Biological community structure on patch reefs in Biscayne National Park, FL, USA

Environ Monit Assess (2010) 164513ndash531DOI 101007s10661-009-0910-0

Biological community structure on patch reefsin Biscayne National Park FL USA

Ilsa B Kuffner middot Rikki Grober-Dunsmore middotJohn C Brock middot T Don Hickey

Received 6 August 2008 Accepted 6 April 2009 Published online 28 April 2009copy The Author(s) 2009 This article is published with open access at Springerlinkcom

Abstract Coral reef ecosystem management ben-efits from continual quantitative assessment of theresources being managed plus assessment of fac-tors that affect distribution patterns of organismsin the ecosystem In this study we investigatethe relationships among physical benthic and fishvariables in an effort to help explain the distribu-tion patterns of organisms on patch reefs withinBiscayne National Park FL USA We visited atotal of 196 randomly selected sampling stationson 12 shallow (lt10 m) patch reefs and measuredphysical variables (eg substratum rugosity sub-stratum type) and benthic and fish communityvariables We also incorporated data on substra-tum rugosity collected remotely via airborne lasersurveying (Experimental Advanced Airborne Re-search LidarmdashEAARL) Across all stations onlyweak relationships were found between physi-cal benthic cover and fish assemblage variables

I B Kuffner (B) middot T D HickeyUS Geological Survey 600 4th St SouthSt Petersburg FL 33701 USAe-mail ikuffnerusgsgov

R Grober-DunsmoreInstitute of Applied Sciences University of the SouthPacific Suva Fiji

J C BrockUS Geological Survey National Center 12201 SunriseValley Dr Reston VA 20192 USA

Much of the variance was attributable to a ldquoreefeffectrdquo meaning that community structure and or-ganism abundances were more variable at stationsamong reefs than within reefs However whenthe reef effect was accounted for and removedstatistically patterns were detected Within reefsjuvenile scarids were most abundant at stationswith high coverage of the fleshy macroalgaeDictyota spp and the calcified alga Halimeda tunawas most abundant at stations with low EAARLrugosity Explanations for the overwhelming im-portance of ldquoreefrdquo in explaining variance in ourdataset could include the stochastic arrangementof organisms on patch reefs related to variablelarval recruitment in space and time andor stronghistorical effects due to patchy disturbances (eghurricanes fishing) as well as legacy effects ofprior residents (ldquopriorityrdquo effects)

Keywords Benthic community structure middotMarine protected areas middot Overfishing middot Rugosity

Introduction

Coral reef ecosystems around the world are de-grading due to a multitude of stressors (Wilkinson1999 Hoegh-Guldberg 1999 Pandolfi et al 2003)and coral reefs in the Caribbean basin are partic-ularly in peril (Hughes 1994 Porter et al 2002Gardner et al 2003 Pandolfi et al 2005) Degra-

514 Environ Monit Assess (2010) 164513ndash531

dation has continued despite concerted efforts atresource management (Keller and Causey 2005)Understanding how and why species are distrib-uted across the seascape is critical to managingcoral reef ecosystems

Controversy exists over what variables in-fluence community structure on reefs and theamount of time these communities spend at equi-librium (Connell 1978) Study results are oftendependent upon scale andor the range of habitatsbeing considered (Syms 1995 Eagle et al 2001Chittaro 2004) Generally one body of literaturesupports niche diversification and predicts highlyordered communities (eg Connolly et al 2005)while another supports a more stochastic viewhighlighting the importance of spatially and tem-porally variable recruitment of larvae (eg Saleand Douglas 1984 Doherty and Fowler 1994)However with backgrounds of considerable tem-poral and spatial variability in fish and benthiccommunity structure many studies support hu-man extraction and alteration of habitat and wa-ter quality as determinants of coral reef status(McClanahan 1994 Chapman and Kramer 2001Halpern and Warner 2002 Graham et al 2006Pandolfi and Jackson 2006 Maliao et al 2008)Human disturbance could in effect mask anynatural relationships between species and theirhabitat by altering the limiting factors that controlpopulations

There are over 4000 patch reefs in the northernFlorida Keys (Marszalek et al 1977) highlightingthis ecotype as one of importance to the Floridareef tract (Jones 1977) Other researchers havedocumented these patch reefs as being biologi-cally diverse with substantial live coral comparedto outer-tract reefs (Miller et al 2000a) Fisheriesand fish habitat (Ault et al 2001) and benthiccommunity structure (Chiappone and Sullivan1997 Miller et al 2000b) assessment effortsconducted over the last few decades have un-derrepresented the patch reef habitat thus wedecided on this habitat as the focus of our studyThough there are a fair number of reports includ-ing data on coral populations in Biscayne NationalPark (BNP Burns 1985 Porter and Meier 1992Greenstein and Pandolfi 1997 Ginsburg et al2001 Lirman and Fong 2007) studies on inverte-brate and macroalgal communities are few

The purpose of this study was first to pro-vide a detailed description of patch reef commu-nity structure in BNP and second to examinethe relationships among physical benthic com-munity and fish assemblage variables Using insitu diver surveys we measured fish abundanceat the species level percent benthic cover bycoral algae and encrusting invertebrates coralrecruit density and other variables at 12 patchreefs within BNP Data were compiled for 196stations where physical and benthic variables weremeasured including a subset of 119 stations wherefish were also surveyed We hypothesized that thedifference in variables between reefs would beinsignificant since we expected the patch reefs torepresent a homogeneous habitat We anticipatedthat specific relationships between fish and ben-thic variables would be evident predicting lowfleshy algal abundance at stations where herbiv-orous fish were abundant (and conversely moresuitable settlement substratum for coral larvae)and high fish abundance at stations where gor-gonians were dense We also expected to seesignificant correlations between benthic variablesand the physical habitat predicting that macroal-gae would be more abundant on topographicallyflatter parts of the reef The relationships betweenphysical (eg rugosity) and fish variables are thesubject of a previous paper (Kuffner et al 2007)and are not discussed here

Our results were different than expected show-ing more variance between rather than withinreefs and revealing no strong relationships be-tween physical benthic and fish variables Wediscuss possible mechanisms that could help ex-plain the patterns in community structure andthe lack of correlations between variables that weobserved on these patch reefs and suggest possi-ble mechanisms influencing patch reef communitystructure in BNP

Materials and methods

Field assessment of physical benthicand fish variables

Underwater surveys were conducted via scubadiving on 12 small (asymp1 ha) patch reefs in Biscayne

Environ Monit Assess (2010) 164513ndash531 515

Table 1 GPS locationsand descriptive data forpatch reefs surveyedSeptember 9 to 16 2003

See Kuffner et al (2007)or httppubsusgsgovof20081330 (Kuffner et al2008) for a map of thestudy area

Reef Northings Eastings Distance to Depth Areanext reef (m) (m (SE)) (m2)

Bravo 280920230 58464120 8356 369 (011) 47486Delta 280899135 58438860 10956 413 (017) 28140Echo 280889240 58436830 10956 448 (015) 25903Golf 280769995 58434015 13099 471 (030) 36336Hotel 280765160 58306190 8841 437 (013) 19055India 280763950 58370330 8684 386 (018) 24990Juliet 280762965 58410145 7214 459 (022) 16915Kilo 280737200 58409460 14416 407 (016) 34060Lima 280729215 58423960 16313 533 (033) 36093November 280554800 58305685 14897 371 (017) 34844Oscar 280553350 58285680 15933 428 (025) 33798Papa 280448340 58324585 7647 546 (024) 23503

National Park FL USA from September 9 to 162003 (see httppubsusgsgovof20081330 for amap of the study area) Patch reefs in the northernFlorida reef tract are generally dome-shaped andsurrounded by dense sea grass beds (Jaap 1984)Reefs were selected based upon similarities inaverage depth (3ndash6 m) area positioning acrossthe reef shelf reef shape and other potentiallyconfounding variables (Table 1) A four-personresearch team visited each reef once to measure

physical and biological community variables usingaccepted survey methods (Table 2)

Variables were measured at n = 16 randomlychosen global positioning system (GPS) coordi-nates (stations) per reef as described by Kuffneret al (2007) Randomized sampling is critical tosurvey design in order to avoid the problems asso-ciated with fixed-interval and haphazard samplingoften employed in these types of studies (Lewis2004) The GPS coordinates for the stations were

Table 2 Field survey methods employed to measure community attributes in Biscayne National Park FL USA

Variable Survey method

Chain rugosity After Risk (1972) rugosity was estimated by laying a 10-m transect tape acrossreef in eastndashwest direction with the 5-m mark over the station marker using a1-m chain with 1-cm links we estimated contoured distance by seriallydeploying the chain across the substratum rugosity was calculated as the ratiobetween contoured and linear distance

Substratum type Percent makeup of the substratum was estimated using 1-m2 quadrat categoriesincluded cemented reef coral rubble (three size classes) pavement and sand

Algae benthic invertebrates and coral Species-level percent cover of algae benthic invertebrates and live coralestimated in 025 times 025-m quadrats number of coral recruits(defined as lt1-cm diameter) was counted within the same quadrats coralspecies richness was estimated by thoroughly searching over the whole patchreef while transiting between stations during each 25-h dive

Urchins and gorgonians Number of urchins by species was counted within 05 times 05-m quadratsgorgonian abundance and volume were estimated within the same quadratsidentified to lowest taxonomic level possible in the field (at least genus)gorgonian volume was estimated by measuring maximum dimensions(length times width times height) with a 3-m tailorsrsquo tape measure

Fish Bohnsack and Bannerot (1986) point count method was used to estimateabundance and size of fish for each species observed within an imaginary75-m-radius cylinder from the benthos to the water-column surface

One sample for each variable (ie rugosity transect fish count quadrat) was performed per station


uploaded to a handheld Garmin Map 76 GPS unitequipped with the Wide Area Augmentation Sys-tem and used to navigate a small vessel to delivermarker buoys to each station Maps were pre-pared for each reef so that field personnel coulduse them to place marker buoys and navigateunderwater from station to station Four scubadivers with expert capabilities in the identificationof coral algae reef fish gorgonians and geologicstructure worked simultaneously rotating fromstation to station All surveys were conducted be-tween 0900 and 1800 EST Physical benthic andfish data are available as geographic informationsystem layers online in a noninterpretive producthttppubsusgsgovof20081330 (Kuffner et al2008)

Fish surveys were conducted using theBohnsack and Bannerot (1986) point count meth-od wherein a diver sits stationary in the middleof a 75-m-radius imaginary cylinder recordingfish species observed in a 5-min period and thenestimates length and abundance for each recordedspecies for the following 10 min Occasionallya point count cylinder included more than onestation due to the random assignment of stationswithin reefs When a cylinder contained morethan one station the fish data were randomlyassigned to one of the stations and the otherstation was left with missing values for fishvariables Thus the number of stations with fishdata varied from ten to 13 per reef

