Reproductive Cycle, Copulating Activity and Dispersion Pattern of the Dogwhelk Nucella Freycineti (DESHAYES)

Benthos Research, 45 : 29-41, Aug., 1993

Reproductive Cycle, Copulating Activity and Dispersion Pattern of the Dogwhelk Nucella freycineti (DESHAYES)

KEI KAWAI and SHIGERU NAKAO

Laboratory of Mariculture. Faculty of Fisheries, Hokkaido University

チヂミボラ Nucella freycineti (DESHAYES)の生殖周期と交尾頻度および分布の集中度

河合渓・中尾繁

Abstract

KAWAI, KEI and SHIGERU NAKAO (Faculty of Fisheries, Hokkaido University). 1993. Reproductive cycle, copulating activity and dispersion pattern of the dogwhelk Nucella freycineti (DESHAYES). Benthos Research, 45 : 29-41. The reproductive cycle of Nucella freycineti was studied based on samples collected at monthly intervals from September 1987 to December 1988 and from May 1990 to July 1991 in Usujiri, southern Hokkaido, Japan. The developmental processes of the gonads and the seminal vesicle were classified into four and three successive stages, respectively. The development of the gonads and the seminal vesicle exhibits a distinct annual cycle. In both sexes, remarkable gonadal development was observed during the warm season from June to October. More than 90% of the males were mature in October. However, oogenesis was observed through the winter until the next breeding season in April and May. The annual cycle of the ovary is not synchronous with that of the testis but with that the seminal vesicle. Size at sexual maturity was 19+ mm and 15+ mm shell length for femalesof and males, respectively. MORISITA index (I8) showed that these snails aggregated all year round. Strongest aggregation was observed during the colder and coldest seasons from November to May, when high copulation and breeding activities successively occurred. During warmer period from June to September, the index was relatively low but high foraging activity was observed.

stones and in crevices in a way similar to its con- INTRODUCTION familial species Thais (=Nucella) lamellosa (SPIGH- cella freycineti Nu (DESHAYES) is a common ,1977) and Nucella crassilabrum (GALLARD0,1979).T prosobranch gastropod found on low intertidal espite the abundance of Nucella freycinetiD in north- cky shores from Touhoku to Hokkaido,ro Japan. ern Japan, neither its reproductive biology nor its This species deposits egg capsules on boulders, behavior has been examined yet. Some studies on the reproductive biology of Received January 5, 1993; Accepted May 21, 1993. cky shore muricidae have been reported.ro KON et

29 No.45 Benthos Research Aug., 1993

al. (1966) described the seasonal changes in the gonads of Purpura (= Thais) clavigera. FEARE (1970) studied the reproductive cycle of the dogwhelk Nucella lapillus. Factors affecting reproduction were also studied in neogastropods. HOUSTON (1971) discussed the relationship of gonadal development to temperature, salinity, photoperiod and lunar period while describing the reproductive biology of Thais (= Nucella) emarginata and T. canaliculata. SPIGHT (1975) examined temperature affecting the embryonic development of T. (= Nucella) lamellosa. MARTEL et al. (1986) studied the reproductive cycle and copulating activity of Buc- cinum undatum and also mentioned the relationship between feeding and reproduction. TAKA- HASHI et al. (1972), TAKAMARU& FUJI (1981), and FUJINAGA(1985) made histological observations on the gonad of Neptunea arthritica and investigated seasonal relationship between body and gonad in weight. The present study aimed to determine the annual reproductive cycle of .N freycineti based on Fig. 1 Map showing the study area and approxi- histological examination, gonad index and size at mate height above M. T. L. in meters. sexual maturity. The relationship between sea Black circles represent the sampling sta- water temperature and gonadal development, tions. copulating period, foraging activity and dispersion pattern was also examined. tissue, the gonad together with the digestive gland MATERIALS AND METHODS were separated as one component and dehydrated The study area covered the intertidal rocky in an ethyl alcohol series. The gonad-digestive shore from 53 cm to 145 cm tide levels, at Usujiri, gland complex was embedded in paraffin with Hokkaido (42° 21' N ; 140° 57' E) (Fig. 1). butyl alcohol, sectioned at 5-8,am, stained with Chthamalus challengeri, Littorina brevicula and DELAFIELD'Shematoxylin, and counterstained with Septifer virgatus were dominant in the platform eosin. from 43 cm to 141 cm tide levels near the study area To determine size at sexual maturity, 230 (FUJI & NOMURA,1990). Snails larger than 20 mm snails of shell length ranging from 7 to 29 mm were shell length were collected from area A (Fig. l) at randomly sampled from area A in the field (Fig, 1) monthly intervals from September 1987 to Septem- on 25 April 1988. After removing the shell, the ber 1988. To determine the seasonal gametogenic ovary and the seminal vesicle were dissected out cycle, histological preparations were done. The and embedded using the same method described length of the shell was measured, the shell was above. Decision of sexual maturity size was foll- cracked, and the sex was checked by the body owed HARVEY & VINCENT (1989). components. And the entire visceral masses (Fig. 2 Because the gonad and digestive gland are -A) from 40 snails of each sex were removed and interconnected and difficult to separate from each fixed in aqueous Bouin's solution. From this fixed other, the following method was used to determine

