Are Echinoderm Egg Size Distributions Bimodal?

9 Pages·1997·3.4 MB·English

by  M A Sewell

Reference:Bin/. Bull. 193:297-305.(December, 1997)
Are Echinoderm Egg Size Distributions Bimodal?
MARY A. SEWELL* AND CRAIG M. YOUNG
Department ofLan'al Ecology, HarborBranch Oceanographic Institution,
5600 U.S. 1 North, Fort Pierce, Florida 34946
Marine invertebrates can be categorized into species In marine invertebrates there is a tradeoffbetween fe-
that reproduce by producing either large numbers of cundityandtheamount ofenergy thatcanbeinvestedin
small, energeticallyinexpensiveeggsthatbecomeplank- eachegg.Thus,asarule,aspeciesproduceseithermany,
totrophic larvae, orfewer, larger eggs with more yolk small eggs with planktotrophic development or fewer,
andlecithotrophicdevelopment(1). Theselectiveadvan- larger eggs with lecithotrophic development (1). As the
tagesofthesealternativestrategieswereconsideredin a size ofeggs may differ between closely related species,
series ofsimple mathematical models by Vance (2. 31. eggsizeisassumedtobesubjecttoconsiderableselective
Thesemodelspredictedthatintermediateeggsizesshould pressure (15-17). This has prompted interest in docu-
havelowerreproductiveefficiency, andthatonlvextreme menting patterns ofegg size among species and higher
egg sizes should be evolutionarily stable (2, 3). Specifi- taxa, and in exploring how factors such as phylogeny
cally, Vance'smodels (2. 3), andlatermodifications (4- (15), fertilization biology (16, 18. 19), length ofthe pre-
7), predictthateggsofmarineinvertebratesshouldhave hatching (14, 20) and prefeeding periods (17), and size
bimodalsizedistributions, reflectingthecontrastbet\veen andorganiccontentatmetamorphosis(e.g., 14,21)might
smallegg/feedingandlargeegg/nonfeedingmodesofde- be important for selection ofegg size.
velopment and the selection against intermediate egg In early mathematical modeling Vance (2, 3) viewed
sizes. Evidenceforbimodalityineggsizedistributionsis, planktotrophy and lecithotrophy asextreme formsoflar-
however, equivocal, with unimodal distributions seen in val development, and his models suggested that only the
the majority ofcomparative studies thatareappropriate extreme egg sizes would confer maximum reproductive
testsofthehypothesis(8-13).Bimodaldistributionshave efficiency (number of newly metamorphosed adults per
been describedonly in afewgroupsofmolluscs (4)and unit of energy devoted to reproduction). Subsequently,
in asteroidandechinoidechinoderms (14). Here we test the prediction ofbimodality in egg sizes within taxa of
theprediction ofbimodalityin theholothuroidandophi- marine invertebrates was tested by a number ofauthors
uroid echinoderms and show that although the natural usingpreviouslypublishedornewdatasets.Mostofthese
log-transformed egg size distributions are visually uni- studies showed unimodal egg size distributions (see also
modal,theholothurianeggsizedistributionisstatistically fig. 2 in ref. 22). Examples include prosobranch gastro-
composedoftwo discrete modes. Moreover, reexamina- pods (9, 10), opisthobranchs (II), muricid gastropods
t(i1o4n)owifththteheasatdedriotiidonanofddeacthaifnrooimd megogresirzeecednitstlriitbeurtaitounrse (w8i)t,hcohuittnounrss(e2e3)g,gsth(o1r2a)c,iIcnadno-bPaarcniafcilcesCo(n2n4)s,(a1n3)d,sbtiovmaaltvoe-s
confirms that there are t\vo statistical modes in the egg pods (25). Bimodal distributions in egg size were de-
size distributions ofthese classes. Thus, in the phylum scribed in American species ofthe genus Crepidula (4),
Echinodermata, there is a bimodal egg size distribution in prosobranch gastropods from Danish waters (4), and
in three ofthe fourclasses in which thisprediction can in echinoid and asteroid echinoderms (14).
