.50/0
P.S.Z.N. I: Marine Ecology, 17 (1-3): 399-410 (1996)
@ 1996 Blackwell Wissenschafts-Verlag,Berlin
ISSN 0173-9565
Accepted: May 1, 1995
BERNHARDRlEGL & ANDREARlEGL
Institut fur Palaontologie,Geozentmm,AlthanstraBe14,A-I091 Wien, Austria.
(fonnerly: Coastal Ecology Unit, Zoology Department,University of Cape Town, Rondebosch 7700, South Africa)
With 8 figures and I table
Key-words: Episodic disturbance,coral community structure,coral reef, South Africa,
Scleractinia, Alcyonacea,fragmentation,regeneration.
Abstract. Africa's southernmostcoral reefs aresituatedin Natal Province, SouthAfrica. The Natal coast
is exposedto openoceanswells andepisodic storm swell conditions. Benthic communities on thesereefs
differentiated into three community types: shallowreefs (8-18 m) weredominatedby alcyonaceancorals
and low-growing, massive Scleractinia; intermediate reefs (18-25 m) were dominated chiefly by
branching and tabular Scleractinia of the genusAcropora (A. austera,A. clathrata); deepreefs were not
dominated by corals but by sponges.Breakageand recovery experimentsindicated thatthe difference
in Acropora dominance between shallow and intermediate sites was causedby breakagein high swell
conditions. Survival of experimentally produced A. austera fragments was significantly higher in
intermediate than in shallow sites,where higher surge made re-attachmentand regenerationunlikely.
Also, colony morphology was adaptedto differential surge conditions: colonies on the shallow reefs
were smaller with shorterbranches,while on intermediatereefs theywere much bigger with long, widely
spreading branches. EpisodiQ breakage and low fragment survival due to high water-motion thus
excludedbranching corals from shallowreef sites.
Problem
Coral reefs can react very sensitively to disturbances. Severe disturbances, usually
episodic events occurring at long, irregular time intervals, can completely change
the entire coral community by killing all or a large proportion of its corals (HARMELIN-VIVIEN& LABOUTE,1986; DOLLAR & TRIBBLE, 1993). Subsequent recovery
can take place from surviving fragments (HIGHSMITH,1982) or by colonization by
species present in the larval pool.
Smaller-scale disturbances, also episodic but more frequent, are only likely to
damage a portion of the resident corals, without necessarily disadvantaging the
other community members (PORTER& MEIER, 1992; ROBERTSet ai., 1994): Only
individual colonies or species will be affected by mortality (GLADFELTER,1982;
CURRANet ai., 1994) and no community turn-over as after a large-scale disturbance
will be observed. These smaller-scale disturbances can nevertheless also profoundly influence community structure.
U. S. CopyrightClearance
CenterCodeStatement:0173-9565/96/1701 -0399 $
400
RlEGL
& RlEGL
Wave energyhas long beenknown as one of the most important factors controlling reef growth. High wave-energycan do considerabledamageto coral reefs
(DOLLAR,1982; ARONSON
et al., 1994; ROGERS,
1994):
On South African reefs, branching corals are particularly at risk of being damaged by high wave-energy. However, breakage in branching corals needs not
necessarilybe a disadvantage,as many speciesare able to reproduceby fragmentation (HIGHSMrrn,1982). For this strategyto be successful,fragmentationmust not
occur too frequently and wave-actionhas to be low enoughto allow fragmentsto
remain stable until they can re-attach.Otherwise, this episodic disturbancewould
gravely disadvantagethe species.
This paperinvestigatesthe coral community structureof reefs in different depths
and therefore in different wave-exposureregimes (DENNY,1988) in SouthAfrica
and the effects of frequently recurring small-scaledisturbancesby high wave-energy. The impact of high wave-energyon the common, open-arborescently-growing,
branching coral Acropora austera (DANA, 1846) and the importance of episodic
high wave-energyevents on this species'role in community structurewere evaluated.
