Coral Reef Health Indices versus the Biological, Ecological and Functional Diversity of Fish and

19 Pages·2016·1.25 MB·English

RESEARCHARTICLE
versus
Coral Reef Health Indices the
Biological, Ecological and Functional Diversity
of Fish and Coral Assemblages in the
Caribbean Sea
LeopoldoDíaz-Pérez1,FabiánAlejandroRodríguez-Zaragoza1*,MarcoOrtiz2,Amílcar
LevíCupul-Magaña3,JoseD.Carriquiry4,EduardoRíos-Jara1,AlmaPaolaRodríguez-
Troncoso3,MaríadelCarmenGarcía-Rivas5
a11111
1 LaboratoriodeEcosistemasMarinosyAcuicultura,DepartamentodeEcología,CentroUniversitariode
CienciasBiológicasyAgropecuarias,UniversidaddeGuadalajara,ZapopanJalisco,México,2 Laboratorio
deModelamientodeSistemasEcológicosComplejos(LAMSEC),InstitutodeCienciasNaturalesAvH,
FacultaddeCienciasdelMaryRecursosBiológicosInvestigacionesOceanológicas,FacultaddeRecursos
delMar,UniversidaddeAntofagasta,Antofagasta,Chile,3 DepartamentodeCienciasBiológicas,Centrode
InvestigacionesCosteras,CentroUniversitariodelaCosta,UniversidaddeGuadalajara,PuertoVallarta,
Jalisco,México,4 InstitutodeInvestigacionesOceanológicas,UniversidadAutónomadeBajaCalifornia,
Ensenada,BajaCalifornia,México,5 ReservadelaBiosferaBancoChinchorro-CONANP.Chetumal,
OPENACCESS
QuintanaRoo,México
Citation:Díaz-PérezL,Rodríguez-ZaragozaFA,
*[email protected]
OrtizM,Cupul-MagañaAL,CarriquiryJD,Ríos-Jara
E,etal.(2016)CoralReefHealthIndicesversusthe
Biological,EcologicalandFunctionalDiversityofFish
andCoralAssemblagesintheCaribbeanSea.PLoS Abstract
ONE11(8):e0161812.doi:10.1371/journal.
pone.0161812
ThisstudyevaluatedtherelationshipbetweentheindicesknownastheReefHealthIndex
Editor:CarloNikeBianchi,UniversitadegliStudidi (RHI)andtwo-dimensionalCoralHealthIndex(2D-CHI)anddifferentrepresentativemet-
Genova,ITALY
ricsofbiological,ecologicalandfunctionaldiversityoffishandcoralsin101reefsites
Received:October3,2015 locatedacrosssevenzonesinthewesternCaribbeanSea.Speciesrichnessandaverage
Accepted:August12,2016 taxonomicdistinctnesswereusedtoassesbiologicalestimation;whileecologicaldiversity
wasevaluatedwiththeindicesofShannondiversityandPielou´sevenness,aswellasby
Published:August31,2016
taxonomicdiversityanddistinctness.Functionaldiversityconsideredthenumberoffunc-
Copyright:©2016Díaz-Pérezetal.Thisisanopen
tionalgroups,theShannondiversityandthefunctionalPielou´sevenness.Accordingtothe
accessarticledistributedunderthetermsofthe
CreativeCommonsAttributionLicense,whichpermits RHI,57.15%ofthezoneswereclassifiedaspresentinga"poor"healthgrade,while
unrestricteduse,distribution,andreproductioninany 42.85%werein"critical"grade.Basedonthe2D-CHI,28.5%ofthezoneswerein
medium,providedtheoriginalauthorandsourceare
"degraded"conditionand71.5%were"verydegraded".Differencesinfishandcoraldiver-
credited.
