Coral communities and reef growth in the southern Great Barrier Reef

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1 Coral Reefs (1997) 16: Coral communities and reef growth in the southern Great Barrier Reef R. van Woesik, T. J. Done Department of Marine Sciences, University of the Ryukyus, Senbaru 1 Nishihara, Okinawa , Japan Australian Institute of Marine Science, PMB No 3 Townsville MC, Queensland 4810 Australia Accepted: 29 July 1996 Abstract. Fringing reef development is limited around 22 S along the inner Great Barrier Reef, although there is substantial development north and south of this latitude. This study examined the relationships among coral communities and the extent of reef development. Reefs were examined to determine coral composition, colony abundance, colony size and growth form between the latitudes 20 S and 23 S. Major reef framework builders (scleractinian genus Acropora and families Faviidae and Poritidae) dominated reefs north and south of 22 S, but declined significantly at 22 S where foliose and encrusting corals (¹urbinaria and Montipora spp.) were most common. Porites spp. were present at 22 S but had encrusting morphologies. Consistently high turbidity at this latitude, caused by a 10 m tidal range and strong tidal flows, resuspends silts from the shallow shelf, and appears to have precluded reef development throughout the Holocene, by limiting the abundance, stunting the growth, and shortening the life expectancies of reef framework corals. The distinctions between natural and human-induced degradation may be interpreted on the basis of the relationship between Holocene development and current benthic community longevity. A mismatch between substantial past reef building capacity (a broad and/or thick reef) and non-existent or limited present reef-building capacity could signify anything from a long-period, natural cycle to an unprecedented deterioration in ecosystem function caused by human influence. Introduction In the Great Barrier Reef (GBR) region, fringing reefs (Fig. 1a) are common on many continental islands close to the mainland shore (Hopley et al. 1989). The best Correspondence to: R. van Woesik developed of these reefs typically have both framework and detrital elements and distinctive reef flats and reef slopes (Hopley 1982; Kleypas 1991). The least developed are termed incipient reefs (Hopley et al. 1989), essentially detrital banks without reef flats, and colonised by hard corals, usually with other sessile benthos such as macro-algae, soft corals and zoanthids. In addition, there are coral communities (Fig. 1a) without appreciable framework or detrital accumulations on the rocky flanks and headlands of the islands (personal observation). Such differences in degree of coral reef development are a consequence of time-varying differences in the rates of production versus destruction, and of accumulation versus dispersal, of the skeletons of reef-building organisms, throughout the time available for the reef to grow (Davies 1983). For many GBR fringing reefs, the entire accretion of reef structure has taken place during the last years (e.g. Chappell et al. 1983; Kleypas 1996). Chappell et al. (1983) proposed two models for the development of fringing reefs with reef flats (Fig. 1b, c); one for those which had reached their current widths soon after sea level peaked y BP (Fig. 1c), and one for those whose seaward edge has gradually advanced across the sea floor since that time (Fig. 1b). In both models, coral growth on the reef s outer margin is a primary source of the skeletal elements comprising the reef matrix. In the present study, we look for relationships between the extent of Holocene reef development and the ecological structure of associated reef slope coral communities. We also seek patterns in community structure in relation to the reef s position and environmental setting. Our hypothesis is that differences in the cumulative production of reef-building materials should reflect differences in the dynamics of benthic communities and populations over that 5000 y period. Our goal was to establish whether such proposed differences in (ecologically) long-term dynamics can be recognised in a survey of community structure and size frequencies over a large number of well developed and incipient reefs in a wide range of environmental settings.

2 104 Fig. 1 Fringing reefs. a Definition of terms and typical dimensions of reefs studied. Dotted lines indicate earlier Holocene positions of reef margin. b Chappell et al. s (1983) model 1 of fringing reef growth for reefs with decreasing age at increasing distance landward from reef edge, and c model 2, for reefs with little lateral extension during the Holocene. The horizontal sea level line represents the 1 m high stand at &6000 y BP, the sloping line represents the gradual fall in sea level to its present level, and the irregular lines represent the position of the reef surface at 0, 2000, 3000, 4000 and 6000 y BP The study area Hopley (1982) noted that inshore reefs of the GBR were generally poorly developed south of 21 S. However extensive fringing reefs were later described around the Keppel Islands in the far south (Fig. 2; VanWoesik 1992), indicating that 22 S represented a hiatus in the distribution of nearshore reefs, rather than their southern limit. Kleypas (1991, 1996) noted that both the inshore limit to reef distribution and the extent of reef development, in this area, were associated with proximity to Broad Sound (Fig. 2), a large, shallow and silty