Table Of ContentReference:Bint.Hull 193:40-46.(August. 1997)
Reduction ofGrowth Rate as the Major Process in the
Miniaturization ofthe Sand Dollar
mai
Sinaechinocyamus
CHANG-PO CHEN AND CHI-MING CHAO
InstituteofZoology,AcademiaSinica,Nankang. Taipei, Taiwan II?, RepublicofChina
Abstract. Sinaechinocyamusmaiisanextremelysmall view,seeHankenandWake, 1993).Thedevelopmental
sand dollar, the maximum size being 10.9mm. It has mechanism that mediatesevolutionary change in body
beensuggestedthatSinaechinocyamusisaminiaturized sizeandform hasbeenaddressedinanumberofstudies
progenetic sand dollar that closely resembles thejuve- in terms ofheterochrony (McKinney and McNamara,
nilesofScaphechinus. In thisstudy,weinvestigatedthe 1991). Changes in onset timing, offset timing, and
mechanisms responsible for the miniaturization. Our growth rate in the entire individual (global hetero-
analysis ofpopulation dynamics, maturity, and annual chrony) or only in different characteristics but not
reproductive cycles suggests that the growth rates ofS. throughouttheindividual(dissociatedheterochrony),or
maiareabout 19%thegrowthratesofScaphechinusmir- even in opposite processes(mosaic heterochrony) have
ahilis, which reaches a maximum size of88mm. The diversifiedbodysizeandform(Skelton, 1993).
developmentalstagesoforalandaboralsurfaceswerede- Thedirect mechanismsthat resultin miniaturebody
finedonthebasisofthenumberofdiscontinuousinter- size are the precocious cessation ofgrowth, known as
ambulacral plates and the number oftube-foot pore- progenesis, and the reduction ofgrowth rate, known as
pairs, respectively. The patterns ofthe oral and aboral neoteny. Precociouscessation ofgrowth meansthatthe
surfacesofthetwospecieswerecompared,bothatorigi- ancestral patterns ofgrowth in massand allometry are
nalsizeandaftertheScaphechinusmirabilispatternhad unchanged, but the duration of growth is truncated.
beenreducedtoasizeproportionaltothatof5.mai(i.e.. Thus, lifespan is reduced by truncatinggrowth and de-
to 19% original). On the oral surface, the patternswere velopment, the reproductive system becomes mature
differentattheoriginal sizes, butsimilarwhen thepro- precociously,andalldevelopmentalstagesremaininthe
portionalsizeswerecompared;thisindicatesthatthede- juvenileform oftheancestor. Reduction ofgrowthrate
velopmentoftheoralplatesisage-dependentinS. mai. means that the ancestral rate ofgrowth in mass is re-
On the aboral surface, the patterns were similar at the duced, but the pattern of allometry and duration of
originalsizes,butdifferentintheproportionalcompari- growth remains unchanged. Thus, all developmental
son,indicatingthatthedevelopmentoftheaboralplates andmaturationratesremainconsistentwiththoseofthe
issize-dependentinS1.mai.S.maibecomessexuallyma- ancestor.Althoughthemorphologicalcharacteristicsare
ture at the age of2 years, and Scaphechiints minihilis present at the expected age, they appear on a smaller
maturesprobably ataboutthesameage. Ourdatasug- scaleasaresultofthereductioningrowthrate. Thede-
gestthatthereductionofgrowthrate(neoteny)isamore scendant is thus a microcosm ofits ancestor. Indeed,
importantmechanismofminiaturizationinS. maithan different characteristics may have different hetero-
isprecociouscessation(progenesis). chronic processes the mechanism of miniaturization
maynotbesimpleatall.
