Marine Pollution Bulletin Vol. 40, No. 7, pp.

606617, 2000
2000 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
PII: S0025-326X(00)00067-9 0025-326X/00 $ - see front matter

Bioerosion of Live Massive Corals and

Branching Coral Rubble on Indonesian
Coral Reefs
KATHERINE E. HOLMES,, EVAN N. EDINGER,,*, HARIYADI, GINO V. LIMMON, and
MICHAEL J. RISK,
Womens Traditional Marine Tenure Project, Vanuatu Cultural Centre, Port Vila, Vanuatu
Department of Earth Sciences, Laurentian University, Sudbury, Ont., Canada
Faculty of Fisheries and Marine Science, Diponegoro University, Semarang, Indonesia
Faculty of Fisheries and Marine Science, Pattimura University, Ambon, Indonesia
Department of Cell and Molecular Biology, Hans Knoell Institute, Jena Germany
School of Geography and Geology, McMaster University, Hamilton, Ont., Canada L8S4M1
UNDIP-McMaster Coastal Ecodevelopment Project, Research Institute, Environmental Studies Centre, Diponegoro
University, Semarang, Indonesia

The degree of bioerosion of live massive corals and rubble
from branching corals were measured on nine reefs from
two regions of Indonesia: the Java Sea and Ambon.
Bioerosion in massive corals was measured by collecting
live corals, cutting and X-raying slabs, and measuring the
cross-sectional area removed from each slab by the vari-
ous bioeroding organisms. A technique analysing branch-
ing coral rubble was developed and similarly used to
evaluate the degree of bioerosion on the reefs. This rubble
technique has potential advantages over the massive coral
technique since it does not require the expense and tech-
nical expertise of making and analysing X-rays, nor does
it require the destruction of living coral heads. The ef-
fectiveness of this rubble technique is evaluated here.
Levels of bioerosion in massive coral heads and rubble
from branching corals are each compared with environ-
mental variables and health parameters of the nine reefs.
Overall, both techniques showed that bioerosion levels
were positively correlated with environmental variables
indicative of eutrophication. Bioerosion of live massive
corals and of branching coral rubble were positively cor-
related. At the Ambon sites, where the eutrophication
levels dier only slightly compared to the Java sites,
bioerosion in coral rubble was a more sensitive indicator of
eutrophication stress than bioerosion measured from
massive coral heads. The rubble technique we outline is a
useful rapid reef assessment technique that could be a
valuable contribution to the `reef survey toolbox'. 2000
Elsevier Science Ltd. All rights reserved.
*Corresponding author. Tel.: +1-705-675-1151; fax: +1-705-675-
4898.
E-mail address: eedinger@nickel.laurentian.ca (E.N. Edinger).
Keywords: bioerosion; eutrophication; Indonesia; coral
reefs; rapid reef assessment.
Introduction
Bioerosion is a key process limiting rates and patterns of
coral reef growth (Goreau and Hartman, 1963; Hutch-
ings and Bamber, 1985). Increased bioerosion in re-
sponse to nutrient availability may limit reef accretion,
possibly contributing to reef death, or reef drowning
during sea level rise (Hallock and Schlager, 1986; Hal-
lock 1988; Glynn, 1997). The most common method of
assessing bioerosion intensity (but not rates) on modern
coral reefs is to measure the area removed from cross-
sections of corals, either in X-rays (e.g. Sammarco and
Risk, 1990) or photographs (e.g. Risk et al., 1995).
These techniques are costly and time-consuming, fre-
quently require computer image analysis equipment not
readily available in the developing world, and, most
signicantly, require killing live corals. Alternatively,
experimental methods using blocks of coral skeleton
(e.g. Kiene and Hutchings, 1994; Chazottes et al., 1995;
Pari et al., 1998) or calcite (e.g. Kobluk and Risk, 1977)
require long experimental periods and are not suitable
for surveys or rapid assessment.
Land-based sources of pollution pose great threats to
coral reefs worldwide (Pastorak and Bilyard, 1985), es-
pecially in Indonesia (Edinger et al., 1998; Edinger et al.,
2000), home to about one-seventh of the worlds coral
reefs (Tomascik et al., 1997), and the centre of world
global coral species biodiversity (Veron, 1993; Wallace,
1997). One of the principle ways in which nutrient pol-
lution threatens coral reefs is by increasing bioerosion