sityamongsitesandzonesweredemonstratedusingpermutationalANOVAs.Differences
DataAvailabilityStatement:Allrelevantdataused
betweenthetwohealthindices(RHIand2D-CHI)andsomeindicesofbiological,ecological
forthisworkareavailableasaSupporting
andfunctionaldiversityoffishandcoralswereobserved;however,onlytheRHIshoweda
Informationfile,publishedwiththismanuscriptas
Excelfile. correlationbetweenthehealthgradesandthespeciesandfunctionalgrouprichnessoffish
atthescaleofsites,andwiththespeciesandfunctionalgrouprichnessandShannondiver-
Funding:ThisworkwassupportedbytheNational
CommissionofNaturalProtectedAreas sityofthefishassemblagesatthescaleofzones.Noneofthehealthindiceswererelatedto
(PROCODES2007,2008,2009,2011),Universidad themetricsanalyzedforthecoraldiversity.Ingeneral,ourstudysuggeststhattheestima-
deGUadalajara(projectP3E2009-2011),University
tionofhealthindicesshouldbecomplementedwithclassiccommunityindices,orshouldat
ofBajaCalifornia–NationalBiodiversityCommission
(projectGM006),andWorldWildlifeFund-CA
(AgreementKL82).Thefundershadnoroleinstudy
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CoralReefHealthIndices
design,datacollectionandanalysis,decisionto leastincludediversityindicesoffishandcorals,inordertoimprovetheaccuracyoftheesti-
publish,orpreparationofthemanuscript. matedhealthstatusofcoralreefsinthewesternCaribbeanSea.
CompetingInterests:Theauthorshavedeclared
thatnocompetinginterestsexist.
Introduction
Coralreefshavesufferedsignificantimpactsoverrecentyearsasaresultoftheimpactof
humanandnaturaldisturbancesontheirbiodiversityandecosystemfunctioning[1–3].These
ecosystemsarefragileandsensitivetodisturbanceandareatgreaterriskofdegradationthan
othermarinesystems[4].Inrecentdecades,arapiddeclineincoralcoveragehasbeendocu-
mentedworldwide,withtotallossesof19%oflivecoralandanother15%ofthecoralcover
classifiedasseriouslythreatened[5].Thissituationistheresultofsynergicfactorssuchasover-
fishing,eutrophicationofseawaterbyexcessiveinputofnutrients,sedimentation,increased
temperatures,oceanacidification,hurricanesandtropicalstorms,amongothers[6–11],and
hasgeneratedanincreaseincoralbleachingeventsandmortalities,overgrowthoffleshy
macroalgae,presenceofdiseasesandadeclineinphysiologicalprocessessuchasgrowthand
calcification[12–14].Thishasdiminishedthehealthorfitnessofthecoralreefs,whichare
nowconsideredtobeincrisisatagloballevel[15–16].
Asaconsequence,researchexploringstrategiesofconservation,aswellstudiesofthehealth
ofcoralreefs,haveincreasedconsiderably[17–19].Todate,reefhealthhasbeenevaluateda
rangeofindicesandsingleindicators,including:totallivecoralcoverandmacroalgaecover
[20],richnessornumberofspecies[21,22,23],Shannondiversityindex(H’)[21,22,23],Pielou
´sevennessindex(J’)[21,22,23],Simpson´sdominanceindex(D)[24],coralmortalityindex
[25],coraldamageindex(CDI)[26],reefconservationvalue[27],deteriorationindex(DI)
[27],coralconditionindex(CCI)[27,28],reefconditionindex(RCI)[29].Someoftheseindi-
ces,suchasthoseofreefcondition(RCI)andcoralmortality,arenowindisusebuttherestare
stillinapplication.
IntheCaribbeanSea,theHealthyReefsInitiative(HRI),formerlycalledtheHealthyMeso-
americanReefEcosystem(HMRE),isaninternationalandinter-institutionalinitiativefocused
onevaluationofreefhealth[18,30]andcollaborativeevaluationofmanagementefforts
throughEco-Audits(See.www.healthyreefs.org);theydevelopedaReefHealthIndex(RHI),
whichcombinesfourindicatorsforevaluation:livecoralcoverage,fleshymacroalgaecoverage,
biomassofherbivorousfishandbiomassofcommercialfishinordertoconveyonesimplified
measureofreefhealthtopolicymakersandthegeneralpublic.Theseindicatorsareaveraged
inordertoobtainvaluesonarangefrom1to5,wherethevalueof1ischaracterizedas“Criti-
cal”,valueof2as“Poor”,valueof3as“Fair”,valueof4as“Good”andvalueof5as“Very
Good”[31,32].Therecent“MesoamericanReef”(MAR)evaluationsreportedanincreasein
thepercentageofreefsincriticalcondition,from6%in2008to30%in2010.Inareportof
2012,thislattervaluehaddecreasedto24%andanimprovementinthehealthofthereefswas
reportedin2015,sinceonly17%oftheevaluatedsiteswerestillconsideredtobeincriticalcon-
ditionatthattime[33–34,35].