be tested. Manyofthe early studies used data sets that were not
adequate for a valid test of the distribution patterns of
R*ePcreeisveendta1d1drMeassr:chDep1t9.77o;faBcicoelpotgeidca2l2ScSieepntc.es1,99U7..S.C.LosAngeles. esegtgs:s(iaz)e.thWeedatdaesfhinoeudldtihnrceleudceritbeortihapfloarnkatpoptrroopprhiiacte(fdeaedt-a
CA90089-0371;e-mail: [email protected] ing) and lecithotrophic (nonfeeding) forms of develop-
297
298 M. A. SEWELL AND C.M. YOUNG
ment; (b) the egg sizes should be from species that span its use fortheoretical discussions oflife-history patterns.
a broad range ofhabitats and a wide geographic range; Hrstly,manyspecieshaveoblatelyorprolatelyspheroidal
and(c)thedatashouldexcludespeciesthatprovideaddi- eggs,sothateggswiththesamediametermayhavediffer-
tional maternal investment (e.g., nurse eggs, capsules). ent egg volumes (30). We did not attempt to convert
Criterion(b) isnecessarybecauseeggsizemaybecorre- publishedeggdiameterstovolumesbecauseinmostcases
lated with habitat for example, more planktotrophs in only one ofthe two linear dimensions required for such
the tropics (1) and use ofspecies from a limited geo- acalculationwaspresented.Secondly,eggmeasurements
graphic area might under- or overemphasize a particular made from histological sections will underestimate egg
developmental type. Criterion (c) is necessary because diameter because of tissue shrinkage during processing
Vance's models (2, 3) assume that reproductive energy and the hydration ofthe egg during spawning (30). We
is invested solely in the egg. Additionally, because the used the diameters of both intraovarian and freshly
models (2, 3) were developed in terms ofenergetic con- spawned eggs in this paper to increase the sample sizes
tent rather than egg size per se. for all data sets it is for statistical analysis (n > 100 species for all classes).
assumed that there is acorrelation between egg size and Because the size classes in the raw (100//m) and In-
energetic content. transformed analyses (In 0.25) are relatively large, we
The primary criterion, that planktotrophic and lecitho- assumed that intraovarian egg diameters would have a
trophic formsbepresent, is violatedby threeofthe taxa: low probability of moving into an adjacent size class
thoracican barnacles (24) and stomatopods (25), neither should a freshly spawned egg diameter be available.
ofwhichgroupsincludespecieswithlecithotrophicdevel- Thirdly, eggs differ in theirorganic components lipid,
opment, and chitons (23), which do not include species protein,etc (27,30)andourassumptionthateggdiame-
with planktotrophic development. Criterion (b) may be ter is an effective measure ofmaternal investment may
violated by Ockelmann's bivalve data set (8) because prove to be untenable.
planktotrophsarerareinEastGreenland(26),incompila- Previous studies of egg size distributions in marine
tions ofegg sizes in American species ofCrepidula (4) invertebrates have determined the number of modes in
and Danish prosobranchs (4), and in studies with low the distribution by visual appraisal. In this paper we in-
samplesizes(4,23,24,25). Violationofcriterion(c)has steadmadeuseofstatisticaltechniquesdesignedtodiffer-
beenavoidedbyremovalofspeciesusingnurseeggs(12, entiate length-frequency classes offish populations (31).
fig. 2inref. 22).Withtheremoval ofstudies thatclearly Histograms ofegg diameter frequencies were generated
violatecriterion (a) there are unimodal egg size distribu- foreachclassusingtherawandIn-transformeddiameters
tionsinsixtaxa(8-13)andbimodaldistributionsinfour as shown in Figures 1-4. A modal analysis using the
taxa (4, 14). method of Schnute and Fournier (31) was then used to
The best known, and most widely cited, example of identify the Gaussian modes presented in these figures.
