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

https://doi.org/10.1016/j.parint.2016.05.006Get rights and content

Highlights

  • A species of aporocotylid trematode is described from Taeniamia fucata.

  • The species is distinguished by morphology, molecules, and host family differences.

  • Prevalence (95%) and intensity of infection (17–25) was relatively high.

  • Phthinomita heinigerae forms a clade with species from a labrid and from mullids.

  • Provide evidence for recent host-switching by aporocotylids of coral reef fishes

Abstract

We report a new species of aporocotylid trematode (Platyhelminthes: Digenea) from the heart of the orangelined cardinalfish, Taeniamia fucata (Cantor), from off Heron Island on the southern Great Barrier Reef. We used an integrated approach, analysing host distribution, morphology, and genetic data from the internal transcribed spacer 2 of the ribosomal DNA, to circumscribe Phthinomita heinigerae n. sp. This is the first species of Phthinomita Nolan & Cribb, 2006 reported from the Apogonidae; existing species and known ‘types’ are recorded from species of the Labridae, Mullidae, and Siganidae. The new species is distinguished from its 11 congeners in having a body 2977–3539 long and 16.5–22.4 times longer than wide, an anterior testis 6.2–8.2 times longer than wide and 8.3–13.0 times longer than the posterior testis, a posterior testis whose width is 35–56% of the body width, and an ovary positioned 11–13% of the body length from the posterior end, and is entirely anterior to the posterior margin of the anterior testis. In addition, 2–34 base differences (0.4–7.0% sequence divergence over 485 base positions) were detected among the ITS2 sequence representing P. heinigerae n. sp. and the 14 representing other Phthinomita species/molecular types. Prevalence and intensity of infection with P. heinigerae n. sp. was relatively high within the heart tissue of T. fucata, with 19 of 20 fish examined from off Heron Island infected (95%) with 7–25 adult worms (arithmetic mean 16.6). Infections by these parasites accounted for an occupation of 7–30% of the total estimated heart volume.

Introduction

The Aporocotylidae Odhner, 1912 (Platyhelminthes: Trematoda) is a family of parasitic flatworms that has, in recent years, emerged as an increasingly rich, and morphologically diverse, group of digeneans. There are currently 142 accepted species from 37 genera [1], [2], [3], [4], [5], which infect a broad range of fishes. Species from seven genera have been recorded from fishes of the Great Barrier Reef (GBR): Ankistromeces Nolan & Cribb, 2004 (see [6]); Braya Nolan & Cribb, 2006 (see [7]); Cardicola Short, 1953 (see [7], [8], [9]); Pearsonellum Overstreet & Køie, 1989 (see [10], [11]); Plethorchis Martin, 1975 (see [12]); Phthinomita Nolan & Cribb, 2006 (see [6]); and, Rhaphidotrema Yong & Cribb, 2011 (see [13]). Phthinomita is the most complex of these, consisting of 11 recognised species and numerous undefined ‘types’ represented by a unique DNA sequence or single morphological specimen. Unlike most aporocotylids, which are typically characterised by a flat body that may be linear, elliptical, or lanceolate, species of Phthinomita are long and thread-like. As adults, they wind through the intertrabecular spaces of the ventricle of their hosts, which to date include species of labrid (wrasses), mullid (goatfishes), and siganid (rabbitfishes or spinefoots). Due to the extreme morphological similarity that exists among species of Phthinomita, an effect most likely due to their site of infection, this group is best described as a complex of cryptic species. As such, genetic data are required to enhance traditional methods of species characterisation (i.e. microscopic and morphological examination, host and geographic distribution) and the delineation of species is only possible though this integrated approach (see [14]). Here, we report Phthinomita heinigerae n. sp. from the ventricle of the orangelined cardinalfish, Taeniamia fucata (Cantor) (Perciformes: Apogonidae), collected during the CReefs project from 2009 to 2012 (http://www.aims.gov.au/creefs/field-program.html), from off Heron Island on the southern GBR.

