Parasite 2013, 20, 56
R.A. Bray and J.-L. Justine, published by EDP Sciences, 2013
DOI: 10.1051/parasite/2013055
urn:lsid:zoobank.org:pub:57C9DB24-D0A5-4730-93BE-1057D4419409
RESEARCH ARTICLE
Available online at:
www.parasite-journal.org
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Bucephalidae (Digenea) from epinephelines (Serranidae:
Perciformes) from the waters off New Caledonia, including
Neidhartia lochepintade n. sp.
Rodney A. Bray1,* and Jean-Lou Justine2,a
1
2
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
UMR 7138, Systématique, Adaptation, Évolution, Muséum National d’Histoire Naturelle, Case postale 51, 55 rue Buffon,
75231 Paris Cedex 05, France
Received 7 October 2013, Accepted 4 December 2013, Published online 19 December 2013
Abstract – Many bucephalid species, mainly of the subfamily Prosorhynchinae, have been described from epinepheline
serranids (groupers) throughout the World’s Oceans. In this paper eight named prosorhynchine species are described
and/or illustrated from epinepheline fishes from New Caledonia. Neidhartia lochepintade n. sp. in Epinephelus chlorostigma differs from other Neidhartia spp. in various combinations of distinct body-size, rhynchus size, previtelline and
pre-mouth distance, post-testicular distance, cirrus-sac reach and egg-size. Other species are: Neidhartia haywardi Bott,
Miller & Cribb, 2013 in Plectropomus leopardus; Neidhartia tyleri Bott, Miller & Cribb, 2013 in Plectropomus leopardus
and Plectropomus laevis; Prosorhynchus freitasi Nagaty, 1937 in Plectropomus leopardus and Plectropomus laevis;
Prosorhynchus robertsthomsoni Bott & Cribb, 2009 in Cephalopholis argus; Prosorhynchus longisaccatus Durio &
Manter, 1968 in Cephalopholis urodeta, Epinephelus areolatus, Epinephelus cyanopodus and Epinephelus maculatus.
Prosorhynchus luzonicus Velasquez, 1959 and Prosorhynchus sp. B. in Epinephelus coioides; Prosorhynchus serrani
Durio & Manter, 1968 in Variola albimarginata and Variola louti; Prosorhynchus sp. A in Epinephelus morrhua;
Prosorhynchus sp. immature in Epinephelus coeruleopunctatus. The new combination Neidhartia longivesicula (Bilqees,
Khalil, Khan, Perveen & Muti-ur-Rehman, 2009) (Syn. Prosorhynchus longivesicula) is formed. Evidence from this paper
and earlier molecular studies indicates that there are numerous morphologically similar prosorhynchine species in
serranids, most of which show a high degree of host-specificity.
Key words: Bucephalidae, Neidhartia, Prosorhynchus, Epinephelus, Cephalopholis, Variola, New Caledonia.
Résumé – Bucephalidae (Digenea) d’Epinephelinae (Serranidae: Perciformes) en Nouvelle-Calédonie, y compris
Neidhartia lochepintade n. sp. De nombreuses espèces de Bucephalidae, principalement de la sous-famille
Prosorhynchinae, ont été décrites de Serranidae Epinephelinae (mérous) à travers les océans du monde. Dans cet article,
huit espèces nommées de Prosorhynchinae sont décrites et / ou illustrées d’Epinephelinae de Nouvelle-Calédonie.
Neidhartia lochepintade n. sp., parasite d’Epinephelus chlorostigma, diffère des autres espèces de Neidhartia par des
combinaisons variées de taille du corps, taille du rhynchus, distance pré-vitelline et pré-bouche, distance post-testiculaire,
étendue du sac du cirre et taille des œufs. Les autres espèces sont : Neidhartia haywardi Bott, Miller & Cribb, 2013 chez
Plectropomus leopardus; Neidhartia tyleri Bott, Miller & Cribb, 2013 chez Plectropomus leopardus et Plectropomus
laevis; Prosorhynchus freitasi Nagaty, 1937 chez Plectropomus leopardus et Plectropomus laevis; Prosorhynchus
robertsthomsoni Bott & Cribb, 2009 chez Cephalopholis argus; Prosorhynchus longisaccatus Durio & Manter, 1968
chez Cephalopholis urodeta, Epinephelus areolatus, Epinephelus cyanopodus et Epinephelus maculatus; Prosorhynchus
luzonicus Velasquez, 1959 et Prosorhynchus sp. B. chez Epinephelus coioides; Prosorhynchus serrani Durio & Manter,
1968 chez Variola albimarginata et Variola louti; Prosorhynchus sp. A chez Epinephelus morrhua; Prosorhynchus sp.
immature chez Epinephelus coeruleopunctatus. La nouvelle combinaison Neidhartia longivesicula (Bilqees, Khalil,
Khan, Perveen & Muti-ur-Rehman, 2009) (Syn. Prosorhynchus longivesicula) est formée. Cet article et des études
moléculaires antérieures indiquent qu’il existe de nombreuses espèces de Prosorhynchinae morphologiquement
semblables chez les Serranidae, dont la plupart présentent un haut degré de spécificité à l’hôte.
*
Corresponding author: rab@nhm.ac.uk
After January 2014: ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, EPHE, MNHN, UPMC), Muséum
National d’Histoire Naturelle, Case postale 51, 55 rue Buffon, 75231 Paris Cedex 05, France
Rodney A. Bray – urn:lsid:zoobank.org:author:C053AFDE-D221-4BE1-9B0A-30307A67D4C0
Jean-Lou Justine – urn:lsid:zoobank.org:author:17643DCB-2C9D-4386-BB94-D2F04966B0E9
a
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
2
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Introduction
Bucephalid digeneans are frequently found in fishes of the
family Serranidae, in particular in members of the subfamily
Epinephelinae [8]. For example, Bray & Justine [5] listed
16 species of Prosorhynchus Odhner, 1905 from serranid
fishes: P. atlanticus Manter, 1940, P. bulbosus Kohn, 1961,
P. caudovatus Manter, 1940, P. chorinemi Yamaguti, 1952,
P. epinepheli Yamaguti, 1939, P. freitasi Nagaty, 1937,
P. gonoderus Manter, 1940, P. jupe (Kohn, 1967), P. longisaccatus Durio & Manter, 1968, P. mcintoshi (Velasquez, 1959)
(this may belong to Neidhartia), P. ozakii Manter, 1934,
P. pacificus Manter, 1940, P. platycephali (Yamaguti, 1934),
P. promicropsi Manter, 1940, P. serrani Durio & Manter,
1968, and P. thapari Manter, 1953, and added a further species
P. maternus Bray & Justine, 2006. Two were missed, namely
P. aguayoi Vigueras, 1955 and P. rarus (Kohn, 1970). Later,
Bott & Cribb [2] added a further five species, P. jexi Bott &
Cribb, 2009, P. lafii Bott & Cribb, 2009, P. robertsthomsoni
Bott & Cribb, 2009, P. conorjonesi Bott & Cribb, 2009 and
P. milleri Bott & Cribb, 2009 and recently Bott et al. [3] added
yet another five species, all from Plectropomus spp., P. lesteri
Bott, Miller & Cribb, 2013, P. wrightae Bott, Miller & Cribb,
2013, P. heronensis Bott, Miller & Cribb, 2013, P. munozae
Bott, Miller & Cribb, 2013 and P. plectropomi Bott, Miller &
Cribb, 2013, making a total of 29 species. Other genera of bucephalids are also reported in serranids, e.g., Neidhartia Nagaty,
1937 (N. neidharti Nagaty, 1937, N. ghardagae Nagaty, 1937,
N. coronata Durio & Manter, 1968, N. epinepheli Bott & Cribb,
2009, N. tyleri Bott, Miller & Cribb, 2013, N. haywardi Bott,
Miller & Cribb, 2013, N. plectropomi Bott, Miller & Cribb,
2013), Pseudoprosorhynchus Yamaguti, 1938 (P. hainanensis
Shen, 1990), Rhipidocotyle Diesing, 1858 (R. angusticolle
Chandler, 1941, R. clavivesiculum Ku & Shen, 1975), Bucephalus
Baer, 1827 (B. heterotentaculatus Bravo-Hollis & LamotheArgumedo, 1956), Myorhynchus Durio & Manter, 1968
(M. pritchardae Durio & Manter, 1968), Muraenicola Nolan
& Cribb, 2010 (syn: Folliculovarium Gu & Shen, 1983
pre-occupied) (M. xishaensis (Gu & Shen, 1983)),
Neoprosorhynchus Dayal, 1948 (N. purius Dayal, 1948) and
Telorhynchus Crowcroft, 1947 (T. arripidis Crowcroft, 1947).
Most of these species belong to the subfamily Prosorhynchinae Nicoll, 1914, but Bucephalus and Rhipidocotyle are in
the Bucephalinae. These may be accidental records. The only
bucephaline species originally described from a serranid is
R. clavivesiculus which, according to the original description
[22], has a recurved pars prostatica and sperm duct, a characteristic of the Prosorhynchinae [33].
This paper expands on the records made in Justine et al.
[19], discussing the systematics of the reports in that paper,
and adding new data obtained subsequently.
Materials and methods
Digeneans were collected live, immediately fixed in nearly
boiling saline and then transferred to 80% ethanol. Whole
mounts were stained with Mayer’s paracarmine, cleared in
beechwood creosote and mounted in Canada balsam. Measurements were made through a drawing tube on an Olympus BH-2
microscope, using a Digicad Plus digitising tablet and Carl
Zeiss KS100 software adapted by Imaging Associates, and
are quoted in micrometres. The following abbreviations are
used: BMNH, British Museum (Natural History) Collection at
the Natural History Museum, London, UK; MNHN JNC,
Muséum National d’Histoire Naturelle, Paris, France.
Use has been made of the visual key to Prosorhynchus
developed by Bray & Palm [6]. (http://www.nhm.ac.uk/
bray2009) and a similar key to the genus Neidhartia recently
devised by us. We use the term ‘‘cirrus-sac reach’’ for the distance from the anterior-most extremity of the cirrus-sac to the
posterior extremity of the body as a percentage of the bodylength.
Results
Family Bucephalidae Poche, 1907
Subfamily Prosorhynchinae Nicoll, 1914
Genus Neidhartia Nagaty, 1937
urn:lsid:zoobank.org:act:380959E0-57F5-44FB-87FE-EB7
B4958CCB6
Neidhartia lochepintade n. sp. (Figures 1, 2)
Syn. Prosorhynchus sp. in Epinephelus chlorostigma of
Justine et al. (2010).
urn:lsid:zoobank.org:act:A3A03B8A-A686-4168-AFE5-5
F6A54C923BA
Type-Host: Epinephelus chlorostigma (Valenciennes)
brown-spotted grouper, Serranidae.
Site: Pyloric caeca.
Type-Locality: Off Récif Toombo, deep-sea (22340 431S,
166270 552E, 04/01/2008);
Other locality: Off Récif Toombo, deep-sea, 200–300m
(22340 187S, 166260 292E, 01/12/2009).
Prevalence: 67% (2 of 3).
Type-specimens: Holotype MNHN JNC 2446d-1, Paratypes, MNHN JNC 2446d-2-5, JNC 3141, BMNH
2013.11.18.1.
Etymology: Loche Pintade is the New Caledonian name for
the host species.
Description
Based on 10 whole-mount preparations. Measurements and
ratios in Table 1. Body fusiform, widest at about mid-body
(Figures 1, 2). Tegument spinous; spines squamous, tiny, reach
to posterior extremity. Rhynchus broad, relatively short and
blunt. Mouth at about level of ovary, distinctly in post-equatorial half of body. Pharynx small, globular. Caecum oval, directed anteriorly.
Testes 2, irregularly oval, oblique, in about mid-body, usually well separated. Cirrus-sac elongate, more-or-less parallel
sided, reaching anterior testis, anteriorly to pharynx. Seminal
vesicle elongate-oval, in proximal cirrus-sac. Pars prostatica
long, in two distinct parts; proximal part narrow, coiled over
seminal vesicle; distal part wider, straighter, surrounded by
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Figure 1–6. 1: Neidhartia lochepintade n. sp. Holotype, uterus in outline. 2: Neidhartia lochepintade n. sp. Paratype, uterus in outline.
3: Neidhartia haywardi Bott, Miller & Cribb, 2013, uterus in outline. 4: Neidhartia tyleri Bott, Miller & Cribb, 2013 ex Plectropomus
leopardus, uterus in outline. 5: Neidhartia tyleri Bott, Miller & Cribb, 2013, ex Plectropomus laevis, uterus in outline. 6: Prosorhynchus
robertsthomsoni Bott & Cribb, 2009. Ventral view, uterus in outline. Scale bars: 500 lm (Figs. 1, 2, 4–6); 200 lm (Fig. 3).
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4
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 1. Measurements and ratios of Neidhartia spp. % refers to % of body-length.
Species
Host
n
Neidhartia
lochepintade n. sp.
