Hypomenia sanjuanensis, Kocot & Todt, 2014

Kocot, Kevin M. & Todt, Christiane, 2014, Three new meiofaunal solenogaster species (Mollusca: Aplacophora) from the north-east Pacific, Journal of Natural History 48 (45 - 48), pp. 3007-3031 : 3022-3028

Hypomenia sanjuanensis sp. nov.

( Figure 2A, C, D , Figures 7–9 )

Type material (13 specimens)

Holotype. ZMBN 94126 , histological section series (5 slides), San Juan Channel near Reid Rock ( Figure 1 ); 48° 19' 26'' N, 122° 35' 08'' E.

Paratypes. ZMBN 94127 , histological section series (4 slides) ; ZMBN 94128 , histological section series (4 slides) ; ZMBN 94129 , 1 whole specimen fixed in 4% formalin and preserved in 70% ethanol ; ZMBN 94130 , sclerite mounts (2 glass slides) ; ZMBN 94131 sclerite mounts (2 glass slides) ; USNM 1231349 , 4 whole specimens fixed in 4% glutaraldehyde in 0.1 M sodium cacodylate buffer and preserved in 70% ethanol ; USNM 1231350 , 3 whole specimens fixed in 4% glutaraldehyde in 0.1 M sodium cacodylate buffer and preserved in 70% ethanol ; USNM 1231348 , 1 whole specimen preserved in 70% ethanol. All paratypes from type locality .

Hypomenia sanjuanensis full length COI sequence NCBI accession number

KJ568515 .

Diagnosis

Body to about 3.5 mm long in life, usually covered with detritus. Mantle sclerites up to about 130 µm in length and with partially or sometimes completely reduced cavity; many with serrated tips. With scale-like peripedal sclerites. With dorsal papillary gland of the pharynx and paired rostral midgut caecum. Radula with three denticles per hook-shaped tooth. One pair of seminal receptacles.

Description

Habitus. Relaxed specimens up to about 3.5 mm in length and 300 µm in diameter ( Figures 2A , 7A ). Virtually all specimens were completely covered in detritus and had a light tan colour at the time of collection. It is possible that this is an artefact of how the specimens were collected and handled in the lab. Because of the detritus sticking to their body, specimens of this species do not appear as shiny as Macellomenia when illuminated from above. Additionally, because of the detritus that is stuck to their body, specimens of this species are well camouflaged when dishes of detritus are being screened for meiofauna. Preserved specimens look similar to living specimens except that they tend to contract and curl ventrally forming a crescent shape.

Mantle. The mantle is covered with elongate, usually recurved sclerites up to about 130 µm long ( Figure 2C, D ). Most of these sclerites have serrations at their tip although some are distally rounded ( Figure 7C, D ). Many of the elongate-type sclerites have a distinct hollow cavity but this cavity is reduced to the proximal half or less of the sclerite. Some sclerites have a largely reduced cavity or lack one altogether. Distally pointed, flat scales up to around 50 µm long by 20 µm wide form a row along either side of the foot ( Figure 7D ). The cuticle is up to about 60 µm thick. Epidermis with some large, possibly glandular cells, but no epidermal papillae are present ( Figure 9).

Pedal groove and mantle cavity. The pedal pit is densely ciliated with associated pedal glands ( Figure 9C). The foot is continuous with the mantle cavity. The mantle cavity is small and without respiratory papillae. No adhesive structures (such as that of Meiomenia ) are associated with the mantle cavity.

Digestive system. The mouth opening is situated behind the vestibular opening and separated from it by a ridge of integument covered by cuticle. The pharynx is distinctly trilobed at and just posterior to the region of the cerebral ganglion ( Figure 9C). It has a wide lumen ( Figure 9B, C) and is lined by a glandular epithelium (no extraepithelial pharyngeal glands) and surrounded by a coat of longitudinal and circular muscle fibres. A dorsal pharyngeal papillary gland is present. This structure generally appears as a dorsal branch of the pharynx surrounded by long-necked glandular cells filled with darkly staining vesicles ( Figure 9B). There is a short, frontally paired rostral midgut caecum. The ventrolateral foregut glands consist of muscular ducts with subepithelial gland cells (type A; Figure 9C).

The radula is distichous with three denticles per tooth (not including the terminally hooked tip of the tooth; Figure 7B ). Approximately 13 pairs of teeth were observed in the radula of an individual that was squash-mounted. There are no constrictions in the midgut.

Nervous system and sensory organs. The atrial sensory organ lacks papillae. The cerebral ganglion ( Figure 9A) is large relative to the body size of the animal, approximately 74 µm from anterior to posterior. Posteriorly, the cerebral ganglion bifurcates and connects to the lateral nerve cords. There is no dorsoterminal sense organ.

Reproductive system. All three specimens examined by histological sectioning were in a reproductive state. Relatively large, well-developed eggs were observed in the gonad and the pericardium ( Figure 9D). The glands of the spawning duct are well developed and stain intensely with toluidine blue. Notably, the dorsal half of the spawning duct stains much more strongly than the ventral half ( Figure 9D). There is a small, tubular seminal receptacle attached to each of the pericardioducts, close to where they fuse with the short paired legs of the spawning duct. The unpaired part of the spawning duct, leading to the (secondary) genital opening in the mantle cavity, is extensive and much longer than the paired legs.

Distribution

Only known from type locality.

Etymology

The species is named for the San Juan Islands.

Comparisons

Similar to the situation for Macellomenia , our findings greatly expand the geographic range for the genus Hypomenia . The only other described species in the genus, H. nierstraszi , is from the Gulf of Naples, European Mediterranean Sea.

