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ArticleTitle New constraints on the spatial distribution and morphology of the Halimeda bioherms of the Great Barrier Reef, Australia Article Sub-Title Article CopyRight Springer-Verlag Berlin Heidelberg (This will be the copyright line in the final PDF) Journal Name Coral Reefs Corresponding Author Family Name McNeil Particle Given Name Mardi A. Suffix Division Geocoastal Research Group, School of Geosciences Organization The University of Sydney Address Sydney, NSW, 2006, Australia Division School of Earth, Environmental and Biological Science Organization Queensland University of Technology Address Level 3, R Block, 2 George Street, Brisbane, QLD, 4000, Australia Phone +61 4 3869 0879 Fax Email [email protected] URL ORCID http://orcid.org/0000-0003-4613-4445

Author Family Name Webster Particle Given Name Jody M. Suffix Division Geocoastal Research Group, School of Geosciences Organization The University of Sydney Address Sydney, NSW, 2006, Australia Phone Fax Email URL ORCID Author Family Name Beaman Particle Given Name Robin J. Suffix Division College of Science and Engineering Organization James Cook University Address PO Box 6811, Cairns, QLD, 4870, Australia Phone Fax Email URL ORCID Author Family Name Graham Particle Given Name Trevor L. Suffix Division Organization GeoCoastal (Australia) Pty Ltd Address Brisbane, Australia Division School of Earth Science Organization The University of Queensland Address St. Lucia, QLD, 4072, Australia Phone Fax Email URL ORCID

Received 29 April 2016 Schedule Revised Accepted 4 August 2016

Abstract Halimeda bioherms occur as extensive geological structures on the northern Great Barrier Reef (GBR), Australia. We present the most complete, high-resolution spatial mapping of the northern GBR Halimeda bioherms, based on new airborne lidar and multibeam echosounder bathymetry data. Our analysis reveals that bioherm morphology does not conform to the previous model of parallel ridges and troughs, but is far more complex than previously thought. We define and describe three morphological sub-types: reticulate, annulate, and undulate, which are distributed in a cross-shelf pattern of reduced complexity from east to west. The northern GBR bioherms cover an area of 6095 km2, three times larger than the original estimate, exceeding the area and volume of calcium carbonate in the adjacent modern shelf-edge barrier reefs. We have mapped a 1740 km2 bioherm complex north of Raine Island in the Cape York region not previously recorded, extending the northern limit by more than 1° of latitude. Bioherm formation and distribution are controlled by a complex interaction of outer-shelf geometry, regional and local currents, coupled with the morphology and depth of continental slope submarine canyons determining the delivery of cool, nutrient- rich water upwelling through inter-reef passages. Distribution and mapping of Halimeda bioherms in relation to Great Barrier Reef Marine Park Authority bioregion classifications and management zones are inconsistent and currently poorly defined due to a lack of high-resolution data not available until now. These new estimates of bioherm spatial distribution and morphology have implications for understanding the role these geological features play as structurally complex and productive inter-reef habitats, and as calcium carbonate sinks which record a complete history of the Holocene post-glacial marine transgression in the northern GBR. Keywords (separated by '-') Halimeda bioherm - Geomorphology - Reticulate - Habitat complexity - Holocene Footnote Information Communicated by Geology Editor Eberhard Gischler Electronic supplementary material The online version of this article (doi:10.1007/s00338-016-1492-2) contains supplementary material, which is available to authorized users. Coral Reefs DOI 10.1007/s00338-016-1492-2

1 REPORT

2 New constraints on the spatial distribution and morphology 3 of the Halimeda bioherms of the Great Barrier Reef, Australia

4 Mardi A. McNeil1,2 • Jody M. Webster1 • Robin J. Beaman3 • Trevor L. Graham4,5

5 Received: 29 April 2016 / Accepted: 4 August 2016 6 Ó Springer-Verlag Berlin Heidelberg 2016

2 Author Proof 7 Abstract Halimeda bioherms occur as extensive geologi- barrier reefs. We have mapped a 1740 km bioherm AQ222 8 cal structures on the northern Great Barrier Reef (GBR), complex north of Raine Island in the Cape York region 23 9 Australia. We present the most complete, high-resolution not previously recorded, extending the northern limit by 24 10 spatial mapping of the northern GBR Halimeda bioherms, more than 1° of latitude.PROOF Bioherm formation and distri- 25 11 based on new airborne lidar and multibeam echosounder bution are controlled by a complex interaction of outer- 26 12 bathymetry data. Our analysis reveals that bioherm mor- shelf geometry, regional and local currents, coupled with 27 13 phology does not conform to the previous model of par- the morphology and depth of continental slope submarine 28 14 allel ridges and troughs, but is far more complex than canyons determining the delivery of cool, nutrient-rich 29 15AQ1 previously thought. We define and describe three mor- water upwelling through inter-reef passages. Distribution 30 16 phological sub-types: reticulate, annulate, and undulate, and mapping of Halimeda bioherms in relation to Great 31 17 which are distributed in a cross-shelf pattern of reduced BarrierED Reef Marine Park Authority bioregion classifica- 32 18 complexity from east to west. The northern GBR bio- tions and management zones are inconsistent and cur- 33 19 herms cover an area of 6095 km2, three times larger than rently poorly defined due to a lack of high-resolution data 34 20 the original estimate, exceeding the area and volume of not available until now. These new estimates of bioherm 35 21 calcium carbonate in the adjacent modern shelf-edge spatial distribution and morphology have implications for 36 understanding the role these geological features play as 37 structurally complex and productive inter-reef habitats, 38 39 A1 Communicated by Geology Editor Eberhard Gischler and as calcium carbonate sinks which record a complete history of the Holocene post-glacial marine transgression 40 A2 Electronic supplementary material The online version of this in the northern GBR. 4142 A3 article (doi:10.1007/s00338-016-1492-2) contains supplementary A4 material, which is available to authorized users. Keywords Halimeda bioherm Á Geomorphology Á 43 A5 & Mardi A. McNeil Reticulate Á Habitat complexity Á Holocene 44 A6 [email protected]

