Coral Reefs (2001) 19: 400±417

DOI 10.1007/s003380000129

R EV IE W

L. J. McCook á J. Jompa á G. Diaz-Pulido

Competition between corals and algae on coral reefs:

a review of evidence and mechanisms

Accepted: 5 August 2000 / Published online: 20 December 2000

Ó Springer-Verlag 2000

Abstract Despite widespread acceptance that competi-

tion between scleractinian corals and benthic algae is
Introduction
important to the structure of coral reef communities,
Competition is an important process determining the
there is little direct experimental evidence that corals and
structure and composition of benthic communities on
algae do compete, and very little data on the processes
coral reefs (Lang and Chornesky 1990; Karlson 1999). In
and causality of their interactions. Most available evi-
particular, competition between hard corals and benthic
dence is observational or correlative, with intrinsic risks
algae is considered fundamental to the overall status of
of confounded causality. This paper reviews and cate-
coral reefs, especially during ``phase shifts'' in which reefs
gorises the available evidence, concluding that compe-
dominated by reef-building corals become dominated by
tition between corals and algae probably is widespread
macroalgae (e.g. Littler and Littler 1984; Lapointe 1989;
on coral reefs, but also that the interaction varies con-
Done 1992; Hughes 1994; Miller 1998). Algae are widely
siderably. Widespread replacement of corals by algae
considered to be competing with corals for space (or
may often indicate coral mortality due to external dis-
light), and interactions between the two are frequently
turbances, rather than competitive overgrowth, but may
interpreted simply in terms of algal competitive superi-
lead to competitive inhibition of coral recruitment, with
ority, often due to reduced herbivory or increased
consequences for reef recovery. We list eight speci®c
nutrient availability. Miller (1998) and McCook (1999)
processes by which corals and algae may a€ect each
showed that competition between corals and macroalgae
other, and suggest life history properties that will in¯u-
is a critical step during such reef degradation.
ence which of these interactions are possible. We propose
However, there is surprisingly little direct, experi-
a matrix for algal e€ects on corals, which lists the subset
mental evidence demonstrating competition between
of processes possible for each combination of coral life
these two groups (Miller 1998; McCook 1999). In this
form and algal functional group. This table provides a
review, we explore the available evidence on interactions
preliminary framework for improved understanding and
between corals and algae, with three speci®c purposes:
interpretation of coral-algal interactions.
(1) to summarise existing information on coral±algal
Key words Coral reef algae á Coral-algal competition á interactions, especially competition, and in particular
Macroalgae á Phase shifts á Overgrowth the processes or mechanisms by which corals and algae
interact; (2) to demonstrate the lack of hard data on
those mechanisms, or even that corals and algae are
L. J. McCook (&) á J. Jompa á G. Diaz-Pulido generally in competition, and hence the need for caution
Australian Institute of Marine Science, in assumptions about the processes involved; and (3)
P.M.B. #3, Townsville MC, 4810 Queensland, Australia
to suggest a preliminary conceptual framework for
L. J. McCook á J. Jompa á G. Diaz-Pulido understanding the processes by which algae may a€ect
CRC: Reef Research Centre
corals.
J. Jompa The review is limited to interactions between sclerac-
Department of Marine Biology, James Cook University tinian corals and macroscopic, free-living benthic algae.
of North Queensland, Townsville, Queensland, Australia,
and Hasanuddin University, Makassar, Indonesia We do not discuss the larger scale consequences of coral±
algal competition for reef composition and structure,
G. Diaz-Pulido
Department of Tropical Plant Sciences,
comprehensively reviewed by Miller (1998), nor the
James Cook University of North Queensland, context for reef degradation and management (reviewed
Townsville, Queensland, Australia by McCook 1999). Given the considerable structural and
 401

taxonomic diversity of both corals and algae, their right. Many of the studies reviewed were not intended to
interactions will not be homogeneous, so we include test the competitive nature of the interaction, or to
consideration of taxa and functional groups or life forms. demonstrate causality, but to document patterns or
Given their importance during reef degradation, we changes in community structure, or e€ects of herbivores.
emphasise the competitive e€ects of algae on corals, and Such studies are intrinsically valuable, especially where
in particular whether algal abundance is necessarily the they include long-term or large-scale data, which are
cause, rather than the consequence, of coral mortality dicult to achieve with manipulative experiments.
(McCook et al. 1997).

Direct experimental tests for competition

Interactions between corals and algae on coral reefs
Only seven studies were found that directly tested com-
Summary of available evidence petitive interactions between corals and algae (Table 1),
of which two were in temperate systems rather than coral
Based on the arguments of Connell (1983), Schoener reefs. Most of the experiments tested e€ects of algae on
(1983), Underwood (1986) and McArdle (1996), we have corals, and only one tested e€ects of corals on algae
classi®ed studies according to the levels of evidence they (McCook 2001). Only two studies simultaneously tested
provide that coral-algal interactions are in fact com- competitive e€ects and herbivory, despite the importance
petitive: that is, the performance of either competitor is of herbivory to algal abundance (Miller and Hay 1996,
reduced by the presence of the other. Speci®cally, we 1998). Most studies demonstrated negative impacts of
distinguish between: (1) experiments that directly ma- algae on corals, but these e€ects varied in intensity, and
nipulate abundance of either competitor (Table 1); (2) in one exceptional case, algae actually protected corals
experiments that manipulate herbivores, and thus are from bleaching (Jompa and McCook 1998).
assumed to indirectly manipulate algal abundance Also relevant are several studies (Table 1) intended to
(Table 2); (3) ``natural experiments'' or comparisons and examine coral recruitment or recovery from lesions, but
observations of correlations between algal and coral which provide de facto tests of the e€ects of corals on
abundances (Table 3); and (4) direct observations of algae. The induction of coral metamorphosis by coral-
coral±algal interactions, at relatively small scales line algae (Heyward and Negri 1999) provides a second
(Table 4). (Individual papers may include data or evi- example of algae enhancing coral success. In the lesion
dence in more than one category.) Within each table, we studies, experimental damage to coral tissue (with con-
have classi®ed studies by location and region, methods trol, undamaged areas) was followed initially by algal
and results, and by the algal taxa and functional group colonisation, but in general the corals regenerated,
and coral taxa and life form. overgrowing and thereby outcompeting the algae. Algae
Proof of competition requires unequivocal evidence did not colonise the control areas, and appeared to in-
that the performance of the study organism is in some hibit but rarely prevent coral recovery in damaged areas,
way inhibited by the presence of the competitor. That indicating competitive superiority of the corals. Larger
evidence can only be provided by (properly replicated lesions persisted for longer periods, often leading to
and controlled) direct manipulation of a competitor, so colonisation by more robust and competitively success-
that the only di€erence between treatments is the pres- ful algal forms (Meesters and Bak 1993; Meesters et al.
ence or abundance of the competitor, and any di€erence 1994, 1997).
in response may be assumed due (directly or indirectly) Some di€erences in competitive potential may be
to the competitor (Underwood 1986). All other ap- discerned between algal groups, such as canopies of large,
proaches are potentially confounded by other factors; leathery algae that shade or whiplash corals, and smaller
although we include some examples to illustrate possible algae that directly contact or smother corals. However,
confounding factors, issues of causality and correlation these studies together still provide very limited coverage
cannot be argued in detail here (see e.g. previous refer- of di€erent combinations of algal functional groups and
ences, and Strong et al. 1984; Diamond 1986). In par- coral life forms, and so provide a very limited basis for
ticular, without experimental evidence, the replacement generalisations about coral±algal competition. Further,
or overgrowth of live coral by algae does not prove that most manipulations were inevitably at relatively small
the algae have outcompeted the corals: the coral may scales (0.1 to <10 m), although several did involve
have been killed by some other, unrelated factor (e.g. more than one reef or large-scale transplantations.
bleaching, corallivory, storm damage, eutrophication,
disease), potentially unknown to the researcher. The
algae may have increased as a consequence of the coral Indirect experiments using herbivore manipulations
loss, and may have been having little or no inhibitory
e€ect on the corals (e.g. McCook 2001). Indirect experimental evidence for competitive e€ects of
We emphasise that recognition of the interpretive algae on corals comes from experimental herbivore
limitations of any study in terms of competitive causality manipulations (Table 2). Only nine such studies were
does not amount to criticism of the study in its own found to include data on coral abundance, and most
 402

Table 1 Comparison of studies which directly test e€ects of algae and corals on each other. Summary table of key aspects of published experimental studies of coral-algal competition
(see text; studies are organised by type of study or evidence, and then chronologically). Impacts are summarised as A impact of algae on corals and C impact of corals on algae; in each
case impacts are summarised as: ± negative (competitive); 0 no impact; + facilitatory or bene®cial. Note that both corals and algae will often be mutually inhibitory, but many studies
did not consider impacts of corals on algae, so impacts represent a biased sample. Methods and evidence listed are only those relevant to this table. Any limitations noted refer only to
the interpretative context of this table, and are therefore not to be taken as criticisms of the studies (in most cases limitations were unavoidable and acknowledged by authors). Final
rows summarise studies of coral recruitment or recovery from experimental lesions, which we have reinterpreted in terms of competition. Algal functional groups are modi®ed from
Steneck and Dethier (1994): Filament Filamentous; Cort Foliose, Creep or Upright foliose, corticated foliose, creeping or upright; Cort Macro corticated macrophytes; Leathery leathery
macrophytes; Artic Calc articulated calcareous; Crustose crustose. Creeping and upright corticated foliose algae refer to growth habit, often variable within a genotype. CCA Crustose
coralline algae; GBR Great Barrier Reef

Reference Location, region Impacts, methods and evidence Comments Algal taxa/functional Coral taxa/life form
group
A C