30 Reproductive biology of Nucella freycineti.

time of the first spring tide, from November 1987 to December 1988. An index (18)derived by MORISITA (1959) was calculated to measure the dispersion pattern of N. freycineti in the field. To know the copulating period, the number of snails in each quadrat and the number of copulating pairs were counted once a month from May 1990 to July 1991. The copulation was distinguished by insertion of a penis into the female. To learn the foraging activity, the number of foraging snails in each quadrat was counted once a month from April 1990 to June 1991. The foraging snails were checked by insertion of the proboscis into the prey. Surface sea water temperatures were monitor- ed every morning at Usujiri throughout the study period. Fig. 2 Diagram of Nucella freycineti showing the RESULTS visceral mass (A), and the cross-sections of the gonad-digestive gland complex (B). G) OOGENESIS gonad ; S) seminal vesicle ; D) digestive The developmental process of female germ gland cells was divided into five stages following TA- KAMARU& FUJI (1981) : the gonad index (G. L). The ovary-digestive gland 1) 4ogonia : These cells were oval, measuring 8-12 complex for the female and the testis-digestive p m in diameter with a thin cytoplasmic layer. The gland-seminal vesicle complex for the male were nucleus contained a few nucleoli and chromatin- divided into three parts : anterior, middle and pos- like granules (Fig. 3-A). terior (Fig. 2--A). Each part was serially sectioned 2) Previtellogenic oocytes : These cells were also and the G. L was calculated as follows : oval and measured 15-30 pm. The cytoplasm was

N scarce, stained basophilically and bulged from the G. L(%)= N x 3 G a2l+Sat1+Da1 follicle epithelium. The nucleus was large and had an enlarged nucleolus and dispersed chromatin (Fig. + Gm Ami + Api x 100 r+Smr+Dmi Gpi+Spt+Dpz 3-B). where N : total number of individuals, Aai : area 3) Early-vitellogenic oocytes : These oocytes were of gonad or seminal vesicle (only for male) in the irregular in shape, about 40-100 pm across, and had anterior part of individual Z,Gat : area of gonad in a round nucleus 35-40pm in diameter. Small yolk the anterior part of individual i, Dai : area of granules were present in the cytoplasm (Fig. 3-C). digestive gland in the anterior part of individual i, 4) Vitellogenic oocytes : At this stage, the oocytes Sat: area of seminal vesicle in the anterior part of were projected well into the follicles from 50 pm to individual i (only for males), mi and pr are the 230 pm. The yolk granules in the cytoplasm mea- respective areas of the middle and posterior parts sured 2-3pm in diameter (Fig. 3-D). of individual i (Fig. 2-B). 5) Mature oocytes : These included pre-mature Sixty-f our fixed quadrats (1 m x 1 m) were set and mature oocytes. The former were about 200- up in the study area (Fig. 1). The number of snails 300 pm and their cytoplasm was filled with in each quadrat was counted once a month at the various-sized yolk granules (Fig. 3-E). The latter

