early larval shell development in mytilid bivalve mytilus

The malacological society of Japan

NII-Electronic Library Service

The malacologicalsociety of Japan

VENUS (Jap, jour, Mulac.) nkVol. 58, No.3 <1999): 119-127

Early Larval Shell Development in

Mytilid Bivalve Mytilus gaUoprovincialis

Emiko HAyAKAzE and Kazushige TANABE

Geological institute, University of lbkyo, 7iokyo 113-O033, Japan

Abstract: The early shcll rnorphogenesis of a mytilid bivalve M),tilus gattoprovincialis

Lamarck was studied by scanning electron microscopy, Larvue were taken at 1 - 1,5 hour inter-

vals after hatching until the early veliger stage. Trochophore larvae appeared within 16 hours

after fertilization at incubating temperatures between 15.0 - 18.2 OC.

They have the same pat-tern in the mode of formation er the prodissoconch 1 (Pd I). The Pd I began to build in the mid-

dlc trochophore stage. It was initially made of an ovul-shaped, fu11y organic univalved shell

(pellicle). The univalved organie shell developed further into a bivalved shape with a median

hinge line in the late trochophore stage. Calcification of the larval shell occurred in the early

veliger stage within 70 h()urs after fertilization. At this stage of development, the shell gland on

the dersal side secreted irregularly orientcd, needle-like spherulites undcrneath the pellicle. An

oval or low, cap-shaped, univulved shell observed in the eariy veliger larvae of the Bivalvia is

known to occur in the early stages of other molluscan groups such as the Monoplacophora,

Cephalopoda and Gastropoda, suggesting its synapomorphic nature amongst the Conchifera.

Keywords: M.vtilus galXoprovincialis, larval shell, development

Introduction

Embryonic dcvelopment and larval morphology of Bivalvia have been described in some edi-

ble and economically important spccies such as Ostrea edutis (Waller, 1981), Chlamys hastata

(Hodgson & Burke, 1988), Ai;gopecten pur;p"ratus (Bellolio et al,, 1993), and others (e.g. Rees,

1950; Loosanoff & Davis, 1963; Yoshida, 1964; Sastry, 1979; Cragg & Crisp, 1991). However, lit-

tle is known on the early development of the larval shell of Bivalvia, especially concerning onto-

genetic changes of shell structures and mineralogical cemposition. Most papers dealing with

bivalve larval shells have been fbcussed on the ecological and taxonomic aspects of the late veliger

stage (Loesanoff et al., 1966; Lutz & Hidu, 1979; Chanley & Diamani, 1980; Fuller & Lutz, 1989).

Only a few workers have described the morphology of living bivalves at early stages of devel-

opment (Ansell. 1962; LaBarbera, 1974; Waller, 1981; Bandel, 1988; Togo et al., 1993; Moueza et

at., 1999). These explained how the shell structure and mineralogical composition changed from

larval to post-larval stagcs. However, microstrucrural features of the shell gland and the primary

shell have not yet been sufficiently described.

in this study, these features were examined in a Japanese common mussel species by means of

optical and scanning electron microscopy and their phylogenetic implications were discussed.

Material and Methods

Sampting ofliving larvae:

Mytilus gallQprovinciatis Lamarck (Mytiliidae) that is

around the Japanese Islands, was used in this study. About

on February 22, 1996 at the intertidal zone of Nojima

distributed cornmonly in the waters

1OO mature individuals were collected

Canal, Yokohama City, Kanagawa




120 VENUS: VoL 58, No.3 (l999)

Prefecture, Gametes were samp]ed by the inducement method to abrupt changes in water tempera-

ture, Oocytcs and sperms were mixed in a small tank (20 liters in volume) and kept at daity meantemperatures of 17.4

"C for the first 20 hours after fertilization (temperature range: 17.0 - 18.2

OC)

and of 15.5 OC

thereat'ter (tcmperature range: 15.0 - 16,O OC).

