Patterns of specificity and diversity in species of Paraorygmatobothrium Ruhnke, 1994 (Cestoda: Phyllobothriidae) in Moreton Bay, Queensland, Australia, with the description of four new species

Abstract

A survey of tapeworms of galeomorph sharks from Moreton Bay (Queensland, Australia) identified a complex of species of Paraorygmatobothrium Ruhnke, 1994 infecting 11 carcharhiniform and two orectolobiform species. Combined morphological and multi-locus molecular analyses (based on the 28S nuclear ribosomal RNA and partial mitochondrial NADH dehydrogenase subunit 1 genes) revealed the presence of 12 species of Paraorygmatobothrium; four species (Paraorygmatobothrium christopheri n. sp., P. harti n. sp., P. sinclairtaylori n. sp. and P. ullmanni n. sp.) are considered to be new to science and are formally described, four represent known species, and four lack sufficient morphological data to allow definitive identification. In contrast to previous records for the genus, four of the species found in this study exhibited low host specificity [P. orectolobi (Butler, 1987) Ruhnke, 2011, P. sinclairtaylori, P. ullmanni and Paraorygmatobothrium sp. 3], three stenoxenic species were each found in two closely-related sharks (P. orectolobi, P. ullmanni and Paraorygmatobothrium sp. 3) and one euryxenic species was found in five species from two shark families (P. sinclairtaylori). One species was found to exhibit mild morphologically plasticity (P. orectolobi), with size range being associated with different shark species. Conversely, collections of almost morphologically indistinguishable specimens from single shark species were found to represent multiple species of Paraorygmatobothrium. The findings of this study indicate that the description of species of this genus on the basis of morphological data alone is problematic and that the inclusion of multi-locus molecular data is essential for future work on Paraorygmatobothrium. Host specificity, morphology and phylogenetic relatedness of species of Paraorygmatobothrium are explored.

Insights from new cestodes of the crocodile shark,Pseudocarcharias kamoharai(Lamniformes: Pseudocarchariidae), prompt expansion ofScyphyophyllidumand formal synonymization of seven phyllobothriidean genera – at last!

“…Category 2: species with bothridia bearing marginal loculi; species given this category designation are the six formerly assigned to Orectolobicestus (now S. chiloscyllii , S. kelleyae , S. lorettae , S. mukahensis , S. randyi and S. tyleri ), the single species formerly assigned to Nandocestus (i.e. S. guariticus ) and, based on re-interpretation of SEMs, also S. orectolobi (of Cutmore et al ., 2017) and S. janineae (of Ruhnke et al ., 2006b). Category 3: species with facial loculi or facial semi-circular muscle bands; taxa given this category designation are the two species with facial semi-circular muscle bands formerly assigned to Paraorygmatobothrium (now S. barberi and S. taylori ) as well as the single species with facial loculi formally assigned to Ruhnkecestus (now S. latipi ).…”

“…1 through 4 of Cutmore et al . (2017) are assigned the designations Scyphophyllidium sp. 1 through 4, respectively.…”

“…Beyond sharing subsets of the above unique ultrastructural features with Scyphophyllidium , Cutmore et al . (2017) found the monotypic Hemipristicola to nest deeply among species now assigned to Scyphyophyllidium in the trees resulting from both their Bayesian and ML phylogenetic analyses of NADH1 amino acid data. Morphologically, H. gunterae differs from species of Scyphophyllidium in its possession of a deep central cavity in each of its bothridia.…”

“…The past decade or so has seen the erection of a series of seven novel genera found parasitizing the spiral intestines of members of three orders of sharks as well as one species of stingray (Caira & Durkin, 2006; Ruhnke et al ., 2006a; Reyda, 2008; Caira et al ., 2011; Cutmore et al ., 2011; Ruhnke & Workman, 2013), and one species of skate (Ivanov, 2006), which, despite sharing a series of unique ultrastructual features and similarities in overall proglottid anatomy (see Ruhnke, 2011; Cutmore et al ., 2017), differ considerably in bothridial morphology. For example, the bothridia of Doliobothrium Caira, Malek & Ruhnke, 2011 each lack an apical sucker and possess a proximal aperture; those of Orectolobicestus Ruhnke, Caira & Carpenter, 2006 each possess an apical sucker and marginal loculi; those of Ruhnkecestus Caira & Durkin, 2006 lack an apical sucker but bear facial loculi; those of Hemipristicola Cutmore, Theiss, Bennett & Cribb, 2011 bear an apical sucker and a deep central cavity; and those of Alexandercestus Ruhnke & Workman, 2013 bear an apical sucker and are highly foliose.…”

“…As molecular phylogenetic analyses have expanded to include greater representation of these genera, the close affinities among these genera have been confirmed. However, these works have also served to call the monophyly of the speciose, yet morphologically uniform, Paraorygmatobothrium into question relative to at least a subset of the above genera (Cutmore et al , 2011, 2017; Caira et al ., 2014a; Ruhnke et al ., 2020). This suggests that a critical re-evaluation of these genera is in order.…”