Observations on the Anatomy of the Scaphopod Mantle and the Description of a New Family, the Fustiariidae

20 Pages·1991·11.2 MB·English

by  Gerhard Steiner

Observations on the anatomy of the scaphopod mantle and the
description of a new family, the Fustiariidae
Gerhard Steiner
Institute of Zoology, University of Vienna, A-1090, Vienna, Austria
Abstract. The mantle offive generaofthe order Dentaliida andten generaofthe orderGadilida are investigated using histological and ultrastructural
methods. Theanteriormantleedgeisdividedintothree functionalunits: 1)afrontal epithelium; 2)acentralfold; 3)an innergland region. Inthe Dentaliida
thefrontalepitheliumisdifferentiatedasanouterglandregionandthecentral foldcarriesanannularciliaryorgan. Rhabdusrectius(Carpenter)(Dentaliida)
hasapairofciliatedslitsinsteadoftheannularorgan. NeitherfeatureisfoundintheGadilida, wherethefrontalepitheliumformssensorypapillae. Different
types ofciliary receptors in the anterior mantle edgeofboth orders are present. The innergland region in the Dentaliida consists ofepithelial gland cells
only; in the Gadilida both epithelial and subepithelial gland cells are present. The epidermis ofthe pallial cavity is low cuboidal but features ciliary rings
in the anal region.
Theposteriorpallial edgeorpavilionofthegadilidshasapowerful ciliary organtoproducewatercurrentsandciliated ridgesonthedorsal mantle process;
both structures are lacking in the dentaliids. Fustiaria differs from other genera ofthe Dentaliida by lacking a ventral bolster ofconnective tissue at the
posterior mantle margin. Abundance and distribution ofsubepithelial gland cells vary between genera. The validity ofthe family Rhabdidae is supported
and a new family, the Fustiariidae, is proposed.
The anatomy ofthe Scaphopodahas receivedthe least Boissevain (1904) described the posterior mantle edge, the
attention of all of the classes of the molluscan subphylum so-calledpavilion, and reportedasmall ciliatedareaandscat-
Conchifera. Early accounts, e.g. Deshayes, 1825; Lacaze- tered gland cells. Reynolds (1988) investigated sensory cells
Duthiers, 1856-7; Fol, 1889; Plate, 1892; and Simroth, 1894, fo the pavilion ofRhabdus rectius (Carpenter) (Dentaliida).
however, contained excellent studies of scaphopod This paperpresents acomparativeanatomyofthe man-
morphology andhistology that remain valid in manyaspects. tle in selected membersoftheorders DentaliidaandGadilida
Although almost all investigations were made on a single (= Siphonodentaliida) todemonstrate the anatomical divers-
genus, Dentalium (=Antalis) (order Dentaliida), the results ity in Scaphopodaand toprovide new information for a bet-
have been generalized subsequently for all Scaphopoda. ter founded classification.
Lacaze-Duthiers(1856-7), Plate (1892), andBoissevain
(1904) described the histological structure of the mantle in MATERIALS AND METHODS
Antalis enlalis (L.). They noted an outer glandular region
at the anterior mantle edge, including two to three types of ThespeciesstudiedarelistedinTable 1. Mediterranean
gland cells, a ring ofconnective tissue supporting the man- species were collected by means ofSCUBA or by a triangle
tle opening, and an inner glandular region consisting of dredgefrom 8-20m in Rovinj and Piran (PeninsulaofIstria,
mucus-producing cells. Plate (1892) found that the genus Yugoslavia). In Norway, animals were gathered by a "Mini-
Cadulus lacked the outer gland region, and later Odhner Sanders" epibenthic sledge and box-core sampler from
(1931) confirmed. Boissevain (1904) reportedaringofciliated 120-590 m in the fjords near Blomsterdalen, Bergen. The
cells between the gland regions that she considered to be a animals from Puget Sound, Washington, U.S.A., were col-
sensory organ. Gabeand Prenant (1950) includedtheanterior lected with a triangle dredge from 75-100 m near Waldrun
mantle edge ofA. entalis in their histological studies ofthe Island.
scaphopod connective tissue.
