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bruno et al 2009
Ecology, 90(6), 2009, pp. 1478–1484
Ó 2009 by the Ecological Society of America
Assessing evidence of phase shifts from coral
to macroalgal dominance on coral reefs
JOHN F. BRUNO,1,5 HUGH SWEATMAN,2 WILLIAM F. PRECHT,3 ELIZABETH R. SELIG,4 AND VIRGINIA G. W. SCHUTTE1
1
Department of Marine Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3300 USA
2
Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland 4810 Australia
3
National Oceanic and Atmospheric Administration, Florida Keys National Marine Sanctuary, 95230 Overseas Highway,
Key Largo, Florida 33037 USA
4
Curriculum in Ecology and Department of Marine Sciences, The University of North Carolina at Chapel Hill,
Chapel Hill, North Carolina 27599-3300 USA
Abstract. Many marine scientists have concluded that coral reefs are moving toward or
are locked into a seaweed-dominated state. However, because there have been no regional- or
global-scale analyses of such coral reef ‘‘phase shifts,’’ the magnitude of this phenomenon was
unknown. We analyzed 3581 quantitative surveys of 1851 reefs performed between 1996 and
2006 to determine the frequency, geographical extent, and degree of macroalgal dominance of
coral reefs and of coral to macroalgal phase shifts around the world. Our results indicate that
the replacement of corals by macroalgae as the dominant benthic functional group is less
common and less geographically extensive than assumed. Although we found evidence of
moderate local increases in macroalgal cover, particularly in the Caribbean, only 4% of reefs
were dominated by macroalgae (i.e., .50% cover). Across the Indo-Pacific, where regional
averages of macroalgal cover were 9–12%, macroalgae only dominated 1% of the surveyed
Reports
reefs. Between 1996 and 2006, phase shift severity decreased in the Caribbean, did not change
in the Florida Keys and Indo-Pacific, and increased slightly on the Great Barrier Reef due to
moderate coral loss. Coral reef ecosystems appear to be more resistant to macroalgal blooms
than assumed, which has important implications for reef management.
Key words: Caribbean; coral reefs; Florida Keys; Great Barrier Reef; Indo-Pacific; macroalgae; phase
shifts; reef management.
INTRODUCTION Knowlton 1992, McManus and Polsenberg 2004; Fig. 1).
Natural and anthropogenic disturbances can cause A widely cited and striking example occurred on nine
the replacement of one group of dominant organisms by reefs in Jamaica during the 1980s (Hughes 1994). In the
another (Petraitis and Dudgeon 2004). Such ecosystem- 1970s, and presumably historically (but see Woodley
level transformations of natural communities can affect 1992), coral cover on Jamaican reefs ranged from 40% to
flows of energy and materials, the abundance and diver- 70% and macroalgal cover was typically ,10% (Hughes
sity of community inhabitants and valuable services for 1994). Following several disturbances including a major
human societies (Sousa 1984, Pickett and White 1985). hurricane (Woodley et al. 1981), coral predator and coral
A topical example is the ‘‘phase shift’’ of coral reefs from disease outbreaks (Knowlton et al. 1990), the regional
coral to macroalgal dominance (McManus and Polsen- loss of the keystone grazer Diadema antillarum in 1983–
berg 2004; Fig. 1). 1984 to a Caribbean-wide epizootic (Hughes et al. 1985),
Coral abundance on reefs around the world began to a second major hurricane (Woodley 1992), and a series of
decline several decades ago (Gardner et al. 2003, Bruno coral bleaching events in the late 1980s (Goreau 1992),
and Selig 2007) due to a variety of factors including coral cover on these reefs plummeted to ,10% and
predator and disease outbreaks, poor land use practices, macroalgae became the dominant benthic functional
destructive fishing techniques, and ocean warming group (Liddell and Ohlhorst 1992, Hughes 1994).
(Glynn 1993, McManus et al. 1997, Aronson and Precht The Jamaican case study is assumed to be illustrative
2001, Hughes et al. 2003). In some locations, the cover of a widespread and ongoing phenomenon (Szmant
and biomass of benthic macroalgae increased concur- 2001, Bellwood et al. 2004, McManus and Polsenberg
rently with coral loss, resulting in community phase 2004, Precht and Aronson 2006). While there are several
shifts to reefs dominated by macroalgae (Done 1992, case reports of decreased coral cover and increased
macroalgal cover on other individual reefs (Endean and
Stablum 1973, Smith et al. 1981, Done 1992, Rogers and
Manuscript received 25 September 2008; revised 19 January
Miller 2006), there have been no regional- or global-
2009; accepted 20 January 2009. Corresponding Editor: R. B.
Aronson. scale analyses of coral reef phase shifts. Therefore, the
5
E-mail: jbruno@unc.edu ecological generality of these observations and the
1478
June 2009 CORAL REEF PHASE SHIFTS 1479
applicability of the Jamaican archetype to reefs around 2005). Most surveys used in our meta-analysis em-
the world (Bellwood et al. 2004) are unknown. ployed the line-transect technique, in which a transect
Epidemiologists perform randomized population (typically a 10–30 m measuring tape or chain) was
sampling to determine the generality of case reports placed on the reef. The coverage of coral and macro-
in the medical literature (Rothman and Greenland algae was then estimated either in situ by recording the
1998). Likewise, ecologists can apply various macro- number of points along each transect that overlaid
ecological and meta-analytical techniques to under- corals, macroalgae, and so forth, or by taking images of
stand the spatial dynamics, severity and impacts of the reef substrate at these points, which were then
major disturbances, community phase shifts, and other analyzed in the laboratory. We only used surveys that
ecological phenomena (Brown 1999). Such basic differentiated macroalgae from other algal groups.
pattern quantification over large spatial scales can put Following Steneck (1988) and others, we defined
more detailed, local studies into a broader context macroalgae (i.e., seaweed) as ‘‘larger (canopy heights
o ´
(Cˆ te et al. 2005). The purpose of this study was to usually .10 mm), more rigid and anatomically complex
assess the frequency, geographical extent, and degree of algal forms.’’ This functional group includes erect
macroalgal dominance of coral reef communities and of calcifying species (e.g., Halimeda spp.) but does not
coral to macroalgal phase shifts around the world. include microalgae and filamentous algae (i.e., turfs) or
Specifically, we used data from quantitative reef crustose algae (Steneck 1988).
surveys to determine the proportion of reefs in four Coral reef degradation and phase shifts are complex,
geographic regions (Greater Caribbean, Florida Keys, multivariate phenomena (Sebens 1994, Graham et al.
