Marine Chemistry 71 Ž2000.

215–231
www.elsevier.nlrlocatermarchem

Heavy metals in seawater, marine sediments and corals from the

Townsville section, Great Barrier Reef Marine Park, Queensland
Graeme Esslemont )
Centre for Coastal Management, Southern Cross UniÕersity, P.O. Box 157, Lismore, NSW 2480, Australia
Received 14 August 1998; received in revised form 10 March 2000; accepted 6 April 2000

Abstract

The capacity of corals to assimilate heavy metals in response to environmental availability, as defined by sediment and
water concentrations, was investigated at three sites in the Townsville region: a harbour ŽTownsville Harbour., a control
ŽOrpheus Island., and a site occasionally influenced by harbour dredge spoils ŽMagnetic Island.. In Townsville Harbour,
biologically available lead, copper, and zinc concentrations were higher than at other sites. Nickel and chromium
concentrations were also higher in harbour sediments, but only in phases relatively inaccessible to biota.
Skeletal records corresponded with environmental availability of some metals. Goniastrea aspera from the harbour
accumulated high lead, copper, and zinc concentrations, relative to G. aspera from Orpheus Island. Nickel concentrations in
G. aspera corresponded with ambient available concentrations in sediments from the harbour and Orpheus Island. However,
nickel concentrations in Pocillopora damicornis from Magnetic Island did not correspond with ambient available
concentrations measured in sediments from this site and Orpheus Island. In some situations, metal availability represented by
skeletal records may have been inadequately represented by sediment data; cadmium and chromium concentrations were
high in skeletons of harbour G. aspera, but intersite differences were not evident in sediment. Copper and zinc
concentrations were high in skeletons of P. damicornis at Magnetic Island, but supporting evidence in sediments was absent.
Tissues did not always correspond with environmental metal loads measured in sediments or skeletons. G. aspera tissues
recorded high copper and zinc availability in the harbour, but not high lead availability. Furthermore, cadmium, nickel, and
chromium concentrations in G. aspera tissues were lower in the harbour than at Orpheus Island, contrasting with skeleton
and sediment data. P. damicornis tissues indicated similar metal availability at Magnetic Island and Orpheus Island, which
corresponded with intersite comparisons using sediment data, but not with skeleton data that indicated differences. Different
tissuerskeleton ratios of metal concentrations in corals from the harbour versus the control site indicate tissue-regulation of
cadmium, lead, zinc, and chromium.
The study indicates that coral skeletons represent environmental metal loads more faithfully than tissues, but nevertheless
coral tissues appear useful for bioassaying a limited range of metals. q 2000 Elsevier Science B.V. All rights reserved.

Keywords: Coelenterata; Environmental geology; Heavy metals; Seawater; Sediments; Townsville, Australia

) 1. Introduction
Present address: CRC for Freshwater Ecology, University of
Canberra, ACT 2601, Australia. Tel.: q61-6-201-5111; fax: q61-
6-201-5999. The Townsville section of the Great Barrier Reef
E-mail address: esslemon@aerg.canberra.edu.au Ž G.
Esslemont..
is one of the few regions in Australia where corals

0304-4203r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 4 2 0 3 Ž 0 0 . 0 0 0 5 0 - 5
216 G. Esslemontr Marine Chemistry 71 (2000) 215–231

