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Reprinted from'. Corul Reet's,ed. by Z. Dubinsky
O 1 9 9 0 E l s e v i e rS c i e n c eP u b l i s h e r sB . V , Amsterdam Printedin The Netherlands
Chapter7
REPRODUCTION, DISPERSAL AND RECRUITMENT OF
SCLERACTINIAN CORALS
P . L .H A R R I S O Na n dC . C .W A L L A C E
INTRODUCTION
Knowledge of coral reproductive biology and the
associatedprocessesof dispersaland recruitment is
an essential prerequisite for ecological studies of
coral populations and communities.Researchon
these topics, particularly on sexual reproduction,
has increasedgreatly during the last decade.These
studies have revealedan extraordinary diversity in
reproductive patterns among corals and have
transformed scientificunderstandingof their repro-
ductive biology. The traditional view that corals
typically brood their larvae and release well-
developed planulae intermittently throughout the
year has been disproved. It is now establishedthat
most corals spawn eggs and sperm for external
fertilization and development;reproduction is usu-
ally seasonal,with breeding occurring during brief
annual periods: many species participate in
predictable mass spawning events; and brooded
planulae of some speciesare produced asexually.
This chapter reviews current knowledge of the
processesof sexual reproduction in scleractinian
corals, aspectsof asexual reproduction, and larval
dispersal,settlement and recruitment. Emphasis is
given to recent papers which were not available for
previous reviews on these subjects (Atoda, 1953;
Connell, 1973;Highsmith, 1982;Fadlallah 1983a),
and to unpublished information contributed by
many colleagues.Topics requiring further research
are highlighted to provide a focus for future studies.
SEXUALREPRODUCTION
Historical perspective
Sexual reproduction in scleractinian corals has
been studied for about 200 years, but during most
o f t h i s p e r i o d l i t t l e w a s d i s c o v e r e d( F i g . 7 . 1 ) .
Cavolini (c. 1790. cited in De Lacaze-Duthiers.
1873) may have been the first to document
reproduction in corals when he observed the
planulae of Astroidesin the Mediterranean.Fol-
lowing this, research continued on brooding
species(De Lacaze-Duthiers, 1873, 1894, 1897;
V o n K o c h , 1 8 8 2 , 1 8 9 7 ;W i l s o n , 1 8 8 8 ;H a d d o n ,
1892;Duerden, 1902a,b, 1904),with early reports
of gamete spawning (Caryophyllia smithii: Thynne,
1859;Astrangia danae:Hargitt, l9l4) either over-
looked by subsequentworkers, or dismissedas
abnormal (Manicina areolata'.Wilson, 1888;Favia
fragum: Duerden, 1902a: see Table 7.4). Thus, by
the early 1900s, brooding had come to be the
"vivipar-
expectedmode of developmentin corals:
ity would appear to be the rule among corals"
(Duerden, 1902a)and "there is little doubt that all
corals are viviparous" (Duerden, 1905).
This misconception was reinforced by subse-
quent studies which continued to focus on brood-
ing species,mainly becausethe sampling methods
used were designed to detect planulation rather
than underlying cyclesof gametogenesisor spawn-
ing (Vaughan, 1908, 1910, 1911, 1912;Mavor,
l9l5; Matthai, 1923;' Edmondson, 1928, 1929,
1946; Boschma, 7929; Stephenson,l93l; Hada,
1932; Marshall, 1932; Marshall and Stephenson,
1 9 3 3 ;Y o n g e , 7 9 3 2 , 1 9 3 5 ;A b e , 1 9 3 7 , 1 9 3 9 ; M o -
toda, 1939; Kawaguti, 1940a,b, 1941a,b, 1942,
1 9 4 4 ; A t o d a ,1 9 4 7 ab, , l 9 5 l a c , 1 9 5 3 ) .A s a r e s u l t ,
the bias towards brooding species increased
(Fig.7.1) and the dogma of viviparity in coral
reproduction became firmly entrenched in the
literature(see,for instance,Marshall and Stephen-
son, 1933; Hyman, 1940; Vaughan and Wells,
1 9 4 3 ;W e l l s , 1 9 5 6 ,1 9 6 6 ) .
 P . L .H A R R I S O A
NN D C . C ,W A L L A C E

spawning and external development to be the

dominant pattern of sexualreproduction in scler-
actinian corals worldwide (Fig.7.l; see also,
among other references, Harriott, 1983a;Harrison
e t a l . . 1 9 8 3 , 1 9 8 4 ;K r u p p , 1 9 8 3 ; B a b c o c k , 1 9 8 4 ;
Wallace, 1985a; Heyward and Collins. 1985a;
S h l e s i n g ear n d L o y a , 1 9 8 5 ;S i m p s o n ,1 9 8 5 ;W i l l i s
e t a l . . 1 9 8 5 ;B a b c o c ke t a l . , 1 9 8 6 ;S z m a n t . 1 9 8 6 ) .
f s e n w r . :c A M E r E s Sexual reproduction has now been more widely
l----__lenooo PLANULAE studied in scleractiniancorals than in any other
cnidarian group. Much of this information has
been obtained during recent studies of the mass
coral-spawningphenomenonon the Great Barrier
Reef and other Indo-Pacificlocations (seep. 165).

Geographicalperspective

Sexual reproduction in corals has been studied

36 fi i n m a n y l o c a t i o n s( s e eF a d l a l l a h . 1 9 8 3 a ,t a b l e l )

i: I ull
but researchhas been concentratedin relatively
few geographicalregions.By 1986,detailed infor-
mation on reproduction in a wide range of corals
e l l l l I l ' o l l was available primarily from the Great Barrier
,.1 rI
1900 1925
ill iJlt
1950 1975 1980
Reef (156 species),northern WesternAustralia (28
species),the Caribbean (20 species),the Red Sea
F i g . 7 . 1 . N u m b e r o f c o r a l s p e c i e sw o r l d w i d e w h o s e m o d e o f ( 1 3 s p e c i e s )O
, k i n a w a ( l l s p e c i e s ) ,H a w a i i ( 1 0
development was recorded in different periods. from prior to species)and Palau (10 species).By contrast. many
1 9 0 0u n t i l 1 9 8 6 ,i l l u s t r a t i n gt h e h i s t o r i c a lb i a s t o w a r d s b r o o d i n g regions with abundant scleractinianfauna have
speciesand the recent exponential increasc in inlormatron on
received little or no study, the most notable
coral reproduction. Includes ten speciesin which both broad-
cast spawning and brooding modcs have been recorded (see omissions being the majority of Indo-Pacific
Tables7.2 and 7.4). oceanicislands,southeastAsian and African reefs,
and equatorial regions.The reproductivebiology
In many of thesestudies,however,the majority of corals from deep-sea environments is also
of species investigated did not produce any largely unknown. Researchon coral reproduction
planulae. Marshall and Stephenson(1933) found in theseareas is neededto obtain a better global
planulae in only 2 of 6 speciesat Low Isles(Great perspectiveof reproductive and life-history pat-
B a r r i e r R e e f ) , w h i l e A t o d a ( 1 9 4 7 a ,1 9 5 1 c ,1 9 5 3 ) terns in scleractiniancorals.
obtained planulae from only l0 of more than 100
species during an extensive four-year study at Patterns of sexual reproduction
Palau. Similar patternswere observedin studiesof
Hawaiian and Eniwetok corals (Harrigan, 1972; Four basic patterns of sexual reproduction are
S t i m s o n ,1 9 7 6 ,1 9 7 8 ) .T h i s l e d C o n n e l l( 1 9 7 3 )a n d discernibleamong scleractiniancorals (Table 7. l).
S t i m s o n( 1 9 7 8 )t o s u g g e s t h a t s o m ec o r a l s p e c i e s These consist of hermaphroditic or gonochoric
may spawn gametes for external lertilization. species(see p. 136) with broadcast spawning or
Subsequentstudiesof gametogenesis and breeding brooding modes of development (see p. 142).
in corals confirmed this for a number of species Hermaphroditicbroadcastspawnersare by far the
(Babcock, 1980;Kojis and Quinn, 1980, 1981. dominant group. with gonochoric broadcast
1 9 8 2 ab, ; S z m a n t - F r o e l i c h e t a l . . 1 9 8 0 ;F a d l a l l a h , spawners common. Hermaphroditic and gono-
l 9 8 l ; B o t h w e l l ,1 9 8 2 ;F a d l a l l a ha n d P e a r s e1, 9 8 2 b ; choric brooders appear to be uncommon because
Tranter et al., 1982),and then rapidly established comparativelyfew brooding specieshavc had their
CORALREPRODUCTIVE
BIOLOGY
1983a), and lrom the application of confusing
terminology (Policansky, 1982). Particular atten-
tion is therefore given to defining the following
patterns of sexualityin corals.
Hermaphroditic coral species have colonies or
solitary corals which typically produce both male
and female gametesduring their lifetime. Among
hermaphrodites,simultaneousand sequentialher-
maphroditism can be distinguished.Simultaneous
hermaphrodile.sdevelop mature ova and mature
sperm at the sametime within the sameindividual
(Policansky, 1982). Sequentialhermaphrodite.tde-
velop ova and sperm at different times,and within
this category a number of sexual patterns are
further distinguished. When male and female
gametes develop sequentiallyfor use within the
same breeding seasonthe term sequentialcosexual
should be applied (Policansky,1982).When indi-
viduals change sex over successivebreeding sea-
sons or over their lifetime they are consideredto
undergo true sex change(.lensaPolicansky, 1982).
Sequentialhermaphroditeswith true sex change
are either: alternating, changing sex more than
once:protandrous, maturing first as male then later
becomingfemale;or protogynous,maturing first as
female and later becoming male (Ghiselin, 1974).
Of the 151 hermaphroditic species listed in
Table7.2, l4l are known to produce both mature
eggsand sperm within the same coral at the same
time and are therefore simultaneoushermaphro-
dites. The remaining ten hermaphroditic species
(Table7.2) may also be simultaneoushermaphro-
dites,but becauseone or both sexeswere immature
in samplestaken throughout eachstudy their exact
status is uncertain. Aoopora (lsoporct) paliJeru,
Goniastreafavulus, St.,-lophcrapistillata, and pos-
sibly Faviafayr./sare adolescentprotandric herma-
phrodites, which develop initially as males but
mature as simultaneoushermaphroditesin subse-
quent breeding seasons (Rinkevich and Loya,
1 9 7 9 b ;K o j i s a n d Q u i n n . 1 9 8 1 , 1 9 8 5 ; H a r r i o t t ,
1 9 8 3 aB; a b c o c k .1 9 8 6 ;K o j i s , 1 9 8 6 a )H . ermaphro-
ditic corals typically develop both ova and sperm
within each polyp ("perfect" or "hermaphroditic"
i n b o t a n i c a l t e r m i n o l o g y : P o l i c a n s k y ,1 9 8 2 ) .I n
contrast,De Lacaze-Duthiers(1873)reported that
Astroidescalyculariscolonieswere hermaphroditic,
but individual polyps were typically only male or
female ("monoecious" in botanical terminology:
G h i s e l i n ,1 9 7 4 ) .D e L a c a z e - D u t h i e r (s1 8 7 3 ) a l s o
t37
implied that some polyps were occasionallyher-
maphroditic in this species.Male, female and
hermaphroditic polyps have also been observed
within hermaphroditic colonies of Porites astreo-
ides (seeChornesky and Peters,1987).
Sequential hermaphroditism has not yet been
demonstratedin scleractiniancorals, although it
has been recordedin some other cnidarian groups
[reviewedby Policansky(1982)and Fautin (1990)].
The early report of protandry in Flabellum rubrum
(see Gardiner, 1902a,b) appears to have been
based on incorrect interpretation of histological
preparations (Matthai, l9l4), so this speciesis
consideredto be gonochoric (Table 7.2).
Gonochoriccoral speciestypically produce only
male or female gametes within each colony or
solitary coral during their lifetime ("dioecious",
separatesexes).Proof of gonochoric sexuality is
complicated by the fact that sequentialhermaphro-
dites and sequentialcosexualsmay appear to be
gonochoric,becauseof the temporal separationin
the developmentof each sex. In sevengonochoric
species,individual male and female colonieshave
been repeatedlysampledover one or more consec-
utive gametogeniccycleswith no evidenceof sex
change: Porites cylindrica, P.lobata and P.lutea
(seeKojis and Quinn, 1982a);Porites australiensis
and P. lutea (see Harriott, 1983a); Turbinaria
mesenterinaand Pavona cactus (see Willis, 1987;
and unpublished data) and Montastrea cavernosa
(A. Szmant, pers. commun.). Repeated sampling
of individuals is impractical in specieswith small
colonies or in solitary corals. To compensatefor
this, some studieshave sampled large numbers of
corals. The observation that each coral typically
contains gametesof only one sex, and a lack of
correlation between sex and coral size, provide
strong evidencefor gonochorism in a further 20
s p e c i e s( S z n a n t - F r o e l i c he t a l . . 1 9 8 0 ;F i s k , l 9 8 l ;
F a d l a l l a h , 1 9 8 2 ; F a d l a l l a h a n d P e a r s e ,1 9 8 2 ab, ,
K r u p p . 1 9 8 3 ;W e l l i n g t o na n d G l y n n , 1 9 8 3 ;O l i v e r ,
1985.unpublisheddata; Szmant, 1986;Tomascik
and Sander, 1981; E. Chornesky, unpublished
data; R. Babcock and P. Harrison, unpublished
data). In other gonochoric coral species
(Table 7.2),both male and femaleindividualshave
been observedbut the recordsare basedon fewer
or infrequent samples.
Although most coralscan be readily classifiedas
either hermaphroditicor gonochoric,someexhibit
r38 P . L .H A R R I S O NA N D ( . C . W A L L A C E

TABLE 7.2
and modeof development
Summaryof informationon sexuality' corals(totalnumberof species
in scleractinian worldwide)" l
I

Sub-order
Fanily
S e x u a lp a t t e r n b Mode of devclopmcnt' I
Hermaphroditic l Mircdld Gonochoric Spawn gametes ( s+ B ) " Brood planulae

Astrocoeniina
Astrocoeniidae I
Pocilloporidae 6 (t) 4 (+ l)*'
Acroporidae 6l 56 (3) 5
Fungiina
Agariciidae (.2) 6 3 6
Siderastreidae 5 I I
Fungiidae l3 6 (l)
Micrabaciidae
Poritidae 5 0) t1 T2 (1) 9
Faviina
Faviidae 49 1' 15 (t) 1
Trachyphylliidae
Rhizangiidae I 2 2 I
Oculinidae (2) I (t) I
Meandrinidae I I
Merulinidae 5 5
Mussidae 8 6 2
Pectiniidae 8 8
Anthemiphylliidae

Caryophylliina
Caryophylliidac 0) 7 6 (l) 3
Flabellidae
Guyniidac
4 I
I
Dendrophylliina
Dendrophylliidac 2 ll 4 (l) ll (+2)*t

Speciestotal l5l (6) 72 157 (l0) s0

u A f t e r H a r r i s o n ( 1 9 8 5 ) .S p e c i e sl i s t s h a v e b e e n i n c r e a s e db y a d d i t i o n a l i n f o r m a t i o n o r r c d u c c db y s y n o n y m i e sa n d r e - e x a m i n a t i o no f
t h e l i t e r a t u r e .O r d e r sa n d l a m i l i e sa r e a r r a n g c ds y s t c m a t i c a l l ya s i n t h e r e r e r e n c e cs i t e d . H e r e , a n d i n o t h e r s u m m a r i c st h r o u g h o u t t h e
chapter where the literaturc is too cxtcnsivcto citc. thc inlormation sourcesare available from the authors. Specieslists are basedon the
c l a s s i f i c a t i o nosf W e l l s ( 1 9 5 6 .1 9 7 3 ) .V e r o n a n d P i c h o n( I 9 7 6 . 1 9 8 0 .1 9 8 2 ) V , cron ct al. ( 1977)V . e r o n a n d W a l l a c e( I 9 8 4 ) ,V e r o n ( I 9 87 ) .
A g a r i t i u s p e c i e sl i s t s b a s e do n t a x o n o m i c r e v i s i o n so f V a n M o o r s e l ( 1 9 8 3 )a n d E . C h o r n e s k y( p e r s .c o m m u n . ) ( T a b l e 7 . 3 . s e ep . 1 3 9 ) .
bAgaricia ttgtrricita.sl. danai. A. hmilis, Carvopht'llia ambrosia. Galaxea astredto, G.
/ascicularis and Porites usteiode.sincluded as
(mixed) (see p. l37ff; Table 7.3). Flubellunt ruhrunt, Helio.fungiaactiniforntis, and Montastrea Larernosdare included as gonochoric
s p e c i e sb e c a u s et h e r e p o r t s o f h e r m a p h r o d i t i s mi n t h e s es p e c i e s( A b e . 1 9 3 7 ;G a r d i n e r , 1 9 0 2 b ;S z m a n t - F r o e l i c he t a l . , 1 9 8 3 )a p p e a r
i n c o r r e c t( H a r r i s o n . 1 9 8 5 ;S z m a n t - F r o e l i c hp. e r s .c o m m u n . ) . l i n c l u d e s C l u t l o t o r uL a e s p i t o s (as e eT a b l e 7 . 3 ) .
'lncludes some inferred spawning records.
u ( M i x e d ) : h e r m a p h r o d i t i c a n d f c m a l c a n d i o r m a l e c o r a l sc o m m o n l : n o d a t a a v a i l a b l c .
" ( S + B ) : s p c c i c s f o r w h i c h b o t h s p a w n i n ga n d b r o o d i n g h a v e b e e n r e c o r d e d( T a b l e 7 . 4 ) .
'(*
) * = s p e c i e sk n o w n t o b r o o d a s e x u a l l yp r o d u c e d p l a n u l a e( s e ep . 1 8 1 ) .

more complex sexual patterns. Astangia denue,

Heteropsammiqcochlea,Porites cylindrit:a, P. por-
the hermaphrodites are rare, these species are
consideredto exhibit stable gonochorism (senst t
ites and Turbinaria mesenterinaare typically gono-
choric, but occasionally a few hermaphroditic
Giese and Pearse. 1914). A low incidence of
hermaphroditismhas also been observedin some
I
polyps or coloniesare encountered(Table 7.3). As other gonochoric cnidarians (see, for instance,
 BE
C O R A LR E P R O D U C T I V IOLOGY
J e n n i s o n .1 9 7 9 ;F a r r a n t , 1 9 8 5 ;F a u t i n , 1 9 9 0 )a n d
may result from polyfactorial sex determination
( s e eF a u t i n . 1 9 9 0 ) .
Mixed sexualpatternshave been observedin six
scleractinian species (Tables7.2, 7.3). Galareu
fast'iculurishas been widely regarded as herma-
p h r o d i t i c ( G u s h i k e n , l 9 8 l ; S h l e s i n g e ar n d L o y a ,
1 9 8 5 ;W i l l i s e t a l . . 1 9 8 5 ; B a b c o c k e t a l . , 1 9 8 6 ;
Y a m a z a t oa n d M i n e i , 1 9 8 6 ) ;h o w e v e r ,s u b s e q u e n t
research has demonstrated that G. f'asciculari.s
populations are composed of female colonies
which produce pinkish-red eggs. and colontes
which produce sperm and lipid-filled white eggs
( H a r r i s o n . 1 9 8 8 a ) .A s i m i l a r s e x u a l p a t t e r n r s
apparent among G. a:;treatu colonies (Harrison,
1988a).Self- and cross-fertilizationtrials of gam-
etesfrom G. /ast'iculariscolonies have shown that
"pseudo-eggs" from hermaphrodites
the white
cannotbe fertilizedor undergoembryogenesis, and
break apart a few hours after spawning(Harrison,
1988a). Therefore the hermaphroditic colontes
function as males, and the populations have a
gonochoristic breeding system. Gynodioecy has
beenobservedin Porites astreoide:;from Jamaica.
where colonies were either female or herma-
phroditic (Chornesky and Peters. 1987). In con-
trast, colonies of this speciesfrom Puerto Rico
were all simultaneous hermaphrodites (Szmant,
r986).
Populations of Agaric'ia agaricites, A. humilis
and Carl'oph1'lliaambrosia, contained large num-
bers of males, females and hermaphrodites
(Table7.3). These corals may exhibit labile gono-
chorism (sensuGiese and Pearse,1974).Alterna-
tively, these corals may be hermaphroditeswith
partially overlapping oogenic and spermatogenic
cycles, and the reports of males and females
resultedfrom samplestaken when only one sexwas
evident. Reports of variable sexuality within
Agaricia speciesmay also result from taxonomic
problems. Wells (1973) recognized five distinct
some of which have
forms of Agaricia ngarit'ite.s,
subsequentlybeen consideredas separatespecies
based on reproductive and other characteristics
(van Moorsel. 1983; E. Chornesky. pers. com-
mun.). Different specieswithin the A.agaritites
complex appear to have different sexual patterns
(Table 7.3);hencethe variablesexualityreportedin
some studies of Agaricia may result from taxo-
nomic differences.
139
Systematictrendsin sexuality.The availableinfor-
mation shows that patterns of sexuality are
generallyconsistentworldwide within eachsclerac-
t i n i a n f a m i l y ( T a b l e7 . 2 ; s e ea l s o H a r r i s o n , 1 9 8 5 ) .
Hermaphroditism predominates in the families
Acroporiidae, Faviidae, Merulinidae, Mussidae,
Pectiniidaeand Pocilloporidae,while the Agaricii-
dae, Caryophylliidae. Dendrophylliidae. Flabelli-
dae, Fungiidae and Siderastreidae contain mainly
gonochoric species(Fig. 7.2). The Poritidae con-
tain both gonochoric and some hermaphroditic
species(Table 7.2). To a lesserextent, trends in
sexuality are apparent within sub-orders;herma-
phroditism predominatesin the Astrocoeniinaand
Faviina, while most of the Caryophylliina, Den-
drophylliina and Fungiina studied to date are
g o n o c h o r i c( T a b l e7 . 2 ; s e e a l s o H a r r i s o n . 1 9 8 5 ) .
The consistencyof hermaphroditismor gonochor-
ism within high-leveltaxa indicatesthat sexualityis
a fundamentally conservative feature of sexual
reproduction in corals, and implies that it has a
phylogeneticbasis(Harrison, 1985).
Szmant (1986) suggestedthat hermaphroditism
was probably ancestralin Scleractiniabecauseof
the numerical dominance of hermaphroditic spe-
c i e s ( F a d l a l l a h , 1 9 8 3 a ,H a r r i s o n , 1 9 8 5 ) . S p e r m
morphology, however, indicates that gonochoric
coralsmay be more primitive (Harrison, 1988b;see
p. 161).The palaeontologicalrecord suggeststhat
scleractiniancorals are not a monophyletic group
(seeWells, 1956).Thereforehermaphroditismand
gonochorismmay have been ancestralin different
sub-orders,with contrastingsexualpatternsevolv-
ing in different directions within some coral
groups.
There are some exceptionsto the familial trends
in sexuality (Tables7 .2, 7.3). Contrasting sexual
patternsoccur within a few genera.and are present
to sonreextent betweengenerawithin six families
( T a b l e s7 . 2 . 7 . 3 ) . T h e s ee x c e p t i o n sa r e i n t e r e s t i n g
becausethey may provide important clues to the
way in which sexual patterns have evolved in
corals. A number of theorieshave been developed
to account for the evolution of hermaphroditism
versusgonochorismin differentorganisms(see,for
i n s t a n c eG , h i s e l i n ,1 9 6 9 , 1 9 1 4C: h a r n o v , 1 9 8 2 ;a n d
Leigh et al., l985). Critical evidence for these
theoriesis likely to come from studies of closely
related specieswith contrasting sexual patterns,
but significantvariation in sexuality often occurs
 P.L. HARRISONAND C.C. WALLACE

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CORAL REPRODUCTIVEBIOLOCY l4l

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t42
o n l y a t h i g h t a x o n o m i c l e v e l s( W i l l i a m s . 1 9 7 5 ) .
The contrasting sexual patterns recorded within
some scleractinianspeciesand genera (Table 7.3)
provide an excellentopportunity to assessthese
theories in a sessile marine invertebrate. Of
particular interest are the contrasting sexual pat-
terns reported in Astrangia. Montastreo and Por-
iles from different zoogeographic regions. The
Porites speciesstudied in the Pacific are gono-
choric, whereasmost of their Caribbeancongeners
are hermaphroditic (Table 7.3). The faunas have
been separated for l0 l5 million years (Wells,
1 9 5 6 ) ,s o t h a t t h e c o n t r a s t i n gt r e n d s i n s e x u a l i t y
may have resulted from evolutionary divergence
. z m a n t( 1 9 8 6 )
d u r i n g t h i s p e r i o d( H a r r i s o n ,1 9 8 5 ) S
suggestedthat selection for outcrossing between
long-lived individuals may have resulted in the
evolution of gonochoriccoral species,and that the
observedreproductivedifferencesbetweenPacific
and Caribbean corals may have resulted from
differences in evolutionary selective pressures
between the two regions. Further comparative
studiesof taxa with variable sexualitywould help
to establishwhich sexual pattern is ancestral in
Scleractinia.and provide some insight into why
certain species have evolved contrasting sexual
patterns.
Mode of development
Two distinctmodesof developmentoccur among
scleractinian corals: gamete release followed by
externalfertilizationand development,and brood-
ing of planula larvae within the polyp. A total of
157 scleractinianspecies are known to spawn
gametesfor external development, and 50 species
have been observed to brood planulae, including
three species in which the planulae originate
asexually(Table 7.2, seep. 181).External fertiliza-
tion and developmentis clearlythe dominant mode
of developmentamong scleractiniancorals.
"spawning" has been used by some
The term
workers to describeboth the releaseof gametes
and planula release.To avoid confusion between
these two different reproductiveactivities,in this
"spawning" is restrictedto the
chapter the term
releaseof gametesfrom the polyp. Corals which
releasegametesinto the sea for external fertiliza-
tion and development are termed broadcast
spawners,while corals which brood developing
larvae within their polyps are termed brooders.
P . L .H A R R I S O A
NN D C . C .W A L L A C E
At present there are no obvious systematic
trendsin the mode of developmentof scleractinian
c o r a l s ( H a r r i s o n . 1 9 8 5 ) .F a d l a l l a h ( 1 9 8 3 a )t e n t a -
tively concludedthat the mode of developmentwas
relatedto the family, but both broadcast-spawning
and brooding modes of development have now
been recorded in most families (Table 7.2), many
genera.and within l3 species(Table 7.4). In some
cases the reports of brooding and broadcasting
within the samespeciesare probably incorrect,and
result from taxonomic problems,abnormal condi-
tions or errors of interpretation (Table 7.4). ln
some speciescontrasting modes of development
have been reported in populations from distant
locations(Table 7.4),which suggeststhat contrast-
ing developmentalpatterns have evolved in differ-
ent geographicalraces,or that these corals have
been incorrectly identified or synonymized.Com-
parative studies of reproduction and taxonomic
and geneticrelatednessin thesecorals are needed
to determinewhether developmentalpatterns are
species-specific or variable in certain speciesof
corals. Further studies at Palau and Eniwetok
would be particularly useful,as many of the species
reportedto brood planulaeat theselocationshave
subsequentlybeen observedto spawn gametesfor
externaldevelopmentin other regions(Table 7.4).
Future studieson coral reproduction will prob-
ably increasethe list of specieswith both broad-
cast-spawningand brooding modes of develop-
ment. For example,specieswhich brood asexually
derived planulae may also spawn gametes for
externaldevelopmentat some stage.The distribu-
tion of brooding specieswithin familiesand genera
in which spawning predominates indicates that
brooding has evolvedindependentlyin many coral
taxa. The mode of developmentin corals therefore
appearsto be a relativelyplastic life-history trait,
compared with sexuality and other reproductive
characteristics(Harrison, I 985).
Broadcast spawning versus brooding. Several hy-
potheseshave been proposed which attempt to
relate the mode of developmentto the life history,
morphology or habitat of corals.Subsequentwork
has tendedto refute rather than substantiatemany
of these hypotheses.Loya (1976a) applied the
concept of r and K strategies, developed by
MacArthur and Wilson (1967), to reproductive
and other life-history traits of corals, but the
I
 BIOLOGY
CORALREPRODUCTIVE
brooding of planulae by relatively r-selectedspe-
ciesis the oppositecharacteristicto that predicted
for typical r-strategists (Rinkevich and Loya,
1919b).Rosen (1981) suggestedthat stresstoler-
ance be considered as an additional ecological
dimension.but noted the difficulty in defining and
measuringstress.
Rinkevich and Loya (1979a) suggestedthat
branching or small-polyped coral species with
gonads developing in their coelenteron produce
small eggs and brood planulae, while massiveor
large-polypedspeciesproduce many eggs which
are spawned for external fertilization. Fadlallah
and Pearse (1982a) proposed that large skeletal
spaces may allow brooding of embryos to an
advancedstage,and that the skeletalarrangement
of corals may be predictive of the mode of
development. The discovery of brooding and
broadcast-spawningmodes of development in
closely related congenerswith similar calical or
colony structure (for instance,speciesof Poc'illo-
pora and Porites)has invalidatedthesegeneraliza-
tions (Fadlallah, 1985),and at presentthere seems
to be no universalrelationshipbetweenpolyp size,
egg size and mode of development in corals
( S z m a n t - F r o e l i ceht a l . , 1 9 8 0 ) .
Stimson (1978) proposed that the mode of
developmentmay be related to habitat, and that
shallow-wateror reef-flatcorals should planulate
to facilitate localized recruitment, whereasdeep-
water speciesshould spawn gametesfor external
developmentto assist dispersal.Although many
brooding speciesoccur in shallow water, many of
these speciesalso planulate throughout an ex-
tendeddepth range, and brooding is by no means
confined to species restricted to shallow-water
habitats (for instance, Balanophyllia elegans:Ger-
rodette, 1981;Fadlallah and Pearse,1982a;Agari-
cia spp.: Van Moorsel, 1983; Acropora (Isopora)
paldbra: Kojis and Quinn, 1984; Kojis, 1986b).
Moreover, most of the shallow-watercorals stud-
ied to date are broadcast-spawningspecieswhose
embryosand larvaeare likely to be dispersedaway
from the parentalhabitat during development(see
p. 186).Thus, the mode of developmentin corals
does not appear to be related to habitat depth.
Van Moorsel (1983) suggestedthat the repro-
ductivetraits ofbrooding coralscould be relatedto
the predictability of their habitat rather than to
depth. Speciesfrom unpredictablehabitats would
143
tend to be smaller and shorter-lived. mature
earlier, and produce many small offspring over a
longer breedingperiod. Relatedspeciesfrom more
predictableenvironmentswould have the opposite
reproductive characteristics.Szmant ( 1986) ex-
tended these ideas, and proposed that brooding
evolved in coral speciesoccupying unstable habi-
tats and subject to high rates of adult mortality
through selectionfor high rates of recruitment.
Szmant (1986) observeda correlation between
mode of development and colony size among
Caribbeancorals. All the brooding speciesknown
in the Caribbean are commonly found as small
colonies,whereasbroadcastspawnersusuallyform
very largecolonies.Brooding is likewiseassociated
with small adult size in many other manne
invertebrates(Strathmann and Strathmann, 1982;
S t r a t h m a n ne t a l . , 1 9 8 4 ) ,a n d a s i m i l a r p a t t e r n i s
apparentamong brooding and spawningspeciesof
Porites in the Pacific (Marshall and Stephenson,
1 9 3 3 ;K o j i s a n d Q u i n n , 1 9 8 2 a )H
. o w e v e r ,t h e r ea r e
exceptionsto this relationshipbecausesome Indo-
Pacific brooding species form relatively large
colonies (for instance,Acropora (Isoporct)pali/bra'.
Kojis, 1986a).
At present,the rangeof reproductivepatternsin
scleractiniancorals defies any simple predictive
model. Further comparative studies of closely
related corals with contrastingmodes of develop-
ment are needed to explain why brooding has
evolved in certain corals, and to test the general
validity of the hypotheseswhich have been pro-
posed to date.
Resourceallocation to sexual reproduction
Interaction of life functions
Corals have a limited set of resourcessuch as
energy and interstitial cells, which have to be
sharedamongsta variety of life functionsincluding
sexualand asexualrcproduction, growth, mainte-
nance and repair. Although these functions are
interrelated by their dependenceon a common
resource pool, their interaction remains poorly
understood.This is primarily due to the practical
difficulties of identifying which, when and how
much of these resourcesare allocated to each
function.
The interaction of reproduction and growth is
particularly important, because these functions
 P.L. HARRISON AND C.C. WALLACE

