The malacologicalsocietymalacological society of Japan
A Chromosome Survey in Sixteen Species of Nudibranchs*
Akihiko INABA and Yasuko SAiKi
(Mukaishima Marine Biological Station)
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(mpEff Plates II-III; tc 1-2)
Abstract
The chromosome numbers in 16 species belonging to 7 families of nudibranchs are here. The chromosomes so far reported reported by preceding investigators are shown in Table 1, and those by the authors are present listedin Table 2. These numbers are uniformly 13 in haploid without exception, and in spite of the remarkable difference in their external rnorphology, these nudibranchs the similar have karyotype, The sperma- togonial chromosomes are regarded as of metacentric nature, The sexual difference of chromosomes is not observed,
In Japanese nudibranchs, the chromosomes of 13 species were observed by INABA and HiRoTA (1958)and INABA b, 1961a). (1959a, Recently, MANcJNo and SoRDi (1964a, b, 1965) reported the chromosomes of 16 Mediterranean nudibranchs, and BuRcH and NATARAJAN (1967) reported the chromosorne numbers of 2 nudibranchs from Eniwetok Atoll. These results are listedin Table 1, with some other previous reports. In this paper, the chromosomes of 16 nudibranchs in opisthobranchiate gastropods are described, and these results are discussed with other investigations. Before further, going the authors express their cordial thanks to Dr, R. HiRoTA, Mukaishima Marine Biological Station, and Mr. H. MuKAi, graduate student of Hiroshima University, for their aids in collecting the materials.
Materials and Methods
In this study, 16 species belonging to 7 families of Nudibranchs were used for the materials, as follows:
CLASS GASTROPODA
Subclass Euthyneura
Order Nudibranchia Suborder Doridoidea
Superfamily Cryptebranchia 's-6I ' '" " * Contributions from the Mukaishima Marine Biological station, No,
8
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INABA and SAIKI: Chromosome of 16 nudibranchs 9
Family Dorididae Aldisa sanguinea
Discodoris concimza
Hoinoiodoris 1'aPonica Superfamily Phanerobranchia
Family Okeniidae Coniodoris stt.oashimae
Superfamily Porostomata
Family Dendrodorididae Dendrodoris rubra itigrontacztlata Suborder Dendronotoidea
Family Dotonidae Doto betla Suborder Eolidoidea
Superfamily Acleioprocta
Family Eubranchidae Et{brancltus ntisaleieitsis
Eubranchzts inabai
Eubranchopsis vizg2'nalis Family Cuthonidae Ctttlzona futairo Catriona PttPillae Catriona Puny>ureoanitlata Catriona signijletra Superfamily CIeioprocta
Family Facelinidae Ht'rviella a.ainis
Rizxolia lineata
Fumily Aeolidiidae Lime'nandra fztsij'ormis Eolidoidean nudibranchs live mostly on algae, mainly on Sargassum, They were ' collected by washing off Sargassum weeds in the vesseL The others inhabiting in the tide or on the rocky shore were collected pool at the low tide. Those materials were all collected from the vicinity of Mu kaishima Marine Biological Station in different
seasons. The materials were fixed and stained by aceto-orcein squash method. Ob- servation was made under the Olympus and Nikon microscopes using a 100 × oil im-
mersion objective and 15-20 × oculars. The magnification of all the figures and the photographs was 3300 times.
Results of Observation
].) Aldisa sanguinea (Co6pER, 1862) A common doris in medium size. Body-length is about 25mm. The back is thickly covered with tiny rounded granules. General body-colour is vivid orange-red sprinkled everywhere with minute and indistinct black dots. It has 2 (or 1 or some- times 4) black spots on the back in the middle line. This species was obtained from rock reefs at an the islet near Mukaishima in July, 1966, The early metaphase of the lst spermatocyte wus examined. There were 13 chromosomes on the haploid nucleus plate. Some of them were ring-shaped (Pl, III, Fig. 1).
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2) Discodoris concin"a (ALDER et HANcocK, 1864) is very soft and the back is covered A large specie$ up to 80mm. The body of back is ashy brown and everywhere with granules. General ground-colour the The underside of the body is overlaid with dark brown mottle of varying intensity. specimen was collected also ashy brown irregularly spotted with dark brown. This 1966. In the lst diakinesis, from the rock reefs at an islet near Mukaishima in July,
chromosomes III, Fig. 2). there were 13 chromosomes containing some ring-shaped (Pl.
