First morphological and molecular characterization of cystacanths of Corynosoma evae Zdzitowiecki, 1984 (Acanthocephala: Polymorphidae) from Antarctic teleost fishes

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Highlights

  • Cystacanths of Corynosoma evae Zdzitowiecki, 1984 were examined and redescribed.

  • Morphological and morphometrical analyses confirmed the validity of C. evae.

  • Sequences of the SSU, LSU and cox1 for C. evae were generated.

  • C. evae is placed as a sister linage to a clade formed by C. validum + C. villosum.

  • Corynosoma arctocephali Zdzitowiecki, 1984 is considered a valid species.

Abstract

Cystacanths of the polymorphid acanthocephalan Corynosoma evae Zdzitowiecki, 1984 were examined and redescribed based on newly collected material from teleost fishes from coastal waters of the Galindez Island (Argentine Islands, West Antarctica). Detailed morphological data, measurements and photomicrographs, including scanning electron microscopy images, are presented. Our morphological and morphometrical analyses confirmed the validity of C. evae; however, three key characteristics of taxonomic importance (i.e., the number of rows of hooks on the proboscis, and the number and arrangement of genital spines in males) showed significant morphological variability. In addition, a genital spine in the posterior body end of a female is reported for the first time. This study provides the first sequences of the small and large subunits nuclear ribosomal RNA genes (SSU and LSU) and the mitochondrial cytochrome c oxidase subunit 1 (cox1) for C. evae. Maximum likelihood and Bayesian inference analyses of the SSU + LSU + cox1 and the cox1 datasets placed C. evae as a sister lineage to a clade formed by C. validum Van Cleave, 1953 and C. villosum Van Cleave, 1953, although with low support. In contrast, the position of C. evae in the phylogenetic analysis of the SSU + LSU dataset remained unresolved. Finally, C. arctocephali Zdzitowiecki, 1984 from pinnipeds from the subantarctic and Antarctic regions is considered as a valid species.

Introduction

Polymorphid acanthocephalans of the genus Corynosoma Lühe, 1904, which comprises ca. 29 species, are mainly intestinal parasites of pinnipeds [1]. Information on the life cycle of most species of Corynosoma is scat, but it is thought to involve amphipods as intermediate hosts [[2], [3], [4]], marine fish as paratenic (transport) hosts [5,6], and typically pinnipeds as definitive hosts [1].

Corynosoma evae Zdzitowiecki, 1984 was described by Zdzitowiecki [7] based on material collected from the ileum of the leopard seal Hydrurga leptonyx (Blainville) (Phocidae) off King George Island, South Shetlands, Antarctica. Adults of this acanthocephalan were later reported from the South American sea lion Otaria flavescens (Shaw) (Otariidae) off Falkland Island (Islas Malvinas), and the South American fur seal Arctocephalus australis (Zimmermann) (Otariidae) off Uruguay [1,8]. The validity of C. evae was questioned by Stryukov [9], who considered this species as a synonym of Corynosoma arctocephali Zdzitowiecki, 1984 based on similar morphological characters, similar definitive host range, and geographical distribution. Later, Aznar [1] and Amin [10] retained C. evae as a valid species. However, these authors did not provide morphological or molecular data to support the taxonomic status of this acanthocephalan.

A single cystacanth female of C. evae was reported from an Antarctic dragonfish Parachaenichthys georgianus (Fischer) (Bathydraconidae) off South Georgia by Zdzitowiecki [7]. Later, Reimer [11] provided a very brief and incomplete description of cystacanths of C. evae from the South Georgia icefish Pseudochaenichthys georgianus Norman (Channichthyidae) and the blackfin icefish Chaenocephalus aceratus (Lönnberg) (Channichthyidae) off the South Shetland and South Georgia Islands. The specific identification of these cystacanths by Zdzitowiecki [7] and Reimer [11] was later questioned by Zdzitowiecki [12] and Zdzitowiecki and White [13], who considered that these materials may belong to cystacanths of C. arctocephali. Laskowski et al. [14] described cystacanths of C. evae from the nototheniid fish Patagonotothen longipes (Steindachner) (Nototheniidae) and the pike icefish Champsocephalus esox (Günther) (Channichthyidae) off Tierra del Fuego, Argentina. Finally, Laskowski and Zdzitowiecki [15] reported cystacanths of C. evae in fishes from off South Georgia and the Beagle Channel.

