Hindawi Publishing CorporationJournal of Marine BiologyVolume 2013 Article ID 363894 8 pageshttpdxdoiorg1011552013363894

Research ArticleNew Records of Atypical Coral Reef Habitat inthe Kimberley Australia

Z T Richards M Bryce and C Bryce

Aquatic Zoology West Australian Museum Locked Bag 49 Welshpool DC WA 6986 Australia

Correspondence should be addressed to Z T Richards zoerichardsmuseumwagovau

Received 17 January 2013 Accepted 13 March 2013

Academic Editor Jakov Dulcic

Copyright copy 2013 Z T Richards et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

New surveys of the Kimberley Nearshore Bioregion are beginning to fill knowledge gaps about the regionrsquos marine biodiversityand the national and international conservation significance of this little-known tropical reef system Here we report the recentfinding of two unique coral habitats documented at Adele Island and Long Reef during theWoodside 20092010 Collection Projectsurveys Firstly we report the finding of a subtidal zone of mixed corallith and rhodolith habitat which appears on current recordsto be unprecedented in Australia Secondly we report the discovery of an atypical Organ Pipe Coral habitat zone and provideempirical evidence that this commercially valuable species reaches an unparalleled level of benthic cover We provide additionaldetails about the wider hard and soft coral assemblages associated with these unique habitats discuss the potential biological causesand consequences of them and make recommendations to benefit their conservation

1 Introduction

Around the globe most tropical reef locations have beenthe focus of at least some scientific studies One of the lastregions of shallow-water reef remaining to be explored is theKimberley (north-west Australia) Renowned for huge tidalexchanges up to 11m frequent cyclones and crocodiles thisregion has experienced little reef-based research apart froma series of biodiversity surveys conducted by the WesternAustralian Museum in the 1990s Despite the growing publicand industrial interest in this frontier region the diversity ofthe tropical Kimberley reefs remains largely unknown evenat the coarse habitat level

Geomorphological surveys of reef development in West-ern Australia suggest that reefs in the Kimberley coastalbioregion are uniquely characterized by the developmentof Holocene accretionary veneers of coral-algal limestone(gt12000 years old) on a Proterozoic basement (2500ndash543million years old) [1] Neighbouring reefs on the north-west shelf (ie within the Western Pilbara and West CoastBioregions) have origins in the Pleistocene (25 millionndash12000 years ago)Thus contemporary reefs in the Kimberley

appear to have more recent origins than others in WesternAustralia however the extent to which the difference in agetranslates to compositional differences between reefs remainsto be resolved

Along the Kimberley continental edge there is extensivedevelopment of oceanic reefs The offshore reefs (such asAshmore Cartier and Scott Reefs) have been extensivelysurveyed as part of National and Regional managementplans [2ndash9] and contain a surprising diversity of marinelife given their isolation including a high diversity of hardand soft corals Despite forming a separate and distinctbioregion to the Oceanic Shoals [10 11] only occasionalcoral collecting has been conducted within the nearshoreKimberley bioregion [12]

To address this information gap a new project beganin 2008 intended to quantify the diversity distribution andabundance of hard and soft corals along the Kimberley coastwith that of other marine fauna and flora The WoodsideCollection Project (Kimberley) 2008ndash2011 (henceforth theWoodside Project) (httpwwwmuseumwagovaukimber-leymarine-life-kimberley-region) will combine inshore andoffshore data to fill various important biogeographic and

2 Journal of Marine Biology

taxonomic knowledge gaps This will help define the currentknowledge concerning the regionrsquos biodiversity to aid conser-vation managers industry and government in establishingthe national and international conservation significance ofthe region

Herewe describe two unusual benthic habitats discoveredduring theWoodside 4Project surveys in 2009 atAdele Islandand in 2010 at Long Reef We will also discuss their potentialbiological causes consequences and significance and makerecommendations to benefit their conservation

2 Methods

21 Site Description Adele Island (15∘3131015840S 123∘9501015840E) issituated approximately 90 kms from the coastline on theinner section of the north-west shelf Approximately 17 kmlong and 9 km wide Adele is a true reef platform with avegetated centre The reef is considered one of the largestand mature of the Sahul Shelf [13] Wilson [14] describesthe reef platform as ldquoa bioherm [whose] top is a cap ofQuaternary reefal limestone built on an inundated rocky hillof the dissected Kimberley Basis margin over a Proterozoicbasementrdquo Prevailing westerly wind swell and diurnal tideswith up to 11m range on high-water springs have shapedthe intertidal reef platform (rampart) that is heavily etchedwith small drainage channels and low widely spaced ridgesrunning parallel to the reef edge that resemble a series oflong low andwide corrugations Beyond the rampart the reefslopes into sublittoral fore-reef and back-reef zones featuringhard corals soft corals hydroids bryozoans and macroalgaesuch as Sargassum

Long Reef (15∘5651015840S 124∘12510158401015840E) is situated approxi-mately 28 kms from the coastline also on the inner part ofthe NW Sahul Shelf It is a north-south orientated elongatedplatform reef that is approximately 27 km long and 12 kmwide with a similar geological history to Adele Island It wasbuilt on antecedent Proterozoic features that are remnants oftopographic high points of the submerged Kimberley Basinmargin [14] Contemporary reef growth is controlled bywindswell and extreme tidal exchanges Long Reef features alarge intertidal reef pavement zone resembling others in theinshore Kimberley such as Adele but in contrast to Adele anisland has not formedThere is however a central sandy spinerunning down the centre of the reef The flat midlittoral reefpavement is covered with turf algae and tide pools which arefringed with small coral colonies The reef pavement extendsdown to a narrow honeycombed and terraced fore-reef rampthat forms small drainage cascades resembling the low tidecascades of Montgomery Reef [15] Subtidally there is a steepfore-reef slope that descends beyond the 20m contour and afractured reef base with hard corals sponges hydroids andother fauna and flora The reef on the leeward side is gentlysloping

22 Field Surveys Hard and soft coral biodiversity at AdeleIsland and Long Reef (Figure 1) were surveyed for thefirst time using standard benthic monitoring techniquesAt Adele Island 13 stations were surveyed in October 2009

KimberleyWestern Australia

Broome

Long Reef

Adele Island

Figure 1 Map of the Kimberley coastline marking the location ofAdele Island and Long Reef

Adele Island-2009 survey stations

08K09

09K09

10K09

13K09

12K09 11K09

01K0903K09

02K09

04K09

07K09

05K09

06K09

lowast

Figure 2 Satellite image of the extensive coral reef surroundingAdele Island with survey stations highlighted the rollolith habitatzone is denoted by a star

(Figure 2) Eleven stations were surveyed using SCUBA andtwo intertidal stationswere surveyed At LongReef 15 stationswere surveyed in October 2010 (Figure 3) nine stations usingSCUBA and six stations were intertidal

The mean species richness (+SE) of hard corals wascalculated at each station from four replicated 15mtimes 1mwide

Journal of Marine Biology 3

Long Reef-2010 survey stations

53K1055K10

52K1047K1048K10

54K10

46K10

49K10

50K10

51K10

57K10

56K10

43K10

44K1045K10

lowast

Figure 3 Satellite image of Long Reef with survey stations high-lighted the Tubipora habitat denoted by a star

coral biodiversity belt transects In addition a 20-minuterapid visual search over the station (covering approximately1000m2) was conducted to detect rare and infrequent speciesThe total hard coral assemblage at each station was docu-mented from pooled transect and rapid visual assessmentrecords For soft corals a 60-minute rapid visual search wasconducted over each station to obtain a thorough list of thesoft coral assemblage

In addition during the spring low tide of the 24thOctober 2010 six 10m long point intercept transects wereconducted in the exposed fore-reef ramp to quantify thebenthic coverage of Tubipora sp Our intention here is todescribe two unusual benthic habitats that were encounteredon these expeditions in an ecological context and articulatethe extent of surveying we have conducted at these inshoreKimberley locations in order to establish the prevalence andsignificance of the new habitats

3 Results

31 Coralliths and Rhodoliths Intertidal and subtidal surveysof Adele Island revealed extensive development of hard andsoft coral communities Seventy-eight species of scleractiniancoral were recorded in intertidal and shallow water stations(lt6m depth) The level of hard coral diversity increased to176 species with additional surveying at subtidal sites (gt14mdepth) These records indicate that approximately half ofall the hard coral species currently known to occur in theoffshore and inshore Kimberley bioregions are present atAdele Island [16]

Octocoral biodiversity in intertidal and shallow waterstations under 6mdepthwas species poor increasing consid-erably with greater depth Only four species of octocoral wererecorded in habitats under 6m depth (Heliopora coeruleaLobophytum sp and Anthelia sp Sansibia sp) whereas 28species were recorded at a depth of 6m to 14m

At station 10K9 on the south west side of Adele Island acurious zone of benthic fauna was observed at the southernedge This station was in lt4m depth on the midlittoral backreef It was a high energy current swept consolidated reefplatform with many depressions leading to a labyrinth ofunderplatform tunnels The depressions contained coursesand and coral rubble Fifty-five species of hermatypic coralwere recorded at this station with the five most commonlyencountered species on transects beingGoniastrea retiformisAcropora papillare Favites halicora Goniastrea pectinata andPorites annae Within the Alcyonaria only the blue coralHeliopora coerulea and one species of Anthelia sp wererecorded