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Fig. 3 Gametogenesis in Nucella freycineti. (A) Oogonia ; (B) Previtellogenic oocyte ; (C) Early-vitellogenic oocyte ; (D) Vitellogenic oocyte ; (E) Pre-mature oocyte ; (F) Mature oocyte ; (G) Spermatogonia ; (H) Primary spermatocytes ; (I) Primary spermatocytes in the first meiotic division ; (J) Secondary spermatocytes ; (K) Spermatids ; (L) Spermatozoa. Scale bars=50 jcm.

32 Reproductive biology of Nucella freycineti.

were 200-400 um. They could be distinguished visible at the center of the cells (Fig. 3-I). After the from the pre-mature ones by the presence of minute primary meiotic division, the chromosomes in the yolk granules about 1 pm across surrounding the secondary spermatocytes (Fig. 3-J) appeared again, nucleus while larger granules about 10 pm in diam- and at this time they were scattered in the nucleus. eter filled the outer cytoplasm (Fig. 3-F). 3) Spermatids : The chromatids of these cells gath- SPERMATOGENESIS ered on one side of the nucleus, forming a meniscus The developmental process of the male germ or a bar (Fig. 3-K). cells was divided into four stages following FEARE 4) Spermatozoa : The head of the spermatozoon (1970) : was stained by hematoxylin and the tail by eosin 1) Spermatogonia : Each spermatogonium had an (Fig. 3-L). Until copulation, sperm were stored in oval nucleus 8-13pm across, containing a few the seminal vesicle. eosinophilic nucleoli (Fig. 3-G). DEVELOPMENTAL STAGES OF THE GONADS 2) Spermatocytes : There were two kinds of sper- The developmental stages of the gonads were matocytes, primary and secondary. Primary sper- classified according to the stage of germ cells matocytes (Fig. 3-H) were round, about 10 pm in which occupied over 50% of the area in the whole diameter. In primary meiotic division, chromo- section. In both female and male gonads, four somes that were attached to the spindles were stages were identified :

Fig. 4 Female gametogenic stages in Nucella freycineti. (A) Recovery stage ; (B) Active stage ; (C) Late- active stage ; (D) Early mature stage ; (E) Mature stage ; (F) Spent stage. Scale bars= 250 pm.

33 No. 45 Benthos Research Aug., 1993

1) Recovery stage : In this stage, the follicles were divided into two phases, active and late-active. In completely devoid of ripe gametes, although some the active phase, cells in the follicles were mainly oogonia, residual oocytes, yolk granules and oocytes in the early-vitellogenic stage (Fig. 4-B). In previtellogenic oocytes were present (Fig. 4-A). In the late-active phase, they were mostly vitellogenic the male gonad in this stage (Fig. 5-A), there were oocytes with a few mature oocytes. (Fig. 4-G). In no ripe gametes in the tubules, although some the testis, from the tubule wall to the lumen, the spermatocytes were present. cells were arranged in the following order : sper- 2) Active stage : The ovaries in this stage could be matogonia, spermatocytes and spermatids. Pri-

Fig. 5 Male gametogenic and seminal vesicle stages in Nucella freycineti. (A) Recovery stage ; (B) Active stage ; (G) Mature stage ; (D) Spent stage ; (E) Seminal vesicle : resting stage ; (F) Seminal vesicle : accumulating stage; (G) Seminal vesicle: spent atage. Scale bars= 250,cm.

