Prosorhynchine trematodes (Digenea: Bucephalidae)from epinephelines (Perciformes: Serranidae)on the Great Barrier Reef, Australia

Nathan J. Bott Æ Thomas H. Cribb

Received: 20 February 2008 / Accepted: 31 July 2008

� Springer Science+Business Media B.V. 2008

Abstract Six new species of bucephalid trematodes

from the prosorhynchine bucephalid genera Proso-

rhynchus Odhner, 1905 and Neidhartia Nagaty, 1937

are reported from the epinepheline genera Cephalop-

holis, Cromileptes, Epinephelus and Variola on the

Great Barrier Reef, Australia. Two species of Pros-

orhynchus and one of Neidhartia are reported from

Epinephelus spp., P. jexi n. sp. from E. quoyanus, P.

lafii n. sp. from E. fuscoguttatus and N. epinepheli n.

sp. from E. maculatus. The other three new species

are P. robertsthomsoni n. sp. from Cephalopholis

argus, C. cyanostigma and C. miniata, P. conorjonesi

n. sp. from Cromileptes altivelis, and P. milleri n. sp.

from Variola louti. Extensive examinations of other

piscivorous fish species from the Great Barrier Reef

have not revealed these six bucephalid species, which

appear to be restricted at least to the host genera from

which they are reported here.

Introduction

Epinepheline serranids are one of the most impor-

tant groups of large predatory fishes found on the

Great Barrier Reef. Of the total of the 159 species

known worldwide, 49 are known from the Great

Barrier Reef (Heemstra & Randall, 1993; Randall

et al., 1997). The Bucephalidae Poche, 1907 is a

large family of digeneans, found as sexual adults in

the alimentary tracts of piscivorous fish. At least 24

bucephalid species from nine genera, Bucephalus

Baer, 1827, Folliculovarium Gu & Shen, 1983,

Neoprosorhynchus Dayal, 1948, Prosorhynchoides

Dollfus, 1929, Prosorhynchus Odhner, 1905, Pseud-

oprosorhynchus Yamaguti, 1938, Rhipidocotyle

Diesing, 1855, Neidhartia Nagaty, 1937 and Tel-

orhynchus Crowcroft, 1947, have been reported

from epinepheline serranids (Cribb et al., 2002).

Despite this, only two species have been previously

reported from epinephelines of the Great Barrier

Reef, i.e. Prosorhynchus epinepheli Yamaguti, 1939

from Epinephelus merra and P. freitasi Nagaty,

1937 from Plectropomus maculatus, both by Durio

& Manter (1968). Here we report on six new

species of bucephalids collected from epinephelines

on the Great Barrier Reef. Parasites from species of

Cephalopholis, Cromileptes, Epinephelus and Vari-

ola collected from Heron Island on the southern

Great Barrier Reef and Lizard Island on the

northern Great Barrier Reef, Australia are

described.

N. J. Bott � T. H. Cribb

School of Molecular & Microbial Sciences,

The University of Queensland, Brisbane,

Queensland 4072, Australia

Present Address:N. J. Bott (&)

Department of Veterinary Science, The University

of Melbourne, 250 Princes Hwy, Werribee, Victoria 3030,

Australia

e-mail: nbott@unimelb.edu.au

123

Syst Parasitol (2009) 72:57–69

DOI 10.1007/s11230-008-9160-8

Materials and methods

Fish were collected by either spear or line and were

killed prior to dissection by severing the nerve chord.

The entire digestive tract was removed and separated

into stomach, pyloric caeca, intestine and rectum.

Each individual section was opened in vertebrate

saline and examined under a stereo microscope. Live

parasites were fixed in near boiling vertebrate saline

without the use of pressure and preserved in 5%

formalin.

Specimens were rinsed in water before being over-

stained in Mayer’s haematoxylin, destained in 0.5%

hydrochloric acid and neutralised in 0.5% ammonia

solution. The worms were dehydrated in a graded

ethanol series, cleared in methyl salicylate and

mounted in Canada balsam. Worms were examined

with an Olympus BH-2 compound microscope, and

drawn with the aid of a drawing tube. Measurements

were taken with an eyepiece micrometer. All mea-

surements are given in micrometres.

Results

We examined 21 species of epinepheline serranids

from the Great Barrier Reef for bucephalid trematode

infection. Table 1 shows the number of specimens of

each host species and the numbers infected with the

six bucephalid species reported below. We have

excluded from this study the complex of bucephalid

trematodes of species of Plectropomus (Serranidae:

Epinephelinae) from the Great Barrier Reef, which

will be reported elsewhere. They did not share any

species with the host species reported on here, except

for two Prosorhynchus species, that are shared

between Plectropomus spp. and Variola louti. These

two species will be reported in an analysis of the

bucephalids of species of Plectropomus, because both

species are common in that genus and we have only

recorded one specimen of each from one individual

host of V. louti. We have also found one specimen of

what appears to be a further new species from

Epinephelus fuscoguttatus, but have not described it

here because more specimens are needed.

Below is a key to the bucephalids of epinepheline

serranids from the Great Barrier Reef (excluding

those from species of Plectropomus) reported here,

followed by their descriptions.