At the southern edge of station 10K9 the consolidatedhabitat gave way to a rubble bed This was dominated by amixed assemblage of coralliths (free-living live coral nodules)and rhodoliths (free-living balls of coralline algae) (hereincalled the rhollolith zone sensu Baarli 2010mdashwhere rollolithrefers to motile balls of mixed origin ie coral algaepolychaete or bryozoan) Among the coralliths four differentspecies of coral were identified (Pavona venosa Psammocoraprofundacella Cyphastrea chalcidicum and Millepora sp)(Figures 4(a) 4(b) and 4(d))Milleporinid corallithswere themost abundant and between 3 and 5 coralliths of the othergenera were observed within the section of the rollolith zonethat was examined The maximum size of the coralliths was12 cm (greater diameter)

Rhodoliths (Figure 4(c)) dominated the assemblage inthe rollolith zone and covered the substrate The largestrhodolith recorded was 8 cm (greater diameter) Generallythe rhodoliths formed as a cluster of short (gt1 cm) densebranches some of which appeared to be formed around coralrubble or shells others appeared to be entirely of algal origin

32 Long Reef Tubipora Intertidal and subtidal surveys atLong Reef revealed extensive development of hard coraland soft coral communities Preliminary systematic studiesindicate 200 species of scleractinian corals occur at LongReef 68 of which occur in the intertidal zone Octocoralbiodiversity followed the same trend as Adele Island with lowbiodiversity in intertidal and shallow water stations under6mdepth and increasing to 29 species between 6mand 14m

During a spring low tide surveys of Long Reef weencountered an atypical habitat zone dominated by theOrganPipe Coral Tubipora sp on the reef platform borderingstation 56K10 (Figures 5(a) and 5(b)) The platform was onthe south west side of Long Reef and featured many tidepools and a covering of algal turf The platform extendeddown to a narrow honeycombed fore-reef ramp that wasterraced forming small drainage waterfalls Numerous blow-holes occurred along the edge of the reef however these wereonly evident for a short duration over the lowest point of thetide

4 Journal of Marine Biology

(a) (b)

(c) (d)

Figure 4 Rolloliths collected from Adele Island (a) Cyphastrea chalcidicum corallith (b) Pavona venosa corallith (c) Red coralline algaerhodolith (d) Milleporina corallith Skeletal photos Roger Springthorpe Australian Museum

(a) (b)

Figure 5 Organ Pipe Coral at Long Reef (a) A single colony of Organ Pipe Coral (Tubipora sp) (b) The narrow fore-reef habitat on thewestern side of Long Reef showing the prolific development of Tubipora as the tide advances

Point-intercept transects conducted to quantify the per-cent cover of Tubipora in the zone verified that Tubiporawas the dominant benthic organism with a mean of 2767(plusmn324 SE) cover Turf algae (22 plusmn 549 SE) sandrubble(18 plusmn 426 SE) and coralline algae (9 plusmn 25 SE) inhabitedthe majority of the remaining space Ten other genera ofscleractinian coral were recorded on benthic cover transectswithin this habitat (Platygyra Acropora Goniastrea FaviaFavites Galaxea Symphyllia Goniopora Seriatopora andPorites) however their combined coverage was lt20 Sixadditional species of octocorallia were recorded within thisTubipora habitat zone (Heliopora coerulea Lobophytum sp

Cladiella sp Capnella sp Xenia sp and Briareum sp) aswell as a small number of sponges and hydroids

4 Discussion

41 Rolloliths Free-living spheroidal corals (ie coralliths)were first noted from shallow tropical reef environments inVanuatu and Indonesia in the late 1800s [17] and palaeon-tological studies have dated coralliths back to the Eocene(approx 65 mya [18])Throughout the 70s numerous papersarose concerning coralliths conferring they occur rightacross the globe from Bermuda toMadagasgar [19 20] More

Journal of Marine Biology 5

recently assemblages of coralliths have been recorded in theCook Islands [21] Barbados [22] the North West IndianOcean [23] Galapagos [24] Mexico and the Red Sea [25]In Australian waters there are currently only isolated recordsof coralliths For example Porites lutea has been observed toformmotile balls on the depositional reef flats atHeron Island[26] and Cyphastrea microphthalma forms motile balls at theCocos Islands [27]

The largest corallith encountered at Adele Island was acolony of Pavona venosawhichwas 12 cm (greatest diameter)This is small in comparison to the normal size of this specieswhich has the potential to grow to at least 1m (greatestdiameter) when attached to the substrate Coralliths are likelyto be size restricted because if they grow too large they wouldbecome partially or completely buried It is also worthwhilenoting that no attached forms of the four corallith specieswere recorded at station 10K9 however these four coralspecies were encountered in low abundance at other AdeleIsland stations

Rhodolith beds however are very widespread They aredistributed from the poles to the tropics and can accumulateto form extensive communities on awide variety of sedimentsin both deep and shallow water [28 29] The largest bedsreported are on the Brazilian Shelf spanning 23 degrees oflatitude [28 30 31] In Brazil rhodoliths are so abundantthey are commercially mined [32] Numerous studies havereported that rhodolith beds are important ecologicallybecause they support a high diversity of associated flora andinfauna [28 33ndash35]

InAustralia rhodolith beds are also relativelywidespreadoccurring offWesternAustralia [36] in cold-temperatewatersof southernAustralia [37] and in southernQueenslandwherethey cover up to 50 of the sea-floor from 50 to 110m depth[38] A study conducted at Montgomery Reef in the Kim-berley describes rhodoliths as being important contemporaryreef builders [15] Rhodoliths are reportedly so abundant atMontgomery Reef that they form containment banks whichimpound a raised lagoonal habitat the water from whichfeeds the unique system of low-tide cascades Some of theMontgomery Reef rhodoliths have a core of coral fragmentbutmany are constructed entirely of algae Similarly on SouthTurtle Reef in Talbot Bay (inshore Kimberley) rhodolithbanks form along the reef crest and enclose small pools thatretain water over the low tide [39]

While there are records of rhodoliths from the Kimberleythere are however no current records of coralliths (at Mont-gomery Reef Talbot Bay or any other Kimberley locations)Moreover there are no current records of Australian coralreef habitat featuring a mixed assemblage of living coralliths(from a variety of genera) and rhodoliths Thus the AdeleIsland fore-reef rollolith zone appears to be relatively rareTherefore our findings provide the first record of mixedcorallith and rhodolith habitat for the Kimberley coastalbioregion and also for Australia

Further taxonomic study is needed to confirm whichspecies of algae form the rhodolith community at AdeleIsland Nongeniculate coralline algae are considered to bechallenging to identify and at least eight genera belonging tothree families of Corallinales (Hapalidiaceae Corallinaceae

and Sporolithaceae) contain species that commonly formrhodoliths The rhololith bed off Western Port Victoria forexample is composed of four species (Hydrolithon rupestre(Foslie) Penrose Lithothamnion superpositum Foslie Meso-phyllum engelhartii (Foslie) Adey and Neogoniolithon bras-sica-florida (Harvey) Setchell and Mason) [37] so it is likelythat the Kimberley rhodolith beds also contains multiplespecies

The rolloliths of Adele Island most likely form in thelee of prevailing wave action as a cumulative responseto unidirectional currents and the tidal pull on surfacesediments This maintains periodic yet constant movementenabling persistent growth on all sides of the colony [21]Thefrequent disturbance of bottom sediments by browsing fishesand gastropods (bioturbation) has also been hypothesized tocontribute towards the unique spherical form [19 40 41]Holothurians and sea urchins have also been observed to aidin keeping coralliths and rhodoliths in motion [25]

42 Tubipora Tubipora sp is the only known hard calciticreef-building alcyonarian (soft) coral Its skeleton consists ofcalcite spicules fused into upright parallel tubes connectedby transverse platforms hence its common name of OrganPipe Coral Organ Pipe Coral is normally sporadic to rarethroughout its range which spans the Indo-Pacific fromthe Red Sea and East Africa to Southeast Asia MicronesiaAustralia and the Pacific [42] Tubipora has however beenobserved in large quantities near Rat Island off Gladstone inQueensland Australia (Philip Alderslade pers comm) andat an undisclosed location in Papua New Guinea [43] Thehighest published benthic coverage estimate ofTubipora sp is119 from one location in the Red Sea [44] Our quantitativedata showing 2767 (+324 SE) coverage of Tubipora at thisone Long Reef location suggests this is an exceptionally rarehigh density population

Tubipora was once thought to be a single ubiquitousspecies Tubipora musica Linnaeus 1758 (Family TubiporidaeOrder Stolonifera Class Anthozoa Phylum Cnidaria) how-ever there are now several nominal species of Tubipora Ourpreliminary systematic study has raised doubt about whichspecies of Tubipora is present in the Kimberley Hence fur-ther investigations based on grossmorphology of its skeletonandmolecular sequencing are necessary to confirm or refuteprior assumptions about the species identity In addition tothe required taxonomic research further biological researchis needed to understand the age growth rate reproductivebiology and molecular ecology of the Long Reef Tubiporain order to understand why they are so prevalent at thisparticular location

Shared among the various nominal species of Tubiporais the distinctive bright red colour of the skeleton Thered colouration is a result of organic pigments includingcarotenoids which give the orange colour to carrots and thered colour to cooked lobsters Carotenoids occur naturally inplants but are not manufactured by animals so it is likely theOrgan Pipe Coral assimilates the pigments via heterotrophicfeeding on phytoplankton Incorporating pigment into theskeleton is likely to serve the coral in two ways firstly itwould assist light absorption and maximize the potential for

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

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Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

2 Journal of Marine Biology

taxonomic knowledge gaps This will help define the currentknowledge concerning the regionrsquos biodiversity to aid conser-vation managers industry and government in establishingthe national and international conservation significance ofthe region

