Reference: Biol. Bull. 195: 319-325. (December, 199X) Effect of Colony Size, Polyp Size, and Budding Mode on Egg Production in a Colonial Coral KAZUHIKO SAKAI Sesoko Station, Tropical Biosphere-Research Center, University ofthe Rvukvus, Sesoko, Motohu-clio, Okinawa 905-0227, Japan Abstract. The factors that influence egg production in the role of non-marginal polyps is reproductive. The fe- the massive coral Goniastrea uspera were examined in cundity ofmature colonies increased linearly with colony colonies ofvarious sizes collected before the first spawn- size, and large colony size cannot be attained without ing of the year. Particular attention was given to polyp expansion of the attachment area. size, measured in three dimensions as volume. Although a polyp in a colony containing as few as 13 Introduction polyps produced eggs, colonies with fewerthan 60 polyps had fewereggs perunit volume ofpolyp. The relationship Recent studies on reproduction of colonial, scleractin- between colony size and colony fecundity suggested that ian corals have revealed that polyps in small colonies 60 polyps is the minimum size at which a colony can produce no eggs or few eggs, and that in large, fecund achieve active maturity. Polyp volume of small colonies colonies polyps at or near the margin of the colony pro- before maturation was also smaller than that ofthe larger duce fewer eggs than those in central positions (Harriott, colonies, suggesting that colony size, as well as polyp 1983; Chornesky and Peters, 1987; HarrisonandWallace, size, is crucial for sexual maturity. 1990; Szmant, 1991; Soong and Lang. 1992; Van Veghel The position of a polyp in the colony (and thus its and Kahmann. 1994; Hall and Hughes, 1996). A coral mode of budding) also affects its maturity (and thus its colony is usually derived from a single polyp by budding, egg production). Marginal polyps (those on the edge of so that the polyps in the colony are usually genetically thecolony) usually exhibited extratentacularbudding, and identical (Jackson and Coates, 1986) and likely to have the resulting polyps were initially immature. Conse- the same structure and the same potential for any physio- quently, egg production by such polyps is a function of logical function (Meesterand Bak. 1995). Thus,therecent their age, calculated from the time of their formation by work has demonstrated that coral polyps may differ in extratentacular budding. In contrast, non-marginal polyps reproductive activity even though they share the same always exhibited intratentacular budding. Moreover, in structure and genetic identity. the non-marginal areas of large colonies (>84 polyps), In colonial corals, colony size is considered to be im- the polyps produced by intratentacular budding were al- portant forthe maturation ofpolyps (reviewedin Harrison ways mature. In all colonies, marginal polyps were and Wallace, 1990), but the size of a coral has another smaller in volume and had a lower number of eggs for aspect, i.e., polyp size. Although the polyp is the basic each unit of volume than did non-marginal ones. This unit forphysiological activities, its size has not often been Two suggests that polyps play different roles according to their studied. exceptions are the studies by Harriott ( 1983) position in a colony: marginal polyps contribute to de- and Van Veghel and Kahmann (1994). Harriott (1983) fense and expansion of the area of attachment, whereas investigated sexual reproduction in four scleractinian coral species, and suggested that polyp size rather than colony size limits gonad production in the mussid coral Received 19 November 1997; accepted 8 September 1998. Lobophyllia corymbosa; she presented no data on polyp E-mail: sakaikz@ryukyu.ne.jp size. Van Veghel and Kahmann ( 1994) studied reproduc- 319 320 K. SAKAI tion in three morphotypes of the faviid coral Montastreu (innularis, measuring polyp size two-dimensionally at the base. They found that the fertility (measured as the percentage of polyps with eggs) of polyps from 27 colonies was less than 40% in small polyps 1.5 mm) and increased with polyp diameter. To date, however, no study of coral reproduction has quantitatively examined the relationship between the size of a polyp and its egg production. Furthermore, polyp size has previously been measured in two dimensions, even though it is the space within a polyp that limits gamete volume. Thus, I measured the three-dimensional size of polyps in the faviid coral Goniastrea aspera. Figure 1. Diagram showing position classification of polyps in a loc\ateixoanmionfepdoltyhpesefofnectegogf pcrooldouncytisoinz.e,Iposlhyopwsitzhea,t annodt ctdhoeeltoepnroym.liynEgeaodcnhasinwtdhhiiectaenteepxstotlhhyieggohrneoswtrennpruuemmsbbeeentrrstoaoftpthohelatylpop,woelasyntpd.ntuRhmeobwneurnmuibnmebaredjriancsweiadnset only colony size but also polyp size is related to egg polyps. 