A7 1 Geocoastal Research Group, School of Geosciences, The A8 University of Sydney, Sydney, NSW 2006, Australia Introduction 45 A9 2 Present Address: School of Earth, Environmental and A10 Biological Science, Queensland University of Technology, Halimeda sediment is a major contributor to the tropical 46 A11 Level 3, R Block, 2 George Street, Brisbane, QLD 4000, back-reef carbonate facies (Maxwell 1973; Orme et al. 47 A12 Australia 1978; Hopley et al. 2007; Rees et al. 2007), where disag- 48 A13 3 College of Science and Engineering, James Cook University, gregated calcium carbonate (aragonite) Halimeda segments 49 A14 PO Box 6811, Cairns, QLD 4870, Australia can accumulate as thick bank-like structures or bioherms, 50 A15 4 GeoCoastal (Australia) Pty Ltd, Brisbane, Australia over millennial time scales. Globally, Halimeda bioherms 51 5 52 A16 School of EarthUNCORRECT Science, The University of Queensland, have been described from Kalukalukuang Bank (K-Bank), A17 St. Lucia, QLD 4072, Australia Eastern Java Sea, Indonesia (Roberts et al. 1987; Phipps 53

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54 and Roberts 1988; Roberts et al. 1988), Miskito Channel, and Abel 1985, 1988; Table 1) based on extensive grab 107 55 Nicaraguan Rise, south–west Caribbean Sea (Hine et al. samples. 108 56 1988), and reported but not described in detail at Big Bank Previously, the widely accepted paradigm of bioherm 109 57 Shoals, Timor Sea (Heyward et al. 1997; Table 1). morphology occurs as a series of 5–20 m-thick linear 110 58 Upwelling of cool nutrient-rich water onto the continental parallel ridges and troughs, sometimes forming hummocky 111 59 shelf from below the adjacent oceanic thermocline has mounds (Table 1). This model was constructed, at the time, 112 60 been proposed as a control on the distribution and forma- by a reasonable interpolation between parallel sub-bottom 113 61 tion of the Halimeda bioherms (Drew 1983; Drew and Abel and single-beam echosounder profiles, forming the linear 114 62 1985; Roberts et al. 1987, 1988; Hine et al. 1988; Marshall ridges and mound-like morphology that permeates the lit- 115 63 and Davies 1988; Phipps and Roberts 1988; Wolanski et al. erature (Orme and Salama 1988; Mathews et al. 2007; 116 64 1988). The reported global distribution appears consistent Fig. 2), including the interpretation of analogous Halimeda 117 65 with this idea (Table 1). In the Great Barrier Reef, the deposits in the geological past (Drew and Abel 1988; Braga 118 66 previously known extent, morphology, age, sedimentation et al. 1996; Martı´n et al. 1997). Some cross-shelf mor- 119 67 rates, and carbonate budget of the Halimeda bioherms were phological variation was reported, with topographic relief 120 68 based on sediment grabs, vibra and piston coring, and being better developed and more pronounced to eastward, 121 69 widely spaced seismic profiling and single-beam echo- and smaller, less complex mounds on the western half of 122 70 sounder profiles (Hopley et al. 2007; Rees et al. 2007; the outer-shelf (Davies and Marshall 1985; Marshall and 123 71 Davies 2011). Crucially, descriptions of the spatial distri- Davies 1988; Orme and Salama 1988). 124

Author Proof 72 bution and 3D morphology of the bioherms in the GBR In this study, we use new high-resolution airborne lidar 125 73 have not been reassessed in the 30 years since this early and multibeam bathymetry datasets to better quantify and 126 74 body of work was initiated nor with the benefit of more redefine the spatial distribution and morphologic variation 127 75 modern survey technologies, such as airborne lidar bathy- of the northern GBRPROOFHalimeda bioherms. Our objectives 128 76 metry (ALB) and multibeam echosounders. are to (1) accurately map the total spatial extent and 129 77 The spatial distribution limits and the boundaries of boundaries of the bioherms, (2) utilise the new bathymetry 130 78 individual bioherms in the northern and southern GBR are datasets to redefine and quantitatively describe the bioherm 131 79 poorly constrained. A pioneering survey of inter-reef sed- geomorphology, (3) investigate how their morphology 132 80 iments from the GBR (Maxwell 1968, 1973) reported varies spatially at different scales both latitudinally and 133 81 Halimeda-rich gravel further north of Raine Island (latitude cross-shelf, (4) propose hypotheses to explain the Hal- 134 82 11°350S). However, a later survey (Drew and Abel 1988) imedaEDbioherm distribution, formation, and morphology, 135 83 recorded a northernmost limit for the Halimeda bioherms and (5) discuss the management/conservation implications 136 84 of 11°300S but did not locate the area further north of these findings for better characterising and understand- 137 85 described by Maxwell. The southern limit of Halimeda ing the inter-reef habitats of the GBR. 138 86 bioherms is poorly defined due to a lack of survey data, 87 which is restricted to one survey of the Swain Reefs (Searle 88 and Flood 1988) where seismic profiling showed internal Materials and methods 139 89 structure similar to the northern GBR bioherms, with 90 vibracoring providing evidence of Halimeda bioherms at To accurately map the total areal extent and redefine the 140 91 latitude 21°350S–21°490S. The known extent of the north- geomorphology of the GBR bioherms, this study synthe- 141 92 ern GBR bioherms is concentrated in two regions: east of sised a range of information derived from new airborne 142 93 Cape York between latitudes 11°300S–13°260S (Drew lidar and multibeam bathymetry datasets, seismic profiling 143 94 1983, 1993; Drew and Abel 1985, 1988; Orme 1985;Orme data, and combining these with existing sediment sampling 144 95 and Salama 1988), and the Ribbon Reefs region east of surveys, seismic profiles, and vibracores taken from the 145 96 Cooktown and Lizard Island between latitudes 14°400S and published literature (Table 2). Comparisons were made 146 97 16°70S (Davies and Marshall 1985; Orme 1985; Marshall between the previously reported Halimeda bioherm spatial 147 98 and Davies 1988; Orme and Salama 1988; Fig. 1). The extent, distribution, and morphology descriptions, and our 148 99 bioherms lie proximal to the landward side of the Ribbon analysis of the new and existing data. 149 100 Reefs at 20–40 m depth, with a maximum vertical thick- 101 ness up to 20 m. Between these two regions, bioherms are GIS methods 150 102 absent in the Princess Charlotte Bay area (latitude 103 13°420S). Of the reported global Halimeda bioherms, very Airborne lidar bathymetry (ALB) data were collected by 151 104 few descriptions of the total spatial extent (area and vol- the Royal Australian Navy and supplied by the Australian 152 105 ume) have actually been quantified, with only one pre- Hydrographic Service using a lowest astronomical tide 153 UNCORRECT2 106 liminary estimate for the entire GBR of c. 2000 km (Drew (LAT) vertical datum and a WGS84 horizontal datum, with 154