Material and Methods
1 .Study area
The study area was situated in the Maputaland reef system in northern Natal, South Africa (Fig. 1). The
geomorphology of these reefs deviates from that found on typical coral reefs (RAMSEY& MASON, 1991;
RlEGL et al., 1995). They generally do not reach the surface (minimum depth 6-8 m) and therefore lack
a typical reef crest, do not enclose a lagoon, and have no pronounced reef slope (mostly sloping at less
than 10°). Major topographical features are gullies and associated drop-offs of up to 5 m, dissecting the
reefs in irregular intervals and orientation.
Two types of reef, which developed on two different types of underlying topography, occur: deep,
flat outcrops between 18 and 24 m depth (4-Mile Reef, Kosi Mouth Reef) and typical fossil dunes or
shallow sandstone outcrops, typically reaching from 8 to about 34 m depth (2-Mile Reef, 9-Mile Reef,
Red Sands Reef).
The Maputaland coastline is influenced by the headwaters of the developing Agulhas current,
flowing north-south. Maximum current speed in the area is around 1.5 m .s-l. Surface waters are a
mixture of tropical water from the Mozambique channel and subtropical water from the east (SCHUMANN
& ORREN,1980).
The area is characterized by high swells, predominantly from the south (SCHUMANN& ORREN,1980).
Swells generated in the Southern Ocean reach the reefs. These usually have a long period (around 10 s)
and deepwater wave heights around 2 m, although they may be considerably larger. Swells generated
by cyclones in the Mozambique channel can also reach the area. Strong coastal lows propagating in a
north easterly direction up the coast can create high wind seas and local currents. Superimposed on
ocean swells, wave heights are sufficient to cause shoaling on the shallow reefs (8 m depth). Such
conditions occurred twice in a three-year observational period (1991-1993). Water velocities created
by surge in 20 m depth ranged from 0.07 m .s-1 in calm to over 1 m. s-1 in medium swell conditions
(unpubl. data).
2. Community structure analysis
Quantitative surveys were carried out using the line-transectmethod with continuousrecording of the
intercepts of all organisms and geological features underlying the transectline (LoYA, 1978). Ideal
transect length was established by means of a species-per-areacurve and was found to be at 10 m.
How episodic coral breakagecan detennine community structure
401
MOZAMBIQUE
27"00' 5
T
, 9-Mile Reef
SOUTH AFRICA
/8
4-Mile Reef
1 2-Mile Reef
Red Sands Reef
I
10km
N
J
Fig. 1.The studysites onthe Maputaland reefcomplexesin northernNatal, SouthAfrica. Only thenames
of reefs sampled for this study aregiven.
r'-\,.../"'-~~~L~
402
RlEGL & RIEGL
Therefore, 10-m-1ong line transects were recorded. Series of at least 10 transects, following the depth
contour with one meter spacing between them, were repeatedly recorded at randomly chosen sites. This
was necessary due to the low topographical differentiation of the reefs. Transect depths varied between
8 and 34 m, and 5-7 sample sites were surveyed per reef.
Phototransects, covering areas of 4x10 m each, were taken for control purposes. These provided
further line-transect information. The photograph's scale was determined by using markings on the
transect line, which was visible in each photograph. Coral intercepts on the transect line were measured
using a ruler; the data were then multiplied by the scale of the photographs to estimate the actual
intercept distances.
The intercepts of corals, all other major invertebrate groups such as sponges and ascidians, as well
as sand and unoccupied rock were recorded. Unoccupied rock was defined as lacking macroalgae or
invertebrates.
A total of 171 transects was recorded on five reefs (Fig. 1), and two data sets were produced: one
with quantitative information, indicating the proportional surface cover of each species, and one with
qualitative information, giving only presence/absence data. Quantitative data were standardized by
standard deviation in order to achieve scale independence (DIGBY & KEMPTON,1987) and then subjected
to hierarchical, agglomerative cluster analysis using W ARD'Smethod of linkage. In a second step, the
transects of each locality were pooled and localities were compared. Squared Euclidian distance or the
Correlation Similarity Coefficient was used as distance measure for quantitative pooled data. For
qualitative data, the Binary LANCE-WILUAMS Dissimilarity Coefficient was used (DIGBY & KEMPTON,
1987).