1 = marginal polyps; ==2 = non-marginal polyps. production, and further suggest that fertility in G. aspera is alsoaffected by polyp age. determined as the time since formation by extratentacular budding. conical. Hence, I estimated the polyp volume as k X TT X [(maximum diameter + minimum diameter)/4]2 x height, Materials and Methods where k ranged from 'A (conical) to 1 (cylindrical). The Collection, colony size, and egg count value of k was subjectively determined for each polyp according to its shape. Each polyp was dissected under a I collected specimens of G. aspera at the lowest low stereoscopic microscope, and all the eggs within a polyp tide level on the fringing reefofSesoko Island, Okinawa, were counted. I measured the diameter of five eggs, ran- southern Japan (26 38'N, 127 52'E). This coral is a si- domly selected from each of four polyps in each of ten multaneous hermaphrodite; in Okinawa it has one or two fecund colonies. The overall mean of the egg diameter salp,aw1n9i8n7g; pHeaaykasshpiebraryaeaert,ail.n.J1u9n9e3:anSdakJauil,y1(9H97e)y.waTrodase-l Tinhetrhee wpaolsynpsoswiagsnif3i1c0antco3l0ounrynef(fMecetaonntheSDe.gg/;di=am2e0t0e).r sess egg production by polyps, 23 G. aspera colonies of (Model III nested ANOVA, df = 9. SS = 9663.98, F = various sizes were collected on 21 May 1991. 10 days 0.99, P = 0.5; when polyps were nested in the colonies). before the predicted date ofthe first spawning ofthe year. Thus,eggproductioncanbecompared in termsofnumber Bceofloorney cwoelrleectmieoan,sutrheedlteongtthh,e wneiadrtehs,ta1ndmmh.eigShitncoefetghge ofPergeglsimpienrarpyoleyxpamvionlautmioen(oNfEt/hPeVe,ffseecet obfelpoowl)y.p position production may be affected by disease or injury and by on ees production in four fecund colonies showed that contact with large benthic organisms such as neighboring marginal polyps had significantly lower NE/PV than non- corals. I chose colonies without such features. marginal polyps (Table I). NE/PV of polyps in row 2 or The collected colonies were fixed in 10% formalin in higher did not differ significantly (P > 0.05). In subse- seawater for at least 24 h, and decalcified in a solution quent analyses I therefore grouped polyps in acolony into of 5% formalin + 5% acetic acid. I counted the number marginal and non-marginal sets. Polyp-group fertility, as ofpolyps in the colony after decalcification and used this percentage ofpolyps witheggs tototal numberofsampled value as a measure of colony size, because the polyp polyps, was calculated separately for marginal and non- number is highly correlated with colony somatic biomass marginal polyps in each colony. (Sakai, 1998). Then, randomly selected polyps (/; ranged from 1 to 20 according to colony size) were cut from Budding mode and polyp hiomass the decalcified colony after the maximum and minimum diameters of the oral side were measured to the nearest To examine the relationship between estimated polyp 0.1 mm. Polyp height was measured afterthe polyps were volume and polyp biomass, I collected 1 1 colonies of G. excised from the colony. I estimated the volume of each axperaofvarious sizes (from40to420polyps) inOctober polyp from its diameter and height. While non-marginal 1993, when reproductive tissue was negligible (Sakai, polyps (in polyp row 2 or higher, away from the colony 1997). These colonies were fixed and decalcified as de- margin: Fig. 1 ) were always cylindrical, marginal polyps scribed for the egg-count specimens. When I counted the (in the row at the colony edge) were frequently more number of polyps in the decalcified colonies. I also re- EGG PRODUCTION IN A COLONIAL CORAL 321 Table I Statistical analyses mInmtra3c)olionnfioaulrvfaerciautnidoncoilnonNiEe/sPV(numberofeggsperpolyp volume. numIbeexra)miannedd ftehretirleiltyatiaonndshmipeabnetwNeEe/nPVco.lofnitytisnigzea(cpuorlvyep Kruskal-Wallis test using the logistic equation, since egg production by coral Colony size among polyp rows Tukey-type multiple polyps overcolony size is expected tobe sigmoidal (Bab- (number ofpolyps) (P value) comparison cock, 1991 ). For the remaining regression analyses, I ex- 8854 <<00..0011 11sstt << 2nd.2n1sdt < 3rd+ atimoinsn,edanldinueasre,detxhpeonoennetiwailt,hptohweerh,igahnesdtlcoograrreiltahtmiiocn fcuonecf-- 3rd+ 2nd = 3rd+ ficients after examining the residuals (Zar, 1996). I used 167 <0.01 1st ,2nd, 1st < 3rd, Model III ANOVA. nesting random-effects such as indi- 349 <0.001 1st311rssttd ~24ntd44h,tt+hh.1+st2,n2orfo0wp.so0,l5y:rpess150 polyps, or >9 cm). The classi- Egg production by a whole colony (colony fecundity) fication was made because (1 ) below 60 polyps, NE/PV was estimated as the sum ofegg production by marginal was extremely small; and (2) after 150 polyps, the fitted and non-marginal polyps. The total egg production for curve using the logistic equation between the colony size each polyp type was calculated as the mean number of and NE/PV leveled off (Table II; Fig. 2C). eggs per polyp multiplied by the number of polyps of No eggs were found in colonies with marginal polyps that type in the colony. only or with marginal polyps and one non-marginal polyp 322 K. SAKAI EGG PRODUCTION IN A COLONIAL CORAL 323 Table IV Meanpolyp volume, polyp fertility, andmenu