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CORAL REPRODUCTIVEBIOLOGY
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146
potentially compete for resourcesremaining after
the requirementsfor maintenanceand repair have
been fulfilleC.Growth rates in many coral species
decreasewith increasing size, and it has been
proposedthat this may be causedby the onset of
sexual reproduction and increasing fecundity as
c o r a l s g r o w [ p . 1 4 9 ; s e e a l s o L o y a ( 1 9 7 6 a )a n d
K o j i s a n d Q u i n n ( 1 9 8 1 ) 1I .n c o n t r a s t ,g r o w t h r a t e s
of female colonies of Porites astreoidesincreased
over the size range associatedwith the onset of
reproduction (Chornesky and Peters, 1987).Wel-
l i n g t o n a n d G l y n n ( 1 9 8 3 )o b s e r v e da c o r r e l a t i o n
betweenthe seasonalcyclic accretionofthe skeletal
high-density band in Pavona gigantea and the
period of gamete production, and suggestedthat
growth and possiblycalcificationare reducedwhen
energy is allocated to reproduction. Buddemerer
a n d K i n z i e ( 1 9 7 6 ) s u g g e s t e dt h a t t h e m o n t h l y
density variations in Porites lobata skeletonsmay
be related to reproductive cycles, while Krempf
(1935)consideredthat the rhythmic successionof
skeletal dissepimentformation in Favia sp. was
correlated with sexual cycles. Localized growth
may also be responsible for zones of reduced
f e c u n d i t ya n d s t e r i l i t yi n s o m e c o r a l s( s e ep . 1 5 2 ) .
S z m a n t - F r o e l i c(h1 9 8 5 )p r o p o s e dt h a t g a m e t o g e n -
esisand budding processesin corals may interact
through competition for interstitial cells, as has
been demonstratedtn Hydra (seeTardent. 1975).
Clearly, the relationship between gametogenesis,
somatic tissue growth, and calcificationin corals
needsmore detailedstudy.
Gonad and planula developmentmay compete
with coral feeding requirementsfor space within
the polyp coelenteron. In some small-polyped
corals such as C.t'phastreooc'ellinuand Stylophora
pistillutu the gonads or planulae may grow to
occupy all the available space within the polyp
( R i n k e v i c ha n d L o y a , 1 9 7 9 aW ; right. 1986)h ; ence
it is likely that little or no feeding occurs when
these polyps are fully gravid. A similar situation
has been observed in the soft coral Alcyoniunt
digitatunr,where the developing gonads occlude
the gastric cavity fbr four months, during which
time the polyps remain contractedand do not feed
( H a r t n o l l , 1 9 7 7 ) .C o n s t r a i n t si m p o s e do n l e e d i n g
by gonadal growth may be compensatedfor by
photosynthetically derived nutrition. Small-po-
lyped corals may rely more upon photosyntheti-
cally derived nutrition than on zooplankton cap-
P . L .H A R R I S O A
NN D C . C .W A L L A C E
ture, compared with larger-polypedspecies(Por-
t e r . l 9 l 6 ; H u g h e s ,1 9 8 3 ) .C o r a l sw i t h l a r g ep o l y p s
generally have proportionally less coelenteronrc
space occupied by gonads. but it is not known
whether feeding requirements or energetic con-
straints ultimately limit the sizeof gonads in these
specles.
Sex allocation
Within each species, resources allocated to
sexualreproductionmust themselvesbe divided in
a number of ways. Firstly, a division must be made
betweenmale and female function. Sex allocation
may take the form of the sex ratio of offspring in
gonochoric species,the ratio of male to female
function in simultaneoushermaphrodites.or the
timing of sexreversalin sequentialhermaphrodites
( S t e a r n s .1 9 8 5 ) .
Sex ratios have been studied in detail for
populations of 17 gonochoric coral species(Ta-
ble 7.5). In nine speciesthe observedsex ratio was
approximately 1:1, which is the predicted optimal
resourceallocation in a population with random
mating (Williams. 1975; Maynard-Smith, 1978;
L e i g h e t a l . , 1 9 8 5 ) .I n t h e r e m a i n i n ge i g h t s p e c i e s ,
the sex ratio in some populations deviated from
unity (Table 7.5). In Siderastrearadians,the large
female bias may have evolved becauseonly the
female colonies brood, and brooding space ls
limited within eachfemalepolyp (Szmant, 1986).If
this female bias is verified in larger samples of
other populations,S. radianswould be an interest-
ing coral in the consideration of sex-allocation
theory, particularly sinceits congenerS. sidereais
a broadcasterwith an equal sex ratio (Szmant,
1986).Balctnophylliaelegunsand Porites porites are
the only other gonochoric brooders whose sex
ratio has been well documented. but in these
s p e c i e st h e s e x r a t i o i s 1 : l ( F a d l a l l a ha n d P e a r s e ,
1982aT ; o m a s c i ka n d S a n d e r ,1 9 8 7 ) .
The skewedsex ratio observedin populations of
somespeciesmay have resultedfrom samplingbias
or environmentalinfluences.Ghiselin (1974)noted
that the apparentsex ratio of a population may be
biasedby samplingprocedureand samplesize.Sex
ratios derived from pooled data can be biased
where gametesof one sex are presentover a longer
period - as in Heterocvalhusaequico.stalu.r', where
the sex ratio was skewedby the absenceof females
in samplestaken after the rnain spawning season
CORAL REPRODUCTIVEBIOLOGY 147

T A B L E7 . 5
Scxratiosin populations
of l7 gonochoric
coralspecies

Sex ratio Sample sizc Sample Location (reference)

male:female type"

Siderastreidae
rutliuns
Siclera.strcu 0.1:l 25 a Pucrto Rico (Szmant, 19116)
S. :idercu I :I 40 x 2 pops. a Puerto Rico (Szmant, 1986)

Fungiidac
F u n g i t tL o n t i n n u 2.5:l 45 b Lizard Is., GBRb (Oliver. 1985)
0 . 9 :I 65 b Orpheusls., GBR
5.5:l 13 b M a g n e t i cI s . , G B R
1.5:l 123 b Total
F. lingite.; 5:l 18 b L i z . a r dI s . . G B R ( O l i v e r . 1 9 8 5 )
(2:0) 2 b OrpheusIs., GBR
2.5:l 46 b M a g n e t i cI s . . G B R
3:l 66 b Total

Poritidae
P o r i t e su u s t r u l i L ' n s i s 0.6:l 13 b Lrzard Is.. GBR (Harriott, 1983a)
P. tt'lirulricu 2:l 17 a Heron ls., GBR (Kojis and Quinn, 1982a)
P. lohuru 0.08:1 43 a Heron Is., GBR (Kojis and Quinn, 1982a)
P. luteu 0.07:1 44 a Heron Is.. GBR (Kojis and Quinn, 1982a)
1.7:l 19 b L i z . a r dI s . , G B R ( H a r r i o t t . 1 9 8 3 a )
P. porite.s 2:1 137 b S G r e e f " , B a r b a d o s( T o m a s c i k a n d S a n d e r .1 9 8 7 )
l:l ll9 b BRI reef',Barbados
l:l I l0 b GS reef", Barbados

Faviidae
Muttustreo (arernosa l:l 40x2 pops. a Puerto Rico (Szmant,1986)

Rhizangiidae
Astrutgiu danue l:l 150 b R h o d e I s . , U . S . A . ( S z m a n t - F r o e l i c he t a l . . 1 9 8 0 )

Meandrinidac
Denth'ogvrut.t'lindritus 1:l 40 x 2 pops. a Puerto Rico (Szmant, 1986)

Caryophylliidae
H e t e r o c y u r h uu
sequitostutLr.s l:lu W i s t a r i R e e f .G B R ( F i s k . 1 9 8 .
1 . 5I: 32 b
Purut.vuthus.steurnsii l:l >46 a C a l i f o r n i a . U . S . A . ( F a d l a l l a h a n d P e a r s c ,1 9 8 2 b )

D e n dr o p hy l l i i dae
B u l t u t o p h . t l l i eu l e g a n . s l:l 286 b C a l i f o r n i a , U . S . A . ( F a d l a l l a h a n d P c a r s e .1 9 8 2 a )
H c t e r o p s u n u t i ut o t h l e u l:l T9 b Wistari Rccf. GBR (Fisk, l98l)
T u r b i n u r i un p s c n t e r i n o l:l lll b MagneticIs., GBR (Willis. 1987)

ua: data fiom single randon.rsan.rple.b: pooled data fiorn

all sarnples.
bGBR: Grcat Barrier Reef.
" S G : S p r i n g G a r d e n s r c c l . B R I : B e l l a i r sR e s e a r c hI n s t i t u t e r e e f .
G S : G r e e n s l e e v erse e f .
d S c xr a t i o d u r i n g b r e e d i n gs e a s o n( s e ep . 1 4 6 ) .

( F i s k , 1 9 8 1 )T
. e s t so f s e xr a t i o sm a y a l s o b e b i a s e d r i o t t , 1 9 8 3 aT
; o m a s c i ka n d S a n d e r ,1 9 8 7 ) .F o r t h e
by clone formation. It has been suggestedthat the fragmentation hypothesis to be accepted, the
apparent dominance of one or other sex in some clonal nature of these populations should be
populationsof Porite.sspecieson the Great Barrier examinedelectrophoretically(seep. 183, and also
R e e f a n d i n t h e C a r i b b e a n( T a b l e7 . 5 ) m a y h a v e Willis and Ayre. 1985).
resulted from sampling dispersedclones of frag- Sexratios could also be skewedif the sexof each
mented colonies (Kojis and Quinn. 1982a; Har- coral was environmentally determined; but sex
148
determinationhas not beeninvestigatedin sclerac-
tinians (Fadlallah, 1983a).Among other cnidar-
ians there is some evidencefor both genetically
controlled and environmentally influenced sex
determination[seereviewsby Tardent (1975) and
Fautin (in press)1.Solitary fungiid corals would be
a convenientgroup in which to study sex determi-
nation in scleractinians.If sex determination ls
geneticallycontrolled, all clones budded from an
anthocaulus(Wells, 1966) should be of the same
sex. If sex is labile, the effectsof the environment
could be tested and related to sex-allocation
theories, such as those which predict a shift to
malenessin responseto stressor decliningenviron-
m e n t a lq u a l i t y ( B u l l . 1 9 8 5 ;S o l o m o n ,1 9 8 5 ) .I n t e r -
estingly, an excess of male colonies of Porites
porites was observed on a polluted reef at
Barbados, whereas populations from nearby less
polluted reefs had equal sex ratios (Table 7.5; see
a l s o T o m a s c i ka n d S a n d e r ,1 9 8 7 ) .
Allocation to male versus female function in
hermaphroditic corals has largely been ignored.
This is despitethe fact that hermaphroditesoffer
greater scopefor analysingtheoriesof sex-alloca-
tion strategies,becausemore factors affect the sex
ratios of hermaphroditesthan those of gonochoric
species(Lloyd. 1985).ff gonad volume is a useful
indicator ofthe resourceallocationto each sex,the
similar volume of ovaries and testesobservedin
some hermaphroditiccorals (for instance,Gonius-
trea aspera'.Babcock, 1984) would indicate that
male and femalefunctions were equally expensive,
as predicted for outcrossedsimultaneousherma-
phrodites (Williams, 1915). In contrast, testes
volume is considerablylarger than that of ovartes
in the brooding species Pocillopora damitornis
(Harriott, 1983b; Stoddart and Black, 1985),
Stylophora pistillata (see Rinkevich and Loya,
1979a),Porites astreiodes,Favia fragum, Myceto-
phyllia ferox (seeSzmant, 1986);and in the non-
brooding corals Lobophyllia spp. (Marshall and
Stephenson,1933)and Astreoporamyriophthalma
(Harrison and Wallace,unpublisheddata). Szmant
(1986) interpreted the large sperm production in
hermaphroditic corals as a means to increase
outcrossing. Such comparisons of sex allocation
based on relative gonad volume assumethat the
resourceinvestmentand relativemetaboliccostsof
spermatogenesis and oogenesisare equal per unit
gonad volume. Until this assumptionis tested,the
P.L.HARRISON AND C.C. WALLACE
allocation to each sex would be better approxl-
mated by measuring the calorific value of sperm
versuseggs, a technique which has recently been
applied to spawned coral gametes (B. Willis,
unpublisheddata). The possibility that the alloca-
tion to each sex may change over the lifetime ol
corals should also be consideredwhen comparing
sex allocations,particularly in adolescentprotan-
dric species.
Reproductiveeffort and fecundity
Resourcesallocated to reproduction must also
be divided among the progeny.The allocationmay
be to a few large or many smaller offspring. and
occur once in a lifetime (semelparity) or over
successive reproductive events (iteroparity)
(Stearns, 1976). Although a discussion of life-
history patterns in corals is beyond the scope of
this chapter,a considerableamount of information
is accumulatingon thesekey life-history traits.
All corals studied to date are iteroparous, and
there is no evidence for Gardiner's (1902b) hy-
pothesisthat corals spawn once and then die (see
also Matthai. l9l9; Marshall and Stephenson,
1933).For example,annual cyclesof gametogene-
sis and spawning have been observedin the same
coloniesof Acropora spp. for six years (Harrison,
unpubl. data). Consequently,corals must partition
their reproductiveeffort over successivebreeding
events throughout their lifetime. Unfortunately,
reproductive effort is difficult to measure.Ratios of
gonad volume or calorific value to somatic tissue
provide an approximation of reproductive effort
(Pianka, 1978),but at present data are available
for only one coral species.Coloniesol Pocillopora
damic'ornisin Hawaii releaseda minimum of 25oh
to 50oh of their total colony biomass as planulae
annually, and one colony released4o/oof its tissue
weight as planulaeduring a 48-hour period (Jokiel,
1985).At Eniwetok, P. damicorniscolonies annu-
ally releasedplanulaewith a total calorific content
equivalentto 50o/oto 180% of the parent colony
tissues(Richmond, 1983).
In the absenceof direct quantitative measure-
ments in other coral species,fecundity has been
used as an estimate of reproductive effort. Fecun-
dity, usually expressedas the number of eggs or
planulaeproduced per polyp, can provide a useful
index of reproductive effort within most coral
specieswhere the size of eggsor planulae and the
CORALREPRODUCTIVE
BIOLOGY
number of reproductive cycles each year are
reasonably consistent. However, fecundity
measurements underestimate reproductive effort
by not accounting for the allocation to sperm
production, and are also inadequate indices of
reproductive effort in species where the size or
energeticvalue of offspring, or the number of
reproductivecycles,varies.For example,Acropora
(Isopora) palifera near Lae (Papua New Guinea)
has a mean annual colony fecundity4.5 times that
of the population at Heron Island (Great Barrter
Reef), due to more frequent reproductive cyclesat
Lae [see data from Kojis (1986b) in Table7.7].
However, the volume of the individual larva at
Heron Island is 2.5 times that near Lae, hencethe
annual reproductive effort of A. palifera near Lae
is essentiallyonly twice that of the Heron Island
population (Table 7.7), and is inadequately
measuredby fecundity alone.
Temporal variation in fecundity. Fecundity varies
over the lifetime of a coral, which includes pre-
reproductive,adolescent,mature and sometimes
senescentstages.Juvenilecorals have a period of
development and growth before becoming repro-
ductive. Delay in the onset of reproduction is
common to most organisms, and is thought to
promote greaterreproductivesuccess by increasing
the availability ofresources through larger size(see
Szmant-Froelich,1985). Reproductive delay has
also been interpreted as an initial allocation to
growth to escapethe greater mortality associated
with smaller size classes(Kojis and Quinn, l98l;
Szmant,1986).The minimum sizeat reproduction
has beenreported for 35 coral species,and in most
casesgrowth data have been applied to estimate
the age at first reproduction (Table 7.6). Brooding
speciestend to become reproductive much earlier
(l 2 yearsof age)than gamete-spawning species(4
yearsor older). The differencemay be even greater
than indicated in Table 7.6, becausegrowth rates
of non-broodedjuveniles are considerablyslower
than brooded speciesin their first year of life (see
p. 19l, and also Babcock, 1985),and hence some
estimatesof age may be incorrect. Azooxanthellate
and temperate ahermatypic (for definitions see
Schuhmacher and Zibrowius, 1985) broadcast
spawning corals are apparently more precocious
than zooxanthellate and hermatypic broadcasters
(Table 7.6).
t49
Size at first reproduction is quite variable
betweencoral species(Table 7.6), partly becauseof
differencesin growth rates and morphology. Onset
of reproduction is also highly variable within some
populations. Thus, whereas some comparatively
small colonies of Acropord spp., Goniastreaaspera,
G. favulus, Platygyra sinensis, Stylophora pistillata
and Turbinqria mesenterina may be gravid, the
majority of colonies are reproductive only in much
larger size classes (Rinkevich and Loya, 1979b;
Kojis and Quinn, l98l; Babcock, 1984, 1986;
Wallace, 1985a; Kojis, 1986a; Willis, 1987).
Whether this is a result of variability in growth
rates within a cohort, or variability in age at first
reproduction within a cohort, is not yet known.
Long-term studies of growth and maturation in
juvenile corals reared from settlement could re-
solve this problem. Specieswith fast growth and
early maturation (Table 7.6) would be most suit-
able for these studies.
Connell (1973) noted the delay in the onset of
reproduction in corals, and asked whether colony
size or polyp age determined when energy was
diverted into gamete production. He suggested
"alternative hypotheses" be tested by
that these
dividing mature colonies into fragments which
would subsequently be monitored for several
years.Thesemethods have been used in two recent
studieson the faviid corals, Goniastreafavulus and
Montastrea annularis. In experimentally manipu-
lated colonies of G.favalas, sexual maturity and
fecundity were found to be a function of the
interaction betweencolony size and polyp age, not
simply a function of either one (Kojis and Quinn,
1985).Colony sizedetermined whether gametogen-
esis occurred, but colony age influenced both size
at first reproduction and polyp fecundity. Thus,
the minimum breeding size was larger for undi-
vided young colonies of G. favulus than for
fragmented older ones, and if two colonies were of
the same size but different ages, the older colony
was more fecund (Kojis and Quinn, 1985). In a
similar study, Szmant-Froelich(1985) found that
colony size affected the ability of Montastrea
annularis colonies to reproduce. Kojis and Quinn
(1985) suggestedthat this integrated colony re-
sponse, where resourcesare reallocated to repair,
regrowth and maintenanceafter severefragmenta-
tion, may enhance the survival of long-lived
massive species.They suggestedthat similar frag-
I
 \
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150 P.L. HARRISON AND C.C. WALLACE
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 t52
mentation experimentsshould be done on a short-
l i v e d s p e c i e sf o r c o m p a r i s o n .
These experimentalstudies show that in some
coralsthereis a minimum colony size,regardlessof
the physiologicalage of the coral, which must be
attained before gametogenesiswill occur (Kojis
and Quinn, 1985). However, this generalization
may not apply to species where polyps are
physiologicallyisolatedwithin colonies(Kojis and
Quinn. 1985),as in Lohophvllia hemprit'hii.where
polyp size rather than colony size apparently
c o n t r o l sg a m e t o g e n e s(i Hs arriott, 1983a).
Having attained reproductive status. fecundity
of a coral normally increaseswith age as a result of
an increasein the number of polyps, an increasein
polyp fecundity,or both. Polyp fecundity may rise
through an increasein the number of egg-bearing
mesenteries (Enallopsammia x'illefi: Gardiner,
1900),or an increasein the number of eggs per
mesentery (Goniastreaaspera, G../avulus,Platv-
gyra sinensis:Kojis and Quinn, 1981; Babcock,
1984. 1986).In thesethree faviids, the number of
eggsper mesenteryinitially increasedsigmoidally
during an extended period of adolescence.but
reacheda stable asymptote after l0 to 15 years
(Babcock,1986).Sizeinfluencedpolyp fecundityin
Acropora valida, Caryophvllia smithii and Favia
fragum, where small corals produced fewer eggsor
planulae per polyp than larger members of the
p o p u l a t i o n( T r a n t e r e t a l . , 1 9 8 2 ;W a l l a c e , 1 9 8 5 a ;
P. Scott,pers.commun.). In contrast,polyp fecun-
dity in female colonies of Porites astreoides was
correlatedwith colony age (thickness)but not with
colony size(Chorneskyand Peters,1987).
As corals continue to grow and reproduce
throughout their lifetime, fecundity should be
maximized in older members of the population
unlesspartial colony mortality reducesthe size of
older corals (Hughesand Jackson.1985;Babcock,
1986),or senescence occurs.Although corals have
traditionally been regarded as essentially non-
ageing, intrinsic tissue senescence may result in
reducedfecundity and be an important cause of
natural mortality among older corals (Rinkevich
and Loya, 1986).A marked decreasein fecundity,
in terms of oocyte production, was observed in
large coloniesof Stylophorapistillata up to l0 to l2
months before tissue degeneration and death
occurred (Rinkevich and Loya, 1986). Gardiner
(1902b) found evidenceof senescence in Flabellum
II
l.
NN D ( - . C W
P . L .H A R R I S O A . ALLACE
rubrum, where intermediate-sized polyps produced
new oocytesto replacethosewhich matured,while
the largest polyps contained only a few isolated
large oocytes, and no new developing oocytes.
Reproductivesenescence has also beenobservedin
populations of Fuvia fragunt and Poc'illopora
domic'orni.s, where the largest colonies released
significantlyfewer planulae per polyp than colo-
n i e s i n i n t e r m e d i a t es i z e c l a s s e s( H o l l o r a n . 1 9 8 6 ;
P. Scott, pers. commun.). Further work is needed
on polyp fecundity in large size classesin other
speciesto determine whether reproductive senes-
cence is a general leature of scleractinian life
histories. Senescence could have particularly im-
portant consequences for demographicinterpreta-
tions of populationsin corals such as Porites spp.
on the Great Barrier Reef.which can be dominated
by a few massive colonies that are assumed to
contribute most of the gamete pool (Potts et al.,
I 985).
Fecundity has also been observedto vary over
shorter time-scales.Seasonal variation in polyp
fecundity has been observed in some brooding
specieswith extended breeding seasons(for rn-
stance, Acropora (lsopora) palil'era'. Kojis and
Quinn, 1984; Porites a:;treoicles'. Chornesky and
Peters, 1987).Significantinterannual variation tn
polyp lecundity occurred in Ac'roporalongir'.1'uthus
colonies re-sampled over three years (Wallace,
I 985a).
Spatial variation in fecundity. Fecundity has been
observed to vary spatially within reproductively
m a t u r e c o l o n i e s ,a m o n g c o l o n i e so f a p o p u l a t i o n ,
and betweenpopulations of some coral species.In
specieswith localizedregionsof growth, polyps in
closeproximity to actively growing branch tips or
plate edgesare reproductively sterile: Stylophora
pistillata (see Rinkevich and Loya, 1979b),many
Acropora species(Oliver, 1984; Wallace, 1985a;
Kojis, 1986a;Harrison, unpubl. data), Montipora
digitata (see Heyward and Collins, 1985a) and
Turbinaria mesenterina(seeWillis, 1987). Behind
"post-sterile" zone
the sterilezone, polyps in the
may have reducedfecundity (Acropora spp.: Wal-
lace, 1985a; T.mesenterina:Willis, 1987) or pro-
duce only testes(A. Heyward, unpublisheddata).
Turbinaria mesenterinapolyps nearest the growing
plate edge are sterileor have lowered fecundity in
their first year of growth, higher but sub-mature
C O R A LR E P R O D U C T I V
BEIOLOGY
levelsof fecundityafter two to three years'growth.
and are only fully fecund in their secondspawning
season(regionscorrespondingto 3 years or older)
(Willis. 1987).In Acropora spp. the length of the
sterile and post-sterilezones varies from |.5 to
8 cm, depending on growth rates and colony
m o r p h o l o g y ( W a l l a c e , 1 9 8 5 a ) .B e y o n d t h e s e r e -
gions the number of oocytesper polyp is relatively
constantwithin eachcolony, includingaxial polyps
which are not actively extending (Oliver, 1984;
W a l l a c e .1 9 8 5 a ) S . t e r i l ez o n e sp r o b a b l y r e p r e s e n t
polyps which formed too late during the gameto-
genic cycle to be gravid. while polyps in the post-
sterilezone may have beenincompletelyformed at
the onset of gametogenesis (Wallace. 1985a;Hey-
ward and Collins. 1985a).Polyp fecundity varied
widely within and between branchesof Acropora
(Isopora)poli/bru and Pocillopora damicorniscolo-
n i e s( H a r r i g a n . l 9 l 2 : K o j i s , 1 9 8 6 a ) a
, nd between
central and peripheraltissuesof Porites astreoides
colonies (Chornesky and Peters, 1987). These
sterilezonesand regionsof loweredfecunditymust
be considered when samples are collected for
studies of gametogenesis.or when total colony
fecundityis estimated.
In contrast to specieswith localized regions of
growth, massivecorals such as Goniastreaf ovulus
normally have similar gonad abundance in all
polyps, including those at the edge of colonies
(Kojis and Quinn, 1981). Montastrea annularis
polyps are similarly all gravid except for small
newly budded polyps, which are sterile (Szmant-
Froelich. 1985).The presenceof sterile polyps in
M. unnulari,smay be related to its extratentacular
mode of budding. whereasnewly budded polyps in
G..favuluscolonies may remain reproductive be-
causethey are formed by division of existinggravid
polyps during intratentacularbudding. The lack of
specificsterile or low-fecundity regions in these
massivespeciesprobably resultsfrom the absence
of an edgezone and more uniform growth over the
colony surface.Energy in all polyps may therefore
be directed to both gametogenesisand growth
(Kojis and Quinn. 1981).
Little information is available on variation in
polyp fecundity among reproductively mature
corals within populations. Wallace (1985a) ob-
served significant variation in polyp fecundity
among reproductivelymature coloniesin popula-
tions of eight Acropora species.but no significant
153
variability wrthin a population of A. hyacinthus.
The number of planulae releasedper coral head
was extremelyvariable in a shallow-waterpopula-
tion of Pocillopora clamicornisin Hawaii (Harri-
gan, 1972), while in other speciesfecundity has
been observed to vary with depth. Fecundity in
Acropora (Isopora) pali/bra colonies near Lae
(Papua New Guinea) varied inverselywith depth
(Kojis and Quinn, 1984), whereas fecundity in-
creasedwith depth in a population of A. .fbrntosan
the central Great Barrier Reef (J. Oliver, unpub-
lisheddata). Planulationsuccessin Agaricia uguri-
ciles did not vary significantly with depth (Van
Moorsel, 1983).Reciprocaltransplantsof colonres
along depth gradients would help to identify
whether the variation in fecundity within these
populations resulted from environmental influ-
encesor genetic differences.
Fecundity also varies between populations of
some coral species.Slight differencesin average
polyp fecundity have been observed between
populations of Acroporaformosa, Goniastreaus-
pera, G.favulus and Platlgyra sinensiswithin the
central and southern regions of the Great Barrier
Reef (Kojis and Quinn, l98l; Babcock, 1986,
J. Oliver, unpublisheddata). Larger differencesrn
fecundity have been observedamong populations
of Acropora palifera near Lae (Kojis and Quinn,
1984),and betweenpopulations at Lae (7"S) and
H e r o n I s l a n d( 2 3 " S )( K o j i s , 1 9 8 6 b ) .
Fecundityand stress.A variety of natural and man-
induced perturbations cause sub-lethal stress in
coralsand resultin loweredfecundity.Fecundity in
Acropora paliJbracolonies near Lae (Papua New
Guinea)was found to be negativelycorrelatedwith
turbidity and sedimentation, as well as depth
(Kojis and Quinn, 1984).These factors may have
acted synergistically by lowering light levels,
thereby decreasingthe overall energy available to
the corals, and increasing the expenditure on
cleaning at the expense of reproduction and
growth (Kojis and Quinn, 1984). Fecundity was
also depressedat all depths during periods of
maximum sea temperature,possibly by thermal
stress (Ko;is and Quinn, 1984). Environmental
disturbancesincluding lowered salinity, unusually
low tides.high seatemperaturesand low irradiance
caused abortion of developing larvae in Pocillo-
pora damicornisin Hawaii, resulting in lowered
t54
planula production (Jokiel, 1985).Reduced plan-
ula production in the absence of ultraviolet
radiation has beendemonstratedexperimentallyin
t h i s s p e c i e s( J o k i e la n d Y o r k , 1 9 8 2 ;J o k i e l , 1 9 8 5 ) .
Mechanical damage and fragmentation can
reduce fecundity in corals. Fragments ol Gonias-
trea.favuluscoloniesseparatedsix months prior to
spawning had lower fecundity than fragments of
the same size which had been separated for two
years, and gonads were absent from polyps
bordering regions which had been recently dam-
a g e d ( K o j i s a n d Q u i n n , 1 9 8 1 , 1 9 8 5 ) .F r e q u e n t
fragmentation or partial colony mortality may
therefore severely reduce the reproductive output
of coral populations (Szmant-Froelich, 1985).
Intraspecific competition has been observed to
depress fecundity in Stylophora pistillata (see
Rinkevich and Loya, 1985). Polyps nearest the
competitive interaction zones showed reduced or
no gametedevelopment,and the number of ovaries
in competingcolonieswas greatlyreduced,particu-
larly in the inferior partners (Rinkevich and Loya,
19 8 s ) .
Pollution also adverselyaffects sexual reproduc-
tion in corals. Loya (1975, 1976c)observeda96uh
reduction in recolonizationof corals on a chroni-
cally polluted reef near Eilat (Israel)and proposed
that, among other effects,chronic oil pollution
may damage the reproductive system of corals.
This was confirmed in a subsequentfield study of
Stylophora pistillata which showed that fecundity
was four times greater on the control reef com-
pared with the chronically polluted reef, where the
population had fewer breeding colonies, fewer
ovaries and planulae per polyp, and a marked
decreasein the overall reproductiveindex (Rinkev-
ich and Loya, 1977). Chronic exposure to sub-
lethal levelsof the water-solublefractions of crude
oil in long-term laboratory experimentscauseda
significantreduction in the number of ovariesper
polyp in S. pistillata (see Rinkevich and Loya,
1979c),and induced premature abortion of planu-
lae and eggs (Loya and Rinkevich, 1979).Acute
and chronic exposures to the water-soluble frac-
tions of fuel oil have also been shown to damage
the reproductive system of Manicina areolata
(Peters, 1978; Peters et al., l98l). Porites porites
colonies sampled from two reefs in Barbados
s,ubjectedto chronic urban and industrialpollution
contained lower numbers of larvae than colonies
P.L. HARRISON AND C.C. WALLACE
from a relativelyunpollutedreef nearby (Tomascik
and Sander, 1987).The reduction in reproductive
activity was associatedwith increased turbidity
and eutrophication on the two polluted reefs,
which may have reducedlight for photosynthesis,
thereby reducing energy for embryogenesisand
larval development.
These studies show that scleractinian corals
divert resourcesaway from sexual reproduction
into other life functions in responseto a variety of
sub-lethalstressconditions. Where stressis local-
ized, fecundity is most severelyaffected in close
proximity to the stress,although some resources
from the entire colony may be divertedas well. The
pattern of stressresponsein corals indicatesthat
resource allocation to various life functions is
hierarchical,with maintenance,repair and growth
taking precedenceover sexual reproduction rn
many situations.How corals control the realloca-
tion of resourcesamong these life functions is
unknown.
As reproduction appears to have a narrower
tolerance to stressthan other life functions, coral
fecundity could be used as a sensitiveindicator of
sub-lethalstresson reefs.Kojis and Quinn (1984)
suggestedthat planulating speciessuch as lcro-
pora (Isopora)palifera would be particularly useful
in monitoring programmes, because they breed
year-round,are abundant, and allow fecundity to
be easily assessed.
Number versussize of coral offspring
Much information is available on the number
and size of eggs and larvae produced by vartous
coral species. Ideally, this could be used to
compare reproductive effort and life-history pat-
terns in thesecorals,but two problemscomplicate
comparative studiesbased on these data. Firstly,
disparate methods have been used to assess
fecundity and size of eggs and larvae in corals.
Some data are based on histological sections,
which underestimatethe size of eggsand planulae
becauseof the considerabletissueshrinkagewhich
accompanies histological processing (20 30o/o:
Harriott, 1983a). Histological methods also
underestimatefecundity by failing to section all the
eggsor larvae within each polyp (Fig.7.2; seealso
Marshall and Stephenson,1933). Fecundity and
size are best measured from live broken coral
sections (Fig. 7.3) or dissectedpolyps (Fig. 7.4).
CORALREPRODUCTIVE
BIOLOGY 155

