Annual growth cycle of the brown alga Ecklonia cava in central Japan

I or le s 1 :--' ~I "'1 \1 N 1:: B IOl oc Y. /W S. J /) (L /1 J SCI E:- l . ~IA R .. 5.'\(:: :; 1: :;.¡<J· 35(, Ánnual growth cycle of the brown alga E cklonia cava in central J apan R. HAROUN 1 ,3, Y . YOKOHAMA 2 & Y. ARUGA 1 JL aboratory of Ph yco logy. Tokyo Un i \'. of Fisherie s. Konan 45-7. Minato -ku . Tokyo. 108. Japan. "S him oda Marine Research Center. Uni\'. of Tsukuba. Shimoda. Shizuoka. 41 5. Japan 'Prese nt address: Dcpartment of Plant Biology. University of La Laguna. Tenerife. Canary I s. Spain. SUMMARY: Ecklonia cava Kjellman (Laminariales. Phaeophyta), a perennial seaweed, is one of the main components of the marine fores ts along th e P ae ifi e eoasls 01' Japan It s standing erop attains a maximum in summer and a minimum in winter. This is due prima ril y lo seasonal varia ti on of pinnate blade bi omas s. The present investigation was condueted on an E. cava community in Naheta Ba y. Shimoda (central Japa n) , with monthly sa mplings at 5 m depth. in order to quantify the growth process of this specics. In the laboratory several biometri ca l parameters were measured. Although there ",ere individual va riations among the sa mples, it was possihle to define se ve ral trends in the growth cyc\e of E. cava on the basis of th e monthly averages. The number of yo un g bl adelets \Vas 0-7: th ey in ereased from autumn to the beginning of winter. remaining constant for a shon period until spring when th ey began to decrease, reaching a minimum in lat e summer. The longest bladelet appeared in spring a nd ea rl y summer. whil e the shortest one \V as found in early winter. The dry we ig ht per unit area of bladele ts increased with growth, and was low (6 -9 mg cm2) during winter-spring a nd high (18-21 mg cm- ') during th e reproductive seaso n. Based on the results, 4 periods can be di stinguished in th e annual growth cyc le 01' the E. cava blade: 1) period of ac tive formation of new primary blade and bladelets; 2) period 01' active growth of bladelcts; 3) period of thicke nin g of bladelets and development of sori, and 4) period of decay of old bladelet s. Key word s: brown algae, growth cycle. E ck lonia, Laminarial es . 1 989 INTRODUCTION In the shallow sublittoral wat e rs of temperate regions the kelps a re major components for the marine primary production (MAN N, 1973) and their large biomass is being used in both the Pacific rim (California, Jap an, Korea , China) and Europ e (France, Norway) for commerci al purposes (MICHANEK, 1975 ; L EVR IN G. 1977; TS ENG, 1981). Recentl y, their ecol og i ca l role (MANN, 19 82) and importance to fisheri es as nur se ry a reas or habitats are being e nhanced (WHEELER , 1980; KIKU CHI & UKI , 19 81; WAR NER, 1984; OHNO, 1985). Sorne member s of the Laminari al es have receiv ed a lo e o f attention. es p ec ially Laminaria and Ma crocystis, with ma ny publish ed pa pers about diverse as pects of th e ir biology (NORTH, 1971; K AIN, 19 7 9: Honshu (O Kyúshu , and their ecologic al role in the shallow marine ecosystems is starting to be understood. In r ece nt years the work of several Japanese investigators has shed sorne light on the structural asp ec ts of community (lWAHASHI , 1968a, 1968b; IWAHASHI el al. , 1979; HAYASHIDA , 1977, 1984,1986 ; KIDA & MAE GAWA , 1982, 1983; OHNO & ISHIKAWA, 1982 ; KASAHARA & OHNO, 1983; MAEGAWA & KIDA , 1984) , on culture (MIGITA, 1984) and productivity (YOKOHAMA, 1977; YOKOHAMA el al., 19 87; MAEGAWA ef al ., 1987) of E. cava. In previous papers (ARUGA, 1981; YOKOHAMA efa!. , 198 7) it was report e d th at the standing crop of E. cava communities attains a maximum in summ e r a nd a minimum in winter; this is mainly re lated to th e seas onal variation of th e pinnate bJ ade biomass . SCHMJTZ. 