MARINE ECOLOGY PROGRESS SERIES Vol. 303: 133–144, 2005 Published November 21 Mar Ecol Prog Ser

Interactions among Florida . I. Reef habitats

Sebastian Engel1, 2, Joseph R. Pawlik1,*

1University of North Carolina at Wilmington, Center for Marine Science, 5600 Marvin K. Moss Lane, Wilmington, North Carolina 28409, USA 2Present address: Scripps Institution of Oceanography, La Jolla, California 92093, USA

ABSTRACT: Spatial interference competition is well described for many sessile marine invertebrates, but few studies have addressed interactions between neighboring sponges. We conducted transect surveys to assess interspecific interactions among sponges in coral reef habitats in Key Largo, Florida, USA. In total, 15 transect sites were surveyed at 5 reef locations with mean densities ranging from 13.0 ± 3.6 to 33.3 ± 5.9 sponges m–2. The most abundant of over 43 species observed were Amphimedon compressa, Aplysina cauliformis, Aplysina insularis, and Niphates erecta, while the least abundant were Hippospongia lachne, campana, and Pseudaxinella lunaecharta. A nearest-neighbor technique was used to determine the degree and frequency of interactions between randomly selected sponge pairs. Overall, 40.4% of sponges occurred alone, 31.0% in proximity to, and 28.6% in contact with other sponge species. Among sponges in contact interactions, 18.7% were epibionts, 19.4% were basibionts, and a relationship could not be resolved for the remainder. Statistical analyses of the frequencies of each interaction category revealed that the ability to overgrow or resist overgrowth varied among species. For example, Aka coralliphagum, Ectyoplasia ferox, and Phorbas amaranthus occurred alone in >60% of their interactions and were never overgrown by other species with which they came into contact. In contrast, schmidti, Ircinia felix, Dysidea janiae, and Scopalina ruetzleri occurred alone in <30% of their interactions, with the first 2 species overgrown by, and the latter 2 overgrowing, most other species with which they came in contact. All contact interactions were further statistically examined, and 41 interspecific sponge pairs revealed significant overgrowth ability by 1 of the interacting species. While the over- growth ability of a species is dependent on sponge morphology, the ability to resist overgrowth is associated with the production of allelochemicals.

KEY WORDS: Coral reef · Interspecific interactions · Nearest-neighbor · Overgrowth · Sponges · Allelopathy

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INTRODUCTION Rubin 1985). On coral reefs, sponges are commonly described as competitively dominant over other ses- Competitive interactions among sessile marine sile invertebrates in their ability to overgrow or resist invertebrates have been studied extensively in many overgrowth by neighboring organisms including bry- hard-substratum environments such as rocky shores ozoans and corals (Jackson & Buss 1975, Aerts 1998, (e.g. Connell 1961, Dayton 1971, Sebens 1986) and Hill 1998). While competitive interactions among coral reefs (e.g. Jackson 1977, Suchanek et al. 1983). corals (Lang 1971, 1973, Sammarco et al. 1983, 1985, In these habitats, space is thought to be the most La Barre et al. 1986) and bryozoans (Buss 1979, important limiting resource, and spatial interference Rubin 1985, Lopez Gappa 1989, Barnes & Dick 2000) competition often results in the overgrowth of one are well documented, relatively few studies have species by another (Stebbing 1973, Quinn 1982, addressed spatial interference interactions among

*Corresponding author. Email: [email protected] © Inter-Research 2005 · www.int-res.com 134 Mar Ecol Prog Ser 303: 133–144, 2005