Hughes (1989) Rio Bueno, Jamaica, ± Macroalgal removal treatment Experiment design not Unspeci®ed/ Agaricia spp.
Caribbean and natural encounters; speci®ed but results ``Fleshy algae'' +20 spp. listed/
coral bleached or dead where clear-cut most forms
in contact with macroalgae;
macroalgae outcompeted
coral by overgrowth
Coyer et al. (1993) California, temperate ± Coral transplantation to Temperate location; Cystoseira; Dictyota; Balanophilia/Solitary
Paci®c rocky kelp di€erent algal abundance; non-reef building CCA; kelp holdfast/ (small)
bed overgrowth of corals after coral; results clear Leathery; Cort Foliose;
1 year; corals damaged cut Crustose
by brushing; 10 years
Tanner (1995) Heron Island, GBR ±0 Algal removal treatment Clear-cut experiment, Variousa/Artic Calc; Acropora brueggemannia;
and natural encounters; limited by low cover Crustose; Filament; Acropora cuneata;
energetic cost to corals of both algae and Leathery; Cort Macro; Pocillopora damicornis/
from algal contact; algae coral ± may Cort Foliose Branching
reduced cover, growth and underestimate e€ects
fecundity of some corals but
not all, and, importantly,
did not a€ect survival
Miller and Hay (1996) North Carolina, ± Algal removal, coral Temperate location; Variousb/Leathery; Oculina arbuscula/
temperate Atlantic; transplantation, herbivore non-reef-building Cort Foliose; Filament; Branching; recruits
inshore±o€shore exclusion, and nutrient coral; results clear cut Cort Macro
gradient enrichment; algae inhibited
growth and recruitment of
coral, due to shading
or abrasion
Miller and Hay (1998) Florida, Caribbean ± Corals transplanted to Coral growth rate Variousc/Cort Foliose; Porites porites/
herbivore exclusion cages di€erences may be Artic Calc; Cort Macro; Branching
with and without algae slightly confounded Filament
present; coral growth by di€erent predator
reduced in presence bite rates on corals
of algae
Jompa and McCook Inshore, central GBR; + Canopy algal removal; Demonstrates variable Sargassum /Leathery Diverse/Diverse
(1998) 2 sites, 2 reefs: algal canopy protected impacts of macroalgal
inshore±o€shore corals from bleaching beds
gradient damage (shading?)
McCook (2001) Inshore, central GBR 0 ± Removal of massive corals Various (listed)/Filament Porites lobata/Massive
or turf algae along gradient
of terrestrial runo€: corals
inhibited turf growth more
than vice versa; coral success
not related to nutrient
or sediment inputs.
Recruitment study:
Heyward and Negri Lizard Island, + Calci®ed red algae induced Demonstrates positive Lithophyllum; Acropora millepora;
(1999) GBR and Ningaloo, metamorphosis/settlement impacts of algae on Hydrolithon; various/Recruits
Western Australia of coral larvae coral. Not intended Neogoniolithon;
to address competition Amphiroa; Mesophyllum;
Peyssonnelia/Crustose;
Artic Calc
Lesion studies:
Bak et al. (1977) SW Curacao, ± Algal turfs which initially Not intended to address Unspeci®ed/Filament Agaricia agaricites;
Caribbean colonised experimental coral±algal competition Montastrea annularis/
lesions on corals were but demonstrates coral Foliose and massive
overgrown by coral overgrowth of colonising
algae
Meesters and Bak Curacao, Caribbean ± ± Colonisation of experimental As above Unspeci®ed/Filament Montastrea annularis;
(1993); Meesters lesions by algae in¯uenced Porites astreoides;
et al. (1994, 1997) but did not generally prevent Meandrina meandrites/
coral overgrowth of algae. Massive
Duration and type of algal
colonisation a€ected
recovery
van Woesik (1998) Okinawa, Japan ± ± As above As above Unspeci®ed; Padina/Fila- Porites spp./Massive
ment; Cort Foliose
a
Halimeda, Peyssonnelia, Chlorodesmis fastigiata, Turbinaria, Sargassum, Amphiroa, Caulerpa, Hypnea, Enteromorpha, Padina
b
Sargassum, Lobophora, Dictyota, Dictyopteris, Zonaria, Ectocarpus, Chondria, Hypnea
c
Dictyota, Halimeda, Laurencia, Coelothrix, Galaxaura, Amphiroa, Stypopodium and ®lamentous reds
403
404

Table 2 Comparison of experiments which indirectly examine e€ects on coral are direct results of increased algae, in turn re-
coral±algal competition using herbivore manipulations. Impacts, sulting from herbivore manipulations, and ignore potential con-
methods, evidence, comments, functional groups and abbreviations founding factors (see text). As such experiments cannot expect to
as for Table 1. Note that impact summaries (column A) assume that detect impacts of corals on algae, these are not summarised
Reference Location, region Impacts, methods Comments Algal taxa/ Coral taxa/
and evidence functional group life form

Vine (1974)a Harvey Reef, ± Settlement plates No data given Unspeci®ed/ Unspeci®ed/
Red Sea caged, uncaged for corals; Filament Recruits
and in damsel®sh Damsel®sh e€ects
territories; confound
observed that herbivore exclusion
invertebrate (incl. with other e€ectsa
coral) recruitment
was reduced where
algae abundant
Sammarco Discovery Bay, ±0 Diadema density Di€erences among 32 spp. listed/ Agaricia spp.;
(1980, 1982) Jamaica, manipulations and between taxa Filament; Artic Porites spp.
Caribbean and removals; in competitive Calc; Crustose +15 spp. listed/
no e€ect of outcomes; Branching;
algae on coral Diadema removal Massive;
recruitment but alone led to Foliose;
some e€ect on increased coral Sub-massive;
survival of recruits abundance Recruits
and cover of adults;
coral recruits
overgrew CCAs
Sammarco Britomart, GBR ±0 Settlement plates Damsel®sh e€ects Palmophyllum; Acropora and
and Carleton inside and outside confoundeda Polysiphonia; Seriatopora
(1981)a territories and cages; Ceramium; +10 spp. listed/
coral recruits shaded Gracilariopsis/ Recruits
by ®lamentous Crustose
algae, but no e€ect (not calci®ed);
of caging on Filament
recruitment
Fitz et al. (1983) St. Croix, ±0 Caged and exposed Variable e€ects Unspeci®ed/Various Agaricia and Porites
Caribbean settlement panels; spp./Recruits
algal growth in
cages reduced coral
settlement in one
size class,
but not in two others
Hay and Taylor St. Thomas, ±? Diadema removal; Coral cover Dictyota/Cort Unspeci®ed/
(1985) Caribbean decreased cover initially low Foliose Unspeci®ed
of ``benthic
invertebrates''
following algal
growth
Lewis (1986) Carrie Bow, ± Herbivore reduction Although Padina; Dictyota; Porites astreoides/
Belize, by fences; signi®cant, Turbinaria; Massive
Caribbean increased algal decline in Gelidiella +26 spp.
biomass killed coral cover listed/Cort Foliose
and bleached only 2% (Creep; Upright);
corals Leathery; Cort
Macro; Filament
Stachowicz North Carolina, ± Removal of Temperate, Sargassum; Dictyota; Oculina arbuscula/
and Hay (1999) temperate symbiotic non-reef- Codium; Branching
Atlantic herbivorous crab building coral Ectocarpus/
led to algal Leathery; Cort
overgrowth (and Foliose; Cort
invertebrates) Macro; Filament
Lirman (2001) Florida, ± Algal additions Algal addition Halimeda and Montastrea faveolata;
Caribbean and cages led to treatment Dictyota/Artic Porites astreoides;
inhibition and unclear Calc; Cort Foliose Siderastrea siderea/
polyp retraction Massive
in corals
a
Comparisons using damsel®sh territories as herbivore reductions are confounded by complex e€ects of damsel®sh on composition of
algae, coral injury, coral recruitment, nutrient conditions, etc. (e.g. Kaufman 1977; Russ 1987)
Table 3 Comparison of evidence for coral±algal competition based on natural experiments and correlations in abundance. Studies are organised chronologically within approach or
theme. Although more studies could be included, list has been limited to those that speci®cally invoke coral±algal competition, have been cited in that context, or that we consider
noteworthy. ``Natural experiment'' refers to studies with a speci®c comparison, but where treatments were not allocated or applied by researchers; in some cases they are human impacts
such as ®shing pressure or eutrophication. In most cases, Diadema die-o€ occurred against a background of over®shing. Where possible, outcome (O) of interaction is summarised as: A
Algae overgrew corals; B no change; C corals overgrew algae; impacts are not summarised as causality is intrinsically confounded (see text). Methods, evidence, comments, functional
groups and abbreviations as for Table 1. Most natural experiments also include or imply negative correlations in abundance of corals and algae. Except where noted, all correlation
studies listed indicate inverse relationships between cover of algae and corals, although not necessarily identi®ed as such by authors
Reference Location, region Outcomes, methods and evidence Algal taxa/functional group Coral taxa/life form

Natural experiment (Algae):