coexist with potentially significant heavy metal pol- tons of P. damicornis, G. aspera, and A. for-
lution, prompting several investigations into interac- mosa.
tions between heavy metals, substrate, and biota in 2. Variation of heavy metal concentrations within
this environment ŽCarey, 1981; Burden-Jones et al., and between colonies of P. damicornis.
1982; Denton and Burdon-Jones, 1986; Jones, 1992; 3. How well coral tissues and skeletons record envi-
Reichelt and Jones, 1994.. Two investigations asso- ronmental heavy metal concentrations, and
ciate heavy metals with harbour activity and coral whether partitioning between tissues and skele-
reefs: Ž1. Reichelt and Jones Ž1994., and Ž2. a moni- tons of the above metals vary with exposure to
toring program of corals within Townsville Harbour different environmental metal concentrations.
that has been ongoing since 1993 ŽGreat Barrier Reef
Marine Park Authority, 1996..
Reichelt and Jones Ž1994. studied dredging activi-
ties in Townsville Harbour and along Platypus Chan- 2. Area description
nel, and showed that particle-bound heavy metals
Orpheus Island, Magnetic Island, and Townsville
can be used to trace the distribution of resuspended
Harbour are located in the Townsville Section of the
dredge spoils on coral reefs at Magnetic Island. Zinc
Great Barrier Reef ŽFig. 1.. Within Townsville Har-
and copper were generally carried in suspension by
bour there is limited coral growth, and extensive
organic phases, and zinc and lead by iron oxides,
fringing reefs occur at Magnetic and Orpheus Is-
with some transfer of lead to carbonates.
lands, which are continental islands that occur near
The Great Barrier Reef Marine Park Authority
the mouths of river systems. Orpheus Island is suit-
monitors a coral community inside Townsville Har-
ably distant from harbour activity to provide a con-
bour, to observe recruitment, growth, and mortality
trol site for assessing anthropogenic inputs associ-
responses to heavy metal availability and salinity
ated with harbour activity.
changes. Genera are predominantly Goniastrea and
Townsville Harbour extends from Platypus Chan-
Montipora, with some Acropora, Porites, Symphyl-
nel into Ross Creek, and is regularly dredged to
lia, and Turbinaria. At the time of sampling, the
allow deep draft shipping. This is the principal port
community was colonising rocks of the harbour walls
for copper, lead, and zinc shipment from the Mount
very close to where lead, copper and zinc ingots, and
Isa and Hilton mines in central Queensland, which
nickel laterite ores are handled.
have produced recent quantities of ore shown in Fig.
Heavy metal accumulation by corals in relation to
2. Copper and lead is refined at Townsville before
environmental availability was assessed within
shipment. Nickel laterite imported from New Cale-
Townsville Harbour, Nelly Bay at Magnetic Island,
donia is refined at the Yabulu plant located slightly
and Pioneer Bay at Orpheus Island. Environmental
availabilities were evaluated by measuring metal
concentrations in filtered and unfiltered seawater,
and in reactive, metal-bearing, sediment phases.
Metal concentrations in tissues and skeletons of
Pocillopora damicornis, Goniastrea aspera, and
Acropora formosa coral were related to these results.
Heavy metals measured in coral tissues were organi-
cally bound in the polyp, mucus, and zooxanthellae,
and also included in particles adhering to the mucus.
Metals in coral skeletons were metabolised, and
precipitated in substitutional solid solution with cal-
cium. Specific aims of this study were to measure:

