sac
(Fig. 1c) extends just anterior to pharynx, displaced sinistrally.
Seminal vesicle ovoid. Pars prostatica straight distally, curves
proximally. Ejaculatory duct narrow, enters genital atrium.
Genital atrium ovoid, contains genital lobe. Genital lobe
hook-shaped. Common genital pore sub-terminal, ventral.
Ovary intertesticular, ovoid. Uterus extending into
anterior third of body, extends anterior to vitelline
follicles. Eggs conspicuously large. Mehlisgland and
Laurers canal not seen in mature specimens.
Vitellarium in two lateral fields, sinistral field unable
to be seen in many specimens because completely
obscured by uterus. Excretory vesicle long, extending
anterior to uterus; excretory pore terminal.
Neidhartia haywardi n. sp.
Type-Locality: Heron Island, Queensland Australia
Other Localities: Lizard Island, Queensland Australia
Type host:P. leopardus (Lacepède) (Heron and Lizard
Islands)
Other hosts:P. laevis (Lacepède) (Heron Island), P.
maculatus (Bloch) (Heron Island)
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia Holotype: QM G 224900, Paratypes: QM G
224901 to 224914
GenBank accession numbers: ITS2 (JX415292)
Etymology: This species is named for Dr Craig Hayward,
honouring his broad contributions to marine parasitology.
Description (Fig. 2a, b) (measurements in Table 3)
Body elongate, widest at mid-body. Tegument spiny.
Rhynchus large, muscular, posterior section highly glandu-
lar. Mouth in posterior half of body. Pharynx muscular,
ovoid; caecum short, sac like, extends anteriorly, obscured
by uterus in ventral field.
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Testes 2, tandem, sinistral, ovoid, displaced dextrally;
anterior testis usually obscured by uterus. Cirrus sac
(Fig. 2b), displaced sinistrally, extends to level of posterior
margin of pharynx. Seminal vesicle ovoid. Pars prostatica
straight distally, proximal portion curving at level of seminal
vesicle. Ejaculatory duct narrow, enters genital atrium.
Genital atrium ovoid, enclosing genital lobe; genital lobe
with a number of small projections. Common genital pore
on ventral surface just posterior to genital lobe. Ovary
intertesticular, ovoid, dextral. Uterus extending well into
anterior third of body. Eggs tanned, small. Mehlisgland
and Laurers canal not seen in mature specimens. Vitelline
follicles apparently in lateral fields, obscured by uterus in
mature specimens, not extending anterior to uterus.
Excretory vesicle extending to posterior margin of
rhynchus; excretory pore terminal.
Neidhartia plectropomi n. sp.
Type-locality: Heron Island, Queensland Australia
Other localities: Lizard Island, Queensland Australia
Type host:P. leopardus (Lacepède) (Heron and Lizard
Islands)
Other hosts:P. laevis (Lacepède) (Heron Island)
Prevalence: see Table 1
Table 1 Prevalences of infec-
tion for bucephalids from this
study taken from Plectropomus
spp. from the Great Barrier Reef,
Australia and the Gambiers Ar-
chipelago, French Polynesia
HI Heron Island, LI Lizard Is-
land, Sw Swain Reefs, Ga
Gambiers Archipelago
Genus Species Host Local nInfected Percentage, %
Neidhartia haywardi P. laevis HI 6 1 17
P. leopardus HI 42 26 62
LI 12 10 83
plectropomi P. maculatus HI 3 1 33
P. laevis HI 6 2 33
P. leopardus HI 42 11 26
LI 12 6 50
tyleri P. leopardus HI 42 13 31
LI 12 1 8
sp. ex Gambiers P. maculatus HI 3 1 33
P. laevis Ga 2 2 100
Prosorhynchus freitasi P. laevis HI 6 2 33
Sw 1 1 100
P. laevis Ga 2 2 100
P. leopardus HI 42 28 67
LI 12 10 83
sp. P. maculatus HI 3 2 67
heronensis P. areolatus LI 1 1 100
lesteri P. laevis HI 6 2 33
P. laevis HI 6 2 33
Sw 1 1 100
P. leopardus HI 42 5 11
LI 12 1 8
sp. lesteri-likeP. laevis Ga 2 1 50
munozae P. laevis HI 6 1 17
P. leopardus HI 42 7 17
P. maculatus HI 3 1 33
plectropomi P. laevis HI 6 1 17
P. leopardus HI 42 5 12
P. maculatus HI 3 1 33
wrightae P. areolatus LI 1 1 100
P. laevis Ga 2 1 50
P. laevis HI 6 1 17
Sw 1 1 100
P. leopardus HI 42 9 21
LI 12 3 25
P. maculatus HI 3 1 33
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Specimen lodgement: Queensland Museum, Brisbane,
Australia Holotype: QM G 224915, Paratypes: QM G
224916 to 224924
GenBank accession numbers: ITS2 (JX415287)
Etymology: This species is named for the host genus from
which it was found, Plectropomus.
Description (See Fig. 3a, b) (measurements in Table 3)
Body elongate, widest at mid-body. Tegument spiny.
Rhynchus large, muscular and highly glandular. Mouth in
posterior third of body, pharynx muscular, ovoid. Caecum
short, sac like, extending anteriorly no further than mid-
body.
Testes 2, tandem, displaced dextrally, small ovoid. Cirrus
sac (Fig. 3b) displaced sinistrally extends anteriorly to pos-
terior level of pharynx, glandular in posterior portion.
Seminal vesicle ovoid. Pars prostatica glandular; glands
not uniform in size or shape; distally straight, proximally
curving in a dextral direction around seminal vesicle.
Genital atrium ovoid, enclosing genital lobe; genital lobe
crescent shaped. Common genital pore, ventral, sub-
terminal.
Ovary intertesticular, ovoid, displaced sinistrally. Uterus
extending well into anterior third of body. Eggs tanned, oper-
culate. Mehlisgland and Laurers canal not seen in mature
specimens. Vitelline follicles erratic, not seen in anterior half of
body, may be obscured by the uterus. Excretory vesicle
extending to just posterior to rhynchus; excretory pore terminal.
Neidhartia sp.
Host:P. laevis (Lacepède)
Locality: Gambier Islands, French Polynesia (23°12S;
134°51W)
Site: Intestine and pyloric caeca
Prevalence: see Table 1
Specimen lodgement: QM G 232005 to 232029
GenBank accession numbers: ITS2 (JX415293)
Table 2 Epinepheline serranid species examined from the tropical Pacific not infected with bucephalid species reported here from species of
Plectropomus
Genus Species FP:
Gambiers
FP:
Marquesas
FP:
Moorea
New
Caledonia
QLD: Heron
Island
QLD: Lizard
Island
QLD:
Swain
Reefs
Total
Anyperodon leucogrammicus 11
Cephalopholis argus 26 3 1 12
boenak 45 9 54
cyanostigma 13 27 1 41
microprion 44
miniata 18 1 19
spiloparaea 1 1
urodeta 56 2 2 15
Cromileptes altivelis 5218
Diploprion bifasciatum 112 13
Epinephelus cyanopodus 92 11
fasciatus 10 53 2 65
fuscoguttatus 213
hexagonatus 11
howlandi 11
iroratus 12 12
macrospilos 2 2
maculatus 66
merra 3332314
ongus 21 3 24
polyphekadion 4116
quoyanus 70 6 76
tauvina 11
undulatostriatus 44
Pseudogramma polyacanthum 88 16
xanthum 4 4
Total 24 41 12 4 259 71 3 414
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Remarks: Specimens identified as belonging to
Neidhartia were recovered from the intestine and pyloric
caeca of P. laevis off the Gambier Islands, French Polynesia.
This OTU can be distinguished from all of the other
Neidhartia and Prosorhynchus species sequenced here by
1056 nucleotides (421 % sequence divergence) in the
ITS2 rRNA region.
Prosorhynchus Odhner, 1905
Prosorhynchus lesteri n. sp.
Type locality: Heron Island, Queensland Australia
(23°27S; 151°55E)
Other locality: Lizard Island, Queensland Australia
(14°40S; 145°28E)
Type host:P. leopardus (Lacepède) (Heron and Lizard
Islands)
Other host: P. laevis (Lacepède) (Heron Island)
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia Holotype: QM G 224965, Paratypes: QM G
224966 to 224974
GenBank accession numbers: ITS2 (JX415290)
Etymology: This species is named for Professor Bob
Lester (Emeritus) of the University of Queensland.
Description (Fig. 4a, b) (measurements in Table 4)
Body elongate, widest at level of anterior testis.
Tegument spiny. Rhynchus, simple, triangular. Mouth in
middle third of body. Pharynx muscular, ovoid, small.
Caecum short, sac like, extends anteriorly to just posterior
to anterior extent of vitelline follicles.
Testes 2, tandem, ovoid, overlapping. Cirrus sac (Fig. 4b)
extending anteriorly to level of posterior testis, small,
displaced sinistrally. Seminal vesicle ovoid. Pars prostatica
straight distally, curving proximally at level of seminal
vesicle, highly glandular. Ejaculatory duct short, enters gen-
ital atrium. Genital atrium ovoid, containing genital lobe;
genital lobe simple, with two lobes. Common genital pore
sub-terminal, ventral.
Ovary anterior to testes, overlaps anterior testis, ovoid,
displaced dextrally. Uterus extending to middle third of
body, just anterior to ovary, anterior extremity does not
extend anterior to vitelline follicles. Eggs small, tanned.
Mehlisgland and Laurers canal not seen. Vitelline follicles
in two lateral fields; both fields extend anteriorly and to-
wards mid-line. Extent of excretory vesicle not known;
excretory pore terminal.
Prosorhynchus wrightae n. sp.
Type-locality: Heron Island, Queensland Australia
(23°27S; 151°55E)
Other locality: Lizard Island, Queensland Australia
(14°40S; 145°28E); Gambiers Archipelago, French
Polynesia (23°12S; 134°51W).
Type host:P. leopardus (Lacepède) (Heron and Lizard
Islands)
Other hosts:P. areolatus (Rüppell) (Lizard Island), P.
laevis (Lacepède) (Heron Island; Gambiers Archipelago,
French Polynesia), Variola louti (Forsskål) (Lizard Island)
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia. Holotype: QM G 224954, Paratypes: QM G
224955 to 224964 and 232030 to 232036
GenBank accession numbers: ITS2 (JX415299)
Etymology: This species is named for Ms. Trudy Wright,
honouring her long contribution to and support of our stud-
ies of marine parasites.
Description (Fig. 5a, b) (measurements in Table 4)
Fig. 1 N. tyleri n. sp. aVentral view of holotype from P. leopardus;b
rhynchus, ventral view; ccirrus sac, ventral view. Scale bars:a
200 μm; b100 μm; c100 μm
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Body ovoid, widest at level of seminal vesicle. Tegument
spiny. Rhynchus, simple, plug-like, wider than long. Mouth
in posterior third of body; pharynx muscular, ovoid; caecum
short, sac like, extends anteriorly.
Testes 2, ovoid, displaced dextrally just posterior to mid-
body. Cirrus sac displaced sinistrally extends to pharynx.
Seminal vesicle ovoid, at level of pharynx. Pars prostatica
straight distally, curving proximally at level of seminal
vesicle. Ejaculatory duct narrow, enters genital atrium.
Genital atrium ovoid, containing genital lobe; genital lobe
C-shaped, obscured by uterus in many specimens.
Ovary anterior to testes but overlaps anterior testis.
Uterus extending well into the anterior third of body,
extends anteriorly to vitelline follicles. Eggs small,
tanned. Mehlisgland and Laurers canal not seen.
Vitelline follicles in two lateral fields in forebody, dex-
tral field longer than sinistral field. Extent of excretory
vesicle not known, not exceeding uterus anteriorly; ex-
cretory pore terminal.