These methods have the advantage of allowing be compensatedfor by multiple reproductivecycles

entire gonadsto be viewed and measured,and are eachyear (seep. l6l). Exceptionallyhigh fecundity
readily applicableto most corals, including small- and egg volume have been reported in some
polyped species (Oliver, 1919: Fadlallah and gonochoric species (for instance, Fungia spp.,
P e a r s e1, 9 8 2 ab, ; K o j i s a n d Q u i n n , 1 9 8 2 a ; W a l l a c e , Siderastreasiderea,Turbinaria mesenterina),and in
I985a). some species with relatively large, deep polyps
Comparativestudiesare also complicatedby the (Favia ./avus, Lobophyllia corymbosa) (Table 7.7).
fact that fecundity is usually estimated per polyp; Comparative studies of reproductive effort could
but polyp size and density vary greatly between therefore be further refined if, in future, fecundity
species.Fecundity is thereforebetter compared on was estimatedper unit tissueto allow for variation
an area basis. Harriott (1983a) observed that in polyp architecture.
fecundity and egg diameter in four coral species
increased with increasing polyp size, but that Gametogenesisand breeding
fecundity was inversely proportional to egg size
when compared in l0 cm diameter colonies.Such Gametogenesis
comparisonsare further improved where fecundity Histological studies indicate that the basic
is expressedper unit area. This has the advantage pattern of gametogenesis in coralsis similar to that
of allowing specieswith different growth forms to of other cnidarians and marine invertebrates
be compared (Table 7.7). (Campbell, 1974a;Giese and Pearse,1974;Fadlal-
When annual reproductive effort is compared in lah, 1983a).However, little detailedinformation is
the 32 coral speciesfor which data are available available on the fundamentally important pro-
(Table7.7), an inverse relationship between the cessesof differentiation,growth and development
size and numbers of eggs and larvae is apparent o l g a m e t e si n S c l e r a c t i n i a .
(Fig. 7.5). The volume of eggsor larvae produced
per unit area is fairly consistentin many of these Origin of germ cells. Cnidarian germ cells are
"trade-off' (Stearns, thought to develop from interstitial cells (Camp-
species(Table 7.7), hence a
1976)is apparent betweenthe size and number of bell, 1974a),but there is some controversy as to
eggsand larvae produced by different coral species. whetheranthozoanspossesstrue interstitialcellsor
Brooding species tend to produce fewer smaller only amoebocytesand mesogloealcells(Chapman,
eggs than related broadcast-spawning species 1974:Larkman. l98l). Germ cells in anthozoans
(Table7.7),but in some brooding speciesthis may are generallyconsideredto be endodermalin origin
(Campbell, 1974a;' Schafer, 1983a) - &S, for
instance, in the corals Agaricia spp., Astrangia
danae, Diploria strigosa, Favia fragum, Madracis
mirabilis and Porites porites (Szmant-Froelich et
al., 1980, 1985; Delvoye, 1982; Wyers, 1985;
E Tomascikand Sander,1987).In contrast,Gardiner
: (1902b)and Matthai (1914)consideredthat coral
E germ cellswere of ectodermal origin. Disagreement
I
over the origin of sex cells in corals could be
E
resolved by detailed ultrastructural studies of the
e a r l y s t a g e so f g a m e t o g e n e s i s .

Oogenesis. The earliest recognizable stages of

oogenesisin Agaricia spp., Astrangia danee,Diplo-
10 100 1000 10,000
l e c u n d i l yc m ?y e a r
- ria strigosa, Favia fragum and Madracis mirabilis
are stem cells or primordial oogonia, which
F i g . 7 . 5 . S i z e( p m ) v e r s u sf e c u n d i t y( c m 2 y r - 1 ) o f s c l e r a c t i n i a n
planulae and eggs (fecundity plotted on a logarithmic scale)
develop in the mesenterialgastrodermisadjacent to
showing the inverse relationship between size and numbers of the mesogloea(Szmant-Froelichet al., 1980, 1985;
e g g sa n d l a r v a e i n 3 2 c o r a l s p e c i e s . Delvoye, 1982; Wyers, 1985). They are distin-
 P.L. HARRISON AND C.C. WALLACE

