MARINE ECOLOGY PROGRESS SERIES Vol. 148: 125-134, 1997 1 Published March 20 Mar Ecol Prog Ser

Quantification of / interactions in a physically stressed reef community, NE Colombia

L. A. M. ~erts',~,*.R. W. M. van soest2~**

'Institute de Investigaciones Marinas Punta de Betin, Santa Marta, Colombia ZInstitute of Systematics and Population Biology. University of Amsterdam. PO Box 94766, 1090 GT Amsterdam, The Netherlands

ABSTRACT. Coral reef are considered to be important space competitors. Competitive inter- actions between sponges and often result in overgrowth of the coral. It is assumed that sponges are even more successful in environments sub-optimal for corals. In order to test the hypothesis that coral overgrowth by reef sponges increases when corals are under stress, the frequency of sponge/ coral interactions was quantified along a gradient of physical stress. At 15 stations, encompassing 5 localities and 3 depths (5, 10 and 20 m) dlong the coast of Santa Marta (NE Colombia), the number and categories of interactions were scored in belt transrcts (10 X 1 m'). Four categories of interactions were distinguished. Physical factors such as sedimentation and visibility were measured. 21 coral and 95 sponge species were encountered In a total of 3866 spongc/coral interactions. Only 2.5";* (96 ~nteract~ons)consisted of ovcrgrowth of corals by sponges. The frequency of such overgrowth depended on the presence of pdrticular sponge specles, which appeared to be more aggressive towards corals In locahtlcs wlth hlgh coral cover, relatively low sedimentation and high visibility. Thus, we reject the hypothesis that coral overgro~vthby sponges occurs more frequently in localities under physical stress. Overgrowth was related to the presence of aggressive sponge specles, rather than to characteristics of the corals. It is concluded that reef sponges differ notably in their competitive abilities. Byinfluencing the sponge cornrnunlty coinposition on the reef, the physlcal environment may indirectly determine the extent of overgrowth of corals by sponges.

KEYWORDS: Interactions Overgrowth Physlcal stress Sponges . Coral reef - Caribbean

INTRODUCTION Intensively studied in the field. It appears that th.e structure of coral/coral interactions is not comp1,etely Space is a limiting resource for sessile organisms hierarchical, because the outcome depends on numer- living on hard substrata (Dayton 1971). This is espe- ous physical and biological factors (Bak et al. 1982, cially the case on coral reefs, which support a high Bradbury & Young 1983, Logan 1984). Mecha.nisms diversity of benthic fauna and flora (Connell 1976, operative in competition differ between coral species Jackson 1977). The ability of a benthic sessile species (reviewed in Lang & Chornesky 1990) and the com- to gain and hold space depends on its competitive petitive hierarchy of corals tends only to be transitive ability. Lang (1971, 1973) demonstrated the existence when the competing species employ similar competi- of an aggressive hierarchy among scleractinian corals. tlve mechanisms. This transitwe hierarchy breaks Since then, coral interspecific interactions have been down when the competing species are able to develop other competitive structures, for example sweeper tentacles, making the outcome of the encounters dependent both on the character of the competing 'Correspondence address: Institute of Systemclticsand Pop- ulation Biology, University of Amsterdam, PO Box 94766, species and the environment (Chornesky 1989). 1090 GT Amsterdam. The Netherlands. Although the ranking of competitive abilities between "E-mail: [email protected]~i.nl species often lacks a simple linear hierarchy, ranking