In the midregion of the animal, ciliated ridges were HISTOLOGICAL PREPARATION
foundjust anterior tothe anal opening inAntalis entalis and Living animals were narcotized with isotonic MgCL
A. dentalis (L.) by Lacaze-Duthiers (1856-7) and Fol (1889). solution (1:2 to 1:1 with sea-water) or MS 222 added to the
Distaso(1906) described them in moredetail and alsoclaimed sea-water(1:4000 - 1:2000). Tissues were fixed in2-4% for-
the presence ofan osphradial sense organ. Leon (1895) and malin or 4% glutaraldehyde buffered in sea-water. Helly's
American Malacological Bulletin, Vol. 9(1) (1991):l-20
1
2 AMER. MALAC. BULL. 9(1) (1991)
Table1. Systematiclistofthespeciesexamined (USNM, UnitedStatesNa- fixative producedgood fixationofcytoplasmatic components
tional MuseumofNatural History, SmithsonianInstitution; NMNZ, National in small specimens and pieces oftissue. Bouin's fluid (aq.)
Museum ofNew Zealand; 'Museum National d'Histoire Naturelle, Paris; penetratestissues rapidly, decalcifies, butoftendamagedcilia-
2GarethDavies, UniversityofEdinburgh; 'ZoologiskMuseum,Kopenhagen;
*prepared for TEM methods) tion. This fluid was used also for decalcification after one
oftheother fixatives. Fixation times ranged from2-24h. The
Order DENTALIIDA specimens were washed in 70% ethanol + NH4 (3
Family Source
drops/lOOml) to remove thepicricacid. Afterdehydration in
Dentaliidae ethanol, tissues were transferred to methyl benzoate as an
Dentalium laqueatwn Verrill, 1885 USNM 765278 antemedium, benzol, 40% paraffinand embedded in58-60°C
D. neohexagonum Sharp and Pilsbry, 1897 Monterey Bay
Graptacme calamus (DalI. 1889) USNM 801250 Paraplast. Sections of 5-7 [an were taken and stained with
Antalis dentalis (L., 1767) Rovinj* Azocarmine and Anilineblue-Orange G after Heidenhain
A. entalis (L., 1758) MB12 (AZAN), Haematoxilin and Eosin after Mayer (HE) or
A. inaequicostatum (Dautzenberg. 1891) Piran*
A. occidentalis (Stimpson, 1851) Bergen, Norway* Kernechtrot + Picroindigocarmine (KP). Recipes for
A. vulgaris (Dacosta, 1778) Rovinj fixation and staining were modified after Adam and Czihac
AA.. sspp.. BPS926760II NNMMNNZZ BP9S26760II (1964). Museum samples, usually kept in alcohol, were
A. sp. 930 NMNZ P930 treated in the same way starting with decalcification or
A. sp. Q 719 NMNZ 0719 dehydration.
Fissidentalium candidum (Jeffreys, 1877) AT 1862
F. majorinum (Mabille and Rochebrune, 1889) USNM 709081 SEM PREPARATION
F. megathyris (Dall, 1899) Galathea Sf7163
F. zelandicum (Sowerby, 1860) NMNZ BS496 The same fixatives were used as for histological pur-
FFusstpi.aria rubescens (Deshayes, 1825) PNiMraNnZ sand lagoon ppoosienst.dTriisesdueswiwtehrelidqeuhiyddrCat0ed ianngdrasdpeusttoefracceotaotneed, cwriittihcala
RhabRdhiadbadeus rectius (Carpenter, 1864) San Juan Islands 200 A gold-layer. The samples2 wereexamined inaJeolJMS
USNM 678797 09 scanning electron microscope.