Key to bucephalids of epinepheline serranids

from the Great Barrier Reef

1a. Ovary intertesticular ……………………………………………… Neidhartia epinepheli n. sp.

1b. Ovary anterior to testes ……………………………………… (Prosorhynchus Odhner, 1905) 2

2a. Pharynx between testes ……………………………………………… Prosorhynchus lafii n. sp.

2b. Pharynx anterior to testes …………………… 3

3a. Vitelline follicles partly posterior to pharynx

………………………………………………… 4

3b. Vitelline follicles entirely anterior to pharynx

………………………………………………… 5

4a. Rhynchus with bulbous anterior section and

slender posterior section; lateral vitelline folli-

cle fields separated into fields, anterior and

posterior to pharynx and caecum …………………………… Prosorhynchus conorjonesi n. sp.

4b. Rhynchus pyriform and muscular; lateral vitel-

line follicle fields not separated into fields:

dextral field extends to level of pharynx

…………………… Prosorhynchus milleri n. sp.

5a. Rhynchus 116–138 lm long; uterus extends

slightly between and anterior to vitelline

follicles; pharynx small and difficult to see in

mid-body ………………………………………………… Prosorhynchus robertsthomsoni n. sp.

5b. Rhynchus 167–212 lm long; uterus not extend-

ing anterior to vitelline follicles; pharynx

prominent in mid-body ……………………………………………… Prosorhynchus jexi n. sp.

Bucephalidae Poche, 1907

Prosorhynchinae Nicoll, 1914

Prosorhynchus Odhner, 1905

Prosorhynchus jexi n. sp.

Syn. P. epinepheli Yamaguti, 1939 of Durio &

Manter (1968)

Type-host: Epinephelus quoyanus (Valenciennes),

longfin grouper (Serranidae: Epinephelinae).

Type-locality: Off Heron Island, Great Barrier Reef,

Australia (238270S, 1518550E).

Other locality: Off Lizard Island, Great Barrier Reef,

Australia (148400S, 1458280E).

58 Syst Parasitol (2009) 72:57–69

123

Site: Pyloric caeca, intestine, rectum.

Type-material: Queensland Museum, Brisbane,

Australia. Holotype: QMG 224762, Paratypes:

QMG 224763 to 224771.

Etymology: This species is named for Dr Aaron Jex,

formerly of the University of Queensland, Brisbane,

Australia and now of the University of Melbourne,

Australia for all his assistance and advice in the

laboratory.

Description (Fig. 1)

Measurements in Table 2. Body fusiform, widest at

level of caecum; entire tegument covered with spines.

Rhynchus large, pyriform, with well-developed mus-

cles, slender, tapersg distally. Pharynx spherical,

muscular, in anterior half of body. Caecum sac-like,

extends anteriorly from pharynx.

Testes 2, tandem, contiguous or overlapping,

ovoid, posterior to pharynx, dextral in mid-body.

Cirrus-sac (Fig. 1b) sinistral, muscular, not thick-

walled, entirely posterior to testes. Seminal vesicle

elongate, dextral in proximal portion of cirrus-sac.

Pars prostatica straight, both muscular and glandular

distally, curved proximally to form convoluted sem-

inal duct, joins with and is dorsal to seminal vesicle.

Ejaculatory duct narrow. Genital atrium ovoid, con-

tains bilobed genital lobe. Common genital pore sub-

terminal on ventral surface, posterior to genital

atrium.

Ovary ovoid, small, dextral at level of pharynx,

overlaps but anterior to anterior testis. Mehlis’ gland

at level of and dorsal to anterior testis, dextral.

Laurer’s canal extends laterally from Mehlis’ gland

to dextral side of worm. Vitelline follicles in two

lateral fields, both beginning at level of mid-caecum,

confluent along longitudinal mid-line, reach into

Table 1 Number of infections of bucephalid species from this study taken from epinepheline serranids on the Great Barrier Reef

n Prosorhynchus Neidhartia

jexin. sp.

lafiin. sp.

robertsthomsonin. sp.

conorjonesin. sp.

millerin. sp.

epinephelin. sp.

Anyperodonluecogrammicus

1 0 0 0 0 0 0

Cephalopholis argus 4 0 0 2 0 0 0

C. boenak 33 0 0 0 0 0 0

C. cyanostigma 24 0 0 1 0 0 0

C. miniata 20 0 0 1 0 0 0

C. urodeta 2 0 0 0 0 0 0

Cromileptes altivelis 8 0 0 0 7 0 0

Epinephelus cyanopodus 8 0 0 0 0 0 0

E. fasciatus 37 0 0 0 0 0 0

E. fuscoguttatus 3 0 2 0 0 0 0

E. maculatus 3 0 0 0 0 0 1

E. merra 8 0 0 0 0 0 0

E. ongus 21 0 0 0 0 0 0

E. polyphekedion 1 0 0 0 0 0 0

E. quoyanus 59 33 0 0 0 0 0

E. tauvina 2 0 0 0 0 0 0

E. undulostriatus 8 0 0 0 0 0 0

Plectropomus laevis 7 0 0 0 0 0 0

Pl. leopardus 51 0 0 0 0 0 0

Pl. maculatus 3 0 0 0 0 0 0

Variola louti 2 0 0 0 0 1 0

Syst Parasitol (2009) 72:57–69 59

123

anterior quarter of body. Uterus extends as far as, or

just beyond the posterior limit of vitelline follicles,

reaches posteriorly beyond posterior margin of cirrus-

sac. Eggs, small, numerous, tanned. Excretory pore

terminal; extent of excretory vesicle not seen but not

exceeding caecum anteriorly.

