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Extraordinary Flexible Shell Sculpture: the Structure and Formation of Calcified Periostracal Lamellae in Lucina Pensylvanica (Bivalvia: Lucinidae)

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Extraordinary Flexible Shell Sculpture: the Structure and Formation of Calcified Periostracal Lamellae in Lucina Pensylvanica (Bivalvia: Lucinidae) See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/261401849 Extraordinary flexible shell sculpture: The structure and formation of calcified periostracal lamellae in Lucina pensylvanica (Bivalvia : Lucinidae) Data in Malacologia · July 2004 CITATIONS READS 8 176 5 authors, including: John D. Taylor Melita Peharda Natural History Museum, London Institute of Oceanography and Fisheries 159 PUBLICATIONS 3,822 CITATIONS 96 PUBLICATIONS 1,035 CITATIONS SEE PROFILE SEE PROFILE Gregorio Bigatti Alexander David Ball Instituto de Biología de Organismos Marinos (IBIOMAR- CONICET) Natural History Museum, London 107 PUBLICATIONS 945 CITATIONS 50 PUBLICATIONS 266 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: SEM Microphotogrammetry View project Sclerochronology as a tool for detecting long-term Adriatic environmental changes - SCOOL View project All content following this page was uploaded by Gregorio Bigatti on 07 April 2014. The user has requested enhancement of the downloaded file. MALACOLOGIA, 2004, 46(2): 277−294 EXTRAORDINARY FLEXIBLE SHELL SCULPTURE: THE STRUCTURE AND FORMATION OF CALCIFIED PERIOSTRACAL LAMELLAE IN LUCINA PENSYLVANICA (BIVALVIA: LUCINIDAE) John D. Taylor1*, Emily Glover1, Melita Peharda2, Gregorio Bigatti3 & Alex Ball1 ABSTRACT The lucinid bivalve Lucina pensylvanica possesses an unusual flexible commarginal shell sculpture formed from calcified periostracal lamellae. The lamellae comprise thick, recurved, periostracal extensions with distal calcified scales. The periostracum is also densely embedded with calcareous granules around 2.0−2.5 µm in diameter and a thin (10 µm) layer of prismatic aragonite covers the ventral face of each lamella. Other species of Lucina in the western Atlantic possess calcified scales but with different morphologies and the continuous commarginal ridges of the eastern Atlantic Lucina adansoni and other Afri- can species are similarly constructed and homologous. The periostracal lamellae are a probable apomorphy of the genus Lucina and morphology of the calcified structures pro- vides a set of systematic characters of importance in the discrimination of species. Key words: Lucina pensylvanica, periostracum, calcification, shell growth, systematics. INTRODUCTION the homology of these as well as investigate their possible use as systematic characters. Detailed understanding of lamellar formation Lucina pensylvanica (Linnaeus, 1758) is one may also suggest hypotheses about their pos- of ten species of chemosymbiotic lucinid sible function. bivalves inhabiting intertidal and shallow Periostracal and extraperiostracal calcifica- subtidal habitats in the middle Florida Keys. tion is an unusual feature of bivalves but has Remarkably, the shell sculpture consists of been described in different forms from a vari- closely spaced commarginal lamellae, faced ety of families. Usually in Lucinidae the with triangular, calcareous scales that are periostracum is relatively thin (Harper, 1997), slightly flexible in live animals. The scales and although exceptionally the genus Rasta has a lamellae become brittle after death and in dense, shaggy periostracum extended into beach-collected shells the surface is white, numerous long pipes (Taylor & Glover, 1997). relatively smooth with low, thin, commarginal Prominent, sculpture-forming calcified ridges, sometimes with traces of periostracum. periostracum appears restricted to the genus Our initial observations suggested that both Lucina, of which L. pensylvanica is the type lamellae and scales were a form of periostracal species (ICZN, 1977). The morphology of the or extra-periostracal calcification, distinct from calcified scales has been used by Gibson- the normal shell. Because of the rarity of Smith & Gibson-Smith (1982) as a character periostracal calcification in bivalves in general to divide “Lucina pensylvanica” of the west- and the probable apomorphy of this character ern Atlantic into four separate species. for Lucina spp., we decided to investigate the Amongst other bivalve families, Veneridae, structure and formation of the lamellae in more such as Lioconcha and Callocardia possess detail and, if possible, determine the periodic- encrustations formed of fine aragonitic needles ity of their secretion. Additionally, we wanted projecting through the periostracum (Ohno, to compare the form of the periostracal lamel- 1996; Morton 2000); others such as lae between Lucina species, both to establish Granicorium and Samarangia secrete extra- 1Department of Zoology, The Natural