Referetmce: Biol. Bull., 156: 196—211.(April, 1979)

LIGHT DEPENDENT ACTIVITY PATTERNS AMONG REEF

CORALS : MONTASTREA CA VERNOSA

HOWARD R. LASKER1

Department of tile Geophysical Sciences, University of Chicago, Chicago, I!linois 60637

The popular literature on coral reefs frequently notes the great numubcr of reefaninuals which arc only visible during the night. Among these nocturnal orgahush-is arc the reef corals. Although their skeletons are always in evidence, thenuajority of reef corals can only be seen in a fully expanded condition during thetuight. The generalized activity cycle for scleractinians is one of daytime contractionand nocturnal expansion and feeding. In fact, not all scleractinians follow thispattern. A number of species expand during the day and there arc some specieswhich expand only during the day (Yongc, 1930 ; Kawaguti, 1937 ; Abe, 1938,1939 ; Porter, 1974 ; Sweeney, 1976).

Expansion activity cycles are also known to vary within species. On theCaribbean coast of Panama, colonies of Montastrea cavernosa can be divided intotwo nuorphs on the basis of their activity cycles and polyp morphology (Lehmanand Porter, 1973 ; Lasker, 1976, 1978) . Polyps of the diurnal morph ofM. cavernosa arc expanded both day at-id night, while those of the nocturnal morphexpand only at night. The presence of these differing activity cycles within a singlespecies provides a unique opportunity to assess ti-ic relative importance of the different proximal and causal factors which control activity cycles among corals.

At the operational level, did patterns of both nocturnal and diurnal expansionhave been linked to a nunuber of intrinsic and extrinsic factors. Innate circadianrhythms have been reported for both penatulids (Mori, 1960) and for corals(Sweeney, 1976). Other authors have related expansion among cnidarians toextrinsic factors like light (Hargitt, 1907; Abe, 1939; Pearse, 1974; Gladfelter,1975; Krezoski, 1977), oxygen concentration (Abc, 1939; Brafield and Chapman,1965, 1967; Sassaman and Mangunu, 1972; Wells, Wells and Van der Walker,1973) and ammonium concetitration (Kawaguti, 1937).

Causally, nighttime expansion has traditionally been related to the increasedavailability of prey (zooplankton) during the evening. Indeed, zoopiankton aremore abundant in reef waters at night (Giynn, 1973; Porter, Porter and Batac

Catalan, 1977). However, a variety of detrital prey items are available duringti-ic day and corals can and do feed ott these particles (Price and Lewis, 1975).

Among cocienterates with synubiotic algae, daytinuc expansion has been relatedto ti-ic effects of expansion on photosynthesis. For instance, Antho pleura elegantissinia, an anemone, has symbiotic individuals which are expanded only during the

day and aposymbiotic individuals which arc expanded both day and night (Pearse,1974). On the other hand, the majority of reef corals, all of which-i have zooxanthellae, do not expand during the day or do so rarely.

1 Present Address: Rosenstiel School of Marine and Atmospheric Science. University of

Miami, 4600 Rickenhacker Causeway, Miami, Florida 33l4@).

196

SCLERACTINIAN ACTIVITY CYCLES 197

MATERIALS AND METHODS

In order to quantify M. cavernosa's activity cycle, 125 colonies from threelocalities on Panama's Caribbean coast ( Portobelo ; Galeta Island ; and KorbiskiReef, Islas San Blas) were labelled and monitored for daytime expansion and atirregular intervals over a two-year period. An additional 36 colonies which hadbeen collected from Portobelo and Isla Salar were maintained in the sea tablesat the Galeta Marine Lab and expansion data from these colonies were also collected.All daytime observations were made between 1000 and 1600 hr and the majorityof observations were made between 1200 and 1500 hr. Individual colonies fromGaleta were scored up to 81 times and those from Korbiski and Portobelo up to24 and 18 times, respectively. Quantitative nighttime observations were made of theKorbiski reef colonies (5—11 observations per colony) and of the sea table colonies( 13—25observations per colony). Qualitative nighttime observations of the Galetacolonies were also made. All nightinie observations were niade betwen 2000 to2400 hr.