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CORAL REPRODUCTIVEBIOLOGY

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158
guished from interstitial cells by their large
transparent nucleus and relatively small cyto-
plasm, and tend to occur singly rather than
aggregated,as in the caseof primary spermatogo-
nia (Szmant-Froelichet al., 1980;Delvoye, 1982).
These cells proliferate and migrate into the
mesogloea,where the nucleus enlarges to form a
germinal vesiclecontaining a prominent nucleolus
(Delvoye, 1982).Ultrastructural studiesof oogene-
sis in Scleractiniaand other Hexacoralliaindicate
that the first yolk granules appear in oogonia
before they migrate into the mesogloea(Schafer
and Schmidt, 1980;Von Schafer,1983a).Histolo-
gical studies of Agaricia spp., Astrangia danae,
Favia fragum and P. porites recorded vitellogenesis
only after oocyteswere establishedin the mesenter-
ial mesogloea(Szmant-Froelichet al., 1980, 1985;
Delvoye, 1982;Tomascik and Sander, 1987).
Subsequentoocyte development is characterized
by growth of the nucleus and cytoplasm, and an
increase in the ratio of cytoplasm to nucleus
volume. With continued growth, oocytes often
become irregularly shaped due to spatial con-
straints within the ovary or polyp. As oocytes
begin to mature, a vitelline membrane or cortical
layer forms beneath the plasma membrane, and the
germinal vesiclemigrates to the periphery of the
cytoplasm at the animal pole. In many species
oocytes become obviously coloured some weeks
prior to spawning (Marshall and Stephenson,
1 9 3 3 ;H a r r i s o n e t a l . , 1 9 8 4 ;B a b c o c ke t a l . , 1 9 8 6 ) .
In the final stages of oocyte maturation, the
nuclear chromatin condenses(Szmant-Froelichet
a1., 1980), holes may develop in the nucleolus
(Marshall and Stephenson,1933; Delvoye, 1982)
and the germinal vesiclegradually disappearsprior
to fertilization (Rinkevich and Loya, 1979a).
No information is availableon the nutrition of
coral oocytesduring oogenesis.ln some speciesa
number of oocytesare resorbedduring oogenesis,
which may provide nutrient for the remaining
oocytes. Oocyte degeneration or fusion is an
unusual feature of cnidarian oogenesis(Campbell,
1974a),and was first observed among Scleractinia
in Euphyllia glabrescensby Bourne (1888). This
phenomenon has since been observed in other
corals, although the stage at which degeneration
occurs varies between species.In Agaricia spp. a
few of the proliferating oogonia are apparently
resorbed (Delvoye, 1982). In Acropora spp., ls-
P.L.HARRISON
AND C.C.WALLACE
trangia danae,Poc'illoporadamicornis, P. meandrina,
Porites porites, Stylophora pistillata and Turbinaria
mesenterinathe number of oocytes in each ovary is
reducedduring development(Stimson, 1976;Oliver,
1979;Rinkevich and Loya, 1979a1, Szmant-Froelich
et al., 1980;Harriott, 1983b;Stoddart and Black,
1985; Kojis, 1986a;Tomascik and Sander, 1987;
Willis, 1987).In Diploria strigosa,up to 30% of the
large advanced oocytes in each colony degenerate
and are rapidly resorbedjust prior to maturation
(Wyers, 1985).Mature eggswhich fail to be released
or fertilized are also resorbed in some species
(Rinkevich and Loya, 1979a;Szmant-Froelichet al.,
1980;Harriott, 1983a;Kojis, 1986a).The phenome-
non of oocyte resorption remains poorly under-
stood; thus it is not known how resorption occurs,
what determineswhich cells are sacrificed in each
ovary, or whether environmental, nutritional or
other physiologicallimitations induce oocyte degen-
eration.
Eggs. Difficulties in distinguishing between the
final, often transitory, maturation stagesin inverte-
brate oocytes have created considerableconfusion
"egg" (seeGieseand
over the definition of the term
"egg" is
Pearse, 1974). In this chapter the term
applied to all later stagesof oogenesisfrom fully
grown maturing oocytes up until fertilization.
Unfertilized scleractinian eggs typically have an
outer microvillous membrane, a cortical layer
composed of numerous vesiclesof varying struc-
ture, mitochondria, rounded fibrillar para-crystal-
line inclusions and heterogenousyolk granules
(Schafer and Schmidt, 1980; Szmant-Froelichet
a l . , 1 9 8 0 ; V o nS c h a f e r ,1 9 8 3 ab, ; H a r r i s o n , 1 9 8 8 a ) .
The yolk granules occupy most of the ooplasm
(Fi5.7.2; seealso Marshall and Stephenson,1933)
and have a band of phosphataseand PAS (Periodic
Acid-Schiff) activity concentrated around them
(Goreau, 1956). The main storage product is
probably lipid, because spawned eggs have a
calorific value approaching that of pure lipid
(B. Willis, unpublished data), and lipid granules
are common in ultra-structural sections of eggs
(Von Schafer,1983a,b; Harrison, 1988a)and their
contentsare dissolvedduring histologicalprocess-
ing (Rinkevich and Loya, 1979a; Stoddart and
Black, 1985). Two types of phospholipids are
present in the eggs of Galaxeafascicularis (Harri-
son.1988a).
I
 BIOLOGY
CORALREPRODUCTIVE
Coral eggs are often highly pigmented, but the
location and composition of these pigments have
not been determined.Eggs are commonly pink or
red, although some speciesproduce yellow, orange,
grey, green, aquamarine or purple coloured eggs
(Babcocket al., 1986).Spawnedeggsof Auopora
millepora, Favia pallida and Goniastrea favulus
contain high levels of an ultraviolet blocking agent
which probably protects them from ultraviolet
radiation during their planktonic development
phase (A. Jackson and R. Babcock, unpublished
data).The presenceof zooxanthellaein the eggsof
Montipora spp. and Porites spp. distinguishesthem
from the eggsof other corals (Goreau, 1956;Kojis
and Quinn, 1982a1' Heyward and Collins, 1985a;
Babcock et al., 1986; Heyward, 1986; Tomascik
a n d S a n d e r , 1 9 8 7 ) . Z o o x a n t h e l l a ea r e u s u a l l y
incorporated into Porites and Montipora eggsa few
weeks prior to maturation (Goreau, 1956; Kojis
and Quinn, 1982a;Heyward, 1986; Tomascik and
Sander, 1987) but in Montipora digitata the
zooxanthellaeappear in the eggs only 24 h before
s p a w n i n g( A . H e y w a r d .p e r s .c o m m u n . ) .
Detailed comparative studies of scleractinian
eggs are generally lacking, so it is not known
whether systematicpatterns occur in egg structure
which correspond to those observed in the sperm
(seep. 160).Systematictrends are apparentin egg
size, which is generally consistentwithin species
and tends to be conservative within some families
(Table7.7). Acroporidae and Mussidae typically
have large eggs (400-800 pm mean diameter),
those of Faviidae and Pectiniidae tend to be
intermediatein size (300 500 pm), while eggs of
Agariciidae,Fungiidae and Pocilloporidaetend to
be small (100-250pm) (Table 7.7). The largest
scleractinianeggsrecordedare producedby Flabel-
lum rubrum and measure 1500x 1000pm (Gard-
iner, 1902a),while the smallestare 50 pm in mean
diameter from Porites astreoides (see Szmant,
1986).Increasedegg size appearsto be correlated
with longer oogenic developmentin corals. How-
ever, not all corals with extended cycles of
oogenesisproduce large eggs (see, for instance,
Astrangia lajollaensis: Fadlallah, 1982; Paracya-
thusstearnsii:Fadlallah and Pearse.1982b).
Spermatogenesis.The first recognizableelementsof
spermatogenesisin corals are small groups of cells
which accumulatein the sastrodermisof mesenter-
159
ies adjacent to the mesogloea. In Agaricia agari-
cites, A. humilis and Favia fragum these cells are I
about 3.5 to 4 um in diameter and resemble
enlargedinterstitial cells (Delvoye, 1982; Szmant-
Froelich et al., 1985).The cells then enter or are
engulfed by the mesogloea,and the incipient testes
are enlargedby immigration of additional cells and
by numerous mitoses (Szmant-Froelich et al.,
1980, 1985; Delvoye, 1982). The spermatogonia
then differentiate into primary spermatocytes,
which undergo meiosis to form secondary sperma-
tocytes,and then spermatids(Delvoye, 1982).As
spermiogenesisproceeds, the cytoplasm and nu-
clear chromatin condense, a single flagellum
develops,and organellesof the sperm midpiece are
arranged to form the characteristic shape of the
mature spermatozoon(Schmidt and Zissler, 1979;
Harrison, 1988b).The final stagesof spermiogene-
sis can proceed very rapidly. In some corals,
sperm-headcondensation is completed and flagel-
lar motility increasesrapidly in the week prior to
spawning(Harrison et al., 1984).This sequenceof
development is readily observed in smears of live
testes,and provides a convenient index of gonad
maturity and proximity to spawningin many coral
species(Harrison et al., 1984; Babcock et al.,
l 986).
Spermatozoa. Two distinct types of sperm have
been observed in scleractiniancorals (Harrison,
1985, 1988b). In one sperm type, the head and
midpiece are pear-shapedor ovoid. The nucleus is
ovoid or bullet-shaped,and may contain a zone of
less electron dense material at the apex of the
condensedchromatin (Fig. 7.6). Adjacent to the
nucleus lie small vesicleswhich correspond in size
"pro-acrosomal" vesiclesof
and position to the
other anthozoans (see Hinsch and Clarke, 1973;
Miller, 1983).A well-definedacrosomeappearsto
be absent. Another unusual feature of these sperm
are the lamellae which lie adjacent to the mito-
chondria and occupy a large volume of the
midpiece compared with other anthozoan sperm
(Fig. 7.6; cf. Schmidt and Zissler, 1979; Schmidt
and Holtken, 1980).The midpiece also contains
aggregated mitochondria or a single fused mito-
chondrion, a lipid body and complex centriolar
structures,and a cytoplasmiccollar surrounds the
anterior portion of the flagellum at the base of the
s p e r m ( F i g . 7 . 6 ; s e ea l s o H a r r i s o n , 1 9 8 5 , 1 9 8 8 b ) .
CORALREPRODUCTIVE
BIOLOGY
( s e e F r a n z e n . 1 9 5 6 , 1 9 7 0 ) ,b o t h t y p e s o f c o r a l
sperm possessultrastructural featureswhich devi-
ate from the archetypalplan. The pear-shapedand
ovoid spermof hermaphroditiccoralsshow greater
modificationthan the conical sperm of gonochoric
species,suggestingthat pear-shapedand ovoid
sperm are relativelyadvanced(Harrison, 1988b).
Some variation in structure is apparent within
both types of coral sperm; and the degree of
variation increaseswith taxonomic level. which
implies that sperm structure has a phylogenetic
basis(Harrison, 1985).However, the basisfor the
more fundamental dichotomy in sperm structure
betweenthe round and pointed sperm types has
not yet been determined. Although these sperm
typesare associatedwith different sexualpatterns,
in most casesthey occur in different families.It is
therefore difficult to determine whether sperm
structurein corals is influencedmore by sexuality
or by phylogeny. If the dichotomy in sperm
structure is under phylogeneticcontrol, the con-
trasting rounded and pointed sperm types would
suggestthat the Scleractiniahad divergedsubstan-
tially during their evolutionary history, or that
they were polyphyletic in origin (Harrison, 1985).
If the contrasting sperm types are ultimately
constrainedby sexuality,the substantialstructural
reorganizationin sperm from hermaphroditicand
gonochoric corals may have a functional basis
( H a r r i s o n , 1 9 8 5 , 1 9 8 8 b ) .S t u d i e s o f s p e r m e g g
interaction, and comparative ultrastructural
studiesof sperm from genera with variable sexual-
ity such as Agaricia, Monlastrea and Poriles
(Table7.3), would help to resolve this issue.
Comparativestudiesof sperm structure in brood-
ing corals with internal fertilization are also
needed.
Gametogeniccycles
Gametogenicprocessesin corals are generally
cyclicand usuallyexhibit annual or lunar rhythms.
Gametogeniccycles have been studied in more
than 80 speciesto date, and contrasting patterns
have been observed in corals with different modes
of developmentor different sexual patterns. Spe-
cies which spawn gametesfor external fertilization
and developmentusually undergo a singlecycle of
gametogenesis each year, whereasmost brooding
specieshave multiple gametogeniccycles.
Single annual gametogenic cycles have been
l6l
reportedin 61 broadcast-spawning species.In most
of thesecorals,gametedevelopmentoccursfor less
than twelvemonths each year, and culminatesin a
short spawning period during spring or summer
( s e ep . 1 6 3 ) .F o l l o w i n gs p a w n i n g a , q u i e s c e nnt o n -
breedingperiod ensuesuntil gametogenesis begins
again and the annual cycle is repeated. The
gonochoric broadcast-spawnersAstrangia lajolla-
ensis,Paracyathusstearnsii and Turbinaria mesen-
terinahave an extendedoogeniccycle lasting 14 to
l5 months (Fadlallah, 1982;Fadlallah and Pearse,
1982b;Willis1 , 9 8 7 )A . l t h o u g h t h e o o c y t e sd e v e l o p
for more than twelvemonths, thesespecieshave an
annual spawningperiod. This is achievedthrough
overlapping oogenic cycles within each female,
whereimmature oocytesbegin developmentbefore
maturing oocytes are released(Fadlallah, 1982;
Fadlallah and Pearse,1982b;Willis, 1987).Sexu-
ally mature femalesof these speciesthus contain
gametesyear-round.
Astrangia danae and Ihree Montipora species
also have only one cycle of gametogenesis matur-
ing each year. However, following spawning, a
secondcycle of gametesbegin to develop but are
apparently resorbed before they mature (Szmant-
F r o e l i c he t a l . , 1 9 8 0 ;R o b e r t s o n ,1 9 8 1 ) .M a r s h a l l
and Stephenson(1933) also found evidenceof a
bimodal gametogeniccycle in Symphyllia recta,but
again only one cycle apparentlymatured. Szmant-
Froelich et al. (1980) found that colonies of
Astrangia danae maintained in the laboratory at
maximum local sea temperatures, and fed regu-
larly, were able to spawn year-round. These
observationssuggestthat under more favourable
environmentalconditions some broadcast-spawn-
ing speciesmay be capable of completing more
than one cycle of gametogenesis each year.
Multiple gametogeniccycles have been docu-
mented in eight brooding species.Acropora (lso-
pora) cuneala colonies at Heron island (Great
Barrier Reef) have two consecutive cycles of
gametogenesis each year, while colonies of Acro-
pora (Isopora) paliJbra near Lae (Papua New
Guinea) have six (Kojis, 1986a,b). In contrast,
A. palifera colonies at Heron Island and colonies
of Mycetophyllia feror in Puerto Rico have single
gametogenic cycles each year (Kojis, 1986a;
Szmant, 1986).In other brooding species,the exact
number of gametogeniccyclesproduced each year
has not been reported, but periodicity of gamete
;
162
development has been established.Lunar cyclesof
spermatogenesisor oogenesishave been observed
in Agaricia species (Delvoye, 1982), Favia fragum
(seeSzmant-Froelich et al., 1985) and Pocillopora
domicornis(Muir, 1984;Stoddart and Black, 1985;
Martin-Chavez, 1986).Acropora paliJ'eracolonies
near Lae have bimonthly gametogenic cycles
(Kojis, 1986b), whlle Balenophyllia elegans and
Goniopora queenslandioedecima have prolonged,
overlapping oogenic cycles lasting at least two
years(Yamazato et al., 1982;cf. Yamazato et al.,
1975; Fadlallah and Pearse, 1982a).
Reproductive cycles of some corals in which
gametogenesis has been studied cannot be clearly
interpreted. Mature gametesor planulae have been
observed in populations of some speciesyear-
round or during extendedbreedingperiods,but it
is not known whether this is a result of multiple
gametogeniccycleswithin eachcoral, or asynchro-
nous reproductionamong membersof the popula-
tion.
In most corals, oogenesisis initiated prior to
spermatogenesiswithin each breeding cycle. Oo-
genesisoften precedes spermatogenesisby a few
months, with both sexessubsequentlydeveloping
and maturing together. The 42 hermaphroditic
coral specieswith this seasonalpattern of develop-
"annual protogynous
ment are often referred to as
hermaphrodites". However, in order to avoid
"protogynous sequentialher-
confusion with true
maphroditism" (see page 137), a new term rs
needed to describe this particular seasonal se-
quenceof egg and sperm developmentin simulta-
neous hermaphrodites.In gonochoric coral spe-
cies, females may begin gametogenesiseither
earlier than males (Porites spp.: Harriott, 1983a;
Montastrea cet)ernosa, Dendrogyra cylindricus:
Szmant, 1986),synchronouslywith males (Porites
spp.: Kojis and Quinn, 1982a),or later than males
(Fungia spp.: Oliver, 1985)within each reproduc-
tive season.The fact that oocytes develop in many
coral speciesfor a considerableperiod of time
before spermatogenesisbeginsgreatly increasesthe
likelihood of finding only oocytes in samples,
particularly from single or infrequent collections.
This probably explainswhy some early studiesof
coral reproduction recordedonly oocytesin many
corals (see, for instance, Fowler, 1885, 1887,
1 8 8 8 ab, , 1 8 9 0 ; B o u r n e , 1 8 8 8 , 1 9 0 5 ; G a r d i n e r ,
1900;Duerden, 1902a,b), and emphasizes the need
P.L.HARRISON
AND C.C.WALLACE
for caution when interpreting sexuality from
incomplete sampling programs (Duerden, 1904;
F a d l a l l a h ,1 9 8 3 a ) .
Gametogenesisis usually synchronizedwithin
eachcolony or solitary coral, and at leastpartially
synchronizedamong members of breeding popula-
tions. In specieswith single annual gametogenic
cycles, gamete development is often variable
during the early stages of gametogenesis, but
becomesprogressivelymore synchronizedwithin
each coral and throughout the population as
development proceeds (Kojis and Quinn, 1981,
1982a; Harriott, 1983a; Wyers, 1985; Szmant,
1986). Gametes usually mature simultaneously
throughout a populationjust prior to spawning;or
maturation may be delayed in some corals,
resulting in the population "split-spawning" (sensu
Willis et al., 1985)over consecutivelunar cycles.In
some gonochoric broadcast-spawning species,
gametedevelopmentoccursasynchronouslywithin
each gonad or polyp (Gardiner, 1902b; Szmant-
Froelich et al., 1980; Oliver, 1985; Harrison,
l 988b).
Various developmental stages of gametes are
present in gonads or polyps of brooding species
with multiple, overlapping gametogeniccycles(see,
for instance,Delvoye, 1982; Kojis, 1986a).Gam-
etesfrom each cycle tend to mature together within
each coral, but less synchrony is apparent at the
population level compared with hermaphroditic
broadcast-spawningspecies.For example, gonad
development is highly synchronous within each
colony of Stylophora pistillata during periods of
planulation, but no synchrony was apparent
among coloniesof the population (Rinkevich and
Loya,1979b). In Acropora (Isopora) palifera near
Lae gametes mature synchronously within each
colony, but different colonies spawn on consecu-
tive lunar cycles(Kojis, 1986b).Individual colonies
have been observed to change cycles; hence these
colonies do not appear to be reproductively
isolated (Kojis, 1986b). Gametogenesisis also
synchronized within each of two coexisting, mor-
phologically different forms of Pocillopora dami-
cornis, but these groups may be reproductively
isolated;the genotypeofeach form is electrophore-
tically distinct and the gametes of each form
mature on different lunar phases (Muir, 1984).
Asynchronous gamete developmenthas been ob-
served in the brooding speciesBalanophyllia ele-
 BIOLOGY
CORALREPRODUCTIVE
gans, Cyphastrea ocellina and Porites porites
(Fadlallah and Pearse,1982a;Wright, 1986; To-
mascik and Sander, 1987). Factors which may
control the synchrony and periodicity of gameto-
genesisin corals are discussedlater (p. 168).
Breedingseasonsand synchrony
Gametogenesisculminates in the production of
mature gametes for spawning and fertilization
during the breeding season. Most corals have
distinct breeding seasonsand well-defined periods
of spawningor planula release.This contrastswith
earlierassumptionsthat reproductionin coralswas
essentiallynon-seasonal,especiallyin the tropics
where environmental conditions were thought to be
relativelyunvarying (Rosen, l98l). In fact, many
tropical regions have large seasonalfluctuations in
environmental factors such as temperature, irradi-
ance and water quality (Wellington and Glynn,
1983;Kojis and Quinn, 1984;Babcocket al., 1986),
and seasonal breeding patterns are particularly
prevalent among tropical corals. Non-seasonal
reproductive activity has been observed in the
abyssalcoral Caryophyllia ambrosiadredgedfrom a
depth of 2000 m in the Mediterranean (Van-Praet,
1985).Other abyssalanthozoansfrom this region
have highly seasonalbreeding cycles linked to the
increaseddetrital fallout during spring (Van-Praet,
1985),hencenon-seasonal reproductionmay not be
typical of all deep-seacorals.
The seasonal timing and length of breeding
periods in corals varies in relation to other
reproductive characteristics,and with latitude.
Broadcast-spawningspecieshave relatively short,
discreteannual breedingseasonswhereasbrooding
speciestend to breed and releaseplanulae through-
out extended periods or year-round. Breeding
patterns have been most widely studied among
hermaphroditicbroadcast-spawners. These corals
spawn predominantly in late spring or summer
during periods of rising or maximum sea temper-
atures, although some species spawn in late
summeron the Great Barrier Reef (Bothwell, 1982;
Wallace, 1985a) or in early autumn on reefs in
Western Australia (Simpson, 1985). Spawning is
usually restricted to one or a few nights each year,
and occurs synchronously throughout each popu-
fation. An exception to this pattern is Hydnophora
exesa whrch has a protracted spawning period
extendingover a few weeks(Babcocket al., 1986).
163
Most gonochoric broadcast-spawnersstudied to
date also breed in late spring or summer; however,
some speciesspawn during colder periods in late
autumn, winter, or early spring: Astrangia danae,
Caryophyllia smithi, Heteropsammia cochlea, He-
terocyathus aequicostatus, Paracyathus stearnsii
and Turbinaria spp. (Thynne, 1859; Hiscock and
H o w l e t t , 1 9 7 7 ; F i s k , 1 9 8 1 ;T r a n t e r e t a l . , 1 9 8 2 ;
Fadlallah, 1982; Fadlallah and Pearse, 1982b:
Harrison et al., 1984;Willis, 1987,and unpublished
data). Gonochoric broadcast-spawners tend to
have longer breeding periods and less tightly
synchronized spawning episodes than their her-
maphroditic counterparts. In some gonochoric
speciesonly a part of the population appears to
spawn during each event, and each coral may
spawn on a number of occasions.This resultsin a
seriesof staggeredspawning episodesthroughout
the population, extending over a few weeks (for
instance,Porites spp.: Kojis and Quinn, 1982a)or
months (for instance,Fungia spp.: Krupp, 1983;
Oliver, 7985; Porites compress(t:Heyward, 1986;
Turbinaria mesenterina: Willis, 1987). No clear
trends are apparent with regard to the breeding
seasons of brooding corals. The season and
duration of breeding and subsequent planula
releasevaries greatly between species(Shlesinger
a n d L o y a , 1 9 8 5 ;K o j i s , 1 9 8 6 a ) .
Latitudinal changesin breeding. Latitudinal varia-
tions in the length and timing of breeding seasons
have been observed in a variety of marine
invertebrates (Orton, 1920; Giese and Pearse,
1974). Corresponding trends are apparent in the
breeding seasonsof corals, particularly in brood-
ing specieswhich have been studied over a wide
latitudinal range. Breedingseasonsand periods of
planula release tend to be shorter at higher
latitudes, and occur over extendedperiods or year-
round in tropical regionsnearer the Equator. For
example, Acropora palifera breeds only once in
spring at Heron Island (23'S), but year-round at
Lizard Island (14"S) and reefs near Lae (7'S)
(Kojis, 1986b).Production of gametesand asexual
planulae in Pocillopora damicorms colonies is
restricted to the warm spring and summer months
on high-latitude reefs in southern Western Austra-
lia (32'S) (Stoddart and Black, 1985),but occurs
over extended periods or year-round on the Great
Barrier Reef (23'S to l4'S) (Marshall, 1932:
i
 164
Marshall and Stephenson,1933; Bothwell, 1982;
H a r r i o t r , 1 9 8 3 b ;M u i r , 1 9 8 4 ) .P l a n u l ap r o d u c t i o n
in this speciesoccursyear-roundin Hawaii (24"N),
Eniwetok (ll"N) and Palau (7"N) (Hada, 1932;
Kawaguti, l94la1' Edmondson, 1946: Atoda,
1947a;Harrigan, 1972; Stimson, 1976; Richmond
a n d J o k i e l , 1 9 8 4 ;J o k i e l , 1 9 8 5 ;R i c h m o n d , 1 9 8 5 b ) .
In contrast, P. damicornis appears to be non-
reproductive on eastern Pacific reefs near Panama
(8"N) (Richmond, 1985b). Similar latitudinal
trends are apparent in Seriatopora hystrix and
Stylophora pistillata, which breed and release
planulaeseasonallyin the Red Sea (29"N) and the
Great Barrier Reef (Loya, 1916a; Rinkevich and
Loya, 1979b;' Sammarco, 1982a; Loya, 1983b;
Shlesingerand Loya, 1985), but releaseplanulae
year-roundin Palau (Atoda, 1947b, l95lc). Inter-
estingly, Stylophora pistillata breeds and releases
planulae during the same months but opposite
seasonsin the Northern (Red Sea) and Southern
(Great Barrier Reef) Hemispheres(Loya, 1983b).
Breeding seasonsof broadcast-spawningspecies
may also be more protracted nearer the Equator.
Breeding seasons appear to be longer and less
synchronized in coral populations near Madang
(5"S) than on the Great Barrier Reef (J. Oliver, pers.
commun.). If the corals identified as Galaxea
fascicularis, Goniqstreaaspera and Heliofungia actini-
formis in Palau are the samespeciesas those studied
on the Great Barrier Reef and in the Red Sea, these
specieswould show both longer breedingseasonsand
a change from spawning to brooding modes of
developmentnearer the Equator (Table 7.4).
In some species the spawning season occurs
during later months at higher latitudes. Goniastrea
favulus spawns during spring or early summer in
October, November or Decemberin the central and
southern regions of the Great Barrier Reef (18" to
23'S) (Kojis and Quinn, 1981;Babcock,1984,1986;
Harrison et a1.,1984;Willis et al., 1985;Babcocket
al., 1986),but in January, shortly after mid-summer,
on Lord Howe Island (31"S) (Kojis and Quinn,
198l). In the Red Sea,Pocilloporaveruucosa spawns
one or two months earlier at Yanbu (24'N) than at
Eilat (29'N) (Fadlallah,1985;Shlesingerand Loya,
1985).In contrast, Diploria strigosaand Montastrect
annularis populations have similar spawning sea-
sons in Puerto Rico (18'N) and Bermuda (32'N),
despite the large latitudinal range (Wyers, 1985,
1 9 8 6 :S z m a n t .1 9 8 6 ) .
t t
P.L.HARRISON
AND C.C.WALLACE I
Lunar periodicity of spawning and planula release.
Reproductiveactivitiesof many scleractiniancor-
als are synchronizedwith lunar phases.Broadcast-
spawning specieswith annual reproductive cycles
usually spawn on the samelunar phaseeach year at
eachlocality. The calendardate of spawningvaries
from year to year because the timing of lunar
phasesoccurs l0 to 12 days earlier each year, due
to differences in the length of solar and synodic
months (Caspers,1984;Willis et al., 1985).Most
speciesspawn during the full or last-quarter moon
phaseson lunar nights l5 to 24, correspondingto
the lunar divisions 5, 6 and 7 defined by Atoda
(1947a).Theseincludemass-spawningspeciesfrom
the Great Barrier Reef and Western Australia
( K o j i s a n d Q u i n n , 1 9 8 1 ,1 9 8 2 ab, ; H a r r i s o n e t a l . ,
1984;Willis et al., 1985;Simpson,1985;Babcocket
a1., 1986; see also p. 165), corals from Okinawa
(A. Heyward, unpublisheddata), and some species
in Hawaii (Heyward, 1986), the Caribbean
(Szmant, 1986; Wyers, 1986) and the Red Sea
(Shlesingerand Loya, 1985).A few specieshave
been recorded spawning about the time of new
moon on the Great Barrier Reef, in Hawaii and the
Red Sea (Shlesingerand Loya, 1985; Babcock et
al., 1986;Heyward, 1986),and during other lunar
phasesin the Red Sea(Shlesingerand Loya, 1985).
Montipora dilitata and Porites compressapopula-
tions in Hawaii have been observed spawning
following both full and new moon phases
(Hodgson, 1985a; Heyward, 1986, and unpub-
lished data), and colonies of Acropora elseyi,whtch
usually spawn following a new moon each year,
switchedphasesin one year and spawnedfollowing
a full moon (Harrison, unpubl. observ.).A. hyacin-
thus, A. latistella atd Goniastrearetformis popula-
tions spawn on different lunar phaseson the Great
Barrier Reef, Western Australian reefs and in the
R e d S e a( H a r r i s o ne t a l . , 1 9 8 4 ;W i l l i s e t a l . , 1 9 8 5 ;
Shlesingerand Loya, 1985; Simpson, 1985; Bab-
cock et al., 1986).
Lunar cyclesof gametematuration and planula
release have been recorded in many brooding
corals. Gamete maturation and release occurs
about the time of full moon or a few days
afterwards in Agaricia agaricites,A. humilis, Favia
fragum and Porites astreoides (Delvoye, 1982'
Szmant-Froelich et al., 1985; Chornesky and
Peters, 19871,E. Chornesky, unpublished data).
Delvoye (1982) also found evidenceof a second
CORALREPRODUCTIVE
BIOLOGY
concomitant series of spermatogeniccycles in
A. agariciteswhich were presentduring part of the
breeding season and matured near new-moon
phases.14 days out of phase with the full-moon
cycles.Breedingoccursafter the last-quartermoon
phase in Acropora (Isopora) pali/bra, but near the
first-quarter lunar phase in A. (Isopnra) cuneata
(Kojis, 1986a).Gamete maturation coincideswith
either full- or new-moon phasesin different forms
of Pocillopora damicornls(Muir. 1984; Stoddart
and Black, 1985).
The lunar timing and duration of planula-release
periodsvarieswidely among brooding species,and
somespeciesexhibit no lunar periodicityof planula
r e l e a s e( s e e F a d l a l l a h . 1 9 8 3 a , t a b l e l ; M o t o d a ,
1 9 3 9 J; e l l . 1 9 8 0 ;S h l e s i n g ear n d L o y a , 1 9 8 5 ;K o j i s .
1 9 8 6 a ;W r i g h t , 1 9 8 6 ) .P e r i o d so f p l a n u l a r e l e a s e
are generallylessclearly delineatedthan breeding
periods. Many brooders releaseplanulae over a
rangeof lunar phases,with shorter periodsof peak
release.For example, colonies of Favia fragum
from Puerto Rico releasedplanulaebetween6 and
15 days after new moon. with peak releasefrom
d a y s8 t o I I ( S z m a n t - F r o e l i ceht a l . , 1 9 8 5 ) S
. imilar
lunar patterns were observed in Favia .fragwn
populations in Jamaica and Barbados (P. Scott,
pers.commun.).In contrast,an earlierstudy of the
same Barbados population reported that planula
releasepeaked at new moon (Lewis, 1974a).The
timing of planula release in Favia .fragunt in
Barbados varied with colony size; peak planula
releasein small colonies occurred at the first-
quarter moon phase,while larger coloniespeaked
around full moon (P. Scott, unpublisheddata).
Contrasting lunar patterns of planula release
have been reported in two sympatric forms of
Pocillopora damicornis in Hawaii and from the
centralGreat Barrier Reef (Muir. 1984:Richmond
a n d J o k i e l , 1 9 8 4 ; J o k i e l , 1 9 8 5 ) ;a n d b e t w e e n
populations at these sites, the northern Great
Barrier Reef, southern Western Australia, Palau
and Eniwetok (Stephenson,1931; Marshall and
Stephenson,1933;Atoda, 1947a;Harrigan, 1972;
Stimson, 1978; Harriott, 1983b; Stoddart and
Black, 1985).In addition, seasonalchangesin the
lunar phaseof planula releasehave been reported
in P.danticornis populations from the northern
Great Barrier Reef (Marshall and Stephenson,
1933; Harriott, 1983b).Planula releaseby Stylo-
phora pistillata shows clear lunar periodicity in
165
Palau (Atoda, 1947b), but not in the Red Sea
(Rinkevich and Loya, 1979b).
Time of spawning and planula release. Spawning
has beenobservedin a wide variety of corals;most
of thesespawnat night betweendusk and midnight
( K o j i s a n d Q u i n n , 1 9 8 2 ab, ; H a r r i s o n e t a l . , 1 9 8 4 ;
S h l e s i n g ear n d L o y a , 1 9 8 5 ;S i m p s o n ,1 9 8 5 ;B a b -
cock et al., 1986;Szmant, 1986).Spawningusually
occurs at a specific period after sunset in each
population, and spawning times are generally
consistentfrom year to year (Harrison et al., 1984;
Babcocket al., 1986).Similar spawningtimes have
also beenrecordedamong populationsof the same
specieson different reefs(Babcock et a1.,1986).A
few specieshave been observedto spawn during
daylight. Fungia concinna and Pavona cactus
spawned at dawn on the Great Barrier Reef
( M a r s h a l l a n d S t e p h e n s o n ,1 9 3 3 ; O l i v e r , 1 9 8 5 ) ,
and a Porite.scolony was observedspawning about
mid-morning in Guam (J. Lucas, pers. commun.).
Caryophyllia smithi, Galaxea fascicularis, Gonias-
trea .favulus and some Fungia species have been
recorded as spawning during the afternoon or
before sunset(Kojis and Quinn, 1981;Tranter et
al., 1982:Krupp, 1983;Babcock et al., 1986).
Planula releasealso occurs predominantly at
night in populationsof Acropora(Isopora)cuneata,
Agaricia spp., Favia fragum, Pocillopora damicor-
nn from the Great Barrier Reef, Porires astreoides
and Stylophora pistillata (Vaughan, 1908; Rinke-
vich and Loya, 1979a; Lewis, 1974a1'Harriott,
1 9 8 3 bV ; a n M o o r s e l , 1 9 8 3 ;S z m a n t - F r o e l i ceht a l . ,
1985;Kojis, 1986a).Colonies of Favia fragum n
Barbados releasedapproximately equal numbers
of planulae during day and night before the first-
quarter moon phase, after which approximately
80% of planulae were releasedat night (P. Scott,
unpublisheddata). Planulareleasetn Balanophyllia
elegansand P. damicornis in Hawaii occurred at
various times, with no apparent differencesbe-
tween day and night (Harrigan, 1972; Fadlallah
and Pearse,1982a).
Regional comparisonsof coral community repro-
ductive patterns
Mass spawning of corals. Breeding patterns ln
scleractiniancorals have been most extensively
studied on the Great Barrier Reef, where many
166
species spawn together during a few short,
predictableannual mass-spawningperiods (Harri-
s o n e t a l . , 1 9 8 3 ,1 9 8 4 ;W i l l i s e t a l . , 1 9 8 5 ;W a l l a c e ,
1 9 8 5 aB ; a b c o c ke t a l . , 1 9 8 6 ;W a l l a c ee t a l . , 1 9 8 6 a ) .
"Mass
spawning" is defined as the synchronous
releaseof gametesby many speciesof coralsin one
eveningbetweendusk and midnight (Willis et al.,
1985),and occurson the Great Barrier Reef during
the week following full moons in late spring or
early summer.The major nights of spawningoccur
on the 3rd to the 6th nights after a full moon
during a period of neap tides, when more than
forty scleractinian species have been recorded
spawning together (Willis et al., 1985;Babcock et
al., 1986).Additional specieshave beenrecordedas
spawning on the nights preceding and following
this period. More than 134of the 356 scleractinian
speciesoccurring on the Great Barrier Reef have
been found to spawn during mass-spawning
periods,and it appearslikely that the majority of
corals there participate in mass spawning events
( H a r r i s o ne t a l . , 1 9 8 4 ;W i l l i s e t a l . , 1 9 8 5 ;B a b c o c k
et a1., 1986;and unpublisheddata). These species
comprisemore than half of the dominant corals in
coral communities from the central Great Barrier
Reef (Done, 1982; Babcock et a1., 1986),and
include taxonomicallydiverserepresentatives from
I I of the 15 scleractinianfamilies present there
(Willis et al., 1985,fig.3). A variety of other
marine invertebratesfrom the Great Barrier Reef
have been observed to spawn during mass-
spawningperiods,including alcyonaceansoft cor-
als and epitokous segmentsof polychaeteworms
( B o w d e n e t a l . . 1 9 8 5 ; B a b c o c k e t a l . , 1 9 8 6 ,a n d
unpublished observations;P.Hutchings, pers.
commun.), and echinoids (R. Olsen, pers. com-
mun.). Relativelyfew scleractiniancorals from the
Great Barrier Reef havebeenrecordedto spawn or
releaseplanulae outside mass-spawningperiods,
on other lunar phases,or at other times of the year
( W i l l i s e t a l . , 1 9 8 5 ,I t g . 3 ) .
Mass coral spawningshave been observed on
many reefs throughout the Great Barrier Reef
region. and synchronous spawnings have been
recorded in the northern. central and southern
regionsof the Great Barrier Reef over a 9" rangeof
latitude and up to 1200km apart (Harrison et al.,
1984;Willis et al., 1985;Babcock et al., 1986;
Oliver and Willis, 1987; and unpublished data).
Within eachreef community, populationsof many
AND C.C.WALLACE
P.L.HARRISON
corals usually spawn together during the same
major spawning period. However, some corals
exhibit delayed maturation, resulting in popula-
tions split-spawningover consecutivelunar cycles,
or some speciesspawning during later months
( H a r r i s o ne t a l . . 1 9 8 4 ;W i l l i s e t a l . , 1 9 8 5 ;B a b c o c k
et al., 1986,and unpublisheddata). The timing of
full moon in relation to the rise in local sea
temperature may determine the extent of split-
spawning within and between populations, and
hence when. and how many. major spawning
periodsoccur at each reef per year [seealso p. I 68;
H a r r i s o n e t a l . ( 1 9 8 4 )a n d W i l l i s e t a l . ( 1 9 8 5 ) 1 .
A few coral specieshave been observedspawn-
ing in Papua New Guinea (L. Colin, pers. com-
mun. to J. Oliver) and Fiji (L. Zann, pers. com-
mun.) during periods of mass spawning on the
Great Barrier Reef, but the extent and synchrony
of spawningin theseand other South Pacificcoral
c o m m u n i t i e si s n o t y e t k n o w n . C a s p e r s( 1 9 8 4 )
suggestedthat mass coral reproduction may be
responsiblefor the characteristicmucus discharge
found on Samoan coral reefs two days before the
annual swarming of the palolo worm on last-
quarter moon phasesin October and November.
These periods also coincide with the annual mass
coral-spawningperiodson the Great Barrier Reef.
Mass coral spawning has more recently been
observed on reefs off Western Australia in the
I n d i a n O c e a n( S i m p s o n ,1 9 8 5 ,u n p u b l . d a t a ) .T h e
pattern of spawningis similar to that found on the
Great Barrier Reef in that it is nocturnal, multi-
specific,and coincideswith a period of neap tides
following full moon (Simpson, 1985). Further-
more, many of the mass-spawningspeciesrecorded
from the Great Barrier Reef also participate in
mass-spawningepisodes on Western Australian
reefs(Simpson, 1985).However, important differ-
encesexistin the seasonaltiming of massspawning
betweenthesecoral communities on the east and