Laevidentaliidae
Laevidentalium callipaplum (Dall, 1889) USNM 765451 TEM PREPARATION
Entalinidae Two methods were applied as follows: 1) 4 hr in 3%
Entalina quinquangularis (Forbes. 1843) Thalassa Y 378' glutaraldehyde in phosphate buffer 0.1M pH 7.2-7.4 (after
Bergen, Norway*
Bathoxiphus ensiculus (Jeffreys, 1877) Incal WS 01' Sorensen) or cacodylate buffer 0.1M pH 7.2; postfix for 2
B. sp. S 153 NMNZ S153 hr in 2% Os04 0.1M in the corresponding buffer. To 100ml
Heteroschismoides subterfissum (Jeffreys, 1877) Nordatlante 85 0.1M buffer, lOg sucrose were added to adjust the osmolar-
ES 2182
ity for sea-water. 2) 2 hr fixation in glutaraldehyde-
PulsePlullisdeaellum lofotense (M. Sars, 1865) Bergen, Norway* paraformaldehyde (1% formalin + 2.5% glutaraldehyde in
P. salishorum Marshall, 1980 San Juan Islands 0.1M cacodylate buffer pH 7.2) and postfix for 2 hr in 2%
APP..nnssuppl..ipPBuSl9s39e74l0lIum euzkadii Scarabino, 1986 BNNIMMONNGZZASBP9SIV39,740DIS631 OEtsh0yl4einn dthieamsianmeetbeutfrfaera.ceAtlilcfaixcaitdive(sEDwTerAe)cwoaosledusteod4°fCo.r
Striopulsellum sandersi Scarabino, in lit. Nordatlante P19' decalcification. Afterdehydration inethanol the samples were
Siphonodentaliidae embedded either in Epon-Araldite (Mollenhauer, 1964) or in
Siphonodentalium grandis (Verill, 1884) Incal WS 02' Spurr's medium (Spurr, 1969). Semi-thin sections (0.5-1 /mi)
SSS... slvpoietbcratetaubumimlMi(s.SoVweSreairrlsbl,y,,118815881650) GIEnrSce1ae6ln4lD.2SEx0p9.' 423 7w0e-r8e0sntaminweedrweimthad0e.1o%ntaolRueiidcihneertblOuMeUso-l3utimoinc.rSoetcotmieonwsitohf
Wemersoniellidae glass or diamond knives, and treated for 45 min with a
Wemersoniella tumerae Scarabino, 1986 Incal WS 07' saturated uranyl-acetate solution (Watson, 1958) and for5 to
Gadilidae 8 min with a0.4% solutionoflead-citrate (VenableandCog-
Gadilafraseri Nickles. 1979 Galathea St. 1013 geshall, 1965). Sections were studiedunderaZeiss EM9/S2
G. metivieri Scarabino, in lit. BIOGAS V, DS66'
G. sp. NMNZ P939 transmission electron microscope.
Cadulus aberrans Whiteaves, 1887 Monterey Bay
C. arctatus Jeffreys in Locard, 1898 Thalassa Z 407' RESULTS
C. cylindratus Jeffreys, 1877 ES 272
CC.. jdeeflfirceaystiul(uMsoSnutteerro,sa1t9o1,3 1875) BNIMONGZASBSV,54D4S66' ANTERIOR MANTLE EDGE
C. propinquus Sars, 1878 BIOGAS VI, DS82'
GENERAL CHARACTERISTICS
C. subfusiformis (M. Sars, 1865) Bergen, Norway*
C. sp. 68 USNM 803468 The anterior pallial opening is supported by a ring of
C. sp. P927 I NMNZ P927 I cartilage-like connective tissue as well as by muscles. It can
STEINER: SCAPHOPOD MANTLE ANATOMY 3
per
Fig. 1. A. Scaphopodinaschematiclongitudinal section; B. AnteriormantleedgeintheorderDentaliida(e.g. Antalis, semischematic longitudinal section;
C. Anterior mantleedge in the orderGadilida (e.g. Pulsellum), semischematic longitudinal section; D. Posterior mantle edge in the order Dentaliida (e.g.
Antalis), semischematiclongitudinalsection, insert(nottoscale)showingcross-sectionofthepavilionproper;E. PosteriormantleedgeintheorderGadilida
(e.g. Entalina), semischematic longitudinal section, inserts (notto scale) showingcross-sectionsofthe pavilionproperandthe valveciliary organ (ciliation
drawnon leftsideonly); a, anus; ae, attachmentepithelium; as, annular sinus; be, buccal cavity; ca, ciliated area; cf, central fold; clc, ciliated ledge cells;
co, ciliaryorgan; ctr, connectivetissue ringwithperiostracal groove; drm, dorsal retractor muscle; e, esophagus; f, foot; fe, frontal epithelium; go, gonad;
i, intestine; ig, inner gland region; 1, lacunae; lc, ledge cells; lm, longitudinal muscles; mc, mantle cavity; mo, mouth opening; n, nerve; nm, neuropil;
og,outerglandregion; per, preanalciliaryridges;pp, pavilionproper; rm, radial muscles; s, socketofconnectivetissue;sm, sphinctermuscle; smg, supramarginal
groove; st, stomach; vb, ventralbolster; vco,valveciliaryorgan;vm, valvemuscle; x, identifiesaxisofcross-sectioninlowerinsertofE;scalebars = 100fim.
