Open Access
Research Article
Issue
Parasite
Volume 21, 2014
Article Number 60
Number of page(s) 19
DOI https://doi.org/10.1051/parasite/2014060
Published online 18 November 2014

© I. Beveridge et al., published by EDP Sciences, 2014

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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 [2123].

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).

thumbnail 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 [2123]. 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.

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.

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).

thumbnail 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. [2123]. 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.

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

  1. Nybelinia sp. A (Fig. 8)

    thumbnail 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.

  2. 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).

  3. 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.

  4. 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.

Acknowledgments

Collecting on the GBR was funded by the Australian Research Council and the Australian Biological Resources Study, the latter in part through the CReefs Program. In New Caledonia, the following students of JLJ participated in the parasitological survey: Julie Mounier, Charles Beaufrère, Anaïs Guillou, Audrey Guérin, Damien Hinsinger, Éric Bureau, Chloé Journo, Violette Justine, Amandine Marie, Aude Sigura, Sophie Olivier, Guilhem Rascalou, Géraldine Colli, Lenaïg Hemery, Pierpaolo Brena, Cyndie Dupoux, Isabelle Mary, Adeline Grugeaud, Marine Briand and Charlotte Schoelinck. Claude Chauvet (UNC, Nouméa) provided several fishes. Angelo di Matteo (IRD) provided technical help. Visiting colleagues who participated were Ian Beveridge, Louis Euzet, Eva Řehulková, František Moravec, Milan Gelnar, Bernard Marchand and Susan Lim. Certain fishes from New Caledonia were identified (often from photographs) by Jack Randall (Bishop Museum, Hawaii), Ronald Fricke (Staatliches Museum für Naturkunde, Stuttgart, Germany), Kent E. Carpenter (Old Dominion University, Norfolk, Virginia, USA), Philippe Borsa (IRD, Nouméa), Bernard Séret (IRD and MNHN, Paris) and Samuel Iglésias (MNHN, Paris).

