Mar Biol (2008) 154:841–853
DOI 10.1007/s00227-008-0977-0

ORIGINAL PAPER



Phase-shift in coral reef communities in the Florida Keys National
Marine Sanctuary (FKNMS), USA
Ronald J. Maliao · Ralph G. Turingan · Junda Lin




Received: 17 September 2007 / Accepted: 7 April 2008 / Published online: 18 April 2008
© Springer-Verlag 2008


Abstract Characterizing the Florida Keys National            structuring of coral reef communities at a spatial scale
Marine Sanctuary (FKNMS), USA, has gained much atten-          larger than the individual reef. Furthermore, it is conceiv-
tion over the past several decades because of apparent         able that these predictor variables exerted inXuence for a
changes in the benthic community structure over space and        long time rather than being a recent event. Results also
time representative of patterns occurring in the Caribbean       revealed a pattern showing reduction in hard coral cover
region. We used a 5-year dataset (1996–2000) of macroal-        and species richness, and subsequent proliferation of mac-
gal and sponge cover and water quality measurements as         roalgae and sponges during the study period. Our analyses
predictor variables of hard coral community structure in the      of the Florida Keys present a pattern that is consistent with
FKNMS. The 16 water quality variables were summarized          the characteristics of a reef that has undergone a “phase-
into 4 groups by principal component analysis (PCA). Hier-       shift,” a phenomenon that is widely reported in the Carib-
archical agglomerative cluster analysis of the mean and         bean region.
standard deviation (SD) of the principal component scores
of water quality variables separated the reef sites into two
main groups (and Wve sub-groups), referred to as reefs of        Introduction
similar inXuence (RSI). The main groups corresponded
with their geographical locations within the Florida Keys:       The community structure of coral reefs in the Caribbean,
the reefs in the Upper and Middle Keys being homoge-          including the Florida Keys, have remained stable for thou-
neous and collectively, having lower water quality scores        sands of years before the region suVered a catastrophic
relative to reefs in the Lower Keys. Canonical correspon-        coral mass mortality in the 1980s (Hughes 1994; Aronson
dence analysis (CCA) between hard coral cover and key          et al. 1998). Since the 1980s die oV, coral reef deterioration
predictor variables (i.e., water quality, macroalgal cover       has been characterized by a reduction in coral cover by as
and sponge cover) also separated the reefs in the Lower         much as 40%, a shift in the composition of surviving spe-
Keys from reefs in the Upper–Middle Keys, consistent with        cies (Hughes 1994; Greenstein and PandolW 1997; Gardner
results of the cluster analysis, which categorized reefs        et al. 2003), and a phase-shift from coral-dominated to
based on RSI. These results suggest that the prevailing         macroalgal-dominated communities (Dustan 1977; Dustan
gradient of predictor variables may have inXuenced the         and Halas 1987; Porter and Meier 1992; Hughes 1994;
                                    McClanahan and Muthiga 1998; Porter et al. 2002; Gardner
                                    et al. 2003, 2005).
Communicated by R. Cattaneo-Vietti.
                                      The magnitude, scale and cause of the deterioration of
                                    Caribbean coral reefs remain controversial (Hughes 1994;
R. J. Maliao (&) · R. G. Turingan · J. Lin               Ginsburg 1994; Murdoch and Aronson 1999; Bellwood
Department of Biological Sciences,                   et al. 2004). Hypothesized mechanisms working at small
Florida Institute of Technology,
150 West University Blvd.,
                                    spatio-temporal scales (meters to kilometers and days to
Melbourne, FL 32901-6975, USA                      years) include hurricanes (Gardner et al. 2003), point-
e-mail: rmaliao@Wt.edu                         source nutrient loading (Ginsburg and Shinn 1994; Leichter

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842                                                Mar Biol (2008) 154:841–853


