Research Article |
Corresponding author: P. Graham Oliver ( graham.oliver@museumwales.ac.uk ) Academic editor: Matthias Glaubrecht
© 2015 P. Graham Oliver.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Oliver PG (2015) Description and morphology of the “Juan de Fuca vent mussel”, Benthomodiolus erebus sp. n. (Bivalvia, Mytilidae, Bathymodiolinae): “Phylogenetically basal but morphologically advanced”. Zoosystematics and Evolution 91(2): 151-165. https://doi.org/10.3897/zse.91.5417
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The Juan de Fuca vent mussel first found in 1990 is formally described as Benthomodiolus erebus sp. n. Comparisons are made with the three other species previously assigned to Benthomodiolus namely B. lignocola, B. geikotsucola and B. abyssicola. The anatomies of all four species are examined and are shown to share the arrangement of pedal and byssus musculature, having largely un-fused mantle margins and a hind gut with a very short loop. The ctenidia were examined using both light and scanning electron microscopy. B. erebus and B. geikotsucola were found to have lamellar filaments with extensive abfrontal expansion and fusion of the ascending and descending arms. In this there is similarity with Bathymodiolus. B. lignocola and B. abyssicola were found to have linear filaments with narrow abfrontal surfaces with little fusion. All four species were shown to have the abfrontal surfaces covered by polygonal cushions of microvilli although these were much less apparent in B. lignocola and B. abyssicola. Although Benthomodiolus was shown by a number of previous studies, using molecular data alone, to be phylogenetically basal to all other Bathymodiolinae the anatomy is highly adapted for chemosymbiosis. Species of Benthomodiolus are found on wood-falls, whale-falls and vent sites and thus mirror the habits of the Bathymodiolus/Idas clade.
Bathymodiolinae , Benthomodiolus , Benthomodiolus erebus New species, Juan de Fuca Ridge, Anatomy, Deep-sea, Hydrothermal-vent
In a forthcoming paper,
None of the published literature illustrates this mussel with the exception of the micro-structure of the ctenidium by
This paper will give a proper taxonomic status to the Juan de Fuca mussel through a description of the shell and anatomy and will make comparisons with other species assigned to Benthomodiolus. The habitat range of Benthomodiolus species includes the three major ecotypes, wood-fall, whale-fall and vent; this paper will investigate whether there are any associated morphological characters. Comparisons with other members of the Bathymodiolinae will attempt to elucidate whether the basal position of Benthomodiolus is reflected in the morphology.
The materials examined in this paper are listed under their respective sections in the results section.
The photographic images were made using a Leica Z6 macroscope and image stacking using Helicon Focus™ software. For some anatomical images the tissues were stained with methyl green to enhance contrast. For scanning electron microscopy gill tissues were excised and cut transversely and longitudinally using a thin razor blade. Tissues were dehydrated in 100% ethanol overnight and critically point dried with liquid CO2 as the intermediate fluid in a Quorum K850 critical point dryer. Dried samples were mounted and gold coated before examination using a Jeol Neoscope™ SEM.
CMN ML Canadian Museum of Nature, Mollusca
MNNZ Museum of New Zealand Te Papa Tongarewa
NMW.Z. National Museum Wales, Zoology
NSMT National Science Museum Tokyo
ZMUC Zoological Museum University of Copenhagen
aa anterior adductor muscle, an anus, apr anterior pedal retractor muscle, au auricle, bys byssus, ct ctenidium, ddd duct to the digestive diverticula, eav exhalant aperture valve, f foot, f(hl) heel of foot, f(t) toe of foot, fme fused mantle edge, h heart, hgl hind gut loop, ifj inter filamentar junction, ilp inner labial palp, imf inner mantle fold, lp labial palps, lps suspensor muscle for labial palps, me/ct mantle edge ctenidial junction, mef mantle edge folds, mmf middle mantle fold, oe oesophagus, olp outer labial palp, omf outer mantle fold, ot oral tube, pa posterior adductor muscle, pbr1 posterior pedal/byssus retractor muscle, pbr2 anterior pedal/byssus retractor muscle, per pericardium, pms posterior mantle septum, ppr posterior pedal retractor muscle, psf polygonal surface, rt rectum, sppr secondary posterior pedal retractor muscles, ss/mg style sac and mid gut, st stomach, vfg ventral food groove, vg visceral ganglion, vt ventricle
Benthomodiolus lignocola Dell, 1987
To 43 mm, Thin, umbonate, narrow modioliform, weakly arcuate with beaks about ¼ distance from the anterior, anterior margin rounded only a little narrower than rounded posterior margin. Median area slightly sulcate, widest part behind the umbos. Hinge margin lacking crenulations, ligament sunken, very long. Periostracum persistent, smooth or with sparse hairs. Pedal/byssus musculature in two groups, a posterior set close to the posterior adductor muscle and a median set attached to rear of the umbo. Mantle edge mostly free, poorly frilled, posterior junction short. Hind-gut with a short or very short loop. Ctenidial filaments linear or laminar. Symbiotic bacteria are extra-cellular.
