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ATOLL RESEARCH BULLETIN
NO. 534
DINOFLAGELLATE DIVERSITY AND ABUNDANCE IN TWO BELIZEAN CORAL-REEF MANGROVE LAGOONS: A TEST OF
MARGALEF’S MANDALA
BY
MARIA A. FAUST, R. WAYNE LITAKER, MARK W. VANDERSEA, STEVEN R. KIBLER, AND PATRICIA A. TESTER
ISSUED BYNATIONAL MUSEUM OF NATURAL HISTORY
SMITHSONIAN INSTITUTIONWASHINGTON, D.C., U.S.A.
NOVEMBER 2005
N mag.
2 km
Tobacco Range
Pelican Cays
Patch Reefs& Sand Bores
TobaccoReef
16˚45'N
88˚15'W 88˚05'W
Twin Cays
Carrie Bow Cay
Manatee Cay Cat Cay
Tobacco Cay
Douglas Cay
Research Area of Twin Cays and Douglas Cay
Island
Reef
Tidal flat
100 m
Lair Channel
100 m
Hidden Creek
GrouperGardens
The Lair
Turtle Pond
Batfish Point
Cuda Cut
Sponge Haven
Twin Bays
Figure 1. Map showing The Lair at Twin Cays, and Douglas Cay sample sites and surrounding cays.
DINOFLAGELLATE DIVERSITY AND ABUNDANCE IN TWO BELIZEAN CORAL-REEF MANGROVE LAGOONS: A TEST OF MARGALEF’S
MANDALA
BY
MARIA A. FAUST1, R. WAYNE LITAKER2, MARK W. VANDERSEA2, STEVEN R. KIBLER2, AND PATRICIA A. TESTER2
ABSTRACT
Dinoflagellatesarefrequentlyabundantinthecoral-reefmangrovelagoonsoffthecoastofBelize.Margalefpredictedthatmarineenvironmentswithlowturbulenceandhighnutrientinputswouldfavordinoflagellates.Along-termstudyofcoral-reefmangroveembaymentcaysofBelize,includingthisstudy,hasshownthatthesesystemscontainabundantdinoflagellatespecies.ConsistentwithMargalef’sprediction,thesehabitatsareprotectedfromwindmixing,showahighdegreeofstratification,andhaverestrictedwaterexchangewithsurroundingoligotrophicwatersoftheopenbarrier-reefsystem.Thislimitedwaterexchangefavorsretentionofdinoflagellatecellsandthetrappingofnutrientrichorganicmaterialthatisrapidlyrecycledprovidingarelativelyhigh-nutrientenvironment.Species-specificbloomsareacommonfeatureofthesesystems.Inthestudy,theecologyanddiversityofdinoflagellatespeciesfromtwonutrient-enrichedhabitats,DouglasCayandTheLairatTwinCay,wereexaminedindetail.AcomparisonofthespeciescompositionfrombothsitesshowedthatDouglasCaycontainedcoastalplanktonicandoffshoreoceanicdinoflagellateswhileTheLairatTwinCaycontainedmainlybenthicdinoflagellates.Atotalof19bloom-formingspecieswereobservedinthesesystemsduringthreetwo-weekstudies.Themorphologyofeightofthesebloom-formingspeciesisillustratedinScanningElectronMicroscopy(SEM)photographs.TheseincludeBysmatrumcaponii,Dinophysiscaudata,Gonyaulaxgrindleyi,Peridiniumquinquecorne,Gonyaulaxpolygramma,Gonyaulaxspinifera,Lingulodiniumpolyedrum,andPyrodiniumbahamensevar.bahamense.Approximatelyhalfofthebloom-formingdinoflagellatesareknowntoxinproducers.ThecongruencebetweenMargalef’spredictionandthedistributionofdinoflagellatesinthesenaturallyeutrophicsystemssuggeststhatincreasednutrientinputsinoligotrohicportionsoftheCaribbeanwillfavorashiftinspeciesdominancetowarddinoflagellatespecies.Theeffectwillbemostpronouncedinbaysorotherregionswhereturbulenceislikelytobereduced.Thisspeciesshiftmayhaveconsequencesforfoodwebdynamicsandtheprevalenceofdinoflagellatetoxinsinthefoodchain._______________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________________
1 DepartmentofBotany,NationalMuseumofNaturalHistory,SmithsonianInstitution, Washington D.C., 20560.2NOS/NOAA,CenterforCoastalFisheriesHabitatResearch,101PiversIslandRoad,Beaufort,NorthCarolina,28516.Manuscript received 29 July 2005; revised 22 August 2005.
106
INTRODUCTION
Dinoflagellatesconstituteoneofthedominantgroupsofoceanicphytoplanktonandareresponsibleforasignificantportionofoverallprimaryproductivity.Manyspeciesarebloomformers,andasubsetoftheseisknowntoproducepotenttoxinsthataccumulateinthefoodchaincausingmassmortalitiesoffish,birdsandmammals,aswellashumanillnessanddeath.Thesebloomsfrequentlyreachdensitiessufficienttodiscolorthewaterandcanreleaseenoughorganicmaterialtoresultinhypoxiaorotherformsofwater-qualitydegradationincludingnoxiousodorsandunsightlyfoams.Occurrencesofharmfulalgalblooms(HABs)nearshoreregionscausesevereeconomicimpact,havemajorenvironmentalandhumanhealthproblems,andcauselossestofisheriesandtourismoperations(Smayda,1997;Ajanietal.,2001).Oftenthesebloomsarecharacterizedbytheproliferationanddominanceofaparticularspecies(Hallegraeff,1993).Globally,HABsareincreasinginscaleandfrequencyandcurrentlythreatenmostcoastalregionsoftheworld.Manyreasonsforthisincreaseinbloomfrequencyhavebeenpostulated,rangingfromanthropogenicnutrientinputstoincreasedawarenessandimprovedsurveillance(PitcherandCockroft,1996).