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intensity (Risk and MacGeachy, 1978; Rose and Risk,
1985; Hallock and Schlager, 1986; Hutchings, 1986;
Glynn, 1997; Szmant, 1997; Pari et al., 1998).
Bioerosion is a key process of carbonate destruction
in coral reef carbonate budgets (Stearn et al., 1977;
Scon et al., 1980; Hubbard et al., 1990), which provide
an integrated, whole-reef perspective on coral reef health
(McClanahan, 1997; Edinger et al., 2000). Barbados reefs
were the site of the rst major comprehensive study of
reef carbonate budgets (Stearn et al., 1977; Scon et al.,
1980). Eutrophication was later shown to be a major
cause of coral reef degradation along the west coast of
Barbados (Tomascik and Sander, 1985, 1987a,b). Sub-
sequent studies of coral rubble along this eutrophication
gradient revealed an increased abundance of bioeroding
sponges in more eutrophic environments (Holmes, 1997).
Holmes (1997) study has been modied here to de-
velop a non-destructive rapid reef assessment (RRA)
technique for indicating eutrophication stress on coral
reefs. RRA techniques form an increasingly important
part of the reef survey toolbox (Risk and Risk, 1997;
Jamieson et al., 1998). This rubble bioerosion technique
may be suitable as a general measure of pollution stress
on coral reefs (sensu Thomascik and Sander, 1987a),
along with stomatopods (Erdmann and Caldwell, 1997),
butterysh (Reese, 1993, but see also Erdmann, 1997),
and stable isotope geochemistry (Risk et al., 1993; La-
zier 1997; Heikoop et al., 2000).
Here, the intensity of bioerosion on Indonesian reefs
along eutrophication gradients is assessed using the
rubble technique along with slabbing and X-raying coral
heads. The two data sets provide a comprehensive view
of bioerosion processes on some of the worlds most
imperiled coral reefs (Tomascik et al., 1993; Chou, 1997;
Tomascik et al., 1997) and allow a comparison of the
two techniques.
Our two study areas, in the Java Sea and around
Ambon, an island in the Moluccas in the Banda Sea,
represent considerably dierent environments. The Java
Sea Reefs are all coral cays in an onshore-oshore se-
quence, and span a wide gradient of nutrient levels and
sedimentation rates. By contrast, the Ambon reefs are
all fringing reefs surrounding high island, which has a
high population density concentrated around Ambon
Bay. Only one of these reefs is isolated and relatively
unaected by anthropogenic factors; the others are af-
fected by a range of human activities including con-
struction damage, sewage pollution, and plywood
factory euent (Limmon, 1996; Edinger et al., 1998).
Bioerosion of live massive coral and of rubble from
branching corals were measured on a total of nine reefs
from the two regions. Bioerosion levels are compared
here with environmental variables and reef health pa-
rameters derived from line transect reef surveys (Edinger
et al., 1998). Five hypotheses are tested:
1. Bioerosion of live massive corals is correlated with
chlorophyll concentration and other environmental
variables indicative of eutrophication.
2. Bioerosion of branching coral rubble is correlated
with chlorophyll concentration and other environ-
mental variables indicative of eutrophication.
3. Bioerosion of live massive corals is correlated with
reef health parameters derived from transect data.
4. Coral rubble bioerosion is correlated with reef health
parameters derived from transect data.
5. Bioerosion levels in coral rubble can provide a reli-
able measure of overall eutrophication stress.
Methods
Study sites
Bioerosion was measured on reefs in the Java Sea, and
at Ambon, an island in the Moluccas. In the Java Sea,
six reefs were sampled: two oshore reefs (G. Cemara,
P. Kecil) and a fringing reef adjacent to a mangrove (L.
Marican) in the Karimunjawa National Marine Park,
and three nearshore reefs in the Jepara area (P. Panjang
North and South, Bondo), along the north coast of
Central Java (Table 1). Four reefs were sampled around
Ambon. These included two relatively unpolluted reefs
on the north coast of Ambon (Tj. Setan, Hila), facing
the Seram strait, one reef in Ambon Bay (Wayame),
subject to harbour pollution and urban runo; and one
reef on the south coast of Ambon (Wailiha), subject to
high sedimentation and immediately adjacent to a ply-
wood factory (Table 1). All of these reefs had been
previously sampled in comprehensive coral reef surveys
which included environmental variables, live coral cover,
corals species diversity, coral growth rates and, in some
cases, stable carbon and nitrogen isotopes (Limmon,
1996; Lazier, 1997; Edinger et al., 1998; Edinger et al.,
2000; Heikoop et al., 2000). Latitudes and longitudes of
all reefs are given in Heikoop et al. (2000), except for
Karimunjawa reefs G. Cemara (5500 S/110300 E), P.
Kecil (5490 S/110310 E), and L. Marican (5500 S/
110300 E). Readers are referred to maps in Edinger et al.
(1998).
Bioerosion of live massive corals
Sampling for bioerosion of live massive corals fol-
lowed a balanced nested analysis of variance design.
Bioerosion of massive Porites lobata heads was mea-
sured from X-rays of three parallel but non-adjacent
slabs through each of three to ve coral heads collected
at 1m depth from each site, yielding a total of 15 X-rays
per site (Sammarco and Risk, 1990). Species identica-
tion of P. lobata was checked prior to slabbing the
corals, according to Veron (1986). Boreholes were
identied by shape as sponges (including Cliona, Cli-
othosa, and Siphonodictyon), bivalves (Lithophaga and
Gastrochaena), gall shrimp (Upogebia), or worms. Si-
punculan and polychaete worms are grouped together
since their borings are dicult to distinguish reliably.
The cross-sectional area of each slab and the borings in
it were measured using a hand-held planimeter (Edinger
and Risk, 1997). Bioerosion intensity is reported as the
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 Marine Pollution Bulletin

TABLE 1
Study site regions, names, morphologies, and summaries of stresses on study reefs.a

Region Reef name and abbreviation Reef morphology Maximum depth (m) Water clarity (m) Stresses