1. The partitioning of cadmium, lead, copper, zinc,

nickel, and chromium, between tissue and skele- Fig. 1. Sample location map.
 G. Esslemontr Marine Chemistry 71 (2000) 215–231
Fig. 2. Recent ore quantities produced by the Mount Isa and
Hilton mines. A s copper concentrate, Bs lead concentrate, C s
zinc concentrate, Ds lead–zinc concentrate.
north west of the port, which commenced operation
in 1974. Between 1993 and 1995, Yabulu processed
about 250 000 tonnes of ore annually ŽCrockett,
1996..
The extent of heavy-metal ore refinement and
shipment in the Townsville region, coupled with its
large population, means that nearby reefs and fishing
grounds are potentially exposed to anthropogenic
inputs of heavy metals. To avoid detrimental im-
pacts, harbour activities such as periodic dredging of
Platypus Channel, and effluent discharge from Yab-
ulu Refinery, are controlled under government li-
cence.
3. Methods and material studied
3.1. Field collection and sample pretreatment
Coral species were chosen for availability and
ease of sampling; G. aspera was the only species in
the harbour of sufficient size and number to be
sampled, and suitably sized branches were removed
from P. damicornis and A. formosa. Analyses of
metal variation in coral populations were based on
an optimum sample size of 15 colonies, calculated
from earlier work. Further to this, five branches from
each of five P. damicornis colonies represented
intracolony variations.
Corals, sediment, and water were collected simul-
taneously from each location between 9–15 Septem-
ber 1995. Corals were randomly sampled at water
depths - 9 m, from fringing reefs at Pioneer Bay
and Nelly Bay. At every second colony sampled,
nearby surface sediment was scraped into acid-rinsed
plastic vials, to provide a total of 10 samples per
217
location. Four surface and four bottom seawater
samples per location were collected in 1l polypropy-
lene bottles, and paired with an equal number of
field blanks Ž1l Milli-Q.. Duplicate samples of sur-
face and bottom water were filtered on site Ž0.45 mm
cellulose acetate filters., and the remaining samples
remained unfiltered. Samples were acidified with
nitric acid ŽAnalar. to about 1.9 pH.
Within Townsville Harbour, G. aspera were col-
lected from the harbour side of the western breakwa-
ter, when emergent at low tide. Because low tide
made it unnecessary to distinguish surface from bot-
tom seawater, four seawater samples were collected
beside the corals, and processed as indicated above.
Sediments were collected by Van-Veen grab from a
boat, 5 m adjacent to where corals were sampled.
Corals were transported live to nearby field sta-
tions, in two large Ž45 l., acid-rinsed, insulated plas-
tic containers filled with seawater. The corals were
briefly rinsed in distilled water, frozen overnight on
acid-rinsed plastic trays, then individually stored in
acid-rinsed plastic bags for frozen transport to South-
ern Cross University. Sediments and waters were
transported from the field on ice, and frozen for
transport to Southern Cross University.
3.2. Analyses of metals in seawater
Samples had their pH increased to about 8.2 using
sodium hydroxide before analysis by anodic strip-
ping voltammetry ŽChemtronics P.D.V. 2000.. Cor-
responding blanks received the same amount of
sodium hydroxide. Five-ml aliquots of samples or
blank were analysed in 5 ml of electrolyte buffer
ŽNASCOH: 4 M sodium chloride, 0.4 M L-ascorbic
acid, 0.39 M sodium hydroxide. to provide uniform
pH and reduced conditions during analysis. Instru-
ment plating times were 300 s.
3.3. Analyses of metals in sediment
To maximise the efficiency of comparing heavy
metal concentrations in sediments from the three
locations, readily bioavailable heavy metals removed
by weakly reactive solvents Žreactive subtotal., and
less bioavailable metals removed by strong solvents
Žtotals extracted., were sequentially extracted from
size-normalised sediments. Sediment samples were
divided into fine and coarse fractions for separate
218 G. Esslemontr Marine Chemistry 71 (2000) 215–231
¨
analyses ŽForstner and Salomons, 1980., by wet
sieving through 63-mm polyethylene mesh with arti-
ficial seawater. Samples were oven dried Ž6 days at
558C. and ground in a ceramic zirconium ring-mill.
Exchangeable heavy metals were extracted first in
barium chloride:ammonium chloride solution ŽGill-
man and Sumpter, 1986.. The procedure of Tessier
et al. Ž1979., designed to extract heavy metals from
carbonate surfaces using sodium acetate:acetic acid
solution was used for the next extraction. Of note,
metals in iron oxide coatings and reactive phases are
also extracted ŽSpan and Gaillard, 1986.. This ex-
tract is termed Areactive phases.B The procedure of
Holmgren Ž1967., which uses sodium dithionite:citric
acid solution to mobilise metals from amorphous
oxides, was used for the next extraction. Sulfides and
labile metals bound by organics may also be in-
cluded, if present. The final extract using aqua regia
represents heavy metals in residual phases, and is
termed Aresistant phasesB. This extract may include
organics that resist earlier treatment, as well as more
crystalline sulphides and oxides. Samples from all
four extracts were analysed by AAS ŽGBC 903..
Detection limits were calculated from procedural
blanks, which were processed and analysed at inter-
vals of 10.
Effective interpretation of environmental metal
loads using sediment data requires analyses of sedi-
ment matrices. This is because minor or even nonde-
tected mineral components in sediments with high
cation exchange capacities, like clays and organic
phases, may have significant bearing on metal con-
centrations measured in sediment. Sediments with
similar mineral compositions have similar capacities
to accumulate metals from surrounding environ-
ments, facilitating quantitative comparison. How-
ever, sediments with different mineral compositions
will accumulate metals in relation to different sorp-
tive capacities, making comparisons more qualita-
tive. To indicate the suitability of sediments for
comparing environmental metal loads at different
sample locations, sediment mineralogy was exam-
ined by optical microscopy and X-ray diffraction.
3.4. Analyses of metals in corals
All sample processing was done in a laminar flow
fume cabinet. Both procedures A and B from Essle-
mont Ž2000. Žextractions by water-pik or hydrogen
peroxide respectively., were used to measure heavy
metal concentrations in coral tissues, so that consis-