west coasts of Australia. Mass spawning on
WesternAustralian reefsoccursin autumn during
March or April, five months later than on the
G r e a t B a r r i e r R e e f ( S i m p s o n ,1 9 8 5 ) .D e s p i t eb o t h
regionsexperiencingsimilar seasonaltemperature
regimes. mass spawning on Western Australian
reefsoccursafter an extendedperiod of maximum
sea temperatures,whereasmass spawning on the
Great Barrier Reefcoincideswith rapidly rising sea
temperatures prior to the summer maxlmum
 BIOLOGY
CORALREPRODUCTIVE
(Simpson1 . 9 8 5 ;B a b c o c ke t a l . , 1 9 8 6 ) I. n a d d i t i o n ,
spawningon Western Australian reefs appearsto
be confinedto the eighth and ninth nights after full
moon (Simpson, 1985),rather than being spread
over the week following full moon as on the Great
Barrier Reef (Willis et al., 1985; Babcock et al..
I986).
Synchronous multispecific coral spawning has
also been recorded in Okinawa (Ryukyu islands,
Japan);however,the spawningperiods tend to be
more diffuse than those observed on Australian
reefs (A. Heyward, pers. commun.). Nocturnal,
multispecificspawningof 18 coral specieshas been
observedin Okinawa following full moons in June
to August throughout the northern summer,
during periods of maximum sea temperatures
(A. Heyward, unpublished data). Most of these
s p e c i easr e k n o w n t o p a r t i c i p a t ei n m a s ss p a w n i n g s
on Australian reefs, but spawning is spread over
one to nine nights after full moon, with a tendency
for populations to split-spawnover two or three
lunar cycles(A. Heyward, unpublisheddata). Far-
ther south in the Ryukyu islands,massesof coral
eggsand larvae have been observedeach May for
many yearson reefsin the island of Ishigaki,where
"punitsu" (Wal-
the spawning was known as the
l a c ee t a l . , 1 9 8 6 a ;S . K a w a g u t i . p e r s .c o m m u n . t o
R. Babcock).
Knowledge of coral reproductive patterns of
other northern Pacific locations has been domi-
nated by studies of planula releasein brooding
c o r a l s( E d m o n d s o n ,1 9 2 9 ;A b e , 1 9 3 1 , 1 9 3 9Al ,t o d a ,
1953;Harrigan, 1912;Stimson, 1976,1918;Fadlal-
l a h a n d P e a r s e ,1 9 8 2 a ; R i c h m o n d a n d J o k i e l ,
1984).Multispecific synchronouscoral spawning
events have been observed at some reefs in the
northwestern Pacific, but it is not yet known
whether these events are comparable in scale to
masscoral-spawningepisodeson Australian reefs.
A variety of spawnedcoral eggswere observedon
reefs in the Philippines in May (B. Kojis, pers.
commun.), and coral spawning or large aggrega-
tions ofcoral spawnhave beenobservedon reefsin
Yap (7"N), four to six nights after full moons in
May and June (M. Falanruw,pers.commun. to
"great
A. Smith). Kawaguti (1940a) witnesseda
clouding of planulae" on a reef in Taiwan about
noon, two days after a full moon in July, and
"premature spawning of the
consideredit to be a
planulae" of Acropora. However, the irregular
t6l
shape and slow developmentrate of the propag-
ules,togetherwith their range of sizesand colours
(Kawaguti, 1940a), suggest that the "planulae"
may have been developingembryos resultingfrom
spawningof more than one species.A similar event
was observedon an outer moat reef in Palau rn
M a r c h ( K a w a g u t i ,1 9 4 1 b ) .
Spawning patterns among Hawaiian corals
appear to be less synchronous than in coral
communities from Australia or Okinawa. Al-
though some specieshave overlapping spawning
periods, many of the dominant corals have
separatespawningtimes staggeredthroughout the
summer, following new and full moon phases
( K r u p p , 1 9 8 3 ;H o d g s o n , 1 9 8 5 a ;H e y w a r d , 1 9 8 6 ,
and unpublished data). Recent observations of
coral spawning and analysis of surface aggrega-
tions of spawnedeggsand larvae, which occur off
Bermuda for a few days each year between July
and September,indicate that synchronousmulti-
specificspawningmay also occur in this northwest-
ern Atlantic coral community (Wyers, 1986).
Temporal partitioning of coral reproduction. In
contrast to the multispecificspawning patterns of
coral communities on Indo-Pacific reefs and
possibly in Bermuda, the dominant coral species
studied to date in the Red Sea and the Caribbean
exhibit temporal separationof spawning or plan-
ula-releaseperiods (Shlesingerand Loya, 1985;
Szmant, 1986).Breedingwas synchronizedwithin
each olthe l3 most abundant scleractinianspecies
studied on reefs at Eilat (northern Red Sea);
however, each specieshad separate periods of
spawningor planula release,occurring in different
seasons,separatemonths, or on different lunar
phases within the same month (Shlesingerand
Loya, 1985).Sevenof thesespecieshave also been
studied from the Great Barrier Reef or Western
Australia, where they spawn togetherduring mass-
spawningepisodes(Harrison et al.. 1984;Simpson,
1 9 8 5 ;W i l l i s e t a l . , 1 9 8 5 ;B a b c o c ke t a l . , 1 9 8 6 ) T
. he
temporal reproductiveisolation these in and other
specieswas consistentthroughout three years of
study, so that significant mass-spawningevents
appear to be absent from coral communities at
E i l a t ( S h l e s i n g ear n d L o y a , 1 9 8 5 ) .
Most coral speciesstudied in the Caribbean
region also spawn or releaseplanulae at different
times throughout the year (Duerden, 1902a;Van
168
Moorsel, 1983: Szmant, 1986; Tomascik and
Sander, 1987; Chornesky and Peters. 1987;
W. Jaap, unpublished data). Comparative studies
of eleven coral species in Puerto Rico found
different patterns of spawning or planula release
for each species (Szmant. 1986). Most species
spawned synchronouslyduring late summer, but
spawning periods did not appear to be synchro-
nized between species. However, the spawning
periods of some Caribbean speciesmay overlap,
becausecoloniesof Atropora (Isoporu)cervic'ornts
and Diploria .strigosawere observed spawning on
the same night.
Environmental factors regulating coral reproduc-
tion
The synchronized sexual reproductive cycles
observed in populations of scleractiniancorals
suggestenvironmental regulation of their sexual
activities (Giese and Pearse, 1974; Olive, 1984).
Environmental conditions may influence sexual
processesas prorimute factors which provide cues
to synchronizereproductivecycles.and as ultintate
"exert
causes that selective pressure" on the
synchrony and timing of breeding within each
species(Giese and Pearse. 1974; Clark, l9l9).
Clark (1979) further distinguishedbetweenproxi-
mate causesthat create the environmentalcondi-
tions necessary for reproduction. from those
factors triggering specificchangesin reproductive
activities. Models of proximate control mechan-
isms regulating sexual cycles in marine inverte-
brates usually incorporate exogenous (external
environmental)factorswhich interactwith endoge-
nous (internal environmental) biorhythms (Giese
a n d P e a r s e1, 9 7 4 ;O l i v e a n d G a r w o o d , 1 9 8 3 ;O l i v e ,
1984). Unfortunately, nothing is known about
endogenousregulation of sexual reproduction in
scleractiniancorals,hencethe following discussion
is necessarilylimited to exogenousfactors.
Proximate factors influencingsexualreproduction
Reproductiveactivities of marine invertebrates
show annual seasonal,monthly lunar, and daily
patterns. A variety of environmental factors are
known to regulate reproductivecycles in marine
invertebrates, including sea temperature, day
length, salinity, food, moonlight, tidal cyclesand
daily light/dark cycles [see reviews by Orton
( 1 9 2 0 ) ,F o x ( 1 9 2 4 ) ,K o r r i n g a ( 1 9 5 7 ) ,G i e s e( 1 9 5 9 ) ,
P,L. I{ARRISON AND C,C. WALLACI]
H a u e n s c h i l d( 1 9 6 0 ) .F i n g e r m a n( 1 9 6 0 ) ,C i e s ea n d
P e a r s e( 1 9 7 4 ) ,H i m m e l m a n ( 1 9 8 0 )a n d N e u m a n n
( 1 9 8 0 ) 1I.t i s i m p o r t a n t t o d i s t i n g u i s hb e t w e e nt h e
factors which influencedifferent stagesof repro-
d u c t i v e c y c l e s .T h c s a m c e n v i r o n m e n t a ll a c t o r s
may act differently to co-ordinate each stage. or
different factors may operate at cach phasc.
Furthermore, different populations of thc samc
speciesmay respond to different environmcntal
s i g n a l si n s e p a r a t el o c a t i o n s ,a s h a s b e e n d e m o n -
s t r a t e di n v a r i o u sm a r i n e i n v e r t e b r a t e(sK o r r i n g a .
1947C ; lark. 1979).
Reproductiveactivitiesin corals are often corre-
lated with seasonalchanges in sea ten-rperature,
l u n a r t i d a l o r n o c t u r n a l m o o n l i g h t c y c l e s ,a n d
d a i l y l i g h t r d a r k c y c l e s( Y o n g e . 1 9 4 0 ; H a r r i g a n .
1 9 7 2 ; S z m a n t - F r o e l i c he t a l . . 1 9 8 0 ; K o j i s a n d
Q u i n n . l 9 8 l ; T r a n t e r e t a l . , 1 9 8 2 ;K r u p p . 1 9 8 3 ;
H a r r i s o ne t a l . , 1 9 8 4 ;F a d l a l l a h ,1 9 8 5 ;W i l l i s e t a l . .
1 9 8 5 ;B a b c o c ke t a l . , 1 9 8 6 ) B . a b c o c ke t a l . ( 1 9 8 6 )
proposedthat theseenvironmentalfactors operate
on progressivelyfiner time-scalesto synchronrzc
mass coral spawning on the Great Barrier Reef.
Lunar and diel light cyclesmay act as Zeitgebersto
entrain spawningto occur after a specificperiod of
darknessduring the first appropriate lunar phase
f o l l o w i n gt h e m a t u r a t i o no f g a m e t e s( W i l l i s e t a l . ,
1 9 8 5 ;B a b c o c ke t a l . , 1 9 8 6 ) .O t h e r e n v i r o n m e n t a l
factors such as seasonalchanges in day length.
water quality and food may also influencerepro-
d u c t i v ec y c l e si n c o r a l s( D e l v o y e ,1 9 8 2 ;F a d l a l l a h ,
1 9 8 2 ;F a d l a l l a ha n d P e a r s e ,1 9 8 2 a ;K o j i s , 1 9 8 6 b ) .
Thesehypothesesare based largely on correlative
evidencewhich is discussedbelow. Experimenta-
tion to test the various elementsof thesehypothe-
sesand to demonstratethe physiologicalbasis for
responseto exogenousfactors has only recently
begun, and thus will not be treated in detail
Seasonality.Seasonalvariation in sea temperature
has been widely acceptedas the most important
environmental factor controlling reproduction in
marine invertebrates (Orton. 1920; Gicsc and
. r t o n ( 1 9 2 0 )p r o p o s e dt h a t b r e e d i n g
P e a r s e1, 9 7 4 )O
in marine invertebrates occurred at a specific
temperature which was characteristic for each
species.and that breeding would be continuous
above or below a characteristic temperature.
However, spawning occurs at different temper-
atures in different populations of the same coral
C O R A LR E P R O D U C T I B
V IEO L O G Y
species.and breedingin most seasonallyreproduc-
tive coral species is not continuous withrn a
certain temperaturerange (Kojis, 1986b).Despite
considerablecorrelativeevidencefor Orton's rule.
there is surprisingly little direct experimental
evidence to prove that seasonal temperature
changesactually causethe observedreproductive
p a t t e r n s( G i e s e a n d P e a r s e ,1 9 7 4 ; C l a r k , 1 9 7 9 ) .
Furthermore, recent experimentalstudies of ma-
rine invertebrateshave shown that environmental
regulationof reproductiveactivitiesis under more
complex control. Seasonalchangesin day length
have been shown to regulate reproductiveactivi-
ties in echinoderms (Pearseand Eernisse, 1982;
Pearseand Walker, 1986).while temperatureand
day length have been shown to work interactively
in controlling gametogenicactivities in polycha-
etes (Garwood and Olive, 1982;Olive and Pillai,
I983).
Seasonalchangein seatemperatureis frequently
cited as an important environmental factor con-
trolling gametogenic cycles or planula-release
periods in scleractinian corals (Yonge, 1940;
S z m a n t - F r o e l i c he t a l . , 1 9 8 0 ; K o j i s a n d Q u i n n ,
1 9 8l ; T r a n t e r e t a l . . 1 9 8 2 ; V a n M o o r s e l , 1 9 8 3 ,
H a r r i s o n e t a l . . 1 9 8 4 ; F a d l a l l a h , 1 9 8 5 ;S t o d d a r t
a n d B l a c k .1 9 8 5W ; i l l i s e t a l . , 1 9 8 5 ;B a b c o c ke t a l . ,
1986).Differencesin the timing of gametematura-
tion and spawning between populations of the
samecoral specieson inshoreand offshorereefsin
the central Great Barrier Reei correspondingto
differencesin the time of the rise in sea temper-
aturesat these sites,provide indirect evidencefor
the influenceof temperatureon gametematuration
i n c o r a l s( H a r r i s o ne t a l . . 1 9 8 4 ;W i l l i s e t a l . . 1 9 8 5 ;
B a b c o c k e t a l . . 1 9 8 6 ; B a b c o c k , 1 9 8 6 ) .I n i t i a t i o n
and developmentof oocytes were similar among
populations of three faviid species studied on
inshoreand offshorereefsin this region, but testes
development.gamete maturation and spawning
occurred one month earlier on the inshore reef.
coinciding with an earlier and more rapid rise in
s e at e m p e r a t u r e( B a b c o c k ,1 9 8 6 ) .B a b c o c k( 1 9 8 6 )
suggested that temperature may regulate the
timing of spawning through controlling testes
development.
Kojis (1986b)suggestedthat seatemperaturesin
shallow reef-flatenvironmentsmay be too variable
to provide a reliable cue for controlling gameto-
genesis in corals, and proposed that seasonal
t69
changes in day length would provide a more
consistentannual pattern for regulatingreproduc-
tion in these habitats. Initiation of oogenesisin
At'ropora (Isopora) palifera colonies may be en-
trained by increasingday lengths, minimum day
l e n g t h so f 1 1 . 2h . o r b o t h ( K o j i s , 1 9 8 6 b ) .D e l v o y e
(1982)found sexualactivity of Agaricia agaric'ites
to be unrelatedto the small seasonalchangesin sea
temperature at Curagao, but correlated with
seasonalchangesin effectivesolar altitude. How
corals perceiveseasonalvariation in solar irradi-
ance (dependent upon solar altitude and day
length), or how this factor might affect their
reproductive activities. is not known. Scleracti-
nians lack specializedphotoreceptors,but they do
contain a variety of pigment cells which might be
light-sensitive(Goreau, 1956; Kawaguti and Yo-
koyama, 1966; Kawaguti, 1966, 1913, Lyons,
1 9 7 3 ab, ; V a n d e r m e u l e n , 1 9 7 4H1a. r r i s o n , 1 9 8 0 ) .I t
is also possiblethat other types of epidermal or
gastrodermalcoral cellsare photosensitive,or that
light acts directly on the gametes (Segal, 1970).
Zooxanthellate scleractiniansmay also perceive
seasonal changes in solar irradiance through
photosyntheticactivities of their symbiotic zoox-
anthellae.Seasonalcyclesof planula releasein the
non-zooxanthellate coral Bolanoph-vlliaelegansdo
not appear to be affectedby seasonalvariation in
photoperiod, as tested by experimental phase-
shifting of day length (J. Pearse,pers. commun.).
Simpson(1985)concludedthat seasonalchanges
in sea temperaturedo not control coral breeding
seasons,becausethe timing of gametogenesis and
massspawningperiodsdiffersbetweenpopulations
of the same specieson the east and west coastsof
Australia, despite the fact that they experience
similar seasonal temperature patterns. He pro-
posed that seasonalchanges in wind or current
patternsmay control the timing of massspawning.
However, theseenvironmentalchangesoccur after
a prolongedperiod of gametogenesis, and thus are
more likely to be ultimate factors exertingselective
pressureon the timing of the mass-spawning events
in each region. It is possible that reproductive
activities of corals in each region respond to
different environmental factors. or that corals in
the two regions may respond differently to the
same factors.
Rigorous experimental tests are required to
determinewhether sea temperature,day length or
t70
other seasonallyvariablefactors act independently
or interactively to exert proximate control over
seasonalreproductive patterns in scleractininian
corals, and at which stages their influence is
exerted.Variability in the timing of the onset of
gametogenesis within coral populations, and sub-
sequentincreasingsynchrony in gametogenicac-
tivities as spawning approaches(seep. 163), sug-
gest that cuesinitiating gametedevelopmentexert
lesssynchronizingeffect than those synchronizing
maturation and spawning of gametes.Differences
in the timing of gametogeniccyclesamong species
which spawn synchronously in mass-spawning
episodes (Babcock et al., 1986) indicate that
different speciesrespond differently to envtron-
mental factors initiating gamete development.
Split-spawningwithin coral populations indicates
that certain membersof thesepopulations exhibit
different physiologicalresponsesto the proximate
f a c t o r sc o n t r o l l i n gg a m e t em a t u r a t i o n .
Lunar rhythms. Lunar patterns of gametogenesis,
spawningand planula releaseare presentin many
coral species,but in most casesit is not known
whethertheserhythms are regulatedby moonlight,
tidal cycles,or related factors. Jokiel et al. (1985)
demonstratedthat night irradiance synchrontzes
lunar cycles of planula release in Pocillopora
damicctrnis.Experimental manipulation of simu-
lated moonlight conditions causedplanula release
from colonies held under shifted-phasenocturnal
illumination to move out of phase with colonies
exposed to natural nocturnal moonlight cycles
(Jokiel et al., 1985). Planula release became
asynchronous when colonies were exposed to
either constant full-moon or new-moon condi-
tions. Associated studies negated the possibility
that monthly planula releasecyclesof P. damicor-
nrswere controlledby 27d cyclesof solar radiation,
or by tide-relatedphysicalfactors (Richmond and
Jokiel, 1984;Jokiel, 1985; Jokiel et al., 1985).
Similar experimentalstudiesusing artificial moon-
light regimesto investigatethe effect of nocturnal
illumination on gametematuration and spawning
in annual broadcast-spawningspeciesare under
way (R. Babcock and B. Willis, pers. commun.).
Simpson (1985) suggesteddifferencesin the lunar
nights of spawning between corals on the Great
Barrier Reef and in Western Australia, but the
coincidenceof mass spawningswith neap tides in
P.L.HARRISON
AND C.C.WALLACE
both regions (see p. l6a), indicates that mass
spawnings are synchronized by tidal rhythms
following the full moon. Babcock et al. (1986)
proposed that tidal patterns may be of ultimate
importancein determiningappropriateperiods for
successfulbreeding, but that corals may use
moonlight as the proximate environmental signal
to predict the tidal regime.If so, populationsin the
two regionsmust responddifferentlyto moonlight
in order to synchronize their spawning periods
with neap tides.
Timing and triggers for spawning and planula
release.Experimentalmanipulationsof daily light
and dark cycles have shown that photoperiod
controls the final synchronizationand timing of
spawningin some corals. Babcock (1984) con-
trolled spawning times of Goniastreaaspera by
modifying photoperiods,while artificiallyextended
light periods delayed spawning in a variety of
species(Harrison et al., 1984, and unpublished
observations).Gamete maturation and spawning
in other cnidarians have been shown to be
controlled by light or dark periods (Ballard, 1942;
Yoshida et al., 1980;reviewedby Campbell, 1974a,
and by Fautin et al., 1990). Populations of
Goniastrea favulus on the Great Barrier Reef
spawn on low tidesduring late afternoon at Heron
Island. but on low tides after dark on reefsin the
c e n t r a l R e e fa r e a( K o j i s a n d Q u i n n , 1 9 8 1 ; B a b c o c k
e t a 1 . ,1 9 8 6 ) .S i m p s o n( 1 9 8 5 )s u g g e s t e tdh a t c o r a l
spawning may therefore be triggered by a tidal
rhythm interacting with diel light cycles.Prelimi-
nary studies on the timing of planula releasein
Pocillopora damicorni.sindicated that peak planula
releaseoccurred during periods of low tide, and
independentlyof photoperiod (Holloran and Wit-
teman, 1986).Harrigan (1972)observedthat water
motion triggered planula releasein P. damit'ornis
colonies held in static water, and suggestedthat
tidal currentsmay be responsible(seealso Stephen-
s o n , l 9 3 l ; M a r s h a l l a n d S t e p h e n s o n1, 9 3 3 ) .
Spawninghas beenartificiallyinducedin A,stran-
gia danae in the laboratory by stimulating corals
with extractsof gonadsof the oppositesex,and by
heat stress(Szmant-Froelichet al., 1980).Sperm
release by Caryophyllia smithi males apparently
inducesspawningby femalesin laboratory condi-
tions (Tranter et al., 1982).Whether gameterelease
by some members of populations acts to trigger
 BIOLOGY
CORALREPRODUCTIVE
epidemic spawning among other corals down-
current should be investigatedin natural coral
populations under normal field conditions. A
variety ofdisturbancesand stressfulconditionsare
known to induce planula releaseor premature
abortion of gametesor planulaein corals(reviewed
by Edmonson,1946;by Loya and Rinkevich, 1980;
by Fadlallah. 1983a;and by Brown and Howard,
r985).
Clearly,little is known about the factorsexerting
proximate control over reproductive activities rn
corals. Most of the ideas advanced to date are
basedon correlationsbetweenreproductiveactivi-
ties and environmental changes.As some of the
correlativeevidenceis conflicting,and correlation
does not prove causality. rigorous experimental
studies of possible proximate causal factors are
needed.Ideally thesestudiesshould be done using
a range of corals from different habitats and
regions.
Ultimate causesof breedingsynchrony
There are obvious advantagesfor synchronized
maturation and spawning of gameteswithin each
coral population, as this increasesthe probability
of fertilization and reducesgamete wastage,and
enhancesthe potential for outcrossingin self-fertile
hermaphrodites.Moreover, synchronizedbreeding
is essentialfor successfulreproduction in popula-
tions of gonochoric and self-infertilehermaphro-
ditic corals. Synchronized breeding periods in
specieswith brief annual spawning episodesare
potentially risky if spawning coincides with en-
vironmental perturbations.This was clearly dem-
onstrated when heavy rain destroyed buoyant
gameteson the water surface following a mass-
spawningevent on the Great Barrier Reef, thereby
negating the entire annual reproductive effort of
the spawningcorals (Harrison et a1.,1984).
The most unusual aspect of coral breeding
patternsis the synchronyof gametereleaseamong
many coral specieswhich occursin somelocalities.
The extent of the phenomenon suggeststhat the
advantagesof massspawningoutweigh the poten-
tial problems of conspecificgamete recognition
and wastage of gametes through hybridization,
and also overrideany ecologicaladvantageswhich
might be gained by partitioning breeding periods
(Harrison et al., l984; Wallace, 1985a). Yet
temporal reproductivepartitioning does occur rn
t7l
other localities,and is thought to enhancerepro-
ductive successby avoiding hybridization and
reducing competition for larval settlement sites
(Shlesingerand Loya, 1985). Reconciling these
contrastingbreedingpatternsand comparing ecol-
ogical characteristicsof different regions should
provide important clues to the ultimate causesof
coral breedingpatterns.
Two explanationshave been proposed for the
mass-spawningphenomenon. Firstly, it has been
suggested that environmental constraints limit
successfulbreeding times for many speciesto the
same few discreteperiods annually [for instance,
on the Great Barrier Reef. see Babcock et al.
(1986)1.As correlativeevidencefor this, breeding
times are less synchronous in regions where
physical factors such as tidal amplitude and the
annual range of sea temperatureare less extreme
(for instance, the Red Sea and the Caribbean:
Shlesingerand Loya, 1985;Babcock et al., 1986).
It has also been suggestedthat mass spawning
may have evolved as a response to predation
pressure(Harrison et al., 1984).Active predators
and filter feedersmay be satiated by an oversupply
of prey during the brief period of gamete release.
By spawning at the same time as other species,
each speciesloses proportionally less gametesto
predators,therebyincreasingits chancesof repro-
ductive success.This factor might also operate at
the larval settlement phase, where a risk of
predationexistsfrom benthic organisms,including
corals, as larvae drift onto a reef (Hamner et al.,
1988). A variety of animals have been observed
preying on coral spawn and planulae, including
planktivorous fish (Atoda, 1953; Simpson, 1985;
Babcock et al., 1986;Westneatand Resing, 1988),
ophiuroids (Szmant, 1986), crabs (P. Harrison,
unpublishedobservations),adult corals (Harrigan,
1972) and pelagic invertebrates (B. Willis, pers.
commun.).Babcocket al. (1986)suggestedthat the
risk from predators depending on vision is reduced
by spawning predominantly during periods of
darknessbetweendusk and moonrise.
Spawning and fertilization
Spawning and planula releasebehaviour
Gamete release has been observed in a great
variety of broadcast-spawningcorals. Prior to
spawningthe gametesare releasedfrom the gonads
t76
clear whether species-specific sperm chemotactic
responsesoccur in corals (R. Miller, pers. com-
mun.).
M a t u r a t i o n o l e g g sb y r e l e a s eo f p o l a r b o d i e s
h a s b e e no b s e r v e dw i t h i n 3 0 m i n u t e so f s p a w n r n g
in Goniastreu.fuvulus and several other faviid
s p e c i e s( B a b c o c k a n d H e y w a r d , 1 9 8 6 ; H e y w a r d
a n d B a b c o c k . 1 9 8 6 ) .W h e n s p e r m e n c o u n t e ra n
appropriate egg. they swim over the surface and
"clots"
s u b s e q u e n t l ya g g r e g a t et o f o r m s p e r m
( B a b c o c k a n d H e y w a r d , 1 9 8 6 ) .T h e s p e r m c l o t s
are similar to those describedin hydrozoans
( M i l l e r . 1 9 7 8 ,l 9 U l ) a n d c o n s i s to f l a r g en u m b e r s
of sperm which temporarily adhere head first to
the egg surface with their flagella orientated
perpendicularlybehind. In Gonictstrea asperueggs
the spermclots formed at the site of polar body
e m i s s i o n . a n d t h e c l e a v a g ef u r r o w w a s s u b s e -
q u e n t l y i n i t i a t e da t t h i s p o i n t , i n d i c a t i n gt h a t t h i s
was the sitc of fertilization (R. Babcock and
P . H a r r i s o n . u n p u b l i s h e d o b s e r v a t i o n s ) .D e t a i l s
of gamete interaction during fertilization and
s y n g a m ya r e n o t w e l l u n d e r s t o o d .U l t r a s t r u c t u r a l
s t u d i e sa r e n e e d e dt o d e t e r m i n ew h e t h e ra c t i v a t e d
s p e r m u n d e r g o a n a c r o s o m a l - t y p er e a c t i o n t o
f a c i l i t a t e f e r t i l i z a t i o n ( c o r a 1s p e r m l a c k a w e l l -
d e f i n e da c r o s o m e ;s e e p . I 5 9 ) . a n d w h e t h e r e g g s
e x h i b i t a c o r t i c a l r e a c t i o n i n r e s p o n s et o s p e r m
eggfusion.
Fertilization in intcrnally fertilized brooding
species is more difficult to observe. Eggs of
Astroides c'al.t'L'ulari.s. isoporan Acroporu species,
somc Porile.r'species. Bulanopht'llioelegon,s, B. pru-
i'otl and one Tuhu.strea speciesare fertilizedwithin
the mesenteries and developingembryos are envel-
oped by mesclgloeaand gastrodcrmis(De Lacaze-
D u t h i e r s .1 8 7 3 .1 8 9 7 ;F a d l a l l a ha n d P e a r s e 1 . 982a;
N. Goreau. pers. commun. in Fadlallah. 1983a;
Kojis. 1986a).Eggs ol Fuviu.frugunrand Porites
ustreoidesmay also be fertilized in .situor released
into thc polyp coelenteron for fertilization and
s u b s e q u c ndt e v e l o p m e n t( S z m a n t - F r o e l i c hc t a l . .
1 9 U 5C : h o r n e s k ya n d P e t e r s .1 9 8 7 ) .
Self- versuscross-fertilization
The majority of scleractiniancorals studied so
far are simultaneoushermaphroditesand rnany of
these release eggs and sperm together. which
il the gametes
createspotential for self-f'ertilization
are self-fertile.Laboratory experimcntswith gam-
P . L ,H A R R I S O N A N D C , C .W A L L A C E
etes frcm the same and different colonies have
shown a complete range of capabilities for self-
fertilization, from completely self-sterilecolonies
in speciesof Montipora (Heyward and Babcock.
1986; Heyward. 1986). through extremely low
incidenceof self-fertilizationin speciesof Auopora
(Heyward and Babcock, 1986: P. Harrison and
J. Oliver, unpublisheddata), to partially self-fertile
coloniesin Gonia.strea.favulus and G. aspera(Kojis
a n d Q u i n n , 1 9 8 1 ;H e y w a r d a n d B a b c o c k . 1 9 8 6 ) .
However, borh Goniaslreaspeciesexhibited mech-
anisms such as delay in polar body release,
separatereleaseof sperm,or delayedability to self-
fertilizewhich probably enhancecross-fertilization
in natural populations of these species(Heyward
a n d B a b c o c k ,1 9 8 6 ) .
The mechanismwhich preventsself-fertilization
in some speciesis unknown, but Heyward and
Babcock (1986) suggesteda self-recognitionre-
sponsemay be used to distinguishsibling gametes
from gametes of other colonies. In this case,
gameteswould exhibit the opposite responseto
that observedin adult tissues.which usually reject
" n o n - s e l f'
t i s s u e sd u r i n g t i s s u e - g r a f i i n gs t u d i e s
( s e ep . 1 8 3 ) .F u r t h e r w o r k o n t h e s e l f - f e r t i l i z a t i o n l
capabilities of other hermaphroditic corals arc
neededto determinewhether selfingis common in I
c e r t a i n s y s t e m a t i cg r o u p s o r c o r a l s w i t h s i m i l a r
l i f e h i s t o r i e s .S z m a n t ( 1 9 t 3 6 )s u g g e s t e dt h a t t h e
large sperm production in hermaphroditic corals
arguesagainst typical selfingin thcse species.and
representsa substantial effort to increase out-
crosslng.
Accessto mature gametesof many coral species
p r o v i d e se x c e l l e not p p o r t u n i t i e sf o r s t u d y i n go t h e r
aspectsof fertilization responsesin corals.Gamete
viability has been tested in four speciesand the
results indicate that gametes remain viable fbr
cross-fertilizationsup to 5 or 6 hours after
spawning. after which time the unfertilized eggs
b e g i nt o l y s e .I ' h i s i n d i c a t e st h a t c r o s s - f e r t i l i z a t i o n
of gametescould occur betweenadults separated
by considerabledistanceson reefs (Heyward and
B a b c o c k . 1 9 8 6 ) . F e r t i l i z a t i o n e x p e r i m e n t sa l s o
p r o v i d ea n i m p o r t a n t m e a n so f t e s t i n gt a x o n o r n i c
hypothesesbasedon skeletalmorphology through
ny b r i d i z a t i o n t e s t s o f g a m c t e s
c r o s s - f e r t i l i z a t i oh
from different species.or from diffcrcnt forms of
t h e c o r a l si d e n t i f i e da s t h e s a m es p e c i e s( H a r n s o n .
I988a).
 BE
C O R A LR E P R O D U C T I V IOLOGY
Embryogenesisand larval development
Considerable confusion has arisen in the
literature on coral reproduction over the terms
embryo and planula larva, which are used inter-
changeablyby some workers. In this chapter the
term embryo is restrictedto describingthe early
developmentof fertilized eggs up until the stage
wherethe epidermisbeginsto differentiateand cilia
form. at which stage the developingpropagule is
termed a planula.
Embryogenesis
Embryogenesishas been studied in a variety of
externally fertilizing species(Szmant-Froelichet
a l . . 1 9 8 0 ;K r u p p . 1 9 8 3 : H e y w a r d a n d B a b c o c k ,
1986; Heyward. 1986). Some information on
embryogenesisin brooding specieswith internal
fertilization is available from studiesof Acropora
(Isopora) (uneta, A. (l:;oporu) paliferu. Fuvia .fra-
gum. Manicina areolata, Prtrite.s astreoicles and
P . p o r i t e s ( W i l s o n , 1 8 8 8 ; S z m a n t - F r o e l i c he t a l . ,
1 9 8 5 ;K o j i s . 1 9 8 6 a ;C h o r n e s k ya n d P e t e r s ,1 9 8 7 ;
T o m a s c i ka n d S a n d e r ,1 9 8 7 ) .
Cleavageof externally fertilized eggs begins at
the site of polar body releasewithin I or 2 hours
after fertilization (Szmant-Froelichet al., 1980;
Babcockand Heyward, 1986).Cleavageoccursby
progressivefurrow formation (Fig. 7.13). and the
first division is complete, resulting in equal or
unequal sized blastomeres(Wilson, 1888;Krupp,
1 9 8 3 ;B a b c o c ka n d H e y w a r d . 1 9 8 6 ;K o j i s , 1 9 8 6 a ) .
Fadlallahand Pearse(1982a)suggestedthat initial
cell divisions in Balanophyllia elegans eggs were
probably superficial,while Uchida and Yamada
(1968) stated that superficialcleavageis common
in scleractinianembryos but provided no evidence
for this claim. The second cleavage plane is
perpendicularto the first. and cleavageis initially
radial. The blastomeresare subsequentlyrotated in
a pseudospiralformation. and cleavagebecomes
asynchronous(Szmant-Froelichet al., 1980; Bab-
cock and Heyward, 1986).Embryos subsequently
developinto a hollow blastulawhich flattensout to
become a concave dish that thickens and re-
develops into a spheroidal form (Babcock and
Heyward, 1986; A. Heyward and P. Harrison,
unpublishedobservations).
There is some disagreementover the mechanrsm
of endoderm formation in scleractinianembrvos.
In some species,gastrulation appearsto occur by
delamination (Wilson, 1888; Szmant-Froelich et
a l . , 1 9 8 0 ;S z m a n t - F r o e l i c he t a l . , 1 9 8 5 ) ,w h e r e a s
Uchida and Yamada (1968)concludedthat gastru-
lation in scleractiniansis generally achieved by
invagination.Babcock and Heyward (1986)found
evidenceof endoderm formation by invagination
in some corals, although delamination may have
occurred in one species.Detailed ultrastructural
studies of embryogenesisin broadcast spawning
and brooding corals would resolve this issue.
Embryogenesis subsequently involves partial
differentiation of the outer epidermis and the
formation of cilia leading to development of an
early planula stage.
Embryogenesisis rapid in externally developed
embryos,with ciliated larvae lorming 6 to 8 hours
after fertilization in A,strangia danae (Szmant-
F r o e l i c he t a l . , 1 9 8 0 ) ,a n d w i t h i n 1 4 t o 2 4 h o u r s i n
other broadcast-spawning species (Kojis and
Quinn, 1982aB ; a b c o c ka n d H e y w a r d , 1 9 8 6 ;B u l l ,
1986;Heyward, 1986;P. Harrison, unpublished
observations).Brooded embryos of Favia fragum
develop more slowly and take about four days to
develop into planulae (Szmant-Froelich et al..
I985).
Planula developmentand behaviour
In externally developedplanulae, an oral pore
and pharynx form by invaginationof the ectoderm
within 24 hours after fertilization (Szmant-Froe-
lich et al., 1980; Krupp, l983; Babcock and
Heyward, 1986). Between 24 and 36 hours, a
coelenteronforms and the partially differentiated
endoderm is separated from the ectoderm by a
layer of mesogloea(Babcock and Heyward, 1986).
Larvae are initially spheroidaland spin about their
axis near the water surface. but with further
developmentthey become mobile pear-shapedor
barrel-shaped planulae (Fig. 7. I ), and swim
throughout the water column (Szmant-Froelichet
al., 1980; Babcock and Heyward, 1986). Subse-
quent developmentinvolvescellular differentiation
of the epidermis and gastrodermis, and the
lormation of mesenteries prior to settlement
( S z m a n t - F r o e l i c he t a l . , 1 9 8 0 ; K o j i s a n d Q u i n n ,
198l; Babcock and Heyward, 1986). Planulae
become elongated and increasingly active with
time, and begin demersalswimming and benthic
searchingbehaviour (seep. 189)within 3 to 7 days
CORALREPRODUCTIVE
BIOLOGY
p. 184). In some cases,planulae are releasedat a
variety of developmentalstages(Duerden, 1905;
A b e , 1 9 3 7 :H a r r i g a n , 1 9 7 2 ;L e w i s , 1 9 1 4 a lR' i n k e -
vich and Loya, 1979a) which may delay the
settlementof some larvae. Rinkevich and Loya
(1979a) found that St.vlophora pistillata planulae
settledonly when they had developedsix pairs of
complete mesenteries.Larvae of other brooding
and broadcast-spawningspecieshave also been
observedto delay settlementuntil three or more
pairs of complete mesenterieshave formed, al-
though larvae of a few speciesare able to settleat
an earlier stage of development(Duerden, 1902a;
A b e . 1 9 3 7 ; A t o d a . 1 9 5 3 ; S h l e s i n g e ra n d L o y a .
r9 8 5 ) .
The morphology, structure and behaviour of
mature coral planulae have been extensivelystud-
ied in brooding species(see,for instance,Duerden.
1902a;Atoda. 1953; Harrigan, 1972; and Fadlal-
l a h , 1 9 8 3 a ) . M o s t s c l e r a c t i n i a np l a n u l a e h a v e
similar basic morphological and behavioural
characteristics,regardless of whether they are
brooded or develop externally, and sexually or
asexuallyderived.They are generallydescribedas
pyriform, barrel-shaped,spheroidal.cigar-shaped
or elongated,and are capable of changing shape
rapidly (see.for instance.Duerden, 1902a;Mavor,
l 9 l 5 ; A b e . 1 9 3 7 ;K a w a g u t i , l 9 4 l a ; A t o d a , 1 9 5 3 ;
H a r r i g a n , 1 9 7 2 ) .B r o o d e d p l a n u l a ea r e g e n e r a l l y
larger than externally developed planulae. The
smallest planulae recorded are produced by the
broadcast-spawningcoral Astangia danaeand are
75 pm in diameter, while the largest planulae are
brooded by Mvcetophl'lliaferox and grow to 3 mm
i n d i a m e t e r ( S z m a n t - F r o e l i c h ,1 9 8 4 ; S z m a n t ,
r9 8 6 ) .
Planulae of many brooding specieshave been
describedin detail histologically(see,for instance,
Wilson, 1888D ; u e r d e n ,1 9 0 2 a .1 9 0 4 ,M a v o r . 1 9 1 5 ;
E d m o n d s o n " 1 9 2 9 , A t o d a . 1 9 5 3 ) ,w h i l e B a l a n o -
p h1,11io r eg i a, Car t,op hvI lia smit hi, P oci IIop ora clant-
icornis and Porites porites planulae have been
studiedultrastructurally(Lyons. 1973a,b; Vander-
meulen, 1974, 1975,Goreau and Hayes, 1977;
H a y e s a n d G o r e a u , 1 9 7 7 a . b ,d ; K i n c h i n g t o n .
1980, 1982). Mature planulae have an outer
epidermis, a central layer of mesogloea,and an
inner layer of gastrodermislining the coelenteron
and mesenteries. The epidermiscontainselongated
columnar eoithelial cells that are ciliated or
179
flagellated,mucouscells,and a variety of secretory
gland cells, nematocystsand spirocysts.The epi-
dermis also containspigment granules(Kawaguti.
1944; Fadlallah and Pearse, 1982a) and basal
muscle filaments adjacent to the mesogloea(Ed-
m o n d s o n , 1 9 2 9 ,L y o n s , 1 9 7 3 b ) .T h e e p i d e r m i so f
C1,-phastrea ocellina planula has numerous, small
"pearly
