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

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Abstract

We examined four species of Plectropomus Oken, 1817 (Serranidae: Epinephelinae), Plectropomus areolatus (Rüppell), Plectropomus laevis (Lacepède), Plectropomus leopardus (Lacepède) and Plectropomus maculatus (Bloch) from sites off Heron Island and Lizard Island on the Great Barrier Reef, Australia (GBR), and the Gambier Islands, French Polynesia. Three new species of Neidhartia Nagaty, 1937, five new species of Prosorhynchus Odhner, 1905, and one previously described species, Prosorhynchus freitasi Nagaty, 1937, are characterised. The three species of Neidhartia, Neidhartia haywardi n. sp., Neidhartia plectropomi n. sp. and Neidhartia tyleri n. sp. are readily distinguishable morphologically. Two of the six species of Prosorhynchus (Prosorhynchus lesteri n. sp. and Prosorhynchus wrightae n. sp.) are easily distinguished from their other congeners by morphology but the other four species (P. freitasi, Prosorhynchus heronensis n. sp., Prosorhynchus munozae n. sp. and Prosorhynchus plectropomi n. sp.) are generally similar in morphology and were only distinguished initially by comparing their ITS2 rRNA sequences. Three additional taxa, one from the GBR and two from French Polynesia, were recognised as distinct on the basis that their ITS2 rRNA sequences differed from those of the new taxa described here; these species remain unnamed for the present. Inter-specific divergence observed within these genera in the ITS2 rRNA ranged from 10 to 42 base pairs (4–16 %) for species of Neidhartia and 2–57 base pairs (3–21 %) for species of Prosorhynchus. Inter-generic divergences were 42–55 base pairs (17–21 %). No intraspecific variation in the ITS2 rRNA region was observed for any of the six species for which multiple sequence replicates were obtained. Phylogenetic analysis of 12 operational taxa from Plectropomus together with sequences of three other species from epinepheline serranids demonstrated that Neidhartia and Prosorhynchus were reciprocally monophyletic with the exception that P. wrightae n. sp. fell either within or basal to the Neidhartia species. The richness of bucephalids in species of Plectropomus appears to be exceptional within the Serranidae relative to that observed in other serranid genera in the tropical Indo-West Pacific.

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References

  • Abdel-Ghaffar F, Morsy K, Mehlhorn H, Bashtar AR, Shazly MA, Saad AH, Abdel-Gaber R (2012) First report of Kudoa species (Myxozoa: Kudoidae) infecting the spotted coral grouper Plectropomus maculates from the Red Sea. A light and ultrastructural study. Parasitol Res 111:1579–1585

    Article  PubMed  Google Scholar 

  • Abu-Zinada NY (1998) Observations on two larval cestodes from Red Sea fishes at Jeddah, Saudi Arabia. Vet Med J Giza 46:193–197

    Google Scholar 

  • Aiken HM, Bott NJ, Mladineo I, Montero FE, Nowak BF, Hayward CJ (2007) Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). F Fish 8:1–14

    Article  Google Scholar 

  • Beveridge I, Chauvet C, Justine JL (2007) Redescription of Pseudogilquinia pillersi (Southwell, 1929) (Cestoda, Trypanorhyncha) from serranid and lethrinid fishes from New Caledonia and Australia. Acta Parasitol 52:213–218

    Article  Google Scholar 

  • Bott NJ, Cribb TH (2009) Prosorhynchine trematodes (Digenea: Bucephalidae) from epinephelines (Perciformes: Serranidae) on the Great Barrier Reef, Australia. Sys Parasitol 72:57–69

    Article  Google Scholar 

  • Boxshall GA, Lin CL, Ho JS, Ohtsuka S, Maran BAV, Justine JL (2008) A revision of the family Dissonidae Kurtz, 1924 (Copepoda: Siphonostomatoida). Syst Parasitol 70:81–106

    Article  PubMed  Google Scholar 

  • Bray RA, Cribb TH (1989) Digeneans of the family Opecoelidae Ozaki, 1925 from the southern Great Barrier Reef, including a new genus and three new species. J Nat Hist 23:429–473

    Article  Google Scholar 

  • Bray RA, Cribb TH, Barker SC (1993a) Hemiuridae (Digenea) from marine fishes of the Great Barrier Reef, Queensland, Australia. Syst Parasitol 25:37–62