thebimodulityineggsizeswithinataxonistheextensive Becausetheanalysisisrelativelyinsensitivetothedimen-
data set compiled by Emlet et al. (14) for asteroid and sionsofthesizeclasses(31;B. Smith,pers.comm.),this
echinoid echinoderms. This data set meets criteria (a)- method provides an objective way to examine the egg
(c) above, incorporating egg sizes from 89 asteroid spe- sizedistribution inaparticulartaxonanddirectlytestthe
ciesand 109 echinoid species from a variety ofhabitats. hypothesis ofbimodality ofegg sizes in marine inverte-
Moreover, in this phylum there is a strong correlation brates (2, 3). The complete raw data sets used forthese
between egg size andenergetic content (27). Ofthe four analysesareavailabletointerestedreadersfromeitherof
remainingclassesofechinoderms,ourcriteriaarenotmet the authors.
in thecrinoids, wherethereare noknownplanktotrophic Holothuroids show an extreme range in egg diameter,
species (28), orintheconcentricycloids, where there are fromaminimumof50pmin the apodidSynaptula reci-
only twodescribedspecies(29). Inthispaperwetestthe procanstoamaximumof4400/urnintheelasipodPsych-
predictionofbimodalityineggsizesinthetworemaining ropoteslongicauda (Fig. 1A). About 80% ofthe species
classes, the holothuroids and ophiuroids, which meetthe have eggs smaller than 1000/jm in diameter (Fig. 1A),
criteriadefined above, andwe incorporate new data into withfourmodesinthesize-frequencydistribution(Table
thepublishedeggsizedistributionsofechinoidsandaster- I). The first mode is at an egg diameterof 194fjm (Fig.
oids (14). 1A, Table 1), and comprises species with eggs from 50
Theegg sizedatasets used in thisanalysis werecom- to about 300/ym with planktotrophic orunknown devel-
piled from the published literature and our own unpub- opment (Fig. 1A). A second, but overlapping, mode is
lisheddata, with the implicit assumption that all echino- seenat421 pm,withspecieswithlecithotrophic.brooded,
derm eggs are basically alike. As noted by Turner and or unknown development (lecithotrophs: 150-950//m;
Lawrence (30), although egg diameter is an easy repro- Fig. 1A). A large number of species in the unknown
ductive character to measure, there are shortcomings in categoryinthismodearedendrochiroteholothurianswith
EGG SIZE IN ECHINODERMS 299
HOLOTHUROIDEA
=184
ooooooooooooooooo~o"oooooo
Egg Diameter((am)
0-
CMCMCNCNCNCNOJCNCMCSICMCNCNCMCNCNCNCvJCMCM
CD^CQ^
oT <oO < Cv-O C*M CCOM CTO CCDO * CO T CD O*OOCDOO*iaCiD
Ln Egg Diameter
Figure 1. Eggsizedistributionpattern intheclassHolothuroidea( = 184). Informationontheegg
sizeofspeciesofholothurianswascompiledfromthepublishedliteratureandourownunpublisheddata.
Ifmore than one egg size was reported for a particular species, the maximum value was used in the
figure.Thetypeoflarvaldevelopment(planktotrophic,lecithotrophic,brooding)wasbasedontheknown
developmentofthatspeciesfromlaboratoryorfieldcollections.Thisresultedinalargenumberofspecies
with unknown developmental type; egg size was not used to infer developmental mode. Species were
categorized as having an auricularia larva (planktotrophic). a doliolaria larva only (lecithotrophic), or
internal/externalbrooding.Twospecies,HolothuriafloridanaandThyonefusus, thatarereportedtohave
pelagicdirectdevelopmentwereincludedwiththelecithotrophs.Thecompleterawdatasetforthisfigure
canbeobtainedfromeitheroftheauthors.(A)Histogramoftheuntransformedeggdiametersintheclass
Holothuroidea;.t-axis shows the midpoint ofthe 100-^m size class. (B) Histogram ofthe natural log-
transformedeggdiametersintheclassHolothuroidea;x-axisshowsthemidpointoftheIn0.25sizeclass.