Herewe describe two unusual benthic habitats discoveredduring theWoodside 4Project surveys in 2009 atAdele Islandand in 2010 at Long Reef We will also discuss their potentialbiological causes consequences and significance and makerecommendations to benefit their conservation

2 Methods

21 Site Description Adele Island (15∘3131015840S 123∘9501015840E) issituated approximately 90 kms from the coastline on theinner section of the north-west shelf Approximately 17 kmlong and 9 km wide Adele is a true reef platform with avegetated centre The reef is considered one of the largestand mature of the Sahul Shelf [13] Wilson [14] describesthe reef platform as ldquoa bioherm [whose] top is a cap ofQuaternary reefal limestone built on an inundated rocky hillof the dissected Kimberley Basis margin over a Proterozoicbasementrdquo Prevailing westerly wind swell and diurnal tideswith up to 11m range on high-water springs have shapedthe intertidal reef platform (rampart) that is heavily etchedwith small drainage channels and low widely spaced ridgesrunning parallel to the reef edge that resemble a series oflong low andwide corrugations Beyond the rampart the reefslopes into sublittoral fore-reef and back-reef zones featuringhard corals soft corals hydroids bryozoans and macroalgaesuch as Sargassum

Long Reef (15∘5651015840S 124∘12510158401015840E) is situated approxi-mately 28 kms from the coastline also on the inner part ofthe NW Sahul Shelf It is a north-south orientated elongatedplatform reef that is approximately 27 km long and 12 kmwide with a similar geological history to Adele Island It wasbuilt on antecedent Proterozoic features that are remnants oftopographic high points of the submerged Kimberley Basinmargin [14] Contemporary reef growth is controlled bywindswell and extreme tidal exchanges Long Reef features alarge intertidal reef pavement zone resembling others in theinshore Kimberley such as Adele but in contrast to Adele anisland has not formedThere is however a central sandy spinerunning down the centre of the reef The flat midlittoral reefpavement is covered with turf algae and tide pools which arefringed with small coral colonies The reef pavement extendsdown to a narrow honeycombed and terraced fore-reef rampthat forms small drainage cascades resembling the low tidecascades of Montgomery Reef [15] Subtidally there is a steepfore-reef slope that descends beyond the 20m contour and afractured reef base with hard corals sponges hydroids andother fauna and flora The reef on the leeward side is gentlysloping

22 Field Surveys Hard and soft coral biodiversity at AdeleIsland and Long Reef (Figure 1) were surveyed for thefirst time using standard benthic monitoring techniquesAt Adele Island 13 stations were surveyed in October 2009

KimberleyWestern Australia

Broome

Long Reef

Adele Island

Figure 1 Map of the Kimberley coastline marking the location ofAdele Island and Long Reef

Adele Island-2009 survey stations

08K09

09K09

10K09

13K09

12K09 11K09

01K0903K09

02K09

04K09

07K09

05K09

06K09

lowast

Figure 2 Satellite image of the extensive coral reef surroundingAdele Island with survey stations highlighted the rollolith habitatzone is denoted by a star

(Figure 2) Eleven stations were surveyed using SCUBA andtwo intertidal stationswere surveyed At LongReef 15 stationswere surveyed in October 2010 (Figure 3) nine stations usingSCUBA and six stations were intertidal

The mean species richness (+SE) of hard corals wascalculated at each station from four replicated 15mtimes 1mwide

Journal of Marine Biology 3

Long Reef-2010 survey stations

53K1055K10

52K1047K1048K10

54K10

46K10

49K10

50K10

51K10

57K10

56K10

43K10

44K1045K10

lowast

Figure 3 Satellite image of Long Reef with survey stations high-lighted the Tubipora habitat denoted by a star

coral biodiversity belt transects In addition a 20-minuterapid visual search over the station (covering approximately1000m2) was conducted to detect rare and infrequent speciesThe total hard coral assemblage at each station was docu-mented from pooled transect and rapid visual assessmentrecords For soft corals a 60-minute rapid visual search wasconducted over each station to obtain a thorough list of thesoft coral assemblage

In addition during the spring low tide of the 24thOctober 2010 six 10m long point intercept transects wereconducted in the exposed fore-reef ramp to quantify thebenthic coverage of Tubipora sp Our intention here is todescribe two unusual benthic habitats that were encounteredon these expeditions in an ecological context and articulatethe extent of surveying we have conducted at these inshoreKimberley locations in order to establish the prevalence andsignificance of the new habitats

3 Results

31 Coralliths and Rhodoliths Intertidal and subtidal surveysof Adele Island revealed extensive development of hard andsoft coral communities Seventy-eight species of scleractiniancoral were recorded in intertidal and shallow water stations(lt6m depth) The level of hard coral diversity increased to176 species with additional surveying at subtidal sites (gt14mdepth) These records indicate that approximately half ofall the hard coral species currently known to occur in theoffshore and inshore Kimberley bioregions are present atAdele Island [16]

Octocoral biodiversity in intertidal and shallow waterstations under 6mdepthwas species poor increasing consid-erably with greater depth Only four species of octocoral wererecorded in habitats under 6m depth (Heliopora coeruleaLobophytum sp and Anthelia sp Sansibia sp) whereas 28species were recorded at a depth of 6m to 14m

At station 10K9 on the south west side of Adele Island acurious zone of benthic fauna was observed at the southernedge This station was in lt4m depth on the midlittoral backreef It was a high energy current swept consolidated reefplatform with many depressions leading to a labyrinth ofunderplatform tunnels The depressions contained coursesand and coral rubble Fifty-five species of hermatypic coralwere recorded at this station with the five most commonlyencountered species on transects beingGoniastrea retiformisAcropora papillare Favites halicora Goniastrea pectinata andPorites annae Within the Alcyonaria only the blue coralHeliopora coerulea and one species of Anthelia sp wererecorded

At the southern edge of station 10K9 the consolidatedhabitat gave way to a rubble bed This was dominated by amixed assemblage of coralliths (free-living live coral nodules)and rhodoliths (free-living balls of coralline algae) (hereincalled the rhollolith zone sensu Baarli 2010mdashwhere rollolithrefers to motile balls of mixed origin ie coral algaepolychaete or bryozoan) Among the coralliths four differentspecies of coral were identified (Pavona venosa Psammocoraprofundacella Cyphastrea chalcidicum and Millepora sp)(Figures 4(a) 4(b) and 4(d))Milleporinid corallithswere themost abundant and between 3 and 5 coralliths of the othergenera were observed within the section of the rollolith zonethat was examined The maximum size of the coralliths was12 cm (greater diameter)

Rhodoliths (Figure 4(c)) dominated the assemblage inthe rollolith zone and covered the substrate The largestrhodolith recorded was 8 cm (greater diameter) Generallythe rhodoliths formed as a cluster of short (gt1 cm) densebranches some of which appeared to be formed around coralrubble or shells others appeared to be entirely of algal origin

32 Long Reef Tubipora Intertidal and subtidal surveys atLong Reef revealed extensive development of hard coraland soft coral communities Preliminary systematic studiesindicate 200 species of scleractinian corals occur at LongReef 68 of which occur in the intertidal zone Octocoralbiodiversity followed the same trend as Adele Island with lowbiodiversity in intertidal and shallow water stations under6mdepth and increasing to 29 species between 6mand 14m

During a spring low tide surveys of Long Reef weencountered an atypical habitat zone dominated by theOrganPipe Coral Tubipora sp on the reef platform borderingstation 56K10 (Figures 5(a) and 5(b)) The platform was onthe south west side of Long Reef and featured many tidepools and a covering of algal turf The platform extendeddown to a narrow honeycombed fore-reef ramp that wasterraced forming small drainage waterfalls Numerous blow-holes occurred along the edge of the reef however these wereonly evident for a short duration over the lowest point of thetide

4 Journal of Marine Biology

(a) (b)

(c) (d)

Figure 4 Rolloliths collected from Adele Island (a) Cyphastrea chalcidicum corallith (b) Pavona venosa corallith (c) Red coralline algaerhodolith (d) Milleporina corallith Skeletal photos Roger Springthorpe Australian Museum

(a) (b)

Figure 5 Organ Pipe Coral at Long Reef (a) A single colony of Organ Pipe Coral (Tubipora sp) (b) The narrow fore-reef habitat on thewestern side of Long Reef showing the prolific development of Tubipora as the tide advances

Point-intercept transects conducted to quantify the per-cent cover of Tubipora in the zone verified that Tubiporawas the dominant benthic organism with a mean of 2767(plusmn324 SE) cover Turf algae (22 plusmn 549 SE) sandrubble(18 plusmn 426 SE) and coralline algae (9 plusmn 25 SE) inhabitedthe majority of the remaining space Ten other genera ofscleractinian coral were recorded on benthic cover transectswithin this habitat (Platygyra Acropora Goniastrea FaviaFavites Galaxea Symphyllia Goniopora Seriatopora andPorites) however their combined coverage was lt20 Sixadditional species of octocorallia were recorded within thisTubipora habitat zone (Heliopora coerulea Lobophytum sp

Cladiella sp Capnella sp Xenia sp and Briareum sp) aswell as a small number of sponges and hydroids

4 Discussion

41 Rolloliths Free-living spheroidal corals (ie coralliths)were first noted from shallow tropical reef environments inVanuatu and Indonesia in the late 1800s [17] and palaeon-tological studies have dated coralliths back to the Eocene(approx 65 mya [18])Throughout the 70s numerous papersarose concerning coralliths conferring they occur rightacross the globe from Bermuda toMadagasgar [19 20] More