TheCoralHealthIndex(CHI)[36]isanotherindicatorofcoralreefhealthandhasbeen
usedontheLineandHawaiianIslandsintheCentralPacificOcean,ontheEastcoastofKenya
andTanzaniaintheIndianOceanandintheDutchAntillesintheCaribbeanSea[36].This
indexusesthreeindicators:benthos(includingthecoveragevaluesofbothencrustingcoralline
algaeandlivecoral),reeffish(totalbiomassoffish)andmicrobes(concentrationofVibrio
spp.).Theseindicatorsareaveragedinordertoobtainfivehealthgradesinvaluesranging
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fromzerotoone,0.0–0.20(verydegraded),0.21–0.40(degraded),0.41–0.60(Fair),0.61–0.80
(healthy),0.81–1.0(veryhealthy).Duetotherelativenoveltyofthebacterialcomponent,there
islittlepertinentinformationavailable.However,Kaufmanetal.(2011)[36]definedthetwo-
dimensionalCoralHealthIndex(2D-CHI),whichwasonlyestimatedwithdatapertainingto
thebenthosandfish.ThismodificationhasbeensuccessfullyusedinmanyplacesintheCarib-
beanSeaandPacificandIndianOceans,indicatinghealthdifferencesbetweenprotectedand
non-protectedareasandbecominganeffectiveindictorwithwhichtoevaluatedifferencesin
temporalandspatialhealth[36].
Thehealthstatusofcoralreefsandothertypesofaquaticecosystemshasalsobeenevaluated
fromacommunityecologyperspectivethatincorporatesattributessuchasspeciesrichness,rela-
tiveabundance,speciesevenness,rarespeciesandcoralcover[37,38,39].Itconsiderschangesin
speciesdiversityasanindicatorofdisturbance[40,41].Inthissense,biodiversityconservation
favorsthenaturalresilienceofthecoralreefstorecoverfromdisturbanceandmaintaintheireco-
systemservices[42].Structuralchangesinthereefecosystemsaffecttheirbiodiversity(e.g.abun-
danceoftaxa)and,withthis,theirecosystemprocesses[43].Theseindicestypesconsiderthe
proportionalabundancesoftaxa,basedondifferentaspectsofthediversity.Theycanbeofstatis-
ticaltype,orinvolveinformationtheory,dominanceofspeciesandtaxonomicdiversity[41].In
coralreefs,thesemetricshavebeenfocusedontheassemblagesofreeffishandcoralspecies[44–
46].Thishasrevealedthatdeclineinspeciesdiversityespeciallythatofrarespeciesisoftenasso-
ciatedwithreducedcoralcoverandincreasedmacroalgae[47–50].
Animportantadvanceiscurrentlytakingplaceintheassessmentofcoralreefhealth,sup-
portedmainlybycommunityattributessuchasbiological,ecologicalandfunctionaldiversity
indices.Nevertheless,nostudieshavebeenconductedtodatethatevaluatetherelationship
betweentheRHIand2D-CHIindicesandthoseofthebiological,ecologicalandfunctional
diversityofreeffishandcoralassemblages.TheRHIand2D-CHIarecommonlyimplemented
byauthorities,managersandinstitutionsinordertoevaluatethehealthandconservationof
coralreefsindifferentpartsoftheworld,butthisremainstobeassessedinmanylocationsof
theMesoamericanCoralReef.Theobjectiveofthisstudywasthereforetodeterminetherela-
tionshipbetweentheRHIand2D-CHIandindicesofthebiological,ecologicalandfunctional
diversityoftheassemblagesofreeffishandhermatypiccoralsofdifferentcoralreefsofthe
westernCaribbean[45,46,48,49,51].
MaterialsandMethods
Studyarea
ThestudyareacoveredthecoastsofMexico,Guatemala,HondurasandNicaragua,where
101samplingsitesinsevenzoneswereevaluated.Thefirstthreeoftheaforementionedcoun-
trieshaveterritoriesontheMesoamericanReefandthefourthispartofthewesternCaribbean.
Thestudyzoneswere:Cancún,BancoChinchorroandXcalak(Mexico);PuntaManabique
(Guatemala);CayosCochinosandMediaLuna(Honduras);andCayosMiskitos(Nicaragua)
(Fig1).TheMesoamericanReefcomprisesthelargestbarrierreefinthewesternCaribbean.
Thissystempresentsalargevarietyofreefstructures,notableamongwhicharefouratolls
locatedataconsiderabledistancefromthecoast.Itextendsoveradistanceof~1000kmand
includesthenorthernYucatánPeninsulaandtheBelize,GuatemalaandHondurascoastlines
[49,52].