Sixteen hours after fertilization liv-ing larvae were taken at 1 - 1.5 hour intervals for about 96 heurs.Scanni.ng electron nticroscopy:

Some living larvae of Ml gattoprovincialis were anacsthetised using 2-phenoxyethanol (WakoPure Chemicals Industries, Ltd.) buffered with sea water. The anuesthctised specimens could still

swim but did not retract the velum. This suggcsts that they swam using ciliary currents which were

unaffected by the nEurcotic agent.

All specimens were fixed with 6% glutaraldehyde-paraformaldehyde in O.2M cacody]ate bufferwith sea water at pH7.5, They were obscrved and photographed using an Olympus model AHBS-515 optica[ microscope. For scanning electron microscopy, specimens were cleaned twice with dis-tilled water and dehydrated through a graded series of ethanol. They wcre freeze-dried with t-butyl-

alcohol and mounted onto SEM stubs using a double-sided carbon tape. Specimens were coated

with p]atinum and then observed using scanning electron microscopes (Hitachi medel S-2400S and

model S-4500).

To ebserve the internal structure of the 1arval shell, selected fixed specimens of M. gatlo-provi.ncialis wcre cut using a razor blade. These fractured specimens were coated with platinumand observed with the SEM.

Laryal Development

Spawned oocytes develeped into trochophere larvae 16 hours after fertilization, and their mean

diumeter attained 60 pt rn (Fig. 1A), Two shallow invaginations on the opposite sidcs were observed

on each trochophore larva, one was the mouth primordium (blastopore) on the anterior side and theother was the shell field on thc posterior side. Each trochophore larva also possessed a prototroch,apical tuft, and telotroch. The apical tuft was about 30 um in length, The prototroch developedfrom the primary trochoblasts and encircled the mid-region of the trochophore larvae (Fig. IA-D).The telotroch occurrcd on the posterior apex of the trochophorc that beared a small tuft of cilia

(Fig, IB).

The trochophore larvae began to develop into the vc]iger Iarvae 66 hours aftcr fertilization (Fig.IE), Each veliger larva, about 70 ltm length, had a D-shaped bivalved shell in which the larvalbody was housed. The shell in the early veliger stage lacked apparent surface sculpture such as

gruwth lines, except for irregular elevations on thc apical portion. At 80 hours after fertilization, the

larva began to secrete an another type of the shell with commarginat growth lines termed the

prodissoconch II (Jablonski & Lutz, 1980) on the anterior side of the prodissoconch I (Fig. IF).

Mode of Laryal Shell Formation

As a result of scanning electron microscopy of 1arvae at different growth stagcs, the larval shelldeveiopment in Ml gaUopn)vincialis may be divided into the fo11owing five stagcs. The relationship

between developmental stages of the 1arval organs and the shell is summarized in Fig. 2.Stage I:

Prior to shell secretion. two invaginations began to appear on oppesite sides of the 1arval bodyin the early trochophore stage (Fig. IA). One of them had a crcscent shape with a relatively deepdepression, and the other was crater shaped with a shallow dcprcssion. Following the criteria of

Kniprath (1980), they are identified as the posterior shell field and the anterior blastopore (mouth




Hayakaze & Tunabe: Early Sheli Devclepmcnt of "dytil"s 121

Fig. 1. Seanning electron micrographs of 1arvae of Mr tilt{s galloprovincialis showing the successive stages

of larval shell development. Scalc bars = 1O um. Abbreviations: at. apical tuft; b, blastopore (future

mouth); h, future hinge line; p, prototroch; p1, prodissoconch I; p2, prodissocench II; sf, shell field;

tc, Lclotroch; vl, velum. A. Early trochQphore larva (16 hours after fertilization; stage I) with invagi-

nuted shell field (postcrior sidc) and blastopore (anterior side). B. Middle trochophere larva (41 hours after fertilization; stagc II) with evaginuting eval-shaped shell field on thc posterior side. C. Middlc trochophore 1arva (44 hours after fortilization; stage III) with evaginating latcral]y elongated

shell ficld. D. Late trochophore larva (47 hours after fertilization; stage IV) with developing

bivalved shell field, E. Early veliger larva (66 hours after fertilization; stage IV) with fully grown prodisseconch I, F. Middle veliger larva <91 huurs after fertilization: stage V) with D-shaped $hell

consisting of prodissoconchs I and II. A slight elevation associated with punctatc patterns (indicat- cd by an asterisk) and distinct divaricate striations can be seen on the prodissoconch I. An arrow

points to the prodissoconch IllI boundary.




