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Home , Catlin Seaview Survey, Coral Sea, Coral Sea Islands, Melithaea, Osprey Reef

The Great Barrier and 20 Tom C.L. Bridge, Robin J. Beaman, Pim Bongaerts, Paul R. Muir, Merrick Ekins, and Tiffany Sih

Abstract agement approaches that explicitly considered latitudinal The lies in the southwestern Pacific , bor- and cross-shelf gradients in the environment resulted in dered by , , the Solomon mesophotic reefs being well-represented in no-take areas in Islands, , , and the . The the GBR. In contrast, mesophotic reefs in the Coral Sea (GBR) constitutes the western margin currently receive little protection. of the Coral Sea and supports extensive submerged reef systems in mesophotic depths. The majority of research on Keywords the GBR has focused on Scleractinian , although Mesophotic coral · Coral · Reef other taxa (e.g., fishes) are receiving increasing attention. · · Australia To date, 192 coral (44% of the GBR total) are recorded from mesophotic depths, most of which occur shallower than 60 m. East of the Australian continental 20.1 Introduction margin, the Queensland Plateau contains many large, oce- anic reefs. Due to their isolated location, Australia’s Coral The Coral Sea lies in the southwestern , cover- Sea reefs remain poorly studied; however, preliminary ing an area of approximately 4.8 million square kilometers investigations have confirmed the presence of mesophotic between latitudes 8° and 30° S (Fig. 20.1a). The Coral Sea is coral ecosystems, and the clear, oligotrophic waters of the bordered by the Australian on the west, Papua New Coral Sea likely support extensive mesophotic reefs. Guinea and the to the north, Vanuatu and Although mesophotic reefs in the GBR and Coral Sea are New Caledonia to the east, and the Tasman Sea to the south among the best-studied globally, most research has focused (IHO 1953). The total areal extent of shallow-water coral on only a few sites, and research effort dedicated to meso- reefs in the Coral Sea is ~48,000 km2, of which about photic coral ecosystems remains negligible compared to shallow-water reefs. Despite the lack of ecological data P. Bongaerts from most mesophotic reef habitats, precautionary man- School of Biological Sciences, The University of Queensland, St Lucia, QLD, Australia California Academy of Sciences, San Francisco, CA, USA The original version of this chapter was revised: The author name P. R. Muir “Tom C.L. Bridge” initials was updated. The correction to this chapter Biodiversity and Geosciences Program, Museum of Tropical is available at https://doi.org/10.1007/978-3-319-92735-0_53 Queensland, Queensland Museum, , QLD, Australia Global Change Institute, University of Queensland, T. C.L. Bridge (*) St. Lucia, Australia Biodiversity and Geosciences Program, Museum of Tropical Queensland, Queensland Museum Network, Townsville, M. Ekins QLD, Australia Biodiversity and Geosciences Program, Museum of Tropical Queensland, Queensland Museum, Townsville, QLD, Australia Australian Research Council Centre of Excellence for Studies, , Townsville, QLD, Australia T. Sih e-mail: [email protected] Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, Australia R. J. Beaman College of Science and Engineering, James Cook University, College of Science and Engineering, James Cook University, , QLD, Australia Cairns, QLD, Australia

© Springer Nature Switzerland AG 2019 351 Y. Loya et al. (eds.), Mesophotic Coral Ecosystems, Coral Reefs of the World 12, https://doi.org/10.1007/978-3-319-92735-0_20 352 T. C.L. Bridge et al.

Fig. 20.1 Map of (a) the Coral Sea region, (b) bathymetry and major geomorphic features of the Coral Sea, (c) location of study sites referred to in this chapter 20 The Great Barrier Reef and Coral Sea 353