1981) In J ap anese waters , s poroph y te s of Ecklonia cava Kjellm an fo rm ext ensi ve ke lp beds on ro ck y sho res alon g th e Pacific coas (s from central The pre se nt investigation was conduct ed to quantify (he growth process of (hi s species durin g a oneye ar peri od a nd to relate the growth pattern to so rne possibl e f acto rs CjRO\\'TH CY( I - 0 1I: C J<: L OSlA CA \ Al. ' .I.\ PA~ 349 ~ MAT RI AL AND ME Tl rODS Mor phologi ca ll y, the E. cava spo roph y te can be dívided into thr ee parts: a conical holdfast with ma nv rhizoids, a long stipe (length > 50 cm in adult plant) and a pinnate blade (HA y ASHIDA, 1977) (Fig. 1) Th e general morphology of E. cava is very similar to that of E. radiata (e. Ag.) J. Ag. ofsouthern Australia (KIRKMAN, 1984), but the form er has a longer stipe and the margins of the primary blade have many digitations from which the bladelets appear. As in other Laminariales primary growth is intercalary, loca ted in the transitional zone between stipe and blade (some also in the proximal portio n of the blade). When growth is initiated the primary blade moves upward , developing several bla delets (usually with lateral protuber a nces), and erodes from the distal ends of both primary blade and bladelets (Fig. 1). T hc rc scar ch was co nducte d on an E. C{l\ 'a f orest l oca tcd at :\'abet a B ay (Izu Peninsula) , n ea r the Shim oda Marine Re 'ea rch Ce nter of the University of Tsu kub a, from April 1986 to March 1987. -very month 10 adult plants (3 or more years old) were randomly sa mpled from a homog e ne ous population of E. cava at 5 m depth (Fig. 2). In the l abo rat ory the following dimensions were measured: total le ngth, stipe le ngth and diameter, primary blade and bladelets length, total number of bladelets , number of young bladelets (Iength < 10 cm), number of bladelets with sori (if present) and the dry weight (80 "C, 24 hours) of a 3.2 cm 2 disc taken from the central part of each bladelet and primary blade (Fig. 1). The bladelet position number was ass igned from the proximal to the distal par!, i.e. number 1 was asigned to the smallest primordia , number 2 to the next one and so on. Later, the different biometrical parameters of each month were averaged. I SORUS >-, ~ "- "- " PRIMARY BLADE LENGTH .. . y O "- " " . ~ .. .. , ~ '-" t 8LADE O + / i ~ / -- .- / / STIPE BLADELET LENGTH /' 1 / O HOLOFAST YOUNG BLAOELETS l ess than 10cm S,de B 1 '1(; . 1. - Slmpltiléu d ru wi ng s of Ih ~ C Ck /f Jllio L1/l ' 1l sp ororhyte showing dlfferent pan s of a frnnd measurl ·d. Central discs 01 biade 1cts were u ,e d 1 <' obta in ¡he dr y weight. 350 R. íi.-\IWI ·' ) . YOKOI¡ \ '1A", Y ,\ ¡{ LlíA ] (' .0' ~ Rocky bed té ;; J Sompling ",.. oreo N L O" 35' 13 5' 11.0' E !-I(; 2. - Map, shnwing the locatio ll nI sampling arca in Nabeta Ba y. Shimoda. central J apa n. RESULTS In figure 3 is represented the seasonal variation of seawater temperature (average of 6 years, ANON ., 1981-'86). It has a minimum in mid-winter (February, 12.8 O C), and a maximum in late summer (August, 25 "C). Figure 4 shows the results of measurements of the bladelet length and dry weight and their averages in April, June, August, October, December and February. From early spring to summer the total number of bladelets increased, but the meristematic tissue activit)' gradually slowed down and finally stopped in .late summer. There was no )'oung bladelet formation in August (Fig. 5). During the summer onl)' upper bladelets had sori, but in earl)' autumn almost all the bladelets had sori and the transitional zone