tency of results could be evaluated between tech-
niques. Detection limits were calculated as for sedi-
ments.
Procedure B ŽEsslemont, 2000. features a se-
quence of oxidising then reducing treatments de-
signed to selectively digest metals from the tissue
coenosarc surrounding coral skeletons, and then re-
cover metals adsorbed onto carbonate surfaces, or
precipitated as oxides, during the tissue-digestion
process. The coral skeleton, isolated from tissues and
inorganic surface coatings, is also analysed. A modi-
fied version Ždescribed below. was also used to
prepare coral skeletons for analyses after extraction
of coral tissues by procedure A, for which solutions
were discarded rather than being kept for analysis.
Coral skeletons were prepared for analysis as
follows. Samples of 4.5 " 0.2 g were sectioned to
represent recent growth Ž; 1 cm from the outer
calice for G. aspera, ; 3 and ; 7 cm from branch
tips for P. damicornis and A. formosa respectively..
These samples were placed in 50 ml test tubes, with
5 ml of hydrogen peroxide Ž9.7 M, pH adjusted to
8.2 with sodium hydroxide.. Reaction was at room
temperature Ž; 208C. for 1 h, then in a heated water
bath Ž708C. for 3.5 h. The hydrogen peroxide was
discarded, and samples rinsed with excess Milli-Q
water Ž3 = 50 ml. for 10 min in an ultrasonic bath.
The rinse was discarded, and samples were stood for
10 min at room temperature in 10 ml of reducing
chelate rinse Ž117 mM sodium diethyldithiocarba-
mate, pH f 5, 0.4 M L-ascorbic acid.. The chelate
was discarded, and samples rinsed with excess Milli
Q water as above. The sequence was repeated, with
reaction of samples in hot, pH buffered hydrogen
peroxide modified from 3.5 to 1.5 h.
After pretreatment, skeletons were ashed Ž5008C
for 15 min., weighed, then digested in 250-ml beakers
at room temperature Ž10 ml of 12 M hydrochloric
acid.. Lanthanum was added Ž5 ml of 0.18 M lan-
thanum chloride. to help analysis of zinc, nickel and
chromium by AAS, and samples were made to 25 ml
with dilute hydrochloric acid Ž12 mM..
Concentrations of cadmium, lead and copper in
skeleton digests were measured by anodic stripping
voltammetry. Aliquots of digests Ž0.3 ml. and blanks
 G. Esslemontr Marine Chemistry 71 (2000) 215–231
Ž0.2 ml. were each analysed in 10 ml of supporting
electrolyte buffer ŽNASCOH.. Instrument parameters
ŽChemtronics PDV 2000. were: plating potential
Žy1000 mV., plating time Ž300 s., hold potential
Žy900 mV., hold time Ž15 s., sweep rate Ž999., Cd
limit Žy550 mV., Pb limit Žy375 mV., Cu limit
Žy50 mV., final potential Ž0 mV., strip time Ž2 s.,
rest potential Žy100 mV.. A thick mercury plate
was precipitated using 0.3 ml of 3.68 mM mercury
ŽII. chloride solution in 5 ml Milli Q water Žrather
than the usual 0.15 ml., to counteract wear induced
by the long plating time.
3.5. Data analyses
Data were first examined to validate statistical
procedures. Metal concentrations below detection
were rounded to half the detection limits, so that
approximate values could be used. When substantial
data were below detection, statistical comparisons
were not attempted.
Specific procedures of statistical comparison are
detailed below:
To elucidate aim 1, metal concentrations in tis-
sues divided by metal concentrations in skeletons
Ži.e. wMx tissuerwMxskeleton ,., were used to obtain ratios
that can be tested by the SPSS w statistical package.
Data were compared by species and locations using
Mann–Whitney U tests, but sample sets were not
grouped to avoid confounding data with unspecified
factors. Inter species comparisons were not made for
lead or nickel, because concentrations of these met-
als were mostly too low for meaningful comparisons.
To elucidate aim 2, means, standard deviations,
and ranges of heavy metal concentrations in colonies
of P. damicornis at Nelly Bay and Orpheus Island
were measured, and tabulated.
To elucidate aim 3, environmental metal loads at
Nelly Bay, Pioneer Bay, and Townsville Harbour
were firstly measured in seawater and sediments, to
base comparisons of metal concentrations accumu-
lated by coral skeletons and tissues. Metal concentra-
tions in filtered and unfiltered seawater were com-
pared by site using Kruskal–Wallis tests Ž a s 0.05..
Individual sites were also compared using Mann–
Whitney U tests with Bonferroni correction for mul-
tiple comparisons.
Solvent extracts from size-normalised sediments
representing readily bioavailable metals Žreactive
219
subtotal., and less bioavailable metals Žtotals., were
also compared by site using Kruskal–Wallis tests
Ž a s 0.05., and significant differences were detailed
by Student’s t-tests or Mann–Whitney U tests with
Bonferroni correction for multiple comparisons. The
three sites were then ranked in order of environmen-
tal metal loads. Influences of different sediment
compositions upon this evaluation are discussed.
Metal concentrations in coral skeletons and tis-
sues were also ranked by site, to see if the same
order was followed. G. aspera was used to compare
Townsville Harbour with Pioneer Bay, and P. dami-
cornis to compare Nelly Bay with Pioneer Bay.
Statistical tests were Mann–Whitney U, or Student’s
t, where appropriate Ž a s 0.05.. Intersite differences
in the partitioning of metals between coral tissues
and skeletons, defined by tissuerskeleton ratios, were
also compared by these tests.
4. Results and analyses
4.1. HeaÕy metals in seawater
Heavy metal concentrations in filtered and unfil-
tered seawater from Nelly Bay and Pioneer Bay were
within the ANZECC Ž1992. guidelines, but lead and
copper concentrations in unfiltered seawater from
Townsville Harbour exceeded the recommended lim-
its of 24 and 79 nM, respectively ŽTable 1..
Lead and copper concentrations seemed higher in
unfiltered seawater samples than in filtered samples
at each location, except for copper in Pioneer Bay,
but differences were not significant Ž p s 0.12–0.14..
Lead and copper concentrations also seemed
higher in both filtered and unfiltered seawater from
Townsville Harbour relative to Pioneer Bay and
Nelly Bay, but differences were not significant Ž p s
0.21–0.22 filtered; p s 0.10–0.15 unfiltered..
Collectively these data are suggestive, but provide
insufficient evidence to show that lead and copper
concentrations were elevated in Townsville Harbour
seawater, or that metals were concentrated and dis-
tributed within the water column by suspended fine
sediment.
220 G. Esslemontr Marine Chemistry 71 (2000) 215–231