sponges (Rützler 1970, Sará 1970, Pansini & Pronzato The purpose of this study was to investigate spatial 1990, Wulff 1997). interference interactions among sponge species in Sponges are abundant and diverse members of ben- coral reef habitats of the Florida Keys, USA. Transect thic communities in coral reef habitats (Reiswig 1973, surveys were conducted to determine local sponge Rützler 1986, Diaz & Rützler 2001, Alcolado et al. demographics and examine interspecific interactions. 2004). Despite their sessile lifestyle and a soft, fleshy In addition, a nearest-neighbor technique was used to tissue that lacks physical protection from predation assess the degree of interaction among individual (Chanas & Pawlik 1995, 1996, Pawlik et al. 1995, Paw- sponge species and their ability to overgrow or resist lik 1997), sponges are often found thriving on coral overgrowth by neighboring sponges. Frequencies of reefs that are characterized by high predation pressure observed sponge interactions were analyzed statisti- (Huston 1985, Dunlap & Pawlik 1996, 1998) and in- cally and comparisons made among overgrowth abil- tense spatial interference competition (Jackson & Buss ity, sponge morphology, and the allelopathic effects of 1975, Suchanek et al. 1983). While sponge–coral inter- sponge extracts (Engel & Pawlik 2000). actions are important to the community structure of Indo-Pacific reefs where coral cover is high (De Voogd et al. 2004), Caribbean reefs are dominated by sponges MATERIALS AND METHODS which attain much greater biomass per unit surface area than other sessile invertebrates (Reiswig 1973), Study areas and sponge identification. Interspecific and surpass corals in diversity and abundance (Sucha- sponge interactions were examined on different coral nek et al. 1983, Targett & Schmahl 1984, Diaz & Rützler reef habitats in Key Largo, Florida (Fig. 1a). Fifteen 2001, Alcolado et al. 2004). Further, studies have transect sites were established on the following 5 reefs, demonstrated that sponges are competitively domi- listed from north to south: 4 sites at North Dry Rocks nant in interference interactions with corals (Suchanek (25° 07.85’ N, 80° 17.52’ W); 3 sites at Dixie Shoal et al. 1983, Porter & Targett 1988, Vicente 1991). In Guam, nearly 1 km of coral reef was covered by a spe- cies of the genus Terpios (Bryan 1973). A long-term study investigating the competitive abilities of organ- isms settling on artificial substrata revealed that spon- ges rank superior to most other marine invertebrates such as bryozoans, barnacles, polychaetes, tubicolous amphipods, and hydroids (Russ 1982). Considering the well-recognized dominance of sponges over other ses- sile marine organisms, it is surprising that only a hand- ful of studies have examined interspecific overgrowth interactions among sponges (Rützler 1970, Sará 1970, Pansini & Pronzato 1990, Wulff 1997). Interspecific sponge interactions are difficult to assess because it is often not clear whether interacting individuals are competing or mutualistic. Sponges have been described as competing for available sub- strata (Hartman 1957, Rützler 1965); however, tissue necrosis or mortality is rarely observed among over- grown individuals, suggesting mutualistic associations (Rützler 1970, Sará 1970). Further, some sponges can undergo specialized tissue adaptations to allow over- growth by epibiotic species (Rützler 1970). Conse- quently, dense and diverse sponge populations are often vertically stratified and can remain stable over long periods of time (Sará 1970, Pansini & Pronzato 1990). Mutualistic relationships have also been described among branching sponges (Wulff 1997). While these studies focused on mutualistic sponge Fig. 1. Map of (a) Southern Florida indicating the location of Key Largo and (b) Key Largo indicating the location of the associations, little is known about the extent to which following 5 study locations: NDR = North Dry Rocks, DXS = competitive interactions shape the community struc- Dixie Shoal, MLR = Molasses Reef, PKR = Pickles Reef, COR = ture of sponges on coral reefs. Conch Reef Engel & Pawlik: Interactions among reef sponges 135

