Carden C. Wallace

One-third of reef-building corals face elevated extinction risk from climate change and local impacts

The conservation status of 845 zooxanthellate reef-building coral species was assessed by using International Union for Conservation of Nature Red List Criteria. Of the 704 species that could be assigned conservation status, 32.8% are in categories with elevated risk of extinction. Declines in abundance are associated with bleaching and diseases driven by elevated sea surface temperatures, with extinction risk further exacerbated by local-scale anthropogenic disturbances. The proportion of corals threatened with extinction has increased dramatically in recent decades and exceeds that of most terrestrial groups. The Caribbean has the largest proportion of corals in high extinction risk categories, whereas the Coral Triangle (western Pacific) has the highest proportion of species in all categories of elevated extinction risk. Our results emphasize the widespread plight of coral reefs and the urgent need to enact conservation measures.

A 30‐YEAR STUDY OF CORAL ABUNDANCE, RECRUITMENT, AND DISTURBANCE AT SEVERAL SCALES IN SPACE AND TIME

Observations over a 30-yr period revealed a considerable degree of natural variation in the abundance of corals on Heron Island, Great Barrier Reef, Queensland, Australia. Cover ranged from 80%, with a similar large range in colony density, at several temporal and spatial scales. Much of this variation was due to the type, intensity, and spatial scale of disturbances that occurred. Coral assemblages usually recovered from acute disturbances, both on Heron Island and on other Indo-Pacific reefs. In contrast, corals did not recover from chronic disturbances of either natural or human origins, or from gradual declines. Recovery was slower after acute disturbances that altered the physical environment than after disturbances that simply killed or damaged corals. The space and time scales of declines and recoveries in abundance were much smaller on the wave-exposed side of the reef than on the side protected from storms. Recruitment rates were reduced by preemption of space by corals or macroalgae, and by storms that altered the substratum. Thus, the dynamics of abundance in this coral community can be largely understood through the variation in types and scales of disturbances that occurred, and the processes that took place where disturbances were rare.

Mass Spawning in Tropical Reef Corals

Synchronous multispecific spawning by a total of 32 coral species occurred a few nights after late spring full moons in 1981 and 1982 at three locations on the Great Barrier Reef, Australia. The data invalidate the generalization that most corals have internally fertilized, brooded planula larvae. In every species observed, gametes were released; external fertilization and development then followed. The developmental rates of externally fertilized eggs and longevities of planulae indicate that planulae may be dispersed between reefs.

Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef

Following observations of mass spawning of hermatypic corals on the Great Barrier Reef in 1981 and 1982, spawning dates were successfully predicted and documented at five reefs on the Central and Northern Great Barrier Reef in 1983. During the predicted times, 105 species from 36 genera and 11 families were observed to spawn. Of these, 15 species were shown to have an annual gametogenic cycle. All but two of the species observed during mass spawnings shed gametes which underwent external fertilization and development. Synchronous spawning was observed both within and between the five reefs studied, which were separated by as much as 5° of latitude (500 km) or almost a quarter of the length of the Great Barrier Reef. The mass spawning of corals took place on only a few nights of the year, between the full and lastquarter moon in late spring. Maturation of gametes coincided with rapidly rising spring sea temperatures. Lunar and diel cycles may provide cues for the synchronization of gamete release in these species. The hour and night on which the greatest number of species and individuals spawned coincided with low-amplitude tides. Multispecific synchronous spawning, or “mass spawning”, of scleractinian and some alcyonacean corals represents a phenomenon which is, so far, unique in both marine and terrestrial communities.

Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora

Multispecies assemblages of the coral genus Acropora occur commonly throughout the Indo-Pacific Ocean. Nine species from such an assemblage comprising 41 species of Acropora, at Big Broadhurst Reef on the Great Barrier Reef, were studied during 1981–1983. Similarities and differences in reproductive modes and timing, oocyte dimensions and fecundity, recruitment by larvae and by fragments, and mortality were recorded. All species had an annual gametogenic cycle, were simultaneous hermaphrodites, and had the same arrangement of gonads in polyps. In six species, most colonies released gametes on the same night of the year, in early summer, during a mass spawning event involving many coral genera. A seventh species had colonies spawning at this as well as other times of the year. Another species spawned in late summer, and gametes were not observed to mature in the last species. Eggs were very large (601 to 728 μm geometric mean diameter) and fecundity of polyps low, compared with other corals; no reduction in oocyte numbers occurred during oogenesis. Reef-flat species had slightly bigger and fewer eggs than reef-slope species. All species recruited by larvae, but four also multiplied by fragmentation, either year-round or during occasional rough weather. Yearround fragmenters had few larval recruits; non-fragmenters had many, and a rough-weather fragmenter had an intermediate number of larval recruits. It was concluded that larval recruitment largely determined species composition, and that reduced larval recruitment was responsible for sparse distribution of fragmenting species. Subsequent mortality in some species and increase by fragmentation in others probably determined relative abundances.

Mitochondrial and Nuclear Genes Suggest that Stony Corals Are Monophyletic but Most Families of Stony Corals Are Not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria)

Modern hard corals (Class Hexacorallia; Order Scleractinia) are widely studied because of their fundamental role in reef building and their superb fossil record extending back to the Triassic. Nevertheless, interpretations of their evolutionary relationships have been in flux for over a decade. Recent analyses undermine the legitimacy of traditional suborders, families and genera, and suggest that a non-skeletal sister clade (Order Corallimorpharia) might be imbedded within the stony corals. However, these studies either sampled a relatively limited array of taxa or assembled trees from heterogeneous data sets. Here we provide a more comprehensive analysis of Scleractinia (127 species, 75 genera, 17 families) and various outgroups, based on two mitochondrial genes (cytochrome oxidase I, cytochrome b), with analyses of nuclear genes (ß-tubulin, ribosomal DNA) of a subset of taxa to test unexpected relationships. Eleven of 16 families were found to be polyphyletic. Strikingly, over one third of all families as conventionally defined contain representatives from the highly divergent “robust” and “complex” clades. However, the recent suggestion that corallimorpharians are true corals that have lost their skeletons was not upheld. Relationships were supported not only by mitochondrial and nuclear genes, but also often by morphological characters which had been ignored or never noted previously. The concordance of molecular characters and more carefully examined morphological characters suggests a future of greater taxonomic stability, as well as the potential to trace the evolutionary history of this ecologically important group using fossils.

Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals

Abstract. Synchronous spawning of many coral species that co-occur on Indo-Pacific reefs raises the possibility that hybridization plays a role in their evolution. Here we use experimental crosses to examine mating compatibilities and breeding barriers in a group of sessile animals whose mating systems are primarily governed by interactions among free-spawned gametes. We found hybridization occurs readily in more than one-third of 42 species pairs from the common genera Acropora, Montipora and Platygyra. Mean fertilization success ranged from 1% to 50% in species crosses, but standard deviations about these means were large and in some cases, fertilization success in individual colony matings was greater than 95%. Cases of high fertility in individual, interspecific matings were found in all three genera. Hybridization occurred most readily between species that were morphologically similar, identifying areas where current taxonomic judgements may require further testing. However, cases of significant hybridization also occurred between species that are morphologically distinct. Evidence of in vitro hybridization combined with the lack of either temporal or spatial barriers to interbreeding among field populations of these species, indicates that natural hybridization may occur commonly between congeneric corals that are currently recognized as distinct species. We also detected mating incompatibilities between some colonies within some species. In some cases, incompatible colonies corresponded to distinct morphotypes, but not in others. Thus some breeding groups in scleractinian corals are potentially larger, but others are smaller, than would be predicted using morphological criteria. Gamete incompatibilities within a morphospecies that readily hybridizes with other species may be the result of a mating system that is governed by gamete-level interactions. Imprecision in the alignment of morphological and breeding boundaries suggests a single species concept may not apply to scleractinian corals and challenges the tacit assumption that currently defined coral species encompass biological, evolutionary and phylogenetic species. Hybridization between supposedly isolated species introduces a reticulate nature to the evolution of corals and has profound implications for present understanding of the population genetics, phylogenetics, and evolutionary biology of scleractinian corals.