34 Reproductive biology of Nucella freycineti.

mary spermatocytes were the most numerous and a sexed individuals were likewise equally divided few spermatozoa were present (Fig. 5-B). into each sex. About 50% of the females having a 3) Mature stage : Female follicles were in contact shell length of 15 mm were mature (Fig. 6). This with each other, each containing less than ten proportion reached 100% for females with a shell polygonal oocytes. In females, this stage was fur- length of about 19 mm. On the other hand, about ther classified into early mature and mature phases 20% of the males larger than 13 mm had seminal with each phase containing mostly pre-mature vesicles in the accumulating stage. This proportion oocytes (Fig. 4-D) or mature oocytes (Fig. 4-F), suddenly increased at 15 mm and reached a peak at respectively. In the testis, spermatozoa formed 17 mm. A considerable percentage of the males at dense masses toward the lumen of the tubule, while 17 mm was at the spent stage. This result reveals cells at earlier stages of development were less that the females larger than 19 mm in shell length numerous at the periphery (Fig. 5-C). and the males larger than 15 mm are sexually 4) Spent stage : Spent ovaries were characterized mature. by the absence of ripe oocytes and the presence of REPRODUCTIVE CYCLE only a few residual oocytes (Fig. 4-F). The periph- Histological examination revealed the sea- eral area of most of the tubules in the testis sonal maturation cycle in the population (Fig. 7). contained few spermatogonia and few or no sper- The recovery stage in females was from June to matozoa, while the lumina were totally empty (Fig. December. Males in the same stage were first 5-D).' DEVELOPMENTAL STAGES OF THE SEMINAL VESICLE The convoluted part of the vas deference func- tions as a seminal vesicle in N. freycineti. The developmental process of this vesicle was divided into three stages according to the features of its epithelium and the quantity of spermatozoa found inside. 1) Resting stage : The fibrillar connective tissue which formed the seminal vesicle was about 50 ,um thick and the lumen was devoid of spermatozoa (Fig. 5-E). 2) Accumulating stage : Many spermatozoa that look like scrollwork were accumulated in the seminal vesicle. The epithelial lining was thin compar- ed to the previous stage (Fig. 5-F). 3) Spent stage : Spermatozoa were still present but less numerous than in the previous stage. The epithelium had begun to thicken again (Fig. 5-G). Fig. 6 Proportion (%) of various gametogenic SIZE AT SEXUAL MATURITY stages (female, ovary ; male, seminal vesi- The snails were classified into male, female cle) by shell length. Number of samples is and unsexed individuals. The total numbers of about 10 for each group. a) Unsexed ; b) histological samples from January to September Recovery stage (female), Resting stage 1988 in males and females were 449 and 407, respe- (male) ; c) Active stage ; d) Mature stage ctively. The sex ratio of N. freycineti was 1:1 (female), Accumulating stage (male) ; e) (binomial test, z =1.12, p >0.05), therefore, the un- Spent stage.

35 No.45 Benthos Research Aug., 1993

quickly in May when about 90% were in spent condition. On the other hand, the frequency of spent testes increased from November and reached 100% in February while the seminal vesicles at the accumulating stage were at their peak. In the females, the gonad index gradually increased from October to January and reached a peak in April (Fig. 8). Beginning in May the index steadily declined (MANN-WHITNEY test, p<0.001), which showed that this was the breeding period. On the other hand, the index of the seminal vesicle was highest in December, two months behind the peak of the male gonad. The histological data obtained here suggest that the breeding season of N. freycineti is from March to May. The male gonad was in the spent to recovery stages then, while the seminal vesicle was in the accumulating to spent stages. From April 29, about 7760 egg capsules were observed in the area. SEASONAL COPULATION ACTIVITY IN THE FIELD Copulating pairs were observed from October to April (Fig. 9). The number was conspicuously large in December. Pairs were not found from May to September. Fig. 7 Diagram showing the proportion (%) of Nucella freycineti by gonad stage (A & B) and seminal vesicle stages (C). a) Spent stage ; b) Recovery stage (gonad), Resting stage (seminal vesicle) ; c) Active stage ; d) Late-active stage ; e) Early mature stage ; f) Mature stage (gonad), Accumulating stage (seminal vesicle).

encountered in March, and were continuously observed until October. Active and late-active ovaries were observed from July to February. In active development of the testis, the frequency increased markedly in July, and declined in Septem- ber. In August there was a sudden increase in the number of seminal vesicles at the accumulating stage. Mature ovaries appeared in November and Fig. 8 Seasonal changes in the gonad index (G. I.) peaked in April, while mature testes were present of Nucella freycineti. Vertical bars are from August to February. Mature ovaries declined standard deviation. n=40 for each sex.