24,000 km2 occurs on the Australian continental shelf as 200 to 3000 m and is separated from the Great Barrier Reef the Great Barrier Reef (GBR). However, the region also by the Queensland Trough (Fig. 20.1). The Queensland includes many deeper submerged reefs and banks, and Plateau supports ~30 reefs and at depths sufficiently accounting for deeper reef habitats would substantially shallow to support coral growth. The Marion Plateau lies to increase the total estimate of reef habitat in the region. The the south of the Queensland Plateau and supports six major Coral Sea region, including the GBR, lies immediately south reef systems (Marion, Saumarez, Frederick, Kenn, Wreck, of the “” biodiversity hotspot and conse- and Reefs). The Queensland and Marion Plateaux are quently contains ~60% of all Indo-Pacific coral and ~50% of separated by the Townsville Trough. all species. The reefs of the Coral Sea are ecologically distinct from The iconic GBR, which extends for 2300 km along the the GBR, and likely act as stepping stones for dispersal northeast Australian , forms the western between the GBR and western Pacific (Bode et al. 2006). boundary of the Coral Sea. One of the best-studied coral reef Due to their remote location, reefs in the Australian Coral ecosystems on (Fisher et al. 2011), the GBR supports a Sea are poorly documented compared to those in the GBR wide variety of reef habitats from turbid, coastal fringing (Ceccarelli 2011). Nonetheless, the region’s clear, oligotro- reefs to the long, linear ribbon reefs along the edge of the phic waters provide an ideal habitat for coral growth at continental shelf. The Great Barrier Reef Marine Park mesophotic depths. Some research has occurred on the (GBRMP), established in 1975, covers an area of Coral Sea reefs closest to the Queensland coast, the best- 344,000 km2; however, the iconic, shallow-water reefs for studied of which is , which lies ~330 km north- which the GBR is known comprise only ~20,000 km2, repre- east of Cairns and is regularly visited by the dive tourism senting 7% of the total area of the Park. The GBRMP also industry. Exploratory surveys have confirmed that the Coral supports many other marine habitats, from coastal man- Sea reefs support mesophotic coral ecosystems, defined as groves and seagrass beds to extensive canyon systems and light-­dependent coral reef communities in depths of deepwater knolls occurring below the photic zone. Recent 30–150 m (Loya et al. 2016), which are dominated by research, primarily using remote mapping and imaging tech- , , and (Bongaerts et al. nologies (e.g., autonomous underwater vehicles [AUVs], 2011a). However, the ecology of most reef systems in the baited remote underwater video stations [BRUVS], and mul- Coral Sea remains poorly known, particularly at meso- tibeam ) have revealed that the GBRMP includes exten- photic depths. sive mesophotic reef habitat, both in the GBR and particularly along the shelf-edge. Although lower reef slopes of emergent reefs do support some mesophotic communities 20.1.1 Research History in the GBR, the majority of mesophotic reef habitat consists of submerged reefs, defined as isolated elevations of the sea- The vast majority of ecological research on the GBR has floor over which the depth of water is relatively shallow but been conducted using conventional SCUBA, with compara- sufficient for safe surface navigation (IHO 2008). These sub- tively little focus on mesophotic depths. A few early ecologi- merged reefs were formed during periods of lower sea level cal studies did extend to upper mesophotic depths (30–60 m; and are now found in depths ranging from 15 to 150 m. They sensu Loya et al. 2016). For example, Veron and Hudson are thought to have drowned as a result of sea-level rise dur- (1978) provided quantitative descriptions of reef zonation in ing the last deglaciation (Abbey et al. 2011). the northern GBR, which included observations of high coral East of the GBR, the Coral Sea supports numerous large, abundance and diversity to at least 45 m depth on the front of oceanic reef systems that rise out of very deep waters. The Tijou Reef. However, the majority of research on mesophotic majority of reef systems in the Coral Sea occur in Australia’s reefs was motivated by geological interest regarding the Exclusive Economic Zone (EEZ) and are administered under effects of eustatic sea-level cycles on the history and evolu- the banner of the Australian Territory. tion of the GBR. Hopley (1982) showed that submerged Some atolls in the far eastern Coral Sea are administered by reefs, interpreted as ribbon reefs which grew at lower sea New Caledonia (including the and levels, occurred over a large section of the central GBR Bellona Reef), the Solomon Islands (Indispensable Reefs), shelf-edge. Subsequent hydrographic surveys off Cairns, and (Eastern Fields). The reefs of the Townsville, and Hydrographers Passage revealed that sub- Coral Sea are located in remote areas far from land and are merged reefs in mesophotic depths are common features of generally poorly documented from an ecological perspec- the GBR shelf-edge (Harris and Davies 1989). tive. This chapter focuses primarily on the reefs and islands The first direct observations of lower mesophotic (60– within Australia’s jurisdiction. 150 m depth) reefs in the GBR occurred in 1984 and used a The coral reefs in the Australian Coral Sea Islands manned submersible to document the habitats and ecological Territory are situated atop of on the Queensland communities of the outer-shelf to >200 m depth at Myrmidon, and Marion Plateaux. The Queensland Plateau covers an area Moss, and Ribbon No. 5 Reefs (described in Hopley et al. of approximately 237,000 km2 in water depths ranging from 2007). Although the primary objectives of these dives were for 354 T. C.L. Bridge et al. geological purposes, detailed descriptions of the benthic et al. 2012; Beaman et al. 2016). Several of these were part assemblages revealed virtually 100% coral cover (predomi- of the XL (Englebert et al. 2017) and nantly Leptoseris and Pachyseris) to depths of ~100 m on the have focused on the reefs of the western Queensland Plateau: fore reef slope at Myrmidon Reef (Hopley et al. 2007). Osprey, Bougainville, Holmes, and Flinders Reefs. Regular Following these pioneering studies, mesophotic reefs in access to Osprey Reef through collaboration with the recre- the GBR received little further attention until the mid-2000s. ational diving industry has enabled longer-term collection of Some information on mesophotic habitats in GBR lagoon environmental and ecological data at that site. was obtained during a large-scale project examining biodi- versity of the “non-reef” seabed on the continental shelf (Pitcher et al. 2007), including data on the fish and benthic 20.2 Environmental Setting communities associated with “deepwater shoals” occurring in depths up to 50 m (Cappo et al. 2009). However, it was not The Coral Sea region generally experiences a wet tropical until 2007 that an expedition aboard the RV Southern climate, with high rainfall, predominant southeasterly trade Surveyor (called “SS07” hereafter) initiated a new era of winds, and frequent tropical cyclones (Wolanski 1982). The research interest in mesophotic coral ecosystems on the dominant surface oceanographic feature in the region is the GBR. The expedition aimed to investigate the geomorphol- South Equatorial (SEC), which flows westwards ogy and biodiversity of the GBR shelf-edge, focusing on across the South Pacific (Church 1987). East of the Australian four sites along 800 km of the GBR shelf-edge from latitudes continental shelf at around latitude 15° S, the SEC bifurcates 15° to 20° S (Webster et al. 2008). into the northward-flowing Coral Sea Coastal Current or Hiri Multibeam bathymetry confirmed that linear submerged Gyre and the southward-flowing reefs are ubiquitous features of the GBR shelf-edge to depths (EAC) (Wolanski et al. 1995). The vast majority of Australia’s of ~140 m and represent an extensive habitat for mesophotic Coral Sea region is composed of pelagic environments and coral ecosystems (Abbey et al. 2011). AUV surveys, supple- covers large plateaux (e.g., Queensland Plateau and Marion mented by specimens collected using a rock dredge, were Plateau), extinct volcanic seamounts (Tasmantid seamounts), conducted at Ribbon No. 5 Reef, Noggin Pass, Viper Reef, and abyssal plains (Coral Sea basin), with shallow-­water and Hydrographers Passage and provided the first opportu- coral reefs occupying only 0.3% of the total area. nity to quantify benthic communities occurring on meso- The Coral Sea region exhibits considerable spatial hetero- photic reefs in the GBR (Bridge et al. 2011a, b, 2012a). geneity in water clarity (De’ath and Fabricius 2008), ranging Since 2007, several additional research expeditions have from very turbid waters near the Australian mainland to very examined mesophotic reefs in the GBR, the most compre- clear, oceanic waters on the GBR outer-shelf and the hensive being the XL Catlin Seaview Survey. Comprising Queensland and Marion Plateaux. On the continental shelf of multiple trips from 2012 to 2014, the project focused primar- the GBR, water quality is affected by both sediment resus- ily on the northern sections of the GBR from Raine Island to pension and terrestrial inputs from rivers, both of which Myrmidon Reef and used open-circuit diving (in the upper result in a general increase in water clarity with increasing mesophotic) and ROVs (in the lower mesophotic) to charac- distance from the coast. Water clarity on the GBR continen- terize benthic communities (Muir et al. 2015; Englebert et al. tal shelf also varies with latitude due to factors such as varia- 2017). To date, mesophotic coral ecosystems have been tions in the amplitude of tidal currents, being generally more examined over a ~1200 km length of the GBR spanning 8° of turbid in the south and the far north and clearest in the central latitude from Raine Island to Hydrographers Passage, pro- GBR where tidal current amplitude is smallest. viding a good overview of the spatial extent of mesophotic reefs in the region. However, most sites have been visited on a single occasion or intermittently, therefore temporal pat- 20.3 Habitat Description terns and ecological dynamics remain largely unknown. Mesophotic coral ecosystems on the Queensland Plateau The morphology and width of the northeast Australian conti- are even less known than those of the GBR. The best-studied nental shelf varies with latitude, which in turn influences reef mesophotic reef in the Australian Coral Sea is Osprey Reef morphology along the GBR (Fig. 20.2). The continental on the Queensland Plateau, due primarily to its popularity shelf is narrower (~40–60 km wide) in the northern section with the industry. Sarano and Pichon between latitude 11–16° S, with long, linear emergent reefs (1988) based the first published observations of the meso- forming a true barrier between the GBR lagoon and the open photic zone at Osprey Reef on manned submersible observa- Coral Sea (Fig. 20.1b and 20.2a). South of latitude 16° S, the tions from an expedition led by . However, central and southern GBR continental shelf widens (~60– as in the GBR, mesophotic reefs on the Queensland Plateau 270 km wide), and emergent reefs consist largely of platform received little attention until 2009, after which several expe- reefs set back from the shelf-edge. With the exception of ditions were undertaken (Bongaerts et al. 2011a; Lindsay Myrmidon Reef (18°16’ S, 147°23′ E) on the central GBR, 20 The Great Barrier Reef and Coral Sea 355

