Effects of Soft Corals on Scleractinian Coral Recruitment. II: Allelopathy, Spat Survivorship and Reef Community Structure
Abstract
Abstract. Two field experiments were performed on the Great Barrier Reef, Australia, at Orpheus Island and Lizard Island, respectively, to investigate the effects of allelopathic soft corals on survivorship and community structure of scleractinian coral spat. Ceramic tiles were placed around the allelopathic soft corals Sinularia flexibilis (Quoy & Gaimard 1833) and Sarcophyton glaucum (Quoy & Gaimard 1833), and controls. One control consisted of settlement plates surrounding a scleractinian coral (non-allelopathic planktivore); another control had no adult soft or scleractinian coral present. The experimental soft corals affected the recruitment of various taxonomic groups of coral spat differentially, as evidenced by the diversity of coral spat settling in treatments and controls. At Orpheus Island (O.I., n = 1038 spat) and Lizard Island (L.I., n = 7032 spat), there were significant differences between recruitment success of the two dominant coral taxa, Pocilloporidae (O.I., 61.4 %; L.I., 20.5 %) and Acroporidae (O.I., 33.7 %; L.I., 53 %). Settlement plates exposed to Sinularia flexibilis at either site had the lowest proportion of acroporid recruits. Diversity indices (Shannon-Wiener Indices) varied significantly between treatments at both Orpheus and Lizard Islands. This appears to be due to selective inhibition of acroporid spat by Sinularia flexibilis at both sites. Growth of coral spat was higher on settlement plates in the presence of Sarcophyton at Lizard Island. Settlement of most associated epibiota was generally inhibited under these conditions. Coral spat survivorship was highest in the presence of Sinularia at Orpheus Island; at Lizard Island, this was the case with the Sarcophyton treatment. Higher survivorship, and in some cases growth, of coral spat near soft corals was apparently due to reduced competition for space between spat and associated epibiota. This hypothesis is supported by the results of a sister experiment where a coating of Sinularia flexibilis extract on settlement tiles significantly decreased fouling by sessile epibiota. Soft corals have an allelopathic effect on recruitment and early development of scleractinian corals and, consequently, on early coral reef community succession.
Problem
The term “allelopathy” was introduced by Molisch [1937, in Rice (1984)] to describe chemically mediated interactions between plants. The phenomenon has been well documented in plant ecology and agriculture, where allelopathic compounds inhibit the establishment of potential competitor plants and play a role in space dominance by reducing competition for other resources (Putnam, 1983). According to the level of chemical compatibility between different species of plants, allelopathic interactions can create certain patterns of associations and species distribution. Allelopathy is thus regarded as an important factor contributing to plant community structure in both natural and cultivated fields (Stowe, 1979; Rice, 1984; Carral et al., 1988).
In the marine environment, chemically mediated interactions (Bakus et al., 1986) have been documented for algae (e. g.Littler et al., 1986; Van Alstyne & Paul, 1988; de Nys et al., 1991, 1995; Schmitt et al., 1995; Friedlander et al., 1996; Suzuki et al., 1998), zooplanktonic organisms (Folt & Goldman, 1981), sponges (e. g.Sullivan et al., 1983; Bingham & Young, 1991; Davis et al., 1991; Thacker et al., 1998; also see McClintock, 1997), nudibranchs (Faulkner & Ghiselin, 1983; Pennings & Paul, 1993; Slattery et al., 1998), ascidians (e. g.Paul et al., 1990), and alcyonacean soft corals (Coll et al., 1982a; Sammarco et al., 1983, 1985; La Barre et al., 1986a; Sammarco & Coll, 1988, 1992; Van Alstyne & Paul, 1988; Coll, 1992; Van Alstyne et al., 1992, 1994; Slattery & McClintock, 1995; Slattery et al., 1995; Slattery et al., 1999).
Chemically mediated interactions play an important role in the life history of alcyonacean soft corals (Sammarco & Coll, 1988, 1992). Soft corals are important contributors to reef community structure, sometimes being the dominant group on coral reefs in the Indo-Pacific region (Benayahu & Loya, 1981; Dinesen, 1983; Fabricius, 1995). Soft corals also produce a diverse range of secondary metabolites, principally terpenoids (Tursch et al., 1978; Sammarco & Coll, 1988; Coll, 1992), to which ecological roles have been attributed. These include defense against predation (Coll et al., 1982b; La Barre et al., 1986b; Wylie & Paul, 1989; Van Alstyne et al., 1994), competition for space with scleractinian corals (Sammarco et al., 1983, 1985; Dai, 1990), reproduction (Bowden et al., 1985; Coll et al., 1995; Slattery & Paul, 1995) and anti-fouling (Bakus et al., 1986; Coll et al., 1987; also see Sammarco & Coll, 1990).