EAARL measurement of substratum rugosity

The Experimental Advanced Airborne ResearchLidar (EAARL) data were collected in August2002 and details of the data acquisition andprocessing are described elsewhere (Brock et al2006a Kuffner et al 2007) as well as the datathemselves (Brock et al 2006b) Briefly theNational Aeronautics and Space AdministrationEAARL equipment was flown aboard an airplaneat 300-m altitude collecting 10-cm-diameter laser-spot elevation soundings at a spatial density ofapproximately one sounding per square meterUsing an approach based upon Dahlrsquos surfaceindex defined as the ratio of the actual surfacearea to that of a flat horizontal two-dimensional

plane with similar boundaries (Dahl 1973)rugosity was estimated from lidar-derived digitalelevation models at 1-m cell resolution

Statistical analyses

Simple linear regression was used to test specific apriori hypotheses regarding relationships betweenindividual physical benthic and fish variablesWhen the assumptions of linear regression wereviolated (eg residuals not normally distributed)the data were transformed as necessary One-way analysis of variance (ANOVA) was used toassess differences in individual variables betweenreefs followed by Tukeyrsquos honestly significantdifference (HSD) test to find the differences us-ing a family alpha = 005 When the data failedto meet the assumptions of the parametric testsdespite transformations nonparametric Kruskal-Wallis ANOVA was used instead followed byKruskal-Wallis all-pairwise comparisons (alpha =005) When there was a pronounced pattern inthe plot of regression residuals against ldquoreefrdquotwo-way ANOVA was utilized to explore the datafurther the explanatory variables were catego-rized by dividing the ordered data into thirds (eglow medium and high Dictyota spp cover) withthe two-way models including the fixed factors(eg ldquoreefrdquo ldquoDictyota categoryrdquo) and the inter-action term

To assess overall patterns in physical variablesand biological community structure and their rela-tion to each other multivariate methods availablein PRIMER v6 software (Clarke and Warwick2001) were employed Physical variables in thisanalysis included all categories of substratumcomposition (Table 2) rugosity measured with thechain-transect method rugosity measured withEAARL at the 2- and 10-m scale (Kuffner et al2007) and the reef attributes of reef arealidar-determined depth and distance to nearestreef Benthic variables included are presented inTable 3 For fish variables data were aggre-gated at the family level separating juvenilesand adults for families Acanthuridae SerranidaeHaemulidae Scaridae and Lutjanidae and notdifferentiating life stage for families Pomacan-thidae Chaetodontidae Pomacentridae Mulli-dae and Labridae With PRIMER we calculated


Tab

le3

Mea

nsan

dst

anda

rder

ror

(SE

)in

perc

entc

over

(exc

eptw

here

note

d)fo

rm

ajor

spac

e-oc

cupy

ing

bent

hic

orga

nism

s(n

=16

stat

ions

exce

ptre

efL

ima

n=

20)

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

ap

valu

e(A

NO

VA

)

Liv

eco

ral

96

108

84

54

43

29

46

44

38

34

20

56

000

35(n

p)SE

26

35

15

24

12

10

17

22

14

10

07

28

Cor

alre

crui

ts(n

ope

rsq

uare

met

er)

90

140

130

60

260

180

60

10

64

110

80

50

006

97(n

p)SE

29

44

55

20

85

74

25

10

21

28

44

28

Cya

noph

ytes

34

71

118

33

82

107

74

98

47

92

97

94

001

82(n

p)SE

09

13

22

13

28

22

16

25

13

36

19

48

Hal

imed

atu

na16

612

112

414

410

214

814

812

86

79

66

610

90

0009

(np)

SE1

91

71

72

01

51

72

12

82

21

81

52

8D

icty

ota

spp

177

185

255

147

17

212

136

178

156

164

86

129

lt0

0001

(np)

SE2

22

72

72

90

42

62

42

81

72

91

62

1Su

itab

lese

ttle

men

tsub

stra

tum

219

204

148

295

276

252

215

184

172

137

179

221

012

77(n

p)SE

32

27

27

50

49

47

36

44

34

29

35

36

Mill

epor

aal

cico

rnis

08

23

12

26

10

04

09

27

10

16

10

38

046

06(n

p)SE

03

09

06

14

03

02

05

12

05

07

05

15

Gor

goni

anho

ldfa

sts

19

06

09

24

33

17

23

25

26

27

48

39

lt0

0001

(np)

SE0

50

30

30

70

40

40

50

60

60

51

01

6G

orgo

nian

dens

ity

(no

per

squa

rem

eter

)30

523

029

041

823

534

340

029

337

928

329

836

5lt

000

01SE

39

19

35

29

20

28

29

33

28

24

36

27

Gor

goni

anvo

lum

e(m

3m

minus2)

014

030

019

027

044

028

017

070

029

033

057

013

002

53(n

p)SE

003

007

005

006

016

006

003

026

006

008

019

019

Ery

thro

podi

umca

riba

eoru

m2

53

33

71

51

90

31

90

73

23

31

71

10

5509

(np)

SE0

92

31

90

71

10

21

60

51

71

50

80

7P

alyt

hoa

cari

baeo

rum

02

01

01

13

05

13

60

46

112

09

38

39

000

58(n

p)SE

01

01

01

09

05

05

31

25

39

07

18

30

Bri

areu

mas

best

inum

12

38

36

18

31

11

24

18

50

13

39

11

004

71(n

p)SE

06

14

12

05

08

07

07

06

17

04

15

06

Por

ifer

a2

93

61

64

63

63

42

61

93

42

66

52

30

2317

(np)

SE1

01

30

61

00

91

00

90

60

81

01

90

6

Rea

ders

shou

ldke

epin

min

dth

atco

nduc

ting

mul

tipl

eon

e-w

ayA

NO

VA

son

data

colle

cted

from

the

sam

esa

mpl

esis

not

advi

sabl

edu

eto

noni

ndep

ende

nce

ofte

sts

The

auth

ors

pres

ent

thes

ere

sult

she

resi

mpl

yto

dem

onst

rate

that

in

gene

ral

ther

ew

asa

pron

ounc

edre

efef

fect

inth

edi

stri

buti

ons

ofbe

nthi

cor

gani

sms

Stat

isti

cal

test

resu

lts

(AN

OV

A)

are

also

incl

uded

wit

hp

valu

eslt

005

inbo

ldnp

nonp

aram

etri

cK

rusk

alndashW

allis

AN

OV

Aap

plie

d(u

sual

lydu

eto

uneq

ualv

aria

nce

amon

gre

efs)

wit

hp

valu

ere

port

edus

ing

chi-

squa

red

appr

oxim

atio

n


Euclidean distances for physical variables thathad been log(x + 1)-transformed (except for thedistance to nearest reef) and normalized Bray-Curtis similarity on square-root-transformed datafor benthic community variables and Bray-Curtissimilarity on log(x + 1)-transformed fish abun-dance data to create triangular resemblance ma-trices To test for significance of the ldquoreefrdquo factorwe used PRIMERrsquos ANOSIM procedure whichcalculates a global R statistic that reflects the dif-ferences in variability between groups comparedto within groups (so R values are proportional todifferences between the groups) and checks forsignificance of R using permutation tests (Clarkeand Warwick 2001) Nonmetric multidimensionalscaling (MDS) was used on matrices derived fromaveraging reefs to visualize the similarities amongreefs To test for significant relationships betweenthe resemblance matrices for physical benthicand fish variables averaged for each reef we usedPRIMERrsquos RELATE procedure which also cal-culates a global R statistic and checks for signifi-cance of R using permutation tests

Results

Physical variables

Substratum surveys revealed that the patch reefswere generally dominated by cemented reef(grand mean 473 plusmn 22 cover) and pavement(201 plusmn 21) with varying amounts of rubbleboulders and sand (Fig 1) Reefs differedsignificantly in the amount of cemented reef(one-way ANOVA F = 557 p lt 00001) andpavement (nonparametric one-way ANOVAKruskal-Wallis statistic = 436 p lt 00001) All-pairwise comparisons (Tukeyrsquos HSD groupings)revealed that reef Lima had significantly lesscemented reef than all reefs except NovemberOscar Bravo and Echo Lima also had signifi-cantly more pavement (Kruskal-Wallis all-pairwise groupings) than India Hotel JulietOscar Delta and November Both chain-transect rugosity and EAARL rugosity weresignificantly different among reefs (Kruskal-Wallis statistic = 436 and 413 respectively both

Fig 1 Mean percentcover of substratum typeson 12 patch reefs inBiscayne National ParkPercent cover within 1-m2

quadrats estimated atrandomly chosen stations(n = 16 per reef exceptreef L n = 20)

0

20

40

60

80

100

B D E G H I J K L N O P

Reef

Su

bstr

atu

m t

yp

e (

c

over)

Sand Pavement Rubble Boulders Cemented reef


p lt 00001) but the all-pairwise comparisontests did not give the same groupings Chain-transect rugosity results indicated that reefsOscar Juliet Papa Golf and Kilo were all morerugose than Hotel whereas EAARL rugosityresults characterized reef Juliet as more rugosethan Delta November Oscar and Bravo (thediscrepancy between the chain and EAARLrugosity measurements is discussed in Kuffneret al (2007)) We found significant effects ofldquoreefrdquo in explaining differences among stationswhen all of the physical variables were combined(ANOSIM Global R = 0415 p = 0001) and thesimilarities among reefs with regards to physicalvariables can be visualized in the MDS plot(Fig 2)

Benthic variables

The benthic community observed on the patchreefs was largely dominated by macrophytes en-crusting invertebrates and ldquosuitable settlementsubstratumrdquo (SSS) found beneath a substantialcanopy of gorgonians (Table 3) A mean of 208 plusmn11 of the bottom was assigned to the categorySSS defined as hard substratum covered mostlyin crustose coralline algae (CCA) and lackingsediments gt1 mm deep macroalgae or thick turfalgae as previously described in Kuffner et al(2006) This category was considered to be anindex of suitable settlement substratum for corallarvae and is analogous to the ldquocropped substra-tumrdquo category of Williams and Polunin (2001)

Macroalgae occupied a large portion of spaceon the reefs we surveyed especially Dictyotaspp (grand mean = 154 plusmn 08 cover) andHalimeda tuna (grand mean=117 plusmn 06 cover)Reefs significantly differed in the extent ofDictyota spp coverage (Kruskal-Wallis p lt

00001) Cyanophytes were also fairly abundant(grand mean = 78 plusmn 07 cover) Live sclerac-tinian corals only accounted for 58 plusmn 06 ofthe benthos Encrusting invertebrates (PoriferaBriareum asbestinum Palythoa caribaeorumErythropodium caribaeorum gorgonian hold-

Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005

Fig 2 Nonmetric multidimensional scaling plots display-ing similarities among reefs using matrices derived fromaveraging stations on each reef for physical benthic andfish variables Symbols are the first letter of the reefs asnamed in Table 1 Two-dimensional stress values lt010indicate that the 2-D representation of the relationshipsamong samples provides a good interpretable ordinationand those lt02 are still useful (Clarke and Warwick 2001)


Fig 3 Mean gorgonianabundance (individualsper square meter) bygenus on each patch reefsurveyed (n = 16 stationsper reef except reef Ln = 19) Legend listsgenera from least to mostabundant (top to bottom)Error bars equal one SEfor total gorgonians

0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia

Fig 4 Mean urchinabundance (individualsper square meter) byspecies on each patch reefsurveyed (n = 16 stationsper reef except Ln = 19) Legend listsspecies from least to mostabundant (top to bottom)Error bars equal one SEfor total urchins

0

10

20

30

40

50


Reef

Diadema antillarum Eucidaris tribuloides Tripneustes ventricosus

Echinometra lucunter Echinometra viridis


fasts and Millepora alcicornis) comprised theremainder of the benthic community contributingabout 2ndash4 cover each

Upright gorgonians were abundant on thepatch reefs (grand mean = 319 plusmn 09 individu-als per square meter) with 42 of individualsobserved belonging to the genus Pseudoptero-gorgia (Fig 3) Gorgonian abundance was sig-nificantly different among reefs (ANOVA p lt

00001) with densities significantly greater atGolf Lima and Papa than at Hotel and Delta(Tukeyrsquos HSD family alpha = 005)

The 888 urchins observed in this study werepatchily distributed among reefs (Fig 4) Themost abundant urchin in the study was Echi-nometra viridis (density ranging from 021 mminus2

on Lima to 34 mminus2 on Echo) Only three Di-adema antillarum were tallied within our quadratsThe total count of urchins was significantly differ-ent between reefs (Kruskal-Wallis p lt 00001)KruskalndashWallis multiple-comparison groupingsshowed that reefs Echo Juliet November DeltaBravo and Oscar had significantly more urchinsthan Golf Kilo Papa and Lima Total urchinabundance did not correlate well with any of thephysical or benthic variables measured

Thirty-one species of scleractinian coral wereobserved during this study plus the hydroco-ral M alcicornis Several species were afflictedwith various stressors at all or some of the reefs(Table 4) Acropora cervicornis infected withwhite-band disease was observed on every reefexcept Hotel and Siderastrea siderea with dark-spot disease was observed on all reefs Black-band disease infected Montastraea cavernosa atfive of the reefs A total of 125 scleractinian coralrecruits were observed within the small-scale sam-pling quadrats with an overall recruit density of102 plusmn 13 mminus2 Coral recruit density did not showsignificant relationships with percent cover of SSSor macroalgae (nor any other physical or benthicvariable measured) either on a per-station basisor when data were averaged per reef

The effect of reef was significant when allbenthic variables were included in a multivariatetest (ANOSIM global R = 0122 p = 0001) Thesimilarities among reefs with regards to benthicvariables can be visualized in the MDS plot(Fig 2)

Fish variables

We observed 12036 reef fish belonging to 80species at the 119 stations where fish were sur-veyed Patterns of reef fish abundance amongreefs were described in a previous manuscript(Kuffner et al 2007) The effect of reef was sig-nificant when all fish variables were included ina multivariate test (ANOSIM global R = 0221p = 0001) The similarities among reefs with re-gards to fish variables can be visualized in theMDS plot (Fig 2) Reef Lima had particularly lowabundances of certain groups of fishes (eg familyHaemulidae) and thus stands out in the MDS plot

Relationships between physicaland benthic variables

Across all stations H tuna was weakly in-versely correlated with EAARL rugosity atthe 10-m scale (linear regression Halimedadata square-root-transformed and rugosity datainverse-transformed R2 = 008 p lt 00001) Fur-ther when the reef effect was taken into ac-count with a two-way ANOVA results showedthat H tuna was more abundant at stations withlow substratum rugosity followed by stations withmedium and high rugosity (Table 5 Fig 5) ATukey HSD all-pairwise comparison test revealedthat H tuna coverage in all three categories ofrugosity was significantly different (p lt 005) Htuna abundance was not significantly related to ru-gosity measured using the chain-transect methodthough the trend was the same

In general the relations between other spe-cific physical and benthic variables were weakGorgonian abundance and genus richness for ex-ample were negatively correlated with thepercent cover of the substratum by rubble(small + medium + large) though the relation-ships were extremely weak (linear regressionabundance R2 = 0093 p lt 00001 genus rich-ness R2 = 0121 p lt 00001) When the resem-blance matrices for all physical and all benthicvariables were compared using PRIMERrsquos RE-LATE procedure the relationship was not signifi-cant (rho = 0252 p = 008)


Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a


Table 5 Two-way ANOVA results for abundance of juve-nile parrot fish (data square-root-transformed) by reef (tenlevels) and Dictyota spp percent cover (low medium andhigh) and H tuna percent cover (square-root-transformed)by reef (12 levels) and rugosity at the 10-m scale (lowmedium and high)

Factor df SS MS F p

Juvenile parrot fishReef 9 19298 2144 1050 00000Dictyota spp 2 2526 1263 619 00030Interaction term 18 3526 196 096 05123Error 89 18168 204Total 118Halimeda tunaReef 11 5406 491 289 00017Rugosity 10 m 2 2673 1337 786 00006Interaction term 22 3341 152 089 06048Error 160 27223 170Total 195

Significant p values highlighted in bold

Relationships between physical and fish variables

When the resemblance matrices for all physi-cal and all fish variables were compared usingPRIMERrsquos RELATE procedure the relationshipwas not significant (rho = 0249 p = 017) Rela-tionships between individual physical (eg differ-ent measures of rugosity) and fish variables weredescribed in a previous manuscript (Kuffner et al2007)

Relationships between benthic and fish variables

Some relationships between herbivorous fish andbenthic community variables were significant butfairly weak Percent cover of SSS was posi-tively related to surgeonfish abundance veryweakly so at the station level (linear regressionn = 119 R2 = 0047 p = 0018) and nominallystronger (but insignificant) when examined atthe ldquoreefrdquo level (Fig 6a linear regression n =10 R2 = 033 p = 0081) Similarly mean per-cent cover of Dictyota spp was not relatedto the abundance of roving adult herbivores(scarids plus acanthurids) at the station level (datalog-transformed linear regression n = 119 R2 =00004 p = 083) but was marginally inverselyrelated at the reef level (Fig 6b linear regres-sion n = 10 R2 = 032 p = 009) In contrast ju-venile scarid abundance was positively (althoughvery weakly) related to Dictyota spp percentcover at the station level (Fig 7a linear re-gression n = 119 data square-root-transformedR2 = 0032 p = 005) but a scatter plot of theresiduals from that regression against the reef fac-tor revealed the substantial reef effect (Fig 7b)When the reef factor was added to the model in atwo-way ANOVA the percent cover of Dictyotawas statistically significant in explaining addi-tional variance in juvenile scarid abundance anda clearer view of the effect can be seen within

Fig 5 Relationshipbetween percent cover ofH tuna and substratumrugosity (in threecategories low mediumand high) on 12 patchreefs in Biscayne NationalPark Error bars equalone SE and are absentwhere n = 1


Fig 6 Reef means with error bars (plusmn1 SE) showing rela-tionship between a the percent cover of suitable settlementsubstratum and the abundance of acanthurids and b thepercent cover of Dictyota spp and the abundance of rovingadult herbivores (acanthurids + scarids) Letters refer toreef names given in Table 1

each reef (Table 5 Fig 7c) A Tukey HSD all-pairwise comparison test revealed that stations inthe high Dictyota spp coverage category (20ndash47cover) had significantly more juvenile scarids than

Fig 7 The abundance of juvenile scarids in relation topercent cover of Dictyota spp shown in a juvenile scaridmean abundance at each station vs Dictyota spp percentcover with regression line and 95 confidence intervals bresiduals from the regression model vs reef and c meanabundance of juvenile scarids per patch reef broken downinto three categories of Dictyota spp abundance (lowmedium and high) Error bars equal one SE and are absentwhere n = 1

stations in the other coverage categories (medium9ndash19 and low 0ndash8) High Dictyota stationshad the highest mean juvenile scarid abundanceon eight out of ten reefs (Fig 7c) Interestinglyconverting herbivorous fish abundance to biomass


did nothing to improve the relationships betweenfish and benthic variables (data not shown)

Neither fish species richness nor abundancewas related to gorgonian abundance or volumeRelationships between the abundance of the eco-nomically important groupers and snappers andbenthic variables could not be assessed due tothe scarcity of sightings of these fishes duringthis study When the resemblance matrices for allbenthic and all fish variables were compared usingPRIMERrsquos RELATE procedure the relationshipwas not significant (rho = 0222 p = 013)

Discussion

Biological communities on the 12 BNP patch reefsthat we surveyed were dominated by gorgoniansand encrusting invertebrates were sparsely popu-lated with live corals afflicted by several diseasesand had fish populations indicative of intensivefishing pressure However the densities of recruit-sized corals were comparable to other sites in theregion There was a moderate amount of fleshymacroalgae but also a lot of suitable settlementsubstratum for coral larvae Urchins were patchilydistributed with populations dominated by Eviridis and D antillarum was nearly absent Ourdata agree with other studies indicating that coral(Dupont et al 2008) and fish populations (Aultet al 2001) in BNP are still depressed comparedto 50 years ago

The data presented here can help reef re-source managers by serving as a baseline assess-ment of physical habitat benthic communitiesand fish assemblages but little insight regard-ing what variables influence community structurewithin the patch reef habitat type can be drawnfrom this study Surveying the biological com-munities on 12 patch reefs showed that stationswithin reefs were more homogenous in the abun-dance of macrophytes invertebrates and fish thanwe had expected Within-reef variation was lessthan among-reef variation as has been previouslyshown for outer-bank reefs in the Florida Keys(Murdoch and Aronson 1999) Possibly becauseof the overwhelming reef effect relationships be-tween physical benthic and fish variables weresurprisingly weak across all stations Here we dis-

cuss possible mechanisms behind these patternsincluding stochastic larval recruitment life his-tory characteristics of the major space-occupyingspecies relatively isolated patches of habitat hu-man disturbance of populations (eg fishing) andthe lasting effects of historical events

Patterns in benthic community structure

Gorgonians were extremely abundant on thepatch reefs surveyed in this study with an overallmean density of 32 colonies per square metercomparable to Goldbergrsquos (1973) average densityof 34 colonies per square meter on patch reefs offBroward County We originally hypothesized thatthe gorgonians found on these patch reefs couldbe contributing to essential fish habitat by provid-ing protective cover and thus predicted that theabundance or volume of gorgonians could predictcertain fish variables Our data did not supportthis hypothesis Gorgonians were abundant on allpatch reefs observed in this study whereas fishshowed marked reef effects

