Abstract
A survey of Pacific coral reef fishes for sanguinicolids revealed that two species of Lutjanidae (Lutjanus argentimaculatus, L. bohar), six species of Siganidae (Siganus corallinus, S. fuscescens, S. lineatus, S. margaritiferus, S. punctatus, S. vulpinus), seven species of Chaetodontidae (Chaetodon aureofasciatus, C. citrinellus, C. flavirostris, C. lineolatus, C. reticulatus, C. ulietensis, C. unimaculatus), three species of Scombridae (Euthynnus affinis, Scomberomorus commerson, S. munroi) and three species of Scaridae (Chlorurus microrhinos, Scarus frenatus, S. ghobban) were infected with morphologically similar sanguinicolids. These flukes have a flat elliptical body, a vestigial oral sucker, a single testis, separate genital pores and a post-ovarian uterus. However, these species clearly belong in two genera based on the position of the testis and genital pores. Sanguinicolids from Lutjanidae, Siganidae, Chaetodontidae and Scombridae belong in Cardicola Short, 1953; the testis originates anteriorly to, or at the anterior end of, the intercaecal field and does not extend posteriorly to it, the male genital pore opens laterally to the sinistral lateral nerve chord and the female pore opens near the level of the oötype (may be anterior, lateral or posterior to it) antero-dextral to the male pore. Those from Scaridae are placed in a new genus, Braya; the testis originates near the posterior end of the intercaecal field and extends posteriorly to it, the male pore opens medially at the posterior end of the body and the female pore opens posterior to the oötype, antero-sinistral to the male pore. The second internal transcribed spacer (ITS2) of ribosomal DNA from these sanguinicolids and a known species, Cardicola forsteri Cribb, Daintith & Munday, 2000, were sequenced, aligned and analysed to test the distinctness of the putative new species. Results from morphological comparisons and molecular analyses suggest the presence of 18 putative species; 11 are described on the basis of combined morphological and molecular data and seven are not because they are characterised solely by molecular sequences or to few morphological specimens (n=one). There was usually a correlation between levels of morphological and genetic distinction in that pairs of species with the greatest genetic separation were also the least morphologically similar. The exception in this regard was the combination of Cardicola tantabiddii n. sp. from S. fuscescens from Ningaloo Reef (Western Australia) and Cardicola sp. 2 from the same host from Heron Island (Great Barrier Reef). These two parasite/host/location combinations had identical ITS2 sequences but appeared to differ morphologically (however, this could simply be due to a lack of morphological material for Cardicola sp. 2). Only one putative species (Cardicola sp. 1) was found in more than one location; most host species harboured distinct species in each geographical location surveyed (for example, S. corallinus from Heron and Lizard Islands) and some (for example, S. punctatus, S. fuscescens and Chlorurus microrhinos) harboured two species at a single location. Distance analysis of ITS2 showed that nine species from siganids, three from scombrids and five from scarids formed monophyletic clades to the exclusion of sanguinicolids from the other host families. Cardicola milleri n. sp. and C. chaetodontis Yamaguti, 1970 from lutjanids and chaetodontids, respectively, were the only representatives from those families that were sequenced. Within the clade formed by sanguinicolids from Siganidae there was a further division of species; species from the morphologically similar S. fuscescens and S. margaritiferus formed a monophyletic group to the exclusion of sanguinicolids from all other siganid species.
References
Anderson, G.R. & Barker, S.C. (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology, 41, 87–94.
Balavoine, G. (1998) Are Platyhelminthes coelomates without a coelom? An argument based on the evolution of Hox genes. American Zoologist, 38, 843–858.
Bartoli, P. & Jousson, O. (2003) The life-cycle of Podocotyle scorpaenae (Opecoelidae: Digenea) demonstrated by comparative analysis of ribosomal DNA sequences. In: Combes, C. & Jourdane, J. (Eds.), Taxonomie, écologie et évolution des métazoaires parasites. Taxonomy, ecology and evolution of metazoan parasites. (Livre hommage à Louis Euzet). Presses Universitaires de Perpignan Perpignan, pp. 17–28.