embayment without any major river running into it. Broad Sound has eastern Australia s highest tidal range (&10 m), and tidal currents suspend fine bottom sediments, making the water too turbid for corals, and excluding reef development adjacent to islands within the sound (Kleypas 1996). Adjacent to Broad Sound, reef development (width and thickness) was also inversely related to tidal range. This study describes coral communities to the north and the south of Broad Sound, both within and beyond its influence. We looked for patterns in the composition of coral communities, the overall abundance of corals per unit area, and their size frequency distributions. As well as providing the first description of coral communities in this area, these measures may also provide some insights into ecological and demographic causes of the hiatus in reef development at 22 S. Previously, Done (1982) described distribution patterns of seventeen coral communities along a nearshore to offshore transect in the central Great Barrier Reef around 19 S. However nearshore reefs were poorly represented in that study, and possible relationships between community structure and reef growth were not considered. Several community attributes (composition, abundance, size frequency distribution, persistence, succession and history) may influence the capacity of sites to accrete reefal limestones, either as in situ reefal framework or as detrital accumulations (Davies 1983). Taxonomic composition is presumed to reflect both the available species pool and the site s physical (Done 1982) and biological (Sheppard 1982) suitability for coral growth and development (see also Ricklefs 1987; Whittaker 1975; Levin 1989). Abundance and size frequency distributions (reflecting persistence of individual coral colonies) may tell us more about the site s disturbance regimes, successional stage and/or history of development (Jackson and Hughes 1985; Hughes 1989). Methods Field methods The study is based on surveys of coral communities on reefs distributed over three degrees of latitude and an area of around 6000 km in four regions defined by the following island groups (Fig. 2): the Whitsunday Islands (region 1, &20 S); the Cumberland Islands (region 2, &21 S), the Northumberland Islands (region 3, &22 S) and the Keppel Islands (region 4, &23 S). One hundred and twenty-five sites were examined on 37 continental islands visited between 1987 and 1991 (Table 1). All the sites were surveyed by RVW and are reported in detail in Van Woesik (1992). At most of the islands visited, one to three selected sites were surveyed on exposed and sheltered sides (Table 1). However at several islands, a greater number of sites (up to 21, Table 1) were surveyed. There was no conscious effort to select sites on the basis of their species composition or their size frequency distributions, which were the main variables to be recorded. The reefs were located with the aid of aerial photographs and navigation charts. A reconnaissance was undertaken to locate the reef margin, to note the general morphological and biological features of the area, and to determine the upper and lower bathymetric limits of coral growth. A site was established in the first apparently representative area of coral growth encountered. The boundaries of the site (20 10 m) were laid out using a 100 m survey tape. Such sites were usually on the shallow reef slope ((5 m below the reef flat). However a small number (10) were inadvertently located on outer reef flats during extreme weather conditions (particularly at Penrith Island). In all cases the long axis of the site was oriented parallel to the reef margin. The sites were sub-divided with tapes into two rows of four contiguous 5 5 m survey plots. In each subsection, the size and identity of all live corals were recorded (for Scleractinia, after Veron

3 105 Fig. 2 The study area showing island location numbers, site numbers, and regions: region 1, Whitsunday Islands; region 2, Cumberland Islands; region 3, Northumberland Islands (adjacent to Broad Sound); region 4, Keppel Islands

4 106 Table 1 Location of island groups and sites (see also Fig. 2) Region Latitude Island group Number Site Number Position of sites S Hayman Island Offshore S Langford Island Offshore S Hook Island Offshore S Hook Island inlet Offshore S Molle Islands Inshore S Shute Harbour Inshore S Long Island Inshore S Pine Island 1 22 Inshore S Whitsunday Island Offshore S Hamilton Island Offshore S Thomas Island Inshore S Goldsmith Island Inshore S Carlisle/Brampton Islands Inshore S Cockermouth Island Offshore S Scawfell Island Offshore S Penrith Island Offshore S Curlew Island Inshore S Digby and Henderson Islands Inshore S Prudhoe Island Inshore S Percy Islands Offshore S Keppel Islands Inshore and Pichon 1976, 1980, 1982; Veron and Wallace 1984; Veron 1986, and for Alcyonaria, after Bayer et al. 1983). In region 2, the first surveyed, each coral colony was allocated to one of four size classes based on maximum diameter: 1 50 cm; cm; cm; '301 cm. In subsequent surveys (regions 1, 3 and 4), the 1 50 cm size class was subdivided into 1 10 cm and cm classes to improve documentation of smaller corals. Scleractinian colonies were recorded to species, except for the highly speciose genera Acropora and Montipora and for families Poritidae and Fungiidae, where genera and life-forms were used to distinguish colonies. Alcyonarian corals were recorded to genus throughout. A single 20 m line transect was laid along the centre line of the site to provide