Review of the Septibranchia ( Mollusca : Pelecypoda ) from the deep sea of Campos Basin , Brazil : Family Lyonsiellidae , with description of a new species CLÉO

A review is made of the members of Lyonsiellidae present on the continental slope (750-2000 m) of Campos Basin (22°S), off south-eastern Brazil. A total of six taxa are recognized. Two taxa were previously unknown to science (Lyonsiella pipoca n. sp., described herein, and Policordia sp.). Lyonsiella frielei and Policordia gemma are recorded from Brazilian waters for the first time. Lyonsiella abyssicola is distributed throughout the Atlantic Ocean, but the present record fills a gap in its distribution in the southwest Atlantic. Lyonsiella cf. formosa has a confused taxonomic status, and we believe that more than one species has been called L. formosa. Lyonsiella abyssicola, L. frielei and L. cf. formosa have the shell surface covered by small spines that typically have a hexagonal column and a stellate structure at the distal end.


INTRODUCTION
Lyonsiellidae Dall, 1895 is a family of small pelecypods, which display an anatomical arsenal developed for a carnivorous mode of life.Like most derived septibranchs, the lyonsiellids have an eversible inhalant siphon surrounded by a ring of small tentacles, a sparsely ciliated gut associated with a muscular gizzard stomach with an extensive gastric shield, and gradual muscular development of the ctenidium (Allen and Turner, 1974;Morton, 1987).
Most lyonsiellids have an almost rectangular shell, usually with the dorso-ventral axis tilted in relation to the antero-posterior axis, instead of the typical perpendicular position of this axis in pelecypods.Moreover, unlike the verticordiids, which usually have a robust shell, the lyonsiellids have a very thin shell and an edentulous hinge.
The Lyonsiellidae have been known since the Pliocene (Harper et al., 2000), and nowadays are present in all deep seas of the world.As in almost all deep-sea species, the number of unnamed species is linked to the difficulties involved in collecting material from great depths.A few studies have dealt with septibranchs in Brazilian waters (e.g.Marini, 1974;Oliveira andAbsalão, 2007, 2009;Simone and Cunha, 2008).
This report is part of a continuing effort to fill gaps in the knowledge of the septibranchs, and contains the results of a taxonomic review of the family Lyonsiellidae from Campos Basin, off Rio de Janeiro state, Brazil.

MATERIALS AND METHODS
One hundred and seventeen samples were taken on the continental slope off south-eastern Brazil (22°S, 41°W), at depths from 700 to 1950 meters, between 2001 and 2003 as part of the program "Environmental Characterization of Campos Basin, RJ, Brazil" under the auspices of PETROBRAS S.A.The continental slope of Campos Basin is 40 km wide, with depths up to 3000 m.It is covered by fine sediment and a sandy fraction that is composed mainly of foraminiferan tests (Soares-Gomes et al., 1999).The samples were taken with a 0.25 m 2 box corer, from the Research Vessel "Astro-Garoupa".Each sample was washed through a 0.5 mm mesh, and conserved in 70% ethanol.In the laboratory, the residues were examined under magnification and the molluscs picked out.Most of the shells were in a good state of conservation, but no live specimens were found.
Each species was photographed under a Scanning Electron Microscope (ZEISS EVO 40), at the Gerência de Bioestratigrafia e Paleoecologia Aplicada (BPA), of the Petrobrás Research Center (Centro de Pesquisas da Petrobrás -CENPES), and under a Scanning Electron Microscope (JEOL -6390LV) at the Museu Nacional -Universidade Federal do Rio de Janeiro.
The generic characterization was adapted from several authors (e.g.Allen and Turner, 1974;Rios, 1994;Poutiers and Bernard, 1995;Simone and Cunha, 2008).The types of most species treated were examined, except in a few cases when the original illustration and/or description were sufficient to identify the taxon.The material is deposited in the Mollusca collection of the following institutions: Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (IBUFRJ) and Muséum National d'Histoire Naturelle, Paris (MNHN).
Table 1 summarizes the characters of Lyonsiellidae treated here.
Remarks: One of the most remarkable characteristics of Lyonsiella is the inclination of the anteroposterior axis in relation to the dorso-ventral axis.
Lyonsiella abyssicola (G.O.Sars, 1872) (Figs.1A-E)  Description: Shell fragile, white, small (height 1-5 mm, length 1-5 mm), inequivalve, inequilateral, inflated, umbones prosogyrate, outline rectangular, postero-dorsal and antero-ventral margins parallel, almost the same size, postero-ventral margin straight, forming an angle of about 90 o with postero-dorsal and antero-ventral margins, antero-dorsal margin rounded.Externally orna-mented with 14 to 20 fine raised axial threads that intercalate sets of about 5-8 close-set equidistant radiating series of delicate spines.Each spine is a polyhedral column that tapers towards its distal end, which has a stellate, usually hexagonal, structure.The threads extend from the edge of the shell towards the umbo, but do not all reach it.Often exhibiting concentric scars caused by damage.Hinges of both valves edentate, with a slender, posterior groove.The anterior muscle scar is less marked, posterior muscle scar and pallial line hardly visible.
Remarks: The name Lyonsiella abyssicola was introduced by M. Sars ( 1869), but without a formal description, and it does not comply with article 12 of the Code (ICZN, 2000: 16), and is therefore a nomen nudum.A proper description of this species was provided by G. O. Sars (1872), as Pecchiolia abyssicola.
This species shows some variation in its outline, probably due to a change in the proportions of the shell during ontogeny.The outline of the smallest individuals is sharply angulated, with a truncated aspect, which grades to a trapezoidal outline in adult specimens.In adult specimens, dirt particles encrusted among the spines of the shell are more noticeable.

Lyonsiella frielei
Lyonsiella frielei Allen and Turner, 1974: 440-442, Figs. 35, 36;Allen (2008: 80, under the name L. freilei).Laevicordia frielei: Poutiers and Bernard (1995: 146 and  Description: Shell fragile, white, small (height 2-3.5 mm, length 2-4 mm), inequivalve, inequilateral, inflated, umbones prosogyrate, outline quadrangular, postero-dorsal margins sloping downwards, merging with a gently curved ventral margin that is almost continuous with the sharply curved anterodorsal margin, antero-dorsal margin extending slightly below the umbo and forming a short indentation.Externally ornamented with, usually, 15 fine raised axial threads that intercalate with sets of about 4-8 close-set equidistant radiating series of delicate spines.Each spine is a polyhedral column that tapers towards the distal end, which bears a stellate, usually hexagonal structure.The threads extend from the edge of the shell towards the umbo, but do not all reach it.Hinges of both valves edentate.Muscle scars and pallial line hardly visible.
Remarks: This species is quite similar to L. abyssicola, and the young specimens of the two species are not easily discriminated.Whereas young specimens of L. abyssicola have a sharply angulated shell with a marked and somewhat truncated rectangular outline, young specimens of L. frielei have a slightly squared, somewhat rounded outline with the shell length and height almost equal.
Although our specimens diverge from the illustration by Allen and Turner (1974: 441, Fig. 35a), the photograph of the holotype (Fig. 1F) clearly agrees with our material.
The shell of one species from the Indian Ocean, Lyonsiella curta Poutiers, 1984, is very similar to that of L. frielei; however, because these taxa are from different oceans, it is very unlikely that they are the same species.(Jeffreys, 1881) (Fig. 2A-G)
Lyonsiella formosa: Allen and Turner (1974: 447-456, Figs. 43-49), Allen (2008: 80).Description: Shell extremely fragile, white (height 2 mm, length 2.5 mm), inequivalve, inequilateral, little inflated, umbones almost central, spiked, blunt, prosogyrate; outline rectangular, postero-dorsal margin almost straight, long, posterior margin truncated, corrugated; ventral margin divided by an axial row of spines that runs from the umbo to the ventral margin; the region between the posterior margin and this axial row is slightly concave, while the region between this axial row and the anterior margin is slightly convex and merges with the rounded anterior margin, antero-dorsal margin curving downward.Covered externally by radiating series of delicate spines.Each spine is a polyhedral column that tapers towards the distal end, which bears a stellate, usually hexagonal, structure.In addition, a series of very long and pointed spines covered by tiny triangular projections extends over the posterior and most of the central parts of the shell; each series of spines grades in size, with the smallest spines nearest the umbo.Each long spine is a hexagonal column with no stellate structure at its distal end.Hinges of both valves edentate.Muscle scars and pallial line hardly visible.Geographic range: Atlantic Ocean: northwest Atlantic: off Woods Hole (Allen, 2008), Gulf of Mexico (Jeffreys, 1881;Allen and Turner, 1974).Southwest Atlantic: Mid-Atlantic Ridge (Allen and Turner, 1974;Allen, 2008), Campos Basin, off south-eastern Brazil (present study).Northeast Atlantic: off Guinea-Bissau (Allen, 2008), off the Canary Islands, Bay of Biscay (Jeffreys, 1881;Allen and Turner, 1974;Allen, 2008), the Azores (Jeffreys, 1881; Allen and Turner, 1974).Bathymetry: from 638 m (Jeffreys, 1881) to 3783 m (Allen and Turner, 1974).
Remarks: This species is one of the most beautiful, rare, and fragile septibranch species studied here.Unfortunately, the only specimen collected was broken during the process of taking the SEM photographs.The fragmented shell is shown here (Fig. 2A, B).
This species has a controversial taxonomic history, and in our opinion, different entities have been treated as L. formosa.Jeffreys (1881: 930, pl. LXX, Figs. 1-1a) described Lyonsia formosa from the Atlantic Ocean, from depths of about 640-1134 m.Smith (1885: 72, pl. VI, Figs. 3-3b), although his study was based on material from the same depths and locality as Jeffreys' material, illustrated a quite different species assigned to L. formosa, which is herein termed L. formosa sensu Smith.Whereas in L. formosa the axial rib is smooth and disappears towards the ventral margin, in L. formosa sensu Smith, the axial rib is nodulose and continues with the same width from the umbo until it reaches the ventral margin, near the middle of the shell.Furthermore, in L. formosa sensu Smith there are about seven faint furrows, visible externally and internally, that extend obliquely to the anterior margin (see also Salas, 1996: 73, Fig. 102).Such structures are absent in L. formosa.Therefore, in our opinion there are in the Atlantic, at least two different species that have been treated as one.In fact, Locard (1898) attempted to evaluate the variation of characters in L. formosa, and even suggested the presence of two distinct forms (a bathyal and an abyssal form) in the Atlantic Ocean, although he did not elucidate the distinction between the two forms.Allen and Turner (1974) gave a detailed account of the anatomical characters and recognized this species as a member of the genus Lyonsiella, and also compared their material with Jeffreys' specimens.Poutiers (1984) obtained specimens similar to Lyonsiella formosa from the Mozambique Channel (11°44'S, 47°35'E, 3716 m).Although the exemplar illustrated by Poutiers (1984: 302, Fig. 9) resembles the illustrations of Allen and Turner (1974: 447-456, Figs. 43-49), Poutiers (1984) perceived anatomical differences from Allen and Turner's material, and, because of these differences, termed his species Lyonsiella cf.formosa.In addition to the anatomical distinctions between these materials, it seems biogeographically unlikely that specimens from the Indian and Atlantic oceans could belong to the same species.
The species termed Lyonsiella formosa by Morton (1984), who gave a detailed account of the functional morphology of material from Hawaii, is different from the Atlantic L. formosa.The specimen illustrated by Morton (1984: 285, Fig. 1a) has a very short postero-dorsal margin and an extended antero-dorsal margin pointing upwards, and the axial rib, which runs from the umbo to the ventral margin, is markedly acute.In addition, this record poses the same biogeographical problem mentioned above.
The record of L. formosa from Brazilian waters was given by Allen (2008), based on a record from Allen and Turner (1974) for the Mid-Atlantic ridge (sta.155: 00°03'S, 27°48'W; sta.156: 00°46'S, 29°28'W).It is clear to us that different taxa were treated under the same name, and that this situation calls for a species revision in the future.Poutiers and Bernard (1995: 169) discussed the generic placement of this controversial species and, like them, we also refrain from adopting any nomenclatural changes until this situation is clarified.We have therefore chosen to treat our specimens as Lyonsiella cf.formosa.
Lysonsiella pipoca n. sp.(Fig. 2H-M) Description: Shell fragile, white, small (height 1-2 mm, length 1-3.5 mm), inequivalve, inequilateral, inflated, umbones prosogyrate, outline somewhat trapezoidal, postero-dorsal margin descending, forming an angle of about 90 o with postero-ventral margin; a marked indentation of the postero-ventral margin may be present and vary in strength; anteroventral margin rounded, slightly merging with the antero-dorsal margin, which is more or less projected below the umbo and forms a short indentation.Ornamented externally with a series of tiny pyramidal projections, more concentrated near the umbo.A few elongated and very delicate projections may be present over the rest of the shell.Irregular concentric growth lines present.One fine, raised thread runs from the ventral margin to the umbo, but does not reach it.Hinges of both valves edentate.Muscle scars and pallial line hardly visible.
Etymology: This species has been named in relation to its white colour and billowing appearance, which resembles popcorn.Pipoca is a Portuguese word for popcorn that originates from Tupi, the native language of most Brazilian indigenous peoples.The name is employed as a noun in apposition.
Remarks: Lysonsiella pipoca n. sp. may show some variation in outline, mainly in the strength of the indentation at the postero-ventral and antero-dorsal margins.On the postero-ventral margin, the strength of the indentation is a result of the variation in the billowing appearance of the shell, and on the anteroventral margin the strength of the indentation is a direct result of the level of projection of this margin.
Lysonsiella pipoca n. sp.can be distinguished from any other congener in the Atlantic Ocean by its characteristic billowed inflation and somewhat trapezoidal outline.The only species that resembles Lysonsiella pipoca n. sp., although placed in a different genus, is Policordia laevis Allen and Turner, 1974.As the definitions of these genera are not clear-cut, we compare the species here.Both species share the general trapezoidal outline, but P. laevis has a sub-central umbo, gently curved posterior margin, and the postero-dorsal margin is little extended and projects slightly more than the postero-ventral margin; whereas in L. pipoca n. sp. the umbo is strongly prosogyrate, the posterior margin is almost straight or slightly sinuous, and the postero-ventral margin is quite extended and more projected than the posterodorsal margin.Moreover, as in all the species in the genus Policordia, P. laevis is devoid of spines or pustules, whereas very small and/or elongated projections are present in L. pipoca n. sp.
Remarks: This species varies greatly in outline, and no clear limits can be established among allegedly distinct taxa.There are several differences among the specimens, including the number of axial threads, the convexity and extension of the posteroanterior margin, the angle formed by the margins, and the strength of the umbo.Certainly, samples of only a few specimens may be classified erroneously, and because of the large number of specimens ex-amined for the present study, it is clear to us that establishing consistent differences among populations is an almost impossible task.Thus, from the conchological point of view, only one species, P. gemma, can be recognized here.Allen and Turner (1974: 478) indicated the difficulty in distinguishing three species, P. gemma, P. densicostata (Locard, 1898), and P. atlantica Allen and Turner, 1974, using shell characters alone.They suggested a classification based on an additional diagnostic character, i.e. the appearance of the radiating lines, because these lines can be slightly raised in P. gemma and P. densicostata, or shallow furrows in P. atlantica.It is difficult to discriminate these species on the basis of this character.Our specimens have raised lines.Allen (2008) recorded this species from the Brazilian Basin, analyzing the same stations as Allen and Turner (1974); however, Allen and Turner (1974) recorded P. gemma from the Mid-Atlantic ridge (sta.156: 00°46'S, 29°28'W), which is far from the Brazilian coast.In addition, Allen (2008) reported the occurrence of this species in the Angola Basin, but this record is not corroborated by the stations he listed in Appendix 3 (p. 163-169).Therefore, until this point can be clarified, this occurrence must be viewed with caution.
Remarks: Policordia gemma shows a great variation in outline, but Policordia sp.does not fit into the range of this variation.Policordia sp. has a larger umbo, a noticeably more convex valve, a slight indentation on the posterior margin, and more axial threads than specimens of P. gemma of the same size.
Although Policordia sp. is probably new to science, to avoid an increase in unwarranted, closely similar species, a formal description is delayed until enough specimens are collected to allow us to evaluate the possible variation and limits of Policordia sp.

GENERAL REMARKS
One kind of external ornamentation, a spine with a stellate structure near its distal end, is present in almost all the species of Lyonsiella treated here.This structure was observed in verticordiids from Cam-pos Basin, and may reinforce the affinities between Verticordiidae and Lyonsiellidae.
Another kind of ornamentation, an ornamented pointed spine with no stellate structure at the distal end (Fig. 1E), is present in Lyonsiella cf.formosa.Such a structure has not been observed for any Lyonsiella species.Lyonsiella pipoca n. sp. is unique among the genera and species examined here because it does not have spines with a stellate structure.Policordia, typically for the genus, has no spines or pustules, but rather raised axial threads.
Because the shell ornamentation is an important character in pelecypod taxonomy, the typical shell ornamentation of the species treated herein may contribute to the discussion on the monophyly of lyonsiellids (e.g.Dreyer et al., 2003).

Table 1 .
-General characters of the species of Lyonsiella and Policordia.H, height; L, length.