Introduction Sinaechinocyamus mai. an endemic species in Tai-
Miniaturization is the evolution ofsmall adult body wan, is an extremely small sand dollar, the maximum
sizeandisawidespreadphenomenoninanimals(forre- sizebeing 10.9mminover2000individualscollected.It
hasanannual reproductivecycle,spawnsfromOctober
Received5July1996;accepted23May1997. toNovember,andhastypicallarvaldevelopment(Chen
90
MIN1ATLIRH OF SAND DOLLAR 91
andChen, 1993). Inaddition,ithasintestinaldiverticu- soaspawningdateof1 Novemberwasusedinestimating
larsand grains that function asweight belts(Chen and age.Thegrowthcurvewasestimatedbyregression lines
Chen. 1994; Mooi and Chen, 1996). Mooi (1990) has from each individual's size and its estimated age
suggestedthatSinaechinocyamusisahighlyderived,ex- (month). Thegrowth rateofS. maiwascomparedwith
tremelyminiaturizedprogeneticsanddollarthatclosely that ofScaphechinus mirahilis as reported by Brykov
resembles juveniles ofScaphechinus in its patterns of andParasyna(1979).
oralandaboral plates, fossilrecord,andgeographicdis-
tribution. Scaphechinus mirahilis is distributed in the Developmentoforalplates
waterssurroundingJapan,anditsmaximumsizemaybe
88mmintransversediameter(Nisiyama, 1968). TestswerecollectedfromtheseashoreinwesternTai-
To reveal the mechanisms of miniaturization in 5. wan (including Hsinchu, Tainan, and Tunghsiao). The
mai, someontogeneticdata, includingage, size,growth outlinesoforalplatesweredrawn fromtestsplaced un-
trautree,adgeev,elwoeprmeecnotlallecstteadg.esG,edneervaellloyp,meangteailsreastte,imaantdedmab-y dWeirldaWTiYlPd M3038Z70d0issdercatwiingngmitcurbeo.scTohpeeevqiusiibpilpietdy woiftthhea
growth zones, orrings(Pearseand Pearse, 1975; Gage, plateswasincreasedbyadjustingthemimntensityandinci-
1991), but growth zones are not easily observed in S denceofthelight.Testslessthan 3 in lengthcould
mat Thus, the age and growth rate wereestimated ac- notbestudiedunderthedissectingmicroscope;therefore
cording to the population dynamics, size at maturity, they weredried and coated, and then examined with a
and annual reproductivecycle. Developmental charac- scanningelectronmicroscope.
teristicsincludetheseparationofinterambulacralplates Thedevelopmental stage ofthe oral plates wasdeter-
on the oral surface, and an increase in the number of mined by counting the discontinuous interambulacral
tube-foot pore-pairsin the petaloids. Therefore, thede- plates. Eachdistinctlyseparateinterambulacralplatewas
velopmental stagesoforal platesandaboral plateswere countedas1point.Platesintheprocessofseparating(i.e..
determinedasthenumberofdiscontinuousinterambu- not easy to distinguish whether separated or not) were
lacral platesandthe numberoftube-footpore-pairs,re- countedas0.5point.Eachsanddollarhas 10interambu-
spectively. The results reveal that the reduction of lacralplates,sothescoreforatestwasderivedbytotaling
growth rate in S. mai is a more important mechanism thenumberofdiscontinuousplatesamongthe 10.
forminiaturizationthanisprecociouscessation.
Developmentofahoralplates
MaterialsandMethods
To trace the developmental characteristics ofaboral
Populationdynamicsandmaturity plates,individualswerefirsttreatedwithhousebleachto
FromOctober 1994toMarch 1996.individualsofSi- remove the spines. The numbers ofgonadal pores and
naechinocyamusmaiwereperiodicallysievedwitha0.5- tube-footpore-pairswerethencountedwiththeaidofa
mm-meshscreen fromsand flatsinthelowtidezoneof dissectingmicroscope.