Prosorhynchus freitasi Nagaty, 1937
Type host:Serranus sp. (Red Sea)
Other hosts: P. laevis (Lacepède) (Heron Island and the
Gambier Islands, P. leopardus (Lacepede) (Heron and
Lizard Islands), French Polynesia), P. maculatus (Bloch)
(Heron Island), V. louti (Forsskål) (Lizard Island)
Type-locality: Red Sea
Other localities: Lizard Island, Queensland Australia
(14°40S; 145°28E). Heron Island, Queensland Australia
413 (23°27S; 151°55E), Gambier Islands, French
Polynesia (23°12S; 134°51W).
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia. Vouchers: QM G 224975 to 224989 and 232037
to 232061
GenBank accession numbers: ITS2 (JX415295)
Description (Fig. 6a, b) (measurements in Table 5)
Body elongate. Tegument spiny. Rhynchus small, plug-
like. Anterior half of body with many glands. Mouth in
middle third of body. Pharynx muscular, ovoid, small.
Caecum short, tube-like extending anteriorly but not beyond
middle third of body.
Testes 2, oblique, ovoid, posterior testis dextral, anterior
testis median. Cirrus sac obscured almost entirely by uterus
in many specimens, extends anteriorly to level of anterior
testis. Seminal vesicle, large, ovoid. Pars prostatica straight
distally, curving proximally. Ejaculatory duct narrow, enters
genital atrium. Genital atrium ovoid, contains genital lobe.
Genital lobe with 3 main lobes.
Ovary, anterior to anterior testis, ovoid, displaced
dextrally. Uterus compact, extends to just posterior to
anterior-most portion of caecum, does not exceed vitelline
Table 3 Measurements of three new species of Neidhartia from species of Plectropomus from the Great Barrier Reef
Measurement N. haywardi n. sp. N. plectropomi n. sp. N. tyleri n. sp.
n=10 n=10 n=10
Length 904 (7311,073) 974 (7001,245) 1,331 (1,2031,544)
Width 223 (179244) 211 (103302) 250 (211325)
Length/width 4.1 (3.64.4) 4.9 (3.99.3) 5.4 (4.66.1)
Caecum 137 (107163) 168 (143193) 244 (228260)
Pharynx 64 (5275)×68 (6575) 59 (4864)× 62 (5577) 63 (5965)× 73 (6881)
Ovary 68 (4985)× 70 (5588) 78 (48103) × 67 (5780) 88 (6598)× 93 (81124)
Anterior testis 75 (5294)× 74 (6881) 70 (48112) ×74 (56106) 154 (137179) × 112 (78146)
Posterior testis 82 (5991)× 125 (6591) 94 (56145) ×79 (48116) 151 (133163) × 106 (78150)
Vitellarium 155 (146163)× 220 (192247) 127 ×150 (132167) 296 (260332)dextral only
Uterus 553 (423650) 665 (411880) 899 (8131,056)
Uterus/length 0.61 (0.560.67) 0.68 (0.560.75) 0.67 (0.620.78)
Cirrus sac 252 (228276) 279 (193353) 342 (296423)
Seminal vesicle 78 (6598)× 27 (1633) 80 (6495) × 52 (4262) 108 (81140) ×68 (4698)
Pars prostatica 168 (130215) 198 (140289) 237 (202276)
Genital atrium 56 (4665)× 61 (4981) 71 (48112) ×67 (4196) 68 (5298)× 69 (5581)
Genital lobe 36 (2642)× 38 (2649) 48 (2996) × 48 (2474) 45 (3349)×49 (3965)
Rhynchus 206 (156228) ×203 (176237) 213 (148289)× 196 (154270) 241 (195241)×177 (143208)
Rhynchus/length 0.23 (0.180.26) 0.217 (0.170.24) 0.16 (0.140.2)
Excretory vesicle 644 (553731) 714 (514937) 1,005 (9101,186)
Excretory vesicle/length 0.72 (0.640.78) 0.75 (0.710.79) 0.76 (0.730.8)
Eggs 21 (2023)× 12 (1113) 31 (2833) × 18 (1620) 42 (3844)×24 (2226)
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follicles anteriorly. Eggs, small, tanned. Mehlisgland
displaced dextrally just posterior to ovary. Laurers canal
not seen. Vitelline follicles in two lateral fields in mid-body,
both fields extending anteriorly, overlapping at mid-line.
Extent of excretory vesicle not known; excretory pore
terminal.
Prosorhynchus munozae n. sp.
Type-locality: Heron Island, Queensland Australia
(23°27S; 151°55E)
Type host:P. maculatus (Bloch) (Heron Island)
Other host:P. leopardus (Lacepède) (Heron Island)
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia. Holotype: QM G 224945, Paratypes: QM G
224946 to 224953
GenBank accession numbers: ITS2 (JX415301)
Etymology: This species is named for Ms. Gabriela
Munoz of the University of Queensland.
Description (Fig. 7a, b) (measurements in Table 5)
With features of genus and conforms to the description of
P. freitasi, differs in having a smaller body size and larger
egg size.
Prosorhynchus heronensis n. sp.
Type-locality: Heron Island, Queensland Australia
(23°27S; 151°55E)
Type host:P. laevis (Lacepède) (Heron Island)
Site in host: Pyloric caeca, intestine, rectum.
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane
Australia. Holotype: QM G 224936, Paratypes: QM G
224937 to 224939.
Fig. 2 N. haywardi n. sp. aVentral view of holotype from P. leopardus;
bcirrus sac, ventral view. Scale bars:a200 μm; b100 μm
Fig. 3 N. plectropomi n. sp. aVentral view of holotype from P.
leopardus;bcirrus sac, ventral view. Scale bars:a200 μm; b100 μm
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GenBank accession numbers: ITS2 (JX415300)
Etymology: This species is named after Heron Island,
Australia.
Description (Fig. 8a, b) (measurements in Table 5)
With features of the genus and conforms to the descrip-
tion of P. freitasi except for having a larger rhynchus and an
elongate U-shaped seminal vesicle.
Prosorhynchus plectropomi n. sp.
Typ e -loc a lity : Heron Island, GBR, Australia (23°27S;
151°55E)
Typ e host:P. leopardus (Lacepède) (Heron and Lizard Islands)
Other hosts:P. laevis (Lacepède) (Heron Island) P.
maculatus (Bloch) (Heron Island)
Other locality: Lizard Island, GBR, Australia (14°40S;
145°28E)
Site in host: Pyloric caeca, intestine, rectum
Prevalence: see Table 1
Specimen lodgement: Queensland Museum, Brisbane,
Australia. Holotype: QM G 224940, Paratypes: QM G
224941 to 224944.
GenBank accession numbers: ITS2 (JX415298)
Etymology: This species is named for the host genus,
Plectropomus.
Description (Fig. 9a, b) (measurements in Table 5)
With features of the genus and closely conforms to the
description of P. freitasi except for having non-confluent
vitelline follicle fields and having its uterus extend just
anterior to and between the two vitelline follicle fields.
Prosorhynchus sp.
Host:P. areolatus (Rüppell)
Locality: Lizard Island, Great Barrier Reef, Australia
(14°40S; 145°28E)
Site: Intestine and pyloric caeca
Prevalence: see Table 1
Specimen lodgement: QM G 232062 to 232065
GenBank accession numbers: ITS2 (JX415296)
Remarks: Specimens identified as belonging to
Prosorhynchus were recovered from the intestine and
pyloric caeca of P. areolatus off Lizard Island, GBR,
Australia. This OTU can be distinguished from all of
the other Neidhartia and Prosorhynchus species se-
quenced here by 1354 nucleotides (520 % sequence
divergence) in the ITS2 rRNA region.
Prosorhynchus sp. lesteri-like
Host:P. laevis (Lacepède)
Locality: Gambier Islands, French Polynesia (23°12S;
134°51W)
Site: Intestine and pyloric caeca
Prevalence: see Table 1
Specimen lodgement: QM G 232066 to 232070
GenBank accession numbers: ITS2 (JX415294)
Remarks: Specimens resembling P. lesteri n. sp. were
recovered from the intestine and pyloric caeca of P. laevis
Fig. 4 P. lesteri n. sp. aVentral view of holotype from P. leopardus;b
cirrus sac, ventral view. Scale bars:a200 μm; b100 μm
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off the Gambier Islands, French Polynesia. Although these
specimens resemble P. lesteri n. sp., differences in molecular
sequence data and geographic locality relative to the other
taxa reported here suggest that this is a distinct species that
needs further characterisation. This OTU can be distinguished
from all of the other Neidhartia and Prosorhynchus species
sequenced here by 250 nucleotides (119 % sequence di-
vergence) in the ITS2 rRNA region.
New records of previously described species
Prosorhynchus robertsthomsoni Bott & Cribb, 2009
Previous records
Typ e h ost: Serranidae: Cephalopholis argus Bloch &
Schneider
Other hosts: Serranidae: Cephalopholis miniata
(Forsskål), Cephalopholis cyanostigma (Valenciennes)
Typ e -loc a lity : Heron Island, GBR, Australia (23°27S;
151°55E)
New records
Hosts: Serranidae: C. argus Bloch & Schneider
Locality: Lizard Island, GBR, Australia (14°40S;
145°28E)
Morphological vouchers lodged: QM G 232071 to
232075
GenBank accession numbers: ITS2 (JX415291)
Remarks: Specimens agreeing well with the original de-
scription of P. robertsthomsoni were recovered from the
intestine and pyloric caeca of C. argus off Lizard Island,
GBR Australia, a new locality report for this species.
Molecular data from the ITS2 rRNA region are presented
for this taxon here.
Prosorhynchus conorjonesi Bott & Cribb, 2009
Previous records
Type host: Serranidae: Cromileptes altivelis (Valenciennes)
Typ e -loc a lity : Heron Island, GBR, Australia (23°27S;
151°55E)
New records
Host: Serranidae: Cromileptes altivelis (Valenciennes)
Locality: Lizard Island, GBR, Australia (14°40S; 154°28E)
Morphological vouchers lodged: QM G 232076 to
232084
GenBank accession numbers: ITS2 (JX415288)
Remarks: Specimens agreeing well with the original de-
scription of P. conorjonesi were recovered from the intestine
and pyloric caeca of Cromileptes altivelis off Lizard Island,
GBR Australia, a new locality for this species. Molecular data
from the ITS2 rRNA region are presented forthis species from
both Heron and Lizard islands; the sequences were identical.
Prosorhynchus jexi Bott & Cribb, 2009
Previous records
Type host: Serranidae: Epinephelus quoyanus
(Valenciennes)
Table 4 Measurements of P.
lesteri n. sp. and P. wrightae n.
sp. collected from Plectropomus
spp. on the Great Barrier Reef,
Australia
P. lesteri n. sp. P. wrightae n. sp.
n=10 n=10
Length 1,790 (1,3412,320) 956 (8001,088)
Width 305 (176416) 174 (128224)
Length/width 6.1 (59) 5.6 (4.86.5)
Caecum 199 (141257) 97 (80114)
Pharynx 59 (3971) × 66 (4583) 38 (3248) × 41 (3945)
Ovary 133 (103180) × 108 (83141) 91 (8596) × 89 (8890)
Anterior testis 135 (116148) × 126 (96148) 95 (9198) × 88 (7898)
Posterior testis 133 (112154) × 116 (96141) 92 (8896) × 78 (7481)
Vitellarium 250 (177327) × 292 (193353) 179 (161196) × 164
Uterus 792 (5971,091) 688 (591780)
Uterus/length 0.45 (0.360.51) 0.72 (0.680.78)
Cirrus sac 439 (334571) 238 (212262)
Seminal vesicle 182 (170193) × 85 (6496) 64 (4977) × 40 (2649)
Pars prostatica 417 157 (128179)
Genital atrium 96 (80112) × 102 (92112) 44 (3648) × 36 (3539)
Genital lobe 86 (7596) × 64 (6464) 23 (2026) × 26 (1332)
Rhynchus 187 (134257) × 157 (127205) 59 (5177) × 70 (5983)
Eggs 25 (1926) × 14 (1415) 21 (2024) × 12 (1213)
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Type locality: Heron Island, southern GBR (23°27S;
151°55E)
New records
GenBank accession numbers: ITS2 (JX415289)
Remarks: Molecular data from the ITS2 rRNA region
from specimens from the type host and type locality are
presented for this species here.