Indo-Pacific, and Great Barrier Reef [GBR]; see 2006) and can involve various combinations of coral loss
Appendix A: Fig. A1) that were dominated by macro- and seaweed gain. To address this issue and to facilitate
algae (.50% absolute macroalgae cover). We deter- graphical and statistical comparisons among regions and
mined the state of each reef along a continuum ranging years, we developed a coral reef phase shift index (PSI),
from coral to macroalgal dominance by developing a a quantitative, one-dimensional measure of the degree to
Reports
‘‘phase shift index’’ based on principal components which a reef has changed from a pristine (high coral, low
analysis of the two benthic categories (coral and macroalgal cover) state to a low coral, high macroalgal
macroalgal cover) included in the meta-analysis. We cover state. PSI is the first component (PCA1) from a
also asked whether phase shift severity changed principal components analysis (eigenvalue, 1.25; vari-
between 1996 and 2006. ance explained, 62%) on the correlation matrix between
macroalgal cover and the inverse of coral cover. The
METHODS analysis essentially combines the two variables (coral
Hughes’ classic study (Hughes 1994) of the degrada- and macroalgal cover) into a single value, which
tion of Jamaican reefs demonstrates the power of simplifies analysis and discussion of what would
repeated surveys of particular sites in detecting phase otherwise be a bivariate phenomenon by reducing the
shifts across broad spatial scales. Unfortunately, very dimensionality of the data set. PSI values were derived
few such longitudinal studies were implemented until the from single site–year combinations and are measures of
early 1990s, years to decades (or longer) after reefs began current reef state at the time of the survey, i.e., they are
to be altered by human activities (Pandolfi et al. 2003). not a measure of the degree to which a particular reef
Therefore, localized monitoring studies alone cannot be has changed over time. By pooling large numbers of
used to quantify the regional-to-global generality and single site-year PSI values, we were able to describe
severity of coral reef phase shifts. As an alternative ap- population-level variation in PSI among years and
proach, we used the extensive data from more recent reef regions. In this analysis, pristine reefs have a PSI of
surveys to make inferences about regional patterns (e.g., À2 to À3 and reefs with low coral and high macroalgal
magnitude and spatial extent) of shifts in coral reef cover have a PSI of 2 to 3 (Fig. 1). The PSI on reefs that
benthic communities. We assumed that most reefs were have undergone a severe phase shift was 3 to 5 (Fig. 1).
historically coral dominated and that macroalgae were The principal components analysis was performed on
relatively scarce. Therefore, the current state (in terms of the most recent survey performed on each reef (i.e., we
coral and macroalgal cover) of reefs across a region can did not include multiple surveys of individual reefs
be used as a measure of regional-scale degradation or through time) and included cover values from Hughes’
phase shift degree. 1994 study of Jamaican reefs in the 1970s and early
Our database included 3581 quantitative surveys of 1990s (Fig. 2).
1851 coral reefs (or sites) performed between 1996 and To determine whether the degree to which reefs are
2006 (see Appendix A). Our analysis was based on dominated by macroalgae has changed over time (i.e.,
quantitative surveys that measured the percentage of to test the null hypothesis that PSI did not change
the substratum covered by living coral and fleshy or between 1996 and 2006), we performed two types of
calcareous macroalgae between 1 and 15 m depth (mean regression analysis. For one analysis we used the entire
depth; 7.1 m). The abundance of macroalgae is con- data set to calculate annual regional mean PSI values
sidered a key metric of reef health (Steneck and Sala and for the other we only used data from monitoring
1480 JOHN F. BRUNO ET AL. Ecology, Vol. 90, No. 6
FIG. 1. The coral reef ‘‘phase shift’’ concept. (A) Images are from neighboring reefs near Discovery Bay Jamaica, in January
2003 (photos by J. Bruno). (B) Examples of different degrees of coral reef degradation around the world, based on the phase shift
index used in this analysis.
studies. Data from each of the four regions were temporal changes in PSI could be due solely to changes
analyzed separately. Time (year) and PSI were treated in the population of reefs that were surveyed each year.
as continuous variables and data were transformed For the second temporal analysis, we used only the
when necessary to meet basic statistical assumptions. subset of 458 reefs that were surveyed in two or more
Reports
The first analysis was a simple linear regression be- years. These data were analyzed with linear repeated
tween year and the annual mean PSI (i.e., the replicate measures regression analysis (using Stata version 9.1,
PSI measures within each region for each year were Stata Corporation, College Station, Texas, USA). This
pooled into a single value). A strength of this analysis, test accounted for the longitudinal structure of the
in contrast to one based on monitoring studies, is that survey data, particularly for the GBR, which was
the sampled reefs were more or less randomly selected, largely based on monitoring data from the Australian
which allows for greater generalization. However, a Institute of Marine Science’s Long Term Monitoring
significant weakness of this approach is that observed Program.
FIG. 2. State of the world’s coral reefs. The top row shows absolute living coral and macroalgal cover. The bottom row shows
count histograms of the phase shift index (PSI) in the four regions; the y-axis shows the lower and upper ranges of PSI in each bin.
Data in panel A are from Hughes (1994). Data in panels B–E are based on the most recent survey from each site.
June 2009 CORAL REEF PHASE SHIFTS 1481
TABLE 1. Reef state in the four study regions.