O Inter-Research 1997 Resale of full article no1 permitted 126 Mar Ecol Prog Ser 148: 125-134, 1997

between the major taxonomic groups is basically hier- relatively high sediment load through terrigenous archical (Russ 1982) effluents. Within the area there is a roughly defined In addition to interactions among themselves, corals gradient, in terms of increasing coral cover, from the frequently come into contact with sponges. In coral city of Santa Marta to the east. This is probably caused reef communities, sponges play an important role in by a decrease of continental run-off from the SW to the competition for space (Suchanek et al. 1983). Because NE (Zea 1994). Related to this gradient are an overall sponges lack special competitive organs such as decrease of coral cover and an increase of sponge mesenterial filaments and associated behaviour, they cover that have been observed over the past years, are thought to use their toxic substances in interaction especially around the city (Werding & Sanchez 1988, with other benthic organisms to actively gain and Zea 1994). This phenomenon can be explained by an maintain their positions on the substrata. Encounters increase of sediment and nutrient loads through exten- between sponges and corals usually result in damage sive deforestation (Zea & Duque 1989) and increased to the coral (Jackson & Buss 1975, Suchanek et al. garbage and raw sewage discharge (Escobar 1988, 1983, Sullivan et al. 1983), even in non contact situa- Cruz & Ramirez 1990). tions (Porter & Targett 1988). Some sponge species are In this study, the most important sources of physical able to occupy large reef areas at the expense of corals stress for corals along reefs were considered to be high (Vicente 1978, Riitzler & Muzik 1993). sedimentatton rates (Porter 1987, Rogers 1990) and As nutrients and sedimentation increase on coral low light conditions (Chalker et al. 1985). To test our reefs, the effect of sponges on corals is becoming hypothesis that coral overgrowth by sponges increases increasingly important. Nutrient enrichment may en- when corals are under stress, natural rates of en- hance benthic algal biomass and primary production counter between sponges and corals were quantified in the water column. Increased primary production along the existing gradient of physical stress. favors benthic filter-feeding organisms, which may out-compete corals (Pastorok & Bilyard 1985). Con- cerning nutrient and sediment increase, sponges and MATERIALS AND METHODS corals can be seen as opposites, with sponge biomass increasing and coral biomass decreasing in reefs with Study area. Fifteen stations, encompassin.g 5 locali- organic pollution and high sediment load (Chalker et ties along the coast of Santa Marta, NE Colombia al. 1985, Rogers 1990, Wilkinson & Cheshire 1990). (from west to east: Punta de Betin, El Morro, Granate, Increasing sedimentation can alter biological Chengue and Gairaca; see Fig, l),and 3 depths (5, 10 processes on a reef, such as interactions between and 20 m) were sampled for sponge/coral interactions organisms (Rogers 1990). Competition in reef corals and physical factors. involves investment of energy (Rinkevich & Loya 1985) and, because physical stress leads to a decline in bio- logical functions of corals (e.g. the recovery from damage; Meesters & Bak 1993), it seems likely that aggressive interactions between sponges and corals may increase and be more successful for sponges in physically stressed localities. The wide-spread over- growth of corals in Japanese reefs by the sponge Ter- pios hoshinotais assumed to occur especially in pollu- tion-stressed zones (Rutzler & Muzik 1993). However, studies on sponge/coral interactions investigated only the effect of individual sponge species and do not pro- vide evidence as to whether a competitive hierarchy exists between sponges and corals at a community level. In our study we hypothesize that coral stress, induced by environmental conditions, is advanta- SANTA geous to sponges, which benefit on a community level by overgrowing living coral. The reefs east of Santa Marta, NE Colombia, are par- ticularly suitable for testing this hypothesis. These coastal reefs are not as well developed as those in Fig. 1 Study area with sampling localit~es(Colombia). PB = other areas of the Caribbean (Von Prahl & Erhardt Punta de Betin. EM = El Morro. GR = Granate, CH = Chengue 1985), due to a combination of seasonal upwelling and and GA -Gairaca Aerts & van Soest: Sponge/coral interactions 127

