Benthos Research Vol.55,No.2:43-51(2000) BENTHOS RESEARCH The Japanese Association of Benthology

Age Determination and Seasonal Growth of the Dogwhelk freycineti(Deshayes)

Kei Kawai

Marine Biodiversity Laboratory,Faculty of Fisheries,Hokkaido University,Minato3-1-1, Hakodate,Hokkaido041-8611,Japan

Abstract:Growth patterns in the shell and soft parts of the dogwhelk Nucella freycineti were examined. Growth rings in the shells were investigated by X-ray photography and were shown to form annually.In snails that hatched in summer,the first rings formed in the first winter.The shell growth equation was determined based on the age character,population age structure,seasonal growth rate and size frequency distribution of the population.The maximum shell growth occurred in summer.The life span was esti mated to be>11years.Low physiological activity and/or starvation induced by low temperature might be main factor(s)causing the formation of annual rings,although age might also influence ring forma tion.Total body weight increased in late summer in males and from late summer to winter in females. Gonad weight showed a similar trend in each sex.After the reproductive season,shell growth occurred in summer,and body weight increased from summer to winter.These growth characteristics might promote higher survival and fitness.

Key words:annual ring,energy allocation,gender,growth,Nucella

spans(Crisp1984;Tamai1988). INTRODUCTION Energy allocation between growth and reproduc tion has also been a central topic in life history studies. Growth has received considerable attention in life his Many reseachers have studied the relationship among tory studies,and the starting point of any comprehen reproduction,shell growth and soft part growth in gas sive analysis of life history is the aging of individuals tropods(e.g.Webber1970;Stickle1973).Differences in in a population(e.g.Roff1992;Stearns1994).Gastro reproduction and growth between males and females pods and bivalves have been aged using rings on their have also been studied.The synchronized reproductive shell surfaces(e.g.Uno1962;Williamson&Kendall output periods in males and females in Nucella lapillus 1981;Goshima et al.1991;Kawai et al.1993).How (see Feare1970a)and lamellosa(see Stickle1973) ever,many have no such distinct characters.In suggest that in both ,males and females have such cases,the size frequency distribution is commonly similar body growth patterns.However,males and fe divided into each age class using the arithmetic prob males of the dogwhelk N.freycineti have completely ability method described by Harding(1949)(Goodwin different reproductive cycles(Kawai&Nakao1993). 1978;Gardner&Thomas1987;Staikou et al.1988),but Therefore,males and females may have different this method is not applicable for animals with long life growth patterns and allocate energy differently. The objectives of this research were to find shell characters that can be used for aging N.freycineti,to Received April14,2000:Accepted September22,2000 *Corresponding author.Present address:Research Cen determine its growth equation,to examine the growth ter for the Pacific Islands,Kagoshima University, patterns of soft parts and shells in males and females, Kourimoto1-21-24,Kagoshima890-8580,Japan. and to discuss different energy allocation patterns

43 Kawai

between males and females,and between shells and soft To ascertain the reliability of the bands as growth parts. markers,the time and cumulative frequency of their formation were determined by observing the shell edges.To estimate the shell length at the time of band MATERIALS AND METHODS formation,a linear regression equation of shell length against shell diameter was calculated.Since males and Sampling was carried out monthly at Usujiri(41•K57'N, females of Neptunea arthritica had different reproduc 140•K58'E),Hokkaido,Japan from September1987to tive cycles (Fujinaga1985)but similar shell growth September1991.Details of the study site are given in patterns(Fujinaga1987),I assumed that the shell Kawai&Nakao(1993).To examine the ring formation, growth of Nucella freycineti is also similar between about30dogwhelks were randomly collected every males and females. month at area A(Fig.1)during spring from To compensate for the problem in the use of the August1987to September1988.After each shell length arithmetic probability method for long life-span ani was measured with a caliper,the shell was cut from the mals,I divided the monthly size-frequency distributions second spiral rib in the vertically against into each age class based on the age distribution in the the columella.The inside of the shell,including the field sample determined by ring analysis,and the sea apex,was removed with a small grinder.About390 sonal growth rate of each age class.The age snails treated in this manner were filed using distribution study was carried out monthly from De

