Diversity of trypanorhynch metacestodes in teleost fishes from coral reefs off eastern Australia and New Caledonia.

Trypanorhynch metacestodes were examined from teleosts from coral reefs in eastern Australia and from New Caledonia. From over 12,000 fishes examined, 33 named species of trypanorhynchs were recovered as well as three species of tentacularioids which are described but not named. Host-parasite and parasite-host lists are provided, including more than 100 new host records. Lacistorhynchoid and tentacularioid taxa predominated with fewer otobothrioid and gymnorhynchoids. Five species, Callitetrarhynchus gracilis, Floriceps minacanthus, Pseudotobothrium dipsacum, Pseudolacistorhynchus heroniensis and Ps. shipleyi, were particularly common and exhibited low host specificity. Limited data suggested a higher diversity of larval trypanorhynchs in larger piscivorous fish families. Several fish families surveyed extensively (Blenniidae, Chaetodontidae, Gobiidae, Kyphosidae and Scaridae) yielded no trypanorhynch larvae. The overall similarity between the fauna of the Great Barrier Reef and New Caledonia was 45%. Where available, information on the adult stages in elasmobranchs has been included. © I. Beveridge et al., published by EDP Sciences, 2014.

Introduction

The identification of significant threats to the coral reefs of the world [9, 17] has been partly responsible for focussing attention on the full diversity of reefs rather than simply on the diversity of fish and corals, the most obvious examples of reef diversity. The contributions of other groups of invertebrates to diversity on reefs have been largely overlooked in the past [7, 32]. Part of this “hidden” invertebrate diversity includes the endoparasites of vertebrates.

In recent years, teleost fish occurring on coral reefs have been recognised as harbouring a particularly diverse array of parasites [20]. Studies to date have focussed either on specific parasite groups such as the Monogenea (e.g. [33]) or Digenea (e.g. [13]), or more recently have examined the diversity of all helminth parasites found in or on specific families of fish such as the Lethrinidae or Serranidae [21-23].

Teleosts found on coral reefs are commonly infected with the larval stages (plerocerci, merocerci or plerocercoids – for terminology see Chervy, 2002 [12]) of cestodes of the order Trypanorhyncha, the adults of which are found in the stomach or spiral valves of elasmobranchs. Larval stages occur most commonly in the body cavity but may also be found in the musculature or other sites such as the gill arches [27]. They constitute a significant component of parasite diversity but have frequently been overlooked because of taxonomic difficulties in identification [27]. However, unlike other orders of cestodes found in marine fish, the larval stages have scolex features, including the distinctive tentacular armature, which are identical to those found in the adult and which allow specific morphological identification. Although taxonomic studies of this group of parasites are frequent, ecological studies are few, and while systematic collecting has been undertaken in several parts of the world (Gulf of Mexico, Gulf of California, Java, Borneo, Australia and Hawaii), there are few published descriptions of the faunas encountered in these areas (see Jensen, 2009 [19] for Gulf of Mexico and Palm and Bray, 2014 [29] for Hawaii). Some species of trypanorhynchs (e.g. Grillotia (Christianella) minuta van Beneden, 1858; Gilquinia squali Fabricius, 1794) have also been used as biological tags in teleosts [25] because the larval stages are readily identifiable and because they are long-lived in the intermediate host. However, such ecological studies of these species are limited.

In this study, we examined the larval trypanorhynch cestode parasites of teleosts, and where applicable the corresponding adults in elasmobranchs, from the Great Barrier Reef (GBR) and compared them with those from similar reef environments in New Caledonia (NC). New Caledonia is separated from the GBR by about 1200 km of deep oceanic waters.

Materials and methods

Great Barrier Reef (GBR)

Teleosts and elasmobranchs were collected opportunistically between 1986 and 2010. The two main collecting sites were Heron Island in the southern Great Barrier Reef and Lizard Island in the Northern Barrier Reef. Small numbers of parasites were collected on reefs between these two sites (Mossman, Townsville) and in these instances, the nearest geographical feature on the coast was recorded rather than the specific reef near which the collection was made (Fig. 1).

Figure 1.

Collection localities off the east coast of Australia and New Caledonia.

Metacestodes were collected mainly from body cavities of teleosts, although in some instances they were sought in regions of the body such as the gill arches and musculature. Metacestodes were removed from surrounding cysts (in the case of plerocerci) and the eversion of tentacles was achieved either by shaking vigorously or by applying pressure under a coverslip. Cestodes were fixed in 70% ethanol or 10% formalin and were stained with Celestine blue or carmine (Palm, 2004) [27], dehydrated in ethanol, cleared in methyl salicylate and mounted in Canada balsam. All specimens were identified by IB and have been deposited in either the British Museum (Natural History) (BMNH), the Queensland Museum, Brisbane (QM) or the South Australian Museum, Adelaide (SAM). Some of the records used in this compilation have been published previously in Beveridge & Campbell, 1996, 2001 [1, 3], Beveridge et al., 2000, 2007 [4, 5], Campbell & Beveridge, 1996 [8], Palm, 2004 [27], Palm & Beveridge, 2002 [28] and Sakanari, 1989 [34].

Records of adults from elasmobranchs are included only for species in which larval stages have been identified in teleosts; these are based on both published data and specimens held in museum collections. Additional species of trypanorhynch cestodes from elasmobranchs have been found and their larval stages may be found in the future, but for the present study, these records have not been added.

New Caledonia (NC)

Fish were collected opportunistically between 2003 and 2009 generally by line fishing, occasionally by spear fishing and on occasions supplemented by fish obtained from a market. Collections were mainly off Nouméa (Fig. 1). All fish were measured, weighed and photographed. Methods for collection from several host families have been explained elsewhere [21-23]. Trypanorhynch plerocerci were opened and compressed between two slides or immersed in hot saline to evert tentacles. Plerocercoids found in the body cavity were also fixed under pressure to evert tentacles. Metacestodes were fixed in 70% ethanol or 10% formalin and were stained with Celestine blue or carmine [27], dehydrated in ethanol, cleared and mounted in Canada balsam. All specimens were identified by IB and have been deposited in the Muséum national d’Histoire naturelle, Paris (MNHN). Particular difficulties were encountered in the identification of tentaculariid cestodes from New Caledonia. Consequently, brief descriptions, some measurements and illustrations of each unidentified species encountered are included. Drawings were made with a drawing tube attached to an Olympus BH 2 microscope. Representative, rather than comprehensive, measurements were made with an ocular micrometer and are presented in micrometers.

In the parasite-host list (Table 1), authorities of cestodes are included and host species are listed in alphabetical order without authorities. In instances where both generic and specific names of cestodes have changed, synonyms have been included. In the host-parasite list (Table 2), fish hosts are arranged in orders, families and genera, but within each group, the order is alphabetical. Authorities of fish are indicated and the parasites are arranged in alphabetical order without authorities.

Table 1.

Parasite-host list. Species of trypanorhynch cestodes collected from teleosts and elasmobranchs on the Great Barrier Reef, Australia and from New Caledonia. Authorities of cestodes are included and host species are listed in alphabetical order without authorities.