Sinularia flexibilis is known to contain the biologically active diterpenes flexibilide and dihydroflexibilide (see Maida et al., 1993a). The allelopathic effects of these compounds on certain species of scleractinian corals are well documented (Coll, 1992). In both field and laboratory experiments, they have been shown to kill scleractinian corals (Coll & Sammarco, 1983; Sammarco et al., 1983, 1985; Aceret et al., 1995). Sarcophyton glaucum is also a chemically rich species (Tursch et al., 1978), although the ecological functions of its diterpenes are still being investigated.
Factors that influence settlement and recruitment have been extensively studied, and the influence of chemical compounds or chemically mediated interactions on these processes is becoming better known (Bingham & Young, 1991; Morse et al., 1994, 1998; Morse & Morse, 1991, 1996; Pawlik, 1992; Bryan et al., 1997; Woodin et al., 1997).
Studies of allelopathy of alcyonacean soft corals against scleractinian corals have generally focused on effects on adult colonies (Sammarco & Coll, 1988). Until recently, it was unknown whether these allelopathic compounds functioned in an analogous fashion to those of some terrestrial plants, affecting settlement and recruitment of juvenile scleractinian corals and other epibenthic organisms on coral reefs (Maida et al., 1995a, 1995b; Artrigenio & Alino, 1996).
We now know that soft corals can suppress nearby recruitment of scleractinian coral spat, and that this effect is a function of current direction and distance from the soft coral (Maida, 1993; Maida et al., 1995a, b). In this study, we demonstrate that allelopathy can affect the community structure of coral recruits by differentially affecting species composition, growth and survivorship of spat.
Material and Methods
1. Design of coral settlement racks
In this experiment, the unglazed sides of ceramic tiles (size: 150 × 150 mm) were used as settlement substrata (see Harriott & Fisk, 1987). Stacks of five tiles were prepared by center-drilling the tiles, mounting them on stainless steel bolts, and separating them by plastic spacers. The settlement units were designed this way to prevent grazing and provide a cryptic microhabitat for coral larval settlement. A 12 mm gap between the plates helped to keep large predators and grazers from accessing the settlement substrata, while permitting water flow and light penetration between the plates (see Maida et al., 1994).
The different plates in each stack represented replicates of distance within a direction, radiating out from the soft coral (or control). The plates are true replicates because coral planulae are “coarse-grained” organisms (Levins, 1968) due to their scale of perception and their settlement behavior. They do not possess focusing eyes or strong swimming apparati, and are ∼ 500 – 1200 µm in length. This limits their perception to only a small part of their environment. Their tactile response relates only to their immediate surroundings within a distance of perhaps several mm; they are therefore unaware of nearby settlement substrata, which may be only 12 mm away. This concept has been discussed in greater detail by Sammarco (1994) and Maida et al. (1995a).
Each of three settlement stacks were placed in a row, separated from each other by 10 cm and bolted to a plastic PVC sheet (15 × 65 cm). They were spaced at distances of 5, 30 and 55 cm from the treatment organism, at the center of the grid. Eight sheets (with attached settlement stacks) were fastened to each of four galvanised steel grids mounted approximately 40 cm above the bottom at a mean depth of 4 m at each site. The PVC sheets were arranged on each steel grid in a radial array extending from the center of the grid along eight compass directions: N, NE, E, SE, S, SW, W and NW. The original purpose of using 8 different directions extending out from the center of the grid was to attempt to determine whether coral settlement varied significantly with respect to direction and distance from the soft coral, hard coral, or other treatment organism placed at the center of the grid. It was also designed to test whether any significant variation was correlated with current direction (see Maida et al., 1993b). Details regarding differences in responses with respect to direction and distance may be found in Maida et al. (1995a, 1995b). Directional and distance factors were not considered in this study.
The experiment was performed at Orpheus Island (18°40′ S, 145°30′ E) and Lizard Island, (14°41′ S, 145°28′ E), Great Barrier Reef, Australia. The specific sites were the southern fringing reef of Pioneer Bay, Orpheus Island, initiated in early October 1990, and the western fringing reef of Palfrey Island, Lizard Island, in the lagoon, started in early November.