    Article  Google Scholar 

  • Bray RA, Cribb TH, Barker SC (1993b) The Hemiuroidea (Digenea) of pomacentrid fishes (Perciformes) from Heron Island, Queensland, Australia. Syst Parasitol 24:159–184

    Article  Google Scholar 

  • Bray RA, Cribb TH, Waeschenbach A, Littlewood DTJ (2007) A new species of Stephanostomum Looss, 1899 (Digenea, Acanthocolpidae) with a bizarre oral sucker: S. adlardi sp. nov. from the common coral trout Plectropomus leopardus (Lacepède, 1802) (Perciformes, Serranidae) from Lizard Island, Great Barrier Reef. Acta Parasitol 52:206–212

    Article  Google Scholar 

  • Bray RA, Justine JL (2007) Pseudopycnadena tendu sp. nov. (Digenea, Opecoelidae) in the yellow-spotted triggerfish Pseudobalistes fuscus (Perciformes, Balistidae) and additional opecoelids parasitizing fishes from the waters off New Caledonia. Acta Parasitol 52:13–17

    Article  Google Scholar 

  • Campbell RA, Beveridge I (1987) Floriceps minacanthus new species Cestoda Trypanorhyncha from Australian fishes. Trans R Soc S Aust 111:189–194

    Google Scholar 

  • Chambers C, Cribb T (2006) Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Sys Parasitol 63:59–80

    Article  Google Scholar 

  • Chen D, Wang G, Yao W, Nie P (2007) Utility of ITS1–5.8S–ITS2 sequences for species discrimination and phylogenetic inference of two closely related bucephalid digeneans (Digenea: Bucephalidae): Dollfustrema vaneyi and Dollfustrema hefeiensis. Parasitol Res 101(3):791–800

    Article  PubMed  Google Scholar 

  • Cribb TH, Bray RA (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Sys Parasitol 76:1–7. doi:10.1007/s11230-010-9229-z

    Article  Google Scholar 

  • Cribb TH, Bray RA, Wright T, Pichelin S (2002) The trematodes of groupers (Serranidae: Epinephelinae) knowledge, nature and evolution. Parasitology 124:S23–S42

    Article  PubMed  Google Scholar 

  • Deveney MR, Whittington ID (2010) Three new species of Benedenia Diesing, 1858 from the Great Barrier Reef, Australia with a key to species of the genus. Zootaxa 2348:1–22

    Google Scholar 

  • Doupé RG, Lymbery AJ, Wong S, Hobbs RP (2003) Larval anisakid infections of some tropical fish species from north-west Australia. J Helminthol 77:363–365

    Article  PubMed  Google Scholar 

  • Durio WO, Manter HW (1968a) Some digenetic trematodes of marine fishes of New Caledonia. Part I. Bucephalidae, Monorchiidae, and some smaller families. Proc Hel Soc Wash 35:143–153

    Google Scholar 

  • Durio WO, Manter HW (1968b) Some digenetic trematodes of marine fishes of New Caledonia. Part II. Opecoelidae and Lepocreadiidae. J Parasitol 54:747–756

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc A Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Francisco CJ, Almeida A, Castro AM, Santos MJ (2010) Development of a PCR-RFLP marker to genetically distinguish Prosorhynchus crucibulum and Prosorhynchus aculeatus. Parasitol Int 59:40–43

    Article  PubMed  CAS  Google Scholar 

  • Froese R, Pauly D (2012) FishBase. World Wide Web electronic publication. http://www.fishbase.org, version (31 Oct 2012)

  • Grant EM (1965) Guide to fishes. Department of Harbours and Marine, Brisbane

    Google Scholar 

  • Gunter NL, Adlard RD (2009) Seven new species of Ceratomyxa Thelohan, 1892 (Myxozoa) from the gall-bladders of serranid fishes from the Great Barrier Reef, Australia. Syst Parasitol 73:1–11

    Article  PubMed  Google Scholar 

  • Heemstra PC, Randall JE (1993) FAO species catalogue. Groupers of the world (Family Serranidae, Subfamily Epinephelinae). An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species. FAO, Rome