et al. 2003), impacts of upstream land use patterns       40 cm above the reef at a constant swim speed of about
(Bellwood et al. 2004), and macroalgal overgrowth (Hughes    4 m/min yielding approximately 9,000 video frames per
1994). Other hypotheses suggest the importance of meso-     transect. Image analysis used a custom software application
to large-scale processes (tens to thousands of kilometers    PointCount for coral reefs, developed speciWcally for the
and decades to millennia), such as sea urchin mass mortal-    CREMP (Wheaton et al. 2001). Percent cover of hard cor-
ity events (Carpenter 1990), larval transport (Galindo et al.  als, macroalgae (Xeshy and Wlamentous and non-coralline)
2006), herbivore reduction due to overWshing (Jackson      and sponges was calculated from the images. Water quality
et al. 2001; PandolW et al. 2003), disease outbreaks (Aron-   monitoring under WQMP was undertaken quarterly from
son and Precht 2001; Porter et al. 2001) and climate change   154 stations. Analyses only included those WQPP stations
(Walther et al. 2002; Hughes et al. 2003). It is unclear     that overlapped with reef sites monitored by CREMP. Six-
whether the current state of the Caribbean coral reefs repre-  teen water quality measurements were included in our anal-
sents a permanent phase-shift or that the community       yses: temperature (°C), salinity (PSU), dissolved oxygen
structure would rebound (Petraitis and Dudgeon 2004).      (DO, mg l¡1), and light attenuation (Kd, m¡1) were col-
Long-term monitoring of coral reefs in the Florida Keys     lected in the Weld; organic carbon (TOC), total nitrogen
(1981–1991) and US Virgin Islands (1989–2003) have        (TN), total phosphorus (TP), silicate (Si (OH)4), nitrite
indicated no evidence of recovery in terms of coral cover or   (NO2¡), dissolved nitrate (NO3¡), ammonium (NH4+),
reduction of algal abundance over a decadal time scale      soluble reactive phosphate (SRP), chlorophyll a (chl a),
(Porter and Meier 1992; Rogers and Miller 2006).         dissolved inorganic nitrogen (DIN), total unWltered
  The main goal of this study is to Wnd evidence of a possi-  concentrations of organic nitrogen (TON) and turbidity
ble phase-shift in coral reef communities in the Florida     (NTU) were determined in the laboratory from the water
Keys National Marine Sanctuary (FKNMS), USA. SpeciW-       collected in situ (reported in g l¡1) (see Keller and Dona-
cally, this study is designed to determine the correspon-    hue 2006 for the complete sampling protocol).
dence between hard coral cover, macroalgal and sponge
cover and water quality variables using the 1996–2000 data    Data analyses
of the FKNMS Water Quality Protection Program (WQPP).
                                 Data analyses were conducted at the level of reef site using
                                 the 1996¡2000 dataset. Average values of percent cover of
Materials and methods                      benthic biota data (hard corals, macroalgae and sponges)
                                 and water quality measurements were used for those reef
Study site and data collection                  sites with stations at varying depths. In the multivariate
                                 analyses, benthic biota data and water quality measure-
The reef tract of the Florida Keys, which represents the     ments were arcsine square-root and square-root trans-
third largest barrier reef in the world and the only living   formed, respectively, and then data matrices were screened
coral reef in North America (Lapointe and Matzie 1996),     for outliers. Outliers are extreme data values relative to
was designated as a marine sanctuary in 1990, and became     others in a sample and have unduly large eVects on the
known as the FKNMS (Keller and Donahue 2006; Fig. 1).      resultant probabilities (McCune and Grace 2002; Quinn and
The reef tract of the FKNMS, referred to here as the Florida   Keough 2006). For example, outliers may distort estimates
Keys, is partitioned into three regions based on geographic   and P values and inXate sums-of-squares, all of which
and environmental criteria: Upper Keys, Middle Keys, and     would result in faulty conclusions. In our analyses, we deW-
Lower Keys (Ginsburg and Shinn 1994). The WQPP was        ned outliers as those reefs, coral species or water quality
implemented in 1996 to monitor both benthic biota (under     variables with SD (standard deviation) >2 (Quinn and
the Coral Reef Evaluation and Monitoring Project or       Keough 2006) and/or those with sample points <3 (i.e., rare
CREMP) and water quality (under the Water Quality Moni-     samples) (McCune and Grace 2002). Outliers were
toring Project or WQMP) in the Florida Keys until 2002      excluded from all data analyses.
(Keller and Donahue 2006). The CREMP includes 40 reef        Principal component analysis (PCA) was used to extract
sites; benthic biota in two to four permanent stations      the underlying patterns of the water quality variables using
(22 £ 2 m transects) were monitored quarterly on each reef    a correlation matrix based on the average values of the 5-
site. Field monitoring consists of station species inventories  year data. Water quality variables with component loading
(SSI) and video transects conducted in four permanent sta-    ¸ §0.5 were retained in the description of each principal
tions (22 £ 2 m transect) in each reef site. SSI consists of   component. The mean and SD of component scores for
timed (15 min) counts of stony coral species (Milleporina    each reef site were then used as input variables in a hierar-
and Scleractinia) present in each station to provide data on   chical agglomerative cluster analysis by unweighed
hard coral species richness. Video recordings were taken     pair-group method (UPGMA) linkage rule using Euclidean

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Mar Biol (2008) 154:841–853                                                        843




Fig. 1 Map of the Florida Keys showing only the 20 reef sites included in the analyses. Reef abbreviations (enclosed): Western Head (Western),
West Washer Women (West)