	Great Barrier Reef	New Caledonia
GYMNORHYNCHOIDEA
Molicola horridus (Goodsir, 1841)
Larval
Diodon hystrix	HA QMC G206954, SAME 44079	Diodon hystrix	MNHND JNC2977D1, 3199C
Diodon liturosus *	LB QM G232552
Pterobothrium lintoni MacCallum, 1916
Larval
Choerodon venustus	H SAM 40480
Pterobothrium acanthotruncatum
Escalante & Carvajal, 1984
Larval
Plectropomus maculatus*	H QM G217640
Scomberomorus commerson	H, L QM G217628
Adult
Pristis zijsron*	TvG SAM 35749
Pterobothrium australiense Campbell & Beveridge, 1996
Larval
Halichoeres trimaculatus*	H QM G217629
Adult
Pristis zijsron	Tv SAM 23898
Pterobothrium pearsoni (Southwell, 1929)
Larval
Sphyraena jello *	L QM G233646
LACISTORHYNCHOIDEA
Bombycirhynchus sphaerenaicum (Pintner, 1930)
Larval
Sphyraena jello*	L QM G233583
Callitetrarhynchus gracilis (Rudolphi, 1819)
Larval
Abudefduf whitleyi*	H QM G212162	Atule mate*	MNHN JNC2814T, 2963, 2964, 2965, 3371
Apogon poecilopterus*	H QM G217587	Carangoides fulvoguttatus*	MNHN JNC463C
Caesio cuning*	H QM G217593	Caranx papuensis*	MNHN JNC1189E
Cephalopholis miniata	H QM G232625	Cephalopholis boenak	[20]J
Cephalopholis cyanostigma*	H, L QM G217575	Cephalopholis spiloparaea*	MNHN JNC2624
Choerodon cyanodus*	H BM 1980.7.10.148–9	Chirocentrus dorab	MNHN JNC3220
Cromileptes altivelis*	H QM G217592	Epinephelus chlorostigma	MNHN JNC2446C
Johnius borneensis*	H QM G217602	Epinephelus fasciatus*	MNHN JNC1256A, 2625, 3039
Lotella rhacina*	H QM G217574	Epinephelus retouti*	MNHN JNC3083
Lutjanus carponotatus*	L QM G233588	Epinephelus rivulatus	MNHN JNC2606C
Naso vlamingii*	H QM G217598	Lethrinus miniatus*	MNHN JNC2113A
Ostorhinchus fasciatus*	H QM G217486	Lutjanus vitta	[22]J
Plectropomus maculatus*	H QM G217641	Megalaspis cordyla	MNHN JNC1186, 1188
Polynemus heptadactyla*	H QM G217591	Nemipterus furcosus	MNHN JNC2596
Pomatomus saltatrix	H QM G217583	Scomberomorus commerson	MNHN JNC435
Scomberomorus commerson	H, L QM G212163	Triodon macropterus*	MNHN JNC2984
Scomberomorus queenslandicus*	H QM G217588	Variola louti	[20]J
Sphyraena obtusata*	H QM G217590
Adult
Carcharhinus melanopterus	H QM G217581	Carcharhinus leucas	MNHN JNC2856
Carcharhinus amblyrhynchoides	SiH SAM 24941
Callitetrarhynchus speciosus (Linton, 1897)
Larval		Cymbacephalus beauforti*	MNHN JNC1833
Dasyrhynchus basipunctatus (Carvajal, Campbell & Cornford, 1976)
Fistularia commersonii*	H QM G232633	Abalistes filamentosus*	MNHN JNC2193
		Abalistes stellatus	MNHN JNC2163, 2926, 2914
		Diodon hystrix	MNHN JNC2977
		Lagocephalus sceleratus*	MNHN JNC2942
		Pseudobalistes fuscus*	MNHN JNC1680E, 2164, 2940
		Triodon macropterus*	MNHN JNC2989
Adult
Carcharhinus brachyurus	L QM G232540	Carcharhinus amblyrhynchos	MNHN JNC435, 1111
Carcharhinus melanopterus*	H QM G232634	Carcharhinus plumbeus*	MNHN JNC442
Diesingium cf lomentaceum (Diesing, 1850)
Larval
		Carangoides fulvoguttatus*	MNHN JNC3169
		Epinephelus chlorostigma*	MNHN JNC3142
Floriceps minacanthus Campbell & Beveridge, 1987
Larval
Cephalopholis boenak*	H QM G212151–3	Cephalopholis miniata	MNHN JNC2627
Cephalopholis cyanostigma*	L QM G233613	Cephalopholis sonnerati*	MNHN JNC2934, 2935, 2936, 3029
Cephalopholis miniata	H QM G217615	Cephalopholis urodeta	[20]J
Epinephelus quoyanus	H SAM 44083	Epinephelus coioides	MNHN JNC3257
Euthynnus affinis	H QM G217612, 7	Epinephelus cyanopodus	MNHN JNC1998
Euthynnus alletteratus*	H SAM 44082	Epinephelus maculatus*	MNHN JNC2937, 3061, 3062, 3066
Grammatorcynus bicarinatus*	H, L QM G217613	Lethrinus miniatus*	MNHN JNC2706A
Lethrinus miniatus*	H QM G233554	Nemipterus furcosus	MNHN JNC3019
Plectropomus areolatus*	L QM G233626	Plectropomus leopardus	MNHN JNC2585A
Plectropomus leopardus	H, L QM G217611, SAM 32139	Plectropomus laevis	MNHN JNC1887
Sphyraena flavicauda*	H QM G217616	Sphyraena putnamae*	MNHN JNC3035
Sphyraena jello*	L QM G233610	Tylosurus crocodilus*	MNHN JNC1262C, 1263A
Tylosurus crocodilus*	H QM G217614	Variola louti	MNHN JNC1859B, 3037
Adult
Carcharhinus amboinensis	StLI SAM 22652	Carcharhinus leucas*	MNHN
		Triaenodon obesus*	MNHN
Floriceps saccatus (Cuvier, 1817)
Larval
Diodon hystrix	H SAM 44081	Caranx papuensis*	MNHN JNC3209
Diodon liturosus*	L QM G232554	Diodon hystrix	MNHN JNC2343, 2977, 3199
Grillotiella exile (Linton, 1909)
Larval
Scomberomorus commerson	L QM G233632
Adult		Galeocerdo cuvier	MNHN JNC1414
Microbothriorhynchus coelorhynchi Yamaguti, 1952
Larval		Conger cinereus*	MNHN JNC2993
Pseudogilquinia microbothria (MacCallum, 1917)
(= Ps. magna; = Dasyrhynchus magnus)
Larval
Lethrinus atkinsoni*	L QM G233653	Lethrinus miniatus*	MNHN JNC2113 B1, 2158C
Lethrinus nebulosus*	L QM G233654
Pseudogilquinia pillersi (Southwell, 1929)
Larval
Lethrinus atkinsoni	H BMF 2004.3.18.98–99	Epinephelus coioides	MNHN JNC1535, 3140, 3265B
Lethrinus miniatus	H BM 2004.3.18.97	Plectropomus laevis	MNHN JNC1865, 1887
Lethrinus nebulosus	L QM G233653	Epinephelus malabaricus	MNHN JNC1536
Pseudolacistorhynchus heroniensis (Sakanari, 1989)
Larval
Cephalopholis miniata*	H QM G212146	Abalistes filamentosus*	MNHN JNC2724
Epinephelus fasciatus	H QM G217518, SAM 17418	Abalistes stellatus*	MNHN JNC2163, 2914, 2926
Epinephelus ongus*	H QM G214949	Cephalopholis boenak	MNHN JNC2889, 2890, 3205