Molecular analyses
Partial ITS2 rRNA sequences for the bucephalid taxa
sequenced here were aligned with that for Bucephalus
polymorphus reported by Stunzenas et al. (2004)aswell
as D. hefeiensis and D. vaneyi reportedbyChenetal.
(2007). The alignment yielded 363 characters for analy-
sis. Table 6shows the pairwise differences and mean
divergence between ITS2 rRNA sequences from the
species of Bucephalidae included here. All combinations
of putative species of Neidhartia and Prosorhynchus
differed by 257 bases. The difference of 2 bp was
between sequences of P. l e s t e r i n. sp. from the GBR
Fig. 6 P. freitasi aVentral view of specimen from P. leopardus;b
cirrus sac, ventral view. Scale bars:a200 μm; b100 μm
Fig. 5 P. wrightae n. sp. aVentral view of holotype from P. leopardus;
bcirrus sac, ventral view. Scale bars:a200 μm; b100 μm
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Table 5 Measurements of Prosorhynchus spp. collected from Plectropomus spp. on the Great Barrier Reef
P. freitasi P. heronensis n. sp. P. munozae n. sp. P. plectropomi n. sp.
n=10 n=3 n=9 n=5
Length 1,420 (1,2161,564) 1,056 (1,0401,104) 845 (7001,040) 1,148 (1,0241,280)
Width 206 (144272) 181 (160208) 145 (128176) 154 (128208)
Length/width 7.1 (5.38.8) 5.9 (4.96.9) 5.9 (4.37.5) 7.55 (6.158.7)
Caecum 163 (128199) 150 (128161) 112 (96128) 128 (113145)
Pharynx 66 (3996) × 63 (4574) 45 × 48 44 (4248) × 47 (4548) 40 (3545) × 42 (3248)
Ovary 85 (64122) × 72 (5896) 80 (7483) × 62 (5867) 51 (4855) × 52 (4855) 67 (6177) × 50 (4855)
Anterior testis 101 (77128) × 89 (64116) 84 (7793) × 75 (5593) 62 (4864) × 56 (4864) 72 (6780) × 60 (5164)
Posterior testis 93 (83116) × 80 (64109) 88 (7793) × 74 (7180) 54 (4864) × 54 (4564) 69 (6477) × 61 (4871)
Vitellarium 216 (154270) × 188 (148238) 167 (154180) × 227 (212238) 125 (103160) × 134 (99177) 141 (103170) × 200 (145289)
Uterus 677 (475835) 447 (443539) 376 (225501) 598 (539686)
Uterus/length 0.48 (0.380.58) 0.45 (0.40.52) 0.43 (0.290.5) 0.52 (0.490.55)
Cirrus sac 282 (250321) 255 (234289) 187 (151218) 243 (202289)
Seminal vesicle 101 (90122) × 64 (5177) 193 × 19 69 (5580) × 34 (2245) 78 (6496) × 36 (3245)
Pars prostatica 177 (161193) 161 136 (127151) 196 (154241)
Genital atrium 83 × 64 47 (4548) × 47 (4548) 64 × 45
Genital lobe 64 × 64 34 (3042) × 38 (2645) 48 × 29
Rhynchus 57 (4571) × 63 (5177) 85 (8087) × 71 (6180) 41 (3942) × 46 (4252) 49 (4258) × 57 (4874)
Eggs 25 (2426) × 14 (1415) 26 (2627) × 14 (1315) 35 (3136) × 22 (1923) 25 (2426) × 14 (1415)
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and the undescribed P. l e s t e r i - like from the Gambiers,
French Polynesia. All other differences observed bet-
ween taxa were of at least 7 bp.
Minimum evolution analysis of the ITS2 rRNA dataset
resulted in a phylogram with most of the Prosorhynchus
taxa reported here from Plectropomus spp. forming a well-
supported clade that was sister to the remainder of their
congeners from non-Plectropomus serranids, which did not
form a distinct clade (Fig. 10). The only exception was P.
wrightae n. sp.
Fig. 7 P. munozae n. sp. aVentral view of holotype from P.
maculatus;bcirrus sac, ventral view. Scale bars:a200 μm; b100 μm
Fig. 8 P. heronensis n. sp. aVentral view of holotype from P. laevis;b
cirrus sac, ventral view. Scale bars:a200 μm; b100 μm
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The five morphologically similar species, P. freitasi,
P. heronensis n. sp., P. munozae n. sp., P. plectropomi
n. sp. and the Prosorhynchus sp. from P. a re o l a t u s at
Lizard Island formed a well-supported clade in both
analyses, with P. l e s t e r i n. sp. and the Prosorhynchus
sp. from P. laevis off French Polynesia observed as
sister taxa.
With the exception of P. wrightae n. sp., all Neidhartia
spp. formed a clade to the exclusion of Prosorhynchus and
Dollfustrema in both analyses. N. tyleri n. sp. was observed
as sister taxon to N. haywardi n. sp., N. plectropomi n. sp.
and Neidhartia sp. from P. laevis off French Polynesia. N.
plectropomi n. sp. was observed as sister taxon to N.
haywardi n. sp. and Neidhartia sp.
Discussion
Approach to species recognition
We approached the study of this complex of species by first
examining all available morphological specimens from the
GBR and grouping them into morphological types. Six
unambiguously distinct species were initially recognised,
the three species of Neidhartia described above and three
Prosorhynchus species, P. lesteri n. sp., P. wrightae n. sp.
and a putative species incorporating the four other
Prosorhynchus spp. reported above (P. f re i t a s i ,P.
heronensis n. sp., P. munozae n. sp. and P. plectropomi n.
sp.). ITS2 rRNA sequence data were then generated for as
many host/parasite/location combinations as possible. We
always retained morphological vouchers for molecular spec-
imens, although sets of morphological voucher specimens
of an apparent single species sometimes proved to incorpo-
rate more than one species upon subsequent careful study.
For example, sequences associated with the putative species
morphotype mentioned above yielded four distinct geno-
types upon sequencing (i.e. those associated with P. freitasi,
P. heronensis n. sp., P. munozae n. sp. and P. plectropomi n.
sp.) which differed from each other by 721 bp. Further
morphometric analysis and sequencing was then
conducted which revealed subtle but distinct morphologi-
cal characters that distinguish the taxa. There were at least
two replicate sequences for 11 of the 15 putative species,
including the species described previously by Bott and
Cribb (2009); no intraspecific variation was observed
among these replicates, including for species that were
collected from widely separated localities (e.g. between
Heron and Lizard Islands or between sites on the GBR
Fig. 9 P. plectropomi n. sp. aVentral view of holotype from P.
leopardus;bcirrus sac, ventral view. Scale bars:a200 μm; b100 μm
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Table 6 Total number of base pair differences (lower diagonal) and percentage of uncorrected ppairwise differences (upper diagonal) between Neidhartia and Prosorhynchus spp. reported here
over the ITS2 rRNA dataset
Species 1 23456789101112131415161718
1Bucephalus polymorphus 28 % 28 % 29 % 30 % 29 % 29 % 27 % 26 % 29 % 32 % 28 % 28 % 27 % 25 % 28 % 29 % 30 %
2Dollfustrema hefeiensis 75 6 % 20 % 22 % 22 % 22 % 20 % 19 % 21 % 20 % 16 % 16 % 18 % 19 % 18 % 18 % 20 %
3Dollfustrema vaneyi 76 15 20 % 21 % 20 % 19 % 20 % 19 % 22 % 21 % 16 % 16 % 18 % 19 % 18 % 19 % 21 %
4Neidhartia tyleri 78 53 54 16 % 15 % 15 % 20 % 19 % 16 % 21 % 17 % 17 % 20 % 20 % 19 % 20 % 20 %
5Neidhartia plectropomi 83 58 55 42 6 % 5 % 19 % 17 % 16 % 21 % 19 % 19 % 19 % 18 % 19 % 18 % 19 %
6Neidhartia sp. ex P. laevis FP 80 58 53 40 16 4 % 19 % 17 % 15 % 21 % 17 % 17 % 19 % 18 % 17 % 19 % 20 %
7Neidhartia haywardi 79 58 52 40 13 10 19 % 17 % 16 % 19 % 18 % 18 % 19 % 18 % 17 % 19 % 20 %
8Prosorhynchus jexi 70 50 51 51 48 47 49 7 % 21 % 17 % 17 % 17 % 16 % 16 % 15 % 14 % 16 %
9Prosorhynchus conorjonesi 65 47 49 48 44 42 44 18 19 % 17 % 16 % 16 % 17 % 17 % 17 % 16 % 17 %
10 Prosorhynchus wrightae 78 56 59 43 43 40 43 53 49 21 % 17 % 17 % 19 % 19 % 20 % 19 % 19 %
11 Prosorhynchus
robertsthomsoni
90 53 55 55 58 56 52 44 42 57 15 % 15 % 13 % 14 % 15 % 16 % 17 %
12 Prosorhynchus lesteri 76 44 44 45 51 47 49 43 41 46 42 1 % 8 % 9 % 9 % 10 % 10 %
13 Prosorhynchus sp. lesteri-
likeex P. laevis FP
76 44 43 45 50 46 48 42 40 46 41 2 8 % 9 % 9 % 10 % 10 %
14 Prosorhynchus plectropomi 73 48 48 53 51 50 50 41 44 51 36 21 21 3 % 5 % 6 % 7 %
15 Prosorhynchus heronensis 69 50 50 54 49 48 48 40 43 51 39 25 25 8 6 % 6 % 8 %
16 Prosorhynchus sp. ex P.
areolatus
74 49 49 50 50 47 47 37 42 54 41 25 25 13 15 4 % 6 %
17 Prosorhynchus freitasi 77 48 51 53 49 50 50 36 40 52 43 28 28 17 17 12 3 %
18 Prosorhynchus munozae 81 54 55 54 52 53 53 41 43 52 45 28 28 19 21 16 7
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and French Polynesia as observed for P. freitasi). This
interpretation requires that the P. lesteri-likeform from
the Gambiers should be considered a distinct species, a
conclusion that requires further work. The combined mor-
phological and molecular analysis approach taken
here indicates that there are at least ten species of
Bucephalidae parasitising the complex of Plectropomus
spp. on the GBR and a further two in French Polynesia.