distance (ED). Groups of reefs produced by the cluster          CCA, the set of water quality variables identiWed by the
analysis were linked objectively using the similarity proWle       BIOENV routine, and macroalgal and sponge cover were
(SIMPROF) routine (Clarke and Gorley 2006). Reef clus-          used as the predictors of hard coral cover. In addition, the
ters were further merged at 0.5 ED to facilitate interpreta-       variation in hard coral cover and predictor variables over
tion and were referred to as reefs of similar inXuence (RSI).      the 5-year period was examined using a Kruskal–Wallis
The outcome of this analysis reveals the variation in water       test. The variation in hard coral, macroalgal and sponge
quality across reefs in the Florida Keys.                cover, as well as indices of Shannon diversity and species
  Canonical correspondence analysis (CCA) (ter Braak          richness of hard corals between 1996 and 2000 were further
1986), the most widely used direct gradient ordination          examined using Mann–Whitney U test.
method (Palmer 1993; ter Braak and Verdonschot 1995;            The robustness of the result of CCA was determined by
McCune 1997; GraVelman 2001; McCune and Grace              Monte–Carlo permutation test (ter Braak 1986). Ordination
2002), was employed to determine the multivariate correla-        scores in the CCA biplots were optimized by coral species
tion between hard coral community structure and predictor        using the linear combination (LC scores) of predictor vari-
variables. The minimal set of water quality variables          ables. LC scores were used because they best represent the
entered in the CCA was identiWed by the BIOENV routine          relative contribution of each predictor variable to the varia-
(Clarke and Ainsworth 1993; Clarke and Gorley 2006). The         tion in hard coral cover (McCune and Grace 2002) and
water quality variables were screened for multicollinearity       have been shown to perform well even in skewed distribu-
prior to running the BIOENV routine and only a representa-        tions (Palmer 1993). In the ordination biplot, predictor
tive of highly correlated water quality variables (i.e., those      variables are represented as arrows and the length of the
with Spearman’s = ¸ §0.8) were used. Pruning of pre-           arrow indicates the relative importance of each predictor
dictor variables to a minimal set that accounts for the larg-      variable (ter Braak 1986). The angle between arrows
est variation in the hard coral community structure was         indicates the degree of correlation between predictor vari-
necessary because the result of CCA becomes less robust as        ables; the location of the reef or species relative to the
the number of predictor variables increases (McCune and         arrow indicates site characteristics or species preferences
Grace 2002) and to minimize the problem associated with         (Palmer 1993). Since ordination scores were calculated
multicollinearity (ter Braak and Looman 1994). In our          using LC scores, the relative contribution of the predictor

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844                                                   Mar Biol (2008) 154:841–853


variables in each axis was determined from the intraset cor-     ond main group (Fig. 2a). The physical property component
relation output (McCune and Grace 2002). A predictor var-       (PC4: salinity, temperature and DO) and the algal bloom
iable with correlation coeYcient of ¸ §0.4 is considered       component (PC2: chl a, TP, and turbidity) appeared to be
ecologically relevant (Rakocinski et al. 1996). The main       the main components driving Florida Keys-wide variation
advantage of CCA is that it allowed simultaneous explora-       in water quality, with higher values in the Lower Keys and
tion of relationships among diVerent reef sites or coral       lower values in the Middle and Upper Keys (Fig. 2b).
species with multiple predictor variables.                Results of running the BIOENV routine revealed that
  Cluster analysis and SIMPROF and BIOENV routines          TN, chl a and salinity are the principal set of water quality
were conducted using PRIMER version 6.1.9 (Plymouth          variables signiWcantly explaining the variation in hard coral
Routines Multivariate Ecological Research, PRIMER-E          community structure ( w = 0.393, P < 0.05, global BEST
Ltd, Plymouth, UK; Clarke and Gorley 2006) while the         permutation test). TN Xuctuated signiWcantly across the
CCA was conducted using PC-Ord version 5 (MjM Soft-          5-year monitoring period (Kruskal–Wallis test, P < 0.01,
ware, Oregon, USA; McCune and MeVord1999; McCune           Fig. 3a); chl a and salinity remained stable (Kruskal–Wallis
and Grace 2002). PCA and univariate tests were conducted       test, P > 0.05, Fig. 3b, c).
using SPSS 14 (SPSS Inc., Chicago, USA).
                                   Reef community structure

Results                                Macroalgal cover signiWcantly increased from 1996 to 2000
                                   (Kruskal–Wallis test, P < 0.001, Fig. 3d), with an almost
Reefs of similar inXuence                       triple increase from the 1996 (5.7%) to 1998 (16.5%) level.
                                   The macroalgal cover in 1996 had signiWcantly increased
The 16 water quality variables were reduced into four prin-      by 68% in 2000 (9.6%) (Mann–Whitney U test, P < 0.05).
cipal components (PC), explaining 82.3% of the total varia-      Although sponge cover had varied signiWcantly across
tion in the data set (Table 1). PC 1 to 4 are referred to as     years (Kruskal–Wallis test, P < 0.01, Fig. 3e), the diVer-
organic component, algal bloom component, inorganic          ence between 1996 and 2000 was not signiWcant (Mann–
nitrogen component and physical properties component,         Whitney U test, P > 0.05).
respectively. Cluster analysis of the mean and SD of the         Forty-two coral species were identiWed in the Florida Keys.
component scores separated the reefs into two main groups       In terms of percent cover, the Montastraea annularis complex
and Wve subgroups; the Upper and Middle Keys reefs form        dominated the hard coral species in the Florida Keys (Fig. 4a).
the Wrst main group and the Lower Keys reefs form the sec-      Collectively, hard coral cover showed a decreasing trend