Epinephelus quoyanus	H QM G212157, SAM 28629	Cephalopholis sonnerati*	MNHN JNC2934
Lethrinus miniatus*	H QM G212154	Gymnocranius grandoculis*	MNHN JNC1726
Lethrinus nebulosus	H [24]J	Epinephelus chlorostigma	MNHN JNC2446C, 3141
Plectropomus leopardus	H QM G212158, SAM 28681	Epinephelus coioides*	MNHN JNC3257
		Epinephelus cyanopodus	[20]J
		Epinephelus fasciatus	MNHN JNC1636A, 1758, 1791, 1792, 3039
		Epinephelus howlandi*	MNHN JNC2768
		Epinephelus polyphekadion	MNHN JNC1915C, 3036
		Epinephelus rivulatus	MNHN JNC1545C
		Lethrinus miniatus*	MNHN JNC2161C
		Lutjanus vitta*	[22]J
		Plectropomus leopardus	MNHN JNC3279
		Pseudobalistes fuscus*	MNHN JNC2164, 2940B
Adult		Stegostoma fasciatum	MNHN JNC1529
Pseudolacistorhynchus shipleyi (Southwell, 1929)
(= Grillotia overstreeti Sakanari, 1989)
Larval
Cephalopholis boenak*	H QM G232626	Cephalopholis sonnerati*	MNHN JNC3032
Cephalopholis cyanostigma*	H, L QM G214957	Cephalopholis urodeta	[20]J
Choerodon cyanodus	H SAM 17416, QM G212160	Epinephelus polyphekadion*	MNHN JNC3036
Choerodon fasciatus*	H QM G217519	Sufflamen fraenatus*	MNHN JNC1421C, 1797, 1798A, 1946, 2928, 3034
Epinephelus ongus*	H QM G212161	Epinephelus ongus*	MNHN JNC3275
Lotella rhacina*	H QM G214995
Rhinecanthus aculeatus*	L QM G232542
Sufflamen fraenatus*	H QM G217520
OTOBOTHRIOIDEA
Otobothrium alexanderi Palm, 2004
Larval
Tylosurus crocodilus	L QM G232555	Tylosurus crocodilus	MNHN JNC1968
Otobothrium parvum Beveridge & Justine, 2007
Larval		Epinephelus maculatus*	MNHN JNC1405
		Lethrinus rubrioperculatus*	MNHN JNC1635A
Adult		Carcharhinus amblyrhynchos	MNHN JNC1111
		Triaenodon obesus	MNHN JNC2109
Otobothrium penetrans Linton, 1907
Larval†		Tylosurus crocodilus	MNHN JNC1968
Proemotobothrium southwelli Beveridge & Campbell, 2001
Larval
Johnius borneensis	H QM G217939
Pseudotobothrium dipsacum (Linton, 1897)
Larval
Abalistes stellatus	H QM G217928–32	Abalistes filamentosus*	MNHN JNC2724
Cephalopholis cyanostigma	H QM G214959	Abalistes stellatus	MNHN JNC2914
Cheilinus trilobatus	L QM G233555	Cephalopholis miniata*	MNHN JNC2627
Epinephelus coioides	Tv SAM 31342	Cephalopholis sonnerati*	MNHN JNC1616, 2934–6
Lethrinus obsoletus	H QM G233888	Cephalopholis urodeta	MNHN JNC2750
Lutjanus gibbus	L QM GL 10508	Cymbacephalus beauforti*	MNHN JNC1833A
Naso vlamingii	H QM G214960	Epinephelus coioides	MNHN JNC1535, 3257
Plectropomus leopardus	H, L QM G217936	Epinephelus fasciatus*	MNHN JNC1791, 3039
Plectropomus maculatus	H QM G206964	Epinephelus malabaricus	[20]J
Pseudocaranx dentex	H QM G214961	Epinephelus retouti*	MNHN JNC2179
Rhinecanthus aculeatus	L QM G232590	Plectropomus laevis*	MNHN JNC1865, 1887
Rhinecanthus rectangulus	H QM G217934	Plectropomus leopardus	MNHN JNC2126
		Pseudobalistes fuscus*	MNHN JNC2927, 2940
		Variola louti	MNHN JNC1629, 1662, 1756–7, 1859, 2116–7, 2301, 3037, 3069
Symbothriorhynchus tigaminacanthus Palm, 2004
Larval		Nemipterus furcosus*	MNHN JNC2586, 2610
		Saurida undosquamis*	MNHN JNC2079
Adult		Sphyrna lewini	MNHN JNC1628
TENTACULARIOIDEA
Hepatoxylon trichiuri
Larval
Diodon hystrix*	H QM G227128	Diodon hystrix*	MNHN JNC2977, 3199D
		Tetrapterus angustirostris*	MNHN JNC1399
		Thunnus obesus*	MNHN JNC1398
Adult†		Prionace glauca*	MNHN JNC1217
Heteronybelinia estigmena (Dollfus, 1960)
Larval
Sarda australis	H QM G218042–6	Atule mate*	MNHN JNC2963–5
		Herklotsichthys quadrimaculatus*	MNHN JNC2669B, 2673, 2943, 2949
		Selar crumenophthalmus	MNHN JNC3043–4, 3126
		Sphyraena putnamae*	MNHN JNC3035
		Trichiurus lepturus*	MNHN JNC3045–6, 3048
Adult
Carcharhinus sp.	Qld SAM 18322	Carcharhinus brevipinna	MNHN JNC3138
Heteronybelinia sp. C
Larval		Sufflamen fraenatus	MNHN JNC3034
Myxonybelinia southwelli (Palm & Walter, 1999)
Larval
Choerodon venustus	H QM G218062
Adult		Stegostoma fasciatum	MNHN JNC1529
Nybelinia aequidentata Shipley & Hornell, 1906
Larval
		Dendrochirus zebra*	QM G218031
Nybelinia basimegacantha Carvajal, Campbell & Cornford, 1976
Larval
Parupeneus bifasciatus*	L QM G232545	Neoniphon sammara*	MNHN JNC2552
		Parupeneus multifasciatus	MNHN JNC2111
Nybelinia goreensis Dollfus, 1960
Larval		Lethrinus genivittatus*	MNHN JNC2033
		Lethrinus rubrioperculatus*	MNHN JNC1148
		Nemipterus furcosus	MNHN JNC2612
		Parupeneus barberinus*	MNHN JNC1838B
		Parupeneus multifasciatus*	MNHN JNC2112
Nybelinia indica Chandra, 1986
(= Nybelinia scoliodoni Vijayalakshmi, Vijayalakshmi & Gangadharam, 1996)
Larval
Diodon hystrix	H QM G218034–41	Caranx sexfasciatus	MNHN JNC3194
		Diodon hystrix	MNHN JNC2977F
		Lagocephalus sceleratus*	MNHN JNC2982
		Leiognathus fasciatus*	MNHN JNC2921
		Nemipterus furcosus*	MNHN JNC2288, 2611, 3016
Adult
Taeniura lymma	H SAM 17646	Triaenodon obesus*	MNHN JNC2109B1
Nybelinia queenslandensis Jones & Beveridge, 1998
Larval
Ostorhinchus cookii*	H QM G232539	Nemipterus furcosus*	MNHN JNC3011–2
Ostorhinchus properuptus*	L QM G2336644
Adult
Carcharhinus melanopterus	H, L QM G217521–31
Nybelinia strongyla Dollfus, 1960
Larval
Johnius borneensis	H QM G218109
Nybelinia sp. A
Larval		Herklotsichthys quadrimaculatus	MNHN JNC2669C
Nybelinia sp. B
Larval		Parupeneus multifasciatus	MNHN JNC2172C