Number Coral Macroalgal Macroalgae Macroalgae
Region of sites Years cover (%) cover (%) . 25% . 50%
Caribbean 530 1996–2006 20.0 6 0.5 23.6 6 0.8 39% 10%
Florida Keys 160 1996–2005 8.1 6 0.7 14.7 6 1.3 23% 4%
Indo-Pacific 963 1996–2006 33.2 6 0.6 11.7 6 0.4 13% 1%
Great Barrier Reef 198 1996–2006 30.5 6 1.2 9.1 6 0.8 10% 1%
Notes: All summary statistics were based on the most recent survey performed at each site. Values for coral and macroalgal cover
are means 6 SE.
Percentage of surveyed reefs.
RESULTS AND DISCUSSION chetype was a PSI . 3, which in our analysis
Presently, there are no defined or generally accepted corresponded to less than 10% coral cover and macro-
thresholds of the degree of coral loss and macroalgal algal cover .60 % (Figs. 1 and 2). Based on this
increase that constitutes a phase shift (Rogers and Miller threshold, only 25 of the 1851 reefs (,1%) could be
classified as having undergone a complete coral to algal
2006). This has led to substantial confusion about the
phase shift (Fig. 2B–E) and all except one of these reefs
causes, generality, severity, and management implica-
were in the Caribbean. Phase shift severity is a
tions of phase shifts on reefs. Many authors appear
continuum, so categorical delineations of relative
implicitly to define coral reef phase shifts as cases where
severity are subjective and may be not be ecologically
macroalgae dominate the reef benthos (Hughes et al.
relevant. Nevertheless, our results indicate that the
2003, McManus and Polsenberg 2004, Knowlton 2008).
severity of phase shifts on a majority of the world’s
Unfortunately, what is meant by ‘‘dominate’’ is rarely
reefs (Figs. 2 and B1) appear to be substantially less
articulated. The use of ‘‘dominance’’ and similar terms
severe than those seen in a few well-known examples.
Reports
such as ‘‘preponderance’’ and ‘‘seaweed reef’’ implies a
Overall, our results indicate that there is no general
threshold of 50% macroalgal cover. Based on this
recent trend (i.e., post-1995) toward macroalgal domi-
definition, only 4% of the 1851 reefs used in our primary
nance (see Appendix C). PSI did not change during 1996
analyses were dominated by macroalgae. Across the
to 2006 in the Florida Keys or Indo-Pacific (Fig. C1,
Indo-Pacific (including the GBR) macroalgae only
Table C1). Many of the changes in these regions and in
dominated 1% of the surveyed reefs (Tables 1 and B1). the Caribbean presumably took place before broad-scale
Species or functional groups do not necessarily need surveying began. Based on one of our two temporal
to occupy or control a majority (.50%) of a limiting analyses, PSI marginally increased (P ¼ 0.07) on the
resource to ‘‘dominate’’ or define a community, but even GBR between 1996 and 2006, presumably due to a 3–4%
based on a much lower threshold of 25%, only 20% of decline in coral cover (there was no concurrent change in
surveyed reefs were seaweed dominated (Tables 1 and macroalgae) caused primarily by outbreaks of the
B1). Furthermore, more than half (53%) of these were in corallivorous seastar Acanthaster planci (Miller 2002).
the Caribbean, which includes only ;8% of the world’s In contrast, PSI decreased slightly in the Caribbean (Fig.
reefs (Spalding and Grenfell 1997). This result confirms C1, Table C1) due to a modest decrease in macroalgal
the common belief that phase shifts have been more cover from 34.0% 6 2.9% to 21.4% 6 1.3% (values are
severe in the Caribbean than elsewhere (Pandolfi et al. mean 6 1 SE) and even smaller increases in coral cover
2003, Bellwood et al. 2004). However, among-region from 19.9% 6 1.5% to 21.8% 6 0.7%, through 2005.
comparisons should be made with caution because reef Our results indicate there was a small increase in PSI
geomorphology, the types of reef habitats that are and a ;5% decrease in mean regional coral cover
surveyed, and possibly even reef community baselines all between 2005 and 2006 (from ;22% to 17%), possibly
vary among our study regions. Surprisingly, our results caused by the mass coral bleaching and mortality event
indicate that few of the world’s reefs fall into either of in late 2005 in the northern and eastern Caribbean
the classically defined coral reef stable points of coral or (Donner et al. 2007).
macroalgal dominance (Petraitis and Dudgeon 2004). A
large majority, including those in the Caribbean, are Coral reef baselines and recent changes
somewhere between these extremes; a pattern not in macroalgal abundance
concordant with the belief (Knowlton 1992, Bellwood Macroalgae play an important ecological role on
et al. 2004) that coral reef communities switch between shallow reefs (Vroom et al. 2006). Tropical macroalgae
coral and macroalgal dominated stable states. are highly diverse and countless species have evolved
We quantified phase shift severity using a phase shift adaptations to consume and utilize them (e.g., fishes
index (PSI) that combined the coral and macroalgal whose camouflage mimics macroalgae). But what was
coverage of a reef into a single variable using principal the historical baseline of macroalgal cover and how
components analysis (Figs. 2 and B1). A rough thresh- much has macroalgae increased? Nearly all surveys of
old for a severe phase shift based on the Jamaican ar- Caribbean reefs during the 1970s and early 1980s
1482 JOHN F. BRUNO ET AL. Ecology, Vol. 90, No. 6
reported absolute macroalgal cover values between 0% R 2 ¼ 0.09; Florida Keys P ¼ 0.008, R 2 ¼ 0.04; Indo-
and 10%. The mean of 19 surveys of 16 sites performed Pacific P ¼ 0.02, R 2 ¼ 0.01; Great Barrier Reef P ¼ 0.28).
