Novelty and phylogenetic affinities of a new family of tapeworms (Cestoda: Rhinebothriidea) from endangered sawfish and guitarfish

With their elongate rostrum equipped with multiple lateral tooth-like denticles, species of the genus Pristis Linck—or sawfish, as they are commonly known—represent one of the most iconic genera of batoids. Based on their global conservation status as determined by the International Union for Conservation of Nature (IUCN, Switzerland), they also represent one of the most threatened genera of elasmobranchs (Faria et al., 2013) with three of the four species recognized as valid by Last et al. (2016) categorized as Critically Endangered and the fourth as Endangered on the IUCN’s Red List (https://www.iucnredlist.org/; accessed 01 December 2022). All four species are also now protected under the Convention on International Trade in Endangered Species (CITES) (https://cites.org/eng; accessed 16 October 2022).

Yet, the cestode faunas of species in this genus remain poorly known. Collectively, they host a total of only seven described species. The trypanorhynch Pterobothrium australiense Campbell and Beveridge, 1996 was described from Pristis zijsron Bleeker by Campbell and Beveridge (1996), the trypanorhynch Pristiorhynchus palmi Schaeffner and Beveridge, 2013 was described from Anoxypristis cuspidata (Latham) and P. zijsron by Schaeffner and Beveridge (2013), the lecanicephalideans Floriparicapitus euzeti Cielocha, Jensen, and Caira, 2014 and Floriparicapitus juliani Cielocha, Jensen, and Caira, 2014 were described from Pristis pristis (Linnaeus) and Pristis clavata Garman, respectively, by Cielocha et al. (2014), the onchoproteocephalideans Matticestus anneae Caira, Fyler, and Jensen, 2018 and Matticestus kathleenae Caira, Fyler, and Jensen, 2018 were both described from P. clavata by Caira et al. (2018), and the rhinebothriidean Mixobothrium queenslandense Coleman, Beveridge, and Campbell, 2019 was described from P. zijsron by Coleman et al. (2019).

In addition—and of particular interest here—a substantial amount of intrigue exists surrounding a tiny undescribed species of rhinebothriidean from P. clavata that was included in the molecular phylogenetic work of Healy et al. (2009). Although not apparent at the time, the erection of the genus Mixobothrium Coleman, Beveridge, and Campbell, 2019 by Coleman et al. (2019) has since helped resolve the identity of this tiny cestode, which was provisionally referred to by Healy et al. (2009) as Rhinebothriinae n. sp. and which has subsequently been referred to as New genus 11 n. sp. 1 (e.g., Ruhnke et al., 2015, Ruhnke et al., 2017, Marques and Caira, 2016, Trevisan et al., 2017). Among the clues that contributed to our resolution of the identity of this taxon was the congeneric nature of the hosts of both species. Mixobothrium queenslandense was described from P. zijsron and the specimen of New genus 11 n. sp. 1 was collected from P. clavata. This led us to examine material that we have collected from rhinopristiform elasmobranchs over the last several decades for additional specimens of this cestode group. Those hosts yielded specimens of a morphologically similar species in P. pristis, additional material of the species sequenced by Healy et al. (2009) in P. clavata, and specimens of a second species parasitizing P. zijsron, all three from Australia. In addition, we found specimens of a fourth species in Glaucostegus obtusus (Müller and Henle) from India and were sent specimens of a fifth species from Pristis pectinata Latham from Florida (USA). Four of the five new species of Mixobothrium, including the taxon provisionally referred to previously as New genus 11 n. sp. 1, are described below.

Prior to this study, the phylogenetic affinities, and thus the familial placement, of these cestodes was also unclear. Healy et al. (2009) found the species from P. clavata to group either among the rhinebothriideans or as sister to all other members of the order, depending on the molecular markers and optimality criterion employed. In their establishment of a family-level classification for the Rhinebothriidea, Ruhnke et al. (2015) refrained from placing this species in a family because its position was unresolved in the tree resulting from their molecular phylogenetic analysis. In fact, Ruhnke et al. (2015) suggested this species may represent a distinct family-level taxon—an opinion also held by Ruhnke et al. (2017). However, Coleman et al. (2019) considered M. queenslandense to belong to the Rhinebothriidae Euzet, 1953. The availability of specimens of three additional species of Mixobothrium fixed in ethanol for molecular work allowed us to explore the phylogenetic affinities of this group more fully. The results of our maximum likelihood analysis support the recognition of species of Mixobothrium as members of an independent family within the Rhinebothriidea. Thus, a new family of rhinebothriideans is established here to house the genus.

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