Reported in the literature from Australia but outside the region of the Great Barrier Reef.

New host records.

Heron Island, Great Barrier Reef.

Lizard Island, Great Barrier Reef.

Queensland Museum, Brisbane.

Muséum national d’Histoire naturelle, Paris.

South Australian Museum, Adelaide.

British Museum, Natural History, London.

Townsville, Queensland.

Snapper Island, Mossman.

St Lawrence, Queensland.

Published report not supported by museum specimen.

Table 2.

Species of trypanorhynch cestodes collected from teleosts on the Great Barrier Reef, Australia and from New Caledonia. Authorities of fish are included and cestodes are listed in alphabetical order without authorities. GBR: Great Barrier Reef; NC: New Caledonia.

Order	Family	Host species	Parasites	Location
Anguilliformes	Congridae	Conger cinereus Rüppell, 1830	Microbothriorhynchus coelorhynchi	NC
Aulopiformes	Synodontidae	Saurida undosquamis (Richardson, 1848)	Symbothriorhynchus tigaminacanthus	NC
Beloniformes	Belonidae	Tylosurus crocodilus (Péron & Lesueur, 1821)	Floriceps minacanthus	GBR, NC
			Otobothrium alexanderi	GBR, NC
			Otobothrium penetrans	NC
Beryciformes	Holocentridae	Neoniphon sammara (Forsskål, 1775)	Nybelinia basimegacantha	NC
Clupeiformes	Chirocentridae	Chirocentrus dorab (Forsskål, 1775)	Callitetrarhynchus gracilis	NC
	Clupeidae	Herklotsichthys quadrimaculatus (Rüppell, 1837)	Heteronybelinia estigmena	NC
			Nybelinia sp. A	NC
Gadiformes	Moridae	Lotella rhacina (Forster, 1801)	Callitetrarhynchus gracilis	GBR
			Pseudolacistorhynchus shipleyi	GBR
Perciformes	Acanthuridae	Naso vlamingii (Valenciennes, 1835)	Callitetrarhynchus gracilis	GBR
			Pseudotobothrium dipsacum	GBR
	Apogonidae	Apogon poecilopterus Cuvier, 1828	Callitetrarhynchus gracilis	GBR
		Ostorhinchus cookii (Macleay, 1881)	Nybelinia queenslandensis	GR
		Ostorhinchus fasciatus (White, 1790)	Callitetrarhynchus gracilis	GBR
		Ostorhinchus properuptus (Whitley, 1964)	Nybelinia queenslandensis	GBR
	Carangidae	Atule mate (Cuvier, 1833)	Callitetrarhynchus gracilis	NC
			Heteronybelinia estigmena	NC
		Carangoides fulvoguttatus (Forsskål, 1775)	Callitetrarhynchus gracilis	NC
			Diesingium cf lomentaceum	NC
		Carangoides sexfasciatus Quoy & Gaimard, 1825	Nybelinia indica	NC
		Caranx papuensis Alleyne & Macleay, 1877	Callitetrarhynchus gracilis	NC
			Floriceps saccatus	NC
		Megalaspis cordyla (Linnaeus, 1758)	Callitetrarhynchus gracilis	NC
		Pseudocaranx dentex (Bloch & Schneider, 1801)	Pseudotobothrium dipsacum	GBR
		Selar crumenophthalmus (Bloch, 1793)	Heteronybelinia estigmena	NC
		Tetrapterus angustirostris Tanka, 1915	Hepatoxylon trichiuri	NC
	Labridae	Cheilinus trilobatus (Lacépède, 1801)	Pseudotobothrium dipsacum	GBR
		Halichoeres trimaculatus (Quoy & Gaimard, 1834)	Pterobothrium australiense	GBR
		Choerodon cyanodus (Richardson, 1843)	Callitetrarhynchus gracilis	GBR
			Pseudolacistorhynchus shipleyi	GBR
		Choerodon fasciatus (Günther, 1867)	Pseudolacistorhynchus shipleyi	GBR
		Choerodon venustus (De Vis, 1884)	Myxonybelinia southwelli	GBR
			Pterobothrium lintoni	GBR
	Leiognathidae	Leiognathus fasciatus (Lacépède, 1803)	Nybelinia indica	NC
	Lethrinidae	Lethrinus atkinsoni Seale, 1910	Pseudogilquinia microbothria	GBR
			Pseudogilquinia pillersi	GBR
		Lethrinus genivittatus Valenciennes, 1830	Nybelinia goreensis	NC
		Lethrinus miniatus (Forster, 1801)	Callitetrarhynchus gracilis	NC
			Floriceps minacanthus	GBR, NC
			Pseudolacistorhynchus heroniensis	GBR, NC
			Pseudogilquinia microbothria	NC
			Pseudogilquinia pillersi	GBR
		Lethrinus nebulosus (Forsskål, 1775)	Pseudogilquinia microbothria	GBR
			Pseudogilquinia pillersi	GBR
			Pseudolacistorhynchus heroniensis	GBR
		Lethrinus obsoletus (Forsskål, 1775)	Pseudotobothrium dipsacum	GBR
		Lethrinus rubrioperculatus Sato, 1978	Nybelinia goreensis	NC
			Otobothrium parvum	NC
		Gymnocranius grandoculis (Valenciennes, 1830)	Pseudolacistorhynchus heroniensis	NC
	Lutjanidae	Caesio cuning (Bloch, 1791)	Callitetrarhynchus gracilis	GBR
		Lutjanus carponotatus (Richardson, 1842)	Callitetrarhynchus gracilis	GBR
		Lutjanus gibbus (Forsskål, 1775)	Pseudotobothrium dipsacum	GBR
		Lutjanus vitta (Quoy & Gaimard, 1824)	Callitetrarhynchus gracilis	NC
			Pseudolacistorhynchus heroniensis	NC
	Mullidae	Parupeneus barberinus (Lacépède, 1801)	Nybelinia goreensis	NC
		Parupeneus bifasciatus (Lacépède, 1801)	Nybelinia basimegacantha	GBR
		Parupeneus multifasciatus (Quoy & Gaimard, 1825)	Nybelinia basimegacantha	NC
			Nybelinia goreensis	NC
			Nybelinia sp. B	NC
	Nemipteridae	Nemipterus furcosus (Valenciennes, 1830)	Callitetrarhynchus gracilis	NC
			Floriceps minacanthus	NC
			Nybelinia indica	NC
			Nybelinia goreensis	NC
			Nybelinia queenslandensis	NC
			Symbothriorhynchus tigaminacanthus	NC
	Polynemidae	Polynemus heptadactyla (Cuvier, 1829)	Callitetrarhynchus gracilis	GBR
	Pomacentridae	Abudefduf whitleyi Allen & Robertson, 1974	Callitetrarhynchus gracilis	GBR
	Pomatomidae	Pomatomus saltatrix (Linnaeus, 1766)	Callitetrarhynchus gracilis	GBR
	Sciaenidae	Johnius borneensis (Bleeker, 1851)	Callitetrarhynchus gracilis	GBR
			Nybelinia strongyla	GBR
			Proemotobothrium southwelli	GBR
	Scombridae	Euthynnus affinis (Cantor, 1849)	Floriceps minacanthus	GBR
		Euthynnus alletteratus (Rafinesque, 1810)	Floriceps minacanthus	GBR
		Grammatorcynus bicarinatus (Quoy & Gaimard, 1825)	Floriceps minacanthus	GBR
		Sarda australis (Macleay, 1881)	Heteronybelinia estigmena	GBR
		Scomberomorus commerson (Lacépède, 1800)	Callitetrarhynchus gracilis	GBR, NC
