Gnathia bermudensis (Crustacea, Isopoda, Gnathiidae), a new species from the mesophotic reefs of Bermuda, with a key to Gnathia from the Greater Caribbean biogeographic region

Abstract Gnathia bermudensissp. nov. is described from mesophotic coral ecosystems in Bermuda; it is distinguished by pronounced and pointed supraocular lobes, two superior frontolateral processes and a weak bifid mediofrontal process, pereonite 1 not fused dorsally with the cephalosome, and large eyes. This is the first record of a species of Gnathia from Bermuda. A synopsis and key to the other Gnathia species from the Greater Caribbean biogeographic region is provided.


Introduction
Gnathiid isopods are temporary ectoparasites that occur in a variety of habitats ranging in depth, water currents, temperature, climate and salinity (Smit and Davies 2004). The parasitic juveniles feed on the blood and lymph of their fish hosts, while the nonfeeding free-living adults are usually hidden in cavities, corals, or sponges (Hadfield et al. 2009). The taxonomic classification of these isopods is based almost exclusively on the morphology of the adult males, and this makes studies reliant on accurate species identification problematic as males can be difficult to obtain. Currently, there are 12 genera in the family Gnathiidae Leach, 1814 (Smit et al. 2019). Of these, the most speciose genus is Gnathia Leach, 1814, with 126 valid species (Boyko et al. 2008 onwards). To date, there are 14 known species of Gnathia from the Greater Caribbean biogeographic region (see Table 1 for a summary of known information on these species). In 1993, Müller (1993) proposed Gnathia puertoricensis Menzies & Glynn, 1968 as a junior synonym for G. virginalis Monod, 1926 based on the variation in the characters that separated these two species (granulation and tubercles on the anterior pereonites and cephalon). Although not recognised in subsequent publications on gnathiids from this region (George 2003;Farquharson et al. 2012), this synonymisation appears to still be valid and the information regarding both species is combined in Table 1.
Bermuda forms part of this Greater Caribbean biogeographic region in the North Atlantic Ocean (Robertson and Cramer 2014). It is situated on the western side of the Sargasso Sea (high salinity, high temperatures and high biodiversity), and has the most northern coral reef system in the world. As part of the Nekton Foundation/XL-Catlin Deep-Ocean Survey -Mission 1 (www.nektonmission.org), fish (Stefanoudis et al. 2019a), zooplankton (Stefanoudis et al. 2019b), black corals (Wagner and Shuler 2017), macroalgae (Schneider et al. 2018(Schneider et al. , 2019 and other benthic communities (NVS pers. obs.) were studied. Macrofaunal collections from mesophotic reef ecosystems of Bermuda (MCEs) contained several specimens of a gnathiid isopod that did not correspond to currently described species. This isopod is here described as a new species of Gnathia and is the first gnathiid isopod to be recorded from Bermuda.

Materials and methods
All benthic samples were collected from 17 July to 14 August 2016 aboard the R/V "Baseline Explorer". Mesophotic benthic surveys and sampling were conducted using Trimix rebreathing divers from the Global Underwater Explorers (GUE) down to 94 m around the edge of the Bermuda platform. The sampling sites North Northeast (NNE), Plantagenet Bank, Spittal, and Tiger, were selected along the northeast, southeast and southern slopes of the Bermuda platform, respectively ( Figure 1). During the same mission, two two-person Triton Class Submersibles (Nomad and Nemo; Vero Beach, FL, United States) equipped with an arm manipulator assisted in sample collection down to 300 m. Divers collected macroalgae, loose gravel, bottom sediment, rhodoliths, sponges, and hard and soft corals to characterise the biodiversity of the Bermudian mesophotic reefs. The depth range for each sample was noted. Once the substrata were brought onto the research vessel, they were placed on a 0.063 μm sieve and washed thoroughly with filtered water. Meiofauna and macrofauna associated with the substrata were captured on the 0.063 μm sieve and preserved in > 95 % ethanol. The preserved samples were sorted, placed in 95 % ethanol, and stored at -20 °C until further processing. Research permits for Bermuda were issued by the Department of Environment and Natural Resources, Bermuda (No. 2016070751). From these samples, several gnathiids were cleaned and prepared for scanning electron microscopy (SEM; PhenomWorld). Gnathiids were also observed and drawn using an Olympus BX41 compound microscope and an Olympus SZX7 dissecting microscope with a camera lucida. Appendages were removed with the aid of dissecting needles and forceps and stained using lignin pink.