Fieldandlaboratorywork
Ahierarchicalsamplingdesignwasconductedforeachzoneanditsrespectivesamplingsites.
Samplingwasconductedwiththecooperationofdifferentgovernmentalinstitutions,non-
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Fig1.StudyareawithzonesofcoralreefsinthewesternCaribbean.Cancún,BancoChinchorro,
Xcalak,PuntaManabique,CayosCochinosMediaLuna,CayosMiskitos.
doi:10.1371/journal.pone.0161812.g001
governmentalorganizations(NGOs)anduniversities,includingtheMexicanNationalCom-
missionforProtectedNaturalAreas(CONANP,byitsSpanishacronym),TheNicaraguan
InstituteofFishery(INPESCA,byitsSpanishacronym),WorldWildlifeFund-CentralAmer-
ica(WWF-CA),CayoCochinosFoundation(Honduras),MarioDaryFoundation(Guate-
mala),UniversityofGuadalajara(UDG,Mexico)andtheAutonomousUniversityofBaja
California(UABC,Mexico).
Atotalof507transectswereconductedbetween2007and2011.Ateachtransect,visualfish
censuses(2x50m)andcharacterizationofthebenthicstructureusingvideotransects(~0.8x
50m)withaunderwatercamera(JVCEverio-HDHardDiskCamcorderandSONYHandy-
camHDAVCHD,resolutionof1920x1080i)wereconductedindepthsfrom3to~30matall
ofthesamplingsites(S1Fig).Thefishandbenthiccomponentswererecordedsimultaneously.
Thefishcensusesdocumentedspeciesrichness,aswellassizeandabundance.Biomasswas
estimatedpertransect,siteandzoneusingtheexponentialfunctionW=aLb,whereWisthe
biomass(gm-2),aandbcorrespondtotheconstantsofthelength-weightrelationshipobtained
fromthedatabaseFishBase1andListhelengthvalueoftheweightedaveragesize[53].Fish
functionalgroupsweredeterminedbasedontheirdifferenttrophic,morphologicalandfunc-
tionalcharacteristics(S1Table)[54].
Foreachvideotransect,40quadrants(~0.8x~0.6m)and13fixedpointswereexamined
usingconventionalvideo-processingsoftware(CyberLinkPowerDVD13)inordertoestimate
therichness,coverandfunctionalgroupsofhermatypiccorals,aswellasthecoverageoffleshy
andencrustingcorallinealgae[48,55].CoralcolonieswereclassifiedusingthecriteriaofArias-
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Gonzálezetal.(2008)[45],basedonthemorphologyofthecolony(i.e.semispherical,boulder,
encrusting,foliose,fleshy,branching,columnar,finger,plateandbraincorals).
Dataanalysis
TheRHI,developedbyHealthyReefsforHealthyPeople[31–34],wasestimatedusingfour
indicators:i)livecoralcover;ii)fleshymacroalgaecover;iii)biomassofherbivorousfish
(g100m-2),ofthefamiliesScaridaeandAcanthuridae;andiv)biomassofcommercialfish
(g100m-2),usingonlythefamiliesLutjanidaeandSerranidae.Thesefamiliesoffishwereused
becauseoftheirimportantfunctionalrolewithincoralreefs;thescaridsandacanthuridsare
consideredthemostimportantgrazerswithinthereefs,sincetheyreducetheovergrowthoffle-
shymacroalgae.Snappers(Lutjanidae)andserranidsareofimportantcommercialvalue,but
alsoplayanimportanttrophicroleascarnivoresthatexertastrongpredatoryinfluenceinthe
coralreefs.Themeanvalueofeachindicatorwasconvertedtoanordinalscale,withvaluesof1
(“critical”)to5(“verygood”),producingfivegradesofhealth(S2Table)[31–33].The2D-CHI
indexdevelopedbyKaufmanetal.(2011)wasestimatedbasedonthecombinationoftwodiag-
nosticparameters:benthosandfish[36].Duetothelackofpertinentdata,abacterialdiagnos-
ticparameterwasnotusedinthepresentstudy[36].Thediagnosticparameterswerescaled
fromavalueofzero(“verydegraded”)toone(“veryhealthy”),producingfivegradesofhealth
(S3Table).Estimationofthebenthoswasobtainedusingthemeanlivecoralandencrusting
corallinealgaevaluesanddividingby100.Estimationofthefishconsideredthetotalbiomass
(gm-2)asafractionof500gm-2,withsubsequentaveragingofthevaluesofeachparameterin
ordertoobtainthefinal2D-CHIvalue[36].