Prosorhynchus lafii n. sp.

Type-host: Epinephelus fuscoguttatus (Forsskal),

brown-marbled grouper (Serranidae: Epinephelinae).

Type-locality: Off Heron Island, Great Barrier Reef,

Australia (238270S, 1518550E).

Site: Intestine.

Type-material: Queensland Museum, Brisbane, Aus-

tralia. Holotype: QMG 224792, Paratypes: QMG

224793 to 224797.

Etymology: This species is named for Mr Feras Lafi

of the University of Queensland, Brisbane, Australia

for all his assistance and advice with phylogenetic

analyses.

Description (Fig. 2)

Measurements in Table 2. Body ovoid, tapers

towards posterior end; entire tegument covered with

spines. Rhynchus large, wide, pyriform; longitudinal

and lateral muscles visible in some specimens.

Pharynx, spherical, muscular, in anterior half of

body. Caecum sac-like, extends anteriorly from

pharynx into anterior quarter of body.

Testes 2, ovoid, tandem, almost contiguous,

dextral; posterior testis extends to posterior margin

of pharynx; anterior testis extends anteriorly beyond

pharynx. Cirrus-sac (Fig. 2b) sinistral, muscular,

not thick-walled, in posterior half of body. Seminal

vesicle elongate, dextral in posterior portion of

cirrus-sac. Pars prostatica straight, both muscular

and glandular distally, curved proximally to form

convoluted seminal duct, joins with and is dorsal

to seminal vesicle. Ejaculatory duct narrow.

Genital atrium elongate, contains bilobed genital

lobe. Common genital pore distinct, posterior to

cirrus-sac.

Table 2 Measurements of species of Prosorhynchus and Neidhartia collected from Epinephelus spp. on the Great Barrier Reef.

No. of specimens P. jexi n. sp. P. lafii n. sp. N. epinepheli n. sp.

10 4 2

Length 1,275 (1,104–1,424) 1,120 (1,040–1,184) 888 (880–896)

Width 267 (208–352) 216 (160–256) 224

Length/Width 4.9 (3.9–5.9) 5.15 (4.2–7.2) 4 (3.92–4)

Caecum 168 (145–202) 191 (177–209) 164 (161–167)

Pharynx 58 (48–71) 9 63 (48–71) 46 (45–48) 9 52 (51–55) 64 9 69 (64–74)

Ovary 73 (58–90) 9 72 (58–109) 87 (74–103) 9 87 (74–103) 74 (71–77) 9 60 (55–64)

Anterior testis 100 (77–118) 9 110 (71–148) 83 (80–87) 9 86 (77–93) 80 9 64

Posterior testis 100 (74–128) 9 109 (77–173) 79 (71–90) 9 82 (74–90) 93 (90–96) 9 76 (71–80)

Vitelline fields 227 (193–273) 9 221 (170–263) 95 (83–103) 9 150 (135–177) 177 9 116

Uterus 853 (752–992) 644 (576–720) 712 (688–736)

Uterus/Length 0.67 (0.58–0.7) 0.58 (0.5–0.62) 0.8 (0.77–0.84)

Cirrus-sac 382 (321–482) 346 (305–385) 262 (250–273)

Seminal vesicle 132 (87–209) 9 62 (39–119) 65 (48–80) 9 33 (32–35) 61 (58–64) 9 39

Pars prostatica 411 (321–562) 241 (209–289) 209 (193–225)

Genital atrium 109 (80–128) 9 110 (90–128) 124 (96–160) 9 55 (48–64) 79 (77–80) 9 76 (71–80)

Genital lobe 61 (48–80) 9 73 (64–96) 36 (32–42) 9 48 (39–55) 32x 37 (35–39)

Rhynchus 184 (167–212) 9 141 (128–151) 189 (183–212) 9

180 (154–202)

167 (161–173) 9

159 (157 9 161)

Excretory vesicle – 853 (784–912) –

Excretory vesicle/Length – 0.78 (0.75–0.83) –

Eggs 32 (32–33) 9 16 30 (29–30) 9 15 (15–16) 26 (25–26) 9 13

60 Syst Parasitol (2009) 72:57–69

123

Figs. 1–2 1. Prosorhynchus jexi n. sp. A. Ventral view of holotype from Epinephelus quoyanus; B. Cirrus-sac, ventral view. 2.

Prosorhynchus lafii n. sp. A. Ventral view of holotype from E. fuscoguttatus; B. Cirrus-sac, ventral view. Scale-bars: A, 200 lm; B,

100 lm

Syst Parasitol (2009) 72:57–69 61

123

Ovary ovoid, dextral, overlaps but anterior to

anterior testis, overlaps caecum. Mehlis’ gland at level

of and dorsal to anterior testis. Laurer’s canal not seen.