an estimate of total and live cover of hard corals, soft corals and macroalgae. Seven site descriptors were recorded at each site: depth (measured in m, relative to Low Water Datum), mean annual tidal range (m), distance to the mainland (km), distance to the nearest river (km), and depth of surrounding continental shelf (m). Each site was also assigned a subjective exposure index in relation to the predominant wave direction (from the south-east); either 0 (sheltered by a headland) or 1 (not sheltered by a headland). In addition, individual and closely adjacent islands were assigned an island location, essentially a sequence number from north to south (Fig. 2). Islands were further classified as inshore or offshore according to their distance from shore, the surrounding shelf depth and position relative to the major channels (Table 1). Data storage and analysis Data were stored and preprocessed on ECOPAK (Minchin 1986). Site groups were then defined on the basis of similarities in their composition and abundance (number of colonies per taxon) using an ordination based on correspondence analysis (CA, Gauch 1982; Ter Braak 1985; Ter Braak 1987a). Taxon abundances were not transformed, so the outcomes of the analysis were strongly influenced by numerically dominant taxa. In the ordination s scatterplot, the distance between points ("sites) reflects their similarity based on taxonomic composition. In order to tabulate the mean abundance of taxa in sites with similar composition the scatterplot was subdivided by scribing a number of equal sized, non-overlapping circles centred on clusters of sites. Partial and full canonical correspondence analyses (pcca and CCA Ter Braak 1986, 1987b) were used to identify correlations between site descriptors and patterns of coral distribution and abundance. pcca is an iterative procedure which extracts the dominant pattern of variation in community composition from the taxon data and relates the first few ordination axes with the site descriptors. Because of the variety of units used, site descriptors were standardised by dividing by their standard deviation, which gives them equal weightings. First, one site descriptor (e.g. depth) was tested against the species data set, then the first derived canonical axis was tested for variation from randomness using a Monte Carlo permutation test (n"99) (Hope 1968). If the site descriptor was significantly related to the species distributions, it was defined as a co-variable and used in combination with the next variable to test its significance. This process was applied to all seven descriptors. The significant descriptors were then used in a full CCA on two primary matrices; (a) taxonomic groupings (either families or genera and species), and (b) taxonomic groupings subdivided into colony size classes. The final output was the apportionment, among the seven site descriptors, of all the explained variance in the two matrices. A t test was used to highlight similarities and differences among two environmentally contrasting regions (regions 1 and 3). Random subsets of 10 sites from each region were compared for densities (colonies 100 m ) of alcyonarian corals, total scleractinian corals, and fast growing, slow growing and arborescent scleractinian corals. Normality of data was examined in a Wilk-Shapiro test (Shapiro and Francia 1972), equality of variances and degrees of freedom were calculated using procedures in Snedecor and Cochran (1980), and a posteriori comparisons of means were undertaken using Tukey s HSD test (Zar 1984). Coral size frequency distributions were examined graphically. Results General overview Corals were found to depths of m in regions 1, 2 and 4, but only to 3 4 m in region 3, which is the shallowest and most turbid region (Fig. 2). The Acroporidae had the

5 107 Regional variation Fig. 3 a Overall mean densities (number of colonies. 100 m ) of the major scleractinian families, and b deviations from mean within each study region highest colony densities ("number of colonies per 100 m, Fig. 3a), and within this family, there were, on average, approximately equal densities of colonies in the genera Acropora and Montipora (Fig. 4a). The most densely covered sites were on leeward slopes of outer reefs in regions 1 and 2. On reefs near the mainland, coral species richness and colony densities were lower, soft coral cover was lower, and macrophyte cover was higher (Table 2). Few scleractinian species were restricted to offshore locations, although the density of colonies in the genus Acropora was consistently highest offshore. At the most wave-exposed sites, the predominant species were Acropora humilis, Porites annae, Stylophora pistillata, Pocillopora damicornis, Seriatopora hystrix, Millepora tenella (hydrocoral), tabulate Acropora spp., and the soft corals Sinularia spp. Other genera and species were markedly more abundant on nearshore reefs than offshore reefs. These included Goniastrea spp., Montipora spp., Cyphastrea spp., eptastrea spp., Moseleya latistellata, Pseudosiderastrea tayamai, Polyphyllia talpina, Alveopora spp., Goniopora spp., and Alcyonium spp.. There were marked differences among the regions in reef development, taxonomic composition and densities of all major benthic groups. Reefs in region 1 were large and well developed. Holocene growth rates have been reported at 4 5 mmy, with reef matrices dominated by framework corals (Hopley et al. 1983). These reefs supported on average 21.7% (SE 2.8) coral cover and higher than average densities of colonies in