Abstract
Ankistromeces Nolan & Cribb, 2004 and Phthinomita Nolan & Cribb, 2006 are sister genera of threadlike blood flukes (Trematoda: Aporocotylidae) infecting teleost fishes of the tropical Indo-west Pacific. Here, we report new collections of these genera from Australia, Indonesia, and Japan. A new species of Ankistromeces, Ankistromeces kawamurai n. sp., is described from Siganus spinus (Linnaeus) off Okinawa, Japan, and a new species of Phthinomita, Phthinomita abdita n. sp., from Choerodon cephalotes (Castelnau), in Moreton Bay, Australia; the new species are morphologically cryptic within their respective genera and are delineated by molecular and ecological data. Ankistromeces olsoni Nolan & Cribb, 2006 is reported from Siganus fuscescens (Houttuyn) off Heron Island (southern Great Barrier Reef), Lizard Island (northern Great Barrier Reef), and Okinawa and Wakayama Prefectures, Japan and from Siganus spinus (Linnaeus) from off Bali, Indonesia. Ankistromeces mariae Nolan & Cribb, 2004 is re-reported from the type-host, Meuschenia freycineti (Quoy & Gaimard), from a new location, Gypsy Bay, Tasmania. Phthinomita poulini Nolan & Cribb, 2006 is re-reported from its type-locality, Lizard Island, from a range of mullids, including five new host species, and its range is extended to include Moreton Bay. Phthinomita symplocos Nolan & Cribb, 2006 is reported from Bali and P. hallae Nolan & Cribb, 2006, P. jonesi Nolan & Cribb, 2006, P. littlewoodi Nolan & Cribb, 2006, and P. munozae Nolan & Cribb, 2006 are each re-reported from their type-host and type-localities. New cox1 mtDNA data were generated for all known species of these two genera from new and archival material. Analyses of these data enabled an evaluation of all known Phthinomita species; P. robertsthomsoni Nolan & Cribb, 2006 is synonymised with P. adlardi Nolan & Cribb, 2006, and P. brooksi Nolan & Cribb, 2006 is synonymised with P. sasali Nolan & Cribb, 2006. We highlight the failure of ITS2 data to delineate closely related aporocotylid species. In contrast, cox1 sequence data are proving reliable and effective in this context and we recommend their incorporation in future studies of blood fluke taxonomy.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Change history
27 September 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11230-021-10005-5
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.
Andres, M. J., Pulis, E. E., & Overstreet, R. M. (2016). Description of three species of Isorchis (Digenea: Atractotrematidae) from Australia. Acta Parasitologica, 61, 590–601.
Blasco-Costa, I., Cutmore, S. C., Miller, T. L., & Nolan, M. J. (2016). Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology, 93, 295–306.
Bray, R. A., & Cribb, T. H. (2015). Are cryptic species a problem for parasitological biological tagging for stock identification of aquatic organisms? Parasitology, 142, 125–133.
Bray, R. A., Cutmore, S. C., & Cribb, T. H. (2018). Lepotrema Ozaki, 1932 (Lepocreadiidae: Digenea) from Indo-Pacific fishes, with the description of eight new species, characterised by morphometric and molecular features. Systematic Parasitology, 95, 693–741.
Bray, R. A., Cutmore, S. C., & Cribb, T. H. (2021). A paradigm for the recognition of cryptic trematode species in tropical Indo-west Pacific fishes: the problematic genus Preptetos (Trematoda: Lepocreadiidae). International Journal for Parasitology.
Brooks, X., Cribb, T. H., Yong, R. Q-Y., & Cutmore, S. C. (2017). A re-evaluation of diversity of the Aporocotylidae Odhner, 1912 in Siganus fuscescens (Houttuyn) (Perciformes: Siganidae) and associated species. Systematic Parasitology, 94, 717–737.
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., Bott, N. J., Bray, R. A., McNamara, M. K. A., Miller, T. L., Nolan, M. J., et al. (2014). Trematodes of the Great Barrier Reef: emerging patterns of diversity and richness in coral reef fishes. International Journal for Parasitology, 44, 929–939.
Cutmore, S. C., Diggles, B. K., & Cribb, T. H. (2016). Transversotrema Witenberg, 1944 (Trematoda: Transversotrematidae) from inshore fishes of Australia: description of a new species and significant range extensions for three congeners. Systematic Parasitology, 93, 639–652.