Species diversity was expressed using SHANNON'S
Diversity Index (PiELOU,1975). Prior to statistical
analysis data were tested using KOLMOGOROF-SMIRNOV
tests. Data fulfilled the assumption of normal
distribution; therefore, parametric statistics were used.
3. Morphological characteristics of fragile species
The most commonbranching species(Acropora austera),which appearedto be susceptibleto breakage
and dislocation in high wave-energy conditions, was examined separatelyon three reefs in different
depths and therefore wave-exposure(2-Mile, 4-Mile, 9-Mile Reefs).
Colony size was expressedas colony volume and was calculated by considering the colonies to
occupy arectangular space,which could becalculatedby width times lengthtimes height. Also, average
branch length and branch diameter at the base of brancheswas measured(averagedfrom 10 measurements per colony). The number of unattachedfragments within 50 cm of each colony (this being a
distance within which the fragments could easily be allocated to their colony of origin) was recorded.
4. Field experiment to determine
different reef zones
fragment survival in
Five sites were chosento test the survival of fragments in localities at different depth and therefore
wave-exposure.The sites representedall major environments on the investigatedreefs and differed in
substratumtype, morphology, and coral cover. One shallow,exposedsite (12 m) wassituated on 2-Mile
Reef, where A. austera is rare. It was the dominant community member on 4-Mile Reef, where sites
were at 18 m on a gentle slopeand at 24 m near a ledge on a flat sand plain and in a shallow depression
on a coral carpet.Thesesitesrepresentedenvironmentsof different wave exposure,as water movement
due to wave action decreaseswith depth (DENNY,1988).
A total of 170 fragments was generatedby cutting or chiselling branches off previously unfragmented colonies. The fragments were then placed near each other on the seafloor within five marked
areas(characterizedabove),where they could be recovered.Only healthybranchescovered entirely by
living tissues were cut off. Initially, therefore, only the areas of breakagewere tissue-free. After one
month the fragments were collected and analyzed.The percentageof fragments recovered from each
site was recorded. Surviving tissues were easily identified by their cream to yellow colour, and the
percentageof surviving tissue was estimated.
How episodic coral breakagecan detennine community structure
403
Results
1. Community structure
Benthic communities were dominated by corals (94.6% of total living coverage).
Scleractinia occupied slightly more spacethan Alcyonacea(52.1% versus42.5%);
otherorganismslike spongesand ascidiansonly covered5.4% of the total intercept.
Among the Scleractinia,the Acroporidae had the highestproportional coverage
(16.2% of total scleractinian cover) followed by the Faviidae (13.8%). Among
Alcyonacea,the leathery, low-growing forms in the genera Lobophytum (20.6%)
and Sinularia (16.3%) dominated.
Classification of quantitative data of all transects(unpooled, all sites; Fig. 2)
showed differentiation into two major community types, one dominated by Scleractinia and another dominated by Alcyonacea and other taxa. Within the major
clusters (A and B, Fig. 2), the transectsfrom different reefs did not separateinto
different subclusters.
Cluster A was made up to the greatestpart by transectsfrom 4-Mile Reef. Almost
all transectsin this cluster were from depths greaterthan 15 m, mostly from 18 to
25 m. Two distinct coral communities were representedin this cluster. One group
of transectsfrom gullies was mostly dominated by Montipora speciesand had low
living coverage. A second group of transectswas from flat parts of the reefs and
representeda distinct Acropora-dominated community. The predominant species
were the open arborescentA. austeraand the vasiform A. clathrata.
ClusterB was made up largely by transectsfrom 2-Mile, 9-Mile, and Red Sands
Reefs, most transectsbeing shallowerthan 15 m, excepta group of sponge-dominatedtransectsfrom 25-34 m. The shallow transectswere characterizedby Alcyonacea of the generaSinularia and Lobophytum.The most common Scleractinia in
this cluster were various Faviidae and the vasiform A. clathrata.
Acropora-dominated
(mainly A. Busters)
(18-25 m)
Fig. 2. Classification of all transects. Clusters correspond to community types within defined depth zones.