all 13 scleractinian families recorded (Fig. 3b), particularly Faviidae, Poritidae and Acroporidae. The densities of Porites spp. and faviids were well above average (Fig. 4b) and colonies were often larger than 2 m in diameter. Inner reefs supported abundant macrophytes (Phaeophyta). The offshore reefs (e.g. Cockermouth and Scawfell Islands) in region 2, were large framework and detrital structures with a rich coral fauna. Their average growth rate also has been measured at 4 5 mmy (Kleypas 1996). Reefs on average supported 26.9% (SE 2.5) coral cover but had below average densities of most families (Fig. 3b). The inshore reefs (e.g. Goldsmith, Carlisle Islands) were narrower, but still faunistically diverse. From Prudhoe Island southwards (region 3), there was a shift in relative coral abundance compared to region 1. Porites spp., faviids and Acropora spp. were well below average densities (Fig. 4b) and macrophytes were again common on inner reefs. In region 3, outer islands supported narrow reef flats (except Penrith Island which is located 70 km from the mainland), whereas reefs on inner islands were incipient. Reefs have been described as detrital structures, with average growth rates at 2 mm y (Kleypas 1996). Overall, average coral cover was 12.8% (SE 2.9), and corals tended to be small (Fig. 4b). Moreover, densities were below average in the genus Acropora (Fig. 4b) and the families Faviidae (Fig. 4b) and Pocilloporidae. By contrast, they were above average in encrusting Montipora spp. and Porites spp. (Fig. 4b). Colonies of Porites which in other places typically have massive growth forms (viz. P. lutea, P. lobata, and P. mayeri) were almost exclusively found as encrusting forms on these poorly formed reefs. Arborescent colonies of Acropora were rare, and even the usually ubiquitous caespitose Acropora had low densities. ¹urbinaria spp. (Dendrophylliidae) were, by contrast, common compared to other regions (Fig. 3b). In region 4 there were extensive reef flats on leeward shores of the islands while windward reef flats were narrow. No geological cores have been taken in this region, although framework corals were dominant during surveys. Average coral cover was 54.3% (SE 9.9). There were below average densities of corals in all families except for the Acroporidae and Pocilloporidae (Fig. 3b). Region 4 reefs were strongly dominated by arborescent colonies of Acropora (Fig. 4b), particularly large stands of A. formosa and A. microphthalma. Small colonies of bushy A. millepora and Pocillopora damicornis were also common. Contrasts between regions 1 and 3 Despite the striking environmental, faunistic, and geomorphological differences between reefs in regions

6 108 Fig. 4a, b Size frequency distributions (colonies.100 m ) of the four most abundant taxa a overall and b by region. The four size classes are based on maximum diameters of (1) 1 50 cm; (2) cm; (3) cm; and (4) '301 cm 1 and 3 noted already, there was no significant difference (P"0.94) in the total densities of scleractinian or alcyonarian corals in a random subsample of 10 sites from each region. Both regions had an overall mean density of &400 scleractinian colonies per site, or 200 colonies per 100 m (see Fig. 5a), but there was very large variability within each region, especially region 1 s small colonies (1 10 cm). Similarly, there was no significant difference between the two regions (P"0.218) in the density of soft corals. Each region had an overall density of &45 colonies per 100 m, but there were far greater densities of small colonies (1 10 cm) in region 1 than in region 3. However there were clear differences in the abundance of some groupings of hard corals. Region 1 supported higher densities of slower-growing corals and arboresent corals than region 3 (P"0.016 and P"0.026 respectively). The slower-growing corals comprised nonfoliaceous and non-branching forms within the families

7 109 Table 2 Comparison of reef communities based on a random sample of 40 sites from both inner and outer islands across all regions. Cover estimates were derived from a 20 m line transect through the middle of each site. Colony densities and taxonomic richness were derived from the quadrat censuses Inshore island Offshore island p reefs reefs (Kolgoromovn"40 n"40 Smirnov test) Hard coral cover % (s.d) 23.2 (22.2) 26.5 (19.5) n.s. Macro-algae cover % (s.d) 37.2 (22.7) 20.8 (28.5) (0.001 Soft coral cover % (s.d) 3.4 (6.8) 12.0 (11.6) (0.001 Colonies. 100 m (s.d) 88.4 (71.8) (169.2) (0.001 Number of taxa per site (s.d) 25.5 (8.3) 36.1 (10.2) (0.001 Fig. 5a e Mean number of coral colonies per 100 m in random samples of ten sites each in regions 1 (Whitsunday Islands) and 3 (Northumberland Islands). Error bars are 1 standard deviation. a Total number of scleractinian coral colonies per 100 m ; b number of soft coral colonies per 100 m ; c number of fast-growing corals per 100 m, which include Acropora spp., Montipora spp., Pocilloporidae, Millepora tenella, and ¹urbinaria spp; d number of slowgrowing corals per 100 m, which comprise massive Faviidae, Poritidae, Agariciidae, Galaxea spp., Mussidae, plus Pectinia spp., Siderastreidae and Caryophylliidae; e number of arborescent colonies per 100 m, which include, Acropora spp., Porites cylindrica, Pocilloporidae, Millepora tenella Faviidae, Poritidae, Agariciidae, Mussidae, Siderastreidae, Caryophylliidae plus Pectinia spp. and Galaxea spp. Collectively, all sizes of these corals (particularly 1 10 cm and cm) were much more abundant in region 1 than region 3 (Fig. 5d).