Table 1 Townsville Harbour ŽTable 2.. Harbour sediments

Heavy metal concentrations Žmean"1 standard deviation. in sea- contained fine quartz, feldspar, and products of tropi-
water ŽnMrl.
cal and marine weathering Žillite and kaolinite clays.,
Location Matrix n Cd Pb Cu
without measurable quantities of iron oxides or alu-
Pioneer Bay Surface water 2 -8 9"2 19"14 minium oxides despite shipping of nickel laterite.
Žfiltered.
Fine sediments Ž- 63 mm grainsize. were more
Surface water 1 -8 18 22
Žunfiltered. abundant in the harbour, and were frequently resus-
Bottom water 2 -8 4"4 -6 pended by tides and shipping activity.
Žfiltered. Metal concentrations sequentially extracted from
Bottom water 2 -8 4"1 -6 sediments are listed in Table 3. Statistical compar-
Žunfiltered.
isons ŽTable 4. showed that lead, copper, and zinc
Nelly Bay Surface water 2 -8 4.3"0.5 4.6"0.2
Žfiltered. were more biologically available in Townsville Har-
Surface water 2 -8 5.8"0.5 9"2 bour, and high concentrations of nickel, chromium,
Žunfiltered. lead, copper, and zinc were also present in less
Bottom water 2 -8 -1.5 -6 biologically available phases. Anomalous copper,
Žfiltered.
zinc, and nickel concentrations extracted from
Bottom water 2 -8 -1.5 14"14
Žunfiltered. Townsville Harbour sediment by dithionite:citric acid
Townsville Surface water 2 -8 10"5 9"2 suggest that amorphous oxide phases, such as lat-
Harbour Žfiltered. erite, may occur in quantities below threshold detec-
Surface water 2 -8 25"5 131"41 tion by XRD scans. Also of relevance, lead concen-
Žunfiltered.
trations in the less biologically available extracts
were significantly higher in sediments of Nelly Bay
relative to Pioneer Bay.
4.2. HeaÕy metals in sediment
In summary, the sediment data show that biologi-
Substrate in the neritic locations of Pioneer Bay cally available lead, copper, and zinc concentrations
and Nelly Bay were carbonate–quartz sediments, were higher in Townsville Harbour than the other
which differed substantially from sediments in two sample locations. Total concentrations of nickel

Table 2
Descriptions and mineral compositions of sorted sediment fractions
Location and size fraction
Pioneer Bay Ž) 63 mm. Ž97–100%.
Pioneer Bay Ž- 63 mm. ŽF 3%.
Nelly Bay Ž- 63 mm. Ž97–100%.
Nelly Bay Ž) 63 mm. ŽF 3%.
Townsville Harbour Ž) 63 mm. Ž44–83%.
Townsville Harbour Ž- 63 mm. Ž13–55%.
Mineral description
Grey, subangular to rounded bioclastic sand. Poor to very well sorted,
fine to coarse grain bioclasts Žmolluscs, foraminifera, echinoderms, coral,
coralline algae.. wXRD analysis: F 45% calcite, F 33% Mg calcite,
35–62% aragonite, 5–30% quartzx.
Grey-brown silt.
Grey to tan, subangular bioclastic to rounded quartz sand. Very poor to
well sorted, medium to very coarse grain bioclasts Žmolluscs, foraminifera,
echinoderms, coral, coralline algae.. wXRD analysis: 4–55% calcite,
F 42% Mg calcite, F 38% aragonite, 9–85% quartz, F 11% albitex.
Grey-brown silt.
Tan, subangular to rounded clayey sand. Well to very well sorted, fine to
very fine grainsize, with very few bioclasts Žforaminifera, molluscs,
sponge spicules.. wXRD analysis: 61–80% quartz, 10–19% albite,
6–15% illite, 1–8% kaolinitex.
Grey-brown silt. wXRD analysis: 37–71% quartz, 10–23% albite, 7–30%
illite, 8–15% kaolinitex.
 G. Esslemontr Marine Chemistry 71 (2000) 215–231 221

Table 3
Heavy metal concentrations in sediment ŽnMrg dry weight.
Exchangeable Reactive phases Reactive subtotal Dithionite: citric Resistant phases Total
acid extract
Cd
Pioneer Bay F 0.18 0.44 " 0.36 0.09–0.98 - 2.58 1.07 " 1.33 0.09–5.97
Nelly Bay F 0.27 1.25 " 0.98 0.27–2.49 - 2.58 - 0.98 0.35–6.05
Townsville Ž) 63 mm. - 2.58 - 0.98 - 3.56 F 0.27 0.62 " 0.27 0.35–4.71
Townsville Ž- 63 mm. 0.36 " 0.18 0.62 " 0.27 0.53–1.42 - 2.67 F 2.05 0.53–6.13

Pb
Pioneer Bay - 1.64 - 2.65 - 4.29 - 2.94 8.69 " 1.50 7.19–16.5
Nelly Bay - 1.98 F 4.30 F 6.27 F 3.28 20.0 " 6.23 13.7–35.8
Townsville Ž) 63 mm. F 2.17 42.3 " 10.2 32.0–54.5 7.67 " 4.25 49.1 " 14.7 70.3–130
Townsville Ž- 63 mm. - 1.98 50.0 " 7.0 43.1–58.9 F 5.21 113.2 " 14.3 142–192