Neidhartia
haywardi
Neidhartia tyleri
Neidhartia tyleri
Epinephelus
chlorostigma
Plectropomus
leopardus
Plectropomus
leopardus
Plectropomus
laevis
10
5
7
6
min. max. mean min. max. mean min.
max. mean
min.
max. mean
Length
938 1,252 1,159 658 744 715 1,031 1,663 1,392 1,204 1,512 1,328
Width
299
460
391 133 209 176
282
355
319
240
396
333
Previtelline distance
193
279
232 185 252 224
442
671
527
310
602
452
Precaecal distance
311
478
428 336 336 336
525
791
646
634
914
756
Pre-uterine distance
259
361
312 168 222 186
217
487
384
262
518
383
Pre-mouth distance
497
734
655 470 472 471
730 1,273
995
903 1,263 1,028
Pretesticular distance
422
588
541 295 385 348
547 1,082
836
565
875
726
Pre-ovarian distance
451
634
596 311 396 368
614 1,070
862
649
1,115
859
Rhynchus length
114
163
145 145 178 165
207
255
225
189
234
218
Rhynchus width
96
132
109 114 133 125
143
216
174
145
198
166
Rhynchus to vitellarium distance
35
235
102 32
93 64
226
426
303
74
387
229
Rhynchus to uterus distance
127
357
183
1
35 21
8
276
163
32
312
161
Rhynchus to caecum distance
196
443
308 152 152 152
317
530
427
408
684
538
Long vitelline field
312
465
375 104 236 149
160
465
344
192
485
297
Short vitelline field
256
511
339 98 142 114
104
355
230
130
336
246
Caecum length
133
203
165 109 109 109
117
279
186
170
260
217
Caecum width
94
131
112 55
55 55
86
133
100
69
86
80
Pharynx length
52
74
65 48
59 54
42
82
72
66
82
73
Pharynx width
59
74
65 58
64 61
53
94
76
67
84
77
Ovary length
98
122
111 62
85 71
73
173
118
105
136
120
Ovary width
77
110
97 50
68 60
79
138
110
99
123
112
Distance between ovary and anterior testis 0
25
3
0
58 12
0
27
4
0
71
26
Anterior testis length
84
128
107 55
91 75
115
179
150
147
217
175
Anterior testis width
75
116
92 54
73 63
116
168
142
130
194
155
Distance between testes
31
109
76
0
72 24
0
29
11
36
80
56
Posterior testis length
89
127
108 72
87 81
114
195
154
159
217
180
Posterior testis width
75
114
89 43
82 63
103
158
130
123
171
142
Posterior testis to cirrus-sac
0
0
0
0
0
0
0
0
0
0
0
0
Cirrus-sac length
363
595
480 179 217 202
217
360
311
239
353
308
Cirrus-sac width
117
169
141 66
94 79
91
148
128
99
116
109
Seminal vesicle length
146
164
158 63
119 78
79
179
118
73
148
112
Seminal vesicle width
70
117
88 37
54 45
40
115
65
41
88
64
Pars prostatica length
459
573
515 240 333 284
295
416
361
0
503
299
Pars prostatica width
64
95
81 51
69 61
59
109
79
61
85
74
Post-testicular distance
322
479
396 193 231 207
217
336
256
124
214
158
Post-vitelline distance
428
685
525 291 369 332
286
656
498
468
644
565
Cirrus-sac reach
490
637
564 278 346 312
322
510
444
355
491
432
Post-ovarian distance
402
463
431 249 303 282
317
502
407
269
473
335
Post-genital pore distance
37
63
50 30
48 42
30
81
47
29
57
41
Egg length
26
32
30 22
25 23
23
31
28
34
39
37
Egg width
13
22
17
11
15 13
15
20
18
16
19
17
Width %
30.1
38.1 33.7 20.2 28.5 24.5
19.3
32.4 23.6
19.2
28.9 25.1
Previtelline distance %
16.0
22.6 20.1 28.1 34.1 31.2
29.5
51.2 38.5
25.7
43.6 33.8
Precaecal distance %
33.1
38.8 36.9 45.4 45.4 45.4
48.4
50.9 49.9
52.7
60.4 55.3
Pre-uterine distance %
23.0
29.4 26.9 22.6 30.0 26.0
21.0
35.9 27.3
21.8
37.5 28.7
Pre-mouth distance %
52.9
60.0 56.7 63.2 63.8 63.5
66.2
76.5 72.6
73.9
83.6 77.3
Pretesticular distance %
44.9
51.3 47.7 44.9 52.1 48.5
53.0
65.0 59.5
46.9
60.8 54.4
Pre-ovarian distance %
48.0
54.2 51.8 47.3 54.3 51.4
58.9
64.4 61.8
51.4
73.8 64.3
Rhynchus length %
11.4
13.4 12.5 19.9 24.1 23.0
14.6
20.9 16.5
13.7
19.4 16.5
Rhynchus width % rhynchus length
63.2 101
75.8 66.9 81.2 76.0
63.0 105
77.8
66.3 105
76.9
Longest vitelline field %
28.1
37.1 32.4 15.8 31.7 20.8
15.6
31.7 24.2
15.3
32.1 22.1
Caecal length %
11.9
16.3 14.2 14.8 14.8 14.8
10.6
19.0 13.9
14.1
17.9 15.9
Ovary length %
8.76 10.5
9.7 8.62 12.1 9.97
6.55
11.1
8.50
8.01 10.8
9.07
(continued on next page)
5
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 1. (Continued)
Species
Host
Neidhartia
lochepintade n. sp.
Neidhartia haywardi
Neidhartia tyleri
Neidhartia tyleri
Epinephelus
chlorostigma
Plectropomus
leopardus
Plectropomus
leopardus
Plectropomus
laevis
n
min.
Anterior testis length %
8.25
Distance between testes %
3.36
Posterior testis length %
7.38
Posterior testis to cirrus-sac %
0
Cirrus-sac length %
30.4
Seminal vesicle length % of cirrus-sac length 27.2
Post-testicular distance %
30.2
Post-vitelline distance %
39.7
Cirrus-sac reach %
41.1
Post-ovarian distance %
35.3
Post-genital pore distance %
3.04
10
max.
11.1
9.43
11.7
0
52.9
35.1
39.7
56.8
59.2
43.0
6.70
5
mean
9.4
6.62
9.7
0
41.8
29.9
34.7
45.3
49.0
37.6
4.41
dense layer of gland-cells, lining of filaments in chevron
arrangement. Ejaculatory duct narrow, opening on large, complex genital lobe inside genital atrium. Genital atrium large.
Genital pore distinctly separated from posterior extremity.
Ovary oval, intertesticular, overlapping posterior testis.
Mehlis’ gland overlapping ovary and posterior testis. Details
of proximal female system obscured by eggs. Uterus not
reaching anteriorly to vitelline fields, fills most of available
space to level of genital pore. Eggs numerous, tanned, operculate. Metraterm not detected, obscured by eggs. Vitellarium
consists of two lateral fields of 12–15 follicles, more or less
symmetrical, but with one field slightly longer than other, anterior extremity distinctly posterior to rhynchus and anterior to
uterus, always anterior to caecum and gonads; posterior extremity at about level of ovary.
Excretory pore terminal; anterior extent of vesicle obscured
by eggs.
Discussion
The features that distinguish N. lochepintade from previously described Neidhartia species are discussed below; comparative metrical data in Table 2.
Neidhartia coronata Durio & Manter, 1968, based on ‘‘six
somewhat macerated, extended specimens’’ from the intestine
of a ‘‘Serranidae’’, ‘‘probably Epinephelus’’, from off New
Caledonia [9], is narrower, with a larger rhynchus, longer previtelline distance, longer pre-uterine distance, longer pre-mouth
distance, shorter post-testicular distance, shorter cirrus-sac reach
and greater egg-size. The host identifications in Durio & Manter
[9] are often rather vague, and this case is no exception. In
this particular case, Durio & Manter’s ‘‘Epinephelus’’ could
be any Serranidae, including any species of Cephalopholis,
Plectropomus, Variola and even Epinephelus.
Neidhartia epinepheli Bott & Cribb, 2009, based on two
specimens from the intestine of the highfin grouper Epinephelus
maculatus (Bloch) (Serranidae) off Lizard Island on the Great
Barrier Reef [2], has a relatively larger rhynchus and a longer
previtelline distance. In N. epinepheli the uterus reaches anterior
min.
8.37
0
10.9
0
24.2
30.7
26.1
39.1
37.6
35.3
4.10
max.
12.4
9.70
12.0
0
31.6
57.0
35.1
56.1
52.7
45.5
6.86
7
mean
10.5
3.27
11.4
0
28.4
39.1
29.0
46.7
43.8
39.5
5.96
min.
8.84
0
9.37
0
20.6
29.6
14.9
27.7
30.1
27.2
1.97
max.
12.5
1.96
13.3
0
26.8
49.7
24.0
42.1
34.5
33.4
5.45
6
mean
10.8
0.79
11.1
0
22.4
36.0
18.6
35.5
32.0
29.4
3.47
min.
10.9
2.58
11.7
0
19.1
28.5
9.2
33.9
28.3
17.8
1.92
max.
18.0
6.33
16.0
0
27.4
44.4
16.9
51.0
38.9
37.4
4.52
mean
13.3
4.33
13.6
0
23.3
35.8
12.1
43.0
32.7
25.6
3.13
to the vitellarium. Other probably differences are the pre-mouth
distance, post-testicular region and cirrus-sac reach.
Neidhartia ghardagae Nagaty, 1937, based on 16 specimens from a ‘‘Serranus sp.’’ from off Ghardaga in the Red
Sea [29], has a relative larger rhynchus, longer previtelline
distance and longer pre-mouth distance and probably a shorter
post-testicular region and a shorter cirrus-sac reach.
Neidhartia haywardi Bott, Miller & Cribb, 2013, based on
10 specimens and ITS2 sequence from Plectropomus
leopardus, P. laevis and the spotted coralgrouper P. maculatus
(Bloch), from Heron and Lizard Islands on the Great Barrier
Reef [3] has a bigger rhynchus, longer previtelline distance
and shorter post-testicular distance.
Neidhartia longivesicula (Bilqees, Khalil, Khan, Perveen &
Muti-ur-Rehman, 2009) n. comb. (Syn. Prosorhynchus longivesicula) is based on seven specimens from the yellow-tail scad
Atule mate (Cuvier) (as Caranx affinus Rüppell) (Carangidae)
off Karachi in the northern Arabian Sea [1]. The ovary is
described as ‘‘posterior to anterior testis and ventro-lateral
to posterior testis’’, indicating that the species belongs to
Neidhartia. This species differs from N. lochepintade particularly in the more anterior mouth and greater body-size.
Neidhartia mcintoshi Velasquez, 1959, based on two
mature and four immature specimens from the muscle, stomach
and intestine of the duskytail grouper Epinephelus bleekeri
(Vaillant) (Serranidae) off Malabon, Rizal, Luzon Island, Philippines [48], has a longer pre-uterine extent, and probably a relatively larger rhynchus, shorter pre-mouth distance and shorter
cirrus-sac reach. In connection with unusual sites of infection
given, Velasquez [48] stated that the ‘‘present species occurs
as metacercaria and adult in the same host, showing evidence
that infection of one fish is brought about possibly through
the eating of the smaller fish by the larger’’.
Neidhartia microrhyncha Chauhan, 1943, based on five
non-ovigerous specimens from the alimentary canal of the
Indian spiny turbot Psettodes erumei (Bloch & Schneider)
(Psettodidae) off Bombay (now Mumbai), India [7], is narrower
and has a shorter cirrus-sac reach. It is reported to grow much
bigger.
6
new data
new data
[3]
[3]
new data
new data
[3]
[9]
[3]
[27]
[1]
[7]
[45]
[27]
[25]
[39]
26–32 · 13–19
22–25 · 11–15
20–23 · 11–13
28–33 · 16–20
23–31 · 15–20
34–39 · 16–19
38–44 · 22–26
33–38 · 17–22
25–26 · 13
31 · 20
29–31 · 11–12
none
26–34 · 17–26
19–29 · 15–19
30–32 · 21–22
21–24 · 12–13
41–59
38–53
31
31
30–35
28–39
30
17
36
29–33
44
19
31
36
38
31
30–40
26–35
18
21
15–24
9–17
18
15
25
21–23
45
33
29
21
30
33
Neidhartia lochepintade n. sp.
Neidhartia haywardi
Neidhartia haywardi
Neidhartia plectropomi
Neidhartia tyleri ex P. leopardus
Neidhartia tyleri ex P. laevis
Neidhartia tyleri
Neidhartia coronata
Neidhartia epinepheli
Neidhartia ghardagae
Neidhartia longivesicula
Neidhartia microrhyncha
Neidhartia mcintoshi
Neidhartia neidharti
Neidhartia polydactyli
Pseudoprosorhynchus hainansis
1,067–1,252
658–744
731–1,073
700–1,245
1,031–1,663
1,204–1,512
1,203–1,544
1,392–1,949
880–896
561–908
1,910–2,120
1,390–2,930
820–1,000
842–2,112
1,415
2,552
30–38
20–28
23–28
11–26
19–32
19–29
16–22
14–15
25
24–27
33–36
14–17
26–30
11–29
16
21
11–13
20–24
18–26
17–24
15–21
14–19
14–20
17
18–19
21–37
15–16
8–10
14–21
20–27
16
9
16–23
28–34
?