The two treatments consisted of an array of settlement plates placed around a large colony of 1) the soft coral Sinularia flexibilis in the center of the steel grid (S1), and 2) the soft coral Sarcophyton glaucum (S2) (Fig. 1). At each grid site, the biological and physical environment of the four grids was the same (see Maida, 1993; Maida et al., 1995a).
Schematic diagram of the basic experimental design. Settlement plates have been arranged on a steel mesh rack around a center point, following compass directions. Pictured is control 1 with settlement plates in the absence of a central organism of potential influence. A second rack was also implanted – control 2 – where a scleractinian coral (planktivorous benthic colonial organism), similar in size to the experimental soft coral, was placed in the center of the settlement plates. A third rack represented treatment 1 where a colony of Sinularia flexibilis was placed at the center of the plates. This soft coral is known to contain allelopathic complementary (secondary; Sammarco & Coll, 1997) metabolites which are released into the environment. A fourth rack represented treatment 2, where another soft coral, Sarcophyton glaucum, also known to possess allelopathic complementary metabolites, was placed at the center of the settlement plates.
Two controls consisted of 1) a similar array with no organism in the center of the grid (C1), and 2) an array of settlement plates placed around a colony of a planktivorous scleractinian coral at the center of the grid (C2). The scleractinian corals used were Porites andrewsi Vaughan at Orpheus Island and Seriatopora hystrix Dana at Lizard Island. The purpose of using these scleractinian corals was to control for a) potential predation upon larvae by the soft coral and b) micro-eddying effects occurring in the lee of the coral due to currents, potentially resulting in entrainment of larvae and patchiness in settlement (see Sammarco & Andrews, 1988, 1989; Sammarco, 1994). It was not expected that the scleractinian corals acting as controls would affect recruitment through the release of their own planulae (Seriatopora hystrix, a brooder) or fertilized eggs (Porites andrewsi, a broadcaster). This is because the larvae would not be expected to be competent to settle for between 4 and 72 h (see Sammarco, 1994) and would most likely be carried away from the experimental site by that time.
Initiation dates for the experiments corresponded to four weeks prior to the annual time of coral spawning for the respective regions (Harrison et al., 1984; Willis et al., 1985; Babcock et al., 1986). After nine months, all settlement stacks were collected from the study site and placed in flow-through seawater tanks. Individual plates were then separated and analyzed in vivo using a dissecting microscope (60 – 360 ×).
2. Analysis of coral recruitment
Only the three lower unglazed surfaces of the settlement plates were analysed for coral recruitment because no recruitment was recorded on the upper surfaces in a preliminary survey of the plates three months into the study (Maida, 1993). Recruitment is defined here as settlement followed by deposition of a recognisable calcareous skeleton, irrespective of whether or not the spat was alive at the time of sampling (sensuSammarco, 1980, 1982, 1991; Sammarco & Andrews, 1988, 1989; Wallace, 1985).
Settlement plates were examined placed in a Perspex® tray filled with seawater and examined for coral spat with the aid of a dissecting microscope. To facilitate processing, larger pieces of branching and filamentous algae were removed first with fine dissecting forceps. Coral spat were assessed for density (no. per 225 cm2 plate) in order to enable calculation of species diversity. Mortality and size were also assessed. To record size and placement of coral spat, a color image of each settlement plate was digitized, labeled and stored in a computer. The images were digitized using a high resolution video camera fitted with a 6 × 12.5 close-up zoom lens (Sony® DXC-151P) mounted on a Wild® microscope and connected to a Quick Capture® frame-grabber (DT2255 – 50Hz) installed on a Macintosh® II Ci computer. Size of coral spat (basal area in mm2) was measured by computer image analysis using Image® 1.47 and Color Image® 1.31.
Settlement plates were also assessed for total cover of sessile organisms using Image® software and routines for color segmentation contained therein. Cover was expressed as total area [cm2] and percent cover.
At the end of the experiment, settlement tiles were bleached in sodium hypochlorite solution and sun-dried to facilitate identification of the coral spat. Coral spat were identified to family where possible, based on the electron micrograph collections prepared by Sammarco, Carleton and Mackley (unpubl.).