between 1977 and 1982 is 6.6% (see Appendix D; Table Surprisingly, macroalgal cover has not increased appre-
D1). However, one survey reported macroalgal cover as ciably on most of the world’s reefs that have very low
high as 20.5% (Liddell and Ohlhorst 1992), and only a coral cover. For example, 379 of the 1851 reefs had
small number of locations were surveyed (primarily in 10% coral cover, but macroalgal cover was also low
St. Croix, U.S. Virgin Islands and along the north coast ( 20%) on nearly two thirds of these reefs. In fact, more
of Jamaica). Additionally, there is speculation that than half the benthic cover on reefs in the Caribbean,
macroalgal cover was unnaturally low during this period Pacific and Indian Oceans consists of organisms other
due to anomalously high densities of the urchin Diadema than hard corals and macroalgae, possibly because other
antillarum caused by the overfishing of its predators taxa, such as sponges and gorgonians, have been the
(Hay 1984, Levitan 1992). primary beneficiaries of coral loss (Aronson et al. 2002,
If the regional baseline was indeed roughly 3–10%, Norstrom et al. 2009). The degree of macroalgal dom-
¨
averaging ;6%, then macroalgal cover in the Caribbean inance is widely considered a key measure of reef health.
has increased fourfold. Although this increase may be For instance, Steneck and Sala (2005) argued that
ecologically significant, it is much smaller than generally ‘‘macroalgal abundance is the single best indicator of
assumed. Additionally, most evidence of negative effects poor conditions for coral reefs.’’ However, since the
of macroalgae on the growth and survival of juvenile cover of coral and macroalgae are only weakly related,
corals comes from studies in which macroalgal cover macroalgal abundance may not be a good indicator of
was far higher, typically 50 –70% (Carpenter and either coral loss or habitat quality.
Edmunds 2006, Hughes et al. 2007). However, one The absence of evidence for expected widespread
recent study found that macroalgal cover as low as 20 – increases in macroalgae could be due to the limited
30% was negatively correlated with coral recruit density extent of nutrient pollution on most reefs (Szmant 2002,
(Mumby et al. 2007). Greenaway and Gordon-Smith 2006), especially isolated
Reports
Another approach to estimating reef baselines of the offshore reef systems. Herbivores can clearly regulate
past is to study modern ‘‘quasi-pristine’’ reefs that are reef macroalgae (Lewis 1986, Steneck 1988, Williams
substantially less affected by human activities, due and Polunin 2001, Carpenter and Edmunds 2006) and
mainly to their isolation but also to legal protections overfishing has reduced the densities of herbivorous
(Knowlton and Jackson 2008). Two recent expeditions fishes on many reefs (Pandolfi et al. 2003, Bellwood et al.
(Vroom et al. 2006, Sandin et al. 2008) surveyed 10 such 2004). But compensatory increases in the abundance of
remote reefs in the central Pacific in part to establish a other herbivores may have partially filled this function
regional baseline. They found that macroalgal cover (Aronson and Precht 2000). One explanation for the low
averaged 13.1% 6 2.0% (mean 6 1 SE) and ranged from macroalgal cover in the Florida Keys and Great Barrier
3% to 28% (Table D2). With minimal or no fishing, Reef is that local management has been effective in
these reefs have intact food webs with plentiful top preventing herbivore populations from being depleted
predators (Vroom et al. 2006, Sandin et al. 2008) and are (Aronson and Precht 2006). Another is that commercial
probably our best window into the past (Knowlton and and recreational fishers in these relatively affluent parts
Jackson 2008). If so, macroalgae were substantially of the world target piscivores. Thus, herbivorous fish are
more abundant than we think, at least on some reefs and both released from predator control and largely
in some regions (Vroom et al. 2006). Macroalgal cover unaffected by direct fishing pressure (Graham et al.
on these ‘‘pristine’’ reefs is similar to the regional 2003). Additionally, the recovery of populations of the
averages for three of our four study regions, suggesting keystone grazer Diadema antillarum on some Caribbean
that macroalgal cover may currently be close to the reefs has reduced seaweed cover close to recent historical
historical baseline across most the world. levels at shallow sites and has also increased coral
recruitment (Carpenter and Edmunds 2006).
Macroalgal blooms, coral decline, and reef management
Macroalgal blooms on coral reefs are generally un- Conclusions
derstood to be caused by reduced herbivory (resulting The mismatch between descriptions of reef degrada-
from fishing and also from urchin die-offs in the tion in the literature and patterns in nature was caused
Caribbean) and coral loss, which allows macroalgae to by the generalization of a relatively small number of
colonize open substrate, thereby increasing primary examples. Case reports of local phase shifts were not
production and overwhelming grazers (Knowlton 1992, intended to be representations of the state and dynamics
Hughes et al. 1999, Williams et al. 2001). Thus, macro- of reefs in general. They were instead published as
algal cover and coral cover are widely assumed to be notable quantitative observations. Although in retro-
causally linked and inversely related. Yet we found only spect atypical, case studies such as the degradation of
weak negative relationships between coral and macro- Jamaican reefs have been invaluable warnings of the
algal cover (linear regression analyses based on the most consequences of subjecting reef communities to multiple
recent survey of each site; Greater Caribbean P ¼ 0.0001, natural and anthropogenic disturbances.
June 2009 CORAL REEF PHASE SHIFTS 1483
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APPENDIX A
A description of procedures and sources of data used in the meta-analysis (Ecological Archives E090-100-A1).
APPENDIX B
Basic analyses performed without data from Reef Check (Ecological Archives E090-100-A2).
APPENDIX C
Analyses of the relationship between time and phase shift index (PSI) values between 1996 and 2006 (Ecological Archives E090-
100-A3).
APPENDIX D
Reported macroalgal cover from early Caribbean reef surveys (1976–1982) and on remote Pacific reefs (Ecological Archives
E090-100-A4).