4 AMER. MALAC. BULL. 9(1) (1991)
exhibitdifferentglandregions. The wholecomplex (see Figs. Towards the anterior aperture, collagen and muscle
1A-C, 2) can be divided into: 1) a frontal epithelium; 2) a fibers become more abundant, replacing the extracellular
central fold; 3) an inner gland region. matrix. Thus, thecartilage-likeappearance islost (Figs. 2,4).
In all scaphopods the central fold consists of a ring This ring provides an attachment site for the pallial
ofconnective tissue and the muscle apparatus. The former muscles on both proximal and distal sides. The periostracal
is a wedge-shaped mass ofextracellular matrix in which col- grooveofthe outer mantleepitheliumhasthe shapeofacon-
lagen and scaffolding fibers (fibers grillage'es) are embedded centric ring. Thus, constant shape and diameter are main-
(Gabe and Prenant, 1950) (Fig. 3). The orientation of the tained by connective tissue for the shell-forming epithelia.
fibers is predominantly radial. The term "cartilage-like" in- In fixed animals the anterior mantle margin is always
dicates the histological and functional resemblance of this retracted, so the groove opens to the anterior (Figs. 1, 4).
tissue to vertebrate cartilage; it does not indicate homology. Towards the anterior aperture the central fold includes a
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Fig. 2. inaequicostatum, anterior mantle edge in longitudinal section (formalin. AZAN, 7 jon); note the well developed fibrous connective tissue
(asterisk); ctr, connectivetissue ring; f, foot; og, outergland region; pg. periostracal groove; rm, radial muscles; sm, sphincter muscle; innerglandregion
(arrow); scale bar = 100 nm. Fig. 3. Fustiaria rubescens, cross-section ofthe connective tissue ring in the anterior mantle edge (Bouin, AZAN, 7 /xm);
note the homogeneous intercellular matrix, where radially arranged collagen fibres (arrows) are embedded; ome, outer mantle epithelium; scale bar
= 10jtm. Fig. 4. Antalisdentalis, longitudinal sectionofthe outer gland region showing the different types and sizes ofsubepithelial gland cells (Bouin,
AZAN, 7tan); ctr, connectivetissue ring; pg, periostracal groove; scalebar = 25urn. Fig. 5.Antalisdentalis, TEM micrographoftheoutergland region
in longitudinal section(glutaraldehyde-Os04, Epon-Araldite); thesubepithelialglandcellcontainsgranulesofvariousdensityandwithsubstructures; scale
bar = 1 /an.
STEINER: SCAPHOPOD MANTLE ANATOMY 5
sphincter muscle that can regulate the width ofthe opening cell, electron density of the vesicles can vary.
(Fig. IB). Radially arranged dilator muscles function as In longitudinal section the anterior mantle margin is
antagonists and longitudinal fibers beneath the inner somewhat triangular. In the Dentaliida the tip representing
epithelium pull the fold back into the mantle cavity (Figs. the pallial orifice carries the section of an annular ciliary
1B-C, 2). Other muscle fibers from the mantle are attached organ (Figs. IB, 6). A ringof5-6 (Fustiaria) or6-8 (Antalis)
tothebase ofthe supporting ring to retract the entire organ. rows ofprismatic, multiciliary cells (Fig. 7) lines the lumen
The dorsal regionofthe organ is innervated by a pair oftheopening, especially ifthelatter iscontractedorclosed.
of cerebral nerves, the ventral portion by a pair of pleural The nuclei are found in the proximal half of the cell, and
nerves. Presenceanddifferentiationofglandcellsandsensory frequently a large nucleolus is present. The cytoplasm is
receptors differ within and between the orders. packed with mitochondria. Kinocilia of 15 length show
the common 9x2+2 pattern and a basal plate. A striated
DENTALIIDA rootlet (banding 56nm) is attached to the basal body at an
In the order Dentaliida all three components of the angle of25° totheciliary axes. Themembranes ofneighbor-
anterior mantle margin are developed. A detailed descrip- ingcellsare strongly interdigitatedandareconnectedtoeach
tion representative for most dentaliid genera is given for other by desmosomes at or close to the apex.