Crossland (1981) H. Abrolhos, B Algae present or absent; coral growth Sargassum and Turbinaria; Acropora and Pocillopora
Western Australia reduced when algae present Eucheuma and Laurencia/ spp./Branching
Leathery; Cort Macro
Natural experiments (Herbivory):
Potts (1977)a Heron Island, GBR AB Colonisation of coral transplants by Unspeci®ed/Filament Acropora palifera/
damsel®sh; variable outcome: generally Branching
reduced coral growth and survival,
but at times growth increased.
Confounded by complex e€ectsa
de Ruyter van Curacao, Caribbean A Diadema die-o€; cover through time; Lobophora; Dictyota; Agaricia agaricites
Steveninck corals and algae generally but not Halimeda; Valonia; +21 spp. listed/Foliose;
and Bak (1986) always inversely related Wrangelia; turfs/Cort Massive; Branching;
Foliose; Artic Calc; Encrusting
Filament; Crustose
Liddell and Jamaica, Caribbean B Diadema die-o€; cover before and Dictyota; Lobophora; Halimeda Unspeci®ed; Acropora/
Ohlhorst (1986) after, along depth gradient; changes +7 spp. listed/Cort Foliose; Branching
in coral cover variable, even increased. Artic Calc; Filament;
Leathery; Foliose
Littler and Great Astrolabe AC High and low ®shing pressure; coral 24 spp. listed/ Acropora/ Branching?;
Littler (1997a) Reef, Fiji recruits could overgrow turfs, but turfs Filament; Cort Recruits
could also exclude recruits; temporal Macro; Artic Calc
and spatial correlation, cover
Natural experiments (herbivory and disturbance):
Hughes (1989, Rio Bueno, Jamaica A Diadema die-o€ and hurricane: temporal Dictyota; Padina; Halimeda; Agaricia spp. +20 spp.
1994, 1996) and spatial negative correlations in Lobophora;and others/ listed/Most forms
algal and coral cover, and coral Filament; Crustose; Cort
recruitment. E€ects variable with Foliose (Creep; Upright);
coral life form Artic Calc; Leathery
Goreau (1992) Jamaica, Caribbean A Diadema die-o€, hurricane, Lobophora; Ceramium; 55 spp. listed/Most forms
eutrophication (review); algae Dictyota; Chaetomorpha;
increased with coral decreases Halimeda; Sargassum/
Cort Foliose; Filament;
Artic Calc; Leathery
405
 406
Table 3 (Continued)

Reference Location, region Outcomes, methods and evidence Algal taxa/functional group Coral taxa/life form

Steneck (1994) Discovery Bay, AB Diadema die-o€, hurricane; temporal Dictyota; Laurencia; 8 spp. listed/Branching;
Jamaica; St. Croix, and spatial negative correlations Lobophora/Cort Foliose; Massive; Foliose
Caribbean in cover of varying strength, Cort Macro; Crustose
also recruits
Shulman and Panama, Caribbean A Diadema die-o€, bleaching; temporal Dictyota; Halimeda/Cort Agaricia agaricites;
Robertson (1996) negative correlation of cover of Foliose; Artic Calc Agaricia tenuifolia;
corals and algae over 7 years; some Porites spp.; Millepora
corals no change spp./Foliose; Massive;
Digitate
Rogers et al. (1997) Virgin Islands, Carib- A Hurricane, herbivorous ®sh; decrease Dictyota; Liagora/Cort Montastrea annularis;
bean in corals and increase in algae Foliose; Cort Macro Agaricia agaricites; Sid-
over 7 years erastrea siderea; Montas
trea cavernosa/Massive;
Foliose
Natural experiments (disturbance):
Banner (1974) Kaneohe Bay, Hawaii A Eutrophication gradient: categorisation Dictyosphaeria cavernosa/ Porites compressa/Digitate
of algal and coral abundances, showing Foliose
inverse relationship
Birkeland (1977) Panama, Paci®c Oligotrophic and upwelling areas; survival Unspeci®ed/Filament Unspeci®ed/Recruits
of recruits higher with less algae;
®lamentous algae trap sediments which
kill corals
Smith et al. (1981) Kaneohe Bay, Hawaii A Eutrophication gradient and before±after Dictyosphaeria cavernosa/ Porites compressa/Digitate
diversion: algal biomass, cover of corals Foliose
and algae. Little relevant data included
Wittenberg and Hunte (1992) Barbados, Caribbean Eutrophication gradient; higher coral Unspeci®ed Porites; Diploria; Agaricia
juvenile size and survival where algae agaricites/Massive;
and sediments less abundant Foliose
Hunter and Evans (1994) Kaneohe Bay, Hawaii A C Natural experiment; spatial and temporal Dictyosphaeria cavernosa/ 5 spp. listed/Most forms
correlations, cover; several reversals in Foliose
abundance; coral not inversely related
to algae at some sites
b
Genin et al. (1995) Gulf of Eilat, Red Sea Eutrophication gradient; coral condition Enteromorpha/Filament /Branching; Massive
inversely related to abundance of algal
bloom
Miller and Hay (1996) North Carolina, Inshore±o€shore gradient; temperate; See Table 1 See Table 1
Atlantic algal cover inversely related to coral
abundance
Connell et al. (1997) Heron Island and A Cyclones; very long term (30 years), Unspeci®ed Unspeci®ed + Recruits
Jamaica negative correlations in algal and coral
cover and coral recruitment
Spatial and temporal correlations:
van Den Hoek et al. (1978) Curacao, Caribbean Spatial correlation in cover: depth, etc. Various (all listed)/All groups Various (all listed)/
gradients Most forms
 407

indicated declines in corals, presumably in response to

46 spp. listed/Most forms

the general increase in algal abundance following her-
5 spp. listed/Branching; bivore exclusion. However, the e€ects on corals were
Various/Branching;
Various (all listed)/
Massive; Foliose;

often variable, or relatively minor. For example, two of

Porites compressa/
the most cited papers in this context are Sammarco
(1982), in which removal of Diadema alone led to in-
Branching

creased coral abundance, and Lewis's (1986) classic

Massive

Digitate
Massive

Various
herbivore exclusion experiment, in which the resulting
decline in coral cover was only about 2% (coral abun-
dance was initially relatively low). Inevitably, most of
these experiments were relatively small scale and short
Various (all listed)/All groups

term, and thus involved smaller, faster growing algal

Sargassum/Cort Foliose;

Dictyosphaeria cavernosa/

taxa (®lamentous and corticated macrophytes).

Hormophysa/Leathery
Sargassum; Turbinaria;
Dictyota ; Lobophora;

Importantly, herbivore experiments (and natural ex-

Stylophora pistillata, Acropora spp., Pocillopora verrucosa, Favia, Favites, Porites spp., Fungia granulosa, Fungia horrida, Ctenactis echinata
Sargassum/Leathery

periments involving herbivore changes) are fundamen-

tally tests for herbivore e€ects, not competition (and are
intended as such by their authors). Although e€ects of
Unspeci®ed

Leathery

algae on corals are generally the most or even the only

Foliose

reasonable interpretation, alternative explanations re-

main possible. For example, the herbivore exclusion
procedure may produce artifacts detrimental to corals
(e.g. shading, reduction in ¯ow; not all experiments in-
Spatial correlation in cover: reef ¯at zones

cluded procedural controls). Declines in corals could also

result from the incidental exclusion of predators that
cover not inversely related to algal
Spatial correlation in cover; among

would otherwise restrict corallivores (e.g. gastropods).

Spatial correlation in cover, along

Spatial correlation in cover: coral

Spatial and temporal correlations

canopy within or between reefs

Spatial correlation in cover

``Natural experiments'' and correlative studies

Considerably more evidence comes from the numerous

comparisons of coral and algal abundance during
stress gradient

``natural experiments'' or along gradients, or simple in-

9 locations

verse relationships between coral and algal abundance in

in cover

space or time (Table 3). Many of these comparisons

have the advantage of wider generality than direct,
planned experiments, due to larger spatial or temporal
Comparisons using damsel®sh territories are confounded (see Table 2)

scales. However, as stated previously, causality is in-

trinsically more ambiguous, since the correlations ob-
served may be coincidental or consequential, rather than
causal.
B

For example, Crossland's (1981) comparison of coral

Gulf of Eilat, Red Sea

Kaneohe Bay, Hawaii

Inshore, central GBR

Inshore, central GBR

growth in the presence and absence of canopy-forming

algae provides valuable and widely cited evidence for
Red Sea, Arabian

competitive inhibition by shading. However, separation

Sea, the Gulf
Arabian Gulf

of corals into shaded and unshaded was retrospective,

since algae appeared in some plots and not others.
Further, there was no evidence that the di€erences were
caused speci®cally by shading, rather than, for example,
abrasion by the algae, or by other unknown factors.
Algal shading was assumed to be the cause of reduced
Benayahu and Loya (1981)

coral growth, with the di€erences in algal growth

unexplained, but there is no a priori evidence that
Stimson et al. (1996)

causality might not be reversed (algal growth reduced

Morrissey (1980)

Sheppard (1988)

McCook (1999)

as a consequence of coral growth, in turn due to

unknown factors), common (same factor/s cause in-
Coles (1988)

creased algal growth and decreased coral growth), or

even coincidental (unrelated factors cause coral and
algal di€erences). Thus, other unmeasured di€erences
between plots, such as variations in light, nutrient,
b
a
 408

Table 4 Comparison of direct observations of coral±algal interactions or contacts. Studies that provide relatively detailed and small-scale descriptions or photographs of coral±algal
interactions. Methods, evidence, comments, functional groups and abbreviations as for Table 1, outcomes (O) as for Table 3

Reference Location, region Methods and evidence Algal taxa/functional group Coral taxa/life form