Extensiveresearchhasbeenconductedtoidentifythephysical,chemicalandbiologicalmechanismsresponsiblefordinoflagellatebloomformation(Smayda,1997).OneoftheearliestandmostrobusthypothesesputforwardisMargalef’sMandala(Margalef,1978;Margalefetal.,1979).Thishypothesispredictsthatlowturbulenceandhighnutrientenvironmentsfavordinoflagellatedominance.Workwithmid-andupper-latitudespeciesdoesindeedseemtoconfirmthatsubstantialnutrientinputsandlowturbulenceconditionscoincidewithdinoflagellateblooms.Theseconditionsalsoincludebloomsthatareenhancedbyaccumulationinstablefrontalzoneswhichrepresentregionsofloweredturbulentdispersion.Thereis,however,apaucityofavailableinformationaboutHABdinoflagellatebloomsthatoccurintropicalregionsincludingtheAtlanticbarriercoral-reefmangroveecosystemsofBelize(Hernández-BecerrilandBecerril,2004).PreliminarysurveyshavefoundthatalthoughsomeHABdinoflagellatesarefoundinlowabundancethroughouttheBelizeanbarrier-reefsystem,thegreatestdiversityandhighestnumberofbloom-formingspeciesappearrestrictedtomangrovecayembaymentsorsimilarenvironments(Faust,2000,2004;MortonandVillareal,1998;Morton,2000).Inthispublication,wereporttheoccurrenceof59dinoflagellatespeciesfromtwolagoonalembaymentslocatedatDouglasCayandTwinCays,Belize.Fifteenofthespeciesidentifiedformedsubstantialblooms.TheecologyandmorphologyofeightofthesearedescribedindetailandanevaluationofhowwelltheprevailingconditionsanddinoflagellateabundanceagreewiththepredictionsofMargelf’sMandalaispresented.
107
METHODS
Study Area
DouglasCay,BelizeissituatednorthofThePelicanCays(16º42.5’N88º10.3’W,Figure1)andispartofthelargestbarrier-reefmangroveecosysteminthenewworld(MacintyreandRützler,2000).Thereefsinthissystemarecharacterizedbychannelsthatformanumberofshelfatolls(JamesandGinsburg,1979)whichareseparatedbyanunusualnetworkofreefridges,bothsubmergedandexposed,whichwereformedduringtheHolocene(Macintyreetal.,2000).Manyoftheselagoonreefshavebeencolonizedbyredmangroves,RhizophoramangleLinnaeus(Purdy,1994).Whenthemorphologyoftheselagoonalreefsisfavorable,thedevelopingmangroveislandswillencompassaninternallagoonlikethatfoundatDouglasCay.Theselagoonsrangefrom1-10mdepthattheircenter.Theyhaveerodedpeatbanksaroundthemarginwithanabundantgrowthofmangroveproproots.Theentrancetotheselagoonsisfrequentlycharacterizedbyasillorothermorphologicalfeaturethatrestrictswaterexchangewiththesurroundingoceanicfore-reefsystems.Asaresult,theselagoonsareconsideredseparatewatermassesandarecharacteristicallywarmerandmoresalinethantheopenwatersofthesurroundingcentrallagoon(Villarealetal.,2000).Themangroveproprootsthatlinetheedgeoftheselagoonsarecolonizedbyabundantcorals,spongesandtunicates(RützlerandFeller,1996).Thehydrographicisolationofthesesystems,andlowtidalamplitude(<20cm)allowsretentionofnutrientandcarbon-richdetritalmaterialsuppliedbythesurroundingmangrovetrees.Theseconditionspromoteahighmicrobialbiomassandtherapidratesofnutrientrecycling.
TwinCays,thesecondsystemstudied(located7kmnorthofPelicanCays(16°49.4’N88°6.1’W),consistsofashallowintertidalmangroveislandcharacterizedbyaseriesoflagoons,channels,mudflatsandponds.The“Lair”,thespecificlocationwheresamplesweretaken,isashallowlagoon(0.5to3mdeep)locatedattheendofTheLairchannel.ThoughTheLairhasapoorlydevelopedsill,the<20cmtideandlongnarrowLairchannelwhichseparatesTheLairfromsurroundingwaters,helprestrictwaterexchangewiththesurroundingwaters.Overallwaterexchange,however,isgreaterthanobservedforDouglasCay(Kibleretal.,2005).TheLairisalsohighinorganicmatteroriginatingfrommangroves,meadowsofturtlegrass,ThalassiatestudiniumBankexKonin,aswellasbenthicproductionassociatedwiththesoftsediments.
Physical Parameters and Chlorophyll a Biomass
Temperature,salinity,dissolvedoxygenandirradianceweremeasuredinthewatercolumnatthreedepthswithaYellowSpringInstrumentprofilingunit(model6600).Irradiancewasestimatedbytheintegratingquantumscalarirradiancemeter,BiosphericalInstruments#QSI-140meter(Testeretal.,2003).AmmoniawasmeasuredfluorometricallyusingthemethodofHolmesetal.(1999).Samplesforchlorophyllaanalysiswerevacuum-filteredthrough25mmGF/Ffilters(<10cmHg)andwereimmediatelyfrozeninliquidnitrogen.Samplesweresubsequentlyextractedwith7.5
108
ml90%acetoneandweremaceratedwithatissuegrinderbeforebeinganalyzedusingtheacidificationmethodforchladescribedbyParsonsetal.(1984).ThewatercolumnconditionsatDouglasCayandTheLairweresimilarin2002,2003and2004.In2004,weformallyquantifiedstratificationateachstationusingtheBrunt-Väisäläfrequency(N),whichdescribestheoscillationthatresultswhenthepycnoclineisdisplaced(MannandLazier,1996).Thismetricwascalculatedatmid-depthinthewatercolumnusingtheexpressionN(rads-1)=(g/ÿ/ÿz)½,wheregisthegravitationalconstant(ms-2) and isdensity (Kg m-3).Tosimplifycomparisons,Nwasconvertedtounitsofcyclesh-1 usingN/2ÿ.Strongstratificationisindicatedbyfrequenciesinexcessof20cycles.h-1(Macintyre et al., 2002).
DinoflagellateSampling
ThedinoflagellateassemblageswerecharacterizedannuallyatbothDouglasCayandLairhabitatsduringatwo-weekperiodineachMayfrom2002to2004(Fig.1).Atotalof42watersampleswerecollectedfromDouglasCayand20watersampleswerecollectedfromTheLair.Subsurfacewaterwascollectedusinga20µmporesizenylonplanktonnettowedbyasmallboatoperatingatitslowestspeedfor1-2minutes.Largepiecesoffloatingdetrituswerealsocollected(Faust,2004).Sampleswereconcentratedto100mlvolumeandfixedwithglutaraldehydeat1%finalconcentrationforlightmicroscopyandSEMspeciesidentification(Faust,1990).BoththeDouglasCayand“Lair”habitatswerecharacterizedbyadiversecommunityofdinoflagellates(Faust,2004).