Section snippets

Sample collection

Between 2009 and 2012, 22 species of apogonid from nine genera (Table 1) were collected from five sites off Heron Island on the southern GBR (23.4420° S, 151.9140° E), eight sites off Lizard Island on the northern GBR (14.6680° S, 145.4617° E), and from seven sites on Ningaloo Reef, off Western Australia (22.5625, 113.810278). Apogonid fishes were stored in an 80 l container before being euthanised by an overdose of clove oil, in strict accordance with the Queensland Museum's Animal Ethics

Aporocotylid prevalence and specificity

The hearts of 19 of the 724 apogonid specimens examined (2.6%) were infected with thread-like aporocotylids (see Table 1). All 19 infected individuals were identified as the orangelined cardinalfish, T. fucata, which were all collected from a single site in the Heron Island lagoon (19/20; 95% prevalence); none of the 27 T. fucata specimens collected from two sites off Lizard Island (Casuarina beach and Turtle beach) were infected.

Morphology

Class Trematoda Rudolphi, 1808

Subclass Digenea Carus, 1863

Order

Taxonomy

Phthinomita heinigerae n. sp. can be differentiated from all current species of Phthinomita by the combined possession of a body 2977–3539 long and 16.5–22.4 times longer than wide, an anterior testis that is 6.2–8.2 times longer than wide and 8.3–13.0 times longer than the posterior testis, a posterior testis whose width is 35–56% of the body width, and having the ovary positioned 11–13% of the body length from the posterior end (see Table 2). In addition, P. heinigerae n. sp. differs further

Conflict of interest

The authors declare they have no competing interests.

Acknowledgements

This study was funded by, and is a contribution from, the Australian node of the CReefs global research initiative (grant number: 209/29), a project generously sponsored by BHP Billiton in partnership with The Great Barrier Reef Foundation, the Australian Institute of Marine Science, the Australian Biological Resources Study, and the Alfred P. Sloan Foundation. CReefs is a field program of the Census of Marine Life. We gratefully thank the staff of the Heron and Lizard Island Research Stations

References (49)

  • G. Alama-Bermejo et al.

    Skoulekia meningialis n. gen., n. sp. (Digenea: Aporocotylidae Odhner, 1912) a parasite surrounding the brain of the Mediterranean common two-banded seabream Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) (Teleostei: Sparidae): description, molecular phylogeny, habitat and pathology

    Parasitol. Int.

    (2011)
  • R. Orelis-Ribeiro et al.

    Blood flukes (Digenea: Aporocotylidae) infecting body cavity of south American catfishes (Siluriformes: Pimelodidae): two new species from rivers in Bolivia, Guyana and Peru with a re-assessment of Plehniella Szidat, 1951

    Folia Parasitol. (Praha)

    (2015)
  • K. Ogawa et al.

    Paradeontacylix buri n. sp. (Trematoda: Aporocotylidae) from Seriola quinqueradiata cultured in Japan with a description of unidentified Paradeontacylix sp. from S. lalandi

    Fish Pathol.

    (2015)
  • R. Orelis-Ribeiro et al.

    Two new genera of fish blood flukes (Digenea: Aporocotylidae) from catfishes in the Peruvian Amazon

    J. Parasitol.

    (2016)
  • M.J. Nolan et al.

    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

    (2006)
  • M.J. Nolan et al.

    Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes

    Zootaxa

    (2006)
  • R.Q.-Y. Yong et al.

    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

    (2013)
  • R.M. Overstreet et al.

    Pearsonellum corventum, gen. et sp. nov. (Digenea: Sanguinicolidae), in serranid fishes from the Capricornia section of the Great Barrier Reef

    Aust. J. Zool.

    (1989)
  • T.H. Cribb et al.

    Trematodes of fishes: a test case for predictions of parasite diversity on the Great Barrier Reef

  • R.Q.-Y. Yong et al.

    Rhaphidotrema kiatkiongi, a new genus and species of blood fluke (Digenea: Aporocotylidae) from Arothron hispidus (Osteichthyes: Tetraodontidae) from the Great Barrier Reef, Australia

    Folia Parasitol.

    (2011)
  • I. Blasco-Costa et al.

    Molecular approaches to trematode systematics: ‘best practice’ and implications for future study

    Syst. Parasitol.

    (2016)
  • S.C. Cutmore et al.

    Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.)

    Parasitol. Res.

    (2013)
  • R.C. Edgar

    MUSCLE: multiple sequence alignment with high accuracy and high throughput

    Nucleic Acids Res.

    (2004)
  • R.C. Edgar

    MUSCLE: a multiple sequence alignment method with reduced time and space complexity

    BMC Bioinform.

    (2004)
  • Cited by (0)

    View full text