Paul R. Muir

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.

Limited scope for latitudinal extension of reef corals

Not as deep As our climate warms, many species ranges are predicted to shift toward the warmer poles. Focusing solely on temperatures, however, ignores many factors that change across latitudes, such as the intensity of solar radiation. Muir et al. looked at global distributions of two groups of reef-building corals (see the Perspective by Kleypas). Most reef-building corals occur deep enough to be protected from surge. However, corals require sunlight to sustain their symbiotic photosynthetic algae. Because solar radiation is more limited farther away from the equator, future populations might be limited to more turbulent shallow waters. Science, this issue p. 1135; see also p. 1086 Solar irradiation during winter constrains how far coral reefs can spread sideways despite ocean warming. [Also see Perspective by Kleypas] An analysis of present-day global depth distributions of reef-building corals and underlying environmental drivers contradicts a commonly held belief that ocean warming will promote tropical coral expansion into temperate latitudes. Using a global data set of a major group of reef corals, we found that corals were confined to shallower depths at higher latitudes (up to 0.6 meters of predicted shallowing per additional degree of latitude). Latitudinal attenuation of the most important driver of this phenomenon—the dose of photosynthetically available radiation over winter—would severely constrain latitudinal coral range extension in response to ocean warming. Latitudinal gradients in species richness for the group also suggest that higher winter irradiance at depth in low latitudes allowed a deep-water fauna that was not viable at higher latitudes.

Mesophotic coral ecosystems on the walls of Coral Sea atolls

A research cruise was undertaken in October 2010 to explore potential mesophotic coral communities (30–150 m) in the recently established Coral Sea Conservation Zone (CSCZ). The CSCZ covers an area of almost one million square kilometres east of the Great Barrier Reef (Australia), with its reefs and atolls located hundreds of kilometres from the nearest landmass and surrounded by deep oceanic water. Three of the atolls in the CSCZ (West Holmes Reef [16.243°S, 147.874°E], East Holmes Reef [16.459°S, 148.024°E] and Flora Reef [16.755°S, 147.738°E]) were assessed using SCUBA and a Seabotix ROV. Shallow reef areas (<30 m) consisted largely of bare substrate with predominantly juvenile corals and very low coral cover due to past cyclone damage and thermal bleaching events. In contrast, the steep walls in 40–100 m depth were covered by extensive Halimeda curtains (Fig. 1a), which harboured diverse scleractinian coral communities, including Acropora, Astreopora, Fungia, Galaxea, Goniastrea, Porites, Mycedium (Fig. 1c), Seriatopora and Turbinaria spp., with Pachyseris (Fig. 1d), Leptoseris and Montipora spp. recorded to 102 m depth. At least one of the collected specimens represents a new species record for Australia: Echino- morpha nishihirai (Fig. 1b). Diverse communities of azooxanthellate octocorals were also observed to 150 m, the maximum depth of the ROV. These observations confirm the presence of mesophotic coral ecosystems (MCEs) along the walls of Coral Sea atolls and indicate that MCEs may form extensive features in the CSCZ. The deep-water coral communities may play an important role in the recovery of shallow reef areas on these isolated atolls by functioning as refugia from the repeated disturbances that have affected these reefs.

A diverse assemblage of reef corals thriving in a dynamic intertidal reef setting (Bonaparte Archipelago, Kimberley, Australia).