History Museum, London SW7 5BD, United Kingdom 2Institute of Oceanography and Fisheries, PO Box 500, 21000 Split, Croatia 3Departado Biologia, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pab II, C1428EHA Buenos Aires, Argentina *Corresponding author: [email protected] 277 278 TAYLOR ET AL. periostracal calcareous cements to form a live animals were found at any bayside sta- crust of sediment on the shell (Taylor et al., tions. Animals were collected by extensive dig- 1999; Braithwaite et al., 2000). Many ging and hand sieving. Voucher specimens Anomalodesmata, such as Laternula and held in BMNH, London. Lyonsia, possess spines formed within the Live animals were fixed in 75% ethanol, 5% periostracum as do some Gastrochaenidae, seawater formalin or Bouin’s fluid. Tissue such as Spengleria rostrata (Spengler) (Carter samples were also fixed in 2.5% solution of & Aller, 1975). Amongst the Mytilidae, glutaraldehyde in phosphate buffer. Sections intraperiostracal aragonitic granules and pro- of mantle were stained with Mallory’s triple. jecting spikes have been described in For optical microscopy of the shell, geological Trichomya and Brachidontes (Carter & Aller, thin sections were made from fresh specimens 1975; Bottjer & Carter, 1980; Carter et al., embedded in resin. Pieces of the same em- 1990), while intra- and extraperiostracal cal- bedded shell were also examined by scanning cified structures are a feature of various spe- electron microscopy (SEM) after cutting, pol- cies of Lithophaginae (Carter et al., 1990). ishing and etching in EDTA. Little is known of biology of Lucina Shell sections were also examined by con- pensylvanica. Stanley (1970) demonstrated focal microscopy using a Leica SP NT in re- using x-rays that animals burrowed with the flected light mode. Simultaneous images were anterior part of the shell lying uppermost in collected at several different wavelengths, and the sediment, an unusual life orientation for a reference image was obtained with the trans- Lucinidae. The general anatomy was de- mitted light detector. We also carried out an scribed by Allen (1958) and Gros et al. (1996) initial test for autofluorescence using a wave- made a detailed description of the gill ultra- length (lambda) scan. The section was structure and chemosymbiotic bacteria. Addi- scanned at a single focal plane with each la- tionally, Taylor & Glover (2000) illustrated the ser in turn. The detector was programmed to large bipectinate mantle gills that lie alongside step through 25 pre-determined 10 nm-wide the pallial blood vessel. detection windows at wavelengths from 495− Lucina pensylvanica and its close allies are 750 nm that produced an intensity profile for often referred to in the literature under the each emission wavelength. This optimised la- generic name Linga. However, the name ser detector position and line. The best results should correctly be Lucina as Lucina were obtained with the 488 nm Argon laser pensylvanica was designated the type species and this was used for all subsequent imaging. of the genus in 1977 (ICZN, 1977). No autofluorescence was detected from within the shell matrix, so the first detector window was set at 486−507 nm. This wavelength gave MATERIALS AND METHODS a direct reflection image of the sample and was false coloured in green. Strong Lucina pensylvanica was live collected from autofluorescence from the periostracum was a number of oceanside intertidal and shallow detected at around 550 nm, so the second water sites in the Florida Keys during the In- detector window was set at 537−568 nm and ternational Marine Bivalve Workshop (IMBW) the images coloured red. A stack of 30 images in 2002 (Mikkelsen & Bieler, 2004, fig. 1 – was collected at ~0.4 µm intervals. Each frame map). Live animals were abundant only at Sta- was scanned three times and run through a tion IMBW-FK-642, mile marker 74.5 frame-averaging filter to reduce background (24°51.4’N, 80º43.7’W) on Lower Matecumbe noise. For single images, the z-axis (depth) Key. Here they occurred in low intertidal to data from the entire stack was combined and shallow, subtidal pockets of medium to coarse the brightest pixel from each point computed sand, located on a wide, coral-rock platform. and displayed (maximum projection image). The area was vegetated with patches of Thalassia and Halodule, as well as growths of Growth Periodicity Penicillus and Halimeda. Despite similar col- lecting effort, Lucina pensylvanica was much Twenty valves from live collected animals less common at other sites, such as Anne’s were used to study growth periodicity. We Beach, Upper Matecumbe Key (Station IMBW- embedded these in MET20 resin (Struers Ltd), FK-638) from Thalassia-covered sand and sectioned them transversely from the umbo Pigeon Key (Station IMBW-FK-657) in a tidal to the ventral edge. They were then ground, stream with Thalassia
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