3. Data analyses
The experiments each followed a balanced, replicated, Model I three-way factorial orthogonal design. The effects of the following three factors on coral spat distribution were assessed: 1) Type of organism in the center of the grid (Sinularia flexibilis, Sarcophyton glaucum, scleractinian coral and no organism; 2) Orientation of the settlement plates around the soft coral (or control) along eight pre-defined compass directions; and 3) Distance of the settlement units from the organisms. Original analyses were performed using full three-way ANOVAs. Here, only the organism-type treatment will be considered in detail. Data from the other treatments have been pooled. Thus, in general, one-way ANOVAs will be considered. As mentioned above, related results have been reported elsewhere (Maida et al., 1995a, 1995b). Here, we will focus on the comparative community structures of coral recruits as a whole with respect to major treatments within a single factor. For the reasons stated earlier, the multiple plates occurring at each distance served as replicates. In general, higher-order interactions will not be discussed unless significant. In this specific experiment, there were no significant higher-order interactions.
Prior to analysis, the data were tested for normality and homoscedascity. When necessary, data were transformed by calculating the square-root of (Y + 0.5) for purposes of normalization (Sokal & Rohlf, 1981). A posteriori statistical tests were also performed using Tukey's Multiple Comparisons of Means Test (Sokal & Rohlf, 1981).
Juvenile corals were assessed for mortality, as evidenced by the absence of tissue, infestation by endolithic green algae, and overgrowth by associated epibenthic organisms (Sammarco, 1980, 1982, 1991). Data regarding distribution, abundance and mortality were analysed using Contingency Analyses (Chi-square and G-tests). Diversity Indices were calculated using the Shannon-Wiener Index, and pair-wise comparisons of indices were made using the procedures of Hutcheson [1970, in Zar (1984)].
4. Inhibition effects of Sinularia flexibilis extracts on epibenthic settlement
To test the ability of the lipophilic extract of Sinularia flexibilis to inhibit coral settlement, soft coral colonies were collected from Lizard Island, frozen at –20 °C and freeze-dried. The freeze-dried coral tissue (236 g) was extracted with dichloromethane [DCM, 10 ml · g–1 (dw) tissue] by soaking the ground tissue in a sealed vial for two 24 h periods and decanting the solvent from the sample. The solvent was evaporated to dryness, and 20 g of the crude solvent extract was dissolved in 2 l DCM.
Settlement inhibition was studied using the unglazed sides of ceramic tiles (150 × 150 × 3 mm) as settlement substrata. Twenty treatment tiles were impregnated with the treatment solution by soaking them in it for 30 min. The plates were removed, and the solvent (DCM) was allowed to evaporate to dryness in a fume hood. Five of the twenty treatment tiles were subsequently extracted with DCM for 24 h, and the extract was evaporated to dryness and weighed. This afforded the weight of crude extract adsorbed onto each tile, which averaged 95 mg (± 4.3 SE) per tile (225 cm2 or ∼ 0.42 mg · cm-2). The other fifteen treatment tiles were mounted in stacks of three tiles on stainless steel bolts. The tiles in each stack were spaced with gaps of 25 mm. Control tiles consisted of 15 tiles soaked in DCM only and mounted in a similar fashion.
After preparation, the stacks were attached to two galvanized steel grids such that each grid had representative stacks of control and treatment tiles. The grids were placed at a depth of 3 m on the eastern reef flat at Palfrey Island, off Lizard Island in late January 1991 (late austral summer). After 21 days, the stacks were collected, separated from each other and stored for subsequent fouling analysis.
Settlement plates were analysed using a dissecting microscope. Density of sessile organisms was measured as number per plate. Images of tile surfaces were digitized and stored, and cover of epibiota was calculated. Algal settlement was analysed by area of cover using the computer image analysis system described above. Data from treatment (extract) and control tiles were then compared.
Results
1. Taxononomic composition of scleractinian coral recruits
Orpheus Island. Of the 1,038 coral spat assessed in the experiment at Orpheus Island, over 90 % of the identifiable ones were from two families. The Pocilloporidae were the dominant taxon (61.4 %), followed by the Acroporidae (33.7 %). The remaining corals were relatively rare, belonging to the families Poritidae, Mussidae, Faviidae and Fungiidae. Three spat of the ahermatypic coral genus Culicia were also found.
There was a significant difference between treatments (presence of soft corals) and controls (absence of soft corals) with respect to relative abundances of the two dominant coral taxa (P < 0.05, G-test; Fig. 2a).
Relative abundances of the taxonomic groups of coral spat by treatment in the two experimental regions: a. Orpheus Island (central Great Barrier Reef) and b. Lizard Island (northern Great Barrier Reef). See Table 2 for sample sizes.