Urchins are important herbivores and bio-eroders on coral reefs and they can either posi-tively or negatively affect reef viability dependingupon species density and feeding mode Beforethe 1983 die-off D antillarum played a largerole in controlling algal distributions in the shal-low Caribbean reef environment (Morrison 1988Carpenter 1988 Aronson and Precht 2000) Thespecies is presently making a moderate come-back in some parts of the region (Edmunds andCarpenter 2001) but has yet to repopulate theFlorida Keys (Chiappone et al 2002) only threeindividuals were observed in our study In con-trast Echinometra spp (the rock-boring urchins)were quite abundant on some of the patch reefswe surveyed Densities of these urchins have beenshown to increase in the absence of D antillarum(Williams 1981) Reef bioerosion by Echinometraspp was apparent during our surveys If reef ac-cretion rates are lower than rates of bioerosionurchins can cause damage to reef framework Itmay be important to monitor the density of Echi-nometra spp especially because their main preda-tors (eg triggerfish porcupine fish stingrays)were never observed during our study


Coral recruitment is a key process determiningthe ability of reef-building coral populations torecover from declines and is an important process-oriented variable defining reef health Measuringthe abundance of juvenile corals is one way to esti-mate coral recruitment rates though recruit mor-tality rates remain unknown The recruit densityreported here (102 plusmn 13 recruits per square me-ter) is similar to that reported in other studies inBiscayne Bay (Miller et al 2000a) and in St JohnUS Virgin Islands (Edmunds 2000) Many speciesof coral larvae require CCA to settle (Morse et al1988 Heyward and Negri 1999) and availabilityof CCA is negatively correlated with macroalgalabundance (Hixon 1997) Dictyota spp the mostabundant fleshy algae observed in this study wasnot as abundant on these patch reefs (154 plusmn 08cover) compared to other locations on the Floridareef tract (Lirman and Biber 2000 Beach et al2003 Kuffner et al 2006) whereas SSS was fairlyabundant (overall mean 21 cover) In a studyconducted in this area in 1981 Burns (1985) re-ported that they observed lots of ldquouncolonizedreef substraterdquo Thus coral recruitment doesnot seem to be limited by available substratum(either historically or now) and appears to beoccurring at levels comparable to other coral reefsin the region Our data do not support recruitmentfailure as a major reason for coral reef declineon the patch reefs in Biscayne National ParkHowever the species that we observed as recruitswere mostly small colony brooders (eg Agariciaspp Porites spp) and not the large reef-buildingspecies (eg Diploria spp Montastraea spp) assimilarly noted for BNP reefs in the 1980s (Porterand Meier 1992) and from 2001 to 2003 (Lirmanand Fong 2007)

Possible mechanisms behind reef-specificpatterns in benthic community structure

Most marine organisms reproduce sexually viaspawned eggs and sperm that are externallyfertilized followed by a protracted larval-dispersal phase characterized by high mortalityrates and very low parental investment per zygoteThe relative importance of presettlement andpostsettlement processes in determining speciespopulation structures is the subject of debate but

at least for certain species recruitment processescan explain a considerable amount of temporaland spatial variation in abundance (Keoughand Downes 1982 Doherty and Fowler 1994)However many benthic invertebrates are verysuccessful at asexual propagation A commonalityamong many of the major space-occupying organ-isms that dominate the substratum on thesepatch reefs is that they all have very successfulmechanisms for short-range dispersal Dictyotamenstrualis and Dictyota pulchella both of whichwere abundant at our stations are very successfulat establishing new plants via vegetative frag-mentation caused by fish grazing (Herren et al2006) and hurricanes (Vroom et al 2005)Halimeda discoidea fragments generated bystorms and fish bites can rapidly produce newattachment rhizoids (Walters and Smith 1994)so it is probable that other Halimeda spp maysimilarly reproduce via vegetative fragmentationThe encrusting gorgonian B asbestinum pro-duces surface-brooded larvae that are competentto settle immediately after release (Brazeau andLasker 1990) and branches that are lost due tofragmentation can readily reattach to the substra-tum to create new colonies (Brazeau and Lasker1992) E caribaeorum is a highly aggressivespecies that can overgrow most other encrustingspecies (Karlson 1980 Suchanek and Green1981) P caribaeorum produces new asexuallypropagated colonies via fission (Acosta et al2005) and fragmentation (Acosta et al 2001)

Present community composition may be verydependent upon the types of organisms that suc-cessfully recruited to the site in the past andwere able to take hold and start asexually repro-ducing especially since the last physical distur-bance event The importance of prior residentsor ldquopriorityrdquo effects on subsequent communitystructure via residentndashrecruit interactions (egpredation) has been shown for reef fish (Almany2003) We suggest priority effects may be impor-tant in shaping the encrusting communities weobserved mainly due to asexual propagation lead-ing to preemption of space and possibly predationupon newly arriving larvae by the lush gorgoniancommunity and other filter feeders This hy-pothesis could be tested using manipulative fieldexperiments


Differential physical disturbance particularlyby Hurricane Andrew in 1992 also could havecontributed to reef-specific patterns in benthiccommunity structure Physical disturbances canhave lasting effects on coral communities (Hughesand Connell 1999 Bythell et al 2000) and impactstudies following Hurricane Andrew revealed thatdisturbance was very patchy (Tilmant et al 1994Blair et al 1994) Further historical changes tocoral communities can affect competitive interac-tions among benthic organisms many years afterthe disturbance event (Hughes 1989)

Possible mechanisms to explain lackof benthicndashfish community relationshipsacross all survey stations

We found only weak relationships between ben-thic and fish community attributes across allstations Previous studies on fish community struc-ture have shown high levels of variance explainedby ldquoreefrdquo with little explained by habitat variables(Sale and Douglas 1984 Syms and Jones 2000)but others incorporating a wider range of habitatshave found that habitat variables explain a largeamount of variance in fish community structure(Chittaro 2004 Gratwicke and Speight 2005) Re-lationships between habitat and fish have alsobeen revealed in cases where the fish commu-nities involved (eg damselfish and other herbi-vores) were directly affecting benthic communitystructure particularly with respects to the algalassemblage (Hixon 1997) and bioerosion of thesubstratum (eg parrot fish Bellwood and Choat1990) In contrast herbivorous fish may respondto food availability (Williams et al 2001 Russ2003) rather than affecting the benthic commu-nity in places where they are not food-limitedHerbivorous fish in the Caribbean were thoughtto be food-limited before the D antillarum die-off in 1983 (Carpenter 1988) but not since then(Williams and Polunin 2001) Our results showingonly weak or positive (in the case of juvenileparrot fish) relationships between herbivorous fishand fleshy algae abundance indicate that herbiv-orous fish do not lack food in Biscayne NationalPark Further evidence for the lack of food lim-itation for herbivorous fish on patch reefs in the

Florida Keys was recently provided by Paddacket al (2006)

Chronic human disturbance of fish populationscould provide an explanation for the lack ofrelationships between habitat and fish commu-nity variables The low abundance of predatorsand strong dominance by herbivores and juve-niles strongly indicate that fishing is a major fac-tor structuring fish populations on BNP patchreefs Historically these patch reefs were well-populated with red black and Nassau groupermutton snapper and hogfish (Jaap 1984) all ofwhich are prized as food fish and were nearly orentirely absent in our surveys Fishing can havesubstantial effects on fish community structureand distribution of trophic guilds usually increas-ing the ratio between herbivorous fish and pisci-vores (Friedlander and DeMartini 2002) In ourstudy there were approximately nine herbivoresfor every piscivore Judging from the amountof derelict fishing gear observed on the reefsthe skewed size distribution toward small fishesand the almost complete absence of many targetspecies observed in this study fishing pressure hasundoubtedly affected reef fish community struc-ture in BNP An extensive overview databaseassimilation and modeling effort revealed the ex-tremely poor status of fish resources in BNP (Aultet al 2001) When the habitat is underpopulatedwith fish relationships between habitat and fishassemblage parameters can be hard to detect assuggested for grouper and adult fishes in the USVirgin Islands by Grober-Dunsmore et al (2007)

Evidence for within-reef relationships betweenfish and benthic variables

Macroalgal abundance was inversely correlatedwith herbivorous fish biomass in a Caribbean-wide study (Williams and Polunin 2001) Whenaveraged across reefs our data indicate a weakpositive relationship between abundance of acan-thurids and SSS and an inverse relationshipbetween Dictyota spp percent cover and theabundance of roving adult herbivores (scarids plusacanthurids) Although converting our data tobiomass did not improve the relationships ob-served our grand mean biomass and correspond-ing algal percent cover estimates fit well with


the large-scale trends reported in Williams andPolunin (2001) Our grand means for acanthurids(192 plusmn 020 g mminus2) scarids (649 plusmn 049 g mminus2)and macroalgae (the sum of our Dictyota sppand H tuna 271 plusmn 11) result in data pointsthat fall very close to those reported from GrandCayman (Williams and Polunin 2001) Addition-ally plots of our grand means for SSS which issimilar to their ldquocropped substratumrdquo categorytogether with our acanthurid and scarid grandmeans would lie close to sites in Jamaica Acrossall stations however there was little variancein Dictyota spp abundance explained by scaridor acanthurid densities Compared to data inWilliams and Polunin (2001) our sites would havefallen very close to each other if overlain on theirfar-ranging spread of data points from around theCaribbean basin

In contrast to what we expected when thereef effect was taken into consideration juvenileparrot fish abundance was positively correlatedwith Dictyota percent cover indicating that thecanopy formed by the algae may provide a nurseryhabitat for parrot fish McAfee and Morgan (1996)found that four out of five species of parrot fishstudied showed ontogenetic shifts in habitatfooduse spending time as juveniles associated withscattered algal mats on pavement and then mov-ing to the reef slope as adults In support of thisbehavioral pattern Paddack et al (2006) foundthat the patch reef environment in the FloridaKeys harbored smaller herbivorous fish than outerreefs indicating that the patch reefs may providea stepping-stone to adult habitat farther out onthe shelf

Conclusions

Our study revealed that the overall relationshipspredicted among physical benthic and fish vari-ables were insignificant and were usually over-whelmed by the reef effect Stations within patchreefs had more in common with each other thanwas to be expected if all patch reefs constituteda homogenous habitat Reefs were unique withrespect to benthic and fish community structureand no variable that we measured could explaina significant portion of the variance observed

among stations The lack of relationships betweenand among biological communities and habitatobserved is consistent with several mechanismsincluding stochastic larval dispersal priority ef-fects of early colonizers and human disturbance(fishing) If Biscayne National Park enacts ldquono-takerdquo-protected areas as planned and fish pop-ulations begin to recover relationships betweenfish assemblages and benthic communities maybecome more closely linked

