Steringophorus merretti n. sp. (Digenea: Fellodistomidae) from the deep-sea fish Cataetyx laticeps Koefoed (Ophidiiformes: Bythitidae) from the Goban Spur, Northeastern Atlantic Ocean

A new species of deep-sea digenean, Steringophorus merretti n. sp., is described from the bythitid fish Cataetyx laticeps in deep waters of the Goban Spur, Northeastern Atlantic. It is distinguishable from other described members of the genus by its tiny eggs and large cirrus-sac. A phylogenetic tree, based on 28S rDNA sequences, indicates that this species is embedded within a clade of deep-sea species and is sister to the eurybathic species S. thulini Bray & Gibson, 1980. Steringotrema robertpoulini Pérez-Ponce de León, Anglade & Randhawa, 2018 falls within the Steringophorus Odhner, 1905 clade. In view of this the morphological and biological characteristics of species of Steringophorus and Steringotrema are discussed.


Introduction
In 1999, we (Bray et al., 1999) published a phylogenetic tree exploring the possible deep-sea radiation of a group of fellodistomid digenean genera, mostly members of Steringophorus Odhner, 1905. All but one species was named. This unnamed species is described here from specimens from the same source as that sequenced in 1999. Several authors have used the named species in subsequent explorations of the fellodistomid phylogeny (Sun et al., 2014;Antar & Gargouri, 2016;Wee et al., 2017a;Wee et al., 2017b;Cutmore et al., 2018;Pérez-Ponce de León et al., 2018), but only one  has included the unnamed species. In describing and naming this species, we hope that the sequences obtained from this rare and difficult to obtain deep-sea digenean will be used by all subsequent workers on fellodistomid phylogeny.

Materials and methods
The host specimens were caught aboard the RRS Challenger, Cruise 43/1994, at the Goban Spur. The Goban Spur is an area of relatively shallower water that forms the southern margin of the Porcupine Seabight, a deep-water oceanic basin located on the continental margin to the west of southern Ireland. The fish were caught using an OTSB (semi-balloon otter trawl) with a single warp and dissected as soon as possible after being brought aboard. The live digeneans were washed in saline and fixed in Berland's fluid for morphological study and 80% ethanol for molecular study. Whole-mounts were stained with Mayer's paracarmine, cleared in beechwood creosote and mounted in Canada balsam. Measurements were made through a drawing tube on an Olympus BH-2 microscope, using a Digicad Plus digitising tablet and Carl Zeiss KS100 software adapted by Imaging Associates, and are quoted in micrometres. The following abbreviation is used: NHMUK, Natural History Museum, London, UK. The discussion of the hosts and distribution of Steringophorus and Steringotrema spp. is based on a database developed by Dr Thomas Cribb, at the University of Queensland, and maintained to date by RAB.
Excretory pore terminal. Vesicle Y-shaped; branching point obscured by eggs; arms reach just prebifurcal.

Differential diagnosis
This is the only Steringophorus species reported from a bythitid and is notable for its tiny eggs, much smaller than reported for any other species of the genus. Steringophorus magnus Manter, 1934, with eggs 30-32 9 14-17 (Manter, 1934), and Steringophorus haedrichi Bray & Campbell, 1995, with eggs 32-41 9 16-22 (Bray & Campbell, 1995;Bray & Gibson, 1998), are those species with the next smallest eggs. It may be that they are deformed, or poorly formed, in the material of the new species, as there is a lot of unattached shell material in the uterus, but all specimens have similar-sized eggs. Steringophorus merretti n. sp. has a relatively larger cirrus-sac (at length 20.5-23.4% of BL) than any other species for which cirrus-sac measurements are available.