Tunghsiao(120 39'45"E;24 29'21"N),Miaoli,western Theoral andaboraldevelopmental stagesofScaphe-
Taiwan. The sizes of individuals collected were mea- chinusmirahiliswerebasedondescriptionsinotherpa-
suredasthelongestlengththroughtheanus. pers(Nishiyama, 1968; Mooi, 1990) and on specimens
Spawningwasinducedinindividualscollectedduring collectedfromJapanbyDr. M. KomatsuandY. Kano.
thespawningsMeason(October 1994and 1995)byinject- Actual-size sketches of Scaphechinus mirahilis were
ing0.1 ml0.5 K.C1intothecoelomthroughtheanus. tracedinpencilonthinpapercoveringthetests.
Eggs were then fertilized artificially, and cleavage was
verifiedwitha Wild M3Zdissectingmicroscope. In ad- Results
dition,thegonadsofindividualsthatdidnotspawnafter
injectionwithKC1wereremovedtodeterminetheirma- Size-frequencydistribution
turity. The gonads were fixed in 10% neutral formalin Livingsanddollarswerecollected at Tunghsiao nine
overnight,andthentransferredto70%ethanol,dissected timesfrom October 1994 to March 1996. With theex-
byremovingtheoralhalfofthetest,andexaminedwith ceptionoftheFebruary 1995collectioncontainingonly
adissectingmicroscope.Thematurityofthegonadswas 5 individuals,thesizedistributionsareshown in Figure
determinedusingthemethodsofChenandChen(1993). 1. Two size groups clearly existed in the sand dollars
gathered in August and October 1995, while the other
GrAocwctohrrdaitnegatnoalCyhseisnandChen(1993),thespawningpe- cOonlelesctainodnsdoclolnartacionleledctaedfeinwOlcatrogebrerin1d9i9vi4dwuaalss1(0F.i9g.m1m).
riod of5. maiis from lateOctobertoearly November, inlength.
92 C.-P. CHEN AND C.-M. CHAO
%
30 Oct.17,1994 30 Sep. 11,1995
20 (n=81) 20 (n=27)
10 10
23456789101112-i 0123456789101112
1
30 30
Jun 30,1995 Oct.23,1995
>o. 20 (n=79) 20 (n=183)
c 10 - 10 Y
3dJ
cr I-t.I
0) 01 23456789101112 01 23456789101112
CND
'(/> 30 Dec.1,1995
0>) 20 - (n=18)
'*-
_ro 10 -
n:
23456789101112 01 23456789101112
Aug. 11,1995 30 Mar 5, 1996
(n=417) (n=16)
10
01 23456789101112 01 23456789101112
Length(mm) Length (mm)
Figure I. SizefrequencydistributionofSinaechimicyamiununfromOctober 1994toMarch 1996.
Arrowsindicatethedivisionbetweentwosizegroupsoneachgraphexceptthelast two, inwhichthe
numberofspecimenswasnotsufficientforgroupstobediscerned.
Maturityofgametes small-size and large-size groups were assumed to be
differentagegroupsspawnedin 1994and 1993. respec-
Onlylarge-sized individualswereabletospawnin re- tively. Consequently, the growth rates ofthe first year
sponsetoinjectionofK.C1solutionduringthespawning and the second year were estimated from the age (in
season. The 33 maleand 32 female sand dollarsexam-
ined duringthe spawningseason showed no significant
sex-related difference in size distribution. Individuals
withmmmature oocytes or sperm were between 5.0 and 30 -,
6.0 inlength(Fig.2).
w 25 -
ruo Spawningindividuals
Thegrowthcurveandcomparison withScaphechinus I 20 Non-spawningindividuals
mirabilis 'o^ 15 -
Since the two size groups ofS. mat were distinct in % 10
degreeofmaturity,thegroupswereconsideredtorepre- 34567
sentdifferentages:specimensbelongingtothesmall-size 5 -I
gTrhoeuepxwterar-ela1rygeeairndyiovuindguearlt(h1a0.n9thmeimrlianrgleerngctohu)ntwearspacrotns.- 8 9
sideredtobeayearolderthanthemembersofthelarge- Length(mm)
sizegroup. Figure2. Sizeandmaturity.Onlylargeindividualsarematurein
Thissanddollarspawnsannually, thereforethe 1995 spawningseason.