Thebiological,ecologicalandfunctionaldiversityofthefishandcoralcomponentswasesti-
mated(separately)foreachbiologicalgroupattransectscale,andmeanvalueswerethencalcu-
latedatsamplingsiteandreefzonescale.Theanalysisofbiologicaldiversityconsideredspecies
richness(S)andaveragetaxonomicdistinctness(Δ+)[56–58].Thetrajectorylengthswere
weighted:ω=1,speciesofthesamegenus;ω=2,speciesofthesamefamilybutofadifferent
genus;ω=3,speciesofthesameorderbutofadifferentfamilyandgenus;ω=4,speciesofthe
sameclassbutofadifferentorder,familyandgenus[58].Ecologicaldiversitywasevaluated
usingShannondiversity(H’,nats),Pielou´sevenness(J’),taxonomicdiversity(Δ)andtaxo-
nomicdistinctness(Δ(cid:1))[58–59].Functionaldiversityconsideringfunctionalrichness(=num-
beroffunctionalgroups)andfunctionalheterogeneitywasestimatedwithShannondiversity
andfunctionalPielou´sevenness[60].
Differentstatisticalmodelswereusedtoevaluatetherelationshipbetweenthereefhealth
indices(RHIand2D-CHI)andtherepresentativemetricsofbiodiversity.Multi-scaleanalyses
wereappliedconsideringthebiological,ecologicalandfunctionalspatialvariationamongsites,
reefzonesanddegreesofhealthoftheRHIor2D-CHIindices,throughpermutationalanalysis
ofvariance(ANOVA)basedonmatricesofEuclideandistances[61].Thisnon-restricted
methodwasutilizedsincethedatadidnotfulfillthecriteriaforparametricstatistics[61–62].
Thefactorsconsideredinthemodelswere:sites(randomeffect,101sites),zones(random
effect,sevenzones)andgradesofhealthintheRHI(fixedeffect,threeorfourgrades)and
2D-CHI(fixedeffect,twoorthreegrades).Allofthemodelsanalyzedwerethusofmixed
effectsintype.
Model1wasacompletelynestedtwo-wayANOVAdesign:Y=zones +sites(zones)+ε ,
i j i ij
whereYisthedependentvariable.Thisdesignanalyzedthespatialvariationoftherepresenta-
tivemetricsoffishandcoraldiversity(Y)amongsamplingsitesandreefzones.Similarly,
model2consideredanestedtwo-wayANOVA,Y=healthgrade +site(healthgrade)+ε ,
i j i ij
whichexplainedthevariationinthebiological,ecologicalandfunctionaldiversityamong
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differenthealthgrade(RHIand2D-CHI,separately)atthescaleofsites.Model3corresponded
toanestedthree-wayANOVA,Y=healthgrade +zones(healthgrade)+sites (zones(health
i j i k i
grade))+ε ,whichexplainedthevariationofthemetricsofdiversityusedamongthediffer-
i ijk
enthealthgradeestimatedbyRHIand2D-CHIseparatelyatthescalesofsiteandzone.
TherelationshipbetweenRHIand2D-CHI,withrespecttothemetricsofbiological,eco-
logicalandfunctionaldiversity,wasevaluatedthroughlinearandnon-linearregressionsusing
anexponentialraisedtomaximumwith2parametersfunction(Y=a(1−e−bx)),wherethe
RHIand2D-CHIweretheindependentvariablesandthedifferentdiversitytypeswerethe
dependentvariables.Inaddition,Pearsoncorrelationswereusedamongallofthesevariablesat
thescalesofsiteandzone.Alloftheanalysesofbiological,ecologicalandfunctionaldiversity,
aswellasthestatisticalmodels,wereperformedusingthesoftwarePrimer6+Permanova.The
linearandnon-linearregressionswereperformedusingSigmaPlot111.
Results
Reefhealthatthescalesofsitesandzones
Reefhealthatthescaleofsites. TheRHIindexshowedthatthehealthconditionofthe
coralreefsofCancúnMexicowasfairinRadioPirataandpoorinBonanza,Chitales,Cuevones,
ElBajito,LaBocana,PuntaNizucandManchones(Fig2A).The2D-CHIindicatedthatthe
healthgradeofElBajito,LaBocana,PuntaNizucandRadioPiratawasdegraded,whilethe
remainingsiteswereverydegraded(Fig3A).AccordingtotheRHI,thesitesChancay,Colora-
dos,CuevaTiburones,LaCalderaandPenélopeinthezoneofBancoChinchorrowereincriti-
calconditionandonlyLaBalizapresentedapoorconditionofhealth(Fig2B).However,the
2D-CHIanalysisindicatedthatallofthesesitespresentedaverydegradedconditionofhealth
(Fig3B).AccordingtotheRHIand2D-CHI,theconditionsofthesitesofthezoneofXcalak
werecriticalandverydegraded,respectively(Figs2Cand3C).