404
RIEGL & RmGL
Kosi Bay Reef
A
qualitative
Red Sands Reef
= presence/absence
L[
0
5
10
lS
20
9 -Mile
Reef
4 -Mile
Reef
2 .Mile
Reef
25
B
Kosi Bay Reef
= intercept
4 -Mile
Reef
9 -Mile
Reef
2 -Mile
Reef
Red Sands Reef
Fig. 3. Classification of valuespooled for eachsite. A) Qualitative datasetgiving only presence/absence
information on species; B) Quantitative data setgiving total coverage information for eachspecieson
eachreef.
Therefore, four different communitiescould be differentiated: a gully community dominated by Scleractinia (Montipora, Faviidae) in all depths; a community
outside the gullies dominated by Alcyonacea (Lobophytumspp. and Sinularia spp.)
in depthsless than 18 m; a Scleractinia-dominatedcommunity (A. austera,A. clathrata) between 18 and 25 m; a very deep community between 25 and 34 m
predominatedby sponges(20-70% of total living cover).
The comparisonof the pooled datasetsof quantitative as well as qualitative data
showed similar trends (Fig. 3). The pooled values of the medium-deep,flat reefs
between 18 and 25 m (4-Mile and Kosi Mouth Reefs)separatedfrom those on the
shallow and very deepreefs (2-Mile, 9-Mile, Red SandsReefs), reflecting the high
Acropora dominanceexclusive to medium depthareas.
Pooled qualitative data (presence/absence
of species)showed the speciescomposition of mo.streefs to be very similar. Only Kosi Mouth Reef fell outside one
cluster with high similarity, which was due to the exclusive occurrence of two
Acropora (A. horrida, A. palifera).
No significant differences existed between coral species diversity and coral
coverage betweenthe depth groupings 8 to 18 m and 18 to 25 m, but these depth
groupings did differ significantly from that at 25 to 34 m (ANOV A, F = 15.9, df:
2,20; P < 0.001; TuKEYHSD test; Table 1).
How episodic coral breakagecandetermine community structure
405
Table 1. Diversity (SHANNON'S
Index, H') in different depthzones,Pooledvalues from all surveyedreefs.
depth
8-18 m
18-25 m
25-34 m
n transects
89
70
13
diversity (H')
2.09:t 0.30
2.23:t 0.36
1.69:t 0.36
The alcyonaceanspecieswhich dominated in shallow water were also common
on the deeperreefs. The branching A. austera,however, which dominated wide
areasof the deeperreefs was uncommon in the shallow areas.Based on the above
findings, we assumedthat this specieswas excluded from shallow areas by the
higher wave-energyexperiencedthere, which can causebreakageand high mortality. Therefore,this specieswas separatelyevaluatedin shallow and deepareasand
the survival of fragmentswas tested.
2. Morphological characteristics of fragile species
Apart from occupyingmore spacein the community, individual colonies of branching A. austera were bigger (t = -2.12, P < 0.05), more upward oriented, and had
longer branches on the deep4-Mile Reef than on the shallow 2-Mile and 9-Mile
Reefs (ANOV A, F = 22.1, df: 2, 20; P < 0.01).
On the shallow reefs, this specieswas generallyrare and where present,colonies
were smaller, low-growing, and had shorterbranches(averagecolony volume on
4-Mile Reef: 562.7 :t 1075.3 (SO) litres, on 2- and 9-Mile Reefs: 3.5 :t 4.1 (SO)
litres; Figs. 4 & 5). There was a significant positive correlation between branch
depth and colony volume (r2 = 0.60, P < 0.05; Fig. 6); averagebranch length and
maximal branch width also increasedlinearly with depth (r2 = 0.62, P < 0.01; r2 =
0.79, P < 0.01; Figs. 7 & 8). The number of unattachedfragments within 50 cm
radius of colonies also differed significantly betweenthe depths (ANOV A: F =
6.32; df: 2, 20; P < 0.05), increasinglinearly with depth(r2 = 0.84, P < 0.05; Fig. 9).
3. Field experiment to determine fragment survival in
different reef zones
The amountof fragmentsrecoveredafterone monthdiffered dependingon the depth
of the experimentalsites.All fragmentswere lost at the shallow(12 m) stations,53%
were found at the middle (18 m) station, and 82% at the deep (24 m) station.