Table 1 Result of the PCA with
                 Water quality parameters          Component
Varimax rotation for 16 water
quality variables                              PC1       PC2       PC3       PC4

                 Total organic nitrogen (TON)         0.865      0.373      0.163     ¡0.010
                 Total nitrogen (TN)             0.860      0.380      0.194     ¡0.017
                 Silicate SI (OH)4              0.819      0.335      0.322      0.141
                 Light attenuation (Kd)            0.781     ¡0.249      0.044      0.053
                 Total organic carbon (TOC)          0.752      0.482      0.326     ¡0.149
                 Nitrite (NO2¡)               0.572      0.017      0.501     ¡0.402
                 Chlorophyll a (Chl a)            0.051      0.843      0.050      0.439
                 Total phosphorus (TP)            0.153      0.834     ¡0.045      0.257
                 Turbidity                  0.361      0.725      0.260     ¡0.082
                 Nitrate (NO3¡)               0.232      0.250      0.887      0.070
                 Soluble reactive phosphorus (SRP)      0.038     ¡0.176      0.847      0.113
                 Dissolved inorganic nitrogen (DIN)      0.384      0.276      0.829     ¡0.176
Water quality variables with   Temperature                 0.208      0.267      0.099      0.873
component loadings ¸ §0.5    Dissolved oxygen (DO)            0.322     ¡0.151      0.047     ¡0.816
(bolded text) were retained to
describe each component (PCA   Salinity                   0.477      0.258      0.147      0.760
PC1 = organic; PC2 = algal    Ammonium (NH4+)               0.320      0.236      0.278     ¡0.475
bloom; PC3 = inorganic      Percent variance explained         28.118      18.791     18.141      17.211
nitrogen; PC4 = physical     (Total = 82.261)
properties)


123
Mar Biol (2008) 154:841–853                                                                              845




Fig. 2 a Dendogram of reef sites based on the cluster analysis of mean                Wve subgroups (1–5); b mean of four PCA component scores of water
and SD of PCA component scores of water quality variables. Objective                 quality variables across RSI; error bars indicate §standard error of
grouping of clusters (dashed line) was based on SIMPROF routine.                   mean. RSI numbers refer to reef clusters in a
Clusters were further merged at 0.5 ED resemblance, forming a total of

     1.4                              4.5
  a        Total nitrogen             b           Chl a
     1.2                              4.0
                                     3.5
     1.0
                                     3.0
     0.8                              2.5
                             mg l-1
mg l-1




     0.6                              2.0
        n=102    140   141  143  143              n=102    140   141   143     143
                                     1.5
     0.4
                                     1.0
     0.2
                                     0.5
     0.0                              0.0
         0.16    0.14  0.13  0.13  0.11
                                        0.315   0.260   0.289  0.312  0.278


     39                               80                           e  35
  c      n=102    140   141  143  143   d          n=136 in each year      Macroalgae          n=136 in each year        Sponge
     38                               70                             30
        Salinity
     37                               60
                                                                   25
     36                               50
                                                                   20
                              cent cover




     35                               40
 PSU




                                                                   15
     34                               30
                                                                   10
                             Per




     33                               20
     32                               10                             5
         36.3    36.3  35.6  36.2  36.3
     31                               0                             0
                                         5.7     4.9   16.5   6.1     9.6       2.2    1.9   1.3  1.4    2.2
     30
         1996   1997  1998  1999  2000              1996    1997  1998   1999    2000       1996   1997   1998  1999   2000
                                        Year

Fig. 3 Box-plots of predictor variables entered in CCA : a TN, b chl                 percentiles. Points outside the whiskers are the outliers. Numbers
a, c salinity, d macroalgae, and e sponge. The center line of the box is               below the box are the median values. These values were calculated
the median, the bottom and top of the box are the 25th and 75th percen-               from the 20 reefs included in the analyses
tiles and the whiskers below and above of the box are the 10th and 90th

across the 5-year monitoring period, with the lowest level                      Correspondence between predictor variables and hard coral
occurring in 1999 (Kruskal–Wallis test, P < 0.01; Fig. 4b).                     community structure
Hard coral percent cover had signiWcantly decreased by
almost 50%, from 8.1% in 1996 to 4.6% in 2000 (Mann–                         Twenty out of the 25 aggregated reef sites and 35 out of the
Whitney U test, P < 0.05). DiVerences in species richness and                    42 coral species were included in the CCA after data
Shannon diversity index over the two periods were not signiW-                    screening. The CCA revealed two gradients in the coral
cant (Mann–Whitney U test, P > 0.05, Fig. 5a, b).                          community structure, with a total variance (inertia) of

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846                                                                                                  Mar Biol (2008) 154:841–853


Fig. 4 a Percent cover of          a 50                                                       b
                                      Montastraea annularis complex                                   Total hard coral
Montastraea annularis
complex, the most dominant                  40                       n=136 in each year                                                  n=136 in each year
hard coral species in the Florida