The taxonomic diversity of coral spat (at the family level) as measured by the Shannon-Wiener Index (H′) also varied significantly between treatments. Settlement plates influenced by Sinularia flexibilis and Sarcophyton glaucum yielded the lowest diversity of coral spat (H′ = 0.329 and 0.427, respectively), while those around the scleractinian coral Porites andrewsi afforded the highest (H′ = 0.670; Table 1a).
| a | treatment | diversity index | |||
| C1 – control 1 | 0.537 | ||||
| C2 –Porites | 0.670 | ||||
| S1 –Sinularia | 0.329 | ||||
| S2 –Sarcophyton | 0.427 | ||||
| comparison | df | t | P | significance | |
| C1 × C2 | 70.1 | – 1.423 | > 0.10 | ns | |
| C1 × S1 | 80.6 | 2.072 | < 0.05 | * | |
| C1 × S2 | 51.4 | 1.098 | > 0.10 | ns | |
| C2 × S1 | 87.9 | 3.52 | < 0.001 | * * * | |
| C2 × S2 | 51.3 | 2.514 | < 0.05 | * | |
| S1 × S2 | 60.9 | – 0.949 | < 0.10 | * * | |
| b | treatment | diversity index | |||
| C1 – control 1 | 0.668 | ||||
| C2 –Seriatopora | 0.638 | ||||
| S1 –Sinularia | 0.774 | ||||
| S2 –Sarcophyton | 0.615 | ||||
| comparison | df | t | P | significance | |
| C1 × C2 | 820.3 | 0.836 | > 0.10 | ns | |
| C1 × S1 | 712.6 | – 3.003 | < 0.01 | * * | |
| C1 × S2 | 1023.6 | 1.622 | > 0.10 | ns | |
| C2 × S1 | 723.9 | – 3.572 | < 0.001 | * * * | |
| C2 × S2 | 879.5 | 0.645 | > 0.50 | ns | |
| S1 × S2 | 757.9 | 4.534 | < 0.001 | * * * |
Lizard Island. Of the 7,032 coral spat observed in the Lizard Island site, the same two groups of spat dominated the community – the families Acroporidae and Pocilloporidae, accounting for 73 % of all identifiable spat. Here, acroporids constituted the dominant taxon with 53 % of the total, followed by the Pocilloporidae with 20.5 %. The remaining corals were relatively rare, being derived from the Faviidae, Poritidae, Mussidae and Fungiidae (in order of abundance). 143 spat belonged to the ahermatypic coral genus Culicia.
The two dominant coral taxa varied significantly in relative abundance with respect to the major treatments at Lizard Island (P < 0.001, G-test). Settlement plates influenced by Sinularia flexibilis yielded the lowest proportion of acroporid recruits (Fig. 2b).
At Lizard Island, taxonomic diversity of coral spat (as measured by H′) also varied significantly between treatments. In contrast to the Orpheus Island experiment, however, settlement plates affected by Sinularia flexibilis exhibited the highest diversity of coral spat (H′ = 0.774), significantly higher than the other treatments (Sarcophyton, H′ = 0.615 and Porites, H′ = 0.668; P < 0.01, Hutcheson's Test; Table 1b).
2. Survivorship of coral spat
Cumulative survivorship of coral spat at Orpheus Island was 34.2 % (Table 2). There was a significant difference in survivorship between treatments here (P < 0.001, G-test frequency analysis). Settlement plates associated with Sinularia flexibilis yielded the highest survivorship of coral spat (Table 2a).
| a | treatment | no. live spat | no. dead spat | % survivorship |
| C1 – control 1 | 88 | 231 | 27.6 | |
| C2 –Porites | 108 | 217 | 33.2 | |
| S1 –Sinularia | 101 | 123 | 45.1 | |
| S2 –Sarcophyton | 58 | 112 | 34.1 | |
| b | treatment | no. live spat | no. dead spat | % survivorship |
| C1 – control 1 | 507 | 1,459 | 25.8 | |
| C2 –Seriatopora | 444 | 1,575 | 21.9 | |
| S1 –Sinularia | 338 | 1,252 | 21.3 | |
| S2 –Sarcophyton | 663 | 794 | 45.5 |
Cumulative survivorship of coral spat at Lizard Island was 27.8 % (Table 2b). There were also highly significant differences in survivorship between treatments (P < 0.001, G-test frequency analysis). Here, plates associated with Sarcophyton glaucum yielded the highest values.