MINIATURE OF SAND DOLLAR 93
10
9
8
^ ^ 7
E 6
94 C.-P. CHEN AND C.-M. CHAO
O
05
MINIATURE OF SAND DOLLAR 95
600
o
Q. 500
O
400
?
cu (/)
% 300
Q_
200 X S. ma/
(D * xS. mirabilis
.EQ 100 Jfc.' oPatternofS. mirabilis
reducedto 19%
10 20 30 40
Length (mm)
Figure7. Developmentalstageanddevelopmentalraleofahoralplates.
that this is a size-dependent characteristic, we propose waters ofJapan duringthe early Pliocene Epoch when
thatothercharacteristicsresponsibleforthesimilarityof the sea temperature was low. When watertemperature
adultS.muitojuvenileScaphechinusmirtihilismayalso rose,only miniaturizedSinaechinocyamuswereableto
bedependentonsize. Thesewould includeaboral peri- continuetheirexistencedowntothepresenttimeinTai-
procts, simple internal partitions, and food grooves wan. WehypothesizethattheselectivepressureonSca-
(listedbyMooi, 1990). phechinus was due to the warming sea temperature,
Thedevelopmentoforalplatesintermsofthenumber which would increase metabolic rates, exhausting the
ofdiscontinuousinterambulacral platesisacontinuous materials and energy needed for maintenance and
processofplaterearrangement,anditissomewhatinde- growth and leading to the disappearance ofScaphechi-
pendentofsize.Changesinonset,offset,andgrowthrate nusfromTaiwan.Conversely,aslowgrower,evenwith
indifferentoralplatesmaycausedifferentconsequences: thesamemetabolicrate,mighthavebeenabletotolerate
thus, thedevelopmentofdiscontinuousplatesbecomes thedisordercausedbyawarmingofthewatertempera-
very variable in sand dollars (as in Echinarachnius ture.Thus,wespeculatethattheadvantageofthesmall
parma; see Lohavanijaya and Swan, 1965). Compari- size ofSinaechinocyamus is related to the slow growth
sons ofthis characteristic should be limited to species rate,whichpassivelyallowsforexistenceinwarmerwa-
thatarecloselyrelated,liketheonesinthisstudy. ters.
SinaechinocyamushasexistedinTaiwansincethePli-
oceneEpoch(Wang. 1984);Scaphechinuswasrecorded
in the Pliocene Epoch in both Taiwan (Hayasaka and Acknowledgments
Morishita, 1947)andJapan (Mooi, 1989), butisextant Wewouldliketoexpressourgratitudeto MissChin-
in Japan only. Since both genera occurred simulta- hsiuTsengforhelpingintheearlyphaseofthisresearch,
inneoSuisnlayedcuhriinnogcythaemuPsliioscdeinfef,ictulhtetionietxipaltaiionn,obfustpetchieatsiuocn- taondDrt.oRbiocthhMDoro.iStfeorvecnritCi.calBleyadrleeadainngdtahne maannounsycrmioputs,
sceasnsdogfrmaiinnisatinurtihzeatdiiovnermtiacyulbaefroerlpatoesdittioonthmeapirnetseenncaencoef sreeavricehwewrasforsuvpaplouratbeldebcyomthmeenNtatsioannadl sSucgigeenscteioCnso.uncRiel-
(ChMeenanangdloCbhaeln.tem19p9e4r)a.turedropped from the Miocene (NSC84-2311-B-001-062)oftheRepublicofChina.