Our comparisons with previously described species
are underpinned by our understanding of host specificity
in this system. We have examined substantial numbers
of 18 other epinepheline species from the GBR and
found six other prosorhynchine species (see Bott and
Cribb 2009) each restricted to only one epinepheline
genus. Of the nine species characterised here, seven
have been found only in species of Plectropomus.The
other two species, P. f r e i t a s i and P. wrightae n. sp.,
were each found once (a single specimen each) in V.
louti from Lizard Island. Because we have examined so
few V. louti, we cannot be sure of the significance of
6.0
Prosorhynchus munozae n. sp. ex Plectropomus maculatus HI
Prosorh
y
nchus
f
reitasi ex Plectro
p
omus laevis FP
Neidhartia tyleri n. sp. ex Plectropomus leopardus LI
Prosorhynchus conorjonesi ex Cromileptes altivelis LI
Prosorhynchus sp. ex Plectropomus areolatus LI
Prosorhynchus jexi ex Epinephelus quoyanus HI
Dollfustrema hefeiensis EF198238
Dollfustrema vaneyi EF198215
Prosorhynchus heronensis n. sp. ex Plectropomus laevis HI
Neidhartia tyleri n. sp. ex Plectropomus leopardus HI
Prosorhynchus lesteri n. sp. ex Plectropomus laevis HI
Prosorhynchus lesteri n. sp. ex Plectropomus leopardus LI
Neidhartia tyleri n. sp. ex Plectropomus leopardus LI
Prosorhynchus sp. ex Plectropomus areolatus LI
Prosorhynchus plectropomi n. sp. ex Plectropomus leopardus HI
Neidhartia haywardi n. sp. ex Plectropomus leopardus HI
Neidhartia sp. ex Plectropomus laevis FP
Prosorhynchus ‘lesteri-like’ ex Plectropomus laevis FP
Prosorhynchus plectropomi n. sp. ex Plectropomus leopardus HI
Prosorhynchus heronensis n. sp. ex Plectropomus laevis HI
Neidhartia haywardi n. sp. ex Plectropomus laevis HI
Prosorhynchus wrightae n. sp. ex Plectropomus areolatus LI
Neidhartia haywardi n. sp. ex Plectropomus leopardus LI
Neidhartia tyleri n. sp. ex Plectropomus maculatus HI
Prosorhynchus freitasi ex Plectropomus leopardus LI
Neidhartia tyleri n. sp. ex Plectropomus laevis HI
Prosorhynchus wrightae n. sp. ex Plectropomus leopardus LI
Prosorhynchus lesteri n. sp. ex Plectropomus leopardus HI
Prosorhynchus freitasi ex Plectropomus leopardus LI
Prosorhynchus jexi ex Epinephelus quoyanus HI
Neidhartia haywardi n. sp. ex Plectropomus laevis HI
Prosorhynchus conorjonesi ex Cromileptes altivelis HI
Prosorhynchus freitasi ex Plectropomus laevis HI
Neidhartia plectropomi n. sp. ex Plectropomus leopardus LI
Neidhartia haywardi n. sp. ex Plectropomus maculatus HI
Prosorhynchus robertsthomsoni ex Cephalopholis argus HI
Prosorhynchus conorjonesi ex Cromileptes altivelis LI
Neidhartia tyleri n. sp. ex Plectropomus leopardus HI
Prosorhynchus robertsthomsoni ex Cephalopholis argus LI
Prosorhynchus freitasi ex Plectropomus leopardus HI
Neidhartia tyleri n. sp. ex Plectropomus laevis HI
Neidhartia tyleri n. sp. ex Plectropomus leopardus LI
Prosorhynchus conorjonesi ex Cromileptes altivelis LI
Prosorhynchus freitasi ex Plectropomus laevis FP
Neidhartia haywardi n. sp. ex Plectropomus leopardus LI
Neidhartia haywardi n. sp. ex Plectropomus leopardus HI
Bucephalus polymorphus AY289239
100
Outgroup
100
100
100
89
99
65
100
93
100
100
75
100
100
100
85
96
88
100
100
93
100
95
*
*
*
Fig. 10 Relationships between the species of Neidhartia and Prosorhynchus reported here based on minimum evolution analysis of the ITS2 rRNA
region. Bootstrap values are shown at the nodes with those <50 % represented by an asterisk
2576 Parasitol Res (2013) 112:25612584
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this sharing. In addition, none of hundreds of indivi-
duals of other fish families known to harbour
bucephalids on the GBR (Apogonidae, Belonidae,
Blenniidae, Carangidae, Haemulidae, Labridae,
Muraenidae, Platycephalidae, Rachycentridae,
Scombridae, Scorpaenidae, Sphyraenidae and
Synodontidae) examined during our surveys of GBR
fishes have been infected with any of these species.
This apparent high host specificity is consistent with
the general pattern of stenoxenicity reported for trema-
todes of coral reef fishes by Miller et al. (2011). We
conclude that the high specificity makes it unlikely that
any of the species reported here occur commonly in
serranids other than Plectropomus spp.andhighlyun-
likely that they are found in non-serranids at all.
Neidhartia
Neidhartia is distinguished from other prosorhynchine gen-
era by its intertesticular ovary and the rhynchus, which is
bulbous and has a glandular cone-like base and an anterior
end that protrudes more apically than in other
prosorhynchines (Overstreet and Curran 2002). Eight nom-
inal species of Neidhartia have been proposed of which
Neidhartia macintoshi Velasquez, (1959) was transferred
to Prosorhynchus by Yamaguti (1971). Four species have
been reported from serranids: Neidhartia ghardagae
Nagaty, 1937, and Neidhartia neidharti Nagaty, 1937, both
from Serranus sp.from the Red Sea (Nagaty 1937), N.
coronata Durio and Manter, 1968, from Epinephelus sp. off
New Caledonia (Durio and Manter 1968a,b)andN.
epinepheli Bott and Cribb, 2009 from Epinephelus
maculatus off the GBR (Bott and Cribb 2009). The forms
reported here most closely resemble the four species
previously reported from serranids; Neidhartia
microrhyncha Chauhan, 1943, Neidhartia polydactyli
Manter, 1953, and Neidhartia pseudorasbora Wang &
Wang, 1998, the three species from non-serranids, are
all easily distinguished from the present forms by as-
pects of the shape of the rhynchus and the distribution
of the vitelline follicles and uterus.
Of the forms previously reported from serranids, two, N.
coronata and N. epinepheli, are easily distinguished from
the three new species proposed here. We examined speci-
mens of N. coronata from the H. W. Manter Laboratory of
Parasitology Museum and found that as originally de-
scribed, it differs from the three species reported here in that
its uterus does not extend anterior to the vitelline follicles
whereas in all three proposed new species the uterine distri-
bution is well anterior to the vitelline follicles. N. epinepheli
differs from the three species reported here in that its uterus
extends consistently anterior to the posterior margin of the
rhynchus. These morphological differences, combined with
the host distribution (i.e. infecting different genera), are
indicative of species-level distinction.
The two species of Neidhartia describedbyNagaty
(1973), N. neidharti and N. ghardagae, both bear significant
resemblance to the three species reported here. Nagatys
specimens were not lodged in a museum; however, he stated
that all species he proposed were deposited in the
Parasitology Department, Faculty of Medicine, Ain-Shams
University, Abbassia, Cairo, A.R. Egypt (Nagaty 1973). We
requested specimens from the Parasitology Department,
Faculty of Medicine, Ain-Shams University, but received
no response. Both species were reported from Serranus sp.
or Nagil(Nagaty 1937). The serranine genus Serranus is
not known in the Red Sea and the common name Nagilis
applied to P. pessuliferus in Saudi Arabia (Heemstra and
Randall 1993). Subject to recollection of these species from
their type-locality, we here presume that this is the true host.
These species thus share the same host genus as the present
material and are thus of special interest.
The five putative species that infect species of
Plectropomus serranids appear to be distinguishable as fol-
lows. N. neidharti is unique in having the vitelline follicles,
the uterus and the excretory vesicle reach or exceed the
posterior margin of the rhynchus. N. tyleri n. sp. is conspic-
uous in having relatively large eggs (3844 μm long)
whereas eggs of other species are not reported to exceed
38 μm (only N. coronata which is otherwise clearly distinct
has eggs 3338 μm long); the anterior extent of the excre-
tory vesicle is also well short of that seen in N. haywardi n.
sp., N. plectropomi n. sp. and N. neidharti.N. ghardagae
differs from N. haywardi n. sp. and N. plectropomi n. sp. in
having the vitelline follicles entirely and well anterior to the
pharynx (also the case for N. tyleri n. sp. and N. neidharti)
whereas the latter two species have them close to and both
anterior and posterior to the pharynx. In the context of the
understanding from molecular analysis that N. tyleri n. sp.
and N. haywardi n. sp. are distinct species, we note the
following differences. The excretory vesicle of N. haywardi
n. sp. reaches the posterior margin of the rhynchus whereas
that of N. plectropomi n. sp. only approaches it. The prox-
imal portion of the pars prostatica of N. haywardi n. sp. is far
more complex than that of N. plectropomi n. sp., and the
eggs of N. plectropomi n. sp. (31-μm mean length) are
distinctly larger than those of N. haywardi n. sp. (21-μm
mean length).
Two aspects of the morphology of the rhynchus of the
species of Neidhartia examined here have potential to cause
confusion in their taxonomy. First, we have observed prom-
inent gland cell ducts leading to the anterior margin of the
body in some but not all specimens of N. tyleri n. sp.
Although such ducts around the oral sucker of other
digenean families may be involved in feeding (Pearson
1972), this is presumably not their role in bucephalids
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because the oral opening is located far posterior to the
rhynchus they probably aid in attachment and locomotion.
Durio and Manter (1968a,b) reported the presence of a
single row of spines around the rhynchus of N. coronata
but that it was lost in the holotype. In some of the specimens
of N. coronata from the H. W. Manter Laboratory of
Parasitology Museum that we examined, we saw no spines
but could see a row of gland ducts, which is what we suspect
Durio and Manter (1968a,b) interpreted as spines. Second,
we noted that in live Neidhartia spp., the shape and size of
the rhynchus changes dramatically during locomotion and
that these differences were reflected in fixed specimens
which can also look dramatically different depending on
the orientation of the specimen. In particular, we have ob-
served that all three species recognised here may have the
rhynchus retracted well into the body. In such specimens,
we did not find any other correlated characters to suggest the
presence of further species and thus conclude that variation
in the shape and position of the rhynchus is not inter-specific
variation but rather an indication of the complex morphol-
ogy of the rhynchus in this genus.
Prosorhynchus
Species of Prosorhynchus can be distinguished from those
of other genera of Prosorhynchinae on the basis that they
possess a simple plug- or cone-like rhynchus that does not
have muscular suckers, the ovary is anterior to the testes,
and they have a curved pars prostatica (Overstreet and
Curran 2002). There are about 70 species of
Prosorhynchus known and about 25 of these have been
reported from serranids. Despite our expectation discussed
above that none of the species here will be found other than
in serranids and rarely other than in species of
Plectropomus, here we compare the species reported here
with all previously described species in three groupsthe
complex of species resembling P. freitasi,P. wrightae n. sp.
and P. lesteri n. sp.
The species in the P. freitasi complex are readily distin-
guished from almost all existing species of Prosorhynchus
by the tiny size of the rhynchus. For all four species, the
rhynchus never exceeds 83 μm in length or width which we
conclude immediately distinguishes them from all the pre-
viously described species in the genus that exceed 100 μm
in at least one dimension. The only previously described
species which have a comparably small rhynchus are P.
bengalensis Gupta & Gupta, 1986, P. freitasi and
Prosorhynchus madhaviae Gupta & Gupta, 1990. Of these,
both P. bengalensis from Sphyraena obstusata and P.
madhaviae from Stromateus niger are immediately distin-
guishable from all the present forms by their uteri
which passes well anterior to the vitellarium. In con-
trast, P. freitasi, as originally described, resembles the
present forms closely and the status of this species is
considered here in detail.