3. Growth in coral spat
The size of the scleractinian coral spat at Orpheus Island (basal area of skeleton produced over a nine-month period) ranged from 0.1 to 51.7 mm2, with 95.4 % of the corals being < 5.3 mm2. Live coral spat at Orpheus Island exhibited the same size range. There were no significant differences in the average size of live coral spat between treatments (P > 0.05, one-way ANOVA). Dead coral spat varied from 0.2 to 15.1 mm2 and also did not differ significantly in average size between treatments (P > 0.05, ANOVA).
At Lizard Island, size of coral spat ranged from 0.2 to 194 mm2, with most of the corals (89.6 %) being very small (< 5 mm2). There was a significant difference in average size of live spat between treatments here (P < 0.001, one-way ANOVA). Specifically, the spat in the Sarcophyton glaucum treatment were significantly larger than those on plates in the other treatments and controls (Tukey's a posteriori Multiple Comparisons Test; Fig. 3a). There were no significant differences between the average size of dead coral spat for the different treatments (P > 0.05, ANOVA).
a. Average size of live scleractinian coral spat at Lizard Island, by treatment. Coral spat on settlement plates under the influence of the soft coral Sarcophyton glaucum were significantly larger than those in the other treatments (P < 0.001, one-way ANOVA). Error bars represent standard errors (SE). Sarcophyton treatment significantly different from other treatments and control 1 (Tukey's a posteriori Multiple Comparisons of Means Test. Sample sizes: control 1, n = 507; Seriatopora (C2), n = 444; Sinularia, n = 338; and Sarcophyton, n = 663. b. Average total cover of living epibiota in cm2 at Lizard Island (black bars) and Orpheus Island (white bars), respectively, by treatment. Error bars represent standard errors (SE). n = 72 in each case. Significant difference (P < 0.001, one-way ANOVA) between controls as a group (control 1 and Porites) vs. soft corals as a group (Sinularia flexibilis and Sarcophyton glaucum) at Orpheus Island; similar results for Lizard Island.
4. Total cover of sessile epibiota
At Orpheus Island, total cover of sessile epibiota ranged between 19.9 % and 55.8 %. In addition to coral spat, the sessile community was comprised mainly of red algae, oysters and ascidians. There were significant differences in total cover between the two treatments and the two controls (P < 0.001, one-way ANOVA). The presence of either Sinularia flexibilis or Sarcophyton glaucum significantly reduced colonization by other organisms when compared to the controls (Fig. 3b).
At Lizard Island, total living cover ranged between 31.4 % and 98 %. The dominant epibiota were similar to those observed in the Orpheus Island experiment, with the addition of green algae. Total cover varied significantly between treatments at Lizard Island, exhibiting a trend similar to that observed at Orpheus Island (P < 0.001, one-way ANOVA), where the presence of Sinularia flexibilis and Sarcophyton glaucum, respectively, significantly reduced successful colonization of epibiota in comparison to controls (control 1 and Seriatopora;Fig. 3b).
5. Inhibition of recruitment by the lipophilic extract of Sinularia flexibilis
After three weeks, the primary fouling organism on the control and treatment tiles was the red alga Ceramium sp. Several serpulid polychaetes were also found on the control tiles.
Tiles coated with a DCM extract of Sinularia flexibilis exhibited significantly reduced algal settlement and growth. Algal cover on the control tiles averaged 43.0 % (96.6 cm2). This was significantly more than on treatment tiles, which averaged 3.0 % (6.5 cm2) (P < 0.001, Wilcoxon's U-test).
Discussion
The finding that pocilloporid, followed by acroporid, coral spat were dominant on the plates at Orpheus Island was consistent with the relative abundance patterns of coral recruits observed in a study performed at the same site one year earlier (Maida et al., 1995b). This dominance relationship was also consistent with the results of other experimental recruitment studies performed on inshore reefs of the central region of the Great Barrier Reef (Sammarco, 1983, 1991).
At Lizard Island, acroporid coral spat were more abundant than pocilloporids. Again, this was consistent with the taxonomic composition of dominants observed here in an earlier coral settlement experiment (Harriott, 1985).
The presence of Sinularia flexibilis dramatically affected the relative abundances of coral spat, thereby influencing spat diversity. At Orpheus Island, the settlement plates around S. flexibilis yielded the lowest diversity of coral spat. By contrast, at Lizard Island, this same treatment yielded the highest diversity. These different responses may be attributable to the species-specific effects of soft coral toxins on different coral spat settling in the different geographic regions.