Physical environment. Sedimentation rate was mea- Non-transformed and log-transformeddata of sedimen- sured using PVC sediment traps with a ratio between tation and visibility showed non-normality (checked length and diameter of 5:l (length: 30 cm, diameter: with Kolmogorov-Smirnov tests; Sokal & Rohlf 1981). 6 cm; as in Larsson et al. 1986).The traps (1 per station) Quantification of spongelcoral interactions. The were left in situ for periods of 2 mo between February quantification was carried out along belt transects. A 1993 and February 1994, resulting in 6 samples per 10 m line was attached to a randomly chosen point and station. The sedimentation data set of this study was stretched out parallel to the isobath of each depth expanded by adding the data of M. Kielman (pers. (5, 10, 20 m). Ten consecutive quadrats of 1 m2 were comm.),sampled in 1991 and 1992. The trap size and laid adjacent to the line. This procedure was repeated sampling method of these additional data were similar 3 times, resulting in a sam.pling area of 30 m2 at each to those described above. Sedimentation was expressed station. In total, 450 m2 were sampled for sponge/coral in g m-' d-l, dry weight. interactions. Because some coral species possess Visibility in the water column was measured at each sweeper tentacles, which can reach a maximum dis- locality using a 30 cm secchi disk. The measurements tance of 5 cm (Richardson et al. 1979), and sponges were carried out weekly, over a 1 pr period, at ap- are able to affect corals even in non contact situations proximately the same hour and under similar weather (Porter & Targett 1988), each sponge encountered conditions. within 5 cm from a coral was considered as a partner Differences in sedimentation rates between localities in an interaction. Four categories of interactions were were analysed using the Wilcoxon signed ranks test defined (Fig. 2): (Sokal & Rohlf 1981) taking depth and dates as blocks. A = overgrowth of living coral by sponges. For differences in depth the same test was used taking B = peripheral contact of sponge along and parallel localities and dates as blocks. Differences in visibility to the living coral for more than 3 cm. This cate- between the localities were also analysed with the gory involves those encounters in which the Wilcoxon signed ranks test, taking dates as blocks. sponge is obviously following the coral boundary.

Fig. 2. Photographs of the 4 categones of interaction. [A)overgrowth of the coral Diploria strigosa by the sponge Desmapsamrna anchorata;(B) peripheral contactof the sponge Rhaphidophlus venosus with the coral Montastrea cavernosa; (C) tissue contact of the sponge Niphates erecta with the coral M, cavernosa; (D)non contact interaction shown by the sponge Scopalina ruetzleri and the coral M. cavernosa Mar Ecol Prog Ser 148: 125-134, 1997

C = tissue contact; a sponge is in contact with the edge of a living coral over a distance less than 3 cm. This category involves those encounters in which contact seemed merely accidental. D = non contact; the sponge grows within 5 cm dis- tance of the living coral boundary. In each quadrat the total number of sponge individ- uals and coral colonies, the total coral perimeter for U PB EM GR CH GA each species and the total cover (in %) of sponges, N corals and sand were noted. The interacting sponge Localities E and coral species were identified and the size of the interacting sponge (in cm2) was measured. In each interaction the affected coral area (in cm2; only for cat- egory A), the extent of interaction (in cm; for B and C) and the distance between the sponge and coral (in cm; only for D) were recorded. To test whether a relation existed between the fre- quency of a certain category of interaction and sponge and coral cover, a multiple regression was used. There 5 10 20 was no relation between the 2 independent variables, Depth sponge and coral cover (simple regression test). To normalise the data, the number of interactions and the Fig. 3. Median of sedimentation rates in y m-2 d-' for (A) localities and (B)depth. Abbreviations of localities as in Fig. 1 sponge and coral cover were log-transformed (logx). Every 10 m2 survey was used as a sample unit, result- ing in 3 replicates at each station. Differences between d-'. In March 1993, due to the influences of a trop~cal regression slopes were tested with the GT2-method storm, sedimentation rates ranged from 22 to 983 g m-' and Gabriel's approximate method (Sokal & Rohlf 1981). d-'. The non-parametric median is used because of the Percentages of overgrowth were calculated from the few high sedimentation rates. total number of interactions (= categories A, B, C, D) Visibility ranged from 4 to 22 m. Two groups of lo- using every 30 m2 survey as a sample unit. These calities could be distinguished: the group with lowest percentages were arcsin-transformed and tested on visibility consisted of PB and EM and the group with differences between depth and localities with a single highest visibility consisted of GR, CH and GA (p < 0.01; classification ANOVA and the T-method. Bartlett's test Fig. 4). was used to test the homogeneity of the sample vari- ances (Sokal & Rohlf 1981). Quantification of spongelcoral interactions