36 Reproductive biology of Nucella freycineti.

FORGING ACTIVITY DISPERSION PATTERN Foraging snails were observed all year round in All year roung Is was over 1 and varied highly the field (Fig. 10). Foraging activity was high from (Fig. 11). This indicates that N. freycineti was dis- May to October, with a peaking in July and Octo- tributed contagiously (F test, p <0.01). From July ber. During the winter (January-March), the activ- to October the index ranged from 2.05 to 2.0, the ity was relatively low. lowest level during the year. At this time, the snails were found in the mussel zone. In November 1988 the index increased markedly to 3.27 and reached 5.05 in February of the next year. During these months, snails aggregated strongly in crevices or on rocks at the low intertidal level. In March, the index went down to 3.47 and went up again to 4.95 in May, which is the end of the breeding period. Mean surface sea water temperature fluctuated seasonally from 19°C to 3°C (Fig. 11).

DISCUSSION

DEVELOPMENT OF THE GONAD In Nucella freycineti, the development of the gonads and the seminal vesicle exhibits a distinct annual cycle. The annual cycles of the ovary and Fig. 9 Proportion (%) of copulating pairs of the seminal vesicle are synchronous. From July to Nucella freycineti in the fixed quadrats. September, the water temperature ranged from 13 The figure above each bar indicates the to 19°C, rising to its maximum in September (Fig. total number of pairs observed. 11). During this period, the ovary and the testis of N. freycineti developed markedly, although the release of gametes was marked by a time lag. Spent testes peaked from February to March, while spent ovaries did from May to June. MARTEL et al. (1986) suggested that spermatogenesis of the whelk Buccinum undatum might be stimulated by slight

Fig. 10 Number of foraging snails in the fixed quadrats. The figure above each bar indi- Fig. 11 Surface sea water temperature at the study cates the total number of foraging individ- site and seasonal changes in MORISITA uals observed. index.

37 No. 45 Benthos Research Aug., 1993

increase in temperatures. NIU & FUJI (1989) stated foraging period (May-June), but in the latter half that sea water temperature played a important role (the warmest months of July-September). For in reproductive activity of the limpet Collisella dogwhelks, growth and reproduction may compete heroldi. The lowest temperatures of both study for energy requirement and this competition may areas above mentioned were about 0°C. In the be avoided by a certain mechanism which these warmer area with lowest temperature 9.5°C in processes do not occur together (FEARE, 1970). In February, water temperature change showed no N. freycineti, the nutrients acquired during the ear- direct correlation with gametogenesis in Thais lier months of the feeding period might have been emarginata and T. canaliculata, although increasing used for the body growth such as somatic and shell temperature appeared to affect breeding in T. growth. canaliculata (HOUSTON, 1971). Gonadal change of COPULATION the abalone Haliotis cracheroidii showed no correla- Copulation was observed from October, when tion with seasonal changes in water temperature the seminal vesicle was in the accumulating stage, but with photoperiod and the lowest temperature to April, when the breeding period began. The was about 12°C in April (WEBBER & GIESE). Within greatest incidence of copulating Paris, about 61%, a short period of time, from July to August, more was found in December. MARTEL et al. (1986) than 90% of male N, freycineti became mature. hypothesized that pheromones from the female During high temperature and high foraging activity induce copulation in B. undatum in the subtidal period, the maturation of the testis was occurred. zone. N freycineti, however, lives in an intertidal However, the ovary does not show the similar area where wave action is strong, and where the tendency, because oogenesis was observed through snails are exposed to air for some hours. This the winter until the breeding time in the spring. hypothesis might not apply to N. freycineti. From These results agree with the previous studies on October to April, the recorded water temperature other species. FUJINAGA (1985) studied the repro- fluctuated heavily (3-15.8°C) and mature ovaries ductive cycle of Neptunea arthritica near Usujiri began to observe in October. It is possible that a and found that more than 90% of the males became certain trigger rather than pheromones and water mature in October, although the females were still temperature is important for copulation. More in the pre-developing stage TAKAMARU& FUJI detailed experimental studies are needed to reveal (1981) also reported the same trend in N, arthritica. the mechanism on this point. In this species males become mature from July to BREEDING August when temperatures are relatively high, and Histological examination showed that the fre- the ovary gradually grows until the breeding period quency of spent gonads was highest from March to in May. May. However, in the field, abundant egg capsules It is possible that high temperature was impor- were found on rocks in protected low-intertidal tant factor for marked gonad development in the area from the end of April to May. AMIO (1963) colder area. reported that among the neogastropods in the STICKLE (1973) suggested that the presence of Northwest Pacific Ocean, 75.7% had a summer prey was important for the increase in the body breeding period (June-August) while 16.2% had a component indices of T. lamellosa, During the spring breeding period (March-May). Spring breed- warmer period, N. freycineti were found in mussel ing in other Nucella species has also been reported beds foraging actively. In the laboratory, the forag- (MOORS, 1938; FEARE, 1970; GALLARDO, 1979). ing activity was relatively high from May to Octo- The newly hatched juvenile of N. freycineti is very ber, with a peak from July to September (KAWAI, small, about 0.9-1.3 mm in length (KAWAI, unpub- unpublished data). Rapid growth of the gonad was lished data). By the time the juveniles hatch out in not observed during the first half of the active the summer, the water temperature has warmed up