Cu
Pioneer Bay - 2.52 1.42 " 0.79 0.63–4.72 F 6.14 8.50 " 1.10 8.03–20.5
Nelly Bay - 3.15 1.10 " 0.79 0.31–5.04 6.45 " 3.30 5.04 " 2.05 6.45–21.9
Townsville Ž) 63 mm. - 2.99 21.1 " 4.09 17.0–28.2 69.9 " 13.1 242.3 " 68.3 249–422
Townsville Ž- 63 mm. F 3.62 30.5 " 7.71 22.8–41.9 97.9 " 13.2 524.8 " 81.0 551–759

Zn
Pioneer Bay - 5.51 F 6.88 F 12.4 - 3.67 27.38 " 3.67 23.7–47.1
Nelly Bay - 6.58 F 5.96 F 12.5 5.81 " 6.27 40.8 " 19.0 21.4–84.4
Townsville Ž) 63 mm. - 6.58 236.3 " 42.7 194–286 333 " 36.1 727 " 157 1060–1545
Townsville Ž- 63 mm. - 6.58 276.3 " 50.9 225–333 518.8 " 55.2 1277 " 84.3 1881–2264

Ni
Pioneer Bay - 3.92 - 15.7 - 19.6 - 15.0 23.2 " 6.47 16.7–64.2
Nelly Bay F 5.62 - 21.1 - 26.8 F 26.4 11.1 " 5.62 5.45–69.9
Townsville Ž) 63 mm. - 4.60 - 20.8 - 25.4 80.6 " 24.9 124.2 " 29.5 150–285
Townsville Ž- 63 mm. F 6.30 F 60.5 F 66.8 130.5 " 37.0 291.7 " 26.1 360–552

Cr
Pioneer Bay - 36.9 - 34.0 - 71.0 - 53.5 59.0 " 32.7 2.64–215
Nelly Bay - 45.0 - 46 - 91.0 - 68.1 39.4 " 25.4 14.0–223
Townsville Ž) 63 mm. F 52.9 - 45.2 F 98.1 - 53.9 152.3 " 40.4 112–344
Townsville Ž- 63 mm. - 44.2 - 45.8 - 90.0 - 54.0 160.0 " 20.0 140–325

Data presented here are available as tables of individual values ŽEsslemont, 1998..

Table 4
Rankings of sediment-bound metal concentrations by site ŽKruskal–Wallis and Mann–Whitney U tests.
Available fraction Cd Pb Cu
Bioavailable T Harb s N Bay s P Bay T Harb ) N Bay s P Bay T Harb ) N Bay s P Bay
Total T Harb s N Bay s P Bay T Harb ) N Bay ) P Bay T Harb ) N Bay s P Bay

Zn Ni Cr
Bioavailable T Harb ) N Bay s P Bay T Harb s N Bay s P Bay T Harb s N Bay s P Bay
Total T Harb ) N Bay s P Bay T Harb ) N Bay s P Bay T Harb ) N Bay s P Bay

Symbols: s represent no significant differences. - and ) represent significant differences Ž a s 0.05.. < and 4 represent highly
significant differences Ž a s 0.01..
222 G. Esslemontr Marine Chemistry 71 (2000) 215–231

and chromium were also higher in Townsville Har-
bour sediment, but were in stable, relatively nonreac-
tive phases and not readily accessible to biota.
4.3. HeaÕy metals in coral
Heavy metal concentrations in coral tissues and
skeletons from Pioneer Bay, Nelly Bay, and
Townsville Harbour are listed in Table 5. Metal
concentrations measured in tissues differed with ex-
traction procedure, and consequently different con-
clusions were sometimes reached in the comparisons,
but both results are presented. Procedure A is better
for biological interpretation, because it gives fully
quantitative measurements of heavy metal concentra-
tions in coral tissues, but incomplete removal of
tissue filaments in A. formosa by this procedure
requires consideration.
Tissues of P. damicornis extracted by procedure
A have similar metal concentrations in Nelly Bay
and Pioneer Bay, indicating similar levels of biologi-
cal accumulation. This corresponds with similar bio-
logical availabilities of metals at both locations evi-
dent in sediment data. Results obtained by procedure
B support these conclusions, except that chromium is
more concentrated in tissues of Pioneer Bay coral
ŽTable 6.. However skeletons of this species provide
an interesting contrast: higher concentrations of cop-
per and zinc, and lower concentrations of nickel, are
accumulated by skeletons of Nelly Bay corals.
Intersite comparisons of G. aspera tissues Žproce-
dure A. from Townsville Harbour and Pioneer Bay,
indicated higher concentrations of copper and zinc,
and lower concentrations of cadmium, nickel, and
chromium, in harbour corals. There was no intersite
difference for lead ŽTable 6.. Results obtained by
procedure B generally support these conclusions, but
intersite differences were not observed for nickel and
chromium. Intersite comparisons using skeletons
showed higher concentrations of cadmium, lead,
copper, zinc and chromium in harbour corals, and no
intersite difference for nickel.
Corals concentrate heavy metals in tissues relative
to skeletons, with evidence for site effects upon
partitioning of metals between tissues and skeletons
ŽTable 7.. Both tissue extraction procedures provided
generally consistent results: metal ratios Žcadmium,
lead, zinc, and chromium. between tissues and skele-
tons were lower in Townsville Harbour than in Pio-
neer Bay. Ratios of copper and zinc between tissues
and skeletons were lower in Nelly Bay than Pioneer
Bay, but ratios of nickel and chromium between