Karimunjawa Gosong Cemara (GC) Coral cay island 25 20 Reference, overshing

(net and trap)
(Central Java) Pulau Kecil (PK) Coral cay, submerged 25 20 Reference, overshing
(net and trap)
Lagun Marican (LM) Mangrove fringe 4 <3 High turbidity
(not anthropogenic)
Jepara Bondo (BD) Fringing reef 5 <2 Sediment, agricultural
runo
(Central Java) Pulau Panjang North (PPN) Coral cay island 8 <3 Sewage, sediment,
aquaculture (shrimp
hatcheries)
Pulau Panjang South (PPS) Coral cay island 8 <3 Sewage, sediment,
agricultural runo
Ambon Tanjung Setan (TS) Fringing reef/wall 40 >20 Reference site
(Moluccas) Hila (HL) Fringing, rubble 20 20 Blast shing,
bottom construction,
local sewage
Wayame (WM) Fringing reef 15 10 Harbour, sewage,
sedimentation
Wailiha (WL) Fringing reef 6 <5 Harbour, sediment,
plywood factory
a
Maximum Depth the maximum depth of coral growth. Water Clarity was measured as average secchi disk extinction depth. Stresses summarize
the impacts experienced by each reef. More detailed descriptions of each reef can be found in Limmon (1996) and Edinger et al. (1998).

percentage of cross-sectional area removed by each type
of boring organism. Total percent bioerosion of live
massive corals is the sum of the cross-sectional area
removed by all types of boring organism divided the
cross-sectional area of the slab (see Fig. 1).
Coral rubble bioerosion
Acropora corals grow very quickly, and have a more
open skeletal architecture and lower skeletal density
than most other branching coral taxa (Veron, 1986).
Under high nutrient conditions, their skeletal extension
rates increase, but skeletal density decreases (Atkinson
et al., 1995). Acropora branching corals are in low
abundance on nearshore reefs subject to sewage pollu-
tion and sedimentation (Edinger et al., 1998). In order to
standardize for species composition of the rubble across
the ve sites, Acropora rubble was excluded from the
Java Sea collections. Branching non-Acropora corals

Fig. 1 Cumulative percent bioerosion, by organism type, of massive

coral heads (Porites lobata) collected from Java Sea reefs. Site
abbreviations as in Table 1. Standard deviations for the to-
tal percent bioerosion are 0.45, 0.77, 1.54, 4.62, 5.07, 4.62, and
5.09 and N 5, 3, 5, 4, 3, and 5 heads for the six reefs, re-
spectively.

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Volume 40/Number 7/July 2000
mainly included Porites cylindrica, P. nigrescens, Pocil-
lopora spp., Stylophora spp., and Hydnophora rigida. In
Ambon, where Acropora is more common at all sites,
two separate rubble collections were made, one for
branching non-Acropora corals, and one for branching
Acropora rubble only. By `branching' we mean that the
pieces were the broken, cylindrical pieces from branch-
ing species. The Acropora and non-Acropora collections
were analysed separately and compared to determine if
dierences in coral rubble skeletal structure inuenced
the bioerosional patterns.
Coral rubble bioerosion sampling also followed a
balanced nested ANOVA design. Coral rubble samples
were collected at the same depth and locations as tran-
sects for reef health parameters. At each reef, at 3 m
depth, 10 pieces of rubble were collected along each of
ten 1m wide and 5 m long transects, totaling 100 pieces
(10 samples of 10) from a 50 m transect. Five random
cuts were made across the long axis of each piece of
rubble with a dry-cut rock saw. Each cut was scored for
presence or absence of bioeroding organisms, including
boring sponges, worms, bivalves, gall shrimps and others.
This yielded a bioerosion score of 05 for each piece of
rubble (one score for every cut containing at least one
boring organism). The length of each piece of rubble
was measured, as were the maximum and minimum
diameters of the centre segment of each rubble piece;
these measurements were used to calculate the approx-
imate volume of each piece of rubble. Bioerosion in-
tensity is reported as the average bioerosion score of the
ten pieces of rubble per sample. Rubble collections were
made from the same reefs as collections of massive
corals except at Bondo, where poor weather conditions
during the rubble sampling period prevented safe access
to that site.
Environmental data
A variety of environmental variables was measured at
each reef, including water column Chlorophyll A con-
centration, suspended particulate matter concentration,
sediment resuspension, and water clarity (secchi disk
extinction depth) (Table 2). Limited access to eld time
TABLE 2
Environmental parameters measured for each reef in the study.a
Reef Chlorophyll A (mg/m3 )
Pulau Kecil (PK) 0.29 (0.17)5
Gosong Cemara (GC) 0.25 (0.14)5
Lagun Marican (LM) 1.24 (0.90)5
Bondo (B) 1.22 (0.52)5
P. Panjang North (PPN) 1.23 (0.54)5
P. Panjang South (PPS) 1.09 (0.62)5
Tanjung Setan (TS) 0.39 (0.19)4
Hila (H) 0.44 (0.21)4
Wayame (WM) 0.38 (0.06)4
Wailiha (WL) 0.46 (0.14)4
a
Averages, followed by standard deviations (in brackets) and number of measurements in subscript. Methods are described in the text.
precluded equal sampling intervals in all locations and
in all seasons. Ambon data were collected in MayAu-
gust 1995; Java Sea data were collected in November
1994January 1995, JulyDecember 1995, and August
December 1996. Ambon environmental data were all
collected during the wet season (AprilSeptember). Java
Sea environmental data were averaged for the wet
season (DecemberMarch) and the dry season (April
November) of each year. (Chlorophyll sampling in
Ambon was repeated in JuneSeptember 1997. Full
environmental data for Ambon sites are reported in
Limmon (1996). Chlorophyll sampling and analysis
followed Parsons et al. (1984) and Burnison (1980). For
each Java Sea site, the average Chlorophyll A con-
centration is calculated as the mean of the means of the
19941996 wet seasons and the 1995 and 1996 dry
seasons so the two seasons are approximately equally
represented.
Suspended particulate matter (SPM) was measured by
ltering one litre of seawater onto a pre-weighed glass
bre lter which was subsequently oven-dried and
weighed (Cortes and Risk, 1985). Total downward
sediment ux (sediment resuspension plus SPM) was
measured using sediment traps consisting of 30 cm long,
5 cm diameter PVC tubes. In Java, sediment traps were
deployed on the reef surface at 3 m depth, 10 m depth,
and the base of the reef in Karimunjawa, and at 1, 3 m,
and the base of the reef in Jepara. Sediment traps at the
Ambon sites were deployed 25, 50, and 75 cm above the
reef surface at 3 m depth and were changed weekly.
Sediment traps were collected weekly in Ambon, bi-
weekly in Jepara, and monthly or bimonthly in Kari-
munjawa, and the accumulated sediment dried and
weighed. The mass of accumulated sediment was divided
by the cross-sectional area of the sediment traps and the
number of days deployed to determine rates of sediment
resuspension. The period of sediment trap sampling
extended over four months on Ambon reefs, and over
three to six months in each of two years on the Java Sea
Reefs. Numbers of samples in Table 2 indicate number
of sample periods at each locality for which sediment
traps were successfully recovered. High standard
SPM (mg/l) Resuspension (mg/cm2 /day)
19.69 (18.27)4 1.63 (1.31)3
22.26 (7.56)7 2.80 (3.62)5
26.39 (11.58)6
21.04 (4.60)8 38.45 (25.7)3
21.83 (8.40)9 26.19 (24.42)8
28.91 (17.86)12 31.69 (38.74)6
4.49 (1.40)13 0.077 (0.018)8
4.91 (2.66)13 0.19 (0.14)8
11.15 (3.40)14 0.55 (0.23)8
15.3 (10.21)14 3.08 (3.13)8
609