38 Reproductive biology of Nucella freycineti.

and their preys, small mussels and barnacles, were were observed from June to August and showed a observed in the study area (KAWAI, unpublished ak in the first week of July (KAWAI; unpublishedpe data). At this point, the environment may work to data). Breeding aggregation could be a possible favor further growth of the young. hield for the eggs against predators. From sJuly to AGGREGATION ctober, when temperatures were high, the snailsO I8 s howed that N. freycineti aggregated all year continued to aggregate, although the index values und. The observed tri-annual aggregation ropulses were relatively lower. During these months, high ing from April to June, from July to Octoberdur and foraging activity and marked gonad development from November to March (although the values were observed and most males had mature gonads. were lower in the summer, they were still above 1) BROWN and RICHARDSON (1987) suggested that ggest that this behavior serves more other func-su aggregated dispersions might be important, tion than the copulation. FEARE (1971) identified because when snails began to forage in groups, they three types of aggregation in N. lapillus ; summer could attack larger prey. Prey consumption by N. for foraging, winter for protection against wave freycineti was highest from July to September action, and pre-breeding for copulation. (KAWAI, unpublished data). Summer aggregation In N. freycineti I8 was highest from November may be related with the high foraging activity to February when the temperature showed range displayed by the snails. from 3 to 9.8°C. This is winter aggregation and the A complex relationship between reproduction snails were found grouped in the crevice or on (gonad development, copulation and breeding) and protected place of low intertidal area away from dispersion pattern was shown throughout the year. strong wave action. LARGEN (1967) found that Snails aggregated strongly between the copulation when N. lapillus was dislodged at 5°C they were and breeding period, but they were relatively unable to regain a foothold and were rolled over dispersed during the period of gonad development. even by slight water movements. He suggested that ACKNOWLEDGMENTS winter aggregation was a defense mechanism to reduce the chances of dislodgment. Peak copula- We wish to thank A. FUJI, S. GOSHIMA and F. tion time in N freycineti was recorded in December. AMAZAKI of Hokkaido University for their Yhelp- Because the snails aggregated in crevices or on ggestions. We also express our thanks toful R. su protected places during the cold period, they could GAMBOA for technical comments on earlier ver- find a mate easily neither to move longer nor to sions of the manuscript. We are also grateful to the fer wave action. Here winter aggregation couldsuf staff of the Maeiculture Laboratory, Hokkaido hance the success in finding a mate. The enindex University, for their help both in the field and in the declined in March, the end of winter, and reached laboratory. another peak in spring in the month of May. Spring REFERENCES was the season for breeding. Observations in each uadrat revealed that the snails moved fromq low ABE, N., 1983. Breeding of Thais clavigera (KUS- intertidal rocks to higher rocks (KAWAI, personal TEE) and predation of its eggs by Cronia observation). The decline and rise of the index margariticola (BRODERIP). Proc. Sec. Interna- values could mean that the site of winter aggrega- tional workshop on the malacofauna of Tong tion is different from that of breeding aggregation. Kong and southern China, Hong Kong, 381- In June, when breeding was finished, the index 392. remained at a high level. ABE (1983) stated that AMIO, M., 1963. A comparative embryology of masses of egg capsule of Thais clavigera could be marine gastropods, with ecological considera- protected from the predators. In N, freycineti a tions, f. Shimonoseki Coll. Fish., 12: 229-353 mber of egg capsules suffering from predationnu (In Japanese with English abstract).