                   Percent cover
Keys, and b total hard coral                 30
percent cover. These values
were calculated from the 20                  20
reefs included in the analyses
                               10

                               0
                                                                  0.77 %               8.10 %        8.20 %       5.70 %         4.42 %       4.60 %
                                  1.30 %     1.51 %      1.11 %      0.97 %


                                  1996      1997       1998       1999      2000               1996           1997         1998       1999        2000
                                                                           Year


Fig. 5 a Shannon’s diversity     a            2.5
index and b species richness
of hard corals across reefs
                               2.0
                  Shannon diversity index




between 1996 and 2000

                               1.5


                               1.0

                                               1996
                               0.5              2000


                               0.0

                               30
                   b
                               25
                  Species richness




                               20

                               15

                               10

                                5

                                0
                                                                Western
                                   Jaap

                                       Looe




                                                       Smith




                                                                                          Tennessee




                                                                                                                   Conch
                                                            West
                                               Sambo

                                                    Sand
                                           Rock




                                                                                                                            Molasses
                                                                                                            Carysfort
                                                                                                      Admiral




                                                                                                                                 Porter
                                                                           Dustan




                                                                                                                       Grecian
                                                                     Alligator



                                                                                Long




                                                                                                 Turtle
                                                                                     Sombrero




                                           Lower Keys                           Middle Keys                               Upper Keys
                                                                                Reef


76.52% (Table 2). The Monte–Carlo permutation test                                 The strength and direction of the relationships between
revealed that the CCA was robust (P < 0.01), indicating a                            the predictor variables and reef sites and coral species are
strong correspondence between hard coral community                               illustrated in the CCA biplots (Fig. 6a, b). Macroalgae had
structure and predictor variables. Correlation between hard                           a negative relationship with chl a (T = ¡0.451), as reXected
coral species and the two canonical axes was statistically                           in their opposing position in the canonical space. Chl a and
signiWcant (Monte–Carlo permutation test, P < 0.01,                               sponge cover run parallel with salinity because of the posi-
Table 2). These canonical axes explained 32% of the varia-                           tive relationships between the two former predictor vari-
tion in coral community structure. Macroalgal and sponge                            ables and salinity (chl a–salinity, T = 0.64; sponge–salinity,
cover accounted for high negative contribution to this vari-                          T = 0.44). Reefs in the Upper and Middle Keys aggregated
ation.                                                     in the upper left corner of the canonical space and toward


123
Mar Biol (2008) 154:841–853                                                          847


Table 2 Results of CCA of 35
                                            Axes                  p (Monte–Carlo
coral species in 20 reef sites in
                                                                permutation test)
relation to the Wve predictor                              1          2
variables
                    a. Summary statistics of ordination axes
                    Eigenvalues (total inertia = 0.765)        0.151        0.094       0.01
                    Species-predictor correlation (T)         0.611        0.684       0.01
                    Cumulative % variance explained         19.7        32.0
                    b. Axis intraset correlation coeYcient of predictor variables (coeYcient ¸ §0.4 are considered ecologically
                     relevant and are in bolded text)
                    Macroalgae                    ¡0.851       ¡0.082
                    Salinity                     0.778       ¡0.056
                    Chlorophyll a                   0.713        0.376
                    Sponge                      0.577       ¡0.647
                    Total Nitrogen                  0.390        0.310




Fig. 6 Biplot of a 20 reef sites and b 35 coral species in relation to the  (mea), Millepora alcicornis (mia), Millepora complanata (mil), Mon-
Wve predictor variables entered in the CCA. Species abbreviations (en-    tastraea annularis complex (moa), Montastraea cavernosa (moc),
closed): Acropora cervicornis (arc), Acropora palmata (acr), Agaricia    Mussa angulosa (mus), Mycetophyllia aliciae (myc), Mycetophyllia
agaricites complex (agg), Agaricia fragilis (agf), Agaricia lamarcki     danaana (myd), Mycetophyllia feroz (myf), Mycetophyllia lamarcki-
(agl), Colpophyllia natans (col), Dendrogyra cylindrus (den), Dicho-     ana (myl), Oculina diVusa (ocu), Porites astreoides (pos), Porites
coenia stokesi (dis), Diploria clivosa (dic), Diploria labyrinthiformis   porites (por), Scolymia cubensis (sco), Siderastrea radians (sic),
(dil), Diploria strigosa (dis), Eusmilia fastigiata (eus), Favia fragum   Siderastrea siderea (sid), Solenastrea bournoni (sol) and Stephano-
(fav), Leptoseris cucullata (lep), Madracis decactis (mad), Madracis     coenia michelinii (ste)
mirabilis (mam), Manicina areolata (man), Meandrina meandrites

the macroalgal space; in contrast, reefs in the Lower Keys          Lower Keys). This pattern suggests that the inXuence of
were spread out (Fig. 6a). Most of the coral species are           water quality in aVecting the structure of the benthic biota
aggregated toward the sponge space; in contrast, none            in the Florida Keys occurs in two levels. On the one hand,
aggregated near the chl a space (Fig. 6b).                  there is similarity in water quality within each locale (e.g.,
                                       within the Lower Keys) and on the other, there is a diVer-
                                       ence in water quality between the two regions (e.g.,
Discussion                                  between the Lower Keys and the Upper–Middle Keys).
                                       Previous studies oVer some bases for the intra and inter-
The separation of reefs into two main RSI based on water           regional variations in water quality in the Florida Keys. The
quality measurements corresponded with their geological           lower physical component scores (i.e., temperature) in the
locations in the Florida Keys (Upper-Middle Keys and             Upper–Middle Keys reefs maybe a reXection of the cold