P. freitasi was described by Nagaty (1937) from the Red
Sea from Serranus guttatus, a junior synonym of C. argus
(Serranidae: Epinephelinae) according to Fishbase (Froese
and Pauly 2012). The species was later reported from an
Epinephelus sp. from New Caledonia and from P. maculatus
from Heron Island on the southern GBR by Durio & Manter
(1968). We have examined specimens of C. argus from the
GBR (four) and French Polynesia (eight) without finding
any bucephalids other than P. robertsthomsoni. In addition,
in the 126 specimens of six further species of Cephalopholis
that we have examined from the tropical Indo-Pacific, we
have found only P. robertsthomsoni, which does not resem-
ble any of the species reported here from Plectropomus.On
the basis of this discrepancy in host distribution (P. freitasi
reported originally only from C. argus but evidently absent
from this genus on the GBR and in French Polynesia), we
were initially inclined to discount P. freitasi as a candidate
identity for the species that we found in species of
Plectropomus. However, we conclude that the striking mor-
phological similarity of these forms makes this untenable.
We think it at least possible, and perhaps likely, that P.
freitasi was taken from a misidentified species of
Plectropomus.P. leopardus,P. laevis and P. maculatus have
not been reported from the Red Sea where Nagaty (1937)
reported these species, but P. areolatus (Rüppell, 1858) and
P. pessuliferus Fowler, 1904, are both known from there
(Heemstra and Randall 1993). Notably, P. freitasi was de-
scribed by Nagaty (1937) in the same study in which he
described the two species of Neidhartia which can be
interpreted as being from P. pessuliferus despite the host
being recorded as Serranus sp. We cautiously suggest that
the identification of Serranus guttatusmight be indirect
evidence that the host of P. freitasi is related to but different
from that of the Neidhartia species; we speculate that it was
P. areolatus, the second species of Plectropomus known in
the Red Sea. Significant in the issue of the identification of
our specimens is the fact that one of the species in this
complex (that ultimately identified as P. freitasi) has been
shown by molecular analysis to have relatively low host
specificity (infecting three species of Plectropomus together
with a single record from V. louti) and to be distributed from
the GBR to French Polynesia, a range of over 8,000 km. In
contrast, however, our evidence also demonstrates the pos-
sibility of host specificity of some species within this com-
plex in that the Prosorhynchus sp. found in P. areolatus at
Lizard island has not been found in P. leopardus there and
there is evidence of a species of Neidhartia not yet found
other than in French Polynesia. These conflicting patterns
make it equally arguable that P. freitasi may be distributed
from the Red Sea to French Polynesia (a straight line sepa-
ration of over 18,500 km) or that it has a more restricted
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distribution. Without access to the type specimens of P.
freitasi, and, perhaps now as importantly, molecular data,
we cannot resolve this question; these matters will only be
resolved by fresh collecting in the Red Sea. We are thus
faced with the issue as to whether it is wise to identify any of
the present species as P. freitasi.Weconcludethatthe
conservative approach is to interpret what is evidently the
most morphologically similar (see below), most common
and most widespread of the species as consistent with P.
freitasi. This approach differs from that taken by Hunter et
al. (2010) for species of Transversotrema where the type-
species of the genus, from a completely unknown fish from
the Red Sea, could be distinguished from forms occurring
on the GBR only with difficulty. In that case the complete
lack of knowledge of the host and evidence that
transversotrematids tend to have highly limited distributions
led to the proposal of new species for the forms from the
GBR. Here the possibility of shared host genus and evi-
dence that species of Prosorhynchus can have very wide
distributions encourages us to the more conservative con-
clusion that one of the forms can be identified as P. freitasi.
Overall, it is evident that taxonomic decisions are difficult in
cases such as these and that, as always, the decisions should
be under review as more information becomes available.
In the concept proposed here, P. freitasi,P. heronensis n.
sp., P. plectropomi n. sp. and P. munozae n. sp. resemble
each other closely morphologically, although their molecu-
lar distinction is unambiguous. Of the four, P. heronensis n.
sp. is the most distinctive in that it has the largest rhynchus,
no less than 80 μm long whereas none of the other species
reach that length in our samples. The original description of
P. freitasi reports the rhynchus as 4284 μm long which
only just overlaps the range of P. heronensis n. sp. P.
munozae n. sp. is smaller overall than the other species
(usually <1 mm whereas the others always exceed 1 mm)
but has larger eggs (3136 μm long) than the other species -
P. freitasi (2129 μm long in original description; 2426
here), P. plectropomi n. sp. (2426 μm long) and P.
heronensis n. sp. (2627 μm long). P. plectropomi n. sp.
can be distinguished from P. fr e i t a s i in that its vitelline
follicles are not confluent anteriorly whereas in P. freitasi
they are confluent and form a distinctive arc. This latter
condition is seen in the original description of P. freitasi
and it is on this basis that we allocate one of the forms
reported here to that species.
P. freitasi was reported from P. maculatus from Heron
Island and from Epinephelus sp. from New Caledonia by
Durio and Manter (1968a,b). P. maculatus is rare at Heron
Island whereas P. leopardus is abundant there (our observa-
tions). At the time of Durio and Manters work it was widely
thought that P. leopardus,P. maculatus and P. laevis were a
single variable species known as P. maculatus (see Grant
1965). The identity of the fish examined at Heron Island by
Manter (who we understand did the actual collecting) is not
now resolvable, but as we found this species in all three
species of Plectropomus at Heron Island there is no real
difficulty created. The report of Epinephelus sp.as a host
from New Caledonia is more problematic. Durio and
Manters work on the trematode fauna of New Caledonia
have many incomplete identifications including some
employing only locally used common names; we strongly
suspect that some of their identifications were mistaken at
the time or became confused subsequently. Certainly in this
case, we think it unlikely that specimens genuinely relatable
to P. f r e i t a s i would have been found in an Epinephelus
species because we have examined so many individuals of
Epinephelus without ever recovering any species resem-
bling P. freitasi. We examined voucher specimens of P.
freitasi deposited at the H. W. Manter Laboratory of
Parasitology Museum from the Durio and Manter (1968)
study (specimens from both New Caledonia and Heron
Island). These specimens and figures all generally resemble
P. freitasi andwehavenobasistoproposeadifferent
identification.
In having a body length of only 8001,088 μm and a
rhynchus only 5177 μmlong,P. w r i g h t a e n. sp. is initially
comparable to 10 species: Prosorhynchus aculeatus Odhner,
1905, P. bengalensis,Prosorhynchus congeri Yamaguti,
1970, P. freitasi,P. h e r o n e ns i s n. sp., Prosorhynchus kahala
Yamaguti, 1970, P. madhaviae,P. munozae n. sp. and P.
plectropomi n. sp. Of these, it is distinguishable from P.
congeri,P. freitasi,P. h e ro n e n s i s n. sp., P. kahala,P. munozae
n. sp. and P. plectropomi n. sp. by having the uterus extend
well anterior to the vitelline follicles. Of the remaining spe-
cies, P. aculeatus is distinctly less elongate than P. wrightae n.
sp. and has its vitelline follicles much closer to the anterior
end. Prosorhynchus bengalensis is generally similar to P.
wrightae n. sp. but has the vitelline follicles essentially parallel
rather than meeting medially and extending posteriorly be-
yond the ovary rather than to its anterior margin. P. m a d h av i a e
has both the vitelline follicles and the uterus passing signifi-
cantly further anteriorly than they do in P. w r i g h t a e n. sp. On
the basis of these distinctions, we conclude that the present
material represents a new species.
In having a body 1,3412,320 μm long and a rhynchus
134257 μm long, P. lesteri n. sp. is initially comparable with
as many as 40 species of Prosorhynchus for which the body
does not exceed 3,000 μm long and the rhynchus is at least
120 μm long and no longer than 300 μm. Of these, the
following 26 species have a posteriorly pointed rhynchus
broadly comparable to that of P. lesteri n. sp.: Prosorhynchus
aguayoi Perez Vigueras, 1955, Prosorhynchus alectis Shen,
1990, Prosorhynchus australis Szidat, 1961, Prosorhynchus
crucibulus (Rudolphi, 1819), Prosorhynchus gonoderus
Manter, 1940, P. j e x i Bott & Cribb, 2009, Prosorhynchus jupe
(Kohn, 1967), Prosorhynchus lafii Bott & Cribb, 2009,
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Prosorhynchus longisaccatus Durio & Manter, 1968,
Prosorhynchus luzonicus Velasquez, 1959, Prosorhynchus
manteri Srivastava, 1938, Prosorhynchus mcintoshi
(Velasquez, 1959), Prosorhynchus milleri Bott & Cribb,
2009, Prosorhynchus mizellei Kruse, 1977, Prosorhynchus
pacificus Manter, 1940, Prosorhynchus paracrucibulus
Velasquez, 1959, Prosorhynchus platycephali Yamaguti,
1934, Prosorhynchus polydactyli Yamaguti, 1970,
Prosorhynchus promicropsi Manter, 1940, Prosorhynchus
rotundus Manter, 1940, Prosorhynchus serrani Durio &
Manter, 1968, Prosorhynchus sinipercae Wang & Wang,
1998, P. thapari Manter, 1953, Prosorhynchus triglae Nicoll,
1914, and Prosorhynchus vietnamensis Moravec & Sey, 1989.
Of these, however, only P. milleri,P. promicropsi,P.
sinipercae and P. thapari are comparable to P. lesteri n. sp.
in having the vitelline follicles so distant from the anterior end.
These four species can be distinguished from the present
material as follows. P. m i l l e r i has the vitelline follicles distrib-
uted over a wider range than in P. l e s t e r i n. sp. and lacks the
distinctive constriction of the anterior part of the body seen for
P. l e s t e r i n. sp. P. promicropsi has the caecum passing well
anterior to the vitelline follicles as opposed to enclosed by
them in P. lesteri n. sp. P. s i n i p e rc a e , although comparable in
length to P. l e s t e r i n. sp., has a larger rhynchus (289 μm long in
measurements derived from the figure) and the vitelline folli-
cles are essentially entirely anterior to the caecum rather than
surrounding it as in P. lesteri n. sp.; P. thapari was reported
from Plectropomus maculata from Fiji by Manter (1953)and
has essentially the same size as P. lesteri n. sp., but differs in
having the vitelline follicles extend distinctly anterior to the
intestinal caecum and well posterior to the pharynx. It further
differs in the posterior extremity of the rhynchus being round-
ed rather than distinctly pointed as in the present specimens.
Notably, P. m a c u la t u s does not occur in Fiji (Heemstra and
Randall 1993) and in line with the confusion mentioned
above, the host was probably P. leopardus which does occur
there (Heemstra and Randall 1993). On the basis of these
distinctions we conclude that the present material represents
a new species.
Biogeography
Given that there remains uncertainty regarding the identity
of infections of bucephalids from species of Plectropomus
from the Red Sea (at least in that no molecular data are
available), we restrict our comments to records from the
tropical Pacific. The first important pattern observable is
the high sharing of species between the northern and south-
ern GBR; seven of ten species found on the GBR were
found at both Heron and Lizards Islands. Of the three found
at only one locality, P. heronensis n. sp. has been found only
in P. laevis which has not been examined at Lizard Island
and the unnamed Prosorhynchus species has been found
only in P. areolatus which has not been examined at
Heron Island. The prevalence of P. munozae n. sp. in P.
leopardus at Heron Island (7 of 42) is not significantly
different (p= 0.19) from the absence (0 of 12) at Lizard
Island. This high level of sharing between the northern and
southern GBR parallels that reported by McNamara and
Cribb (2011) for monorchiids of chaetodontids of the GBR.