Journal of Marine Biology 5

recently assemblages of coralliths have been recorded in theCook Islands [21] Barbados [22] the North West IndianOcean [23] Galapagos [24] Mexico and the Red Sea [25]In Australian waters there are currently only isolated recordsof coralliths For example Porites lutea has been observed toformmotile balls on the depositional reef flats atHeron Island[26] and Cyphastrea microphthalma forms motile balls at theCocos Islands [27]

The largest corallith encountered at Adele Island was acolony of Pavona venosawhichwas 12 cm (greatest diameter)This is small in comparison to the normal size of this specieswhich has the potential to grow to at least 1m (greatestdiameter) when attached to the substrate Coralliths are likelyto be size restricted because if they grow too large they wouldbecome partially or completely buried It is also worthwhilenoting that no attached forms of the four corallith specieswere recorded at station 10K9 however these four coralspecies were encountered in low abundance at other AdeleIsland stations

Rhodolith beds however are very widespread They aredistributed from the poles to the tropics and can accumulateto form extensive communities on awide variety of sedimentsin both deep and shallow water [28 29] The largest bedsreported are on the Brazilian Shelf spanning 23 degrees oflatitude [28 30 31] In Brazil rhodoliths are so abundantthey are commercially mined [32] Numerous studies havereported that rhodolith beds are important ecologicallybecause they support a high diversity of associated flora andinfauna [28 33ndash35]

InAustralia rhodolith beds are also relativelywidespreadoccurring offWesternAustralia [36] in cold-temperatewatersof southernAustralia [37] and in southernQueenslandwherethey cover up to 50 of the sea-floor from 50 to 110m depth[38] A study conducted at Montgomery Reef in the Kim-berley describes rhodoliths as being important contemporaryreef builders [15] Rhodoliths are reportedly so abundant atMontgomery Reef that they form containment banks whichimpound a raised lagoonal habitat the water from whichfeeds the unique system of low-tide cascades Some of theMontgomery Reef rhodoliths have a core of coral fragmentbutmany are constructed entirely of algae Similarly on SouthTurtle Reef in Talbot Bay (inshore Kimberley) rhodolithbanks form along the reef crest and enclose small pools thatretain water over the low tide [39]

While there are records of rhodoliths from the Kimberleythere are however no current records of coralliths (at Mont-gomery Reef Talbot Bay or any other Kimberley locations)Moreover there are no current records of Australian coralreef habitat featuring a mixed assemblage of living coralliths(from a variety of genera) and rhodoliths Thus the AdeleIsland fore-reef rollolith zone appears to be relatively rareTherefore our findings provide the first record of mixedcorallith and rhodolith habitat for the Kimberley coastalbioregion and also for Australia

Further taxonomic study is needed to confirm whichspecies of algae form the rhodolith community at AdeleIsland Nongeniculate coralline algae are considered to bechallenging to identify and at least eight genera belonging tothree families of Corallinales (Hapalidiaceae Corallinaceae

and Sporolithaceae) contain species that commonly formrhodoliths The rhololith bed off Western Port Victoria forexample is composed of four species (Hydrolithon rupestre(Foslie) Penrose Lithothamnion superpositum Foslie Meso-phyllum engelhartii (Foslie) Adey and Neogoniolithon bras-sica-florida (Harvey) Setchell and Mason) [37] so it is likelythat the Kimberley rhodolith beds also contains multiplespecies

The rolloliths of Adele Island most likely form in thelee of prevailing wave action as a cumulative responseto unidirectional currents and the tidal pull on surfacesediments This maintains periodic yet constant movementenabling persistent growth on all sides of the colony [21]Thefrequent disturbance of bottom sediments by browsing fishesand gastropods (bioturbation) has also been hypothesized tocontribute towards the unique spherical form [19 40 41]Holothurians and sea urchins have also been observed to aidin keeping coralliths and rhodoliths in motion [25]

42 Tubipora Tubipora sp is the only known hard calciticreef-building alcyonarian (soft) coral Its skeleton consists ofcalcite spicules fused into upright parallel tubes connectedby transverse platforms hence its common name of OrganPipe Coral Organ Pipe Coral is normally sporadic to rarethroughout its range which spans the Indo-Pacific fromthe Red Sea and East Africa to Southeast Asia MicronesiaAustralia and the Pacific [42] Tubipora has however beenobserved in large quantities near Rat Island off Gladstone inQueensland Australia (Philip Alderslade pers comm) andat an undisclosed location in Papua New Guinea [43] Thehighest published benthic coverage estimate ofTubipora sp is119 from one location in the Red Sea [44] Our quantitativedata showing 2767 (+324 SE) coverage of Tubipora at thisone Long Reef location suggests this is an exceptionally rarehigh density population

Tubipora was once thought to be a single ubiquitousspecies Tubipora musica Linnaeus 1758 (Family TubiporidaeOrder Stolonifera Class Anthozoa Phylum Cnidaria) how-ever there are now several nominal species of Tubipora Ourpreliminary systematic study has raised doubt about whichspecies of Tubipora is present in the Kimberley Hence fur-ther investigations based on grossmorphology of its skeletonandmolecular sequencing are necessary to confirm or refuteprior assumptions about the species identity In addition tothe required taxonomic research further biological researchis needed to understand the age growth rate reproductivebiology and molecular ecology of the Long Reef Tubiporain order to understand why they are so prevalent at thisparticular location

Shared among the various nominal species of Tubiporais the distinctive bright red colour of the skeleton Thered colouration is a result of organic pigments includingcarotenoids which give the orange colour to carrots and thered colour to cooked lobsters Carotenoids occur naturally inplants but are not manufactured by animals so it is likely theOrgan Pipe Coral assimilates the pigments via heterotrophicfeeding on phytoplankton Incorporating pigment into theskeleton is likely to serve the coral in two ways firstly itwould assist light absorption and maximize the potential for

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

Journal of Marine Biology 3

Long Reef-2010 survey stations

53K1055K10

52K1047K1048K10

54K10

46K10

49K10

50K10

51K10

57K10

56K10

43K10

44K1045K10

lowast

Figure 3 Satellite image of Long Reef with survey stations high-lighted the Tubipora habitat denoted by a star

coral biodiversity belt transects In addition a 20-minuterapid visual search over the station (covering approximately1000m2) was conducted to detect rare and infrequent speciesThe total hard coral assemblage at each station was docu-mented from pooled transect and rapid visual assessmentrecords For soft corals a 60-minute rapid visual search wasconducted over each station to obtain a thorough list of thesoft coral assemblage

In addition during the spring low tide of the 24thOctober 2010 six 10m long point intercept transects wereconducted in the exposed fore-reef ramp to quantify thebenthic coverage of Tubipora sp Our intention here is todescribe two unusual benthic habitats that were encounteredon these expeditions in an ecological context and articulatethe extent of surveying we have conducted at these inshoreKimberley locations in order to establish the prevalence andsignificance of the new habitats

3 Results

31 Coralliths and Rhodoliths Intertidal and subtidal surveysof Adele Island revealed extensive development of hard andsoft coral communities Seventy-eight species of scleractiniancoral were recorded in intertidal and shallow water stations(lt6m depth) The level of hard coral diversity increased to176 species with additional surveying at subtidal sites (gt14mdepth) These records indicate that approximately half ofall the hard coral species currently known to occur in theoffshore and inshore Kimberley bioregions are present atAdele Island [16]

Octocoral biodiversity in intertidal and shallow waterstations under 6mdepthwas species poor increasing consid-erably with greater depth Only four species of octocoral wererecorded in habitats under 6m depth (Heliopora coeruleaLobophytum sp and Anthelia sp Sansibia sp) whereas 28species were recorded at a depth of 6m to 14m

At station 10K9 on the south west side of Adele Island acurious zone of benthic fauna was observed at the southernedge This station was in lt4m depth on the midlittoral backreef It was a high energy current swept consolidated reefplatform with many depressions leading to a labyrinth ofunderplatform tunnels The depressions contained coursesand and coral rubble Fifty-five species of hermatypic coralwere recorded at this station with the five most commonlyencountered species on transects beingGoniastrea retiformisAcropora papillare Favites halicora Goniastrea pectinata andPorites annae Within the Alcyonaria only the blue coralHeliopora coerulea and one species of Anthelia sp wererecorded

At the southern edge of station 10K9 the consolidatedhabitat gave way to a rubble bed This was dominated by amixed assemblage of coralliths (free-living live coral nodules)and rhodoliths (free-living balls of coralline algae) (hereincalled the rhollolith zone sensu Baarli 2010mdashwhere rollolithrefers to motile balls of mixed origin ie coral algaepolychaete or bryozoan) Among the coralliths four differentspecies of coral were identified (Pavona venosa Psammocoraprofundacella Cyphastrea chalcidicum and Millepora sp)(Figures 4(a) 4(b) and 4(d))Milleporinid corallithswere themost abundant and between 3 and 5 coralliths of the othergenera were observed within the section of the rollolith zonethat was examined The maximum size of the coralliths was12 cm (greater diameter)

Rhodoliths (Figure 4(c)) dominated the assemblage inthe rollolith zone and covered the substrate The largestrhodolith recorded was 8 cm (greater diameter) Generallythe rhodoliths formed as a cluster of short (gt1 cm) densebranches some of which appeared to be formed around coralrubble or shells others appeared to be entirely of algal origin

32 Long Reef Tubipora Intertidal and subtidal surveys atLong Reef revealed extensive development of hard coraland soft coral communities Preliminary systematic studiesindicate 200 species of scleractinian corals occur at LongReef 68 of which occur in the intertidal zone Octocoralbiodiversity followed the same trend as Adele Island with lowbiodiversity in intertidal and shallow water stations under6mdepth and increasing to 29 species between 6mand 14m