EnumerationandIdentificationofDinoflagellates
Toenumeratemicroalgae,cellconcentrationsofthreereplicatesforeachwatersamplewereestimatedat100xmagnificationinaPalmer-Maloneycellchamberorinsettlingchambers(Guillard,1973).DinoflagellateswereidentifiedunderdifferentialinterferencecontrastilluminationwithCarlZeissAxiophotmicroscope.Therelativeabundanceofdinoflagellateswasdeterminedastheproportionoforganismspresentinatotalof500cells.
ForSEM,glutaraldehyde(1%concentration)-preserveddinoflagellateswereisolated using a capillary pipette under a compound microscope. Cells were concentrated ontoapolycarbonatefilteratroomtemperature,rinsedsixtoeighttimeswithdeionizedwater,dehydratedinagradedseriesofethanolconcentrationsandcriticalpointdried.Thepreparationwascoatedwithcarbonandbyalayerofgold-palladium(Faust,1990).CelldimensionsweredeterminedfromSEMphotographsofatleast10cells;valuesgivenrepresentthemean.Kofoidiannomenclaturewasusedforidentifyingdinoflagellatespecies(Kofoid,1909).SamplesofthisinvestigationaredepositedinTheDinoflagellateCollectionoftheU.S.A.NationalHerbarium,SmithsonianInstitution,WashingtonD.C.
109
RESULTS
Physicalenvironment
BothtemperatureandsalinitywerehighinDouglasCayandTheLairandvariedonlyslightlyoverthecourseofallthreeMaystudyperiods(Table1).Bothlagoonswereprotectedfromprevailingwindsbythesurroundingmangrovetrees.Stabletemperatureandsalinityconditions,lowtidalexchangeandreducedwindmixingresultedinalowturbulenceenvironment(Table2).
Table1.RangeofenvironmentalvariablesmeasuredinDouglasCayandTheLair,TwinCays during the three two week study periods.
Study Site DissolvedNH4+
Temperature Salinity DissolvedO2 Light Chlorophyll a
ÿmole.L-1 ºC psu ppm ÿE.m-2. s-1 ÿg.L-1
Douglas Cay 0.6-6.0 28.3-29.3 35.6-36.1 2.2-6.5 1500-2000 5.0-15.0
The Lair 0.1-0.8 29.1-31.2 37.5-38.0 2.0-5.0 1200-2000 0.8-15.0
Table2.Brunt-VaisalafrequencycalculatedatDouglasCayandatTheLair
Dissolvedoxygenvariedfromhypoxictosupersaturateddependingonthetimeofday.Thisfluctuationisduetothebalancebetweenbacterialrespirationandphotosyntheticoxygenproduction.Intheseshallowsystems,middayphotosyntheticallyactiveradiationissufficienttosaturatephotosynthesisinthewatercolumn(Table1)andatthebenthicsurfaceaswell.DissolvedNH4+ishigherinDouglasthaninTheLair,butbothareon
The Lair 2004 Date Time B-V Frequency (cycles h-1)
12 May 04 1530 37.6 13 May 04 0800 23.5 13 May 04 1415 34.2 17 May 04 0830 28.3 17 May 04 1430 33.8 18 May 04 1000 34.3 18 May 04 1615 40.7
Douglas Cay 2004 Date Time B-V Frequency (cycles h-1)
10 May 04 0630 10.3 11 May 04 0645 25.0 11 May 04 1400 48.6
110
averageapproximatelyanorderofmagnitudegreaterthanconcentrationsfoundinthesurroundingoligotrophiclagoon.TheBrunt-Väisälänumbersexceeded20cyclesh-1duringeachperiodmeasuredexceptone,indicatingthatthewatercolumnishighlystable(Table2). DistributionandDiversityofDinoflagellatesObservedinDouglasCayandTheLair
ThedinoflagellateassemblagepresentinDouglasCayduring2002wasquitediverse.Therewere45dinoflagellatespeciespresent.Twenty-oneofthesewereplanktonic,11benthicand5bentho-planktonic.Thirty-threeofthespeciesareknownautotrophs,6wereheterotrophsand3mixotrophs.Fifteenareknowntoformtoxicbloomsinotherregions(Table3).AcomparisonofthedinoflagellatespeciespresentinDouglasCayandTheLairin2004demonstratedthatdinoflagellatecommunitiesweresimilarlydiversetothatobservedin2002,andthattheysharedapproximately65%ofthespeciesincommon.Overall,benthicspecieswerecommoninTheLairthaninDouglasCay(Tables3and4).Acompilationofthedatafromallthreeyearsidentifiedatotalof19bloom-formingspeciesfromDouglasCayandTheLair(Table5).Someofthesespeciesweremorepersistentintimeandspacethanothers.Ofthese19species,11areknowntoxinproducers(Table6).Adetaileddescriptionoftheecologyandmorphologyfor8ofthese19bloom-formingspeciesfollows:
Gonyaulax grindleyiReinecke1967Synonym:Protoceratiumreticulatum(Claparède&Lachmann)Bütschli,1885:p.1000,pl. 52.
Figures2-6
Morphology: Cellsconicalwitharoundedhypotheca;cells(30-45µmL,and28-43µmW)(Fig.2).Surfaceisdeeplyareolate(Fig.3).Apicalporecomplexisoblongwiththeapicalporeinthecentercoveredbyamucusplug(Fig.4).Sulcusisoblongandnarrow(Fig.5).Morphologyofthedissociatedplatesisinlinedrawings(Fig.6):species-specificfeaturetheintercalaryplate1aandtheventralporesituatedinrightmarginonapicalplate1’(Fig.6b).Formscysts.
Ecology:CellspresentinCatCay,DouglasCay,ElbowCay,andManateeCay(Faust,2000).Bloomof9.85x104 cells L-1causedbrownwaterdiscolorationatTobaccoRange(Fig.1)inMay2000.Cystsinthesedimentgerminatethatinitiatedthebloom(Reinicke,1967).Distribution:neritic,estuarine;coldtemperatetosubtropicalwaters.
Toxicity:Producerofparalytictoxinaffectingshellfishbeds(Table6).
Peridinium quinquecorneAbé1927Synonym:Protoperidiniumquinquecorne(Abé)Balech,1974:p.59.
Figures7-10
111
Morphology: Epithecaisconicalwithapointedapex,cells(23-40µmLand20-36µmW)(Fig.7);Hypothecaisangular,4antapicalspinesvariableinlength.Intercalaryplateslapentagonaland2aheptagonal(Fig.8).ApicalplateisaroundchamberwithaPoplateandXcanalplate(Fig.9).Cellshapeisrhomboid(Fig.10b-c).Redeye-spotpresent.