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BROWN,K. M. and T. D. RICHARDSON,1987. Forag- lapillus (Gastropods : Prosobranchia). J. ing ecology of the sourhern oyster drill Thais Anim. Ecol., 36: 207-214. haemastoma (GRAY) : Constraints on prey MARTEL, A., D. H. LARRIVEE,K. R. KLEIN , and. J. choice. J. Exp. Mar. Biol. Ecol., 114: 123-141. H. HIMMELMAN,1986. Reproductive cycle and FEARE, C. J., 1970. The reproductive cycle of the seasonal feeding activity of the neogastopod dog whelk (Nucella lapillus). Proc. Malac. Soc. Buccinum undatum. Mar. Biol., 92 211-221. ond., 39: 125-137. L MOORE, H. B., 1938. The biology of Purpura lapil- FEARE, C. J., 1971. The adaptive significance of us. III. Life history and relation to environ- l aggregation behavior in the dogwhelk Nucella mental factors. J. Mar. Biol. Ass. U. K., 23: 67 lapillus (L.). Oecologia, 7 : 117-126. FUJI -74 . , A. and H. NOMURA, 1990. Community struc- MORISITA, M., 1959. Measuring of the dispersion of ture of the rocky shore macrobenthos in south- individual and analysis of the distributional ern Hokkaido, Japan. Mar. Biol., 107: 471-477. patterns. Mem. Fac. Sci., Kyushu Univ., Ser. E INAGA, K., 1985. The reproductive ecologyFUJ of (Biol.), 2 : 215-235 (In Japanese). the neptune whelk (Neptunea arthritics BER- NIU, C, and A. FUJI, 1989. Gametogenesis and NARDI) population, with special reference to reproductive cycle of the limpet Collisella her- the reproductive cycles, depositions of egg oldi (DUNKER,1861). Bull. Fac. Fish. Hokkaido masses and hatchings of juveniles. Bull. Fac. Univ., 40: 214-227. Fish. Hokkaido Univ., 36: 87-98 (In Japanese SPIGHT, T. M., 1975. Factors extending gastropod with English abstract). embryonic development and their selective GALLARDO, C. S.,1979. Developmental pattern and cost. Oecologia, 21: 1-16. adaptations for reproduction in Nucella SPIGHT, T. M., 1976. Hatching size and the distri- crassilabrum and other muricacean gastropods. bution of nurse eggs among prosobranch em- Biol. Bull. 157: 453-463. bryos. Biol. Bull., 150: 491-499. GIESE, A. C., 1959. Comparative physiology : SPIGHT, T. M., 1977. Do intertidal snails spawn in Annual reproductive cycles of marine inverte- the right places? Evolution, 31: 682-691. brates. Ann. Rev. Physiol., 21: 547-576. STICKLE, W. B.,1973. The reproductive physiology HARVEY, M. and B. VINCENT, 1989. Spatial and the intertidal prosobranch Thais oflamellosa temporal variations of the reproductive cycle (GMELIN). I. Seasonal changes in the rate of and energy allocation of the bivalve Macoma gee consumption and body component oxy .in- balthica (L.) on a tidal flat. J. Exp. Mar. Biol. xes. Biol. Bull., 144: 511-524. de Ecol., 129: 199-217. TAKAHASHI, N., K. TAKANO and S. MURAI, 1972. HOUSTON, R. S., 1971. ReprOductive biology of Histological studies on the reproductive cycle Thais emarginata (DESHAYES, 1839) and T. the male neptune whelk, ofNeptunea Arth- canaliculata (DUCLOS,1832). Veliger,13 : 348- itica. Bull. Fac. Fish. Hokkaido Univ., 23: r65- 357. 72 (In Japanese with English abstract). KON, T., Y. HONMA, and S. MURAKAWA, 1966. TAKAMARU, N, and A. FUJI, 1981. Reproductive Studies on the maturity of gonad in some cle of the neptune whelk, Neptunea cy arthritica marine invertebrates-I. Seasonal changes in (BERNARDI), in southern Hokkaido. the gonads of prosobranch mollusc, Purpura Aquaculture, 29: 78-87 (In Japanese with Eng- (Mancinella) clavigera. Bull. Jap. Soc. Sci. Fish., ish abstract). l 32: 484 - 491 (In Japanese with English WEBBER, H. H. and A. C. GIESE, 1969.. Reproduc- abstract). tive cycle and gametogenesis in the black aba- LARGEN, M. J., 1967. The influence of water tem- one Haliotis cracheroidii (Gastropoda l perature upon the life of the dog-whelk Thais Prosobranchiata). Mar. Biol., 4 : 152-159.