(25° 04.66’ N, 80° 18.74’ W); 3 sites at Molasses Reef the focal nor the nearest-neighbor sponges were (25° 01.02’ N, 80° 22.53’ W); 2 sites at Pickles Reef selected twice for either category. (24° 59.07’ N, 80° 24.97’ W); 3 sites at Conch Reef Observations of interacting sponge pairs were lim- (24° 57.01’ N, 80° 27.25’ W) (Fig. 1b). Individual sites ited to those with a maximum distance of 5 cm be- within a given reef location were variable with regard tween them. This limit was assigned under the to water flow, temperature fluctuation, and light expo- assumption that the only interaction mechanism in sure. In addition to analyzing data for all reef sites, non-contact encounters is the release of water-soluble location-dependent factors were taken into considera- allelochemicals with a maximum effective range of tion by analyzing data grouped by reef location. 5 cm. This assumption is supported by Turon et al. The sponge communities at all reef locations are (1996), who found that a strong non-random pattern of similar to those found throughout the Caribbean and negative sponge associations diminished with in- contain most of the same species (Reiswig 1973, creasing distance and was absent beyond 5 cm from Alvarez et al. 1991, Diaz et al. 1991, Schmahl 1991, the edge of the interacting sponge species. In addition, Van Soest 1994, Alcolado et al. 2004). All sponge indi- studies investigating interactions among corals and viduals were identified by spicule and tissue prepara- between sponges and corals have indicated that non- tions based on the available literature (DeLaubenfels contact interactions may have an interactive range of 1936, Wiedenmayer 1977, Rützler 1986, Zea 1987, up to 5 cm (Richardson et al. 1979, Sheppard 1981, Hopper & Van Soest 2002). Conforming to most previ- Aerts & Van Soest 1997, Aerts 1998). Given the above, ous assessments of sponge communities (references we defined the following 3 categories of interactions: above), this study quantified sponge number rather Alone: includes encounters in which the focal than biomass or substratum coverage. As defined by sponge is found without a neighboring sponge grow- Hartman & Reiswig (1973), a sponge individual is ing within a 5 cm radial margin around its edge (dis- contained within continuous tissue connected by an tance to nearest-neighbor > 5 cm). unbroken surface pinacoderm. Attached multiple lobes, Proximate: includes encounters in which the focal tubes, or branches were considered part of the same sponge is found next to a neighboring sponge within individual. its 5 cm radial margin but does not come in direct Transects and nearest-neighbor analysis. Belt tran- contact with it. sects were conducted to determine the abundance and Contact: includes encounters in which the focal diversity of sponge species and examine interspecific sponge is in direct contact with its neighboring sponge interactions at different coral reef locations. Each tran- (distance to nearest-neighbor = 0 cm). sect was established by attaching a 10 m line, marked Statistical analyses were conducted on data for at 1 m intervals, to a randomly chosen point and sponge species that occurred 5 or more times. A chi- stretching it parallel to the isobath of a chosen depth. A square goodness of fit test (χ2 × 5.991, df = 2, p < 0.05) quadrat (1 m2) was placed directly over the transect was used to assess differences in frequencies between line, with 2 opposing edges centered and perpendicu- the above interaction categories for each sponge spe- lar to the transect line. The quadrat was moved along cies. The null hypothesis (H0) tested assumed equal the 1 m interval marks of the transect line 10 times, distribution of individuals occurring alone, in proxi- 2 2 covering a total of 10 m . Three 10 m transects were mate, and contact interactions. Rejecting the H0 led to performed at each site, resulting in a total survey area further investigations to examine species aggregation of 30 m2 of benthos at each transect site. patterns (Zar 1996). In each quadrat, the total number of sponge individ- All contact interactions were subject to further uals was recorded and each identified to species level. analysis. In each case the sponge individuals encoun- These data were used to determine species abundance tered in a contact interaction were classified into 1 of 3 and diversity at each of the 5 reef locations. In addi- categories defined by the following 3 possible out- tion, a nearest-neighbor technique was used to assess comes: the degree of interactions between randomly chosen Over: includes encounters in which the focal sponge sponge pairs (Brower et al. 1997). Focal sponges were occurs as the epibiont, overgrowing an individual of randomly selected by dropping 4 plastic markers into another species. the quadrat, and choosing the closest sponge to each Under: includes encounters in which the focal marker. The nearest-neighbor of each focal sponge sponge occurs as the basibiont, being overgrown by was identified and the distance between the 2 indi- an individual of another species. viduals measured. Distance measurements were con- Equal: includes contact interactions in which the ducted along the shortest line connecting the proximal degree of overgrowth is not sufficient to distinguish edges of 2 neighboring sponge individuals. This proce- between epi- and basibionts. Both interacting sponge dure was repeated 4 times, making certain that neither individuals are classified as equal. 136 Mar Ecol Prog Ser 303: 133–144, 2005