deviations indicate more variable sediment resuspension
rates.
Reef health parameters
Reef health was estimated using line intercept tran-
sects to measure percent live coral cover, coral mortality
index (Gomez et al., 1994), and coral species diversity
(Edinger et al., 1998). At each reef, 12 replicate 20 m line
intercept transects were measured, six at 3 m depth,
and six at 10 m depth. Cover of live corals, dead coral,
algae, other fauna, and abiotic substrates (e.g. sand
and rubble) were measured along each transect. Other
fauna included sessile invertebrates such as sponges,
gorgonians, alcyonarian soft corals, zooanthids, and
ascidians. Transect locations were non-adjacent, non-
overlapping and dispersed over at least 200 m laterally
along each reef, to account for spatial variation (Edm-
unds and Bruno, 1996). On three reefs, where coral
depth did not extend beyond 6 m depth (Wailiha, Lagun
Marican, and Bondo), transects were measured at 3 m
depth only. At Pulau Panjang in Jepara, transects were
measured at 3 and 6 m depths. Coral mortality index
(MI) (Gomez et al., 1994) at each site and depth was
computed as:
dead coral cover
MI :
live coral cover dead coral cover
Possible MI values range from zero (all corals live) to
one (all corals dead). Complete transect data are re-
ported in Edinger et al. (1998); only summaries of
transect data are used here.
Data analysis
Bioerosion intensity was compared among reefs using
simple and nested one-way ANOVAs followed by mul-
tiple range tests, with separate analyses for Java and
Ambon. Where necessary, data were square root trans-
formed to homogenize variance. Non-normal data were
tested using non-parametric statisics. Bioerosion inten-
sity was correlated with environmental variables and
reef health parameters using simple linear correlation.
Results
Java Sea
Bioerosion of live massive corals. Total bioerosion, and
bioerosion by all of the individual bioeroding taxa, were
higher on the polluted reefs (Bondo and Pulau Panjang
North and South) than on the reference reefs (Gosong
Cemara and Pulau Cecil) or the mangrove fringing reef
(Lagun Marican). Total bioerosion and bioerosion by
almost all of the individual bioeroding taxa were highest
at Pulau Panjang South, the site with the greatest inux
of domestic sewage and aquacultural runo (Edinger et
al., 1998). Boring worms were slightly more abundant at
Bondo, the site with primarily agricultural runo, than
at Pulau Panjang South (Fig. 1).
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Marine Pollution Bulletin
Total bioerosion of massive corals was signicantly
higher on polluted reefs than on reference reefs or the
mangrove fringing reef (Table 3). Total bioerosion by
boring sponges in the massive coral heads was also
higher on the polluted reefs than on the reference reefs
or the mangrove fringing reef (ANOVA, d.f. 5, 19,
F 2:91; p < 0:05), unlike bioerosion by boring worms
or Lithophaga. For all bioeroding organisms except
worms and Upogebia, bioerosion was most intense at
Pulau Panjang South (Fig. 1), the site with the most
intense sewage pollution.
Total bioerosion of live massive corals was weakly
positively correlated with Chlorophyll A concentration
(r 0:59; n 6 reefs), as was total sponge bioerosion
(r 0:56; n 6 reefs) (Table 7(a)). Total bioerosion of
live massive corals was signicantly positively correlated
with coral mortality index (r 0:92; p < 0:01; n 6
reefs), and weakly negatively correlated with live coral
cover (r 0:68; n 6 reefs) (Table 7(a)).
Coral rubble bioerosion. Bioerosion levels in branching
coral rubble were higher on reefs suering from eu-
trophication or sediment stress than on reference reefs,
although there were some anomalies (Fig. 2). One of the
reference reefs, Gosong Cemara, had signicantly lower
coral rubble bioerosion scores than the four other reefs
sampled (Table 4). The other reference reef, Pulau Kecil,
however, did not signicantly dier from the three
polluted reefs (Table 4). Lagun Marican, which has
naturally high sediment and nutrient levels, supported
rubble with signicantly lower bioerosion scores than
Pulau Panjang North, which suers from sewage,
aquacultural and agricultural runo (Fig. 3(a)),
Fig. 2 Branching coral rubble bioerosion scores from Java Sea reefs.
(a) Total bioerosion score, (b) boring sponge frequency. Means
95% condence limits. Site abbreviations as in Table 1.
N 10 rubble samples for all ve reefs.
Volume 40/Number 7/July 2000