Ecology: IdentifiedinfloatingdetritusatDouglasCayandTheLair,cellshape,andlengthvariable.Formsredtides(1.15x104 cells L-1),cellsadaptedtobothbenthicandplanktonicshallow-tropicalwaters.Cellstoleratehightemperatures(38to42°C).Presentintropicaltidepools(HoriguchiandPienaar,1991).
Toxicity: Duringveryhighcellnumbersthisspeciescancauseanoxiaandfishkills(Fukuyoetal.,1990).
Bysmatrum caponii (HoriguchietPienaar)FaustandSteidinger1998Synonym:PeridiniumgregariumLombardetCapon,1971a:p.184-187.
Figures11-12
Morphology:Epithecaisconicalandhypothecatrapezoidal;epithecaandhypothecaalmostequal(Fig.11).Cellsare35µmLto30µmWandcellsurfacevermiculate.Hypothecaisindented(Fig.12a).Apicalintercalaryplates1aand,2aadjacentand3aseparated(Fig.12b).Apicalporecomplexischamber-likeFig.12b).Sulcusiswidefoursulcal platelets present (Fig. 12c). Red stigma is present.
Ecology:Speciesisanewredtide-formingdinoflagellatefromBelize.Cellconcentrations,1.85x102 cells L-1, observedinDouglasCay.CellsalsopresentinElbowandManateeCays(Faust,2000).Speciessanddwelling,attachtoparticlesviamucusstrandsemergingfromtheapicalpore(Po).Distribution:coastal,warm,tropicalandestuarinetidepools.
Toxicity:Nottoxic(Table6).
Dinophysis caudataSaville-Kent1881Synonym:DinophysishomunculusStein,1883:p.3,24,pl.21,figs.5-7.
Figures13-14
Morphology:Epithecaverysmallandhidden,cellsflattenedand110µmLto80µmW(Fig.13).Hypothecaisprominentwithalongventralfinger-likeprojection.Leftsulcallistextendsthelengthofthemainbody;rightsulcallistisshorter.Cellsurfaceisdelicately areolated. Cells may occur in pairs, dorsally attached (Fig. 14).
Ecology:Speciesisanewredtide-formingdinoflagellatespeciesfromBelize.ConcentrationsofD. caudata2.8-3.2x102 cells L-1observedinDouglasCay,and550-
112
2010 cells L-1inManateeCay(Morton,2000);dinoflagellatesalsopresentinCatCayandFishermanCay(Faust,2000).The‘bloom’populationinDouglasCaymaysuggestthathighorganicnutrientsenhancedgrowthof D. caudatatoaredtidelevelinDouglasCaythatisanunusualoccurrence(Maestrini,1998).Distributions:Neriticandestuarineinwarmtemperatetotropicalwatersworldwideexceptincoldwater,cosmopolitan.
Toxicity:Producerofichthyotoxinsthatmaycausemassivefishmortality(Table6).
Gonyaulax polygrammaStein1883
Figures15-18
Morphology: Cellelongatewithtaperedepitheca;epithecaangularwithashorthorn(Fig.15).Cellsize(42-65µmLand26-56µmW).Hypothecaroundedortruncate(Fig.16) with three short antapical spines. Theca is ornate with reticulae, longitudinal ridges andstriae(Fig.17).Linedrawingsofplatesarecharacterizedbylongitudinalraisedandserratedreticulaeextendingfromapextoantapex(Fig.18).
Ecology:Speciesisanewredtide-formingdinoflagellatespeciesfromBelize.Cellconcentrations1.2x103cells L-1observedinDouglasCay.Thefirstreportedofadenseredtideof3.5x106 cells L-1andcausedbrowndiscolorationofthewaterinManatee(MortonandVillareal,1998).Distribution:neritic,oceanic,cosmopolitanincoldtemperatetotropicalwaters,worldwidedistribution.
Toxicity:Non-toxinproducingspecies(Table6);causinganoxiaandfishkillsduringthemicroalgalcellsdecompositionandreleaseofhighsulfideandammoniaconcentrations(Koizumietal.,1996).
Gonyaulax spinifera(ClaparèdeetLachmann)Diesing1866Synonym: Peridinium spiniferum ClaparèdeetLachmann,1859:p.405,pl.20,figs4-5.
Figures19-22
Morphology:Epithecaelongate,conicalwithashortapicalhorn(Fig.19),cells(35-40µmLand21-33µmW).Cellandhypothecarounded;twoshortantapicalspinespresent(Fig.20).Apicalporecomplexisoblong,Poelliptical.Apicalplate1´bearsaventralpore(Vp)(fig.22a).Cingulumisexcavated,descendingwithanoverhang(Fig.21).Cellsurfaceisornate,characterizedbyreticulae,extendingfromtheapextoantapex.Striae associated with round trichocyst pores. Thecal plate morphology illustrated in line drawing(Fig.22).TheshapeofG. spinifera isvariableanddifficulttoidentify.Formscysts.Ecology: Gonyaulax spinifera formedredtide1.5x103 cells L-1 in Douglas Cay, was also
113
observedinCatCay,ManateeCayandLagoonCayreef-mangroveponds.Distribution:neritic,oceanic,estuarine,cosmopolitan.
Toxicity: Non-toxic(Table6).
Lingulodinium polyedrum (Stein)Dodge1989Synonym: Gonyaulax polyedraStein,1883:p.13,pl.4,figs.7-9.
Figures23-26
Morphology:Cellspolyhedralshapedwithoutantapicalspinesandapicalhorn(Fig.23).Cellsize(40-50µmLand37-53µmW).Epithecaispointedandhypothecaroundtoflat;sulcuslong,narrowandexcavated(Figs.24,26a).TheAPCoblongandtheapicalporeplatePoappearsasalatticeinsidewithraisedridge(Fig.25).Surfaceofthecalplatessculptured,reticulationincludesring-shapedridgesroundtrychocystsporesindepressions(Fig.25).Linedrawingsdescribemorphologyofthecalplates(Fig.26).Forms cysts.
Ecology: Speciesisanewred-tide-formingdinoflagellatefromBelize.L polyedrum formedredtides1.8x103cells L-1outside Douglas Cay, and species present in Cat Cay, FishermanCayandManateeCay(Faust,2000).Cellsduringthenightdisplaybrilliantphosphorescence. Distribution:neriticoceaniccoastalwarmtemperatetotropicalwaters.