Tydeman Reef

Australia

Yonge Reef

Great Barrier Reef

20 km Ribbon No. 5 Reef

palaeo-channel

Holmes Reefs

Myrmidon Reef

Queensland Plateau

Flinders Reefs

Australia Hydrographers Pass

Great Barrier Reef

40 km

Fig. 20.2 Bathymetry models showing changes in morphology of the GBR shelf between the northern GBR (top) and the central GBR (below). Vertical exaggeration (VE) x6. (Images: Robin J. Beaman, www.deepreef.org, can be reused under CC BY license) 356 T. C.L. Bridge et al. outer-shelf emergent reefs are set back from the shelf-edge (Fig. 20.2b). These changes in shelf morphology have a a ­substantial influence on both the extent and type of meso- photic reef habitat in the GBR. The ribbon reefs of the northern GBR are situated on the depth (m) continental shelf-edge and slope away steeply into very 0 deep waters (>1000 m) on their seaward margin (Fig. 20.3a; -40 Hopley et al. 2007). The continental slope contains exten- submerged reef -80 sive canyon systems, and in some cases canyons incise onto -120 the shelf through interreef passages between the ribbon shelf break reefs (Puga-Bernabéu et al. 2011). The first description of -160 this habitat was made using a manned submersible at -200 Ribbon No. 5 Reef in 1984 (Hopley et al. 2007). The reef 1.5 km -240 front of Ribbon No. 5 Reef consists of a vertical wall to a depth of ~30 m and a talus slope from 30 to 70 m punctu- ated by a narrow, linear submerged reef at ~45 m. A “brow” b at the shelf break at ~70 m covered with dense gorgonians separated the talus slope from a vertical wall below. Additional recent observations from a range of sites on the shelf break depth (m) northern GBR (Raine Island, Great Detached, Tydeman, -30 Yonge, and Day reefs) have indicated two predominant shoals -50 -60 habitat morphologies at mesophotic depths: a gently slop- -70 -80 ing sand and rubble slope dominated by Halimeda that -90 submerged reef -100 gradually morphs into a steep slope or vertical wall at -120 -130 70–90 m depth and limestone reef of moderate slope (45°) -140 -150 that steepens gradually into a wall at 80–100 m depth -160 (Englebert et al. 2017). -180 2.0 km There is potential for large areas of mesophotic reef habi- -200 tat in the lagoon of the northern GBR because of the numer- ous banks found there with an upper surface at ~27 m c surrounded by deeper water to ~40 m (Harris et al. 2013). lagoon Extensive Halimeda mounds, or bioherms, do occur land- ward of the ribbon reefs (McNeil et al. 2016). The biodiver- depth (m) sity associated with the Halimeda banks is poorly -20 reef flat -60 documented; however, they are known to support some -100 Scleractinia, including unique species such as tori- reef wall -200 -300 halimeda (Wallace 1994). The northern GBR also supports -400 deep channels, attributed to fluvial erosion during lower sea -500 levels and/or to scouring by strong tidal currents (Harris -600 et al. 2005). -700 The wider and deeper continental shelf of the central -800 3.5 km GBR south of latitude ~16° S exerts a strong influence on -932 reef morphology (Hopley 2006). Emergent reefs in this region are set back from the shelf-edge, and the shelf-edge Fig. 20.3 Differences in mesophotic reef habitat in the Coral Sea: (a) is occupied by a series of linear submerged reefs and ter- steeply sloping reef front at Ribbon No. 5 Reef, northern GBR; (b) gently sloping shelf slope with parallel lines of submerged reefs at races running parallel to the shelf break in depths of ~15– Hydrographers Passage, central GBR; and (c) steep walls at North 145 m (Fig. 20.3b; Abbey et al. 2011). These submerged Horn, Osprey Reef, Coral Sea. (Photo credits: Robin J. Beaman, www. reefs grew during periods of lower sea levels but now sup- deepreef.org, can be reused under CC BY license) port extensive mesophotic communities. Benthic communi- ties in upper mesophotic depths are generally dominated by phototrophic taxa including hard corals and octocorals 2012a). Generally, submerged banks on the continental (Fig. 20.4a, b), while lower mesophotic reefs are dominated shelf – and therefore potential mesophotic habitat – are most by azooxanthellate octocorals and to a lesser extent by extensive in the northern GBR and southern GBR. The and black corals (Fig. 20.4b; Bridge et al. 2011a, b, smallest surface area of banks is located in the central GBR, 20 The Great Barrier Reef and Coral Sea 357