3) llomot'odoris J'oponica BERGH, 1881 This is a very common doris. Body length of this species is about 50-60mm. General The back is covered with globular tubercles of varying sizes, ground-colour and maculated with black here and of the back is bluish yellow to bluish green is vicinity of the Station there. This species was obtained from the rock reefs in the were ob- in April, 1966. In each of the lst spermatocyte nucleus, 13 chromosomes served (PL IIL Fig. 3).
4) Coniodoris sztgashimae BABA, 1960 length is about 2e mm General body- This species is rather small in size. Body here and there with dark colour. colour is pale yellowish brown shaded or maculated the back and sides. The speci- It is covered with clusters of opaque white dots on ascidians on rocks or algae near the mens were collected on some compound the metaphase show 13 chromo- Station in April and June, 1966. The lst diakinesis and size being ring-shaped (Pl.II, somes as haploid, one or two of comparatively large
Figs. 1, 2). 1913) 5) Dendrodoris (Dendrodoris) rubra, var. nigromaculata (EL[oT, General body-colour is orange- This is also a common large doris, up to 70mm black blotches irregularly. The yellow, the back is smooth and covered with bold reefs at an near Mukaishima in June, specimens were obtained from the rock islet The haploid complex 1965. The early metaphase of the spermatocyte was examined. them were ring-shaped (Pl.II, of this species consisted of 13 bivalents. Some ef
Fig. 3).
6) Doto (Doto) bella BABA, 1938 lives on Sa?lgtissum Body length is 5-10mm. This species is small in size and is and The branchial papillae are pinecone-shaped. Genera! body-colour golden yellow in May, 1960 near the Station spotted with dark green. This specimen was collected in the spermatogonial metaphase, from Sargasszt]n weeds. There were 26 chromosomes The others were not strongly bent but several pairs of them were Iarge V-shaped. metaphase, 13 chromo- were all metacentric (Pl. II, Fig. 4). In the lst spermatocyte II, Fig. 5). somes were observed. Some of them were ring-shaped (Pl. 7) Eubranchus misakiensis BABA, 1960 5mm. The branchial This is a very small eolis. Body-length is about papillae and bluish liver-vein. General are long fusiform, with a yellow subapical ring green everywhere on ground-colour is yellow white, with chocolate-brown spots scattered
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INA}tA and SATK[: Chromosome of 16 nudibranchs 11.
of the the bodv. This species was collected from Sailgassum weeds in the vicinity diakinesis Station in June, 1965. There were 13 bivalents in the lst spermatocyte (Pl. IL Fig. 6).
8) Ettbranchus inabai BABA, 1964' discovered near the Mukaishima This species is also a very small eolis and first is stoutish, Marine Biological Station CBAB,N, 1964). Body-length is about6mm. Body opaque white markings The back and sides are deep reddish brown and a series of from weeds Iies on the back in median line. This species was collected Sargtissz{m In the lst spermatocyte dia- in the shallow water near the Station in October, 1965. III, Fig. 4). kinesis, there were 13 bivalents and some of them were ring-shaped (Pl.
9) EttbranchoPsis i)irg･inctlis BAB.A, 1949 is about 1?mm. The branchialpapillae, This species is a small eolis. Body-length body-colour is olive- faintly vermilion-tinted, are long and fall off easily. General of deep blue on the back, sides, yellow and beautifully ernamented with round spots from SargassuTn weeds in the vicinity papillae and tentacles. This species was obtained bivalents in the diakinesis nucleus of the Station in October, 1965. There were 13 of the lst spermatocyte CPI. II, Fig. 7). 10) Cztthona fzttairo B,xB,x, 1963 and the branchial Body-length is 20--30 mm. General body-colour is orange-yellow tip. This species papillae are orange-yellow, with a dark green vein and a white near the Station in May, 1966. was eollected on Sargassttm weeds in shallow water 13 dot-shaped bivalents II, Fig. 8). The lst spermatocyte metaphase contained CPI. 11) Catriona PuPiltae BABA, 1961 length. Cephalictentacles and rhino- Animal is always small and 3-5 mm in total below the tips and liver-veinsare dark phores marked with an opaque white band shallow water around brown. Thi$ species was collected on Sai:gassum weeds in the the Station in March, 1960. In the diakinesis of the lst spermatocyte, 13 bivalents showed the ring-shape II, were observed. Frequently one or two chromosomes (Pl.
