Description and molecular data of a new cestode parasite, Cladotaenia anomala n. sp. (Paruterinidae) from the Australasian harrier (Circus approximans Peale) in New Zealand

Syst Parasitol (2024) 101:25 https://doi.org/10.1007/s11230-024-10147-2 Description and molecular data of a new cestode parasite, Cladotaenia anomala n. sp. (Paruterinidae) from the Australasian harrier (Circus approximans Peale) in New Zealand Bronwen Presswell · Jerusha Bennett Received: 31 August 2023 / Accepted: 2 January 2024 / Published online: 6 March 2024 © The Author(s) 2024 Abstract Currently comprising 12 species infecting the gastrointestinal tracts of diurnal raptors (Falconiformes, Accipitriformes), species of Cladotaenia are diagnosed by their branching uterus, testes in two fields reaching the same level anteriorly, and small rostellum armed with taenioid hooks arranged in two rows. In this study we describe a new species of Cladotaenia recovered from a number of Australasian harriers Circus approximans, from the southern half of South Island, New Zealand. The new species is distinguished from other species by its single circle of hooks. It is closest, morphologically, to C. circi, but differs in the shape of the terminal proglottids and the number of uterine branches. Sequences of 28S and cox1 gene are presented. Genetically, Cladotaenia anomala n. sp. is closest to Cladotaenia globifera but differs morphologically in the size of the suckers, testes and eggs. This description constitutes the first record of a Cladotaenia species in New Zealand. We discuss some potential routes this parasite may have taken to arrive in New Zealand. B. Presswell (*) · J. Bennett Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand e-mail: Introduction The genus Cladotaenia Cohn, 1901 (Cyclophyllidea: Paruterinidae) was erected for Taenia globifera Batsch, 1786 which was described from hawks (Aves: Accipitridae). The genus was originally included in the family Taeniidae Ludwig, 1886 (Joyeux & Baer 1961; Abuladze 1958; Yamaguti 1959), but was believed to belong to Dilepididae Fuhrmann, 1907 by Fuhrmann & Baer (1943) a placement followed by both Freeman (1959) and Schmidt (1986). Subsequently, Cladotaenia was excluded from the Taeniidae on zoogeographical, morphological and ontogenetic grounds by Rausch (1985) a decision recently supported by genetic data (Guo et al. 2019). The genus is now considered a member of the family Paruterinidae (Georgiev and Kornyushin 1994, Mariaux et al. 2017), and it is a close sister taxon to Paruterina, the type genus of the family. In addition, the mitochondrial gene order is the same as Paruterina but different from members of Taeniidae (Guo et al. 2019). Genus Paracladotaenia Yamaguti, 1935 was also established for a cestode from a hawk, and was distinguished from Cladotaenia mainly by the absence of rostellar hooks. However, Cladotaenia spp. characteristically lose their hooks if specimens are not fixed immediately after the death of their host; consequently, Schmelz (1941) placed Paracladotaenia in synonymy with Cladotaenia, a position now widely accepted (Yamaguti 1959; Georgiev & Kornyushin 1994). Freeman (1959) Vol.: (0123456789) 13 25 Page 2 of 12 reviewed in detail the complex history of the species of this genus, as well as elucidating the life cycle and providing a character for differentiating between Cladotaenia and Paruterina plerocercoids in the liver and mesenteries of small mammals. Cladotaenia currently contains 12 nominal species, all of which infect the gastrointestinal tract of diurnal raptors (Accipitriformes and Falconiformes), with rodents and insectivores as intermediate hosts (Georgiev & Kornyushin 1994). Species of Cladotaenia have been reported from Europe, Africa, East Asia, India and North America (Freeman 1959; Georgiev & Kornyushin 1994). There are specimens of Cladotaenia sp. from Australia in the South Australia Museum, and C. circi from Vanuatu in Australian and British collections. However, there are no previous records of any species of Cladotaenia from New Zealand. The Australasian harrier Circus approximans Peale (Accipitriformes: Accipitridae), also known as swamp harrier, harrier hawk or kāhu, is native to Australia, New Zealand and some islands in the South Pacific (Debus & Kirwan 2020). The Australasian harrier, and the rare New Zealand falcon Falco novaeseelandiae Gmelin (Falconiformes: Falconidae), are the only two diurnal raptors extant in New Zealand. An opportunistic hunter of live prey such as small birds, mammals and invertebrates, the Australasian harrier is also a scavenger, with carrion making up a major part of the diet (BakerGabb 1981). In New Zealand a constant supply of road-kill carcasses has enabled the harrier to rise to very healthy population numbers (Eakle 2008). Its conservation status is Non-Threatened (Robertson et al. 2021), but the bird is considered a “taonga” (treasured) species by Māori and is partially protected by law (Wildlife (Australasian Harrier) Notice 2012). Harriers are seen frequently throughout New Zealand and are instantly recognisable. Many are themselves victims of roadkill or injury (Sadleir & Linklater 2016), and there are large numbers of deceased birds available, so it is testament to the lack of study on New Zealand wildlife parasites that not a single cestode has ever been reported for the harrier in New Zealand. Access to a number of harrier carcasses from the southern half of South Island since 2017 has allowed the authors to conduct a survey of all helminth parasites found, and what follows is a description of the paruterinid cestode Cladotaenia Vol:. (1234567890) 13 Syst Parasitol (2024) 101:25 found in some of these host birds, which was found to be new to science. We provide DNA sequences of the cox1 and 28S gene which confirm placement within Paruterinidae, and show that the new species is closest to C. globifera of those sequences available. A description of a new species of polymorphid acanthocephalan and a report on other helminths recovered from the New Zealand harriers, including a new species of nematode, have been published elsewhere (Presswell & Bennett 2023, 2024). Materials and methods Harrier collection and processing In total, 65 harriers were examined for parasitic helminths: 46 individuals from Otago were donated by the Dunedin Wildlife Hospital or collected as roadkill by the first author between 2017 and 2022, and 19 individuals from Canterbury were donated by the New Zealand Raptor Trust between 2022 and 2023. Birds were frozen upon collection and defrosted prior to dissection. Cestodes were collected and preserved in 70% ethanol for whole-mount, 96% ethanol for genetic analysis and 4% buffered formalin for SEM imaging. Morphological data Cestode specimens were stained using acetic iron carmine, dehydrated in an ethanol series, cleared in clove oil and mounted in Canada Balsam. Measurements were made using ImageJ software (Wayne Rasband, NIH, USA) from photographs taken on an Olympus BX51 compound microscope mounted with DP25 camera attachment (Olympus, Tokyo). All measurements are in micro (...truncated)