Fig. 20.4 Examples of mesophotic coral communities on the GBR. (From Bridge et al. 2012c) mimicking the distribution of the near-surface reefs. The (Englebert et al. 2017). The shaded undersides of sea-level area of submerged banks in mesophotic depth range is equal notches often support profuse growth of azooxanthellate to the area of known (mapped) near-surface GBR reefs octocorals (Fig. 20.5). (Harris et al. 2013). Mesophotic reefs in the Australian Coral Sea have only been examined in a few locations but appear to be similar to 20.4 Biodiversity other large, oceanic reef systems in the tropical Pacific. Englebert et al. (2017) provide a description of the deep fore 20.4.1 Macroalgae reef at Osprey, Bougainville, Holmes, and Flinders Reefs, which generally exhibited steep slopes (~60°) starting from a Macroalgae are abundant on mesophotic reefs of the GBR, ledge at 30–40 m depth, down to a narrow terrace at 60–70 m, although they have received little research attention. followed by a very steep slope or vertical wall to at least Halimeda is an important carbonate producer in the GBR, 120 m. A few sites (e.g., North Horn at Osprey Reef) exhibit and associated with tidal flow through the narrow a more moderately sloping profile (45°) (Beaman et al. 2016; passages between the long, linear ribbon reefs results in the Englebert et al. 2017), at least within mesophotic depths formation of large Halimeda banks leeward of the outer bar- (Fig. 20.3c). The deep fore reef slopes at Osprey, Holmes, rier in the northern GBR lagoon (Hopley et al. 2007; McNeil and Bougainville Reefs are dominated by azooxanthellate et al. 2016). Fields of Halimeda several kilometers across octocorals, although Antipatharians, Scleractinians, and were recorded in depths of 50–75 meters at Yonge and Day macroalgae (particularly Halimeda) also occur (Bongaerts Reefs in the northern GBR and off Viper Reef in the central et al. 2011a). Scleractinian corals are more abundant and GBR (Bridge et al. 2011b; Englebert et al. 2017), and occur at greater depths on sloping sites rather than walls Halimeda meadows have been observed at ~80 m depth in 358 T. C.L. Bridge et al.

Fig. 20.5 Octocorals, predominantly Chironephthya, growing on the western wall of Osprey Reef in the Coral Sea at ~ 70 m depth. (Photo credit: , www.mesophotic.org, can be reused under CC BY license) 20 The Great Barrier Reef and Coral Sea 359

Fig. 20.6 Macroalgae (Caulerpa sp.) growing at 55 m depth at Fig. 20.7 Colony of Acropora tenella from Tydeman Reef, northern Hydrographers Passage, central GBR. (Photo credit: Australian Centre GBR. A. tenella is one of a number of coral species previously consid- for Field Robotics, , http://imos.org.au/facilities/ ered rare and geographically restricted to the Coral Triangle, but now aodn/, can be reused under CC BY license) known from numerous sites in the GBR and Coral Sea. (Photo credit: Emre Turak/Lyndon DeVantier, www.coralsoftheworld.org, can be reused under CC BY license) the Gulf of Papua (Harris et al. 1996). The Halimeda fields in the central GBR, and potentially elsewhere, may be due to intrusions of cold, nutrient-rich water onto the continental The first assessments of mesophotic corals were con- shelf (Benthuysen et al. 2016). Dense “curtains” of Halimeda ducted using SCUBA (to 60 m depth) and submersibles and were also observed on the outer-reef walls of Holmes Reef in recorded common mesophotic taxa including Leptoseris, the Coral Sea (Bongaerts et al. 2011a). Cladophora was Pachyseris, Mycedium, and Echinophyllia (Sarano and observed as the dominant benthic component at the equiva- Pichon 1988; Hopley et al. 2007). Corals were recorded to lent depths at Tydeman Reef (Englebert et al. 2017). Other depths of 100 m at Myrmidon Reef in the central GBR and green macroalgae (e.g., Caulerpa spp.) have been observed 110 m at Osprey Reef (Sarano and Pichon 1988), with coral at mesophotic depths in AUV surveys (Fig. 20.6), but overall cover at Myrmidon Reef ~100% at 60–80 m (Hopley et al. macroalgae on mesophotic reefs in the GBR remain poorly 2007). AUV surveys in 2007 demonstrated that corals were known. Crustose also occur throughout the widespread at mesophotic depths on the GBR shelf-edge. mesophotic GBR, with taxa recorded including Hydrolithon, Specimens collected in 11 rock dredges at depths of Neogoniolithon, Lithoporella, Lithophyllum, Lithothamnion, 47–102 m from Ribbon No. 5 Reef, Noggin Pass, Viper Reef, Mesophyllum, Sporolithon, and Peyssonnelia (Abbey et al. and Hydrographers Passage recorded at least 29 nominal 2013). Most taxa appear restricted to the upper mesophotic species from 18 genera across 9 families (based on the (< 60 m), although Melobesoids (Lithothamnion, revised molecular phylogeny for the Scleractinia using Mesophyllum), Sporolithon, and Peyssonnelia are also nomenclature from the World Register of Marine recorded in the lower mesophotic (Abbey et al. 2013). In the Species http://www.marinespecies.org/), including 3 species Coral Sea, encrusting were observed to depths of not previously reported for the region (Bridge et al. 2012a). ~200 m at Osprey Reef, the deepest record for any photo- Importantly, species accumulation curves indicated that trophic taxon in the region (Beaman et al. 2016). mesophotic coral diversity was considerably higher than pre- viously appreciated (Bridge et al. 2012a). From 2010–2016, numerous expeditions using open-­ 20.4.2 Anthozoans circuit SCUBA and remotely operated vehicles (ROV) col- lected specimens from the northern and central GBR and Anthozoans are the best-studied taxonomic group in meso- Osprey, Bougainville, Holmes, and Flinders Reefs on the photic zone of the Coral Sea region. The majority of research Queensland Plateau (Fig. 20.1c). These surveys recorded a has focused on zooxanthellate Scleractinia, with some addi- wide range of coral species, particularly at upper mesophotic tional research on other anthozoan groups. Octocorallia are depths (30–60 m). The Acropora was well-represented the dominant benthos at lower mesophotic depths (Bridge with 38 species, including 4 commonly detected below 50 m et al. 2011a, 2012a), and the increasing interest in meso- and extending to 72 m (Fig. 20.7; Muir et al. 2015). Most photic reefs will likely lead to a greater focus on this group. other shallow-reef genera in the region were recorded below 360 T. C.L. Bridge et al.