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848                                                Mar Biol (2008) 154:841–853


freshwater Xowing from Florida Bay through the island      Third, diVerential recruitment of corals between regions
passages in the Middle Keys (Smith and Lee 2003; Keller     could help explain the prevailing regional variation in coral
and Donahue 2006) and to some extent from Biscayne Bay      community structure in the Florida Keys (Hughes and Tan-
(Jones and Boyer 2002). Water quality measurements in      ner 2000). It is well known that the recruitment of corals is
reefs within the Upper–Middle Keys were similar, perhaps     aVected by several factors, including larval supply, substra-
because of the mixing of water masses in these areas       tum availability, disturbance and regional oceanography
through wind-forced currents and gravity-driven transport    (Chiappone and Sullivan 1996). Recently, Moulding (2005)
produced by cross-Key sea level diVerences (Smith and Lee    demonstrated that the density and diversity of recruits var-
2003). The strength of these water exchanges exhibit sea-    ies between regions, being signiWcantly lower in the Upper
sonal variations in response to prevailing winds and other    Keys than in the Lower Keys. Finally, it is possible that the
oceanographic factors, for example, the Loop current (Kel-    Upper Keys is exposed to severe environmental stresses
ler and Donahue 2006). The higher salinity and algal bloom    and selective pressures due to the fact that this region
component scores (i.e., for chl a, TP and turbidity) in the   is closer to the northern limit of the Florida reef tract
Lower Keys relative to the rest of the FKNMS could be      (Moulding 2005).
attributed to the onshore movement of high-saline and        Coral reef degradation in the Florida Keys was charac-
nutrient-rich deep water into this region (Leichter et al.    terized by marked reduction in coral cover, and subsequent
2003) brought about by cyclonic gyres spun oV of the Flor-    proliferation of macroalgae from 1996 to 2000. In the Flor-
ida Current (Szmant and Forrester 1996; Jones and Boyer     ida Keys, the concurrent dominance of macroalgae relative
2002). Higher nutrient concentration in the Lower Keys      to hard corals over time were documented previously by
could also have an anthropogenic origin, considering that    several authors, including Dustan (1977), Dustan and Halas
the density of human population in the Lower Keys is       (1987), Porter and Meier (1992), Murdoch and Aronson
higher than the rest of the Florida Keys (Ward-Paige et al.   (1999), and Porter et al. (2002) (Table 3). Such dramatic
2005). Alternatively, the lower nutrient concentration in the  changes in coral reef community structure are widely
Upper–Middle Keys relative to the Lower Keys could be      reported in the Caribbean region (Done 1992; Hughes
attributed to the much higher likelihood of mixing between    1994; McClanahan and Muthiga 1998; Gardner et al. 2003,
waters in these regions and the relatively clean Atlantic    2005). This phenomenon is often considered an indicator of
Ocean waters (Boyer and Jones 2002).               a coral reef community that is undergoing a phase-shift
  The separation of reefs in the Lower Keys from the      (McCook 1999; McManus and Polsenberg 2004; Rogers
Upper–Middle Keys in CCA corroborates the clustering of     and Miller 2006). In the Florida Keys, the phase-shift from
reefs based on RSI, further illustrating the strong inXuence   coral-dominated to macroalgal-dominated reef communi-
of the predictor variables (macroalgae, sponge, chl a, TN    ties may be attributed to the diminished resilience of corals
and salinity) in the structuring of reef communities at a    against perturbations (Jackson 2001; Aronson and Precht
spatial scale larger than the individual reef. This pattern is  2006), hypothesized to be caused by top-down mechanisms
consistent with the Wndings of Ogden et al. (1994) and      such as herbivore reduction (Hughes 1994; Jackson et al.
Murdoch and Aronson (1999) who attributed the inter-reef     2001) and bottom-up processes such as nutrient enrichment
variations in coral community structure in the Florida Keys   (Lapointe 1999; Leichter et al. 2003) (Fig. 7 for a diagram-
to the region-wide diVerences in environmental characteris-   matic presentation of how we perceive these interacting
tics. The inXuence of environmental gradients in the struc-   factors that result in a phase-shift).
turing of reef communities in the Florida Keys may be        More recent evidence elucidates the potential mecha-
explained by several possible mechanisms. First, anteced-    nisms underlying macroalgal-coral interactions that may
ent topography determine the suitability of present sub-     lead to a localized phase-shift in the Florida Keys. Miller
strate for coral settlement and development. For example,    and Hay (1998) demonstrated that Dictyota spp. and Hali-
Ginsburg and Shinn (1994) reported that the predominance     meda opuntia, the two most abundant macroalgal species in
of mobile sand substrates in the Middle Keys and seaward     the Florida Keys, inhibited the growth of Porites porites.
of Biscayne Bay may render these areas unsuitable for coral   Jompa and McCook (2003a, b) have also shown that some
recruitment, thereby causing reefs in these areas to become   algae (Anotrichium tenue, Corallophila huysmansii) can
impoverished. Second, Florida Bay waters that pass        directly cause coral tissue death. Furthermore, KuVner et al.
through the Middle Keys may potentially inhibit coral      (2006) have provided empirical evidence that macroalgae
growth, survival and recruitment into this region and adja-   (e.g., Dictyota) can directly inhibit the settlement of coral
cent reefs by introducing pulses of waters with extremely    recruits (e.g., Porites astreoides). The decline in coral
variable temperature and salinity as well as with high nutri-  diversity and cover has also been associated with an
ent and sediment loads (Ginsburg and Shinn 1994; Chiap-     increase in coral disease prevalence (Porter et al. 2001).
pone and Sullivan 1994; Szmant and Forrester 1996).       Increased physical contact between corals and macroalgae