The species description was prepared in DELTA (DEscriptive Language for TAxonomy) using a general Gnathiidae character set (as used in Svavarsson and Bruce 2012). The description is based on the adult male gnathiid. Terminology follows Monod (1926), Cohen and Poore (1994) and Bruce (2012, 2019). Isopod classification follows that of Brandt and Poore (2003).
Material is deposited in the Natural History Museum of Bermuda.  Monod, 1922).
Diagnosis. Frontal margin of cephalosome generally straight (not deeply excavated), with frontal processes. Mandibles not elongate, usually with mandibular incisor and dentate mandibular blade. Paraocular ornamentation and/or a dorsal sulcus may be present on cephalosome. Pereonite 1 possibly immersed in cephalosome. Pylopod broad and distinct, with two or three articles, operculate; article 1 enlarged, generally with dense external margin of plumose setae; article 3 reduced or absent.
Remarks. Gnathia can be identified by the presence of frontal processes, a straight frontal border, a broad 2 or 3 articled pylopod, and non-extended mandibles with a dentate blade.
It is the most speciose genus in the family Gnathiidae (currently with 126 valid species). Gnathia is a cosmopolitan genus, commonly found in coral-reef habitats, and its parasitic larvae have been reported from both teleost and elasmobranch hosts (Smit and Davies 2004). The most recent revision of this genus was by Cohen and Poore (1994).  Description of male. Body 2.3 times as long as greatest width, widest at pereonite 3; dorsal surfaces sparsely punctate, sparsely setose. Cephalosome quadrate, 0.7 as long as wide, lateral margins sub-parallel; dorsal surface with sparse granules; dorsal sulcus narrow, shallow, short; translucent region absent; paraocular ornamentation strongly developed, posteromedian tubercle present. Frontolateral processes present. Frontal margin slightly produced. External scissura present, wide, shallow. Mediofrontal process present, weak, bifid, without fine setae. Supraocular lobe pronounced, pointed; accessory supraocular lobe not pronounced. Superior frontolateral process present, single, strong, conical, with two long simple setae. Inferior frontolateral process absent. Mesioventral margin concave. Eyes present, elongate, 0.3 times as long as cephalosome length, bulbous, standing out from head surface, ommatidia arranged in rows, eye colour black.
Antennula peduncle article 2 0.8 times as long as article 1; article 3 1.9 times as long as article 2, 2.7 times as long as wide; flagellum 1.1 times as long as article 3, with five articles; article 3 with one aesthetasc seta and one simple seta; article 4 with one aesthetasc seta and one simple seta; article 5 terminating with one aesthetasc seta and three simple setae. Antenna peduncle article 4 2.5 times as long as wide, twice as long as article 3, and four simple setae; article 5 1.3 times as long as article 4, 2.8 times as long as wide, inferior margin with three penicillate setae, with six simple setae; flagellum 1.5 times as long as article 5, with seven articles.
Pylopod first article 1.5 as long as wide, without distolateral lobe; posterior and lateral margins forming rounded curve; lateral margin with 23 large plumose setae; mesial margin with continuous scale-setae; distal margin with three simple setae; second article 1.1 as long as wide.
Pereopods 2-6 with long simple setae and randomly covered in pectinate scales; pereopod 2 with tubercles on carpus and basis to ischium. Pereopod 2 basis 2.8 times as long as greatest width, superior margin with five setae, inferior margin with two setae; ischium 0.6 times as long as basis, 2.6 as long as wide, superior margin with one seta, inferior margin with three setae; merus 0.5 as long as ischium, 1.5 as long as wide, superior margin with two setae, inferior margin with four setae; carpus 0.6 as long as ischium, 1.9 as long as wide, superior margin without setae, inferior margin with two setae; propodus 0.8 times as long as ischium, 2.8 times as long as wide, superior and inferior margins without setae, and two robust setae; dactylus 0.7 as long as propodus. Pereopods 3 and 4 similar to pereopod 2. Pereopod 5 similar to pereopod 6. Pereopod 6 with tubercles on merus and carpus; basis 3.1 times as long as greatest width, superior margin with two setae, inferior margin with two setae; ischium 0.7 as long as basis, 2.7 as long as greatest width, superior margin with three setae, inferior margin with four setae; merus 0.6 as long as ischium, 2.1 times as long as wide, superior margin with three setae, inferior margin with two setae; carpus 0.6 as long as ischium, 1.7 times as long as wide, superior margin and inferior margin with one seta; propodus 0.9 as long as ischium, 3.8 times as long as wide, superior margin with three setae, inferior margin with one seta, and two robust setae; dactylus 0.6 as long as propodus.