			Grillotiella exile	GBR
			Pterobothrium acanthotruncatum	GBR
		Scomberomorus queenslandicus Munro, 1943	Callitetrarhynchus gracilis	GBR
		Thunnus obesus (Lowe, 1839)	Hepatoxylon trichiuri	NC
	Serranidae	Cephalopholis boenak (Bloch, 1790)	Callitetrarhynchus gracilis	NC
			Floriceps minacanthus	GBR
			Pseudolacistorhynchus heroniensis	NC
			Pseudolacistorhynchus shipleyi	GBR
		Cephalopholis cyanostigma (Valenciennes, 1828)	Pseudolacistorhynchus shipleyi	GBR
			Callitetrarhynchus gracilis	GBR
			Floriceps minacanthus	GBR
			Pseudotobothrium dipsacum	GBR
		Cephalopholis miniata (Forsskål, 1775)	Callitetrarhynchus gracilis	GBR
			Floriceps minacanthus	GBR, NC
			Pseudolacistorhynchus heroniensis	GBR
			Pseudotobothrium dipsacum	NC
		Cephalopholis sonnerati (Valenciennes, 1828)	Floriceps minacanthus	NC
			Pseudolacistorhynchus heroniensis	NC
			Pseudotobothrium dipsacum	NC
		Cephalopholis spiloparaea (Valenciennes, 1828)	Callitetrarhynchus gracilis	NC
		Cephalopholis urodeta (Schneider, 1801)	Floriceps minacanthus	NC
			Pseudolacistorhynchus shipleyi	NC
			Pseudotobothrium dipsacum	NC
		Cromileptes altivelis (Valenciennes, 1828)	Callitetrarhynchus gracilis	GBR
		Epinephelus coioides (Hamilton, 1822)	Dasyrhynchus pacificus	NC
			Floriceps minacanthus	NC
			Pseudogilquinia pillersi	NC
			Pseudolacistorhynchus heroniensis	NC
			Pseudotobothrium dipsacum	GBR, NC
		Epinephelus chlorostigma (Valenciennes, 1828)	Callitetrarhynchus gracilis	NC
			Dasyrhynchus pacificus	NC
			Diesingium cf lomentaceum	NC
			Pseudolacistorhynchus heroniensis	NC
		Epinephelus cyanopodus (Richardson, 1846)	Floriceps minacanthus	NC
			Pseudolacistorhynchus heroniensis	NC
		Epinephelus fasciatus (Forsskål, 1775)	Callitetrarhynchus gracilis	NC
			Pseudolacistorhynchus heroniensis	GBR, NC
			Pseudotobothrium dipsacum	NC
		Epinephelus howlandi (Günther, 1873)	Pseudolacistorhynchus heroniensis	NC
		Epinephelus maculatus (Bloch, 1790)	Floriceps minacanthus	NC
			Otobothrium parvum	NC
		Epinephelus malabaricus (Bloch & Schneider, 1801)	Pseudogilquinia pillersi	NC
			Pseudotobothrium dipsacum	NC
		Epinephelus ongus Bloch, 1793	Pseudolacistorhynchus heroniensis	GBR
			Pseudolacistorhynchus shipleyi	GBR, NC
		Epinephelus polyphekadion (Bleeker, 1849)	Pseudolacistorhynchus heroniensis	NC
			Pseudolacistorhynchus shipleyi	NC
		Epinephelus retouti (Bleeker, 1868)	Pseudotobothrium dipsacum	NC
			Callitetrarhynchus gracilis	NC
		Epinephelus quoyanus (Valenciennes, 1830)	Floriceps minacanthus	GBR
			Pseudolacistorhynchus heroniensis	GBR
		Epinephelus rivulatus (Valenciennes, 1830)	Callitetrarhynchus gracilis	NC
			Pseudolacistorhynchus heroniensis	NC
		Plectropomus areolatus (Rüppell, 1830)	Floriceps minacanthus	GBR
		Plectropomus laevis (Lacépède, 1801)	Floriceps minacanthus	NC
			Pseudogilquinia pillersi	NC
			Pseudotobothrium dipsacum	NC
		Plectropomus leopardus (Lacépède, 1802)	Floriceps minacanthus	GBR, NC
			Pseudolacistorhynchus heroniensis	GBR, NC
			Pseudotobothrium dipsacum	GBR, NC
		Plectropomus maculatus (Bloch, 1790)	Callitetrarhynchus gracilis	GBR
			Pseudotobothrium dipsacum	GBR
			Pterobothrium acanthotruncatum	GBR
		Variola louti (Forsskål, 1775)	Callitetrarhynchus gracilis	NC
			Floriceps minacanthus	NC
			Pseudotobothrium dipsacum	NC
	Sphyraenidae	Sphyraena flavicauda (Rüppell, 1838)	Floriceps minacanthus	GBR
		Sphyraena jello Cuvier, 1829	Bombycirhynchus sphaerenaicum	GBR
			Floriceps minacanthus	GBR
			Pterobothrium pearsoni	GBR
		Sphyraena obtusata Cuvier, 1829	Callitetrarhynchus gracilis	GBR
		Sphyraena putnamae Jordan & Seale, 1905	Floriceps minacanthus	NC
			Heteronybelinia estigmena	NC
Syngnathiformes	Fistulariidae	Fistularia commersonii Rüppell, 1838	Dasyrhynchus basipunctatus	GBR
	Trichiuridae	Trichiurus lepturus Linnaeus, 1758	Heteronybelinia estigmena	NC
Tetraodontiformes	Balistidae	Abalistes filamentosus Matsuura & Yoshino, 2004	Dasyrhynchus basipunctatus	NC
			Pseudolacistorhynchus heroniensis	NC
			Pseudotobothrium dipsacum	NC
		Abalistes stellatus (Anonymous, 1798)	Dasyrhynchus basipunctatus	NC
			Pseudolacistorhynchus heroniensis	NC
			Pseudotobothrium dipsacum	GBR, NC
		Pseudobalistes fuscus (Bloch & Schneider, 1801)	Dasyrhynchus basipunctatus	NC
			Pseudolacistorhynchus heroniensis	NC
			Pseudotobothrium dipsacum	NC
		Rhinecanthus aculeatus (Linnaeus, 1758)	Pseudolacistorhynchus shipleyi	GBR
			Pseudotobothrium dipsacum	GBR
		Rhinecanthus rectangulus (Bloch & Schneider, 1801)	Pseudotobothrium dipsacum	GBR
		Sufflamen fraenatus (Latreille, 1804)	Heteronybelinia sp. C	NC
			Pseudolacistorhynchus shipleyi	GBR, NC
	Diodontidae	Diodon hystrix Linnaeus, 1758	Floriceps saccatus	GBR, NC
			Hepatoxylon trichiuri	GBR, NC
			Molicola horridus	GBR, NC
			Nybelinia indica	GBR, NC
		Diodon liturosus Shaw, 1804	Floriceps saccatus	GBR
			Molicola horridus	GBR
			Dasyrhynchus basipunctatus	NC
	Tetraodontidae	Lagocephalus sceleratus (Gmelin, 1789)	Nybelinia indica	NC
			Dasyrhynchus basipunctatus	NC
		Triodon macropterus Lesson, 1831	Callitetrarhynchus gracilis	NC
			Dasyrhynchus basipunctatus	NC
Scorpaeniformes	Platycephalidae	Cymbacephalus beauforti (Knapp, 1973)	Callitetrarhynchus speciosus	NC
			Pseudotobothrium dipsacum	NC
	Scorpaenidae	Dendrochirus zebra (Cuvier, 1829)	Nybelinia aequidentata	NC

Authorities of hosts or parasites which are indicated in the lists are not repeated in the text. The systematic arrangement of trypanorhynch taxa follows Palm (2004) [27]. All host names were verified in FishBase [15].