Acknowledgements The US Geological Survey (Geo-logic Discipline Coastal and Marine Geology Programand Biological Resource Discipline Terrestrial Freshwa-ter and Marine Ecosystems Program) funded this projectThis work was performed under the National Park Servicepermit BISC-2003-SCI-0046 We thank R Curry (Bis-cayne National Park) for his support of our work and VBonito for help in the field including gorgonian and coralidentification We dedicate this work to the memory ofCapt Barry Denton whom we will greatly miss He wasa great supporter of USGS coral reef research and alwayskept us safe and comfortable aboard the MV ldquoWinningTicketrdquo We also thank W Jaap G Piniak J Lisle JMorrison and several anonymous reviewers for helpfulsuggestions that greatly improved the manuscript Any useof trade names herein was for descriptive purposes onlyand does not imply endorsement by the US Government

Open Access This article is distributed under the termsof the Creative Commons Attribution NoncommercialLicense which permits any noncommercial use distribu-tion and reproduction in any medium provided the origi-nal author(s) and source are credited

References

Acosta A Sammarco P W amp Duarte L F (2001) Asex-ual reproduction in a zoanthid by fragmentation Therole of exogenous factors Bulletin of Marine Science68(3) 363ndash381

Acosta A Sammarco P W amp Duarte L F (2005) Newfission processes in the zoanthid Palythoa caribaeo-rum Description and quantitative aspects Bulletin ofMarine Science 76(1) 1ndash26

Almany G R (2003) Priority effects in coral reef fishcommunities Ecology 84(7) 1920ndash1935 doi1018900012-9658(2003)084[1920PEICRF]20CO2

Aronson R B amp Precht W F (2000) Herbivoryand algal dynamics on the coral reef at DiscoveryBay Jamaica Limnology and Oceanography 45(1)251ndash255

Ault J S Smith S G Meester G A Juo J ampBohnsack J A (2001) Site characterization for


Biscayne National Park Assessment of fisheries re-sources and habitats (p 156) NOAA Technical Mem-orandum NMFS-SEFSC-468

Beach K Walters L Borgeas H Smith C Coyer Jamp Vroom P (2003) The impact of Dictyota spp onHalimeda populations of Conch Reef Florida KeysJournal of Experimental Marine Biology and Ecology297 141ndash159 doi101016jjembe200307003

Bellwood D R amp Choat J H (1990) A functionalanalysis of grazing in parrot fishes (family Scaridae)The ecological implications Environmental Biology ofFishes 28 189ndash214 doi101007BF00751035

Blair S M McIntosh T L amp Mostkoff B J (1994)Impacts of Hurricane Andrew on the offshore reefsystems of central and northern Dade County FloridaBulletin of Marine Science 54(3) 961ndash973

Bohnsack J A amp Bannerot S P(1986) A stationary vi-sual census technique for quantitatively assessing com-munity structure of coral reef fishes (p 15) NOAATechnical Report 41

Brazeau D A amp Lasker H R (1990) Sexual repro-duction and external brooding by the Caribbean gor-gonian Briareum asbestinum Marine Biology (Berlin)104 465ndash474 doi101007BF01314351

Brazeau D A amp Lasker H R (1992) Growth rates andgrowth strategy in a clonal marine invertebrate theCaribbean octocoral Briareum asbestinum The Bio-logical Bulletin 183 269ndash277 doi1023071542214

Brock J C Wright C W Kuffner I B HernandezR amp Thompson P (2006a) Airborne lidar sensingof massive stony coral colonies on patch reefs in thenorthern Florida reef tract Remote Sensing of Envi-ronment 104(1) 31ndash42 doi101016jrse200604017

Brock J C Wright C W Patterson M NayegandhiA Patterson J Harris M S amp Mosher L (2006b)USGS-NPS-NASA EAARL submarine topographyBiscayne National Park US Geological Survey OpenFile Report 2006-1118

Burns T P (1985) Hard-coral distribution and cold-water disturbances in South Florida Variationwith depth and location Coral Reefs 4 117ndash124doi101007BF00300870

Bythell J C Hillis-Starr Z M amp Rogers C S (2000)Local variability but landscape stability in coralreef communities following repeated hurricane im-pacts Marine Ecology Progress Series 204 93ndash100doi103354meps204093

Carpenter R C (1988) Mass mortality of a Caribbean seaurchin Immediate effects on community metabolismand other herbivores Proceedings of the NationalAcademy of Sciences of the United States of America85 511ndash514 doi101073pnas852511

Chapman M R amp Kramer D L (2001) Gradients incoral reef fish density and size across the BarbadosMarine Reserve boundary Effects of reserve pro-tection and habitat characteristics Marine EcologyProgress Series 181 81ndash96 doi103354meps181081

Chiappone M amp Sullivan K M (1997) Rapid assessmentof reefs in the Florida Keys Results from a synopticsurvey In Proc 8th int coral reef symp (pp 1509ndash1514)Panama

Chiappone M Swanson D W Miller S L amp SmithS G (2002) Large-scale surveys on the FloridaReef Tract indicate poor recovery of the long-spinedsea urchin Diadema antillarum Coral Reefs 21(2)155ndash159

Chittaro P M (2004) Fishndashhabitat associations acrossmultiple spatial scales Coral Reefs 23(2) 235ndash244doi101007s00338-004-0376-z

Clarke K R amp Warwick R M (2001) Change in ma-rine communities An approach to statistical analy-sis and interpretation (2nd ed) Plymouth PRIMER-ELtd

Connell J H (1978) Diversity in tropical rain forestsand coral reefs Science 199 1302ndash1310 doi101126science19943351302

Connolly S R Hughes T P Bellwood D R ampKarlson R H (2005) Community structure of coralsand reef fishes at multiple scales Science 309 1363ndash1365 doi101126science1113281

Dahl A L (1973) Surface area in ecological analysisQuantification of benthic coral-reef algae Marine Bi-ology (Berlin) 23 239ndash249 doi101007BF00389331

Doherty P amp Fowler T (1994) An empirical test of re-cruitment limitation in a coral reef fish Science 263935ndash939 doi101126science2635149935

Dupont J M Jaap W C amp Hallock P (2008) A retro-spective analysis and comparative study of stony coralassemblages in Biscayne National Park FL (1977ndash2000) Caribbean Journal of Science 44(3) 334ndash344

Eagle J V Jones G P amp McCormick M I (2001)A multi-scale study of the relationships betweenhabitat use and the distribution and abundance pat-terns of three coral reef angelfishes (Pomacanthi-dae) Marine Ecology Progress Series 214 253ndash265doi103354meps214253

Edmunds P J (2000) Patterns in the distribution of ju-venile corals and coral reef community structure inSt John US Virgin Islands Marine Ecology ProgressSeries 202 113ndash124 doi103354meps202113

Edmunds P J amp Carpenter R C (2001) Recovery ofDiadema antillarum reduces macroalgal cover and in-creases abundance of juvenile corals on a Caribbeanreef Proceedings of the National Academy of Sciencesof the United States of America 98(9) 5067ndash5071doi101073pnas071524598

Friedlander A M amp DeMartini E E (2002) Con-trasts in density size and biomass of reef fishesbetween the northwestern and the main Hawaiianislands The effects of fishing down apex preda-tors Marine Ecology Progress Series 230 253ndash264doi103354meps230253

Gardner T A Cote I M Gill J A Grant Aamp Watkinson A R (2003) Long-term region-widedeclines in Caribbean corals Science 301 958ndash960doi101126science1086050

Ginsburg R N Gischler E amp Kiene W E (2001) Par-tial mortality of massive reef-building corals An indexof patch reef condition Florida reef tract Bulletin ofMarine Science 69(3) 1149ndash1173

Goldberg W M (1973) The ecology of the coralndashoctocoral communities off the southeast Florida coast


Geomorphology species composition and zonationBulletin of Marine Science 23(3) 465ndash488

Graham N A J Wilson S K Jennings S PoluninN V C Bijoux J P amp Robinson J (2006) Dy-namic fragility of oceanic coral reef ecosystems Pro-ceedings of the National Academy of Sciences ofthe United States of America 103(22) 8425ndash8429doi101073pnas0600693103

Gratwicke B amp Speight M R (2005) The relationshipbetween fish species richness abundance and habi-tat complexity in a range of shallow tropical ma-rine habitats Journal of Fish Biology 66 650ndash667doi101111j0022-1112200500629x

Greenstein B J amp Pandolfi J M (1997) Preservationof community structure in modern reef coral life anddeath assemblages of the Florida Keys Implicationsfor the Quaternary fossil record of coral reefs Bulletinof Marine Science 61(2) 431ndash452

Grober-Dunsmore R Frazer T K Lindberg W Jamp Beets J (2007) Reef fish and habitat relation-ships in a Caribbean seascape The importance ofreef context Coral Reefs 26 201ndash216 doi101007s00338-006-0180-z

Halpern B S amp Warner R R (2002) Marine reserveshave rapid and lasting effects Ecology Letters 5 361ndash366 doi101046j1461-0248200200326x

Herren L W Walters L J amp Beach K S (2006) Frag-ment generation survival and attachment of Dictyotaspp at Conch Reef in the Florida Keys USA CoralReefs 25 287ndash295 doi101007s00338-006-0096-7

Heyward A J amp Negri A P (1999) Natural inducers forcoral larval metamorphosis Coral Reefs 18 273ndash279doi101007s003380050193

Hixon M A (1997) Effects of reef fishes on corals andalgae In C E Birkeland (Ed) Life and death of coralreefs (pp 230ndash248) New York Chapman and Hall

Hoegh-Guldberg O (1999) Climate change coral bleach-ing and the future of the worldrsquos coral reefs AustralianJournal of Marine and Freshwater Research 50 839ndash866 doi101071MF99078

Hughes T P (1989) Community structure and diversityof coral reefs The role of history Ecology 70(1) 275ndash279 doi1023071938434

Hughes T P (1994) Catastrophes phase shifts and large-scale degradation of a Caribbean coral reef Science265 1547ndash1551 doi101126science26551781547

Hughes T P amp Connell J H (1999) Multiple stressorson coral reefs A long-term perspective Limnologyand Oceanography 44(3) 932ndash940

Jaap W C (1984) The ecology of the South Florida coralreefs A community profile (p 138) Minerals Manage-ment Service MMS 84-0038

Jones J A (1977) Morphology and development of south-eastern Florida patch reefs In Proceedings of the3rd international coral reef symposium (pp 231ndash235)Miami

Karlson R H (1980) Alternative competitive strategiesin a periodically disturbed habitat Bulletin of MarineScience 30(4) 894ndash900

Keller B D amp Causey B D (2005) Linkages be-tween the Florida Keys National Marine Sanctuary

and the South Florida Ecosystem Restoration Initia-tive Ocean and Coastal Management 48 869ndash900doi101016jocecoaman200503008