B. lignocola Dell, 1987; B. geikotsucola Okutani & Miyazaki, 2007; B. erebus this paper; B. abyssicola (Knudsen, 1970).
Described species are restricted to the Pacific Ocean from New Zealand, Japan, British Columbia and Panama at bathyal to abyssal depths. An undescribed species from the South Atlantic is reported by
Benthomodiolus lignocola, B. geikotsucola and B. erebus are regarded as congeneric, based on a combined analysis of COI mtDNA and 28S rRNA (
Consequently the generic diagnosis is based on a combination of characters from B. lignocola, B. geikotsucola and B. erebus. If M. abyssicola is included, then the shell form needs to be expanded to include the more wedge shaped form.
Taxon | Max shell length AL/TL | Bathymetric range | Distribution | Habitat |
---|---|---|---|---|
B. lignocola | 18.1 mm 0.23 |
810–2670m | Chatham Isds, SW Pacific | Wood |
B. geikotsucola | 42.5 mm 0.28 |
4020m | Torishima Seamount, W. Pacific | Whale bone |
?B. abyssicola | 17.2 mm 0.22 |
3670–3270m | Gulf of Panama, CE. Pacific | Wood |
B. erebus | 39.9 mm 0.23 |
2195m | Juan de Fuca Ridge, NE Pacific | Vent |
Adipicola sp. (n. sp.?)
Bathymodiolus sp. JdeF
Adipicola MV Southward, 2008: 139–146, shell not illustrated
Holotype. 1 specimen, ROV ROPOS dive R682, Clam Bed, Endeavour Segment, Juan de Fuca Ridge, 47°57.8’N 129°05.5’W, 2195m, 19/August/2002. CMNML 097165
Dimensions in mm. Length 39.9; Height 15.4; Width 13.2; Anterior length 9.5
Paratype. 1 broken and partly dissected specimen, Alvin dive 2803, clam bed, Kini’s Site, Middle Valley, Juan de Fuca Ridge, 48°27.40’N 128°42.52’W, 2416m, 24/July/1994. NMW.Z.2015.013.1. This is the remainder of the material used by
Dimensions in mm. Length 39.2; Height 12.9; Width 10.3; Anterior length 10.1
Holotype, (Fig.
Paratype, (Fig.
Pedal byssus musculature. (Fig.
Adductor muscles. The adductor muscles are of almost equal size, the posterior is circular in section while the anterior is oval (Fig.
Ctenidium and labial palps. The ctenidia (Figs
Scanning electron microscopy reveals that the abfrontal surfaces are extensive giving a triangular plate like form to the largely fused ascending and descending arms of each filament (Fig.
The labial palps (Fig.
The mantle edges are free for their entire length (Fig.
a–e The ctenidium of Benthomodiolus erebus sp. n. a gross anatomy, b SEM of whole filament, c SEM of tip of a single filament, d SEM of inter filamental junction, e SEM of polygonal surface of microvilli. f–h The ctenidium of B. geikotsucola. f gross anatomy, g SEM of a whole filament, h SEM of the polygonal surface.