Toxicity:Speciesproducerofparalyticshellfishpoisonandsaxitoxin(Table6).
Pyrodinium bahamense var. bahamensePlate1906
Figures27-30
Morphology:Cellshapenearlyround,epithecaandhypothecaaboutequalinsize;prominentapicalhornandapicalspinewithalist(Fig.27).Cellsize(33-47µmLand37-52µmW);inbloomconditioncellsizelarger(34-77µmLand38-67µmW).ApicalporeplatetriangularshapedandcomposedofthePoplateandclosingplate(cp)(Fig.30).Cingulumequatorial,listswelldeveloped(Fig.27).Platesutureswithacrestarisingbetweenplates(Fig.29);andthecalsurfacelacedwithspinulaeofroundtip(Fig.28).Forms cysts.
Ecology: Speciesformedredtide2.5x103 cell L-1outside the Douglas Cay and species presentoutsideCatCay,FishermanCayandManateeCay.Thisspeciesmayconfinetomangrove-fringedcoastalwatersoftheAtlanticandIndo-WestPacificandcausesred-brownwaterdiscolorationunderbloomcondition(Hallegraeff,1993).Distribution:SpeciespresentworldwideinCaribbean,AtlanticandPacificOceansinsubtropicaltotropicalwaters.
Toxicity: P. bahamensevar.bahamense producerofDSPandparalyticshellfishpoison(Table6).
114
Dinoflagellate species Benthic,Planktonic or
Both
AutotrophHeterotroph, or
Mixotroph
BloomForming
Akashivo sanguinea Both Autotroph -Amphidinium carterae Benthic Autotroph +Bysmatrum caponii Both Autotroph +Ceratium furca Planktonic Autotroph +Ceratium pulchellum Planktonic Autotroph -Ceratium trichoceros Planktonic Autotroph +Ceratium tripos Planktonic Autotroph -Cochlodinium polykrikoides Planktonic Mixotroph +Coolia monotis Benthic Autotroph -Dinophysis caudata Planktonic Autotroph -Dinophysis rotundata Planktonic Mixotroph -Diplopelta symmetrica Planktonic Mixotroph -Diplosalis bomba Planktonic Mixotroph -Gambierdiscus australes Benthic Autotroph -Gambierdiscus polynesiensis Benthic Autotroph -Gambierdiscus toxicus Benthic Autotroph -Goniodoma sphaericum Planktonic Autotroph -Gonyaulax digitale Benthic Autotroph -Gonyaulax grindleyi Both Autotroph +Gonyaulax. polygramma Planktonic Autotroph +Gonyaulax. spinifera Planktonic Autotroph +Gonyaulax verior Planktonic Autotroph -Heterocapsa triquetra Planktonic Autotroph +Lingulodinium polyedrum Planktonic Autotroph +Ostreopsis labens Benthic Mixotroph -Ostreopsis lenticularis Benthic Mixotroph -Ostreopsis ovata Benthic Autotroph -Ostreopsis siamensis Planktonic Autotroph -Peridinium quinquecorne Planktonic Autotroph +Peridinium venestrum Planktonic Heterotroph +Plagonidium belizeanum Benthic Autotroph -Prorocentrum caribbeanum Benthic Autotroph -Prorocentrum elegans Planktonic Autotroph +Prorocentrum hofmanianum Benthic Autotroph -Prorocentrum lima Benthic Mixotroph -Prorocentrum mexicanum Both Autotroph -Prorocentrum rhathymum Both Autotroph +Protoperidinium depressum Planktonic Heterotroph -Protoperidinium divergens Planktonic Heterotroph -Protoperidinium oblongum Planktonic Heterotroph -Protoperidinium oceanicum Planktonic Heterotroph -Protoperidinium pallidum Planktonic Autotroph -Protoperidinium steidingerae Planktonic Heterotroph -Pyrodinium bahamense v. b. Both Autotroph +Pyrophacus steinii Planktonic Autotroph -
Table3.Characteristicsofthe45dinoflagellatespeciesidentifiedin2002atDouglasCay.
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Dinoflagellate species DouglasCay
The Lair Benthic,Planktonic or
Both
Autotroph,Heterotroph or
MixotrophAkashiwo sanguinea + + Both AutotrophAlexandrium balechii - + Planktonic AutotrophBysmatrum caponii - + Both AutotrophBysmatrum subsalsum - + Benthic AutotrophCeratium furca + - Planktonic AutotrophCeratium pulchellum + - Planktonic AutotrophCeratium trichoceros + - Planktonic AutotrophCeratium tripos + - Planktonic AutotrophCochlodinium polykrikoides* + - Planktonic AutotrophCoolia monotis* hportotuAcihtneB++Coolia tropicalis hportotuAcinotknalP+-Dinophysis accuminata* - + Planktonic AutotrophDinophysis caudata* + + Planktonic AutotrophDinophysis rotundata* + - Planktonic MixotrophGambierdiscus belizeanus* - + Benthic AutotrophGambierdiscus polynesiensis* - + Benthic AutotrophGambierdiscus toxicus* + + Benthic AutotrophGonyaulax grindleyi + - Benthic AutotrophGonyaulax monocanta + - Planktonic AutotrophGonyaulax reticulatum* + - Planktonic AutotrophGonyaulax polygramma* + - Planktonic AutotrophGonyaulax spinifera + - Planktonic AutotrophHeterocapsa triquetra + + Planktonic AutotrophOstreopsis labens* + + Benthic MixotrophOstreopsis marina - + Benthic MixotrophOstreopsis siamensis* + - Benthic MixotrophPeridinium quinquecorne + + Planktonic AutotrophPeridinium quinquecorne + + Planktonic AutotrophPeridinium venestrum Planktonic HeterotrophPlagodinium belizeanum + + Planktonic AutotrophProrocentrum belizeanum* + + Benthic AutotrophProrocentrum elegans - + Planktonic AutotrophProrocentrum emarginatum + - Benthic AutotrophProrocentrum hoffmannianum* - + Benthic AutotrophProrocentrum mexicanum* + + Both AutotrophProrocentrum micans + - Planktonic AutotrophProrocentrum lima* + - Benthic AutotrophProrocentrum rathymum - + Both AutotrophProrocentrum ruetzlerianum - + Benthic AutotrophProrocentrum tropicalis - + Benthic AutotrophProtoceratium spinulosum + - Planktonic AutotrophProtoperidinium crassipes + + Planktonic HeterotrophPyrodinium bahamense v. b + - Planktonic AutotrophScrippsiella trochoidea - + Planktonic AutotrophScrippsiella tifida + + Planktonic Autotroph
Table4.BiodiversityofdinoflagellatesindetritusatDouglasCayandTheLair,TwinCays(2004)includingwhetherspeciesproducingtoxin(*)werepresent(+)or(-)absent.