123
   Table 3 Studies in the Caribbean region (Western Atlantic, including Florida and the Bahamas) documenting changes in benthic community structure in the region
   Sites              Period               Mean % cover                            Proposed direct and indirect agents of change   Source

                                     Coral       Macroalgae            Sponge

                                     Initial  After  Initial  After          Initial After

   Caribbean region        1970 s–2000 s           50    10   Increasing            Increasing   White band disease; hurricanes;          Gardner et al. (2003) and
                                                                       indirectly attributed to increased         López-Victoria
                                                                                                               Mar Biol (2008) 154:841–853




                                                                       abundance of macroalgae following          and Zea (2005)
                                                                       mass mortality of the herbivorous
                                                                       D. antillarum(DA) in 1983
   Florida Keys          1996–2000              8.1    4.6  5.7     9.6 (16.5 in 1998)  2.2   2.2  Disease; bleaching; anomalous extreme       This study; also see
                                                                        salinity and temperature events; eutrophication  Porter et al. (2002)
                                                                        and sedimentation; low herbivory due to
                                                                        overWshing and mass mortality of DA;
                                                                        high cover of macroalgae and probably sponges
   Florida Keys (Carysfort Reef)  1975–1982                                               Boat grounding and anchor damage; hurricanes;   Dustan and Halas (1987)
                   Mean percent cover (all species)  31.6   32.2                            sedimentation; coral diseases; eutrophication

                   Acropora palmata          63    33
                    (mean colony size in cm)
                   Agaricia agaricites cm       4     6
                    (mean colony size in cm)
   Florida Keys         1984–1991              28.4    6.6                           Disease; bleaching                 Porter and Meier (1992)
     (Carysfort and Looe Reefs)                                                                                and Connell (1997)
   Gulf of Mexico         1980–1990             55.2    8.7                           Disease; bleaching                 Connell (1997)
    (Flower Gardens Reef)
   St. John, US Virgin Islands   1988–2003             43.4   12.3  Reported macroalgae competing           Hurricane; high sea surface temperature (SST);   Edmunds and Elahi (2007)
     (Yawzi Point)                                    with corals for space               coral disease; macroalgae
   St John, US Virgin Islands   1999–2000 (coral) Before- after  18    14   7.3    33.5                  Hurricane; diseases; low herbivory due       Rogers and Miller (2006)
                    Hurricane Hugo                                             to overWshing and DA mass mortality;
                    in 1989 (macroalgae)                                          failure of settlement
   Panama (Punta de San Blas)   1983–1990             43–45 12–26 <2       10–32                  Bleaching; DA mass mortality; sedimentation    Shulman and
                                                                        and eutrophication                 Robertson (1996)
   Jamaica             1977–1980 vs. 1990–1993      52     3   4     92                   OverWshing of herbvivores; hurricane;       Hughes (1994)
                                                                        disease; DA mass mortality
   Jamaica (Dairy Bull)      1995–2004             <1    11   90    45–6                  Long-lived colonies of Montastraea annularis    Idjadi et al. (2006)
                                                                        provided structural refugia
   Belize (Glovers Reef lagoon)  1970–71 vs. 1996–1997       80    20   20    80                   Diseases; low herbivory due to overWshing     McClanahan and
                                                                        and DA mass mortality               Muthiga (1998)
   Belize (Channel Cay)      1997–2001             »43    »0   <10 (no change)          »15   43   Bleaching due to high SST             Aronson et al. (2000, 2002)
                    (mainly Agaricia tenuifolia)
   Costa Rica (Cahuita)      1980–1993             40.4   29.2                           Natural disturbances; human impacts        Connell (1997)