started again lO divide at a high rate, producing numerous primordial bladelets for the next growing season (Figs. 4 and 5). In December. the upper parts of the blades still held bladelets with sori, however, these bladelets as weH as the sori were very eroded and in a progressive process of degradation. Moreover, in the proximal pan of the blade the next season 's primar)' blade was in ac tive growth with man)' bladelets in formation (Fig. 4). Between December and January the remnants of the old blades finally broke from a weak area, leaving the fresh blade alone. In winter (Fig. 4) , the E. cav a sporoph)'te was at the peak of the growing season producing man)' long bladelets which through the spring will start to thicken and subsequently produce so ri. The longest bladelets \Vere usua l] )' located at bladelet position 7-17, with the smallest position number in September and the largest position number in November after the onset of bladelet primordia formation. The length of bladelets increased quickly during late winter and early spring and the erosion process dominated in late summer and autumn; the shortest bladelet appeared in early winter (Fig. 6). The dr)' weight per unit area of each bladelet, represented by cireles in the histograms in figure 4, also showed elear seasonal variations (Fig. 6), increasing with growth through the spring and reaching maximum values of 18-21 mg cm -2 during the reproductive season; the minimum values of 6-7 mg cm2 were found in winter (Fig. 6). Another interesting trend is that in winter and earl)' spring (Fig. 30,-------------------------------, 25 ~ 20 :J ~ c¡¡ a. E 15 ~ 10 J F M A M J J A S O N O Months FICi. - Se J"o na l change 0t the 'lIrfacc' ,~a\\a t e r temperatllrc in Nahc ta Ba\. Average of 6 vears fr om 1 981 to 198 6. GRO \\rH C ~ C L E O F [C {O' L() .' \I . \C A\·AI"'J P .. \i" 351 l ~ " Wia ":, . ' ~ .• __ : f ~& · ~! : .b , :' ~ & ~ . ~ , ;,! . :!II! ~~ :1 ~ "" , il~ . :, :' i j ·~ " J . . . JO 10 C ~Y )!tE IGHl '. le )O JO 10 100 rng/e m1,0 0JI'r .. 'E JG .... • 0R1'~ 2 ~ LENGTH LEN G1 H 60 L.() 20 20 2' o ~ 21 o o o v; o o o o ce 16 o >- o o ~ o o W o o o 11 o o APRIL 5 o o <D o o o o o o 30 20 10 mg /cm2 10 ORY WEIGHT 'O 2Q 60 30 20 " ,a 60 ,o JUNE JO 20 20 cm 20 o o o o 'o 10 mg /cmZ 10 20 ORY WEIGHT F1G. 4a . FI G. 4. - Di agrams show in g lh e bladelel length (histogram s) a nd dry weig h¡ (open cireles. wilhoul sori ; so lid ci reles, wi¡h so ri ) of individuals sa mples of Ec kl onia cava in Na be¡a Bay. The lo wermosl di agram sh ow s ¡he average of 10 samples in each month. April 1 986 - February 1987. 4) the dry weight per unit ar ea of eac h bladel et was more or less similar a ll along the bla de , but in ¡h e reproducti ve se ason ¡h e values of the upper blad elets \\' ere 2-3 times higher than tho se of the l owe r on es (Fi g. 4) . There were o nl y a few bladelets with ma ture sori in spring. The numb er of blad elet with ma tur e sori gradu a ll y incr e ased during summ er until it re ached a' peak in Oct o ber. In D ece mber a gr ea ter part of the so ri sloughed off, discolored and d eg raded. During Ja nuary and F eb ruar y not one s orus was enco untered (F igs. 4 and 5). Th e formati on of sori in one particul ar b lade started from the upp er bladelets a nd subs e qu ently the pro cess moved downward (Fig. 4). The sori first a ppeared at the basal portion of blad ele ts and th en they extend ed to the apical portion. Th e sha pe of the ear ly s pring so ri \Ve re irregular and of sma ll ar ea cover age, while the so ri form ed in s umm er occupied m ost of the bladel et ar eas a nd fi t the g en eral morphology of the bladelets. There was an incr ease of 352 