30 m, bringing the total number of species recorded below . Additional azooxanthellate genera (e.g., 30 m depth to 192 (Muir and Pichon 2019). A list of species ) have also been observed in AUV images, sug- recorded in the GBR/Coral Sea region to date is given in gesting that additional research effort will yield new generic Muir and Pichon (2019). The number of mesophotic species records for octocorals. represents 44% of the total shallow-reef corals reported for Zooxanthellate octocorals, particularly members of the the region to date (Muir et al. 2015; Muir and Pichon 2019). family Xeniidae, are an important component of upper meso- Many species are recorded only rarely below 30 m and not photic benthos on the GBR (see Benayahu et al. 2019). below 40 m, although this may be at least partially due to Species of Xeniidae (e.g., Cespitularia sp.) are common on sampling effort (despite the wide geographic coverage, taxo- wave-protected outer-shelf reefs in the GBR (Fabricius and nomic surveys below 30 m were restricted by the constraints Alderslade 2001), and AUV surveys show that their depth of using no- open-circuit SCUBA and ROVs). range extends well into the mesophotic zone. Lower meso- Taxonomic surveys require collected specimens for many photic depths along the GBR shelf-edge and in the Coral Sea coral genera, particularly for mesophotic specimens, which atolls support rich communities of azooxanthellate octo- can display unusual morphologies (Muir and Pichon 2019). corals; indeed, like many other Indo-Pacific locations, they Furthermore, most surveys have been restricted to lower reef are the dominant habitat-forming­ taxon in this habitat. slopes, with no reported surveys of submerged banks at Azooxanthellate octocorals are common throughout all meso- mesophotic depths for the region. The capacity to spend photic depths, but on the GBR shelf-edge were most abun- additional time at mesophotic depths and to survey addi- dant at depths of 90–120 m (Bridge et al. 2011a). Based on tional habitats would no doubt increase the number of spe- SS07 specimens, the most abundant taxa at lower mesophotic cies recorded from mesophotic depths and would allow depths include Siphonogorgia, Keroeides, Ellisella, and investigation of ecological questions such as species’ abun- Viminella, with other azooxanthellate genera including dances and recruitment processes. Annella and common throughout meso- Coral diversity decreases at lower mesophotic depths photic depths. Deepwater shoals inside the GBR lagoon are (> 60 m). Nonetheless, 42 species representing 24 genera are also known to support azooxanthellate octocorals (Pitcher recorded from depths ≥60 m (Englebert et al. 2017; Muir et al. 2007), and collections of specimens from these habitats and Pichon 2019). The deepest recorded zooxanthellate coral would likely yield many additional genera. in the region to date is a colony of Leptoseris sp. from 127 m Unlike the GBR, no systematic surveys of mesophotic octo- in the far northern GBR (Englebert et al. 2017). Six species corals have been conducted in the Australian Coral Sea. were only recorded below 40 m (Muir et al. 2015, Englebert However, exploratory dives using an ROV (Lindsay et al. 2012) et al. 2017). No mesophotic coral surveys have been con- and closed-circuit at Osprey, Bougainville, and ducted on the GBR south of Hydrographers Passage (20° S); Holmes Reefs (Fig. 20.6) confirm early observations by Sarano however, submerged reefs extend further south that almost and Pichon (1988) that azooxanthellate octocorals are abun- certainly support corals at mesophotic depths. Living dant at lower mesophotic depths to at least 140 m (Beaman Scleractinian corals are recorded from well south of the GBR et al. 2016). Octocorals, particularly Chironephthya, occur in at locations such as Gardner Banks off (25° S) high abundance at 60–80 m depth on the sediment-free under- (Marshall et al. 1998). Relatively diverse coral assemblages side of ledges carved by waves during periods of lower sea have recently been discovered at mesophtic depths around level (Fig. 20.5). Unlike the submerged reefs of the GBR outer- Lord Howe Island, the world’s southernmost coral reef, and shelf, the steep walls of the Coral Sea reefs provide an ideal the even more southerly Ball’s Pyramid (32° S) (Linklater location for diver-based sampling. The reefs of the Queensland et al. 2016). Submerged reefs in the southern GBR are there- Plateau are becoming popular dive sites among recreational fore likely to support mesophotic corals, and additional sur- closed-circuit divers, which could provide opportu- veys of mesophotic habitats focusing on the southern GBR nities for equivalent scientific surveys in the future. are required. Other anthozoan groups, including Actiniaria (sea anemo- Octocorals are also abundant at mesophotic depths on the nes) and Antipatharia (black corals), are also recorded from GBR and Coral Sea. The most comprehensive taxonomic mesophotic depths in the GBR and Coral Sea. The sea anem- survey of mesophotic octocorals, based on specimens col- ones Entacmaea quadricolor and Heteractis crispa were lected on the SS07 expedition, recorded 27 genera, 25 of observed hosting symbiotic anemonefishes (Amphiprion which were azooxanthellate (Bridge et al. 2012a). Subsequent akindynos and A. perideraion) at depths of 50–65 m in the examination of additional SS07 specimens (Y. Benayahu, central GBR (Bridge et al. 2012b). Similarly, pers. comm.) has identified four additional zooxanthellate genera including Antipathes, Cirrhipathes, and Stichopathes genera among the SS07 specimens: Anthelia, Capnella, are all commonly observed in AUV images; however, no Sinularia, and the recently-described Lohowia koosi comprehensive taxonomic surveys have been conducted on (Alderslade 2003), which was previously known only from mesophotic Antipatharia. 20 The Great Barrier Reef and Coral Sea 361