A LONG‐TERM STUDY OF COMPETITION AND DIVERSITY OF CORALS

Variations in interspecific competition, abundance, and alpha and beta diversities of corals were studied from 1962 to 2000 at different localities on the reef at Heron Island, Great Barrier Reef, Australia. Reductions in abundance and diversity were caused by direct damage by storms and elimination in competition. Recovery after such reductions was influenced by differences in the size of the species pools of recruits, and in contrasting competitive processes in different environments. In some places, the species pool of coral larval recruits is very low, so species richness (S) and diversity (D) never rise very high. At other sites, this species pool of recruits is larger, and S and D soon rise to high levels. After five different hurricanes destroyed corals at some sites during the 38- year period, recovery times of S and D ranged from 3 to 25 years. One reason for the variety of recovery times is that the physical environment was sometimes so drastically changed during the hurricane that a long period was required to return it to a habitat suitable for corals. Once S and D have peaked during recolonization, they may either remain at a high level, or decline. In shallow water, with no deleterious changes in environmental conditions, S and D may not decline over time, because superior competitors cannot overtop inferior competitors without exposing themselves to deleterious aerial exposure at low tide. At other times and places, S and D did decline over time. One cause of this was a gradual deterioration of the physical environment, as corals grew upward into the intertidal region and died of exposure. S and D also fell because the wave action in hurricanes either killed colonies in whole or part, or changed the drainage patterns over the reef crest, leaving corals high and dry at low tide. At deeper sites, declines in S and D were sometimes caused by heavy wave action, or by interspecific competition, as some corals overgrew or overtopped their neighbors and eliminated them.

Analysis of the mitochondrial 12S rRNA gene supports a two-clade hypothesis of the evolutionary history of scleractinian corals

Scleractinian corals have long been assumed to be a monophyletic group characterized by the possession of an aragonite skeleton. Analyses of skeletal morphology and molecular data have shown conflicting patterns of suborder and family relationships of scleractinian corals, because molecular data suggest that the scleractinian skeleton could have evolved as many as four times. Here we describe patterns of molecular evolution in a segment of the mitochondrial (mt) 12S ribosomal RNA gene from 28 species of scleractinian corals and use this gene to infer the evolutionary history of scleractinians. We show that the sequences obtained fall into two distinct clades, defined by PCR product length. Base composition among taxa did not differ significantly when the two clades were considered separately or as a single group. Overall, transition substitutions accumulated more quickly relative to transversion substitutions within both clades. Spatial patterns of substitutions along the 12S rRNA gene and likelihood ratio tests of divergence rates both indicate that the 12S rRNA gene of each clade evolved under different constraints. Phylogenetic analyses using mt 12S rRNA gene data do not support the current view of scleractinian phylogeny based upon skeletal morphology and fossil records. Rather, the two-clade hypothesis derived from the mt 16S ribosomal gene is supported.

Recognition of separate genera within Acropora based on new morphological, reproductive and genetic evidence from Acropora togianensis, and elevation of the subgenus Isopora Studer, 1878 to genus (Scleractinia: Astrocoeniidae; Acroporidae)

Many attempts have been made to recognise divisions within Acropora, the most diverse reef building coral genus on modern reefs, but only subgenera Acropora and Isopora are currently recognised. In this paper, morphological and genetic analyses, and study of reproductive mode and anatomy, demonstrate that an endemic Indonesian species A. (Acropora) togianensis, Wallace, 1997, belongs to Isopora. Despite the presence of a clear central axial corallite (indicating sub-genus Acropora), this species has supplementary axial corallites, broods planula larvae rather than broadcast-spawning for external fertilisation and develops stalked ova: all characters in common with the type species of subgenus Isopora A. (Isopora) palifera and the other species for which such data are available, A. (I.) cuneata and A. (I.) brueggemanni. Phylogenies are based on the protein-coding genes, mitochondrial cytochrome b (cytb) and nuclear histone 2a and 2b (h2ab) also group A. togianensis with these Isoporans. High bootstrapping and Bayesian support in the major lineages of the family Acroporidae demonstrate significant differences between Isopora (including A. togianensis) and Acropora. As the type species of both subgenera, A. (Acropora) muricata (Linneaus 1758) and A. (Isopora) palifera (Lamarck, 1816) are used in these analyses, elevation of Isopora Studer, 1878 to genus is formally proposed.