On a broader scale, it is of interest that from the exami-
nation of just two individuals of P. laevis at the Gambiers
Archipelago in French Polynesia we have detected four
bucephalid species, two identifiable as species that occur
on the GBR and two that are clearly genetically distinct and
probably specifically distinct. Several previous studies have
demonstrated exceptionally wide distributions for other
tropical Indo-West Pacific fish trematodes on the basis of
molecular analyses. Aiken et al. (2007)showedthatthe
aporocotylid Cardicola forsteri Cribb, Daintith & Munday,
2000 has an essentially cosmopolitan distribution in its
mobile scombrid hosts. For trematodes of site-attached coral
reef fishes, ranges of at least 6,000 km have been reported
for species of Apocreadiidae, Cryptogonimidae,
Lecithasteridae and Lepocreadiidae (Chambers and Cribb
2006; Lo et al. 2001; Miller et al. 2010; Miller and Cribb
2007a; Miller and Cribb 2007b; Miller et al. 2009). These
findings are further relatable to other comparisons between
the GBR and French Polynesia. McNamara et al. (2012)
found that richness of the monorchiid genus
Hurleytrematoides declined modestly from 10 species on
the GBR to six in French Polynesia, despite the presence
of hosts susceptible to infection with three of the species
missing in French Polynesia. An interesting point of contrast
with the findings for monorchiids of chaetodontids is that
here we have evidence of two species not found on the
GBR. In this context the presence of P. thapari in
Plectropomus in Fiji, a species not yet reported elsewhere,
also hints at important biogeographical heterogeneity in this
group. Thus, vicariance may also be a significant factor
leading to the apparently restricted distributions observed
for some species. Trematodes of the Aporocotylidae,
Cryptogonimidae and Monorchiidae have now been
reported with some species that have wide geographic dis-
tributions and others that are evidently restricted in their
range (Miller and Cribb 2007a; Miller and Cribb 2008;
Nolan and Cribb 2006). The bucephalid fauna of
Plectropomus thus appears to fit this bimodal pattern of
species distribution incorporating both widespread and geo-
graphically restricted species.
Host specificity
Of the 12 putative species reported from Plectropomus spp.
here, 8 infect at least 2 species of Plectropomus. Overall we
suspect that the hostparasite combinations not found relate
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mainly to incomplete sampling, especially of P. areolatus (n
=1), P. laevis (n=6) and P. maculatus (n=3). Two of the
species found in only one host species are known only from
French Polynesia where only one species of Plectropomus
occurs. However, on the GBR, the unnamed species of
Prosorhynchus is known only from P. areolatus at Lizard
Island despite the examination of 12 P. leopardus there and
P. heronensis n. sp. is known only from P. laevis at Heron
Island, despite the examination of 42 P. leopardus and 3 P.
maculatus there. The high level of sharing between these
Plectropomus species is consistent with the close relation-
ships between P. laevis,P. leopardus and P. maculatus
reported by van Herwerden et al. (2002).
Molecular data
Few previous studies of bucephalid identity have incorpo-
rated molecular approaches. Hutson et al. (2004) used anal-
ysis of the mitochondrial cytochrome c oxidase subunit 1
gene to differentiate between unidentified bucephalid spe-
cies infecting southern Australian scallops and attempted to
match larval bucephalids with adults endemic to the region.
Chen et al. (2007) used rRNA sequences to explore distinc-
tions between two species of Dollfustrema from Chinese
fishes. Francisco et al. (2010) used 18S rRNA sequences
and RFLP analysis to distinguish two species of
Prosorhynchus in life cycle studies.
Here, the four markedly similar species, P. freitasi,P.
heronensis n. sp., P. munozae n. sp. and P. plectropomi n.
sp., were first recognised as distinct because of the use of
molecular analysis. Despite their morphological similarity,
these four species still differed by no fewer than 7 and as
many as 28 bases. These levels exceed those found between
some combinations of aporocotylids, cryptogonimids and
transversotrematids considered distinct species on the basis
of a range of morphological and biological characters in
addition to the molecular distinctions (Hunter and Cribb
2012; Miller et al. 2009; Nolan and Cribb 2006). Overall,
the inter-specific divergence in the ITS2 rRNA of 10 to
42 bp (416 %) difference for Neidhartia species and 2 to
57 bp (3-21 %) difference for Prosorhynchus species and
inter-generic divergence of 42 to 55 base pairs (1721 %)
differences is broadly consistent with the levels of variation
that have been reported previously.
Relationships
The molecular analyses reported here strongly support the
distinction between Prosorhynchus and Neidhartia with the
notable exception that P. wrightae n. sp. groups as a close
sister-taxon to the Neidhartia clade. The morphology of P.
wrightae n. sp. is certainly consistent with Prosorhynchus in
terms of the form of its relatively simple rhynchus and in the
ovary being anterior to the testes. It does resemble the three
clear species of Neidhartia from Plectropomus in that, un-
like all the species of Prosorhynchus, the uterus extends
well anterior to the vitelline follicles. Despite the molecular
discrepancy, we conclude that P. wrightae n. sp. is best
housed in Prosorhynchus for the present.
A striking aspect of these analyses is that species of
Prosorhynchus from Plectropomus (excluding P. wrightae n.
sp.) form a well-supported clade relative to those from non-
Plectropomus epinephelines; those from serranids other than
Plectropomus do not form a clade. We lack sequences for
enough of the bucephalid species of other epinepheline serra-
nids for this result to be definitive, but these results suggest
that the Prosorhynchus species of Plectropomus may have
speciated exclusively with that genus.We can presently see no
morphological evidence that unites the species from
Plectropomus. The five species that comprise the P. freitasi
groupalso form a well-supported clade. Restriction of the
uterus entirely or mainly posterior to the vitellarium may be a
morphological character that unites these taxa, although com-
parable conditions are seen in a few other species.
Richness
We have reported here evidence for a total of 12 species (nine
formally named and three awaiting formal description) of
Bucephalidae in the 4 species of Plectropomus; 8 of these
species infecting P. leopardus. This level of species richness
is exceptional, although not unique for the Bucephalidae.
According to published records, other exceptionally rich hosts
for bucephalids are Sphyraena barracuda (Sphyraenidae)
which has nine species reported from four genera
(Bucephalus Baer, 1827, Prosorhynchoides Dollfus, 1929,
Prosorhynchus and Rhipidocotyle Diesing, 1858), a freshwater
sisorid, Bagarius bagarius, which has been reported with nine
species from three genera (Bucephalus,Dollfustrema
Eckmann, 1934 and Prosorhynchus), and Caranx sexfasciatus
(Carangidae) which has seven species from four genera
(Alcicornis MacCallum, 1917, Bucephalus,Prosorhynchoides
and Rhipidocotyle). These records have been reported from a
number of different localities and from a number of different
studies (Madhavi 1974; Moravec and Sey 1989; Nahhas and
Cable 1964; Sogandares-Bernal 1959; Sogandares-Bernal and
Sogandares 1961; Williams and Bunkley-Williams 1996;
Yamaguti 1970; Yamaguti 1971), unlike the bucephalids from
P. leopardus, for which all species have been reported from the
GBR, Australia. In addition, the present system has species of
only two genera as opposed to three or four in the systems
mentioned above. There has been no exploration of these other
systems by the use of molecular analysis to confirm the dis-
tinctness and identities of the species of the multiple congeners.
We have examined many species of other families that harbour
bucephalids on the GBR (including Apogonidae, Belonidae,
Parasitol Res (2013) 112:25612584 2581
Author's personal copy
Blenniidae, Carangidae, Muraenidae, Scombridae,
Sphyraenidae, Synondontidae and other serranids) and have
not observed the high level of bucephalid richness reported
here for Plectropomus.
The richness reported here is most striking in compar-
ison with that known for other serranids, especially the
heavily studied Epinephelinae. Cribb et al. (2002)
reviewed patterns of trematode parasitism in species of
Epinephelinae. They found 36 species of epinephelines for
which there were reports of bucephalids. Of these, 21
harboured just a single bucephalid species, seven
harboured two species and five harboured three
bucephalid species. It is notable that in that dataset, the
two Plectropomus species (P. leopardus and P. maculatus)
were each recorded as harbouring only two species. This
can be taken as an indication of the incompleteness of the
literature then, and doubtless still now. However, taken
with our own findings for the comparative richness of
bucephalids in species of Plectropomus and other
epinephelines on the GBR, it seems clear that the
bucephalid richness in Plectropomus is exceptional.
The findings presented here build on a growing body of
work that demonstrates that species of Plectropomus are sub-
ject to infection with a very wide range of parasites. There are
now records of ciliates (Mori et al. 2007), copepods (Boxshall
et al. 2008; Ho and Dojiri 1977;1966a,Kabata1966b,1991;
Lewis 1964), myxosporeans (Abdel-Ghaffar et al. 2012;
Gunter and Adlard 2009), nematodes (Doupé et al. 2003;
Justine 2011;Jabbaretal.2012), cestode larvae (Abu-
Zinada 1998; Campbell and Beveridge 1987;Beveridgeet
al. 2007), monogeneans (Deveney and Whittington 2010;
Justine and Euzet 2006; Young 1967,1969), and especially
a wide range of trematodes (in addition to the bucephalids
reviewed above): Acanthocolpidae (Bray et al. 2007),
Aporocotylidae (Nolan and Cribb 2004; Overstreet and Køie
1989), Hemiuroidea 1993a (Bray et al. 1993b)and
Opecoelidae (Bray and Cribb 1989; Bray and Justine 2007;
Durio and Manter 1968a,b;Manter1963; Shen 1990). Given
that much of this work is recent, it seems likely that there
remains much to be reported from the genus.
Acknowledgments This study was funded by the Australian Re-
search Council Discovery grant DP110105389. It was also partly
funded by, and is a contribution from, the Australian node of the
CReefs global research initiative (grant number 209/29), a partner-
ship between the ABRS, BHP Billiton, the GBR Foundation, the
Census of Marine Life and the Australian Institute of Marine
Science. The CReefs Australia Project is generously sponsored by
BHP Billiton in partnership with The GBR Foundation, the Aus-
tralian Institute of Marine Science, the Australian Biological Re-
sources Study and the Alfred P. Sloan Foundation. CReefs is a
field programme of the Census of Marine Life. We thank Rob
Adlard, Rod Bray, Matthew Nolan, Holly Heiniger, Timothy Lucas,
Jonathon Yantsch, Barton McKenzie, Ashley Roberts-Thomson,
Conor Jones, Gaines Tyler and Nicole Elphinstone for assistance
with collecting. We also gratefully thank the staff of the Heron and
Lizard Island research stations for their support and hospitality
during our many long stays.
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... Bray & Justine (2013) listed a total of 29 valid species infecting members of the family Epinephelidae (P. ozakii Manter, 1934, P. platycephali Yamaguti, 1934, P. freitasi Nagaty, 1937, P. epinepheli Yamaguti, 1939, P. atlanticus Manter, 1940, P. caudovatus Manter, 1940, P. pacificus Manter, 1940, P. gonoderus Manter, 1940, P. promicropsi Manter, 1940, P. chorinemi Yamaguti, 1952, P. thapari Manter, 1953, P. aguayoi Vigueras, 1955 (Velasquez, 1959), P. bulbosus Kohn, 1961, P. jupe (Kohn, 1967), P. longisaccatus Durio & Manter, 1968, P. serrani Durio & Manter,1968, P. rarus (Kohn, 1970), P. maternus Bray & Justine, 2006, P. jexi Bott & Cribb, 2009, P. lafii Bott & Cribb, 2009, P. robertsthomsoni Bott & Cribb, 2009, P. conorjonesi Bott & Cribb, 2009, P. milleri Bott & Cribb, 2009, P. lesteri Bott, Miller & Cribb, 2013, P. wrightae Bott, Miller & Cribb, 2013, P. heronensis Bott, Miller & Cribb, 2013, P. munozae Bott, Miller & Cribb, 2013and P. plectropomi Bott, Miller & Cribb, 2013 and described two Prosorhynchus species without species identification. Rückert et al. (2009) also reported P. australis Szidat, 1961 from E. coioides, which was re-identified as Prosorhynchus sp. 1 by Bray & Palm (2009). ...
