Two new rapacious nematodes from intertidal sediments, Gammanema magnum sp. nov. and Synonchium caudatubatum sp. nov. (Nematoda, Selachinematidae)

Two new species of the family Selachinematidae Cobb, 1915 from an intertidal sandy fl at in the East China Sea are described. Both species are distinct rapacious nematodes, preying on other nematodes. Gammanema magnum sp. nov. is characterized by its leaf-like labial setae, large loop-shaped amphideal fovea in the male and small spiral ones in the female, an anterior buccal cavity reinforced by 12 rhabdia, each rhabdion with about six denticles, and two unequally long spicules. Gammanema magnum sp. nov. is a striking species, exhibiting extreme sexual dimorphism in the amphideal fovea, but lacking a gubernaculum or precloacal supplements, all features by which it can be differentiated from congeneric species. Synonchium caudatubatum sp. nov. is characterized by a posterior buccal cavity, with three mandibles each with a large tooth fl anked by three smaller teeth on both sides, a transverse oval-shaped multispiral amphideal fovea, and a bluntly rounded tail with a protuberant caudal duct. Synonchium caudatubatum sp. nov. is unique in the genus in having a protuberant caudal duct in the tail end. Furthermore, it differs from its congeners by its mandibles, which have seven teeth each. Synonchium caudatubatum sp. nov. lacks a gubernaculum and a precloacal supplement, both features present in congeners except S. depressum Gerlach, 1954.


Introduction
Within the order Chromadorida Chitwood, 1933, the family Selachinematidae Cobb, 1915 is distinctly characterized by a large buccal cavity divided into two compartments. Nematodes of Selachinematidae

R e s e a r c h a r t i c l e
urn:lsid:zoobank.org:pub:CEA229D3-4B76-4BED-92E5-9D761B7A02D0 are mostly reported from relatively coarse sediments in shallow marine environments worldwide and may also occur in deep-sea habitats (Leduc 2013;Miljutin et al. 2010;Okhlopkov 2002;Tchesunov & Okhlopkov 2006). Many of them are repeatedly reported as predators of other nematodes, and may play a key role in the ecosystems of coarse sandy sediments given their high diversity and high numbers (Okhlopkov 2003;Tchesunov & Okhlopkov 2006).
The taxonomy of Selachinematidae was revised by Gerlach (1964) based on the classification of the buccal cavity structure. Later, Gerlach & Riemann (1973) differentiated two subfamilies within the Selachinematidae based on buccal cavity and cuticular structures. The subfamily Choniolaiminae Schuurmans-Stekhoven & Adam, 1931 is characterized by a buccal cavity reinforced by cuticularized rhabdia in both compartments: six well-developed rhabdia in the broad cup-shaped anterior chamber and three weaker rhabdia in the cylindrical posterior chamber (Tchesunov & Okhlopkov 2006). Members of the subfamily Selachinematinae Cobb, 1915 have a buccal cavity with a reduced anterior chamber and a posterior chamber with mandibles. At present, 15 genera are included in the family Selachinematidae (Vanaverbeke 2015).
So far, only five selachinematid species belonging to three genera, Halichoanolaimus de Man, 1886;Richtersia Steiner, 1916 andSynonchiella Cobb, 1933, have ever been reported from the sea areas of China (Liu 2008;Fu et al. 2013). In this paper we describe two new species of Selachinematidae from a sand beach in the East China Sea: Gammanema magnum sp. nov. (Choniolaiminae) and Synonchium caudatubatum sp. nov. (Selachinematinae). Both species are rapacious and prey on other nematodes. This is also the first record of both genera in the sea areas of China.

Material and methods
Sediment samples were collected from the Dasha'ao Sand Beach in the Nanji Islands National Marine Natural Reserve in the East China Sea (27°27.76′ N, 121°3.48′ E) in May 2014. Samples were fixed with formalin (5% final concentration) in filtered sea water. The fixed samples were stained with 0.1% Rose Bengal for 12 hours (Higgins & Thiel 1988) and subsequently rinsed on a 500 μm sieve to remove large particles and on a 31 μm sieve to retain meiofauna. Meiofauna was extracted from the remaining sediments using Ludox HS 40 by centrifugation (Platt & Warwick 1983) and sorted to higher taxa under a dissecting microscope. Nematodes were transferred into 9:1 (v/v) solution of 50% alcohol-glycerol in a cavity block to slowly evaporate to pure glycerol, and then mounted into permanent slides (Platt & Warwick 1983).
Species descriptions were made from glycerol mounts (Platt & Warwick 1983) using a differential interference contrast microscope (Nikon E80i). Line drawings were made with the aid of a drawing device. Type specimens have been deposited in the Marine Biological Museum of Chinese Academy of Sciences, Qingdao, China (MBMCAS). All measurements are in μm, and all curved structures are measured along the arc. The terminology used for describing the arrangement of morphological features follows Coomans (1979).  Order Chromadorida Chitwood, 1933Family Selachinematidae Cobb, 1915Subfamily Choniolaiminae Schuurmans-Stekhoven & Adam, 1931 Genus Gammanema Cobb, 1920