Polyp expansion was scored for each of the colonies on a scale ranging from 0,complete contraction, to 4, full expansion. The scores refer to individual polypsand the values presented for whole colonies are field estimates of the averagedegree of POlYP expansion occurring on a single colony. The five classes areillustrated in Figure 1. An expansion state of 0 indicates complete contractionof the polyp such that neither tentacles nor oral disk are in view. When the polypexpands to the point at which its tentacles, though still contracted, are visible it isassigned a score of 1. Further expansion bringing the oral disk into sight is indicative of a score of 2. A score of 3 indicates expansion of the outer whorl of tentaclesand a score of 4 indicates complete expansion of all of the tentacles. The presenceor absence of sweeper tentacles (Den-Hartog. 1977) is not considered in the scale.The scale is also independent of tentacle length and other characteristics whichdiffer systematically between the two morphs. Adjustments for factors like tentaclelength and individual “¿�quirks―in behavior require an experienced observer forconsistent observations. However, an inexperienced observer can readily dis

tinguish expansion states two units apart.In addition to having their expansion behavior monitored, 18 sea table colonies

were used for two sets of experiments. The first of these, the altered light experinients, tested the sensitivity of the activity cycle to light. During these experi

nients colonies were subjected to nighttime lighting and to niid-day darkness. Inthe nighttinie lighting experiments colonies were exposed to 120 nuin of lowintensity light (9 @E-nr2sec1 at the top of the sea table) provided by an outdoorfloodlight. The period of artificial illumination extended from 2100 to 2300 hr oneach of five evenings. Daytime darkness was achieved by covering the sea tableswith black polyethylene sheets for a two hour period betwen 1100 and 1300 hr.The daytinie darkening experinient was also replicated five tinues for each colony.Expansion states of the colonies were monitored at 30 mm intervals starting 90mm before the altered light condition and continuing to 90 ruin past the lighttreatment. Noontinie light levels in the sea tables were characteristically between75 and 100 @.tE-nr2sec'. Colonies were kept in flowing aerated seawater (27—290 C) at all times during the experiments.

HOWARI) R. LASKER198

@,) ;@

@) ,,, @k

@-I@

.@fl

1 cm

FIGURE 1. Expansion states of jii. cazerizosa. Photographs of the five expansion states ofM. caveriioso colonies. The scores in the lower right hand corner of each photograph arevisual averages for the entire field of view. Note the variation between individual potmyps inexpansion state 2. See text for complete description of the expansion states.

Tlue secOn(l set of experiments involved the treatment of diurnal nuorph colonieswith the photosynthetic inhibitor DCMU (3—(3,4—dichlorophenvl) —¿�1,1—diniethylurea). Colonies used in the DCMU experiments were transferred from the sea

tables to a 10 liter aquariunu several hours prior to the experinuent and were kel)t inflowing aerated sea water until the start of the experiment at which time waterflow was discontinued and DCMU added. One liter of DCMU saturated sea waterwas added to the aquarium to yield a theoretical concentration of 10@ @r. Difficulties in dissolving the DCMU suggests a soniewhat lower realized concentration(see Vandernuuelen, Davis and Muscatine, 1972). Expansion was monitored at30 nuin intervals starting 90 nun prior to the DCMU addition and continuing for120 nuin into the treatnient. Light levels during the experiments were the sanieas those for the daytime darkening experinients.

RESULTS

Actiz'ifv cycles of the morphs

The observations of daytime expansion for each of the colonies froni three ofthe localities were subjected to a Q-mode cluster analysis using a quantified

SCLERACTINIAN ACTIVITY CYCLES 199

noct urna I

1.0 0.8 0.6 0.4 0.2

Coefficient of Association

0.0

FIGURE 2. Cluster analysis of colonies on Korbiski reef based on their daytime expansion

patterns. Two clusters corresponding to the two morplis are distimctly visible.

Jacard's coefficient of similarity (Scpkoski, 1974). Ti-ic fourth data set, Portobelo,was not clustered due to at-i insufficient nuniber of observations. Ti-ic clusteringprocedure broke the colonies it-ito groups with-i similar behaviors. A dendrogramrelating ti-ic sinuilarities itt expansion behavior of ti-ic Korbiski colonies is presented

Expansion state.Number of

totatobservations02

4I)iurnal

Morph day(28 colonies) night

Nocturnal Morph day(33 colonies) night0.20

0.030.810.030.24

0.040.120.030.32

0.22 0.02 5510.04 0.12 0.77 27S0.05 0.02 0.00 6050.03 0.14 0.77 238

200 HOWARD R. LASKER

TABLE I

Frequency of expansion of diurnal and nocturnal morph colonies from Korbiski Reef, Is!as San Bias.