Pairs of sponge species observed in 5 or more contact 400 interactions were chosen for statistical analysis. The overgrowth ability of each sponge species was exam- ined by calculating the average overgrowth rate from 300 the observed frequencies of each contact category. This method was adapted from Russ (1982), who 200 assigned points to interacting individuals to determine the competitive dominance of different marine inverte- brates. For each observed contact interaction, 2 points 100 were assigned to the overgrowing sponge and 0 points

to the species being overgrown. For each observed Abundance (ind. per transect) ‘equal’ interaction, 1 point was given to both individu- 0 2 North Dry Dixie Molasses Pickles Conch als. A chi-square goodness of fit test (χ × 3.841, df = 1, Rocks Shoal Reef Reef Reef p < 0.05) was conducted on the sums of these points as Reef locations the observed values, and the total number of inter- Fig. 2. Number of sponge individuals (mean + SD) per actions (n) was used as the expected value for both transect for each reef location species. The H0 tested was that there was no differ- ence in the overgrowth ability of the 2 interacting spe- cies. If the H0 was rejected, the species with the higher and lowest at Dixie Shoal and Pickles Reef (31 species) overgrowth rate was regarded to be more likely to (Table 1). Sponge abundance was greatest at North overgrow the other species and considered epibiotic. Dry Rocks with a total of 3273 sponges averaging The extent of the overgrowth of each sponge species 332.9 ± 59.0 ind. transect–1, followed by Molasses Reef observed in contact interactions was determined by cal- (2491; 283.8 ± 46.8), Conch Reef (2085; 234.9 ± 50.2), culating a species-specific overgrowth index using the Dixie Shoal (1144; 129.8 ± 36.3), and Pickles Reef (925; results from the sponge pair analysis. The overgrowth 158.2 ± 70.6) (Fig. 2, Table 1). Simpson’s diversity index was calculated by subtracting the number of indices indicated high species diversity at all reef basibiotic interactions from the number of epibiotic in- locations, with the sponge community at Conch Reef teractions, and dividing by the total number of statisti- being the most diverse and that of Pickles Reef the cally tested pair interactions. This overgrowth index least diverse (Table 1). Morisita’s indices revealed ranged from 1 to –1, indicating a species that is always some differences in the sponge communities at each overgrowing other sponges to a species that is always reef location, with the communities at Conch Reef and being overgrown by other sponges, respectively. Molasses Reef being most similar, and those at Dixie Shoal and Pickles Reef most different (Table 2). The most abundant sponge species were Amphime- RESULTS don compressa and Niphates erecta, with over 1000 total individuals averaging over 200 individuals at Sponge species abundance and diversity each reef location (Fig. 3). The sponges Aplysina cauli- formis, Aplysina insularis, and Scopalina ruetzleri Overall, 9984 sponge individuals comprising 43 spe- were also relatively abundant, with over 500 total cies were recorded at all reef locations (Table 1). Spe- individuals averaging over 100 individuals at each reef cies richness was highest at Molasses Reef (41 species), location (Fig. 3). Third most abundant were Agelas schmidti, Callyspongia vaginalis, Ectyoplasia ferox, Table 1. Sponge abundance and diversity indices for all reef Iotrochota birotulata, Monanchora arbuscula, and Ni- locations. Species with less than 5 individuals were not phates digitalis, with over 300 total individuals averag- included. S = species richness, n = total number of individuals, lS = Simpson’s dominance, DS = Simpson’s diversity, ES = evenness, NDR = North Dry Rocks, Dixie Shoal, MLR = Table 2. Morisita’s index of community similarity between each Molasses Reef, PKR = Pickles Reef, COR = Conch Reef reef location based on Simpson’s dominance (lS) (Table 1); see Table 1 for reef abbreviations Overall NDR DXS MLR PKR CON Reef NDR DXS MLR PKR S 43 35 31 41 31 40 n 9984 3273 1144 2491 925 2085 COR 0.753 0.816 0.942 0.656 lS 0.057 0.079 0.062 0.056 0.092 0.055 PKR 0.917 0.638 0.757 DS 0.943 0.922 0.939 0.944 0.908 0.945 MLR 0.891 0.769 ES 0.966 0.948 0.969 0.967 0.938 0.969 DXS 0.641 Engel & Pawlik: Interactions among reef sponges 137