Results
Gammanema magnum sp. nov. urn:lsid:zoobank.org:act:C86AD66F-ECB9-48A8-8D6A-15D777EB9749 Figs 1-4; Table 1 Diagnosis Body cylindrical, length 2540-4085 μm. Six short leaf-like inner labial setae with broad base, six long leaf-shaped outer labial setae with broad base and four slender cephalic setae arranged in three circlets. Anterior buccal cavity broad and cup-shaped, reinforced by 12 sclerotized rhabdia, each rhabdion with about six denticles at posterior end; posterior buccal cavity narrow and cylindrical with six broad rhabdia, surrounded by pharyngeal tissue. Amphideal fovea exhibiting extreme sexual dimorphism: large loop in about 1.3 turns occupying 79-82% of corresponding body diameter in males and very small spiral in about two turns occupying 12-14% of corresponding body diameter in females. Pharynx with anterior end slightly swelling, but not bulb-like enlarged. Two opposed testes. Sperm globular to oval. Two spicules unequally long and slightly curved, with left spicule (51-56 μm long) slightly shorter than right one (62-69 μm long). Two reflexed ovaries. Spermatheca large, filled up with sperm. Three caudal glands with spinneret. Tail short and conical.

Etymology
The specific epithet is from the Latin adjective 'magnus' (large) and refers to two distinct features of the species, i.e., the large body size and the large amphideal fovea in male.

Description
MeasureMents. See Table 1.
Body. Cylindrical. Cuticle thick and distinct annulated, rows of punctuations on the annules, without lateral differentiation (Figs 1A, 2D, 3A). Head blunt with six pairs of thin, membrane-like cuticle extensions. Anterior sensilla in three circles: six inner labial setae leaf-shaped with a broad base, six outer SHI B. & XU K., Two new rapacious nematodes from an intertidal flat labial setae leaf-shaped with a broad base and four slender cephalic setae (Figs 1A-B, 2B-C, 3A-B). Buccal cavity spacious, divided into two portions. Anterior buccal cavity broad, cup-shaped, with 12 cuticularized rhabdia, each rhabdion with about six pointed denticles at its posterior end. Posterior buccal cavity narrow and cylindrical, surrounded by six broad rhabdia (Figs 1B, 2C, 3B, 4A). Pharynx cylindrical, with slight anterior end swelling, not bubliform, surrounding the posterior buccal cavity, without posterior bulb. Numerous cells surrounding the pharynx. Intestine cells large, filled of orangebrown inclusions. Intestine lumen with irregular and variable appearance. Prey nematode species often observed in the intestine are probably members of Epacanthion Wieser, 1953, as observed in the intestine  European Journal of Taxonomy 405: 1-17 (2018) of a paratype specimen (Fig. 4F). Three caudal glands with spinneret. Tail short and conical (Figs 1D, 2A, 3E).

Female
Similar to male in body shape. Outer labial setae slightly shorter than in male but cephalic setae slightly longer than in male. Amphideal fovea small spiral, in about two turns, covering 12-14% of corresponding body diameter (Figs 2B, 4B). Two reflexed ovaries. Vulva a transverse slit, located at 62-67% of body. Vagina surrounded by well-developed constrictor muscles. Uterus broad. Spermatheca large, filled up with sperm (Fig. 4D).

Remarks
The new species is assigned to the genus Gammanema Cobb, 1920 based on its broad and cup-shaped anterior buccal cavity reinforced by 12 cuticularized rhabdia each with about six pointed denticles at posterior end and a narrow and cylindrical posterior buccal cavity surrounded by six broad rhabdia. The genus Gammanema now contains 13 valid species (Leduc 2013). Among these, sexual dimorphism in the amphideal fovea occurs in species where both males and females are known. However, the males of two species, G. mediterraneum Vitiello, 1970 andG. cancellatum Gerlach, 1955, remain hitherto unknown. Compared to the females, Gammanema magnum sp. nov. differs from G. mediterraneum in the greater body size, which is four times larger, the leaf-like labial setae (vs papillate) and the absence (vs presence) of long somatic setae. It differs from G. cancellatum in the leaf-like outer labial setae distinctly shorter than the cephalic setae (vs slender outer labial setae longer than the cephalic setae).
Gammanema magnum sp. nov. is a striking species exhibiting extreme sexual dimorphism in the amphideal fovea: large loop-shaped in males and small spiral in females. Only G. fennicum Gerlach, 1953, G. conicauda Gerlach, 1953and G. agglutinans Leduc, 2013 show such dimorphism. However, Gammanema magnum sp. nov. differs distinctly from the three aforementioned species by the two unequally long spicules without gubernaculum (vs equal sized spicules with gubernaculum) and the lack of precloacal supplement (vs with supplements). The new species differs also distinctly from G. conicauda and G. agglutinans by its larger amphideal fovea in males (in 1.75 turns covering 79-82% of cbd vs a single loop covering 34-41% of cbd and a small open loop covering 28-29% of cbd, respectively) and the leaf-like labial setae (vs slender and conical setae, respectively).