TABLE 3
(a) ANOVA comparing the mean total percent bioerosion (square root transformed) of massive coral heads (P. lobata) from Java Sea reefs. (b)
Tukey-b post hoc multiple comparisons matrix of pairwise probabilities for the six reefs.

Source of variation Sum of squares d.f. Mean square F-ratio p-value

(a)
Reef 15.968 5 3.194 6.768 0.001
Error 8.965 19 0.472
(b)
Reef GC PK LM BD PPN PPS

Cemara 1.000
Kecil 0.987 1.000
Marican 0.985 1.000 1.000
Bondo 0.011 0.099 0.040 1.000
Panjang N. 0.425 0.858 0.758 0.614 1.000
Panjang S. 0.003 0.037 0.011 0.998 0.362 1.000
*
p < 0:05.
**
p < 0:01.

TABLE 4
(a) ANOVA comparing the bioerosion scores for rubble samples from Java Sea reefs. (b) Tukey-b post hoc multiple comparisons matrix of pairwise
probabilities for the ve reefs.

Source of variation Sum of squares d.f. Mean square F-ratio p-value

(a)
Reef 22.079 4 5.52 17.99 0.0001
Error 13.807 45 0.307
(b)
Reef GC PK LM PPN PPS

Cemara 1.000
Kecil <0.001 1.000
Marican 0.039 0.163 1.000
Panjang N. <0.001 0.057 <0.001 1.000
Panjang S. <0.001 1.000 0.177 0.052 1.000
*
p < 0:05.
***
p < :001.

Fig. 3 Cumulative percent bioerosion, by organism type, of massive

coral heads (P. lobata), collected from Ambon reefs. Site ab-
breviations as in Table 1. Standard deviations for the total
percent bioerosion are 1.18, 0.83, 1.98, and 0.93 for the four
reefs, respectively, and N 5 heads for all four reefs.

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Table 4(b)). Bioerosion score was weakly positively
correlated with Chlorophyll A concentration
(r 0:49; n 5 reefs) (Table 7(a)). In addition, the
average frequency of boring sponge occurrence was
positively correlated with Chlorophyll A concentration
(r 0:43; n 5 reefs) (Fig. 3(b); Table 7(a)), but there
were no signicant trends in the frequency of boring
bivalves or worms. Rubble bioerosion score was in-
versely correlated with live coral cover
(r 0:41; n 5 reefs) (Table 7(a)). The bioerosion
score of rubble pieces was positively correlated with
average percent bioerosion of massive corals from the
reefs (r 0:70; n 5 reefs).
Ambon
Bioerosion of live massive corals. There were no sta-
tistically signicant dierences in massive coral bioero-
sion intensity among the four Ambon reefs sampled
(Table 5) and no trends with regard to the various taxa
invading coral heads were revealed (Fig. 3). Similarly,
there were no signicant correlations between total
massive coral bioerosion and any of the environmental
variables or reef health parameters measured (Table
7(b)).
Coral rubble bioerosion. The average bioerosion score
of non-Acropora rubble pieces from the cleanest water
reef, Tanjung Setan, was signicantly less than that for
the three polluted Ambon reefs (Fig. 4(a), Table 6).
Average sponge bioerosion score was highest at Way-
ame, followed by Hila, Wailiha, and Tanjung Setan
(Fig. 4(b)). Acropora rubble bioerosion scores were
lower at Tanjung Setan than at the other three reefs
sampled in Ambon (Fig. 4(c)), but this pattern was only
weakly signicant (Table 6(c)). The average bioerosion
score of non-Acropora rubble was weakly correlated
with Chlorophyll A concentration (r 0:54; n 4
reefs), and SPM (r 0:69; n 4 reefs), and inversely
correlated with water clarity (r 0:81; n 4 reefs).
Non-Acropora bioerosion score was signicantly posi-
tively correlated with coral mortality index

TABLE 5
ANOVA comparing the mean total percent bioerosion of massive coral heads (P. lobata) from Ambon reefs.