R. H.' RO l ', . \ YU ¡';' O I I. 1-1 ,\ & ~ A RI ( ;,\ so rus coverag e from spring (20 %) to late summ er (8 090 %). In late s ummer many bladelets were covered by e pizoon , especially br yo zoans, so that in some way they may h ave inhibited the normal deve lo pment of the sori. From the abo ve -menti oned results it is possible to d ef ine the growth process of th e E. cava blad e on an annu al ba s is with 4 sucessive pe ri ods (Fig. 7): 1) Pe ri od of active forma ti on of new primary blad e a nd bladelets. In early autumn the tran sitional zone betw e en stipe a nd blade started to produc e the next year 's prim ary blade and numer ous bladelet primo rdia app ea red. The activity of the meris temati c tissu es increased until winter, then remain ed c onstant for a sho rt time , a ndin late spring the pr o du ction of y oun g bladelets d ec r ease d; in summ er not on e young bladelet a pp e ared. Thu s, the formation of the primary blade is mainly con ce ntr ated in wint er a nd ea dy spr ing. 2) Period of ac ti ve growth of bl adelets The bl ade lets produ c ed in w inter elongated very q ui c kl y 60 30 :J ~ , L' " iIIi '~ •• ,., '1 11\ .. • ... • .. . .. I !'> •• •• '. • • '.1 •• : , 'c '"" ¡¡ "1 1; ' " " " JO 10 10 - "V~"..I tO 10 ?l) l a 20 le ."rpc-nl ~ . 0 )Q • " .,: '1 60 22 le lO 10 "'9/cm 110 10 )O 1 '¡i Rr ·"E.lGHf AUGU S T 30 QR r WE IO~ ORT wE.J (", T LO · · · · . · · · 20 20 o o 10 LENGTH o o mg /c m2 10 DRY WEIGHT o . · · . · 20 L ENGTH lE NG'H JO '::L~ I~ "" I '" • 1 I í' , 1 , , lO 10 lO"'t;/'erO>1 10 20 :JO JO 10 10 .... 9/ 011 ' 0 ') ;¡ O J: Cq · w(I C HT cq y \ ." ~ !C +li L ENGTH 60 LO 20 cm 20 LO 6.0 "[ fJ . . . · ¡¡> \ 8. g o w DEC EM BE.° ~ 13 o a: el o o e 30 1 mgic.¡n2 'O 2Q JO QRY W EIGH ' " ., .' a ;: .' , '{ ~ \, ", " ' '1 24 :: 1 :e" ' \"~" ·C. "j ' { .1' , .' " . ~~~..J.I---.,_,~ ~ » ~o 10 " \1 "e",1 tO . "0 JO. ;ID W 10 ", g f ~ ..,1 tQ 2<2 ~ O ~ f ..... E IC HI 01;;'" ' ~ n o ;.n LEN G TH I • 60 LO 20 O ,," , 20 LO 60 :f. :;, : 1 28 [ ~- -'-- - -'---.--+- - --'-;- -~ " . •• I · · , JO 10 '0 ... .q rc ml ,,, ;o J t'I a=', w El GriT 2. · . · . · . · . · . . · · · · · · · vo ~ 15 . . · . w OCTOBER §1O al o o o o o FI G. 4b. 20 10 mg / cm 2 10 20 DRY WEIGHT JO JO :;[ : ,,::.i : : ~:: ¡ti: :: : iii : ': ¡ IA~ JO 20 10 ~/(",I la 20 lO la 20 10 IT"; /C."TI" 10 20 JO :~. JO ro 10 mq" ... I ,O ¡) lO DAr ''''€ l~ r '1 t: 1, ~ ~ FE BRU4.PY "' 1 ~ .. ;;; . FI(;. 4(:. 60 JO CA l -.1:.I GH T ~1' ..... EI C,¡.;l 20 20 LE NG TH cm o o 20 LO 10 m;/tm~ 10 10 O R'I' It' EIC,J-r¡ 60 GRO\\T H CYCLc or ru:/ ().\1.·1 c'l!',\ 1:-\ .lAPA:" 353 10 20 8 ,i rt-• o 15 15 VI - VI ~ ..c. e¡¡ , u 6 \ 'i Cl \ :o \ VI \ 10 ~ g' j, e¡¡ 'O :;J l. E o >, .D 'O 'O (¡¡ 2t--t/t' 5 ~ .D E E :;:¡ :;J z J. O z , \ O A M A S O N O F M Mo nths FI G, 5. -Seasonal changes of lhe nu mb er of young bl adelels le ss lhan 10 cm and Ih e numher of bl adelels wilh so ri of Ecklonia cava in Nabel3 Bay. A ve rage of 10 samples and SO, Ap ril 1986 - March 1987 . and attain ed 50-60 cm long in spring . Th e elon ga ti on rate 01' th e prim ary bla de was very high, a nd it was possible to observe many thin and long prim ary blades movin g by the surge force during the pe ri o do 3) Period of thickening of blad elets a nd developm ent of so ri , Fr om late sprin g th e bladelets gradually started to thicken and many of th em , especia ll y the distal on es, bega n to de velop sori. At the sa me time , the prim ary bl ade beeame he avier. Although we encount er ed bl ade lets with sor i as ea rl y as in March , th e re pr o dueti ve season of E. cava can be de - lineated from ea rly s ummer to autumn, Bef o re the general development of sori preceed ed so me