paper, steeped in0.1N Hydrochloric acid for12hours, cember1987to December1988and from April1989to and then photographed using X-ray photography September1992at70stations(area B)(Fig.1)using a (CMB-2,Softex Inc.).Bands in the photos were identi 1x1m2quadrat.Six subtidal stations were observed fied and the shell diameter of each band was measured. from December1987to December1988,but eliminated in the latter survey because no dogwhelks were observed at these stations.After measuring their shell lengths in the field,they were returned to their original positions in the field.To determine the age distribution,all dogwhelks at64stations were collected in September 1992and aged by the methods mentioned earlier.To de termine the seasonal changes in mean shell length in each age class,samples were collected from15stations (area C)(Fig.1)in June,September,December1991 and March1992.Ages in each sample were determined by the method descrived above.The size frequency dis tributions in area B were divided into each age class using a computer program(Tsutsumi&Tanaka1987), based on the population age structure in September1992 and the seasonal mean shell length of each age class in area C.To construct the growth curve,mean shell lengths at successive growth bands were fitted to the von Bertalanffy equation,which was modified by Moreau(1987)as follows:

Lt=L•‡(1-exp(-k(t/12t0)+A sin

(2ƒÎ(t/12-ts)))),

where Lt,is the shell length(mm)at time t(month),

L•‡is the theoretical maximal shell length(mm),k is a

growth constant,t0is the theoretical time(month) when the shell length equals zero,A is ck/2ƒÎ,c is a con Fig.1.Map showing the study areas(A,B and C)and ap stant of fluctuation in monthly growth,and ts is the proximate height in meter from M.T.L.Black circles time(month)from t0to the beginning of the first fluc show the sampling stations. tuation of shell growth.Parameters of the equation

44

Œû‘¸/AB•ç•œd•œƒS'.'•ç‡_..‹œ‡_‚ïƒÌ"6'•A•E•E.•‰•B.•E•E•c.—•9..'‚•99/Om440•œHokkaido•œ•`“±;}.•E42•E•œ/ŽOUsujiri•E‚ñ.q•E•E'“K•E4•E.•E42.•E44.'Ž¢•œ•A•c•`•`6Š••A•E•E•••E•œŽOƒÁ•A•œ•œ..•E•E!tq‘Ï•E...Šs•E•E•B'•œ"•œ'50m'•E.•œ•B•B•E•B50..•œ./.ƒ{8.ƒ{'•‘‹¿•œƒÁ•E’Ê•Eˆñ‰T'•E.c•ˆ.!•œ•A•E'•œ•‰!•œ.'•E•Emáo•œ.•œ.•œ•œmle/“ñ7•œ•œ•œ Growth in Nucella freycineti

were calculated by a computer program using the sim 100 plex method(Okumura1986). Using the formula describing the relationships δ among shell length,total soft part dry weight and 呂75 ・∈ gonad in each sex(Kawai1993),and the von Bertalanffy equation determined in this research, 畜 monthly dry weights of each part in each age classwere ε5・ calculated.The sizesat maturity of males and females 皇 ・ § were15mm and19mm,respectively(Kawai&Nakao 1993).For snails smaller than these sizes,the equation §25 for the sex-undetermined classwas used. L/

O ASONDJFMAMJJAS Month RESULTS

Rings as an age character and age determination Fig.3.Diagram showing the proportion(%)of the ani mals with a new band at the shell margin from August Growth rings were clearly observed in the X-ray photos 1987to September1988. (Fig.2).White-colored rings were distinguished from black-colored parts.About5%of the specimens had

formed a new ring by August(Fig.3).The frequency of 40Jun.1990 dogwhelks with a new ring steeply increased from No- 30 vember,reaching100%in February.

The liner regression equation between shell length 20

(SL)and shell diameter(SD)was SL=1.48SD-0.97 10

(r2=0.97,n=50).The maximum number of rings ob 0 served was eleven.The mean(±SD)shell lengths for

ring#1,2,3,4,5,6,7and8were6.01±2.20,12.05 40Sep .1990 ±1.20,16.40±1.23,19.64±2.01,23.99±3.01,25.90 30 ±2 .20,27.01±3.05,and28.12±2.10mm,respectively.

The mean shell length of the newly settled dogwhelks in毒諜、伽._、.藤 ω20 冠

';弓10

も0 .≡

逼40D。 、.1990 230 ∈

≡20,

10

0

40Mar ,1991

30

20

10

0 12340

Fig.2.Growth bands in an adult Shelllength(mm》 Numbers show each growth band,andNucella freycineti.d7corresponds to Fig.4.Size-frequency distribution of shell length at sta the diameter of the7th ring formation. tion C from June1990to March1991.