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Article No. : 1492 h LE h TYPESET MS Code : CORE-D-16-00109 h44CP h DISK Coral Reefs ) 2007 ), Orme 1985 ), Phipps ) ), Phipps and ) 1985 ), Drew and Abel 2007 ) 1988 ) , ), Rees et al. ( 1988 ), Orme ( ) 1985 1993 1997 ) 1987 1988 ), Marshall and Davies 1978 1988 1988 1985 ), Rees et al. ( ), Drew ( 1988 1988 Roberts ( and Salama ( ( et al. ( ( Hine et al. ( References Max 140 (m) ) Thickness 2 Author Proof 2000 5–20 Drew and Abel ( Not quantified 20–50 Roberts et al. ( * 118 10–15 Davies and Marshall ( 184 5–19PROOF Orme et al. ( 150 m across Not quantified Heyward et al. ( \ ED hummocky mounds 10–30 mto across, broad undulating areas limestone pinnacles in valleys. irregular form and size ridges and valleys. Elongate ridges and valleys, to ridges and valleys, 3 m high-eroded Banks and ridges, troughs and hollows, Morphology not described Not quantified Up to 14 Searle and Flood ( 70 m 80 m * * bioherm distribution and morphology descriptions near vertical slope edge, thermocline at thermocline at Cato Trough Adjacent basin depth (m) Morphology descriptions Area (km Halimeda mound tops (m) 20–40 800–1000 m strait of Makassar, 40–50 Cayman trough 1000 m Mounds with lens-like geometry Not quantified 20–30, 28–45 300 m depth to base of shoal Distinct hummocks, 25–40 Queensland Trough 1–2000 m, 30–50 Queensland Trough 1–2000 m Mounds, often elongate; 20–40 Queensland Trough 1–2000 m Discrete circular mounds, and parallel 20–32 Capricorn Channel 1–3000 m in Summary of reported global (K Bank) Eastern Java Sea, Indonesia Miskito Channel, Southwest Caribbean Timor Sea northern Great Barrier Reef northern Great Barrier Reef Barrier Reef Great Barrier Reef Kalukalukuang Bank, Nicaraguan Rise, Big Bank Shoals, Lizard Island region, Cooktown region, Whole northern Great Swain Reefs, southern Table 1 UNCORRECTLocation Depth to

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Fig. 1 Regional map of 143°E 144°E 145°E 146°E northern Great Barrier Reef (GBR) with comparison of Torres Strait previous and new (this study) Halimeda bioherm distribution in relation to the Cape York and Ribbon Reefs regions and 11°S surrounding reefs. Locations of Fig. 4 figures referred to in this study are marked for geographical Australia reference Raine Island

12°S

Cape York Coral Sea Fig. 5

13°S Author Proof Fig. 3 PROOF

14°S Princess Charlotte Bay

Lizard Fig. 2 ED Island

15°S Previous bioherm distribution Ribbon New bioherm distribution Reefs Reefs and Shoals GBRMP boundary Cooktown

16°S 0525 0100km

155 point spacing varying between 6 and 30 m. LAT to MSL additional 0.0005 arc degree (*50 m) DEM was generated 167 156 (Mean Sea Level) vertical adjustment was made to the for the northern GBR, combining all available bathymetry 168 157 bathymetry data to give a MSL vertical datum. Maximum data, including the new ALB and multibeam data and the 169 158 depths for ALB data vary due to clarity of water but may older single-beam survey data. This regional-scale seam- 170 159 be up to 50 m depth on the outer-shelf. Fledermaus 3D less DEM across the shelf and into the adjacent continental 171 160 visualisation software was used to edit the data of noise slope revealed the deeper inter-reef passages and upper- 172 161 then generate a compiled digital elevation model (DEM) slope canyons of the northern GBR. The 50 m DEM was 173 162 with a 0.00025 arc degree (*25 m) pixel size and a cor- then analysed with the ArcGIS Benthic Terrain Modeller 174 163 responding hillshaded geotif image (Fig. 3). The resulting (BTM) plug-in (Wright et al. 2005) to derive a slope model 175 164 DEM was converted to an ESRI raster grid for further (in degrees) and a rugosity model (measure of terrain 176 165 spatial analysis in ArcGIS 10.1 software. Because of the complexity) to visualise the bioherm morphology and 177 166 relatively shallowUNCORRECT depth limit of the ALB data, an distribution limits within the adjacent landscape features. 178

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Fig. 2 a Bioherm morphology a conceptual diagram derived by interpolating between parallel echo-sounder profiles (adapted Stewart from Mathews et al. 2007), Shoal b new 3D view of lidar bathymetry for the same sea level 9 0 5.6 3.6 km area showing 10 their actual complex reticulate 20 Petricola morphology. See Fig. 1 for 30 Shoal