Our specimens clearly fall within the diagnosis of the genus Hypomenia , including the mouth being separated from the vestibulum, the presence of a dorsal papillary gland in the pharynx, and the lack of respiratory organs in the pallial cavity, of copulatory stylets or abdominal spicules, and of a dorsoterminal sense organ. A rostral caecum of the midgut is also present in both of the known species of the genus, but in H. nierstraszi it is simple whereas in H. sanjuanensis it is paired.

The very detailed and well-illustrated description of H. nierstraszi was based on a single juvenile specimen that – in a fixed state – was 4.34 mm long (Lummel 1930), which is larger than the largest adult specimens of H. sanjuanensis studied herein. Further diagnostic differences between the two species are the radula, where in H. nierstraszi the radular teeth have only one denticle (versus three denticles in H. sanjuanensis ), and the vestibular cavity that bears numerous papillae in H. nierstrazi and none in H. sanjuanensis . The pericardium in H. nierstraszi is described as having pronounced posterior extentions or ‘horns’ posterior to where the pericardioducts are originating. In H. sanjuanensis , in contrast, the pericardioducts originate in the posteriormost portion of the pericardium. In addition, there is a seminal vesicle attached to each of the pericardioducts in H. sanjuanensis , while such organs are not known for H. nierstraszi . It has to be considered, though, that the H. nierstraszi specimen was a juvenile with clearly underdeveloped spawning ducts (Lummel 1930) and that at this ontogenetic level the genital accessory organs might not be developed yet. Regardless, the great geographic disparity strongly supports our hypothesis that H. sanjuanensis is a valid new species, but a re-investigation of adult specimens of H. nierstraszi is desirable.

On the generic level, we can support a lack of respiratory organs and a dorsoterminal sense organ.

Natural history

Meiofaunal animals tend to have adaptations for living in a dynamic environment where they could be swept up and suspended in the water column ( Higgins and Thiel 1988). None of the three species of solenogasters described herein have an adhesive structure like that of Meiomenia swedmarki , which it uses skilfully to adhere to the substratum when disturbed ( Morse 1979 and own observations). Specimens of Macellomenia schanderi and Hypomenia sanjuanensis that were observed in the laboratory tended to burrow downwards whenever possible. As solenogasters lack eyes, this is potentially a response to gravity (positive gravitaxis). As so few specimens of Macellomenia morseae were examined, we cannot comment on whether or not this species also exhibits a similar burrowing behaviour.

Little is known about the diet of most species of solenogasters and very few species have been observed feeding ( Scheltema and Jebb 1994). Although none of the species described herein fed when provided hydroid polyps in the lab, we were able to screen the transcriptome assemblies for the barcoding gene cytochrome c oxidase subunit I (COI). In the transcriptome of Macellomenia schanderi , we found five contigs (NCBI accession nos. KJ950445–KJ950449) whose top hits when searched against the NCBI nucleotide database using BLASTN with the default settings were Leptothecata or Anthoathecata (Cnidaria, Hydrozoa). One of the recovered contigs was most similar to the anthoathecate Leuckartiara octona (Fleming) (NCBI accession no. GQ120057.1); one was most similar to the leptothecate Eucheilota sp. (NCBI accession no. KF962126.1); one was most similar to the anthoathecate Clava multicornis (Forsskål) (NCBI accession no. JN700935.1); and the remaining two were most similar to the leptothecate Laomedea flexuosa (Alder) (NCBI accession no. JN700945 ). The recovery of five different hydrozoan contigs indicates that the specimen we sequenced fed on no fewer than five genetically distinct hydroids within the last days of its lifetime. Notably, the leptothecate hydrozoan Aglaophenia latirostris Nutting was observed in the meiofaunal samples examined but no COI sequences for this genus are currently publicly available. The orange colour of this hydroid may correspond to the orange material observed in the gut of some specimens of both species of Macellomenia . In the transcriptome of Hypomenia sanjuanensis , we found two contigs (NCBI accession nos. KJ950450–KJ950451) whose top hit when searched against the NCBI nucleotide database using BLASTN with the default settings was the anthoathecate hydrozoan Ectopleura larynx (NCBI accession no. JN700938 ). Ectopleura sp. was observed in the meiofaunal samples examined and thus is probably the prey of H. sanjuanensis .

Figures

Figure 1. Schematic map of the San Juan Islands showing the type locality of the species described herein with a star.

Figure 2. (A) Three new meiofaunal solenogaster species from Reid Rock, Friday Harbor: Ms, Macellomenia schanderi; Mm, Macellomenia morseae; Hs, Hypomenia sanjuanensis; note the similar size, colour, and body shape. Scale bar 1 mm; (B) posterior body end of M. schanderi showing: asp, abdominal spicules. Scale bar 150 µm; (C, D) epidermal sclerites of H. sanjuanensis sp. nov., light micrographs, polarized filter; (C) note the criss-cross arrangement of sclerites (cuticle removed with household bleach); scale bar 50 µm; (D) sclerite types: a, dorsolateral sclerites are acicular with small or almost reduced cavity, often serrated; b, most anterior sclerites are recurved and serrated; c, ventral scales; d, ventral scales found close to the pallial cavity opening; scale bar: 50 µm.

Figure 7. Hypomenia sanjuanensis sp. nov. (A) Light micrograph of fixed specimen, lateral view, anterior body end (ant) to the left. Scale bar 300 µm; (B) light micrograph of extracted radula, teeth (rt) of one side only; sc, epidermal sclerite. Scale bar 40 µm (photo: P. Morse); (C) lateral sclerites partially covered with detritus (dt); Scale bar 100 µm (photo: P. Morse); (D) detail of ventral furrow with pedal scales (ps) in the centre of the image; note the serrated tips of most acicular sclerites. Scale bar 20 µm.