... Consequently, often molecular data are important for a more detailed analysis of the intra and inter-specific variability. Bott et al. (2013) used DNA sequence data and could recognize 4 different species, although all were very similar in morphology, and also reported co-infection of 4 different Prosorhynchus species from the same fish species (the Leopard Grouper Plectropomus leopardus [Lacepède]). The 5 species recorded in the present study were all recorded from a single host species, E. coioides. ...
... This demonstrates that Prosorhynchus species diversity within a single host species is high, and also that host specificity is not necessarily strict within this taxon. Recently, new species of bucephalids have increasingly been found from epinephelids (Bray & Justine 2013;Bott et al. 2013;Bott & Cribb 2009;Bray & Justine 2006 ), demonstrating the importance of these fish for the total species diversity in this group of trematodes. Consequently, the five recorded Prosorhynchus species, distinguished morphologically (including one new species), which are reported in the present study reinforces the view that Prosorhynchus genus is frequently distributed in Epinephelids. ...
Article
Full-text available
A total of 169 specimens of the orange-spotted grouper Epinephelus coioides (Hamilton) were collected from fishermen and marine fish farms in the Gulf of Tonkin, Vietnam. Five different species of Prosorhynchus Odhner, 1905 were recorded, including P. tonkinensis n. sp. The new species differs from all other Prosorhynchus species in the presence of an indented posterior extremity. It can be distinguished from the most closely related P. atlanticus Manter, 1940 and P. crucibulum Rudolphi, 1819 by the extension of the uterus always to the level of the ovary, the width and premouth distance in the former, and the arched vitellarium and smaller egg size in the latter, and a different host and geographical region. Prosorhynchus sp. A (not fully identified in this study) has been earlier reported from E. coioides from New Caledonia (see Prosorhynchus sp. B of Bray and Justine, 2013), P. luzonicus Velasquez, 1959 is reported throughout South-East Asia, and Prosorhynchus sp. B (no further identification possible based on a single specimen in this study) and P. maternus Bray & Justine, 2006 are reported for the first time from Vietnam. The present study demonstrates a close relationship of the Prosorhynchus species composition in Vietnam with the Indo-Australian region, warranting further comparative studies among the different epinephelids.
... Another group of fishes found in Australian waters that are exceptional hosts for bucephalids is the Serranidae. The species richness of Tylosurus, with five species of Prosorhynchoides reported from two host species, appears to be comparable to that of Plectropomus (Serranidae), which have had ten species of bucephalids (two genera) reported from four host species [38]. Four other species of epinepheline serranids have a further six bucephalid species [39]. ...
... Four other species of epinepheline serranids have a further six bucephalid species [39]. At least 40 species of bucephalids reported from serranids globally [38][39][40]. Further exploration of piscivorous fish, from these groups and others, may uncover further bucephalid species richness. ...
Article
We surveyed 14 individuals of Tylosurus crocodilus Péron & Lesueur 1821 (Belonidae) collected from the waters around Lizard Island and Heron Island, Great Barrier Reef, Queensland, Australia, and the waters around Moorea, French Polynesia. We describe two new species of bucephaline trematodes from them, Prosorhynchoides galaktionovi n. sp. and P. kohnae n. sp. They are morphologically distinct from existing Prosorhynchoides spp., with molecular data from 28S and ITS-2 ribosomal DNA, as well as cox1 mitochondrial DNA, further supporting our morphological findings. Neither species has been observed in other belonid fishes. The new species fall into the clade of species of Prosorhynchoides from belonids previously identified in Australian waters. These findings strengthen the observation that groups of bucephaline species have radiated, at least in part, in tight association with host taxa. There are now five species of Prosorhynchoides known from two belonid species in Australian waters. We, therefore, predict further richness in the nine other belonid species present.
... The ITS-2 region is considered generally suitable for delineating morphologically similar trematode species and for assessing intraspecific variation [47]. Here, the ITS-2 sequences showed no intraspecific variability for all three new species, with triplicate sequences used for each species providing unambiguous confirmation of their distinction. ...
... Other host families have been described as exceptional hosts for bucephalids, with epinepheline serranids having the greatest number of reported bucephalids on the GBR to date [4]. In that system, four species of Plectropomus were reported to be hosts of 10 bucephalid species of Neidhartia and Prosorhynchus [18,47]. Some of the greatest levels of species richness come from reports from individual fish. ...
Article
We surveyed 30 individuals of Tylosurus gavialoides (Castelnau) (Belonidae) collected from Moreton Bay, Queensland, Australia, and describe three new species of Prosorhynchoides Dollfus, 1929 from them. The new species are morphologically distinct from existing Prosorhynchoides spp. and 28S and ITS-2 ribosomal DNA data further supports our morphological findings. We also conduct the first mitochondrial DNA analysis of species of Prosorhynchoides. The new species from T. gavialoides form a strongly supported clade on the basis of the two ribosomal markers, further supporting the emerging hypothesis that bucephaline clades are strongly associated with host groups. We have not observed any of the new species reported here in over 3500 surveyed individuals of other piscivorous fish in Australia, suggesting that these species are host-specific at least to belonids, if not to only T. gavialoides. Our findings support previous reports that suggest that belonids are exceptional hosts for bucephalids. We predict that further sampling of the numerous other belonid species present in Australian waters, for which nothing is known of the bucephalid fauna, will uncover further bucephalid richness.
... This is the first report of Prosorhynchus parasitizing chaetognaths worldwide [10,11,19]. However, it is likely that this infection was accidental because only a single specimen was found among the 16,407 chaetognath specimens analyzed, and it is known that Bucephalidae larvae typically parasitize benthic molluscs as their first intermediate host, followed by marine fish as secondary intermediate and definitive hosts [29,30]. ...
Article
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The prevalence of endoparasites associated with chaetognath abundance in the coastal waters of the Mexican Central Pacific was studied fortnightly from November 2010 to December 2011. A total of 35 (0.21%) out of 16,407 chaetognaths were found to be parasitized. Five out of twelve chaetognath species (Flaccisagitta enflata, F. hexaptera, Parasagitta euneritica, Serratosagitta pacifica, Zonosagitta bedoti) were found to be parasitized by nine endoparasitic taxa: Protists (two morphotypes), digenean metacercariae [Didymozoidae, Hemiuridae, Parahemiurus sp., Lepocreadiidae, Prosorhynchus sp. (Bucephalidae)], and cestodes (metacestodes) [Tetraphyllidea (two morphotypes)]. Parasagitta. euneritica and Z. bedoti were the most abundant chaetognath species, and Protist sp. 2 and Tetraphyllidea sp. 1 were the most abundant parasites. The highest prevalence for most of the endoparasite species occurred in June, and the values varied according to three hydroclimatic periods: stratified (S), semi-mixed (SM), and mixed (M). Eight non-infected chaetognath species, two parasitized chaetognaths (F. enflata and S. pacifica), and two parasites (Protist sp. 1 and Tetraphyllidea sp. 2) were associated with warm temperatures (S and SM periods); in contrast, P. euneritica, Z. bedoti, parasitized F. hexaptera, and the parasite Tetraphyllidea sp. 1 showed a strong local preference for cooler temperatures, high productivity, and high biomass conditions (M periods). We discovered the occurrence of the digenean Prosorhynchus sp. (Bucephalidae) parasitizing the chaetognath P. euneritica, and this is the first report of Prosorhynchus parasitizing chaetognaths worldwide. We also confirmed the presence of Lepocrediidae (metacercariae larval stage) infecting F. hexaptera, a parasite that had only been recorded infecting other chaetognaths of the Atlantic Ocean. The parasite diversity affecting the chaetognath populations of the Central Mexican Pacific coast likely differs between the offshore, outer slope areas, and the surveyed coastal system.
... (Holocentridae). It has not been found in other well-sampled serranids such as species of Plectropomus Oken, which are voracious piscivores as shown by their rich fauna of bucephalids (Bott et al., 2013) or in species of Cephalopholis which harbour a different species of Bivesicula sympatrically (this study). These discrepancies have no clear explanation. ...
Article
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The taxonomy of species of Bivesicula Yamaguti, 1934 is analysed for samples from holocentrid, muraenid and serranid fishes from Japan, Ningaloo Reef (Western Australia), the Great Barrier Reef (Queensland), New Caledonia and French Polynesia. Analysis of three genetic markers ( cox 1 mtDNA, ITS2 and 28S rDNA) identifies three strongly supported clades of species and suggests that Bivesicula as presently recognized is not monophyletic. On the basis of combined morphological, molecular and biological data, 10 species are distinguished of which five are proposed as new. Bivesicula Clade 1 comprises seven species of which three are effectively morphologically cryptic relative to each other; all seven infect serranids and four also infect holocentrids. Bivesicula Clade 2 comprises three species of which two are effectively morphologically cryptic relative to each other; all three infect serranids and one also infects a muraenid. Bivesicula Clade 3 comprises two known species from apogonids and a pomacentrid, and forms a clade with species of Paucivitellosus Coil, Reid & Kuntz, 1965 to the exclusion of other Bivesicula species. Taxonomy in this genus is made challenging by the combination of low resolving power of ribosomal markers, the existence of regional cox 1 mtDNA populations, exceptional and unpredictable host-specificity and geographical distribution, and significant host-induced morphological variation.
... ITS2 rDNA has been widely used for determining species boundaries for many trematode families (Nolan & Cribb, 2005;Blasco-Costa et al., 2015), including the Bucephalidae (Bott et al., 2013;Nolan et al., 2015;Cutmore et al., 2018). The cox1 region has been far less utilised for species delineation in the Bucephalidae, with only two previous studies utilising this region (Hammond et al., 2018(Hammond et al., , 2020. ...
Article
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Three new species of the family Bucephalidae Poche, 1907 (Trematoda: Digenea) are described from the yellowtail pike, Sphyraena obtusata Cuvier (Sphyraenidae), from Moreton Bay, Queensland, Australia. The three species are morphologically consistent with the present broad concept of the genus Bucephalus Baer, 1827, but significant phylogenetic and ecological differences relative to the type-species of Bucephalus require the proposal of a new genus. Aenigmatrema n. g. is proposed for A. undecimtentaculatum n. sp. (type-species), A. inopinatum n. sp. and A. grandiovum n. sp. In addition, based on morphological, ecological and biogeographical similarities, we recombine two existing species of Bucephalus as Aenigmatrema kaku (Yamaguti, 1970) n. comb. and Aenigmatrema sphyraenae (Yamaguti, 1952) n. comb. Although the three species described in this study are extremely morphologically similar, they can be differentiated from each other, and from A. kaku and A. sphyraenae, morphometrically on the basis of egg size, tentacle number and a combination of the caecum and vitelline field lengths. Complete ITS2 rDNA, partial 28S rDNA and partial cox1 mtDNA sequence data were generated for the three new species, which formed a well-supported clade in all 28S phylogenetic analyses. An expanded phylogenetic tree for the subfamily Bucephalinae Poche, 1907 is presented, demonstrating unresolved issues with the morphology-based taxonomy of the subfamily. The three largest genera, Bucephalus, Rhipidocotyle Diesing, 1858 and Prosorhynchoides Dollfus, 1929 remain extensively polyphyletic, indicating the need for significant further systematic revision.
... Despite extensive study on the GBR (e.g. Bott & Cribb, 2005Bott et al., 2013), there are few records of bucephalids from elsewhere in Australian waters (e.g. Lebedev, 1968;Hutson et al., 2007;Nolan & Cribb, 2010). ...
