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

7 Pages·1998·2.9 MB·English

by  K Sakai

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: [email protected] 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 per-
centage of polyps with eggs) of polyps from 27 colonies
was less than 40% in small polyps 1.5 mm) and in-
creased 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,n2<dnd3rd, cvnlioadrsumsaaellsict(oyZlaoarn,nide1s9h9ow6mi)to.hgieTnnheeWfiitxayesds-ouefmffpvetacirtoisnansscuefc)ohrwaAesrNecOoelVxoAanymi(sin.ieez.de,
3rd = 4th+ with the Shapiro-Wilk test and O'Brien's tests. Loga-
rithmic transformation was made if necessary; when the
Note: Ordinals in the multiplecomparison (Zar. 1996) represent pol- assumptions were severely violated even after the trans-
ypsoftheithrowfromthecolonyedge;3rd+ and4th+ indicatedpolyps formation, a nonparametric analysis such as the Wilcoxon
mmuo:lrtei,pcleenPtcrao<lmpt0ah.ra0in0s1o2.nn:dNuamndb,eP3rrd>orfo0wp.so0,l5y:rpess<p,eecxtPaimvi<elnye0d(.F0i5ign:.e1a)c.hP,rroPboawb<irlia0tn.yg0e1id:n npiaeisr.edSt-astaimsptilcealtesatnawlayssepserwfeorremepderufsoirngmemdeawnitshfcroommpcuotleor-
from 5 to 10. software packages (Data Desk, Data Description Inc., Ith-
aca, NY; JMP, SAS Institute, Gary, NC; Kaleida Graph,
Synergy Software, Reading, PA).
corded the mode ofbudding (i.e., intratentacular or extra-
tentacular) for marginal and non-marginal polyps sepa- Results
rately. Formation of a new bud outside the polyp wall Marginal and non-marginalpolyps
was recorded as extratentacular budding, and formation
of a new polyp wall dividing the original polyp was re- Sixoftwenty-threecolonies smallerthan 2 cm in diam-
corded as intratentacular budding. eter(9polyps) had only marginal polyps. Hence, the com-
Fourpolyps, two marginal and two non-marginal, were parisons between marginal and non-marginal polyps were
randomly selected from each colony after decalcification. conducted for the 17 colonies that had both polyp types.
These 44 polyps were measured and excised from the Values for mean polyp volume, fertility, and mean NE/
colonies as described for egg-count polyps, and then PV ofnon-marginal polyps were significantlygreaterthan
rinsed in distilled water and dried at 60C to constant thoseofmarginal polyps from the samecolony (Wilcoxon
weight. Each polyp was weighed to the nearest 0.1 ing. paired-sample test, all P < 0.01; Fig. 2A-C). The mode
Theestimated polyp volume showeda strong linearcorre- of budding was also significantly different between the
lation with the somatic biomass, both in marginal (r = two groups (Fisher exact test, P < 0.0001). All the bud-
0.87, P < 0.0001, n = 22) and non-marginal (r = 0.84, ding (total = 58) in non-marginal polypswasintratentacu-
P < 0.0001, n = 22) polyps, with nosignificantdifference lar, and 96% of the budding (total = 53) in marginal
between the two regression lines (ANCOVA. df = 1, SS polyps was extratentacular.
= 0.29, F = 0.17, P = 0.7). Therefore, assuming that the
polyp volume represents the somatic biomass, I calculated Colony size, polyp size, and egg production by polyps
tmhme"av3)erfaorgemanrugminbaelraonfdengogns-mpaerrgipnoallyppovloylpsumien e(aNcEh/cPoVl,- sizTe,oaenxdaemgigneprtohdeucretliaotni,onIsghriopsupaemdotnhge ccoolloonniyessiiznet,optohlryepe