?
29–51
26–44
42
47
35
34–40
12
27
23
24
41
26
23–29
23–30
31
28
21–36
22–38
30
52
14
29–33
20
?
56
21
28
17
Premouth
distance
%
53–60
63–64
66
67
66–77
74–84
76
81
65
77
34
59
48
74
78
57
Pre-uterine
distance %
Previtelline
distance %
Rhynchus
length %
Width
%
Length
lm
Species
Table 2. Comparisons of Neidhartia spp., blue shading shows major distinctions, green shading shows minor distinctions.
Post-testicular
distance %
Cirrussac
reach %
Egg-size
lm
Source
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Neidhartia neidharti Nagaty, 1937, based on eight specimens from Serranus sp. locally called ‘‘Nagil’’, from off Ghardaga in the Red Sea [29], has a relatively larger rhynchus and
longer pre-mouth distance and probably a shorter post-testicular
region and a shorter cirrus-sac reach. The vitellarium overlaps
the rhynchus. According to Froese & Pauly [15] the common
name ‘‘Nagil’’ refers to either the squaretail coralgrouper
Plectropomus areolatus (Rüppell, 1830) or the roving coralgrouper Plectropomus pessuliferus (Fowler, 1904) (Serranidae).
Neidhartia plectropomi Bott, Miller & Cribb, 2013 based
on 10 specimens and ITS2 sequence from Plectropomus
leopardus and P. laevis from Heron and Lizard Islands on the
Great Barrier Reef [3] has a bigger rhynchus and longer previtelline distance.
Neidhartia polydactyli Manter, 1953, based on a single
specimen from the intestine of the striped threadfin Polydactylus plebeius (Broussonet) (Polynemidae) off Suva, Fiji [26], has
a relatively larger rhynchus and longer previtelline and premouth distances.
Neidhartia tyleri Bott, Miller & Cribb, 2013 based on 10
specimens and ITS2 sequence from the Plectropomus leopardus, P. laevis and P. maculatus, from Heron and Lizard Islands
on the Great Barrier Reef [3] is narrower, with longer previtelline and pre-mouth distances, shorter post-testicular distance
and cirrus-sac reach, and larger eggs.
Pseudoprosorhynchus hainansis Shen, 1990, based on two
specimens from the intestine of the Plectropomus leopardus off
Hainan Island, southern China [41] is similar to Neidhartia
lochepintade (and indeed the whole genus) in that the ovary
is between the testes, but the rhynchus is disc-like, and the
worm is long and narrow. It also appears to have a short cirrus-sac reach and smaller eggs.
These data, and the record from this deep-water serranid,
indicate to us that the specimens described here belong to a
new species. Prosorhynchus epinepheli Yamaguti, 1939 has
been reported twice from this host, from off Tuticorin, India
[18] and from the Arabian Gulf [40]. The illustrations in both
papers show that the ovary lies partly anterior to and partly
overlapping the anterior testis, and thus do not indicate that
the worm in question is a Neidhartia. The Indian record [18]
is from several host species and it is not stated from which
the illustrated worm was collected. E. chlorostigma has also
been listed as a host for unnamed Prosorhynchus spp. in the
Arabian Gulf [11, 39].
As discussed below, the generic status of Prosorhynchus
epinepheli and P. longisaccatus is ambiguous as often the ovary
does not lie distinctly anteriorly to the testes, suggesting that
they may be Neidhartia spp. Comparison of data in Tables 2
and 6 indicates that the rhynchus is relatively much larger in
P. epinepheli and P. longisaccatus. The pre-uterine
distance tends to be larger in P. longisaccatus, but overlaps
considerably.
Neidhartia haywardi Bott, Miller & Cribb, 2013
(Figure 3)
urn:lsid:zoobank.org:act:47F33650-B6E4-414C-9F58-320
F4F05E504
7
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 3. Measurements and ratios of Prosorhynchus spp. from Cephalopholis spp. % refers to % of body-length.
Species
Prosorhynchus robertsthomsoni
Prosorhynchus longisaccatus
Cephalopholis argus
Cephalopholis urodeta
7
1
Host
n
Length
Width
Previtelline distance
Precaecal distance
Pre-uterine distance
Pre-mouth distance
Pretesticular distance
Pre-ovarian distance
Rhynchus length
Rhynchus width
Rhynchus to vitellarium distance
Rhynchus to uterus distance
Rhynchus to caecum distance
Long vitelline field
Short vitelline field
Caecum length
Caecum width
Pharynx length
Pharynx width
Ovary length
Ovary width
Distance between ovary and anterior testis
Anterior testis length
Anterior testis width
Distance between testes
Posterior testis length
Posterior testis width
Posterior testis to cirrus-sac
Cirrus-sac length
Cirrus-sac width
Seminal vesicle length
Seminal vesicle width
Pars prostatica length
Pars prostatica width
Post-testicular distance
Post-vitelline distance
Cirrus-sac reach
Post-ovarian distance
Post-genital pore distance
Egg length
Egg width
Width %
Previtelline distance %
Precaecal distance %
Pre-uterine distance %
Pre-mouth distance %
Pretesticular distance %
Pre-ovarian distance %
Rhynchus length %
Rhynchus width % rhynchus length
Longest vitelline field %
Caecal length %
Ovary length %
Anterior testis length %
Distance between testes %
Posterior testis %
min.
1,088
251
192
345
117
504
390
467
112
97
82
79
231
247
181
84
68
42
44
83
75
0
86
81
0
75
61
0
308
96
134
37
346
59
350
588
428
440
53
32
16
22.5
17.7
31.6
10.8
44.8
35.9
42.9
9.95
82.8
19.8
6.7
7.12
7.23
0
6.77
max.
1,256
291
281
474
298
577
654
676
144
145
144
170
475
319
264
120
114
53
55
98
99
0
100
109
89
107
109
0
417
141
185
59
523
128
460
713
550
604
113
38
20
24.3
23.3
38.0
25.7
47.5
52.5
56.0
12.4
106
26.3
10.4
8.51
8.84
8.14
9.79
mean
1,171
270
238
399
245
540
549
559
130
122
108
131
309
284
236
103
96
48
51
90
87
0
93
96
34
91
88
0
368
119
152
47
435
95
405
653
505
512
74
34
18
23.1
20.3
34.1
20.9
46.0
46.7
47.7
11.1
94.2
24.3
8.9
7.72
7.94
2.96
7.81
836
333
192
261
289
458
326
341
223
166
0
58
36
288
228
138
125
67
75
81
62
0
90
81
30
82
96
0
340
161
?
?
?
?
375
406
427
421
58
30
20
39.8
23.0
31.3
34.5
54.8
39.0
40.8
26.7
74.4
34.4
16.4
9.66
10.8
3.59
9.85
(continued on next page)
8
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 3. (Continued)
Species
Prosorhynchus robertsthomsoni
Prosorhynchus longisaccatus
Cephalopholis argus
Cephalopholis urodeta
7
1
Host
n
Posterior testis to cirrus-sac %
Cirrus-sac length %
Seminal vesicle length % cirrus-sac length
Post-testicular distance %
Post-vitelline distance %
Cirrus-sac reach %
Post-ovarian distance %
Post-genital pore distance %
min.
0
27.7
35.0
30.9
53.0
38.6
36.4
4.56
Host: Plectropomus leopardus (Lacepède) (Perciformes:
Serranidae), leopard coralgrouper.
Site: digestive tract
Localities: Grande Rade, Nouméa 22150 S 16624E, 23/10/
2007 and 24/10/2007; Between Larégnière and Récif Crouy,
22200 702S, 166190 295E, 05/05/2008.
Prevalence: 57% (4 of 7).
Vouchers: MNHN JNC2333B, JNC2333C, JNC2334,
JNC2513; BMNH 2013.11.18.5-6.
Description
Based on five whole-mount preparations. Measurements
and ratios in Table 1. Body widest at about mid-body (Figure 3).
Tegument spinous; spines squamous, tiny, reach to posterior
extremity. Rhynchus broad, conical or bluntly conical. Mouth
just posterior to ovary, well into post-equatorial half of body.
Pharynx small, globular. Caecum oval, directed anteriorly.
Testes 2, irregularly oval, oblique, in about mid-body, usually well separated. Cirrus-sac elongate, more-or-less parallel
sided, reaching to or almost to anterior testis, anteriorly to pharynx. Seminal vesicle elongate-oval, in proximal cirrus-sac. Pars
prostatica long, in two distinct parts; proximal part narrow,
coiled over seminal vesicle; distal part, wider, straighter,
surrounded by dense layer of gland-cells, lining of filaments
in chevron arrangement. Ejaculatory duct narrow, opening on
large, complex genital lobe inside genital atrium. Genital
atrium large. Genital pore distinctly separated from posterior
extremity.
Ovary oval, intertesticular, overlapping testes. Mehlis’
gland overlapping ovary and posterior testis. Details of proximal female system obscured by eggs. Uterus reaches anteriorly
to vitelline fields, occasionally to level of vitellarium, fills much
of available space to level of genital pore. Eggs numerous,
tanned, operculate. Metraterm not detected, obscured by eggs.
Vitellarium consists of two lateral fields of 12–15 follicles,
more or less symmetrical, but with one field slightly longer than
other, anterior extremity posterior to rhynchus and anterior
extent of uterus, reaches anterior to caecum and gonads; posterior extremity at about level of ovary.
Excretory pore terminal; anterior extent of vesicle obscured
by eggs.
max.
0
33.7
44.5
39.6
58.1
48.0
48.8
10.4
mean
0
31.4
39.0
34.7
55.8
43.1
43.7
6.28
0
40.6
?
44.9
48.6
51.0
50.3
6.99
Discussion
This form appears to be N. haywardi or N. plectropomi differing only in the previtelline distance, as calculated from the
illustration [3, Figure 3], but it should be noted that in both species Bott et al. [3] found that the extent of the vitellarium was
obscured by the uterus. N. haywardi and N. plectropomi are sister species according to the molecular study of Bott et al. [3].
We consider our specimens to be P. haywardi as the egg-sizes
more nearly coincide (Table 2), but the cirrus-sac reach of our
specimens tends to be greater than is apparent in either species.
Both P. haywardi and P. plectropomi are reported from P. leopardus and P. laevis, and from Heron and Lizard Islands on the
Great Barrier Reef.
The features distinguishing this species from its congeners
can be seen in Table 2, and two further species are not easily
distinguished, namely N. neidharti Nagaty, 1937 and N. epinepheli Bott & Cribb, 2009.
N. neidharti was first reported in Serranus sp. locally
known as ‘‘Nagil’’ from the Red Sea [29]. According to Froese
& Pauly [15] this common name refers to the squaretail coralgrouper Plectropomus areolatus (Rüppell) or the roving coralgrouper P. pessuliferus (Fowler). It seems clear, therefore, that it
is a parasite of Plectropomus. Chauhan [7] recorded, but did not
describe, this species in Belone sp. (Beloniformes: Belonidae)
from Mumbai (Bombay), India. As unlikely as this combination
of hosts is, its putative hosts associations become even more
puzzling when the record by Maurya et al. [27] in the freshwater long-whiskered catfish Sperata (= Mystus) aor (Hamilton)
(Siluriformes: Bagridae) from Uttar Pradesh, India is considered. We are discounting the Indian records of this species.
N. neidharti apparently grows to a much greater size than
N. plectropomi, although there is room for confusion. In
Nagaty’s [29] description (p. 119) the length range is given
as 561–908, whereas in the table of measurements (p. 166)
the length is given as 842–2,112 (vs. 658–744 (715) for
P. haywardi). This confusion also applies to width where, using
the data from the description, the range is 24–27% and in
the table it is 11–29% of body-length (vs. 20–24%).
The body-width in Nagaty’s Figure 56 is about 24% of the
body-length. The pre-mouth distance may be greater than in
N. haywardi.
Reference
new data
[2]
[47]
[2]
[9]
[27]
[44]
32–38 · 16–20
29–30 · 16
40 · 26
32–33 · 16
24–29 · 15–21
25–29 · 17–21
19–25 · 14–17
45–47
48
46
43
49
53–62
47
18–23
27
21
20
20
30–34
22
9
Neidhartia epinepheli. Bott & Cribb stated that it ‘‘It bears a
superficial resemblance to the type-species, N. neidharti
Nagaty, 1937, in that its uterus extends past the posterior margin of the rhynchus. N. epinepheli differs by having a caecum
that does not extend into the anterior third of the body and the
eggs are smaller, 25–26 · 12–13, compared with 30 · 15 for
N. neidharti (see Nagaty, 1937)’’. The confusion in the egg-size
as given by Nagaty [29] for N. neidharti, in that he gives the
egg-size as 30 · 15 in the text, but 19–29 · 15–19 in the table
may well invalidate one of Bott & Cribb’s [2] distinctions. The
other distinction is rather minor and it may be found that these
species are synonymous. The pre-uterine distance is
shorter than in N. haywardi in that the uterus overlaps the
rhynchus.