During a spring low tide surveys of Long Reef weencountered an atypical habitat zone dominated by theOrganPipe Coral Tubipora sp on the reef platform borderingstation 56K10 (Figures 5(a) and 5(b)) The platform was onthe south west side of Long Reef and featured many tidepools and a covering of algal turf The platform extendeddown to a narrow honeycombed fore-reef ramp that wasterraced forming small drainage waterfalls Numerous blow-holes occurred along the edge of the reef however these wereonly evident for a short duration over the lowest point of thetide

4 Journal of Marine Biology

(a) (b)

(c) (d)

Figure 4 Rolloliths collected from Adele Island (a) Cyphastrea chalcidicum corallith (b) Pavona venosa corallith (c) Red coralline algaerhodolith (d) Milleporina corallith Skeletal photos Roger Springthorpe Australian Museum

(a) (b)

Figure 5 Organ Pipe Coral at Long Reef (a) A single colony of Organ Pipe Coral (Tubipora sp) (b) The narrow fore-reef habitat on thewestern side of Long Reef showing the prolific development of Tubipora as the tide advances

Point-intercept transects conducted to quantify the per-cent cover of Tubipora in the zone verified that Tubiporawas the dominant benthic organism with a mean of 2767(plusmn324 SE) cover Turf algae (22 plusmn 549 SE) sandrubble(18 plusmn 426 SE) and coralline algae (9 plusmn 25 SE) inhabitedthe majority of the remaining space Ten other genera ofscleractinian coral were recorded on benthic cover transectswithin this habitat (Platygyra Acropora Goniastrea FaviaFavites Galaxea Symphyllia Goniopora Seriatopora andPorites) however their combined coverage was lt20 Sixadditional species of octocorallia were recorded within thisTubipora habitat zone (Heliopora coerulea Lobophytum sp

Cladiella sp Capnella sp Xenia sp and Briareum sp) aswell as a small number of sponges and hydroids

4 Discussion

41 Rolloliths Free-living spheroidal corals (ie coralliths)were first noted from shallow tropical reef environments inVanuatu and Indonesia in the late 1800s [17] and palaeon-tological studies have dated coralliths back to the Eocene(approx 65 mya [18])Throughout the 70s numerous papersarose concerning coralliths conferring they occur rightacross the globe from Bermuda toMadagasgar [19 20] More

Journal of Marine Biology 5

recently assemblages of coralliths have been recorded in theCook Islands [21] Barbados [22] the North West IndianOcean [23] Galapagos [24] Mexico and the Red Sea [25]In Australian waters there are currently only isolated recordsof coralliths For example Porites lutea has been observed toformmotile balls on the depositional reef flats atHeron Island[26] and Cyphastrea microphthalma forms motile balls at theCocos Islands [27]

The largest corallith encountered at Adele Island was acolony of Pavona venosawhichwas 12 cm (greatest diameter)This is small in comparison to the normal size of this specieswhich has the potential to grow to at least 1m (greatestdiameter) when attached to the substrate Coralliths are likelyto be size restricted because if they grow too large they wouldbecome partially or completely buried It is also worthwhilenoting that no attached forms of the four corallith specieswere recorded at station 10K9 however these four coralspecies were encountered in low abundance at other AdeleIsland stations

Rhodolith beds however are very widespread They aredistributed from the poles to the tropics and can accumulateto form extensive communities on awide variety of sedimentsin both deep and shallow water [28 29] The largest bedsreported are on the Brazilian Shelf spanning 23 degrees oflatitude [28 30 31] In Brazil rhodoliths are so abundantthey are commercially mined [32] Numerous studies havereported that rhodolith beds are important ecologicallybecause they support a high diversity of associated flora andinfauna [28 33ndash35]

InAustralia rhodolith beds are also relativelywidespreadoccurring offWesternAustralia [36] in cold-temperatewatersof southernAustralia [37] and in southernQueenslandwherethey cover up to 50 of the sea-floor from 50 to 110m depth[38] A study conducted at Montgomery Reef in the Kim-berley describes rhodoliths as being important contemporaryreef builders [15] Rhodoliths are reportedly so abundant atMontgomery Reef that they form containment banks whichimpound a raised lagoonal habitat the water from whichfeeds the unique system of low-tide cascades Some of theMontgomery Reef rhodoliths have a core of coral fragmentbutmany are constructed entirely of algae Similarly on SouthTurtle Reef in Talbot Bay (inshore Kimberley) rhodolithbanks form along the reef crest and enclose small pools thatretain water over the low tide [39]

While there are records of rhodoliths from the Kimberleythere are however no current records of coralliths (at Mont-gomery Reef Talbot Bay or any other Kimberley locations)Moreover there are no current records of Australian coralreef habitat featuring a mixed assemblage of living coralliths(from a variety of genera) and rhodoliths Thus the AdeleIsland fore-reef rollolith zone appears to be relatively rareTherefore our findings provide the first record of mixedcorallith and rhodolith habitat for the Kimberley coastalbioregion and also for Australia

Further taxonomic study is needed to confirm whichspecies of algae form the rhodolith community at AdeleIsland Nongeniculate coralline algae are considered to bechallenging to identify and at least eight genera belonging tothree families of Corallinales (Hapalidiaceae Corallinaceae

and Sporolithaceae) contain species that commonly formrhodoliths The rhololith bed off Western Port Victoria forexample is composed of four species (Hydrolithon rupestre(Foslie) Penrose Lithothamnion superpositum Foslie Meso-phyllum engelhartii (Foslie) Adey and Neogoniolithon bras-sica-florida (Harvey) Setchell and Mason) [37] so it is likelythat the Kimberley rhodolith beds also contains multiplespecies

The rolloliths of Adele Island most likely form in thelee of prevailing wave action as a cumulative responseto unidirectional currents and the tidal pull on surfacesediments This maintains periodic yet constant movementenabling persistent growth on all sides of the colony [21]Thefrequent disturbance of bottom sediments by browsing fishesand gastropods (bioturbation) has also been hypothesized tocontribute towards the unique spherical form [19 40 41]Holothurians and sea urchins have also been observed to aidin keeping coralliths and rhodoliths in motion [25]

42 Tubipora Tubipora sp is the only known hard calciticreef-building alcyonarian (soft) coral Its skeleton consists ofcalcite spicules fused into upright parallel tubes connectedby transverse platforms hence its common name of OrganPipe Coral Organ Pipe Coral is normally sporadic to rarethroughout its range which spans the Indo-Pacific fromthe Red Sea and East Africa to Southeast Asia MicronesiaAustralia and the Pacific [42] Tubipora has however beenobserved in large quantities near Rat Island off Gladstone inQueensland Australia (Philip Alderslade pers comm) andat an undisclosed location in Papua New Guinea [43] Thehighest published benthic coverage estimate ofTubipora sp is119 from one location in the Red Sea [44] Our quantitativedata showing 2767 (+324 SE) coverage of Tubipora at thisone Long Reef location suggests this is an exceptionally rarehigh density population

Tubipora was once thought to be a single ubiquitousspecies Tubipora musica Linnaeus 1758 (Family TubiporidaeOrder Stolonifera Class Anthozoa Phylum Cnidaria) how-ever there are now several nominal species of Tubipora Ourpreliminary systematic study has raised doubt about whichspecies of Tubipora is present in the Kimberley Hence fur-ther investigations based on grossmorphology of its skeletonandmolecular sequencing are necessary to confirm or refuteprior assumptions about the species identity In addition tothe required taxonomic research further biological researchis needed to understand the age growth rate reproductivebiology and molecular ecology of the Long Reef Tubiporain order to understand why they are so prevalent at thisparticular location

Shared among the various nominal species of Tubiporais the distinctive bright red colour of the skeleton Thered colouration is a result of organic pigments includingcarotenoids which give the orange colour to carrots and thered colour to cooked lobsters Carotenoids occur naturally inplants but are not manufactured by animals so it is likely theOrgan Pipe Coral assimilates the pigments via heterotrophicfeeding on phytoplankton Incorporating pigment into theskeleton is likely to serve the coral in two ways firstly itwould assist light absorption and maximize the potential for

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

4 Journal of Marine Biology

(a) (b)

(c) (d)

Figure 4 Rolloliths collected from Adele Island (a) Cyphastrea chalcidicum corallith (b) Pavona venosa corallith (c) Red coralline algaerhodolith (d) Milleporina corallith Skeletal photos Roger Springthorpe Australian Museum

(a) (b)

Figure 5 Organ Pipe Coral at Long Reef (a) A single colony of Organ Pipe Coral (Tubipora sp) (b) The narrow fore-reef habitat on thewestern side of Long Reef showing the prolific development of Tubipora as the tide advances

Point-intercept transects conducted to quantify the per-cent cover of Tubipora in the zone verified that Tubiporawas the dominant benthic organism with a mean of 2767(plusmn324 SE) cover Turf algae (22 plusmn 549 SE) sandrubble(18 plusmn 426 SE) and coralline algae (9 plusmn 25 SE) inhabitedthe majority of the remaining space Ten other genera ofscleractinian coral were recorded on benthic cover transectswithin this habitat (Platygyra Acropora Goniastrea FaviaFavites Galaxea Symphyllia Goniopora Seriatopora andPorites) however their combined coverage was lt20 Sixadditional species of octocorallia were recorded within thisTubipora habitat zone (Heliopora coerulea Lobophytum sp

Cladiella sp Capnella sp Xenia sp and Briareum sp) aswell as a small number of sponges and hydroids