40 Reproductive biology of Nucella freycineti.

低水温期を通して産卵期までゆっくりと生殖腺を発達和文摘要させていた.各期の季節変化に雌雄で異なった傾向が河合渓・中尾繁:チヂミボラN鰯6伽加ッ6勿観あることが示唆された。一方,卵巣と貯精嚢の発達過 (DESH:AYES)の生殖周期と交尾頻度および分布の集程には同調的な季節変化が示された。性成熟サイズは中度。雄で殻長15mm,雌で殻長19mmであった。10月から見北海道南部臼尻潮間帯において,1987年9月からられた交尾は,12月に全交尾対数の約61%が観察され, 1988年12月まで毎月採集したチヂミボラN%06〃 α その後産卵期直前までの7ヶ月間にわたって行われて〃6ッ6勿観(DESHAYES)をもとにして,生殖周期,性いた。産卵期は4月～5月と考えられる。1δ指数は調成熟サイズ,交尾期,産卵期を,また,毎月の定点調査期間中を通して1以上の値を示しており,チヂミボ査より,森下の1δ指数を求め,分布の集中度にっいてラは周年にわたり集申分布をしていることがわかった。検討を行った31990年4月から1991年7月には交尾頻摂食が活動に見られる夏期には比較的低い集中分布度と摂食活動にっいて検討を行った、そして,これら (1δ篇2.05～2.20)をしているが,交尾期と産卵期の冬の結果と水温との関係にっいて考察した。生殖腺発達～春期にはより高い集中分布(1δ=3 .27～6.75)をして過程は雌雄共に回復期,成長期,成熟期,放出終了期いることが分かった。の4期に,また,雄個体の貯精嚢の発達過程は休止期, 貯留期,放出期の3期に分類した.精巣と卵巣の発達 KEI KAWAI 過程は,共に年周期を示し,雌雄共に高水温期の6月 Laboratory of Mariculture, Faculty of Fisheries, ～10月に著しい生殖腺の発達を示した。10月には雄の Hokkaido University. 90%以上が成熟し,貯留期の貯精嚢を所有していた. Minato-cho 3-1-1, Hakodate, Hokkaido 041, Japan 一方 ,雌は高水温期に生殖腺を著しく発達させた後,