O
a
Fishelson (1973) Eilat, Red Sea C (Photograph) Coral regeneration by Various; esp. Dichotrix; /Branching; Massive
overgrowth of areas colonised by algae Sphacelaria; Lobophora/
Filament; Cort Foliose (Creep)
Banner (1974) Kaneohe Bay, Hawaii A (Photograph) Algal overgrowth of corals Dictyosphaeria cavernosa/Foliose Porites compressa/Digitate
Birkeland (1977) Panama, Paci®c A (Photograph) Algae reduce recruit Unspeci®ed/Filament Unspeci®ed/Recruits
survival and trap sediment
Bak and Engel (1979) Curacao, Caribbean A (Photograph) Algal overgrowth Porolithon and unspeci®ed/ Agaricia agaricites +21 spp.
of 20% recruits Crustose; Filament listed/Recruits
Lewis (1986) Belize, Caribbean A (Photograph) See Table 2 See Table 2 See Table 2
Hughes et al. (1987); Jamaica, Caribbean A (Photograph) Algal overgrowth of corals See Table 3 See Table 3
Hughes (1994)
de Ruyter van Steveninck Curacao, Caribbean (Photograph) Algal growth reduced Lobophora/Cort Foliose (Creep) Agaricia; Meandrina;
et al. (1988b) in close proximity to corals Mycetophyllia;
Stephanocoenia/Foliose;
Massive; Encrusting
James et al. (1988) Bahamas, Atlantic; A (Photograph) Peyssonnelia overgrows Peyssonnelia/Crustose Acropora cervicornis; Acropora
St. Croix, Barbados, and kills corals palmata; Montastrea
Antilles, Caribbean annularis/Branching; Massive
Lapointe (1989) Caribbean A (Photograph) Algal overgrowth of coral Cladophoropsis; Cladophora/ Unspeci®ed
Filament
Stimson et al. (1996) Kaneohe Bay, Hawaii A (Photograph) Algal overgrowth of coral Dictyosphaeria cavernosa/Foliose Porites compressa/Digitate
Keats et al. (1997) Indo-Paci®c A (Photograph) CCA overgrowth of coral Pneophyllum conicum/Crustose Porites spp./Massive
Littler and Littler (1997a) Great Astrolabe Reef, Fiji AC (Photograph) Coral recruits overgrew See Table 3 See Table 3
turfs; turfs overgrew adult corals
Littler and Littler (1997b) Caicos Island, Caribbean A (Photograph) Algae killed coral tissue Dasyopsis spinuligera/Filament Madracis decactis/Digitate
allelochemically or Cort Macro?
Antonius (1999) Belize +?, Caribbean A (Photograph) Crust overgrowth of coral Metapeyssonnelia corallepida/ Millepora complanata
crustose
Finckh (1904) Funafuti Atoll, Paci®c A Algal overgrowth of corals Lithothamnion/Crustose Pocillopora; Heliopora; Porites/
Branching
Smith et al. (1981) Kaneohe Bay, Hawaii A Algal overgrowth of corals Dictyosphaeria cavernosa/Foliose Porites compressa/Digitate
Chadwick (1988) Kaneohe Bay, Hawaii A Algal overgrowth of coral Dictyosphaeria cavernosa and Fungia scutaria/Mushroom
CCA/Foliose; Crustose
Wittenberg and Barbados, Caribbean A Algal overgrowth of juvenile corals Unspeci®ed Porites astreoides; Agaricia
Hunte (1992) agaricites; Diploria spp./
Massive; Foliose
Tanner (1995) Heron Island, GBR B Contact with algae reduced coral growth See Table 1 See Table 1
Shulman and Panama, Caribbean A Bleaching of corals underneath algae See Table 3 See Table 3
Robertson (1996)
Lirman (2001) Florida, Caribbean A Polyp retraction and overgrowth See Table 2 See Table 2
near algae
a
Stylophora pistillata, Pocillopora danae, Acropora, Favia favus, Platygyra lamellina, Favites spp., Goniastrea pectinata, Lobophyllia corymbosa, Millepora dichotoma, Porites lutea
 409

sediment or herbivory regimes, may have contributed to Direct observations of apparent competition
the di€erences in both algal abundance and coral
growth rates. Finally, evidence for coral±algal competition comes
Similarly, in Potts' (1977) demonstration of reduced from numerous direct observations of small-scale inter-
coral growth inside damsel®sh territories, corals were actions, many supported by photographs (Table 4; Fig. 1),
not randomly allocated to treatments, but selected by in which corals appear to be overgrown by algae. Al-
the damsel®sh, presumably non-randomly (territory though convincing, such observations do not necessarily
boundaries also changed during the study, so that some prove that the algae are killing the coral. Any area of coral
corals changed treatments). The damsel®sh may have tissue killed by other causes (e.g. corallivorous ®sh or
selected less vigorous corals, or even have damaged the invertebrate feeding, temporary sediment burial, bleach-
corals directly (Kaufman 1977). Further, aside from algal ing) will generally be rapidly colonised by algae, whereas
abundance, damsel®sh modify numerous aspects of their adjacent healthy coral tissue may continue to vigorously
territories, including nutrient regime and algal compo- defend itself from algal recruitment or vegetative over-
sition (Russ 1987), which may modify coral growth growth. Thus, close matches between coral tissue damage
rates. Thus, although valuable, these results should not and algal overgrowth may not indicate algal competitive
be taken uncritically as evidence that the algae inhibited success, but rather the successful competitive exclusion of
coral growth. algal growth from areas of healthy coral tissue (de Ruyter
Importantly, even where abundant algae have re- van Steveninck et al. 1988b; McCook 2001), unless ex-
placed formerly abundant corals, the major cause of perimental evidence is also available.
coral mortality may be external disturbances, rather Several of the listed observations illustrate the vari-
than direct competition from the algae (e.g. fresh-water ability of coral±algal interactions. Littler and Littler
kills in Kaneohe Bay: Smith et al. 1981; Kinsey 1988; (1997a) provide contrasting photographs of coral recruits
Hunter and Evans 1994; hurricane at Discovery Bay: apparently overgrowing ®lamentous turf algae, and of
Hughes 1994). Thus, although corals and algae may be ®lamentous turfs apparently killing adult corals. Littler
competing for space, and competition may explain the and Littler (1997b) appear to demonstrate algae over-
algal bloom when corals are removed, the algae may not growing and killing healthy coral tissue by means of
have directly outcompeted the corals. allelochemicals, a process otherwise undocumented (but
Particular caution is required in interpreting causality see also Fig. 1D; de Nys et al. 1991 for soft corals). De
in studies based on correlations in cover of algae and Ruyter van Steveninck et al. (1988b) document inhibition
corals (Table 3). Despite the general assumption that the of algal growth rates by proximity to corals, the only de-
inverse correlations are caused by competition (e.g. tailed demonstration of coral e€ects on algae. Finally,
Benayahu and Loya 1981), the patterns may simply re- Coyer et al. (1993) and Lirman (2001) noted polyp re-
¯ect coincident di€erences in other factors in¯uencing traction in response to algal brushing, providing other-
their distributions, or causality may even be reversed. wise scarce evidence for the mechanisms of competition.
For example, o€shore to inshore reversals in coral and
algal abundance could be due to coral intolerance of
inshore turbidity and algal susceptibility to the abundant Discussion of evidence: general points
herbivores on o€shore reefs (coincident causality; e.g.
McCook 1996, 1997). The same pattern could also arise Overall, there is little evidence that unambiguously
because corals are killed by inshore sediment loads, demonstrates competition between corals and reef algae,
allowing algae to persist (Umar et al. 1998). and very little demonstrating competitive overgrowth of
Several of the other studies listed (Table 3) warrant corals by algae. Only 7 of the 57 papers reviewed pro-
particular mention. The relatively long time span of vided direct experimental tests for competition. Much of
temporal comparisons by Shulman and Robertson the available evidence is indirect, anecdotal or correla-
(1996; 7 years), Connell et al. (1997; 30 years), Rogers tive, and provides little understanding of the processes
et al. (1997; 7 years) and the long time span and broad by which algae may replace corals. Interpretations of
coverage of some of the Diadema die-o€ studies (e.g. algal competitive superiority are frequently justi®ed by
Hughes et al. 1987; Hughes 1989, 1994, 1996; 17 years; citing one of a limited number of speci®c studies (in
Steneck 1994; 9 years), make them particularly valuable, particular, Birkeland 1977; Potts 1977; Crossland 1981;
especially since most include considerable background Smith et al. 1981; Sammarco 1982; Lewis 1986), many of
data and evidence for the competitive nature of the which were not designed to test competition. In some
changes documented. Historical synthesis of coral and cases papers have been cited that have no relevant ®rst-
algal abundances and terrestrial runo€ in Kaneohe Bay hand evidence, but merely refer to other studies (usually
suggest that changes in reef composition involve complex one of the above), or that include no more than passing
and uncertain interactions between fresh-water kills, speculation about the process.
eutrophication, sedimentation and coral±algal competi- Nonetheless, competition between corals and algae
tion (Hunter and Evans 1994; 20 years; in contrast Smith generally seems the most realistic explanation of most
et al. 1981 and Banner 1974 include little hard data on of the available evidence. Despite the limitations of
coral or algal abundances). that evidence, the breadth and range of observational
410
 411