4 Discussion

41 Rolloliths Free-living spheroidal corals (ie coralliths)were first noted from shallow tropical reef environments inVanuatu and Indonesia in the late 1800s [17] and palaeon-tological studies have dated coralliths back to the Eocene(approx 65 mya [18])Throughout the 70s numerous papersarose concerning coralliths conferring they occur rightacross the globe from Bermuda toMadagasgar [19 20] More

Journal of Marine Biology 5

recently assemblages of coralliths have been recorded in theCook Islands [21] Barbados [22] the North West IndianOcean [23] Galapagos [24] Mexico and the Red Sea [25]In Australian waters there are currently only isolated recordsof coralliths For example Porites lutea has been observed toformmotile balls on the depositional reef flats atHeron Island[26] and Cyphastrea microphthalma forms motile balls at theCocos Islands [27]

The largest corallith encountered at Adele Island was acolony of Pavona venosawhichwas 12 cm (greatest diameter)This is small in comparison to the normal size of this specieswhich has the potential to grow to at least 1m (greatestdiameter) when attached to the substrate Coralliths are likelyto be size restricted because if they grow too large they wouldbecome partially or completely buried It is also worthwhilenoting that no attached forms of the four corallith specieswere recorded at station 10K9 however these four coralspecies were encountered in low abundance at other AdeleIsland stations

Rhodolith beds however are very widespread They aredistributed from the poles to the tropics and can accumulateto form extensive communities on awide variety of sedimentsin both deep and shallow water [28 29] The largest bedsreported are on the Brazilian Shelf spanning 23 degrees oflatitude [28 30 31] In Brazil rhodoliths are so abundantthey are commercially mined [32] Numerous studies havereported that rhodolith beds are important ecologicallybecause they support a high diversity of associated flora andinfauna [28 33ndash35]

InAustralia rhodolith beds are also relativelywidespreadoccurring offWesternAustralia [36] in cold-temperatewatersof southernAustralia [37] and in southernQueenslandwherethey cover up to 50 of the sea-floor from 50 to 110m depth[38] A study conducted at Montgomery Reef in the Kim-berley describes rhodoliths as being important contemporaryreef builders [15] Rhodoliths are reportedly so abundant atMontgomery Reef that they form containment banks whichimpound a raised lagoonal habitat the water from whichfeeds the unique system of low-tide cascades Some of theMontgomery Reef rhodoliths have a core of coral fragmentbutmany are constructed entirely of algae Similarly on SouthTurtle Reef in Talbot Bay (inshore Kimberley) rhodolithbanks form along the reef crest and enclose small pools thatretain water over the low tide [39]

While there are records of rhodoliths from the Kimberleythere are however no current records of coralliths (at Mont-gomery Reef Talbot Bay or any other Kimberley locations)Moreover there are no current records of Australian coralreef habitat featuring a mixed assemblage of living coralliths(from a variety of genera) and rhodoliths Thus the AdeleIsland fore-reef rollolith zone appears to be relatively rareTherefore our findings provide the first record of mixedcorallith and rhodolith habitat for the Kimberley coastalbioregion and also for Australia

Further taxonomic study is needed to confirm whichspecies of algae form the rhodolith community at AdeleIsland Nongeniculate coralline algae are considered to bechallenging to identify and at least eight genera belonging tothree families of Corallinales (Hapalidiaceae Corallinaceae

and Sporolithaceae) contain species that commonly formrhodoliths The rhololith bed off Western Port Victoria forexample is composed of four species (Hydrolithon rupestre(Foslie) Penrose Lithothamnion superpositum Foslie Meso-phyllum engelhartii (Foslie) Adey and Neogoniolithon bras-sica-florida (Harvey) Setchell and Mason) [37] so it is likelythat the Kimberley rhodolith beds also contains multiplespecies

The rolloliths of Adele Island most likely form in thelee of prevailing wave action as a cumulative responseto unidirectional currents and the tidal pull on surfacesediments This maintains periodic yet constant movementenabling persistent growth on all sides of the colony [21]Thefrequent disturbance of bottom sediments by browsing fishesand gastropods (bioturbation) has also been hypothesized tocontribute towards the unique spherical form [19 40 41]Holothurians and sea urchins have also been observed to aidin keeping coralliths and rhodoliths in motion [25]

42 Tubipora Tubipora sp is the only known hard calciticreef-building alcyonarian (soft) coral Its skeleton consists ofcalcite spicules fused into upright parallel tubes connectedby transverse platforms hence its common name of OrganPipe Coral Organ Pipe Coral is normally sporadic to rarethroughout its range which spans the Indo-Pacific fromthe Red Sea and East Africa to Southeast Asia MicronesiaAustralia and the Pacific [42] Tubipora has however beenobserved in large quantities near Rat Island off Gladstone inQueensland Australia (Philip Alderslade pers comm) andat an undisclosed location in Papua New Guinea [43] Thehighest published benthic coverage estimate ofTubipora sp is119 from one location in the Red Sea [44] Our quantitativedata showing 2767 (+324 SE) coverage of Tubipora at thisone Long Reef location suggests this is an exceptionally rarehigh density population

Tubipora was once thought to be a single ubiquitousspecies Tubipora musica Linnaeus 1758 (Family TubiporidaeOrder Stolonifera Class Anthozoa Phylum Cnidaria) how-ever there are now several nominal species of Tubipora Ourpreliminary systematic study has raised doubt about whichspecies of Tubipora is present in the Kimberley Hence fur-ther investigations based on grossmorphology of its skeletonandmolecular sequencing are necessary to confirm or refuteprior assumptions about the species identity In addition tothe required taxonomic research further biological researchis needed to understand the age growth rate reproductivebiology and molecular ecology of the Long Reef Tubiporain order to understand why they are so prevalent at thisparticular location

Shared among the various nominal species of Tubiporais the distinctive bright red colour of the skeleton Thered colouration is a result of organic pigments includingcarotenoids which give the orange colour to carrots and thered colour to cooked lobsters Carotenoids occur naturally inplants but are not manufactured by animals so it is likely theOrgan Pipe Coral assimilates the pigments via heterotrophicfeeding on phytoplankton Incorporating pigment into theskeleton is likely to serve the coral in two ways firstly itwould assist light absorption and maximize the potential for

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

Journal of Marine Biology 5

recently assemblages of coralliths have been recorded in theCook Islands [21] Barbados [22] the North West IndianOcean [23] Galapagos [24] Mexico and the Red Sea [25]In Australian waters there are currently only isolated recordsof coralliths For example Porites lutea has been observed toformmotile balls on the depositional reef flats atHeron Island[26] and Cyphastrea microphthalma forms motile balls at theCocos Islands [27]

The largest corallith encountered at Adele Island was acolony of Pavona venosawhichwas 12 cm (greatest diameter)This is small in comparison to the normal size of this specieswhich has the potential to grow to at least 1m (greatestdiameter) when attached to the substrate Coralliths are likelyto be size restricted because if they grow too large they wouldbecome partially or completely buried It is also worthwhilenoting that no attached forms of the four corallith specieswere recorded at station 10K9 however these four coralspecies were encountered in low abundance at other AdeleIsland stations

Rhodolith beds however are very widespread They aredistributed from the poles to the tropics and can accumulateto form extensive communities on awide variety of sedimentsin both deep and shallow water [28 29] The largest bedsreported are on the Brazilian Shelf spanning 23 degrees oflatitude [28 30 31] In Brazil rhodoliths are so abundantthey are commercially mined [32] Numerous studies havereported that rhodolith beds are important ecologicallybecause they support a high diversity of associated flora andinfauna [28 33ndash35]

InAustralia rhodolith beds are also relativelywidespreadoccurring offWesternAustralia [36] in cold-temperatewatersof southernAustralia [37] and in southernQueenslandwherethey cover up to 50 of the sea-floor from 50 to 110m depth[38] A study conducted at Montgomery Reef in the Kim-berley describes rhodoliths as being important contemporaryreef builders [15] Rhodoliths are reportedly so abundant atMontgomery Reef that they form containment banks whichimpound a raised lagoonal habitat the water from whichfeeds the unique system of low-tide cascades Some of theMontgomery Reef rhodoliths have a core of coral fragmentbutmany are constructed entirely of algae Similarly on SouthTurtle Reef in Talbot Bay (inshore Kimberley) rhodolithbanks form along the reef crest and enclose small pools thatretain water over the low tide [39]

While there are records of rhodoliths from the Kimberleythere are however no current records of coralliths (at Mont-gomery Reef Talbot Bay or any other Kimberley locations)Moreover there are no current records of Australian coralreef habitat featuring a mixed assemblage of living coralliths(from a variety of genera) and rhodoliths Thus the AdeleIsland fore-reef rollolith zone appears to be relatively rareTherefore our findings provide the first record of mixedcorallith and rhodolith habitat for the Kimberley coastalbioregion and also for Australia

Further taxonomic study is needed to confirm whichspecies of algae form the rhodolith community at AdeleIsland Nongeniculate coralline algae are considered to bechallenging to identify and at least eight genera belonging tothree families of Corallinales (Hapalidiaceae Corallinaceae

and Sporolithaceae) contain species that commonly formrhodoliths The rhololith bed off Western Port Victoria forexample is composed of four species (Hydrolithon rupestre(Foslie) Penrose Lithothamnion superpositum Foslie Meso-phyllum engelhartii (Foslie) Adey and Neogoniolithon bras-sica-florida (Harvey) Setchell and Mason) [37] so it is likelythat the Kimberley rhodolith beds also contains multiplespecies