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Dinoflagellate species Douglas Cay The LairTwin Cays
Reference
4002300230022002Akashivo sanguinea -* ++ ++ ++ Faust, M.A., 2004Bysmatrum caponii ++ + - + Faust M.A. & K.A. Steidinger, 1998Bysmatrum subsalsum - ++ ++ ++ Faust M.A. & K.A. Steidinger, 1998Ceratium furca - - - ++ Steidinger K.A. & K. Tangen, 1996Cochlodinium polykrikoides +* ++ ++ ++ Sournia, A., 1986Coolia monotis + + - + Faust, M.A., 1992Dinophysis caudata + ++ + + Balech, E., 1988Gonyaulax grindleyi + ++ - - Balech, E., 1988Gonyaulax polygramma + ++ - - Balech, E., 1988Gonyaulax spinifera + + - - Balech, E, 1988Heterocapsa triquetra - - ++ + Horiguchi, T. & Pienaar, R. N.,1991Lingulodinium polyedra + ++ - - Dodge, J.D., 1989Peridinium quinquecorne +++ ++ ++ ++ Horiguchi, T. & Pienaar, R.N., 1991Plagonidium belizeanum ++ - - ++ Faust M.A. and E. Balech, 1993Prorocentrum belizeanum - + - + Faust, M.A., 1993Prorocentrum caribbeanum + - ++ + Faust, M.A., 1993Prorocentrum elegans ++ ++ +++ + Faust, M.A., 1993Prorocentrum mexicanum + ++ ++ ++ Martin, G.W., 1929Pyrodinium bahamense ++ ++ - - Steidinger, K.A., 1983
Dinoflagellate species Produced Toxins Reference
Akashivo sanguinea Ichthyotoxins Carlson, R.D. & D.R. Tindall, 1985Bysmatrum caponii Non toxic Faust, M.A. & K.A. Steidinger, 1998Bysmatrum subsalsum Non toxic Faust, M.A. & K.A. Steidinger, 1998Ceratium furca Non toxic Steidinger, K.A. & T. Tangen, 1996Cochlodinium polykrikoides Ichthyotoxins Yuki, K. & S. Yoshimatsu, 1989Coolia monotis Cooliatoxin Holmes M.J. et al., 1995Dinophysis caudata Ichthyotoxin, DSP Okaichi, T., 1967Gonyaulax grindleyi Paralytic toxin Reinecke, P., 1967Gonyaulax polygramma Fish kills due to anoxia Koizumi, Y. et al., 1996Gonyaulax spinifera Non toxic Steidinger, K.A. & K. Tangen, 1996Lingulodinium polyedrum PSP toxins; STX Bruno, M.P. et al., 1990Peridinium quinquecorne Fish kills due to anoxia Fukuyo, Y. et al., 1990Plagodinium belizeanum Non toxic Faust, M.A. & E. Balech, 1993Prorocentrum belizeanum DSP toxins: DTXI, OA Morton, S.L. et al., 1998Prorocentrum caribbeanum Non toxic Faust, M.A., 1993Prorocentrum elegans Non toxic Faust, M.A. & E. Balech, 1993Prorocentrum mexicanum FAT Tindall D.R. et al., 1984Pyrodinium bahamense DSP, Ichthyotoxin Hallegraeff, G.M. 1993
Table5.Relativeabundanceofbloom-formingdinoflagellatespeciesatDouglasCayandTheLair,TwinCaysindifferentyears.*CellconcentrationsL-1are:cells+(<102),++(<103)and+++(<104).*Speciespresent(+)andspeciesabsent(–).
Table6.Toxinandnon-toxinproducingdinoflagellatesatDouglasCayandTheLair,TwinCays.Abbreviations:DSP=diarrheticshellfishpoisoning;FAT=fastactingtoxins;PSP=paralyticshell-fishpoisoning;andSTX=saxitoxin.
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DISCUSSION
Mandala’sPredictionValidatedforTropicalMangroveLagoons
ThehydrographicandresidualammoniadatafrombothDouglasCayandTheLairareconsistentwiththeselagoonalsystemsbeingstable,lowturbulenceenvironmentswithhighratesofnutrientregeneration(Fig.2,Tables1-2,Kibleretal.,2005).Elevatednutrientsinthesesystemslikelyresultfromtherapidrecyclingoforganicmatterbybacteria(ChróstandFaust,1999).Thisorganicmatteriscontributedbythesurroundingmangroveforest,seagrasses,macroalgalmeadowsandthedenseassemblageoffilter-feedinginvertebratesandspongesthatcolonizethepeatwallsandmangroveproproots(RützlerandFeller,1996).Theserelativelyhighernutrientlevelsarereflectedinthe4to40timeshigherchlorophyllabiomassinthelagoonscomparedtothesurroundingoligotrophicwatersofthecentralBelizeanreefsystemwhicharegenerally<0.2µgchlaL-1(Table1).Bothlagoonsarealsoprotectedfromwindmixingduetoprevailingwindsbythesurroundingmangrovetreeswhichfurtherpromotethestabilityofthewatercolumn.Margalef’sMandalapredictsthattheselow-turbulence,high-nutrientenvironmentswouldfavordinoflagellatespecies(Margalef,1978;Margalefetal.,1979;Smayda,1997;SmaydaandReynolds,2001).
Thereasonisrootedinthebasicbiologyoftheseorganisms.Dinoflagellatesaresensitivetophysicaldisturbancewithturbulenceregimesdisruptingtheirbasicmetabolismresultinginasignificantdecreaseindivisionratesrelativetootherspeciessuchasdiatoms(Sullivanetal.,2003).Dinoflagellatesarealsoknowntohaveslowergrowthratesatlownutrientconcentrationsthanmanyotheralgalgroups(BroekhuizenandOldman,2002).Itisonlyatrelativelyhighernutrientconcentrationsthatdinoflagellateshaveacompetitivegrowthadvantage.Thelowturbulence,highnutrientenvironmentlagoonssampledinthisstudywouldthereforerepresentidealenvironmentsfordinoflagellates.