Article
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Eight species of the trematode family Bucephalidae Poche, 1907 are reported from teleost fishes in Moreton Bay, Queensland, Australia. Heterobucephalopsis yongi n. sp. is described from Gymnothorax eurostus (Muraenidae); the new form is distinguished from its congeners in the possession of a tiny cirrus-sac relative to body length, the length of the caecum, the position of the mouth and pharynx, and the position of the testes and ovary. Two known species of Dollfustrema Eckmann, 1934, D. durum Nolan, Curran, Miller, Cutmore, Cantacessi & Cribb, 2015 and D. gibsoni Nolan & Cribb, 2010, are reported from Gymnothorax pseudothyrsoideus (Bleeker) (Muraenidae); although both species were described from Australian waters, this represents the first reports from Moreton Bay and G. pseudothyrsoideus. Four species of Prosorhynchus Odhner, 1905 are reported, including one new, P. brayi n. sp., which is described from Epinephelus coioides (Hamilton) (Serranidae); P. brayi n. sp. is distinguished from its congeners in the possession of vitelline follicles in a confluent arc distinctly posterior to a conical rhynchus, uterine coils that do not extend anterior to the vitelline arc, contiguous testes, a cirrus-sac that reaches anteriorly to at least the level of the posterior testis and a short excretory vesicle. Three known species of Prosorhynchus are reported from Australia, for the first time: P. luzonicus Velasquez, 1959 and P. maternus Bray & Justine, 2006 from E. coioides and Prosorhynchus platycephali (Yamaguti, 1934) Srivastava, 1938 from Ambiserrula jugosa (McCulloch) and Inegocia japonica (Cuvier) (Platycephalidae). Skrjabiniella Issaitschikow, 1928 is re-recognised for new specimens of Skrjabiniella uniporus (Ozaki, 1924) n. comb. collected from Conger cinereus Rüppell (Congridae); three additional species of Prosorhynchus are considered members of this genus, two of which are synonymised with S. uniporus.
... This low level of genetic variation has more frequently been interpreted as intraspecific variation especially, as here, across wide geographic ranges (e.g. Bott et al., 2013;McNamara et al., 2014;Cutmore et al., 2016). We conclude that these species are best interpreted as synonymous; as first revisers we propose that C. lafii be retained as the senior synonym. ...
Article
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The aporocotylid fauna of the mottled spinefoot, Siganus fuscescens (Houttuyn), from Moreton Bay, Queensland, Australia, was characterised using a combined morphological and molecular approach. Four aporocotylid species were identified, three belonging to the genus Ankistromeces Nolan & Cribb, 2006 and one to Cardicola Short, 1953. Specimens of Cardicola matched an undescribed species from the same host and locality; this species is described as Cardicola mogilae n. sp. Phylogenetic analyses of ITS2 and 28S data showed that C. mogilae n. sp. forms a strongly supported clade with other Cardicola species from siganid fishes. We record Ankistromeces olsoni Nolan & Cribb, 2006 in Moreton Bay for the first time, redescribe A. dunwichensis Nolan & Cribb, 2006 on the basis of new specimens and sequence data and re-report Ankistromeces sp. X from Moreton Bay based on molecular data. We review the status of the ten putative species of aporocotylids reported from siganids. Small variation in ITS2 rDNA sequences, in association with different geographic localities, was previously used to separate Cardicola lafii Nolan & Cribb, 2006 from C. parilus Nolan & Cribb, 2006, C. bartolii Nolan & Cribb, 2006 from C. watsonensis Nolan & Cribb, 2006, C. tantabiddii Nolan & Cribb, 2006 from Cardicola sp. 2, Ankistromeces sp. Y from A. olsoni and Ankistromeces sp. X from Ankistromeces sp. Z. These five combinations are reinterpreted as each representing a single species; Cardicola lafii is recognised as the senior synonym of C. parilus and C. bartolii as the senior synonym of C. watsonensis. This study thus suggests that six, rather than ten, species should be recognised as infecting S. fuscescens. This richness remains greater than is known for any other fish species and siganids are, so far, unique among fishes in harbouring two strongly radiated lineages of aporocotylids.
Article
During 2021 through 2023, the golden mussel Limnoperna fortunei and freshwater fishes were sampled from 28 sites in the Tone River system, Japan, and adult trematodes of Dollfustrema were found in the fishes. Molecular and morphological analyses based on 28S rDNA and the ITS1À5.8SÀITS2 region revealed the trematode as 'Dollfustrema hefeiense', previously reported in Mainland China and likely introduced to Japan. Given that its scientific name was considered invalid, we re-described the species as Dollfustrema invadens n. sp. Additionally, the DNA-based survey helped clarify the trematode's life cycle in the river system. A sporocyst and metacercariae were detected in the golden mussel's visceral mass and in the muscles of two small freshwater fish species, respectively. The channel catfish Ictalurus punctatus harboured mature trematodes in its intestine, and adult trematodes were also found in the muscles of fishes infected with meta-cercariae, suggesting direct metacercariae development in fish muscle. Furthermore, another introduced bucephalid trematode, Prosorhynchoides ozakii, previously reported in the river system, was detected in the mussels and fishes. Moreover, co-infection of both bucephalid trematodes was observed in certain fishes.
Article
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Species-level delineation of digenetic trematodes is complex and can be best achieved by integrative taxonomy using both genetic characterisation and morphological analysis. Two new Bucephalidae species of the genus Rhipidocotyle Diesing, 1858 are described here based on specimens collected from the intestine of Sphyraena putnamae Jordan & Seale following this approach. Adults of R. siphonyaka n. sp. and R. nolwe n. sp. possess tentacles and a tegument with scales. They are distinguished from their congeners by the arrangement of the digestive structures, the extent of the uterus relative to vitelline fields, and the arrangement of the reproductive structures. Rhipidocotyle siphonyaka n. sp. differs from R. nolwe n. sp. in having the pharynx and mouth positioned in the pre-uterine field, tandem testes, longer body length, and shorter pre-vitelline and post-testicular distance. Rhipidocotyle siphonyaka n. sp. differs from its congeners in having a tube-like intestinal caecum, pharynx and mouth opening positioned in the pre-vitelline field. Rhipidocotyle nolwe n. sp. appears to be similar, morphologically and morphometrically to Rhipidocotyle khalili (Nagaty, 1937). Despite their similarities, R. nolwe n. sp. has a shorter body length and egg size. Moreover, the molecular analysis of 28S and ITS rDNA fragments indicate that R. siphonyaka n. sp. and R. nolwe n. sp. are closely related phylogenetically but distinct from one another and other Bucephalidae for which molecular data are available.
Book
The purpose of this book is to serve as a fish parasite guide for sport fishermen, commercial and tour-guide fishermen, fishery biologists, ecologists, scientists, and anyone interested in the health and welfare of big game fishes. We hope it will encourage the study of the interrelationships between fishes and their intimate parasite partners around Puerto Rico and throughout the Atlantic. Big game fishes are important sportfishing and food resources. Many of their fish parasites attract the attention of fishermen because they are large, abundant and always on particular host species. The health of these fishes, and the humans who enjoy catching and eating them, is of great concern. The environments of many coastal areas have deteriorated and there is little agreement about how much of this environmental damage has spilled over into the open ocean. The abundance and diversity of big game fish parasites might be used as an indicator of environmental changes. Many parasites are useful as biological tags for tracing stock movements, mixing, migrations and other aspects of the biology of big game fishes. They can also provide readily available examples of many invertebrate phyla which can be used for classroom examinations. The present knowledge of parasites of big game fishes is at the most basic level, describing species, but the interrelationships between big game fish parasites and their intermediate and final hosts are as complex and intricate as food webs described by ecologists. It is extremely difficult to study the parasites and diseases of live oceanic, fast-moving fishes. Hook and line fishing selects for healthy fishes because sick fishes seldom bite lures or baits. Debilitated fishes in the open sea are quickly eaten, or sink, and seldom wash ashore. Still, we can assume that parasites and diseases cause as many problems for these big game fishes as they do for fishes in more easily examined habitats. A study found that the presence of one species of parasite reduced the yield of a big game fishery by about one fifth. We estimate that somewhere between one third to one half of all big game fish resources are lost due to disease. We need to understand the workings of diseases throughout the ecosystem if we are to have any hope of recuperating losses due to diseases. Unfortunately, we lack complete knowledge of these processes in a single fish, or even of a single disease organism! Most big game fishes are either already overexploited, or are soon to be over fished. As dolphin, greater amberjack and other big game fishes are raised in captivity, we are beginning to discover their deadly parasitic, bacterial and viral diseases. We cannot afford to ignore manageable problems that have the potential to double the stocks of big game fishes We hope that this book will serve as a beginning to better understand these forces in the ecology of big game fishes. Williams, E. H., Jr. and L. Bunkley-Williams. 1996. Parasites of offshore, big game sport fishes of Puerto Rico and the western North Atlantic. Puerto Rico Department of Natural and Environmental Resources, San Juan, Puerto Rico, and Department of Biology, University of Puerto Rico, Mayagüez, Puerto Rico, 384 pp.
Chapter
A book is presented providing illustrated keys for the identification of the sexual adults of trematodes to help both specialist and non-specialist alike to identify material to generic level. Each genus is described including morphological, host, distributional and life history data. This is the first of 3 volumes and includes the Aspidogastrea and digenean groups belonging to the order Strigeida (including the blood flukes, brachylaemids, bucephalids, clinostomids, diplostomids, fellodistomids, gymnophallids and hemiuroids; the Didymozoidae will be included in the next volume).
Article
Examination of the humpback red snapper, Lutjanus gibbus (Perciformes: Lutjanidae), from Lizard Island off the Great Barrier Reef and Rasdhoo Atoll, Maldives revealed the presence of a new species of Lobosorchis (Digenea: Cryptogonimidae), L. polygongylus n. sp. Lobosorchis polygongylus n. sp. is distinguished from the typeand only other species, L. tibaldiae by the combination of body size, oral spine number (60–81 in L. polygongylus, 47–56 in L. tibaldiae) and number of testes (13–25 in L. polygongylus, 9 in L. tibaldiae). Bayesian inference analysis using data from the internal transcribed spacers 1 and 2 (ITS1 and ITS2), 5.8S and the large subunit (LSU) nuclear ribosomal DNA of L. polygongylus, L. tibaldiae and species of Beluesca, Caulanus, Chelediadema, Neometadena, Latuterus, Retrovarium and Siphoderina was performed to explore phylogenetic relationships of species of Lobosorchis with other cryptogonimid taxa. Despite the significant morphological differences between Lobosorchis polygongylus and L. tibaldiae, these two species differed consistently by only 5 base pairs (bp) over the entire ITS region (3 bp in ITS1, 0 bp in 5.8S and 2 bp in ITS2) and 1 bp in the LSU rDNA regions examined. The ITS2 rDNA region was sequenced from metacercariae obtained from the fins, flesh or body cavities of a number of fishes belonging to the Blenniidae, Pomacentridae and Tetraodontidae and analysed using minimum evolution analysis with L. polygongylus and L. tibaldiae. This revealed the presence of two additional genotypes (putative Lobosorchis sp. A and B), which consistently differed from L. polygongylus by 1 and 4 bp, L. tibaldiae by 1 and 4 bp and from each other by 3 bp over the ITS2 dataset. Although these genetic differences are relatively small, when evaluated in light of the differences observed between L. polygongylus and L. tibaldiae (which are morphologically quite distinct) and differences seen in other congeneric cryptogonimid taxa, the ITS2 rDNA data alone suggest that at least two more species of Lobosorchis are present at Lizard Island. These data also suggest that the ITS2 rDNA region alone is suitable for resolving operational taxonomic units (OTUs) at the species level within the Cryptogonimidae based on what was observed in this and other cryptogonimid systems. A morphological description of metacercariae of L. tibaldiae obtained from two species of Pomacentridae at Heron Island, off the Great Barrier Reef is also provided.