Huston, D. C., Cutmore, S. C., & Cribb, T. H. (2018). Trigonocephalotrema (Digenea: Haplosplanchnidae), a new genus for trematodes parasitising fishes of two Indo-West Pacific acanthurid genera. Invertebrate Systematics, 32, 759–773.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549.
Kuriiwa, K., Hanzawa, N., Yoshino, T., Kimura, S., & Nishida, M. (2007). Phylogenetic relationships and natural hybridization in rabbitfishes (Teleostei: Siganidae) inferred from mitochondrial and nuclear DNA analyses. Molecular Phylogenetics and Evolution, 45, 69–80.
Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution, 3, 221–229.
Littlewood, D. T. J., Curini-Galletti, M., & Herniou, E. A. (2000). The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.
Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species?—Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology, 27, 1289–1297.
Maddison, W. P., & Maddison, D. R. (2020). Mesquite: a modular system for evolutionary analysis. Version 3.31 http://mesquiteproject.org.
Manter, H. W. (1963). Studies on Digenetic Trematodes of Fishes of Fiji. II. Families Lepocreadiidae, Opistholebetidae, and Opecoelidae. Journal of Parasitology, 49, 99-113.
Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2018). Revision of Podocotyloides Yamaguti, 1934 (Digenea: Opecoelidae), resurrection of Pedunculacetabulum Yamaguti, 1934, and the naming of a cryptic opecoelid species. Systematic Parasitology, 95, 1–31.
Morgan, J. A., & 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.
Nadler, S. A., & Pérez-Ponce de León, G. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology, 138, 1688–1709.
Nolan, M. J., Cantacessi, C., Cutmore, S. C., Cribb, T. H., & Miller, T. L. (2016). High-intensity cardiac infections of Phthinomita heinigerae n. sp. (Digenea: Aporocotylidae) in the orangelined cardinalfish, Taeniamia fucata (Cantor), off Heron Island on the Great Barrier Reef. Parasitology International, 65, 371–377.
Nolan, M. J., & Cribb, T. H. (2004). Ankistromeces mariae n. g., n. sp. (Digenea: Sanguinicolidae) from Meuschenia freycineti (Monacanthidae) off Tasmania. Systematic Parasitology, 57, 151–157.
Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.
Nolan, M. J., & Cribb, T. H. (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.
Orélis-Ribeiro, R., Halanych, K. M., Dang, B. T., Bakenhaster, M. D., Arias, C. R., & Bullard, S. A. (2017). Two new species of Elopicola (Digenea: Aporocotylidae) from Hawaiian ladyfish, Elops hawaiensis (Eastern Sea) and Atlantic tarpon, Megalops atlanticus (Gulf of Mexico) with a comment on monophyly of elopomorph blood flukes. Parasitology International, 66, 305–318.
Palacios-Abella, J. F., Georgieva, S., Mele, S., Raga, J. A., Isbert, W., Kostadinova, A., et al. (2017). Skoulekia erythrini n. sp. (Digenea: Aporocotylidae): a parasite of Pagellus erythrinus (L.) (Perciformes: Sparidae) from the western Mediterranean with an amendment of the generic diagnosis. Systematic Parasitology, 94, 669–688.
Palacios-Abella, J. F., Raga, J. A., Mele, S., & Montero, F. E. (2018). Blood fluke diseases in Pagellus spp. (Sparidae): pathology and description of a new species of Skoulekia in the blackspot seabream P. bogaraveo (Brünnich). Aquaculture, 495, 472–483.
Parukhin, A. M. (1976). [Parasitic worms of food fishes in the southern seas] (in Russian). Kiev, USSR: Naukova Dumka, 184 pp.
Pérez-Ponce de León, G., & Poulin, R. (2018). An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology, 92, 197–202.
Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., et al. (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371.
Poulin, R. (2011). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters, 7, 241–244.
Rabosky, D. L., Chang, J., Title, P. O., Cowman, P. F., Sallan, L., Friedman, M., et al. (2018). An inverse latitudinal gradient in speciation rate for marine fishes. Nature, 559, 392–395.
Repullés-Albelda, A., Montero, F. E., Holzer, A. S., Ogawa, K., Hutson, K. S., & Raga, J. A. (2008). Speciation of the Paradeontacylix spp. (Sanguinicolidae) of Seriola dumerili. Two new species of the genus Paradeontacylix from the Mediterranean. Parasitology International, 57, 405–414.
Snyder, S. D., & Tkach, V. V. (2001). Phylogenetic and biogeographical relationships among some Holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–1440.