  • Ho JS, Dojiri M (1977) Parasitic copepods on the fishes of the Great Barrier Reef Australia 2. Caligoida Dissonus, Lepeophtheirus and Dentigryps. Publ Seto Mar Biol Lab 24:77–98

    Google Scholar 

  • Hunter JA, Cribb TH (2012) A cryptic complex of species related to Transversotrema licinum Manter, 1970 from fishes of the Indo-West Pacific, including descriptions of ten new species of Transversotrema Witenberg, 1944 (Digenea: Transversotrematidae). Zootaxa 3176:1–44

    Google Scholar 

  • Hunter JA, Ingram E, Adlard RD, Bray RA, Cribb TH (2010) A cryptic complex of Transversotrema species (Digenea: Transversotrematidae) on labroid, haemulid, and lethrinid fishes in the Indo-West Pacific region, including the description of three new species. Zootaxa 2652:17–32

    Google Scholar 

  • Hutson KS, Styan CA, Beveridge I, Keough MJ, Zhu XQ, Abs El-Osta YG, Gasser RB (2004) Elucidating the ecology of bucephalid parasites using a mutation scanning approach. Mol Cell Probes 18:139–146

  • 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. Mar Freshw Res 63:1283–1299

    Article  Google Scholar 

  • Justine JL (2011) Huffmanela plectropomi n. sp. (Nematoda: Trichosomoididae: Huffmanelinae) from the coralgrouper Plectropomus leopardus (Lacepede) off New Caledonia. Syst Parasitol 79:139–143

    Article  PubMed  Google Scholar 

  • Justine JL, Euzet L (2006) Diplectanids (Monogenea) parasitic on the gills of the coralgroupers Plectropomus laevis and P. leopardus (Perciformes, Serranidae) off New Caledonia, with the description of five new species and the erection of Echinoplectanum n. g. Syst Parasitol 64:147–172

    Article  PubMed  Google Scholar 

  • Kabata Z (1966a) Copepoda parasitic on Australian fishes. V. Genus Dissonus (Dissonidae). Ann Mag Nat Hist 9:211–226

    Google Scholar 

  • Kabata Z (1966b) Copepoda parasitic on Australian fishes. VI. Some caligoid species. Ann Mag Nat Hist 9:563–570

    Google Scholar 

  • Kabata Z (1991) Copepoda parasitic on Australian fishes, xiii—family Hatschekiidae. J Nat Hist 25:91–121

    Article  Google Scholar 

  • Kleeman SN, Adlard RD (2000) Molecular detection of Marteilia sydneyi, pathogen of Sydney rock oysters. Dis Aquat Org 40:137–146

    Article  PubMed  CAS  Google Scholar 

  • Ku C, Shen J (1975) Studies on the genus Rhipidocotyle Diesing (Bucephalidae, Trematoda) from some marine fishes of China. Acta Zool Sin 21:205–211

    Google Scholar 

  • Lewis AG (1964) The caligid copepod genus Dentigryps (Crustacea: Caligoida). Proc U S Nat Mus 115:347–380

    Article  Google Scholar 

  • Lo CM, Morgan JAT, Galzin R, Cribb TH (2001) Identical digeneans in coral reef fishes from French Polynesia and the Great Barrier Reef (Australia) demonstrated by morphology and molecules. Int J Parasitol 31(14):1573–1578

    Article  PubMed  CAS  Google Scholar 

  • Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72 http://mesquiteproject.org

  • Madhavi R (1974) Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Bucephalidae. Riv Parassitol 35:189–199

    Google Scholar 

  • Manter HW (1953) Two new species of Prosorhynchinae (Trematoda: Gasterostomata) from the Fiji Islands. Thapar Commemoration Vol 1953:193–200

    Google Scholar 

  • Manter HW (1963) Studies on digenetic trematodes of fishes of Fiji. II. Families Lepocreadiidae, Opistholebetidae, and Opecoelidae. J Parasitol 49:99–113

    Article  Google Scholar 

  • Matthews RA (1973) The life-cycle of Prosorhynchus crucibulum (Rudolphi, 1819) Odhner, 1905, and a comparison of its cercaria with that of Prosorhynchus squamatus Odhner, 1905. Parasitology 66:133–164

    Article  Google Scholar 

  • Matthews RA (1974) The life-cycle of Bucephaloides gracilescens (Rudolphi, 1819) Hopkins, 1954 (Digenea: Gasterostomata). Parasitology 68:1–12