Fig, 9). 12) Catric)na PztvPetrc.oav･tttlata BABA, 1961 are long. The This is a smaH eolis und 6-10mm in length. Branchial papillae a band below the tip of each. coloration of branchial papillae is distinctive with purple The specirnens Two bands of purple occur also on cephalic tentacle and rhinophores. water around the Stationin August, were obtained on Sargassttm weeds in the shallow II,Fig.10). 1965. In the lst diakinesis, there were 13 bivalentswhich varied in size (Pl.
13) Catriona sig'nifera BABA, 196] This species is This is a very small eolis. Total length of animal is 5-8mm. or black-green marking behind very distinctive with an ovoid dark brownish green branchial are dark the rhinopheres on the back. Liver branches within the papillae weeds in the shallow water around green, The specimens were obtained on Sargassttm the islet near Mukaishima in October and November, 1965. The lst prometaphase
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nucleus contained 13 dot- or rod-like bivalents varying in size (Pl. III, Fig. 5). 14) Hbrviella qtffnis BABA, 1960 Body-length is about 10mm. Ground-eolour of body is yellow white. The back and sides are thickly spotted with black. Each of the branchial papillae is marked with a subapical vermilion ring, This specimen was collected on Sai'gTissztm weeds in the vicinity of the Station in August, 1966, In the lst spermatocyte prometaphase, there occurred 13 bivalents varying in size in a considerable degree (Pl. III, Fig. 6). 15) Ri2aolia lineata (ELioT, 1904) ==Cratena lineata (ELioT, 1904) This is a small eolis and 10-15mm long. The branchial papillae are elongated fusiform and fall off easily. The back and sides are marked with fine, irregular, longitudinal opaque white lines. This is very distinctive with 2 conspicuous red blotches in the head and 1 on each side. This species was collected on Sargassblm weeds near the Station in November, 1965. As the generic name of this species, Rig2olia must be used instead of Crateha (BABA, 1964). In the lst diakinesis, 13 biva- lents containing some ring-shaped chromosomes were observed (PI. II, Fig. 11). I6) Limenandra .ktstfbrmis (BABA., 1949) This eolis attains large up to 70mm in Iength. The branchial papillae are long fusiform and fall off very easiiy. Body-colour is brown with yellowish spots here and there on the back. This species was obtained from Sa71gussunz weeds in the shallow water around the Station in November, 1965. In the lst spermatocyte nucleus, the chromosomes varying in size were observed. The number was 13 (Pl. III, Fig. 7).
Discussion
The chrornosome numbers of 33 species of nudibranchs so far published by the mvestigators past are shown in Table 1. The work of the classical authors listed in Table bracket) is unsatisfactory (in by present-day standards. The chromosome numbers studied by the present authors are listed in Table 2. It is evident from these tables that the chromosome number of nudibranchs is uniformly 13 in haploid, and that there are no species which have 12 or 17 chromo- somes as reported in other orders of opisthobranchiate gastropods (INABA, 1959b, 1961a ; MANciNo and SoR])[ 1964a, b, 1965, BuRcH and NATARAJAN, 1967). The chromosomes of 16 species of nudibranchs here under study are also closely alike with each other in every morphological aspect. It is noticeable that the species belonging to the different suborders, such as Doridoidea, Dendronotoidea, Arminoidea and Eolidoidea, show a close similarity as to their chromosomes, irrespective of the remarkable difference in their morphological and anatomical characteristics.