Antalis, the genus with three species available for TEM Theciliaryorgan wasfound inall Dentaliidaexamined
studies (Table 1). Fustiaria (= Pseudantalis) rubescens except for Rhabdus rectius (Carpenter). Here, instead, two
(Deshayes); for nomenclatural considerations (see Emerson, dorsolateral slits are formed by the epithelium ofthe distal
1951, 1952) is the only species for comparison on the outergland region (Figs. 8, 9, 10A). The floorofthese more
ultrastructural level. Light microscopical differencesbetween or less tubular invaginations is covered by cells resembling
the other genera are listed in Table 2. epithelial cells, whereasthe epitheliumofthe walls contains
at least two types of specialized cells (Fig. 10B):
FRONTAL EPITHELIUM 1) Highly columnar cells of 50 /im height with long
The frontal epithelium covers the vertical surface of microvilli, a nucleusclose tothebasal lamina, andcytoplasm
the anterior mantle margin facing the environment. In the that stains faint-blue with AZAN. These cells are arranged
Dentaliida it is identified as a glandular structure by the in two rows, one on each lateral wall, close to the bottom
presence ofsubepithelial gland cells. It is referred to as the of the slit.
outer gland region. Two types of epithelial cells can be 2) Columnar, sometimes very slender, multiciliary
distinguished: 1) "normal" epithelial cells of6-10/mi height cells 20-30 iim high forming similar rows right above type
withrelativelyelectron-densecytoplasmandabasallylocated 1. Their nuclei also lie basally, but take the red stain better
nucleus; 2) cells with less densecytoplasm anda lowerden- than those ofthe first type. The cytoplasm is less dense and
sity oforganelles. Thesecellsare most clearlydistinguished contains many evenly distributeddarkgranules. Apically, the
from type 1 by foldings of the basal membrance which basal bodies ofthe cilia appear as a line parallel to the cell
sometimesreachtheupperquarterofthecell body. Numerous membrane. These can be accompanied by gland cells that
small vesicles can be seen on either side ofthe membrane. could represent athird cell type. Histologically, theouterand
All cells arecovered with2-2.3 nm long microvilli andcon- inner gland regions are comparable to those in the other
nectedtoeachotherby desmosomes andtothe basal lamina members of the order.
by hemidesmosomes.
The subepithelial gland cells characterize the ap- RECEPTOR CELLS
pearance ofthe entire dentaliid anterior mantle margin and Theoutergland region andtheepitheliumofthe cen-
occur in two forms (Fig. 4): barrel-shaped gland cells of tral foldare markedby thepresenceofciliary sensory recep-
70-110 itm length can be distinguished from bottle- or flask- tors. InthethreespeciesofAntalisultrastructurallyexamined,
shapedcellsthatreachasfaras500itmdown intothe mesen- two types can be distinguished.
chyme ofthe pallia! edge. The latter communicate with the Type 1 (Figs. 11A, 12, 13), very abundant in Antalis
surfaceonlyby long, thinducts. Bothcell types havebasally spp., represents a swollen process ofa nerve cell. This sen-
located nuclei with large nucleoli. Inhistological sectionsthe sorycell is moreorlesscylindrical witha maximumdiameter
mucus stains from red to violet with AZAN and greenish between 2.4 (tm and 3.8 /xm. No nucleus was found. It is,
orange with KP. Frequently the cell contents are continuous therefore, thought to lie in the perikaryon ofthe nerve cells
withthe mucus layercoveringthe frontal pallial epithelium. in the underlying mesenchyme. Thedendritic processes were
In TEM sections the cell contents consist of spherical, traced only for short distances beneath the epidermis. The
membrane-bound vesiclesofabout 1 /xmdiameter. InAntalis cytoplasm appears electron lucent except for scattered
spp. they show asub-structureofstraightorcurved lines (Fig. neurotubules. Close to the epithelial surface several large,
5), which is absent inFustiaria rubescens. Within the same elongated mitochondria can be found. They adjoin the
6 AMER. MALAC. BULL. 9(1) (1991)
Fig. 6. Fustiaria albescens, SEM micrograph ofthe anterior mantle edge showing the ciliary organ; cfe, central fold epithelium; kc, kino-cilia; og, outer
gnoltaendthreegaibonu;ndsacnalceeboafrd=ark5/girma.nuFliegs.c7.loAsnetatloisthoeccciedllenatpailcise,s;TcEo,Mcemlilcsroofgrtahephciolfiatrhyeocrilgiaanr;ysocraglaenbianrcr=oss5-s^emc.tioFnig(.gl8.utRarhaalbddeuhysdere-ctOiuss0,4S,EEpMon-mAircarlodgirtaep);h
ofthe anterior mantle edge in dorso-frontal view; note the slit-like invaginations; pg, periostracal groove; scale bar = 300 ^m. Fig. 9. Rhabdus rectius,
cross-section ofthe anterior mantle edge with the dorso-lateral slits (formalin, AZAN, 7 /mi); f, foot; sm, sphincter muscle; scale bar = 250 urn.