45 Kawai

Table1.Mean shell length(mm•}SD)in each age class February in the field was5.25•}1.53mm and was not

from June1990to March199 1.MonthAgeJun.Sep.Dec.Mar.17.72•}2.5410.54•}4.14212.75•}2.1915.0217.91•}0.3916.67•}1•B15318.64•}3.7219.22•}4.2719.35•}2.0621.27•}5.00421.82•}4.6922.97•}5.2523.43•}4.6424.55•}3.35524.46•}3.4725.13•}6.0324.58•}3.5227.58•}8.07626.71•}5.5228.62•}9.1027.87•}4.2727.81•}1.11727.91•}6.5431.69•}6.9528.64•}4.8733.01•}7.05828.70•}2.4835.61937.85 significantly different from the mean shell length of

ring#1(U-test,P>0.05),suggesting that the first

ring recognized in the X-ray photos formed in the first

winter for newly hatched snails.

Growth equation

One main peak was observed in the size-frequency dis tribution of snails at area C in June1991,and one more distinct peak appeared in September and December 1991 (Fig.4).The number of the small-sized snails(<10 m)increased in March 1992.Ages of the snailsm in each month were determined by ring analysis(Table1).One large and a few small cohorts was observed at area B

Table2.Monthly mean shell length(mm)and standard deviation in each year class as determined by the growth ring . Samples were taken from1987to1991.

YearClassMonthNo.1990198919881987198619851984198319821981Dec.1987140911.4•}1.716.0•}1.519.6•}1.322.4•}1.325.5•}1.529.1•}1.5Jan.1988144912.2•}1.616.3•}1.619.6•}1.422.4•}1.325.4•}1.429.0•}2.OFeb.151912.7•}2.618.0•}1.021.0•}1.224.0•}1.026.0•}0.929.0•}1.3Mar.10336.2•}1.511.6•}2.216.4•}1.620.0•}1.523.1•}2.026.4•}2.031.2•}4.1Apr.10377.4•}1.612.7•}1.917.6•}1.321.0•}1.224.4•}1.327.5•}1.230.9•}4.5May9927.7•}1.713.0•}2.418.4•}1.621.5•}1.525.0•}2.029.9•}2.534.7•}3.2Jun.13007.7•}1.711.7•}1.717.0•}1.721.5•}1.124.5•}1.126.1•}1.829.0•}3.OJul.130810.4•}1.514.6•}1.619.0•}1.322.0•}1.024.6•}1.727.1•}1.630.9•}2.OAug.10978.5•}1.715.1•}2.420.0•}1.723.0•}1.325.4•}1.528.5•}1.632.0•}2.3Sep.106610.0•}1.815.4•}1.119.1•}1.122.0•}1.224.6•}1.227.2•}2.130.9•}1.70ct.103012.1•}1.216.5•}1.519.6•}1.322.4•}1.425.1•}1.428.0•}1.830.8•}3.1Nov.81213.0•}3.117.2•}2.519.8•}1.623.2•}1.326.0•}1.028.0•}1.432.0•}1.5Dec.91412.6•}1.617.4•}1.821.1•}1.124.0•}1.227.6•}1.432.0•}0.9Apr.19894575.6•}5.712.3•}2.317.5•}1.421.5•}1.024.4•}1.127.6•}0.8Apr.19905408.0•}1.113.0•}1.417.0•}1.821.0•}1.725.0•}1.027.5•}1.332.0•}1.5May6066.1•}2.013.2•}1.417.4•}1.521.3•}1.824.4•}1.327.6•}1.332.0•}1.8Jun.7798.0•}1.612.9•}2.118.6•}1.321.6•}1.324.4•}1.528.0•}2.032.4•}2.5Jul.6128.0•}0.912.0•}1.019.0•}1.622.0•}1.224.7•}1.426.9•}1.829.8•}2.2Aug.47012.0•}1.115.0•}3.119.0•}1.222.0•}1.425.4•}1.929.0•}1.532.1•}1.9Sep.45412.0•}1.814.0•}0.919.5•}2.223.0•}1.826.0•}1.829.1•}1.432.1•}1.70ct.4759.0•}2.214.0•}1.819.6•}1.823.0•}1.126.0•}1.429.0•}1.032.0•}1.2Nov.46811.6•}1.515.0•}0.719.0•}1.322.4•}1.426.0•}1.729.0•}1.431.8•}1.8Dec.5475.0•}0.012.1•}1.916.0•}1.219.5•}1.922.5•}1.325.0•}1.128.3•}1.533.0•}1.6Jan.19915406.0•}0.010.2•}1.318.0•}2.020.9•}1.423.6•}1.026.0•}0.728.0•}0.630.9•}2.OFeb.3086.3•}2.512.5•}1.316.9•}1.421.1•}1.324.5•}1.725.6•}2.430.7•}2.6Mar.4715.8•}1.310.7•}2.417.6•}2.520.9•}2.124.2•}1.527.0•}2.132.0•}1.9Apr.5617.0•}0.911.8•}0.717.5•}2.022.0•}1.524.7•}0.826.9•}1.831.1•}2.5May5548.9•}0.713.1•}1.917.6•}1.120.7•}0.923.2•}1.526.6•}2.230.8•}3.3Jun.5136.0•}5.413.1•}1.218.0•}1.821.4•}1.324.6•}1.127.0•}1.832.0•}0.9Jul.5498.0•}2.114.1•}1.518.7•}1.121.5•}1.124.5•}1.327.0•}2.130.4•}4.7Sep.549}7.8•}1.515.0•}2.219.6•}1.322.3•}1.524.8•}1.326.9•}2.030.1•}5.146 Growth in Nucella freycineti