8 110 For arborescent corals, (including staghorn Acropora spp., Porites cylindrica, Pocillopora damicornis, Seriatopora hystrix, Stylophora pistillata, Palauastrea ramosa, Millepora tenella), all size classes, especially colonies between cm (Fig. 5e), were more abundant in region 1 than in region 3. Coral communities The differences and similarities among the regions were also reflected in the ordination of the sites (Fig. 6a). The ordination (which accounts for 79% of the variation in taxonomic composition of the sites) shows region 1 sites covering a large central triangular area; region 2 sites overlapping with this area almost completely; and region 4 sites confined entirely within the area. Region 3, by contrast, has little overlap, by virtue of the relative paucity of Acropora and abundance of Montipora, and Penrith Island stands apart because it contained mainly reef flat sites, which were faunistically distinct from the other, deeper sites. The composition and mean density of dominant corals in eight arbitrarily defined groups (Fig. 6c) are presented in Table 3. This shows an increasing diversity of hard corals from group A to group C; i.e. assemblage A is essentially a sub-set of B, which in turn is a subset of C. Assemblages D through G include all or most of the species of A to C, plus various others, either with abundant soft corals (D, F, G) or without (E). Given this nested faunistic relationship between assemblages, their geographic distributions can be plotted as contours (Fig. 7). The assemblages are arranged concentrically around a focal point centred on the poorly developed windward reefs close to Broad Sound. Radiating from this point, the regional distribution reflects an increase in richness of hard corals. Soft corals (notably the genera Briareum, obophytum, and Capnella) were only occasionally abundant in sites out to and including contour C. Outside this contour, by contrast, sites of type D, F and G were all rich in both hard and soft corals, with type G sites in particular having very high soft coral densities (Table 3). Environmental correlates The partial and complete CCAs provide some insights into possible environmental determinants of community structure within and between regions, although some variables may be interrelated. The partial CCAs indicated there were significant correlations (P)0.05) between a site s taxonomic composition and three site descriptors: &&&&&&&&&&&&&&&&&&&&&&&&" Fig. 6a c Ordination of sites derived by correspondence analysis, showing: a each site, and the positions of eight arbritary site groups (circles); b the position of island groups in the ordination; and c notation (A H) and grouping (dark and light shading) of arbitrary site groups discussed in text and defined in Table 3. The dark shading includes a series with increasing taxonomic diversity (B(C(E) while the light shading includes groups with abundant soft corals

9 111 Table 3 Taxonomic composition and mean density (colonies. 100 m ) of corals in site groups A to H, defined in Fig. 6. A B C D E F G H HARD CORALS n"8 n"11 n"23 n"24 n"13 n"6 n"4 n"5 Montipora encrusting ¹urbinaria spp Porites encrusting Montipora foliose Goniopora spp Porites massive Favites spp Goniastrea spp Acropora caespitose Pavona venosa 3.3 Favia spp Pachyseris speciosa Cyphastrea spp Pocillopora damicornis Acropora tabulate Acropora arborescent Seriatopora hystrix Stylophora pistillata obophyllia spp Millepora tenella Acropora palifera Platygyra spp Galaxea spp Fungia spp Pectinia spp eptastrea spp Porites cylindrica Montipora branched Merulina ampliata Astreopora spp. 1 Pobabacia crustacea 3.8 Echinopora spp. 3.1 eptoria phrygia 2.9 Pachyseris rugosa 1.1 Diploastrea heliopora 1 Symphyllia spp. 1.3 SOFT CORALS Capnella spp obophytum spp Briareum spp Sinularia spp Alcyonium spp Sarcophyton spp Cladiella spp Nephthea spp Xenia spp depth, distance to the mainland, and exposure (Table 4). These correlations were only significant when taxa were defined to the level of genus or better. Pooling genera and species into their taxonomic families resulted in the loss of all significant correlations. However subdividing them into their size classes resulted in significant correlations with two additional site descriptors: island location (sequence number from north to south, Fig. 2) and mean annual tidal range. Surprisingly, distance from river and shelf depth were poorly correlated with taxonomic composition throughout all analyses. The full CCAs (Tables 5 and 6) showed that inclusion of size data greatly increased the amount of explained variance. Based on taxonomic data alone (Table 5), ordinations of sites explained a maximum of 40% of the variance. Site ordinations based on scleractinian (hard) corals (29% explained variance) were negatively related to depth and positively related to distance to the mainland while those based on alcyonarian (soft) corals (44%) were positively related to exposure and distance to the mainland. However the use of size classes in addition to taxonomy (Table 6) explained up to 63% of the variance. For scleractinian corals (48%), there were two very strong correlations: a positive correlation with distance to the mainland and a strong negative correlation with mean annual tidal range.