NE/PV(numherofeggsperpolyp volume) among the colony si:.e classes Colony si/e class Mean polyp volume (mm1) Fertility (%) Mean NE/PV (mrrT1) Marginal polyps 324 K. SAKAI x 10" fragments produced gametes. In G. aspera, non-marginal 10 polyps were formed in colonies with more than eight 68 -- Colonytotalr(22=600.9p9ol(ypps<)0.0001) pnwooelnry-epmsaf,errgtwiilhneia,clhprpeotslhuyepmnsabblienygacbnoelcoiannuitsreeasteallnaltragtcehurelatprhoalbnyupds8d4ihnagpv.oelyAapltsl- tained maturity upon extratentacular budding. o 4 - This study demonstrates that polyps within a mature o O colony ofG. aspera play different roles according to their 2 ~ Non-marginal polyps position, even though all the polyps in a colony share the Marginalpolyps same structure and are likely to be genetically identical 100 150 200 250 300 350 and physiologically connected to each other. Significant differences in polyp volume, NE/PV, and mode of bud- Colonysize (polyp number) ding were detected between marginal and non-marginal Figure4. Relationshipbetweencolony size(numberofpolyps)and polyps within a colony. Moreover, NE/PV of marginal colony fecundity. The total colony fecundity and the contribution of polyps was relatively constant in mature colonies, mseapragriantaelly.anLdinneoanr-mreagrrgeisnsailonspowleyprse ctooncdoulcotneyd ffeocrucnodliotnyieasrelaprrgeesrenttheadn whereas NE/PV ofnon-marginal polyps was significantly 60 polyps. higher in the larger mature colonies (>150 polyps) than in smaller mature colonies (60-150 polyps; Tables IIIC, HID and IV). This implies that marginal polyps function budding that produced it. In large colonies of mature G. as a buffer for the non-marginal polyps, which produce aspera (>84 polyps), the non-marginal polyps, which the bulkofthe gametes (Fig. 4). against external perturba- showed intratentacular budding, always contained eggs tions such as competition and grazing, which are likely regardless ofpolyp size, but less than70% ofthe marginal to be heavier at the colony edge (Jackson, 1979; Hughes polyps were fertile (Fig. 3). New polyps produced by and Jackson, 1985; Chornesky and Peters, 1987; Soong intratentacular budding of mature non-marginal polyps and Lang, 1992). In addition, marginal polyps may also appear to share the developmental stage of their parent contribute to the expansion of the attachment area of the polyps, whereas new small polyps produced by extraten- colony (Chornesky and Peters. 1987). In a massive coral tacular budding are rarely fertile and may be regarded colony, polyps in the central area contribute to colony as developmentally "young" polyps. In the Caribbean growth, increasing the surface area of the colony. How- massive faviid coral Montastrea annularis, not all the ever, large colony size cannot be attained without expan- polyps in the central area are fertile, and polyp fertility sion ofthe attachment area as well. As a colony becomes is positively correlated with polyp size (Van Veghel and larger, its total fecundity becomes greaterwith an increase Kahmann, 1994), as in marginal polyps from the large in the number of fecund, non-marginal polyps. Thus, the colonies ofG. aspera (Fig. 3). One ofthe generic charac- differences between the marginal and the non-marginal ters ofMontastrea is that it exhibits only extratentacular polyps play a role in promoting high colony fecundity. budding (Veron, 1986). So for this species, polyp size likely reflects the polyp age afterextratentacularbudding; Acknowledgments ti.rea.s,t,eancehwppoollyyppshapsriotdsuocwend bdeyvienltorpamteennttaaclulcalrocbku.ddIinncgoni-n forIctohmanmkenRt.sAo.nKtihnezimeanIuIIs,crEi.ptF.. CIoaxl,soatnhdanJk. SK..SKtairmisnoon, G. aspera are mature from inception. Thus the age of T. Kuwamura, Y. Nakashima, Y. Loya, and H. Yamashiro these polyps should also be measured from the time of for comments on the earlier manuscripts, and E. Hirose original formation by extratentacular budding, not from for discussion on polyp age. This study was partly sup- the time of intratentacular budding. ported by grants from theJapanese Ministry ofEducation, sizEe,ggpolpyropdsuicztei,oanndofbuGd.diansgpemroadew.asThaeffceocltoendiebsybceoclaomney SSceiseonkcoe,StSaptoirotns, aUnndiveCruslitutrye.ofThthiesRisyuakycuonst.ribution from actively reproductive at a size of60 polyps, and the polyp volume of the reproductive colonies was significantly Literature Cited larger than that of the pre-reproductive colonies (Tables IIIA, IIIB, and IV). An effect ofpolyp age on egg produc- Babcock, R.C. 1991. Comparative demography of three species of tion has been suggested by Kojis and Quinn (1985). They sEccloelr.acMtOiIniWaKnI:co6r1a:ls2u2s5i-n2g44a.ge- and size-dependent classifications. divided mature colonies of Goniastreafavulus into frag- Chornesky, E.A., and E.C. Peters. 1987. 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Effect of Colony Size, Polyp Size, and Budding Mode on Egg Production in a Colonial Coral

Similar Effect of Colony Size, Polyp Size, and Budding Mode on Egg Production in a Colonial Coral