l22 VENUS: VeL 58, No.3 (1999)

HOURS AFTERFERTILIZATION

24 48 72 96

Trochophore

------

Veliger

llIHIV

wwwwvakXXXXXXXNXXXXN""N"XtXNXXXXXXNXX)tXXXS

---------ny----------s-mt-flf-!/.iZV--------

c --

sasrmceww Early trochophore stage (prototroch, apical tuft)

t,N,,"",,N Late trochophore stage (telotroch, two invaginations)x4(ncrno Early veliger stage (vetum, prodissoconch 1)

- Middle-late veliger stage (prodissoconch l, prodissoconch lt)

jl: Stage 11 (an oval univalved shell secreted)

ltl; Stage lll (univalved shell developed to bivalves)

IV: Stage IV (hinge line occurred; prodissoconch l)

V: Stage V (prodissoconch ll appeared), C: Calcification started

Fig. 2. Relatienship between developmental stages and shell formation in larvae of Mytitus gaUny)rovin- ciatis examined.

primordia) respectively. The shell gland primordium did not secrete a shell in this stage.Stage IJ:

In this stagc of development, the central ponion of the shell field was distinctly evaginated and

covered with a primary shell consisting of a very thin organic sheet (pellicle), less than O.2umthick (Fig. 3B). The pellicle appeared 41 hours after fertilization. It was univalved with an oval out-

]ine, measuring about 10 - 15 um in lenger diameter.

Stage M:

Soon after stage II, the oval organic shell enlarged and covered about 30% of the larval body

(Fig. IC). The longer diameter attained about 30 um. There was no trace of a ca]cified structure

under the pellicle,Stage IV (prodissoconch I):

In the middle to late trochophore stage, a shallow t'urrow began to appear along the mid-line of

the elongated organic shell (Fig. ID). Along this 1'urrow, the shell was distinctly partitioned intotwo valves that were gently curved inward. The furrow was changed into the hinge line in the sub-

sequent early veliger stage. Hinge tccth and ligament were still undeveloped in the trochophore

stage. Thc bivalved larval shell in this stage of development is defined as the prodissoconch 1. Asdevelopmcnt proeeeded, the hinge area rapidly enlarged laterally, and the prodissocench I became

a typical D shape in the early veliger stage (Fig. IE). The full-grown prodissoconch I was 70 um

in length.

Threughout the trochophore and earliest veliger stages, the prodissoconch I lackcd apparent

growth lines (Fig, 1D) and censisted only of a very thin petlicle (Fig. 3A-B). Calcification of the

prodissoconch I started in the early veliger stage. Name}y, a thin calcified layer, about O.5 - 1,O ptmthick, consisting of aggregations of irregularly oriented, needle-likc spherulitic prisms, began to




Hayakaze & Tanabe: Early Shell Deyelupment of M.ytilus l23

Fig.3. Scanning electron micrographs of larvae of Mytilus galloprovineiatis showing thc larval shcll

microstructure. Abbreviations: pe, organic sheet (pellicle); ip. irregular prismatic layer. For other

abbreviations see the explantion of Fig. 1. Scale bars = 10 ptm (A, C & E) & 1 "m (B, D & F). A.