20.4.3 Sponges central GBR at depths of 50–260 m (Sih et al. 2017). BRUVS surveys conducted to date suggest that the diversity of these Sponges are common on mesophotic reefs in the GBR taxa in the GBR is similar to elsewhere in the Indo-Pacific, (Bridge et al. 2011a). Most sponges are heterotrophic filter-­ and is dominated by a range of species from the families feeders and therefore unaffected by reduced light irradiance Lethrinidae, Lutjanidae, Carangidae and Serranidae at mesophotic depths; however, a subset of species obtain (Fig. 20.8). nutrients through symbiosis with photosynthetic cyanobac- Despite limited research effort, preliminary studies indi- teria (Keesing et al. 2012). No studies have explicitly exam- cate that deeper reefs in northeastern Australia support rich ined mesophotic community composition in the and abundant fish communities (Last et al. 2011, 2014). Coral Sea. However, several Queensland Museum expedi- Depth appears to be the dominant factor structuring meso- tions have made collections that include material from meso- photic fish communities on the GBR, with species richness photic depths and provide a broad overview of sponge and abundance declining with increasing depth (Sih et al. diversity in the region. Records from the Queensland 2017). In addition, distinct communities of fishes occur at Museum Database, accessible via the Atlas of Living different depths, with little species overlap between depths Australia https://www.ala.org.au/, indicate that the most of 50–80, 80–120, and >120 m (Sih et al. 2017). Shallower abundant sponge at mesophotic depths on the GBR is mesophotic (50–80 m) fish assemblages throughout the Clathria (Thalysis) vulpine. Bridge et al. (2011b) report high latitudinal extent of the GBR are characterized by various abundance Carteriospongia foliascens at upper mesophotic lethrinid and carangid species (e.g., Lethrinus rubriopercu- depths on the GBR outer-shelf, particularly at Hydrographers latus, L. miniatus, Carangoides coeruleopinnatus, and C. Passage. Both species contain photosynthetic bacteria, sug- dinema) (Cappo et al. 2007). Intermediate depths (80–120 gesting that sunlight does play a role in sponge ecology at m) are dominated by members of the family Lutjanidae but upper mesophotic depths. Despite their heterotrophic capac- also include deepwater representatives of diverse range of ity, the number of orders, families, genera, and species of families (e.g., Acanthuridae, Pomacentridae, Balistidae, sponges appears to decline with increasing depth. and Labridae). Some species, such as Gymnocranius gran- Nonetheless, sponge diversity at mesophotic depths remains doculis, G. euanus, and Pentapodus aureofasciatus, appear high, with 20 orders, 73 families, and almost 700 morpho- common across both depth strata. In contrast, assemblages species representing 73 families and 20 orders contained in >120 m are comprised of distinctly deep-reef taxa, includ- the Queensland Museum collections. Two groups of sponges, ing species of Aphareus, Etelis, Pristipomoides, Seriola, Lithistids and Verongids, increase slightly in diversity at and Wattsia. Sih et al. reported depth range extensions for mesophotic depths compared to shallow reefs, while all over 30 species, at least 12 new occurrence records for other orders decreased with depth at the same rate as species Australian/GBR species, and potential novel species diversity. Virtually all sponge data from the mesophotic records (species not yet scientifically described). Many GBR comes from epibenthic sleds targeting the soft seabed species recorded in BRUVS surveys were rare, highlight- habitats, with only limited sampling of steep walls. In con- ing the lack of knowledge regarding fish diversity in the trast, reef walls have been well-sampled in shallow-water deeper of the GBR. habitats accessible via SCUBA. Increased sampling of Despite BRUVS being best-suited for surveying larger mesophotic reefs will increase the known diversity of fish species, these surveys also recorded some small reef- sponges from the mesophotic GBR. associated species from families such as Pomacentridae and Labridae. A number of these species (e.g., Chromis okamu- rai, and C. circumaurea) represented new records for 20.4.4 Fishes Australia, and also large range extensions suggesting some mesophotic species may be more widespread than currently Despite increased interest in Australian MCEs, fish commu- understood. Additional surveys targeting smaller reef-asso- nities of the GBR and Coral Sea remain relatively understud- ciated species, particularly using closed-circuit rebreathers, ied compared to MCEs in other regions. Research has been and expanding sampling to other regions of the GBR and sporadic and relied on a variety of opportunistic data sources; Coral Sea would no doubt greatly increase the number of for example, exploratory scientific deepwater fishing MCE species known in the region. (Kramer et al. 1994; Last et al. 2014) and BRUVS data from MCEs in the GBR also appear to support a diverse the deeper sections of the GBR lagoon (Cappo et al. 2007, assemblage of , with BRUVS surveys recording a 2009) have resulted in new species occurrence records for wide range of species with different life histories at all Australia. BRUVS were also used recently to investigate the depths. Species observed included composition of fish communities on the outer-shelf of the (Triaenodon obesus), sliteye shark (Loxodon macrorhinus), 362 T. C.L. Bridge et al.