Ó 2009 by the Ecological Society of America
Assessing evidence of phase shifts from coral
to macroalgal dominance on coral reefs
JOHN F. BRUNO,1,5 HUGH SWEATMAN,2 WILLIAM F. PRECHT,3 ELIZABETH R. SELIG,4 AND VIRGINIA G. W. SCHUTTE1
1
Department of Marine Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3300 USA
2
Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland 4810 Australia
3
National Oceanic and Atmospheric Administration, Florida Keys National Marine Sanctuary, 95230 Overseas Highway,
Key Largo, Florida 33037 USA
4
Curriculum in Ecology and Department of Marine Sciences, The University of North Carolina at Chapel Hill,
Chapel Hill, North Carolina 27599-3300 USA
Abstract. Many marine scientists have concluded that coral reefs are moving toward or
are locked into a seaweed-dominated state. However, because there have been no regional- or
global-scale analyses of such coral reef ‘‘phase shifts,’’ the magnitude of this phenomenon was
unknown. We analyzed 3581 quantitative surveys of 1851 reefs performed between 1996 and
2006 to determine the frequency, geographical extent, and degree of macroalgal dominance of
coral reefs and of coral to macroalgal phase shifts around the world. Our results indicate that
the replacement of corals by macroalgae as the dominant benthic functional group is less
common and less geographically extensive than assumed. Although we found evidence of
moderate local increases in macroalgal cover, particularly in the Caribbean, only 4% of reefs
were dominated by macroalgae (i.e., .50% cover). Across the Indo-Pacific, where regional
averages of macroalgal cover were 9–12%, macroalgae only dominated 1% of the surveyed
Reports
reefs. Between 1996 and 2006, phase shift severity decreased in the Caribbean, did not change
in the Florida Keys and Indo-Pacific, and increased slightly on the Great Barrier Reef due to
moderate coral loss. Coral reef ecosystems appear to be more resistant to macroalgal blooms
than assumed, which has important implications for reef management.
Key words: Caribbean; coral reefs; Florida Keys; Great Barrier Reef; Indo-Pacific; macroalgae; phase
shifts; reef management.
INTRODUCTION Knowlton 1992, McManus and Polsenberg 2004; Fig. 1).
Natural and anthropogenic disturbances can cause A widely cited and striking example occurred on nine
the replacement of one group of dominant organisms by reefs in Jamaica during the 1980s (Hughes 1994). In the
another (Petraitis and Dudgeon 2004). Such ecosystem- 1970s, and presumably historically (but see Woodley
level transformations of natural communities can affect 1992), coral cover on Jamaican reefs ranged from 40% to
flows of energy and materials, the abundance and diver- 70% and macroalgal cover was typically ,10% (Hughes
sity of community inhabitants and valuable services for 1994). Following several disturbances including a major
human societies (Sousa 1984, Pickett and White 1985). hurricane (Woodley et al. 1981), coral predator and coral
A topical example is the ‘‘phase shift’’ of coral reefs from disease outbreaks (Knowlton et al. 1990), the regional
coral to macroalgal dominance (McManus and Polsen- loss of the keystone grazer Diadema antillarum in 1983–
berg 2004; Fig. 1). 1984 to a Caribbean-wide epizootic (Hughes et al. 1985),
Coral abundance on reefs around the world began to a second major hurricane (Woodley 1992), and a series of
decline several decades ago (Gardner et al. 2003, Bruno coral bleaching events in the late 1980s (Goreau 1992),
and Selig 2007) due to a variety of factors including coral cover on these reefs plummeted to ,10% and
predator and disease outbreaks, poor land use practices, macroalgae became the dominant benthic functional
destructive fishing techniques, and ocean warming group (Liddell and Ohlhorst 1992, Hughes 1994).
(Glynn 1993, McManus et al. 1997, Aronson and Precht The Jamaican case study is assumed to be illustrative
2001, Hughes et al. 2003). In some locations, the cover of a widespread and ongoing phenomenon (Szmant
and biomass of benthic macroalgae increased concur- 2001, Bellwood et al. 2004, McManus and Polsenberg
rently with coral loss, resulting in community phase 2004, Precht and Aronson 2006). While there are several
shifts to reefs dominated by macroalgae (Done 1992, case reports of decreased coral cover and increased
macroalgal cover on other individual reefs (Endean and
Stablum 1973, Smith et al. 1981, Done 1992, Rogers and
Manuscript received 25 September 2008; revised 19 January
Miller 2006), there have been no regional- or global-
2009; accepted 20 January 2009. Corresponding Editor: R. B.
Aronson. scale analyses of coral reef phase shifts. Therefore, the
5
E-mail: jbruno@unc.edu ecological generality of these observations and the
1478
June 2009 CORAL REEF PHASE SHIFTS 1479
applicability of the Jamaican archetype to reefs around 2005). Most surveys used in our meta-analysis em-
the world (Bellwood et al. 2004) are unknown. ployed the line-transect technique, in which a transect
Epidemiologists perform randomized population (typically a 10–30 m measuring tape or chain) was
sampling to determine the generality of case reports placed on the reef. The coverage of coral and macro-
in the medical literature (Rothman and Greenland algae was then estimated either in situ by recording the
1998). Likewise, ecologists can apply various macro- number of points along each transect that overlaid
ecological and meta-analytical techniques to under- corals, macroalgae, and so forth, or by taking images of
stand the spatial dynamics, severity and impacts of the reef substrate at these points, which were then
major disturbances, community phase shifts, and other analyzed in the laboratory. We only used surveys that
ecological phenomena (Brown 1999). Such basic differentiated macroalgae from other algal groups.
pattern quantification over large spatial scales can put Following Steneck (1988) and others, we defined
more detailed, local studies into a broader context macroalgae (i.e., seaweed) as ‘‘larger (canopy heights
o ´
(Cˆ te et al. 2005). The purpose of this study was to usually .10 mm), more rigid and anatomically complex
assess the frequency, geographical extent, and degree of algal forms.’’ This functional group includes erect
macroalgal dominance of coral reef communities and of calcifying species (e.g., Halimeda spp.) but does not
coral to macroalgal phase shifts around the world. include microalgae and filamentous algae (i.e., turfs) or
Specifically, we used data from quantitative reef crustose algae (Steneck 1988).
surveys to determine the proportion of reefs in four Coral reef degradation and phase shifts are complex,
geographic regions (Greater Caribbean, Florida Keys, multivariate phenomena (Sebens 1994, Graham et al.