Table 5
Heavy metal concentrations in coral skeletons and tissues extracted by procedures A Žwater-pik. and B Žhydrogen peroxide., ŽnMrg, dry
weight.
Location Species Matrix n Cd Pb Cu Zn Ni Cr
Pioneer Bay G. aspera Tissues ŽA. 20 29 " 4 33 " 10 153 " 44 1947 " 754 813 " 411 2119 " 471
Tissues ŽB. 19 7.1 " 1.8 17 " 5 71 " 14 190 " 81 187 " 58 398 " 133
Skeletons 20 - 0.09 0.33 " 0.14 3.0 " 0.8 F 28 34 " 7 F 29
P. damicornis Tissues ŽA. 19 25 " 9 36 " 11 164 " 44 1972 " 280 - 1056 1152 " 415
Tissues ŽB. 19 - 23 - 22 41 " 9 436 " 77 191 " 56 767 " 171
Skeletons 19 - 0.09 - 0.24 1.6 " 0.3 F 23 31 " 10 44 " 33
Nelly Bay A. formosa Tissues ŽA. 11 39 " 14 F 78 183 " 80 3620 " 1849 F 4,243 1002 " 508
Tissues ŽB. 10 26 " 6 - 46 47 " 8 678 " 141 337 " 99 1246 " 492
Skeletons 17 0.18 " 0.09 F 0.24 1.9 " 0.6 21 " 8 53 " 12 67 " 21
P. damicornis Tissues ŽA. 11 F 53 52 " 24 208 " 76 3200 " 1003 4,197 " 4,570 1819 " 806
Tissues ŽB. 19 5.3 " 0.9 F 11 33 " 13 577 " 182 155 " 32 494 " 40
Skeletons 19 - 0.09 0.19 " 0.10 5.5 " 1.6 37 " 8 10 " 7 F 21
Townsville G. aspera Tissues ŽA. 15 F 18 49 " 17 579 " 94 13,761 " 5534 356 " 157 1071 " 281
Harbour Tissues ŽB. 15 - 19 43 " 32 437 " 183 3380 " 1614 233 " 89 285 " 90
Skeletons 15 0.09 " 0.09 8.2 " 1.7 14 " 4 447 " 112 32 " 15 31 " 21

Data presented here are available as tables of individual values ŽEsslemont, 1998..
 G. Esslemontr Marine Chemistry 71 (2000) 215–231 223

Table 6
Rankings of heavy metal concentrations in coral from different sites ŽStudent’s t or Mann–Whitney U tests.
Cd Pb Cu Zn Ni Cr
P. damicornis
Tissue Žprocedure A. N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay s P Bay
Tissue Žprocedure B. N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay s P Bay N Bay - P Bay
Skeleton N Bay s P Bay N Bay s P Bay N Bay ) P Bay N Bay ) P Bay N Bay - P Bay N Bay s P Bay

G. aspera
Tissue Žprocedure A. T Harb - P Bay T Harb s P Bay T Harb ) P Bay T Harb ) P Bay T Harb - P Bay T Harb - P Bay
Tissue Žprocedure B. T Harb - P Bay T Harb s P Bay T Harb ) P Bay T Harb ) P Bay T Harb s P Bay T Harb s P Bay
Skeleton T Harb ) P Bay T Harb ) P Bay T Harb ) P Bay T Harb ) P Bay T Harb s P Bay T Harb ) P Bay

Symbols are as for Table 4.

tissues and skeletons were higher in Nelly Bay than
in Pioneer Bay.
There were interspecific differences in the parti-
tioning of heavy metals between tissues and skele-
tons, observed in A. formosa and P. damicornis at
Nelly Bay, and in G. aspera and P. damicornis at
Pioneer Bay ŽTable 7.. However, results differed
with tissue recovery procedure. For reasons outlined
in Esslemont Ž2000., procedure A allows better com-
parison between massive species, and species with
surface rather than filamentous tissues Že.g. G. as-
pera and P. damicornis.. Procedure A indicated that
G. aspera partitioned more cadmium and chromium,
and less copper, into tissues relative to skeletons than
did P. damicornis. Procedure B allows better com-
parison between P. damicornis and A. formosa,
because tissue filaments in A. formosa are included.
Procedure B indicated that A. formosa partitioned
more cadmium, copper and zinc in tissues relative to
skeletons than did P. damicornis.
Heavy metal concentrations in P. damicornis
colonies from Pioneer Bay and Nelly Bay are listed