140Dec .198788J1990Feb,1991 120n =13877n塁311 1器

=

蒐

;::Jan、19888Jul・1990Mar・1991 100n314229n=633n=437 = £ o

胴oF eb.19888A1990Apr.1991

100n=15498n=539 80 60 40 20 0

個。M19888Sep .1990May1991

1001n=456n=581 80 60 紛 20 0

個0 88Dec,19880ct.1990Jun,1991

1004n=86gn=465n=497 80

器

鴛

1;:8Apr・198gN・v.1990Jul.1991 10◎n・=477n=479n=479 80

宏

鷺

:1:Jun・1988Apr.1990Dec・1990Sep.1991 100n=1314n=526n3532n塁549 00 60 紛 20 0 10203040

11:Jul・19880Jan.1991 100n31332n=526

80 60

紛 20

0 102030401020304010203040

Shell length(mm)

Fig.5.Size-frequency distribution of shell length at station B from December1987to September1991.

47

Number of snails Kawai

40 from December1987to September1991(Fig.5).The

monthly size-frequency distribution was divided into

about7age classes(Table2)based on the age distribu 1E30・.:.;'● ●.●・ EO、 ㌔.・.・".' )㌦=覧' tion in September1991in area B and seasonal growth 」昌..。"

留20,三 ・ ●…'・●● rate in area C. 』盛.。:…'= On the basis of the mean shell length at each ring,

2.・'1・ …i..' oり10・.・ ・ the growth equation was calculated as follows(Fig.6):

Lt=44.66(1-exp(-0.16(t/12+0.27)+ 0 0.01sin(2ƒÎ(t/12-0.63)))) 012243648(10728496108120

Age in month Growth of soft parts

Fig.6.The growth curve for shell length versus age in Fig.7shows the seasonal changes in total body weight months.Dots show monthly mean shell length in each age in each sex.In males,body weight increased from class. August,but decreased from October until February in 5-to7-year-old specimens.Likewise,younger male snails decreased in weight from December to February. 一一 回一 〇YEARGROUP-一 一1トー4YEARGROUP

一一 ◆一一一1YEARGROUP--o--5YEARGROUP On the other hand,the weights of females increased -「 ■一一2YEARGROUP-一 」一一6YEARGROUP from September to February or April,although there → 一一3YEARGROUP→ 一一7YEARGROUP O.5 was a fluctuation during this period.The seasonal pat tern of testis weights was distinctly different from

0.4 that of ovary weights(Fig.8).In males,the highest value was observed in October,but in females the high

0.3 est value was observed from February to April.

0.05 A+3yeargroupl 0.1 +4yeargroup

6ご O.04+5yeargroup → ←-6yeargroup

'～5号o.o・ ・1・.・ ・1・` I+7yeargroup O.03一 響}}}

0 0.02 0.5

90.01

0.4 だ 9 茎o >0・08 も8 0.2 霊 ぎo・06 0.1 0

0.04 0.0・ ・.・ ・ ● 昏'. JASONDJFMAMJ

Month 0.02

Fig.7.Growth curve in total body weight(g)for each age 0 JASONDJFMAMJ group of males(A)and females(B). Month

Fig.8.Growth curve expressed in gonad dry weight(g) for each age group of males(A)and females(B).