Keough M J amp Downes B J (1982) Recruitmentof marine invertebrates The role of active larvalchoices and early mortality Oecologia 54 348ndash352doi101007BF00380003

Kuffner I B Walters L J Becerro M A Paul V JRitson-Williams R amp Beach K S (2006) Inhibi-tion of coral recruitment by macroalgae and cyanobac-teria Marine Ecology Progress Series 323 107ndash117doi103354meps323107

Kuffner I B Brock J C Grober-Dunsmore R BonitoV E Hickey T D amp Wright C W (2007) Re-lationships between reef fish communities and re-motely sensed rugosity measurements in BiscayneNational Park Florida USA Environmental Biologyof Fishes 78(1) 71ndash82 doi101007s10641-006-9078-4

Kuffner I B Brock J C Grober-Dunsmore R HickeyT D Bonito V Bracone J E amp Wright C W(2008) Biological communities and geomorphology ofpatch reefs in Biscayne National Park Florida USAUS Geological Survey Open File Report 2008-1330

Lewis J B (2004) Has random sampling been neglectedin coral reef faunal surveys Coral Reefs 23(2) 192ndash194 doi101007s00338-004-0377-y

Lirman D amp Biber P (2000) Seasonal dynamics ofmacroalgal communities of the northern Florida reeftract Botanica Marina 43 305ndash314 doi101515BOT2000033

Lirman D amp Fong P (2007) Is proximity to land-basedsources of coral stressors an appropriate measure ofrisk to coral reefs An example from the FloridaReef Tract Marine Pollution Bulletin 54 779ndash791doi101016jmarpolbul200612014

Maliao R J Turingan R G amp Lin J (2008) Phase-shiftin coral reef communities in the Florida Keys NationalMarine Sanctuary (FKNMS) USA Marine Biology(Berlin) 154 841ndash853 doi101007s00227-008-0977-0

Marszalek D S Babashoff G Noel M R amp Worley DR (1977) Reef distribution in South Florida In Pro-ceedings of the 3rd international coral reef symposium(pp 223ndash229) Miami

McAfee S T amp Morgan S G (1996) Resource use byfive sympatric parrot fishes in the San Blas Archipel-ago Panama Marine Biology (Berlin) 125 427ndash437

McClanahan T R (1994) Kenyan coral reef lagoonfish Effects of fishing substrate complexity andsea urchins Coral Reefs 13 231ndash241 doi101007BF00303637

Miller M W Weil E amp Szmant A M (2000a)Coral recruitment and juvenile mortality as structur-ing factors for reef benthic communities in BiscayneNational Park USA Coral Reefs 19(2) 115ndash123doi101007s003380000079

Miller S L Swanson D W amp Chiappone M (2000b)Multiple spatial scale assessment of coral reef andhard-bottom community structure in the Florida KeysNational Marine Sanctuary In Proceedings of the 9thinternational coral reef symposium (pp 69ndash74) BaliIndonesia


Morrison D (1988) Comparing fish and urchin grazingin shallow and deeper coral reef algal communitiesEcology 69(5) 1367ndash1382 doi1023071941634

Morse D E Hooker N Morse A N C amp JensenR A (1988) Control of larval metamorphosis andrecruitment in sympatric agariciid corals Journal ofExperimental Marine Biology and Ecology 116 193ndash217 doi1010160022-0981(88)90027-5

Murdoch T J T amp Aronson R B (1999) Scale-dependent spatial variability of coral assemblagesalong the Florida Reef Tract Coral Reefs 18(4) 341ndash351 doi101007s003380050210

Paddack M J Cowen R K amp Sponaugle S (2006)Grazing pressure of herbivorous coral reef fisheson low coral-cover reefs Coral Reefs 25 461ndash472doi101007s00338-006-0112-y

Pandolfi J M amp Jackson J B C (2006) Ecologicalpersistence interrupted in Caribbean coral reefsEcology Letters 9 818ndash826 doi101111j1461-0248200600933x

Pandolfi J M Bradbury R H Sala E Hughes TP Bjorndal K A Cooke R G et al (2003)Global trajectories of the long-term decline of coralreef ecosystems Science 301 955ndash958 doi101126science1085706

Pandolfi J M Jackson J B C Baron N Bradbury RH Guzman H M Hughes T P et al (2005) AreUS coral reefs on the slippery slope to slime Science307 1725ndash1726 doi101126science1104258

Porter J W amp Meier O W (1992) Quantification ofloss and change in Floridian reef coral populationsAmerican Zoologist 32 625ndash640

Porter J W Kosmynin V Patterson K L Porter K GJaap W C Wheaton J L et al (2002) Detectionof coral reef change by the Florida Keys Coral ReefMonitoring Project In J W Porter amp K G Porter(Eds) The everglades Florida Bay and coral reefs ofthe Florida Keys An ecosystem sourcebook (pp 749ndash769) Boca Raton CRC Press

Risk M J (1972) Fish diversity on a coral reef in theVirgin Islands Atoll Research Bulletin 153 1ndash6

Russ G R (2003) Grazer biomass correlates morestrongly with production than with biomass of algalturfs on a coral reef Coral Reefs 22 63ndash67

Sale P F amp Douglas W A (1984) Temporal variabil-ity in the community structure of fish on coral patch

reefs and the relation of community structure toreef structure Ecology 65(2) 409ndash422 doi1023071941404

Suchanek T H amp Green D J (1981) Interspecific com-petition between Palythoa caribaeorum and other ses-sile invertebrates on St Croix reefs US Virgin IslandsIn Proceedings of the 4th international coral reef sym-posium (pp 679ndash684) Manila

Syms C (1995) Multi-scale analysis of habitat associationin a guild of blennioid fishes Marine Ecology ProgressSeries 125 31ndash43 doi103354meps125031

Syms C amp Jones G P (2000) Disturbance habitat struc-ture and the dynamics of a coral-reef fish communityEcology 81(10) 2714ndash2729

Tilmant J T Curry R W Jones J Szmant A ZiemanJ C Flora M et al (1994) Hurricane Andrewrsquos ef-fects on marine resources Bioscience 44(4) 230ndash237doi1023071312227

Vroom P Walters L Beach K Coyer J Smith JAbgrall M et al (2005) Hurricane induced propa-gation and rapid regrowth of the weedy brown algaDictyota in the Florida Keys Florida Scientist 68161ndash174

Walters L J amp Smith C M (1994) Rapid rhizoidproduction in Halimeda discoidea Decaisne(Chlorophyta Caulerpales) fragments A mechanismfor survival after separation from adult thalliJournal of Experimental Marine Biology andEcology 175(1) 105ndash120 doi1010160022-0981(94)90178-3

Wilkinson C R (1999) Global and local threats to coralreef functioning and existence Review and predic-tions Marine amp Freshwater Research 50 867ndash878doi101071MF99121

Williams A H (1981) An analysis of competitive inter-actions in a patchy back-reef environment Ecology62(4) 1107ndash1120 doi1023071937008

Williams I D amp Polunin N V C (2001) Large-scaleassociations between macroalgae cover and grazerbiomass on mid-depth reefs in the Caribbean CoralReefs 19(4) 358ndash366

Williams I D Polunin N V C amp Hendrick V J (2001)Limits to grazing by herbivorous fishes and the impactof low coral cover on macroalgal abundance on a coralreef in Belize Marine Ecology Progress Series 222187ndash196 doi103354meps222187


dation has continued despite concerted efforts atresource management (Keller and Causey 2005)Understanding how and why species are distrib-uted across the seascape is critical to managingcoral reef ecosystems

Controversy exists over what variables in-fluence community structure on reefs and theamount of time these communities spend at equi-librium (Connell 1978) Study results are oftendependent upon scale andor the range of habitatsbeing considered (Syms 1995 Eagle et al 2001Chittaro 2004) Generally one body of literaturesupports niche diversification and predicts highlyordered communities (eg Connolly et al 2005)while another supports a more stochastic viewhighlighting the importance of spatially and tem-porally variable recruitment of larvae (eg Saleand Douglas 1984 Doherty and Fowler 1994)However with backgrounds of considerable tem-poral and spatial variability in fish and benthiccommunity structure many studies support hu-man extraction and alteration of habitat and wa-ter quality as determinants of coral reef status(McClanahan 1994 Chapman and Kramer 2001Halpern and Warner 2002 Graham et al 2006Pandolfi and Jackson 2006 Maliao et al 2008)Human disturbance could in effect mask anynatural relationships between species and theirhabitat by altering the limiting factors that controlpopulations

There are over 4000 patch reefs in the northernFlorida Keys (Marszalek et al 1977) highlightingthis ecotype as one of importance to the Floridareef tract (Jones 1977) Other researchers havedocumented these patch reefs as being biologi-cally diverse with substantial live coral comparedto outer-tract reefs (Miller et al 2000a) Fisheriesand fish habitat (Ault et al 2001) and benthiccommunity structure (Chiappone and Sullivan1997 Miller et al 2000b) assessment effortsconducted over the last few decades have un-derrepresented the patch reef habitat thus wedecided on this habitat as the focus of our studyThough there are a fair number of reports includ-ing data on coral populations in Biscayne NationalPark (BNP Burns 1985 Porter and Meier 1992Greenstein and Pandolfi 1997 Ginsburg et al2001 Lirman and Fong 2007) studies on inverte-brate and macroalgal communities are few

The purpose of this study was first to pro-vide a detailed description of patch reef commu-nity structure in BNP and second to examinethe relationships among physical benthic com-munity and fish assemblage variables Using insitu diver surveys we measured fish abundanceat the species level percent benthic cover bycoral algae and encrusting invertebrates coralrecruit density and other variables at 12 patchreefs within BNP Data were compiled for 196stations where physical and benthic variables weremeasured including a subset of 119 stations wherefish were also surveyed We hypothesized that thedifference in variables between reefs would beinsignificant since we expected the patch reefs torepresent a homogeneous habitat We anticipatedthat specific relationships between fish and ben-thic variables would be evident predicting lowfleshy algal abundance at stations where herbiv-orous fish were abundant (and conversely moresuitable settlement substratum for coral larvae)and high fish abundance at stations where gor-gonians were dense We also expected to seesignificant correlations between benthic variablesand the physical habitat predicting that macroal-gae would be more abundant on topographicallyflatter parts of the reef The relationships betweenphysical (eg rugosity) and fish variables are thesubject of a previous paper (Kuffner et al 2007)and are not discussed here

Our results were different than expected show-ing more variance between rather than withinreefs and revealing no strong relationships be-tween physical benthic and fish variables Wediscuss possible mechanisms that could help ex-plain the patterns in community structure andthe lack of correlations between variables that weobserved on these patch reefs and suggest possi-ble mechanisms influencing patch reef communitystructure in BNP

