Proposal of Troglocephalinae n. subfam. (Monogenea: Monocotylidae) to accommodate existing and two new monocotylids from the gills of rhinopristiform shovelnose rays

Syst Parasitol (2024) 101:51 https://doi.org/10.1007/s11230-024-10174-z Proposal of Troglocephalinae n. subfam. (Monogenea: Monocotylidae) to accommodate existing and two new monocotylids from the gills of rhinopristiform shovelnose rays David B. Vaughan · Haakon Hansen Leslie A. Chisholm · Received: 22 May 2024 / Accepted: 26 June 2024 © The Author(s) 2024 Abstract Troglocephalinae n. subfam. is proposed for Spinuris Doran, 1953, Neoheterocotyle Hargis, 1955, Anoplocotyloides Young, 1967, Troglocephalus rhinobatidis Young, 1967 (previously incertae sedis), Nonacotyle pristis Ogawa, 1991, Mehracotyle insolita Neifar, Euzet & Ben Hassine, 2002, Scuticotyle cairae n. gen. et sp., and Brancheocotyle imbricata n. gen. et sp. All members of the proposed new subfamily are gill parasites of shovelnose rays of the order Rhinopristiformes. The subfamilies Heterocotylinae Chisholm, Wheeler & Beverley-Burton, 1995, and Dasybatotreminae Bychowsky, 1957, are amended to exclude Spinuris, Nonacotyle, Neoheterocotyle, and Anoplocotyloides and Mehracotyle, respectively. Heterocotylinae includes gill parasites of members of the orders Myliobatiformes and Torpediniformes. Dasybatotreminae includes parasites of the gills and pharyngeal cavity of members of the orders Myliobatiformes and Rajiformes. A revised phylogeny of the Monocotylidae Taschenberg, 1879 is presented and discussed, based on 28S rDNA sequences, including new sequences for Myliocotyle pteromylaei Neifer, Euzet & Ben Hassine, 1999, Heterocotyle tokoloshei Vaughan & Chisholm, 2010, Neoheterocotyle robii Vaughan & Chisholm, 2010, and the two newly proposed species and genera. Additional locality records are also provided for Monocotylidae from off South Africa. Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s11230-024-10174-z. D. B. Vaughan (*) Aquatic Animal Health Research, Two Oceans Aquarium, Cape Town, South Africa e-mail: Present Address: D. B. Vaughan School of Access Education, Tertiary Education Division, Central Queensland University, Rockhampton, QLD, Australia Present Address: D. B. Vaughan Coastal Marine Ecosystems Research Centre, Central Queensland University, Rockhampton, QLD, Australia H. Hansen Norwegian Veterinary Institute, P. O. Box 64, 1433 Ås, Norway L. A. Chisholm Parasitology Section, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia L. A. Chisholm Faculty of Sciences, Engineering and Technology, School of Biological Sciences, University of Adelaide, North Terrace, Adelaide, SA 5005, Australia Vol.: (0123456789) 51 Page 2 of 32 Introduction Monocotylids (Monogenea: Monocotylidae Taschenberg, 1879) are parasites of chondrichthyans of marine, brackish and fresh waters. Their host microhabitats are diverse, including the gill lamellae, pharyngeal cavity, skin surface, nasal tissue, urogenital system, and inner wall of the body cavity (Chisholm and Whittington 1998a; Derouiche et al. 2019, Bullard et al. 2021; Ruiz-Escobar et al. 2022). Traditionally, the morphology of the haptor, including the number of loculi (or a 3-part attachment organ; Bullard et al. 2021), and the presence of a variety of ventral and dorsal haptoral structures, presumably to facilitate attachment to the variety of host microhabitats, has been of primary importance in discriminating higher-level monocotylid taxa (Chisholm and Whittington 1998a; Bullard et al. 2021). The morphology of the male copulatory organ and vagina is useful for discriminating between species. Comparatively little attention has been afforded to the importance of the anterior head region, and its structures that might demonstrate relatedness between taxa. An inconsistent approach exists for including details of the head glands of the anterior head region historically. Some additional details, such as the presence of ventral pits in the anterior head region (e.g., Hargis 1955; Young 1967, for Neoheterocotyle Hargis, 1955 species) or differences in the nature of the gland-duct openings, have largely been ignored. Notably, Young (1967) described both Neoheterocotyle rhinobatidis (Young, 1967) Chisholm, 1994 and Troglocephalus rhinobatidis Young, 1967 in the same work, yet only described ventral pits for the latter. This feature is confirmed in all Neoheterocotyle species (Chisholm and Whittington 1997). Young (1967) also referred to the ventral pits as “clear markings of unknown nature” for Anoplocotyloides papillatus (Doran, 1953), Young, 1967, perhaps because the function of these ventral pits has never adequately been experimentally demonstrated. Some of these subtle characters are undoubtedly difficult to observe, but with current, modern technology, a renewed focus on this region in monocotylids is warranted. Recently, workers have begun to include the relative importance of these subtle characters in phylogenetic analyses of the family (e.g., Boeger et al. 2014; Bullard et al. 2021). Monocotylidae currently contains nine subfamilies: Calicotylinae Monticelli, 1903, Cathariotrematinae Vol:. (1234567890) Syst Parasitol (2024) 101:51 Bullard in Bullard, Warren & Dutton, 2021, Dasybatotreminae Bychowsky, 1957, Decacotylinae Chisholm, Wheeler & Beverley-Burton, 1995, Euzetiinae Chisholm & Whittington, 2001, Heterocotylinae Chisholm, Wheeler & Beverley-Burton, 1995, Loimoinae Price, 1936, Merizocotylinae Johnston & Tiegs, 1922 and Monocotylinae Taschenberg, 1879. Heterocotylinae was proposed in the morphological revision of the family of Chisholm et al. (1995) and was considered monophyletic based on two purported apomorphies: four dorsal haptoral accessory structures, and their rounded shape. In addition to Heterocotyle Scott, 1904 and Potamotrygonocotyle Mayes, Brooks & Thorson, 1981, these authors included Neoheterocotyle, Nonacotyle Ogawa, 1991 and Spinuris Doran, 1953 in the subfamily, which have four, six or 14 projecting, mostly spiculate dorsal haptoral sclerites. This variation was considered a modification of the character states within the subfamily (Chisholm et al. 1995). At that time, Heterocotylinae was considered the only subfamily to include representatives with dorsal haptoral accessory structures; however, Decacotylinae, which was also proposed in the same publication, was later revised to include dorsal haptoral accessory structures (Chisholm and Whittington 1998b). Subsequently, Heliocotyle Neifar, Euzet & Ben Hassine, 1999, and Malalophus Chisholm & Whittington, 2009 were proposed as representatives of Heterocotylinae with only a single dorsal haptoral accessory structure. Euzetiinae includes two genera, Euzetia Chisholm & Whittington, 2001, without these structures, and Denarycotyle Pulido-Flores, Monks & Violante-González, 2015 with them present, indicating that the presence of dorsal haptoral accessory structures is not restricted to Heterocotylinae, and that their presence or absence is also characteristic within Euzetiinae. Dasybatotrem (...truncated)