The rolloliths of Adele Island most likely form in thelee of prevailing wave action as a cumulative responseto unidirectional currents and the tidal pull on surfacesediments This maintains periodic yet constant movementenabling persistent growth on all sides of the colony [21]Thefrequent disturbance of bottom sediments by browsing fishesand gastropods (bioturbation) has also been hypothesized tocontribute towards the unique spherical form [19 40 41]Holothurians and sea urchins have also been observed to aidin keeping coralliths and rhodoliths in motion [25]

42 Tubipora Tubipora sp is the only known hard calciticreef-building alcyonarian (soft) coral Its skeleton consists ofcalcite spicules fused into upright parallel tubes connectedby transverse platforms hence its common name of OrganPipe Coral Organ Pipe Coral is normally sporadic to rarethroughout its range which spans the Indo-Pacific fromthe Red Sea and East Africa to Southeast Asia MicronesiaAustralia and the Pacific [42] Tubipora has however beenobserved in large quantities near Rat Island off Gladstone inQueensland Australia (Philip Alderslade pers comm) andat an undisclosed location in Papua New Guinea [43] Thehighest published benthic coverage estimate ofTubipora sp is119 from one location in the Red Sea [44] Our quantitativedata showing 2767 (+324 SE) coverage of Tubipora at thisone Long Reef location suggests this is an exceptionally rarehigh density population

Tubipora was once thought to be a single ubiquitousspecies Tubipora musica Linnaeus 1758 (Family TubiporidaeOrder Stolonifera Class Anthozoa Phylum Cnidaria) how-ever there are now several nominal species of Tubipora Ourpreliminary systematic study has raised doubt about whichspecies of Tubipora is present in the Kimberley Hence fur-ther investigations based on grossmorphology of its skeletonandmolecular sequencing are necessary to confirm or refuteprior assumptions about the species identity In addition tothe required taxonomic research further biological researchis needed to understand the age growth rate reproductivebiology and molecular ecology of the Long Reef Tubiporain order to understand why they are so prevalent at thisparticular location

Shared among the various nominal species of Tubiporais the distinctive bright red colour of the skeleton Thered colouration is a result of organic pigments includingcarotenoids which give the orange colour to carrots and thered colour to cooked lobsters Carotenoids occur naturally inplants but are not manufactured by animals so it is likely theOrgan Pipe Coral assimilates the pigments via heterotrophicfeeding on phytoplankton Incorporating pigment into theskeleton is likely to serve the coral in two ways firstly itwould assist light absorption and maximize the potential for

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

6 Journal of Marine Biology

photosynthesis by symbiotic dinoflagellates and secondlycarotenoidsmay help protect chlorophyll from photo damage[45]

43 Conservation Implications Both hard coral and calcifiedmacroalgae are vital components of nearshore ecosystems intropical and temperate systems through their contributionsto carbon cycling and productivity [46] the provision ofhabitats and their associated biodiversity their role as nurseryareas [47 48] and their contribution to the developmentof reef structures [49] Rhodoliths also offer the potentialto serve as paleoclimate proxies [40 50ndash52] A recentstudy measuring carbonate deposition in two slow-growingrhodolith species (lt200120583myminus1) permitted biweekly sam-pling resolution leading the authors to suggest rhodoliths areunique globally distributed palaeothermometers whichmayhelp refine regional climate histories during the Holocene[53]

The remote location and lack of conservation manage-ment of Adele Island and Long Reef combined with the highdensity of rhodolithscoralliths and Organ Pipe Coral in theunusual habitat zones we describe here renders these marineresources highly susceptible to harvesting pressure in thefuture Traditional fishers have utilized the marine resourcesof the Kimberley region since the early eighteenth century[54 55] but there is currently no historical record of hardcorals soft corals or calcifying macroalgae being targetedThere is however substantial and rapidly growing trade incorals [56] including Organ Pipe Coral which is used inthe curio jewellery and aquarium industries because of itsattractive bright red skeleton [57] In consideration of thisOrgan Pipe Coral is currently listed as Near-Threatened onthe IUCN red-list of threatened species [57]

Scleractinian and nonscleractinian corals are affordedsome amount of protection from international trade as theyare listed under Appendix I and II of CITES howevercalcifying macroalgae are not listed At an internationallevel we advocate the inclusion of rhodoliths under CITESregulation and that special conditions be made to ensure thetrade of coralliths is monitored Further more timely accessto national-level CITES trade data is needed to monitortrends in the export of marine resources

It is important that regional marine resource managersdirect special attention towards these atypical Kimberleyhabitats because corals and calcifying macroalgae are vul-nerable to changes in the environment Specific recom-mendations for conserving these unique benthic habitatsinclude the establishment of marine protected areas in theKimberley encompassing Adele Island and Long Reef andthe inclusion of these locations in the existing program ofCustoms surveillance Further research into Tubipora andrhodolith taxonomy is also important to support conserva-tion efforts Ongoing adaptive management and long-termmonitoring of wild coral harvest in Western Australia areneeded to manage risks and to ensure Western Australiarsquosunique natural resources are protected The Kimberley is thenew frontier for tropical reef research and given the industrialinterest in the region more information is needed to provide

the basis for sound decision-making and sustainable resourcemanagement

Acknowledgments

This research was conducted as part of the Woodside Collec-tion (Kimberley) project The project is a Western AustralianMuseum initiative and sponsored by Woodside EnergyProject partner organisations are the Australian MuseumQueensland Museum Museum and Art Gallery of theNorthern Territory Museum Victoria and the Herbariumof Western Australia (DEC) The second author was fundedas part of the Australian node of the Census of Marine Life(CReefs Program) studying the biodiversity of Australianbiota funded by the Australian Government under auspicesof the Australian Institute of Marine Science the GreatBarrier Reef Research Foundation and BHP Billiton Thisresearch is part of Australian Biological Resources Study(ABRS) National Taxonomic Research Grant (no 209-05)Taxonomy of tropical Australian Octocorallia (AnthozoaCoelenterata) primarily from the Census of Marine LifeldquoCReefsrdquo expeditions (J N A Hooper amp P N A Alderslade)The authors are thankful for the help received by the projectscientific staff and shiprsquos company during survey voyagesaboard the Kimberley Quest II Special thanks to Dr BarryWilson for his useful discussions Thanks also to AlisonSampey for the compilation of Figures 1ndash3

References

[1] B Brooke ldquoGeomorphologyrdquo inMarine Biological Survey of theSouthern Kimberley Western Australia F E Wells J R Hanleyand D I Walker Eds pp 21ndash51 Western Australian MuseumPerth Australia 1995

[2] J K Griffith ldquoThe corals collected during SeptemberOctober1997 at Ashmore Reef Timor Seardquo A Report to Parks AustraliaWestern Australian Museum Perth Australia 1997

[3] M Kospartov M Beger D Ceccarelli and Z Richards AnAssessment of theDistribution andAbundance of SeaCucumbersTrochus Giant Clams Coral Fish and Invasive Marine Speciesat Ashmore Reef National Nature Reserve and Cartier IslandMarine Reserve 2005 UniQuest Pty Limited DEWHA 2006

[4] D CecarelliM KospartovM Beger Z Richards andC BirrellAn Assessment of the Impacts of Illegal Fishing on InvertebrateStocks at Ashmore Reef National Nature Reserve 2006 C amp RConsulting DEWHA 2007

[5] P F Berry Ed Faunal Surveys of the Rowley Shoals ScottReef and Seringapatam Reef North-Western Australia vol 25 ofRecords of theWestern AustralianMuseum SupplementWesternAustralian Museum Perth Australia 1986

[6] P F Berry Ed Marine Faunal Surveys of Ashmore Reef andCartier Island North-Western Australia vol 44 of Records ofthe Western Australian Museum Series Western AustralianMuseum Perth Australia 1993

[7] C Bryce Marine Biodiversity Survey of Mermaid Reef (RowleyShoals) Scott and Seringapatam Reef vol 77 of Records of theWestern Australian Museum Supplement Western AustralianMuseum Perth Australia 2009

[8] K Fabricius ldquoA brief photo guide to the shallow-wateroctocorals of the Rowley Shoals Western Australiardquo Report

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

Journal of Marine Biology 7

Department of Environment andConservation Government ofWestern Australia 2008

[9] Z Richards M Beger J P Hobbs T Bowling K Chong-seng andM Pratchett ldquoAshmore Reef National Nature Reserveand Cartier Island Marine Reserve Marine Survey 2009rdquo ARCCentre of Excellence for Coral Reef Studies Department of theEnvironment Water Heritage and the Arts 2009

[10] R Thackway and I D Cresswell Interim Marine and CoastalRegionalisation for Australia An Ecosystem-Based Classificationfor Marine and Coastal Environments Environment AustraliaCanberra Australia 1998

[11] M Wood and D Mills A Turning of the Tide Science forDecisions in the Kimberley-Browse Marine Region A WesternAustralian Marine Science Institution (WAMSI) Perth Aus-tralia 2008

[12] J E N Veron and L M Marsh Hermatypic Corals of West-ern Australia Records and Annotated Species List vol 29 ofRecords of the Western Australian Museum Western AustralianMuseum Perth Australia 1988

[13] C Teichert and R W Fairbridge ldquoSome coral reefs of the SahulShelfrdquo Geographical Review vol 28 no 2 pp 222ndash249 1948

[14] B R Wilson The Biogeography of the Australian North WestShelf Elsevier New York NY USA 2013

[15] B Wilson and S Blake ldquoNotes on the origins and biogeomor-phology of Montgomery Reef Kimberley Western AustraliardquoJournal of the Royal Society ofWestern Australia vol 94 pp 107ndash119 2011