RESULTS Interactions in general

Physical environment There were 95 sponge species and 21 coral species engaged in sponge/coral interactions. A total of 3866 Sedimentation rates fl.uctuated greatly throughout interactions was scored: 96 (2.5%) overgrowths, 670 the year and between years. Seasonal changes, such as the rainy and dry seasons, caused fluctuations of sedi- mentation rates within a year. Depending on the extent of rainfall, wind force and the prevailing wind direc- tion, the sedimentatlon rate and visibility varied for each locality and depth within seasons. Due to these annual and seasonal fluctuations, analyses were carried out with dates as blocks. Sedimentation was significantly higher in the westernmost locality (PB) than in the other localities (p < 0.01; Fig. 3A). Between Pi3 EM GR CH GA depths, the sedimentation was significantly higher at Localities 5 m than at 10 and 20 m (p < 0.001; Fig. 3B). The Fig. 4. Mean visibility in meters for each locality. Abbrevia- 'normal' sedimentation rate ranged from 4 to 247 g m-' tions of localities as in Fig. 1 Aerts & van Soest Sponge/coral~nteractions 129

Table 1 Percentage occurrence of each interaction category foreach sponge and coral species. A: overgrowth;B: peripheral contact;C: tissue contact;D: non contact.n: total number of interactions.Species with less than 5 intel-actionswere omitted

CDn BCDn

Sponge species laevis 0.5 Acanthella cubensls Mycale laxissima Acarnus nicolae Mycale sp. Agelas clathrodes Myxillldae Agelas conifera Neofibular~anolitangere Agelas sp. 1 Nlphates dlgitalls Agelas sp. 2 N~phateserecta 2.5 Aka cachacrouensls Plei-aplysillasp. Anthosigrnella vanans Polymastia tenax Aplysilla sp. Pseudoceratlna crassa Aplysina ca uliforrnis Rhaphidophlusisodictyoides Aplysina fistularis Rhaphidophlusmin U tus Artemisinamelana Rhaphidophlus venosus 0.2 Axinyssa an]brosia Scopalina ruetzlen 0.7 Axinyssa flavolivescens Spirastrella coccinea Ba tzella rosea Terpios belindae Batzella sp. Terpios sp- Callyspongiaarrnigera Topsentia ophiraphiditis Callyspongia vaginalis Verongularigida Clathria affinis Xestospongia caminata Clathria echinata Xestospongia rnuta 5.7 Clathria sp. 1 Xestospongiaproxima Clathria sp. 2 Clathria sp. 3 Coral species Clathria spinosa Acropora palrnata Cliona sp. Agarlcla agaricites 4 Coelosphaerasp. Agarlc~alamarckii Desmapsammaanchorata Colpophyllia natans Discoderma dissoluta Dichocoeniastokes1 6.3 Dragmaxia sp. Diploria la byrjnthiformis Dysidea etheria Diploria strigosa 1.8 Eurypon laughlini Helioseris cucullata Eurjpon sp. hadracisdecactis 3.7 Forccbpia sp. Madracis pharensis Habclona in~plexiformis MiUepora sp. 8.2 Haliclona sp. Montastrea annularis 2.2 Halisarca caerulea Montastrea cavernosa 0.7 Iotrochota birotulata Meandnna meandrites 6 Ircinia carnpana Mycelophylllaferox lrcinia felix Pontes astreoides 2.2 lrcinia strobilina Scolymia lacera 2.6 Monanchora arbuscula Siderastrea siderea 10.6 Mycale diversisigrnata Stephanocoenjamlchelinii 3