Vitelline follicles in 2 tight lateral clusters at level of

caecum; sinistral field extends just anteriorly to

caecum. Uterus extends anteriorly to posterior margin

of vitelline follicles. Eggs small, tanned. Excretory

pore terminal; extent of excretory vesicle not seen.

Prosorhynchus robertsthomsoni n. sp.

Type-host: Cephalopholis argus Bloch & Schneider,

peacock hind (Serranidae: Epinephelinae).

Other hosts: Cephalopholis miniata (Forsskal), coral

hind, and C. cyanostigma (Valenciennes), bluespotted

hind (Serranidae: Epinephelinae).

Type-locality: Off Heron Island, Great Barrier Reef,

Australia (238270S, 1518550E).

Site: Pyloric caeca, intestine.

Type-material: Queensland Museum, Brisbane,

Australia. Holotype: QMG 224772, Paratypes:

QMG 224773 to 224781.

Etymology: This species is named for Mr Ashley

Roberts-Thomson from the University of Queens-

land, Brisbane, Australia for his field collecting

abilities, which contributed in part to the collection

of these parasites.

Description (Fig. 3)

Measurements in Table 3. Body ovoid, widest at

level of vitelline follicles; entire tegument covered

with spines. Rhynchus, small, distinctly glandular.

Pharynx spherical, small, in mid-body, not easily

seen in most specimens. Caecum sac-like, short,

extends anteriorly from pharynx, obscured by uterus

in most specimens.

Testes 2, ovoid, tandem, not contiguous, dextral,

posterior to pharynx, not overlapping, obscured by

uterus in mature specimens; anterior testis in mid-

body; posterior testis in posterior third of body.

Cirrus-sac (Fig. 3b) sinistral in posterior half of body,

muscular, relatively thick-walled. Seminal vesicle

elongate, dextral within proximal portion of cirrus-

sac. Pars prostatica straight, both highly glandular

Table 3 Measurements of Prosorhynchus spp. from Cephalopholis, Cromileptes and Variola spp. from the Great Barrier Reef

No. of specimens P. robertsthomsoni n. sp. P. conorjonesi n. sp. P. milleri n. sp.

10 10 2

Length 1,230 (1,072–1,408) 2,520 (1,904–3,360) 1,520 (1,392–1,648)

Width 264 (192–320) 176 (112–224) 200 (192–208)

Length/Width 4.78 (3.9–6.5) 14.6 (11.1–18.7) 7.6 (7.25–7.9)

Caecum 117 (90–141) 245 (193–321) 201 (193–209)

Pharynx 38 (32–45) 9 39 (32–48) 72 (58–90) 9 69 (61–87) 63 (58–67) 9 71 (64–77)

Ovary 84 (64–100) 9 82 (67–112) 89 (61–116) 9 86 (61–119) 87 (74–99) 9 74 (67–80)

Anterior testis 86 (67–106) 9 96 (80–116) 103 (83–119) 9 102 (77–128) 105 (103–106) 9 88 (80–96)

Posterior testis 83 (67–103) 9 88 (64–100) 100 (83–122) 9 97 (74–128) 95 (90–99) 9 80 (77–83)

Vitelline fields 249 (199–305) 9 300 (247–360) 497 (347–722) 9 555 (446–706) 361 (305–417) 9 437

Uterus 888 (640–1088) 1150 (896–1552) 752

Uterus/Length 0.72 (0.6–0.85) 0.46 (0.42–0.53) 0.46

Cirrus-sac 404 (350–450) 466 (376–565) 325 (289–360)

Seminal vesicle 121 (103–145) 9 49 (35–64) 157 (138–189) 9 55 (48–71) 103 (83–122) 9 52 (45–58)

Pars prostatica 390 (321–450) 588 (450–706) 273 (225–321)

Genital atrium 119 (96–135) 9 105 (80–128) 112 (96–119) 9 87 (77–96) 136 (128–144) 9 104 (96–112)

Genital lobe 55 (42–64) 9 65 (48–80) 66 (55–77) 9 65 (48–80) 105 (103–106) 9 110 (103–116)

Rhynchus 126 (116–138) 9 131 (116–148) 245 (177–305) 9 141 (112–161) 142 (132–151) 9 109 (103–114)

Excretory vesicle – – 334

Excretory vesicle/Length – – 0.24

Eggs 29 (29–30) 9 16 32 (31–32) 9 16 25 9 16

62 Syst Parasitol (2009) 72:57–69

123

and muscular distally, curved proximally to form

seminal duct, dorsal to and joins with seminal vesicle.

Ejaculatory duct narrow. Genital atrium large,

contains bilobed genital lobe. Common genital pore

subterminal on ventral surface, posterior to genital

atrium.

Figs. 3–4 3. Prosorhynchus robertsthomsoni n. sp. A. Ventral view of holotype from Cephalopholis argus; B. Cirrus-sac, ventral view. 4.