Neidhartia tyleri Bott, Miller & Cribb, 2013 (Figures 4, 5)
urn:lsid:zoobank.org:act:E131C73F-7D32-4B80-8656-EB
8411FAAE8B
Hosts: Plectropomus leopardus (Lacepède) (Perciformes:
Serranidae), leopard coralgrouper; Plectropomus laevis
(Lacepède), blacksaddled coralgrouper.
Site: digestive tract
Localities: (P. leopardus & P. laevis) Off Ouano
(21490 430S, 166440 278E, 25/10/2007), P. leopardus Near
Récif Toombo (22340 107S, 166280 816E, 30/09/2009).
Prevalences: P. leopardus, 29% (2 of 7), P. laevis, 50%
(1 of 2).
Vouchers: (P. leopardus) MNHN JNC2340, JNC 3060B;
BMNH 2013.11.18.2-3; (P. laevis) JNC2339; BMNH
2013.11.18.4.
1,088–1,256
1,072–1,408
1,700
1,104–1,424
1,027–2,245
816–1,826
1,500–1,800
23–24
18–23
29
19–25
22
30–32
24–25
10–12
10–11
9
15
12–18
15–16
7–9
Description
P. robertsthomsoni Bott & Cribb, 2009
P. robertsthomsoni Bott & Cribb, 2009
P. aguayoi Vigueras, 1955
P. jexi Bott & Cribb, 2009
P. serrani Durio & Manter, 1968
P. serrani Durio & Manter, 1968
P. tsengi Tsin, 1933
Previtellarium
%
Rhynchus
L%
Width
%
Length
Species
Table 4. Comparisons of Prosorhynchus robertsthomsoni, green shading shows minor distinctions.
PreUterine
%
10–26
24
18
32
17
31
19
Mouth
Posttesticular
%
31–40
31
44
41
27
24–31
34
Cirrussac
reach %
39–48
35
36
37
33
31–36
41
Eggs
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Based on seven whole-mount preparations from
P. leopardus and six from P. laevis. Measurements and ratios
in Table 1. Body fusiform, widest in posterior third (Figures
4, 5). Tegument spinous; spines squamous, tiny, reach to posterior extremity. Rhynchus broad, with narrow conical posterior
extension. Mouth at about level of ovary or just posterior, well
into post-equatorial half of body. Pharynx small, globular. Caecum elongate-oval, directed anteriorly.
Testes 2, irregularly oval, oblique to tandem, in about
mid-body, slightly separated or not. Cirrus-sac elongate,
more-or-less parallel sided, reaching anterior testis, anteriorly
to pharynx. Seminal vesicle elongate-oval, in proximal cirrussac. Pars prostatica long, in two distinct parts; proximal part
narrow, coiled over seminal vesicle; distal part, wider, straighter, surrounded by dense layer of gland-cells, lining of filaments
in chevron arrangement. Ejaculatory duct narrow, opening on
large, complex genital lobe inside genital atrium. Genital atrium
large. Genital pore distinctly separated from posterior extremity.
Ovary oval, intertesticular, overlapping testes. Mehlis’
gland overlapping ovary and posterior testis. Details of proximal female system obscured by eggs. Uterus not reaching
anteriorly to vitelline fields, fills much of available space to
level of genital pore. Eggs numerous, tanned, operculate. Metraterm not detected, obscured by eggs. Vitellarium consists
of two lateral fields of follicles, more or less symmetrical, but
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R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
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10
Figure 7–12. 7: Prosorhynchus longisaccatus Durio & Manter, 1968 ex Cephalopholis urodeta. Ventral view, uterus in outline. 8:
Prosorhynchus longisaccatus Durio & Manter, 1968 ex Epinephelus areolatus. Ventral view, uterus in outline. 9: Prosorhynchus longisaccatus
Durio & Manter, 1968 ex Epinephelus cyanopodus. Ventral view, uterus in outline. 10: Prosorhynchus longisaccatus Durio & Manter, 1968 ex
Epinephelus maculatus. Ventral view, uterus in outline. 11: Prosorhynchus serrani Durio & Manter, 1968 ex Variola albimarginata. Ventral
view, uterus in outline. 12: Prosorhynchus serrani Durio & Manter, 1968 ex Variola louti. Ventral view, uterus in outline. Scale bars: 500 lm.
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11
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 5. Measurements and ratios of Prosorhynchus longisaccatus from Epinephelus spp. % refers to % of body-length.
Host
Epinephelus areolatus
16
n
Length
Width
Previtelline distance
Precaecal distance
Pre-uterine distance
Pre-mouth distance
Pretesticular distance
Pre-ovarian distance
Rhynchus length
Rhynchus width
Rhynchus to vitellarium distance
Rhynchus to uterus distance
Rhynchus to caecum distance
Long vitelline field
Short vitelline field
Caecum length
Caecum width
Pharynx length
Pharynx width
Ovary length
Ovary width
Distance between ovary and anterior testis
Anterior testis length
Anterior testis width
Distance between testes
Posterior testis length
Posterior testis width
Posterior testis to cirrus-sac
Cirrus-sac length
Cirrus-sac width
Seminal vesicle length
Seminal vesicle width
Pars prostatica length
Pars prostatica width
Post-testicular distance
Post-vitelline distance
Cirrus-sac reach
Post-ovarian distance
Post-genital pore distance
Egg length
Egg width
Width %
Previtelline distance %
Precaecal distance %
Pre-uterine distance %
Pre-mouth distance %
Pretesticular distance %
Pre-ovarian distance %
Rhynchus length %
Rhynchus width % rhynchus length
Longest vitelline field %
Caecal length %
Ovary length %
Anterior testis length %
Distance between testes %
Posterior testis %
Posterior testis to cirrus-sac %
Epinephelus cyanopodus
min
639
185
142
194
177
359
250
299
146
135
0
0
0
147
99
101
65
44
49
54
34
0
59
51
0
58
48
0
206
84
83
27
243
43
250
341
347
269
16
26
17
20.9
14.2
23.6
19.4
39.9
27.3
32.6
17.8
70.3
16.7
9.81
6.12
7.28
0
7.37
0
max
1,203
382
239
347
348
499
464
467
262
300
26
148
148
337
280
164
134
72
78
112
124
66
147
133
95
141
149
23
439
178
150
54
655
83
596
716
668
690
115
36
21
41.5
25.4
34.1
38.2
56.1
47.3
50.7
24.8
114
28.3
21.8
11.6
16.0
8.63
15.4
2.28
Epinephelus maculatus
13
mean
887
276
176
255
260
433
339
367
192
182
4
64
62
218
192
131
100
56
58
77
69
6
92
82
24
92
87
1
284
108
117
40
348
63
390
504
455
442
67
30
18
31.6
20.2
29.0
29.4
49.6
38.9
42.3
21.9
94.3
24.6
15.3
8.79
10.3
2.50
10.2
0.14
min
920
298
167
263
267
502
334
308
209
178
0
0
35
242
146
94
77
56
58
66
65
0
85
78
0
84
73
0
294
112
111
40
401
61
410
513
496
484
59
24
14
25.0
14.7
26.2
21.8
44.0
30.5
33.5
18.4
71.8
19.6
9.44
6.02
7.65
0
7.62
0
max
1,403
471
293
420
441
621
548
590
347
307
0
148
129
355
309
177
157
86
81
122
111
0
149
121
107
156
135
0
483
188
211
92
401
81
710
848
747
744
118
33
23
43.1
23.8
34.1
40.1
54.7
46.3
48.0
26.5
119
32.2
14.8
11.1
12.1
10.8
12.2
0
22
mean
1,134
359
212
342
322
567
441
460
263
245
0
63
81
282
236
142
104
72
75
99
92
0
118
97
38
113
114
0
377
138
161
66
401
69
518
659
587
574
86
27
18
32.0
18.7
30.1
28.6
49.4
39.0
40.5
23.2
94.5
25.1
12.5
8.73
10.4
3.42
9.90
0
min
784
191
105
225
184
367
272
295
159
131
0
0
2
131
108
88
66
49
46
54
41
0
58
42
0
50
42
0
240
82
72
21
275
28
350
435
435
408
36
24
17
23.0
11.4
23.9
20.0
41.4
29.6
31.7
17.4
60.4
16.1
10.2
6.46
6.83
0
5.67
0
max
1,160
386
197
348
339
497
402
416
244
223
1
291
341
292
283
154
133
78
88
102
109
16
117
117
179
118
106
59
461
165
155
74
766
91
583
682
653
705
98
40
25
45.8
21.6
37.8
36.9
58.2
44.4
46.5
26.8
103.1
29.1
15.4
11.5
12.1
19.4
11.6
6.50
mean
937
297
167
266
285
449
339
338
204
170
0
91
81
215
194
121
94
62
65
76
68
1
86
75
43
85
76
5
331
127
115
42
424
57
436
556
518
521
75
33
21
31.6
17.9
28.5
30.5
47.7
36.4
36.2
21.9
83.6
22.9
12.9
8.11
9.11
4.53
8.98
0.49
(continued on next page)
12
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 5. (Continued)
Host
Epinephelus areolatus
16
n
Cirrus-sac length %
Seminal vesicle length % of cirrus-sac length
Post-testicular distance %
Post-vitelline distance %
Cirrus-sac reach %
Post-ovarian distance %
Post-genital pore distance %
Epinephelus cyanopodus
min
25.4
38.8
37.7
50.9
39.6
40.8
2.42
max
36.9
56.2
55.1
66.3
61.7
58.6
10.6
with one field slightly longer than other, anterior extremity distinctly posterior to rhynchus and anterior to uterus, always
reaches anterior to caecum and gonads; posterior extremity at
or just posterior to level of ovary.
Excretory pore terminal; anterior extent of vesicle obscured
by eggs.
Epinephelus maculatus
13
mean
32.2
44.8
43.7
56.4
51.9
48.9
7.65
min
26.5
37.8
36.9
50.7
45.1
45.7
5.62
max
43.0
43.7
53.1
64.0
59.6
56.7
10.5
22
mean
33.2
40.7
45.8
57.9
51.7
50.6
7.66
min
26.2
20.5
40.1
52.2
43.8
46.7
4.29
max
43.6
46.5
54.3
64.5
63.7
61.2
10.5
mean
35.4
35.4
47.3
59.4
55.5
55.4
7.96
Locality: Near Récif Toombo (22310 3000 S, 166260 4000 E,
03/11/2006).
Prevalence: 50% (1 of 2).
Vouchers: MNHN JNC 2110; BMNH 2013.11.18.25.
Discussion
Discussion
We have identified the larger Neidhartia specimens as
belonging to N. tyleri. Most morphological characters are similar (Table 2), but the eggs in our specimens from P. leopardus
(the type-host of N. tyleri) are distinctly smaller than those
described for this species [3] and our specimens from P. laevis.
This species is readily distinguished from most described species (Table 2). N. neidharti is not distinguishable from the specimens from P. laevis in major features of the visual key and
differs from the P. leopardus specimens only in rhynchus length
(Table 2). This feature probably distinguishes this form from
N. neidharti as the P. laevis specimens do not overlap in this
feature. Comparison with N. neidharti as described by Nagaty
[29] is problematical as the measurements given in the description and table do not coincide, but our specimens are very distinct from the illustrated specimen [28, Figure 56] in shape
(relatively more elongate, although the measurements in the
table do not bear this out), the previtelline distance and pre-uterine distance.
N. coronata Durio & Manter, 1968, described from ‘‘Serranidae, probably Epinephelus sp.’’ from off New Caledonia [9],
differs from our specimens in the visual key in the pre-uterine
distance and cirrus-sac reach. It should be borne in mind, however, that Durio & Manter [9] stated that their description was
‘‘based on six somewhat macerated, extended specimens’’. The
previtelline distance may also be a distinguishing feature.
Genus Prosorhynchus Odhner, 1905
urn:lsid:zoobank.org:act:21111289-7672-4028-830DA37199B68E26
Prosorhynchus robertsthomsoni Bott & Cribb, 2009
(Figure 6)
urn:lsid:zoobank.org:act:0EEE6ED7-01CE-45A0-A2B9-2
7F32EBC64CC
Host: Cephalopholis argus Bloch & Schneider (Perciformes: Serranidae), peacock hind.
Site: digestive tract
Measurements and ratios are given in Table 3. This species
is known only from Cephalopholis argus, the coral hind
Cephalopholis miniata (Forsskål) and the bluespotted hind
C. cyanostigma (Valenciennes) from off Heron and Lizard
Islands on the Great Barrier Reef [2, 3]. Using the visual key
our specimens align with four species, in addition to
P. robertsthomsoni. Distinctions are tabulated in Table 4.
Prosorhynchus aguayoi Vigueras, 1955 from the greater
soapfish Rypticus saponaceus (Bloch & Schneider) (Serranidae) from off Cuba, Curaçao and Jamaica [30, 31, 50] is a
very similar species to P. robertsthomsoni but is probably
wider and more fusiform, with a longer post-testicular region.