Consistentwiththisprediction,boththeDouglasCayandLairlagoonscontainedarichassemblageofdinoflagellateswithatotalof52speciesbeingidentifiedfromDouglasCayand30fromTheLair(Tables3-5).Interestingly,only15specieswereidentifiedfrombothenvironments(Tables4and5).PlanktonicandautotrophicspeciescommontomoreoceanicenvironmentsweredominantinDouglasCayandincluderepresentativesfrom7genera:Ceratium,Cochlodinium,Dinophysis,Gonyaulax,Lingulodinium,Peridinium,andPyrodinium(Tables3and4).Ofthese,thearmoreddinoflagellatespecieswerethemostcommonwithunarmoredspeciessuchasAkashiwosanguinea,Amphidiniumcarterae,Cochlodiniumpolykrikoides,andHeterocapsatriquetrarepresentingaminorcomponent(Table3).Incontrast,benthicdinoflagellatescomposedagreaterproportionofthespeciesobservedinTheLair(Tables3and4).Becausedinoflagellatestendtobenichespecialists(Smayda,1997),thelargediversityofdinoflagellatespeciesrecoveredfrombothDouglasCayandTheLairimplythattheseenvironmentscontainadiversearrayoftemporallyandspatiallyvaryingniches.ThatamajorityofspeciesareuniquetoeachenvironmentalsoimpliesthattherearedifferentsourcepopulationsforDouglasCayandTheLair,orthattheselectionregimeissignificantlydifferent.
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Differencesinthewaterexchangeinthesesemienclosedmangrovelagoonsmayaccounttosomeextentfortheseobserveddifferencesinspeciescomposition(Levasseuretal.,1984).DouglasCayhasapredominantsillthatmayrestrictexchangetoagreaterextentthanoccursinLairwhichismainlyrestrictedduetothelengthofTheLairChannelandthelowtidalamplitude(<20cm)(MacintyreandRützler,2000).AlowerrateofexchangeinDouglaswouldfavorretentionofdinoflagellatecells(Villarealetal.,2000)andalargerportionofincomingorganicmatter,therebyincreasingthenutrientrecyclingcapacityofthesystem.DouglasCayisalsoalargerlagoonwithamorecomplicatedgeomorphology(unpublisheddata).Furthermore,DouglasCayreceivednutrientinputsfromtheabundantpelicansthatcometofishinthelagoonandroostinthemangroves.Treessurroundingthelagoonwereconsequentlystreakedwithguano.Thesehighlymobilepelicanpopulationsfeedonawiderangeoffoodsourcesandthusimportnutrientsdailytothelagoon.AlltheseconditionscombinetofosterthegreaterdiversityofdinoflagellatespeciesinDouglasCay.Despitethericherenvironment,DouglasCaystillprovidessufficientconfinementandnutrientsupplytoenhancetheproliferationofspecies-specificdinoflagellateblooms(Table5;SmaydaandReynolds,2001).TheobserveddiversityisalsohigherthangenerallyreportedatanygiventimeforthedeepoffshorewatersoftheEasternCaribbeanSea(Halim,1967;Hulburt,1968;Marshall,1973).
Anotherlow-turbulence,high-nutrientmicroenvironment,whichexiststoamuchlargerextentinTheLairthanintheDouglasCay,aretheloosedetritalmatswhichcovermuchofthebenthos.Theseflocculentmatssitontopofthesedimentswherenutrientfluxesarelikelytobehigh.Evidenceforthisnutrientfluxcanbefoundintherichassemblageofdinoflagellateandotheralgalspeciesthatoccupythesemats.Intheafternoon,oxygenproductionbyalgaeinthematcauseslargesectionstodetachandbeginfloatingupwardinthewatercolumn.ThisfloatingbiodetrituscarrieslargenumbersofdinoflagellatesintothewatercolumnandcanaccountforthehigherproportionofbenthicdinoflagellatesobservedinTheLaircomparedtothoseinDouglassCay,wherethebenthosisdominatedtoagreaterextentbyattachedmacrophytesandseagrasses(Tables3and4;Faust,2004).
Bloom-formingDinoflagellates
Inadditiontohighdiversity,weobservedanumberofdinoflagellatebloomsinbothlagoonalsystems.InDouglasCay,14bloom-formingspecieswereobservedin2002and15in2003.TheLairexperiencedaslightlysmallernumberofbloomsinvolving9speciesin2003and13in2004(Table5).Themostintensebloom-formingspecieswerePeridiniumquinquecorneinDouglasCayandProrocentrumelegansinTheLair.BloomsofGonyaulaxgrindleyiinDouglasCaywerealsosufficientlyhightodiscolorthewater.SimilarG.polygramma,bloomshavebeenreportedinManateeCay(MortonandVillareal,1998;Morton,2000).PreviousstudiesinDouglasCayconductedinMay1997,1999and2000alsofoundoneormore>20µmdinoflagellatesbloomedineachofthesestudiesreachingcellconcentrationsinexcessof1x10-3 cells L-1.Frequentbloomsthereforecanbeconsideredapersistentfeatureofthesesystemsfromyear-to-yearduringthe May study period.
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Ofthe19bloom-formingspeciesobserved,themostconsistentspeciesbetweensiteswereAkashivosanguinea,Bysmatrumsubsalsum,Cochlodiniumpolykrikoides,Dinophysiscaudata,Peridiniumquinquecorne,ProrocentrumelegansandP.mexicanum.Bloomstypicallyvariedinintensityanddurationwithmanylastingonlyafewdays.Apotentialreasonfortherapiddeclineofmanyofthesebloomsispredationbythelargenumberofheterotrophicciliates,nematodes,anddinoflagellatessuchastheProtoperidiniumspecies.Mixotrophicspecies,suchasthosethatbelongtothegeneraProrocentrumandOstreopsis,werealsocommonandareknowntofeedheterotrophicallyonothersmallmicroalgae(Faust,1998).Therapidgrowthanddeclineoftheseblooms,inconjunctionwithelevatednutrientconcentrations,mayimplyatightcouplingbetweenbottom-upnutrientdrivengrowthandtop-downcontrolbypredators.