of them started to rel ease zoos pores as early as in J une. a nd in August a ll th e blades sa mpled were in a re pr o du etive stage, Later, during the peak of the r epro du e ti ve sea so n so ri on the upp er bladelets were alm os t ex60 o 20 E E ~ 2 O' L ~ g>4 0 15 :c / O' ~ / o Oí :g; / ~ e¡¡ / >. '8 30 o / / 10 'O ro / o Cii Cii 'O o 20 5 iñ Months r l (ó, 6, - Seaso na l cha ng es 01' lhe hladelel le ng lh and dr\ weighl ror rhe l o n ge~1 bladelel in' t he a\ cr a ~e diagram (Fi ~ , -+ ) nf Éc kl o711a <'</1'11 in la 'beta Bav. The shaded ar 'Ca rc¡ ;rcse nt s lhe rcr roduc ti\ é season, April 198 6-M arch 19i{ ~ • Formo lí on 01 new prímor y bl ode (1) and b la delel s (2) !tt l Growth 01 bladel els (3) F ::::::::: :¡ Th íc kening 01 bladelets . :-: . :. : .:.: .: and development of sorl (1. 1 tw&. 1 Oecoy 01 old blodelets F IG 7, - The annual growth cy cl e of a bl ade of the adu lt Ecklonia ca va sporophyte in Nabeta Bay. hau s ted , but th ose on the me dian a nd l owe r on es st a rted to re l eas e z oos por es. 4) Peri od of de ea y of old bladelets. When th e reproduetiv e seaso n was over , the old bla del ets with empty a nd bl eac hed sori eroded a nd their le ngth slowly deer ease d during the autumn mo nth s; the fate of the se bl ade lets wo uld have bcen to e nt er into the detrit al f oo d chains of the surroundin g coas tal a reas, In the me a ntim e the next seas on 's prim ary blade was d eve loping in th e pr ox imal part of the blade, DISCUSSION As in other Laminarial es. the Eck/onia cava sp oro ph yte exhibits a distinct seaso nal gro wth cyc\e, with a re pr od uetive period in late s umm er a nd a rapid grow th phase in mid-wint er. The same pa ttern of gr ow th was obser ve d by IW AH AS HI (1968 b) and HAYASHI OA (1984) in a d ee per eo mmunit y of E. cava, with a little dela y in the onset of vege tative growt h, More ov er , the results of sta ndin g erop m eas - ur eme nt s by KIRKMAN (1984) suggest th at the E, ra - dia ra sporo ph yte may we ll have th e same type of bl ade gr ow th process, In E. cava the sporoph yte st oppe d to grow in July. the number of youn g bl ade lets dec reased to a lo \\' \' alue. and al that time the seawat er temperature ,>u rpass ecl 22 " c. ami then the reprocluetive aetivity reached a peak. Th e slowdown 01' the growth rate "" ' as in verseJy correlated with the reproduetive activity. and this feature could be explained by diversion of the supply of photoassimilates from the growth processcs to the development of sori as l,vas pointed out by DIECKMANN (1980) a[Jd YOKOHAMA el al. (1987). During the period of formation of new primary blade and bladeletes it was possible to distinguish two different phases in E. cava: one is the phase of slow growth (October-December) and the other is thar of rapid growth (January-ApriJ). A similar pattern was observed in Laminaria sClcc harina (L.) Lamour. (PARKE, 1948) and in L. digitala (Huds.) Lamour. (MANN, 1972). The shape of the bladelets in E. cava at each phase was different, with few lateral protuberances in the short autumn bladelets (maximum length, 22 cm) in contrast with the profusely branched, long winter bladelets (maximum length. 60 cm). Futhermore, in E. cava the sori never appeared in the autumn bladelets; there was a gap of 5-6 months between the onset of vegetative growth and that of the development of sori. The slowdown of the growth rate during the summer months may well conelate with seawater temperature increase and/or nutrient supply. The triggering mechanism is still speculative and several hypotheses are being proposed. In L. pallida (Grev.) J. Ag. (D[ECKMAN, 1980) it was found that the light factor played an important role in regulating growth rate, but in the literature other factors have been pointed out, such as temperature (SUNDENE. 