location Depth (m) 40 50

Pleistocene

N

1 km

olocene Reef H Pleistocene Halimeda banks 1 km seismic reflector

Author Proof Pleistocene b PROOF

Depth (m) 10 15 20 ED 1 km 25 30 35 1 km 40 N 45 vertical exagg. x6

179 Using these derived models, the characteristic geomor- 1993) to quantify the previously known distribution and 196 180 phology of the Halimeda bioherms was clearly distin- compare to the areal extent of the new map. The ArcMap 197 181 guishable from coral reefs, inter-reef passages, and deeper Calculate Geometry Tool was used to calculate the 2-D 198 182 palaeochannels. Care was taken to avoid false-positive surface area of both shapefiles. Defining the three mor- 199 183 identification of bioherms and a conservative approach was phological sub-type boundaries required a broader-scale 200 184 taken when comparing different sized DEMs and their approach and was manually digitised in ArcMap at 201 185 derived models. 1:100,000 scale. 202 186 An ArcGIS polyline shapefile was created by hand 187 digitising polygons over the 25 m hillshade image and 188 50 m slope and rugosity models to delineate the boundaries Results 203 189 of the bioherms at 1:25,000 scale. The new polygons were 190 cross-referenced against existing seismic profiles (Davies Based on a comprehensive analysis of the new and existing 204 191 and Marshall 1985; Drew and Abel 1985, 1988; Phipps high-resolution bathymetry datasets, we have quantified the 205 192 et al. 1985; Marshall and Davies 1988; Webster et al. 2012) spatial distribution and morphologic variation of bioherms 206 193 and the original maps of bioherm distribution (Drew and across the entire northern GBR (Table 3). We have inclu- AQ3207 194 Abel 1985; Drew 1993). A second shapefile was created ded the estimate of the small (73 km2) area previously 208 195 from the originalUNCORRECT maps (Drew and Abel 1985, 1988;Drew reported in the Swain Reefs from the southern GBR within 209

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Article No. : 1492 h LE h TYPESET MS Code : CORE-D-16-00109 h44CP h DISK Coral Reefs ) ) ), Orme 1988 1993 1985 ), Drew and ), Phipps et al. ), Marshall and ), Drew and ) ) 1985 1985 ), Drew ( 1985 1993 ) ) 1988 1988 ), Orme ( 1988 ) 1988 ) ) 2007 1978 ) ), Marshall and Davies ), Drew ( 1988 2010 2010 1985 1985 ), Marshall and Davies ( ) 1983 1985 1988 Abel ( Davies ( ( and Salama ( ( Abel ( Drew and Abel ( Drew ( Beaman ( Davies and Marshall ( References S Orme et al. ( 0 S Davies and Marshall ( S Davies and Marshall ( 02 0 0 ° Author Proof by species 46 46 Halimeda ° ° S Searle and Flood ( S Searle and Flood ( 0 0 S–15 0 24 24 ° ° S–15 S–15 27 0 0 ° 10 10 ° ° Halimeda S–22 S–22 0 PROOF0 53 53 ° ° 25 m depth * Halimeda

bioherm boundaries and distribution ED ), sediment % 2 - Halimeda Entrance and Second Three-Milebanks Opening. clearly visible to Level (MSL) vertical datum; WGS84 horizontal datum survey tracks (echosounder). Georeferencedto in determine ArcMap area (g m Lizard Island region, northern GBR 14 Cooktown region, northern GBR 15 Great Barrier Reef Seabed Biodiversity Project Pitcher et al. ( Swain Reefs, southern GBR 20 Swain Reefs, southern GBR 20 Nov 1993 to Sep 2013 LADSI & II system, Mean Sea Multiple surveys forming gbr100 DEM Beaman ( Original distribution map, based on sediment grabs and Cooktown region, northern GBR 15 Includes lat/long, depth (m), living Atlas Atlas Halimeda Halimeda Service CSIRO Queensland Queensland Service Service 1984 RV James Kirby Geoscience Australia August 1972 routine aerial photography flight over Hibernia Australian Hydrographic Multiple survey cruises 1983 HMAS Kimbla, RV The Harry Messel 1984 RV James Kirby 1983 HMAS Kimbla, RV The Harry Messel 129 172 217 236 ? ? ? ? survey maps Ed Drew Summary of new and existing data sources used to delineate new Halimeda Seismic profilesVibracores Australian Hydrographic Geoscience Australia CAB-7082 RUN 22 Frame 032 CAB-7082 RUN 23 Frame 048 CAB-7082 RUN 19 Frame 189 CAB-7082 RUN 20 Frame 145 CAB-7082 RUN 21 Frame 127 Sediment grab sample stations Geoscience Australia and CAB-7082 RUN 18 Frame 170 CAB-7082 RUN 17 Frame 215 Seismic profiles Geological Survey of Airborne lidar bathymetry Royal Australian Navy Vibracores Geological Survey of Aerial photographs CAB-7082 RUN 16 Frame 234 Multibeam bathymetryPrevious Australian Hydrographic Seismic profiles Geoscience Australia Sediment grab sample stations Ed Drew Data Source Description Table 2 UNCORRECT

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Fig. 3 Three-dimensional view a c of the northern Cape York area, N N with a 2 m multibeam data palaeochannel (rainbow scale) overlaid on palaeochannel 25 m lidar data (grey scale), Z’ reef b sub-bottom profile between 0 Z’ points Z - Z shows distinct Depth (m) Halimeda bioherm morphology 17.5 20.0 Z accreting above a prominent 22.5 25.0 seismic reflector. c The 25 m Z 27.5 30.0 lidar data across the same area 32.5 35.0 clearly delineates bioherms, 0 2 km vertical exagg. X6 inter-reef reefs, and palaeochannels. See b passage Z bioherm Z’ Fig. 1 for location 10 10

20 20 reef channel 30 30

40 palaeochannel reflector A 40

50 50

Table 3 Spatial distribution, two dimensional surface area, and proportion of continental shelf covered by the new Halimeda bioherm map Author Proof Region Latitude Bioherm Bioherm Latitudinal Continental shelf Bioherm area Bioherm shelf °S northern limit southern limit distance (km) area (km2)b (km2) area (%)

Northern GBR 0 0 PROOF Cape York 10–11 10°24 S13°26 S 347 6434 1104 17.2 11–12 12,719 1630 12.8 12–13 6312 1563 24.8 13–14 6366 408 6.4 31,831 4705 14.8 Ribbon Reefs 14–15 14°140S16°70S 187 10,017 864 8.6 15–16 ED5624 373 6.6 16–17 6810 153 2.3 22,451 1390 6.2 Northern GBR total 10°240S16°70S 534 54,282 6095 11.2 Swain Reefsa 21°350S21°90S34 72 Total GBR 568 6167 All dimensions are based on calculations of digitised polygon shapefiles in ArcMap a Preliminary estimate based on limited available data (southern GBR) b Data source Lewis and Hutchinson (2001)