Overall loss of fragments was clearly depth-dependent.Most fragmentsdid not
remain in the same locality where they were initially depositedbut were moved by
watermotion. None remained in their initial position atthe shallowsite (12 m), 75%
at the middle site (18 m), and 90% at the deepsite (24 m, Fig. 8).
Also, survival rates varied with depth. In the deep (24 m) stations,56% of all
fragments lost up to half of their living tissueswithin one month; 30% lost all their
tissues.If lost fragments were counted as dead,48% of all fragmentshad died. In
the middle (18 m) station,41 % of fragments lost up to 50% of their tissues,while
18%were found dead.Again, if lost specimenswere countedasdead,the total loss
would have been58%. In the shallow (12 m) station,no fragmentswere recovered,
RIEGL & RIEGL
406
Acropora-dominated
community
E
§.
-
.c
C)
c
.!
.c
u
c
m
..
,Q
depth (m)
Fig. 4. Mean differences in averagebranch length (:t: SO) on unbroken colonies between depth zones
pooled from all reefs.
as they were washedoff the reef by wave action. We suspectthat all lost fragments
had died and therefore the total failure to recover any fragment led to assumed
100% mortality.
Discussion
The community studyshoweda clear differentiation of coral communitiesinto four
basic types: a shallow (8-18 m) Alcyonacea- (Lobophytum spp., Sinularia spp.)
dominatedcommunity, a medium-depth(18-25 m) Scleractinia- (Acropora austera,
A. clathrata)dominatedcommunity, and a deep(25-34 m) sponge-dominatedcommunity. A distinct gully community (dominated by Scleractinia, Montipora spp.,
Faviidae) alternatedwith the shallow and the medium-depthcommunities.
The factor causing the differentiation into gully- and non-gully community is
believed to be high sedimentation in the gullies due to resuspendedlocal sand
(RIEGLet al., 1995). The differentiation betweenthe coral-dominated shallow and
medium-depthcommunities and the sponge-dominateddeep community was most
likely caused by different light availability (PORTER
et al., 1985; JOKIEL,1988).
Corals did not appearto receive sufficient light below 28 m depth.
The differentiation betweenthe shallowand medium-depthcommunity is unlikely to be causedby light availability. Coral speciesdiversity and coral coverage in
the medium depth community is as high as in the shallow community. Species
composition is also similar, only branching Acropora, suchas A. austera,are rare
13
How episodic coral breakagecandetennine cornrnunity structure
407
Acropora-dominated
community
depth (m)
Fig. 5. Mean differences in colony volume (:t SD) betweendepthzonespooled from all reefs.
Acropora--dominated
30
community
Alcyonacea-dominated
community
E
.§.
A
i
i
E
I""
A
~"""
""",
..
U
~
u
c
..
~
10
11
15
18
22
depth (m)
Fig. 6. Mean differences in averagemaximum branch diameter (:f: SD) on unbrokencolonies between
depthzonespooled from all reefs.
in the shallows. It is thereforeassumedthat small-scaleepisodicdisturbanceswhich
only disadvantageone dominant speciesare responsiblefor this community differentiation.
A. austera is an aggressiveand efficient spaceutilizer, achievingdominancein
the coral community by rapid linear extension of the skeleton.This leads to rapid
colony growth and overtopping of competitors.Furthermore,this speciesis capable
of reproducing by fragmentation(HIGHSMITH,
1982; WALLACE,1985).
-
16,
RlEOL& RIEGL
408
Acropora -dominated
community
III
C
E
14-
~
12-
Q)
I"
CI
'C
>-
Q)
.c c0
(.)
ca
::ca
c
~
'0
..
Q)
.Q
E
~
c
10-
"0
t)
iQ.
A..:-"",\
81
6~
Alcyonacea-dominated
community
4-'
211
13
15
18
22
depth (m)
Fig. 7. Mean number of unattachedbranches(:t SO) found within 50 cm radius of colonies between
depthzonespooled from all reefs.
100
EJ fragment mortality
~ fragments retrieved
;-
(Q
80
~
3
II
~
1Z
~
iU
t:
60
~
40
;:
0
E
fII
~
m
C
.,
E
g)
~
~
~
3
0
20
~
SO
~
.!.