Late trochephure larva (47 hours after fertilization; stage IV) with dcvcloping bivalved shell field

(bf). p, prototroch. B. Close-up of the middle sheil field, showing a partly peeled very thin pellicLe (pe). C. Fractured dorso-ventral section of early veliger larva with prodisgoconch I (66 hours after

ferti]ization). D. Close-up of the middle shell portion or C, showing irregularly oriented spherulitic

prisms underneath the pellicle. E. Fractured slightly oblique dorso-ventral section of middle veliger

larva with prodissoconchs 1 and tl (7 days after fertilization). Slight elcvation associatcd with irreg-

ular punctate patterns and distinct divaricate striations are developed on thc apical rcgion and rim of

the prodissoconch I respectively. The prodissoconchs I III boundary is murked by a distinct demur-

cation furrow (pointed by an arrow). F. Close-up of the demarcated portion of C, showing the con-

tinuous arrangement of the spherulitic prismatic layer undcrncath pcriostracum.




124 VENUS: VoL 58, No.3 (1999)

appear undcrneath the preformed pellicle in the dorsal region of each valve (Fig. 3C-D). At this

stage of development, the upical shell portion had a slight elevation (Fig. IE). Distinct divaricate

striations were present at the rim ef the apical shell elevation and were cxtendcd te the margin ef

the prodissoconch I (Fig, 3E). These surface sculptural pattcms of the prodissoconch I were

described previously us "punctate-stellate

puttem" (Carricker & Palmer, 1979) or "pitted

and stel-

late-radial zones" (Waller, 1981).

Stage V (Prodissoconch ll):

After stage IV, the bivalved shell grew rapidly, and the two D-shttped valves became to contact

each other at the ventral margin. Then, the prodissoconch II with commiarginal growth lines began

to appear at the shell margin of the prodissoconch I. The boundary between prodissoconchs I and

II is marked by thc prcscncc of a shallow demarcation furrow (indicated by arrows in Figs. IF &

3E). As the shell growth proceeded, the calcified layer broadly covered the inner surft!ce of prodis-soconch Il (Fig. 3E). There was no discontinuity in the shell microstructurc at the boundary (Fig.3F).

Discussion

EarL>' development qf the larvat shelt

As a result uf this study, it was realized that in M. galloprevincialis, trochophore larvae devel-

oped two invaginations on the anterior and posterior sides of the body, They correspond respec-

tively to the mouth primordium (blastopore) and shell field, The invaginated shell field and mouth

have been described in trochophore larvae of the same species from southern France (Kniprath,1980), S()isLfta sotidissin'ta from the north Atlantic coast in Massachusetts (Eyster, 1986) and

Anom.alocaidia brasiliana from the tropical mangrovc swamps of western Atlantic (Moueza et al,,

1999). These lines of evidence indicate that the development of an invaginated shell field and

mouth in the trochophore larvae is a common feature in the Bivalvia.

Our SEM observations revealed that the trochophore ]arvac of M. galloprovinc'iatis first secret-

ed a univalved, elliptical-shaped orgttnic shell (Fig. IB). A similar oval-shaped univalved organic

shell wus figured in larvae of the tridinid c]am, 71eredora malleotus from the Mediterranean Sea

(Bandel, 1988) and the tropical mangrove clam A. brasiliana (Moueza et aL, 1999), Bande] (1988)regarded those of the fbrmer species as abnormal larval shells, but they apparently correspond in

the degree of development to the univalved organic shells secreted in the late trochophore stage

(stage tl) of M. gattoprovinciati,g described herein. Hayakaze (1997) has also recognized an oval,

univalved organic shell in the late trochophore larvae of Pinctada fLtcata martensii and Ruditapes

philillpinarum. Sccretion of an organic shcll prior te the calcification in the larval and/or embryon-

ic stage has been knowri in other molluscan groups such as gastropods (Iwata, 1980; Togo,1984;

Togo et aL, 1993) and cephalepods (Tanabe & Uchiyama, 1997).