210 Table 3; however, it should be noted that the density of continuous bioherms are separated by a region of absence 222 211 lidar and multibeam surveys do not exist in the southern in the Princess Charlotte Bay region (13°260S–14°140S). 223 212 GBR, and so we do not change this estimate in this current The Cape York region is the largest region, running con- 224 213 work. tinuously for 347 km from latitudes 10°240S–13°260S, 225 spanning up to 35 km in width to within 6 km of the shelf 226 214 Northern GBR spatial distribution and coverage break. The Ribbon Reefs region spans 187 km from lati- 227 tudes 14°140S–16°70S, lying proximal to the Ribbon Reefs 228 215 The newly mapped Halimeda bioherms cover a total area and within 4 km of the shelf break. In this region, there is a 229 216 of 6167 km2 (Table 3) spanning the entire northern GBR small break in bioherm continuity between latitudes 230 217 (6095 km2) and including the smaller area estimate from 15°350S and 15°480S. The previously known Halimeda 231 218 the Swain Reefs in the southern GBR (72 km2). In the meadow distribution (Drew and Abel 1988) based on 232 219 northern GBR, bioherms span 534 km in distance from original maps and sediment grabs of living Halimeda 233 220 latitude 10°240S–16°70S. Distributed in two distinct covers 3474 km2 (Fig. 1), with locations of bioherms 234 221 regions, CapeUNCORRECT York and the Ribbon Reefs, the near- generally consistent to this new map, with the exception 235

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Fig. 4 Map of the northern 143°E 144°E Cape York region showing extensive bioherms north of Torres Strait Raine Island not previously Newly mapped area mapped, and their relationship GBRMPA General Use zone to the Great Barrier Reef Marine Park Authority (GBRMPA) Previous bioherm distribution General Use zone (hatched) and New bioherm distribution marine park boundary Reefs and Shoals GBRMP boundary

11°S Author Proof PROOF

Raine Island ED Cape York 12°S

Coral Sea 010205 km

236 that we have defined and mapped a vast (1740 km2) bio- bioregions. In northern Cape York, the bioherms extend 246 237 herm complex north of 11°300S, extending into the Torres beyond the GBR Marine Park boundary into the Torres 247 238 Strait and not previously mapped (Fig. 4). Strait, and 60% of the bioherms (1036 km2) are overlapped 248 239 In the Cape York region, 6–25% (mean 15%) of the by the GBRMPA General Use zone (Fig. 4), which permits 249 240 continental shelf area is covered by bioherms, decreasing in trawling in benthic habitats. 250 241 proportion southwards from 2 to 9% (mean 6%) of the 242 shelf area covered in the Ribbon Reefs region (Table 3). Morphology 251 243 Due to their considerable latitudinal and cross-shelf extent, 244 the bioherms span a number of different Great Barrier Reef The 25 m lidar data reveal a range of bioherm morpho- 252 245 Marine Park AuthorityUNCORRECT (GBRMPA) management zones and logical variation, from complex net-like reticulate 253

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Table 4 Morphological sub-type nomenclature, description, spatial distribution, and type example of (a) reticulate, (b) annulate and (c) undulate Sub-type Description Spatial Distribution Proportion Example (%)

Reticulate High-relief, irregular ridges with sharp Proximal to reef and shelf 16 sinuous crests, complex honeycomb break to east, grading into rugosity, non-circular annulate zone

Annulate Smooth, circular ring shapes, hollow centred More distal to reefs and shelf 16 with or without central pinnacle, often break, generally increasing coalescing together with shared boundaries. in size westward Typically 200 to 250 m across from crest to crest, but can be up to 500 m across Author Proof Undulate Sinuous and wave-like, smooth crests, with Between and around annulate 68 low relief above surrounding sediment and reticulate zones, grading into surrounding inter-reef sediment PROOF

ED 254 structures to circular ring-shaped end members, with 200–250 m across, but can be up to 500 m across from 274 255 smooth undulating zones between (Table 4). We define and crest to crest. This sub-type comprises 16% of the total 275 256 describe three distinct morphological sub-types based on bioherm distribution. 276 257 recurrent patterns of shape, texture, and size, termed as (1) 258 reticulate, (2) annulate, and (3) undulate (Table 4). Undulate 277

259 Reticulate Connecting the reticulate and annulate morphology types 278 and grading out to the limit of bioherm boundaries, the 279 260 The reticulate morphology is characterised by complex remaining substrate is smooth, sinuous, and wave like, with 280 261 honeycomb or net-like irregular ridges, with high relief and low relief but still discernible from the surrounding sea- 281 262 sharp sinuous crests, which are non-circular (Fig. 5). The floor (Fig. 5). The undulate sub-type comprises 68% of the 282 263 reticulate morphological sub-type comprises 16% of the total total bioherm distribution. 283 264 bioherm distribution and is dominant on the eastern half of The morphological variation generally follows an east– 284 265 the bioherms proximal to the shelf-edge barrier reefs. west cross-shelf gradient, with the complex reticulate 285 morphology dominating proximal to the eastern margin of 286 266 Annulate the bioherms adjacent to the shelf-edge barrier reefs 287 (Fig. 5b). The annulate sub-type generally occurs west of 288 267 The annulate morphology is defined by smooth circular, the reticulate zone, becoming less complex but with indi- 289 268 hollow-centred ring shapes. Rings can be singular, but vidual rings increasing in size to westward. The undulate 290 269 often coalesce together sharing boundaries (Fig. 5). A morphology sub-type is most prevalent, connecting the 291 270 sharp high-relief pinnacle described in the literature as reticulate and annulate zones out to the limit of the bioherm 292 271 remnant Pleistocene karst antecedent topography (Phipps boundaries, where it grades into the deeper surrounding 293 272 et al. 1985; Drew and Abel 1988) is clearly visible in the seafloor. These patterns of size, shape, texture, and cross- 294 273 centre of someUNCORRECT rings. Individual rings are commonly shelf gradation are generally consistent latitudinally. 295

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a a b Morphological sub-types reticulate annulate reticulate undulate reef annulate