it-i Figure 2. Ti-ic colonies it this den(lrogram and iii the (lendrogratuls for thieother localities cat-i readily be divided it-ito two classes. These correspond to colonieswhicl-i were not regularly expamidcd and those which were. This classificationagrees, of course, with the definitions of ti-ic nuorphs and clctuonstratcs that ti-icdichotomous view of ti-ic activity cycles accurately reflects ti-ic natural distributionof behavioral patterns within @1J.caz'ernosa. Both the nuean amid tuuodal expansionstate of ti-ic colonies in Figure 2 muirror the two-morl)l-i classification, but a chassificatiot-i based on ti-ic ircset-ice or al)sence of a imori-zero n-iode appears to muiostaccuratelyreflect the results of ti-ic cluster amalvsis. \Vhucn tITlecolonies were scparate(l according to their muodal expansion state 927 of ti-ic classifications were in agreemuent withtile cluster analysis.

Ti-ic frequcmcv of expansion for ti-ic two muuorphusduring 1)0th (hay aiul night arepreset-ite(l it-i Table I. There are radical differences iii expansion l)etwecn thediurnal morph and ti-ic nocturtual nuorl)h1 during ti-ic day, when ti-ic nocturnalmorph is alnuost always contracted. At night, however, when time nocturnal morpi1expands, there arc no significatut differences itt the expansion states of ti-ic twomorphs. It is of interest to note that ti-ierc arc significat-it chifferet-ices (x2 test,P < 0.001 ) il-i the exi)ansion state of ti-ic diurnal niorph l)etween ti-ic (hay at-id night.During ti-ic day expansion states 2 an(l 3 are most common while at night state 4is nuost commuon.

The clustering pattern im Figure 2 and those of ti-ic colonies from-i-iti-ic otherlocalities, despite their dichotomous nature, also suggest that a variety of behavioral patterns cat-i be found vvithin cad-i of ti-ic two classes. In the Korbiskidendrogram (Fig. 2) a considerai)le spread of simuilarities cat-i i)e found within thenocturnal class, and within both clusters similarities as low as 0.60 cat-i be found.Dissimilarity within clusters cart be attributed to ti-ic preset-ice of colonies withinterniediate behaviors. During ti-ic day ti-ic archetypical diurnal morph colony isfully expanded all of ti-ic tim-i-icand ti-ic archetypical nocturnal muorph colony isfully contracted. However, in nature many intermuediates occur. Diurnal morphintern-iediates are expanded during ti-ic day but are not always fully expanded, andnocturnal morph-i intermediates arc sometimes expanded during ti-ic day, but usuallyat very low levels of expansion. Internmediates provide a substantial middle grounditt ti-ic nocturnal/diurnal ciassi fications.

Environmental effects also play a role in blurring ti-ic (histinction between ti-icmorphs. The cluster analysis of the Galeta Island colonies suggested tl-iat ti-ic

NOCTU RNALFIELDN'238 (14)

SCLERACTI NIAN ACTIVITY CYCLES 201

10 •¿� DIURNAL DIURNALLAB FIELD

@ N:299 (8) N: 287 (17)

0.5

>-0zUiD .0Ui

U-

0.5

EXPANSION STATE

FIGURE 3. Effects of the laboratory environment on daytime expansion behavior. Frequet-icy distributions of expansion behavior are presented for colonies from Portobelo, whichwere observed iti the field, at-id for a second set of Portobelo colonies which were maintainedin sea tables at the Galeta Marine Laboratory. Separate distributions are Presented for thet\vo niorphs. N indicates the total number of observations at-id ti-ic value in paretflheses indicatesthe number of colonies observed.

diurnal morph colonies could be divided it-ito tivo sttbgroups @vhuich ha(l a level of

association of 0.64. Those sul)grou@)s corresponded very strongly with ti-ic distribution of ti-ic coiot-iies. M. caz'ernosa colonies at Gaicta Island occur pre

(lominatftly in two localities each-i of which is subject to differing amounts of waveaction. TI-ic colonies front these different areas cluster togeth-ier. Although ti-ic

@roxit-iuityof ti-ic corals to each-iother and their situihar appearatces suggests a strongdegree of relationshil) @vithunareas, ti-ic existence of etivirotmnental tuodificatioti is@L(histinct possii)iiitv.