Larval shclls secrcted in thc early veligcr stagc have been described in the spiny scallop,

Chlamys hastata from the west coast of Canada (Hodgson & Birke, 1988), the European oyster,

Ostrea edulis t'rom Long Islund, northeast ot' the United States (Waller, 1981), and the south Pacific

scallop, Aigopecten purpiiratus from Chile (Bellolio et al., 1993), They are dorsovcntrally elongat-

ed, with a pair of notches on the mid-lateral sides of the shclls. A shallow and straight furrow con-

nects the notches, by which the larval shel] is distinctly partitioned into two equal-sized "valves".

At that stage of development, the bivalved larval shell in these species is made up of a single thin

organic membrane, without any trace of hinge teeth and provinculum, These larval shells may be

compared to the larval shells at stage IV in our definition,

Calcification of bivalve larval shells was previously considered to start at the central part of

each valve (MacBride, 1904). This study has revealed that in M. gatloprovincialis, calcification




Hayakaze & Tanabe: Early Shell Devcloprnent of M.vtilus 125

first occurred underneath the erganic shell in the regien of thc retractor muscles in the early veliger

stagc (Fig. 2C), LaBarbera (1974), however, realized by means of polarized microscopy and X-ray

diffraction anatysis that in larvae of 7-7'idacna squamosa, calcification began along the hinge line.

Kniprath (1980) also demonstrated with a polarized microscopc that in larvae of M, gatlru)rovin-

cialis fi'om southern France, the region covered with the retracter muscles was first calcified. These

lines of cvidence suggest that in rnany bivalve species, culcification appears to occur in the early

veliger stage.

Thc size of prodissoconch [ and the relatiye length of prodissoconch II have been regarded as

important criteria to infer the modes of development and capability of dispersal in the Bivalvia

(Jablonski & Lutz, 1980). According to these authors, it has been generally interpreted that the

prodissoconch I and II boundary was fbrmed when the shell gland developed into the mantle, since

the abrupt appearance uf grewth lines at the boundary refiected secretion of CaC03 at the shell

margin, However, our study makes clear that in M. gatl(provinciatis, the shell gland in the poste-

rior region secreted spherulitic prisms undemeath the pellicle in thc early veliger stage (Fig. 3D).

There is no major break in the shell microstructure at thc boundary between prodissoconchs I and

II (Fig. 3F). Waller (1981) concluded that in O, edulis, the shell gland gradually changed into the

mant]e prior to the appearance of Pd II. Our observations on M. galloprovinciali.s corre]ate well

with those on O. edulis by Waller (1981), both suggesting that the prodissoconchs I and II de not

reflect the ditTerentiation of the mantle.

Comparison (lf larval shell moilpholegy with other molluscs

The pre$encc of calcified bivalves aniculated by the ligament is now regarded as one ef the

important autapomorphies in the class Bivalvia (Salvini-Plawen & Steiner, 1996), Howcver, our

work makes clear that bivalves first sccrete a univalved, oval-shaped organic shell in the middle

trochophore stage. A similar eval-shaped or low cap-shaped shell was known to occur in the early

stage of other molluscan classes such as extunt menoplacophorans Laevipilina and Micropilina

(Waren & Hain, 1992) and the cephalopod Ntit{titus (Tanabe & Uchiyama, 1997), The early 1arval

shell development of the Gastrepoda has not yet been well docuTnented, though a flat organic pri-

mary shell (pellicle) secreted by a shell gland was describcd in trochophore larvae of Limnaea

stangnalis by Raven (1958, fig. 43). Furthermore, Sasaki (1998) has shown that the primitive gas-

tropods (Patellogastropoda) share an uncoiled, high conical protoconch with a bilatera] symmetry.

These lines ef evidence seems to suggest that the ancestor of thc Bivalvia had a univalved calcified

shell.