Results

Species found and other data

Larval trypanorhynchs were recovered primarily from the body cavities of the teleosts examined (Figs. 2–7). Plerocerci were usually encountered attached to the mesentery enclosed within white envelopes (Fig. 2), although in some hosts melanisation of the cyst wall had occurred rendering the cysts brown (Fig. 3). Some brown or even black envelopes contained only remnants of plerocerci (Fig. 4). Plerocercoids of tentaculariids were found either in the body cavity or in the gastrointestinal lumen; the latter were not contained within a “cyst”. Occasionally, plerocerci were found in the musculature and in the gill arches (Fig. 7), although there was no systematic search of such sites for plerocerci. Merocerci of Molicola horridus occurred in the livers of a limited number of species of teleosts, but the intensity of infection was high and the infections were readily observable at autopsy (Fig. 6).

Figures 2–7.

Metacestodes of trypanorhynch cestodes from teleost fishes. 2. Viable plerocerci of Callitetrarhynchus gracilis in the body cavity of Scomberomorus commerson. 3. Melanised trypanorhynch plerocerci in the body cavity of Epinephelus sp. 4. Melanised and contracted cysts of trypanorhynch metacestodes in the body cavity of Cephalopholis miniata; no viable plerocerci were recovered from these cysts. 5. Plerocerci of Pseudogilquinia spp. (arrows) around the oesophagus of Lethrinus nebulosus. 6. Merocerci of Molicola horridus in the liver of Diodon hystrix. 7. Plerocerci of Grillotiella exile in the gill arches of Scomberomorus commerson (histological section).

Species of larval trypanorhynch cestodes found in both teleost (as larvae) and elasmobranch (as adult) hosts at sites along the GBR and off NC are shown in Tables 1 and 2.

From the GBR, the specimens examined were obtained from the dissection of more than 9000 fish, although not all were specifically examined for trypanorhynch cestodes. Likewise, from NC, approximately 3800 fish were examined but the body cavity was not examined in every fish, as explained by Justine et al. [21-23]. Consequently, prevalence data were available for some species only and abundance data were not available; for most species only presence-absence data were available (with one exception from Lizard Island).

No trypanorhynch metacestodes were found in the families Blenniidae (n = 215), Chaetodontidae (n = 1638), Gobiidae (n = 183), Kyphosidae (n = 30) and Scaridae (n = 147) from the GBR. Likewise, no metacestodes were found in the families Atherinidae (n = 13), Apogonidae (n = 19), Echeneidae (n = 10) and Haemulidae (n = 10) in NC. In addition, although the families Serranidae, Lethrinidae and Lutjanidae were frequently infected with trypanorhynch metacestodes, this pattern was not uniform across all species within these families and in NC, no trypanorhynch metacestodes were found in Epinephelus areolatus (n = 12), E. merra (n = 18), Lethrinus atkinsoni (n = 12), L. nebulosus (n = 14), Lutjanus fulviflamma (n = 10) and Lu. kasmira (n = 14).

Members of the Tentacularioidea differ from other trypanorhynch metacestodes as they are present as plerocercoids (= post-larvae) rather than plerocerci [14] and may be found in intestinal contents as well as in the viscera. In New Caledonia, tentacularioids were frequently found in smaller schooling fishes, often being the only trypanorhynchs encountered in these fishes.

In total, 33 named species were found (Tables 1 and 3) as well as three species of tentaculariid cestodes to which no current name could be applied. Lacistorhynchoid and tentacularioid trypanorhynchs dominated the fauna in terms of numbers of species recovered (Table 3), with the otobothrioid and gymnorhynchoid trypanorhynchs being less numerous.

Table 3.

Summary of the fully identified taxa of larval trypanorhynch cestodes found in teleost fishes from the Great Barrier Reef and from New Caledonia.

Order	Total number of species	Great Barrier Reef	New Caledonia	Number of shared species (%)
Gymnorhynchoidea	5	5	1	1 (20%)
Lacistorhynchoidea	14	10	12	8 (57%)
Otobothrioidea	6	3	5	2 (33%)
Tentacularioidea	9	6	7	5 (55%)
All orders	33	22	23	15 (45%)

Prevalence data were obtained from 182 fish from various families collected during a single collecting trip to Lizard Island. The prevalence of trypanorhynch larvae was: 4/6 (77%) in scombrids, 5/7 (71%) in lethrinids, 2/13 (15%) in lutjanids, 8/9 (89%) in serranids and 1/109 (0.9%) in apogonids. Other fish families were represented by smaller numbers and were excluded.

Tentacularioid metacestodes of uncertain identity

Superfamily Tentacularioidea Poche, 1926

Family Tentaculariidae Poche, 1926

Nybelinia sp. A (Fig. 8)

Figures 8–11.

Tentacularioid metacestodes incompletely identified. 8.Nybelinia sp. A from Herklotsichthys quadrimaculatus (Rüppell, 1937). Scolex, basal and metabasal armature, hook profiles. Scale-bars: scolex and tentacle, 0.1 mm; hooks, 0.01 mm. 9. Nybelinia sp. B from Parupeneus multifasciatus (Quoy & Gaimard, 1825). Scolex, basal and metabasal armature, hook profiles. Scale-bars: scolex and tentacle, 0.1 mm; hooks, 0.01 mm. 10. Heteronybelinia sp. C from Sufflamen fraenatus (Latreille, 1804). Scolex, bothrial metabasal armature and antibothrial metabasal armature. Scale-bars: scolex 0.1 mm; hooks 0.01 mm. 11.Nybelinia basimegacantha Carvajal, Campbell & Cornford, 1976, specimen from Neoniphon sammara (Forsskål, 1775). Scolex, basal and metabasal armature. Scale-bars: scolex 0.1 mm; tentacle 0.01 mm.

Material examined: plerocercoids from Herklotsichthys quadrimaculatus (Rüppell, 1937), New Caledonia, MNHN JNC2669C1, 2671A1.

Scolex length 1200, pars bothrialis 580, pars vaginalis 520; bulbs ovoid, bulb length 250; velum 160; metabasal hooks: length 15, base 10.

Remarks

This species is similar to N. queenslandensis, but all measurements including those of the hooks are substantially smaller. In addition, the shape of the hooks differs (Fig. 8). The hook shape aligns the species with N. lingualis (Cuvier, 1817), N. bisulcata (Linton, 1889), N. anthicosum Heinz & Dailey, 1974 and N. hemipristis Palm & Beveridge, 2002, but N. lingualis and N. bisulcata differ in having much larger scoleces (2025–2700 and 2500, respectively) and bulbs (365–425 and 450–505, respectively) while the latter two species have much larger hooks (25–40). Consequently, these plerocercoids most closely resemble N. lingualis but cannot be assigned to this species with certainty.

Nybelinia sp. B (Fig. 9)

Material examined: plerocercoid from Parupeneus multifasciatus (Quoy & Gaimard, 1825), New Caledonia, MNHN JNC2172 C4.