(17.3 %) peripheral contact, 1255 (32.5%) tissue contact sponge species with a certain frequency are shown for and 1845 (47.7%) non contact interactions. In Table 1 each category of interaction (Fig 5). Concerning over- the total number of interactions and the frequency of growth and peripheral contact, most sponge species each category of interaction are given for each sponge display frequencies which correspond to the mean fre- and coral species. All sponge species except 1 were quencies and only a few species show very high or encountered in non contact interactions (n = 63).Over- very low frequencies. For tissue contact and non con- growth occurred in 16 species, peripheral contact in tact interactions, the difference between the number of 52 species and tissue contact in 57 species (see Fig. 5). sponge species with mean frequencies and wlth higher Because the above-mentloned percentages are or lower frequencies is much smaller. Sponges wlth ex- derived from the total number of interactions scored, tremely low or high frequencies of a certaln interaction they can be regarded as 'mean' frequencies for each category were mostly those species with only 6 to 8 interaction category. To demonstrate differences in interactions. Exceptions were the sponges Mycale these mean frequencies displayed by individual laevjs, with 182 interactions of which 61.5% consisted sponge species involved in interactions, the number of of peripheral contact and 10.4% of non contact interac- Mar Ecol Prog Ser 148: 125-134, 1997

tions, and Desmapsamma anchorata, with 37.1 % over- ,,,. non contact growth out of 89 interactions. I I non contact + The frequency of peripheral contact, tissue contact - -0- - and non contact interactions is related to the density of t~ssuecontact - - both corals and sponges, as is shown by the positive tissue contact % regression coefficients for sponge and coral cover (p < peripheral contact - +. 0.001; see Table 2). Overgrowth was not related to peripheral contact 1 1 sponge and coral cover (p > 0.05). In contrast with the other interaction categories, the frequency of over- 0.0 0.2 0.4 0.6 0.8 1.0 growth seemed to be due to factors other than sponge Regression slope and coral cover. To determine the relative magnitude of the effects of sponge and coral cover on the number Fig. 6. Regression slopes and 95 % confidence intervals for each category of interaction with sponge cover (%) and of peripheral contact, tissue contact and non contact coral cover (d). Slopes- are significantly different at the interactions, differences between regression coeffi- 0.05 level iftheir intervals do not overlap cients were tested for significance. For tissue and non contact interactions the regression coefficient of sponge cover was significantly higher than the regres- cover. For the frequency of peripheral contact interac- sion coefficient of coral cover (Fig. 6). This means that tions there is no difference in effect of sponge and the frequency of tissue contact and non contact inter- coral cover. actions is determined more by sponge than by coral

Overgrowth by sponges Table 2. Results of multiple regression analysis of sponge and coral cover on number of interactions. Regression lines were fitted to the linear model: log(no. of interactions) = a + The occurrence of overgrowth was tested for simi- blog(sponge cover) + clog(cora1 cover), where a is a con- larities between depths and localities to determine its stant and b and c are the slopes of sponge and coral cover, relation with the physical environment. There was a respectively. R~scoefficient of determination; p is probability that rejection of the hypothesis that both slopes are equal significantly higher frequency of overgrowth at 5 m to zero is incorrect; n is number of data points compared to 20 m (p c 0.05; Fig. 7A),which corre- sponds with a higher sedimentation load at 5 m (Fig 3B). However, no significant difference in over- growth was found between 5 and 10 m depths. Also, no Overgrowth -0.13 0.13 0 23 0.06 0.277 43 significant difference in the frequency of overgrowth Peripheral growth -0.18 0.55 0.75 0.58 <0.001 45 Tissue contact 0.64 0.60 0.28 0.56 <0.001 44 could be detected between localities (Fig. ?B), al- Non contact 0.62 0.71 0.35 0.59 <0.001 45 though Punta de Betin is the most stressed locality con- cerning sedimentation load and visibility (Figs. 3A & 4).