A sccon(l line of cvi(lcncc for at-i environmental effect is to be found in acotuparison of ti-ic davtimuc observations of Portobelo colonies from-i-i ti-ic field and

in ti-ic laboratory. Ti-ic ial)eiied colonies in ti-ic field at-id those collected for seatable observations were 1)0th-ichosen in at-i essentially randotu fashion, and shouldwithin sampIirtg error have similar behavioral patterns. Among ti-ic nocturnalcolonies, which are hardly ever expanded dntritug ti-ic (lay, this is m(lee(l ti-ic case.However, ti-ic expansion patterm-is of ti-ic field and hal) diurnal morph colonies differsignificantly (x2 test, P < 0.001) (Fig. 3). Laboratory colonies expanded asfrequently as ti-ic field colonies, but when expanded ti-ic ial)Oratory colonies were morefully expan(led. This cat-i be seen in the relative proportions of expansion scores of 1and 2 versus those of 3 at-id 4 im-iFigure 3. \Vhile the differences between ti-iclaboratory and field environments do not affect (haytimue expansion itself, they doapparently inhibit the degree of expansion.

During ti-ic nigh-it, ti-ic laboratory environment inhibits expansion. Korbiski

0 I 2 3 4 0 I 2 3 4

NOCTURNALLABN'517 (15)

202 HOWARD R. LASKER

Reef colonies observed in the field were fully expanded (luring ti-ic nigh-it (Table I)and qualitative observations at Galeta Island and at oth-ier localities indicate that inthe field ain-iost all colonies of M. cavernosa are fully expanded at night. In ti-iclaboratory, however, fewer colonies of both t-iiorphs were expanded, and colonieswere frequentiv only partially expanded. In ti-ic field there were no nightime differences between ti-ic niorphs, 1)ut at night in ti-ic lai)oratory ti-ic diurnal morphwas less frequently expanded ti-ian ti-ic nocturnal nmorph (x2 test, P < 0.001).This indicates that ti-ic diurnal morph was nuore strongly affected 1w ti-ic laboratoryenvironment.

The preset-ice of ti-ic intermediates and of environmental effects makes itimpossible to present a statistically homogeneous ch-iaractcrization of ti-ic behaviorsof ti-ic two morphs. As seen in Figure 3, distributiot-is from different environmentsdiffer from-i-ieach-i other and itt oth-ier cases colonies within the sam-i-iclocality at-idmorph can be font-id to have significantly differcmit expansion patterns. It is possible, however, to describe generalized patterns for ti-ic muorphs. Ti-ic frequency (histributions of daytime expansion behavior of four representative colonies are presented in Figure 4.

Effects of altered light regimes

The results of altering ti-ic daily high-it cycle are illustrated in Figures 5 at-id 6.As can be seen, ti-ic exl)erit-i-ients (lenlotstratc rather drat-iiaticahly thuat ti-ic nocturnalmorph cues its contraction to ti-ic presence of light. In ti-ic darkening experituent

@::L315@353b

Ui (0 —¿�SB—3I6 SB—333

U

I 2 I 41 3 I I

EXPANSION STATE

FIGURE4. Distribution of expansion states occurring within the niorphs of M. caz'eriwsa.Frequency distributions are presented for the daytime expansion behaviors of colonies representative of the end member and intermediate conditions of the diurnal (SB-315 and SB-353h)and nocturnal (SB-316 and SB-333) morphs.

SCLERACTINIAN ACTIVITY CYCLES 203

4. I

3,

z0U)za.w

I I I I I I 1 I I0@ 0 0 00@ 0 0 00 —¿� c,J to ‘¿�@‘

TIME

FIGURE 5. Effects of darkness on daytime expansion. Means with standard errors areplotted for the t@eansof 5 replicate tests of eaclu of 9 diurnal ( I) ) am-id25 nocturnal ( N)colonies which were shaded from all light for a 120 mit-i period at midday. Periods of (larkness and light are indicated by the shaded bar at the top of ti-ic graph.

(Fig. 5) there is a muarkedincreaseitt cxl)ansionof ti-icnocturnal tuorph inmiediatciv after ti-ic colonies are shade(i. Observations in(hicate th-iat this expansiontook place l)rim-iariiy during ti-ic first 30 i-i—inof (larkmwss l)ut contimuued through ti-icfollowing 30 mimi period. \Vithin minutes after reexopsure to shaded sunlightti-ic nocturnal morph colonies began to contract. Most of ti-ic contraction occurre(iwithin ti-ic first 10 mum of light, but ti-ic tren(l continued ti-ic first hour, at whichtin-ic ti-ic colonies reached their daytime level of expansion.