References

  1. Beveridge I, Campbell RA. 1996. New records and redescriptions of trypanorhynch cestodes from Australian fishes. Records of the South Australian Museum, 29, 1–22. [Google Scholar]
  2. Beveridge I, Campbell RA. 1998. Re-examination of the trypanorhynch cestode collections of A.E. Shipley, J. Hornell and T. Southwell with the erection of a new genus, Trygonicola, and redescriptions of seven species. Systematic Parasitology, 39, 1–34. [CrossRef] [Google Scholar]
  3. Beveridge I, Campbell RA. 2001. Proemotobothrium n.g. (Cestoda: Trypanorhyncha), with the redescription of P. linstowi (Southwell, 1912) n. comb. and description of P. southwelli n. sp. Systematic Parasitology, 48, 223–233. [CrossRef] [PubMed] [Google Scholar]
  4. Beveridge I, Campbell RA, Jones MK. 2000. New records of the cestode genus Pseudotobothrium (Trypanorhyncha: Otobothriidae) from Australian fishes. Transactions of the Royal Society of South Australia, 124, 151–162. [Google Scholar]
  5. Beveridge I, Chauvet C, Justine J-L. 2007. Redescription of Pseudogilquinia pillersi (Southwell, 1929) (Cestoda: Trypanorhyncha) from serranid and lethrinid fishes from New Caledonia and Australia. Acta Parasitologica, 52, 213–218. [CrossRef] [Google Scholar]
  6. Beveridge I, Justine J-L. 2007. Pseudolacistorhynchus nanus n. sp. (Cestoda: Trypanorhyncha) parasitic in the spiral valve of the zebra shark, Stegostoma fasciatum (Hermann, 1783). Transactions of the Royal Society of South Australia, 132, 177–183. [Google Scholar]
  7. Bouchet P, Lozouet P, Maestrati P, Heros V. 2002. Assessing the magnitude of species richness in tropical marine environments: exceptionally high numbers of molluscs at a New Caledonia site. Biological Journal of the Linnean Society, London, 75, 421–436. [CrossRef] [Google Scholar]
  8. Campbell RA, Beveridge I. 1996. Revision of the family Pterobothriidae Pintner, 1931 (Cestoda: Trypanorhyncha). Invertebrate Taxonomy, 10, 617–662. [CrossRef] [Google Scholar]
  9. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema AW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro EA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E. 2008. One third of reef building corals face elevated extinction risks from climate change and local effects. Science, 321, 560–563. [CrossRef] [PubMed] [Google Scholar]
  10. Carvajal JG, Campbell RA, Cornford EM. 1976. Some trypanorhynch cestodes from Hawaiian fishes with the description of four new species. Journal of Parasitology, 62, 70–77. [CrossRef] [Google Scholar]
  11. Chambers CB, Cribb TH, Jones MK. 2000. Tetraphyllidean metacestodes of teleosts of the Great Barrier Reef, and the use of in vitro cultivation to identify them. Folia Parasitologica, 47, 285–292. [CrossRef] [PubMed] [Google Scholar]
  12. Chervy L. 2002. The terminology of larval cestodes or metacestodes. Systematic Parasitology, 52, 1–33. [CrossRef] [PubMed] [Google Scholar]
  13. Cribb TH, Bray RA, Barker SC, Adlard RD, Anderson GR. 1994. Ecology and diversity of digenean trematodes of reef and inshore fishes of Queensland. International Journal for Parasitology, 24, 851–960. [CrossRef] [PubMed] [Google Scholar]
  14. Dollfus RP. 1942. Études critiques sur les Tétrarhynques du Muséum de Paris. Archives du Muséum National d’Histoire Naturelle, Paris, 19, 1–466. [Google Scholar]
  15. Froese R, Pauly D. 2014. FishBase, World Wide Web electronic publication. www.fishbase.org. [Google Scholar]
  16. Haseli M, Malek M, Valinasab T, Palm HW. 2011. Trypanorhynch cestodes of teleost fish from the Persian Gulf, Iran. Journal of Helminthology, 85, 215–224. [CrossRef] [PubMed] [Google Scholar]
  17. Hoeg-Guldberg O, Bruno JF. 2010. The impact of climate change on the world’s ecosystems. Science, 328, 1523–1528. [CrossRef] [PubMed] [Google Scholar]
  18. Jabbar A, Asnoussi A, Norbury LJ, Eisenbarth A, Shamsi S, Gasser RB, Lopata AL, Beveridge I. 2012. Larval anisakid nematodes in teleost fishes from Lizard Island, northern Great Barrier Reef, Australia. Marine and Freshwater Research, 63, 1283–1299. [CrossRef] [Google Scholar]
  19. Jensen K. 2009. Cestoda (Platyhelminthes) of the Gulf of Mexico, in Felder DL, Camp DK, Editors. Gulf of Mexico. Origin, Waters, and Biota. Texas A & M University Press: USA, p. 487–522. [Google Scholar]