The vitellarium reaches the testes in P. aguayoi and the cirrussac does not.
Prosorhynchus jexi (syn: P. epinepheli of Durio &Manter
(1968)) from the longfin grouper Epinephelus quoyanus (Valenciennes) (Serranidae) from the Great Barrier Reef [2, 9] differs
from P. robertsthomsoni in the more restricted uterus. Bott &
Cribb [2] considered that the reach of the uterus anterior to
the vitellarium is a distinctive feature of P. robertsthomsoni
but our observations indicate that this does not always occur
(Figure 6). The cirrus-sac does not reach the testes in P. jexi.
Prosorhynchus serrani Durio & Manter, 1968 (syn: Prosorhynchus crucibulus of Nagaty (1937)) from the yellow-edged
lyretail Variola louti (Forsskål) (Serranidae) from the Red Sea
and off New Caledonia [9, 29] is very similar to P. robertsthomsoni but apparently has a distinctly different shaped rhynchus,
in that it has a distinct narrow elongate posterior extension in
contrast to the blunt rounded posterior of the P. robertsthomsoni
rhynchus. It may be that the vitellarium reaches slightly more
posteriorly in P. serrani in that the follicles extend just posterior
to the pharynx, rather than just to the pharynx (see below).
Prosorhynchus tsengi Tsin, 1933 is a parasite of the bartail
flathead Platycephalus indicus (Linnaeus) (Platycephalidae) off
China [42, 47]. Bray & Palm [6] pointed out that the ‘‘original
illustration of P. tsengi by Tsin [47, Figure 8] shows a lobed
rhynchus, apparently with an aperture, and a straight pars prostatica, indicating that the species may in fact belong to the genus
new data
new data
new data
new data
[9]
[42]
[24]
[5]
[51]
[2]
20
17–21
14–23
17–25
17–32
16–23
14–22
18–20
18–21
15–16
·
·
·
·
·
·
·
·
·
·
30
26–36
24–33
24–40
30–33
30–32
27–34
31–36
28–30
29–30
23
14–25
15–24
11–22
21
14
22–27
23–25
14
26
40
21–41
25–43
23–46
29–30
29–40
18–28
27–33
40–43
15–22
P. longisaccatus ex C. urodeta
P. longisaccatus ex E. areolatus
P. longisaccatus ex E. cyanopodus
P. longisaccatus ex E. maculatus
P. longisaccatus Durio & Manter, 1968
P. longisaccatus Durio & Manter, 1968
P. atlanticus Manter, 1940
P. atlanticus Manter, 1940
P. epinepheli Yamaguti, 1939
P. lafii Bott & Cribb, 2009
863
639-1,203
920–1,403
784–1,160
1,096–1,201
1,888–2,088
705–1,677
996–1,047
1,250–2,350
1,040–1,184
27
18–25
18–27
17–27
24
14–17
17–24
24–26
14–19
18
Previtellarium
%
Rhynchus
L%
Width
%
Length
Table 6. Comparisons of Prosorhynchus longisaccatus, green shading shows minor distinctions.
PreUterine
%
35
19–38
22–40
20–37
33
39
41–52
36–48
22
34
Premouth
%
55
40–56
44–55
41–58
52
53
45–47
45–48
54
44
Posttesticular
%
45
38–55
37–53
40–54
43
25
39–45
38–44
41
49
Cirrussac
reach %
51
40–62
45–60
44–64
48
27
36–39
36–42
41
47
Eggs
Reference
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
13
Rhipidocotyle’’. In addition the rhynchus and eggs appear
slightly smaller than in P. robertsthomsoni.
Prosorhynchus longisaccatus Durio & Manter, 1968
(Figures 7–10)
urn:lsid:zoobank.org:act:FAB66691-C264-4A99-9585-FF
7BEDC41316
Hosts: Cephalopholis urodeta (Forster), Serranidae, darkfin
hind; Epinephelus areolatus (Forsskål), Serranidae, areolate
grouper; Epinephelus cyanopodus (Richardson), Serranidae,
speckled blue grouper; Epinephelus maculatus (Bloch), Serranidae, highfin grouper.
Site: Intestine, pyloric caeca, stomach, digestive tract.
Locality : C. urodeta, Off Récif Kué, New Caledonia (07/
10/2008); E. areolatus, Off Pointe Bovis (22140 S, 166200 E,
21/10/2008); Nouméa Fish Market (15/06/2007); E. cyanopodus, Passe de Dumbéa (22200 0000 S, 166150 0000 E, 25/11/2005
and 05/10/2006), Passe de Boulari (22300 00S, 166240 0000 E,
05/10/2006), Near Îlot Mato (22330 E, 166470 E, 05/08/
2007), Baie Maa (22120 762S, 166190 924E, 13/11/2007), Baie
des Citrons, Nouméa (22180 S, 166260 E, 31/03/2009);
E. maculatus, Phare Amédée (22270 S, 166260 E, 20/06/
2006), Off Ever Prosperity, external slope, depth 60 m;
(22270 S, 166210 E, 22/08/2006), Off Ever Prosperity, external
slope, depth 60–80 m (22270 S, 166210 E, 17/04/2007), Récif
Kué, External slope (22340 892S, 166290 673E, 19/06/2007),
Off Récif Kué (22360 S, 166310 E, 07/10/2008), Shallow, Interior Lagoon near Récif Toombo (22320 583S, 166280 978E, 05/
11/2008), Shallow, Interior Lagoon near Récif Toombo
(22320 536S, 166290 069E, 20/11/2008), Baie des Citrons,
Nouméa (22180 S, 166260 E, 09/04/2009), Interior Lagoon near
Récif Toombo (22320 536S, 166290 069E, 30/04/2009).
Prevalence: C. urodeta, 33% (1 of 3); E. areolatus, 75% (3 of
4); E. cyanopodus, 87% (7 of 8); E. maculatus, 61% (16 of 26).
Voucher specimens: C. urodeta, MNHN JNC 2683;
E. areolatus, JNC2690, JNC2691, JNC2175; BMNH
2013.11.18.15-16; E. cyanopodus, JNC2270a, JNC1659,
JNC1998B, JNC1998C, JNC2000A, JNC2000B, JNC2270,
JNC2395, JNC2891A, JNC2891B; BMNH 2006.4.27.1-10,
2013.11.18.22-23; E. maculatus, JNC1874, JNC1927,
JNC2157D, JNC2187A, JNC 2680, JNC 2754, JNC 2759,
JNC2894B, JNC2929, JNC3031, JNC3052, JNC3053,
JNC3061, JNC3066, JNC3067; BMNH 2007.5.2.39-41,
2013.11.18.17-21.
Description
See Tables 3 and 5 for measurements and ratios based on 52
specimens. Ovary in variable position relative to testes: preovarian distance is greater than the pre-testicular distance in
the specimen from C. urodeta, in 13 of 16 from E. areolatus,
8 of 13 from E. cyanopodus and 10 of 22 from E. maculatus.
Discussion
Our study of this species is based on 52 measured specimens.
In our visual key only four species showed no non-overlapping
features with our specimens, namely P. atlanticus,
14
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 7. Measurements and ratios of Prosorhynchus serrani. % refers to % of body-length.
Host
n
Length
Width
Previtelline distance
Precaecal distance
Pre-uterine distance
Pre-mouth distance
Pretesticular distance
Pre-ovarian distance
Rhynchus length
Rhynchus width
Rhynchus to vitellarium distance
Rhynchus to uterus distance
Rhynchus to caecum distance
Long vitelline field
Short vitelline field
Caecum length
Caecum width
Pharynx length
Pharynx width
Ovary length
Ovary width
Distance between ovary and anterior testis
Anterior testis length
Anterior testis width
Distance between testes
Posterior testis length
Posterior testis width
Posterior testis to cirrus-sac
Cirrus-sac length
Cirrus-sac width
Seminal vesicle length
Seminal vesicle width
Pars prostatica length
Pars prostatica width
Post-testicular distance
Post-vitelline distance
Cirrus-sac reach
Post-ovarian distance
Post-genital pore distance
Egg length
Egg width
Width %
Previtelline distance %
Precaecal distance %
Pre-uterine distance %
Pre-mouth distance %
Pretesticular distance %
Pre-ovarian distance %
Rhynchus length %
Rhynchus width % rhynchus length
Longest vitelline field %
Caecal length %
Ovary length %
Anterior testis length %
Distance between testes %
Posterior testis %
Posterior testis to cirrus-sac %
Variola albimarginata
Variola louti
1
1,322
253
314
395
379
630
628
582
177
141
136
377
218
350
300
177
101
0
0
107
81
0
126
108
65
138
109
0
338
80
0
0
0
0
371
658
444
635
112
24
13
19
24
30
29
48
48
44
13
80
27
13
8
10
5
10
0
10
min.
1,163
169
352
409
443
611
615
571
147
102
158
253
214
193
201
0
60
0
0
77
63
0
84
76
13
72
70
0
222
77
0
0
0
0
263
508
376
493
0
24
15
9.9
26.3
31.8
26.2
52.1
49.4
45.4
7.8
55.1
16.6
0
4.74
5.49
1.12
4.77
0
max.
2,321
311
714
963
919
1,263
1,396
1,301
247
139
505
871
875
637
547
327
121
78
76
134
128
0
178
162
115
168
138
0
359
135
130
69
387
87
577
1,041
579
908
203
33
22
17.5
33.3
43.4
52.1
59.3
65.2
60.7
16.7
79.2
29.7
15.7
9.02
9.73
5.84
12.24
0
mean
1,775
224
524
694
670
985
1,046
976
187
122
337
514
579
448
374
200
84
53
54
108
94
0
126
116
67
128
111
0
294
103
43
17
137
51
404
773
491
676
91
28
18
13.0
29.4
38.7
38.4
55.5
58.5
54.6
11.0
66.2
24.9
11.2
6.23
7.21
3.71
7.39
0
(continued on next page)
15
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 7. (Continued)
Host
Variola albimarginata
n
Cirrus-sac length %
Seminal vesicle length % of cirrus-sac length
Post-testicular distance %
Post-vitelline distance %
Cirrus-sac reach %
Post-ovarian distance %
Post-genital pore distance %
P. longisaccatus, P. epinepheli and P. lafii (Table 6). We consider
that our specimens conform to the species P. longisaccatus, a
species originally reported from a ‘‘leche’’, a serranid from off
New Caledonia [9]. Later, we [5] considered our specimens from
E. cyanopodus as this species and then [19] reported E. areolatus,
and E. maculatus as hosts; all these reports are from New Caledonia. In the latter paper we reported the specimen from C. urodeta
as Prosorhynchus sp.
Prosorhynchus atlanticus Manter, 1940 is an Atlantic species, originally described in the serranids, the black grouper
Mycteroperca bonaci (Poey), the gag Mycteroperca microlepis
(Goode & Bean) and the yellowfin grouper Mycteroperca
venenosa (Linnaeus) off Florida [25]. The ovary is, apparently,
always pre-testicular, the uterus almost never reaches anteriorly
to ovary (only slightly in 1 of 29) and the cirrus-sac reach is
generally smaller (Table 6).
Prosorhynchus epinepheli Yamaguti, 1939 was originally
described from the Hong Kong grouper Epinephelus akaara
(Temminck & Schlegel) (Serranidae) from the Inland Sea of
Japan [52]. The name has been widely used subsequently for
Prosorhynchus specimens from serranids [8], although some
may be misidentified. P. longisaccatus is closely similar to
P. epinepheli. We believe that either P. epinepheli or P. longisaccatus is the most appropriate identification, particularly as
the variable position of the ovary, which is anterior to (and
overlapping) the testes or between the testes in our specimens
is similar to that described for both of these species. Yamaguti
[52] described the position of the ovary in P. epinepheli as
‘‘overlapping right testis or entirely on its dorsal side (in the
type it lies anterodorsal to the right testis, but may be dorsal,
dorsolateral or posterodorsal to it)’’. Durio & Manter [9] found
that in P. longisaccatus the ovary is ‘‘to the right of, or partly
posterior to, anterior testis’’. This sheds some doubt on the generic classification of the worm, the variation of which includes a
characteristic feature of the genus Neidhartia Nagaty, 1937,
which according to Overstreet & Curran [33] is ‘‘Ovary at level
between testes’’. Durio & Manter [9] compared their new species to P. epinepheli, using Yamaguti’s [52] original description
and new material reported from the honeycomb grouper
Epinephelus merra Bloch, 1793 off Heron Island, southern
Great Barrier Reef. It should be noted, however, that Bott &
Cribb [2] examined one of Durio & Manter’s ‘‘P. epinepheli’’
specimens and considered that it belonged to their new species
P. jexi, and that the host was most probably not E. merra, but
the similar species, the longfin grouper Epinephelus quoyanus
(Valenciennes), which is much commoner in the waters around
Variola louti
1
26
0
28
50
34
48
8
10
min.