Prosorhynchus conorjonesi n. sp. A. Ventral view of holotype from Cromileptes altivelis; B. Cirrus-sac, ventral view. Scale-bars: A, 200 lm;

B, 100 lm

Syst Parasitol (2009) 72:57–69 63

123

Ovary ovoid, anterior to but overlapping anterior

testis, at level of pharynx, dextral. Mehlis’ gland and

Laurer’s canal not seen. Vitelline follicles in 2 lateral

fields, beginning at level of pharynx and extending

anteriorly into anterior third of body; both fields arc

towards longitudinal mid-line but do not meet. Uterus

extends between and slightly anterior to vitelline

follicles and posteriorly to cirrus-sac, heavily filled

with eggs, usually obscuring other body organs. Eggs

small, tanned, numerous. Excretory pore terminal;

extent of excretory vesicle obscured by uterus but not

reaching anterior to vitelline follicles.

Prosorhynchus conorjonesi n. sp.

Type-host: Cromileptes altivelis (Valenciennes),

barramundi cod (Serranidae: Epinephelinae).

Type-locality: Off Heron Island, Great Barrier Reef,

Australia (238270S, 1518550E).

Other locality: Off Lizard Island, Great Barrier Reef,

Australia (148400S, 1458280E).

Site: Pyloric caeca, intestine.

Type-material: Queensland Museum, Brisbane, Aus-

tralia. Holotype: QMG 224782, Paratypes: QMG

224783 to 224791.

Etymology: This species is named for Dr Conor

Jones, formerly of the University of Queensland,

Brisbane, Australia for his field collecting abilities,

which contributed in part to the collection of these

parasites.

Description (Fig. 4)

Measurements in Table 3. Body elongate, of almost

uniform width along entire length; entire tegument

covered with spines. Rhynchus large, with bulbous

anterior section and slender posterior section, mus-

cular and glandular. Pharynx spherical, muscular, in

anterior half of body. Caecum short, sac-like extends

anteriorly from pharynx.

Testes 2, ovoid, not contiguous, near longitudinal

mid-line; anterior testis near mid-body; posterior

testis in posterior half of body. Cirrus-sac (Fig. 4b),

sinistral in posterior quarter of body, muscular, not

thick-walled, short relative to body length. Seminal

vesicle elongate, dextro-proximal region in cirrus-

sac. Pars prostatica straight, both muscular and

glandular distally; curved proximally to form

convoluted seminal duct, joins with and is dorsal to

seminal vesicle. Ejaculatory duct narrow. Genital

atrium ovoid, contains bilobed genital lobe. Common

genital pore prominent, ventrally subterminal.

Ovary ovoid, small, just anterior to anterior testis,

near longitudinal mid-line. Mehlis’gland at level of

and dorsal to anterior testis. Laurer’s canal extends

dextrally from Mehlis’ gland. Vitelline follicles in

two lateral fields, both separated into 2 fields located

anterior and posterior to digestive system; posterior

fields begin near level of ovary and extend anteriorly

to near level of pharynx; anterior fields begin near

level of anterior margin of caecum and extend further

anteriorly into anterior third of body. Uterus extends

anteriorly only to posterior margin of anterior testis.

Eggs small, tanned, numerous. Excretory pore termi-

nal; extent of excretory vesicle not known.

Prosorhynchus milleri n. sp.

Type-host: Variola louti (Forsskal), yellow-edged

lyretail (Serranidae: Epinephelinae).

Type-locality: Off Lizard Island, Great Barrier Reef,

Australia (148400S, 1458280E).

Site: Pyloric caeca

Type-material: Queensland Museum, Brisbane,

Australia. Holotype: QMG 224798, Paratype: QMG

224799.

Etymology: This species is named for Mr Terrence

Miller of the University of Queensland, Brisbane,

Australia for his assistance in the laboratory.

Description (Fig. 5)

Measurements in Table 3. Body elongate, of similar

width along entire length; entire tegument covered

with spines. Rhynchus pyriform, with highly visible

longitudinal and lateral muscles. Pharynx spherical,

muscular, in mid-body. Caecum short, sac-like,

oriented anteriorly.

Testes 2, ovoid, tandem in posterior half of body,

not contiguous, just dextral to longitudinal mid-line.

Cirrus-sac (Fig. 5b) sinistral, in posterior third of

body, muscular, not thick-walled, extends anteriorly

as far as posterior testis. Seminal vesicle, elongate,

reniform, dextral within proximal portion of cirrus-

sac. Pars prostatica straight, muscular and glandular

distally, curved proximally to form seminal duct

64 Syst Parasitol (2009) 72:57–69

123

Figs. 5–6 5. Prosorhynchus milleri n. sp. A. Ventral view of holotype from Variola louti; B. Cirrus-sac, ventral view. 6 Neidhartiaepinepheli n. sp. A. Ventral view of holotype from Epinephelus maculates; B. Cirrus-sac, ventral view. Scale-bars: A, 200 lm; B, 100 lm

Syst Parasitol (2009) 72:57–69 65

123

which joins with and dorsal to seminal vesicle.

Ejaculatory duct narrow, straight. Genital atrium,

large, ovoid, contains large, hook-shaped genital

lobe. Common genital pore posterior to genital

atrium, with associated glands.