b 1993 in Table 1). The interaction is apparently compet-

Fig. 1 Coral±algal interactions: examples of a range of interactions itive, since the algae have been released from competitive
between corals and algae. A Overgrowth of coral (Porites cylindrica inhibition by the corals, but the corals may have been
in this case) by the brown alga Lobophora variegata, a widespread
phenomenon, especially on Caribbean reefs. B Same coral showing the superior competitor (in the absence of disturbance).
bleached tissue after removal of algae. Experimental removals of It is likely that external disturbances and competition
either coral or algae near boundary showed that both algae and will interact: stressed corals will probably be less suc-
corals inhibit each other's growth (inshore GBR; Jompa and cessful competitors, or algae may colonise outward from
McCook, unpublished data). C Shading by Sargassum canopy
protected corals from bleaching damage during 1998 mass
patches killed by external events. It is also important to
bleaching: right side of Porites lobata shown was underneath the distinguish between competitive abilities of established
Sargassum canopy, and was not bleached, whereas left side was not and recruiting corals. Even if competitively inferior to
shaded and was bleached (inshore GBR; experimental removal of established corals, algae, once established by distur-
canopy demonstrated causality: Jompa and McCook 1998). D bance, may successfully pre-empt space and inhibit coral
Coral tissue death following overgrowth by ®laments of the red
alga Corallophila huysmansii, possibly due to chemical e€ects recruitment, preventing recovery from disturbances
(P. cylindrica, inshore GBR); arrow shows swollen coral tissue (such as bleaching, storms or crown of thorns; Hughes
around algal ®laments. E Substantial amounts of sediments and 1996; Connell et al. 1997). These distinctions among
mucus adhering to individual ®laments of Anotrichium tenue di€erent competitive processes may have important
(arrow; Ceramiales, Rhodophyta) overgrowing P. lobata (inshore
GBR). It appears that coral mucus production could e€ectively consequences in terms of management of reef degrada-
remove settling sediment particles except where they were trapped tion (McCook 1999).
by algal ®laments. This secondary e€ect of algae appeared to It is important that algal replacement of corals be
signi®cantly increase damage to underlying coral tissue viewed in the context of herbivore e€ects on algal
abundance. Much of the evidence for algal e€ects on
and correlative studies are consistent with coral±algal coral come from studies of herbivore reductions (herbi-
competition as a widely general structuring process. vore exclusions, Diadema die-o€ and over®shing and
However, the interaction is also highly variable in damsel®sh studies). Herbivory is a key factor mediating
mechanism and outcome, and the detailed processes and the e€ects of algae on corals, since the standing crop or
mechanism of coral±algal competition warrant careful biomass (per unit area) of algae is largely controlled by
scrutiny. Many of the studies listed showed variable ef- herbivores (reviews by Hatcher 1983; Steneck 1988;
fects or outcomes not limited to inhibitory e€ects of Carpenter 1997; McCook 1999) and the ability of algae
algae on corals (16 of 43 studies in Tables 1, 2 and 3). to compete will depend on the accumulation of sucient
Corals can inhibit algal growth (de Ruyter van Steven- biomass to overgrow corals (Miller and Hay 1996, 1998).
inck et al. 1988b; McCook 2001) or even overgrow and However, it is also noteworthy that algal replacement
kill the algae (e.g. Meesters and Bak 1993; Meesters of corals does not necessarily require reductions in her-
et al. 1994, 1997). Algae may have no e€ects or even bivory (various papers in Table 3). The area occupied by
positive e€ects on corals (Jompa and McCook 1998; algae can increase dramatically and rapidly in response
Heyward and Negri 1999) and overgrowth may not lead to coral death without signi®cant changes in herbivory
to coral death. Many areas experience seasonal blooms (e.g. Williams 1986 for crown of thorns star®sh damage,
of ephemeral brown algae (e.g. Dictyota, Hydroclathrus, Diaz-Pulido and McCook unpublished data for coral
Chnoospora, Colpomenia) which entangle and overgrow bleaching). The role of substrate availability is signi®-
corals for weeks to months, without causing signi®cant cant in the context of the relative roles of nutrients and
harm to the coral population (Coles 1988, personal herbivory during phase shifts (Lapointe 1997; Hughes
observations). Competitive superiority is by no means et al. 1999). Although herbivores may control algal
®xed: turf algae may be both aggressive to or overgrown abundance in terms of biomass per unit area, area oc-
by live corals (Potts 1977 c.f. Fishelson 1973; Bak et al. cupied is also controlled by disturbance and competitive
1977) and may exclude or be overgrown by coral recruits inhibition by corals. Nutrients can only a€ect algal
under di€erent circumstances (Littler and Littler 1997a). growth, which may or may not accumulate as increased
Crustose corallines appear relatively invasive and ag- biomass, depending on herbivory rates. Herbivory can
gressive to corals (Table 4), but may also facilitate coral only a€ect algal standing crop or biomass (per unit ar-
settlement (Heyward and Negri 1999). ea), although this may lead to changes in algal area by
In particular, evidence for algal overgrowth as the increased vegetative or sexual colonisation. Substrate
direct cause of coral mortality is very limited. Algal re- availability, determined by competitive inhibition by
placement may be confounded with algal competitive corals and disturbance, will a€ect algal areal abundance,
superiority at the scales of both populations and polyps with potential subsequent competitive e€ects on coral
(previous sections). Coral mortality for any reason is recovery (Miller 1998; McCook 1999).
generally followed by colonisation by algal turfs, indi- The geographic coverage of the evidence is patchy,
cating that corals widely inhibit algal cover. Where algae even if observational and correlational studies are in-
are found overgrowing dead coral (polyps or popula- cluded. Studies from the Caribbean are prevalent (27+3
tions), it cannot be assumed that the algae are the cause, from temperate west Atlantic), with a few from the Paci®c
not simply the consequence, of coral mortality (without (10), GBR (4), Red Sea/Arabian Sea/Gulf (6), and a single
experimental evidence, e.g. Hughes 1989; Coyer et al. study from Japan. We found only three relevant studies
412

from the Indian Ocean and none from Southeast Asia, are the limiting resources for which corals and algae
where coral diversity is greatest. Even within the regions compete (Carpenter 1990), since other resources, such as
covered, a few speci®c locations dominate (e.g. Discovery nutrients, are unlikely to be signi®cantly depleted by
Bay, Jamaica). Notwithstanding the various limitations competitors. There are six distinct mechanisms, listed in
of the data, there is no indication of geographic di€erences Table 5, by which algae are able to directly compete with
in the nature of coral±algal interactions. corals for space or light. A number of studies refer to
Taxonomic coverage is inevitably very limited, but, energetic or metabolic costs of interactions as a
more critically, a large proportion of studies do not competitive process (leading to e.g. reduced growth or
specify the competitors, even to functional groups (none reproduction), but we consider these costs are actually
of the studies reviewed noted lodging of herbarium consequences of the interaction, not a kind of competi-
specimens of algal taxa involved). Thus only a few, tion. Although not discussed here, it is worth emphas-
limited generalisations about the variability in processes ising that corals and algae may have numerous indirect
or mechanisms of interactions are possible. e€ects on each other. Such e€ects may increase the
In general, few algal taxa appear able to actually impact of the interaction (e.g. sediment trapping shown
overgrow healthy corals by direct contact. Records of in Fig. 1E).
overgrowth predominantly involve Lobophora (Fig. 1A, Clearly, di€erent species of coral and algae will be
B), Dictyota, Halimeda, Dictyosphaeria and crustose di€erently capable of, or susceptible to, the di€erent
coralline algae, as well as a few speci®c, ®lamentous red mechanisms listed in Table 5, depending on factors such
algae (Table 4). However, this may simply re¯ect the as size, structure, shape, growth form, growth patterns,
relative abundance of these taxa, since the ®rst three polyp and tentacle size, and sexual and vegetative re-
genera are particularly abundant in the Caribbean (refs. productive mechanisms, as well as environmental factors
in Diaz-Pulido and Diaz 1997). With the exceptions of a such as nutrients, herbivory and light levels. Where
few, apparently allelopathic species (Littler and Littler feasible, coral±algal interactions should therefore be
1997b; Fig. 1D) and of blue-green algae that induce considered on a case by case basis, and this approach
coral diseases (e.g. Antonius 1988), we propose that ®l- may be e€ective where a few key species are especially
amentous algae and large, leathery algae can rarely important. For example, on Caribbean reefs, interac-
colonise healthy coral tissue, and that observations of tions between a limited set of corals (e.g. Montastrea
such overgrowth often result from prior coral injury or spp., e.g. M. annularis, Agaricia agaricites, Acropora
death. tenuifolia, Acropora palmata and Porites astreoides) and
algae (e.g. Dictyota spp., Lobophora variegata and Hal-
imeda spp., e.g. H. opuntia) may account for most of the
Mechanisms of competitive inhibition signi®cant interactions in terms of shifts in reef status.
between corals and algae Overall, however, a species-by-species (or even genus-
by-genus) approach is unlikely to yield e€ective sum-
Few studies have explicitly considered the mechanisms mary of the possible interactions, for several reasons.
or processes by which algae and corals compete, beyond Firstly, the enormous species (or genus) diversity of both
widespread reference to ``overgrowth'' or ``metabolic corals and algae (approx. 330 and 500 spp. respectively
costs''. These processes will inevitably vary with for the GBR) means that a species-by-species (or even
circumstances such as disturbance history, herbivory, genus-by-genus) approach is simply not practical. Fur-
nutrients, etc., and especially with the life history and ther, some species of both corals and algae have highly
structure of both corals and algae. A coral competing plastic growth forms with distinctly di€erent competitive
for space on a reef will be subject to very di€erent potential (e.g. Lobophora, an alga widely important in
stresses in response to overgrowth by a creeping, foliose coral overgrowth, may have crustose, creeping, leafy or
alga (e.g. Lobophora; Fig. 1A, B) or a large, canopy- upright, bushy habits, depending on grazing regimes,
forming alga (e.g. Sargassum species with a small at- etc: de Ruyter van Steveninck et al. 1988a; Littler et al.
tachment holdfast and no vegetative dispersal; Fig. 1C). 1989; Diaz-Pulido and Bula-Meyer 1997). Finally, many
The ability of corals to compete with algae also varies species of algae are impractical to identify and quantify
signi®cantly among coral life forms. Hughes (1989) at relevant scales for ecological studies, since they occur
observed that encrusting or platelike (foliose) Agaricia as assemblages (e.g. turfs), rather than as clearly
was more susceptible to algal smothering than massive distinguishable taxa.
colonies (also Shulman and Robertson 1996). We propose that algal e€ects on corals can be e€ec-
As a ®rst step toward a framework for understanding tively considered in terms of algal functional groups,
the variability in mechanisms of these interactions, we based on those of Littler (1980), Littler and Littler
list the possible processes by which algae can inhibit (1984) and Steneck and Dethier (1994), and coral life
corals and vice versa (Table 5, derived from Schoener forms (de Vantier 1986). By considering each combina-
1983; Carpenter 1990; Lang and Chornesky 1990; Olson tion of algal functional group and coral life form, a
and Lubchenco 1990; Karlson 1999), and then consider limited subset of the six mechanisms can be seen to be
the circumstances under which these processes can take possible or likely (Table 6). This interaction matrix
place (Table 6). It can be assumed that space and light provides a preliminary but useful basis for structuring
 413