13.7
0
17.6
37.3
23.7
33.2
0
max.
22.1
40.0
31.7
50.3
39.3
47.7
8.75
mean
17.1
14.8
23.0
43.8
28.6
38.5
4.96
Heron Island (see also [20]). Durio & Manter [9] summarised
the differences between P. epinepheli and P. longisaccatus as
‘‘(1) the uterus does not extend even to midatrial level, whereas
in all specimens of P. epinepheli it extends postatrially; (2) the
rhynchus is wider, and the arrangement of muscles at its anterior edge gives a distinctive appearance’’. The first distinction
probably relies just on the amount of eggs produced and the
second is rather vague and difficult to assess. It seems quite possible that these species are synonymous. There appear to be no
morphological criteria for separating these species and we are
recognising this species based on the locality of collection,
and expect the status of this worm to be elucidated or at least
clarified by molecular studies at present in progress.
Prosorhynchus lafii Bott & Cribb, 2009 from the brownmarbled grouper Epinephelus fuscoguttatus (Forsskål) from
off Heron Island, Great Barrier Reef [2] differs from P. longisaccatus in the vitelline fields which are ‘‘tight lateral clusters
at level of caecum’’. It is probably a more slender worm than
P. longisaccatus (Table 6). The ovary is anterior to, but overlapping, the anterior testis.
Suriano & Martorelli [45] reported P. longisaccatus in the
Remo flounder Oncopterus darwinii Steindachner (Pleuronectidae) off Buenos Aires Province, Argentina. It is larger than previously described for this species, with a shorter post-testicular
region and cirrus-sac reach, and probably a shorter rhynchus
(Table 6). In agreement with Etchegoin et al. [12] we believe
that these worms are not conspecific with the worms from serranids in the Pacific Ocean.
Prosorhynchus serrani Durio & Manter, 1968
(Figures 11, 12)
(syn. Prosorhynchus crucibulus (Rudolphi, 1819) from
Serranus louti of Nagaty (1937))
urn:lsid:zoobank.org:act:1B73DB12-40AC-419C-9986EE6EB612A6AF
Hosts: Variola albimarginata Baissac, Serranidae, whiteedged lyretail; Variola louti (Forsskål), Serranidae, yellowedged lyretail.
Site: digestive tract.
Locality: V. albimarginata, Off Ever Prosperity, external
slope, depth 60m (22270 S, 166210 E, 07/11/2006); V. louti,
Near Passe de Dumbéa (22200 0000 S, 166150 0000 E, 01/03/
2006, 02/03/2006); Off Ever Prosperity, external slope, depth
60m (22270 S, 166210 E, 07/11/2006); Récif Kué, External
slope (22340 892S, 166290 673E,21/06/2007); External Slope
16
21
28
20
31
27
33
30
11
9–12
15
9
10–11
12
16–20
37
52
32
51
24
44
?
38
45
43
56
48
53
63
50
31
41
24
31
25
21
36
20
37
25
35
28
20
31–32 · 16
32–33 · 16
25 · 16
29–30 · 16
27–34 · 19–22
35–40 · 18–20
new data
new data
[9]
[27]
[41]
[17]
[10]
[14]
[4]
[2]
[2]
[2]
[2]
[25]
[46]
· 13
· 15–22
· 15–21
· 17–21
· 13–15
· 11–13
· 19–22
· 21–25
24
24–33
24–29
25–29
19–21
19–21
38–45
32–43
24
26–33
20
30–34
28
42
18–31
13
8–17
12–18
15–16
9–13
6
10–17
19
10–18
22
30–32
17–20
14
17–20
27–30
12
6–7
19–25
13–14
18–23
15–16
23–24
1,322
1,163–2,321
1,027–2,245
816–1,826
693–1,107
2,980
2,000–4,000
1,715–2,245
3,672
1,904–3,360
1,104–1,424
1,392–1,648
1,072–1,408
1,778–2,282
1,760–2,600
P. serrani ex V. albimarginata
P.serrani ex V. louti
P. serrani Durio & Manter, 1968
P. serrani Durio & Manter, 1968
P. attenuatus Siddiqi & Cable, 1960
P. caballeroi Gupta & Ahmad, 1976
P. caudovatus Manter, 1940
P. caudovatus Manter, 1940
P. caudovatus Manter, 1940
P. conorjonesi Bott & Cribb 2009
P. jexi Bott & Cribb, 2009
P. milleri Bott & Cribb, 2009
P. robertsthomsoni Bott & Cribb, 2009
P. thapari Manter, 1953
P. truncatus Verma, 1936
Previtelline
%
Rhynchus
L%
Width
%
Length
Table 8. Comparisons of Prosorhynchus serrani, green shading shows minor distinctions.
PreUterine
%
29
26–52
17
31
27
36
25–46
Premouth
%
48
52–59
49
53–62
55
57
39–44
Posttesticular
%
28
18–32
27
24–31
30
18
38–46
Cirrussac
reach %
34
24–39
33
31–36
33
25
29–35
Eggs
Reference
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
of Récif Toombo (22330 866S, 166260 597E, 09/10/2007);
Récif Toombo (22330 172S, 166260 589E, 20/11/2007).
Prevalence: V. albimarginata, 1 of 1; V. louti, 6 of 10 (60%).
Vouchers: V. albimarginata, MNHN JNC2115; V. louti,
JNC1756, JNC1757, JNC2117, JNC2198, JNC2301,
JNC2401; BMNH 2007.11.14.44, 2013.11.18.13-14.
Description
It should be noted that the uterus reaches anteriorly beyond
the ovary. Measurements and ratios are given in Table 7.
Discussion
Prosorhynchus serrani is known previously only from the
yellow-edged lyretail Variola louti (Forsskål) (Serranidae) from
the Red Sea and off New Caledonia [9, 29]. Our specimens
appear indistinguishable from those described by these authors.
This species is very similar to several other species and their
relationships will probably only be resolved by molecular
means. However, there seem to be minor morphological features which may allow the continued recognition of the Variola
parasites as distinct (Table 8). Of those with no distinction in
the parameters used in the visual key two can immediately be
distinguished by other features.
P. attenuatus Siddiqi & Cable, 1960 from the Atlantic bumper Chloroscombrus chrysurus (Girard) (Carangidae) off Puerto
Rico was described with a ‘‘spherical, suckerlike’’ rhynchus
and it certainly looks like a sucker in the illustration. The pars
prostatica is described as ‘‘tubular’’ and appears straight in the
illustration [43], thus indicating that it may have been placed in
the wrong subfamily.
P. caudovatus Manter, 1940 (syn. P. crucibulus of Eckmann
(1932)) from serranids in the waters around Africa [4, 10, 13,
14, 46] has distinctive filamented eggs.
Other similar species are:
Prosorhynchus caballeroi Gupta & Ahmad, 1976 known
from one specimen from the shrimp scad Alepes djedaba
(Forsskål) (as Caranx kalla Cuvier) (Carangidae) in the Bay
of Bengal [17] grows larger than P. serrani, with a smaller
rhynchus and a longer previtelline distance.
Prosorhynchus conorjonesi Bott & Cribb 2009 from the barramundi cod Cromileptes altivelis (Valenciennes) (Serranidae)
on the Great Barrier Reef [2] grows larger than P. serrani, is
much narrower, with a more anterior mouth and a shorter cirrus-sac reach.
Prosorhynchus jexi has a more anterior mouth than
P. serrani and a longer post-testicular region [2, 9].
Prosorhynchus milleri Bott & Cribb, 2009 based on two
specimens from Variola louti from Lizard Island, Great Barrier
Reef [2] is very similar to P. serrani and from one of the same
host species. It is said to differ from P. serrani in that the latter
has ‘‘a uterus that extends anterior to the vitelline follicles into
the anterior quarter of the body’’. Our results complicate things
in that the anterior uterine extent varies considerably in our
specimens from V. louti. Judging from the illustration of
P. milleri in Bott & Cribb [2] the pre-uterine extent is about
51% of body-length and judging from Durio & Manter’s [9] illustration of P. serrani this ratio is about 17%. Durio & Manter [9]
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Figure 13–18. 13: Prosorhynchus freitasi Nagaty, 1937 from Plectropomus leopardus, uterus in outline. 14: Prosorhynchus freitasi Nagaty,
1937 from Plectropomus laevis, uterus in outline. 15: Prosorhynchus luzonicus Velasquez, 1959, uterus in outline. 16: Prosorhynchus
luzonicus Velasquez, 1959, cirrus-sac. 17: Prosorhynchus sp. A ex Epinephelus morrhua. Ventral view, uterus in outline. 18: Prosorhynchus
sp. B ex Epinephelus coioides. Ventral view, uterus in outline. Scale bars: 500 lm (Figs. 13–15, 17, 18); 200 lm (Fig. 16).
17
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18
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 9. Measurements and ratios of Prosorhynchus freitasi and P. luzonicus. % refers to % of body-length.
Species
Host
Prosorhynchus freitasi
Prosorhynchus freitasi
Prosorhynchus luzonicus
Plectropomus leopardus
Plectropomus laevis
Epinephelus coioides
17
6
14
n
Length
Width
Previtelline distance
Precaecal distance
Pre-uterine distance
Pre-mouth distance
Pretesticular distance
Pre-ovarian distance
Rhynchus length
Rhynchus width
Rhynchus to vitellarium distance
Rhynchus to uterus distance
Rhynchus to caecum distance
Long vitelline field
Short vitelline field
Caecum length
Caecum width
Pharynx length
Pharynx width
Ovary length
Ovary width
Distance between ovary and anterior testis
Anterior testis length
Anterior testis width
Distance between testes
Posterior testis length
Posterior testis width
Posterior testis to cirrus-sac
Cirrus-sac length
Cirrus-sac width
Seminal vesicle length
Seminal vesicle width
Pars prostatica length
Pars prostatica width
Post-testicular distance
Post-vitelline distance
Cirrus-sac reach
Post-ovarian distance
Post-genital pore distance
Egg length
Egg width
Width %
Previtelline distance %
Precaecal distance %
Pre-uterine distance %
Pre-mouth distance %
Pretesticular distance %
Pre-ovarian distance %
Rhynchus length %
Rhynchus width % rhynchus length
Longest vitelline field %
Caecal length %
Ovary length %
Anterior testis length %
Distance between testes %
Posterior testis length %
min.
848
134
322
358
343
573
488
452
37
42
281
296
314
119
112
86
22
36
41
51
37
0
63
44
0
57
47
0
204
57
64
17
360
55
163
331
266
308
24
24
13
12.2
35.3
39.3
37.7
63.2
53.6
49.6
3.2
83.0
13.4
8.0
5.24
5.04
0
4.6
max.
1,650
363
778
923
918
1,134
1,085
1,052
61
67
717
874
900
329
249
190
87
71
73
105
97
38
140
126
53
141
113
0
380
120
197
61
509
101
394
629
529
552
71
32
21
22.8
50.0
56.5
60.0
71.2
68.1
66.0
5.0
123.8
20.6
13.9
8.8
10.1
3.33
10.8
mean
1,239
207
560
640
629
888
771
729
51
53
510
587
602
205
170
128
51
51
52
79
66
9
95
80
13
97
73
0
281
89
139
48
444
73
284
473
398
427
57
27
17
16.6
44.8
51.1
50.1
66.6
61.9
58.3
4.2
104.9
16.5
10.4
6.47
7.7
0.98
8.0
min.
1,365
214
633
736
693
947
837
801
55
48
564
646
665
194
153
148
51
47
56
87
73
0
92
74
0
89
80
0
303
89
?
?
?
?
283
493
455
455
39
24
16
13.5
43.9
51.1
50.2
66.7
61.3
57.3
3.6
75.6
12.2
9.7
5.47
5.82
0
6.0
max.
1,591
290
860
878
928
1,131
1,095
1,039
63
63
802
917
876
270
223
180
67
57
62
108
96
47
138
114
18
136
104
0
360
157
?
?
?
?
454
605
496
558
82
28
19
20.0
54.2
55.6
58.8
71.6
69.0
65.5
4.4
102.1
17.9
11.3
7.5
9.6
1.11
8.7
mean
1,502
255
717
795
807
1,020
959
912
60
54
658
754
752
235
182
161
59
52
59
95
82
8
114
93
3
114
91
0
330
115
?
?
?
?
344
536
465
485
68
26
17
17.0
47.6
53.5
53.6
68.6
63.7
60.6
4.0
89.2
15.7
10.9
6.33
7.6
0.19
7.6
min.
792
129
142
219
263
327
315
276
126
99
0
133
78
186
154
80
58
42
46
58
54
0
69
66
0
69
71
0
230
70
101
37
302
54
308
411
363
410
82
27
15
16.3
15.6
25.2
31.0
37.7
37.9
33.0
12.9
76.3
23.5
9.4
7.10
6.55
0
6.9
max.