   A majority of these studies indicate a decrease in coral cover (or a change in species composition), followed by subsequent increase in macroalgal and sponge cover over time
   This list in not meant to be exhaustive. For worldwide summary of the impacts of diVerent array of disturbances, see Connell (1997) and Goreau et al. (2000)




123
                                                                                                               849
850                                                          Mar Biol (2008) 154:841–853




Fig. 7 Diagram showing an array of factors that potentially contrib-      human disturbances. Regional-global factors include f increase sever-
uted to the phase-shift in Florida Keys coral reefs from coral-domi-      ity and incidence of marine diseases, which is partly attributed to the
nated to algal/sponge-dominated community. Only dominant            mass mortality of g Diadema antillarum in 1983–1984 and regional-
pathways are presented in the diagram. Solid and dashed lines indicate     wide coral bleaching events; h global climate change, which has been
negative and positive interactions, respectively, and the arrowhead of     associated with increased severity and frequency of anomalous high
the line indicates the trajectory of the interaction. Inside the dashed cir-  SST causing regional-wide bleaching events; and i and historical and
cle are the dominant benthic organisms (corals, macroalgae and spong-     natural disturbances such as hurricanes. Symbols courtesy of the Inte-
es). Inside the dashed square are array of local factors that potentially   gration and Application Network (ian.umces.edu/symbols/), Univer-
contributed to the phase-shift in the Florida Keys coral reefs: a Wshing    sity of Maryland Center for Environmental Science, USA. For a
indirectly impact corals through anchor damage and extraction of b       comprehensive review of phase-shift in coral reefs, see Done (1992);
herbivores and c spongivores Wshes; d extreme seasonal changes of       McCook (1999); McManus et al. (2000); McManus and Polsenberg
temperature and salinity; and e eutrophication, sedimentation and other    (2004); and Aronson et al. (2006)


due to macroalgal bloom has been hypothesized to provoke            in sponge cover from 1996 to 2000; this agrees with earlier
coral diseases (Green and Bruckner 2000). This observation           reports of Aronson et al. (2002) and López-Victoria and
was empirically supported by the Wndings of Nugues et al.           Zea (2005) in the Caribbean region. Cliona delitrix,
(2004) that the increasing physical contact between Hali-           C. lampa, and C. caribboea, known to be aggressive
meda opuntia triggered a virulent disease known as white            bioeroders, were among the dominant species of sponges in
plague type II in Montastraea faveolata. The combination            the Florida Keys (Keller and Donahue 2006). Ward-Paige
of these mechanisms may have contributed to the negative            et al. (2005) reported that the Lower Keys had the highest
relationship between coral and macroalgal cover in the             sponge abundance and size, and they attributed this to
Florida Keys over the 5-year study period, as demonstrated           sewage contamination based on higher 15 N levels in the
by the CCA.                                  sponge tissues. Reduction in abundance of spongivorous
  Sponge cover was also negatively correlated with hard            Wshes as postulated by Hill (1998) could also play a role in
coral cover in the Florida Keys. There was a subtle increase          the increase of sponge cover in the Florida Keys. Spongivory

123
Mar Biol (2008) 154:841–853                                                     851


was previously demonstrated by Pawlik (1998) to be an       factors (e.g., source of propagules), frequency of occurrence
important agent in controlling the population of at least     of physical disturbance, and historical processes may inXu-
some sponges. Sponge proliferation could aVect corals       ence the community structure of corals in the Florida Keys.
through several mechanisms: allelopathy (Engel and        Future investigations that focus on mechanistic processes
Pawlik 2005; Pawlik et al. 2007), physical smothering and     need to address whether these factors act alone or interac-
cellular digestion (Hill 1998) as well as direct space      tively, either through mitigative or exacerbative pathways.
competition (Lopez-Victoria et al. 2006). These mecha-
nisms would lead to increased bioerosion, resulting in a net   Acknowledgments R. J. Maliao is supported by the Fulbright-
                                 Philippines Agriculture Scholarship Program. We thank the FKNMS
loss of carbonate, thus compromising the integrity of the
                                 management through its coordinator, Fred McManus, for allowing us
coral skeletal structure. However, the positive and negative   to use their monitoring database. Edward Webb, Kathe Jensen, J. R.
relationships between hard coral and sponge in the Wrst and    Kerfoot, Matt Wittenrich, Zan Didoha, Vutheary Hean, Justin Anto,
second CCA axis, respectively, indicate that sponge-coral     and Bernice Polohan provided valuable comments on an earlier version
                                 of this manuscript. We particularly appreciate the advice of Bruce
relationships are species-speciWc. This pattern is consistent   McCune on the use of CCA. The valuable comments and recommen-
with the Wndings of Aerts (1998) who reported that the out-    dations of three anonymous reviewers greatly improved this manu-
come of coral-sponge interactions depends on the species     script.
of both corals and sponges and the frequency of previous
encounters between coral and aggressive sponge species.
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