Molecular phylogeny
Molecular results indicate that Steringophorus merretti is distinct from all other Steringophorus species for which sequences are available. A molecular phylogeny, inferred from 28S rDNA sequences obtained from GenBank (Table 1), is presented in Fig. 3. This is similar to that published by Pérez-Ponce de León et al. (2018) but includes more shallow waters species of the genera Tergestia Stossich, 1899 and Proctoeces Odhner, 1911 in addition to S. merretti. In Table 1, we have included bathymetric data for these species, when available, which, in conjunction with the tree, shows that the family Fellodistomidae consists of two readily distinguished clades, characterised by the bathymetry of the species. The main caveat with this finding is the position of the shallowwater form Steringotrema robertpoulini Pérez-Ponce de León, Anglade & Randhawa, 2018. This species is from the New Zealand sole Peltorhamphus novaezeelandiae Günther (Pleuronectidae) off South Island, New Zealand (Pérez-Ponce de León et al., 2018). According to Froese & Pauly (2019) it 'inhabits shallow waters, generally at depth of less than 50 m'. It is the only member of its genus for which molecular data are available, so it is not currently possible to state that this a genuinely anomalous position or that a group of related species have invaded shallow water.
Pleuronectiforms are not rare hosts of Steringophorus spp. (see below), but the vast majority of reports are of the species S. furciger, a species which is thought to range into deeper waters (Bray, 2004). Steringophorus merretti is resolved as the sister species of another deep-sea species, S. thulini, and is embedded within a clade of deep-sea species. Odhner, 1905 We are aware of 338 host/parasite reports of the 15 members of this genus, 242 (72%) of which are of S. furciger. Therefore, in any discussion of the biological characteristics of the genus, the predominance of data on this species must be considered. If we look at the fish orders harbouring species of Steringophorus (Fig. 4), we see a predominance of reports in the pleuronectiforms (55%). Considering S. furciger (Fig. 5) only, we see that 76% of records are from this order, but non-furciger species have about 4% of records from this order, and none are identified to species and may well be S. furciger (see Arthur & Albert, 1994;Chambers, 2008). The predominant host orders for non-furciger species are the deep-water taxa, the Osmeriformes (with 28% of records) and the Gadiformes (22%) (Fig. 6). Other predominantly deep-sea orders constitute the majority of the other reports: Ophidiiformes (11%), Aulopiformes (8%), Scorpaeniformes (3%) and Argentiformes (3%). Even the perciform hosts reported for Steringophorus spp. (10% for S. furciger, 15% for non-furciger species) are almost entirely zoarcids (with many upper bathyal species) or Antarctic notothenioids (Artedidraconidae, Bathydraconidae). The genus is, therefore, predominantly found in deep-sea or demersal cold-water fishes.

Steringophorus
The distribution patterns are mapped in Fig. 7, showing the ecoregions of Spalding et al. (2007), with the red circles referring to Steringophorus spp. and the orange circles to Steringotrema spp. The numbers in the red circles (which are not to strictly to scale but give some impression of the number of records) are the number of records of all Steringophorus species, followed by the number of S. furciger records separated by a comma. All reports of S. furciger, and the vast majority of all records, are in the high northern latitudes. The infrequent reports from elsewhere may be affected by sampling effort but are also likely to be indicative of a genuine dearth, as findings of Steringophorus spp. are virtually absent from among the many reports of digeneans from tropical and subtropical regions. Existing reports from apparently warm water regions should be examined closely. For example, the report of specimens from ecoregion 20 (Western Indian Ocean) is of S. dorsolineatus from the deep-sea ipnopid Bathypterois phenax Parr (Reimer, 1985). The three records in ecoregion 17 (Gulf of Guinea) are of parasites of members of the deep-sea family Alepocephalidae (Gaevskaya & Aleshkina, 1983;Aleshkina & Gaevskaya, 1985). The report from off northern Chile (ecoregion 45, Warm Temperate Southeastern Pacific) is of an unnamed species from the macrourid Coryphaenoides ariommus Gilbert & Thompson (Nacari & Oliva, 2016). All reports with identified hosts from the Gulf of Mexico (ecoregion 6, Warm Temperate Northwest Atlantic, and ecoregion 12, Tropical Northwestern Atlantic) are from the deepsea families Ophidiidae, Argentinidae or Alepocephalidae (Manter, 1934(Manter, , 1947Harris & Dronen, 1999). There is no evidence that species of Steringophorus occur in shallow-water or reef fishes in lower latitudes.