The nocturnal morpi-i colonies exhil)ite(1 ti-ic sat-i-ic light response mi ti-ic eveningexperinmetuts (Fig. 6). In those cxpcrit-i-ients lighting led to a decrease in expansion. Ti-ic light levels, which approxin-iated (lawn lighting, did not, however,cause ti-ic nocturnal morph-i colonies to return to full daytimue contraction. Afterti-ic high-itswere extinguished, ti-ic contracted colonies slowly expanded to ti-ic prelighting condition.

In both-i cxperit-i-ients ti-ic expansion of ti-ic diurnal muuorphremiuained alnuost constat-it. However, there were distinct, though small, high-it effects ott ti-ic diurnalmuorpl-ias well as ott the nocturnal. It-i ti-ic (Iavtinue darkening experiments a slightincrease in expansion occurred in ti-ic (hark condition. That increase was reversedwhien ti-ic colonies were returned to natural lightit-ig. Similarly, there was a (lecreasein expansion during ti-ic light l)eriod of ti-ic nightimuc experiments afl(l ti-iat too wasreversed when ti-ic colonies were returned to natural lighting. It appears that1)0th-i i-i-iorphs cam-i setse and react to relatively low light intensities. Ti-ic effect

of high-iton ti-ic diurnal morph. however, causes only a shighit decrease in poiyp

D

N

204 HOWARD R. LASKER

4-

z3-0

U)z @2-a.

Ui

I I I I I I I I I I0@ 0 0 00 0 0 00 - C@J @()CsJ C@J C'J C'J

TIME

FIGURE6. Effects of lighting on nighttime expansion. Means with statdard errors areplotted for the means of 5 replicate tests of each of 9 diurnal (D) and 25 nocturnal ( N)colonies which were exposed to 120 mm of low level light during the night. Periods of darkness and light are indicated by the shaded bar at the top of the graph.

expansion while in thic nocturnal mimorph ti-ic high-it in(luce(l contraction is almost

conui)letc.

Effects of J)CMU

The results of ti-ic DCMU experim-iuci-itsare i)resemted in Figure 7. As is evident,ti-ic DCMU has no effect on expansion. Shick at-id Brown (1977) have argued thatphotosyt-iti-ietic products like oxygen may mediate expansion in sytubiotic coelente

rates. In otler corals DCMU is kmtown to inl-iibit ithotosyntl-iesis (Vandermuuelcn,Davis, and Muscatine, 1972), and respiromuietric tucasurement of a M. cavernosacolony treated with DCMU resulted in a 94% (±6%) decrease in gross prim-i-iarypro(luctivity. Ti-ic failure of DCMU to affect expansion despite its inhibition ofphotosynthesis suggests that, under laboratory conditions, phuotosyt-iti-ictic products

are not n-iportant itt ti-ic i)roxinual control of (laytimue expansion.

Discussiox

Ti-ic experituentai results indicate that under nort'nal conditions ti-ic additionof DCMU and ti-ic subsequent inhibition of photosynthesis does not affect daytimeexpansion. This result, itt concert with the altered high-itexperiments, suggests thatat ti-ic proximal level expansion behavior is controlled by direct light sensing andnot by the sensing of a photosynthetic product.

SCLERACTINIAN ACTIVITY CYCLES 205

4

3

2

z0Cr,za.xw

‘¿�190 80TIME (mm)

FIGURE 7. Effects of I)CMU on daytme expanson. Means and standar(l errors for thebehavior of 15 diurnal morph colonies which were exposed to I)CMU. The colonies werekept in aerated sea water in shaded sunlight throughout the experiment. The I)CMU was

added at the time marked by the arrow.

Although flue production of photosynthetic products (hoes not control expanSi011 per se, the zooxanthelhae and presmlnlah)hy their products can be shown to he

of nuajor iniportance to daytime expansion. M. caz'ernosa, like other corals, expelsits zooxanthuehlae when subjected to extrenies of sahinit@, temperature. light atudother physical paratuieters (see, for instance, Goreau. 1964). Colonies usually(10 not expel all of their zooxanthehlae, hut they (ho take on a white bleachedappearance and regeneration of the zooxanthielhae population, if it occurs, requiresseveral months. In December 1976 one small region of a colony which @@-asbeingmonitored host its zooxanthuelhae an(l developed a distinct bleached appearance

FIGURE 8. Partial bleaching of a M. cavernosa colony. The colony, shown on the left, isapproximately 1 ni in height and was found at 8 m depth on the reef at Galeta Island. Thebleached area, shown in closeup on the right, does not have expanded polyps. Note that lightlypigmented polyps exluibit partial expansion.