Table 5 Mechanisms for competition between corals and algae. Adapted from Schoener (1983); Carpenter (1990), Olson and Lubchenco
(1990), Lang and Chornesky (1990) and Karlson (1999), modi®ed for corals and algae speci®cally

Algal inhibition of corals Coral inhibition of algae Includes: Categories

Overgrowth Overgrowth Smothering; Direct, interference, overgrowth (Fig. 1A, B)

Shadinga Shading Overtopping; Indirect, exploitative, consumptive (Fig. 1C)
Abrasion Abrasion Whiplashb; Direct, interference, encounter
Stinging, etc. including sweeper tentacles Direct, interference, encounter
and polyps, mesenterial
®laments
Chemicalc Chemical Allelopathy Direct, interference, chemical (Fig. 1D?)
Pre-emption/ Space pre-emption Direct, exploitative, consumptive
Recruitment barrierd
Epithelial sloughinge Mucus secretion Defensive mechanism
a d
Shading or overtopping may include establishment of dense Canopy-forming macrophytes will actually occupy little of the
canopy, with numerous e€ects on the chemical and physical con- substrate, but may still form an e€ective barrier to coral settlement
e
ditions, hydrodynamics, etc Epithelial sloughing and mucus secretion are defence mechanisms
b
Whiplash, often cited as damaging corals, will generally also be against epibiotic colonisation, rather than mechanisms for expan-
very detrimental to the softer algal tissue sion (Lang and Chornesky 1990; Littler and Littler 1999; personal
c
Allelopathic chemical e€ects have been demonstrated on soft observations)
corals (de Nys et al. 1991) and hard corals (Littler and Littler
1997b); see our Fig. 1D

the variability in e€ects of algae on corals, with several are apparently signi®cant qualitative di€erences among
immediate general implications. For example, a com- algal groups in terms of their potential competitive
parison of the variation between algal groups (rows) and interactions. Thus research into algal overgrowth of
between coral life forms (columns) in Table 6 suggests corals would bene®t from more detailed identi®cation
that potential competitive processes are more dependent and description of the algae, at least to functional
on the properties of the algae than the corals. There groups.

Table 6 Matrix of competitive interaction mechanisms by func- representative not exhaustive, and amount to hypotheses, not lit-
tional group and life form. Proposed mechanisms for algal e€ects erature review. O Overgrowth; S shading; A abrasion; C chemical;
on corals, based on algal functional group (as for Table 1) and P pre-emption; R recruitment barrier; Sl epithelial sloughing; ± no
coral life forms. Each cell contains two rows, top row indicating the mechanism applicable. Superscripts indicate references for exam-
competitive mechanisms we propose are probable or common ples; * indicates mechanisms suggested by our own observations or
processes, second (italicised) row indicating processes we suggest unpublished data
occur but are less important or common; entries are intended to be
Algal functional groups Coral life forms

Branching Digitate Tabulate Encrusting Foliose Massive Mushroom Recruits

Microalgae O1 ; C 2 O; C2 O; C2 O; C2 O*; C O3,4, C ± O; C

± ± ± ± ± ± O; C ±
Filamentous ± ± ± ± ± ± ± O12
O1,5,6,7,8,9; C* O; C10 O; C O; C O11; C O8,11; C ± S; A; C
Foliose ± ± ± O O ± ± O; S; P
O14,15 O O ± ± O O16 ±
Upright corticated ± ± ± O O17,19,20 O17,19 ± O; S; P17,22
foliose O7,17,18; A6 O; A O ± A A O21; A21 ±
Creeping corticated O7,18 ± ± O* O17,19 ± ± O; S; P17
foliose ± O O* ± ± O8,17,19,24 O ±
Corticated macrophytes ± ± ± A A A A O; A; P/R22
O23; A A A O O19 O19 O ±
Leathery macrophytes S6 S*; S*; S*; A S*; A S*; A* S* R; A
O9,23; A6 A A* O* O* ±
Articulated calcareous ± ± ± O ± ± ± O; S; P24
O8,9 O O ± O17 O8,17 O
Crustose O18,25,26; ± ± O ± ± ± O12; Sl28
S25,26 O O ± O O26,27 O16 ±
1
Littler and Littler (1997a); 2Antonius (1988); 3Kuta and Rich- 15
Smith et al. (1981); 16Chadwick (1988); 17Hughes (1996);
ardson (1997); 4Santavy and Peters (1997); 5Potts (1977); 6Miller 18
Hughes et al. (1987); 19Lewis (1986); 20Shulman and Robertson
and Hay (1996); 7Stachowicz and Hay (1999); 8Goreau (1992); (1996); 21Coyer et al. (1993); 22Steneck (1994); 23Crossland (1981);
9
Tanner (1995); 10Littler and Littler (1997b); 11Sammarco (1980); 24
Hughes (1994); 25Finckh (1904); 26James et al. (1988); 27Keats
12
Bak and Engel (1979); 13Birkeland (1977); 14Banner (1974); et al. (1997); 28Littler and Littler (1999)
414

In contrast, comparison of the coral life forms sug- sive standing crops of ephemeral algae may accumulate
gests that the di€erences between adult life forms are (e.g. Banner 1974; Genin et al. 1995). These may create
largely quantitative: similar mechanisms are involved, chemical and physical conditions (Ra€aelli et al. 1998)
but di€erent life forms are more or less vulnerable. For for underlying corals that are not indicated by the
example, massive corals may be more vulnerable than functional group of the component algal taxa. Similarly,
branching corals to whiplash by larger algal fronds, algae may often interact with corals as complex assem-
since the algae may become entangled in a branching blages of taxonomically and structurally diverse algae,
coral, resulting in more damage to the algae than the rather than as distinct taxa or functional groups. Ex-
coral. Within life forms, there is also likely to be con- amples of such assemblages include closely adherent
siderable quantitative variation with both colony size creeping mats (0.2±1 cm thick), tough, interwoven, turf
and polyp size. Larger colonies are less liable to over- mats (2±10 cm thick), thick tangles of more delicate
growth or shading, and corals with larger polyps (or ephemerals (20±50 cm thick), and distinct algal cano-
tentacles) may generally be able to better defend them- pies (10±200 cm high). In such cases it may be more
selves against algae. Importantly, however, there are appropriate to describe the assemblage than the com-
considerable qualitative di€erences between adult life ponent algae. Algal assemblage canopy height at least
forms (collectively) and coral recruits. Coral recruits should be estimated and reported.
appear vulnerable to more forms of algal competition In terms of structuring the potential e€ects of corals
than established corals. on algae, coral polyp and tentacle size and colony size
The di€erent combinations of interaction type and appear important, whereas we found the functional
functional groups will have distinctly di€erent conse- form/life form approach was less successful. Coral life
quences for the viability of coral populations. Few corals form does in¯uence competitive ability and some gen-
will survive direct overgrowth by creeping, prostrate eralisations are possible. For example, tabulate corals
algae, whereas many could adapt to shading by canopy- will be more likely to shade competitors than encrusting
forming leathery algae, or could increase mucus pro- or massive taxa (Hughes 1989). However, several of the
duction to shed recruiting ®laments. Algal impacts on mechanisms by which corals a€ect competitors (Table 5)
coral recruits may have severe consequences for the are not related to life form, but to polyp and tentacle
long-term maintenance of sustainable coral populations, size, which may vary considerably within groups. The
even where the algae have little impact on adult corals ability of coral recruits to settle on and overgrow dif-
(previous section). ferent algal groups (crusts and turfs especially) will be
We emphasise that Table 6 is not intended as com- important. The more complex matrix required to orga-
plete or ®nal, but as an initial attempt to organise the nise these e€ects is beyond the scope of this review.
possible variability in the interaction. The lists indicate Corals will also have important indirect e€ects on algae,
which processes we consider conceptually relevant to a including in particular the provision of habitat for
particular combination of coral and algal types, with herbivorous ®shes.
illustrations from the literature where possible. The
paucity of detailed research means that many of the
possible combinations have not been documented and Conclusions
Table 6 is not a literature summary. Entries are intended
to be generally relevant, rather than exhaustive, and In summary, there is surprisingly little known about the
exceptions will occur. There are also several limitations causality and processes by which corals and algae in-
to a scheme based on functional groups and life forms teract, especially about the e€ects of algae on corals.
(Table 6). It does not directly incorporate the variation There is little experimental evidence available, and most
due to coral colony size or polyp size, nor the supply- evidence is correlative or based on simple observations.
side ecology of both algae and corals. For example, an The weight of that evidence suggests that competition
algal canopy may serve as a barrier to release and set- between algae and corals is widespread on coral reefs,
tlement of broadcast spawning corals, but have little and largely mediated by herbivory. However, there is
impact on recruitment of corals which brood planula little evidence that where algae have replaced corals,
larvae. Algal ability to colonise or overgrow corals will algae are generally the cause, and not simply the
be enhanced for taxa which can spread and attach veg- consequence, of coral mortality.
etatively, or which have wide dispersal and rapid Research into coral±algal interactions, especially al-
growth. In contrast, algae that require large size and gal overgrowth of corals, will bene®t from more explicit
sexual reproduction for dispersal, or have limited dis- consideration of the mechanisms by which the organ-
persal distances (e.g. some species of Sargassum) will isms interact, and the properties that in¯uence those
have limited opportunity to colonise substrate made interactions. The potential impacts of algal overgrowth
available by disturbances. Such properties are only on recruiting corals deserve particular attention, as they
partly accounted for by the functional groupings. may be critical to coral population viability. There is a
Algal functional groups may also be inadequate need for improved description of algal competitors,
summaries of algal properties under some competitive particularly their taxonomy (as far as feasible) and
circumstances. During algal blooms or outbreaks, mas- structure including functional group, but ideally in-
 415