Ape Reef undulate

Bligh Reef Author Proof

0246810 km PROOF Fig. 5 a Distribution of cross-shelf variation in morphological sub- morphology becomes less complex and size of rings increases types on a large bioherm area in the Cape York region, and b 25 m westward. The smooth, low-relief undulate morphology connects and lidar data for the same area. The complex reticulate morphology surrounds the reticulate and annulate sub-types. See Fig. 1 for dominates proximal to reefs, grading into the annulate zone, where location 296 Discussion known to influence bioherm formation (Wolanski et al. 321 1988). A new geophysical and coring survey of the far 322 297 Spatial distribution northernED bioherms would reveal their thickness, internal 323 structures, relationship to antecedent topography, age, and 324 298 Few attempts at quantifying the spatial extent of the GBR accretionary history since the start of the Holocene marine 325 299 bioherms have been published (Table 1), with just one transgression. 326 300 estimate of the GBR bioherms covering an area of The oligotrophic waters of the GBR lagoon lack the 327 301 approximately 2000 km2 (Drew 1993). When the original volume of essential nutrients (nitrogen and phosphorous) 328 302 maps were digitised, we found them to actually cover an required to produce sufficient living Halimeda biomass, to 329 303 area of 3474 km2. The new bioherm map presented here accumulate calcium carbonate bioherms (Drew and Abel 330 304 covers an area of 6167 km2, three times the original 1985, 1988; Wolanski et al. 1988;Drew2001). Substantial 331 305 2000 km2 estimate. Reported Halimeda-rich gravel quantities of cool, nutrient-rich waters upwelling from 332 306 deposits north of Raine Island (Maxwell 1973) were not below the thermocline in the Coral Sea have been shown to 333 307 found by a subsequent later survey (Drew and Abel 1988); pump through the narrow passages between outer-shelf 334 308 however, our investigation found evidence of extensive reefs via tidal jets (Thomson and Wolanski 1984; Wolanski 335 309 Halimeda bioherms north of Raine Island extending into et al. 1988;Drew2001), delivering the required volume of 336 310 the Torres Strait, covering an extra 1° of latitude and an nutrients. Outer-shelf geometry (Marshall and Davies 337 311 area greater than the Ribbon Reefs bioherms area com- 1988) and bathymetry of the inter-reef passages (Thomson 338 312 bined. This newly mapped area represents an additional and Wolanski 1984; Wolanski et al. 1988) interacting with 339 313 1740 km2 of bioherm inter-reef habitat not previously surface wind stress, residual currents, and topographically 340 314 recorded (Fig. 4). This far northern Cape York region is induced mixing (Andrews and Furnas 1986) have been 341 315 remote and poorly studied; therefore, no seismic or vibra- proposed as contributing factors to whether upwelled 342 316 coring data from this area were available to the present nutrients will reach the GBR lagoon in sufficient concen- 343 317 study. However, previous temperature and current mod- trations to accumulate bioherms. Oddly, there are no 344 318 elling shows that upwelling of cool nutrient-rich water obvious bioherms on the outer-shelf adjacent to Princess 345 319 from below the Coral Sea thermocline occurs at Raine Charlotte Bay, despite its well-developed chain of barrier 346 320 Island EntranceUNCORRECT (Thomson and Wolanski 1984), which is reefs with narrow inter-reef passages comparable to the 347

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348 Cape York and Ribbon Reefs regions (Fig. 1). This absence and troughs representation which permeates the literature 397 349 has been attributed to the input of fluvial mud from the (Fig. 2). The previous description has been compared to 398 350 Normanby River catchment, reducing light levels and the lenticular morphology of phylloidal algal mounds from 399 351 smothering vegetation (Drew and Abel 1988). However, the the late Palaeozoic (Wray 1977; Drew and Abel 1988) and 400 352 Princess Charlotte Bay shelf-edge barrier reefs and inter-reef Halimeda deposits from the upper Miocene reefs of the 401 353 passages are some 70 to 80 km distant from the coast, and Sorbas basin, southeastern Spain (Braga et al. 1996; Martı´n 402 354 unlikely to be regularly influenced by coastal sediment dis- et al. 1997), which are considered to be analogous to their 403 355 charge which is generally restricted to within 10–20 km Holocene counterparts in the GBR. However, the northern 404 356 from the coast (Furnas 2003; Devlin and Brodie 2005), and GBR Halimeda bioherms appear to exhibit much more 405 357 inshore of the 20 m-depth contour (Furnas 2003). Other complex and variable morphologies over very large spatial 406 358 contributing mechanisms are considered here to possibly scales. We have identified and described three new mor- 407 359 explain the absence of bioherms in this shelf interval. phological sub-types, the boundaries of which grade into 408 360 The North Queensland coastline and shelf-edge lies each other (Table 4; Fig. 5). These reticulate/annulate 409 361 generally north–south, and a strong longshore current runs patterns are reminiscent of coral patch reef morphology 410 362 northerly to north-westerly in response to the dominant observed in shallow lagoons, which are interpreted to be 411 363 south-easterly trade winds (Wolanski and Ruddick 1981; controlled by antecedent topography (e.g. Purdy 1974; 412 364 Devlin and Brodie 2005). At Princess Charlotte Bay, the Purdy and Winterer 2006) coupled with hydrodynamic 413 365 coastline and shelf edge change direction from north–south influences. However, recent studies of Holocene reticulate 414