Blair, D., Agatsuma, T., Watanobe, T., Okamoto, M. & Ito, A. (1997) Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences. Parasitology, 115, 411–417.
Blair, D., Waikagul, J., Honzako, Y. & Agatsuma, T. (1998) Phylogenetic relations among the Thai species of Paragonimus inferred from DNA sequences. Parasitology International, 47, 135.
Blum, S.D. (1989) Biogeography of the Chaetodontidae: an analysis of allopatry among closely related species. Environmental Biology of Fishes, 25, 9–31.
Bullard, S.A., Goldstein, R.J., Goodwin, R.H. & Overstreet, R.M. (2004) Cardicola forsteri (Digenea: Sanguinicolidae) from the heart of a northern bluefin tuna, Thunnus thynnus (Scombridae), in the northwest Atlantic Ocean. Comparative Parasitology, 71, 245–246.
Bullard, S.A. & Overstreet, R.M. (2003) Elaphrobates euzeti gen. and sp. n. (Digenea: Sanguinicolidae) from snappers (Lutjanidae) in the Gulf of Mexico. In: Combes, C. & Jourdane, J. (Eds.), Taxonomie, écologie et évolution des métazoaires parasites. Taxonomy, ecology and evolution of metazoan parasites. (Livre hommage à Louis Euzet). Presses Universitaires de Perpignan Perpignan. 97–113.
Bullard, S.A. & Overstreet, R.M. (2004) Two new species of Cardicola (Digenea: Sanguinicolidae) in drums (Sciaenidae) from Mississippi and Louisiana. Journal of Parasitology, 90, 128–136.
Chambers, C.B. & Cribb, T.H. (2006) Phylogeny, evolution and co-accommodation of the Quadrifoliovariinae Yamaguti, 1965 (Lecithasteridae, Digenea). Systematic Parasitology, 63, 61–68.
Cribb, T.H., Anderson, G.R., Adlard, R.D. & Bray, R.A. (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology, 28, 1791–1795.
Cribb, T.H. & Bray, R.A. (1998) Trematodes of fishes: a test case for predictions of parasite diversity on the Great Barrier Reef. In: Greenwood, J.G. & Hall, N.J. (Eds.), Proceedings of the Australian Coral Reef Society 75th Anniversary Conference, Heron Island October 1997. School of Marine Science Brisbane. p. 43–56.
Cribb, T.H., Daintith, M. & Munday, B. (2000a) A new blood fluke, Cardicola forsteri, (Digenea: Sanguinicolidae) of southern bluefin tuna (Thunnus maccoyii) in aquaculture. Transactions of the Royal Society of South Australia, 124, 117–120.
Cribb, T.H., Pichelin, S., Dufour, V., Bray, R.A., Chauvet, C., Faliex, E., Galzin, R., Lo, C.M., Lo, Y.A., Morand, S., Rigby, M.C. & Sasal, P. (2000b) Parasites of recruiting coral reef fish larvae in New Caledonia. International Journal for Parasitology, 30, 1445–1451.
Galazzo, D.E., Dayanandan, S., Marcogliese, D.J. & McLaughlin, J.D. (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology, 80, 2207–2217.
Goto, S. & Ozaki, Y. (1929) Brief notes on new trematodes II. Japanese Journal of Zoology, 2, 369–381.
Goto, S. & Ozaki, Y. (1930) Brief notes on new trematodes III. Japanese Journal of Zoology, 3, 73–82.
Hasegawa, M., Kishino, H. & Yano, T.-a. (1985) Dating of the Human-ape splitting by a molecular clock of mitochondrial-DNA. Journal of Molecular Evolution, 22, 160–174.
Herbert, B.W., Shaharom-Harrison, F.M. & Overstreet, R.M. (1994) Description of a new blood-fluke, Cruoricola lates n. g., n. sp. (Digenea: Sanguinicolidae), from sea-bass Lates calcarifer (Bloch, 1790) (Centropomidae). Systematic Parasitology, 29, 51–60.
Jousson, O. & Bartoli, P. (2001) Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. International Journal for Parasitology, 31, 706–714.
Jousson, O., Bartoli, P. & Pawlowski, J. (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology, 29, 1853–1858.