    Article  PubMed  CAS  Google Scholar 

  • 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. Parasitol Int 61:288–306

    Article  PubMed  CAS  Google Scholar 

  • McNamara MKA, Cribb TH (2011) Taxonomy, host specificity and dietary implications of Hurleytrematoides (Digenea: Monorchiidae) from chaetodontid fishes on the Great Barrier Reef. Parasitol Int 60(255–269)

    Google Scholar 

  • Miller TL, Bray RA, Cribb TH (2011) Taxonomic approaches to and interpretation of host specificity of trematodes of fishes: lessons from the Great Barrier Reef. Parasitology 138:1710–1722. doi:10.1017/S0031182011000576

    Article  PubMed  CAS  Google Scholar 

  • Miller TL, Bray RA, Justine J-L, Cribb TH (2010) Varialvus gen. nov. (Digenea: Cryptogonimidae), from species of Lutjanidae (Perciformes) off the Great Barrier Reef, New Caledonia and the Maldives. Caledonia Maldives Acta Parasitol 55:327–339

    Article  Google Scholar 

  • Miller TL, Cribb TH (2007a) Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. Int J Parasitol 37:1023–1045. doi:10.1016/j.ijpara.2007.01.006

    Article  CAS  Google Scholar 

  • Miller TL, Cribb TH (2007b) Two new cryptogonimid genera (Digenea: Cryptogonimidae) from Lutjanus bohar (Perciformes: Lutjanidae): analyses of multiple ribosomal DNA regions reveals wide geographic distribution and presence of cryptic species. Acta Parasitol 52:104–113. doi:10.2478/s11686-007-0019-y

    Article  CAS  Google Scholar 

  • Miller TL, Cribb TH (2008) Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitol 53(4):344–364

    Article  Google Scholar 

  • Miller TL, Downie AJ, Cribb TH (2009) Morphological disparity despite genetic similarity; new species of Lobosorchis Miller & Cribb, 2005 (Digenea: Cryptogonimidae) from the Great Barrier Reef and the Maldives. Zootaxa 1992:37–52

    Google Scholar 

  • Moravec F, Sey O (1989) Some trematodes of freshwater fishes from North Vietnam with a list of recorded endohelminths by fish hosts. Fol Parasitol 36:243–262

    CAS  Google Scholar 

  • Mori KI, Yamamoto K, Teruya K, Shiozawa S, Yoseda K, Sugaya T, Shirakashi S, Itoh N, Ogawa K (2007) Endoparasitic dinoflagellate of the genus Ichthyodinium infecting fertilized eggs and hatched larvae observed in the seed production of leopard coral grouper Plectropomus leopardus. Fish Pathol 42:49–57

    Article  Google Scholar 

  • Nagaty HF (1937) Trematodes of fishes from the Red Sea Part 1. Studies on the family Bucephalidae Poche, 1907. Egyptian University, Cairo

    Google Scholar 

  • Nagaty HF (1973) Trematodes of fishes from the Red Sea. Parts 1 to 20: a recapitulation. Bull Soc Zool Egypt 25:1–13

    Google Scholar 

  • Nahhas FM, Cable RM (1964) Digenetic and aspidogastrid trematodes from marine fishes of Curacao and Jamaica. Tul Stud Zool 11:169–228

    Google Scholar 

  • Nelson JS (2006) Fishes of the world. Wiley, New Jersey

    Google Scholar 

  • Nolan MJ, Cribb TH (2004) Two new blood flukes (Digenea: Sanguinicolidae) from Epinephelinae (Perciformes: Serranidae) of the Pacific Ocean. Parasitol Int 53:327–335

    Article  PubMed  Google Scholar 

  • Nolan MJ, Cribb TH (2006) An exceptionally rich complex of Sanguinicolidae von Graff, 1907 (Platyhelminthes: Trematoda) from Siganidae, Labridae and Mullidae (Teleostei: Perciformes) from the Indo-West Pacific Region. Zootaxa 1218:1–80

    Google Scholar 

  • Overstreet RM, Køie M (1989) Pearsonellum corventum, gen. et sp. nov. (Digenea: Sanguinicolidae), in serranid fishes from the Capricornia section of the Great Barrier Reef. Aust J Zool 37:71–79