PartBfollowsEmletetal.(14)inusingthenaturallogtransformationofeggdiametertocombinespecies
with large lecithotrophic eggs into asmallernumberofcategories. Legendto developmental type isas
showninpartB:P = planktotrophic(n = 20); L = lecithotrophic(n = 22);B = brooded( = 38); ?=
unknowndevelopment(H = 104). Solidlinedifferentiatesmodesidentifiedinthestatisticalanalysis(see
TableIfordetails).
egg sizes in the 200-800//m range. As there are no development type (Fig. 1A) the majority ofthe latter
known planktotrophs in this order (32), this mode may species are elasipod holothurians and may have direct
additionally include 20 lecithotrophic species. The last development(33).Thus,intheholothuriansthefirstmode
twomodes,at 1024and2603//m,areprimarilycomposed containsmainlyspecieswithplanktotrophicdevelopment;
ofspeciesthatarelecithotrophic,brood,orhaveunknown the following three modes are species with nonfeeding
300 M. A. SEWELL AND C.M. YOUNG
Table1
Kexnllxnliinx/iiliiiiiil\'xixfurcw.v/'rcilixtrilnitiniixinnxteroul
(n = 149),t'chmoid(n = Ml), hclotliurniilIn = 1X4).
andophiuroidechinodemu in = /->'-)
No ol
Class modes
EGG SIZE IN ECHINODERMS 301
oooooooooooooooooooo
n in m m in
n co r co 01
Egg Diameter
Lnininininininininininmininininininmin
CMCNCNCNCNCNCNJCNJCSJOMCNJCMCNCNCSJCNICNCNCMCN
CO COT-CD CO COT-COT CO' CD i- cp T- cp
06 od <T> CD
Ln Egg Diameter(jam)
Figure2. EggsizedistributionpatternintheclassOphiuroidea(n= 1321.Informationontheeggsize
ofspeciesofophiuroidswascompiledfrom Hendler(109ophiuroidspecies,ret". 38)andlaterpublished
literature.ThetypeoflarvaldevelopmentwasbasedonHendler'sclassification(ref.38,p.456):plankto-
trophic =witharelativelylong-livedophiopluteuslarvae;abbreviated= reducedophioplutei.embryosin
an attached fertilization envelope, lecilhotrophic vitellaria larvae, or demersal larvae; brooded/direct =
viviparous,internalorexternalbrooding,orwithaneggcapsule.Thecompleterawdatasetforthisfigure
canbeobtainedfromeitheroftheauthors.(A)Histogramoftheuntransformedeggdiametersintheclass
Ophiuroidea; .v-axis shows the midpoint of the 100-jjm size class. (B) Histogram of the natural log-
transformedeggdiametersintheclassOphiuroidea;.v-axisshowsthemidpointofthe In 0.25 sizeclass.
LegendtodevelopmentaltypeisasshowninpartB: P= planktotrophic(n = 22);A=abbreviated(n =
12);B/D =brooded/direct(n = 31);?= unknowndevelopment(n =67).Solidlinedifferentiatesmodes
identifiedinthestatisticalanalysis(seeTableIfordetails).
planktotrophicdevelopment,buthastheshortestperiodof asteroidsthatshowtwoseparate,distinct,andstatistically
development (65 days) ofany ofthe Antarctic asteroids differentiatedmodes(Fig.3B).Therearefewspecieswith
studiedby BoschandPearse(35). Forthese species,par- egg sizes in the size class In 5.5 to 5.75, equivalent to
ticularly, it would be ofinterest to examine whether the egg diameters of245 to 314//m (Fig. 3B).
energetic content or biochemical composition of their Twenty-two egg sizes were added to the echinoid data
eggs differs from those of other asteroids of the same set of Emlet et al. (14). The untransformed distribution
developmental type. comprises four modes (Fig. 4A, Table I). The first two
In the fourechinoderm classes analyzed, it is only the modes, at 102 and 317//m. overlap considerably and are
302 M. A. SEWELL AND C.M. YOUNG
50
ASTEROIDEA
N=149
40-
cfl
g>
'8
Q.