In general morphology the spermatogonial chromosome of Nudibranchs are repre- sented by typical V-, wide-open V- or slightly curved rod-shaped in appearance, in both figuresdrawn from parathn section (INABA and HiRoTA 1958 ; INABA 1959a, b) and
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INABA and SAim: Chromosome of 16 nudibranchs IS
Table 1, Chromosome numbers of nudibranchs hitherte reported. .--. 't'T.7tZ...･---/.. .". .. ' . '- Species Name 2n n Note ' -- ' '- ' '1 - Doridoidea'"'- / Cryptobranchia ･ Giossoderis 1 '58 Pallescens ' 13 S. (I ) & HmoTA ' Glossodoris .festiva 13S Doris verrucosa 26s, o, m '64a 138, 9(I) n Rostanga arbutus '59b 26s 138 Discodoris Pardatis 138(I) ' KaloPlocmnus rczTnosus /, ' ' 13g(I) INAHA &MANclNoHI.RcyTA 58'6558'65 rCaleplocamus] ramosus 26s*26s26s*26s"26s* 13S(I) & SOH)I 11 PlocamoPherzts titesii ' ! 13S INABA &rvCANe[NoH"((rrA Po4vcera quadrt'lineata 1/ 13S(I) 1 & SORDI Aegirus leukarti 11 138(I) .v castanea Goniodoris 13S(I) "HTHeTA i Ohenia ' barnardi !: 13S(1) INAyA &MANcrtso 58'65'64b 7'raPania i11/ fltsca 26s'26s 138(I) & SORI)T TraPania sP. / 138(I) " Prostomata Dendrodoris 7iigra '5B 26s26s, 13S(I) INABILINA]ABuRcliINABA& Hmoi'A '59a& :t1 m 139(I, ll) '67 13S(I) NA'vARA"AN Dendrodoris miniata '58 13S(I) & HiRcrrA Arminoidea /1/ / Dermatobranchus striatus 26s 1' 138(I) " Armina tig. rina '65 1 26s*(20-24m) 13S(I> MANc]No & SoBm (Armina califbrnica) '97) TPIeurophyllidia] (10-12?(")) (MAcFAJiT,AND Dendronotoidea ! Melibe 26s(32m) '59b PaPiilosa 13 D,(I) 'INABA 1:1 '90) (Phytlirhoe bucePhala) (169(I, [)) CBovEHr Eolidoidea Acleioprocta 1! Sakuraeotis enesimensis '58 13S(I) INABA IHervia ceylonical & HrRoTA Sahuraeolis [Hervia] ]'aPonica 138(I) " Hbrvia '64b Peregrina 26s*(32nl)(32m)26s*26s" 13S(I) MANclNo & SoRpl '05) (CraXena[Montaguel.aauldi) i1/ (169(I, n)) i (SMAImwOOD :CCratena [MontaguelPitata) " (169(I, ll)) ( ) Trinchesia coerulea '65 13S(I) MANtllNo & SoRbl Trinchesia aurantia i 138(I) ' m Cleioprocta Catoria maczalata 26s* '64b 138(I) e Hbrvieita mietta 26s* '67 138(I) BuRcH & NAIiAHA,mN Facelina rubrovittata 26s* '65 ! 13S(I) ' " neaPolitana /] SPurilta 26s' 138(I) v 1 t tttttt ttttt tt ttttttti NII-Electronic Library Service The malacologicalsocietymalacological society of Japan 14 VENUS: 26 (1) 1967 Tab]e 2. Chromosome numbers of Nudibranchs determined by the prese.ntauthors. ' ' "' -= ' '-- ･-' -- '"' ------F' Species Name 2.n-. n Note 'r' 1 -. ' ''-- [ Do,-id.id-.i 1 Cryptebranchia m 1Fig. T;i ･;f 13as(I) Pl.Pl.Pl,m,m,m,Fig, Aldisa sangest'nea ff- t-'t9 i ' - 13S(I) 2Fig, Diseodoris cvncinna v･v' tz x) l- Vv ' -x''? :. - 3 Hbmoiodoris ]'aPonica 1- i7 L)v 138CI) Phanerobranchia , ,yv - 138(I) Pl. ll) Figs. 1, 2 Goniodoris sugashimae -ffv-?