centrioles of the sensory cilia. The number of cilia varies tures have been observed for one sensory cell. One 5-6 /xm
from 5 to25, but the higher number is morecommon. With longciliumis surroundedby 8 modified microvilli, so-called
a length of 2-4 fim, the cilia are shorter than those of the stereomicrovilli (Haszprunar, 1985; Salvini-Plawen, 1988),
ciliated epithelial cells ofthe central fold. The bases ofthe which arebasally connectedby a membrane. Many filaments
receptorsare slightly sunken in, although thecell apicescan canbeobserved withinthe stereomicrovilli, especially inthe
protrudeover the otherepithelial cells. Some scanning elec- region adjacent to the cilium.
tron microscographs reveal tapering cilia, suggesting reduc- In Fustiaria rubescens, type 1 is rare and pre-
tionofpairs ofmicrotubules towards the tip. Connections to dominantly found in the outer gland region. Type 2, the
neighboring cells are effected by desmosomes and septate collar-receptor, is more common and found mainly in the
junctions. epitheliumofthe central fold. Both receptortypes aresimilar
Type 2 representsacollar-receptor(Figs. 11C, 14, 15), in all aspects to the respective types inAntalis spp. Another
which is much lessabundant inAntalis spp. than inFustiaria kind of receptor cell, here termed type la (Figs. 11B, 16),
rubescens. The dendritic process is more slender than that appears inboth epithelial regions. It has adiameterofabout
oftype 1, measuring 1-2 /xmacross. One ortwocollarstruc- 1.5 to 2 fim and the cytoplasm is packed with ellipsoidal
STEINER: SCAPHOPOD MANTLE ANATOMY
zExnr
alargerbasal portionandathinprocesspassingbetweenthe
othercells to reach the surface (Fig. 2). Their contents vary
from violet to bright red with AZAN and greenish orange
in KR At present, it is not clear whether these cells are
epithelial or subepithelial. Apart from these, no subepithelial
gland cells were recognized in the inner gland region of
Dentaliida. The surface ofthe gland cells is partly covered
by ciliated epithelial cells with apically located nuclei (Fig.
17). These cells are attached to the basal lamina by very
Fig. 10.Rhabdusrectius. A. semischematiccross-sectionoftheanteriorman- slender processes only.
tle edge; scale bar = 300 jim; B. detail from A. showing the epithelium
ofthe dorso-lateral slit; scale bar = 200 /im.
GADILIDA
mitochondria (0.4 x 0.6 ^im). Apically, 4-5 cilia of normal Theanteriorpallial edge inGadilidahasthe samebasic
structure can be seen. A tiny rudiment of a rootlet inserts structureas indentaliids, buttheentireorgan has undergone
at the single centriole. differentelaboration(Fig. 1C). Theringofcartilage-likecon-
nectivetissue isgenerally notasextensiveas inthe Dentaliida.
INNER GLAND REGION In some species only a narrow band at the base of the
The inner gland region, a differentiation ofthe inner periostracalgroove isdifferentiated. Plate (1892) andOdhner
pallial epithelium, terminates the complex of the anterior (1931) notedtheabsenceoftheoutergland region inmembers
mantle edge proximal to the central fold. It forms a tube of ofthis order. The ciliary organ ofthe central fold is absent.
epithelial, mucus-secreting cells ofvariable extent, probably
dependingonthe stateofcontractionofthe underlying man- FRONTAL EPITHELIUM
tie muscles. Thebarrel-shapedepithelial glandcells (Fig. 17), Characteristic forthe gadilid frontal epithelium is the
measuring approximately 40-90x20x20 jim, are filled with elaboration of papillae. Their number is high in the repre-
densely packed vesicles of light- and electron lucent ap- sentatives examined ofthe families Entalinidae, Pulsellidae
pearance, which have the tendency to coalesce to a single and Wemersoniellidae. InSiphonodentaliidaeand Gadilidae,
droplet ofmucus. The nucleus is generally located close to however, papillae are more scattered. In Entalina quin-
thethinbasal lamina. Anothertypeofglandcells, restricted quangularis (Forbes), papillae are 15 and 20 /tm high.
to few specimens ofAntalis species only, is flask-like with Dependingonthe stateofcontractiontheconical protrusions
Fig. 11. Reconstruction ofciliary sensory cells ofthe anterior mantle edges. A. Type 1 ofAntalis; B. Type laofFustiaria; C. Type 2 (collar receptor) of
Antalis; kc, kinocilium; mv, microvilli; nt, neurotubules; sj, septatejunction; za, zonula adherens; scale bars = 0.5 /im.