1,172
288
221
311
409
471
456
407
170
170
72
272
163
344
257
125
108
66
75
95
79
0
99
111
39
92
92
0
360
124
165
63
439
97
534
636
532
682
160
35
20
25.2
20.8
30.6
46.6
44.3
43.2
39.8
17.6
105.5
29.6
14.0
8.8
10.7
3.73
10.2
mean
925
202
171
257
336
381
372
338
142
130
29
194
114
251
207
105
79
53
58
74
65
0
82
80
10
80
80
0
281
95
138
51
357
73
383
506
426
510
108
30
18
21.7
18.5
27.6
36.7
41.3
40.3
36.6
15.5
91.4
27.1
11.3
7.98
8.9
0.97
8.7
(continued on next page)
19
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 9. (Continued)
Species
Host
Prosorhynchus freitasi
Prosorhynchus freitasi
Prosorhynchus luzonicus
Plectropomus leopardus
Plectropomus laevis
Epinephelus coioides
17
6
14
n
Posterior testis to cirrus-sac %
Cirrus-sac length %
Seminal vesicle length % of cirrus-sac length
Post-testicular distance %
Post-vitelline distance %
Cirrus-sac reach %
Post-ovarian distance %
Post-genital pore distance %
min.
0
17.3
30.1
18.7
32.2
26.6
28.9
2.12
max.
0
25.2
55.7
29.3
45.1
35.1
44.0
6.29
considered P. crucibulum from V. louti of Nagaty [29] a synonym
of P. serrani and judging from Nagaty’s illustration the pre-uterine
distance is about 31% of body-length. This ratio in our worms varies between 26 and 52%, and without a distinct bimodal pattern
(26, 29, 30, 32, 33, 38, 39, 40, 45, 49 and 52%). It may well be that
there are two forms here, but we do not as yet have enough data to
be certain where to draw the line.
Prosorhynchus robertsthomsoni Bott & Cribb, 2009 is very
similar to P. serrani but apparently has a distinctly different
shaped rhynchus, in that it has a blunt rounded posterior extension in contrast to the distinct narrow elongate posterior extension of the P. serrani rhynchus [2]. It may be that the
vitellarium reaches slightly more posterior in P. serrani in that
the follicles extend just posterior to the pharynx, rather than just
to the pharynx.
Prosorhynchus thapari Manter, 1953 was based on 17 specimens from the spotted coralgrouper Plectropomus maculatus
(Bloch) (Serranidae) from off Fiji [26]. We can detect no morphological distinctions from P. serrani and retain the species as
separate based on host distinction, and the knowledge that as
yet unpublished studies indicate some specificity and cryptic
speciation in the genus. Nevertheless, it may well be that this
is the oldest valid name for this species.
Prosorhynchus truncatus Verma, 1936 is based on two
specimens, one ovigerous and lost and the other without eggs,
from the intestine of the river catfish Cephalocassis jatia
(Hamilton) (as Arius j.) (Ariidae) off Puri, Bay of Bengal
[49]. It has a more posteriorly situated mouth and a shorter
cirrus-sac reach.
Prosorhynchus freitasi Nagaty, 1937 (Figures 13, 14)
urn:lsid:zoobank.org:act:D5FF3B1F-10B1-4447-ACB7-C
7D544C36AFE
Host: Plectropomus laevis (Lacepède), Serranidae, blacksaddled coralgrouper; Plectropomus leopardus (Lacepède), Serranidae, leopard coralgrouper.
Site: digestive tract.
Localities: P. laevis Off Ouano (21490 430S, 166440 278E,
25/10/2007); P. leopardus Grande Rade, Nouméa (22150 S
16624E,
23/10/2007),
Off
Ouano
(21490 430S,
0
16644 278E, 25/10/2007), Between Larégnière and Récif
Crouy (22200 702S, 166190 295E, 05/05/2008).
mean
0
22.0
43.6
23.1
38.5
31.2
34.9
4.17
min.
0
21.0
?
17.8
31.1
29.0
28.7
2.89
max.
0
24.3
?
28.5
38.2
33.7
35.0
5.65
mean
0
22.3
?
23.0
35.7
31.4
32.4
4.60
min.
0
25.4
37.7
37.8
50.5
42.6
51.8
10.24
max.
0
36.9
61.4
45.6
59.3
50.9
58.5
14.96
mean
0
30.5
48.8
41.3
54.7
46.3
55.1
11.72
Prevalence: P. laevis 1 of 2 (50%); P. leopardus 5 of 7
(71%).
Vouchers: P. laevis JNC2339; P. leopardus MNHN
JNC2333A, JNC 2334, JNC2340, JNC2513, JNC 2514;
BMNH 2013.11.18.7-12.
Discussion
Table 9 measurements, Table 10 comparisons.
In terms of the parameters used in the visual key there are
no differences between our specimens from Plectropomus laevis and Prosorhynchus freitasi as described from ‘‘Serranus
guttatus’’ from the Red Sea [29]. According to Froese & Pauly
[15] S. guttatus is now known as the peacock hind Cephalopholis argus (Bloch) (Serranidae). It has also been reported in
Epinephelus sp. and the spotted coralgrouper Plectropomus
maculatus (Bloch) (Serranidae) from off New Caledonia [9]
and Plectropomus leopardus and Plectropomus laevis from
the Great Barrier Reef [3]. It has an unusual morphology in that
all the internal organs are restricted to the posterior half of the
body and the rhynchus is relatively small.
Bott et al. [3] described six Prosorhynchus species from Plectropomus spp. on the Great Barrier Reef, five of which are new
and one, P. freitasi already known. They are mostly distinguished
by minor morphological characters and by analysis of ITS2
rDNA sequences. P. lesteri is distinguished by its distinctly larger
rhynchus. P. wrightae differs in the pre-uterine extent, being the
only one of these species where the uterus extends well beyond
the vitellarium anteriorly. P. heronensis also has a larger rhynchus, although not as large as in P. lesteri, and a distinct U-shaped
seminal vesicle. In P. plectropomi the uterus extends to, or just
anterior to the anterior extent of the vitellarium, apparently forcing the anterior follicles apart, breaking up the continuous arc
found in other related species. P. munozae is a rather small worm,
but with larger eggs. Our specimens agree closely with Bott
et al.’s [3] description of P. freitasi.
Prosorhynchus luzonicus Velasquez, 1959 (Figures
15, 16)
urn:lsid:zoobank.org:act:25F350A1-F852-4CA9-91D8-A28
8F9B3F7DD
20
Table 10. Comparisons of Prosorhynchus freitasi, blue shading shows major distinctions, green shading minor distinctions.
width %
Rhynchus
L%
Previtelline
%
848–1,506
1,365–1,591
919–1,870
1,216–1,564
3,300–4,500
1,040–1,104
3,360–4,480
1,341–2,320
1,392–1,648
700–1,040
3,600
1,024–1,280
1,056–1,227
1,778–2,282
1,760–2,600
800–1,088
12–20
14–20
10–23
12–17
12–13
15–19
11–12
13–18
13–14
17–18
8
13–16
16–22
15–16
23–24
16–21
4–5
4
4–6
4–5
6–9
8
4–5
10–11
9
4–6
5
4–5
5–10
12
16–20
6–7
35–47
44–54
49–50
39
64
45
50
41
31
46
47
47
38
33
30
38
PreUterine
%
38–55
50–59
61
46
41
55
37
51
51
57
47
44
58
44
?
30
Premouth
%
63–68
67–72
63–65
60
62
70
60
60
56
68
65
66
56
53
63
66
Posttesticular
%
19–29
18–24
22–26
29
18
17
16
23
24
24
14
24
20
25
21
22
Cirrussac
reach %
28–35
29–34
27–28
?
22
?
19
30
25
28
14
29
24
28
20
33
Eggs
Reference
24–30 · 13–21
24–28 · 16–19
21–29 · 17–21
24–26 · 14–15
23 · 12
26–27 · 13–15
17–19 · 8–11
19–26 · 14–15
25 · 16
31–36 · 19–23
22–30 · 11–17
24–26 · 14–15
16–18 · 11–15
27–34 · 19–22
35–40 · 18–20
20–24 · 12–13
new data
new data
[27]
[3]
[43]
[3]
[23]
[3]
[2]
[3]
[17]
[3]
[41]
[25]
[46]
[3]
Eggs
Reference
27–35 · 15–20
30–39 · 17–24
32–33 · 16
27–28 · 14–22
24–27 · 12–17
28–31 · 15–16
29–30 · 16
32–38 · 16–20
29–32 · ?
new data
[45]
[2]
[5]
[24]
[5]
[2]
new data
[30]
Table 11. Comparisons of Prosorhynchus luzonicus, green shading shows minor distinctions.
P. luzonicus Velasquez, 1959
P. luzonicus Velasquez, 1959
P. jexi Bott & Cribb, 2009
P. maternus Bray & Justine, 2006
P. pacificus Manter, 1940
P. pacificus Manter, 1940, types
P. robertsthomsoni Bott & Cribb, 2009
P. robertsthomsoni Bott & Cribb, 2009
P. squamatus Odhner, 1905
Length
Width
%
Rhynchus
L%
Previtelline
%
792–1,172
1,060–2,020
1,104–1,424
2,052–2,227
1,206–1,444
1,232–1,359
1,072–1,408
1,088–1,256
1,000–1,500
16–25
22–25
19–25
19–21
25–27
26–30
18–23
23–24
34
13–18
10–19
15
13–17
14–16
18–19
10–11
10–12
10–15
16–21
20
20
19–23
31
26–30
27
18–23
12
PreUterine
%
31–47
42
32
34–41
47
41–46
24
10–26
22
Premouth
%
38–44
39
43
38–40
45
46–48
48
45–47
49
Posttesticular
%
38–46
38
41
45–53
37
38–49
31
31–40
28
Cirrussac
reach %
43–51
38
37
32–39
42
44–48
35
39–48
34
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
P. freitasi ex Plectropomus leopardus
P. freitasi ex Plectropomus laevis
P. freitasi Nagaty, 1937
P. freitasi Nagaty, 1937
P. arabiana Srivastava, 1938
P. heronensis Bott, Miller & Cribb, 2013
P. indicus Madhavi, 1974
P. lesteri Bott, Miller & Cribb, 2013
P. milleri Bott & Cribb, 2009
P. munozae Bott, Miller & Cribb, 2013
P. orientalis Gupta & Ahmad, 1976
P. plectropomi Bott, Miller & Cribb, 2013
P. stunkardi Siddiqi & Cable, 1960
P. thapari Manter, 1953
P. truncatus Verma, 1936
P. wrightae Bott, Miller & Cribb, 2013
length
21
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 12. Measurements and ratios of Prosorhynchus spp. from Epinephelus spp. % refers to % of body-length.
Species
Prosorhynchus sp. A
Prosorhynchus sp. B
Host
Epinephelus morrhua
Epinephelus coioides
2
3
n
Length
Width
Previtelline distance
Precaecal distance
Pre-uterine distance
Pre-mouth distance
Pretesticular distance
Pre-ovarian distance
Rhynchus length
Rhynchus width
Rhynchus to vitellarium distance
Rhynchus to uterus distance
Rhynchus to caecum distance
Long vitelline field
Short vitelline field
Caecum length
Caecum width
Pharynx length
Pharynx width
Ovary length
Ovary width
Distance between ovary and anterior testis
Anterior testis length
Anterior testis width
Distance between testes
Posterior testis length
Posterior testis width
Posterior testis to cirrus-sac
Cirrus-sac length
Cirrus-sac width
Seminal vesicle length
Seminal vesicle width
Pars prostatica length
Pars prostatica width
Post-testicular distance
Post-vitelline distance
Cirrus-sac reach
Post-ovarian distance
Post-genital pore distance
Egg length
Egg width
Width %
Previtelline distance %
Precaecal distance %
Pre-uterine distance %
Pre-mouth distance %
Pretesticular distance %
Pre-ovarian distance %
Rhynchus length %
Rhynchus width % rhynchus length
Longest vitelline field %
Caecal length %
Ovary length %
Anterior testis length %
Distance between testes %
Posterior testis %
2,157
470
310
?
540
1,035
964
1,002
513
231
0
30
?
454
478
?
?
112
104
147
137
0
181
161
0
168
170
0
611
198
226
68
791
142
905
1,348
927
1,001
97
35
18
21.8
14.4
?
25.02
48.0
44.7
46.4
23.8
44.9
21.1
?
6.81
8.41
0
7.79
2,110
508
222
888
?
1,062
1,175
1,186
335
320
malformed
malformed
555
?
?
275
253
126
108
146
142
0
202
197
0
171
169
0
593
251
182
74
861
159
569
0
863
797
96
malformed
malformed
24.1
10.5
42.09
?
50.3
55.7
56.2
15.9
95.4
?
13.0
6.92
9.59
0
8.12
min.
1,006
217
217
306
451
570
556
584
155
121
61
292
148
220
217
183
113
64
80
57
50
0
70
75
0
75
64
0
233
80
?
?
?
56
324
566
355
348
42
29
18
21.6
19.3
27.0
43.5
50.6
55.3
54.9
12.6
78.1
17.6
17.5
4.41
5.99
0
5.78
max.