Materials and methods

Field assessment of physical benthicand fish variables

Underwater surveys were conducted via scubadiving on 12 small (asymp1 ha) patch reefs in Biscayne



























Tab

le3

Mea

nsan

dst

anda

rder

ror

(SE

)in

perc

entc

over

(exc

eptw

here

note

d)fo

rm

ajor

spac

e-oc

cupy

ing

bent

hic

orga

nism

s(n

=16

stat

ions

exce

ptre

efL

ima

n=

20)

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

ap

valu

e(A

NO

VA

)

Liv

eco

ral

96

108

84

54

43

29

46

44

38

34

20

56

000

35(n

p)SE

26

35

15

24

12

10

17

22

14

10

07

28

Cor

alre

crui

ts(n

ope

rsq

uare

met

er)

90

140

130

60

260

180

60

10

64

110

80

50

006

97(n

p)SE

29

44

55

20

85

74

25

10

21

28

44

28

Cya

noph

ytes

34

71

118

33

82

107

74

98

47

92

97

94

001

82(n

p)SE

09

13

22

13

28

22

16

25

13

36

19

48

Hal

imed

atu

na16

612

112

414

410

214

814

812

86

79

66

610

90

0009

(np)

SE1

91

71

72

01

51

72

12

82

21

81

52

8D

icty

ota

spp

177

185

255

147

17

212

136

178

156

164

86

129

lt0

0001

(np)

SE2

22

72

72

90

42

62

42

81

72

91

62

1Su

itab

lese

ttle

men

tsub

stra

tum

219

204

148

295

276

252

215

184

172

137

179

221

012

77(n

p)SE

32

27

27

50

49

47

36

44

34

29

35

36

Mill

epor

aal

cico

rnis

08

23

12

26

10

04

09

27

10

16

10

38

046

06(n

p)SE

03

09

06

14

03

02

05

12

05

07

05

15

Gor

goni

anho

ldfa

sts

19

06

09

24

33

17

23

25

26

27

48

39

lt0

0001

(np)

SE0

50

30

30

70

40

40

50

60

60

51

01

6G

orgo

nian

dens

ity

(no

per

squa

rem

eter

)30

523

029

041

823

534

340

029

337

928

329

836

5lt

000

01SE

39

19

35

29

20

28

29

33

28

24

36

27

Gor

goni

anvo

lum

e(m

3m

minus2)

014

030

019

027

044

028

017

070

029

033

057

013

002

53(n

p)SE

003

007

005

006

016

006

003

026

006

008

019

019

Ery

thro

podi

umca

riba

eoru

m2

53

33

71

51

90

31

90

73

23

31

71

10

5509

(np)

SE0

92

31

90

71

10

21

60

51

71

50

80

7P

alyt

hoa

cari

baeo

rum

02

01

01

13

05

13

60

46

112

09

38

39

000

58(n

p)SE

01

01

01

09

05

05

31

25

39

07

18

30

Bri

areu

mas

best

inum

12

38

36

18

31

11

24

18

50

13

39

11

004

71(n

p)SE

06

14

12

05

08

07

07

06

17

04

15

06

Por

ifer

a2

93

61

64

63

63

42

61

93

42

66

52

30

2317

(np)

SE1

01

30

61

00

91

00

90

60

81

01

90

6

Rea

ders

shou

ldke

epin

min

dth

atco

nduc

ting

mul

tipl

eon

e-w

ayA

NO

VA

son

data

colle

cted

from

the

sam

esa

mpl

esis

not

advi

sabl

edu

eto

noni

ndep

ende

nce

ofte

sts

The

auth

ors

pres

ent

thes

ere

sult

she

resi

mpl

yto

dem

onst

rate

that

in

gene

ral

ther

ew

asa

pron

ounc

edre

efef

fect

inth

edi

stri

buti

ons

ofbe

nthi

cor

gani

sms

Stat

isti

cal

test

resu

lts

(AN

OV

A)

are

also

incl

uded

wit

hp

valu

eslt

005

inbo

ldnp

nonp

aram

etri

cK

rusk

alndashW

allis

AN

OV

Aap

plie

d(u

sual

lydu

eto

uneq

ualv

aria

nce

amon

gre

efs)

wit

hp

valu

ere

port

edus

ing

chi-

squa

red

appr

oxim

atio

n



Results

Physical variables




0

20

40

60

80

100


Reef

Su

bstr

atu

m t

yp

e (

c

over)




Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






















































































































Tab

le3

Mea

nsan

dst

anda

rder

ror

(SE

)in

perc

entc

over

(exc

eptw

here

note

d)fo

rm

ajor

spac

e-oc

cupy

ing

bent

hic

orga

nism

s(n

=16

stat

ions

exce

ptre

efL

ima

n=

20)

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

ap

valu

e(A

NO

VA

)

Liv

eco

ral

96

108

84

54

43

29

46

44

38

34

20

56

000

35(n

p)SE

26

35

15

24

12

10

17

22

14

10

07

28

Cor

alre

crui

ts(n

ope

rsq

uare

met

er)

90

140

130

60

260

180

60

10

64

110

80

50

006

97(n

p)SE

29

44

55

20

85

74

25

10

21

28

44

28

Cya

noph

ytes

34

71

118

33

82

107

74

98

47

92

97

94

001

82(n

p)SE

09

13

22

13

28

22

16

25

13

36

19

48

Hal

imed

atu

na16

612

112

414

410

214

814

812

86

79

66

610

90

0009

(np)

SE1

91

71

72

01

51

72

12

82

21

81

52

8D

icty

ota

spp

177

185

255

147

17

212

136

178

156

164

86

129

lt0

0001

(np)

SE2

22

72

72

90

42

62

42

81

72

91

62

1Su

itab

lese

ttle

men

tsub

stra

tum

219

204

148

295

276

252

215

184

172

137

179

221

012

77(n

p)SE

32

27

27

50

49

47

36

44

34

29

35

36

Mill

epor

aal

cico

rnis

08

23

12

26

10

04

09

27

10

16

10

38

046

06(n

p)SE

03

09

06

14

03

02

05

12

05

07

05

15

Gor

goni

anho

ldfa

sts

19

06

09

24

33

17

23

25

26

27

48

39

lt0

0001

(np)

SE0

50

30

30

70

40

40

50

60

60

51

01

6G

orgo

nian

dens

ity

(no

per

squa

rem

eter

)30

523

029

041

823

534

340

029

337

928

329

836

5lt

000

01SE

39

19

35

29

20

28

29

33

28

24

36

27

Gor

goni

anvo

lum

e(m

3m

minus2)

014

030

019

027

044

028

017

070

029

033

057

013

002

53(n

p)SE

003

007

005

006

016

006

003

026

006

008

019

019

Ery

thro

podi

umca

riba

eoru

m2

53

33

71

51

90

31

90

73

23

31

71

10

5509

(np)

SE0

92

31

90

71

10

21

60

51

71

50

80

7P

alyt

hoa

cari

baeo

rum

02

01

01

13

05

13

60

46

112

09

38

39

000

58(n

p)SE

01

01

01

09

05

05

31

25

39

07

18

30

Bri

areu

mas

best

inum

12

38

36

18

31

11

24

18

50

13

39

11

004

71(n

p)SE

06

14

12

05

08

07

07

06

17

04

15

06

Por

ifer

a2

93

61

64

63

63

42

61

93

42

66

52

30

2317

(np)

SE1

01

30

61

00

91

00

90

60

81

01

90

6

Rea

ders

shou

ldke

epin

min

dth

atco

nduc

ting

mul

tipl

eon

e-w

ayA

NO

VA

son

data

colle

cted

from

the

sam

esa

mpl

esis

not

advi

sabl

edu

eto

noni

ndep

ende

nce

ofte

sts

The

auth

ors

pres

ent

thes

ere

sult

she

resi

mpl

yto

dem

onst

rate

that

in

gene

ral

ther

ew

asa

pron

ounc

edre

efef

fect

inth

edi

stri

buti

ons

ofbe

nthi

cor

gani

sms

Stat

isti

cal

test

resu

lts

(AN

OV

A)

are

also

incl

uded

wit

hp

valu

eslt

005

inbo

ldnp

nonp

aram

etri

cK

rusk

alndashW

allis

AN

OV

Aap

plie

d(u

sual

lydu

eto

uneq

ualv

aria

nce

amon

gre

efs)

wit

hp

valu

ere

port

edus

ing

chi-

squa

red

appr

oxim

atio

n



Results

Physical variables




0

20

40

60

80

100


Reef

Su

bstr

atu

m t

yp

e (

c

over)




Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






































































































Tab

le3

Mea

nsan

dst

anda

rder

ror

(SE

)in

perc

entc

over

(exc

eptw

here

note

d)fo

rm

ajor

spac

e-oc

cupy

ing

bent

hic

orga

nism

s(n

=16

stat

ions

exce

ptre

efL

ima

n=

20)

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

ap

valu

e(A

NO

VA

)

Liv

eco

ral

96

108

84

54

43

29

46

44

38

34

20

56

000

35(n

p)SE

26

35

15

24

12

10

17

22

14

10

07

28

Cor

alre

crui

ts(n

ope

rsq

uare

met

er)

90

140

130

60

260

180

60

10

64

110

80

50

006

97(n

p)SE

29

44

55

20

85

74

25

10

21

28

44

28

Cya

noph

ytes

34

71

118

33

82

107

74

98

47

92

97

94

001

82(n

p)SE

09

13

22

13

28

22

16

25

13

36

19

48

Hal

imed

atu

na16

612

112

414

410

214

814

812

86

79

66

610

90

0009

(np)

SE1

91

71

72

01

51

72

12

82

21

81

52

8D

icty

ota

spp

177

185

255

147

17

212

136

178

156

164

86

129

lt0

0001

(np)

SE2

22

72

72

90

42

62

42

81

72

91

62

1Su

itab

lese

ttle

men

tsub

stra

tum

219

204

148

295

276

252

215

184

172

137

179

221

012

77(n

p)SE

32

27

27

50

49

47

36

44

34

29

35

36

Mill

epor

aal

cico

rnis

08

23

12

26

10

04

09

27

10

16

10

38

046

06(n

p)SE

03

09

06

14

03

02

05

12

05

07

05

15

Gor

goni

anho

ldfa

sts

19

06

09

24

33

17

23

25

26

27

48

39

lt0

0001

(np)

SE0

50

30

30

70

40

40

50

60

60

51

01

6G

orgo

nian

dens

ity

(no

per

squa

rem

eter

)30

523

029

041

823

534

340

029

337

928

329

836

5lt

000

01SE

39

19

35

29

20

28

29

33

28

24

36

27

Gor

goni

anvo

lum

e(m

3m

minus2)