0 5 10 15 20 25 0 5 10 15 20 25 Number of species

Fig. 5. Frequencies of interaction category displayed by sponge species encountered In interactions. (A)overgrowth; (B)penph- era1 contact; (C) tissue contact; (D)non contact. The number of sponge species involved in each interaction category is shown In parentheses. Frequencies were ordered in classes with increments of 10%. For each category of interact~onthe vertical axis shows the frequency classes and the horizontal axis the number of sponge species with frequencies within a certain class Aerts & van Soest: Sponge/coral ~nteractions 131

palina ruetzleri the least. Corals most affected by sponge overgrowth were the species Siderastrea siderea and the genus Millepora. Least affected were the corals Mon tastrea ca vernosa and Diploria strigosa. To determine if the frequency of aggressiveness is related to the presence of particular sponge or coral species, the occurrence of sponge individuals and the coral perimeter were compared fol- species and depth P - 5 10 20 (Figs. 8 & 9) In Desn~apsamrnaanchorata, the most F Depth (m) aggressive sponge species, 78.7%) of all individuals occur at 5 m depth (Fig. 8). The aggressive sponge spe- cies Aplysina fistularisand Callyspongia arrnigera also reach their highest densities at 5 m depth, with respec- tively 97.3 and 66.7% of all sponge individuals. The coral specles most affected by overgrowth of sponges, Siderastrea siderea and Millepol-a sp., also mainly occur at 5 m (Fig. 9). Most sponge species were aggressive towards more than 1 coral species. Susceptibility of corals to over- Localities

growth by sponges~ - varies in a species-specific manner Fig. 7. Percentage overgrowth (+ SE) from total number of Encounters between particular sponge and coral spe- interactions for (A) depth (n = 5) and (B)localities (n = 3). cies depended on the distribution of those sponge and Abbrev~ationsof localities as in Fig. 1 coral species. The frequency of overgrowth was related to the presence of aggressive sponge species, Apparently, there is no clear relation between occur- rather than to characteristics of corals. rence of overgrowth and physical stress. Since there Until this point we included all sponge species when are some obvious differences in coral overgrowth be- looking at differences in frequency of overgrowth tween sponge species and in coral species overgrown between localities and depth. However, since fre- by sponges (Table l), the sponge and coral species quency of overgrowth depends on the presence of composition may determine the higher frequency of aggressive sponge species, this obfuscates the relation overgrowth at 5 m. The sponges Desrnapsamma between physical environment and frequency of over- anchorata, Callyspongiaarmigera and Aplysina cauli- growth. To determine if overgrowth occurred more formis for example displayed the most overgrowths frequently in physically stressed localities we focussed and Rhaphidophlus venosus, Mycale laevisand Sco- on the aggressive sponge species Desmapsamma

Fig. 8. Percentage occurrence from total number of sponges for each depth and sponge species. ACLA= Agelas clathrodes; Fig. 9. Percentage occurrence from total perimeter for each ACON = Agelas conifera;ACAU = Aplysina cauliformls; AFIS depth and coral species. AAGA = Agarlcia agaricites; DSTO = = Aplysina fistularis; AVAR = Anthosigmella varians; CARM = Dichocoenia stokesi; DSTR = Diploria strigosa; MDEC = Callyspongia armlgera; DANC = Desmapsamma anchorata; Madracjs decactis; MSP = Millepora sp.;MANN = Montastrea DETH = Dys~deaetheria; lFEL = Ircinia fel~x,ISTR = Ircinia annular~s; MCAV = Montastrea cavernosa; MMEA = strobilina; MLAE = ; NERE = N~phateserects; Meandrlna ~neandrites;PAST = astreoides; SL,\C = RVEN = Rhaphidophlus venosus; SRUE= Scopaljna ruetzleri; Scolymla lacera; SSlD = Siderdstrea s~derea;and SMlC = and XMUT= Xestospongia muta Stephanocoen~amichelini Mar Ecol Prog Ser