1964; LÜNING, 1982; KIRKMANN. 1984). nutrient concentration (HATCHER el al., 1977: CHAPMAN & CRAIGIE, 1977; GAGNE el al., 1982). or canopy density (YOKOHAMA el al., 1987). Probably the seasonal cyele of kelp is regulated by more than one factor (endogenous or environmental), each one affecting different phases of the growth cycle. CHAPMAN el al., (1978) suggested that light conditions and nutrient supply may control the growth process of Laminaría. Although we found so me sori from March to December. the peak of reproduction activity was reached during August-October in E. cava. Both the sorus development and the frond weight of E. cava followed the same trends as KAIN (1975) reponed for L. hyperbor ea. Another interesting feature is that the first sori appeared in the upper bladelets and then the maturation process moved downward, suggesting a possible meristematic inhibition or age-related control (PARK E. 1948: LÜNING. 1982). In mid-summer. when no young bladelets were growing, almost all the bladelets were in some reproductive stage. As the life span of the E cava sporophyte is of 5-7 yea rs (HAY S HIDA. 1977) and the fronds become acJ ul t III lhe 2nd or ~ rd ,' ..::a r. the ahove-dcscr ibecl annual growth cycle of lhe blacle of E cava is probably repeated 2-4 times without any external disturbance. The blade growth 01' the E cava sporophyle looks like the «conveyer belt» as mentioned by M AN ;' (1973) with new ti ssues formed in th e junction between blade and stipe which are lost by erosion or grazing 111 the distal ends. In late autumn large pie ces of the blade broken off and the resulted organic matter would play an important role in the detrital food chain 01' the surrounding coastal waters. The blade of E. cava can be treated like a storage deposit of organic matter that is slowly liberated from the tips when grazed and in large quantities after the breakdown of old blades in late autumn. REFERENCES ANONYMOUS, 1981·'86. Repon of Coastal Oseryations. Shimoda Mar. Res. Cenrer Univ. Tsukllba. 31-36: 1-7 . ARUGA. Y 19 81. Physiological characteristics of Eisenia bicvc/is and Ecklonia cava. R epo n Marine Ranchin g Program 1980: 29·34. CHAPMAN. A. R. O. & CRAIGIE. J. S. 1977. Seasonal growth in Laminaria longicruris: relations wi¡h dissolyed inotganic nutrients and internal reserves of nitrogen. Mar. Biol .. 40: 19 7·205. CHAPMAN. A. R. O .. MARKHAM. J. W. & L ÜN tN G. K. 197 8. Effects of nitrate concentration on ¡he growth and physiology of Laminaria saccharina (Phaeophyta) in culture. 1. Phycol .. 14: 195-198. DIECKMANN. G. S. 1980. Aspects of the ecology of Laminaria pal· lida (Grey.) J. Ag off the Cape Peninsula (South Africa) \. Seasonal growth. Bol. Mar .. 23: 579-585. G AGNE. 1. A .. MANN K. H. & CHAPMAN. A. R. 0.1982. Seasonal patterns of growth and storage in Laminaría longicruris in relation 10 different patterns of avaiJability of nitrogen in the water. Mar. Biol .. 69: 91-101. HA TCHER. B. G .. CHAPMAN. A. R. O. & M ANN. K. H 1977. An annual carbon budget for the kelp Laminaria longicruris. Mar. Biol., 44: 85-96. HAYASHIDA. F. 1977. On age and growth of a brown alga. Eeklonia cava Kjellman. forming aquatic fores\. Bu/!. lapo Soc. Sei. Fish .. 43: 1043·1051 (in Japanese ,,'ith English summary). HAYASHIDA . F. 1984. Synecological studies of a brown alga. Ecklonia cava Kjellman. forming aquatic forest - 11. On growth 01' Ecklollia cava. l. Fae. Mar. Sd. Techno/., Tokai Uni\'., 18: 275-280 (in Japanese with English su mm ary). HAY ASH ID A, F. 1986. 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