The alimentary system (Fig.
The stomach (Fig.
Internally the major typhlosole runs longitudinally across the floor, to its right side there is a smooth depression and leading off this are tracts to the right side ducts. There is a deep embayment running from the anterior floor and up the anterior left side into the shallow caecum and sharply curving into the dorsal hood. A small duct exits this trough on the anterior floor and medially it opens into the left pouch where a large duct exits. The gastric shield is shaped into the dorsal hood and extends posteriorly of the left posterior dorsal face. Sorting ridges are nowhere apparent except for a well defined but small area on the posterior edge of the left pouch.
The pericardium (Figs
After Erebus (Greek), Noun in apposition, “place of darkness between earth and Hades” alluding to the abyssal, hydrothermal vent, type locality.
Located in low temperature vent flows (<20 °C) associated with other vent endemic animals but is sparse and rarely collected. At Endeavour, it was recovered in a grab of the siboglinid Ridgeia piscesae at the base of the tubeworm cluster. At Middle Valley, it was recovered nestled in crevices of a sulphide block, also colonized by R. piscesae. Overall setting at both sites featured sulphide deposits with limited high temperature venting surrounded by ponds of sediment where vesicomyid clams also occurred (
In the following section the other species assigned to Benthomodiolus are described with reference to B. erebus rather than in full detail.
Benthomodiolus geikotsucola Okutani & Miyazaki, 2007: 49–55, figs 2–3.
Holotype. 1 shell, NSMT-Mo-76703, Summit of Torishima Seamount, 30°55’N 141°49’E, 4020m. Not examined, image courtesy of NSMT.
Paratype. 1 specimen, NSMT Mo-76704j as holotype.
The holotype (Fig.
The arrangement of the pedal and adductor muscles (Fig.
The ctenidium consists of both demibranchs and as in B. erebus the filaments are relatively short (Fig.
The mantle edge is free for most of its length and fused only posteriorly to separate the ventral gape for the exhalant aperture. The entire length of the ventral gape the middle fold is thrown into a dense series of folds (Fig.
The stomach was not dissected. The gut follows a similar path to that in B. erebus but the hindgut loop is distinct with a short reversed portion (Fig.
Benthomodiolus lignocola Dell, 1987: 33–34, figs. 44, 45, 48, 49, 52, and 53.
Holotype. 1 shell, NW of Orete Point, White Island, 37°23.7’S 177°39.5’E, 1075–1100m, 23/Nov/1981; Museum of New Zealand Te Papa Tongarewa M.075023. Not examined, image courtesy of NMNZ.
Paratype. 5 specimens, NE of Chatham Islands, 42°47.10’ 175°45.60’W, 1174–1180m, 22/Aug/1984; NMNZ M–075248/1.
The shells have a maximum length of 18.1 mm (Holotype, Fig.
Shells and anatomy of Benthomodiolus lignocola Dell, 1987. a exterior of the right valve of the holotype (MNNZ M.075023), b-d the shell of the dissected paratype MNNZ M-075248/1, e–g gross anatomy stained with methylene green. e after removal of left valve and mantle, f after further removal of the ctenidium, g diagram of the adductor, pedal and byssal musculature.
The byssal retractors (Fig.
The ctenidium consists of both demibranchs with relatively short strap-like filaments and has a flimsy appearance with weak inter-filamentar junctions (Fig.
The mantle edge (Fig.
The stomach was not dissected. The gut follows a similar path to that in B. erebus but the hind gut loop is distinct with a short reversed portion.
Modiolus abyssicola Knudsen, 1970: 92–94, text figs 55–57, pl. 14, fig. 6.
Benthomodiolus abyssicola (Knudsen) —
Benthomodiolus abyssicola (Knudsen) —
Benthomodiolus abyssicola (Knudsen) —
Holotype. Gulf of Panama, E. Pacific, 05°49’N 78°52’W, 3670-3270m. ZMUC, not examined.
Paratype. From type locality, 10 specimens examined, ZMUC-BIV-30.