damage and growth inhibition of algal thallae were C] coral cover 1 overgrowth observed at the periphery of, or at short distance from, a coral (De Ruyter van Steveninck et al. 1988). If the neighboring organism is a sponge competing by means of toxic chemicals, inflicting damage could have a reverse effect because damaged sponges release increased levels of secondary metabolites (Thompson 1985). In our study no visible negative effects on sponges or corals were observed in peripheral, tissue Fig. 10. Frequency of overgrowth (in %) from total number of or non contact interactions. The actual competitive interactions of the sponge Desmapsamma dnchorata and event of sponge/coral interaction may result in an coral cover (in %. + SE) for the localities Punta de Betin (PB. equilibrium through growth inhibition of both organ- most stressed), El Morro (EM, intermediately stressed) and Chenyue (CH, least stressed) at 5 m depth. At Granate this isms (Karlson 1980). sponge was not recorded and at Gairaca there was only 1 The growth forms of partners in interaction is im- interaction portant in spatial competition (Lang 1973) and can determine the frequency of specific categories of interactions. Massive sponge species, displayed more anchorata.Coral overgrowth by this species and mean peripheral contact than branched speci.es, as IS shown coral cover at 5 m depth are shown for the localities by the massive species Ircinia strobilina and the PB (highest sedimentation and low visibility; most branched species Aplysina cauliformis,with respec- stressed locality), CH (low sedimentation and high tively 31.3 and 3.3% of peripheral contact. Supposedly, visibility; least stressed) and EM (low sedimentation, encrusting and massive species will be more effective low visibility; intermediately stressed). Coral cover was than branching species in gaining space by means of significantly highest at CH and lowest at PB, but overgrowth, because branching species can avoid overgrowth occurred more often in CH (Fig. 10). competition by 'escaping in height' (Meesters et al. Apparently the frequency of overgrowth is not related 1996).However, growth form is not the most important to stress. On the contrary, the sponge D. anchoratawas feature in determining the frequency of overgrowth. more frequently engaged in aggressive encounters The sponge species Desmapsanlrna anchorata and A. in localities with relatively less stress and h~ghcoral cauliformis were the 2 most aggressive species, cover. despite their ability to 'escape in height'. The ability to overgrow corals may depend on the possession of spe- cific characteristics which vary between species. The DISCUSSION possession of toxic secondary metabolites is consid- ered to be a favourable feature in competition for Nature of sponge/coral interactions space, but possession of toxic substances does not automatically imply use in competition for space. The Sponges are reported to be competitively dominant toxic activity can be very specific, as is shown in vari- over corals (Jackson & Buss 1975, Vicente 1978, Such- ous bioassay studies (Bakus et al. 1990, Green et al. anek et al. 1983, Sullivan et al. 1983, Porter & Targett 1990). The aggressive sponge species A. cauliformis1s 1988, Riitzler & Muzik 1993). However, the first study known to possess toxic chemicals demonstrating quantifying sponge/coral interactions on a community antiviral activity (Gunasekera et al. 1991). The sponge level (our study) shows only 2.5% of all sponge/coral D. anchorata also possesses unusual organic mole- encounters to be directly aggressive, i.e. overgrowth cules, e.g. alkylglycerol monoethers (Quijano et al. of corals by sponges. Sponge/coral interactions oc- 1994), and it was the sponge species most aggressive curring most frequently were, in decreasing order towards corals. Whether D. anchorata, A. cauliformis of occurence, (1) non contact, (2) tissue contact. or other sponge species use their secondary metabo- (3) peripheral contact. The degree and quality of inter- lites in competition for space with corals still remains to action in these encounters is unknown. Some sponges be demonstrated. exude toxic substances in their direct vicinity (Thomp- son 1985) and affect corals by direct or indirect contact (Porter & Targett 1988), but other species release no Overgrowth and physical stress waterborne allelopathic substances (Bingham & Young 1991). Corals can damage neighboring organisms Competitive dominance of sponges as a group over using mesenterial filaments and sweeper tentacles corals as a group is not shown by our results, and it (Lang & Chornesky 1990). In coral-alga interactions appears impossible to generalize about effectiveness Aerts & van Soest: Sponge/coral interactions 133