48 Growth in Nucella freycineti

Different body growth patterns were observed be

DISCUSSION tween the sexes(Fig.7).The cost of reproduction,

availability of prey and starvation induced by low tem

In the present study,rings were observed with X-ray peratures are considered the main factors that affect photography and used as growth markers.Generally, the seasonality of body weight of Thais(Nucella) such rings are observed on the shell surface in marine lamellosa(see Stickle1973),and the cost of reproduc gastropods(e.g.Uno1962;Williamson&Kendall tion(oxygen consumption and decrease of body weight) 1981).However,it is very difficult to observe these is very high in both sexes.In a laboratory study,most rings in N.freycineti because the shell surface in this female Neptunea antiqua died within3months after species is complicated.In this case,examination by X spawning due to exhaustion(Pearce&Thorson1967). ray photograph is a very useful method. In the present study,the body weight of Nucella

Many biological(predator,availability of prey,re freycineti decreased considerably in the copulating pe production,sex,and age)(Moore1938;Feare1970b; riod in males and spawning period in females(Fig.7). Palmer1983;Chow1987;Erlandsson&Johannesson On the other hand,the lowest temperature was

1994)and physical factors(temperature,microhabitat, observed in February.Body weight of females slightly and wave action)(Ekaratne&Crisp1984;Gosselin& dropped in February but soon increased in March.The

Bourget1989;Etter1994)can influence shell growth in lowest value in males occurred when water tempera gastropods.The effect of temperature,reproduction tures were low.However,this coincided with the main and availability of prey can be periodical.Rings in copulating period(from December to February)

Nucella freycineti formed annually(Fig.3),and the (Kawai&Nakao1993).As mentioned before,many first rings formed during the first winter in newly prey were present in the of the dogwhelks. hatched snails.The reproductive periods differ between Therefore,reproduction could be a more influential fac the sexes(Kawai&Nakao1993).The copulating period tor on body growth,although starvation induced by was from October to April,and females produced egg low temperature might also have an effect. capsules from April to June.Moreover,the age at first The timing of allocation of food intake and energy maturation was2.5and3.5years old in males and fe storage has been the focus of recent life history studies males,respectively.The main prey of N.freycineti is (Doughty&Shine1998).The soft parts(foot and di the Septifer virgatus(see Kawai1993),and the gestive gland)of gastropods function to store energy mussel density remained high throughout the year.This (Webber1970;Stickle1973).N.lapillus does not feed suggests that there was enough prey available through at low temperatures(especially below5•Ž)in the labo the year at Usujiri.However,the lowest temperature in ratory(Largen1967).Winter water temperature in the the research area occurred in February.When tempera present research area was about2•Ž,and feeding in the tures are low,dogwhelks aggregate in crevices,stop field is seldom observed in winter(Kawai&Nakao feeding and decrease their physiological activity 1993).Although female body weights were high in win (Kawai1993;see also Largen1967;Feare1971).On the ter,shells did not grow in winter(Figs.3and7).This other hand,although all individuals had formed rings suggests that stored energy was not allocated into shell by winter,rings formed as early as August in the same formation in winter.On the other hand,the maximum specimens(Fig.3).N.lapillus shells stop growing when shell growth rate was observed in summer(Fig.6and they reach the mature size(e.g.Fear1970b),however Table1).Feeding activity in the field is very high in shells of N.freycineti continuied to grow slightly after summer(Kawai&Nakao1993),and body weights in reaching this size(Fig.6).Because shell growth was both sexes were relatively light.Therefore,the energy highest in summer in this study,shell growth of large from food intake might be directly allocated into shell adult dogwhelks might occur only in summer and stop growth in summer. in the other seasons.Therefore,ring formation would Testes matured rapidly in September(Fig.8;see start after summer in large adults,and the rate of indi also Kawai&Nakao1993).Body weights increased viduals with rings might continuously increase until from September.Feeding activity of N.freycineti in the winter.Accordingly,decreasing temperatures and field is higher from summer to autumn(Kawai& starvation induced by low temperature might be the Nakao1993).Both growth patterns of testes and body main factor(s)that cause the annual rings of N. weight corresponded with feeding activity.Accord freycineti to form.Moreover,size might also influence ingly,the maturation of testes was synchronized with the time of ring formation. body growth,and energy for both testes and body