Ovary ovoid, dextral, anterior to but overlaps

anterior testis. Mehlis’ gland between testes. Laurer’s

canal not seen. Vitelline follicles in 2 lateral fields

which extend anteriorly from pharynx into anterior

third of body, confluent anteriorly; dextral field

longer, with gap between 3 posterior vitelline folli-

cles and rest of field, extend posteriorly to beyond

level of caecum; sinistral field does not extend

posteriorly beyond mid-caecum. Uterus extends just

anterior to pharynx. Eggs small, tanned. Excretory

pore terminal; excretory vesicle extends into poster-

ior half of body.

Neidhartia Nagaty, 1937

Neidhartia epinepheli n. sp.

Type-host: Epinephelus maculatus (Bloch), highfin

grouper (Serranidae: Epinephelinae).

Type-locality: Off Lizard Island, Great Barrier Reef,

Australia (148400S, 1458280E).

Site: Intestine.

Type-material: Queensland Museum, Brisbane,

Australia. Holotype: QMG 224800, Paratype: QMG

224801.

Description (Fig. 6)

Measurements in Table 2. Body fusiform, widest at

level of vitelline follicles; entirely covered with

spines. Rhynchus large, bulbous anteriorly, tapers

towards posterior extremity, with visible musculature

and glands. Pharynx spherical, muscular, median, in

posterior half of body. Caecum short, sac-like,

extends anteriorly from pharynx only into mid-body.

Testes 2, ovoid, tandem, dextral, muscular; poster-

ior testis posterior to but overlapping pharynx; anterior

testis anterior to but overlapping pharynx. Cirrus-sac

(Fig. 6b) sinistral in posterior half of body; anterior

extremity overlaps pharynx. Seminal vesicle elongate,

dextral in anterior part of cirrus-sac. Pars prostatica

straight, both muscular and glandular distally, curved

proximally to form seminal duct, joins with and is

dorsal to seminal vesicle. Ejaculatory duct narrow.

Genital atrium ovoid, contains small, reinform genital

lobe. Common genital pore at posterior margin of

genital atrium, ventro-subterminal.

Ovary ovoid, sinistral, at level of pharynx, inter-

testicular. Mehlis’ gland and Laurer’s canal not seen.

Uterus extends to, or anterior to, posterior margin of

rhynchus. Vitelline follicle fields obscured by uterus;

dextral field extends further than sinistral field into

anterior third of body. Eggs small, tanned. Excretory

pore terminal; extent of excretory vesicle not seen.

Discussion

Taxonomy

Five of the six species reported here belong to

Prosorhynchus Odhner, 1905 on the basis that they

possess a simple cone-like or pyriform rhynchus that

does not have any suckers, the ovary is anterior to the

testes and they have a curved pars prostatica. One

species belongs to Neidhartia Nagaty, 1937 on the

basis that it has a muscular, glandular rhynchus, a

curved pars prostatica and an intertesticular ovary

(Overstreet & Curran, 2002).

The five species of Prosorhynchus reported here had

completely non-overlapping host distributions and are

easily distinguished by the characters given in the key

(see above). In addition, the following differences have

been noted. P. jexi n. sp. differs from the other Pro-

sorhynchus species reported here by the arc-like

configuration of its vitelline fields and by the uterus

not extending anterior to the vitelline follicles. P. lafii

n. sp. differs from all other Prosorhynchus species

reported here by the clumped configuration of its

vitelline follicles and its ovary and anterior testis being

anterior to the pharynx. P. robertsthomsoni n. sp. differs

from the other Prosorhynchus species described above

by the uterus extending anteriorly and between the

vitelline follicle fields and the small size of the pharynx

relative to the body. P. conorjonesi n. sp. differs from

the other Prosorhynchus species reported here in the

configuration of its vitelline follicles, greater body

length and in the large gap between its testes. P. milleri

n. sp. differs from the other species reported here by its

reniform seminal vesicle, large genital atrium relative

to body size and its inter-testicular Mehlis’ gland.

66 Syst Parasitol (2009) 72:57–69

123

We compared the five new species of Prosorhyn-

chus with those species of the genus that have been

reported from the Great Barrier Reef and with species

from epinephelines that bear a superficial resemblance

to them. In this we have been influenced strongly by

our understanding of the host-specificity of these

species. During the course of this work, we have

examined over 1,500 teleosts from the Great Barrier

Reef representing other families susceptible to

infection with bucephalids (Apogonidae, Belonidae,

Blenniidae, Carangidae, Labridae, Muraenidae, Scom-

bridae, Sphyraenidae and Synodontidae) without ever

finding any of the species reported here. We conclude

that it is highly unlikely that any of these species infect

non-serranids. Below we compare the five new species

with the 11 species of Prosorhynchus from epineph-

eline serranids that most closely resemble them.

Prosorhynchus epinepheli Yamaguti, 1939 was

originally described from Epinephelus akaara from

off Japan and was subsequently reported from E.

merra from off Heron Island on the Great Barrier

Reef by Durio & Manter (1968). As described by

Yamaguti (1939), this species resembles P. jexi n. sp.

but differs from it in having oblique rather than

tandem testes and by its vitelline follicles reaching

the posterior margin of the rhynchus, whereas the

vitelline follicles of P. jexi reach only into the

anterior quarter of the body and not to the rhynchus.

We are confident that these two species are distinct.