ony. size classes: small (S; ==60 polyps, or s4.5 cm in mean
colony diameter), medium (M; 60-150 polyps, or 4.5-
Colonyfecundity 9 cm), and large (L; >150 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. Sexual reproduction and
mentssmallerthan the minimum size at maturityobserved colony growth in the scleractinian coral Porites astreoides. Biol.
in naturally growing colonies, and found that some ofthe Bull. 172: 161-177.
EGG PRODUCTION IN A COLONIAL CORAL 325
Hall.V. R.,andT. P.Hughes. 1996. Reproductivestrategiesofmod- ageorsizelimited?Proc. _V/iInt. CoralReefCongr., Tahiti4: 289-
ularorganisms: comparative studiesofreef-buildingcorals. Ecology 293.
77: 950-963. Meester, E.H., and R.P.M. Bak. 1995. Age-related deterioration
Harriott, V.J. 1983. Reproductive ecology offourscleractinian spe- ofaphysiologicalfunctioninthebranchingcoralAcroporapalmata.
cies at Lizard island. Great Barrier Reef. Coral Reefs 2: 9-18. Mar. Ecol. Prog. Ser. 121: 203-209.
Harrison, P. L., and C. C. Wallace. 1990. Reproduction, dispersal Sakai, K. 1997. Gametogenesis, spawning, and planula brooding by
and recruitment ofscleractinian corals. Pp. 133-207 in Ecosystems the reefcoral Goniastrea aspera (Scleractinia) in Okinawa, Japan.
ofthe World, Vol. 25. CoralReefs, Z. Dubinsky. ed. Elsevier. Am- Mar. Ecol. Prog. Ser. 151: 67-72.
sterdam. Sakai, K. 1998. Delayed maturation in the colonial coral Goniasin-a
Hayashibara,T., K. Shimoike,T. Kimura,S. Hosaka. A. Heyward, aspera (Scleractinia): whole-colony mortality, colony growth and
P. Harrison, K. Kudo, and M. Omori. 1993. Patterns of coral polyp egg production. Res. Popul. Ecol. (Kyoto) 40: (in press).
spawningat Akajima Island, OkinawaJapan. Mar. Ecol. Prog. Ser. Soong, K., and J.L. Lang. 1992. Reproductive integration in reef
101: 253-262. corals. Biol. Bull. 183: 418-431.
Heyward,A.,K.Yamazato,T.Y'eemin,andM.Minei. 1987. Sexual Szmant, A.M. 1986. Reproductive ecology ofCaribbeanreefcorals.
reproduction ofcorals in Okinawa. Galaxea 6: 331-343. Coral Reefs 4: 43-54.
Hughes,T.P.,andJ.B.C.Jackson. 1985. Populationdynamicsand Szmant,A.M. 1991. SexualreproductionbytheCaribbeanreefcorals
life histories offoliaceous corals. Ecol. Monogr. 55: 141-166. Montastrea anniilaris and Montastrea cavernosa. Mar. Ecol. Prog.
Jackson, J.B.C. 1979. Morphological strategies of sessile animals. Ser. 74: 13-25.
Pp. 499-555 in BiologyandSystematic!ofColonialOrganisms, G. Van Veghel, M.L.J., and M. E. H. Kahmann. 1994. Reproductive
Larwood and B. R. Rosen, ed. Academic Press. New York. characteristics of the polymorphic Caribbean reef building coral
Jackson,J. B.C.,and A.G. Coates. 1986. Lifecyclesandevolution Montastreaannularis. II. Fecundityandcolonystructure.Mar. Ecol.
ofclonal (modular) animals. Phil. Trans. R. Soc. Land. B 313: 7- Prog. Ser. 109: 221-227.
T-> Veron, J.E.N. 1986. Coralx ofAustralia and the Indo-Pacific. An-
Jackson, J.B.C., and T.P. Hughes. 1985. Adaptive strategies of gus & Robertson, North Ryde. Australia.
coral-reef invertebrates. Am. Sci. 73: 265-274. Zar,J.H. 1996. BiostatisticalAnalysis. 3rd ed. Prentice-Hall, Upper
Kojis, B. L., and N.J. Quinn. 1985. Puberty in Goniastreafavulus: Saddle River, NJ.