A new species of Leiochrides Augener, 1914 (Annelida: Capitellidae) from the Beibu Gulf, South China Sea

Abstract Background Polychaetes of the family Capitellidae are poorly studied in Chinese waters. Amongst the known capitellid genera in China, Leiochrides Augener, 1914 is an unusual genus encountered in marine surveys. New information In this study, a Leiochrides specimen was obtained during a survey conducted in the Beibu Gulf, northern South China Sea and described herein as a new species Leiochrides guangxiensis sp. nov. The new species differs from its congeners by having uniramous chaetiger 1, chaetigers 11–12 with notopodial capillaries and neuropodial hooks, abdominal hooks with seven teeth above the main fang in three rows, pygidium with four anal cirri, and branchial fascicles with up to 17 filaments. The taxonomic status of the monospecific genus Pseudoleiocapitella Harmelin, 1964 and Leiochrides norvegicus Fauchald, 1972 are discussed.


Introduction
Polychaetes in the family Capitellidae resemble terrestrial earthworms (Rouse and Pleijel 2001). They are a group of organisms frequently encountered in marine surveys, especially in some highly-polluted habitats (Fauchald 1977). This family exhibits high generic diversity with 43 valid genera, including Leiochrides (García-Garza et al. 2019). Leiochrides was initially erected by Augener (1914) for the type species L. australis from West Australia, based on the following characters: thorax having 12 chaetigers with only capillaries; abdominal chaetigers with only hooks; transition between thorax and abdomen indistinct; and branchiae absent. The additional four described species agreed well with the original definition of Leiochrides, namely L. africanus from Congo (Augener 1918), L. pallidior from California (Chamberlin 1918), L. biceps from northern Marshall Islands (Hartman 1954), and L. andamanus from the Andaman Sea, Thailand (Green 2002). The definition of Leiochrides changed as new species were described. Hartman assigned two new species (namely L. branchiatus from the Indian Ocean and Leiochrides sp. from California) with one or two transitional chaetigers in posterior thorax to the genus (Hartman 1963, Hartman 1974), a unique character not found in previous reports. However, the new character was not accepted by Day (1967) and Fauchald (1977). Later, Blake (2000) and Green (2002) re-confirmed the presence of the transitional thoracic chaetigers in some Leiochrides species, and expanded the generic definition. The latest definition proposed by Magalhães and Blake (2017) followed Blake's and Green's, the genus being characterized as follows: chaetiger 1 uniramous or biramous; twelve thoracic chaetigers; chaetigers 1-10 with only capillaries; chaetigers 11-12 may have only capillaries or be transitional with notopodial capillaries and neuropodial hooks; branchiae present or absent. The emended definition of Leiochrides overlapped with that of Pseudomastus (Capaccioni-Azzati and Martín 1992), a monospecific genus from the Mediterranean Sea, as pointed out by Jeong et al. (2017). After morphological comparison between these two closely related genera, Jeong et al. (2017) considered Pseudomastus as a junior synonym of Leiochrides. To date, the genus Leiochrides contains 10 valid species worldwide, as shown in Fig. 1.
In China, capitellid polychaetes are frequently encountered in marine surveys. However, they are poorly understood, as most recorded species lack taxonomic descriptions and illustrations. Based on personal collections from southern China, more than 10 genera are recognized within this family, including Barantolla, Capitella, Heteromastus, Leiocapitella, Leiochrides, Mediomastus, Notodasus, Notomastus, Parheteromastus, and Promastobranchus. Of these, the genus Leiochrides is rarely collected, as well as Leiocapitella and Parheteromastus. Leiochrides specimens have been previously collected from Chinese waters, and they were usually identified as Leiochrides australis (Liu 2008). However, these species records need further confirmation, as Leiochrides australis was described from Australian waters. In this study, a complete Leiochrides specimen was collected from shallow soft sediment in the Beibu Gulf, northern South China Sea. It clearly differs from its congeners in a combination of morphological characters, and is described herein as a new species, Leiochrides guangxiensis sp. nov. Additionally, the taxonomic status of the monospecific genus Pseudoleiocapitella Harmelin, 1964 and Leiochrides norvegicus Fauchald, 1972 was found to be doubtful when reviewing the original descriptions and illustrations of capitellid species related to Leiochrides. The taxonomic relationship of the Capitellethus-Leiochrides-Leiocapitella complex needs a revision in the future.