cluding indications of standing crop and canopy struc- de Nys R, Coll JC, Price IR (1991) Chemically mediated interac-
ture (e.g. height). The consequences of this emphasis tions between the red alga Plocamium hamatum (Rhodophyta)
and the octocoral Sinularia cruciata (Alcyonacea). Mar Biol
would include more meaningful understanding of the 108: 315±320
processes taking place, their variability, and hence their de Ruyter van Steveninck ED, Bak RPM (1986) Changes in
consequences in terms of severity of impact, and long- abundance of coral-reef bottom components related to mass
term community structure. This understanding should in mortality of the sea urchin Diadema antillarum. Mar Ecol Prog
Ser 34: 87±94
turn improve our ability to interpret, predict and man- de Ruyter van Steveninck ED, Kamermans P, Breeman AM
age ``phase shifts'' in which abundant corals are replaced (1988a) Transplant experiments with two morphological
by algae (McCook 1999), with severe ecological, envi- growth forms of Lobophora variegata (Phaeophyceae). Mar
ronmental, and economic consequences. Ecol Prog Ser 49: 191±194
de Ruyter van Steveninck ED, Van Mulekom LL, Breeman AM
Acknowledgements We thank T. Hughes, A. Szmant, M. Miller, J. (1988b) Growth inhibition of Lobophora variegata (Lamou-
Tanner, T. Done, J. Skeat and two reviewers for discussion and roux) Womersley by scleractinian corals. J Exp Mar Biol Ecol
comments on the manuscript, and I.R. Price for assistance with 115: 169±178
algal identi®cations (Fig. 1). This is contribution number 1045 from de Vantier LM (1986) Studies in the assessment of coral reef eco-
the Australian Institute of Marine Science, supported by the Co- systems. In: Brown BE (ed) Human induced damage to coral
operative Research Centre for the Ecologically Sustainable De- reefs. UNESCO Rep Mar Sci 40: 99±111
velopment of the Great Barrier Reef, an AusAid fellowship to J.J. Diamond J (1986) Overview: laboratory experiments, ®eld
and Instituto Colombiano para el Desarrollo de la Ciencia y la experiments and natural experiments. In: Diamond J, Case TJ
TecnologõÂ a (Colciencias) fellowship to G.D.-P. (eds) Community ecology. Harper and Row, New York, pp 3±22
Diaz-Pulido G, Diaz JM (1997) Algal assemblages in lagoonal reefs
of Caribbean oceanic atolls. In: Proc 8th Int Coral Reef Symp
Publ 1, pp 827±832
References Diaz-Pulido G, Bula-Meyer G (1997) Marine algae from oceanic
atolls in the southwestern Caribbean (Albuquerque Cays,
Antonius A (1988) Black band disease behavior on Red Sea reef Courtown Cays, Serrana Bank, and Roncador Bank). Atoll Res
corals. In: Proc 6th Int Coral Reef Symp Publ 3, pp 145±150 Bull 448: 1±18
Antonius A (1999) Metapeyssonnelia corallepida, a new coral-kill- Done TJ (1992) Phase shifts in coral reef communities and their
ing red alga on Caribbean reefs. Coral Reefs 18: 301 ecological signi®cance. Hydrobiologica (The ecology of man-
Bak RPM, Engel MS (1979) Distribution, abundance and survival grove and related ecosystems) 247: 121±132
of juvenile hermatypic corals (Scleractinia) and the importance Finckh AE (1904) Section VI. Biology of the reef forming organ-
of life history strategies in the parent coral community. Mar isms at Funafuti Atoll. In: The atoll of Funafuti. Royal Society
Biol 54: 341±352 of London, London, pp 125±150
Bak RPM, Brouns JJWM, Heys FML (1977) Regeneration and Fishelson L (1973) Ecological and biological phenomena in¯u-
aspects of spatial competition in the scleractinian corals Agar- encing coral-species composition on the reef tables at Eilat
icia agaricites and Montastrea annularis. In: Proc 3rd Int Coral (Gulf of Aqaba, Red Sea). Mar Biol 19: 183±196
Reef Symp Publ 1, pp 143±148 Fitz HC, Reaka ML, Wolf NG (1983) Coral recruitment at mod-
Banner AH (1974) Kaneohe Bay, Hawaii: urban pollution and a erate depths: the in¯uence of grazing. In: Reaka ML (ed) The
coral reef ecosystem. In: Proc 2nd Int Coral Reef Symp Publ 2, ecology of deep and shallow coral reefs. Symposia Series for
pp 685±702 Undersea Research. NOA's Undersea Research Program,
Benayahu Y, Loya Y (1981) Competition for space among coral Washington, pp 89±96
reef sessile organisms at Eilat, Red Sea. Bull Mar Sci 31: Genin A, Lazar B, Brenner S (1995) Vertical mixing and coral
514±522 death in the Red Sea following the eruption of Mount Pina-
Birkeland C (1977) The importance of rate of biomass accumula- tubo. Nature 377: 507±510
tion in early successional stages of benthic communities to the Goreau TJ (1992) Bleaching and reef community change in
survival coral recruits. In: Proc 3rd Int Coral Reef Symp Publ 1, Jamaica: 1951±1991. Am Zool 32: 683±685
pp 15±21 Hatcher BG (1983) Grazing in coral reef ecosystems. In: Barnes DJ
Carpenter RC (1990) Competition among marine macroalgae: a (ed) Perspectives on coral reefs. Brian Clouston, Canberra,
physiological perspective. J Phycol 26: 6±12 pp 164±179
Carpenter RC (1997) Invertebrate predators and grazers. In: Hay ME, Taylor PR (1985) Competition between herbivorous
Birkeland C (ed) Life and death of coral reefs. Chapman and ®shes and urchins on Caribbean reefs. Oecologia 65: 591±598
Hall, New York, pp 198±229 Heyward AJ, Negri AP (1999) Natural inducers for coral larval
Chadwick NE (1988) Competition and locomotion in a free-living metamorphosis. Coral Reefs 18: 273±279
fungiid coral. J Exp Mar Biol Ecol 123: 189±200 Hughes TP (1989) Community structure and diversity of coral
Coles SL (1988) Limitations on reef coral development in the reefs: the role of history. Ecology 70: 275±279
Arabian Gulf: temperature or algal competition? In: Proc 6th Hughes TP (1994) Catastrophes, phase-shifts and large-scale
Int Coral Reef Symp Publ 3, pp 211±216 degradation of a Caribbean coral reef. Science 265: 1±23
Connell JH (1983) On the prevalence and relative importance of Hughes TP (1996) Demographic approaches to community
interspeci®c competition: evidence from ®eld experiments. Am dynamics: a coral reef example. Ecology 77: 2256±2260
Nat 122: 661±696 Hughes TP, Reed DC, Boyle M-J (1987) Herbivory on coral reefs:
Connell JH, Hughes TP, Wallace CC (1997) A 30 year study of community structure following mass mortalities of sea urchins.
coral abundance, recruitment, and disturbance at several scales J Exp Mar Biol Ecol 113: 39±59
in space and time. Ecol Monogr 67: 461±488 Hughes TP, Szmant AM, Steneck RS, Carpenter R, Miller S (1999)
Coyer JA, Ambrose RF, Engle JM, Carroll JC (1993) Interactions Algal blooms on coral reefs: what are the causes? Limnol
between corals and algae on a temperate zone rocky reef: Oceanogr 44: 1583±1586
mediation by sea urchins. J Exp Mar Biol Ecol 167: 21±37 Hunter CL, Evans CW (1994) Reefs in Kaneohe Bay, Hawaii: two
Crossland CJ (1981) Seasonal growth of Acropora cf. formosa and centuries of western in¯uence and two decades of data. In:
Pocillopora damicornis on a high latitude reef (Houtman Ab- Ginsburg RN (compiler) Proc Conf on The Colloquium on
rolhos, Western Australia). In: Proc 4th Int Coral Reef Symp Global Aspects of Coral Reefs: Health, Hazards, and History,
Publ 1, pp 663±668 University of Miami, Miami, pp 339±345
416