Illustration.Paratypes were dissected by Vita Kenk and her drawing was published in
Shells and anatomy of paratypes Benthomodiolus abyssicola Knudsen, 1970 (ZMUC-BIV-30). a exterior of the right valve of the dissected specimen, b interior of left valve, c dorsal view of a small specimen with well preserved periostracal bristles, d gross anatomy, stained with methylene green after removal of right valve, mantle and ctenidium, e pedal and byssal musculature, f diagram of the gross anatomy of a paratype after Kenk in
The shells have a maximum length of 17.2 mm and the dissected specimen was 17.1 mm in length (Fig.
The byssal retractors (pbr2 and pbr1) are widely separated with pbr2 attached immediately behind the umbonal cavity (Fig.
The ctenidium consists of both demibranchs with relatively short strap-like filaments and has a flimsy appearance with weak inter-filamentar junctions (Figs
a–e The ctenidium of Benthomodiolus lignocola a gross anatomy, b SEM of whole filaments, c SEM of inter filamentar junction, d SEM of tip of filament, e SEM of polygonal surface of microvilli (
The mantle edge is free along its entire length except for a small junction with the gill axis of the ctenidium to form a small exhalant aperture (Fig.
The gut follows a simple route with the oesophagus, stomach and mid gut in a line running across the dorsal surface of the visceral mass (Fig.
Benthomodiolus erebus is regarded as a distinct species but does bear close resemblance to B. geikotsucola, which differs in having the shell more extended anteriorly, having a distinct hind-gut loop and strongly folded mantle edge. The molecular data also confirm B. erebus and B. geikotsucola to be sister taxa (
The molecular data link B. erebus, B. geikotsucola and B. lignocola but there are some distinct morphological difference that sets the latter apart from the former two. Benthomodiolus lignocola is much smaller; the shell is not quite so umbonate and bears periostracal hairs. The byssal retractor muscles although widely separated are less so than in the other species and reflects the more expanded posterior of the shell.
The ctenidial filaments are linear, strap-like, and unlike the triangular laminar forms seen in B. erebus and B. geikotsucola. In this, the ctendium of B. erebus and B. geikotsucola resembles that of Bathymodiolus and is highly adapted to host symbiotic bacteria. Although laminar the symbionts are extracellular unlike the intracellular condition of many species of Bathymodiolus and Gigantidas (
Morphologically one might propose B. erebus and B. geikotsucola to be in a separate genus from B. lignocola and B. abyssicola, based on the shell shape, lack of periostracal hairs and laminar gill filaments. However, there is currently no molecular support for any generic distinctions within the Benthomodiolus clade and there is as yet no molecular data for B. abyssicola.
The morphological basis to the generic systematics of the Bathymodiolinae has been shown by
The shell form B. erebus and B. geikotsucola is rather unusual with the narrow arcuate outline and relatively long anterior portion, as such they can scarcely be described as modioliform where the outline is more wedge shaped. Although scarce this shell form occurs in other genera notably Terua but also in some species of Bathymodiolus and Gigantidas. The smaller B. lignocola and B. abyssicola are more modioliform and resemble Idas. Shell shape has no consistency within Benthomodiolus a situation mirrored in the other clades such Bathymodiolus and Gigantidas (
The Benthomodiolus clade is considered to be the sister to the entire remainder of the bathymodiolines and occupies a basal position in all published phylogenetic trees (
I would like to thank Prof. Verena Tunnicliffe for the opportunity to write this paper and to her and Dr Eve Southward for their help with the manuscript and sourcing materials. Also to Justine Thubaut and Rudo von Cosel for giving me access to a prepublication copy of their forthcoming monograph on the Bathymodiolinae and to Rudo again for reading the first draft of the manuscript. To Bruce Marshall of Te Papa, National Museum of New Zealand; to Tom Schiøtte of the Zoological Museum, Copenhagen and to Hiroshi Saito of the National Science Museum, Tokyo for the loan of comparative material. To Paul Valentich-Scott for the copy of the original drawing of the anatomy of B. abyssicola by Vita Kenk. To Clara Rodrigues for discussions concerning the molecular trees.