12
18
21
depth (m)
Fig. 8. Fragmentretrieval and fragment mortality betweenthree experimentalsites at different depths.
Wave energy is a limiting factor in A. austera distribution on the reefs. While
disadvantagingthis coral in shallow water, however, episodic disturbancesmay
benefit this species in deeperwater. On the deeperzones of all surveyed reefs
(18-25 m), A. austera is dominant or amongthe dominant species.In this area it
exhibits all traits typical for an aggressive,well-adapted species. Competitive
strategiesinclude fast growth, aggressiveinteractions,and frequent propagationby
fragmentation. All colonies surveyed on 4-Mi1e Reef had produced unattached
fragments,and numerouscolonies appearedto have resulted from reattachedfragments. Sexualrecruits can be distinguished from asexuallyproducedcolonies by a
different basal attachmentto the substratum(HIGHSMITH,
1982).
Howepisodiccoralbreakagecandeterminecommunitystructure
409
In this depth zone, severe stonns could advantagefragmenting corals such as
A. austera. Drag induced by unusually high water motion is likely to break many
of the long, upward-growing coral branches(DENNY,1988).The breakageexperiment showed high survival chancesof fragments (between50 and 80% in the first
month). The high number of unattachedfragmentsand colonies supportsthis point
of view. Therefore, periodic high wave-energy events do not disadvantagethe
branchingAcropora between18 and 25 m, but aid asexualreproduction.
In the shallow areas, however, colonies are small with short, low-growing
branches close to the substratum. Coral size is a poor indicator for coral age
(HUGHES
& JACKSON,
1980) and it is therefore difficult to evaluate whether the
small corals are young or simply old corals unable to grow to a larger size. Both
possible casesindicate that only small corals can survive on shallow reefs, while
larger colonies, which experience more drag during high wave-action, become
eliminated by episodic disturbances.
No signs of asexual reproduction by fragmentationwere observed.None of the
colonies had produced fragments, which is not surprising given the small colony
sizesand short branchlengths, which add to mechanicalstability. Furthennore,the
breakage experiment showed survival chancesof fragments to be extremely low.
Already during the first month of the experimentall fragmentswere washedoff the
reef.
Episodic high wave-energyeventstherefore effectively bar the branchingA. austera from dominating shallow reef parts in two ways: colonies cannotgrow aslarge
as on the deepreef, since the longer branchesare more easily broken; oncebroken,
fragments have a low survival chanceand asexual reproduction by fragmentation
is not possible.
Therefore, A. austera cannot utilize the samelife history strategiesin shallow
water which allows it to dominate deeper reef zones. Breakage and fragment
dislocation during recurrent high wave-energyevents severely disadvantagethis
speciesin shallow water. Alcyonaceaand massiveScleractinia are not affected by
these disturbancesdue to their growth fonn. This led to the dominance of these
slower-growing species in reef areas where fast-growing, branching Acropora
cannotprevail.
Summary
The community structure of South African coral reefs was influenced by episodic
disturbancesdue to high wave-energyevents.Thesecausedbreakageand dislodgement of Acropora austera, a dominant competitor for space with a branching
morphology.A. austeradominatedreefs between18and 24 m depth,wherecolonies
were less frequently broken than in shallow areas,and where fragments survived
and could serve as asexual propagules. In shallow water (8-18 m), A. austera
colonies were broken during high wave-energyevents;fragmentswere washed off
the reefs and died. Suchcolonies thereforeremained small and were largely unable
to reproduceasexuallyby fragmentation.This allowed other, competitively inferior
speciesto dominate shallow communities.
410
RlEGL & RlEGL
Acknowledgements
Financial support from the South African Foundation for Research Development, Department for
National Education, Association for Marine Biological Researchand the University of Cape Town as
well as logistic support by the Natal Parks Board and the Oceanographic Research Institute are
acknowledged. Specialthanks are due to Dr. M. H. SCHLEYER
for his support during field work. This
paperis a result of Natal Parks Board/University of Cape Town ResearchProject SM 6/1/14.
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