of sponges in killing corals or about susceptibility of Acknowledgements. We are grateful to Mr P. A. J. van der corals to sponge aggression. The frequency of over- Wolf for his help with practical problems and to Dr S. Zea for growth of corals by sponges was found to depend on his help in identifying some sponge species and for hls comments on our manuscript. Dr L. Botero is thanked for the the presence of particular sponge species. Only 16 of facilities offered by the INVEMAR, and boatsman J Gonzalez the 95 sponge species were engaged in aggressive for his support on the field trips. We thank Prof. Dr R. P. M. interactions and these 16 sponge species were not Bak for his suggestions and constructive critisism with regard equally aggressive in terms of overgrowth. Since the to the n~anuscript,Dr M. J. de Kluijver for the discussions on sponge/coral interactions, and h4sc. M. Kielman for making mechanisms of competition for space differ between available to us her data on sedimentation rates of the coral individual sponge and coral species, and because a reef communities of Santa Marta. The manuscript has been number of other factors may influence the outcome improved considerably due to the comments of 3 anonymous of these interactions, sponge/coral interactions likely reviewers. This research was made possible by a grant from form complex networks. When space is limited and the Netherlands Organization for Scientific Research in the tropics (WOTKO, project no. W84-342). disturbance low (e.g. in cryptic habitats; Jackson & Buss 1975, Buss & Jackson 1979), overgrowth capabil- ity will be selectively favoured and aggressive sponge LLTERATURE CITED species will be able to out-compete corals. That over- Bak RPM, Terrnaat RM, Dekker R (1982) Complexity of coral growth was rather rare compared to the other cate- interactions: influence of t~me,locality of interaction and gories of interactions may be indicative of its minor epifauna. Mar Biol 69:215-222 importance as a competitive strategy in the physically Bakus GJ, Schulte B, Jhu S, Wright M, Green G, Gomez P stressed coral reef communities of Santa Marta. Exter- (1990) Ant~biosisand antifouling in marine sponges: labo- nal disturbances can alter existing competitive hierar- ratory versus field stud~es.In: Rutzler K (ed) New per- spectives in sponge biology. Smithsonian Inst Press, chies or networks by reducing the competitive ability Washington, DC, p 102-108 of some species more than that of others (Connell 1976). Bingham BL,Young CM (1991) Influence of sponges on inver- The hypothesis that physical stress reduces the com- tebrate recruitment: a field test of allelopathy. Mar Biol petitive ability of corals more than that of sponges, 109:19-26 Bradbury RH, Young PC (1983) Coral interactions and com- leading to a relative increase of overgrowth of corals munity structure: an analysis of spatial pattern. Mar Ecol by sponges (e.g. Rutzler & Muzik 1993), is not con- Prog Ser 11:265-271 firmed by our results. Environmental stress did not Buss LW, Jackson JBC (1979) Competitive networks: non- lead to an increase in overgrowth of corals by sponges. transitive competitive relationships In cryptic coral reef No significant differences in the frequency of over- environments. Am Nat 113:223-234 Chalker BE. Carr K, Gill E (1985) Measurement of primary growth were found among our 5 localities, although production and calcification in situ on coral reefs using Punta de Betin was most stressed in terms of sedi- electrode techniques. Proc 5th Int Coral Reefs Congr, mentation load and light conditions. Focussing on the Tahiti 6.167-172 aggressive sponge species Desrnapsarnma anchorata, Chornesky EA (1989) Repeated reversals during spatial competition between corals. Ecology 70(4):843-855 it appears that overgrowth is related to coral cover Connell JH (1976) Competitive interactions and the species rather than to physical stress. We reject the hypothesis diversity of corals. In Mackie GO (ed) Coelenterate that the frequency of aggressive sponge/coral inter- ecology and behaviour Plenum Press, New York, p 51-58 actions is related to physical stress for corals. Sponges Cruz E, Ramirez G (1990) Caracterizacion quimica de las do not necessarily overgrow corals when they are con- aguas residuales del municipio de Santa Marta, costa Caribe Colombiana. 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This article was submitted to the editor Manuscnpt first received. March 8, 1996 Rev~sedversion accepted December 30, 1996