Jousson, O., Bartoli, P. & Pawlowski, J. (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology, 13, 778–785.
Jousson, O., Bartoli, P., Zaninetti, L. & Pawlowski, J. (1998) Use of the ITS rDNA for elucidation of some life-cycles of Mesometridae (Trematoda, Digenea). International Journal for Parasitology, 28, 1403–1411.
Kirk, R.S. & Lewis, J.W. (1993) The life-cycle and morphology of Sanguinicola inermis Plehn, 1905 (Digenea: Sanguinicolidae). Systematic Parasitology, 25, 125–133.
Knoff, M. & Amato, J.F.R. (1992) Nova especie do genero Cardicola Short, 1953 (Sanguinicolidae, Cardicolinae) parasita de tainhas Mugil platanus Günther, 1880 da costa do estado do Rio De Janeiro, Brazil. Revista Brasileiro de Biologica, 51, 567–570.
Korotaeva, V.D. (1970) [Parasite fauna of two species of commercial fish of the family Cheilodactylidae in the region of Australia and New Zealand] (In Russian). In: Vodjanitskii, V.A. (Ed.), Problems in marine parasitology. Naukova Dumka Kiev. p. 44–46.
Kuiter, R.H. & Debelius, H. (2001) Surgeonfishes, Rabbitfishes and their relatives. A comprehensive guide to Acanthuroidei, TMC Publishing Chorleywood, United Kingdom, 208 pp.
Lebedev, B.I. & Mamaev, Y.L. (1968) Two new species of Cardicola Short, 1953 (Trematoda: Sanguinicolidae) from fishes in the South China Sea. In: Skryabin, K.I. & Mamaev, Y.L. (Eds.), Helminths of animals of the Pacific Ocean. Gelminty Zhivotnykh Tikhogo Okeana. p. 72–75.
Lebedev, B.I. & Paruchin, A.M. (1972) New sanguinicolids (Trematoda) of fishes from the Gulf of Mannar (coasts of India). Biologisckie Nauki, 4, 7–14.
Littlewood, D.T.J., McDonald, S.M., Gill, A.C. & Cribb, T.H. (2004) Molecular phylogenetics of Chaetodon and the Chaetodontidae (Teleostei: Perciformes) with reference to morphology. Zootaxa, 779, 1–20.
Littlewood, D.T.J., Rohde, K. & Clough, K.A. (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biological Journal of the Linnean Society, 66, 75–114.
Lo, C.F., Morgan, J.A.T., Galzin, R. & Cribb, T.H. (2001) Identical digeneans in coral reef fishes from French Polynesia and the Great Barrier Reef (Australia) demonstrated by morphology and molecules. International Journal for Parasitology, 31, 1573–1578.
Loftin, H. (1960) An annotated check-list of trematodes and cestodes and their vertebrate hosts from northwestern Florida. Quarterly Journal of the Florida Academy of Sciences, 23, 302–314.
Luton, K., Walker, D. & Blair, D. (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology, 56, 323–328.
Mamaev, Y.L. (1968) [Helminths of tuna fish in the South China Sea]. In: Skryabin, K.I. & Mamaev, Y.L. (Eds.), [Helminthes of Animals of the Pacific Ocean]. Izdatel’stvo "Nauka" Moscow. p. 5–27.
Manter, H.W. (1947) The Digenetic trematodes of marine fishes of Tortugas, Florida. The America Midland Naturalist, 38, 257–416.
Manter, H.W. (1954) Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand, 82, 475–568.
Mladineo, I. & Tudor, M. (2004) Digenea of Adriatic cage-reared northern bluefin tuna (Thunnus thynnus thynnus). Bulletin of the European Association of Fish Pathologists, 24, 144–152.
Morgan, J.A.T. & Blair, D. (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology, 111, 609–615.
Nahhas, F.M. & Short, R.B. (1965) Digenetic trematodes of marine fishes from Apalachee Bay, Gulf of Mexico. Tulane Studies in Zoology and Botany, 12, 39–50.
Nolan, M.J. & Cribb, T.H. (2004a) Ankistromeces mariae n. g., n. sp. (Digenea: Sanguinicolidae) from Meuschenia freycineti (Monacanthidae) from Tasmania. Systematic Parasitology, 57, 151–157.
