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Statoconia Formation in Molluscan Statocysts

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Statoconia Formation in Molluscan Statocysts Scanning Electron Microscopy Volume 1986 Number 2 Article 48 6-22-1986 Statoconia Formation in Molluscan Statocysts Michael L. Wiederhold The University of Texas Health Science Center Christine E. Sheridan The University of Texas Health Science Center Nancy K. R. Smith The University of Texas Health Science Center Follow this and additional works at: https://digitalcommons.usu.edu/electron Part of the Biology Commons Recommended Citation Wiederhold, Michael L.; Sheridan, Christine E.; and Smith, Nancy K. R. (1986) "Statoconia Formation in Molluscan Statocysts," Scanning Electron Microscopy: Vol. 1986 : No. 2 , Article 48. Available at: https://digitalcommons.usu.edu/electron/vol1986/iss2/48 This Article is brought to you for free and open access by the Western Dairy Center at DigitalCommons@USU. It has been accepted for inclusion in Scanning Electron Microscopy by an authorized administrator of DigitalCommons@USU. For more information, please contact digitalcommons@usu.edu. SCANNING ELECTRON MICROSCOPY /1986/ll (Pages 781-792) 0586-5581/86$1.00+05 SE M Inc., A MF 0' Hare (Chicago), IL 60666-0507 USA STATOCONIAFORMATION IN MOLLUSCANSTATOCYSTS Michael L. Wiederhold*, Christine E. Sheridan, and Nancy K. R. Smith# Division of Otorhinolaryngology The University of Texas Health Science Center at San Antonio, and Audie L. Murphy Memorial Veteran's Hospital; Department of Cellular and Structural Biology The University of Texas Health Science Center at San .l\ntonio# (Received for publication March 05, 1986: revised paper received June 22, 1986) Introduction Abstract In all molluscs studied to date, gravity The gravity sensors of all molluscs phylo­ reception is mediated by bilateral paired stato­ genet i cal ly below the cepha l opods a re spherical cysts. The general form of the statocysts is organs called statocysts. The wall of the sphere that of a fluid-filled sac with ciliated ~echano­ contains mechanosensory cells v1hose sensory cilia receptor cells along its wall. The ciliated project into the lumen of the cyst. The lumen is surface of the receptor cells faces the lumen of filled with fluid and dense "stones", the stato­ the cyst. The gravitational stimulus is trans­ conia or statol iths, which sink under the in­ duced by the interaction of "stones" in the lumen fluence of gravity to load, and stimulate, those with the cilia of the receptor cells. Since the receptor cells which are at the bottom. The stones have a greater specific gravity than that statuconia of ~~ cal ifornica are shown_to be of the fluid, gravitational forces are norn.ally calcified about a lamellar arrangement or mem­ exerted on the receptor-cell cilia. In some branes. Similar lamellar membrane arrangements species, either a single stone or a concretion of a re seen within the rPceptor cells, and their many smaller stones exists, in which case the possible role in the formation of the statoconia mass is referred to as a "statol ith". In other is discussed. SEM of unf,ixed statoconia species, many individual stones move indeµendent• reveals plate-like crystallization on their ly under the influence of gravity, animal move­ surface. Elemental analysis shows a relatively ment and beating of the sensory cilia; in these high Sr content, which is of interest, since cases, the stones are referred to as "stato­ others have recently reported that Sr is required conia". In those statoliths made up of multiple in the culture medium of several laboratory­ adherent stones, the individual stones are also reared molluscs in order for the statoconia to referred to as statoconia. Thus, the term develop. "statoconia" is usually used to denote relatively small (1-50 µm diameter), independent paracrys­ talline elements. It will be the airn of this paper to review the literature suggesting differ­ ent sites and mechanisms of generation of these stones, as well as the emerging body of experi­ mental evidence pertinent to this problem. In order to put this material in perspective, the structure and function of various molluscan statocysts will first be reviewed. Materials and Methods Specimens of Aplysia californica were obtained from Pacific Bio- marine Laboratories, Venice, CA. Animals were maintained in the laboratory in artificial sea water (Instant key Words: Statocyst, statoconia, otoconia, Ocean), which lacks Sr (Bidwell et al. 1986). sensory receptor, gravity receptor, hair eel I, Specimens were either 20 - 30 grams (those cilia, Aplysia, calcification, strontium. illustrated in Figures 2, 5, 6, 8 - 10) or 75 - 125 grams (Figures 3, 4 and 7). For light and *Address for correspondence: transmission electron microscopy (TEM), stato­ Michael L. Wiederhold cysts were dissected free from live circumesopha­ Division of Otorhinolaryngology geal rings of ganglia and imtrersed directly into The University of Texas