Steringotrema Odhner, 1911
As Steringotrema robertpoulini is, apparently, embedded within Steringophorus, according to our tree (Fig. 3) and that of Pérez-Ponce de León et al. (2018), it seems appropriate to discuss this genus and its relationship with Steringophorus. According to Bray (2002), the genera are distinguished by the vitelline configuration of their constituent species, the shape of the ovary and the excretory vesicle. In Steringotrema spp. the vitellarium is mainly, or has a significant proportion, in the forebody, whereas in Steringophorus the vitellarium is mainly in the hindbody. The ovary is multilobate in Steringophorus spp., but in Steringotrema spp. the ovary is entire or tri-lobed. The excretory vesicle is Y-shaped in Steringophorus spp. and V-shaped in Steringotrema spp. Individual species in these genera exhibit some variation in these features. For example, in Steringophorus dorsolineatum, the ovary was originally described as smooth (''glattrandig'') (Reimer, 1985) and later as ''weakly multilobate'' (Bray, 1995). It remains to be seen how useful these characters are in reflecting the  Manter, 1935, Megenteron Manter, 1934, Prudhoeus Bray & Gibson, 1980and Steringovermis Bray, 2004 await molecular study. We are aware of 176 host/parasite records of 12 Steringotrema spp. There is no single predominant species, but three species make up 81% of records. These are the northern temperate species S. pagelli (van Beneden, 1871) (35%), S. ovacutum (Lebour, 1908) (28%) and S. divergens (Rudolphi, 1809) (18%). Perciformes (53%) and Pleuronectiformes (43%) are the predominant host groups (Fig. 8). There are six records from Gadiformes, four of which are not identified to species, and there are single records of named species from Clupeiformes and Tetraodontiformes. In contrast to Steringophorus, the majority of reports from perciform hosts are from the shallow water groups Sparidae (50%) and Blennidae (23%). Kellermanns et al. (2009) found an unnamed Steringotrema in the macrourid Coryphaenoides mediterraneus (Giglioli) from the Charlie-Gibbs Fracture Zone on the Mid-Atlantic Ridge, with a range of depths for the host species (but not necessarily for the parasite) of 1,700-3,050 m. Nevertheless, the finding in a macrourid is certainly worthy of note as an anomalous finding for the parasite. Other records of Steringotrema spp. in macrourids are by Palm & Klimpel (2008)  Steringotrema spp. are distributed mainly in cold to temperate waters, with most records in the northern parts of the Atlantic and Pacific Oceans (Fig. 7). They may be more tolerant of warmer waters than Steringophorus spp.; for example, it is much more commonly reported in the Mediterranean Sea (i.e. ecoregion 4). The few reports from warm waters are, however, not definitive. Fischthal & Thomas (1968) reported, but did not describe, three immature specimens of Markevitschiella sp. (a genus widely  . Not enough information is available to be confident that this was a correct identification. Steringotrema divergens (Rudolphi, 1809) has been reported in Pagellus bogaraveo (Brünnich) off Senegal (ecoregion 16, West African Transition) (Fischthal & Thomas, 1972;Vassiliadès, 1982). These are the only records of this species from sparids but there are no descriptions.

Conclusion
It is more satisfactory for phylogenies to include named and described species and, to this end, we have described here a species for which some molecular data are available. This species is not morphologically highly distinct, but it is from a rarely seen and difficult to obtain host. The only other report of a digenean from this species is that of the hemiurid Merlucciotrema praeclarum (Manter, 1934) by Bray (1996) from the same individual fish. This is a glimpse into the poorly known digenean fauna of the deep-sea, which is worthy of much more sustained study.  trawling; and to many other colleagues and shipmates. We are also grateful to David Cooper who made the serial sections.
Funding The research for this paper did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of interest.
Ethical approval All applicable institutional, national and international guidelines for the care and use of animals were followed.
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