Indo-Pacific, and Great Barrier Reef [GBR]; see 2006) and can involve various combinations of coral loss
Appendix A: Fig. A1) that were dominated by macro- and seaweed gain. To address this issue and to facilitate
algae (.50% absolute macroalgae cover). We deter- graphical and statistical comparisons among regions and
mined the state of each reef along a continuum ranging years, we developed a coral reef phase shift index (PSI),
from coral to macroalgal dominance by developing a a quantitative, one-dimensional measure of the degree to
Reports
‘‘phase shift index’’ based on principal components which a reef has changed from a pristine (high coral, low
analysis of the two benthic categories (coral and macroalgal cover) state to a low coral, high macroalgal
macroalgal cover) included in the meta-analysis. We cover state. PSI is the first component (PCA1) from a
also asked whether phase shift severity changed principal components analysis (eigenvalue, 1.25; vari-
between 1996 and 2006. ance explained, 62%) on the correlation matrix between
macroalgal cover and the inverse of coral cover. The
METHODS analysis essentially combines the two variables (coral
Hughes’ classic study (Hughes 1994) of the degrada- and macroalgal cover) into a single value, which
tion of Jamaican reefs demonstrates the power of simplifies analysis and discussion of what would
repeated surveys of particular sites in detecting phase otherwise be a bivariate phenomenon by reducing the
shifts across broad spatial scales. Unfortunately, very dimensionality of the data set. PSI values were derived
few such longitudinal studies were implemented until the from single site–year combinations and are measures of
early 1990s, years to decades (or longer) after reefs began current reef state at the time of the survey, i.e., they are
to be altered by human activities (Pandolfi et al. 2003). not a measure of the degree to which a particular reef
Therefore, localized monitoring studies alone cannot be has changed over time. By pooling large numbers of
used to quantify the regional-to-global generality and single site-year PSI values, we were able to describe
severity of coral reef phase shifts. As an alternative ap- population-level variation in PSI among years and
proach, we used the extensive data from more recent reef regions. In this analysis, pristine reefs have a PSI of
surveys to make inferences about regional patterns (e.g., À2 to À3 and reefs with low coral and high macroalgal
magnitude and spatial extent) of shifts in coral reef cover have a PSI of 2 to 3 (Fig. 1). The PSI on reefs that
benthic communities. We assumed that most reefs were have undergone a severe phase shift was 3 to 5 (Fig. 1).
historically coral dominated and that macroalgae were The principal components analysis was performed on
relatively scarce. Therefore, the current state (in terms of the most recent survey performed on each reef (i.e., we
coral and macroalgal cover) of reefs across a region can did not include multiple surveys of individual reefs
be used as a measure of regional-scale degradation or through time) and included cover values from Hughes’
phase shift degree. 1994 study of Jamaican reefs in the 1970s and early
Our database included 3581 quantitative surveys of 1990s (Fig. 2).
1851 coral reefs (or sites) performed between 1996 and To determine whether the degree to which reefs are
2006 (see Appendix A). Our analysis was based on dominated by macroalgae has changed over time (i.e.,
quantitative surveys that measured the percentage of to test the null hypothesis that PSI did not change
the substratum covered by living coral and fleshy or between 1996 and 2006), we performed two types of
calcareous macroalgae between 1 and 15 m depth (mean regression analysis. For one analysis we used the entire
depth; 7.1 m). The abundance of macroalgae is con- data set to calculate annual regional mean PSI values
sidered a key metric of reef health (Steneck and Sala and for the other we only used data from monitoring
1480 JOHN F. BRUNO ET AL. Ecology, Vol. 90, No. 6
FIG. 1. The coral reef ‘‘phase shift’’ concept. (A) Images are from neighboring reefs near Discovery Bay Jamaica, in January
2003 (photos by J. Bruno). (B) Examples of different degrees of coral reef degradation around the world, based on the phase shift
index used in this analysis.
studies. Data from each of the four regions were temporal changes in PSI could be due solely to changes
analyzed separately. Time (year) and PSI were treated in the population of reefs that were surveyed each year.
as continuous variables and data were transformed For the second temporal analysis, we used only the
when necessary to meet basic statistical assumptions. subset of 458 reefs that were surveyed in two or more
Reports
The first analysis was a simple linear regression be- years. These data were analyzed with linear repeated
tween year and the annual mean PSI (i.e., the replicate measures regression analysis (using Stata version 9.1,
PSI measures within each region for each year were Stata Corporation, College Station, Texas, USA). This
pooled into a single value). A strength of this analysis, test accounted for the longitudinal structure of the
in contrast to one based on monitoring studies, is that survey data, particularly for the GBR, which was
the sampled reefs were more or less randomly selected, largely based on monitoring data from the Australian
which allows for greater generalization. However, a Institute of Marine Science’s Long Term Monitoring
significant weakness of this approach is that observed Program.
FIG. 2. State of the world’s coral reefs. The top row shows absolute living coral and macroalgal cover. The bottom row shows
count histograms of the phase shift index (PSI) in the four regions; the y-axis shows the lower and upper ranges of PSI in each bin.
Data in panel A are from Hughes (1994). Data in panels B–E are based on the most recent survey from each site.
June 2009 CORAL REEF PHASE SHIFTS 1481
TABLE 1. Reef state in the four study regions.
Number Coral Macroalgal Macroalgae Macroalgae
Region of sites Years cover (%) cover (%) . 25% . 50%
Caribbean 530 1996–2006 20.0 6 0.5 23.6 6 0.8 39% 10%
Florida Keys 160 1996–2005 8.1 6 0.7 14.7 6 1.3 23% 4%
Indo-Pacific 963 1996–2006 33.2 6 0.6 11.7 6 0.4 13% 1%
Great Barrier Reef 198 1996–2006 30.5 6 1.2 9.1 6 0.8 10% 1%
Notes: All summary statistics were based on the most recent survey performed at each site. Values for coral and macroalgal cover
are means 6 SE.