Health Science Center fixative. For the material for Figures 2, 5, 6 San Antonio, Texas 78284 and 8, the specimens were fixed for 4 hours with Phone No. (512) G91-6563 3% glutaraldehyde in 0.15M sodium cacodylate 781 M. L. Wiederhold, C. E. Sheridan, N. K. R. Smith buffer solution prepared with artificial sea examples counted) long cilia (approximately 12 µm water (Instant Ocean) (1,004 mOsm, pH 7.35). long, as illustrated in Figure 2 below). The Specimens were post-fixed in 1% osmium tetroxide statoconia are indicated schematically as ellip­ for 1 h, dehydrated in a graded series of etha­ soids. They vary from approximately 3 to 20 µmin nols and embedded in epon. diameter. The number of statoconia varies from Thick sections (1 µm) were cut at 10 - 20 µm only one in larval Aplysia (Bid~iell et al. 1986) intervals through the cyst and stained with 0.5% to as many as 1,000 in an adult (McKee and toluidine blue in 1.0% sodium borate for examina­ Wiederhold, 1974). The cilia all have the tion by light microscopy. For TEM, 90 nm sec­ typical morphology of motile cilia, possessing a tions were cut and stained with uranyl acetate central pair of microtubules as well as nine and Reynold's lead citrate. Thin sections were doublet microtubules arcund the periphery of the examined in a Philips 301 transmission electron cilium. In fact, these cilia are motile, as well microscope. Statoconia in Figure 8 were decalci­ as sensory, as will be discussed below. fied prior to dehydration by immersion in cacody- 1ate buffer ~,ith the pH adjusted to 5. 3 for 24 hours. For the thin section in Figure 7, fixa­ tion was in 2.5% glutaraldehyde in 250 r.iMof 2,4,6-trimethylpyridine (s-collidine) buffer (pH 7 .4) for 12 - 24 h. No additional decalcifica­ tion was performed. For SEMof whole statocysts (Figures 3 and 4), this same fixative was applied to an exposed statocyst still in the circumeso­ phageal ring of ganglia and the whole ring was fixed for 12 - 24 h. The cyst was then bisected and most of the statoconia washed out when these blocks were returned to the fixative. These specimens were dehydrated through a graded series of ethanols, followed by ethanol-amyl acetate solutions, critical point dried using liquid carbon dioxide, mounted on copper studs and coated with a 25 nm thick layer of 60/40 gold/­ palladium. These specimens were examined in a JEOL JSM-U3 SEMat 15 kV. For the SEMof i so- 1ated statoconia (Figures 9 and 10) statoconia Figure 1. Schematic drawing of Aplysia cal ifor­ were isolated into deionized water which was nica statocyst. Note that supporting cells blotted away, rinsed and blotted once more, on between receptor cells are not indicated. carbon planchets. The mounted specimens were Modified from Gallin and Wiederhold, 1977. coated with 60/40 gold/palladium at 20 nm thick­ ness and examined in a JEOL JSM 35 SEMat 20 kV. A more accurate picture of the Aplysia For elemental analysis, similarly prepared but statocyst is given in Figure 2, a cross-section, uncoated statoconia were examined in the same illustrating statoconia and receptor cells at the electron microscope using a Tracor Northern "bottom" of the cyst. Sections of many statoco­ energy dispersive X-ray detector and a Tracor nia are seen, as well as cilia on the lumenal Northern NS880 X-ray analysis system. surface of three receptor cells. The statoconia are ellipsoidal in shape, varying here from 5 x 2 Structure of Statocysts µm to 17.5 x 5 µm. Note several cilia. whose complete length of 12 µm can be seen. In live The general plan of molluscan statocysts preparations, it can he seen that the mass of will be described using that of Aplysia califor­ stones falls to fill approximately the bottom nica as an example, because it is representative one-third of the lumen. Note that the statoconia of the "simplest" form (Coggeshall, 1969; McKee appear to be free from one another. In other and Wiederhold, 1974). The statocysts are species (described below), the statoconia are paired, one being located between the pedal and held together to form a statolith. If a dissec­ pleural ganglia (parts of the ci rcumesophageal ted live Aplysia statocyst is rotated under a ring of ganglia) on each side of the animal. microscope, the statoconia can be seen to tumble Figure 1 is a schematic drawing of the organ. over one another as they fall to the new "bottom" Each statocyst is a sphere, approximately 200 µm of the lumen. Figures 3 and 4 are scanning in diameter. The wall of the cyst is made up of electron micrographs (SEM) of fixed, bisected a basal lamina surrounding thirteen large recep­ cysts and give an appreciation of the relative tor ce 11s. Each receptor ce 11 has its own axon size of the statoconia and the cilia. In Figure and these thirteen axons join to form the stato­ 3, most of the stones have been washed out, by cyst nerve, indicated schematically in the figure gentle flushing with fixative, to offer a better as proceeding to the right of the cyst.
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