CO
20-
10-
ooooooooooooooooooooo
Egg Diameter (|im)
CoTNdJcCroN^-CN: JCTCO-Nc1*C\NiCccNo\I*iCcNoJccCooN'^CT-N*cI3oC:NCNICCON'CCNCONTC-NCCNOI*CNCCNOC*N-CCNOI
Ln Egg Diameter(jam)
Figure3. EggsizedistributionpatternintheclassAsteroidea(n = 149).Informationontheeggsize
ofspeciesofasteroidsderivedfromEmletetal. (14)andmorerecentliterature. Thecompleterawdata
setforthis figure can be obtained from eitherofthe authors. (A) Histogram ofthe untransformedegg
diametersintheclassAsteroidea;.r-axisshowsthemidpointofthe 100-/jm sizeclass.(B)Histogramof
thenaturallog-transformedeggdiametersintheclassAsteroidea:.v-axisshowsthemidpointoftheIn0.25
size class. Legend to developmental type is as shown in part B: P = planktotrophic (n = 47): L =
lecithotrophic(n=57);B=brooded(n=26);?=unknowndevelopment(n= 19).Solidlinedifferentiates
modesidentifiedinthestatisticalanalysis(seeTable1fordetails).
composed of planktotrophic, facultative planktotrophic. Brisaster latifrom, 14) as well as all the lecithotrophic
and some lecithotrophic species (Fig. 4A). The last two and brooding species (Fig. 4B).
modesareoflecithotrophicandbroodingspecies(Fig.4A). Twoconclusionscanbedrawnfromthestatisticalanal-
The In-transformed histogram shows statistically two yses presented here. Firstly, in all classes the untrans-
modes (Fig. 4B, Table I). The first (In 4.60) comprises formed egg size distributions show three to four modes,
68% of the species and is composed almost entirely of the first being primarily of planktotrophic species, and
planktotrophic species, with the facultative planktotroph theremainingtwotothreecontainingmainlyspecieswith
Encope inicltelini (37) at the point of overlap between nonfeedingdevelopment(i.e., lecithotrophic,abbreviated,
modes 1 and 2 (Fig. 4B). The second mode, at In 6.22, brooded, or direct development). Secondly, the In-trans-
has ahigh standard deviation (Table I) and includes two formed distributions are bimodal in the holothurians, as-
speciesoffacultativeplanktotrophs(Clypeasterrosaceus. teroids,andechinoids, but unimodalintheophiuroids. In
EGG SIZE IN ECHINODERMS 303
60
ECHINOIDEA
50-
40-
'o
a
CO 30-
O 20-
10-
f"pfr III
I
n m
Egg Diameter (jam)
CNCNCNfMCMCMCNCNCMCMCNCNCMCSIOJCMCMOlCNCSI
TO- COD TT-- CTD- CM CCND CO CD CDI CD CD cd coop cp
Ln Egg Diameter
Figure4. EggsizedistributionpatternintheclassEchmoidea< = 131).Informationontheeggsize
ofspeciesofechinoidsderivedfromEmletettil. (14)andmorerecentliterature.Thecompleterawdata
setforthis figurecan be obtained from eitherofthe authors. (A) Histogram ofthe untransformedegg
diametersintheclassEchinoidea:.Y-axisshowsthemidpointofthe 100-/jmsizeclass.(B)Histogramof
thenaturallog-transformedeggdiametersintheclassEchinoidea;.v-axisshowsthemidpointoftheIn0.25
sliezceithcolatsrso.phiLceg(ennd=t1o6)d;evPe-lLopm=enftaaclulttavtpieveisplaasnkstohtorwonphin(npa=rt3)B;:BP==brpolaondketdot(rnop=hic8);( ?==8u5n);knLow-n
development(n = 19).Solidlinedifferentiatesmodesidentifiedinthestatisticalanalysis(seeTableIfor
details).