We have examined eight E. merra from the Great

Barrier Reef and have not recovered any bucephalid

species. E. merra and E. quoyanus are similar species

that are often confused (see Grant, 1978; Johnson,

1999). In addition, E. quoyanus is a far more common

species than E. merra off Heron Island, where Durio

& Manter’s specimens were collected. Durio &

Manter (1968) did not figure P. epinepheli from E.

merra or provide a description. We examined the one

known museum specimen of P. epinepheli from the

Durio & Manter (1968) study (H.W. Manter Labo-

ratory of Parasitology, Collection Acc. No. 31206)

and confirm that it is P. jexi. As a result of these

considerations we conclude that it is likely that they

examined E. quoyanus and the species of Prosorhyn-

chus they reported was P. jexi n. sp. We therefore

propose that P. epinepheli of Durio & Manter (1968)

should be considered conspecific with P. jexi.

Other species of bucephalids from epinephelines

that resemble the present species can be distinguished

as follows. P. thapari Manter, 1953 was described

from Plectropoma maculatum (probably Pl. leopar-

dus) (see Grant, 1978) from off Fiji (Manter, 1953).

We examined specimens of P. thapari from the H.W.

Manter Laboratory of Parasitology (Collection Acc.

No. 580) to confirm that it was not one of the six

species reported here. It resembles P. milleri n. sp.

but differs in that its convoluted seminal duct passes

ventrally over the seminal vesicle before recurving,

while in P. milleri the seminal duct is always dorsal

to seminal vesicle; and by the shape of the rhynchus,

with P. thapari having a more elongate posterior

section than that of P. milleri. P. caudovatus Manter,

1940 has been described from numerous epinepheline

species (Bray, 1984; Fischthal, 1980; Fischthal &

Thomas, 1968; Manter, 1940) but it differs from all

five new species in possessing filamentous eggs. P.

serrani Durio & Manter, 1968 was described from off

New Caledonia in Serranus louti (now Variola louti).

We examined type-specimens of P. serrani from the

H.W. Manter Laboratory of Parasitology (Collection

Acc. No. 588) and found that it most closely

resembles P. milleri n. sp. (also from Variola louti),

but differs by having a uterus that extends anterior to

the vitelline follicles into the anterior quarter of the

body. P. ozakii Manter, 1934 was described from E.

niveatus and differs from all five new species in

having an intertesticular ovary, which also suggests

that the generic status of the species needs reconsid-

eration; we propose that type-material be examined to

determine the generic identity of this species. P. lafii

n. sp. is similar to P. atlanticus Manter, 1940, P.

pacificus Manter, 1940, P. promicropsi Manter, 1940

and P. gonoderus Manter, 1940 in general appear-

ance; however, it differs from P. atlanticus and P.

pacificus in that they have vitelline follicles arranged

in lateral fields as opposed to being clumped in P.

lafii; from P. promicropsi by the more anterior

position of its vitelline follicles, ovary and testes; and

from P. gonoderus by the ovary being dextral. P. jupe

(Kohn, 1967) differs from all five new species in that

its vitelline follicle fields are at different levels, the

sinistral field being posterior to the pharynx, whereas

the dextral field is anterior to the pharynx. P.

maternus Bray & Justine, 2006 differs from P. jexi

n. sp., P. robertsthomsoni n. sp. and P. milleri n. sp.

in that its uterus does not extend past the anterior

margin of the ovary; from P. lafii n. sp. by the

vitelline follicles being arranged in lateral fields; and

Syst Parasitol (2009) 72:57–69 67

123

from P. conorjonesi n. sp. in that the vitelline fields

extend to, and the pharynx is at, the level of the

testes.

Neidhartia epinepheli n. sp. differs from all

previously described species of Neidhartia. 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 n.

sp. differs by having a caecum that does not extend

into the anterior third of the body and the eggs

are smaller, 25–26 9 12–13 lm, compared with

30 9 15 lm for N. neidharti (see Nagaty, 1937).

Patterns of infection

We have examined five of 26 species of Cephalop-

holis and found only one bucephalid species, P.

robertsthomsoni n. sp., and it occurred in three of

them, C. argus, C. cyanostigma and C. miniata. We

have examined 33 specimens of Ce. boenak from the

Great Barrier Reef and never found any bucephalids,

and conclude that P. robertsthomsoni does not infect

this species. This is apparently the first record of a

bucephalid from species of Cephalopholis. The rarity

of bucephalids in this genus stands in stark contrast to

the rich fauna in species of Epinephelus. There are

two species of Variola on the Great Barrier Reef, of

which we have examined only two individuals of V.

louti and found only one species, P. milleri n. sp., that

is restricted to this host plus two other species

commonly found in Plectropomus species; however,

we have only found one specimen of each of the latter

from one individual host.

Although some bucephalid species have been

collected only in low numbers (P. lafii n. sp. and N.

epinepheli n. sp.), perhaps what is most striking is the

number of hosts in which these bucephalids appear to

be absent. We have never found these seemingly rare

species in any of the 59 examinations of Plectrop-

omus spp. or the 83 examinations of Cephalopholis

spp. All six species described here have each only

been found in one host genus, albeit three species of

Cephalopholis for P. robertsthomsoni n. sp.