According to the schemc of early molluscan evolution by Runnegar (1983) and Runnegar &

Pojeta (1985), the Bivalvia branched off from the Rostroconchia clade with a laterally compressed

univalved shcll by the development of paircd adductor muscles and decalcification of the pos-terodorsal shell margin, The prodissoconch I of M. gattoprovirtcialis observed in this study was

developed into an elongated form with a median furrow in stagc IV. It was distinctly partitioned

into two "valves",

but the "valves"

were not articulated by a ligament ner hinge teeth. These fea-

tures are very similar to the conditions of adult shells in the Rostroconchia and support Runnegar's

(1983) hypothesis that the ancestors of the Bivalvia probably had a hatchet-shaped foot and well-

diversified pallial and adductor muscles, both of which were suitable for collecting food.

The phylogenetic relationships and origin of mollusean classes have not yet been sufficiently

clucidated, This subject shouLd be considered by combining different approachcs such as molecu-

lar systematics, molcculur developmental biology, and comparative anatomy and embryology of

extant forms us well as paleobiological studies on Cambro-Ordoyician fussils. Further cemparative

analysis focusing on organogenesis and biomineralization of growing larvae will provide a lot of

important infbrmation te understund the morphological evolution of molluscs.



The 　malaoologioal 　sooiety 　of 　Japan

】26 VENUS ：Vol．58，　No ．3 （1999）

Acknowledgn 昭 nts ；一

　We 　thank　Drs．　Neil　H 、　Landman 　and 　John　D ．　Taylor　for　critical　reading 　of 　a　firstdra丘 of 　this　manuscript ，　alld　Ms ．　Keiko　Shimizu　lbr　her　asslstance 　in　the　SEM ，　and 　Messrs．　Yuji　Uchimura，Yurimasa　Terao 　and 　Dr．　Shin’ichi　SaIo　f｛〕r　lheirhelp 　in　collccting 　growing 　bivalve　larvae．　This　manuscriptwas 　much 　improved　by　critical 　 comments 　of　two　anonymous 　referees ．　This　work 　was 　supported 　by ［heGrant−In−Aid　of　the 　Japanese　Ministry　of 　Education ，　Science，　Culture　and 　Sports（No ，07304042 　f｛〕r　1996 ；

No ．09304049　fbr　1997 − 1999），

ムラサキイガイの初期幼生殻の発達過程

早風恵美．了・棚部

・成

　（．東京大学地質学教室）

要　約

　ムラサキイガイ（Mytilus　galloprovinciati．s　Lanlarck）の幼生殻形態を走査型電子顕微鏡を用いて観察

し，その発達過程を記載した。水温 15．O − 182 ℃ の条件下で，受精後 16 時間でトロコフォア幼生が

出現し，さらに約 40 時問を経過してベリジャー幼生に変化した。トロコフォア幼生中期に楕円形の

一

枚の有機質薄層からなる原殻 1 が現れた。時問とともに原殻 1はひょうたん型に変わり，中央のくびれ

に沿ってヒンジが出現して 2 枚の殻が形成された。受精後約 70 時間を経過したベリジャー幼生初期に

原殻 1 の石灰化が確認され，さらに受精後約 80 時間で，原殻 1の周囲に明瞭なくびれを伴って原殻 II

が発達し始めた。有機質でできた 1 枚の楕円形の殻は，他の二枚貝類ばかりでなく単板類，腹足類，

頭足類の発生初期にも確認されることから，貝殻亜門の共有派生形質のひとつと解釈される D

References

Ansell，　A ．　D ．1962．　The　functional　morphology 　of 　the 　Iarva　and 　pc｝stlarval 　devclopment　of 　Venus 　striatuta