49 Kawai

weight was supplied by food intake.On the other hand, activities. ovaries developed in winter.However,body weight of females did not decrease even in winter in spite of their low feeding activity.Energy from food was first stored REFERENCES in the body,and then the ovary eventually developed from the energy stored in the foot or digestive gland. Chow,V.1987.Patterns of growth and energy allocation Both sexes showed different reproductive cycles in northern California population of Littorina and body growth patterns(Figs.7and8).Males ma (:Prosobranchia).Journal of Experimen tured before winter,while females matured after win tal Marine Biology and Ecology,110:69-89. ter.The origin of the energy supply for testes and ova Crisp,D.J.1984.Energy flow measurements.In,Methods ries might be different.Doughty&Shine(1998)showed for the Study of Marine Benthos,Holme,N.A.and that reptile females with large energy stores produce A.D.,McIntyre(eds.),IBP handbook No.16, large litters in the following year.Because of low tem Blackwell,Oxford,pp.284-372. peratures,dogwhelks can not feed during winter Doughty,P.and R.Shine1998.Reproductive energy allo (Kawai&Nakao1993).But females need to store much cation and long-term energy stores in a viviparous liz energy for wintering and spawning,because the cost of ard(Eulamprus tympanum).Ecology,79:1073-1083. female reproduction is very high(Stickle1973)and Ekaratne,S.U.K.and D.J.Crisp1984.Seasonal growth feeding activity in winter is very low in N.freycineti. studies of intertidal gastropods from shell microgrowth This suggests that the feeding activity of female band measurements,including a comparison with al dogwhelks before winter strongly influence reproduc ternative methods.Journal of the Marine Biological As tion in the following spring as well as the survival rate sociation of the United Kingdom,64:183-210. during winter.On the other hand,males started copula Erlandsson,J.and K.Johannesson1994.Sexual selection tion from October.Because dogwhelks aggregate in of female size in marine snail,Littorina littorea(L.). winter,males can easily find females to copulate. Journal of Experimental Marine Biology and Ecology, Therefore,the amount of allocation of intake energy 181:145-157. into testis will directly influence fitness.Because of Etter,R.J.1994.The effect of wave action,prey type, and this energy allocation,survival rates might decrease in time on growth of the predatory snail Nucella winter,but males can increase their fitness. lapillus(L.).Journal of Experimental Marine Biology Shell growth occurred in summer and body weight and Ecology,196:341-356. increased from summer to winter.Larger shell size Feare,C.J.1970a.The reproductive cycle of the dogwhelk helps increase the tolerance against lethal environ (Nucella lapillus).Proceedings of the Malacological mental factors(predator,desiccation and wave action, Society of London,39:125-137. etc.)in many gastropods(Hughes1986).The mortality Feare,C.J.1970b.Aspect of the ecology of an exposed of N.lapillus decreases with increasing size(Feare shore population of the dogwhelks Nucella lapillus 1970b).On the other hand,generally soft part growth (L.).Oecologia,5:1-18. and the reproductive output were usually restricted by Feare,C.J.1971.The adaptive significance of aggrega the volume of the shells,and larger snails have bigger tion behaviour in the dogwhelk Nucella lapillus(L.). shell volumes.Therefore,the early growth period of Oecologia,7:117-126. shells prior to the growth of soft parts increases the Fujinaga,K.1985.The reproductive ecology of the ability to store enough energy during winter and will neptunea (Neptunea arthritica Bernardi)popula result in higher reproductive outputs.This means that tion,with special reference to the reproductive cycles, these growth patterns increase the survival rates and depositions of egg masses and hatchings of juveniles. fitness. Bulletin of the Faculty of Fisheries,Hokkaido Univer sity,36:87-98(in Japanese). Acknowledgments.I am grateful to A.Fuji,S.Nakao Fujinaga,K.1987.On the growth pattern of the neptune and S.Goshima for their advice during the study and to whelk Neptunea arthritica Bernardi.Bulletin of the G.Shinohara for his technical support on X-ray photog Faculty of Fisheries,Hokkaido University,38:191-202. raphy.I also thank A.Ilano for improving the English Gardner,J.P.A and M.L.H.Thomas1987.Growth, text and the members of the Marine Biodiversity Labo mortality and production of organic matter by a rocky ratory and Usujiri Marine Station,Hokkaido Univer intertidal population of Mytilus edulis in the Quoddy re sity for their help in both the field and laboratory gion of the Bay of Fundy.Marine Ecology Progress