white vesicles" of unknown function
( E d m o n d s o n ,1 9 2 9 ,1 9 4 6 ;W r i g h t , 1 9 8 6 ) .
In planulae of many species,the aboral epider-
mis is thickened and contains a complex "nerve
cell" layer beneaththe columnar epithelium (Wil-
son, 1888; Duerden, 1902a, 1904, 1905; Atoda,
1953). Ultrastructural analysis of this region in
Poc'illoporadamicornis larvae showed evidence of
neurosecretoryactivity in the basal ramifications
ofoverlying flagellated"sensory" cells,but discrete
nervecellswere not present(Vandermeulen,1974).
The aboral epidermis is thought to play an
important role in substratumsearchingand testing
behaviour by planulae(seep.189). The aboral
epidermis of Astrangia danae, Carvophvllia sntithi
and Stylophora pistillata planulae develop apical
ciliary tufts, blister-likeswellingsor noduleswhich
may also aid settlement (Rinkevich and Loya,
1 9 7 9 aS ; z m a n t - F r o e l i ceht a l . , 1 9 8 0 ;T r a n t e r e t a l . ,
I 982).
The stomodaeum and mesenterial filaments
contain a variety of epidermalcell types,while the
gastrodermalcells are spheroidalor polygonal in
shape and contain numerous lipid bodies and
i n c l u s i o n s( W i l s o n , I 8 8 8 ; A t o d a . 1 9 5 3 ; L y o n s ,
1 9 7 3 b ;V a n d e r m e u l e n .1 9 7 4 ) .Z o o x a n t h e l l a ea r e
usually present in the gastrodermis of brooded
planulae.and may be aggregatednear the oral pole
or along the mesenteries, or uniformly distributed
t h r o u g h o u t t h e e p i d e r m i s( D u e r d e n , 1 9 0 2 a ) .A l -
though zooxanthellaeare exclusivelygastrodermal
in adult corals, some brooded planulae have
zooxanthellaein the oral region of the epidermrs
( D u e r d e n .1 9 0 2 ;M a t t h a i . l 9 l 9 ; K a w a g u t i , 1 9 4 1 a :
Atoda, 1951b).Euphylliaglabresc'ens planulae are
u n u s u a l i n h a v i n g z o o x a n t h e l l a em a i n l y i n t h e
e p i d e r m i s( K a w a g u t i . 1 9 4 1 a )B . r o o d e dp l a n u l a eo f
isoporan Acropora speciesand non-zooxanthellate
coralsdo not contain zooxanthellae.and are often
brightly pigmented (De Lacaze-Duthiers, 1873;
Atoda, 1951aF ; a d l a l l a ha n d P e a r s e 1 , 9 8 2 aK ; ojis.
1986a).Externally developedplanulae also gener-
a l l y l a c k z o o x a n t h e l l a e( K o j i s a n d Q u i n n , 1 9 8 1 ;
lE0
B a b c o c ka n d H e y w a r d . 1 9 8 6 ) e , x c c p tf o r p l a n u l a e
ol Montiporu ttnd Poritesspeciesthat developfron.r
e g g sc o n t a i n i n gz o o x a n t h e l l a eZ. o o x a n t h e l l a eu p -
take was observedin Fungiu.st'uturiuplanulae4 or
5 d a y s a f t e r f e r t i l i z a t i o n( K r u p p . 1 9 8 3 ) .
Abnorrnal. deformed planulac have bccn ob-
s e r v e di n s o m e b r o o d i n g a n d b r o a d c a s t - s p a u n i n g
corals (De Lacaze-Duthiers. | 873; Duerden.
1902a;Abe, 1931: Kawaguti. l94lb; Atoda.
1 9 4 1 a .l 9 5 l b : H a r r i g a n . 1 9 1 2 : P . H a r r i s o n . u n -
p u b l i s h e d o b s e r v a t i o n s ) .T h e y a r c c o m m o n l y
t w i n n e d p l a n u l a ew i t h a d o u b l e o r a l r e g i o n o r a
bifurcated aboral region. Twinned planulae of'
Pot'illoporu dunrit'orni.s have been observed to
settle and metamorphose successfully (Reed.
1971).although at a slightly lower rate than
n o r m a l p l a n u l a e( H a r r i g a n . 1 9 7 2 ) .
M o s t p l a n u l a e a r e a c t i v e s w i m m e r s .a n d n o r -
mally swim with their aboral end forward while
rotating about their longitudinal axis. Various
c a t e g o r i e so f s w i m m i n g b e h a v i o u r h a v e b e e n
describedincluding: straight swimming, swimming
w i t h d i p s , d o w n w a r d o r u p w a r d s w i m m i n g .c i r -
c l i n g , s t o p p i n g ,s p i r a l l i n g ,s p i n n i n g ,s w a y i n ga n d
r e v e r s i n g( A b e . 1 9 3 7 A ; t o d a . 1 9 5 3 ;H a r r i g a n ,1 9 7 2 ; .
Rinkevich and Loya. 1979a).In contrast, Balano-
pht'llio elegansproducesbenthic crawling planulae
w h i c h d o n o t s w i m ( G e r r o d e t t e ,l 9 8 l ; F a d l a l l a h
and Pearse,1982a).Astroidescalycularis.Buluno-
phvllia regiu and Tuba.streaf uulkneri produce
similar large crawling planulae. although these
m a y n o t b e s t r i c t l yb e n t h i ca s s o m c p l a n u l a eh a v e
been observedswimming in aquaria (reviewedin
Fadlallah and Pearse.1982a:see also De Lacaze-
D u t h i e r s , 1 8 9 7 ;K i n c h i n g t o n ,1 9 8 2 ;T r a n t e r e t a l . ,
1 9 8 2 ;B a b c o c ke t a l . . 1 9 8 6 ) .
I n t h e l a b o r a t o r y , b r o o d e d p l a n u l a ee x h i b i t a
strong tendencyto swim to the water surfaceafter
releasefrom their parent polyp (see.for instance.
D e L a c a z e - D u t h i e r s1, 8 7 3 ; D u e r d e n . 1 9 0 2 c ;E d -
m o n d s o n ,1 9 2 9A . b e , 1 9 3 7A ; t o d a . 1 9 5 3H : arrigan.
1 9 7 2 ;L e w i s . 1 9 7 4 a S ; z m a n t - F r o e l i c eh t a l . . 1 9 8 5 ) .
Later they reverse this behaviour and swlm
throughout the water column or becomedemersirl
or benthic. This behaviour is usually attributed to
changing phototactic and geotactic responsesby
the planula, however, in most cases the taxic
responsesof the planulae have not been tested
e x p e r i m e n t a l l y .K a w a g u t i ( 1 9 4 1 a ) s t u d i e d t a x i c
responses in planulae of Acrhelia horrescens.
P.L. HN RRISON ANI) C"C. WALLA(]E l
l
Euph.vlliugluhresL'en.s. PoLilloporu duntit'ornis and
Seriutopora/l,r'.i/ri.v. and found evidenceof'photo-
t a x i s ,g e o t a x i s t. h i g m o t a r i s .a n d r h e o t a x i si n s k r w
c u r r c n t s .A l l p l a n u l a ee x h i b i t e dn e g a t i v eg e o t a x i s .
a n d w e r e p o s i t i v c l y p h o t o t a c t i cw i t h i n a c e r t a i n
r a n g eo f l i g h t i n t e n s i t y .b u t b e c a m cp h o t o n e g a t i v e
i n h i g h c r l i - s h t i n t e n s i t i e s .P h o t o t a x i c r c s p o n s e s
varied between species.and thc responsescorre-
latedwell with the distribLrtion and conccntration
o f z o o x a n t h e l l a ei n t h e p l a n u l a c .a s w e l l a s t h e
observeddistribution of adult corals of each
s p e c i e si n t h e f i e l d . K a w a g u t i ( 1 9 4l a ) c o n c l r , r d e d
t h a t t a x i c r e s p o n s eosf p l a n u l a ep l a y a n i m p o r t a n t
r o l c i n t h e s c t t l c m c na t n c ld i s t r i b u t i o no f c o r a l so n
reefs.
T h e c h a n g ei n v c r t i c a ld i s t r i b u t i o no f d e v e l o p i n g
embryos and planulacwithin the water column
o v e r t i m e m a y a l s o b e i n f l u e n c e db y c h a n g e si n t h e
locomotory powcrs and buoyancyol the larvae
d u r i n g d e v e l o p m e n t .F o r e x a m p l e . R i c h m o n d
(1987) fbund that buoyant Pocilloporutluntitornis
p l a n u l a ew h i c h r e m a i n e dn e a r t h e w a t e r s u r f a c e
c o n t a i n e dl 7 % om o r e l i p i d t h a n p l a n u l a es w i m m i n g
n e a rt h e b o t t o n -or f a q u a r i a .P r e l i m i n a r ys t u d i e so n
I
t h e v e r t i c a l d i s t r i b u t i o n o f ' c o r a l p l a n u l a ei n t h e I
p l a n k t o n s u g g e s tt h a t p l a n u l a e o l ' s o m e s p e c i c s
may undergo diurnal vertical migration. but
further researchis neededto confirm this (Kawa-
g u t i . 1 9 4 0 b ;H o d g s o n , 1 9 8 5 ab. ) .
V e r y l i t t l e i s k n o w n a b o u t t h e p h y s i o l o g yo f
c o r a l p l e i n u l a e .P l a n u l a e c o n t a i n s t o r e d e n e r g y
reservesthat may be supplementedby transloca-
t i o n o l m e t a b o l i t e sf r o m s y m b i o t i cz o o x a n t h e l l a e .
and planktonic leeding in planktotrophic forms.
Pocilloporudunricornisplanulae contain wax and
sterol estersand triglycerides.and lipid levels of
p l a n u l a e d e c r e a s eo v e r t i m e ( R i c h m o n d , 1 9 8 7 ) .
Por'Illoporuduntit'ornisplanulaealso contain abun-
d a n t z o o x a n t h e l l aw e h i c ha r ek n o w n t o t r a n s l o c a t e
m e t a b o l i t e st o t h e l a r v a l t i s s u c s( R i c h m o n d . 1 9 8 7 ) .
Respirometrymeasurementsindicate that oxygen
production by photosynthesis of zooxanthellae
m a y b e g r e a t e r t h a n t h e d a i l y c o n s u r n p t i o no f
oxygen through respirationin Type Y P. tlonticor-
n i s p l a n u l a ef r o m H a w a i i a n d t h e M a r s h a l lI s l a n d s
( R i c h m o n d , 1 9 8 7 ) .H o w e v e r , o x y g e n p r o d u c t i o n
by zooxanthellaephotosynthesiswas lessthan the
d a i l y c o n s u m p t i o n o l o x y g e n b y r e s p i r a t i o no f
planulaeof P. dunrit:orni.s and Poritesspeciesfrom
t h e G r e a t B a r r i e rR e e f( M a r s h a l l .1 9 3 2 ) .
CORALREPRODUCTIVE
BIOLOGY
Cart'ophl'llia sntithi planulae exhibit a complex
feedingbehaviourwhich commences48 hours after
f e r t i l i z a t i o n( T r a n t e r e t a l . . 1 9 8 2 ) .M u c u s s t r i n g s
are trailed behind the planula while swimming,and
food particlestrapped in the mucus are gradually
drawn into the mouth. When feedinghas finished,
the planula disengagesfrom the mucus string by
rotating rapidly until the string breaks. In the
absence of a mucus string, food particles are
passedacrossthe surfaceof the epidermisand into
the mouth by ciliary currents(Tranter et al., 1982).
Particulatematter has been observedmoving into
the oral pore of C1'phastrea oc'ellina planulae
(Wright, 1986),and Pot'illoporadanticornisplanu-
lae are capable of developing into a planktonic
p o l y p w i t h t e n t a c l e s( R i c h m o n d , 1 9 8 5 a ) ,w h i c h
suggeststhat these planulae are able to feed.
Zooxanthellae translocation and planktotrophy
may considerably enhance the longevity and
dispersal potential of some coral planulae (see
p . 1 8 7 ) . F a d l a l l a h ( 1 9 8 3 a ) s u g g e s t e dt h a t c o r a l
planulae may also be able to utilize dissolved
o r g a n i cm a t t e r a s a s o u r c eo l n u t r i t i o n .
ASEXUALREPRODUCTION
In addition to sexual reproduction, various
asexualprocessesof reproductioncan result in the
formation of new coloniesor solitary corals.These
include fragmentation of established colonies,
budding and transverse or longitudinal fission,
single polyp bail-out (see below, p. 182), detach-
ment of groups of polyps as drifting polyp balls,
and asexually produced planulae (Scheer, 1959;
Wells, 1966; Rosen and Taylor, 1969; Fadlallah,
1 9 8 2 ;S a m m a r c o .1 9 8 2 a S
; t o d d a r t ,1 9 8 3 ;A y r e a n d
Resing. 1986).The diversity of reproductivemeth-
ods employed by corals and other anthozoans
(reviewedby Chia, 1976;seealso Walker and Bull,
1983;Dinesen,1985)is testamentto the extraordi-
nary plasticity of cnidarian tissues(reviewed by
Campbell, 1974b),and it seemslikely that other
modes of asexual propagation remain to be
discovered.As the biological and ecological as-
pects of reproduction by fragmentation, lission,
and polyp balls in corals have been reviewed
elsewhere(Highsmith, 1982), this discussionem-
phasizesother recent developmentsin studies of
asexualreoroduction in corals.
l8l
Asexual production of planulae
Brooding of planula larvae by scleractinian
coralshas traditionally been regardedas a form of
sexualreproduction resulting from internal fertili-
zation and developmentof eggs.A sexual origin
for brooded planulae has been confirmed by
isoenzymeelectrophoresisof Acropora palifera and
Seriatopora hystrir planulae (Ayre and Resing,
1986),and inferred from observationsof develop-
ing embryos within polyps of Ac'ropnracuneata,
A. palifera, Favia fragum, Manicina areolata, Tu-
bastrea sp. and five Porites species from the
Caribbean (Wilson, 1888; Szmant-Froelichet al.,
1 9 8 5 ;K o j i s , 1 9 8 6 a ;C h o r n e s k ya n d P e t e r s ,1 9 8 7 ;
Tomascik and Sander, 1981; N. Goreau pers.
commun. in Fadlallah, 1983a).However, electro-
phoreticstudieshave shown that brooded larvaein
three coral speciesare produced asexually.
Brooded planulae of Pocillopora damicornis
from reefs in Western Australia and Hawaii were
shown to be geneticallyidentical to their brood-
parents, indicating that the planulae were pro-
duced asexually (ameiotically) (Stoddart, 1983,
1986).Similar resultswere obtained from electro-
phoretic studies of brooded larvae and adults in
this speciesfrom the Great Barrier Reef (Muir,
1984)and in the non-zooxanthellatecorals Tuhas-
traea coccinea and T. diaphana (see Ayre and
Resing, 1986).Brooded planulae in the anemones
Actinia equina and A. tenebrosawere also found to
be geneticallyidentical to their parents (Ottaway
a n d K i r b y , 1 9 7 5 ;B l a c k a n d J o h n s o n , 1 9 7 9C
; arter
and Thorpe, 1979;Orr et al., 1982).Consequently,
brooding by anthozoanscan no longer be assumed
to be an exclusivelysexualprocess.
While the existenceof asexuallyproducedlarvae
has been establishedfor some corals, their origin
remainsa mystery. Stoddart (1983)suggestedthat
asexual planulae rn Pocillopora damicorms may
develop by budding or parthenogenesis. Intensive
histologicalstudiesof gametogenesis and planula
development have produced conflicting interpreta-
tions. Martin-Chavez(1986)concludedthat planu-
lae in P. damicornis colonies from Hawaii origi-
nated from internal parthenogenetic development
of oocytes. In contrast, studies of P. damicornis
from Western Australia and the Great Barrier Reef
suggestthat gametesdo not play a role in asexual
planula development becauseplanulae appeared
182
before gametesmatured during some gametogenic
cycles,planulae sometimesdeveloped in the ab-
sence of oogenesis, and developmental stages
connectingeggs and planulae were not observed
( M u i r . 1 9 8 4 ;S t o d d a r ta n d B l a c k . 1 9 8 5 ) .
Muir (1984) proposed an alternativeorigin for
the brooded planulae in Pocillopora tlami<:orni:;
whereby planulae develop from lipid storage
bodieswhich are budded from the polyp pharynx
(seeStimson, 1916).Thesepharyngeallipid bodies
are of similar form and histologicalstructureto the
earliest planula stages observed and. unlike the
oocytes,their developmentand cellular differentia-
tion coincides with the appearance of early
planulaein Great Barrier Reef populations(Muir,
1984). Although definitive developmental stages
linking the lipid bodiesand early planulaehave not
been observed(Muir, 1984),planula tissuecould
develop quite rapidly from dedifferentiation,mi-
gration and redifferentiationof parentalgastroder-
mal tissue(seeHaynes and Burnett, 1963;Camp-
bell, 1974b).If gametesdo not play a role in the
production of brooded planulae in P. damicorni.s,
the development and abrupt disappearanceof
gametes during lunar cycles of gametogenesis
indicatesthat they are either spawnedfor external
fertilization or rapidly resorbed.It is ironic that,
despitereproductionhaving beenmore extensively
studied in Pocillopora damicorni.sthan in any other
coral. the roles of gametogenesis, sexualreproduc-
tion, and the origin of its brooded planulaeremaln
enigmatic.
Asexual production of brooded larvae in some
other corals and anemones is also thought to
involve some form of budding or somatic embryo-
g e n e s i s( G a s h o u t a n d O r m o n d , 1 9 1 9 ;O ' rr et al..
1 9 8 2 ;A y r e a n d R e s i n g , 1 9 8 6 ) .T h e s eh y p o t h e s e s
seem quite credible in the light of the bizarre
brooding habits of the anemone Bunodettp.si.t
ntetlusoitle,;.In this species, tentacle tips are
thought to be occasionallyautotomized and in-
gested during leeding. and subsequentlydevelop
into juvenile anemoneswhile brooded within the
coelenteron(Cutress,1979).Further electrophore-
tic studies are neededto determine the sexual or
asexualorigin of brooded planulaein other corals.
Studies on brooding corals in which developing
embryos have not been observed (e.g. Astroides
calyculuri.s'. De Lacaze-Duthiers,I 873),and species
in which both spawning and brooding modes of
P . L . H A R R I S O N A N D C ] . C ]W
. ALLACE
I
T
developmenthave beenreported(Table 7.6) would
be particularly worthwhile.
I
Polyp bail-out
Another recently reported form of asexual
reproduction, termed "polyp bail-out" (Sam-
marco, 1982a), involves the dissociation and
dispersal of coral polyps from adult colonies.
Under unlavourablelaboratory conditions,polyps
from colonies of Seriatopora h1'strir became
isolated,detachedfrom their calices,and in a few
instancesre-attachedand secreteda new skeleton
( S a m m a r c o .1 9 8 2 a ) A . lthough bail-outwas prim-
arily induced in laboratory and field experimentsin
responseto stress,dissociationof S. h r'.rlru.r polyps
was also observedto occur naturally in the Great
Barrier Reef on a number of occasions.Sammarco
( 1 9 8 2 a )s u g g e s t e dt h a t p o l y p b a i l - o u t m a y h a v e
contributed to the dominance of this speciesin
some shallow reef biotopes,but geneticstudiesof
S. h-vstrixpopulations on the Great Barrier Reef
show little evidenceof asexualrecruitment(Resing
and Ayre, 1985).Polyp bail-out was inferred in the
recruitment of juveniles of Pocilloporaspp. in the
easternPacificfrom nearby non-reproductivecolo-
nies which were stressedby predation (Richmond,
1985b).A similar processto polyp bail-out from
adult colonies has been observedduring demeta-
morphosis and resettlementof polyps in juvenile
c o r a l s o f s o m e s p e c i e s( R i c h m o n d , 1 9 8 5 a ; s e e
p. 191).
Extent of asexual reproductionin coral
populations
Asexual reproduction in many scleractinian
speciesresults in the proliferation of successful
genotypesas physically separatedindividuals or
clones: but it is dilicult to assessthe extent and
importance of cloneswithin natural coral popula-
tions. Observationson breakage,recruitment and
survival of coral fragments have shown that
fragmentation is an important form of asexual
reproduction in some reef corals (Gilmore and
H a l l , 1 9 7 6 ;H i g h s m i t h , 1 9 8 0 , 1 9 8 2 ;H i g h s m i t h e t
a l . , 1 9 8 0 ;T u n n i c l i f f e ,1 9 8 1 :B o t h w e l l , 1 9 8 2 ;W a l -
lace. 1985a)but other forms of reproduction and
recruitment are less obvious. and the relative
contribution of the various asexual and sexual
CORALREPRODUCTIVE
BIOLOGY
modesof reproductionto the geneticstructureand
maintenanceof coral populations is largely un-
known. Owing to the difliculty of visually identify-
ing clonal lineageswithin coral populations.recent
studieshave used severalindirect methods includ-
ing histo-compatibilityresponsesof grafted tissue
and isoenzymeelectrophoresisto test for clonal
population structureson reefs.
The applicationof tissue-grafting bioassaysto the
study of clonal structurewithin coral populationsis
"self-recognition"hypothesiswhich
based on the
assertsthat scleractiniancorals possessa preclse
immuno-recognitionsystemcapableof discrimrnat-
ing betweengeneticallydistinct tissues(Hildemann
et al., 1977).Accordingly,tissuefusionshouldoccur
only in allografts of tissuesfrom individualswith
identical genotypes. while allograft rejection re-
sponsesdenote different genotypes.
Studies using tissue-graftingtechniques have
indicatedthat significantclonal replicationexistsin
populations of various arborescentAcropora spp.,
two Montipora species and Porites compre.\sa
( B o t h w e l l , 1 9 8 2 ;J o k i e l e t a l . . 1 9 8 3 ; N e i g e l a n d
A v i s e , 1 9 8 3 ;H e y w a r d a n d C o l l i n s , 1 9 8 5 b ;H u n t e r
and Kehoe, 1986). These results need to be
interpretedcautiouslybecausemore recent studies
in five coral specieshave shown that tissuesfrom
electrophoreticallydistinct genotypesare in fact
capable of fusing (Heyward and Stoddart. 1985;
R e s i n ga n d A y r e , 1 9 8 5 W ; i l l i s a n d A y r e , 1 9 8 5 )T
. he
"self-recognition" hypothesis has
therefore been
rejected in most corals in which tissue-grafting
responseshave been independently tested with
isoenzyme electrophoresis.Consequently, histo-
compatibilitycriteriacannot be assumedto reliably
indicateclonal identity, and should not be usedas
evidencefor geneticstructurein coral populations
without independent verification (Heyward and
Stoddart, 1985;Resingand Ayre. 1985;Stoddartet
al., 1985W ; i l l i s a n d A y r e . 1 9 8 5 )H . isto-compatibil-
ity responseswere of use, however. in identifying
clone-matesin Porites ('ontpressa, where the genetic
identity of clonal morphotypes.distinguishedby
visual censusand allograft fusions,was confirmed
by electrophoresis and ultravioletchromatography
(Hunter, 1985).In addition. tissue-graftingstudies
proved useful in three coral species.where allograft
rejectionswere able to discriminatebetweenelectro-
phoreticallyindistinguishable colonies(Resingand
Avre. 1985).
183
Electrophoreticsurveyshave shown that sclerac-
tinian populations show a range of genotypic
structure,from predominantly clonal populations
maintained by extensivelocalizedasexualrecruit-
ment, to essentiallyaclonal populations resulting
primarily from sexual reproduction and recruit-
ment. Pocillopora damicornis populations have
been studied extensively,and are typically domi-
nated by a few prolific genotypeswhich account
for up to 80% of colonies, with various other
genotypesrepresentedby one or a few individuals
( S t o d d a r t ,1 9 8 3 ,1 9 8 4 a ,1 9 8 6 ) .T h i s , t o g e t h e rw i t h
the dominanceof residentadult genotypesamong
first-year recruits, indicatesthat localizedasexual
proliferation of clones plays a major role in the
maintenanceof thesepopulations(Stoddart, 1983,
1984a,b). Although some form of sexual repro-
duction in P.damicornls is apparent from the
pooled gene frequenciesand diversity of coral
genotypes,sexualrecruitmentis limited and varies
considerablybetweensites(Stoddart, 1983,1984a).
Similar, predominantly clonal population struc-
tures have been observedin Pavonacactus.PLtrites
compressoand Tubastreat:occinea(Hunter, 1985;
W i l l i s a n d A y r e , 1 9 8 5 ;A y r e a n d R e s i n g , 1 9 8 6 ) ,
while some replication of clonal genotypes was
apparent in populations of Montipora dilatata,
Porites cylindrica and P. nigre.scens (Heyward and
Stoddart, 1985; Resing and Ayre, 1985). By
contrast,patternsofgenotypic diversityin popula-
tions of Acropora pali/bra, Seriatopora h1'strir and
St1'lorToro pi.stillata indicated that these popula-
tions were dependenton sexual recruitment, and
showedlittle or no evidenceof a clonal population
structure (Resing and Ayre, 1985; Ayre and
Resing, 1986).Further electrophoreticstudiesare
needed to determine whether these patterns are
representativeof populations in other locations
and habitats, to allow the life-history patterns of
these speciesto be better assessed.Comparative
studiesof populations would also provide impor-
tant information on genetic differentiation, gene
flow and larval dispersal among populations
( S t o d d a r t ,1 9 8 4 b ) .
LARVAL DISPERSAL
Most marine benthic invertebrateshave a pe-
lagic larval phase in their life history (Thorson,
I li4
1 9 6 1 ,1 9 6 4 D : o y l e . 1 9 7 5 )P . e l a g i cl a r v a ep r o v i d ea n
important meansof dispersalin otherwisesessileor
sedentaryspccies.and enablecolonization of ncw
habitats. recolonization following local extinc-
tions, and genetic exchangebetwecn populations
( T h o r s o n . 1 9 6 1 ; S c h e l t e r n a .l 9 l 1 : G e r r o d e t t e .
l98l). The planula larvae of most scleractiniln
coralsspendsome time in the water column before
settling;however.the cxtent of dispersalby coral
larvae is poorly known. and is the subjectof some
controversy.
Debate over the dispersalcapabilitiesof coral
planulae currently centresupon two issueswhich
operate at different spatial scales. There are
opposing views as to whether planulae are pri-
marily retained on their natal reel or disperscd
betweenreefs.Corollaries of theseviews arc that
reefsare either primarily self-seeded (Done, 198221
S a m m a r c oa n d A n d r e w s .1 9 8 8 ) .o r i n t e r c o n n e c t e d
and interdependentfor larval recruits(Harrison et
a l . , 1 9 8 3 .1 9 8 4 :W i l l i a m s e t a l . . 1 9 8 4 ;B a b c o c ka n d
Heyward. 1986).On a broader geographicalscale.
considerablecontroversy exists over the potential
for long-distancedispersalby coral larvae and its
biogeographic importance, particularly with re-
gard to the origin of the easternPacificcoral fauna
( D a n a , 1 9 7 5 ;H e c k a n d M c C o y . 1 9 7 8 ;R i c h m o n d .
I987).
Dispersal potential and scalesof dispersionof
coral planulae
Coral planulae have limited powers of move-
ment. Averageswimming ratesmeasuredin planu-
I (Abe,
lae of six speciesrange from I to 5 mm s
1 9 3 7 ;M o t o d a . 1 9 3 9 ;A t o d a . 1 9 4 7 a ,l 9 5 l a . b . c ;
Harrigan. 1912). A faster swimming rate
(1 3 cm s t) was reported for planulae of Caryo-
pht'llia sntithi during early development, but loco-
motion decreased with subsequentgrowth (Tranter
et al., 1982)A . v e r a g es w i m m i n gs p e e d so f p l a n u l a e
are orders of magnitude slower than the current
velocities likely to be encounteredduring their
p e l a g i c e x i s t e n c e( H o d g s o n , 1 9 8 5 a ;W a l k e r a n d
C o l l i n s . 1 9 8 5 ;W o l a n s k i a n d P i c k a r d , 1 9 8 5 ;W o l -
anski et al., 1986), hence coral planulae are
essentiallypassivemeroplanktonic larvae. Conse-
quently, their dispersionand settlementpatterns
will be largely determinedby the duration of the
planktonic phase.the prevailinghydrologicalcon-
P.L. HARRISON ANI) C,C. WALLAC'E
d i t i o n s .t h e c o m p e t e n c vp e r i o d ( . i e n . i rC h i a . 1 9 7 8 )
o f t h e p l a n r . r l a ea.n d t h e i r v e r t i c a ld i s t r i b u t i o n i n
t h e w a t e r c o l u m n . B e c a u s eo f t h e d i l i l c u l t i e s
i n v o l v e d i n o b s e r v i n gl a r v a l d i s p e r s a li n n a t u r e .
d i r e c ti n f o r m a t i o ni s l i m i t e d .I n m o s t c o r a l s .l a r v a l
d i s p e r s apl a t t c r n sh a v e u s u a l l yb e e ni n f e r r e df r o m
p l a n u l a b e h a v i o u ra n d s e t t l c m c n t i m e s i n l a b o r a -
t o r y s t u d i e so. r f r o m p a t t e r n so f l a r v a l r e c r u i t m e n t
o r a d u l t d i s t r i b u t i o n ( s c c . f b r i n s t a n c e .L e u ' i s .
1 9 7 4 ab. ) .
Dispersalpatternsof planulae
Brooded planulae are usually releasedat an
advanceddevelopmentalstagcand may alreadybe
competent to settle. whereasthe entirc larval
developmentalphase of broadcast-spawningspc-
cies is spent in the plankton. Thesecontrlrsting
d e v e l o p m e n t a lp a t t e r n s i n f l u e n c e t h c m i n r m u m
p l a n k t o n i c p e r i o d u n t i l s e t t l e m e n ta
. nd result in
somewhat different patterns of larval dispersalin
brooding versusbroadcast-sparvning corals.
Broodedplanulae
Brooded coral planulae exhibit a range of
s e t t l e m e ntti m e s i n t h e l a b o r a t o r y .b u t m o s t s c t t l c
q u i c k l y a f t e r r e l e a s ef r o m t h c i r p a r e n t p o l y p
( H a r r i g a n . 1 9 7 2 ;F a d l a l l a h .1 9 8 3 a t. a b l c l ) . S e t t l e -
ment within a few hours of release has been
observedin some planulae. while the majority of
v i a b l e b r o o d e d p l a n u l a eu s u a l l ys e t t l ew i t h i n o n e
o r a f e w d a y s o f r e l e a s c ( D u e r d e n . 1 9 0 2 ac. ;
Vaughan. l9l0; Mavor. l9l5; Boschma. 1929:
S t e p h e n s o n1. 9 3 1 ;A b e . 1 9 3 7 ;A t o d a . 1 9 4 7 ab. ,
l 9 5 l c ; H a r r i g a n . 1 9 7 2 ; L e w i s , 1 9 7 , 1 aR ; inkcvich
a n d L o y a . 1 9 1 9 a lG ' errodette. 1981: Kojis and
Q u i n n . 1 9 8 2 a ;T r a n t e r e t a l . , 1 9 8 2 ;V a n M o o r s e l ,
1 9 8 3 ; R i c h m o n d . 1 9 8 5 a . 1 9 8 7 ; S h l e s i n g e ra n d
L o y a . 1 9 8 5 ;S z m a n t - F r o e l i c h e t a l . . 1 9 8 5 ) .I f t h i s
settlement pattern is representativcof planula
behaviour in the fleld. dispersalof the majority of
b r o o d e dp l a n u l a ei s l i k e l y t o b e l i m i t e d .p r o m o t i n g
settlementnear parents or within thc natal reef.
Extremcly restricted larval dispersal has been
observed in field and laboratory studies of the
solitary coral Balanophyllioelegunr.which releases
large. crawling. benthic planulae (Gerrodette,
1 9 8 1 ;F a d l a l l a ha n d P e a r s e ,1 9 8 2 a ) A . lthough the
planulae may remain unattached for some days
after release.they do not swim. and disperseon
CORALREPRODUCTIVE
tsIOLOGY
average less than 0.5 to I m from the f-emale
parent before settling (Gerrodette. l98l ). The
restricteddispersionof these larvae is insufiicient
to account for the range of this species(2000km).
hence some other means of dispersal must also
o c c u r ( G e r r o d e t t e .1 9 7 9 , l 9 8 l ) . L o c a l i z e dd i s p e r -
sal has also bccn observedamong pelagic.swim-
ming planulaewhich settlerapidly after release.In
a recent field study in the central Great Barrier
Reef, divers observed the release of Acroporcr
palileru planulae in situ. and monitored dispersal
d u r i n g t h e i r b r i e f p e l a g i c p h a s e ( J . R e s i n g ,p e r s .
c o m m u n . ) . P l a n u l a ew e r e o b s c r v c da t t a c h i n g t o
t h e r e e f w i t h i n 5 m o f t h e i r p a r e n tc o l o n y ( J . R e s -
i n g . u n p u b l i s h c dd a t a ) . R a p i d s e t t l e m e n o t f y'. -
puli/era planulae has also been observed in the
l a b o r a t o r y( P o t t s . 1 9 8 4 a ) .
S o m e w h a tg r e a t e rd i s p e r s i o ni s l i k e l y t o o c c u r
a m o n g p l a n u l a cw h i c h s p e n dl o n g e rp e r i o d si n t h e
p l a n k t o n .P l a n u l a eo f m a n y b r o o d i n gs p e c i e s l r i m
upwards and accumulertenear the sea surface
immediately afier release.thereby increasingthe
likelihood of dispersalaway from the parent coral.
"dispersalphase"
This is followed some time later
by a reversal of behaviour. and demersal swrm-
n.ringor settlement.Following extensiveobserva-
t i o n s o f t h e b e h a v i o u r a n d s e t t l e m e n tt i m e s o f
Pocilloporudantit'ornisplanulae in the laboratory.
S t e p h e n s o (n1 9 3 1 )a n d H a r r i g a n ( 1 9 8 2 )c o n c l u d e d
that the free-swimming period ol P. damitttrni.s
planulaeat the seasurfaceand in the water column
w a s g e n e r a l l i ,s h o r t . H a r r i g a n ( 1 9 1 2 ) c o n s i d e r e d
t h a t u p t o h a l f t h c p l a n u l a ew e r e l i k e l y t o s e t t l c
w i t h i n 6 h o f r e l e a s e .a n d t o d i s p e r s er e l a t i v e l y
short distancesbcforc settling. with pro-eressively
fewer planulaeremainingin the plankton over
subsequentdays to effectgeneticexchangebetween
p o p u l a t i o n s .I n d i r c c t c v i d c n c el b r t h i s p a t t e r n o f
larval dispersalcomes lrom genotypic studies of'
P . d a m i t ' o r n i p" io p u l a t i o n s( S t o d d a r t .1 9 8 3 .1 9 8 4 b .
1 9 8 6 ) .S t o d d a r t ( 1 9 8 4 b )c o n c l u d e dt h a t d i s p c r s a l
of asexuallyproduced planulae was effectiveonly
at short range in reel\ off southwesternAustralia.
and was insulicicnt to geneticallyconncct reefs
separated by more than I km. Larval re-
c r u i t s i n e a c h p o p u l a t i o n w c r e d e r i v e dp r e d o m i -
nantly from local asexual reproduction. with
occasionalrecruitment ol sexually produccd pro-
p a g u l e sp r o v i d i n g o n l y w e a k c o n n e x i o n sa m o n g
the highly genctically differentiated populations
185
(Stoddart, 1984a.b). Similarly,the effectivedisper-
sal range of asexuallyderivedplanulae of P. dami-
cornis in Kaneohe Bay, Hawaii, was limited to a
few kilometres(Stoddart, 1986).
A large range in the duration of the free-
swimming and settlement periods of planulae has
been observedboth within and between broods of
some species(Harrigan. 1972,table4l; Fadlallah.
1983a,table l). Variation in settlementtimesduring
the first few days following planulation appears to
result from differencesin the developmentalstages
of the planulae when released.or from genetic
lactors (Harrigan, 1972; Jokiel, 1985; Richmond,
1985a).Longer delays until settlementmay be an
artefact of laboratory conditions (De Lacaze-Du-
thiers. 1873)or due to lack of suitablesettlement
substrata(seep. 190).Delayed scttlementhas also
been induced experimentally during laboratory
studiesof planulacompetencyand longevity(Harri-
gan, 1972: Richmond. 1987),and has important
implicationsfor the long-distancedispersalpoten-
t i a l o f c o r a l p l a n u l a e( s e ep . 1 8 7 ) .
,
t
Externally developedplanulae ,l
In contrast to the rapid settlementtimes of most
b r o o d e dp l a n u l a e a . m i n i m u m p l a n k t o n i cd e v e l o p - I
ment period of approximately 4 to 6 days is
required before externally developedplanulae of
many gamete-spawningcorals are capable of
s e t t l e m e na t n d m e t a m o r p h o s i s( H o d g s o n , 1 9 8 5 a ;
S h l e s i n g earn d L o y a , 1 9 8 5 ;B a b c o c ka n d H e y w a r d .
1 9 8 6 ;R . B a b c o c k . P . H a r r i s o n . A . H e y w a r d , u n -
published data). A shorter developmentalperiod
has been observed among a few precocious
planulae of fbur Acroporctspecies.which attached
or metamorphosedonly 2 to 3 days after fertiliza-
t i o n ( R . B a b c o c k .P . H a r r i s o n . A . H e y w a r d , u n -
published data). A greatly delayed settlement
period was observed in externally developed
planLrlae of Car.t'oph.t'lliasmithi. which settled
a p p r o r i m a t e l yl 0 w e e k sa f t e r s p a w n i n g( T r a n t e re t
a l . , 1 9 8 2 ) .T h e l a c k o f s e t t l e m e n to, r r e d u c e da n d
delayed settlement patterns, reported in some
studiesof externally developedplanulae (Szmant-
F r o e l i c he t a l . , 1 9 8 0 ;K o j i s a n d Q u i n n . l 9 8 l ;
F a d l a l l a ha n d P e a r s e .1 9 8 2 b ;K r u p p , 1 9 8 3 ;B a b -
c o c k . 1 9 8 4 .H a r r i s o n e t a l . , 1 9 8 4 )a p p e a rt o h a v e
been an artefact ol laboratory rcaring conditions
( B a b c o c ka n d H e y w a r d , 1 9 8 6 ) .o r l a c k o f s u i t a b l e
s e t t l e m e n st u b s t r a t a .F u r t h e r d e t a i l e ds t u d i e sa r e
186
needed to determine the settlement rates of
externallydevelopedplanulae under more natural
c o n d i t i o n si n o r d e r t o p r e d i c ta c c u r a t e l yt h e l i k e l y
d i s p e r s a lp a t t e r n s o f p l a n u l a e w i t h p l a n k t o n i c
development.
The delayed settlement capabilities. and the
highly buoyant nature ol most coral embryos and
larvac during their first few days of planktonic
development.considerablyenhancetheir dispersal
potential, and indicate that the majority of exter-
nally developedplanulaeare likely to be dispersed
a w a y f r o m t h e i r n a t a l r e e f ( H a r r i s o ne t a l . . 1 9 8 3 ,
1 9 8 4 ;B a b c o c k .1 9 8 4 .1 9 8 6 ;W i l l i a m s e t a l . , 1 9 8 4 ;
Babcock et al., 1986; Babcock and Heyward,
1 9 8 6 ) .T h i s h y p o t h e s i sh a s b e e n s u p p o r t e db y a
number of recentfield studiesof larval dispersalin
the central Great Barrier Reef following mass
coral-spawning e p i s o d e s( B u l l , 1 9 8 4 .1 9 8 6 ;O l i v e r
a n d W i l l i s , 1 9 8 7 ;W i l l i s a n d O l i v e r . 1 9 8 8 ) .
Plankton tows near inshore fringing reefsin the
central Great Barrier Reef showed that the
majority of coral eggsand embryosaccumulatedat
the seasurfaceimmediatelyfollowing massspawn-
ings, and were dispersedoffshore within l2 hours
( B u l l . 1 9 8 6 ) .R a p i d d i s p e r s aol f s p a w n e de g g sa n d
developingembryosaway from the parent reef was
also observed during comprehensive plankton
sampling studies at Bowden Reef (a mid-shelf
p a t c h r e e f ) ( B u l l . 1 9 8 4 ;W i l l i s a n d O l i v e r . 1 9 8 8 ) ,
and from aerial surveysaround many reefsin the
centralGreat Barrier Reel (Oliver and Willis, 1987;
Willis and Oliver, 1988).When masscoral spawn-
ings coincidedwith calm weatherconditions,most
eggsand embryosformed into surfacecoral-spawn
slickswhich were subsequentlytransportedoff the
r e e f ( O l i v e r a n d W i l l i s , 1 9 8 7 ;W i l l i s a n d O l i v e r ,
1988).The majority of theseslicks were observed
trailing away from reefs or between reefs on the
morning after spawning, and high concentrations
of developing larvae remained associatedwith
surface oceanographicfeatures after the surface
slicksdispersed.Plankton samplingaround radar-
tracked drogues placed in coral-spawn slicks
showedthat coral planulaewere transportedfrom
Bowden Reef to another reef 26 km down-current
within two days of spawning (Willis and Oliver.
1988).These important observationsprovide the
first direct evidencefor dispersalof coral larvae
between reefs.
While the majority of larvae appear to be
P.L. IIARRISOi\- AND C.C. WALLACE
dispersedaway lrom the reef, significantconcen-
trations of planulae may also bc entrainedin
leeward back-reef topographic eddies during
p e r i o d s o f c a l m w e a t h e r ( B u l l , 1 9 8 4 ,O l i v e r a n d
W i l l i s , 1 9 8 7 :W i l l i s a n d O l i v e r , 1 9 8 8 ) T
. h e s el a r v a e
m i g h t p o t e n t i a l l ya c t a s c o l o n i s t si n t h e b a c k - r e e f
area adjacentto the eddies,but are lesslikely to be
r e t u r n e dt o t h e r e m a i n d e ro f t h e r e e f ( B u l l , 1 9 8 4 ) .
Developingembryosand larvaewere also observed
within Bowden Reef lagoon for up to 5 days
following spawning, indicating that some exter-
nally developed larvae may be retained within
t h e p a r e n t r e e f ( W i l l i s a n d O l i v e r . 1 9 8 8 ;c f . B u l l .
r984).
A completelydifferentpattern of larval dispersal
was observedwhen coral spawningcoincidedwith
s t r o n gw i n d s ( W i l l i sa n d O l i v e r , 1 9 8 8 )U . nderthese
conditions,coral spawn did not form into surface
slicks but was rapidly swept off the reef in the
opposite direction to that observed during calm
weather.The initial direction of dispersaland the
extent of larval retention is thus highly dependent
upon the prevailingweatherconditions,and hence
the dispersalpatterns of coral planulae between
reefs could vary substantiallyfrom year to year.
This may explain some of the large interannual
variation observedin larval recruitment patterns
within the central Great Barrier Reef (Wallace.
1 9 8 5 b s; e ep . 1 9 5 ) .
A p l a n k t o n - s a m p l i n gp r o g r a m m e ( H o d g s o n ,
1985a)in Kaneohe Bay, Hawaii, also showed
evidenceof significantdispersalof developingcoral
embryos and larvae away from reefs following
c o r a l s p a w n i n g sH . o d g s o n( 1 9 8 5 a )c o n c l u d e dt h a t
there was a high potential for export of coral
planulaefrom Kaneohe Bay, estimatingthat up to
4x 106 planulae were exported during a 44-day
study period.
A lower potential for larval dispersalmay exist
in corals spawning small, neutrally or negatively
buoyant eggs which develop quickly, such as
A,strangictdanae. Fungiu scutaria and Parucyuthus
stearnsii(Szmant-Froelichet al.. 1980; Fadlallah
a n d P e a r s e1. 9 8 2 b K ; rupp, 1983)B . e n t h i cd e v e l o p -
ment of Goniastrea.favultrslarvae may promote
t h e i r r e t e n t i o no n t h e r e e f f l a t ( K o j i s a n d Q u i n n ,
198l); however, once these planulae become
mobile they swim up into the water column.
thereby increasingtheir chancesof dispersal(Bab-
cock.1986).
C O R A LR E P R O D U C T I B
V IEO L O G Y
Implications of larval retention and dispersal
Speculationthat coral populations on reefi in
the central Great Barrier Reef are primarily
m a i n t a i n e db y s e l f - s e e d i n(gD o n e , 1 9 8 2 )w a s b a s e d
on the assumption that corals typically brooded
planulaewhich were competentto settlesoon after
release.and were thereforelikely to be retainedin
t h e p a r e n t a lh a b i t a t o r r e c f s y s t c m .N o w t h a t i t i s
known that the majority of corals spawn eggsfor
external development.and that planktonic planu-
lae can to be dispersedaway from their natal reef,
the self-seeding hypothesis needs reappraisal.
A n a l y s i s o f c o r a l r e c r u i t m e n tp a t t e r n sa r o u n d a
small. isolated reef in the central Great Barrier
R e e f r e g i o nl e d S a m m a r c oa n d A n d r e w s( 1 9 8 8 )t o
conclude that coral reefsare primarily self-seeded
with respect to coral larvae. However, as the
sourceof the recruitswas not identified.the results
of this study provide little direct information on
the extent of self-seedingin coral populations
(Willis and Oliver. 1988).
The extent and demographicimportanceof self-
seedingof coral populations through retention of
planulae. versus the immigration of planulae
through dispersalfrom other reefs, is difficult to
assess. Factors such as the mode of larval
development, meteorological and hydrological
, n d t h e l o c a t i o na n d t o p o g r a p h yo f t h e
c o n d i t i o n sa
reef directly influencelarval dispersal.Contrasting
larval dispersal patterns have been observed in
brooding and broadcast-spawningcorals al-
though this is not a strict dichotomy, becausesome
brooded planulae are probably dispersedbetween
reefs, while some externally developed planulae
may be retained on their natal reef in lagoons or
topographiceddies.The potential for larval reten-
tion is enhancedin large reefs with deep lagoons
becausethey have lower flushingrates(Williams et
al., 1984). Large reefs are also traversed more
s l o w l yb y p l a n k t o n i cp l a n u l a e( B u l l . 1 9 8 4 ) a
, nd are
m o r e l i k e l y t o h a v e l a r g e r .m o r e p e r s i s t e nt o p o -
graphic eddies(Williams et al., 1984).The persis-
tenceofan eddy is further enhancedby isolationof
the reef and its proximity to the continental slope
where mainstreamcurrentsare stronger(Williams
et al., 1984). However, larval retention in large
lagoonsor persistenttopographiceddiesis unlikely
to be effectivefor periods exceeding4 to 5 days
( W i l l i a m se t a l . . 1 9 8 4 )
ItiT
The relative contribution to recruitment from
planulae which are retained on their natal reef
versusthosedispersedto other reefswill dependto
a large extent upon the proportion of larvae in
each category and their mortality. The effective-
nessof dispersedplanulae will also depend upon
their competencyperiod, the proximity of down-
stream reefs.and the diffusion of larvae. There is
some evidencethat predation on plankton is much
higher within reefsthan in open water (Johannes,
1 9 7 8 ;H a m n e re t a 1 . , 1 9 8 8a) ,n d h e a v yp r e d a t i o no n
coral embryos and planulae has been observed
within reef waters (Westneat and Resing, 1988;
B. Willis. pers. commun.). If mortality is signifi-
cantly greaterwithin reefs,retainedplanulae may
provide relativelyfew larval recruits.
The extent to which reefs are self-seedingor
interdependenthas important consequences for the
recolonization and recovery potential of coral
communities following disturbances(reviewedby
Pearson,l98l). Reefsisolatedby distance(such as
oceanic atolls - see Wells, 1957) or by lack of
connecting currents may rely heavily on larval
retention and self-seedingfor population mainte-
nance.Such reefsare likely to recovermore slowly
from severeperturbationsthan reefswhich are part
of extensive reef systems, where recruits from
nearby unaffected reefs could recolonize more
rapidly. Conversely.damage to coral populations
supplying recruits to other reefs could adversely
affectpopulationson reefsdown-current(Williams
et al., 1984).Clearly,the dispersalpatternsof coral
larvae and the degreeof interdependenceof reefs
must be taken into account when determiningthe
scaleand spatial extent of reef-management zones
(see Williams et al., 1984). Knowledge of these
patternsis an essentialprerequisitefor determining
biologically appropriate reef-managementunits,
and has important implications for scleractinian
biogeographyand evolution.
Long-distancelarval dispersaland coral
biogeography
Most scleractinian specieshave a very wide
geographical distribution (Vaughan and Wells,
1943: Veron, 1985, 1986), and this is often
attributed to long-distancedispersalofplanulae by
o c e a n i cc u r r e n t s( V a u g h a n ,1 9 0 8 ,1 9 1 0 ,1 9 1l , 1 9 1 6 .
1 9 1 9 ,1 9 2 4 .1 9 3 0 ;V a u g h a na n d W e l l s , 1 9 4 3 ;P o t t s ,
188
1 9 8 4 b ,1 9 8 5 ;V e r o n . 1 9 8 5 ,1 9 8 6 ) .O b s e r v a t i o n so f
coral planulae dispersing away from reefs into
mainstream or oceanic currents (Vaughan, 1910;
Bull, 1984;Oliver and Willis, 1987;Willis and
Oliver, 1988)and the extendedsettlementperiods
of weeks or months observed in some planulae,
suggestthat considerablepotential existsfor long-
distancedispersalof larvae of some species.Some
workers, however, consider that corals are poor
d i s p e r s e r (sR o s e n ,1 9 7 5 ,1 9 8 1 ;H e c k a n d M c C o y ,
l 978).
Debate over the origins of the depauperate
easternPacific coral fauna has focussedattention
on the dispersalcapabilitiesof coral larvae. Dana
(1975) proposed that the present-day eastern
Pacificcoral fauna was derivedfrom long-distance
dispersal of planulae from corals in the central
Pacific.This hypothesiswas strongly criticized by
Heck and McCoy (1978),who argued that trans-
Pacificmigration of planulaewas highly unlikely in
view of the rapid settlementtimes and restricted
survival periodsreported for most brooded planu-
lae. They proposed instead a vicariancemodel of
coral zoogeography,whereby the global distribu-
tion of hermatypic corals has been altered pri-
marily by tectonicevents,speciationand extinction
(see also Rosen, 1975). Subsequentresearch on
larval energeticsand extendedcompetencyperiods
in Pocillopora dantir:ornis and Tuba,streaco(L'itrcd
p l a n u l a es u p p o r tD a n a ' s( 1 9 7 5 )h y p o t h e s i so f l o n g -
distance larval dispersal for the origin of these
speciesin the eastern Pacific coral fauna (Rich-
m o n d , 1 9 8 2 ,1 9 8 7 ) .C o m p e t e n c ye x p e r i m e n t h s ave
demonstrated that P. damicornis planulae are
capableof successfullysettlingand metamorphos-
ing for periods up to 103 days after release,which
is suffrcienttime for their dispersalfrom the central
Pacific to the eastern Pacific (Richmond, 1987).
Stored energyreserves,translocationof photosyn-
thetically fixed products from symbiotic zooxan-
thellae, and the ability to undergo partial meta-
morphosis into a planktonic polyp capable of
feeding, allow P. damicornis planulae to remain
competent for extended periods and greatly en-
hance their potential for iong-distancedispersal
( R i c h m o n d ,1 9 8 2 ,1 9 8 5 a 1 , 987).
While the presentdebate over the long-distance
dispersalcapabilitiesof coral planulae centreson
the easternPacific fauna. it is also relevantto the
distribution patterns of scleractinian corals in
P . L H A R R I S OA
NN D C . C W
. ALLACE
other regions.For example,the recent recoloniza-
tion of the Hawaiian Islands by At'roporu spp.
( G r i g g e t a l . . 1 9 8 1 ) .a p p e a r st o r e s u l t f r o m l o n g -
distancedispersaland recruitment of larvae from
o u t s i d et h e a r c h i p e l a g o C. r i g g ( 1 9 8 1 )c o n s i d e r e d
that the most likely sourceof recruitswas Johnston
Island, 720 km away a processrequiring larval
transport by the SubtropicalCountercurrentfor at
least50 days.The extendedsurvival period of some
Aoopora planulae lend support to this hypothesis
( H a r r i s o ne t a l . . 1 9 8 4 ) H
. o w e v e r ,p l a n u l al o n g e v i t y
is not necessarilya reliable indicator of larval
dispersalpotential, becausedispersalwill only be
effective during the period in which planulae
remain competentto successfullysettle and meta-
m o r p h o s e( H a r r i g a n , 1 9 7 2 ;R i c h m o n d , 1 9 8 7 ) .
An alternative mechanism for long-distance
dispersal of scleractiniancorals is by rafting of
corals attached to floating objects (reviewed by
J o k i e l , 1 9 8 4 ) . V a u g h a n ( 1 9 1 8 ) c o n s i d e r e dt h a t
rafting of attachedcorals was lessimportant than
transportation of larval corals in determining the
distribution of corals by oceancurrents.However.
rafting may be an important dispersalmechanism
in some species,enabling colonization beyond the
range of larval dispersal; hence, long-distance
dispersalby rafting should also be considere.lh.,
coral zoogeographers(Jokiel, 1984).
Contrasting models of scleractinianbiogeogra-
phy and evolution have been proposed which
attempt to explain the distribution patterns of
scleractinian corals. and discuss the effects of
glacial sea-levelfluctuations on speciationin the
S c l e r a c t i n i(ar e v i e w e db y R o s e n ,1 9 8 l , 1 9 8 4 ;P o t t s .
1 9 8 5 ) .M o s t o f t h e s e m o d e l s m a k e a s s u m p t i o n s
about the long-distancedispersal capabilities of
corals. Earlier vicariancemodels of coral biogeo-
graphy assumed that corals are relatively poor
d i s p e r s e r(sH e c k a n d M c C o y , 1 9 7 8 ;R o s e n , l 9 8 l ) .
whereasmore recent models have emphasizedthe
role of long-distancedispersal(seePotts, 1985).
Rosen's(1984)vicariance-and-refuge model pro-
posedthat speciationoccurredon isolatedoceanic
islandsduring periods of high sea-level,when the
distancebetweenpopulationsincreasedbeyondthe
dispersalcapacity of planulae. Rosen noted that
dispersalcapacityis likely to vary betweenspecies,
but arguedthat few coral speciesappearcapableof
routine long-distancedispersalover grcat distances
of open ocean. Rosen'smodel, however. requires
CORALREPRODUCTIVE
BIOLOGY
somemeansof long-distancedispersalto transport
newly evolved oceanic species to continental
r e f u g e s( s e eP o t t s , 1 9 8 5 ) .I n c o n t r a s t ,P o t t s ( 1 9 8 3 ,
1984b) has argued that glacial sea-levelchanges
have induced chronic evolutionary disturbance
among coral populations with long generation
times, thereby inhibiting processesof speciation
and increasingintraspecificvariation within shal-
low-water corals. Potts's model assumesthat the
capacity for routine long-distancedispersal is a
common feature of shallow-watercorals. and that
long-distancedispersalhas retardedratesofevolu-
t i o n a r y d i v e r g e n c eb y m a i n t a i n i n g g e n e f l o w
b e t w e e nd i s t a n t p o p u l a t i o n s( P o t t s , 1 9 8 5 ) .V e r o n
( 1 9 8 5 )c o n c l u d e dt h a t t h e w i d e d i s t r i b u t i o no f m o s t
coral speciesand genera,the homogeneityand lack
of speciesendemisnr among Indo-Pacific coral
fauna. and the high degreeof intraspecificvariabil-
ity in most reef corals, support Potts's model of
inhibited speciation and the concept of long-
distancedispersalof coral larvae.
Clearly, further research on the competency
periods of coral planulae is required before the
long-distancedispersalpotential of coral planulae
and its biogeographicimplicationscan be properly
assessed.Comparisons of competency periods
among widely distributed and endemic species.
brooded and externally developedplanulae, and
z o o x a n t h e l l a t ea n d n o n - z o o x a n t h e l l a t p el a n u l a e ,
would be particularly worthwhile.
LARVALSETTLEMENT
AND RECRUITMENT
Following larval development and dispersal.
coral planulae must settle. metamorphose and
grow to form the next generation. The conse-
quences ol these events for coral populations
depend upon whether the larvae are sexually or
asexuallyproduced, brooded or externally devel-
oped, dispersedor locally recruited.For some time
after settlement.young corals are so small that
they are for all practical purposes, invisible to
h u m a n o b s e r v e r (sW a l l a c e ,l 9 8 3 ; s e ep . l 9 l ) . T h e s e
stages in the life cycle of corals from newly
settled polyp to visible coral colony have had
little attention becauseof the difficultiesinvolved
in working on them.
Thc role of larval recruitment in influencing
population and community structures has only
189
recently drawn interest (Bak and Engel. 1979;
Underwood and Denley, 1984; Connell, 1985;
H a r r i o t t , 1 9 8 5 ;R o u g h g a r d e nc t a l . , 1 9 8 5 ) .I t w a s
previously assumed that the plankton carried a
taxonomicallydiverseover-supplyof coral larvae.
which was acted upon by various selectiveforces
that operate after settlement. such as habitat
suitability for adult physiology (Rosen, 1915;
P i c h o n . 1 9 7 8 ;C h a p p e l l , 1 9 8 0 ; D o n e . 1 9 8 2 ) a n d
competition for resourcesby adults with other
o r g a n i s m sa n d o t h e r c o r a l s( S h e p p a r d ,1 9 8 2 ) .l t i s
now known that recruitment ol scleractinian
larvae is characterizedby significant temporal,
spatial and taxonomic variability (Wallace and
B u l l , 1 9 8 2 ;S a k a i a n d Y a m a z a t o , 1 9 8 4 ;W a l l a c e .
1 9 8 5 b ;H a r r i o t t a n d F i s k , 1 9 8 7 . 1 9 8 8 ) .L a r v a l
recruitment patterns are therefore likely to
p l a y a n i m p o r t a n t r o l e i n s t r u c t u r i n gc o r a l c o m -
munities.
Searchingand settlementbehaviour
Settlementol coral larvae is normally initiated
when competent planulae encounter solid sub-
strata which are deemed suitable for attachment
and metamorphosis. Laboratory studies have
shown that settlement of scleractinianlarvae is
usuallyprecededby intensivetestingand searching
behaviour, and extensiveexploration of the sub-
stratum. Planulaenormally swim and explore the
substratumwith their aboral end foremost.and the
aboral epidermis appears to have an important
sensoryrole in the recognition of suitable settle-
m e n t s i t e s( V a n d e r m e u l e n1, 9 7 4 )D . uring theinitial
testing phase the aboral epidermis is closely
a p p l i e dt o t h e s u b s t r a t u m w , h i l e t h e p l a n u l as p i n s
on its axis or sways from side to side (Atoda.
1 9 4 7 a ;H a r r i g a n , 1 9 7 2 1V.a n M o o r s e l . 1 9 8 3 ) .T h i s
may be followed by settlement,attachment and
metamorphosis,or temporary attachment (sen.r'l.r
C h i a a n d B i c k e l l . 1 9 7 8 ) .I n t h e l a t t e r c a s e . r h e
planula subsequentlydetachesand initiates exten-
sivecreepingand searchingbehaviour.or swimsoff
to a new area wherethe procedureis repeateduntil
a s u i t a b l es e t t l e m e n st i t e i s f o u n d ( W i l s o n . 1 8 8 8 ;
M a v o r . l 9 l 5 ; S t e p h e n s o n1, 9 3 1 ; A t o d a , l 9 5 l a ;
H a r r i g a n . 1 9 7 2 ;K r u p p . 1 9 8 3 ) .
The "sensory" and "nerve" componentsol the
aboral epidermis may integrate and co-ordinate
t h e s e a r c h i n gb e h a v i o u r b, ut it is not known which
190
aspectsof the substratumare sensedor what cues
induce settlementand metamorohosisof scleracti-
nian larvae.
Settlementsubstratum preferences
Substratumselectionand settlementpreferences
of scleractinian larvae have only been tested
quantitatively on a few species in laboratory
studies.Natural substrata,or artificial ones,which
"conditioned"
have been by submersion in
seawaterprior to use in experiments,seem to be
generally preferred (Harrigan, 1972: Harriott,
1983b;Babcock, 1986;cf. Lewis, 1974a).Thigmo-
tactic responsesare evident in the preferencefor
settlement in crevices or ridges of irregular or
roughenedsubstrata,and in the cornersof culture
v e s s e l (sV a u g h a n ,1 9 1 0 ;S t e p h e n s o n1, 9 3 1 ;A t o d a ,
1941b: Lewis, 1974a:Bull, 1984; Babcock, 1986).
Preferentialsettlementon biologicallyconditioned
or roughenedsurfaces,or both, may be related to
physicalfactors suchas wettability,which has been
shown to influence the attachment ability of
scyphozoan larvae (Brewer, 1984). In addition,
biologically conditioned surfacesare colonized by
bacteria, diatoms, algae and other organisms,
someof which induce settlementof coral and other
cnidarian larvae through physical contact by
tactile or chemicalstimuli (Williams. 1965:Harri-
gan, 1972: Brewer, 1976;Chia and Bickell, 1978;
S e b e n s 1, 9 8 3 ;B e n a y a h ua n d L o y a , 1 9 8 4 ) .
A r a n g eo f p h o t o t a c t i co r g e o t a c t i cr e s p o n s e so,r
both, are apparent in the settlementbehaviour of
coral larvae. Planulaegenerallyattach or settleon
the under surfacesof objectsin aquaria or on the
sidesor bottom of culture vessels(Duerden, 1902a:
Vaughan, 1910; Atoda, 1941a,b: Wainwright,
1 9 6 3 ; H a r r i g a n , 1 9 1 2L; e w i s , 1 9 7 4 a G
l ' o r e a ue t a l . ,
l98l). The preferred settlement orientation ap-
pears to vary betweenspecies,and in responseto
physicalfactors suchas light. Experimentalstudies
of the effect of light intensity on settlement
orientation of Acropora millepora planulae have
demonstrateda shift in settlementpreferencesfrom
under surfacesto upper surfaceswith decreasing
l i g h t i n t e n s i t y ( R . B a b c o c k , u n p u b l i s h e dd a t a ) .
Similar shifts in orientation have been observedin
coral recruitment patterns with increasingdepth
(see p. 193). In contrast, the planulae of the
sciaphilic coral Ox-vporalac'eraalways settled on
P . L .H A R R I S O N
A N D C ] , CW
. ALLACE
the under surfacesof plates, irrespectiveof the
light regime(R. Babcock,unpublisheddata). Light
intensity has likewise been found to have no
influenceon the orientation of settlementof some
soft-coral larvae (Benayahu and Loya, 1984).
Phototacticand geotacticresponsesthus appear to
play an important role in guiding planulae to
suitable settlement sites. This behaviour is in-
triguing in view of the structural simplicity of
planulae, and their apparent lack of sensory
structures which could act as light or gravity
receptors.
Under laboratory conditions,planulae of many
coral speciesshow a strong tendencyto settleclose
to one another and subsequentlyfuse to form an
aggregatedcolony (Duerden, 1902a.c; Boschma,
1 9 2 9 ;E d m o n d s o n ,1 9 2 9 ,1 9 4 6 ;S t e p h e n s o nl,9 3 l ;
Atoda, 194'la, 1951b,c; Lewis, l9l4a; Goreau et
a 1 . ,1 9 8 1 ;H i d a k a , 1 9 8 6 ;B a b c o c k ,1 9 8 6 ) .G r e g a r i -
ous behaviour is apparenl in FaviaJragum larvae.
from experiments in which significantly more
larvae settledin bowls containing settledjuveniles
or adults of F. fragum, comparedwith bowls which
contained either no corals or adults of other
species(Lewis, 1974a).Patchinessin settlementof
Poritesporites has also been shown to result from
non-random aggregatedsettling behaviour in the
laboratory (Goreau et al., l98l). Among aggre-
gated primary polyps of Pocillopora tlamicttrnit,
tissue fusion has been observed between polyps
derived from the samecolony and betweenpolyps
from genotypically distinct colonies, including
differentcolour morphs (Hidaka, 1986).The histo-
incompatibility system of the adult colonies thus
appearsto be lacking or maskedin juvenile polyps
(Hidaka, 1986),and hencethe potential exists for
the creation of scleractinianchimeras.Aggregated
settlementand tissuefusion may be advantageous
in reducing the size-dependentmortality rates of
juvenile corals, but its extent in natural coral
communitiesis not known.
Studies of settlement behaviour have shown
t h a t s c l e r a c t i n i a np l a n u l a e a r e d i s c r i m i n a t i n gi n
their choice of settlement site. and generally
prefer cryptic microhabitats, often on the under
surfaces of conditioned natural substrata. The
potential for active selectionof suitablesettlement
s i t e s b y p l a n u l a e h a s o b v i o u s a d v a n t a g e si n
enhancing the post-metamorphic survival of
iuvenile corals.
 BIOLOGY
CORALREPRODUCTIVE
Metamorphosis
When conditions suitable for settlement are
encounteredthe planula attachesto the substratum
and metamorphosesinto a juvenile polyp. Attach-
ment is thought to occur through the dischargeof
nematocysts and mucus from cells in the aboral
epidermisto form an adhesiveplug (Mavor' 1915;
Wainwright, 1963;Harrigan, 1912:Vandermeulen,
1974;Goreauand Hayes, 1977;Kinchington, 1982).
Once the pianula is securelyattachedit contracts in
the oral-aboral plane, to form a flattened disc
subdivided radially by mesenteries,with a slightly
raised central region surrounding the mouth (De
Lacaze-Duthiers,1873, 1897; Wilson, 1888; Ste-
phenson, 1931;Vandermeulen,1975;Goreau and
Hayes, 191'7:Jell, 1980; Le Tissier, 1988). This
process occurs over a few hours (De Lacaze-
D u t h i e r s , 1 8 7 3 , 1 8 9 7 ;W i l s o n , 1 8 8 8 )a n d m a y b e
followed almost immediately by the onset of
calcificationand formation of calcareousaggregates
beneaththe flattenedaboral epidermis(Stephenson,
l 9 3 l : V a n d e r m e u l ea n n d W a t a b e , 1 9 1 3 J: e l l ' 1 9 8 0 ;
Le Tissier, 1988). The attached epidermis then
metamorphoses from a tall columnar epithelium
into a squamous calicoblastic epithelium (Wain-
wright, 1963;illustratedin Goreauand Hayes' 1911'
fig. 2). This radical transformation involves the
secretionor loss of the heterogeneouscell types of
the larval epidermis, and their replacement by a
single calicoblastic cell type, characteristic of the
calcifying calicoblastic epidermis of older corals
(Vandermeulen,1975;Johnston,1976;Goreau and
Hayes, 1977;Hayes and Goreau, 1977a;Kinching-
t o n , 1 9 8 0 ,1 9 8 2 ) .
Subsequentdevelopment of tentacle buds and
tentacles, additional cycles of mesenteries.and
formation of the primordial skeleton, completes
the transformation into a juvenile polyp. The
timing and order of development in these final
stages of metamorphosis are highly variable
among individuals and between species,but the
juvenile polyp form is usually attained within a
week after settling(reviewedin Atoda, 1953).
Metamorphosisin marine invertebratelarvae is
generallyconsideredto be an irreversibleprocess
(Chia, 1978);sessilebenthic invertebratessuch as
corals are assumed to remain attached to the
substrataupon which they first settledthroughout
their life. However, recent observations have
l9l
shown that if newly settled polyps of Cyphastrea
ocellina, Favia Jiagum and Pocillopora clamicornis
are stressedwithin a few days of settlement,many
are able to resorbtheir tissuefrom their primordial
skeleton,revert to a planktonic planula form, then
resettleand re-metamorphoseinto a benthic polyp
(Richmond, 1985a; Wright, 1986; P. Scott, pers.
"Demetamorphosis" has also been
commun.).
observed in one instance in a newly settled
Acropora formosa polyp (Harrison, unpubl' ob-
serv.). At present nothing is known about the
extent of this phenomenonin field populations of
corals,but reversiblemetamorphosiscould consid-
erably enhancethe microhabitatselectionability of
corals (Richmond, 1985a),and allow newly settled
spat to escapemortality from stressin unpredict-
able habitats. Reversiblemetamorphosisalso al-
lows each planula to produce more than one
skeleton, which may affect settlement and mor-
tality studiesrelying on counting skeletonsrather
t h a n l i v i n g p o l y p s ( G o r e a ue t a l . , l 9 8 l ) .
Laboratory studieshave shown that when coral
planulae are deprived of suitable settlementsub-
strata, partial metamorphosis into a planktonic
polyp with a mouth and tentacles can occur
(Edmondson, 1929; Harrigan, 1972; Richmond,
1985a).Metamorphosisand calcificationhave also
been observed to occur at the water surface or
againstother planulae in the water column under
t h e s ec o n d i t i o n s( M a v o r , 1 9 15 ; S t e p h e n s o n1, 9 3 1;
Harrigan, 1972; Richmond, 1985a;Harrison, un-
publ. observ.; P. Scott, pers. commun.). These
observationsdemonstratethat contact with a solid
benthic substratumis not an absoluterequirement
for triggering metamorphosis or calcification in
scleractinianplanulae.
Growth rates in the first year of life
Field studies of coral communities often esti-
mate the age of the smallestmeasured colonies'
This is usually restrictedto colonies within a size
rangeof I to 5 cm (see,for instance,Connell, 1973;
S c h u h m a c h e r1, 9 7 4 ,1 9 7 7 ;P e a r s o n ,l 9 8 l ; R y l a a r s -
d a m , 1 9 8 3 ; R o g e r s e t a l . , 1 9 8 4 ) ,b u t s o m e t i m e s
smaller than this if the substratum is scrutinized
closely for corals down to a few millimetres in
diameter (Dustan, 1977: Bak and Engel, 1979;
Sakai and Yamazato, 1984).Lack of information
on growth of very young corals has meant that
t92
s o m eo f t h e s es t u d i e sh a v eu n d e r - e s t i m a t etdh e a g e
of easily visible coral recruits. For example.
C o n n e l l ( 1 9 7 3 ) a n d S c h u h m a c h e (r 1 9 7 4 , 1 9 7 1 )
e s t i m a t e dt h a t c o r a l s o f I c m d i a m e t e r w e r e o n e
month old or less.
N e w l y s e t t l e dp o l y p s a r e s i m i l a r i n s i z e t o t h e
planula from which they develop- generallyless
t h a n 2 m m i n d i a m e t e r( S t e p h e n s o nl ,9 3 l ; Y o n g e ,
1 9 3 2 ;J e l l , 1 9 8 0 ;F i s k . l 9 8 l ; V a n M o o r s e l , 1 9 8 3 ;
B a b c o c k . 1 9 8 5 ) .B e c a u s eo f t h e i r s m a l l s i z e t h e y
a r e i n v i s i b l et o t h e n a k e d e y e . T h e r e a r e e x c e p -
tions for example, newly settled Balanophl'llia
elegan,s polyps are large (2 3 mm diameter) and
brightly coloured.enabling them to be reliably
c e n s u s e (dG e r r o d e t t e 1 . 9 7 9 .l 9 8 l ; F a d l a l l a ha n d
P e a r s e ,1 9 8 2 a ) . D u r i n g t h e f i r s t y e a ro f l i f e . c o r a l s
rarelyattain a s i z e g r e a t e rt h a n 1 0 m m d i a m e t e r .
Differences in rates of growth have been attrib-
uted to taronomic differences at the family level
and in the mode of spawning (gametes or
p l a n u l a e )( B a b c o c k . 1 9 8 5 ) ,a n d t o v a r i a t i o n s i n
m i c r o h a b i t a ct o n d i t i o n s( S a t o .1 9 8 5 ) .
C o r a l s w h i c h b e g i n l i f e a s e x t e r n a l l yl e r t i l i z e d
g a m e t e ss h o w s l o w e r g r o w t h r a t e s t h a n t h o s e
w h i c h b e g i na s p l a n u l a e .T h e y a r e m o r e d i l h c u l t t o
c u l t u r et h a n p l a n u l a t i n gs p e c i e sa, n d h a v en o t b e e n
studieduntil recently(Babcock, 1985).Goniustea
osp er a and P Iu t t'g t't'a sinen.si.s,broadcasting species
f r o m t h e f a m i l y F a v i i d a e ,g r e w t o o n l y 1 . 3m m a n d
1 . 2m m m e a n d i a m e t e rr e s p e c t i v e liyn 7 . 8 m o n t h s ,
w h i l ea n o t h e rb r o a d c a s t i n gs p e c i e A s t ' r o p o r ut n i l l e -
p o r a ( o f t h e f a m i l y A c r o p o r i d a e )g r e w 3 . 5 t i m e s
f a s t e r . r e a c h i n g5 . 1 m m m e a n d i a m e t e r i n 9 . 3
m o n t h s ( B a b c o c k .1 9 8 5 ) .F i v e p l a n u l a t i n gs p e c i e s
s t u d i e db y o t h e r a u t h o r sa l l h a d g r o w t h r a t e sf a s t e r
t h a n t h i s ( B a b c o c k .1 9 8 5 .t a b l e l ) . J u v e n i l e so f
Pocilloporu datit'ornis lrom brooded planulae
r e a c h e da b o u t 9 l r l m m e i i nd i a r n c t c ri n 6 m o n t h si n
e x p e r i m e n t sa t O k i n a w a ( S a t o . 1 9 8 5 ) .
J u v e n i l e so f t h e s a m e a g e u s u a l l y s h o w a
c o n s i d e r a b l er a n g c o f ' g r o w t h r a t e s . S a t o ( 1 9 8 5 )
found that the rate of growth in juvcniles of
Pot'illopora danritorni.s was grcatcr when the
s u b s t r a t u mw a s o r i e n t e dv e r t i c a l l yo r d o w n w a r d s
r a t h e r t h a n u p w a r d s .B i r k e l a n d ( 1 9 7 1 )r e c o r d c d
fasterratesin coralssettledon the upper surfaceof
p l a t e s a n d a d e c r e a s ei n g r o w t h r a t e s w i t h
i n c r e a s i n gd e p t h . V a u g h a n ( 1 9 1 2 )c u l t u r e d t w o
planulating speciesof'Porite.sand one of .Folia for
o n e y e a r . T h e s es h o w e da r a n g c o f g r o w t h r a t e s .
P.L. HARRISON AND C.C. WALLAC]E
t h e s l o w e s tr e a c h i n go n l y 4 m m x 3 m m a n d t h e
" f a s t e s t "2 3 m m x 1 4 . 5m m b u t h e r e m a r k st l . r a t
the latter was probably a fuscd colony lrom six
p l a n u l a eO . t h e r t h a n t h i s .v a r i a t i o nw a sm o s t l yd u c
t o d i f f e r e n c eisn t h e a m o u n t o f s m o t h e r i n gc a u s e d
b y g r o w t h o f a d j a c e n ta l g a ea n d o t h e r o r g a n i s m s .
R a t e so f g r o w t h i n c o h o r t s o f j u v e n i l e c o r a l s ,
estimatedfrorn the placemcntperiod of settlement
plates, confirm these records of slow growth in
e a r l y l i f e . B e i n g b a s e do n m a x i m u m p o s s i b l ea g c .
t h e y w i l l a l w a y sb e u n d e r e s t i m a t eosf g r o w t h ; b u t
i f t h e p l a c e m e n tp e r i o d i s s h o r t a n d t h e s p a w n i n g
t i m e k n o w n t h e y p r o b a b l y a r e r e a s o n a b l ya c c u -
r a t e .J u v e n i l ec o r a l so n s e t t l e m e npt l a t e si m m e r s e d
f o r 4 m o n t h so n t h e G r e a t B a r r i e r R e c fi n e a c ho f 3
years showed a range of mean diameters from
0 . 8 6m m ( S . E .+ 0 . 0 3 ) t o 1 . 0 6m m ( S . E .+ 0 . 0 4 )
( W a l l a c e ,1 9 8 5 b ) .T h e s ec a m e f r o m a m i x t u r e o f
g a m e t e - s p a w n i nagn d p l a n u l a t i n gs p e c i e sa,p p r o x i -
m a t e l y 8 8 % b e i n g g a m e t e - s p a w n i nm g e m b e r so f
the family Acroporidae.The mean ages of the
j u v e n i l e s ,c a l c u l a t e df r o m t h e k n o w n s p a w n i n g
d a t e e a c hy e a r t o r e t r i e v a d l a t e .w a s 8 . 8 t o I 1 . 7
w e e k s ,s o a t t h i s r a t e t h e y w o u l d r e a c h a m e a n
d i a m e t e ro f a b o u t 5 m m i n a y e a r .H a r r i o t t ( 1 9 8 5 )
f o u n d n o j u v e n i l e so v e r 4 m m d i a m e t e ra n d 5 m m
i n h e i g h to n p l a t e ss u b m e r g e df o r u p t o 9 m o n t h s .
a n d c a l c u l a t e dt h a t c o r a l s I c m i n d i a m e t e r a t
study sites were at least one year old. In the
C a r i b b e a n , R y l a a r s d a m( 1 9 8 3 ) f o u n d t h e m e a n
g r o w t h o f j u v e n i l e c o r a l s o n e x p c r i m c n t a ls u b -
s t r a t at o b e a p p r o x i m a t e l y5 m m i n 9 t o l 0 m o n t h s .
R o g e r se t a l . ( 1 9 8 4 )q u o t e d a m u c h f a s t e r r a t e o f
1.2 cm yr I for the largest specimenin their
s a m p l e sb. u t t h e m e a nr a t ew a sm u c h l e s st h i t n t h i s .
Definitionsof settlementand recruitment
B e c a u s el a r v a e a n d n e w l y m e t a m o r p h o s e dp o -
l y p s a r e e x t r em e l y s m a l la n d d i f h c u l to r i r n p o s s i b l e
t o d e t e c ti n f i e l dc o n d i t i o n s( s e ep . l 9 l ) . t h e r ei s u
"settlemer.rt"
need to distinguish betrveen and
"recruitment".
S e t t l e m e n ti s u s u a l l y t a k e n b y
b e n t h i c e c o l o g i s t st o r e l e r t o t h e p o i n t a t w h i c h
l a r v a ea t t a c h t h e m s e l v e sr.v h i l er e c r u i t n t e n tr e f e r s
t o t h e s t a g ew h e n n e w m c m b c r so f t h e c o m m u n i t l
b c c o m e v i s i b l e t o b e c e n s u s e d( s e e .f o r i n s t a n c e .
K e o u g h a n d D o w n e s . 1 9 8 2 ;C l o n n e l l ,1 9 8 5 ) .F o r
m o s t c o r a l s .r e c r u i t m c n to c c u r sa t a b o u t 8 t o l 0
m o n t h s a f t c r i n i t i a l s c t t l e m e n t( s e ea b o v e ) . T h i s
C O R A LR E P R O D T ] C T IBVIE
OLOGY
m c a n s t h a t s t u d i e so f t h e e a r l y h i s t o r y o f c o l o n r z -
i n g e v e n t sm u s t u s e s o m e s o r t o f s e t t l i n gs u r f a c e
t h a t c a n b c c x a m i n e du n d e r t h e m i c r o s c o p eO . nce
a s k e l e t o nw i t h r e c o g n i z a b l e s c p t ai s l a i d d o w n , a
p r o c e s st a k i n g I t o 5 d a y s ( V a n d e r m e u l e na n d
W a t a b e .1 9 7 3J: e l l .l 9 u 0 ;B a b c o c k .1 9 8 5 )a. r e c o r d
r e m a i n sc v e ni f t h e p o l y p d i e sb e f o r ct h c s u r f a c ei s
e x a m i n e d .a n d i s o n l y l o s t i f t h e y o u n g s k e l e t o ni s
r e m o v e do r c o v e r e do v e r .
I f e x p e r i r r e n t a lc o n d i t i o n s e x c l u d c p r e d a t o r s ,
and if the time before collection of settlement
p l a t e si s s h o r t e n o u g ht o a v o i d o v e r g r o w t hb y f a s t -
g r o w i n g b e n t h i c o r g a n i s m s ,c o u n t s o f s k e l e t o n s
s h o u l d a p p r o a c h a n a c c u r a t ea s s e s s m e notf s u c -
t n p l a t e s( W a l l a c e .1 9 8 5 b ) .
c e s s f u ls e t t l e m e n o
Patternsof settlementand recruitment
Studies using settlementplates usually are de-
signed to distinguish the influences of vanous
factors on recruitment. The major factors these
studiesseckto examineerre:(a) temporaland spatial
variability in the availability of larvae for settle-
ment; (b) orientation of settlement(or of survival
after causesof early mortality have operated);(c)
effectof other organismson settlementand/or early
survival;and (d) taronomic compositionof recruits.
Various types of plate have been used, including
terracotta tiles (Brock. 1979; Baggett and Bright.
1985B ; a b c o c k .1 9 8 9 )p, o l y v i n y lc h l o r i d e( P V C ) a n d
o t h e r p l a s t i c s( B i r k e l a n d ,1 9 7 7 :D a y , 1 9 7 7 ;B i r k e -
l a n d e t a l . . 1 9 8 2 :N e u d e c k e r .1 9 8 2 ;W a l l a c ea n d
Bull, 1982),cement blocks (Hada. 1932: Fitzhar-
dinge. 1985).slicesor cubes of coral presentinga
smooth surface for settlement (Bothwell. 1982;
S a m m a r c oa n d C a r l e t o n ,1 9 8 2 ;R o g e r se t a l . . 1 9 8 4 ;
Harriott, 1985).and portions of dead coral present-
ing an irregular surface(Sammarco,1980;Wallace
and Bull. 1982; Rylaarsdam, 1983; Wallace.
1985b,c; Wallace et al.. 1986a; Carleton and
Sammarco,1987).Field studiesof recruitmenthave
used various artificial objects (Stephensonand
Stephenson,1933; Loya. 1976b,c; Schuhmacher,
1977)and natural basaltor reef substrata(Connell,
1973;Grigg and Maragos, 1974; Bak and Engel.
1 9 7 9 ;H u g h e s . 1 9 8 5 ;H u g h e sa n d J a c k s o n .1 9 8 5 ) .
Choice of substratum type should be carefully
consideredbefore initiation of any experimental
study of recruitment.In a systematiccomparisonof
a wide rangeof materials.plate type hasbeenshown
l9l
to influenceboth the number and type of recruits,
and thc clliciencyof data collcction (Harriott and
F i s k .1 9 8 7 ) .
Orientation of settlement
Settling larvae of many marine invertebrates
show prelerencesfor particular orientations of
settlement,such as predominantly on vertical or
upper or lower horizontal surfacesof plates.While
settlementhas not been directly observedin corals
in the field, recruitment may reflect settlement
preferences if early mortality can be assumedto be
uniform in space. Preferencesby corals for differ-
ent orientationsmay change.usually with a trend
from more shelteredto more exposed positions
with increasing depth (Bak and Engel. 1919,
B i r k e l a n d e t a l . , 1 9 8 2 ;W a l l a c e a n d B u l l . 1 9 8 2 ;
Rogerset al., 1984;Baggettand Bright, 1985;
Harriott, 1985;Wallace. 1985b,c). While not well
tested,this preferenceis thought to be related to
diminishing light intensity, or the associated
diminution of algal recruitment and growth, or
both (Birkeland, 1917: Birkeland et al., 1982;
Sammarcoand Carleton, 1982;Wallace and Bull,
1982).Sedimentaccumulatingon upper horizontal
surfacesis also thought to be a lactor preventing
settlement in some localities (Birkeland, 1911:
Rogers et al.. 1984).Scouring by wave action on
sedimentmay also act in shallowsites(Birkelandet
al., 1982). In some casesthe absenceof juvenile
coralson exposedparts of platesis probably due to
predationor accidentalgrazing(Harriott. 1985).In
a study using settlementplatesbearingsmall cones
which were assumedto excludegrazers(Wallace,
1985b.c), orientation of recruits was site-specific
and did not alter among seasons or years
( F i g . 7 . l 5 ) . L a r v a e d i d o c c u r o n t o p s o f p l a t e si n
shallow water. but significantlymore occurred (or
survived) on under surfaces;in deeper water the
oppositewas the case.When another type of plate
with longer coneswas usedat shallorvsites,almost
all recruitmentwas to upper surfaces(C. Wallace
and A. Watt. unpublished data). Possibly the
deeper valleys between cones offered suftrcient
shadingand protection,so that larvaehad no need
to migrate to the more shelteredunder surfaces.
Harriott and Fisk (1987)found that terracottatiles
"gap"
bolted togetherto provide a habitat between
them offeredan attractivesettlementsituation.