Agelas clathrodes - 118 considerably among sponge species. The - 105 following species occurred alone more fre- Agelas schmidti - 490 quently than in proximity to or in contact Ailochroia crassa - 182 Aka coralliphagum - 88 with other sponge species: Aka coralli- Amphimedon compressa - 1060 phagum, Anthosigmella varians, Aplysina Anthosigmella varians - 67 Aplysina cauliformis - 939 insularis, Aplysina lacunosa, Cliona Aplysina fulva - 78 delitrix, Ectyoplasia ferox, Monanchora Aplysina insularis - 687 arbuscula, Mycale laevis, Phorbas ama- Aplysina lacunosa - 82 Callyspongia armigera - 93 ranthus, Ptilocaulis walpersi, Rhaphi- Callyspongia plicifera - 90 dophlus juniperinus, Spirastrella coccinea, Callyspongia vaginalis - 426 and an unknown species of the genus Chondrilla nucula - 128 Cinachyra alloclada - 33 Verongula (Fig. 4a). Amphimedon com- Cliona delitrix - 191 pressa and Dysidea janiae occurred most Dysidea janiae - 86 frequently in proximal interactions, and Ectyoplasia ferox - 400 Geodia neptuni - 23 Agelas schmidti, Callyspongia armigera, Holopsamma helwigi - 32 Iotrochota birotulata, and Scopalina ruetz- Hippospongia lachne - 14 leri were observed more frequently in con- Iotrochota birotulata - 403 Ircinia campana - 13 tact interactions than in proximal inter- Ircinia felix - 142 actions or alone (Fig. 4a).

Sponge species - 131 Monanchora arbuscula - 348 Among all 1512 sponge individuals Mycale laevis - 135 observed in contact interactions, 61.9% Mycale laxissima - 131 occurred in ‘equal’ interactions, while only Myrmekioderma styx - 43 Niphates digitalis - 407 18.7% were encountered as epibionts Niphates erecta - 1078 and 19.4% as basibionts to other sponge Phorbas amaranthus - 204 species (Fig. 4b). Overall, 86% of all spe- Pseudaxinella lunaecharta - 19 Ptilocaulis walpersi - 34 cies encountered in contact interactions Rhaphidophlus juniperinus - 30 occurred more frequently in ‘equal’ inter- Scopalina ruetzleri - 777 actions than in those resulting in over- Smenospongia cerebriformis - 77 Spirastrella coccinea - 203 growth (Fig. 4b). Because of the high fre- Verongid sp. - 77 quency of ‘equal’ interactions between Verongula gigantea - 31 most sponges, the average overgrowth Verongula rigida - 118 Xestospongia muta - 171 ability for each of the 29 species encoun- Other - 130 tered in contact interactions was examined 0 100 200 300 400 by conducting a chi-square goodness of fit Individuals reef–1 test on assigned points (χ2 × 3.841, df = 1, p < 0.05). While Dysidea janiae and Fig. 3. Number of sponge individuals (mean + SD) per reef location for 43 Scopalina ruetzleri overgrew other species most abundant species. Total number of individuals for each species is given next to the species name. ‘Other’ includes species with <5 ind. most frequently, Agelas schmidti and Ircinia felix were overgrown by other species most frequently (Fig. 4b). ing over 50 individuals at each reef location (Fig. 3). Given that the percentages of each category are The least abundant sponges were Hippospongia lachne, derived from the total number of observations, they Ircinia campana, and Pseudaxinella lunaecharta, with can be regarded as the average frequencies for each less than 20 total individuals and only present at some interaction category. Most sponge species displayed but not all reef locations (Fig. 3). frequencies close to the average frequencies of each category (Fig. 5). However, a few species displayed frequencies well above or below the average fre- Interactions among sponge species quency of a given category. For example, Aka coral- liphagum, Cliona delitrix, Mycale laevis, and Ectyo- Interspecific sponge interactions were examined plasia ferox occurred alone in >65% and in contact in with the nearest-neighbor data from a total of 5289 <10%, of all interactions (Figs. 4a & 5b). In contrast, focal sponges recorded at all transect sites. Overall, Agelas schmidti, Callyspongia armigera, and Iotro- 40.4% of focal sponges occurred alone, 31.0% in prox- chota birotulata occurred alone in <25% and in con- imal, and 28.6% in contact interactions (Fig. 4a). The tact in >55% of all interactions (Figs. 4a & 5a). Among frequencies of these 3 interaction categories varied those species encountered in contact interactions, 138 Mar Ecol Prog Ser 303: 133–144, 2005 Under of equal frequency and (b) con- Equal 0 Occurrence H Under) for all sponges and individual spe- Over 0% 25% 50% 75% 100% 2 3 3 2 4 1 0 3 5 3 1 1 1 4 3 28 37 11 12 36 10 47 87 12 20 22 54 43 39 33 65 12 14 43 18 32 - 39 126 139 120 130 109 138 sp. illa nuclua - - nuclua illa *Ircinia felix - - felix *Ircinia Verongid Verongid Mycale laevis - - laevis Mycale Aplysina fulva - Aplysina - fulva Cliona delitrix - - delitrix Cliona Ircinia campana Ircinia - *Geodia neptuni - - neptuni *Geodia Agelas conifera - *Dysidea janiae - *Ircinia strobilina - strobilina *Ircinia Niphates erecta - - Niphates erecta *Verongula rigida - rigida - *Verongula Aplysina lacunosa - Ailochroia crassa - Ectyoplasia ferox - Aka coralliphagum - Mycale laxissima - - laxissima Mycale Niphates digitalis - Aplysina insularis - - insularis Aplysina Chondr Ptilocaulis walpersi - - walpersi Ptilocaulis ALL SPONGES - 1512 ALL SPONGES - *Agelas schmidti - * - - *Agelas clathrodes Cinachyra alloclada - Verongula gigantea - - gigantea Verongula Holopsamma helwigi - Holopsamma - helwigi Myrmekioderma styx - Myrmekioderma - styx *Xestospongia muta - muta - *Xestospongia Hippospongia lachne - *Scopalina ruetzleri - - *Scopalina ruetzleri Anthosigmella varians - - varians Anthosigmella Spirastrella coccinea - coccinea - Spirastrella *Phorbas amaranthus - - amaranthus *Phorbas *Iotrochota birotulata - - birotulata *Iotrochota *Callyspongia - plicifera *Aplysina cauliformis - Callyspongia vaginalis - Callyspongia armigera - *Monanchora arbuscula - - arbuscula *Monanchora Pseudaxinella lunaecharta - Pseudaxinella - lunaecharta Rhaphidophlus juniperinus - *Amphimedon - compressa Smenospongia - cerebriformis b of no difference in overgrowth ability 0 H Alone :significant results from the chi-square goodness of fit test (a) with * Proximal Occurrence ducted on assigned points with Contact 0% 25% 50% 75% 100% 8 5 5 81 37 47 32 72 85 19 53 58 77 25 44 14 25 89 60 25 21 10 54 80 38 11 95 331 119 184 272 104 428 165 140 473 215 549 275 138 229 - 296 201 sp. *Ircinia felix - *Verongid *Verongid *Mycale laevis - *Aplysina fulva - Ircinia campana - *Dysidea janiae - Agelas conifera - Geodia neptuni - *Cliona delitrix - *Ircinia strobilina - *Verongula rigida - *Verongula Chondrilla nuclua - Agelas clathrodes - *Niphates erecta - Mycale laxissima - *Agelas schmidti - Ailochroia crassa - *Aplysina lacunosa - *Aplysina insularis - *ALL SPONGES - 5289 *Niphates digitalis - *Ectyoplasia ferox - *Aka coralliphagum - Verongula gigantea - Verongula Cinachyra alloclada - *Ptilocaulis walpersi - Hippospongia lachne - *Scopalina ruetzleri - Xestospongia muta - Myrmekioderma styx - Holopsamma helwigi - *Spirastrella coccinea - *Aplysina cauliformis - *Callyspongia plicifera - *Iotrochota birotulata - *Anthosigmella varians - *Phorbas amaranthus - *Callyspongia armigera - *Callyspongia vaginalis - Pseudaxinella lunaecharta - *Monanchora arbuscula -