50 Growth in Nucella freycineti

Series,39:31-36. Okumura,H.1986.Introduction to data analysis by com Goodwin,B.J.1978.The growth and breeding cycle of puter,Gijyutsu Hyouron Nyuumon,Tokyo,244pp(in Littorina obtusata(Gastropoda:Prosobranchia) from Japanese). Cardigan Bay.Journal of Molluscan Studies,44:231- Palmer,A.R.1983.Growth rate as a measure of food 242. value in thaidid gastropods:Assumptions and implica Goshima,S.,K.Nagamoto,K.Kawai and S.Nakao1991. tions for prey morphology and distribution.Journal of Reproductive cycle and growth of the northern great Experimental Marine Biology and Ecology,73:95-124. tellin,Megangulus venulosus,in Shiriuchi,Hokkaido. Pearce,J.B.and G.Thorson1967.The feeding and repro Benthos Research,40:23-33(in Japanese). ductive biology of the red whelk,Neptunea antiqua(L.) Gosselin,L.A.and E.Bourget1989.The performance of (Gastropoda,Prosobranchia).Ophelia,4:277-314. an intertidal predator Thais lapillus in relation to Roff,D.A.1992.The evolution of life histories.Chapman structural heterogeneity.Journal of Ecology, and Hall,New York,535pp. 58:287-303. Staikou,A.,M.Lazaridou-Dimitriadou and E.Pana Harding,J.P.1949.The use of probability paper for the 1988.The life cycle,population dynamics,growth and graphical analysis of polymodal frequency distribu secondary production of snail Bradybaena fruticum tions.Journal of the Marine Biological Association of (Muller,1774)(Gastropoda Pulmonata)in northern the United Kingdom,28:141-152. Greece.Journal of Molluscan Studies,56:137-146. Hughes,R.N.1986.A functional biology of marine gas Stearns,S.C.1994.The Evolution of Life History.Oxford tropods.Croom Helm,London&Sydney,245pp. University Press,New York,249pp. Kawai,K.1993.Ecological energetics of the dogwhelk Stickle,W.B.1973.The reproductive physiology of the Nucella freycineti(Deshayes)population.Ph.D. thesis, intertidal prosobranch Thais lamellosa (Gmelin)I. Hokkaido University,150pp(in Japanese). Seasonal changes in the rate of oxygen consumption Kawai,K.and S.Nakao1993.Reproductive cycle,copu and body component indexes. Biological Bulletin,144: lating activity and dispersal pattern of the dogwhelk 511-524. Nucella freycineti(Deshayes).Benthos Research,45: Tamai,K.1988.Estimation of productivity of benthos. 29-41. Kaiyou to Seibutu,11:49-53(in Japanese). Kawai,K.,S.Goshima and S.Nakao1993.Reproductive Tsutsumi,A and M.Tanaka1987.Analysis of population cycle and shell growth of the tellin Nitidotellina dynamics of polychaete.Benthos Research,31:18-28(in nitidula(Dunker)in Hakodate Bay.Bulletin of the Fac Japanese). ulty of Fisheries,Hokkaido University,44:105-115. Uno,Y.1962.Studies on the aquiculture of Turbo Largen,M.J.1967.The diet of the dog whelk,Nucella cornutus Solander with special reference to the ecology lapillus(Gastropoda,Prosobranchia).Journal of Zo and periodicity of the growth.Journal of the Tokyo ology(London),151:123-127. University of Fisheries,6:1-76 (in Japanese). Moore,J.B.1938.The biology of lapillus.‡V. Webber,H.H.1970.Changes in the metabolite composi

Life history and relation to environmental factors. tion during the reproductive cycle of the abalone

Journal of the Marine Biological Association of the Haliotis cracherodii(Gastropoda:Prosobranchia).

United Kingdom,23:57-74. Physiological Zoology,43:213-231. Moreau,J.1987.Mathematical and biological expression Williamson,P.and M.Kendall1981.Population age of growth in fish:Recent trends and further develop structure and growth of the trochid Monodonta lineata ments.In.Age and Growth of Fish,Summerfelt,R.C. determined from shell rings.Journal of the Marine Bio and G.E.Hall(eds.),Iowa State Univ.Press,pp.81- logical Association of the United Kingdom,61:1011- 113. 1026.

51