Differences in overall settlement could also be due to differences in larval supply, mortality due to predation or physical disturbance, or patchiness in settlement. Previous coral recruitment studies have indicated that levels of coral settlement in the northern region of the Great Barrier Reef, near Lizard Island and further inshore, are higher than similar areas in the central Great Barrier Reef region (Sammarco, 1983, 1991; Harriott & Fisk, 1988; Fisk & Harriott, 1990). But the allelopathic effects examined here will be region-specific due to the sensitivity of the individual species. Analyses using numerical diversity indices smooth these effects during analysis. In addition, previous analyses of these data have indicated that the coral spat exhibited extremely similar responses to the presence or absence of soft corals with respect to distance and current direction in these two different geographic regions. Estimates of comparative larval supplies were derived from settlement on the control grids, clear of the influence of any organism at the center of the grid, and these differences have been reported and discussed earlier (Maida, 1995a, 1995b).
The local distribution of pocilloporid and acroporid spat was dependent upon the presence or absence of soft corals. Acroporid spat appear to be particularly sensitive to the allelopathic effects of Sinularia flexibilis. Certain species of Acropora are known to be particularly susceptible to (secondary) metabolites produced by this soft coral. Coll & Sammarco (1983) demonstrated in a laboratory experiment that these toxins kill colonies of Acropora formosa.Webb & Coll (1983) also observed that the same chemicals alter the photosynthetic and respiratory rates in this coral. Approximately 70 species of Acropora inhabit the Great Barrier Reef. Those which recruit on the inner shelf in the central region may not necessarily be the same as those which recruit at the outer shelf (see Sammarco, 1991) in the northern region. Some species-specificity apparently exists in the response of the respective sets of recruits to the toxins. It is possible that toxin production by soft corals or larval production by hard corals may vary geographically, adding to overall variation in response to the treatments in the two regions.
Pocilloporids are known to recruit most abundantly in inshore waters of the central Great Barrier Reef region, with acroporids recruiting less abundantly (Sammarco, 1983, 1991). At Orpheus Island (inshore), the settlement of acroporids and other scleractinians was lower around Sinularia flexibilis, thus further increasing the relative abundance of pocilloporid spat. This decrease in equitability was primarily responsible for reducing of overall spat diversity as measured by H′ near S. flexibilis.
At Lizard Island, where acroporid spat are known to be dominant (see Harriott, 1985), settlement of acroporids was significantly reduced around Sinularia flexibilis. The decreased dominance of this group and thus increased equitability in taxonomic representation boosted coral spat diversity (H′) within this treatment.
Interestingly, survivorship of coral spat around the soft corals was higher than around the controls. On the average, survivorship at Orpheus Island was 34.2 % – significantly higher than that observed in a previous experiment (10 %; Maida et al., 1995b). The overall higher survivorship may have been due to the stacked settlement plates, providing better protection from predators and grazers.
The highest survivorship on Orpheus Island occurred on settlement plates around the soft coral Sinularia flexibilis, and on Lizard Island around Sarcophyton glaucum. Once again, the secondary metabolites of different soft corals may affect the types of newly settled coral spat differentially in regions with different environments. Orpheus Island is a continental island in the central region of the GBR with inshore reefs characterized by high sedimentation, a variable temperature regime, variable salinity and low wave exposure. On the other hand, Lizard Island is a northern continental island with mid-shelf reefs characterized by lower to moderate sedimentation, lower variability in temperature, lower variation in salinity and moderate wave exposure (see Done, 1982; Sammarco & Crenshaw, 1984; Sammarco, 1991).
Higher survivorship of coral spat in the presence of the soft corals would appear to be counter-intuitive. This is because previous studies of allelopathic interactions between soft corals and adult scleractinians have demonstrated that toxins released by Sinularia flexibilis and Sarcophyton crassocaule induce tissue necrosis and mortality in various corals (Coll et al., 1982a; Sammarco et al., 1983). These earlier results would imply that, all other things being equal, soft coral allelochemicals should also negatively affect survivorship in larval and juvenile scleractinians. Clearly, however, this was not the case. Those spat that successfully settled near these soft corals, although fewer in number, experienced lower mortality and, at Lizard Island, within the Sarcophyton glaucum treatment, enhanced growth.