　　　（da　Costa）．ノl　Mar ．　Biθ1．　Ass θ c．　U ．　 K，42 ： 419 − 443 ，Bande1 ，　K ．1988．　Stages　in　the　 ontc 》geny 　and 　a　model 　of 　the　evolution 　of 　bivalves（Mollusca）．　Pal伽砿 Z．．　　　62 ： 217 − 254 ．Bellolio，　G ．　Lohrma 冂 n ，　K ．＆ Dupr6，　E．1993 ．　Larval　m 【〕rphc〕logy　of 　the 　scallop 　Argopecten 　purpurat“ s　as

　　　revealed 　by　scanning 　electron 　microscopy ．　Vetiger，36 ： 332 − 342 ．Carricker．　M 、　R ．＆ Palmer ，　R ．　E ．1979a ，　UltrastructUral　morphogenesis 　of 　prodissoconch 　and 　early 　disso−

　　 conch 　valvcs 　of 　the　oyster 　Cr α・s’・9t爪 t厂 ea 　vi厂ginica．　Proc ．　Natn ．　Shelltfisheries　A ∬ oc ．，69 ： 103 − 128 ．Chanley，　P．＆ Diamani，　P．1980 ．　Comparative　descriptions　of 　some 　oyster 　larvac　from　New 　Zealand 　and

　　 Chile，　and 　a　description　of 　a 　new 　genus 　of　oyster ，　Tioslrea．　N ．　Z ．」．　Ma 　r．　Fre，yhwater 　Res ．，14 ：103 −

　　　120．Cragg ．　S ．　M ．＆ Crisp，　D ．」．1991，The　bi｛｝bgy 　of 　scallop 　larvae，　pp．75 − 132．ノη ：Shulnway，　S．　E．（ed ．）　　 Devetopments 　in　Aquaculture 硼 d　Fishe 厂ies ∫cien （：e，21 ’ Sca〃ops ．’Biolo8y，　 Ec θ 1θ gy 　and

　　 Aquaculture ．　Elsevier，　New 　York，Eyster，　L ．　S ，1986．　Shell　inorganic　composit ．ion　and 　onset 　Qf　shell　mineralization 　during　bivalve　and 　gas−

　　 tr〔〕pod 　embryogenesis ．　Biθ 1．　Bu 〃．．170：211 − 231．Fuller，　S，　C．＆ Lutz，　R ．　A ．1989 ．　Shell　morpho 豆ogy 　of　larval　and 　post−larval　mytilids 　from　the 　North −

　　 Western　Atlantic．．1．〜瞼臥 Biot，　A ∬ oc ．σ，　K ．，69 ： 181 − 218 ．Hyayakazc ．　E．1997．　Larval　developmcnt　and 　shell 　morphology 　of 　five　species 　of　Bivalvia．42pp，　Mastcr　　 Thesls，　GeoL 　Inst．，　Univ．　TokyQ ．Hodgsun ．　C ，　A ．＆ Burke ，　R ．　S．1988．　Development　and 　larval　morphology 　of 　the　spiny 　scallop ，　C〃 αm メs

　　 hastata．　Biθ1．　Bull．，174 ：303 − 318．Iwata，　 K ．1980．　 Minera ］ization　 and 　 architecture 　 of 　the　 larval　 shell 　 of 　Haliotis　di，ycus 　 hannai　 Ino　　（Archaeogastropoda）．ノ，　Fac ．　Sci．，　H θkkaido しJniv，，　Ser．ハ／ ‘6eol．＆ Mineral ．丿，

19 ： 305 − 320 ．Jablonski．　D ．＆ Lutz，　R ．　A ．1980 ．　Molluscan 　larval　8hell　morphology ，　Ecoiogical　and 　paleontological　appli 一

N 工工一Eleotronio 　Library 　




Hayakaze & Tanabe; Early Shell Development of dytilus 127

cations, pp. 323 - 377. In: Rhoads, D. C. & Lutz, R. A. (eds) Skeletal Growth ofAquatic Organisms.

Plenurn Press, New York.Kniprath, E. 19RO. Larval development of the shell ttnd the shcll g}and in Mytitus (Bivalvia). RouxFs

Archives Devel(w. Biot,, 188: 201 - 204.

LaBarbera, M. 1974. Calcification of the first larva] shell of 1:ridacna squamosa (Tridacnidae: Bivalvia).

Man Biol,, 25: 233 J 238.