  20. Justine J-L. 2010. Parasites of coral reef fish: how much do we know? With a bibliography of fish parasites in New Caledonia. Belgian Journal of Zoology, 140, 155–190. [Google Scholar]
  21. Justine J-L, Beveridge I, Boxshall GA, Bray RA, Moravec F, Trilles J-P, Whittington ID. 2010. An annotated list of parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda and Nematoda) collected from groupers (Serranidae, Epinephelinae) in New Caledonia emphasizes parasite biodiversity in coral reef fish. Folia Parasitologia, 54, 237–262. [CrossRef] [PubMed] [Google Scholar]
  22. Justine J-L, Beveridge I, Boxshall GA, Bray RA, Moravec F, Trilles J-P, Whittington ID. 2010. An annotated list of fish parasites (Copepoda, Monogenea, Digenea, Cestoda and Nematoda) collected from Emperors and Emperor Bream (Lethrinidae) in New Caledonia further highlights parasite biodiversity estimates on coral reef fish. Zootaxa, 2691, 1–40. [Google Scholar]
  23. Justine J-L, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles J-P, Whittington ID. 2012. An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquatic Biosystems, 8, 22. [CrossRef] [PubMed] [Google Scholar]
  24. Lester RJG, Sewell KB. 1989. Checklist of parasites from Heron Island, Great Barrier Reef. Australian Journal of Zoology, 37, 101–128. [CrossRef] [Google Scholar]
  25. MacKenzie K. 1990. Cestode parasites as biological tags for mackerel (Scomber scombrus L.) in the northeast Atlantic. Jounal du Conseil International pour l’Exploration de la Mer, 46, 155–166. [CrossRef] [Google Scholar]
  26. McNamara MKA, Adlard RD, Bray RA, Sasal P, Cribb TH. 2012. Monorchiids (Platyhelminthes: Digenea) of chaetodontid fishes (Perciformes): biogeographical patterns in the tropical Indo-West Pacific. Parasitology International, 61, 288–306. [CrossRef] [PubMed] [Google Scholar]
  27. Palm HW. 2004. The Trypanorhyncha Diesing, 1863. PKSPL-IPB Press: Bogor. [Google Scholar]
  28. Palm HW, Beveridge I. 2002. Tentaculariid cestodes of the order Trypanorhyncha (Platyhelminthes) from the Australian region. Records of the South Australian Museum, 35, 49–78. [Google Scholar]
  29. Palm HW, Bray RA. 2014. Marine Fish Parasitology in Hawaii. Westarp & Partner: Hohenwarsleben. [Google Scholar]
  30. Palm HW, Caira JN. 2008. Host specificity of adult versus larval cestodes of the elasmobranch tapeworm order Trypanorhyncha. International Journal for Parasitology, 38, 381–388. [CrossRef] [PubMed] [Google Scholar]
  31. Palm HW, Waeschenbach A, Littlewood DTJ. 2007. Genetic diversity in the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1797: evidence for a cosmopolitan distribution and low host specificity in the teleost intermediate host. Parasitology Research, 101, 153–159. [CrossRef] [PubMed] [Google Scholar]
  32. Plaisance L, Caley MJ, Brainard RE, Knowlton N. 2011. The diversity of coral reefs: What are we missing? PLoS One, 6(10), e25026. [CrossRef] [PubMed] [Google Scholar]
  33. Rohde K. 1976. Marine parasitology in Australia. Search, 7, 477–482. [Google Scholar]
  34. Sakanari J. 1989. Grillotia heroniensis, sp. nov., and G. overstreeti, sp. nov., (Cestoda: Trypanorhyncha) from Great Barrier Reef fishes. Australian Journal of Zoology, 37, 81–87. [CrossRef] [Google Scholar]
  35. Shaharom FM, Lester RJG. 1982. Description of and observations on Grillotia branchi n.sp., a larval trypanorhynch from the branchial arches of the Spanish mackerel, Scomberomorus commerson. Systematic Parasitology, 4, 1–6. [CrossRef] [Google Scholar]
  36. Trevett AJ, Mavo B, Warrell DA. 1997. Tetrodotoxic poisoning from ingestion of a porcupine fish (Diodon hystrix) in Papua New Guinea: nerve conduction studies. American Journal of Tropical Medicine and Hygiene, 56, 30–32. [Google Scholar]

Cite this article as: Beveridge I, Bray RA, Cribb TH & Justine J-L: Diversity of trypanorhynch metacestodes in teleost fishes from coral reefs off eastern Australia and New Caledonia. Parasite, 2014, 21, 60.

All Tables

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.

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.

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.

All Figures

thumbnail Figure 1.

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

In the text
thumbnail 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).

In the text
thumbnail 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.

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.