Materials and methods
The Leiochrides specimen was obtained from the Beibu Gulf, northern South China Sea in October, 2017. The sediment was characterized by high percentage of mud. Sediment samples were collected with a grab sampler (surface area 0.05 m ) and washed through a 0.5 mm sieve on board. All specimens retained by the sieve were fixed with 7% diluted formalin in seawater. In the lab, the Leiochrides specimen was transferred to 70% ethanol. The methyl green staining pattern (MGSP) was used to identify the distribution of glandular areas, following the protocol of Warren et al. (1994). The specimen was submerged in a solution of methyl green staining in 70% ethanol for 1 minute, then washed in clean 70% ethanol to eliminate excess stain. Light microscope images were obtained by means of a Leica M205A stereomicroscope equipped with a Leica DFC 550 digital camera. The structure of abdominal hooks was observed under a light stereomicroscope (Axio Imager Z2, ZEISS) using oil immersion. Scanning Electron Microscopy (SEM) observation was conducted on a middle fragment of the worm using a ZEISS SUPRA 55 SAPPHIRE at Xiamen University, following a process of dehydration, critical point drying, and gold coating.
The type material of the new species was deposited in the Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, China.
Transition between thorax and abdomen indistinct, marked by change in chaetal arrangement ( Fig. 3A and E) and MGSP ( Fig. 2A and B). Abdominal segments shorter than posterior thoracic chaetigers in anterior abdomen, tapering gradually to pygidium. Parapodial lobes slightly swollen in anterior abdomen ( Fig. 3D and F), yet reduced in posterior abdomen ( Fig. 3G and I). Notopodial hooks present from chaetiger 13 (first abdominal chaetiger). Notopodial lobes well separated throughout abdomen ( Fig. 2A, B, E and F). From abdominal chaetiger 11, gap between notopodial lobes of same chaetiger becoming larger to end of anterior fragment ( Fig. 2A). Chaetal fascicles positioned posterior to mid-segment in anterior abdomen ( Fig. 3D and E), and near posterior edge of segment in posterior abdomen (Fig. 3G-I). Abdomen with hooks only, approximately 30 hooks per fascicle in notopodia and more than 100 hooks per fascicle in neuropodia.
Notopodial and neuropodial abdominal hooks similar along body, with long anterior shaft, developed shoulder, angled node, distinct constriction, and short hood (Fig. 2H); posterior shaft longer than anterior one, attenuated to terminal end (Fig. 3L). Hooks (Fig. 3M) with three rows of teeth above main fang: two large teeth in basal row, a larger median tooth, and four smaller teeth above basal teeth. Main fang subtriangular, longer than wide (Fig. 2I).

Etymology
The specific name is derived from the type locality, Guangxi Province.

Distribution
Currently known from the Beibu Gulf, northern South China Sea.

Taxon discussion
The taxonomic and ecological knowledge of this genus is very rare in China, although Leiochrides species have been previously recorded (Liu 2008). This genus is characterized by having 12 thoracic chaetigers, of which the last one or two thoracic chaetigers may only have capillaries or be transitional with notopodial capillaries and neuropodial hooks (Magalhães and Blake 2017). Our specimen in the present study agrees well with the generic diagnosis. Morphological characters used for the separation of species within this genus include the following: the number of transitional thoracic chaetigers, the shape of first chaetiger, the dentition of abdominal hooks, the number of anal cirri, and the presence/absence of branchiae on posterior abdomen. Amongst all described Leiochrides species worldwide, L. guangxiensis sp. nov. is closely similar to L. branchiatus Hartman, 1976 from the Bay of Bengal and L. deltaicus (Capaccinoi-Azzati & Martin, 1992) from north-western Mediterranean Sea in having the last two thoracic chaetigers transitional with notopodial capillaries and neuropodial hooks, uniramous chaetiger 1, and the presence of notopodial branchiae on posterior abdomen. However, L. guangxiensis sp. nov. differs from L. branchiatus in that abdominal hooks of the new species have seven teeth in three rows above main fang instead of three teeth in triangular arrangement as in L. branchiatus. L. guangxiensis sp. nov. can also be distinguished from L. deltaicus in the maximum number of branchial filaments per fascicle and the number of anal cirri. L. guangxiensis sp. nov. bears branchiae with up to 17 branchial filaments per fascicle and pygidum with four anal cirri, whereas in L. deltaicus, posterior abdomen has 2-4 branchial lobes per fascicle and pygidium with three anal cirri. As for MGSP, the new species stains dark blue from the postchaetal area of chaetiger 7 to chaetiger 10, medium blue on the remaining thoracic chaetigers, and light green staining on the abdomen, these characters being distinct from those of other Leiochrides species.
The dentition of abdominal hooks is widely used in capitellid taxonomy, as their ultrastructure is highly specific (Hartman 1947). The characteristic feature of the genus Leiochrides is that abdominal hooks bear two larger teeth in the basal row above the main fang, although the number of small teeth may vary amongst Leiochrides species. Green (2002) pointed out that this mentioned character is conservative in Leiochrides species, as also present in species of Capitellethus and Leiocapitella. These three genera show similarities in general appearance and the difference amongst these genera is in relation to the number of thoracic chaetigers (Magalhães and Blake 2017). In addition to one or two transitional chaetigers, the structural similarity of basal teeth in abdominal hooks amongst these three genera (Capitellethus-Leiochrides-Leiocapitella complex) indicates that they might have a close taxonomic relationship, which should be reviewed as suggested by Green (2002) and Magalhães and Blake (2017). Molecular data should be incorporated to help verify their phylogenetic relationship in the future.
In  (2017), indicating it might be a Leiochrides species. Leiochrides norvegicus was described by Fauchald (1972), based on specimens from the deep Sognefjorden off western Norway. Fauchald (1972) assigned this species to the genus Leiochrides, due to the thorax with 12 chaetigers. However, L. norvegicus has the first two abdominal chaetigers with notopodial capillaries and neuropodial hooks, which did not match the generic diagnosis of Leiochrides. Observed from its chaetal arrangement in the anterior part, L. norvegicus actually bears 14 instead of 12 thoracic chaetigers, of which the last two thoracic chaetigers are transitional. If so, L. norvegicus should be a Leiocapitella species rather than a Leiochrides species. In addition to the number and location of transitional chaetigers, other morphological characters of L. norvegicus have also been found in the members of Leiocapitella, such as uniramous chaetiger 1 and the presence of branchiae on posterior abdomen (Green 2002, Magalhães and Blake 2017). According to the above analysis, the genus Pseudoleiocapitella Harmelin, 1964 and Leiochrides norvegicus Fauchald, 1972 need a revision, and it would be necessary to examine the type materials of Pseudoleiocapitella fauveli and Leiochrides norvegicus.