Gross Primary Productivity(@g 0,-cm hr')

Light Intensity(@i E.m@.sec') J)iurnat Morph (N = 8) Nocturnat Morph (N = 8)

Expanded ContractedContracted25

931890*22.36

(2.01) 17.64 (1.20)28.07 (2.53)41.75 (2.78)9.78

(1.59)21.63 (1.42)31.48 (2.62)

206 HOWARD R. LASKER

TABLE II

Gross primary productivity. Mean gross primary productivity (E one standard error) for expandedand contracted colonies of the two morphs of Montastrea cavernosa.

* N = 10.

(Fig. 8). TI-icbleachingepiso(icoccurre(lduringa nine day i)eriodof heavywaveaction during which oi)scrvations could not be made. After ti-ic appearance of thebleacl-ied area, ti-ic pigmemted portion of ti-ic colony continued to expand during ti-icday as it always had. Ti-ic bleached section, however, no longer expanded duringtile day, but did expand at nigh-it. As ti-ic bleached area slowly developed son-icpigmentation, it also began to exhibit sot-i-ic daytime expansion. Ti-ic (legrec ofdaytime expansion increased as ti-ic degree of pigmentation increased. The colonycottinue(l to expand nocturnally throughout this tituc period, and in all otherrespects behaved nornahly. TI-ic loss of the daytinue expansion appears, therefore,to have been integrally linked to ti-ic absence of zooxanthellac. This sam-i-icsequencehas beet-i observed it other colonies frequently involving areas as stuall as a singleP0lYi). In all of these cases ti-ic poly'ps appeared otherwise hcalthiy but nighttinueexpansion data arc avaialable only for ti-ic single case. TI-ic presence of zooxatthcllac apparently has a definite effect on M. cavernosa's expansion behavior even ifthic zooxanthehiae (ho not control expansion behavior on a day to (hay basis.

The short-term effect of ti-ic zooxanthehiac as deduced from-i-iti-ic DCMU cxperiments an(l ti-ic longer tern-i effects implied 1))' ti-ic behavior of partially bleachedcolonies are, at first inspection, contradictory. Pearse ( 1974) described a simuilarsituation amuong individuals of A. elegantissiina. SI-icnote(i that bleached individualsretained a diurnal expansion rhythm, unlike ti-ic naturally occurring aposytuubionts,and si-ic suggested that ti-ic retained behavior had been entrained in ti-ic previouslysymi)iotic individuals. Her hypothesis also explains ti-ic failure of DCMU to haveany effect on M. cavernosa. If M. cavernosa colonies also develop an entrained daytime expansion response, ti-ic DCMU experimucnts would have occurred over tooshort a tim-i-icperiod to detect any change in behavior. Ti-ic maximum of nit-ic dayswhich was required for ti-ic colony described above to have host its expansion l)ehavior suggests ti-iat the tin-ic required for M. cavernosa to overcotue the entrainedresponse is relatively shuort.

Ti-ic long-tert'n imuiportance of piotosynticsus to the diurnal behavior is furthersupported by the distribution of daytinue expansion over depthi. Observation of592 colonies in ti-ic Islas San Bias failed to produce a single observation of (haytinieeXi)amlsion below 20 mn (Lasker, 1977). Increased depth corresponds with (he

SCLERACTINIAN ACTIVITY CYCLES 207

creased light and with-i reduced photosynthesis. This suggests that ti-ic diurnalbehavior, if it is based on primary @)roductivity, is sensitive not only to ti-ic prcsencc or absence of photosynthesis but also to its absolute tuagnitude. A dependenceon son-ic tuinitual l)hlotosynthctic rate may explain ti-ic absetuce of ti-ic daytinc expansioI-i in ti-ic nocturnal nuorpl-i which, though photosynthetic. is not as productiveas ti-ic diurnal morph ( Table II).

Thie final lit-ic of evidence su@)porting a mo(lcl of photos@'nthcticaily controlledexpansion behavior is to be found in ti-ic results of a series of colony transi)latt

experiments which were started in February 1977. At that tim-i-icseven colonieswere transi)lanted from 2 to 14 ni and vice versa. Eacht of ti-ic colonies transplantedwas one of a Sit) pair. Ti-ic sib, a morphologically identical colons' occurring ontile sante ancestral corallum i)ut now separated l)y a dca(l or overgrown area, wasleft at its original deptl-i. Ti-ic expansion behaviors of ti-ic 5i1)5 were comupared atmonthly intervals over ti-ic following six months and again after 18 tuonths. Ti-iccolonies transplanted to shallow water showed no change in behavior, but of ti-iccolonies transplanted to deep water, th-iree showe(l a significant (lecrcasc in cxpansion behavior (randomuization test, (Siegel, 1956) P < 0.05). Possibly ti-ic (Iecp

water nocturnal morph colonies which naturally luave lower rates of @)hotosynthesus(Lasker, 1978and Table II) coul(lnot develop(laytimeexpansioneven in a highlight environiucnt. On ti-ic other han(I, ti-ic shallow water (Iiurnal nuorph colonies,when derprived of suffcient light, ceased daytinic expansion.