Fig. 20.8 Fishes of the mesophotic GBR from BRUVS: (a) Abalistes stellatus, (b) Epinephelus cyanopodus, (c) Seriola dumerili, (d) Gymnocranius euanus, (e) G. grandoculis, and (f) Lutjanus sebae. (Photo credits: Tiffany Sih, www.mesophotic.org, can be reused under CC BY license) 20 The Great Barrier Reef and Coral Sea 363 scalloped hammerhead (Sphyrna lewini), and numerous species of carcharhinids (e.g., Carcharhinus amblyrhynchos, C. albimarginatus, and C. plumbeus) (Sih et al. 2017; Fig. 20.9). Other species known to occur at mesophotic depths (at least to ~50 m) from BRUVS include Coate’s shark (C. coatesi), blacktip sharks (C. tilsoni/limbatus), (Galeocerdo cuvier), sicklefin lemon shark (Negaprion acutidens), Australian sharpnose shark (Rhizoprionodon tay- lori), tawny nurse shark (Nebrius ferrugineus), Australian weasel shark (Hemigaleus australiensis), spotted wob- begong (Orectolobus maculatus), and (Sphyrna mokarran) (Espinoza et al. 2014). With ongoing concern regarding declining shark abundance on the GBR and globally (Robbins et al. 2006; Worm et al. 2013), meso- photic reefs may represent critical habitat for threatened shark populations.

20.4.5 Other Biotic Components

Large benthic foraminifera are commonly observed in AUV images from the GBR outer-shelf at mesophotic depths. Sediment samples collected on the SS07 expedition allowed Renema et al. (2013) to examine modern and fossil assemblages of large benthic foraminifera (LBF) in the mesophotic zone at Hydrographers Passage, and recorded eight species of living LBF to a maximum depth of 129 m which were partitioned into two assemblages strati- fied by depth. Operculina sp. was the most abundant species in the shallow (50–80 m) assemblage, whereas Planostegina operculinoides and Cycloclypeus carpenteri were the domi- nant species in the deep assemblage (Renema et al. 2013). No other taxa have received significant research attention, although mesophotic reefs clearly present opportunities for numerous taxonomic groups. AUV surveys recorded the pres- ence of various benthic macrofaunas, including gastropods, holothurians, asteroids, ophiuroids, and crinoids, which are commonly observed in association with gorgonians at meso- photic depths on the GBR outer-shelf. Woolsey et al. (2013) used AUV images to describe dense aggregations (418 indi- viduals m−2) of the suspension-feeding ophiuroid Ophiopsila pantherina on sand dunes at 67–70 m at Hydrographers Passage (Fig. 20.10). The shelf-edge of the GBR and Coral Sea reefs are also important habitats for unique species such as chambered , Nautilus pompilius, which occur at Fig. 20.9 Examples of shark species commonly observed in BRUVs mesophotic depths but are more common in the sub-photic surveys of mesophotic depths on the GBR outer-shelf: , (Barord et al. 2014). The outer-shelf of the GBR and Coral Carcharhinus albimarginatus (top); gray reef shark, C. amblyrhynchos Sea would no doubt yield rich communities of many other (middle); whitetip reef shark, Triaenodon obesus (bottom). (Photo credits: Tiffany Sih, www.mesophotic.org, can be reused under CC BY marine taxa if afforded sufficient research effort. license) 364 T. C.L. Bridge et al.

reef geomorphology, clearly influences the structure and composition of benthic communities at mesophotic depths (Muir et al. 2015; Englebert et al. 2017). The deep slopes of emergent reefs are often subjected to high sediment flux, particularly carbonate sediments originating from the adja- cent shallow reefs. The Coral Sea is exposed to southeast- erly for most of the year, and leeward reef slopes are therefore regularly subjected to sediments trans- ported downslope by wind and wave action. Even in excep- tionally clear waters with extensive shallow-reef development, sediment deposition can result in depauper- ate benthic communities at mesophotic depths. For exam- ple, coral abundance at mesophotic depths at Mantis Reef in the far northern GBR was considerably higher on the windward compared to the leeward reef slope, probably Fig. 20.10 AUV image showing dense aggregations of the suspension-­ due to the influence of sedimentation (T. Bridge and feeding ophiuroid Ophiopsila pantherina on sand dunes at 67–70 m at P. Bongaerts, pers. obs.). The high rates of sediment trans- Hydrographers Passage, central GBR. (Image: Australian Centre for port, indicated by active “sand falls,” result in depauperate Field Robotics, University of Sydney http://imos.org.au/facilities/ aodn/, can be reused under CC BY license) benthic communities at mesophotic depths despite high coral abundance and diversity in the shallows.