James NP, Wray JL, Ginsburg RN (1988) Calci®cation of encrusting Meesters EH, Bak RPM (1993) E€ects of coral bleaching on tissue
aragonite algae (Peyssonneliaceae): implications for the origin of regeneration potential and colony survival. Mar Ecol Prog Ser
late Paleozoic reefs and cements. J Sediment Petrol 58: 291±303 96: 189±198
Jompa J, McCook LJ (1998) Seaweeds save the reef?!: Sargassum Meesters EH, Noordeloos M, Bak RPM (1994) Damage and re-
canopy decreases coral bleaching on inshore reefs. Reef Res 8:5 generation: links to growth in the reef-building coral Montas-
Karlson RH (1999) Dynamics of coral communities. Kluwer, trea annularis. Mar Ecol Prog Ser 112: 119±128
Dordrecht Meesters EH, Pauchli W, Bak RPM (1997) Predicting regeneration
Kaufman L (1977) The three spot damsel®sh: e€ects on benthic of physical damage on a reef-building coral by regeneration
biota of Caribbean coral reefs. In: Proc 3rd Int Coral Reef capacity and lesion shape. Mar Ecol Prog Ser 146: 91±99
Symp Publ 1, pp 559±564 Miller MW (1998) Coral/seaweed competition and the control of
Keats DW, Chamberlain YM, Baba M (1997) Pneophyllum coni- reef community structure within and between latitudes. Ocea-
cum (Dawson) comb nov. (Rhodophyta, Corallinaceae), a nogr Mar Biol Annu Rev 36: 65±96
widespread Indo-Paci®c non-geniculate coralline algae that Miller MW, Hay ME (1996) Coral±seaweed±grazer±nutrient
overgrows and kills live coral. Bot Mar 40: 263±279 interactions on temperate reefs. Ecol Monogr 663: 323±344
Kinsey DW (1988) Coral reef system response to some natural and Miller MW, Hay ME (1998) E€ects of ®sh predation and seaweed
anthropogenic stresses. Galaxea 7: 113±128 competition on the survival and growth of corals. Oecologia
Kuta KG, Richardson LL (1997) Black band disease and the fate 113: 231±238
of diseased coral colonies in the Florida Keys. In: Proc 8th Int Morrissey J (1980) Community structure and zonation of macro-
Coral Reef Symp, pp 575±578 algae and hermatypic corals on a fringing reef ¯at of Magnetic
Lang JC, Chornesky EA (1990) Competition between scleractinian Island (Queensland, Australia). Aquat Bot 8: 91±139
reef corals ± a review of mechanisms and e€ects. In: Dubinsky Z Olson AM, Lubchenco J (1990) Competition in seaweeds: linking
(ed) Ecosystems of the world, vol 25. Coral reefs. Elsevier, plant traits to competitive outcomes. J Phycol 26: 1±6
Amsterdam, pp 209±252 Potts DC (1977) Suppression of coral populations by ®lamentous
Lapointe BE (1989) Caribbean coral reefs: are they becoming algal algae within damsel®sh territories. J Exp Mar Biol Ecol 28:
reefs? Sea Front 35: 84±91 207±216
Lapointe BE (1997) Nutrient thresholds for bottom-up control of Ra€aelli DG, Raven JA, Poole LJ (1998) Ecological impact of green
macroalgal blooms on coral reefs in Jamaica and southeast macroalgal blooms. Oceanogr Mar Biol Annu Rev 36: 97±125
Florida. Limnol Oceanogr 42: 1119±1131 Rogers CS, Garrison V, Grober-Dunsmore R (1997) A ®shy story
Lewis SM (1986) The role of herbivorous ®shes in the organization about hurricanes and herbivory: seven years of research on a
of a Caribbean reef community. Ecol Monogr 56: 183±200 reef in St. John, US Virgin Islands. In: Proc 8th Int Coral Reef
Liddell WD, Ohlhorst SL (1986) Changes in benthic community Symp Publ 1, pp 555±560
composition following the mass mortality of Diadema at Russ GR (1987) Is rate of removal of algae by grazers reduced
Jamaica. J Exp Mar Biol Ecol 95: 271±278 inside territories of tropical damsel®shes? J Exp Mar Biol Ecol
Lirman D (2001) Competition between macroalgae and corals: 110: 1±17
e€ects of increased algal biomass on the survivorship and growth Sammarco PW (1980) Diadema and its relationship to coral spat
of the Caribbean corals Siderastrea siderea, Porites astreoides, mortality: grazing, competition, and biological disturbance.
and Montastrea faveolata. Coral Reefs (in press) J Exp Mar Biol Ecol 45: 245±272
Littler MM (1980) Morphological form and photosynthesis per- Sammarco PW (1982) Echinoid grazing as a structuring force in
formances of marine macroalgae: tests of a functional/form coral communities: whole reef manipulations. J Exp Mar Biol
hypothesis. Bot Mar 22: 161±165 Ecol 61: 31±55
Littler MM, Littler DS (1984) Models of tropical reef biogenesis: Sammarco PW, Carleton JH (1981) Damsel®sh territoriality and
the contribution of algae. Prog Phycol Res 3: 323±363 coral community structure: reduced grazing, coral recruitment,
Littler MM, Littler DS (1997a) Disease-induced mass mortality of and e€ects on coral spat. In: Proc 4th Int Coral Reef Symp Publ
crustose coralline algae on coral reefs provides rationale for the 2, pp 525±536
conservation of herbivorous ®sh stocks. In: Proc 8th Int Coral Santavy DL, Peters EC (1997) Microbial pests: coral disease in the
Reef Symp Publ 1, pp 719±724 western Atlantic. In: Proc 8th Int Coral Reef Symp Publ 1,
Littler DS, Littler MM (1997b) Epizoic red alga allelopathic (?) to a pp 607±612
Caribbean coral. Coral Reefs 16: 168 Schoener TW (1983) Field experiments on interspeci®c competi-
Littler MM, Littler DS (1999) Epithallus sloughing: a self-cleaning tion. Am Nat 122: 240±285
mechanism for coralline algae. Coral Reefs 18: 204 Sheppard CRC (1988) Similar trends, di€erent causes: responses of
Littler DS, Littler MM, Bucher KE, Norris JN (1989) Marine corals to stressed environments in Arabian seas. In: Proc 6th Int
plants of the Caribbean: a ®eld guide from Florida to Brazil. Coral Reef Symp Publ 3, pp 297±302
Smithsonian Institution Press, Washington Shulman MJ, Robertson DR (1996) Changes in the coral reefs of
McArdle BH (1996) Levels of evidence in studies of competition, San Blas, Caribbean, Panama: 1983 to 1990. Coral Reefs 15:
predation, and disease. N Z J Ecol 20: 7±15 231±236
McCook LJ (1996) E€ects of herbivores and water quality Smith SV, Kimmerer WJ, Laws EA, Brock RE, Walsh TW (1981)
on the distribution of Sargassum on the central Great Kaneohe Bay sewage diversion experiment: perspectives on
Barrier Reef: cross-shelf transplants. Mar Ecol Prog Ser 139: ecosystem responses to nutritional perturbation. Pac Sci 35:
179±192 279±385
McCook LJ (1997) E€ects of herbivory on zonation of Sargassum Stachowicz JJ, Hay ME (1999) Mutualism and coral persistence:
spp. within fringing reefs of the central Great Barrier Reef. Mar the role of herbivore resistance to algal chemical defense.
Biol 129: 713±722 Ecology 80: 2085±2101
McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral Steneck RS (1988) Herbivory on coral reefs: a synthesis. In: Proc
reefs: scienti®c issues and management consequences for the 6th Int Coral Reef Symp Publ 1, pp 37±49
Great Barrier Reef. Coral Reefs 18: 357±367 Steneck RS (1994) Is herbivore loss more damaging to reefs than
McCook LJ (2001) Competition between coral and algal turfs hurricanes? Case studies from two Caribbean reef systems
along a gradient of terrestrial runo€ in the nearshore central (1978±1988). In: Ginsburg RN (ed) Proc Conf on The Collo-
Great Barrier Reef. Coral Reefs (this issue) quium on Global Aspects of Coral Reefs: Health, Hazards, and
McCook LJ, Price IR, Klumpp DW (1997) Macroalgae on the History, University of Miami, Miami, pp 220±226
GBR: causes or consequences, indicators or models of reef Steneck RS, Dethier MN (1994) A functional group approach
degradation? In: Proc 8th Int Coral Reef Symp Publ 2, to the structure of algal-dominated communities. Oikos 69:
pp 1851±1856 476±498
 417

Stimson J, Larned S, McDermid K (1996) Seasonal growth of the van Den Hoek C, Breeman AM, Bak RPM, G Van Buurt (1978)
coral reef macroalga Dictyosphaeria cavernosa (Forskal) The distribution of algae, corals and gorgonians in relation to
Borgesen and the e€ects of nutrient availability, temperature depth, light attenuation, water movement and grazing pressure
and herbivory on growth rate. J Exp Mar Biol Ecol 196: 53±77 in the fringing coral reef of Curacao, Netherlands Antilles.
Strong DR, Simberlo€ D, Abele LG, Thistle AB (1984) Ecological Aquat Bot 5: 1±46
communities: conceptual issues and the evidence. Princeton van Woesik R (1998) Lesion healing on massive Porites spp. corals.
University Press, Princeton Mar Ecol Prog Ser 164: 213±220
Tanner JE (1995) Competition between scleractinian corals and Vine PJ (1974) E€ects of algal grazing and aggressive behaviour of
macroalgae: an experimental investigation of coral growth, the ®shes Pomacentrus lividus and Acanthurus sohal on coral-
survival and reproduction. J Exp Mar Biol Ecol 190: 151± reef ecology. Mar Biol 24: 131±136
168 Williams DM (1986) Temporal variation in the structure of the reef
Umar J, McCook LJ, Price IR (1998) E€ects of sediment deposi- slope ®sh communities (central Great Barrier Reef): short-term
tion on the seaweed Sargassum on a fringing coral reef. Coral e€ects of Acanthaster planci infestation. Mar Ecol Prog Ser 28:
Reefs 17: 169±177 157±164
Underwood AJ (1986) The analysis of competition by ®eld exper- Wittenberg M, Hunte W (1992) E€ects of eutrophication and
iments. In: Kikkawa J, Anderson DJ (eds) Community ecology: sedimentation on juvenile corals. I. Abundance, mortality and
pattern and process. Blackwell, Oxford, pp 240±268 community structure. Mar Biol 112: 131±138