Oti-ier inter- at-id intraspecific comparisons of coelcnterates with simuilar (lichotomies of l)ehavior have associated (havtimuc expansion with ti-ic presence of symubionts (Kawaguti, 1937 ; Pearse, 1974 : Gladfelter, 1975 : Sehens and de Riemuer,1977 ) . Although nuorphs of Ill. caz'ernosa are synubiotic, similar argunuents iuaystill be applic(i to their (liffering expansion l)ehavuors.

TI-ic presence of expansion in synul)iotic coelenterates l-ias 1)ecnll)reviously attribute(i to an expansion related itcrease in @)hotosynthesis (Laskcr. 1977 ; Sebens andde Rictuer. 1977) . It i-ias also beet-i hypothesized that ti-ic lack of zooxanthehiacand therefore, photosynthesis, makes (iavtimuc expansion disadvantageous for muostspecies. This of course itu-iplies a “¿�cost―of expansion. Ti-ic i)rimcii)ai argumuent forthese hypothesized costs and benefits of expansion are ti-ic (listributions of ti-iczooxanti-icilac and ti-ic observed activity i)atterts themselves. Unfortunately, fewdata have been presented which directly document ti-ic existence of ti-ic costs andbenefits.

One advantage of daytime expansion relates to ti-ic rate of photos'tthesisoccurring within ti-ic polyps. Much of ti-ic tissue of a polyp which is exposedto direct sunlight in ti-ic expanded state is shaded when ti-ic polyp is contracted.In Al. caz'ernosa an increase in gross primuary productivity associated with expansion l-ias been ol)scrved (Table II, Mann Whitney U-test, P < 0.05). Similarly,Kanwisher and Wainwright (1967) and Svoboda (1978) i-iavc reported tiuat oxygen production in soft corals is greatest wi-icn ti-ic colony is expanded.

Ti-ic nature of ti-ic costs of expansion are less clear ti-ian ti-ic benefits. Energeticcosts, daytime l)re(iation on expanded polyps, and nitrogen conservation have beenconsidered by either Lasker (1977) or Sebens and de Rietuuer (1977). Scbens andde Ricnuer (1977) have noted that lack of evidence for differential predation onexpanded poiyps, and field observations made in thic course of this study suggest

208 HOWARD R. LASKER

that species expanded during ti-ic day arc no more heavily preyed upon than contracted species. However, ti-ic differences between expanded at-id contractedspecies may also inciu(Ie ott-icr types of anti-predator adaptations. Until morestudies arc carried out on ti-ic natttre and extent of predation on corals it isitui)Ossibic to dismiss a predator-related cost of expansion.

Daytime contraction tuay also be a nutrient conserving adaptation and Scbensat-id dc Riemer ( 1977) have argued that nitrogen conservation n-iay be ti-ic basis forthe observed did activity patterns of reef antl-iozoans. Again, however, there isno direct evidence for or against this hypothesis. In M. cavernosa ti-ic noctttrnalmorph, which is ti-ic superior zooplankton predator ( Lasker, 1976) , does not expandduring ti-ic day while ti-ic diurnal nuorph does. If nitrogen is a limiting resourceand if expansion does incur a nitrogen loss, one might predict that ti-ic diurnalmorph, which is less adept at capturing prey and should therefore be ut(her greaternitrogen stress, would be less likely to expand during the day. It iuay i)e the casethat daytitue expansion by ti-ic diurnal Iuor1)h results in a net nitrogen gain throughthe cal)tttrc of dctrital matter.