Scolex length 1750, pars bothrialis 1100, pars vaginalis 1000, bulbs elongate, 560 long, velum 200, metabasal hooks: length 20, base 14.

Remarks

This specimen most closely resembles N. strongyla Dollfus, 1960 in scolex length, bulb length and hook size and shape, but differs in the length of the velum (690–830 in N. strongyla compared with 200 in the present material).

Heteronybelinia sp. C (Fig. 10)

Material examined: plerocercoid from Sufflamen fraenatus (Latreille, 1804), New Caledonia, MNHN JNC3034.

Scolex length 1440, pars bothrialis 770, pars vaginalis 680, bulbs elongate, bulb length 375, velum 125, metabasal hooks on antibothrial surface: length 17–19, base 8; on bothrial surface: length 25, base 18; basal armature heteromorphous.

Remarks

This specimen clearly belongs to Heteronybelinia as the hooks differ markedly in shape on the bothrial versus the antibothrial surfaces of the tentacle. Hook sizes are closest to H. eureia (Dollfus, 1960), but the specimen differs from this species in the number of hooks per half spiral and by the fact that in this specimen the bulbs are entirely posterior to the pars bothrialis while in H. eureia, they do not extend beyond the pars bothrialis. Therefore, this specimen cannot be accommodated within any known species of Heteronybelinia.

Nybelinia basimegacantha Carvajal, Campbell & Cornford, 1976 (Fig. 11)

Material examined: plerocercoid from Parupeneus multifasciatus (Quoy & Gaimard, 1825), New Caledonia, MNHN JNC2111 C1; plerocercoid from Neoniphon sammara (Forsskål, 1775), New Caledonia, MNHN JNC2552.

Specimen from P. multifasciatus: Scolex length 2600, pars bothrialis 1400, pars vaginalis 900, bulb length 1060, bulb width 130, velum 90.

Specimen from N. sammara: Scolex length 1380, pars bothrialis 840, pars vaginalis 350; bulb length 450, bulb width 70, velum 70.

Remarks

Two specimens have been identified as belonging to this species with its characteristic armature. In spite of the fact that the armature of both specimens is identical, scolex measurements differed substantially and for this reason, the measurements of both specimens are presented. The specimen from P. multifasciatus although quite flattened, corresponds more closely with the original description of the species, also from P. multifasciatus from Hawaii [10]. In the specimen from N. sammara, all measurements are shorter but the tentacular armature is identical.

Discussion

General comments

Although the records of trypanorhynch infections listed here are based on the dissection of thousands of fish from both the GBR and NC, the data collected are based on opportunistic collecting and must be viewed in this light. Few prevalence or intensity data were collected and the data are based largely on the presence of trypanorhynch metacestodes. Fish examined that did not harbour metacestodes were not included in the data presented in the tables but representative examples have been indicated in the results.

In spite of these limitations, the large numbers of metacestodes collected from both regions provide a significant basis for comparing trypanorhynch metacestodes of teleosts inhabiting coral reefs.

Several features are evident from the data presented. In spite of potential differences in the fish faunas between the two regions examined and possible biases in sampling approaches, an extremely large number of fish specimens (thousands) was examined at each locality and even though the methods of examination varied to some degree, the study encompassed a wide range of fish families at both sites. Overall, 45% of the trypanorhynch species recorded here occurred in both regions. In addition, the trypanorhynch species most commonly encountered were similar in both locations. Records of adults from elasmobranchs from both of these regions provided additional information on potential life cycles and the collection included numerous new host and geographical records.

Host specificity

Notwithstanding the opportunistic nature of the collecting, several aspects of host specificity are detectable within the data set and are worthy of discussion particularly since Palm & Caira, 2008 [30] have shown that specificity of the larval stages of trypanorhynchs is generally lower than that of the adults. First, it is evident that several fish taxa were rarely infected with trypanorhynchs. Thus, despite examination of substantial numbers of Blenniidae, Chaetodontidae, Gobiidae, Kyphosidae and Scaridae, no trypanorhynchs were found in these taxa. Other taxa strikingly underrepresented, though heavily sampled, were the Acanthuridae, Pomacentridae and Echeneidae. We do not suggest that these taxa have been exhaustively examined, but certainly they are depauperate relative to families such as the Balistidae, Lethrinidae, Scombridae and Serranidae.

Among the teleost fishes that were infected, there was evidence of both stenoxenicity (parasitism of closely related species) and euryxenicity (parasitism of distantly or ecologically related species). In the stenoxenous category, Molicola horridus was seen in two species of Diodontidae, Pterobothrium australiense has been seen only in labrids (one record), Pseudogilquinia microbothria was found only in lethrinids (both in NC and the GBR) and Dasyrhynchus basipunctatus occurred overwhelmingly in tetraodontiforms (five species) although also once in a fistulariid. The apparently restricted distributions of such species are doubtless subject to refinement with further collecting but it seems highly unlikely that they will prove to be euryxenous in the same way as are some other species.

We detected some evidence of the absence of trypanorhynch species in particular fish groups. The best evidence comes from the family Serranidae which is probably the most thoroughly characterised for its trypanorhynch fauna. The serranid fishes collected tend to be large and easily examined for trypanorhynchs with which they are often heavily infected. Our results incorporate reports from 25 serranid species and of the 181 host/parasite combinations detected, 55 were from serranids; the next highest number of combinations came from the Lethrinidae with 14. The extent to which the characterisation of this family is comprehensive is demonstrated by the fact that six of the ten trypanorhynch species recorded in this family have been reported from more than one serranid species; three species were found in ten or more serranid species although four species were found in only one. We infer that the true trypanorhynch richness is thus not likely to be very much greater than the 10 species reported so far in this region. Thus, we predict that species that have been reported relatively frequently in other fishes are genuinely absent, rather than have simply not yet been collected. Most striking in this respect are the species of the Tentacularioidea. Twelve species of this superfamily are reported here in 34 host/parasite combinations, but none in serranids. The apparent absence of a range of species from the Serranidae thus appears consistent with the high host specificity seen for the species described above.

Several species showed remarkably low specificity. Thus, Callitetrarhynchus gracilis was reported here from five fish orders and 18 families, Floriceps minacanthus from two orders and six families, Pseudotobothrium dipsacum from three orders and six families, Pseudolacistorhynchus heroniensis from two orders and four families and Pseudolacistorhynchus shipleyi from three orders and five families. The absence of any detectable specificity in these species leads to the prediction that further sampling will lead to even larger host ranges for these species.

Callitetrarhynchus gracilis exhibited the widest host range and has a cosmopolitan distribution [27] with carcharhinid sharks as its primary definitive hosts in the Australian region [1]. Currently recorded in the intermediate stage from approximately 130 species of teleosts [16, 27, 29], 23 new host records have been added in the present study.

Floriceps minacanthus appears to be limited to the Indo-Pacific region, and again, its known definitive hosts are carcharhinid sharks [26], with adults having been reported from four species of Carcharhinus. However, the present record in Triaenodon obesus is the first from a shark not belonging to this genus. Plerocerci have been reported from 13 species of teleosts [27, 29] from the Red Sea, Australia and off Indonesia and Hawaii while 14 new species of teleosts are reported here as hosts.

Pseudotobothrium dipsacum was also found in a wide variety of teleosts. It has previously been reported from numerous species of teleosts ranging from the west coast of Africa to Australia [4, 27]. Eight new hosts, all from New Caledonia, have been added in the present study. In spite of its wide host range and distribution, its definitive hosts remain unknown.