*Amphimedon compressa - *Rhaphidophlus juniperinus - Sponge species Sponge Smenospongia cerebriformis - a Fig. 4. Percentage occurrence of (a) contact, proximal, Equal, and no interactions (Alone) (b) each contact category (Over, cies. Total number of individuals is given next to the species name. cies. Total Engel & Pawlik: Interactions among reef sponges 139

by sponges with which they came into contact 90–100% a Alone Proximal Contact 80–90% 40.4% 31.0 % 28.6% (Fig. 6). n = 43 n = 42 n = 42 70–80% All sponge species were grouped into 7 cat- 60–70% egories defined by distinct morphological 50–60% growth characteristics (Jackson 1979, Boury- 40–50% Esnault & Rützler 1997) (Table 3). Overall, 30–40% 39.5% of all species were lobate, 20.9% were 21 20–30% - branching, 11.6% were encrusting, 9.3% were 10–20% globular, 7% were tubular, 7% were barrel 0–10% shaped, and 4.7% were turbinate (Table 3). The average overgrowth index of each species

90–100% b Over Equal Under in each category was used to assess the over- 80–90% 18.7% 61.9% 19.4% Frequency growth ability of each morphological growth n = 24 n = 40 n = 29 70–80% form (Fig. 7). The only encrusting sponge 60–70% observed in contact interactions was Scopalina 50–60% ruetzleri, which was epibiotic on 9 of the 13 40–50% species with which it interacted (Fig. 6), and 30–40% ranked at the top of the overgrowth hierarchy 20–30% with and overgrowth index of 0.69 (Fig. 7). 10–20% The branching sponges observed in contact 0–10% interactions included Amphimedon compressa, 0 5 10 15 20 0 5 10 15 20 0 5 10 15 20 Aplysina cauliformis, Iotrochota birotulata, Number of species and Niphates erecta (Table 3); these sponges had an average overgrowth index of 0.25, Fig. 5. (a) Frequencies of each interaction category and (b) each contact cat- overgrowing most sponges in the other cate- egory displayed by the number of reef species encountered in each cate- gory. Frequency data were pooled in increments of 10%. Overall percent- gories except for the encrusting sponge S. age occurrence and total number of species (n) for each category is given ruetzleri, and the lobate sponges Dysidae janiae and Phorbas amaranthus (Figs. 6 & 7). Lobate sponges comprised the largest group of Dysidea janiae overgrew other species in >85%, while morphologically similar species occurring in contact Agelas schmidti was overgrown by other species in interactions (Table 3). The average overgrowth index >50% of all contact interactions (Figs. 4b & 5b). of all lobate species was 0.07, reflecting clear differ- The overgrowth ability for the 21 most abundant ences in the overgrowth ability of lobate species over species occurring in contact interactions was further branching or globular sponge species (Fig. 7). All tubu- examined by statistically analyzing the frequencies of lar and turbinate sponges averaged a combined over- contact categories between each species pair. The chi- growth index of –0.25 because they were frequently square test results for each interacting sponge pair are overgrown by encrusting and branching sponges and presented in a matrix of interspecific contact inter- only in some cases were found growing on globular actions along with the calculated overgrowth index for and barrel sponges (Figs. 6 & 7). No significant over- each species (Fig. 6). Dysidea janiea, Phorbas amaran- growth ability was observed between lobate, tubular, thus, and Scopalina ruetzleri were the only species or turbinate sponges. Globular and barrel sponges with an overgrowth index of 0.5 or greater because ranked lowest in the overgrowth hierarchy, with aver- they were rarely overgrown and frequently overgrew age overgrowth indices of –0.5 and –0.54, respectively species with which they came into contact (Fig. 6). (Figs. 6 & 7). The globular sponges Ircinia felix and Ailochroia crassa was also rarely overgrown; however, Ircinia strobilina and the barrel sponges Verongula its overgrowth index of 0.4 reflects a relative increase gigantea and Xestospongia muta were frequently in ‘equal’ interactions (Fig. 6). Positive overgrowth overgrown by encrusting, branching, tubular, and indices were also observed for Amphimedon com- turbinate sponges (Fig. 7). pressa, Aplysina cauliformis, Iotrochota birotulata, and Niphates erecta (Fig. 6). Mycale laxissima was the only species with an overgrowth index of 0 because it was DISCUSSION equally likely to overgrow and be overgrown by other sponge species (Fig. 6). The remaining sponge species The competitive dominance of sponges over other surveyed in this study had negative overgrowth in- sessile marine invertebrates is well documented dices because they were most frequently overgrown (e.g. Jackson & Buss 1975, Jackson 1977, Russ 1982, 140 Mar Ecol Prog Ser 303: 133–144, 2005

XMUT VRIG VGIG SRUE PAMA NERE NDIG MLAX MARB ISTR IFEL IBIR DJAN CVAG CPLI ACA U ACOM ACRA ASCH ACON

1 ACLA NS 2 22 11 1 NS 4 6 NS 2 3 1 5 112 5 2

ACON 21 NS 6 3 11NS 5 4 2 1 1 1 ASCH 1 25 NS 7 2 3 2 NS 5 2 NS 7 NS 3 7 1 92 1 7 3 9 2 1 2 ACRA 21 12521NS 5 2 2 NS 3 2 7 1 1 1 1 1 12 1 6 5 1 4 2 3 4 12 ACOM 1 NS 5 10 1 20 NS 10 NS 5 6 2 NS 7 NS 18 5 NS 12 2 NS 47 1 7 3 2 2 11 1 20 7 1 3 1 5 2 1 7 12 8 2 ACAU 1 5 2 NS 19 NS 7 4 NS 3 NS 5 1 16 16 NS 5 8 4 1 2 3 CPLI NS 4 1 NS 7 13 4 5 6 1 CVAG 3 NS 6 4 NS 8 NS 7 1 NS 3 26 4 1 2 11 16 1 DJAN 11

1 5 5 5 7 IBIR 1 5 1 NS 12 322 NS 6 4 ACLA – Agelas clathrodes (–0.4; LO) 1 12 2 1 ACON – Agelas conifera (–0.33; TU) IFEL 11 21411ASCH – Agelas schmidti (–0.38; LO/TU) 5 5 ACRA – Ailochroia crassa (0.4; LO) ISTR 14234 2 1 ACOM – Amphimedon compressa (0.19; BR) 5 5 4 6 1 ACAU – Aplysina cauliformis (0.21; BR) MARB NS 8 NS 6 NS 4 1 CPLI – Callyspongia plicifera (–0.33; TR) 2 2 2 CVAG – Callyspongia vaginalis (–0.22; TU) MLAX 21 1 NS 6 NS 5 DJAN – Dysidea janiae (1; LO) 2 1 IBIR – Iotrochota birotulata (0.33; BR) NDIG NS 5 NS 3 4 3 IFEL – Ircinia felix (–0.38; GL) 2 71 9 13 4 ISTR – Ircinia strobilina (–0.63; GL) NERE 11 5 1 NS 26 4 MARB – Monanchora arbuscula (–0.14; LO) 1 5 3 MLAX – Mycale laxissima (0; LO) PAMA NS 6 NDIG – Niphates digitalis (–0.11; TR) 1 6 NERE – Niphates erecta (0.27; BR) SRUE 31 PAMA – Phorbas amaranthus (0.5; LO)

1 SRUE – Scopalina ruetzleri (0.69; EN) VGIG NS 4 VGIG – Verongula gigantea (–0.5; BA) VRIG – Verongula rigida (–0.4; LO) VRIG 2 XMUT – Xestospongia muta (–0.57; BA )