Penes opening flush with surface of sternite 7. Pleopod 2 exopod 1.9 as long as wide, distally broadly rounded, with eight plumose setae; endopod 1.9 as long as wide, distally broadly rounded, with eight plumose setae; appendix masculina absent; peduncle 1.5 times as wide as long, mesial margin with two coupling setae, lateral margin with one simple seta.
Uropod rami extending beyond pleotelson, apices narrowly rounded. Uropod endopod 2.4 as long as greatest width, dorsally with five setae; lateral margin straight; proximomesial margin weakly convex, with seven long plumose setae. Uropod exopod not extending to end of endopod, 2.9 times as long as greatest width; lateral margin straight, with two simple setae; proximomesial margin straight, distally convex, mesiodistal margin with seven long plumose setae.
Etymology. The epithet bermudensis is for the country Bermuda, being the first Gnathia record from this island nation.
Hosts. Not known. Remarks. Gnathia bermudensis sp. nov. may be identified by the produced frontal margin; presence of two superior frontolateral processes; a weak and bifid mediofrontal process; and pronounced and pointed supraocular lobes. The uropod rami extend past the posterior point of the pleotelson; pereonite 1 is not dorsally fused with the cephalosome; large eyes (0.3 as long as cephalosome length); and a weakly curved, dentate mandible.
This species is from a moderate depth of 56-90 m and was collected from several habitat types (algae, loose gravel, rhodoliths, sediment associated with scleractinian corals, muddy sand, and sponges) encompassing the mesophotic reef ecosystems of Bermuda. The Mesophotic Coral Ecosystems (MCEs) of Bermuda represent the most northern coral reef systems of the Atlantic; they are visually dominated by scleractinian corals at the upper depth limits, which are replaced gradually at greater depths by rhodoliths, macroalgae beds and fossilised reefs (Goodbody-Gringley et al. 2019). The new gnathiid species has been found on the mesophotic slopes of the main seamount (i.e., the main island of Bermuda) and the smaller seamount Plantagenet ( Figure 1); therefore, it is expected to be found throughout the deeper reefs of Bermuda. Only four other species of Gnathia have been collected from greater depths in this region.
Gnathia bermudensis sp. nov. is most similar to G. beethoveni Paul & Menzies, 1971, G. calsi Müller, 1993, G. johanna Monod, 1926, G. magdalenensis Müller, 1988, and G. virginalis Monod, 1926 from the region. The frontal margin of G. beethoveni differs from Gnathia bermudensis in having less pronounced supraocular lobes, four frontolateral processes, a shallow median notch, and the cephalosome is lacking dorsal tubercles. Gnathia calsi also has a deeply notched mediofrontal process with two lobes (and setae), and well developed but angular supraocular lobes, not seen in Gnathia bermudensis sp. nov. Gnathia johanna is narrower than Gnathia bermudensis sp. nov., with less pronounced supraocular lobes and a single convex mediofrontal process (with setae) between the supe- rior frontolateral processes. Gnathia magdalenensis and G. virginalis differ from Gnathia bermudensis sp. nov. in having slightly pointed supraocular lobes, a single pointed mediofrontal process with setae, and a longer cephalosome that is fused with pereonite 1.
Although adult females and zuphea juveniles were collected with the males, they cannot be confidently linked to this species without molecular or ecological data. More collections and rearing of the gnathiid isopods would need to be made in the future for more information and validation of these different life stages, as well as to determine the hosts of the juvenile stages.

Key to members of the genus Gnathia known from the Greater Caribbean biogeographic region
This key is based on the morphological characters of the adult male: