Research Article |
Corresponding author: John D. Taylor ( j.taylor@nhm.ac.uk ) Academic editor: Richard Willan
© 2016 Emily A. Glover, John D. Taylor.
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:
Glover EA, Taylor JD (2016) Pleurolucina from the western Atlantic and eastern Pacific Oceans: a new intertidal species from Curaçao with unusual shell microstructure (Mollusca, Bivalvia, Lucinidae). ZooKeys 620: 1-19. https://doi.org/10.3897/zookeys.620.9569
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A new shallow water species of the lucinid bivalve Pleurolucina is described from Curaçao in the southern Caribbean Sea and compared with known species of the genus from the western Atlantic and eastern Pacific Oceans. Although confused with the Floridian species P. leucocyma, it is most similar to the eastern Pacific P. undata. As in all studied lucinids, the new species possesses symbiotic bacteria housed in the ctenidia. The shell microstructure is unusual with repeated and intercalated conchiolin layers that have sublayers of ‘tulip-shaped’ calcareous spherules. Predatory drillings by naticid gastropods frequently terminate at the conchiolin layers.
Bacterial symbionts, Caribbean, conchiolin layers, defensive adaptation, Lucinidae , Pleurolucina
The tropical and subtropical western Atlantic is one of the major centres of marine molluscan diversity and bivalves in the speciose family Lucinidae, with an estimated 46 species in this ocean, have been the focus of many studies since the discovery of their chemosymbiosis with sulphide-oxidising bacteria (e.g.
Pleurolucina (Dall, 1901) is a genus of small lucinids characterised by broad radial ribs. The type species, Lucina leucocyma Dall, 1886, first described from off the Florida Keys, is documented as having a distribution from North Carolina to Colombia including Yucatan Peninsula (
We describe this new Pleurolucina from Curaçao in comparison with other western Atlantic and Eastern Pacific species, detail its phylogenetic position and illustrate its unusual shell microstructure with calcified conchiolin layers.
Samples of the new species were collected in southern Curaçao – location below. Details of ctenidia and sperm were studied using critical point dried glutaraldehyde-fixed specimens. Shells, microstructure and anatomy were imaged using a Quanta FEI 650 FEG scanning electron microscope. Comparative shell material was studied in
Institutional abbreviations
Other abbreviations
H shell height
L shell length
LV left valve
PI protoconch I length
PII protoconch II length
RV right valve
SEM scanning electron microscopy
T tumidity single valve
Dallucina Olsson & Harbison, 1953. Type species, by original designation, Lucina (Here) amabilis Dall, 1898. Pliocene, Florida. Gender feminine.
Lucina leucocyma Dall, 1886, by original designation. Recent, western Atlantic Ocean. Gender feminine.
Shell small, L to 27 mm (P. sombrerensis usually less than 10 mm), subcircular to ovate, generally higher than long, inflated to highly inflated. Sculpture of 4–6 broad radial ribs separated by broad sulci, sometimes absent in adult shells, crossed by closely-spaced, often terraced, commarginal lamellae. Lunule deeply excavated to shallow. Ventral margin finely beaded. Hinge: RV with two cardinal teeth, posterior-most sometimes bifid, anterior and posterior lateral teeth present; LV with two cardinal teeth, anterior smaller, with anterior and posterior lateral teeth. Anterior adductor muscle scar relatively short, broad, separate from pallial line for about ½ to 2/3 of length, pallial line entire.
Western Atlantic: P. leucocyma (Dall, 1886), P. hendersoni Britton, 1972, P. sombrerensis (Dall, 1886). Eastern Pacific: P. leucocymoides (Lowe, 1935), P. taylori Coan & Valentich-Scott, 2012, P. undata (Carpenter, 1865).
Western Atlantic: northern Florida to Brazil (P. sombrerensis Espirito Santo,
Early Oligocene to Recent. Pleurolucina amabilis (Dall, 1898) is a distinctive, laterally compressed species from the Late Pliocene to mid-Pleistocene of Florida. It was made type species of the new genus Dallucina by Olsson and Harbison (1954) but other than the lateral compression it is similar in most characters to P. leucocyma. From Miocene deposits of Ecuador
Pleurolucina quadricostata (Dall, 1903) from the Pliocene Bowden Formation of Jamaica (
From morphological characters of the shells, Pleurolucina species are usually regarded as being related to Lucina s.s. or Cavilinga (
In the absence of molecular evidence, other than for P. harperae, our concept of Pleurolucina embraces a range of shell morphologies from species like P. leucocyma, P. undata and P. taylori that have prominent radial ribs, through the less ribbed P. hendersoni and P. leucocymoides, to the small P. sombrerenis that has a rounded shell lacking radial ribs. Nevertheless, they are all rather inflated with similar dentition, anterior adductor muscle scars and beaded inner margins.
Lucina
leucocyma
:
Pleurolucina
leucocyma
:
Holotype: 1 whole shell L 8.8, H 8.5 T 3.2 mm (
Paratypes: 92 valves (
19 ethanol preserved specimens (
Shell subovate, slightly anteriorly extended, L to 9.6 mm, H to 9.7 mm, H/L 0.99, moderately inflated, sculpture of flat, closely spaced commarginal lamellae, with four prominent, broad ribs with interspaces variable in width, but always narrower than ribs themselves; microsculpture of tight rows of shallow pits (Fig.