A B C O E A E C
F I
* f
g A1o
z g
3 '
, J
' '
REEF FLAT
Fig. 7.15.Variation ofrecruitment ofcoral larvae in time, spaceand orientation: Mean numbers ofjuvenilcs observedon upper and lowcr
surfacesof settlementplates at 4 sites in the Great Barrier Reef over two years. divided into three seasons,wintcr spring (June to
October). spring summer (October to February) and summer winter (Fcbruary to June). Plotted as log (.r+ l)(from Wallace. l9tl5b).
Irregularities in surface structure enhance settle-
ment by providing more space for settlementand
refugesfrom predators(Edmondson, 1929;Lewis,
1974b;Schuhmacher,1914:Brock, 1979;Birkeland
and Randall, 1982;Birkeland et al., 1982;Baggett
and Bright, 1985).Carleton and Sammarco(1987)
examined this effect with ridged plates of the coral
Pachyseris speciosa,which were protected from
grazing by the activities of territorial fish. Abun-
dance of juvenile corals was correlatedpositively
with surlace irregularity and averagesurface angle
on a scaleof I cm. Genericdiversityand degreeof
aggregation (in areas of 4 sq cm) were correlated
with thesefactors also.
Effects of other organisms
Other organisms can apparently affect settle-
ment, or survival after settlement,in positive or
negative ways. Heavy algal cover can act as a
deterrent to settlement,either directly by occupy-
ing spaceand/or smothering newly settledjuveniles
(Sammarco, 1982a), or indirectly through the
effects of sediment trapped among the algae
(Birkeland, 1977).Accumulation of fouling orga-
nisms such as barnacles,hydrozoans,tunicatesand
sponges which grow rapidly in areas of high
nutrient input was also assumed by Birkeland
P.L. HARRISONAND C.C. WALLACE
D E T A B C O €
JULY80 OCT AO
ocT m- FEa al
FEB 81_JUNE81
JUNE8T OCT 81
ocT ar - FEa'82
FEB'82_JUN€'82
- I
UPPER SLOPE' MIO SLOPE
(1977)to be a factor preventingsurvival of settled
planulae. High rates of recruitment were found by
Rogerset al. (1984)to be associatedwith low algal
cover.
Under natural conditions algal cover is often
maintainedat a low level by the efforts of grazers.
These grazers may facilitate settlemcnt (Brock,
1979; Sammarco, 1982a,b) and enhance survival
(Birkeland, 1977). Heavy grazing might also lead
to removal of juveniles,probably accidentally.This
was demonstratedfor grazing by echinoids(Sam-
marco, 1980; Rylaarsdam, 1983) and small fish
(Brock, 1979), but Birkeland (1977) found that
some fish of the families Acanthuridae and
Scaridaeavoided corals above 3 mm in diametcr.
The major grazersinfluencing algal cover on corarl
reefs are fish, particularly of the families Acanthu-
ridae. Pomocentridaeand Scaridae.and echinoids.
The relativeinfluenceof thesevariesfrom place to
place (Brock, 1979; Sammarco, l985). Some
echinoid grazers actually alter the topographical
complexity of the substratum by forming burrows.
thus facilitating settlement(Birkeland and Ran-
dall, 1982).Sammarco(1980)found that both the
speciescomposition and the density of echinoid
grazers influencedcoral settlementand survival.
Territorial damsellish (Pomacentridac) prevent
CORALREPRODUCTIVE
BIOLOGY
other grazing fish from entering their territories,
and thus maintain areasof substratumwith only a
low level of grazing (Kaufman, 1971;'Potts, 19171-
Wellington, 1982).In these conditions, settlement
has been found to be enhancedover that on either
caged substratum with no grazing or uncaged
substratum(Sammarcoand Carleton, 1982).Inter-
mediateamounts of grazing pressure,especiallyin
combination with refuges provided by complex
surface topography. seemsto give the best settle-
ment conditions (Brock, 1919: Sammarco and
C a r l e t o n ,1 9 8 2 ) .
Temporal patterns
Since reproduction by many corals in many
localities is seasonal(see p. 163) and larval life
generallyshort, settlementshould be mostly sea-
sonal.Seasonalityin recruitmenthas beenreported
for the U.S. Virgin Islands (Dustan. 1977), the
Great Barrier Reef (Bothwell, 1982;Wallace and
B u l l . 1 9 8 2 ; H a r r i o t t , 1 9 8 5 ; W a l l a c e , 1 9 8 5 bc, ;
Harriot and Fisk, 1988), Okinawa (Sakai and
Yamazato, 1984), the northern Gulf of Mexico
(Baggett and Bright, 1985),and Hawaii (Fitzhar-
dinge, 1985). In all cases, most recruitment
occurred in the spring and summer months,
following the major spawning season.
Larvae of the family Pocilloporidae are released
for extended periods and settle on plates through-
out most of the year in Palau, Okinawa, Hawaii
and the Great Barrier Reef (Hada, 1932;Stephen-
son and Stephenson,1933; Bothwell, 1982: Sakai
and Yamazato, 1984;Fitzhardinge,1985:Harriott,
1985;Wallace, 1985b.c). The family Acroporidae
contains mostly gametic spawners in the genera
Acropora (subgenus Acropora), Astreopora and
Motttipora. These recruit from late spring to late
summeron the Great Barrier Reef (Bothwell, 1982;
Wallace, 1985b,c). Harriott ( 1985) found some
recruitmentof Ac'roporaduring the winter months.
which could be attributed to planulatingspeciesin
the Acropora subgenus Isopora (Atoda l95la;
Kojis, 1984). These strong seasonal trends in
number and type of recruits must now be con-
sideredin the designof all future studies.
Variability among yearsin recruitmentis harder
to study, since this can only be determined by
repeated sampling over several years. The longest
series of settlement plates thus far extended over
five years on the Great Barrier Reef (Wallace,
195
1985b,c). Recruitment during this series, at a
single locality, indicated that there were "good"
"bad" years
and for larval recruitment. It remains
to be seenhow local this effect is. and whether it is
determined by fluctuations in reproductive output,
hydrological conditions, larval survival or survival
after settlement. Other studies which have set
plates down for the same seasonin more than one
year have also found significant variability (Bag-
gett and Bright, 1985; Fitzhardinge, 1985).Inter-
annual variability was also seen in recruitment of
visible corals on the reef at Heron Island by
Connell (1973), and in larval recruitment into
clearedplots on Jamaicanreefs(Hughes, 1985).
Spatial patterns
Settlement rates and taxonomic composition of
settlers may be expected to vary spatially due to
variations in geographic availability of larvae,
prevailing hydrographic conditions and physical
characteristicsof sites. None of these factors has
had much attention thus far, and few comparisons
can be made betweenstudiesbecauseof differences
in experimental methods, especiallytypes of plate,
seasonsand durations of placement. Almost all
studies examining more than one site show
significant differencesin recruitment between sites,
but replicated time-seriesshow that many of these
patterns are complicated by temporal variations
(Baggettand Bright, 1985;Wallace, 1985c).
Significantdifferencesin total number of recruits
have however been demonstrated by Harriott and
Fisk (1987, 1988).These studiescompared settle-
ment rates at fore-reef and back-reef sites. and
found higher numbers settling at the latter. This
pattern has also been found on other reefs
(Harriott and Fisk, 1988). Hydrological factors
such as back-reef eddieshave been proposed as an
explanation for theseresults;however such conclu-
sionsawait confirmationby oceanographicstudies.
Taxonomic differencesin recruitment patterns
have also been found at the scale of individual
reefs. Harriott and Fisk (1988) found acroporid
juveniles were most abundant on the back-reef,
while pocilloporid juveniles dominated on the fore-
reef. At still smaller scales,cryptic shaded habitats
have been shown to be less attractive to recruits
(mostly Acroporidae and Pocilloporidae) which
settle most abundantly at exposed sites. In these
cryptic habitats, taxa such as Dendrophylliidae,
 196
Faviidae and Mussidae dominate (Wallace,
r985b).
Geographic variation in availability of larvae
has beenshown by Sammarco(1983)in a study of
recruitmenton the Great Barrier Reef acrossthe
Australian continental shelf. A major distinction
between inshore and offshore adult communities
on the shelf is the prevalenceof staghorn corals,
Acroporu,on the mid- and outer-shelfreefs(Done.
1982).A similar distinction occurred in the taxa
settlingin the two localities.and wzrsreinlorcedby
a similar pattern of differentialsurvival of the taxa
on transplanted settlement plates (Sammarco.
1983). Thus, rccruitment may be influenced by
geographicallylocalized settlement and region-
specificlocal environmcntalfactors operatingsoon
after settlement.
Comparisonsof recruitmentstudiesare compli-
cated by differencesin iissumptionsand methods.
Any single study can be better interpretedwhen
supported by information on dates of spawning
and prevailing hydrological conditions (see, for
instance.Harriott and Fisk, 1988).Clearly many
factors influence larval recruitment into coral
populations or communities. The dilliculty is to
assessthe relativecontribution of each factor. To
do so requirescomplex experimentaldesigns,and
almost any appropriateprogram will incur logistic
diflrcultiesin its applicationin the field.
Past ecologicalstudieson reefshave had to rely
on assumptionsabout coral biology - particu-
larly, that corals reproducedby releasingbrooded
larvaewhich were alreadycompetentto settle.and
that these planulae were released year-round,
hencebeing always availablein the water column.
The new information compiled in this chapter
shows that theseassumptionsare untrue for most
coral species.As might be expectedfor an order of
some 21 extant families. scleractiniancorals dis-
play a broad range of reproductive and develop-
mental traits. The flexibility of the scleractinian
modular body plan and the plasticity of their
tissuesadds another dimension to this range by
allowing for interplay of different functions: sexual
and asexualreproduction.adult and larval asexual
propagation, and production and resorption of
reproductive and developmental tissues. Most
remarkable of all is the finding that most coral
spawning in many locations is concentratedinto
brief synchronousevents,and that it is unfertilized
t
P.L. HARRISON AND C.C, WALLACE
gametes.not competent larvae, that are released.
Thesefindingswill profoundly influencethe wuy in
which biologistsview coral communities and the
dynamic processes occurringwithin them.
ACK\OWLEDGE}IENTS
We sincerely thank B. Harrison for sustained
support and encouragementduring the writing of
this review. We also thank colleaguesat James
Cook University. particularly R. Babcock, B. Wil-
lis, J. Oliver and A. Heyward lor their stimLrlating
discussions and contributionsto coral reproduction
rcsearchover the past sevenyears.We thank the
following colleagueswho provided us with invalu-
able unpublishedinformation andior drafts or pre-
publication copies of their papers during the
preparation of this chapter: D. Ayre. R. Babcock,
G. Bull, J. Carleton, E,.Chornesky. Y. Fadlallah,
D. Fautin. D. Fisk, V. Harriott, A. Heyward,
G. Hodgson. T. Hughes, W. Jaap, P.Jokiel,
S. Kawaguti, B. Kojis, Y. Loya, R. Miller, J. Oliver,
J. Pearse.J. Resing. R. Richmond, P. Sammarco,
H. Schmidt. P. Scott, C. Simpson, J. Stimson.
J. Stoddart.A. Szmant,M. Van-Praet.B. Willis and
S. Wyers. We also thank C. Alexander, B. Willis,
R. Babcock. B. Harrison, J. Collins, J. Connell.
J. Oliver, J. Resingand D. Fautin for commentson
variousparts of the manuscript;A. Sharp,B. Harri-
son and B. Gordy for assistance with typing tables
and references; and P. Arnold, M. Pichon.J. Oliver
and J. Darley for translating papers. Finally. we
thank Z. Dubinsky for his encouragementand
editorialpatience.This reviewwas supportedin part
by a grant from the Marine Sciences and Technolo-
giesGranting Scheme,Australia.
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