The susceptibility of reef-building corals to climatic anomalies is well documented and a cause of great concern for the future of coral reefs. Reef corals are normally considered to tolerate only a narrow range of climatic conditions with only a small number of species considered heat-tolerant. Occasionally however, corals can be seen thriving in unusually harsh reef settings and these are cause for some optimism about the future of coral reefs. Here we document for the first time a diverse assemblage of 225 species of hard corals occurring in the intertidal zone of the Bonaparte Archipelago, north western Australia. We compare the environmental conditions at our study site (tidal regime, SST and level of turbidity) with those experienced at four other more typical tropical reef locations with similar levels of diversity. Physical extremes in the Bonaparte Archipelago include tidal oscillations of up to 8 m, long subaerial exposure times (>3.5 hrs), prolonged exposure to high SST and fluctuating turbidity levels. We conclude the timing of low tide in the coolest parts of the day ameliorates the severity of subaerial exposure, and the combination of strong currents and a naturally high sediment regime helps to offset light and heat stress. The low level of anthropogenic impact and proximity to the Indo-west Pacific centre of diversity are likely to further promote resistance and resilience in this community. This assemblage provides an indication of what corals may have existed in other nearshore locations in the past prior to widespread coastal development, eutrophication, coral predator and disease outbreaks and coral bleaching events. Our results call for a re-evaluation of what conditions are optimal for coral survival, and the Bonaparte intertidal community presents an ideal model system for exploring how species resilience is conferred in the absence of confounding factors such as pollution.

Diverse staghorn coral fauna on the mesophotic reefs of north-east Australia

Concern for the future of reef-building corals in conditions of rising sea temperatures combined with recent technological advances has led to a renewed interest in documenting the biodiversity of mesophotic coral ecosystems (MCEs) and their potential to provide lineage continuation for coral taxa. Here, we examine species diversity of staghorn corals (genera Acropora and Isopora) in the mesophotic zone (below 30 m depth) of the Great Barrier Reef and western Coral Sea. Using specimen-based records we found 38 staghorn species in the mesophotic zone, including three species newly recorded for Australia and five species that only occurred below 30 m. Staghorn corals became scarce at depths below 50 m but were found growing in-situ to 73 m depth. Of the 76 staghorn coral species recorded for shallow waters (depth ≤ 30 m) in north-east Australia, 21% extended to mesophotic depths with a further 22% recorded only rarely to 40 m depth. Extending into the mesophotic zone provided shallow water species no significant advantage in terms of their estimated global range-size relative to species restricted to shallow waters (means 86.2 X 106 km2 and 85.7 X 106 km2 respectively, p = 0.98). We found four staghorn coral species at mesophotic depths on the Great Barrier Reef that were previously considered rare and endangered on the basis of their limited distribution in central Indonesia and the far western Pacific. Colonies below 40 m depth showed laterally flattened branches, light and fragile skeletal structure and increased spacing between branches and corallites. The morphological changes are discussed in relation to decreased light, water movement and down-welling coarse sediments. Staghorn corals have long been regarded as typical shallow-water genera, but here we demonstrate the significant contribution of this group to the region’s mesophotic fauna and the importance of considering MCEs in reef biodiversity estimates and management.

Deepest zooxanthellate corals of the Great Barrier Reef and Coral Sea

Lower mesophotic depths on coral reefs remain poorly studied and little is known about zooxanthellate coral communities at the deepest limit of their bathymetric distributions. Maximum depths have been reported for reef systems including the Bahamas (119 m) and Hawaii (153 m) (reviewed in Kahng et al. 2010). For the world’s largest coral reef ecosystem, the Great Barrier Reef (GBR), it remained unclear to what depth zooxanthellate coral communities extend, although initial surveys indicated that this may be down to at least 100 m depth (Bridge et al. 2012). As part of the “Catlin Seaview Survey”, we surveyed lower mesophotic reefs across East Australia (2012–2013) using a Seabotix ROV (vLBV300). Although zooxanthellate scleractinian corals were often scarce below ∼80 m depth, we encountered Leptoseris communities extending to depths of 125 m (Fig. 1) on the GBR at Day Reef and Yonge Reef (respectively 14°28.46′S, 145°32.34′E and 14°36.96′S, 145°38.22′E), and in the Coral Sea at Bougainville Reef (15°30.17′S, 147°06.15′E). All observed Leptoseris spp. colonies at these depths (∼115–125 m) were small

Lower mesophotic coral communities (60-125 m depth) of the northern great barrier reef and coral sea