Author Proof 366 to east–west, disrupting the predominant northerly long- reef patterns have revealed that these morphologies also 415 367 shore current. This abrupt change in shelf-edge geometry form on flat erosional surfaces lacking in karstified 416 368 and subsequent disruption to prevailing currents may topography (Blakeway and Hamblin 2015; Schlager and 417 369 impact nutrient upwelling and delivery into the GBR Purkis 2015). ThesePROOF authors propose that at small to 418 370 lagoon through the reefs, thereby precluding bioherm for- intermediate scales (m to km), reticulate patterns can be 419 371 mation. The geomorphology of the adjacent continental biologically controlled rather than substrate controlled, 420 372 slope submarine canyons should also be considered due to with access to nutrients and protection from predation and 421 373 their close relationship to the shelf-edge barrier reefs and erosion cited as possible drivers of ‘‘biotic self-organisa- 422 374 inter-reef passages. For example, the southern limit of the tion’’ (Schlager and Purkis 2015). For example, modelling 423 375 Ribbon Reefs bioherms (latitude 16°70S) coincides with the by Blakeway and Hamblin (2015) showed that organisms 424 376 location where the numerous canyons indenting the shelf- whichED tend to collapse, such as branching Acropora, pro- 425 377 edge changes to being less abundant and slope-confined duce ‘‘cellular’’ (i.e. reticulate) reefs similar to the reticu- 426 378 (see Puga-Bernabe´u et al. 2011, 2013 for descriptions of late and annulate bioherm morphology described here. 427 379 canyon morphology). Therefore, more detailed hydrologi- However, the relationship between Halimeda bioherm 428 380 cal and seabed survey data are required to help explain the origin, accumulation, morphological variation, and the 429 381 absence of bioherms in the Princess Charlotte Bay region. underlying antecedent topography is currently poorly 430 382 The new calculations of Halimeda bioherm spatial extent understood due to the lack of detailed and dense geo- 431 383 and therefore volume of Holocene calcium carbonate clearly physical survey and sediment core data across the full 432 384 exceed that of the modern shelf-edge barrier reefs of the extent of bioherm distribution. Bioherms are accreting 433 385 northern GBR; however, this volume is challenging to above a prominent seismic reflector (Fig. 3b) interpreted to 434 386 quantify in detail (Rees et al. 2007). The current GBRMPA- be the Pleistocene erosional unconformity (‘‘Reflector A’’; 435 387 gazetted ‘‘reef’’ area includes both shallow coral reefs and Orme et al. 1978; Davies and Marshall 1985; Marshall and 436 388 relatively deeper shoals and banks, which our analysis Davies 1988), but the available data are insufficient to 437 389 reveals are in some cases Halimeda bioherms, thereby elucidate any unambiguous relationship with antecedent 438 390 making quantitative comparisons between modern reefs and topographical highs or pinnacles, or to test the Blakeway 439 391 bioherms difficult. Future research will aim to more accu- and Hamblin (2015) self-organisational model against liv- 440 392 rately quantify their volume and role as carbonate sinks and ing Halimeda growth and collapse. Regardless of the pro- 441 393 shelf carbon budgets in comparison to coral reefs. cesses controlling the origin of these morphological sub- 442 types, the question remains as to whether these patterns are 443 394 Morphology unique to the GBR; however, high-resolution bathymetry 444 data from elsewhere in the modern (e.g. Kalukalukuang 445 395 The bathymetry analysis reveals that bioherm shapes and Bank, Indonesia; Nicaraguan Rise; Big Bank Shoals, Timor 446 396 patterns are notUNCORRECT consistent with the previous parallel ridges Sea) is required. 447

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448 Implications for conservation and management population connectivity in adjacent reef ecosystems expe- 500 riencing unprecedented pressures from a changing climate, 501 449 The vast expanse of living Halimeda veneer on top of the ocean acidification, and human impacts from coastal 502 450 bioherms, and the relief and topography of the bioherms development. 503 451 themselves, create a significant and structurally complex This study significantly advances our understanding of 504 452 inter-reef habitat. Ecosystems with this type of structural the vast spatial extent of the northern GBR Halimeda 505 453 complexity are recognised as having higher species rich- bioherms, their morphology, and structural complexity, and 506 454 ness, fish density, and biomass (Alvarez-Filip et al. 2009; provides a crucial new geomorphic context for future 507 455 Graham and Nash 2013). This habitat complexity is studies. Their vast size and volume perhaps elevate their 508 456 extended to the local scale within each individual bioherm importance to rival that of the northern GBR coral reefs as 509 457 and annulate ring having diverse physical and biological calcium carbonate sinks and structures of geological sig- 510 458 characteristics between the flatter mound tops in shallow nificance. This new bioherm map will facilitate managers 511 459 water, their outer and inner sloping surfaces, and within the in clarifying the northern GBR Halimeda bioherms biore- 512 460 deeper hollows and any central pinnacles. Their ecosystem gion classification and contribute to the appropriate man- 513 461 value in terms of biodiversity and nursery refugia (e.g. agement and conservation of these important benthic 514 462 Adams et al. 2006; Mumby 2006) and role in larval dis- habitats. 515 463 persal and patch reef connectivity (e.g. Almany et al. 2009; 464 Munday et al. 2009) may be comparable to that of seagrass Acknowledgments Funding for this Project was provided by a 516 research scholarship from the School of Geosciences, The University 517 Author Proof 465 meadows and mangrove habitats. 518 466 of Sydney. The authors wish to acknowledge the work of the scien- The sheer size of the northern GBR bioherms, the most tists and crew of the many survey voyages and flights from which data 519 467 extensive, actively accumulating Halimeda deposits in the for this project were gathered, particularly the CSIRO Marine 520 468 world, contributes to their Outstanding Universal Value National Facility, Geoscience Australia, Royal Australian Navy and 521 the Australian HydrographicPROOF Service. M.A.M acknowledges and AQ4522 469 from a geological and geomorphological perspective 523 470 thanks L. Nothdurft for suggestions and support. J.M.W acknowl- (Whiteway et al. 2013). The suggestion that the Halimeda edges the Australian Research Council (DP1094001) for support. 524 471 bioherms may contain a more complete record of Holocene 472 calcium carbonate history than the adjacent coral reefs 473 (Drew 1983; Drew and Abel 1985; Phipps et al. 1985) has References 525 474 global implications for Holocene reef carbonate budgets 475 ED 526 due to their contribution as a geological carbon sink within Adams AJ, Dahlgren CP, Kellison GT, Kendall MS, Layman CA, Ley 476 the carbon budget. Additionally, these bioherms are linked JA, Nagelkerken I, Serafy JE (2006) Nursery function of tropical 527 back-reef systems. Mar Ecol Prog Ser 318:287–301 528 477 to upwelling, so their up to 20 m-thick sediments may also 529 478 Almany GR, Connolly SR, Heath DD, Hogan JD, Jones GP, McCook preserve high-resolution records of palaeoclimate and LJ, Mills M, Pressey RL, Williamson DH (2009) Connectivity, 530 479 palaeoceanography. biodiversity conservation and the design of marine reserve 531 480 The spatial distribution of the bioherms extends across a networks for coral reefs. Coral Reefs 28:339–351 532 Alvarez-Filip L, Dulvy NK, Gill JA, Coˆte´ IM, Watkinson AR (2009) 533 481 number of different GBRMPA management zones and 534 482 Flattening of Caribbean coral reefs: region-wide declines in bioregions. Large portions of the new bioherm map lie architectural complexity. Proc R Soc Lond B Biol Sci 535 483 within the Marine National Park and Habitat Protection 276:3019–3025 536 484 zones. However, some regions fall within the General Use Andrews JC, Furnas MJ (1986) Subsurface intrusions of Coral Sea 537 water into the central Great Barrier Reef—I. Structures and 538 485 Zone (Fig. 4), where benthic trawling is permitted, poten- 539 486 shelf-scale dynamics. Cont Shelf Res 6:491–514 tially impacting the living Halimeda habitat and underlying Beaman R (2010) 3DGBR: A high-resolution depth model for the 540 487 structural complexity. There are inconsistencies in the Great Barrier Reef and Coral Sea. Marine and Tropical Sciences 541 488 GBRMPA-assigned bioregions across the Halimeda bio- Facility (MTSRF) Project 2 542 543 489 herms. For example, bioherm areas overlap both the Reef Blakeway D, Hamblin MG (2015) Self-generated morphology in lagoon reefs. Peer J 3:935 544 490 and the Non-Reef bioregion maps (GBRMPA 2009), and Braga JC, Martı´n JM, Riding R (1996) Internal structure of segment 545 491 the bioregion designated as Halimeda banks does not reefs: Halimeda algal mounds in the Mediterranean Miocene. 546 492 represent the actual Halimeda bioherm distribution; there- Geology 24:35–38 547 Davies PJ (2011) Halimeda bioherms. In: Hopley D (ed) Ency- AQ5548 493 fore, their classification remains unclear. Undoubtedly, 549 494 clopaedia of modern coral reefs: structure, form and process. coral reefs and Halimeda bioherms are very different Springer, Dordrecht, pp 539–549 550 495 habitats and need to be classified unambiguously to ensure Davies PJ, Marshall JF (1985) Halimeda bioherms—low energy reefs, 551 496 appropriate management and conservation. The boundaries Northern Great Barrier Reef. Proc 5th Int Coral Reef Congress 552 5:1–7 553 497 of protected areas may need to be reconsidered if these 554 498 Devlin M, Brodie J (2005) Terrestrial discharge into the Great Barrier important carbonateUNCORRECT sinks and inter-reef habitats are to be Reef Lagoon: nutrient behavior in coastal waters. Mar Pollut 555 499 conserved and maintained, ensuring resilience and Bull 51:9–22 556