Source of variation Sum of squares d.f. Mean square F-ratio p-value

Reef 1.98 3 0.661 0.632 0.605

Error 16.72 16 1.045

Fig. 4 Branching coral rubble bioerosion scores from Ambon reefs.

(a) Total bioerosion score, non-Acropora rubble, (b) boring
sponge frequency, non-Acropora rubble, (c) Total bioerosion
score, Acropora rubble, (d) Boring sponge frequency, Acropora
rubble. Means 95% condence limits. Site abbreviations as
in Table 1. N 10 for all values except Wayame Acropora,
where N 9 rubble samples.

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Volume 40/Number 7/July 2000

TABLE 6
(a) ANOVA comparing the bioerosion scores for non-Acropora rubble samples from Ambon reefs. (b) Tukey-b post hoc multiple comparisons
matrix of pairwise probabilities for the four reefs. (c) ANOVA comparing the bioerosion scores (square root transformed) for Acropora rubble
samples from Ambon reefs. N 39 since one outlier was removed. (d) Tukey-b post hoc multiple comparisons matrix of pairwise probabilities for the
four reefs.

Source of variation Sum of squares d.f. Mean square F-ratio p-value

(a)
Reef 5.624 3 1.875 4.688 0.007
Error 15.195 38 0.4
(b)
Reef TS HL WM WL

Tj. Setan 1.000

Hila 0.042 1.000
Wayame 0.007 1.000 1.000
Wailiha 0.031 0.926 0.939 1.000
(c)
Reef 7.825 3 2.428 4.715 0.007
Error 18.026 35 0.515
(d)
Reef TS HL WM WL

Tj. Setan 1.000

Hila 0.177 1.000
Wayame 0.004 0.338 1.000
Wailiha 0.148 1.000 0.386 1.000
*
p < 0:05.
**
p < 0:01.
***
p < 0:001.

(r 0:98; p < 0:01; n 4), and signicantly negatively
correlated with live coral cover (r 0:97) and coral
species diversity (r 0:91; Table 7(b)). Massive coral
bioerosion and non-Acropora rubble bioerosion score
were not signicantly correlated.
Overall patterns. Both massive coral bioerosion and
coral rubble bioerosion reected productivity patterns
in the Java Sea and at Ambon. When the Java Sea and
Ambon datasets were combined, massive coral bioe-
rosion was strongly correlated with Chlorophyll A
concentration (r 0:69; n 10 reefs). Likewise, non-
Acropora rubble bioerosion score was strongly corre-
lated with Chlorophyll A concentration
(r 0:62; n 9 reefs), and rubble bioerosion score was
strongly correlated with massive coral bioerosion
(r 0:66; n 9 reefs) (Table 7). In all these cases, the
strong correlations are driven by the nearshore Java
Sea sites, where productivity levels and bioerosion in-
tensity are highest.
Rubble bioerosion was also inuenced by the char-
acteristics of the rubble itself. There was a strong posi-
tive correlation between non-Acropora coral rubble size
(measured as cross-sectional diameter) and bioerosion
score (r 0:49; n 92), with similar relationships in
the Ambon and Java Sea when analysed separately.
Coral skeletal structure did not have a strong inuence
on rubble bioerosion score. Acropora and non-Acropora
rubble in Ambon had similar bioerosion scores and had
similar responses to environmental variables (Tables
6(a) and 6(c), although the non-Acropora rubble showed
more distinct dierences between polluted and reference
reefs than did Acropora rubble (Fig. 4(a) and (c), Table
6(b) and (d)).
Discussion
Levels of bioerosion in both live massive corals and in
branching coral rubble were signicantly higher on reefs
subject to eutrophication than on reference reefs. In the
Java Sea, massive coral bioerosion was positively cor-
related with environmental variables indicative of eu-
trophication. This pattern was clearly supported by the
Java Sea data, and all sites pooled, but not by the
Ambon data alone. We attribute this regional dierence
to the strength of environmental dierences among sites
within each region (Table 2). Bioerosion of live massive
corals was negatively correlated with transect measure-
ments indicative of coral reef health in the Java Sea, but
not in Ambon.
In all cases, coral rubble bioerosion was positively
correlated with environmental variables indicative of
eutrophication. The Ambon Acropora and non-Acro-
pora rubble datasets both showed similar results. Both
Acropora and non-Acropora rubble distinguished pol-
luted from non-polluted sites, but the non-Acropora
rubble showed this distinction more clearly. In all cases,
coral rubble bioerosion was negatively correlated with
transect measurements indicative of coral reef health
such as live coral cover and coral species diversity.

613
 Marine Pollution Bulletin

TABLE 7
Correlations between bioerosion measures, environmental variables, and transect-based reef health parametres. (a) Java Sea. N 6 reefs for
bioerosion of live massive corals and N 5 reefs for rubble bioerosion except for sediment resuspension where N 5 and 4, respectively, due to lack
of data from Lagun Marican. (b) Ambon. N 4 reefs across all measures. (c) All sites combined, N 10 reefs for bioerosion of live massive corals
and N 9 for rubble bioerosion except for sediment resuspension where N 9 and 8, respectively.