Kuzmina et al. [[15], [16], [17], [18], [19]] found cystacanths of C. evae in C. aceratus, the Antarctic spiny plunderfish Harpagifer antarcticus Nybelin (Harpagiferidae), the Antarctic dragonfish Parachaenichthys charcoti (Vaillant) (Bathydraconidae), the black rockcod Notothenia coriiceps Richardson (Nototheniidae), the marbled rockcod Notothenia rossii Richardson (Nototheniidae), and the emerald rockcod Trematomus bernacchii Boulenger (Nototheniidae) off the Argentine Islands, Antarctica. Recently, Kuzmina et al. [19] reported cystacanths of C. evae in C. aceratus, the humped rockcod Gobionotothen gibberifrons (Lönnberg) (Nototheniidae), N. coriiceps, the painted notie Nototheniops larseni (Lönnberg) (Nototheniidae), N. rossii, Ps. georgianus and Pa. charcoti off the South Orkney Islands area, West Antarctica.

As part of extensive parasitological studies on teleost fish helminths from the Argentine Islands, West Antarctica (e.g., [17,19]), numerous cystacanths of C. evae were collected and examined. This study presents detailed morphometrical data and scanning electron microscopical (SEM) micrographs of these cystacanths to facilitate their identification and differentiation from the closely related species of Corynosoma. In addition, we used near-complete sequences of the small and large subunits nuclear ribosomal RNA genes (SSU and LSU, respectively) and partial sequences of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene to explore the phylogenetic relationships of C. evae and other members of the genera Andracantha Schmidt, 1975, Corynosoma Lühe, 1904 and Bolbosoma Porta, 1908 with publicly available sequences.

Section snippets

Sample collection

Encapsulated cystacanths of C. evae were collected from the mesenteries of two species of teleost fishes, the black rockcod N. coriiceps and the blackfin icefish C. aceratus off the Galindez Island (Argentine Islands, West Antarctica; 65°15′S, 64°16′W). Fishes were captured by angling (depth 10–30 m) between 2014 and 2020 (see [17] for details) and dissected following standard parasitological procedures. Internal organs were removed, placed in Petri dishes with saline, and examined under a

General

Polymorphidae, with characters of Corynosoma. Living specimens white. Females slightly larger than males. Proboscis subcylindrical, widens markedly at posterior third (Figs. 1B, 2B, 3B), armed with 18–22 longitudinal rows (Fig. 3C), with 11–13 hooks (Figs. 1B, 2B); each row with 7–9 anterior rooted hooks, and 3–5 small basal spiniform hooks (Figs. 1B, 2B, 3B) without basal discs. Hook combinations (anterior/basal) of 7/4 (n = 2), 7–8/4 (n = 1), 8/3–4 (n = 3), 8/4 (n = 3), 8/4–5 (n = 1), 9–9/3–4

Discussion

Corynosoma evae has been reported parasitizing phocids and otariids of the West Antarctic region (South Shetland Islands) and the South-West Atlantic (Falkland Island and Uruguay) [1,7,8]. Laskowski and Zdzitowiecki [15] suggested that C. evae may probably represent a subantarctic rather than an Antarctic acanthocephalan because cystacanths of this species were only collected in fishes from South Georgia and the Beagle Channel by them. The present study provided evidence of the occurrence of

Data availability

Voucher material is deposited in the Parasitological collection of the Department of Parasitology I. I. Schmalhausen Institute of Zoology NAS of Ukraine, Kyiv, Ukraine. DNA sequences generated in this study were deposited in the GenBank database (see Table 1 for details).

Declaration of Competing Interest

The authors declare that there are no conflicts of interest associated with this publication.

Acknowledgements

The authors are indebted to Jan Brabec (Institute of Parasitology, Czech Republic) for his review, comments and suggestions to improve our molecular analyses and Yuriy Kuzmin (Institute of Zoology NAS of Ukraine) for his help in preparation of microphotographs of cystacanths. The authors are grateful to Oleksandr Salganskiy for collecting acanthocephalans in teleost fishes during the fieldwork on the Galindez Island, Antarctica. This study was partially supported by the National Research

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