InthezoneofPuntaManabique,Guatemala,allofthesiteswereinacriticalcondition
accordingtotheRHI(Fig2D),whilethe2D-CHIindicatedthatthesesiteswereinvery
degradedcondition(Fig3D).InthezoneofCayosCochinos(Honduras),theRHIanalysis
showedthatRoatanBankpresentedafairhealthgrade,whilethesitesPelicanosandLaGru-
perawereinpoorconditionandMariposalesandSalamandingawereincriticalcondition(Fig
2E).Accordingtothe2D-CHI,RoatanBankwasdegraded,whiletheothersiteswerevery
degraded(Fig3E).InthereefsofMediaLunainHonduras,theRHIresultsindicatedthree
siteswithacriticalhealthgrade(ML1,ML3andML4),withafurthertwoclassifiedaspoor
(ML2andML5)andonewithfaircondition(ML6)(Fig2F).Evaluationwiththe2D-CHI
showedthatthreeofthesiteswereinaverydegradedhealthgrade(ML1,ML2andML3),
whiletheotherthreesitesweredegraded(Fig3F).Finally,thesitesofCayosMiskitos,Nicara-
guawereinpoorconditionaccordingtotheRHI(Fig2G),however,theresultsobtainedfrom
the2D-CHIindicatedthatPorgeeReefandLamarkaReefwereinaverydegradedhealthgrade
whiletherestofthesitesweredegraded(Fig3G).
Reefhealthatthescaleofzones. TheRHIshowedthatMediaLuna,CayosMiskitos,
CayosCochinosandCancuncoralreefpresentedapoorhealthgrade,withCancunandCayos
Miskitospresentingthebesthealthofallofthesereefs.Theworstconditionswereobservedat
BancoChinchorro,XcalakandPuntaManabiquepresentedacriticalhealthgrade(Fig4A).
The2D-CHIindicatedadegradedconditioninMediaLuna,andCayosMiskitos,where
althoughMediaLunaonceagainpresentedthebesthealthgradeofthisgroup.Incontrast,
Xcalak,BancoChinchorro,CayosCochinos,CancunandPuntaManabiquepresentedanout-
standingdegradedhealthgrade,withPuntaManabiquepresentingthehighestdegradation
(Fig4B).Ingeneral,theRHIfoundthat57.15%ofthereefzonespresentedapoorhealthand
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Fig2.CoralreefhealthinsamplingsitesevaluatedwithRHI.a)Cancun:Bonanza(Bo),Chitales(Ci),Cuevones(Cu),El
Bajito(EB),LaBocana(LB),Manchones(Ma),PuntaNizuc(PN),RadioPirata(RP);b)BancoChinchorro:Sixsitesfor
Baliza(Ba1,Ba2,Ba3,Ba4,Ba5,Ba6),sixsitesforChancay(Ch1,Ch2,Ch3,Ch4,Ch5,Ch6),sixsitesforColorados(Co1,
Co2,Co3,Co4,Co5,Co6),sixsitesforCuevaTiburones(CT1,CT2,CT3,CT4,CT5,CT6),sixsitesforLaCaldera(LC1,
LC2,LC3,LC4,LC5,LC6),andsixsitesforPenelope(Pe1,Pe2,Pe3,Pe4,Pe5,Pe6);c)Xcalak:sixsitesforAlejandro
Reefs(Al1,Al2,Al3,Al4,Al5,Al6),sixsitesforHobná(Ho1,Ho2,Ho3,Ho4,Ho5,Ho6),sixsitesforBacalarChico(Bac1,
Bac2,Bac3,Bac4,Bac5,Bac6),sixsitesforPozaRica(PZ1,PZ2,PZ3,PZ4,PZ5,PZ6),andsixsitesforRioHuach(RH1,
RH2,RH3,RH4,RH5,RH6);d)PuntaManabique:Piedradelabarracuda(PBA),BajodelCabo(BCA),Motaguilla(Mo);e)
CayosCochinos:threesitesforPelicanos(PL1,PL2,PL3),threesitesforGrupera(Gr1,Gr2,Gr3),twositesfor
Mariposales(Mr1,Mr2),twositesforSalamandinga(Sa1,Sa2),andtwositesforRoatanBank(RB1,RB2);f)MediaLuna:
sixsitesforMediaLuna(ML1,ML2,ML3,ML4,ML5,ML6)andg)CayosMiskitos:LondonReef(LOR),NeeReef(NER),
PorgeeReef(POR),LamarkaReef(LAR),MartinezReef(MAR),CayoMuerto(MUK).Errorbarscorrespondtostandard
deviationvalue.