Environmental Total percent bioerosion of Bioerosion of massive Total coral rubble bioerosion Coral rubble sponge bioerosion
variables live massive corals corals by sponges score score

(a)
Chlorophyll A 0.59 0.56 0.49 0.43
SPM 0.39 0.43 )0.19 0.35
Sediment 0.93 0.91 0.52 0.35
resuspension
Water clarity )0.70 0.68 )0.35 0.25
Reef health parameters
Live coral cover )0.68 0.65 )0.41 0.29
Coral mortality 0.92 0.96 0.17 0.07
index
Coral species )0.43 0.42 )0.78 0.77
diversity
(b)
Environmental Total percent bioerosion of Bioerosion of massive Total coral (non-Acropora) Coral rubble (non-Acropora) sponge
variables live massive corals corals by sponges rubble bioerosion score bioerosion score

Chlorophyll A )0.17 )0.71 0.54 )0.49

SPM 0.73 0.14 0.69 0.01
Sediment 0.54 )0.10 0.57 )0.41
resuspension
Water clarity )0.60 )0.07 )0.81 )0.15
Reef health parameters
Live coral cover 0.03 0.62 )0.97 )0.20
Coral mortality )0.07 )0.64 0.98 0.24
index
Coral species 0.31 0.82 )0.91 )0.19
diversity
(c)
Environmental Total massive coral bioersion Massive coral bioerosion Total coral (non-Acropora) Coral rubble (non-Acropora) sponge
variables by sponges rubble bioerosion score bioerosion score

Chlorophyll A 0.69 0.60 0.62 0.58

SPM 0.40 0.41 0.61 0.66
Sediment 0.94 0.89 0.69 0.62
resuspension
Water clarity )0.59 )0.54 )0.59 )0.42
Reef health parametres
Live coral cover )0.44 )0.43 0.41 )0.12
Coral mortality 0.53 0.708 0.15 )0.13
index
Coral species )0.69 )0.53 )0.89 )0.79
diversity
*
p < 0:05.
**
p < 0:01.

Bioerosion of live massive corals was positively corre-
lated with coral rubble bioerosion in the Java Sea and in
the entire dataset pooled, but not in Ambon alone.
These patterns have important implications for re-
gional dierences in productivity and bioerosion, eects
of coral morphology on bioerosion, reef carbonate
budgets, and the use of our technique as a rapid as-
sessment tool in reef health surveys.
Regional dierences in productivity and bioerosion. The
intensity of massive coral bioerosion was much greater
on the nearshore Java Sea Reefs than on any of the
Ambon reefs (i.e. 4.39.1% vs 0.91.7%; Figs. 2 and 4).
Massive coral bioerosion levels on the Ambon reefs were
all similar to the reference reefs of the Java Sea, as were
Chlorophyll A concentrations. Likewise, rubble bioe-
rosion levels on the polluted Java Sea Reefs were higher
than on any of the Ambon sites.
Bioerosion in massive and branching corals were most
strongly correlated among the Java Sea sites, where
dierences in nutrient availability between sites are
dramatic, rather than subtle (Table 2). These patterns
relate to the pattern of productivity dierences among
the sites in the two regions, and to overall dierences in
productivity between the Java Sea and Ambon. The
Java Sea sites segregate much more clearly into oshore,
clearwater reefs and nearshore, eutrophic reefs, while