Toxin-producingSpecies
Approximatelyhalfofthe19bloom-formingspeciesfoundineitherDouglasCayorTheLairareknowntoxinproducers(Table6).Thisimpliesthatthenaturaleutrophicationpresentintheselagoonsfavorsselectionoftoxicbloomformers.Itisnotcurrentlyknownifthesepotentiallytoxicbloom-formingspeciesactuallyareproducingtoxin.ThereisgrowingevidencethatHABtoxinscanserveanantigrazingfunction(Teegardenet.al.,2001).Thiswouldleadtothepredictionthat,ininstancesofintensegrazingpressure,bloomsproducingtoxinwillbefavored.Furtherresearchisneededtoaddressthispossibility.Ifgrazersfindthesespeciesunpalatableortoxic,itcanleadtosignificantandoftenadversealterationsofthefoodweb(PitcherandCockroft,1996).Itshouldbenotedthatallthetoxicbloom-formingspecieswerephototrophsasaremostreportedHABtaxa(SmaydaandReynolds,2001).
Margalef’sMadala,andtheresultsforDouglasCayandTheLair,alsohaveprofoundimplicationsforecosystemhealth.Boththetheoryandthespeciesfoundinthesenaturallyeutrophiedsystems(Tables3-5)wouldpredictthatasanthropogenicinputsintotheoligotrophicwatersoftheCaribbeanincrease,sowilltheproportionofdinoflagellatesintheassemblage.Thisspeciesshiftwouldlikelybemostpronouncedinshelteredbaysorotherregionswhereturbulenceandhydrodynamicdilutionareminimizedandintheveryregionsmostlikelytobereceivingincreasednutrientinputs.(Smayda,1997).Ifthetoxicdinoflagellatespeciesarefavoredduetoselectivegrazingpressuresorotherfactors,theirtoxinswilllikelyaccumulateinthefoodweb.Itisnowknownthatalltrophiccompartmentsofmarinefoodwebarevulnerabletothechronic,sublethalimpactsoftheseHABtoxins(Hallegraeff,1993).Incaseswheretoxinaccumulationissignificant,acuteimpactsincludingalterationoffood-webdynamicssufficienttoresultintrophicdysfunction,aswellasadverseeffectsonfisheriesandhuman health, can result.
Evenifthenontoxin-producingbloom-formingdinoflagellatescometopredominate,theycanstillcauseproblems(Alongi,1998).Thoughthesebloomsposenoseriousthreatintheenvironment,theyoftendiscolorthewaterandareconsideredtobeaestheticallyunpleasantandnoxious.Anoxiaformationresultingfromthedegradationoforganic-richmaterialderivedfromphytoplanktonbloomscanalsocausefishkills(PitcherandCockroft,1996;Koizumietal.,1996).Highammoniaconcentrationreleasedaftercelllysiscanadverselyaffectfishaswell(Ajanietal.,2001).
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CONCLUSIONS
TheresultsofthisstudydemonstratethatthephytoplanktonspeciescompositionoftwonaturallyeutrophiclagoonalsystemsintheBelizeanBarrierReefsystemconformtothepredicationsofMargelf’sMandala.Thistheorypredictsthathighnutrient,lowturbulencemarineenvironments,suchasthoseexaminedinthisstudy,willfavorthediversityandabundanceofdinoflagellates.Consistentwiththisprediction,arichassemblageofdinoflagellatesisfoundinbothlagoonalsystems.Approximately19ofthesespecieswereconsistentbloomformers,andofthesebloomformers,approximatelyhalfwereknowntoxinproducers.Theecologyandtaxonomyofeightofthesebloomformersweredescribedindetail.IfthepredictionsofMargalef’sMandalaholdtrue,thenincreasedanthropogenicnutrientinputsintotheoligotrophicCaribbeanwatersmayfavorashiftinspeciescompositiontowardpotentiallytoxicdinoflagellatespecies.Thisshiftcouldprofoundlyalterthefood-webdynamicsaswellasadverselyaffectingfisheriesandhuman health.
ACKNOWLEDGEMENTS
WethankDr.KlausRützlerattheNationalMuseumofNaturalHistory(NMNH),SmithsonianInstitution,foruseofthefacilitiesatCarrieBowCayFieldStation,Belize.Wearealsogratefultonumerousindividualswhocontributedtoitssuccessanddeservecredithere:Dr.IanG.Macintyreforhisvaluablecommentsonthismanuscript;Ms.MollyRyanforherartworkandgraphics;andMrs.JuditA.Quasneyforphotographiclayoutsthatpavedthewayforpublishingthisresearchpaper.IconveyaspecialthankstoScottWhitakerintheSEMlaboratoryfortechnicalassistanceandMikeCarpenterforlogisticsupport,NMNH.ThisinvestigationwassupportedbygrantsfromtheCaribbeanCoralReefEcosystemprogram(CCRE)attheNationalMuseumofNaturalHistory.ThispaperisContributionNo.729fromtheCCREProgram.
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Figures 2-6. MorphologyofGonyaulax grindleyidinoflagellatespeciescausingwaterdiscolorationinsamplingareasillustratedinscanningelectronmicrographs,anddissectedplatetabulationsinlinedrawings.
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Figures 7-10.MorphologyofPeridinium quinquecornedinoflagellatespeciesassociatedinfloatingdetritusinTheLairatTwinCaysillustratedinscanningelectronmicrographs,anddissectedplatetabulationsinline drawings.
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Figures 11-12.MorphologyofBysmatrum caponii sanddwellingdinoflagellatespeciesidentifiedfromDouglas Cay and The Lair at Twin Cays sampling areas illustrated in scanning electron micrographs anddissectedplatetabulationsinlinedrawings.
Figures 13-14.MorphologyofDinophysis caudata planktonicdinoflagellatespeciesidentifiedfromDouglas Cay and The Lair at Twin Cays sampling areas illustrated in scanning electron micrographs, anddissectedplatetabulationsinlinedrawings.
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Figures 15-18.MorphologyofGonyaulax polygramma cosmopolitanoceanic,red-tidedinoflagellatespeciesidentifiedfromDouglasCayillustratedinscanningelectronmicrographsanddissectedplatetabulationsinlinedrawings.
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Figures 19-22. MorphologyofGonyaulax spinifera, anoceanicred-tidedinoflagellatespeciesidentifiedfromDouglasCaysamplingarea,illustratedinscanningelectronmicrographsanddissectedplatetabulationsinlinedrawings.
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Figures 23-26. MorphologyofLingulodinium polyedrumoceanicbioluminescentdinoflagellatespeciesidentifiedfromDouglasCaysamplingareaillustratedinscanningelectronmicrographsanddissectedplatetabulationsinlinedrawings.
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Figures 27-30. MorphologyofPyrodinium bahamense var.bahamenseplanktonicworldwidedistributeddinoflagellatespeciesidentifiedfromDouglasCaysamplingareaillustratedinscanningelectronmicrographs.
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