Pleurolucina harperae sp. n. A–C Holotype
General anatomy resembles most other described lucinids (Fig.
Pleurolucina harperae, general anatomy, ctenidia, bacteria, oocytes and sperm. A Right side, with mantle removed, right demibranch and extended foot stained with methylene blue L 7 mm B Left demibranch and foot, critical point dried preparation. Scale bar = 1 mm C Cut section to show general anatomy, stained with methylene blue L 8 mm D Transverse section through single ctenidial demibranch. Scale bar = 100 µm E Surface of bacteriocytes and intercalary cells on lateral view of a ctenidial filament. Scale bar = 15 µm F Spirochaete bacteria on surface of bacteriocytes. Scale bar = 2 µm G, H Symbiotic bacteria contained in bacteriocyte. Scale bar = 5 µm I Developing oocytes. Scale bar = 500 µm J, K Sperm. Scale bars = 5, 2 µm respectively. aa anterior adductor muscle bz bacteriocyte zone cz ciliated zone dg digestive gland f foot lp labial palps me mantle edge ov ovary with oocyctes pa posterior adductor r rectum rd right demibranch st stomach tm thickened mantle ventral to anterior adductor muscle.
The sperm of P. harperae were 9 µm long and 1.2 µm wide at the base, tapering and curved distally (Figs
Within a very thin (ca 1 µm) periostracum, Pleurolucina harperae has a basic four layered shell (Figs
Shell microstructure of Pleurolucina harperae. A Fractured section of shell margin showing major notch growth halt and conchiolin layer. Scale bar = 400 µm B Fractured section showing succession of shell layers. Shell exterior at top. Scale bar = 100 µm C Conchiolin layer with regular bands of spherulites. Scale bar = 40 µm D Individual spherulite. Scale bar = 2 µm E Adjacent spherulites embedded in conchiolin with narrow channels between layers. Scale bar = 5 µm F Single spherulites with channels below and above. Scale bar = 5 µm. cl crossed lamellar layer co conchiolin layer cp composite prismatic layer ip irregular prismatic layer p periostracum sp spherulitic prismatic layer.
Drill holes in Pleurolucina harperae produced by predatory naticid gastropods were observed with full penetration in 14 out of 114 single valves, but with 12 records of incomplete drill holes that terminated at an internal conchiolin layer (Fig.
Similar conchiolin calcified sheets were identified in Pleurolucina hendersoni (Figs
Shell microstructure of other species Pleurolucina hendersoni, P. undata, Lucina pensylvanica and Cardiolucina quadrata. A Pleurolucina hendersoni Guadeloupe, fractured section with prominent calcified conchiolin layer, periostracum at base. Scale bar = 20 µm B P. hendersoni, detail of conchiolin layer with lines of calcareous spherulites. Scale bar = 20 µm C Pleurolucina undata Baja California, fractured section with thin conchiolin layer Scale bar = 200 µm D P. undata, detail of conchiolin layer with spherulites. Scale bar = 20 µm E P. undata, single spherulites embedded in conchiolin. Scale bar = 3 µm F Lucina pensylvanica Florida Keys, calcified conchiolin layer. Scale bar = 20 µm G L. pensylvanica, single spherulite. Scale bar = 2 µm H L. pensylvanica, section of periostracum with calcareous granules. Shell interior to top. Scale bar = 20 µm I Cardiolucina quadrata Philippines, fractured section with conchiolin layer. Scale bar = 200 µm J C. quadrata detail of conchiolin layer with calcareous aggregates. Scale bar = 50 µm K C. quadrata detail of calcareous aggregate. Scale bar = 10 µm.
Pleurolucina harperae is an intertidal to shallow subtidal species collected from sand amongst seagrass rhizomes (largely Thalassia testudinum, Halodule sp.) in contrast to P. leucocyma that is usually recorded from deeper water, for example 30–180 m around the Florida Keys (
Southern Caribbean: Panama (
Named for Elizabeth (Liz) Harper, University of Cambridge, bivalve researcher, colleague and friend, who helped collect the new species.
Pleurolucina leucocyma (Fig.
Pleurolucina leucocyma. A–C Lucina leucocyma Dall, 1881 lectotype
Other less similar species are: P. hendersoni (Figs
Other Pleurolucina species. A, B Pleurolucina hendersoni Britton, 1972, exterior and interior of left valve Guadeloupe station GD 69 (
Pleurolucina is a genus of seven living species from the tropical to subtropical western Atlantic and eastern Pacific with none recognised from the eastern Atlantic or Indo-West Pacific. In that respect, it is similar to Radiolucina (
An interesting and unusual feature of Pleurolucina harperae is the repeated conchiolin sheets that are calcified with layers of embedded spherules. A model of conchiolin sheet formation in another lucinid genus, Cardiolucina, was proposed by
Conchiolin layers within the shell have been recorded in several bivalve families but those in the Corbulidae have attracted most attention because of the supposed resistance to predation by drilling gastropods evidenced by the high incidence of failed borings that terminate at the organic layers (e.g.
The field workshop in Curaçao was organized by Rüdiger Bieler as part of the Bivalve Assembling the Tree-of-Life project (bivatol.org) and supported by the U.S. National Science Foundation (NSF) Assembling the Tree of Life (AToL) program (award DEB-0732854 to RB and colleagues). We thank our colleagues at the workshop for logistic support especially Liz Harper and André Sartori for help with digging and sieving. Ellen Strong (