doi:10.1371/journal.pone.0161812.g002
42.85%wereincriticalcondition,butthe2D-CHIindicatedthat28.5%and71.5%ofthezones
presenteddegradedandverydegradedconditions,respectively.
Indicesofhealthvs.biological,ecologicalandfunctionaldiversity
TheresultsofModel1showedthatthemajorityoftheindicesofthebiological,ecologicaland
functionaldiversityoffishandcoralvariedsignificantlyamongzonesandamongthesites
withineachzone(Table1).Nevertheless,nodifferenceswereobservedbetweenzonesandsites
withrespecttothetaxonomicdiversity(Δ)estimatedforfishandcorals,norinthePielou´s
evennessestimatedforcoralsamongzones(Table1).However,theindicesoffunctionaldiver-
sitydidshowsignificantdifferencesatthescalesofzoneandsite(Table1).
Model2showedthatthemajorityoftheindicesrepresentativeofthefishandcoraldiversity
(separately)didnotpresentsignificantdifferencesamongthecategoriesoftheRHIand
2D-CHI,exceptfortheaveragerichnessofspeciesandfunctionalgroupsoffish.Moreover,
speciesevennessdifferedsignificantlyamongthehealthgradesofbothindices.FunctionalPie-
lou´sevennessalsodifferedamongthehealthgradesproducedbythe2D-CHI(Table2).The
functionalShannondiversityofthehermatypiccoralsvariedsignificantlyamongthehealth
gradesoftheRHIand2D-CHI,whilefunctionalPielou´sevennessonlydifferedwiththeRHI
(Table2).Incontrast,theanalysesconductedamongsitesperofhealthgrade(RHI-2D-CHI)
showedthatthemajorityofindicesrepresentativeofthediversityoffishandcoralsdifferedsig-
nificantlyamongsites(Table2).
Nosignificantdifferenceswereobservedwithrespecttothetaxonomicdiversityoffishand
coralsinbothhealthindicesandnodifferenceswereobservedintheaveragecoralrichness
(Table2).
Model3showedthatthemajorityoftheindicesofthebiological,ecologicalandfunctional
diversityoffishandcorals(separately)didnotdiffersignificantlyamongthecategoriesofthe
RHIand2D-CHI(Tables3and4),exceptforthetaxonomicdistinctnessoffishamonghealth
gradesoftheRHIandfunctionalShannondiversityofcoralsinthe2D-CHI.Theanalyses
amongzonesperhealthgradeoftheRHIor2D-CHIalsorevealedsignificantdifferencesin
mostofthediversityindicesforfish(Table3)andcorals(Table4).
Nodifferenceswerefoundinthetaxonomicdiversityoffishinbothhealthindices,orin
theirtaxonomicdistinctnesswiththeRHI.Regardingthecorals,Pielou´sevennessandtaxo-
nomicdiversitydidnotpresentdifferencesineitherofthetwohealthindices(Table4).Finally,
atthescaleofsitesnestedperzone,mostoftheanalysisshowedsignificantdifferencesamong
theindicesofbiological,ecologicalandfunctionaldiversity;however,nodifferencewas
detectedinthetaxonomicdiversityofthefish(Table3)orcorals(Table4).