Epoch totheQuaternaryIceAge. Afterwards,thetrend
reversed, and global temperature reached its current LiteratureCited
state(Skelton, 1993).Onthebasisofwatertemperature
changes and the geographical and stratigraphic occur- Br.vkot,V.A.,andA.S.Parasyna.1979.Quantitativegrowthcharac-
aremnucseomfigthhetsehatvweoegveonlevread,wfreopmraoploocsael,thmaatrSgiinnaaelcphoipnuolcay-- 2Btei6rd6i/.s,ti(castorfantshleatsiaonndofdoBliltairloSgciavaphMeochrivnaus(Vmliardaihivloisxt.okS)ov5.(4)./:. 2Ma6r2.-
tionofScaphechinusthatextendedtoTaiwan from the Chen,B.-Y.,andC.-P.Chen.1993.Reproductionanddevelopmentof
96 C.-P. CHEN AND C.-M. CHAO
aminiaturesanddollar,Sinaechinocyamiii unit(Echinodermata: Mooi.R. 1989. Livingand fossilgeneraoftheClypeasteroida(Echi-
Echinoidea)inTaiwan.Bull ln\l /.ool Acutl Sin (Taipei)32(2): noidea:Echinodermata):anillustratedkeyandannotatedchecklist.
100-110. Sniillisun C'onlnh./ji/il.488:51pp.
Chen,C.-P.,andB.-Y.Chen. 1994.Diverticulumsandinaminiature Mooi,R.1990.ProgeneticminiaturizationinthesanddollarSimicclii-
sanddollarSinaechinocyamusnun(Echmodermata:Echinoidea). iioc\'iiniu\-implicationsforclypeasteroidphylogenv.Pp. 137-143
Mar Biol 119:605-609. inEc/inioilermRi:wari-li.C.D. Ridder. P. Dubois, M.-C. Lahaye,
Gage.J.D. 1991.Skeletalgrowthzonesasage-markersinseaurchin andM.Jangoux.eds.A.A.Balkema:Rotterdam.
Puimmirlii>iit\iiiiliun<: Mm Ui,,l 110:219-228. Mooi,R.,andC.-P.Chen.1996.Weightbelt,diverticulaandthephy-
Hanken,J..andD.B.\\ake. 1993.Miniaturizationofbodysize:or- logenyofthesanddollars.Bull Mar.Sci.58:186-195.
ganismalconsequencesandevolutionarysignificance.Annii- Rc\' Nisiyama,S. 1968.TheEchinoidfaunafromJapanandadjacentre-
Ecu! SY.W.24:501-509. gions,partII.I'dlacoiilnl SueJP.\Spec Pap 13:I12-122.
Ilayasaka,I.,andA.Morishita. 1947.Notesonsomefossilechinoids Pearse.J.S.,andR.A.Cameron.1991.Echinodermata:Echinodea.P.
ofTaiwan,II.Ada(Jcl Tannin 1:93-110. 561inReproductionofMarineInvertebrates, !'/. 17:Echiniiiicrm.s
Lawrence,J.M. 1987..1 FunctionalBinlngy"/Echinoderms. Johns tiiulLophophorates.A.C.Giese,J.S.Pearse,andV.B.Pearse.eds.
HopkinsUniversityPress,Baltimore. BoxwoodPress.PacificGrove,CA.
Lohavanijaya, P., and E.F. Swan. 1965.Theseparation ofpost-ba- Pearse,.1.S.,and V.B. Pearse. 1975.Growthzonein theEchinoid
sicoronalareasfromthebasicoronalplatesintheinterambulacraof skeleton.,tin /,>/ 15:731-753.
thesanddollar,Ec'hinarucfiniWipurma(Lamarck).Biol Bull 129: Skelton,P.\V.1993.P.959inEvoliiiutn.aBiologicalamiI'alMonlo-
167-180. logicalApproach Addison-Wesley,Reading.MA.
McKinney,M.L.,andK.J.McNamara.1991.Ilcicrnchrony Plenum \\ang,C.-C.1984.Newclassificationofciypeasteroidechinoids.Prm:
Press.NewYork. licul Soc China21:119-152.