Etymology
The specific epithet is a composite of the Latin noun 'cauda' (tail) and the Latin adjective 'tubatus' (with tube), referring to the presence of a protuberant caudal duct, a main feature of the species.

Description
MeasureMents. See Table 2.
Body. Cylindrical. Anterior end of head almost truncate. Labial region with 12 lobes and six pairs of thin, membrane-like cuticle extensions (Figs 5D-E, 6A). Six inner labial papillae minute and conical situated on the lips, six outer labial papillae and four cephalic papillae large and conical. Cuticle thick and distinctly annulated, with lateral pores; each annule with a transverse row of punctations, without lateral differentiation. Amphideal fovea multispiral in about three turns, transverse oval-shaped (Figs 5D, 6B). Buccal cavity in two compartments: anterior one with 12 cuticularized rhabdia; posterior one surrounded by pharyngeal tissue, with three mandibles each bearing a large tooth flanked by three smaller teeth to each side (Fig. 5E). Pharynx cylindrical, with anterior end swollen. Nerve ring surrounding pharynx near its middle portion. Cardia flattened. Intestine cells large, filled with numerous small granules. Intestine lumen of irregular and variable appearance, containing remnants such as spicules and mandibles of prey nematodes (Fig. 7C). Three caudal glands with spinneret. Tail bluntly rounded, with a protuberant caudal duct (Fig. 7C).

Male
Two opposed testes short and broad, with anterior one slightly larger than posterior one, situated ventrally left to the intestine. Sperm cells globular to oval. Spicules sclerotized, almost straight, with proximal end weakly cephalated, distal end pointed and slightly bent ventrally. Gubernaculum and precloacal supplement absent.

Female
Similar to male except for reproductive system and sexual features. Two reflexed ovaries. Vulva a transverse slit in ventral view, located at posterior half of body (about 60%). Vagina short. Uterus broad.

Remarks
Synonchium Cobb, 1920 is characterized by the posterior buccal cavity equipped with three mandibles each composed of a large tooth flanked by several teeth and transverse oval-shaped multispiral amphideal fovea. The genus now contains nine valid species (Heyns & Swart 1995;Vinciguerra & Orselli 1997; European Journal of Taxonomy 405: 1-17 (2018) Kamran et al. 2009). Synonchium caudatubatum sp. nov. is unique in the genus by having a protuberant caudal duct in the tail end. The new species also differs from congeners by its mandibles, each with seven teeth, while all other known members have either three or five teeth (Table 3). Synonchium caudatubatum sp. nov. lacks a gubernaculum and a precloacal supplement; both features occur in congeners except S. depressum Gerlach, 1954, a species with a conical tail.

Discussion
The two new species discovered in beach sand from the East China Sea represent the two subfamilies of Selachinematidae. Both species have a robust body, a broad truncated cephalic end and a spacious buccal cavity with well-developed cuticularized rhabdia and denticles or mandibles. Warwick (1971) indicates there is an increase in the dominance of predatory or omnivorous nematode species in sandy sediments. This is clearly shown by the nematode community in the Dasha'ao sand beach, where predatory nematodes dominated the meiofaunal assemblages contributing to about 62% of the total meiofaunal abundance. Among these nematodes, Thoracostomopsidae Filipjev, 1927 are the most predominant Teeth, number European Journal of Taxonomy 405: 1-17 (2018) group occupying more than 60% of the nematode abundance. Members of Thoracostomopsidae are mostly large and predatory and thus may be significant in the sand beach due to their high dominance (Shi & Xu 2016). Selachinematidae contributed to only about 4.6% of the total nematode abundance. However, the two selachinematid species described here are more rapacious nematodes feeding on other nematodes, including members of Thoracostomopsidae Filipjev, 1927. Thus, it can be assumed that Gammanema magnum sp. nov. and Synonchium caudatubatum sp. nov. play a key role in regulating the micro-and meiobenthic communities of this sand beach environment.