those classes with a bimodal distribution, it is only the allclasses,thereissomeoverlapineggsizebetweenthese
asteroidsandechinoidsthatshowademarcationbetween planktotrophic speciesandspecies with lecithotrophicor
modes with feeding and nonfeeding development. In the brooded development (Figs. 1-4). Egg sizes ofspecies
holothuroids, the modes are less visually distinct, and with "intermediate" forms ofdevelopment, suchasfac-
lecithotrophic and brooding developmental types are ultative planktotrophy (e.g., 17) or modified benthic de-
found in both modes. velopment(e.g., Patiriellaexigua, egg400/jm:34),gen-
Theegg sizedataexaminedhere(Figs. 1-4) illustrate erally fit within the mode for other lecithotrophic and
the need to view marine invertebrate development as a brooding species (Figs. 3 and 4).
reproductive continuum (5, 17, 22). Histograms of the An important direction for future research on echino-
egg size distribution show species with planktotrophic derm eggs is examination ofthe assumption made here,
development forming a distinctive group at smaller egg and in othercomparative studies (e.g.. 14), that all eggs
sizes (max. egg size <300^m; Figs. 1-4). However, in are basically equal (27). This question should be ad-
304 M. A. SEWELL AND C.M. YOUNG
dressedat two levels. Firstly, withinanechinodermclass 7. Havenhand,J.N.1995. Evolutionary'ecologyoflarvaltypes.Pp.
wcheemnieceadl icnofmopromsaittiioonnoonfstpheecieenserwgietthicacpoanrtteinctulaarnddevbeilo-- X. e7Odc9.k-Ce1l2Rm2CainnPnr,EescsKo,.loN\geVy.wo1f9Y5oM8ra.kr.inTeheInzveorotleobgryatoefLEaans'taGe,reLe.nlMacnEddmwaarridn,e
opmental type. For example, in the Holothuroidea it Lamellibranchia.Medd. Groenl. 122: 1-256.
would be of interest to determine whether the eggs of 9. kohn, A.J. 1961. Studies on spawning behavior, egg masses,
known lecithotrophs (egg diameter 150-950/jm) differ andlarvaldevelopmentinthegastropodgenusConns. II.Observa-
in any way from those ofthe planktotrophic species or tions in the Indian Oceanduring the Yale Seychellesexpedition.
fpSeorcdoosmntdthhlaeyt,laarrwegheseu(ns1p5esc0utf-fe4id4cio0ef0nth/audvrnai)tnaeggdhgiasrveoecfttbdheeeevnedelecopop-mmspeeinalteed(l,3a3s)ii.-t TwH\uihlmtlohm.m.epBcisMotol.ionggh,1ia9ci6aTn3l..OeEcm.epAah1nac9os6ogi7mrs.p..arJC.aDotliSlirh.evicemt1oe7:nmdobe3srv-eye5kol1ilo.poCmgoelyln.otfFmiisanhr.ithn1ee2:gnau2sd2ti9rbo-rp2ao5nd3cs.h,
wouldbeofinteresttocompareeggcharacters(size,ener- Catllnui laevis, with a discussion ofdevelopmental processes in
getic content, and composition) between echinoderm Opisthobranchia../. Mar. Biol.Ass. U.K.47: 1-22.
classes. In a recent review of the relationship between 12. Spight,T.M. 1976. Ecologyofhatchingsizeformarinesnails.
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