Fig. 6. Matrix of interspecific contact interactions for 21 sponge species occurring in overgrowth interactions 5 or more times. Each cell in the matrix represents the interactions between a pair of sponge species. The top number in each cell represents the total number of occurrences in which the species in the vertical column is observed overgrowing the species in the horizontal col- umn. Middle numbers represent the number of equal occurrences. Bottom numbers represent the total number of occurrences in which the species in the vertical column is observed to be overgrown by the species in the horizontal column. Arrows represent results from the chi-square goodness of fit test, and point to the species that is more likely to be overgrown by the other. Blank cells did not have enough interactions to be considered for statistical analysis. Overgrowth index and morphology of each sponge species are given in parentheses next to the species name. NS = no significant overgrowth ability, EN = encrusting, LO = lobate, GL = globular, TU = tubular, TR = turbinate, BR = branching, BA = barrel (see Table 3)

Suchanek et al. 1983, Aerts 1998, Hill 1998); however, contact interactions occurred in ‘equal’ rather than not much is known about interference interactions clear overgrowth interactions (Figs. 4b & 5b). How- among sponge species. To date, most studies investi- ever, our large sample size among diverse sponge pop- gating interspecific interactions among sponges have ulations (Tables 1 & 2) allowed us to examine the only focused on mutualistic associations (Rützler 1970, remaining contact interactions that resulted in the Sará 1970, Pansini & Pronzato 1990, Wulff 1997). The overgrowth of one species by another. relatively stable and non-transitive nature of most The majority of sponge species were encountered sponge interactions often makes it difficult to identify alone or in close proximity to one another (Fig. 4a). epi- from basibiotic species (Rützler 1970, Sará 1970, Only 28.6% of all sponge individuals were observed Pansini & Pronzato 1990). This difficulty was mirrored in direct contact with other species (Fig. 4a), limiting in our study, where over 86% of all sponge species in our analysis of interspecific contact interactions to Engel & Pawlik: Interactions among reef sponges 141

Table 3. Percentage occurrence of the 7 basic sponge morphologies in Key Largo, Florida. Morphological growth characteristics and descriptions modified from Jackson (1979)

Growth form Description Examples

Encrusting (EN) Flat, 2-dimensional encrustations Aka coralliphagum (11.6%) Lateral growth only Cliona deletrix Completely attached to substratum Scopalina ruetzleri Lobate (LO) Irregular encrustations Ailochroia crassa (39.5%) Lateral and vertical growth Dysidea janiae Most basal area is attached Mycale laxissima Verongula rigida Globular (GL) Regular encrustations Geodia neptuni (9.3%) Lateral and vertical growth Ircinia felix Most basal area is attached Ircinia strobilina Tubular (TU) Regular or irregular branching tubes Agelas conifera (7.0%) Vertical and minimal lateral growth Aplysina lacunosa One restricted zone of basal attachment Callyspongia vaginalis Turbinate (TR) Erect vase forms Callyspongia plicifera (4.7%) Vertical and minimal lateral growth Cribrochalina vasculum One restricted zone of basal attachment Niphates digitalis Branching (BR) Linear or branching forms Amphimedon compressa (20.9%) Vertical and lateral growth Aplysina cauliformis One or multiple restricted zones of basal attachment Iotrochota birotulata Niphates erecta Barrel (BA) Erect barrels Ircinia campana (7.0%) Vertical and lateral growth Verongula gigantea Most basal area attached to substratum Xestospongia muta

21 of the 43 species surveyed in this study. Of 210 cally tested interaction pairs, 41 resulted in over- possible interaction pairs among 21 species, only 81 growth by 1 of the interacting species (Fig. 6). While species pairs interacted frequently enough to be con- sponge morphology was a good indicator of the over- sidered for statistical analysis (Fig. 6). Of all statisti- growth ability of some species (Fig. 7), several inter- actions could not be explained by morphological differences alone. In these cases, sponges in contact ENCRUSTING (0.69) interactions appeared to resist overgrowth by other species through the production of allelochemicals (Engel & Pawlik 2000). The top of the overgrowth hierarchy was occupied by Dysidea janiae, Phorbas amaranthus, and Sco- BRANCHING (0.25) palina ruetzleri, which were never observed to be overgrown by other species. Among these 3 species, S. ruetzleri was the most abundant (Fig. 3) and inter- acted with more species than either D. janiae or P. amaranthus (Fig. 6). The tissue of S. ruetzleri is deli-

LOBATE (0.07) TUBULAR/TURBINATE (–0.25) cate and thinly encrusts the substratum, including many other sponge species. The overgrowth ability of S. ruetzleri is likely a result of its ability to laterally overgrow available substrata, and the apparent inability of other sponges to overgrow such delicate tissue. In contrast, D. janiae and P. amaranthus have a GLOBULAR (–0.50) BARREL (–0.54) lobate growth form, which does not lend itself to lat- eral overgrowth as readily as an encrusting growth Fig. 7. Overgrowth ability for each morphological growth cat- form. Instead, the overgrowth ability of D. janiae and egory defined in Table 3. Average overgrowth indices of all species in each category are given in parentheses. Arrows P. amaranthus appears to be mediated by allelochem- point from categories that are likely to overgrow to categories icals that prevent overgrowth by other sponges. In a that are likely to be overgrown previous study investigating allelopathic interactions 142 Mar Ecol Prog Ser 303: 133–144, 2005