Loosanoff, V. L, & Davis, H. C. 1963. Rearing of bivalve motluscs, pp. 1 - 136. In: F. S. Russel (ed.)

Advances of Marine Biolog.),, 1. Academic Press, London,Loosanoff, V. L., Davis, H. C. & Chanley, P. E. 1966. Dimensions and shapes of larvae ef seme marine

bivalve mollusks. Malacologia. 4: 351 - 435,

Lutz, R, A, & Hidu, H. I979. Hinge merphogenesis in the shells of larval and early post-larval mussels

(M>,tilzas edulis L. and Modiolus mediolus (L.)). J. Mar, Biol. Assoc. U. K., 59: 1 1 1 - 121.

MacBride, E. W. 1904. The Canadian oyster. Canad. Rec. Sci., 9: 145 - 156.

Moueza, M., Gros, O. & Frenkiel, L. 1999. Ernbryonic, larval and postlarval developrnent of the tropical

clam Anomalocardia hrasitiana (Bivalvia, Veneridae). J. MotL Stud., 65: 73 - 88.

Raven, C. P. I958. Morphogenesis; 71he Analysis of Moltuscan Development. 311pp. Pergamon Press,

London.Rees, C. B. 1950. The idcntification and classification of lamellibranch larvae. HuU ButL Mar. EcoL, 3: 73

- 104,

Runnegar, B., 1983: Molluscan phylogeny revisited. Mem. Assoc. Australasian Palaeont., 1: 121 - 144.

Runnegar, B. & Pojeta, J. Jr. 1985. 0rigin and diversification of the Mollusca, pp, 1 - 57. ltu Trueman,

E.

R. & Clarke, M. R, (eds) 7)Pie Molluh'ca, 10: Evolution. Academic Press, Orlando.

Sastry, A. N. 1979. Pelecypoda, pp., 113-292. In: Giese, A. C. & Pearse, J. S. (eds.) Reproduction of Marine Invertehrates. 5. Academic Press, New York.

Sa]vini-Plawen, L. v. & Steiner, G, 1996. Synapomorphics and plesiomorphies in higher classification of

Mollusca, pp, 29 - 52. In: J. D. Taylor (ed.) Origin and Evol"tionarly Radiation of the Moliusca,

Oxford Univ. Press, Oxford.Sasaki, T. 1998. Comparative anatomy and phylogeny of the Recent Archtteogastropoda <Mollusca:

Gastropoda). U}iiv. Mus., Univ. 71}kyo, Bull., (38), 223pp.Tanabe, K. & Uchiyama, K. 1997. Development of the embryonic shell stmcturc in Nautilas. Veliger, 40:

2U3 -

215.Togo, Y. 1984, Scanning electron microscepy ef larval and early postlarval shells in the freshwater snail,

Cipangopaludina .iaponica (V. Martens) (Mesogastropoda, Viviparidae). I GeoL Soc. Jap., 90: 565

-

576.Togo, Y., Suzuki, S, & Hikida, Y. 1993. 0ntogenic changes in the shell structurc of the freshwater bivalve

SPhaerium J'aponicum (Heterodonta), pp. 55 - 63. bi: Kobayashi, T., Mutvei, H. & Sahni, A. (eds.)

Structure, Formation and Evolution of Fossil Hard 7'issues. Tokai University Press, Tokyo.

Waller, T. R. 1981. Functional morphology and 1arval development of veliger larvae of the European oys-

ter, Ostrea edulis Linn6. Smithson. Contr. Zbol., 328, 1 -70.

War6n, A. & Hain, S. 1992. Laevipitina antarctica and Micropolina artzi, two new monoplacophorans from

the Antarctic. Vketiger, 5: 165 - 176.

Yoshida, H. 1964. Seedings of Shelij}sh. Hokuryu-kan Beok Company, Tokyo 221pp. (in Japanesc).

[Received: April 9, 1999; Accepted; June 25, 1999]

early larval shell development in mytilid bivalve mytilus

Documents