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Trieu, N., Cutmore, S. C., Miller, T. L., & Cribb, T. H. (2015). A species pair of Bivesicula Yamaguti, 1934 (Trematoda: Bivesiculidae) in unrelated Great Barrier Reef fishes: implications for the basis of speciation in coral reef fish trematodes. Systematic Parasitology, 91, 231–239.
Wee, N. Q-X., Cribb, T. H., Bray, R. A., & Cutmore, S. C. (2017). Two known and one new species of Proctoeces from Australian teleosts: variable host-specificity for closely related species identified through multi-locus molecular data. Parasitology International, 66, 16–26.
Xia, X. (2018). DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 35, 1550–1552.
Xia, X., & Lemey, P. (2009). Assessing substitution saturation with DAMBE. In: Lemey, P., Salemi, M. & Vandamm, A.-M. (Eds) The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. 2nd edition. Cambridge, UK: Cambridge University Press, pp. 615–630.
Xia, X., Xie, Z., Salemi, M., Chen, L., & Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.
Yamaguti, S. (1958). The Digenetic Trematodes of Fishes, Vol 1. New York: Interscience, 1575 pp.
Yamaguti, S. (1970). Digenetic Trematodes of Hawaiian Fishes. Tokyo: Keigaku Pub. Co., 436 pp.
Yong, R. Q-Y., Cribb, T. H., & Cutmore, S. C. (2021). Molecular phylogenetic analysis of the problematic genus Cardicola (Digenea: Aporocotylidae) indicates massive polyphyly, dramatic morphological radiation and host-switching. Molecular Phylogenetics and Evolution, 164, 107290.
Yong, R. Q-Y., Cutmore, S. C., Bray, R. A., Miller, T. L., Semarariana, I. W. Y., Palm, H. W., et al. (2016). Three new species of blood flukes (Digenea: Aporocotylidae) infecting pufferfishes (Teleostei: Tetraodontidae) from off Bali, Indonesia. Parasitology International, 65, 432–443.
Yong, R. Q-Y., Cutmore, S. C., Jones, M. K., Gauthier, A. R. G., & Cribb, T. H. (2018). A complex of the blood fluke genus Psettarium (Digenea: Aporocotylidae) infecting tetraodontiform fishes of east Queensland waters. Parasitology International, 67, 321–340.
Yong, R. Q-Y., Cutmore, S. C., Miller, T. L., Adlard, R. D., & Cribb, T. H. (2013). The ghost of parasites past: eggs of the blood fluke Cardicola chaetodontis (Aporocotylidae) trapped in the heart and gills of butterflyfishes (Perciformes: Chaetodontidae) of the Great Barrier Reef. Parasitology, 140, 1186–1194.
Acknowledgements
For assistance with host collections in Australia we thank John Page, Dave Thompson, Dr Daniel Huston and the various members of the Marine Parasitology Laboratory; in Indonesia we thank Dr Harry Palm, Dr Rod Bray and Stefan Theisen; and in Japan we thank Takuya Katsuki, Riko Kokaji, Tomoya Matsuda of Kindai University and Dr Shiori Kunihiro, Dr Piera Biondi, Dr Hin Boo Wee, Iori Kawamura and Masaru Mizuyama of the University of the Ryukyus. We also thank the staff of Moreton Bay, Heron Island and Lizard Island Research Stations for their support in the field.
Funding
We acknowledge the Australian Biological Resources Study (ABRS) for their ongoing support. This study was funded by the ABRS National Taxonomy Research Grant RG19-37, awarded to SCC and THC. Collecting in Japan was supported by an Australian Society for Parasitology (ASP) Network Researcher Exchange, Training and Travel Award grant to SCC. Collecting in Indonesia was conducted during the First Educational Workshop on Fish Parasites in Indonesia, July 21st - August 2nd 2013, supported by the German Federal Ministry for Education and Science (BMBF Grant No. 03F0641D) within the framework of the joint Indonesian-German research programme SPICE III - MABICO (Science for the Protection of Indonesian Coastal Marine Ecosystems).
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Cutmore, S.C., Yong, R.QY., Reimer, J.D. et al. Two new species of threadlike blood flukes (Aporocotylidae), with a molecular revision of the genera Ankistromeces Nolan & Cribb, 2004 and Phthinomita Nolan & Cribb, 2006. Syst Parasitol 98, 641–664 (2021). https://doi.org/10.1007/s11230-021-10002-8
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DOI: https://doi.org/10.1007/s11230-021-10002-8