10 112 Fig. 7 Schematic regional and within-island distribution of coral communities on reefs fringing continental islands in the southern Great Barrier Reef. Contours enclose areas including indicated communities and those higher in alphabetical order. i.e. the C line contains A, B or C singly or in combination; the B line A or B singly or in combination, and the A line, A only Table 4 Results of Monte Carlo tests on eigenvalues derived from a series (n"35) of partial canonical correspondence analyses on coral composition. Table shows significance of correlation between seven site descriptors (see Methods) and coral composition identified in terms of families, genera/species and/or size classes. S"Scleractinia; A"Alcyonaria. Bold indicates where first eigenvalue was significant at P)0.05. Discussion This study and a companion study by Kleypas (1996) provide evidence of a link between coral community structure and the degree of reef development. The sparse coral communities near Broad Sound in region 3 were predominantly comprised of encrusting and foliaceous growth forms. They lacked essential framework elements, namely, an abundance of large massive and branching colonies. Colonies of Acropora spp., the major rubble producer elsewhere in the GBR, were present in region 3, but, unlike the Keppel Islands (region 4), they did not occur as the large monospecific stands necessary to produce significant sedimentary accumulations. Moreover, region 3 s massive Porites spp. rarely grew into the large hemispherical heads which are important reef builders elsewhere (Done and Potts 1992). Kleypas (1996) interpreted the region s variation in reef development in terms of turn-ons and turn-offs. Clues to the nature of the turn-on/turn-off mechanisms may be provided by interpretation of patterns in community structure in the present study. To the north of Broad Sound (regions 1 and 2), reef growth is turned on as a result of a combination of high settlement densities, and long individual life expectancies which lead to large colony sizes, especially in massive and branching forms. Here, it appears that individual colonies persist Depth Location Tide Mainland River Shelf Exposure Families (S#A) Families (S) Size Families (A) Genera/species (S#A) Genera/species size (S#A) Table 5 Explained variance and intraset correlation coefficients from full canonical correspondence analysis between sites defined by the attributes genera and/or species, and the significant site descriptors: depth, distance to mainland and exposure. Strong correlations (bold) indicated by large departure from 0.0. S"Scleractinia; A"Alcyonaria Attributes Explained variance Correlation coefficient % Depth Mainland Exposure Axis Axis Total Axis Axis Axis Axis Axis Axis Species (S)# Genera (A) !0.76! !0.58 Species (S) ! !0.32!0.18 Genera (A) !0.48! !0.43 Table 6 Explained variance and intraset correlation coefficients from full canonical correspondence analysis between sites defined by the attributes genera and/or species in combination with size classes, and the significant site descriptors depth, distance to mainland, exposure, location and tidal range. Strong correlations (bold) indicated by large departure from 0.0. S"Scleractinia; A"Alcyonaria Attributes Explained Variance (%) Correlation coefficient Depth Mainland Exposure Location Tide Axis 1 Axis 2 Total Axis 1 Axis 2 Axis 1 Axis 2 Axis 1 Axis 2 Axis 1 Axis 2 Axis 1 Axis 2 Species/Genera !0.04! ! (S#A) Species/Genera (S) !0.58! !0.32! !0.01!

11 113 longer and accrete more often into the existing framework. To the south of Broad Sound (region 4), reef growth is also turned on, in this case by a good supply of staghorn rubble from extensive staghorn Acropora thickets. Although the diversity of species and growth form is lower than region 1, the Acropora colonies appear to provide framework and rubble at a rate which would, if sustained through the Holocene, lead to substantial net accretion in spite of periodic natural perturbations (Van Woesik 1994; Van Woesik et al. 1995). In contrast, the sparsely covered and poorly developed reefs near Broad Sound appear to be turned off. If we assume that the present sparse assemblage of predominantly small encrusting, and fast growing corals typifies what has been present in Broad Sound throughout the Holocene period, it would be no surprise if they were unable to build substantial reefs. High population turnover, high rates of skeletal decay, and a narrow euphotic zone may have combined to limit the accumulation of reef framework and detritus necessary for reef accretion. Although fast colony growth may offset negative effects of a sparse and ephemeral coral community in terms of production of reef framework and rubble, short life expectancies and low recruitment densities, in combination, are not conducive to the accumulation of a carbonate matrix. Upon death, the small, lightly calcified and poorly cemented skeletons are probably more prone to disintegration by bio-eroders, and to breakage. High sediment loadings may account for the failure of coral communities to establish well-developed reefs close to Broad Sound. Kleypas (1996) showed a strong correlation between suspended sediment loadings and tidal range. On a day with a tidal range of 7.4 m and a shelf position close to Broad Sound, tidal currents kept 89 mg.l of fine ((63 μm) sediments in suspension for most of the tidal cycle. High sediment loadings in the water column influence species presence or absence, growth form, growth rates, and survival of established corals (Cortes and Risk 1985; Rogers 1990; Stafford-Smith 1993). They are probably a major cause for the exclusion of some species (reflected in Broad Sound area s low taxonomic diversity). Sediments coating hard substrates affect the composition and density of coral populations by interfering with the settlement of coral larvae (e.g. Hodgson 1990; Sammarco 1991) and reducing early post-settlement survival (Sammarco 1991). Ecological processes and reef growth Our data suggest some underlying dynamics of the