Mesophotic coral ecosystems in the Indo-Pacific remain relatively unexplored, particularly at lower mesophotic depths (≥60 m), despite their potentially large spatial extent. Here, we used a remotely operated vehicle to conduct a qualitative assessment of the zooxanthellate coral community at lower mesophotic depths (60–125 m) at 10 different locations in the Great Barrier Reef Marine Park and the Coral Sea Commonwealth Marine Reserve. Lower mesophotic coral communities were present at all 10 locations, with zooxanthellate scleractinian corals extending down to ~100 metres on walls and ~125 m on steep slopes. Lower mesophotic coral communities were most diverse in the 60–80 m zone, while at depths of ≥100 m the coral community consisted almost exclusively of the genus Leptoseris. Collections of coral specimens (n = 213) between 60 and 125 m depth confirmed the presence of at least 29 different species belonging to 18 genera, including several potential new species and geographic/depth range extensions. Overall, this study highlights that lower mesophotic coral ecosystems are likely to be ubiquitous features on the outer reefs of the Great Barrier Reef and atolls of the Coral Sea, and harbour a generic and species richness of corals that is much higher than thus far reported. Further research efforts are urgently required to better understand and manage these ecosystems as part of the Great Barrier Reef Marine Park and Coral Sea Commonwealth Marine Reserve.

A rare ‘deep-water’ coral assemblage in a shallow lagoon in Micronesia

Pohnpei is a continental island in central Micronesia with extensive fringing coral reefs (Turak and DeVantier 2005). During a reef coral survey in 2009, we found a shallow (10–20 m) southwest lagoon site (6.93° N, 158.11° E) with a scleractinian reef coral assemblage typical of the mesophotic zone (Kahng et al. 2010; Muir et al. 2015), dominated by deep-water Acropora species [mainly A. pichoni Wallace, 1999 and A. tenella (Brook, 1892)] and large coral plates of the genera Mycedium, Oxypora, Pachyseris and Montipora (Fig. 1). Leptoseris hawaiiensis (Vaughan, 1907) and other ‘deep-water’ species including Acropora elegans (Milne Edwards and Haime, 1860), A. walindii Wallace, 1999, A. batunai Wallace, 1997, A. turaki Wallace, 1994, A. desalwii Wa l l a c e , 1 9 9 4 , A . h a lmah e r a e Wa l l a c e a n d Wolstenholme, 1998, A. speciosa (Quelch, 1886), A. lokan i Wal lace , 1994 , A. awi Wal lace and Wolstenholme, 1998, and A. rongelapensis Richards and Wallace, 2004, were also recorded. Several of the rare Acropora species were previously documented for central Indonesia and northern PNG, some 1500 km to the southwest (Wallace et al. 2012), and therefore show considerable expansion of their recorded biogeographical ranges. Levels of light were noticeably low at the site, which we attributed to high levels of dissolved tannins giving

Response to letter regarding “Limited Scope for Latitudinal Extension of Reef Corals”

In their recent letter, Madin et al. (2016) dispute our findings in Muir et al. (2015a) that reduced levels of light during winter confine staghorn corals to shallower depths at higher latitudes and will ultimately limit their scope for latitudinal expansion as oceans warm. We based our conclusions on a rich global dataset analysed using two types of analyses: polynomial quantile regression models and species distribution models. Madin and colleagues’ reanalysis of our data focuses only on the quantile regression model, and in our view, provides no convincing quantitative evidence in support of their proposition that most species exhibit either no trend or a reverse trend to the one we described.

Correction to ‘Species identity and depth predict bleaching severity in reef-building corals: shall the deep inherit the reef’

Proc. R. Soc. B 284 , 20171551 (Published Online 11 October 2017) ([doi:10.1098/rspb.2017.1551][1]) Correction: Refers to page 3, second column: … [1]: http://dx.doi.org/10.1098/rspb.2017.1551