20.5 Ecology 20.6 Threats and Conservation Issues Mesophotic research in the Coral Sea is still in its infancy, reflected in the large number of papers focused on descrip- The GBRMP is considered a world-leading example of a tive “discovery” studies (Loya et al. 2016). Consequently, marine reserve network, with approximately 33% of the the majority of research published to date has documented GBRMP included in no-take zones. Importantly, the design spatial patterns of biodiversity across the region (e.g., of the GBRMP zoning network explicitly considered latitu- Bongaerts et al. 2011b; Bridge et al. 2011a, b, 2012c; Muir dinal and cross-shelf gradients in environmental condi- et al. 2015; Englebert et al. 2017). At the GBR scale, typical tions, which were assumed to influence the distribution of “mesophotic” communities are not equivalent to a fixed biodiversity (Day et al. 2002). This precautionary approach depth range but rather exhibit significant spatial heterogene- has proven effective at achieving representation of a broad ity due to cross-shelf variability in light penetration. Water range of marine habitats, including incidental protection of clarity in the GBR is reduced near coastal river features that were unknown at the time the zoning plan was plumes, and latitudinal variability from the macrotidal south- developed (Bridge et al. 2015). Consequently, MCEs are ern GBR where waters are more turbid, to the central mes- well-represented in no-take areas – an important finding otidal GBR, and then to northern GBR where turbid Torres applicable to other regions where biodiversity data to Strait waters make a seasonal incursion. In addition, intru- inform the design of marine reserve networks are scarce. sion of cold, nutrient-rich water onto the continental shelf is Although further research on the biology of specific species known to occur on the GBR and may exert an important (e.g., commercially important fish species) is required to influence on mesophotic ecosystems (Benthuysen et al. identify key sites such as spawning aggregations, many 2016). Importantly, these intrusions may lower near-seafloor mesophotic fish species should theoretically benefit from water on the outer-shelf by 1–3 °C over periods no-take areas in the GBRMP. The Australian government of ~1 week which are not reflected by near sea surface tem- has proposed a large marine reserve in the Coral Sea Islands peratures. The timing of these intrusions during the austral Territory, but the process has been hindered by political tur- summer has important implications not only for the ecology moil. In contrast, 1.3 million square kilometers of the New of mesophotic reefs in the region but also in their susceptibil- Caledonian Coral Sea were recently designated a new ity to thermal stress. Despite reasonable spatial coverage of marine protected area, known as the Natural Park of the mesophotic research in the region, there is a need for an Coral Sea. increasing focus on research that investigates ecological pro- Many commercially important fish species utilize meso- cesses and the long-term dynamics of mesophotic reefs photic reefs, and, therefore, MCEs represent important fish- (Loya et al. 2016). eries resources in need of effective management (Lindfield At a local scale, sediment transported down the reef et al. 2015). Slow life histories and high vulnerability to slope by wind and/or waves, which in turn is influenced by overexploitation are characteristics of deep-sea fishes and 20 The Great Barrier Reef and Coral Sea 365 also many mesophotic species (Newman et al. 2016). Given abundance globally (Pratchett et al. 2014). On the GBR, out- the limited understanding of the distribution, abundance, breaks appear most common on upper reef slope habitats, and life histories of many mesophotic reef fishes, it is criti- and while COTS have been observed at mesophotic depths, cal that they be considered explicitly for management and they are not recorded at outbreak levels (Pratchett et al. conservation purposes. Mesophotic depths elsewhere 2014). However, it is possible that this may be due to a lack exhibit high occurrence of endemic species (Kane et al. of observation effort on reefs at mesophotic depths. While 2014), and evidence to date suggests the GBR region is no COTS may settle in deepwater habitats (sensu Johnson et al. exception. Australia’s fish fauna in general exhibits high 1991), known settlement substrates do occur in shallow habi- endemism (Last et al. 2011), suggesting high endemism will tats, and large numbers of newly settled COTS have been occur at mesophotic depths. For instance, Last et al. (2014) detected on reef slopes <15 m depth (Zann et al. 1990; reported ~50% endemism in deepwater fishing surveys in Wilmes et al. 2016). the Coral Sea. Furthermore, 78 species caught by scientific Explicit consideration of mesophotic coral ecosystems in trawl in the Coral Sea (20% of the total catch) were previ- regular long-term monitoring is urgently needed to under- ously undescribed for the region, and 96 species were new stand the trajectories and threats to these ecosystems. Australian records (Last et al. 2014). While these species Fortunately, the GBRMPA has identified mesophotic reefs as were largely caught at depths beyond the mesophotic zone a key knowledge gap, and future reef monitoring is likely to (196–800 m), these findings suggest that the fish fauna of see a far greater interest in mesophotic coral reefs. the Coral Sea region may be quite distinct from elsewhere in the Indo-Pacific.­ Similarly, recent research on the GBR has Acknowledgements We thank the pioneering researchers who first revealed new records for Chromis and Bodianus species, as reported mesophotic reef communities on the GBR and Coral Sea well as several potentially new species from the lower meso- atolls, including David Hopley, Peter Davies, Charles Veron, Terry Done, Peter Harris, and Michel Pichon. We also thank the dedicated photic (Sih et al. 2017; Fig. 20.8). Further mesophotic research vessels and vessels of opportunity, as well as funding agencies, research using a range of sampling techniques will likely that have supported the research of authors over the years, in particular reveal many new discoveries within mesophotic fish RV Cape Ferguson (AIMS), RV Southern Surveyor and RV Investigator communities. (Australia’s Marine National Facilities), RV James Kirby (JCU), MV Spoilsport (Mike Ball Dive Expeditions), and the Australian Centre for Long-term datasets sufficient to determine the trajectories Field Robotics and the Integrated Marine Observing System (IMOS), of mesophotic coral reef communities are currently lacking. without which our research would not be possible. We also thank our Mesophotic reefs in the GBR will no doubt face similar pres- funding sources, particularly the Australian Research Council, Pacific sures to shallow-water coral reefs, particularly the effects of Blue Foundation, XL Catlin Group, Waitt Foundation, Ian Potter Foundation, and the Joy Foundation. We thank Dr. Simon Mitchell for global . In 2016, the northern GBR and Coral providing photographs. Sea experienced severe (Hughes et al. 2017). Extensive bleaching surveys focused almost entirely on shal- low reefs (<12 m depth), but qualitative observations sug- gested that while some bleaching did occur at depths of References 30–40 m at some sites, with the incidence of bleaching declined with depth. Nonetheless, observations from other Abbey E, Webster JM, Beaman RJ (2011) Geomorphology of sub- regions clearly show that mesophotic reefs are not immune merged reefs on the shelf edge of the Great Barrier Reef: the influence of oscillating Pleistocene sea-levels. 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