ecological processes identified in the Chappell et al. (1983) models for fringing reef development. Net reef growth is the sum of frame work accretion, sedimentological accretion and destruction (Davies 1983). These factors may be described in terms of the demography of calcifying organisms: their densities and frequency of settlement; their rates of growth; their mean longevities and maximum sizes; their fates following death. The increasing mass and decreasing surface area to volume ratio which accompanies aging of reef building corals are both conducive to retention of large reef building blocks on site (Done and Potts 1992; Massel and Done 1993), and the progradation of the reef across the sea floor (Chappell et al. 1983). By contrast, short-lived colonies have a larger surface-area to volume ratio at time of death, and are thus more prone to be disintegrated and dispersed by bioeroders (Hutchings 1986) and by breakage, waves and currents (Denny et al. 1985; Massel and Done 1993). Reefs thus become well developed (Fig. 1a) as a consequence of high settlement densities and great longevity maximising retention of large framework elements on site (Chappell et al. 1983). They fail to develop (e.g. on the rocky headlands) or to progress beyond the incipient stage, if settlement densities and/or longevities are too low to counteract the bioerosional and physical losses. Implications for managers The present study has implications for current concerns about coral reef degradation (Grigg and Dollar 1990; Hughes 1994). The characteristics of the benthic communities associated with the incipient reefs of Broad Sound may be powerful indicators of anthropogenic stress, i.e. if there is a mismatch between the evidence of substantial past reef building capacity (a broad and/or thick reef) and non-existent or limited present reef-building capacity. This mismatch could signify anything from a long-period, natural cycle to an unprecedented deterioration in ecosystem function. The latter may be the case where periodic or ongoing human influence favours non-reef building biota, more ephemeral reef-builders, lower life expectancy in previously long-lived reef-builders and/or shorter periods of uninterrupted succession along a reef building trajectory. Take, for example, a reef flat which is studded by fossil micro-atolls from the early or late Holocene (e.g. Chappell et al. 1983). If they are of species which are not currently as abundant or large on the living reef margin, this may be indicative of change which is significant in terms of a reef s long term ability to sustain its structure (Done 1995). There should be particular concern if a coral reef slope is colonised predominantly by non-reef building organisms, substantially to the exclusion of reef building organisms. There might be equal concern if the area is currently dominated by ephemeral corals where the dead framework on the slope and in the reef flat is of more long-lived forms, such as centuries-old massive corals (Endean et al. 1989; Done and Potts 1992). A natural cycles explanation may be indicated if analysis could show the current change is consistent with the type, extent, duration and return period of similar changes in the geological past (e.g. Dollar and Tribble 1993). However the simple existence of a precedent within the geological record is not of itself sufficient evidence to establish a natural cycles explanation (Keesing et al. 1992; Walbran et al. 1989). Ideally, the interpretation for any specific location should be based on an appreciation of both its geological history, its ecology, (especially those aspects concerned with the resilience, longevity and interactions within and among reef-builders, non-reef builders, and bio-eroders), and its environment.

12 114 Successional communities, following a natural disturbance, could be confused with reefs which have been degraded as a result of human insults to the environment. While we are not suggesting the Broad Sound coral communities and incipient coral reefs are reflecting anthropogenic impact, some of their characteristics may guide us in identifying reefs that have become anthropogenically stressed through turbidity and/or sedimentation by showing (1) a narrowing of the coral zone, (2) a change in coral morphologies to encrusting and laminar forms, (3) a high population turnover rate, (4) low diversity within a diverse region, and (5) no indication of any successional change toward a framework community. Acknowledgments. This study was part of PhD research undertaken by RVW at James Cook University of North Queensland, where Professor David Hopley gave encouragement and support. We thank James Cook University, the Marine Science and Technology Council and the Australian Research Council for funding the major part of this study, and the Great Barrier Reef Marine Park Authority, and the Department of Marine Sciences, University of the Ryukyus, Japan for augmentative support. The Australian Institute of Marine Science and the CRC Reef Research Centre also provided invaluable time and resources for the study. Many thanks to Tim Ward, Lyn DeVantier, Joanie Kleypas, Laurence McCook for comments on drafts and for reviewers comments on the manuscript, and Sandra van Woesik for editorial assistance. References Bayer FM, Grasshoff M, Verseveldt J (1983) Illustrated trilingual glossary of morphological and anatomical terms applied to Octocorallia. EJ Brill, Leiden, Netherlands Chappell J, Chivas A, Wallensky E, Polach HA, Aharon P (1983) Holocene palaeo-environmental changes, central to north Great Barrier Reef inner zone. BMR J Aus Geol Geophys 8 : Cortes JN, Risk MJ (1985) A reef under siltation stress: Cahuita, Costa Rica. Bull Mar Sci 36 : Davies PJ (1983) Reef Growth. In: Barnes DJ (ed) Perspectives on Coral Reefs. Australian Institute of Marine Science, pp Denny MW, Daniel TL, Koehl MAR (1985) Mechanical limits to size in wave swept organisms. Ecol Monogr 55 : Dollar SJ, Tribble GW (1993) Recurrent storm disturbance and recovery: a long-term study of coral communities