Cardicola beveridgei n. sp. (Digenea: Aporocotylidae) from the mangrove jack, Lutjanus argentimaculatus (Perciformes: Lutjanidae), and C. bullardi n. sp. from the Australian spotted mackerel, Scomberomorus munroi (Perciformes: Scombridae), from the northern Great Barrier Reef

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Highlights

  • Two species of Cardicola are described from lutjanid and scombrid fishes.

  • The species are distinguished by morphological and molecular differences.

  • Cardicola beveridgei forms a clade with a species from a lutjanid and from a chaetodontid.

  • Cardicola bullardi, from a scombrid, does not form a clade with other scombrid species.

Abstract

Cardicola Short, 1953 is a genus of the Aporocotylidae Odhner, 1912 (Digenea), with 25 currently recognised species described from 32 species of Perciformes and Mugiliformes fishes around the world, including eight species from the Great Barrier Reef. Here, we describe two new species from this region, namely Cardicola beveridgei n. sp. from the ventricle and atrium of the mangrove jack, Lutjanus argentimaculatus (Forsskål) (Perciformes: Lutjanidae), and Cardicola bullardi n. sp. from the ventricle of the Australian spotted mackerel, Scomberomorus munroi Collette & Russo (Perciformes: Scombridae), from off Lizard Island, Queensland, Australia. These two new species are most easily distinguished from the 25 current members of Cardicola in having the combination of i) a spinous oral sucker, ii) an anteriorly intercaecal ovary, iii) a uterus that extends anteriorly from the oötype, iv) the number of spines per ventrolateral transverse row, and in v) body size and the length/width ratio, vi) the oesophagus and caecal length(s) relative to body total length, vii) the length of the posterior caeca relative to the anterior pair, viii) the testis length/width ratio and its total size relative to that of the body, ix) the postovarian field as a percentage of body length, and x) egg size. In addition, C. beveridgei n. sp. is further differentiated by possessing a female genital pore that opens anterodextral to the male pore while C. bullardi n. sp. differs further in possessing a testis that is almost entirely intercaecal and does not extend anteriorly to the level of the intestinal bifurcation. Employing genetic analysis of ITS2 rDNA sequence data, representing these species and a further 13 recognised and three putative species of Cardicola, we were able to unequivocally confirm these specimens as distinct (9–22% different over 420 nucleotide positions). Distance analysis of ITS2 showed that i) species of Cardicola from the Siganidae formed a monophyletic clade, to the exclusion of other Cardicola species reported from the Scombridae, Sparidae, Lutjanidae and Chaetodontidae, ii) a general phylogenetic isolation exists between the species of Cardicola reported from scombrid fishes, and iii) C. beveridgei n. sp. and Cardicola milleri Nolan & Cribb, 2006 from lutjanids and Cardicola chaetodontis Yamaguti, 1970 from chaetodontids are phylogenetically close, despite the evolutionary remoteness between the host groups and their highly disparate biology. Given the likelihood of many additional species being attributed to Cardicola, we predict that continued molecular analyses will indicate that this genus will prove to incorporate a series of radiations in association with particular fish taxa as well as evidence of host-switching. (Nucleotide sequences reported in this paper are available in the GenBank database under accession no. KF752497).

Introduction

The parasite fauna of teleost fishes of the Great Barrier Reef (GBR) and throughout the Indo-West Pacific Region (IWP) remains incompletely known, both at genus and species levels [1]. Within the Digenea (Platyhelminthes), the family Aporocotylidae Odhner, 1912 (syn. Sanguinicolidae von Graff, 1907; the blood flukes of fishes) is as poorly known as any group of trematodes [2] and the taxonomic confusion within the family is not exceeded in any other [3]. This is perhaps because these parasitic flatworms are especially cryptic; not only are they hidden within the circulatory system of teleosts, elasmobranchs and holocephalans, they are also not limited to the heart or gills, which are relatively obvious and easily examined (e.g., Skoulekia meningialis Alama-Bermejo, Montero, Raga & Holzer, 2011 is found in the vessels surrounding the optic lobes of the brain; see [4]). In addition, many aporocotylid species are characterised by low prevalence and/or intensities of infection (e.g. [5], [6]), which represent a major obstacle to current efforts aimed at clarifying taxonomic and systematic aspects of this family.

Cardicola Short, 1953 currently has the greatest number of marine species of any genus in the Aporocotylidae (although future taxonomic revision may alter this; see [7]). In 2006, eight species of Cardicola were reported from six species of the Siganidae (rabbitfishes) and one species of the Lutjanidae (snappers) from Australia from the southern and northern GBR, Ningaloo Reef and Moreton Bay [5]. Due to difficulties in obtaining sufficient study material during that investigation four further putative species were reported, but not described, from either a single morphological specimen or a single sequence from the second internal transcribed spacer (ITS2) of ribosomal DNA (rDNA). Here, as part of an ongoing survey of the Aporocotylidae of fishes of the waters surrounding Lizard Island, we are now able to describe two of these as new. Employing a combined morphological and molecular-based approach, we here describe Cardicola beveridgei n. sp. from the mangrove jack, Lutjanus argentimaculatus (Forsskål) (Lutjanidae), and C. bullardi n. sp. from the Australian spotted mackerel, Scomberomorus munroi Collette & Russo (Scombridae).

Section snippets

Sample collection

Fishes were collected from off Lizard Island (14°40′S 145°27′E), on the northern GBR, by spear and line fishing, and were euthanised via neural pithing. Immediately upon death the heart, gills and viscera were excised and examined separately in 0.85% saline solution, utilising a stereomicroscope. The three chambers of the heart were dissected along their lengths using micro-scissors and gently teased apart with fine forceps before being flushed with saline solution. Each branchial arch was

Comparative DNA analysis

We conducted sequence analysis of the amplicons (n = 2) representing both species described here. These sequences had mean nucleotide frequencies of 21.3 (A), 16.7 (C), 26.3 (G) and 35.7 (T) (sequence represented by GenBank accession no. DQ059632; [5]) and 20.2 (A), 16.9 (C), 26.7 (G) and 36.2 (T) (KF752497), and were 60 bases different from each other (14% over 420 nucleotide positions in the aligned dataset). Comparison of the present data with information currently available in GenBank

Taxonomy

According to Bullard [17] there are currently 25 valid species of Cardicola. This figure excludes Cardicola congruenta Lebedev & Mamaev, 1968, Cardicola grandis Lebedev & Mamaev, 1968 (see [18]), Cardicola ahi Yamaguti, 1970, and Cardicola kurochkini (Parukhin, 1976) Bullard & Overstreet, 2006 (see [7]), which are currently considered incertae sedis. C. beveridgei n. sp. may be differentiated from all current species, except C. milleri Nolan & Cribb, 2006 and C. aurata, by the combined

Conflict of interest

The authors have no conflict of interest.

Acknowledgements

This study was partly funded by the Australian Research Council and the Australian Biological Resources Study grants awarded to THC. TLM is supported by a Queensland Smart Futures Fund Fellowship. CC is supported by an NHMRC Peter Doherty Early Career Fellowship. We gratefully thank the staff of the Lizard Island Research Station for their support and hospitality during our stays.

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