This may be due to several factors. Firstly, there may be a difference in the resistance of these coral species to the two sets of soft coral toxins in the two different environments. Sammarco et al. (1983, 1985) found that the allelopathic effects were highly species-specific –i. e. some alcyonacean species are much more effective allelopathic and some scleractinians are much more susceptible than others. Secondly, it is possible that the effectiveness of an alcyonacean species in influencing coral settlement varies with respect to local environment, or it may be population-specific.
How can a newly settled spat grow faster under the influence of allelopathic compounds than under normal conditions? There are two possible mechanisms. Firstly, some scleractinian corals may be more tolerant of or resistant to such allelochemicals. Thus, they will successfully settle and appear to grow faster because their counterparts will be growth-inhibited. Secondly, survivorship and growth could be enhanced by reducing competition with other sessile epibiota. The soft corals reduced the total amount of all sessile epibiota on the settlement plates and also on the plates coated with a DCM extract of Sinularia flexibilis. Coral spat under these circumstances would have had fewer and most likely less intense contact encounters with sessile epibiotic competitors for space (Sammarco, 1980, 1982) and experienced less shading by associated epibiota (Sammarco & Carleton, 1981), thereby increasing their probability of survival.
The reduced coral recruitment observed in the presence of the soft corals does not appear to be caused by post-settlement mortality (see Keough & Downes, 1982). If this were the case, one would expect higher levels of mortality around the soft corals, as indicated by the remaining skeletons. The results from an earlier pilot experiment (Maida et al., 1995b) and from this study indicate that spat survivorship around the soft corals was similar to or higher than the controls. We hypothesize that the lower density of coral recruits around the soft corals was caused by a negative preference on the part of the coral planulae to settle near the latter (Sammarco & Carleton, 1981; Keough & Downes, 1982).
Most coelenterate larvae have specialized chemosensory apparati (see Chia & Bickell, 1978). Based on the results of this and related studies, we hypothesize that, as coral larvae enter the vicinity of a soft coral, they sense allelochemicals either in the water column or on the substratum, reject the area, and resume their search for a suitable settlement site. It is also possible that the planulae settle and die prior to secreting a calcareous skeleton, in which case there would be no tell-tale skeleton left behind to count or assess for condition. (This is a problem in working with all sessile invertebrate larvae which secrete a calcareous skeleton.)
The results reported here provide new evidence that, through allelopathic interference, alcyonacean soft corals can influence the recruitment and survival of scleractinian corals on immediately surrounding substrata. In this way, they can influence coral colonization processes and patterns of coral distribution and abundance.
Summary
Field experiments have demonstrated that the soft corals Sinularia flexibilis and Sarcophyton glaucum affected the recruitment of various scleractinian coral spat differentially. At Orpheus Island (n = 1038 spat) and Lizard Island (n = 7032 spat), there were significant differences between recruitment success of the two dominant coral taxa, the Pocilloporidae (O.I., 61.4 %; L.I., 20.5 %) and Acroporidae (O.I., 33.7 %; L.I., 53 %). Diversity indices (Shannon-Wiener Indices) varied significantly between treatments at both islands, due to selective inhibition of acroporid spat by Sinularia flexibilis at both sites. Coral spat growth was higher in the presence of Sarcophyton at Lizard Island. Settlement of most associated epibiota was generally inhibited. Coral spat survivorship was highest in the presence of Sinularia at Orpheus Island; at Lizard Island, this was the case with Sarcophyton. Higher survivorship, and in some cases growth, of coral spat near soft corals may have been due to reduced competition for space between spat and associated epibiota. A coating of Sinularia flexibilis extract on settlement tiles significantly decreased fouling by sessile epibiota.
Acknowledgements
We thank B. P. Ferreira for her invaluable assistance in the field and comments throughout the study and on the manuscript. We are also grateful to M. Becerro, R. de Nys, K. Fabricius, P. Spratt, P. Stephenson, C. Wilkinson, D. Zeller and many others who assisted in the field. We also thank G. Charles, S. Charles (Orpheus Island Research Station), L. Vail, A. Hoggett, M. & L. Pearce (Lizard Island Research Station) for logistic support and assistance at the research stations. We are grateful to A. R. Carroll for comments throughout the study and R. Powell and T. Rider for assistance with the graphics. This research was supported by the Australian Research Council (ARC) and CAPES (Brazilian Education Ministry). The manuscript benefited greatly from comments made by S. McKillup and several anonymous reviewers.