Nolan, M.J. & Cribb, T.H. (2004b) Two new blood flukes (Digenea: Sanguinicolidae) from Epinephelinae (Perciformes: Serranidae) of the Pacific Ocean. Parasitology International, 53, 327–335.
Nolan, M.J. & Cribb, T.H. (2005a) Chaulioleptos haywardi n. gen., n. sp (Digenea: Sanguinicolidae) from Filimanus heptadactyla (Perciformes: Polynemidae) of Moreton Bay, Australia. Journal of Parasitology, 91, 630–634.
Nolan, M.J. & Cribb, T.H. (2005b) Sanguinicola maritimus n. sp (Digenea: Sanguinicolidae) from Labridae (Teleostei: Perciformes) of southern Australian waters. Systematic Parasitology, 61, 99–106.
Nolan, M.J. & Cribb, T.H. (2005c) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.
Overstreet, R.M. (1983) Aspects of the biology of the spotted seatrout, Cynoscion nebulosus, in Mississippi. Gulf Research Reports, Supplement, 1, 1–43.
Overstreet, R.M. & Køie, M. (1989) Pearsonellum corventum, gen. et sp. nov. (Digenea: Sanguinicolidae), in serranid fishes from the Capricornia section of the Great Barrier Reef. Australian Journal of Zoology, 37, 71–79.
Paxton, J.R., Hoese, D.F., Allen, G.R. & Hanley, J.E. (1989) Pisces. Petromyzontidae to Carangidae, Australian Government Publishing Service Canberra, 665 pp.
Pearson, J.C. (1992) On the position of the digenean family Heronimidae: an inquiry into a cladistic classification of the Digenea. Systematic Parasitology, 21, 81–166.
Plehn, M. (1905) Sanguinicola armata und inermis (n. gen., n. sp.) n. fam. Rhynchostomida. Ein ento-parasitisches turbellar im blute von Cypriniden. Zoologischer Anzeiger, 29, 224–252.
Rambaut, A. (1996) Se-Al: Sequence Alignment Editor.
Russell, B.C. (1993) Fishes. In: Mather, P. & Bennett, I. (Eds.), A coral reef handbook. A guide to the geology, flora and fauna of the Great Barrier Reef. Surrey Beatty & Sons PTY LTD Sydney. p. 185–197.
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Springs Harbour Laboratory Press, USA Cold Springs Harbour, New York, E3-E4.
Schulenburg, J.H.G.v.d., Englisch, U. & Waegele, J.W. (1999) Evolution of ITS1 rDNA in the Digenea (Platyhelminthes: Trematoda): 3’ end sequence conservation and its phylogenetic utility. Journal of Molecular Evolution, 48, 2–12.
Short, R.B. (1953) A new blood fluke, Cardicola laruei n. g., n. sp. (Aporocotylidae) from marine fishes. Journal of Parasitology, 39, 304–309.
Smith, J.W. (2002) Family Sanguinicolidae von Graff, 1907. In: Gibson, D.I., Jones, A. & Bray, R.A. (Eds.), Keys to the Trematoda. Wallingford: CAB International Cambridge. p. 433–452.
Swofford, D.L. (2002) PAUP: Phylogenetic Analysis Using Parsimony and other methods (Version 4). Sunderland, Massachusetts, Sinauer.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
Tkach, V.V., Pawlowski, J. & Sharpilo, V.P. (2000) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Muller, 1780). Systematic Parasitology, 47, 9–22.
Wilson, B.R. & Allen, G.R. (1987) Major components and distribution of marine fauna. In: Dyne, G.R. & Walton, D.W. (Eds.), Fauna of Australia. General Articles. Australian Government Publishing Service Canberra. p. 43–68.
Woodland, D.J. (1990) Revision of the fish family Siganidae with descriptions of two new species and comments on distribution and biology, Bishop Museum Press Bishop, 136 pp.
Yamaguti, S. (1970) Digenetic trematodes of Hawaiian fishes, Keigaku Publishing Co. Tokyo, 436 pp.