1,297
294
263
414
621
685
769
729
175
155
95
446
237
262
275
241
129
85
114
77
69
9
94
81
45
82
78
30
266
120
123
53
?
84
394
803
379
519
57
32
21
22.7
21.6
31.9
47.9
56.7
59.3
58.1
15.4
91.0
21.9
18.6
5.96
7.22
3.44
8.13
mean
1,199
266
244
357
545
637
694
675
165
142
82
379
191
237
239
217
122
78
97
64
58
3
80
77
15
78
73
15
251
102
41
18
?
73
368
708
369
459
49
30
19
22.2
20.4
29.8
45.4
53.4
57.7
56.4
13.9
85.8
19.9
18.1
5.36
6.71
1.15
6.63
(continued on next page)
22
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Table 12. (Continued)
Species
Prosorhynchus sp. A
Prosorhynchus sp. B
Host
Epinephelus morrhua
Epinephelus coioides
2
3
n
Posterior testis to cirrus-sac %
Cirrus-sac length %
Seminal vesicle length % of cirrus-sac length
Post-testicular distance %
Post-vitelline distance %
Cirrus-sac reach %
Post-ovarian distance %
Post-genital pore distance %
0
28.3
37.0
42.0
62.5
43.0
46.4
4.48
Host: Epinephelus coioides (Hamilton) (Serranidae),
orange-spotted grouper.
Site: Digestive tract.
Locality: Fish Market, Nouméa (14/10/2010).
Prevalence: 1 of 1.
Vouchers: MNHN JNC3277; BMNH 2013.11.18.24.
Discussion
See Table 9 for measurements and Table 11 for morphological comparisons. These specimens from E. coioides are clearly
different from those from this host mentioned below as Prosorhynchus sp. B, particularly in pre-mouth distance (see Table 13)
and vitelline distribution, but also in post-testicular distance and
cirrus-sac reach. On the other hand they are very similar to
P. luzonicus as originally described [48] from the barramundi
Lates calcarifer (Bloch), (Latidae) from Malabon, Rizal, Luzon
island, Philippines. It has been reported in E. coioides in Lampung Bay, southern Sumatra, Indonesia [34–36]. Rückert [35]
described and illustrated this species from Epinephelus fuscoguttatus, also from Lampung Bay, and later reported it again
in this host, both in culture and in the wild [38]. It is slightly
disconcerting that Rückert et al. [37] failed to find this species
in L. calcarifer in her study of Lampung Bay. Two useful, but
not infallible, recognition features are the separated vitelline
fields (occasionally they appear to form an arch), and the
mainly postovarian uterus (but according to the figure and illustration by Rückert [35] this is not invariable). Our specimens
differ slightly from Velasquez’s [48] description in the greater
extent of the cirrus-sac reach as a proportion of body-length
(43–51% vs. about 38%). Rückert [35] shows a proportion of
about 39%.
Prosorhynchus jexi is similar, but differs in cirrus-sac
extent, in the arched vitelline fields and in the extension of
the uterus anterior to the ovary (but note that these latter features appear to be variable in P. luzonicus) [2, 9].
Prosorhynchus maternus Bray & Justine, 2006 from the
Malabar grouper Epinephelus malabaricus (Bloch & Schneider) off New Caledonia [5] differs in size, post-testicular region
and cirrus-sac reach.
Prosorhynchus pacificus Manter, 1940 is an eastern Pacific
form, having been reported originally from the serranids, the
0
28.1
30.8
27.0
0.0
40.9
37.8
4.53
min.
0
18.0
?
29.7
56.3
27.4
34.6
3.65
max.
2.34
26.5
46.3
32.3
61.9
37.0
40.0
4.39
mean
1.14
21.3
?
30.8
58.8
31.2
38.0
4.08
sailfin grouper Mycteroperca olfax (Jenyns), the broomtail
grouper Mycteroperca xenarcha Jordan and an unidentified
grouper off the Galapagos [24]. Later records were summarised
by Bray & Justine [5], who re-measured two type-specimens.
Slight differences from our specimens can be detected in previtelline, pre-mouth and post-testicular distances, cirrus-sac reach
and egg-size range. Some specimens from cultured E. coioides
in Vietnam have been identified as this species, others as
P. epinepheli [51].
Prosorhynchus robertsthomsoni (see above, including new
data) differs slightly in pre-uterus, pre-mouth and post-testicular
distances [2].
Prosorhynchus squamatus Odhner, 1905 is a Northern
Hemisphere species, originally reported from the shorthorn
sculpin Myoxocephalus scorpius (Linnaeus) (Cottidae) [32],
but since reported in many cold-water hosts [16, 21]. It differs
from P. luzonicus in width, previtelline, pre-uterine, pre-mouth
and post-testicular distances, cirrus-sac reach and probably in its
arched vitellarium and pre-ovarian uterine extent.
Prosorhynchus sp. A (Figure 17)
Epinephelus morrhua (Valenciennes, 1833), Serranidae,
comet grouper.
Site: digestive tract.
Locality: Off Récif Kué, deep-sea (22350 511S,
16690 893E, 23/01/2008).
Prevalence: 1 of 4 (25%).
Vouchers: MNHN JNC2453; BMNH 2013.11.18.26.
Discussion
No species are identical to these two specimens according
to the visual key (Tables 12, 13). As only one specimen is in
good condition, the worms have not been described as new,
but the very elongate rhynchus seems to be a distinguishing feature. Also note that the ovary lies beside the anterior testis.
One species, Prosorhynchus epinepheli, has one major distinguishing feature in the visual key, i.e., width (Table 13).
Minor distinguishing features are the pre-mouth distance and
the egg-size.
[46]
35–40 · 18–20
20
21
63
16–20
23–24
?
21
31
31
26–30
23
11
9
14–16
18–19
12–16
1,760–2,600
30
11–14
14
19–22
18–31
16–24
14–19
13–15
10–17
2,110–2,157
1,250–2,350
1,006–1,297
2,000–4,000
1,715–2,245
3,672
1,392–1,648
1,206–1,444
1,232–1,359
1,096–1,600
sp. in Epinephelus morrhua
epinepheli Yamaguti, 1939
sp. in Epinephelus coioides
caudovatus Manter, 1940
caudovatus Manter, 1940
caudovatus Manter, 1940
milleri Bott & Cribb, 2009
pacificus Manter, 1940
pacificus Manter, 1940, types
paracrucibulus Velasquez,
1959
P. truncatus Verma, 1936
P.
P.
P.
P.
P.
P.
P.
P.
P.
P.
23
Prosorhynchus sp. B. (Figure 18)
22–24
40–43
22–23
17–20
27–30
12
13–14
25–27
26–30
30–36
37
51
47
41–46
?
38
56
45
46–48
57
50
24
37
38–49
34
36
25
42
44–48
27
25 · 16
24–27 · 12–17
28–31 · 15–16
none
new data
[51]
new data
[10]
[14]
[4]
[2]
[23]
[5]
[45]
35
· 18–21
· 18–21
· 19–22
· 21–25
28–30
29–32
38–45
32–43
Reference
Eggs
Cirrussac
reach %
41–43
41
27–37
29–35
Posttesticular
%
27–42
41
30–32
38–46
Premouth
%
48–50
54
51–57
39–44
PreUterine
%
25
22
44–48
25–46
Previtelline
%
Rhynchus
L%
Width
%
Length
Table 13. Comparisons of Prosorhynchus spp. from Epinephelus spp., blue shading shows major distinctions, green shading minor distinctions.
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Host: Epinephelus coioides (Hamilton, 1822) (Serranidae),
orange-spotted grouper.
Site: Digestive tract.
Locality: Fish Market, Nouméa (27/11/2009).
Prevalence: 1 of 1.
Vouchers: MNHN JNC3140; BMNH 2013.11.18.27.
Discussion
Measurements of the three specimens are given in Table 12.
Several species are very similar to Prosorhynchus sp. B, and
show no differences in the visual key but may be distinguished
by combinations of minor features (Table 13). More specimens
are needed to describe this form as new as so many similar
Prosorhynchus species are known.
Prosorhynchus caudovatus Manter, 1940 (syn. P. crucibulus
of Eckmann (1932)) from serranids in the waters around Africa
[4, 10, 13, 14, 46] has a distinctive filamented egg. It is also distinctly larger than P. sp. B, has a more anterior mouth and a
longer post-testicular region.
Prosorhynchus milleri Bott & Cribb, 2009 based on two
specimens from Variola louti from Lizard Island, Great Barrier
Reef [2] is longer, narrower, with a smaller rhynchus, a longer
previtelline region and a shorter post-testicular region. The
vitelline fields reach to the pharynx (vs. distinctly anterior).
Prosorhynchus pacificus belongs to a group of Prosorhynchus spp. with the uterus restricted to the post-ovarian region.
In this aspect it differs from P. sp. B. It also differs in previtelline distance, pre-mouth distance, post-testicular region and cirrus-sac reach. The vitelline fields reach the ovary (vs. well
anterior to the pharynx).
Prosorhynchus paracrucibulus Velasquez, 1959 based on
three non-ovigerous worms (presumably metacercariae) from
the scales (!) of the Buru glass perchlet Ambassis buruensis Bleeker (Ambassidae) Manila Bay, Paranaque, Rizal, Luzon Island,
Philippines [48]. It is a little wider, with symmetrical testes. The
worm is not developed sufficiently enough to recognise, but conceivably it is the metacercaria of a serranid parasite.
Prosorhynchus truncatus Verma, 1936 is based on two
specimens, one ovigerous and lost and the other without eggs,
from the intestine of the river catfish Cephalocassis jatia
(Hamilton) (as Arius j.) (Ariidae) off Puri, Bay of Bengal
[49]. It is considerably longer than P. sp. It also differs in previtelline distance, pre-mouth distance, post-testicular region and
cirrus-sac reach.
Prosorhynchus specimens from cultured E. coioides in
Vietnam have been identified as Prosorhynchus luzonicus and
P. epinepheli [51].
Prosorhynchus sp. immature
Host: Epinephelus coeruleopunctatus (Bloch, 1790)
Site: Digestive tract.
Locality: Îlot Lebris, off Ouano (21500 S, 166450 E, 25/10/
2007).
Prevalence: 1 of 3.
Vouchers: MNHN JNC2338.
24
R.A. Bray & J.-L. Justine: Parasite 2013, 20, 56
Discussion
A single unidentifiable immature specimen was recovered
from this host species.
3.
4.
Conclusions
The molecular evidence presented by Bott et al. [3] indicated that there are many distinct, but very similar species of
prosorhynchines in serranids, especially Epinephelus and
Plectropomus. The morphological similarity of these forms
has led to many problems in identification, and some unlikely
combinations of hosts in the literature, as for example the
quoted hosts for Neidhartia neidharti, which in addition to serranids, includes a belonid and a freshwater siluriform. Recent
molecular studies of a wide range of digeneans have indicated
that most species exhibit oioxenous or stenoxenous specificity
and ‘‘that no euryxenous host distribution should be accepted
on the basis of morphology only’’ [28]. Although it is dangerous to identify parasites solely on the basis of their hosts, consideration should be taken of the relatedness of the hosts and
the geographical distribution.
Cribb et al. [8] discussed the digenean fauna of epinepheline serranids and found that Prosorhynchus was the commonest parasite, both in the Atlantic/Eastern Pacific region and the
Indo-West Pacific Region, and is the only bucephalid genus
which has ‘‘apparently strongly radiated within the Epinephelinae’’. Since that paper [8] our knowledge of epinepheline bucephalids has increased markedly [2, 3, 5] reinforcing that
point, but suggesting that Neidhartia has also radiated, at least
in the Indo-West Pacific region. The morphological distinctions
between Prosorhynchus and Neidhartia are minor, but molecular evidence [3] indicates that these distinctions are reflected by
the molecules. Those species of Prosorhynchus with a variable
ovary configuration (e.g., P. epinepheli, P. longisaccatus) may
invalidate this distinction, or may belong to either monophyletic
genus.
Acknowledgements. Julie Mounier, Charles Beaufrère, Anaı̈s Guillou,
Audrey Guérin, Damien Hinsinger, Éric Bureau, Chloé Journo,
Violette Justine, Amandine Marie, Aude Sigura, Guilhem Rascalou,
Géraldine Colli, Lenaı̈g Hemery, Pierpaolo Brena, Cyndie Dupoux,
Isabelle Mary, Adeline Grugeaud, and Marine Briand, students, participated in the parasitological survey. Claude Chauvet (UNC, Nouméa)
caught several fishes. Angelo di Matteo (IRD) provided technical help.
Certain fishes were identified from photographs by Ronald Fricke
(Staatliches Museum für Naturkunde, Stuttgart, Germany) or by Jack
Randall (Bishop Museum, Hawaii). The authors wish to report that
there are no competing interests.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
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Cite this article as: Bray RA & Justine J-L: Bucephalidae (Digenea) from epinephelines (Serranidae: Perciformes) from the waters off
New Caledonia, including Neidhartia lochepintade n. sp. Parasite, 2013, 20, 56.
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