Percentage of surveyed reefs.
RESULTS AND DISCUSSION chetype was a PSI . 3, which in our analysis
Presently, there are no defined or generally accepted corresponded to less than 10% coral cover and macro-
thresholds of the degree of coral loss and macroalgal algal cover .60 % (Figs. 1 and 2). Based on this
increase that constitutes a phase shift (Rogers and Miller threshold, only 25 of the 1851 reefs (,1%) could be
classified as having undergone a complete coral to algal
2006). This has led to substantial confusion about the
phase shift (Fig. 2B–E) and all except one of these reefs
causes, generality, severity, and management implica-
were in the Caribbean. Phase shift severity is a
tions of phase shifts on reefs. Many authors appear
continuum, so categorical delineations of relative
implicitly to define coral reef phase shifts as cases where
severity are subjective and may be not be ecologically
macroalgae dominate the reef benthos (Hughes et al.
relevant. Nevertheless, our results indicate that the
2003, McManus and Polsenberg 2004, Knowlton 2008).
severity of phase shifts on a majority of the world’s
Unfortunately, what is meant by ‘‘dominate’’ is rarely
reefs (Figs. 2 and B1) appear to be substantially less
articulated. The use of ‘‘dominance’’ and similar terms
severe than those seen in a few well-known examples.
Reports
such as ‘‘preponderance’’ and ‘‘seaweed reef’’ implies a
Overall, our results indicate that there is no general
threshold of 50% macroalgal cover. Based on this
recent trend (i.e., post-1995) toward macroalgal domi-
definition, only 4% of the 1851 reefs used in our primary
nance (see Appendix C). PSI did not change during 1996
analyses were dominated by macroalgae. Across the
to 2006 in the Florida Keys or Indo-Pacific (Fig. C1,
Indo-Pacific (including the GBR) macroalgae only
Table C1). Many of the changes in these regions and in
dominated 1% of the surveyed reefs (Tables 1 and B1). the Caribbean presumably took place before broad-scale
Species or functional groups do not necessarily need surveying began. Based on one of our two temporal
to occupy or control a majority (.50%) of a limiting analyses, PSI marginally increased (P ¼ 0.07) on the
resource to ‘‘dominate’’ or define a community, but even GBR between 1996 and 2006, presumably due to a 3–4%
based on a much lower threshold of 25%, only 20% of decline in coral cover (there was no concurrent change in
surveyed reefs were seaweed dominated (Tables 1 and macroalgae) caused primarily by outbreaks of the
B1). Furthermore, more than half (53%) of these were in corallivorous seastar Acanthaster planci (Miller 2002).
the Caribbean, which includes only ;8% of the world’s In contrast, PSI decreased slightly in the Caribbean (Fig.
reefs (Spalding and Grenfell 1997). This result confirms C1, Table C1) due to a modest decrease in macroalgal
the common belief that phase shifts have been more cover from 34.0% 6 2.9% to 21.4% 6 1.3% (values are
severe in the Caribbean than elsewhere (Pandolfi et al. mean 6 1 SE) and even smaller increases in coral cover
2003, Bellwood et al. 2004). However, among-region from 19.9% 6 1.5% to 21.8% 6 0.7%, through 2005.
comparisons should be made with caution because reef Our results indicate there was a small increase in PSI
geomorphology, the types of reef habitats that are and a ;5% decrease in mean regional coral cover
surveyed, and possibly even reef community baselines all between 2005 and 2006 (from ;22% to 17%), possibly
vary among our study regions. Surprisingly, our results caused by the mass coral bleaching and mortality event
indicate that few of the world’s reefs fall into either of in late 2005 in the northern and eastern Caribbean
the classically defined coral reef stable points of coral or (Donner et al. 2007).
macroalgal dominance (Petraitis and Dudgeon 2004). A
large majority, including those in the Caribbean, are Coral reef baselines and recent changes
somewhere between these extremes; a pattern not in macroalgal abundance
concordant with the belief (Knowlton 1992, Bellwood Macroalgae play an important ecological role on
et al. 2004) that coral reef communities switch between shallow reefs (Vroom et al. 2006). Tropical macroalgae
coral and macroalgal dominated stable states. are highly diverse and countless species have evolved
We quantified phase shift severity using a phase shift adaptations to consume and utilize them (e.g., fishes
index (PSI) that combined the coral and macroalgal whose camouflage mimics macroalgae). But what was
coverage of a reef into a single variable using principal the historical baseline of macroalgal cover and how
components analysis (Figs. 2 and B1). A rough thresh- much has macroalgae increased? Nearly all surveys of
old for a severe phase shift based on the Jamaican ar- Caribbean reefs during the 1970s and early 1980s
1482 JOHN F. BRUNO ET AL. Ecology, Vol. 90, No. 6
reported absolute macroalgal cover values between 0% R 2 ¼ 0.09; Florida Keys P ¼ 0.008, R 2 ¼ 0.04; Indo-
and 10%. The mean of 19 surveys of 16 sites performed Pacific P ¼ 0.02, R 2 ¼ 0.01; Great Barrier Reef P ¼ 0.28).
between 1977 and 1982 is 6.6% (see Appendix D; Table Surprisingly, macroalgal cover has not increased appre-
D1). However, one survey reported macroalgal cover as ciably on most of the world’s reefs that have very low
high as 20.5% (Liddell and Ohlhorst 1992), and only a coral cover. For example, 379 of the 1851 reefs had
small number of locations were surveyed (primarily in 10% coral cover, but macroalgal cover was also low
St. Croix, U.S. Virgin Islands and along the north coast ( 20%) on nearly two thirds of these reefs. In fact, more
of Jamaica). Additionally, there is speculation that than half the benthic cover on reefs in the Caribbean,
macroalgal cover was unnaturally low during this period Pacific and Indian Oceans consists of organisms other
due to anomalously high densities of the urchin Diadema than hard corals and macroalgae, possibly because other
antillarum caused by the overfishing of its predators taxa, such as sponges and gorgonians, have been the
(Hay 1984, Levitan 1992). primary beneficiaries of coral loss (Aronson et al. 2002,
If the regional baseline was indeed roughly 3–10%, Norstrom et al. 2009). The degree of macroalgal dom-
¨
averaging ;6%, then macroalgal cover in the Caribbean inance is widely considered a key measure of reef health.