=3=t) ;- ' Porostomata Dendrodoris (Dendrodoris) rubra, , ' ' 13SCI) Pl, llt Fig. 3 var. nigromac"lata ?a'') 'r) x'V-y Dendronotoidea / 26s 138(I) PL rrJ Figs. 4, 5 Dote (Doto) bella ri V)" ;i:yLy VJ ii'VsT) vi Eolidoidea Acleioprocta `V'aat ･Jf - P].Pl.Pl.Pl.PLPI,PLFig.Fig,Fig.Fig.Fig.Fig.Fig.64789105 Eubranchus misafeiensis l- s :- 1 T) i t] 138(I) ll)N,llIn,n,E,m, - Euhranchus inabai /f ti'Ai7VE t7y 13S(I) - ., 7 ij aij v' 13S(I) EubranchoPsis virginalis );uti.7 / - v i. 19 ;- vy 138(I) C"thona ftttairo 7S rf ij -Y - 13S(I) Catriona PuPiUae =r- ;:'-EIVi ij T7 :) T) - 138(I) Catriona PurPureoanulata r, lf' i/ i v tt - 13S(I) Catriona signifera zyy fiV lt7 l- Vy Cleioprocta , i ･ r 138 are regarded squash preparations (INABA 1959b; present paper) . These chromosomes ' the cleavage as of metacentric nature, though they vary in size and shape. In first metacentric nature characterized of Deizdrodvris nigra, all the chromosomes display a MANc[No and also by median or submedian fiber attachment (INABA 1959a). SoRDi ' - verrucosa confirmed these features in the embryonal mitosis of Doris (1964a). frequently appear as In the early metaphase (diakinesis), a few Iarge bivalents are trans- a ring in almost all species. In metaphase, these chromosomes generally formed into bivalents of dot-type. INABA reported In the paper on the chromosomes of Dendrodoris nigra, (1959a) between the two sexes. the evidence that there is no sexual differenceof chromosomes of Doris verrucosa, MANciNo and SoRDi C1964a) also studied female and male germ-cells difference of chromo- and reported the same results. In the present study, the sexual somes was also not observed. NII-Electronic Library Service The malacologicalsocietymalacological society of Japan IN.x]m and SA[-: Chromosome of 16 nudibranchs 15 rk ec -c 'ecre,H. -e-f･qvctqil･･[･'k/#.･twktgli･a -)s: s 7 16 ux, 1sc.ptll･rllkL･ }iit, [] tt,1-Fitoveth･frfge'.iEjlfiL ftz.rc9,(-VqiL Efnl abo-L L･ idlIC .]1 o. ]tL. 'c Fb oD cD 1 n =: 13S 2n=26s 7o I]kL Yk･C!IMgtwP'i, h'('tt i;tfMf/Xl (Table 8 P,]ff.)2:nva･ee, (! ), t'" L 4 CTable -e-･i,-( 'ceP'me}7T' -vea)'Umats{]l:l)-ft;v=･ n=13 2 a.H,t,i,).BIIft..IEtNe-.,., ,ll}1, 4i#tHt,cI)･l,j'F,)ix64clbIItf5-gt, .k -n 'iTi ii ,"i). ;// =12 n= 18 n=7, 17 cD < t,Lf:Sk fr 1'L-, (I-T,F,tsLl), 17 (fl,",tEM), n=17, (/IiCSEff), (pt H) .kb lk 'i v(T ･l) ts SIk UiPktw 6ti,ri,-) cD thi' 7k L･ lu･s, flMaklS e Et va.ha/ Etl ?IEvpt EI.3 6. Reference ABE{, T., 1954: Opisthobranchia of Toyama Bay. IIokuryukan, Tokyo. BABA, K,, 1949: Opisthobranchia of Sagami Bay. Iwanami-shoten, Tokyo. -- , 1955: Ibid.,Supplernent. Iwanami-shoten. Tokyo, 1960a: The Genera and , Ohenia, Coniodoridella Gvniodoris from Japan (Nudibranchia- Goniodoridae) Pttbt. Selo matr. Biol, Lab., 8 (1): 79-83, 2 pls, ･ new species of the Etfbranchus from , 1960b : Two genus Japan (Nudibranchia-Eolidacea). Ibid,, 8 (2): 299-302, 1 pl, new species of the