8 AMER. MALAC. BULL. 9(1) (1991)
Fig. 12. Antalis occidentalis, SEM micrograph ofa ciliary sensory cell oftype 1 in the frontal epithelium ofthe anteriormantleedge; kc, kinocilia; scale
bar = 0.5 /im. Fig. 13. Antalis occidentalis, TEM micrograph ofa type 1 receptor in a longitudinal section (glutar-paraformaldehyde - Os04, Spurr); bb,
basalbody; bp. basal plate; m, mitochondrion; septatejunctions(arrows), zonulaeadherentes(arrow-heads); scalebar = 0.5nm. Fig. 14.Antalisoccidentalis,
SEM micrograph ofatype 2 receptor (collar receptor) ofthe frontal epithelium; scalebar = 0.5 /im. Fig. 15. Antalis dentalis, TEM micrograph ofatype
2micrreocfeipltaomrenitnsainloangsitteurdeioncaillisuemct(iaornrow(-ghleutaadr)a;ldsechayledeba-rO=s00.45, ^Empo.n-FAirga.ld1i6.teF)u:stnioatreiatrhuebetswcoensco,llTarEMstrmuictcurroegsr;apsch,osftaeretoycpielilaa(r=escteeprteoormiccerlloviinlltih)e;frdoenntsael
epithelium (glutaraldehyde - Os04, Epon-Araldite); bp, basal plate; m, mitochondrion; septatejunction (arrows); zonula adherens (arrow-head); scale bar
= 0.5 pm.
areeitherapproximately 30/xm apart, so theyareelaborated The frontal epithelium cells are rather flat - 3 jtm in
on a flat base of tissue close to each other (Figs. 18, 19). Cadulussubfusifonnis (M. Sars), 5fim inbothEntalinaquin-
Generally, papilladensity is highestclose to the mantle open- quangularis (Forbes)andPulseHum lofotense(M. Sars). The
ing and decreases towards the periphery. latter also possess vesicle containing cells which appear to
The transition from the frontal epithelium to the outer be epithelial gland cells.
mantlesurface is markedby acrestofconnectivetissue (Figs. An unsual tissue is located beneath the frontal epi-
18, 19). Theperiostracalgroove isvisiblesomedistancebelow thelium of Entalina quinquangularis. Being only about 15
the crest on the outside of the mantle. In fixed specimens ^im thick, this layer is poorly visible in histological sections
the frontal epithelium is sunken in, givingthe mantle margin (Fig. 19, x). The tissueconsistsofspherical, vacuolizedcells
the appearance ofa crater rimmed by the above-mentioned thatprovedtobe problematic in TEM preparations, because
crest. their contents, perhaps ofmucoid nature, were washed out.
STEINER: SCAPHOPOD MANTLE ANATOMY 9
Fig. 17. Fustiaria rubescens, cross-section ofthe inner gland region (Bouin, AZAN. 7 /an) showing epithelial gland cells; note the position ofthe nuclei
ofthe ciliatedepithelial cells (arrows); c, captaculum; n, pallial nerve; scale bar = 25 /im. Fig. 18. Entalina quinquangularis, frontal viewofthe anterior
mantleedgeinaSEM micrograph(glutaraldehyde-Os04, Spurr); notethe numerouspapillae; mc,openingofthemantlecavity; periostracal groove(arrow-
heads); rim ofthe "crater" (arrow); scale bar = 100/*m. Fig. 19. Entalina quinquangularis, anterior mantle edge in longitudinal section (Bouin, AZAN,
7/xm); notethelessvoluminousringofturgidconnectivetissue(ctr); f, foot; ig, innerglandregion; x, mucoidtissuelayer;papillae(arrow-heads); periostracal
groove (arrow); rim ofthe "crater" (asterisk); scale bar = 100 /im. Fig. 20. Entalina quinquangularis, TEM micrograph ofa frontal epithelial papilla in
longitudinal section(glutaraldehyde- Os04, Spurr); cp, sensory cell process; ciliumoftheapical sensorycell (arrow); scalebar = 1 //m. Fig. 21. Entalina
quinquangularis, ciliary sensorycell at thetipofapapilla (glutaraldehyde - Os04. Spurr); bb, basal body; m, mitochondria; scalebar = 0.5^m. Fig. 22.
pCraodcuelsusswsiutbhfunseiufroortmuibsu,lip;ittsecd, csitleiraeroycsileinusmor(y=scteellre(otmyipcero2v,ilcloulsl)a;r-rseccaelpetobra)rat=t0h.e5ti/pimo.fa papilla (glutarparaformaldehyde - Os04, Spurr); cp, sensory cell
AMER. MALAC. BULL.