Energetic costs of expansion have been noted ( Pcarse, 1974 ; johtannes andTcplev, 1974 ; Lasker, 1977 ; Schcns at-id de Riemer, 1977). Ahthough expansionmay involve several (iifferent costs, ti-ic only cost which has been measured to dateis ti-ic increased respiration of expanded polyps. Increased respiration rates havei)cen reported for ti-ic expanded polyps of Anthro/'leura elegantissiiniiia ( Buch-isbaum, 1968) an(l for It!. caz'ernosa ( Lasker, 1978) . Johannes at-id Tcpley (1974)l)resentcd data suggesting ti-ic sat-i-ic is true of Porites lobata. Simuuilariy, resl)iromuetric imucreases related to expansion have been reported for several aposyn-ibioticSi)CCics of coelenterate ( Brafleid an(i Chapman, 1965, 1967 ; Newell and North

craft, 1967).Al. caz'ernosa, like other symui)iotic coelenterates, exhibits characteristics demuuon

strating ti-ic existence of expansion related costs and benefits. It-i Or(ier to explainthe differing i)eh-iaviors of ti-ic two iuorphs it is necessary to fit-id differences in ti-iccosts amd/or benefits of expansion for the two niorphs. Although-i both muorphs

of Al. cavernosa have zooxanthellac, there arc differences in ti-ic distrii)ution ofthe zooxanthellac arid il-i their photos)'nthetic capabilities, which affect ti-ic valueof (Iaytimc expansion.

In colonies frotu shallow water (10 muor less) poi@'ps of ti-ic diurnal iuorph havegreater numbers of zooxantheilac than do those of ti-ic nocturnal muorph (Lasker,1978). A large proportion of ti-ic polyps' zooxanthellac are shaded in ti-ic contractedstate (Laker, 1978) and expansion increases gross photosynthesis.

Calculations based oi-i m-i-icasuredpi-iotosyt-iti-ictuc rates of whole colonies and onzooxanthehlae concentrations within ti-ic two nuorphs reveal that ti-ic increase ingross prituary productivity (GPP) effected by expansion is greater for the diurnalmorph-i ti-ian ti-ic nocturnal n-iorpi-i (Laskcr, 1978). However, in ti-ic case of bothtuorpi-is ti-ic expansion induced increase in respiration is even greater ti-ian ti-icincrease in GPP. TI-ic net effect of expansion is, ti-icrcfore, an energetic cost to ti-iccolony.

Tic occurrence of expansion despite its net energetic cost suggests tl-iat thebasis for the bci-iavior, though triggered by light, is not purely photosynthetic.However, ti-ic photosynthetic differences between ti-ic two morpiis and ti-ic presence

SCLERACTINIAN ACTIVITY CYCLES 209

of expansion in the diurnal morph (the morph with the greater photosyntheticrates) suggests that sonue minimal photosynthetic input is necessary before nonphotosynthetic advantages of expansion can be balanced against the energetic costof expansion. Such a view is further supported by the absence of expansion indeeper waters where photosynthesis is reduced and by the absence of expansionin portions of colonies which have expelled their zooxanthehhae. The differences inproductivity and behavior of the morphs clearly indicates the importance of photosynthesis in the costs and benefits which ultimately control expansion behavior.

I thank Ira Rubinoff, Director and Gordon L. Hendler of the SmithsonianTropical Research Institute, for nuaking available the facilities at the Galeta MarineLaboratory. Discussions with G. L. Hendher and K. Sebens and the comnuentsOf R. S. Ahberte, R. A. Ahher, T. J. M. Schiopf and two anonymous reviewers

have all been helpful and are appreciated. This research has been funded by theHenry Hinds Fund for Evolutionary Biology of the University of Chicago andNational Science Foundation Grant OCE 77—00148.

This paper has been abstracted from a Ph.D. thesis submitted to the Department of the Geophysical Sciences, University of Chicago.

SUMMARY

1. Colonies of M. cavernosa exhibit two separate types of activity cycle, one ofnighttinue expansion and one of night and daytime expansion. These activitycycles correspond to the nocturnal and diurnal nuorphs of this species.

2. At the operational level, light per se controls expansion beluavior. Coloniesare sensitive to light and react quickly to it. This sensivitiy is not, on the shortterm, dependent on photosynthesis. The reaction to light of both morphus is oneof contraction, but in the diurnal nuorph the contraction response is inhibited.

3. The inhibition of daytime contraction only occurs in the diurnal morph, whichhasa highrateofphotosynthesis,and onlyoccursabove20 nu (inPanama). Lossof zooxanthellae, or renuoval to deep water, both of which reduce photosynthesis,results in the loss of daytime expansion.

4. Although photosynthetically based higlut sensing is not involved in shortternu control of expansion behavior, colonies may measure their photosyntheticproduction, and if photosynthesis falls below sonue level, daytinue expansion ishalted. The sensing of conditions conducive to daytime expansion can occurwithinsnuallareasof a singlecolony.

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