[16] Z T Richards A Sampey and L Marsh ldquoSynthesis of historicmarine species data for the Kimberley Western Australia(1880sndash2009) hard coralsrdquo Records of the Western AustralianMuseum In press

[17] MWeber Introduction et description de lrsquoExpedition Mongraphno 1 Siboga-Expeditie 1902

[18] PD Taylor andDN LewisFossil Invertebrates NaturalHistoryMuseum London UK 2005

[19] P W Glynn ldquoRolling stones amongst the scleractinia mobilecoralliths in the Gulf of Panamardquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 183ndash198 1974

[20] M Pichon ldquoFree-living scleractinian coral communities inthe coral reefs of Madagascarrdquo in Proceedings of the 2ndInternational Coral Reef Symposium vol 2 pp 173ndash181 1974

[21] T P Scoffin D R Stoddart A W Tudhope and C WoodroffeldquoRhodoliths and coralliths of Muri Lagoon Rarotonga CookIslandsrdquo Coral Reefs vol 4 no 2 pp 71ndash80 1985

[22] J B Lewis ldquoSpherical growth in the Caribbean coral Siderastrearadians (Pallas) and its survival in disturbed habitatsrdquo CoralReefs vol 7 no 4 pp 161ndash167 1989

[23] M R Claereboudt ldquoPorites decasepta a new species of sclerac-tinian coral (Scleractinia Poritidae) from Omanrdquo Zootaxa no1188 pp 55ndash62 2006

[24] P W Glynn and G M Wellington Corals and Coral Reefs ofthe Galapagos Islands University of California Press BerkeleyCalif USA 1983

[25] H Reyes-Bonilla R Riosmena-Rodriguez and M S FosterldquoHermatypic corals associated with rhodolith beds in the Gulfof California Mexicordquo Pacific Science vol 51 no 3 pp 328ndash3371997

[26] G Roff ldquoCorals on the move morphological and reproductivestrategies of reef flat corallithsrdquo Coral Reefs vol 27 no 2 pp343ndash344 2008

[27] J E N Veron Re-Examination of the Reef Corals of Cocos(Keeling) vol 14 Records of the Western Australian MuseumWestern Australian Museum Perth Australia edition 1990

[28] M S Foster ldquoRhodoliths between rocks and soft placesrdquoJournal of Phycology vol 37 no 5 pp 659ndash667 2001

[29] B Konar R Riosmena-Rodriguez andK Iken ldquoRhodolith beda newly discovered habitat in theNorth PacificOceanrdquoBotanicaMarina vol 49 no 4 pp 355ndash359 2006

[30] MKempf ldquoNotes of the benthic bionomyof theN-NEBrazilianshelfrdquoMarine Biology vol 5 no 3 pp 213ndash224 1970

[31] G M Amado-Filho G Maneveldt R C C Manso B VMarins-Rosa M R Pacheco and S M P B GuimaraesldquoStructure of rhodolith beds from 4 to 55 meters deep along thesouthern coast of Espırito Santo State BrazilrdquoCienciasMarinasvol 33 no 4 pp 399ndash410 2007

[32] G B Baarli M Cachao C M da Silva M E Johnson JLedesma-Vazquez and A M E Santos ldquoFossil nodules offree living biota from the upper Pleistocene Mulege formationPlaya La Palmita Baja California SurMexicordquo Publicaciones delSeminario de Paleontologıa de Zaragoza vol 9 pp 75ndash78 2010

[33] C Barbera C Bordehore J A Borg M Glemarec et alldquoConservation and management of northeast Atlantic andMediterranean maerl bedsrdquo Aquatic Conservation Marine andFreshwater Ecosystems vol 13 no 1 pp S65ndashS76 2003

[34] G Hinojosa-Arango and R Riosemena-Rodrıguez ldquoInfluenceof rhodolith-forming species and growth-form on associatedfauna of rhodolith beds in the Central-West gulf of CaliforniaMexicordquoMarine Ecology vol 25 no 2 pp 109ndash127 2004

[35] J Hall-Spencer J Kelly and C A Maggs Assessment of MaerlBeds in the OSPAR Area and the Development of a MonitoringProgram Department of Environment Heritage and LocalGovernment Dublin Ireland 2008

[36] N Goldberg ldquoAge estimates and description of rhodolithsfrom Esperance Bay Western Australiardquo Journal of the MarineBiological Association of the United Kingdom vol 86 no 6 pp1291ndash1296 2006

[37] A SHarvey andF L Bird ldquoCommunity structure of a rhodolithbed from cold-temperate waters (Southern Australia)rdquo Aus-tralian Journal of Botany vol 56 no 5 pp 437ndash450 2008

[38] M Lund P J Davies and J C Braga ldquoCoralline algal nodulesoff Fraser Island Eastern Australiardquo Facies no 42 pp 25ndash342000

[39] B Wilson S Blake D Ryan and J Hacker ldquoReconnaissanceof species-rich coral reefs in a muddy macro-tidal enclosedembayment mdashTalbot Bay Kimberley Western Australiardquo Jour-nal of the Royal Society ofWestern Australia vol 94 pp 251ndash1652011

[40] M S Foster R Riosmena-Rodrıguez D L Steller and W JWoelkerling ldquoLiving rhodolith beds in the Gulf of Californiaand their implications for paleoenvironmental interpretationrdquoGeological Society of America Bulletin vol 318 pp 127ndash139 1997

[41] E C Marrack ldquoThe relationship between water motion andliving rhodolith beds in the Southwestern Gulf of CaliforniaMexicordquo Palaios vol 14 no 2 pp 159ndash171 1999

[42] K Fabricius and P Alderslade Soft Corals and Sea FansmdashAComprehensive Guide to the Tropical Shallow Water Genera ofthe Central-West Pacific the Indian Ocean and the Red SeaAustralian Institute of Marine Science Townsville Australia2001

[43] J E N Veron Corals of the World vol 1ndash3 Australian Instituteof Marine Science 2000

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg

8 Journal of Marine Biology

[44] Y Benayahu andY Loya ldquoSpace partitioning by stony corals softcorals and benthic algae on the coral reefs of the Northern Gulfof Eilat (Red Sea)rdquo Helgolander Wissenschaftliche Meeresunter-suchungen vol 30 no 1ndash4 pp 362ndash382 1977

[45] J Cvejic S Tambutte S Lotto M Mikov I Slacanin and DAllemand ldquoDetermination of canthaxanthin in the red coral(Corallium rubrum) from Marseille by HPLC combined withUV and MS detectionrdquoMarine Biology vol 152 no 4 pp 855ndash862 2007

[46] S Hetzinger J Halfar B Riegl and L Godinez-Orta ldquoSedi-mentology and acoustic mapping of modern rhodolith facieson a non-tropical carbonate shelf (Gulf of California Mexico)rdquoJournal of Sedimentary Research vol 76 no 3-4 pp 670ndash6822006

[47] N A Kamenos P G Moore and J M Hall-Spencer ldquoSmall-scale distribution of juvenile gadoids in shallow inshore waterswhat role does maerl playrdquo ICES Journal of Marine Science vol61 no 3 pp 422ndash429 2004

[48] N A Kamenos P G Moore and J M Hall-Spencer ldquoNursery-area function of maerl grounds for juvenile queen scallopsAequipecten opercularis and other invertebratesrdquo Marine Ecol-ogy Progress Series vol 274 pp 183ndash189 2004

[49] W A Nelson ldquoCalcified macroalgae critical to coastal ecosys-tems and vulnerable to change a reviewrdquoMarine and FreshwaterResearch vol 60 no 8 pp 787ndash801 2009

[50] A Freiwald R Henrich P Schafer and H Willkomm ldquoThesignificance of high-boreal to subarctic maerl deposits innorthern Norway to reconstruct holocene climatic changes andsea level oscillationsrdquo Facies vol 25 no 1 pp 315ndash339 1991

[51] C E Cintra-Buenrostro M S Foster and K H MeldahlldquoResponse of nearshore marine assemblages to global changea comparison of molluscan assemblages in Pleistocene andmodern rhodolith beds in the Southwestern Gulf of Califor-nia Mexicordquo Palaeogeography Palaeoclimatology Palaeoecol-ogy vol 183 no 3-4 pp 299ndash320 2002

[52] R Nalin C S Nelson D Basso and F Massari ldquoRhodolith-bearing limestones as transgressive marker beds fossil andmodern examples from North Island New Zealandrdquo Sedimen-tology vol 55 no 2 pp 249ndash274 2008

[53] N A Kamenos M Cusack and P G Moore ldquoCoralline algaeare global palaeothermometers with bi-weekly resolutionrdquoGeochimica et Cosmochimica Acta vol 72 no 3 pp 771ndash7792008

[54] S Fox ldquoReefs and shoals in Australia-Indonesian relations tra-ditional Indonesian fishermanrdquo in Australian in Asia EpisodesA C Milner and M Quilty Eds Oxford University PressMelbourne Australia 1988

[55] N Stacey Boats to burn bajo fishing in the Australian fishingzone [PhD thesis] Northern Territory University Common-wealth of Australia 2002 Ashmore Reef National NatureReserve and Cartier IslandMarine Reserve Management PlansEnvironment Australia Canberra Australia 1999

[56] A Rhyne R Rotjan A Bruckner and M Tlusty ldquoCrawlingto collapse ecologically unsound ornamental invertebrate fish-eriesrdquo PLoS ONE vol 4 no 12 Article ID e8413 2009

[57] D Obura D Fenner B Hoeksema L Devantier and CSheppard ldquoTubipora musicardquo in IUCN 2012 IUCN Red List ofThreatened Species Version 2012 2 2008 httpwwwiucnred-listorg