Pseudolacistorhynchus heroniensis is known only from the GBR and from NC but is found in a wide range of teleosts, with 12 new teleost hosts being added in the current study. The only record of the adult parasite is a single collection from Stegostoma fasciatum from New Caledonia [6]. The specimens collected were either immature or hyperapolytic such that some doubt exists as to whether this is the usual definitive host species.

Pseudolacistorhynchus shipleyi occurs widely in the Indo-West Pacific, with the adults being found in Nebrius ferrugineus off Sri Lanka [2]. In the current study, eleven new intermediate host records are reported.

The above five species occurred in a wide variety of teleost hosts with serranids (25 species), carangids (5), balistids (5), scombrids (5) and sphyraenids (5) being most frequently encountered. The same five species of trypanorhynch were the most commonly encountered species both on the Great Barrier Reef and off New Caledonia in spite of obvious differences in the species of fish infected at the two localities. There was no intentional bias in collecting activities, but it may have been that more of these larger fishes were collected than other smaller taxa.

Other species of trypanorhynch had a more restricted host distribution. Limited data on prevalence based on a single series of collections from Lizard Island suggested that trypanorhynch larvae were prevalent in larger fishes (serranids, sphyraenids, scombrids, lutjanids) but in small fish (a single family, Apogonidae) they occurred at a very low prevalence. However, these data were based on a very small sample of fish and need to be interpreted with caution.

Overall, the patterns of host specificity seen here, a mixture of stenoxenicity and euryxenicity, resemble that reported by Chambers et al., 2000 [11] for tetraphyllidean (sensu lato) metacestodes of GBR fishes. In that study, metacestode Type 4 was found in two orders and 12 families, whereas Types 9 and 10 were found only in labrids. However, in the study of tetraphyllidean metacestodes it is often not possible to be confident that a single morphotype represents only one species whereas the complex morphology of trypanorhynch scoleces makes identification to species quite reliable.

Biogeography

Of the 33 trypanorhynch species reported here, 15 (45%) were found both in NC and on the GBR. Almost certainly this number underestimates the level of sharing between the two areas. Noticeably, the nine species reported in the largest number of host/parasite combinations were all found at both sites. Of the 21 species found in only one or two host/parasite combinations, only one (Molicola horridus) was found both in NC and on the GBR. It seems likely, or at least possible, that some species are restricted to one or other of the two sites but at present the evidence is generally marginal in this respect. The only robust parasitological study of which we are aware that has previously compared parasites of NC and the GBR is that of McNamara et al., 2012 [26] who analysed monorchiid trematodes of chaetodontids from NC and the GBR (as well as other sites in the Tropical Indo-West Pacific [TIWP]). Thirteen species of Hurleytrematoides Yamaguti, 1953 were found in total for the two sites of which just six were found at both sites for a similarity of 46%; four species were found only from the GBR and three only from NC. In every case, hosts suitable for the species not found in each area had been examined in numbers sufficient to suggest that they would have been found if present. The proportion of monorchiid species shared (46%) is thus remarkably similar to that for the trypanorhynchs. Given the much stricter specificity of monorchiids of chaetodontids (none known convincingly other than from chaetodontids) than of trypanorhynch metacestodes in general, we predict that further sampling for trypanorhynchs will see the levels of sharing increase.

Of the species found, eight (C. gracilis, F. saccatus, Gr. exile, Hep. trichiuri, Het. estigmena, M. horridus, N. goreensis, O. penetrans) have a cosmopolitan distribution, based on records in Palm, 2004 [27], while ten species are widely distributed in the Tropical Indo-West Pacific (TIWP) (D. pacificus, F. minacanthus, N. basimegacantha, N. indica, Psgi. microbothria, Psgi. pillersi, D. basipunctatus, Psl. shipleyi, Psd. dipsacum, Pt. acanthotruncatum). By contrast, seven species occur only in south-east Asia and Australasia (N. queenslandensis, O. alexanderi, O. parvum, Psl. heroniensis, Psl. nanus, Pt. australiense, S. tigaminacanthus). Several additional species (e.g. Pt. lintoni) with few, highly disjunct records are difficult to categorise. Nevertheless, with many of the trypanorhynch species encountered having extremely wide geographical distributions [31], it was not surprising that the species found on the GBR and from NC were broadly similar.

Localisation in host

Apart from potential differences in the species of fish present at the two sites studied, or their abundance and hence ease of obtaining a particular species, other factors may be involved such as the location of trypanorhynch metacestodes in the body of the teleost. Most are found in the body cavity and are easily recognised. However, the metacestodes of Gr. exile occur only in the gill arches of Sc. commerson [35] and this site is not always examined for the presence of metacestodes. Similarly, the metacestodes of Psg. microbothria cluster around the oesophagus of L. nebulosus (unpublished) while those of Pt. lintoni are found in the musculature (unpublished). Failure to examine sites other than the body cavities may lead to differences in the species recovered.

Life cycles

Combining the data obtained here with that available for adult trypanorhynchs in elasmobranchs in the same region has provided some insights into life cycles such as finding the adult of Pt. acanthotruncatum for the first time in Pristis zijsron. In addition, the definitive host range of F. minacanthus is expanded to include the shark Triaenodon obesus. Many life cycles remain to be identified, but broad scale collecting, such as that undertaken in this study, can be useful in identifying both potential intermediate and definitive hosts.

Species of Diodon warrant a particular mention as they are parasitised by several well-recognised trypanorhynch species including Floriceps saccatus and Molicola horridus. Infections with the latter species are particularly striking as much of the hepatic parenchyma may be replaced by metacestodes (Fig. 5). Species of Diodon are not only highly toxic [36], but can also inflate their bodies when threatened. As adults of these cestodes are found in large sharks such as Prionace glauca (Linnaeus, 1758) (see Dollfus, 1942) [14], it is tempting to assume that only large sharks are able to consume species of Diodon. Alternatively, it may be that the life cycles of these cestodes are completed using alternative intermediate hosts and their presence in species of Diodon indicates an occurrence in “dead-end” hosts. By comparison, in a study of the larval anisakid nematodes of teleosts off Lizard Island, Jabbar et al., 2012 [18] found no larval anisakids in their sample of tetraodontiform fishes, which would potentially be “dead-end” hosts for these nematodes.

Conclusion

This is the first study to attempt to examine the trypanorhynch larval cestode fauna of coral reef teleosts in the west Pacific, examining reefs on the GBR and NC. The trypanorhynch fauna was dominated numerically by a small number of species at both sites with considerable similarity between the two localities examined. Although large numbers of teleosts were examined at both sites, it is most unlikely that the trypanorhynch fauna has been exhaustively surveyed and more detailed comparisons must await much more extensive sampling. Nevertheless, apart from characterising the general features of the fauna, this study has provided additional insights into host specificity and life cycles of these cestode parasites.

Conflict of Interest

The Editor-in-Chief of Parasite is one of the authors of this manuscript. COPE (Committee on Publication Ethics, http://publicationethics.org/), to which Parasite adheres, advises special treatment in these cases. COPE wrote: “Editors should not be denied the ability to publish in their own journal, but they must not exploit their position. The journal must have a procedure for handling submissions from the editor or members of the editorial board that ensures that peer review is handled independently of the author/editor. This process should be detailed once the paper is published.” In this case the peer-review process was handled by Invited Editor Dominique Vuitton.