among sponges, extracts from P. amaranthus inhibited cases were observed with the sponge Ircinia felix the lateral overgrowth of 3 other species (Engel & growing on the surface of Agelas clathrodes (Fig. 6). Pawlik 2000). While extracts of D. janiae were not These overgrowth interactions are most likely a result tested in this study, extracts of the related sponge of larval settlement or the secondary attachment of the Dysidea etheria also inhibited the overgrowth of the epibiont sponge on the basibiont. In all cases, globular same 3 sponge species (Engel & Pawlik 2000). In and barrel sponges were likely to be overgrown by all addition, a study conducted by Thacker et al. (1998) other species with which they came into contact demonstrated that a sponge of the genus Dysidea pro- (Figs. 6 & 7). duces a secondary metabolite that causes tissue The sponges Aka coralliphagum, Cliona delitrix, necrosis in field assays which therefore facilitates its Mycale laevis, and Ectyoplasia ferox were observed to ability to overgrow other species. occur alone more frequently than in proximity to or in The sponges Niphates erecta, Amphimedon com- direct contact with other sponge species (Fig. 4a). pressa, Iotrochota birotulata, and Aplysina cauliformis C. delitrix and A. coralliphagum are boring and bur- all have a branching growth form that provides a good rowing sponges, respectively, and are usually found mechanism for escaping overgrowth by others ‘in growing in coral mounds and ledges. While the height’ (Meesters et al. 1996). These species were sponge M. laevis is not classified as a boring sponge, among the most abundant (Fig. 3) and occurred in it has strong similarities to both C. delitrix and A. more contact interactions than any other sponge spe- coralliphagum in that it is usually found growing cies (Fig. 6). Overgrowth by these sponges was usu- among the branches of many different coral species. ally the result of branches attaching to the side of All 3 species are often described as occurring in con- other species and subsequently ‘wrapping’ around or tact with different coral species (Aerts 1998). The ‘creeping’ up and over them (Wulff 1979, 1997). Both sponge E. ferox is a low-growing and lobate species A. cauliformis and I. birotulata were often observed known to produce triterpene glycosides that prevent wrapping around the tubular sponge Callyspongia overgrowth by other species (Engel & Pawlik 2000, vaginalis, and the turbinate sponges Callyspongia Kubanek et al. 2002). Because of the low frequency of plicifera and Niphates digitalis (Fig. 6). In contrast, contact interactions, it is hard to assess the over- N. erecta is usually found ‘creeping’ over lobate growth ability of E. ferox with other sponges. How- sponges such as Ailochroia crassa and Verongula ever, given the abundance of E. ferox (Fig. 3), the rigida as well as both globular sponges Ircinia felix and probability of interspecific interactions is high. There- I. strobilina (Fig. 6). Niphates erecta was also observed fore, the ability of E. ferox to prevent overgrowth ‘creeping’ up larger sponges such as the barrel appears to be mediated by the production of allelo- sponges Verongula gigantea and Xestospongia muta chemicals. (Fig. 6). Interestingly, both N. erecta and I. birotulata In conclusion, interference interactions among reef were frequently overgrown by A. compressa and A. sponges frequently resulted in encounters in which cauliformis, respectively (Fig. 6). Further, the extracts it was not possible to distinguish the epi- from the from A. compressa and A. cauliformis inhibited over- basibiotic species. However, interspecific overgrowth growth by other sponge species; however, extracts interactions revealed 2 trends in the overgrowth abil- from N. erecta and I. birotulata did not have allelo- ity of a species: (1) sponge morphology provided a pathic effects on sponge growth (Engel & Pawlik good indicator of the overgrowth ability of some spe- 2000). While morphology enhanced the overgrowth cies, and (2) the production of allelochemicals appears ability of some branching sponges, the production of to play an important role in preventing overgrowth by allelopathic metabolites appears to play an important others. role in preventing overgrowth by other, morphologi- cally similar, species. Acknowledgements. This study was funded by grants Lobate, tubular, and turbinate sponges did not rank from the NOAA/National Undersea Research Program high in their ability to overgrow other species (Fig. 7). (UNCW9523, 9812) and from the Biological Oceanography In only 2 cases were tubular or turbinate sponges Program of the National Science Foundation (OCE-9711255, observed to overgrow other sponges: tubular Cally- 0095724). Permits to perform this research were provided by the NOAA/Florida Keys National Marine Sanctuary and the spongia vaginalis was observed growing on the giant State of Florida. We thank Greg McFall and the staff of barrel sponge Xestospongia muta, and turbinate Ni- NOAA/NURC in Key Largo, Florida, for logistical support. phates digitalis was observed growing on the globular Special thanks to Robyn M. Palmer for her daily assistance sponge Ircinia strobilina (Fig. 6). In both cases it is with the collection of transect data. This research benefited from the advice of Timothy P. Henkel regarding data inter- clear that overgrowth did not occur via the lateral pretation and presentation. We also thank William G. O’Neal growth of sponge tissue; rather, the sponges were for his assistance in the field. Dedicated to the memory of observed growing on top of the other species. Similar Sophie. Engel & Pawlik: Interactions among reef sponges 143

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Editorial responsibility: Otto Kinne (Editor-in-Chief), Submitted: February 14, 2005; Accepted: July 28, 2005 Oldendorf/Luhe, Germany Proofs received from author(s): October 15, 2005