10 9(1) (1991)
Delicate fibers of connective and muscle tissue fill the in- fromthe secretoryduct, arelocatedbeneaththebasal lamina.
tercellular spaces. Forother members ofthe family Entalini- Like other areas ofthe mantle cavity the inner gland region
dae, available from museum samples only, this tissue could is covered by a cuboidal epithelium. The form ofthe gland
not conclusively be found. cells, influencedby thepackingbetweenthebasal laminaand
thepallia! muscles, iscuboidaltohoneycomb-like. Frequently,
RECEPTOR CELLS they over- and underlay each other (Figs. 23, 24).
Although some type 1 receptorcells were found in the Staining with AZAN revealstwotypesofsubepithelial
frontal epithelium of Cadulus subfusiformis, the sensory secretory cells: one staining violet to red, the other taking
elements ofthe gadilid anterior mantle margin are found in no stain (Fig. 23). In TEM-sectionsboth typescontainsmall
the papillae. Each papilla carries one or more sensory vesicles that show tendencies to coalesce to larger secretion
processes of neurons (Fig. 20), whose perikarya lie in the vacuoles. A cell can be completely filled with a single,
connective tissue beneath. A connection betweena receptive membrane-bound droplet (Fig. 24). Electron density seems
process and such a perikaryon was not found. Nor was it to parallel the histological staining properties. The nucleus
possible to trace the process ofthe sensory cell beneath the with a large nucleolus usually lies near the base ofthe cell.
base ofthe papilla. The cytoplasm appears optically empty The cytoplasm surrounding the nucleus is rich in golgi
and only neurotubles can be seen orientated mainly in the complexes.
direction ofthecell axis. Two or more cilia (9x2+2 pattern) The proximal borderofthe gland region is formed by
protrude from the apex (Fig. 21). A basal plate and a single a few rows of epithelial gland cells. They are prismatic in
centriole form the anchoring apparatus. No rootlet is shape and stain in a faint blue or remain unstained with
developed, but small bundles offibers spread from the cen- AZAN. Unfortunately, this tissue is easily damaged by im-
triole to the surrounding mitochondria (Fig. 21). The mito- proper fixation, processing, or long storage; therefore, it is
chondria are elongted and measure about 1x0.4 ixm. Some usually not preserved in museum material. Table 2 lists the
similarity to the type 1 receptors of dentaliids is evident. characters of the anterior mantle margin for the examined
Papillae withcollar-receptorsappear in Cadulussubfusiformis genera.
(Fig. 22).
EPITHELIUM OF THE
INNER GLAND REGION
MANTLE CAVITY
The inner gland region in Gadilida is mainly formed
by subepithelial glandcells. Accordingly, thecell bodies, apart Mostofthepallial cavity is linedby flatepithelial cells.
Table 2. Characters ofthe anterior mantle margin: (++) abundant; (+) present: (±) scarce, few; (—) absent: (?) no information.
Frontal Epithelium Ciliary Organ Receptor Cell Types Inner Gland Region
subepith. epith. papillae "mucoid" cell slits 1 la 2 papil- subepith. mucoid dark
gland cells gland cells tissue rows lae gland epith. epith.
cells gland cells gland cells
Antalis ++ 6-8 +- t + +
Dentalium ++ 6-8 9 ? 7 +
Fissidentalium ++ 6-8 ? 9 ? +
Graptacme ++ 9 ? 9 7 +
Fustiaria ++ 5-6 ± + + +
Laevidentalium ++ + ? ? 7 +
Rhabdus + ( + ? 7 7 +
Entalina ± ++ + + + +
Bathoxiphus 7 ++ 7 7 9 7 ? + +
Heteroschismoides 7 ++ 7 7 9 7 7 + +
Pulsellum + ++ + t +
Annulipulsellum 7 ++ 7 7 7 7 + +
Striopulsellum 7 ++ 7 7 +
Siphonodentalium ? + 7 7 + +
Wemersoniella 7 ++ ? 7 + +
Gadila 9 + 7 7 + +
Cadulus + + + + +