in Hawaii. Coral Reefs 12 : Done TJ (1982) Patterns in the distribution of coral across the central Great Barrier Reef. Coral Reefs 1 : Done TJ (1995) Ecological values for coral reefs and their implications for managers and researchers. Coral Reefs 14 : Done TJ, Potts DC (1992) Influences of habitat and natural disturbances on contributions of massive Porites corals to reef communities. Mar Biol 114 : Endean R, Cameron AM, DeVantier LM (1989) Acanthaster planci predation on massive corals: the myth of rapid recovery of devastated reefs. Proc 6th Int Coral Reef Symp 2 : Gauch HG (1982) Multivariate analysis in community ecology. Cambridge University Press, Cambridge Grigg RW, Dollar SJ (1990) Natural and anthropogenic disturbance on coral reefs. In: Dubinsky Z (ed) Ecosystems of the world. vol 25, Coral Reefs. Elsevier, Amsterdam pp Hodgson G (1990) Sediment and the settlement of larvae of the reef coral Pocillopora damicornis. Coral Reefs 9 : Hope ACA (1968) A simplified Monte Carlo significance test procedure. J R Stat Soc Ser B 30 : Hopley D (1982) The geomorphology of the Great Barrier Reef: Quaternary development of coral reefs. John Wiley-Interscience, New York, pp 453 Hopley D, Slocombe AM, Muir F, Grant C (1983) Nearshore fringing reefs in North Queensland. Coral Reefs 1 : Hopley D, Parnell KE, Isdale PJ (1989) The Great Barrier Reef Marine Park: dimensions and regional patterns. Aust Geogr Studies 27 : Hughes TP (1989) Community structure and diversity of coral reefs: the role of history. Ecology 70 : Hughes TP (1994) Catastrophe, phase shifts and large-scale degradation of a Caribbean coral reef. Science 226 : Hutchings PA (1986) Biological destruction of coral reefs: a review. Coral Reefs 4 : Jackson JBC, Hughes TP (1985) Adaptive strategies of coral-reef invertebrates. Am Sci 73 : Keesing JK, Bradbury RH, De Vantier LM, Riddle MJ, De ath G (1992) Geological evidence for recurring outbreaks of crownof-thorns starfish: a reassessment from an ecological perpective. Coral Reefs 11 : Kleypas JA (1991) Geological development of fringing reefs in the southern Great Barrier Reef. PhD Thesis, James Cook University of North Queensland, Townsville, Australia, pp 245 Kleypas JA (1996) Coral reef development under naturally turbid conditions: fringing reefs near Broad Sound, Australia. Coral Reefs 15(3) : Levin SA (1989) Challenges in the development of a theory of community and ecosystem structure and function. In Roughgarden J, May RM, Levin SA (eds), Perspectives in ecological theory. Princeton University Press, New Jersey, USA. pp Massel SR, Done TJ (1993) Effects of cyclone waves on massive coral assemblages on the Great Barrier Reef: meteorology, hydrodynamics and demography. Coral Reefs 12 : Minchin PN (1986) An ecological database ECOPAK, Technical memorandum 86/6, CSIRO Institute of Biological Resources, Division of Water and Land Resources, Canberra, Australia Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235 : Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62 : Sammarco PW (1991) Geographically specific recruitment and postsettlement mortality as influences on coral: the cross-continental shelf transplant experiment. Limnol Oceanog 36(3) : Shapiro SS, Francia RS (1972) An approximate analysis of variance test for normality. J Am Stats Assoc 67 : Sheppard CRC (1982) Coral populations on reef slopes and their major controls. Mar Ecol Prog Series 7 : Snedecor GW, Cochran WG (1980) Statistical methods. 7th edn. The Iowa State University Press, Ames, Iowa Stafford-Smith MG (1993) Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Mar Biol 115 : Ter Braak CJF (1985) Correspondence analysis of incidence and abundance data: properties in terms of a uni-modal response model. Biometrics 41 : Ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multi-variate direct gradient analysis. Ecology 67(5) : Ter Braak CJF (1987a) CANOCO a FORTRAN program for canonical community ordination by [partial] [detrended] [canonical] correspondence analysis, principal components analysis and redundancy analysis (version 2.1), TNO Institute of Applied Computer Science, Wageningen, pp 95 Ter Braak CJF (1987b) Partial canonical correspondence analysis. Vegetatio 69 : Van Woesik R (1992) Ecology of coral communities on continental islands in the southern section of the Great Barrier Reef, Australia. PhD Thesis, James Cook University of North Queensland, Townsville, Australia, pp 227 Van Woesik R (1994) Contemporary disturbances to coral communities of the Great Barrier Reef. J Coast Res (Special Issue) 12 : Van Woesik R, De Vantier LM, Glazebrook JS (1995) Effects of Cyclone Joy on nearshore coral communities of the Great Barrier Reef. Mar Ecol Prog Ser 128 :

13 115 Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus and Robertson, Australia, pp 644 Veron JEN, Pichon M (1976) Scleractinia of eastern Australia. Part 1. Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae Australian National University Press, Canberra. Australian Institute of Marine Science Monograph Series 1, pp 1 86 Veron JEN, Pichon M (1980) Scleractinia of eastern Australia. Part 3. Families Agariciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophylliidae. Australian National University Press, Canberra. Australian Institute of Marine Science Monograph Series 4, pp Veron JEN, Pichon M (1982) Scleractinia of eastern Australia. Part 4. Family Poritidae. Australian National University Press, Canberra. Australian Institute of Marine Science Monograph Series 5, pp Veron JEN, Wallace CC (1984) Scleractinia of eastern Australia. Part 5 Family Acroporidae. Aust Nat Uni Press, Canberra, Aust Inst Mar Sci Mono Ser 6, pp Walbran PD, Henderson RA, Jull AJT, Head MJ (1989) Evidence from sediments of long-term Acanthaster planci predation on corals of the Great Barrier Reef. Science 245 : Whittaker RH (1975) Communities and ecosystems. 2nd edn, Mac- Millan Press, New York, USA Zar JH (1984) Biostatistical analysis. 2nd edn Prentice-Hall International, pp 718

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