614
Volume 40/Number 7/July 2000
the Ambon sites are all fringing reefs around a high is-
land with similar levels of natural terrigenous nutrient
supply. Chlorophyll A concentrations at the nearshore
Java Sea Reefs are four to ve times those of their o-
shore counterparts, while Chlorophyll A concentrations
on contaminated Ambon reefs are only about 1.5x those
of the cleanest reef, Tanjung Setan.
In the Java Sea, both massive coral bioerosion and
coral rubble bioerosion were inversely correlated with
transect measurements indicative of coral reef health. In
Ambon, however, these patterns only held true for coral
rubble, where rubble bioerosion apparently provided a
more sensitive proxy measurement for reef health than
did massive coral bioerosion.
Massive coral bioerosion vs rubble bioerosion. Bioero-
sion intensity was generally greater in rubble from
branching corals than in live massive corals, although
the numbers from the two techniques are not directly
comparable. The same suite of boring organisms was
observed in both live massive corals and in branching
coral rubble, although their relative abundances varied.
Boring sponges (Cliona, Cliothosa, Siphonodictyon) were
the most abundant borers in both live massive corals
and in rubble. Boring bivalves (Lithophaga, Gastrocha-
ena) and gall shrimp (Upogebia) were more abundant in
live massive corals than in branching coral rubble.
In the Java Sea, where eutrophication stress on
nearshore reefs is intense, the two methods of measuring
bioerosion intensity broadly agreed. In Ambon, how-
ever, there is only a weak correlation between massive
coral bioerosion and coral rubble bioerosion. Rubble
bioerosion is positively correlated with environmental
indicators of eutrophication and negatively correlated
with reef health measurements, while massive coral
bioerosion showed no signicant trends whatsoever.
Taphonomic processes may help to explain some of the
dierences between massive coral bioerosion and rubble
bioerosion.
Rubble bioerosion is inuenced by breakage, pro-
ductivity and burial (Pandol and Greenstein, 1997;
Edinger and Risk, 1997; Lescinsky and Edinger, 1997).
Residence time on the surface is a key factor determin-
ing the intensity of boring into dead corals (Brett, 1990;
Pandol and Greenstein, 1997). On average, larger
pieces of rubble can be expected to remain on the sur-
face on a reef for a longer period of time, explaining the
positive relationship between rubble size and bioerosion
score. Blast shing also aects residence time of rubble
on the reef surface, because blasting breaks many
branching corals in a short period of time. Although
blast shing has been observed on one of the reefs we
studied (Hila, Ambon), the portions of the reef which we
sampled had not been aected by blast shing. Levels of
grazing intensity may also aect total bioerosion, both
internal (Risk and Sammarco, 1982) and external
(Chazottes et al., 1995).
Non-Acropora and Acropora rubble were sampled
separately to determine whether the structure of rubble
strongly inuenced bioerosion patterns. The broad
similarities in results between the Acropora and non-
Acropora datasets suggest that taxonomic anity and
attendant dierences in skeletal structure have less in-
uence on bioerosion levels than productivity, deposi-
tional environment, and residence time at the surface (cf.
Pandol and Greenstein 1997).
Application as a rapid assessment technique. The de-
gree of bioerosion of coral rubble can be used as an
indicator of sewage or other eutrophication pollution on
coral reefs, and is most useful in concert with other
measures of eutrophication and reef health (cf. Risk
et al., in press). Rubble bioerosion was more sensitive to
subtle environmental gradients and reef health mea-
surements in Ambon than massive coral bioerosion. On
the Java Sea Reefs, where eutrophication stress is much
more intense, massive and branching coral bioerosion
yielded similar results, both reecting environmental
and reef health patterns. Both live massive coral bioe-
rosion and rubble bioerosion scores showed dramatic
dierences between a reef adjacent to a mangrove, and
subject to natural runo (Lagun Marican), versus
nearshore reefs subject to anthropogenic sewage pollu-
tion (Pulau Panjang, Bondo; Edinger et al., 1998).
The rubble bioerosion measure has distinct advanta-
ges as a rapid assessment tool, specically as a proxy
recorder of eutrophication damage to coral reefs. First,
it does not require killing live corals. Second, it is rapid,
inexpensive, and requires little infrastructure or equip-
ment. Two divers completed rubble sampling in less
than an hour per reef, and sample processing and data
reduction were completed within a day. Furthermore,
rubble sampling could be done on snorkel if necessary,
obviating the need for SCUBA support. Students and
volunteers were trained in the rubble technique within a
day. By contrast, massive coral bioerosion measure-
ments required SCUBA, a large rock saw, and access to
an X-ray unit and computer digitizing board. Further-
more, training students in techniques for massive coral
bioerosion measurements required several days. These
requirements and the sampling procedure made massive
coral bioerosion much more costly and time-consuming
than the rubble bioerosion measurements. Transect
measurements for reef health estimates required ap-
proximately 12 diver-hours per reef, as well as signi-
cant training of eld workers in SCUBA diving, transect
methodology, and coral identication. Because the
rubble bioerosion technique is inexpensive and requires
very little infrastructure or training, it is suitable for
rapid surveys in remote locations, and for community-
based reef monitoring eorts.
Conclusions
1. On the reefs studied, massive coral bioerosion was
positively correlated with environmental variables in-
dicative of eutrophication.
615

2. Bioerosion of live massive corals was negatively cor-
related with transect measurements indicative of coral
reef health in the Java Sea. Coral rubble bioerosion
was negatively correlated with transect measurements
indicative of coral reef health in both Ambon and the
Java Sea. The Ambon Acropora and non-Acropora
rubble datasets showed similar results.
3. Bioerosion of live massive corals was positively corre-
lated with coral rubble bioerosion in the Java Sea, but
not in Ambon. This regional dierence resulted from
a much greater degree of eutrophication on polluted,
Java Sea Reefs than on any of the Ambon reefs.
4. Coral rubble bioerosion was more sensitive to low
levels of eutrophication and sedimentation stress than
was massive coral bioerosion. Coral rubble bioero-
sion can be used as a general indicator of eutrophica-
tion stress on coral reefs.
5. Coral rubble bioerosion presents an inexpensive, low
technology indicator of eutrophication stress on coral
reefs, and forms a valuable rapid reef assessment
technique. It is particularly appropriate in remote sit-
uations, for community-based monitoring eorts, or
on reefs already so stressed that further collection
of coral heads for bioerosion studies would emperil
the reef.
We thank B. Zaman, H. Zahidin, I. Azhar, C. Boerboom, M. Keer,
W. Widjatmoko, and several other UNDIP, UNPATTI, and
McMaster sta, students, and volunteers for assistance in the eld and
the lab. Nur Utama and Marilyn Kereliuk assisted with X-radiogra-
phy, in Indonesia and Canada, respectively. Henna Rya Sunoko and
Irdez Azhar facilitated lab and eld work in Indonesia. Wisnu Wid-
jatmoko and Dr. Lachmuddin Syarani supervised UNDIP student
thesis projects related to this project. D. Browne, P. Copper, J. Ren-
dell, and P. Sammarco made helpful comments on the manuscript.
Supported by the UNDIP-McMaster Coastal Ecodevelopment Project
(CIDA University Partnerships in Cooperation and Development
agreement # 098/S47074-099), and by NSERC operating grants to
MJR. EE thanks the Geology Department, St. Francis Xavier Uni-
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