    Article  Google Scholar 

  • Overstreet RM, Curran SS (2002) Superfamily Bucephaloidea Poche, 1907 Keys to the Trematoda. CABI Publishing, Wallingford, pp 67–110

    Google Scholar 

  • Pearson JC (1972) A phylogeny of life-cycle patterns of the Digenea. Adv Parasitol 10:153–189

    Article  PubMed  CAS  Google Scholar 

  • Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. University of Hawai'i Press, Honolulu

    Google Scholar 

  • Shen J (1990) Digenetic trematodes of marine fishes from Hainan Island. Science Publications, Beijing

    Google Scholar 

  • Sogandares-Bernal F (1959) Digenetic trematodes of marine fishes from the Gulf of Panama and Bimini, British West Indies. Tul Stud Zool 7:71–117

    Google Scholar 

  • Sogandares-Bernal F, Sogandares LM (1961) Nine digenetic trematodes of marine fishes from the Atlantic coast of Panama. Tul Stud Zool 8:141–153

    Google Scholar 

  • Stunkard HW (1976) The life cycles, intermediate hosts, and larval stages of Rhipidocotyle transversale Chandler, 1935 and Rhipidocotyle lintoni Hopkins, 1954: life-cycles and systematics of bucephalid trematodes. Biol Bull 150:294–317

    Article  PubMed  CAS  Google Scholar 

  • Stunzenas V, Cryan JR, Molloy DP (2004) Comparison of rDNA sequences from colchicine treated and untreated sporocysts of Phyllodistomum folium and Bucephalus polymorphus (Digenea). Parasitol Int 53:223–228

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • van Herwerden L, Davies CR, Choat JH (2002) Phylogenetic and evolutionary perspectives of the Indo-Pacific grouper Plectropomus species on the Great Barrier Reef, Australia. J F Biol 60:1591–1596

    Article  Google Scholar 

  • Welch DJ, Mapstone BD, Begg GA (2008) Spatial and temporal variation and effects of changes in management in discard rates from the commercial reef line fishery of the Great Barrier Reef, Australia. Fish Res 90:247–260

    Article  Google Scholar 

  • Williams EH, Bunkley-Williams L (1996) Parasites of offshore big game fishes of Puerto Rico and the Western Atlantic. Antillean College Press, Mayaguez

    Google Scholar 

  • Yamaguti S (1970) Digenetic trematodes of Hawaiian fishes. Keigaku Publishing Company, Tokyo

    Google Scholar 

  • Yamaguti S (1971) Synopsis of the digenetic trematodes of vertebrates, vol 1 and 2. Keigaku Publishing Company, Tokyo

    Google Scholar 

  • Young PC (1967) New Monogenoidea from Australian brackish water and reef fishes. J Parasitol 53:1008–1015

    Article  PubMed  CAS  Google Scholar 

  • Young PC (1969) Some monogenoideans of the family Diplectanidae Bychowsky, 1957 from Australian teleost fishes. J Helminthol 43:223–254

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was funded by the Australian Research Council Discovery grant DP110105389. It was also partly funded by, and is a contribution from, the Australian node of the CReefs global research initiative (grant number 209/29), a partnership between the ABRS, BHP Billiton, the GBR Foundation, the Census of Marine Life and the Australian Institute of Marine Science. The CReefs Australia Project is generously sponsored by BHP Billiton in partnership with The GBR Foundation, the Australian Institute of Marine Science, the Australian Biological Resources Study and the Alfred P. Sloan Foundation. CReefs is a field programme of the Census of Marine Life. We thank Rob Adlard, Rod Bray, Matthew Nolan, Holly Heiniger, Timothy Lucas, Jonathon Yantsch, Barton McKenzie, Ashley Roberts-Thomson, Conor Jones, Gaines Tyler and Nicole Elphinstone for assistance with collecting. We also gratefully thank the staff of the Heron and Lizard Island research stations for their support and hospitality during our many long stays.

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Bott, N.J., Miller, T.L. & Cribb, T.H. Bucephalidae (Platyhelminthes: Digenea) of Plectropomus (Serranidae: Epinephelinae) in the tropical Pacific. Parasitol Res 112, 2561–2584 (2013). https://doi.org/10.1007/s00436-013-3423-2

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