014

030

019

027

044

028

017

070

029

033

057

013

002

53(n

p)SE

003

007

005

006

016

006

003

026

006

008

019

019

Ery

thro

podi

umca

riba

eoru

m2

53

33

71

51

90

31

90

73

23

31

71

10

5509

(np)

SE0

92

31

90

71

10

21

60

51

71

50

80

7P

alyt

hoa

cari

baeo

rum

02

01

01

13

05

13

60

46

112

09

38

39

000

58(n

p)SE

01

01

01

09

05

05

31

25

39

07

18

30

Bri

areu

mas

best

inum

12

38

36

18

31

11

24

18

50

13

39

11

004

71(n

p)SE

06

14

12

05

08

07

07

06

17

04

15

06

Por

ifer

a2

93

61

64

63

63

42

61

93

42

66

52

30

2317

(np)

SE1

01

30

61

00

91

00

90

60

81

01

90

6

Rea

ders

shou

ldke

epin

min

dth

atco

nduc

ting

mul

tipl

eon

e-w

ayA

NO

VA

son

data

colle

cted

from

the

sam

esa

mpl

esis

not

advi

sabl

edu

eto

noni

ndep

ende

nce

ofte

sts

The

auth

ors

pres

ent

thes

ere

sult

she

resi

mpl

yto

dem

onst

rate

that

in

gene

ral

ther

ew

asa

pron

ounc

edre

efef

fect

inth

edi

stri

buti

ons

ofbe

nthi

cor

gani

sms

Stat

isti

cal

test

resu

lts

(AN

OV

A)

are

also

incl

uded

wit

hp

valu

eslt

005

inbo

ldnp

nonp

aram

etri

cK

rusk

alndashW

allis

AN

OV

Aap

plie

d(u

sual

lydu

eto

uneq

ualv

aria

nce

amon

gre

efs)

wit

hp

valu

ere

port

edus

ing

chi-

squa

red

appr

oxim

atio

n



Results

Physical variables




0

20

40

60

80

100


Reef

Su

bstr

atu

m t

yp

e (

c

over)




Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References





























































































Tab

le3

Mea

nsan

dst

anda

rder

ror

(SE

)in

perc

entc

over

(exc

eptw

here

note

d)fo

rm

ajor

spac

e-oc

cupy

ing

bent

hic

orga

nism

s(n

=16

stat

ions

exce

ptre

efL

ima

n=

20)

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

ap

valu

e(A

NO

VA

)

Liv

eco

ral

96

108

84

54

43

29

46

44

38

34

20

56

000

35(n

p)SE

26

35

15

24

12

10

17

22

14

10

07

28

Cor

alre

crui

ts(n

ope

rsq

uare

met

er)

90

140

130

60

260

180

60

10

64

110

80

50

006

97(n

p)SE

29

44

55

20

85

74

25

10

21

28

44

28

Cya

noph

ytes

34

71

118

33

82

107

74

98

47

92

97

94

001

82(n

p)SE

09

13

22

13

28

22

16

25

13

36

19

48

Hal

imed

atu

na16

612

112

414

410

214

814

812

86

79

66

610

90

0009

(np)

SE1

91

71

72

01

51

72

12

82

21

81

52

8D

icty

ota

spp

177

185

255

147

17

212

136

178

156

164

86

129

lt0

0001

(np)

SE2

22

72

72

90

42

62

42

81

72

91

62

1Su

itab

lese

ttle

men

tsub

stra

tum

219

204

148

295

276

252

215

184

172

137

179

221

012

77(n

p)SE

32

27

27

50

49

47

36

44

34

29

35

36

Mill

epor

aal

cico

rnis

08

23

12

26

10

04

09

27

10

16

10

38

046

06(n

p)SE

03

09

06

14

03

02

05

12

05

07

05

15

Gor

goni

anho

ldfa

sts

19

06

09

24

33

17

23

25

26

27

48

39

lt0

0001

(np)

SE0

50

30

30

70

40

40

50

60

60

51

01

6G

orgo

nian

dens

ity

(no

per

squa

rem

eter

)30

523

029

041

823

534

340

029

337

928

329

836

5lt

000

01SE

39

19

35

29

20

28

29

33

28

24

36

27

Gor

goni

anvo

lum

e(m

3m

minus2)

014

030

019

027

044

028

017

070

029

033

057

013

002

53(n

p)SE

003

007

005

006

016

006

003

026

006

008

019

019

Ery

thro

podi

umca

riba

eoru

m2

53

33

71

51

90

31

90

73

23

31

71

10

5509

(np)

SE0

92

31

90

71

10

21

60

51

71

50

80

7P

alyt

hoa

cari

baeo

rum

02

01

01

13

05

13

60

46

112

09

38

39

000

58(n

p)SE

01

01

01

09

05

05

31

25

39

07

18

30

Bri

areu

mas

best

inum

12

38

36

18

31

11

24

18

50

13

39

11

004

71(n

p)SE

06

14

12

05

08

07

07

06

17

04

15

06

Por

ifer

a2

93

61

64

63

63

42

61

93

42

66

52

30

2317

(np)

SE1

01

30

61

00

91

00

90

60

81

01

90

6

Rea

ders

shou

ldke

epin

min

dth

atco

nduc

ting

mul

tipl

eon

e-w

ayA

NO

VA

son

data

colle

cted

from

the

sam

esa

mpl

esis

not

advi

sabl

edu

eto

noni

ndep

ende

nce

ofte

sts

The

auth

ors

pres

ent

thes

ere

sult

she

resi

mpl

yto

dem

onst

rate

that

in

gene

ral

ther

ew

asa

pron

ounc

edre

efef

fect

inth

edi

stri

buti

ons

ofbe

nthi

cor

gani

sms

Stat

isti

cal

test

resu

lts

(AN

OV

A)

are

also

incl

uded

wit

hp

valu

eslt

005

inbo

ldnp

nonp

aram

etri

cK

rusk

alndashW

allis

AN

OV

Aap

plie

d(u

sual

lydu

eto

uneq

ualv

aria

nce

amon

gre

efs)

wit

hp

valu

ere

port

edus

ing

chi-

squa

red

appr

oxim

atio

n



Results

Physical variables




0

20

40

60

80

100


Reef

Su

bstr

atu

m t

yp

e (

c

over)




Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






























































































Results

Physical variables




0

20

40

60

80

100


Reef

Su

bstr

atu

m t

yp

e (

c

over)




Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






























































































Benthic variables




Physical

B

DE

G

H

I

J

K

L

N

O

P

2D Stress 009

Benthic

B

D

E

G

H

I

JK

L

N

OP

2D Stress 014

Fish

B

D

E G

I

JL

NO

P

2D Stress 005




0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






























































































0

10

20

30

40

50


Reef

Plexaurella

Muriceopsis

Muricea

Briareum

Pseudoplexaura

Gorgonia

Plexaura

Eunicea

Pseudopterogorgia


0

10

20

30

40

50


Reef











Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References




































































































Fish variables






Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References





























































































Tab

le4

Spec

ies

listo

fhar

dco

rals

at12

patc

hre

efs

inB

isca

yne

Nat

iona

lPar

k

Bra

voD

elta

Ech

oG

olf

Hot

elIn

digo

Julie

tK

iloL

ima

Nov

O

scar

Pap

a

Acr

opor

ace

rvic

orni

sx

(wm

c)

x(w

)x

(w)

x(w

)x

(w)

x(w

)x

(wm

)x

(w)

x(w

m)

x(w

mc

)x

(w)

Aga

rici

aag

aric

ites

xx

xx

xx

xx

xx

xx

Aga

rici

afr

agili

sx

xx

xx

xx

xx

xx

Col

poph

yllia

nata

nsx

xx

xx

xx

xx

xx

Dic

hoco

enia

stok

esii

xx

xx

xx

xx

xx

xx

Dip

lori

acl

ivos

ax

xx

xx

xx

xx

xx

xD

iplo

ria

laby

rint

hifo

rmis

xx

xx

xx

xx

xx

xx

Dip

lori

ast

rigo

sax

xx

xx

xx

xx

xx

xE

usm

iliaf

astig

iata

xx

xx

xx

xx

xx

xx

Fav

iafr

agum

xx

xx

xx

xx

xx

xH

elio

ceri

scu

culla

tax

xx

xx

xx

xx

xx

Isop

hylli

asi

nuos

ax

Mad

raci

sde

cact

isx

xx

xM

anic

ina

areo

lata

xx

Mea

ndri

nam

eand

rite

sx

xx

xx

xx

xx

xx

xM

illep

ora

alci

corn

isx

xx

xx

xx

xx

xx

xM

onta

stra

eaan

nula

ris

x(p

)x

(pc

)x

xx

(p)

xx

(p)

x(p

)X

x(p

c)

x(p

c)

x(p

)M

onta

stra

eafa

veol

ata

xx

xx

x(p

)x

xx

xx

xM

onta

stra

eafr

anks

ix

xM

onta

stra

eaca

vern

osa

x(b

)x

(b)

xx

xx

(b)

x(b

)x

xx

(b)

xx

Mus

saan

gulo

sax

Myc

etop

hylli

ala

mar

ckia

nax

xx

xX

xM

ycet

ophy

llia

fero

xx

xx

Ocu

lina

diff

usa

xx

xx

Por

ites

astr

eoid

esx

xx

xx

xx

xx

xx

xP

orite

spo

rite

sx

xx

xx

xx

xx

x(h

)x

(h)

xP

orite

sfu

rcat

ax

xx

xx

xx

xx

xx

xSc

olym

iasp

x

xx

xx

xx

xx

Side

rast

rea

radi

ans

xx

xx

xx

xx

xx

xx

Side

rast

rea

side

rea

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

x(d

)x

(d)

Step

hano

coen

iain

ters

epta

xx

x(d

)x

xx

xx

xx

xx

Sole

nast

rea

bour

noni

xx

xx

xx

xx

xx

xSp

ecie

sri

chne

ss26

2424

2521

2527

2526

2625

28

ldquoxrdquo

deno

tes

pres

ence

ofth

esp

ecie

sw

ith

lett

ers

inpa

rent

hese

sde

noti

ngpr

esen

ceof

cora

lstr

esso

rsas

defin

edin

foot

note

Dis

ease

sb

blac

k-ba

ndd

dark

spot

ww

hite

band

fish

dam

age

ppa

rrot

fish

mda

mse

lfish

cor

alpr

edat

ors

cC

oral

lioph

ilaab

brev

iata

hH

erm

odic

eca

runc

ulat

a



Factor df SS MS F p
















Discussion
























Conclusions





References






























































































Factor df SS MS F p
















Discussion
























Conclusions





References




































































































Discussion
























Conclusions





References































































































Discussion
























Conclusions





References













































































































Conclusions





References







































































































Conclusions





References































































































Conclusions





References


































































































































































































































































Biological community structure on patch reefs in Biscayne National Park, FL, USA

Documents