Catriona from , 1961: Three genus Japan (Nudibranchia-Eolidacea), Ibid., 9 (2): 367-37Z, 2 pls,, 1 text-fig. : Description of n sp,, , 1964a Eubranchus inabai from Mukaishima, Japan (Nudibranchia- Eolidoidea). Ibid., 12 <4): 285-287, 1 text-fig. ---- .1964b: The anatomy of Rizaolia lineata (EiiJnT) (Nudibranchia-Eolidoidea). Tbid., 12 (4): 289-294, 2 pls. Bt/HcH, J.B. and R. NA'rA,t opistobranchi. Arch. .7.ool. Italiano, 50:73-87, 3 text-figs. NII-Electronic Library Service The malaoologioalmalacological societysooiety of Japan 16 VENUS ： 26 （1） 1967 Explanation of Plates II−−III The magnification of all the figures and the photographs is 3300 times ． Plate II． Fig ． ． lst spermatocyte metaphase 1 The of Goniodoris sugrashimae ， ス ガ シ マ u ネ コ ウ ミ ウ ツ の 第 1 分 裂 II ・則 Fig ． ． lst spermatocyte diakinesis 2 The of the same ，ス ガ シ マ コ ネ コ ウ ミ ウ シ の 第 1 分 裂 前 期 （デ ．｛ ア キ ネ シ ス ） Fig． 3． The lst spermatocyte diakinesis of Dendrodoris rubra nigromaczaiata ， マ ダ ラ ウ ミ ウ シ の 1 ， za 分 裂 前 期 FF置 ロ 45コ The spermatogonial コ 99 metaphase of Doto bella， ガ ネ マ ツ ヵ サ ウ ミ ウ シ の ■ 精原 細胞 中 期 − コ The lst ’ spermatocyte metaphase of the same ，コ ガ ネ マ ッ カ サ ウ ミ ウ シ の 第 正分 裂 中 期 Fig ー ． 6． The lst spermatocyte diakinesis of Eubranchus misakiensis ， ミ サ キ ヒ メ ミ ノ ウ ミ ウ シ の 第 1 分裂前 期 Fig ． 7． The lst spermatocyte diakinesis of virginalis ジ ． Eubranchopsis ， ／， オ ゥ ミ ノ ウ ミ ウ シ の 第 1 分 裂 前 期 Fig． 8． The lst spermatocyte metaphase of Cuthona 70 卩 ・ ノ密 如 ， フ タ イ ミ ノ ウ ミ ウ ン の 第 1 分 裂 中 期 Fig ． 9 ． The lst spermatocyte diakinesis of Catriona puPillae．コ マ ユ ミ ノ ウ ミ ウ シ の 第 1 分 裂前 期 Fig．10 ． The lst spermatocyte ユ diakinesis of Catrion α purpureoanutata， ビ ワ ミ ノ ウ ミ ゥ シ の 第 1 分 裂 前 期 Fi晋．11． The lst spermatocyte diakinesis of Riazolia lineata バ セ ． ， ク ソ ミ ノ ウ ミ ゥ シ の 第 1 分 裂 前期 P 置ate III． The figures in upper half correspond to the photographs in lower half Fig．1． The lst spermatocyte diakinesis of Aldisa san8uinea ，チ シ オ ウ ミ ウ シ の 第 1 分裂 前 期 Fig ．2． The lst spermatocyte diakinesis of Discodoris concinna ， ツ ヅ レ ウ ミ ウ シ の 1 第 1 分 裂 前期 ・ Fig ．3． The lst spermatocyte diakinesisof Homoiodoris α o 雇 c α マ ン ブρ ， ヤ ト ウ ミ ウ の 第 1 分裂 前 期 Fig．4． The lst spermatocyte diakinesis of Eubranchus inα bai，イ ナ バ ミ ノ ウ ミ ウ シ の 第 1 分 裂 蔚 期 Fig ．5． The lst spermatocyte diakinesis of Catriona signifera モ ソ ミ ノ ， シ ョ ウ ウ ミ ウ シ の 第 1 分 裂 前 期 Fig ．6． The lst spermatocyte metaphase of Herviella a ゴ マ フ ミ ノ ミ シ の ． ／nnis， ウ ゥ 第 1 分裂 中 期 ’ 17 Fig．7。 The lst spermatocyte diakinesis of Li menandra fusifermis， ホ ソ r ・ラ グ ッ ウ ミ ゥ ’ シ の 第 1 分 裂 前 期 一 NII-ElectronicN 工 工 Eleotronio Library Service The malacological society of Japan VENUS 26 （1） 1967 Plate ロ 馨爵鍛 噸簿ミr藷 ♂ 韈 INABA and SAIKI Chromosome of 16 NII-Electronic Library Service The malaoologloalmalacological societysoolety of Japan 讖 INABA and SAIKI Chromosome of 16 NII-Electronic Library Service