For Epinephelus, the most speciose epinepheline

genus with 23 species common from Great Barrier

Reef waters, we have described three bucephalid

species from two genera, and we know of one other

Prosorhynchus from E. fuscoguttatus which we have

not described here because we have only one

specimen. Species of Epinephelus have different

diets, ranging from primarily fish to a mixture of

fishes, crustaceans and molluscs (Blaber et al., 1990;

Connell, 1998; Heemstra & Randall, 1993). The

transmission of bucephalids relies on the piscivory of

the second intermediate host, so it is likely that some

species of Epinephelus do not eat enough fish or the

correct species of fish to maintain bucephalid infec-

tions (see Table 1, E. fasciatus), although it is

probable that there are more bucephalid species in

Epinephelus spp. still to be discovered from the Great

Barrier Reef.

Acknowledgements The authors thank Dr Rob Adlard, Dr

Rod Bray, Dr Matt Nolan, Ashley Roberts-Thomson, Jon

Yantsch, Barton McKenzie, Dr Tim Lucas and Dr Conor Jones

for field assistance. We would also like to thank Trudy Burge

for all her assistance. We thank the staff of the Heron Island

and the Lizard Island Research Stations. We are grateful to the

staff of the H. W. Manter Laboratory for Parasitology Museum

for lending us specimens.

References

Blaber, S. J. M., Milton, D. A., Rawlinson, N. J. F., Tiroba, G.,

& Nichols, P. V. (1990). Diets of lagoon fishes of the

Solomon Islands: Predators of tuna baitfish and trophic

effects of baitfishing on the subsistence fishery. FisheriesResearch, 8, 263–286.

Bray, R. A. (1984). Some helminth parasites of marine fishes

and cephalopods of South Africa: Aspidogastrea and the

digenean families Bucephalidae, Haplosplanchnidae,

Mesometridae and Fellodistomidae. Journal of NaturalHistory, 18, 271–292.

Connell, S. D. (1998). Patterns of piscivory by resident pred-

atory reef fish at One Tree Reef, Great Barrier Reef.

Marine and Freshwater Research, 49, 25–30.

Cribb, T. H., Bray, R. A., Wright, T., & Pichelin, S. (2002).

The trematodes of groupers (Serranidae: Epinephelinae):

Knowledge, nature and evolution. Parasitology, 124,

S23–S42.

Durio, W. O., & Manter, H. W. (1968). Some digenetic

trematodes of marine fishes of New Caledonia. Part I.

Bucephalidae, Monorchiidae, and some smaller families.

Proceedings of the Helminthological Society of Wash-ington, 35, 143–153.

Fischthal, J. H. (1980). Some digenetic trematodes of marine

fishes from Israel’s Mediterranean coast and their zoo-

geography, especially those from Red Sea immigrant

fishes. Zoologica Scripta, 9, 11–23.

Fischthal, J. H., & Thomas, J. D. (1968). Digenetic trematodes

of marine fishes from Ghana: Families Acanthocolpidae,

Bucephalidae, Didymozoidae. Proceedings of the Hel-minthological Society of Washington, 35, 237–247.

Grant, E. M. (1978). Guide to fishes. Brisbane: The Department

of Harbours and Marine, 768 pp.

68 Syst Parasitol (2009) 72:57–69

123

Heemstra, P. C., & Randall, J. E. (1993). FAO Species Cata-logue. Groupers of the world (Family Serranidae,Subfamily Epinephelinae). An annotated and illustratedcatalogue of the grouper, rockcod, hind, coral grouperand lyretail ppecies. Rome: FAO, 382 pp.

Johnson, J. W. (1999). Annotated checklist of the fishes of

Moreton Bay, Queensland, Australia. Memoirs of theQueensland Museum, 43, 709–762.

Manter, H. W. (1940). Gasterostomes (Trematoda) of Tortugas,

Florida. Papers from the Tortugas Laboratory of theCarnegie Institute of Washington, 33, 1–19.

Manter, H. W. (1953). Two new species of Prosorhynchinae

(Trematoda: Gasterostomata) from the Fiji Islands. In J.

Dayal & K. Suresh Singh (Eds.), Thapar CommemorationVolume 1953: a collection of articles presented to Prof.G. S. Thapar on his Sixtieth Birthday (pp. 193–200).

Lucknow.

Nagaty, H. F. (1937). Trematodes of fishes from the Red Sea,Part I. Studies on the Family Bucephalidae Poche, 1907.

Cairo: Egyptian University, 172 pp.

Overstreet, R. M., & Curran, S. S. (2002). Superfamily

Bucephaloidea Poche, 1907. In D. I. Gibson, A. Jones &

R. A. Bray (Eds.), Keys to the digenean parasites ofvertebrates (Vol. 1, pp. 67–110). Wallingford: CAB

International.

Randall, J. E., Allen, G. R., & Steene, R. C. (1997). Thecomplete divers’ and fishermen’s guide to fishes of theGreat Barrier Reef. Bathurst: Crawford House Publishing,

557 pp.

Yamaguti, S. (1939). Studies on the helminth fauna of Japan.

Part 26. Trematodes of fishes, VI. Japanese Journal ofZoology, 8, 211–230.

Syst Parasitol (2009) 72:57–69 69

123