has increased fourfold. Although this increase may be For instance, Steneck and Sala (2005) argued that
ecologically significant, it is much smaller than generally ‘‘macroalgal abundance is the single best indicator of
assumed. Additionally, most evidence of negative effects poor conditions for coral reefs.’’ However, since the
of macroalgae on the growth and survival of juvenile cover of coral and macroalgae are only weakly related,
corals comes from studies in which macroalgal cover macroalgal abundance may not be a good indicator of
was far higher, typically 50 –70% (Carpenter and either coral loss or habitat quality.
Edmunds 2006, Hughes et al. 2007). However, one The absence of evidence for expected widespread
recent study found that macroalgal cover as low as 20 – increases in macroalgae could be due to the limited
30% was negatively correlated with coral recruit density extent of nutrient pollution on most reefs (Szmant 2002,
(Mumby et al. 2007). Greenaway and Gordon-Smith 2006), especially isolated
Reports
Another approach to estimating reef baselines of the offshore reef systems. Herbivores can clearly regulate
past is to study modern ‘‘quasi-pristine’’ reefs that are reef macroalgae (Lewis 1986, Steneck 1988, Williams
substantially less affected by human activities, due and Polunin 2001, Carpenter and Edmunds 2006) and
mainly to their isolation but also to legal protections overfishing has reduced the densities of herbivorous
(Knowlton and Jackson 2008). Two recent expeditions fishes on many reefs (Pandolfi et al. 2003, Bellwood et al.
(Vroom et al. 2006, Sandin et al. 2008) surveyed 10 such 2004). But compensatory increases in the abundance of
remote reefs in the central Pacific in part to establish a other herbivores may have partially filled this function
regional baseline. They found that macroalgal cover (Aronson and Precht 2000). One explanation for the low
averaged 13.1% 6 2.0% (mean 6 1 SE) and ranged from macroalgal cover in the Florida Keys and Great Barrier
3% to 28% (Table D2). With minimal or no fishing, Reef is that local management has been effective in
these reefs have intact food webs with plentiful top preventing herbivore populations from being depleted
predators (Vroom et al. 2006, Sandin et al. 2008) and are (Aronson and Precht 2006). Another is that commercial
probably our best window into the past (Knowlton and and recreational fishers in these relatively affluent parts
Jackson 2008). If so, macroalgae were substantially of the world target piscivores. Thus, herbivorous fish are
more abundant than we think, at least on some reefs and both released from predator control and largely
in some regions (Vroom et al. 2006). Macroalgal cover unaffected by direct fishing pressure (Graham et al.
on these ‘‘pristine’’ reefs is similar to the regional 2003). Additionally, the recovery of populations of the
averages for three of our four study regions, suggesting keystone grazer Diadema antillarum on some Caribbean
that macroalgal cover may currently be close to the reefs has reduced seaweed cover close to recent historical
historical baseline across most the world. levels at shallow sites and has also increased coral
recruitment (Carpenter and Edmunds 2006).
Macroalgal blooms, coral decline, and reef management
Macroalgal blooms on coral reefs are generally un- Conclusions
derstood to be caused by reduced herbivory (resulting The mismatch between descriptions of reef degrada-
from fishing and also from urchin die-offs in the tion in the literature and patterns in nature was caused
Caribbean) and coral loss, which allows macroalgae to by the generalization of a relatively small number of
colonize open substrate, thereby increasing primary examples. Case reports of local phase shifts were not
production and overwhelming grazers (Knowlton 1992, intended to be representations of the state and dynamics
Hughes et al. 1999, Williams et al. 2001). Thus, macro- of reefs in general. They were instead published as
algal cover and coral cover are widely assumed to be notable quantitative observations. Although in retro-
causally linked and inversely related. Yet we found only spect atypical, case studies such as the degradation of
weak negative relationships between coral and macro- Jamaican reefs have been invaluable warnings of the
algal cover (linear regression analyses based on the most consequences of subjecting reef communities to multiple
recent survey of each site; Greater Caribbean P ¼ 0.0001, natural and anthropogenic disturbances.
June 2009 CORAL REEF PHASE SHIFTS 1483
Since the Jamaica story was an anomaly, it makes a Proceedings of the National Academy of Sciences (USA) 104:
poor foundation for general models of reef ecology (e.g., 5483–5488.
Endean, R., and W. Stablum. 1973. The apparent extent of
Knowlton 1992, Bellwood et al. 2004). The current recovery of reefs of Australia’s Great Barrier Reef devastated
paradigm of reef management and ‘‘resilience’’ is based by the crown-of-thorns starfish. Atoll Research Bulletin 168:
in large part on the perception that most of the world’s 1–41.
reefs are being overrun by seaweed (Szmant 2001, Precht o ´
Gardner, T. A., I. M. Cˆ te, J. A. Gill, A. Grant, and A. R.
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APPENDIX A
A description of procedures and sources of data used in the meta-analysis (Ecological Archives E090-100-A1).
APPENDIX B
Basic analyses performed without data from Reef Check (Ecological Archives E090-100-A2).
APPENDIX C
Analyses of the relationship between time and phase shift index (PSI) values between 1996 and 2006 (Ecological Archives E090-
100-A3).
APPENDIX D
Reported macroalgal cover from early Caribbean reef surveys (1976–1982) and on remote Pacific reefs (Ecological Archives
E090-100-A4).