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557 Drew EA (1983) Halimeda biomass, growth rates and sediment Phipps CV, Davies PJ, Hopley D (1985) The morphology of 620 558 generation on reefs in the central Great Barrier Reef province. Halimeda banks behind the Great Barrier Reef east of Cook- 621 559 Coral Reefs 2:101–110 town, QLD. Proc 5th Int Coral Reef Congress 5:27–30 622 560 Drew EA (1993) Production of geological structures by the green alga Phipps CVG, Roberts HH (1988) Seismic characteristics and 623 561 Halimeda. SPUMS J 23:93–102 accretion history of Halimeda bioherms on Kalukalukuang 624 562 Drew EA (2001) Ocean nutrients to sediment banks via tidal jets and Bank, eastern Java Sea (Indonesia). Coral Reefs 6:149–159 625 563 Halimeda meadows. In: Wolanski E (ed) Oceanographic Pitcher RC, Doherty PP, Arnold PP, Hooper JJ, Gribble NN (2007) 626 564 processes of coral reefs: physical and biological links in the Seabed biodiversity on the continental shelf of the Great Barrier 627 565 Great Barrier Reef. 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Elsevier, Palaeogeogr Palaeoclimatol Palaeoecol 331–332:75–89 663 601 Amsterdam Whiteway T, Smithers S, Potter A, Brooke B (2013) Geological and 664 602 Maxwell WGH (1973) Sediments of the Great Barrier Reef. In: Jones Geomorphological features of outstanding universal value in the 665 603 OA, Endean R (eds) Biology and geology of coral reefs. Great Barrier Reef World Heritage Area. Geoscience Australia 666 604 Academic, New York, pp 299–345 Wolanski E, Ruddick B (1981) Water circulation and shelf waves in 667 605 Mumby PJ (2006) Connectivity of reef fish between mangroves and the northern Great Barrier Reef lagoon. Mar Freshw Res 668 606 coral reefs: algorithms for the design of marine reserves at 32:721–740 669 607 seascape scales. 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Proc 5th Int Coral Reef Symp 5:31–37 Wright D, Lundblad E, Larkin E, Rinehart R, Murphy J, Cary- 676 614 Orme GR, Salama MS (1988) Form and seismic stratigraphy of Kothera L, Draganov K (2005) ArcGIS Benthic Terrain AQ7677 615 Halimeda banks in part of the northern Great Barrier Reef Modeler, Corvallis, Oregon, Oregon State University, Davey 678 616 Province. Coral Reefs 6:131–137 Jones Locker Seafloor Mapping/Marine GIS Laboratory and 679 617AQ6 Orme GR, Flood PG, Sargent GEG (1978) Sedimentation trends in NOAA Coastal Services Center. http://www.csc.noaa.gov/pro 680 618 the lee of outer (ribbon) reefs, northern region of the Great ducts/btm 681 619 Barrier ReefUNCORRECT Province

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Author Proof Query Details Required Author’s Response AQ1 Please check and confirm that the authors and their respective affiliations have been correctly identified and amend if necessary. AQ2 Please check and confirm the street information is correctly identified for affiliation 2. AQ3 Kindly check and confirm the edit made in the Table 3 footer. AQ4 Kindly check and confirm the Electronic supplementary material is correctly identified. AQ5 Please check and confirm the publisher name is correctly identified for references Davies (2011), Purdy (1974). AQ6 Please provide the complete details for references Orme et al. (1978), Pitcher et al. (2007), Whiteway et al. (2013) AQ7 Please check and confirm the URL is correctly identified for reference Wright et al. (2005).