Theresultsofthelinearandnon-linearregressionsshowedthatthehealthgradesofthe
2D-CHIwerenotrelatedtothediversityindicesoffishandcorals(separately)ateitherzoneor
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CoralReefHealthIndices
Fig3.CoralreefhealthinsamplingsitesevaluatedwithCHI.a)Cancun:Bonanza(Bo),Chitales(Ci),Cuevones
(Cu),ElBajito(EB),LaBocana(LB),Manchones(Ma),PuntaNizuc(PN),RadioPirata(RP);b)BancoChinchorro:
SixsitesforBaliza(Ba1,Ba2,Ba3,Ba4,Ba5,Ba6),sixsitesforChancay(Ch1,Ch2,Ch3,Ch4,Ch5,Ch6),sixsitesfor
Colorados(Co1,Co2,Co3,Co4,Co5,Co6),sixsitesforCuevaTiburones(CT1,CT2,CT3,CT4,CT5,CT6),sixsites
forLaCaldera(LC1,LC2,LC3,LC4,LC5,LC6),andsixsitesforPenelope(Pe1,Pe2,Pe3,Pe4,Pe5,Pe6);c)
Xcalak:sixsitesforAlejandroReefs(Al1,Al2,Al3,Al4,Al5,Al6),sixsitesforHobná(Ho1,Ho2,Ho3,Ho4,Ho5,Ho6),
sixsitesforBacalarChico(Bac1,Bac2,Bac3,Bac4,Bac5,Bac6),sixsitesforPozaRica(PZ1,PZ2,PZ3,PZ4,PZ5,
PZ6),andsixsitesforRioHuach(RH1,RH2,RH3,RH4,RH5,RH6);d)PuntaManabique:Piedradelabarracuda
(PBA),BajodelCabo(BCA),Motaguilla(Mo);e)CayosCochinos:threesitesforPelicanos(PL1,PL2,PL3),three
sitesforGrupera(Gr1,Gr2,Gr3),twositesforMariposales(Mr1,Mr2),twositesforSalamandinga(Sa1,Sa2),and
twositesforRoatanBank(RB1,RB2);f)MediaLuna:sixsitesforMediaLuna(ML1,ML2,ML3,ML4,ML5,ML6)and
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CoralReefHealthIndices
g)CayosMiskitos:LondonReef(LOR),NeeReef(NER),PorgeeReef(POR),LamarkaReef(LAR),MartinezReef
(MAR),CayoMuerto(MUK).Errorbarscorrespondtostandarddeviation.
doi:10.1371/journal.pone.0161812.g003
sitescale.Incontrast,thehealthgradesoftheRHIpresentedaweakbutsignificantrelationship
withspeciesrichnessandthefunctionalgroupsoffishonlyatthescaleofsite(Fig5)andzones
(Fig6Aand6B),aswellaswiththeShannondiversityamongzones(Fig6C).
Discussion
Reefhealthindices
Thisstudyrevealedverysimilarhealthprofilesatsiteandzonescalesusingbothhealthindices.
However,theRHIpresentedhigherreefhealthvaluesinallzonesandsitescomparedto
2D-CHI.TheRHIanalysissuggeststhat57.15%ofthezonespresentedpoorhealth,while
42.85%wereincriticalcondition.Incontrast,the2D-CHIestimatesshowedhigherdegrada-
tioninallofthestudiedsites,since28.5%wereconsideredtobedegradedand71.5%tobevery
degradedhealth.Thisdiscrepancybetweenthetwoindicesistheresultofdifferencesinthe
variablesconsideredforestimatingreefhealth.The2D-CHIconsidersthetotalfishbiomass,as
wellasthecoverageofencrustingcorallinealgae,whiletheRHIonlyconsidersthebiomassof
theherbivorousfishandspeciesofcommercialimportance,limitedtospecificfamilies,without
consideringencrustingcorallinealgae.Itshouldbenoted,however,thatbothreefhealthindi-
cesconsidertotallivecoralcover[32,33,36].Ingeneral,bothindicesindicatedthatMedia
Luna,CayosMiskitos,andCancunwerethezonesthatpresentedthebesthealthcondition(i.e.
poorstatus)andthereportsfromHealthyReefsforHealthyPeopleduringtheyears2008,
2010and2012,inthereefsofCancun,presentsimilarresultswheretheRHIwastheindexuti-
lized[31–33].Itisimportanttohighlighttheabsenceofprevioushealthreportsusingtheindi-
cesRHIand2D-CHIforthesitesofMediaLunaandCayosMiskitos,sincethesesitesarenot
consideredpartoftheMesoamericanReef[34,36].ThezoneofBancoChinchorropresenteda
“critical”healthstatusundertheRHIand“verydegraded”withthe2D-CHI,thiswasnotsimi-
lartothatreportedforthesesitesintheyears2010and2012[32–33].However,bothhealth
Fig4.GradeofreefhealthestimatedwiththeindicesRHIand2D-CHIineachstudyzone.a)RHIhealthgradeperzone;b)CHIhealthgradeper
zone.
doi:10.1371/journal.pone.0161812.g004
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