Table 7
Statistical comparisons of metal partitioning between tissues and skeletons
Cd Pb Cu Zn Ni Cr
Intersite comparisons of metal ratios (tissuer skeletons by species)
Procedure A
G. aspera TH - PB TH - PB TH s PB TH - PB TH s PB TH - PB
P. damicornis NB s PB NB s PB NB - PB NB - PB NB ) PB NB s PB
Procedure B
G. aspera TH - PB TH - PB TH s PB TH - PB TH s PB TH - PB
P. damicornis NB s PB NB s PB NB - PB NB - PB NB ) PB NB ) PB

Interspecies comparisons of metal ratios (tissue r skeletons by location)

Procedure A
Pioneer Bay Ga ) Pd n.a. Ga - Pd Ga s Pd n.a. Ga ) Pd
Nelly Bay Pd s Af n.a. Pd s Af Pd s Af n.a. Pd ) Af
Procedure B
Pioneer Bay Ga ) Pd n.a. Ga s Pd Ga - Pd n.a. Ga s Pd
Nelly Bay Pd - Af n.a. Pd - Af Pd - Af n.a. Pd s Af

Symbols are as for Table 4, with TH s Townsville Harbour, NB s Nelly Bay, PB s Pioneer Bay, Ga s G. aspera, Pd s P. damicornis,
Af s A. formosa, n.a.s not assessed.
224 G. Esslemontr Marine Chemistry 71 (2000) 215–231

in Tables 8 and 9. Ranges of metal concentrations 5. Discussion

within some colonies almost matched the range in
the coral population, but were insubstantial within 5.1. HeaÕy metals in seawater
other colonies Žfor example the intracolony range of
copper concentrations in skeletons from Pioneer Seawater concentrations of cadmium, lead, and
Bay.. It should be noted that metal concentrations in copper in Orpheus Island and Nelly Bay were within
skeletons were very low, and net concentration dif- the ANZECC Ž1992. guidelines, and resembled con-
ferences were therefore small. centrations in filtered seawater measured by earlier
Table 8
Heavy metal concentrations ŽnMrg. in tissues of P. damicornis, represented by colonies and populations
Procedure A Procedure B
n Mean Standard Range n Mean Standard Range
deviation deviation
Pioneer Bay Pioneer Bay
Cd Cu
Population 15 23.1 14.2 55.1 Population 19 42.5 18.9 59.8
Colony 1 4 57.8 15.1 34.6 Colony 3 6 48.9 1.57 6.29
Colony 2 4 66.7 18.6 41.8 Colony 4 6 47.2 14.2 34.6
Pb Zn
Population 15 39.1 20.8 70.9 Population 19 439 158 158
Colony 1 4 78.2 56.0 116 Colony 1 6 477 165 165
Colony 3 4 63.7 50.7 111 Colony 2 6 534 121 121
Cu Ni
Population 15 156 86.6 340 Population 19 191 116 434
Colony 1 4 127 58.2 135 Colony 1 6 434 250 591
Colony 2 4 134 28.3 67.7 Colony 2 6 394 250 634
Zn Cr
Population 15 1972 561 2095 Population 19 767 354 1356
Colony 1 5 1831 815 2043 Colony 3 6 762 354 915
Colony 4 3 1982 390 780 Colony 4 6 706 86.5 206
Cr Nelly Bay
Population 15 1152 752 2454 Cd
Colony 1 4 683 404 404 Population 19 5.34 2.67 7.12
Colony 2 4 1548 217 217 Colony 3 4 5.34 2.67 4.49
Nelly Bay Colony 4 5 5.34 0.89 1.78
Cu Cu
Population 11 252 118 406 Population 19 31.5 26.8 94.4
Colony 1 4 247 164 362 Colony 2 4 14.2 7.87 18.9
Colony 4 2 362 156 220 Colony 4 5 22.0 4.72 14.2
Zn Zn
Population 11 3850 1785 5385 Population 19 577 378 1721
Colony 2 2 3905 635 898 Colony 1 5 685 350 772
Colony 3 5 4171 1930 4665 Colony 2 3 258 21.4 38.2
Cr Ni
Population 11 2110 1444 4146 Population 19 155 66.5 300
Colony 1 3 1358 565 1125 Colony 3 4 169 80.1 187
Colony 3 2 625 700 990 Colony 4 5 177 78.4 198
Cr
Population 19 494 325 1073
Colony 1 5 846 288 677
Colony 4 5 612 706 1021

For brevity, only colonies that show the full extent of intracolony metal variation encountered in each population are listed. Note also that
some metals are not represented where concentrations were below detection.
 G. Esslemontr Marine Chemistry 71 (2000) 215–231 225

Table 9 than concentrations for unfiltered seawater measured

Heavy metal concentrations ŽnMrg. in skeletons of P. damicor- by Jones Ž1992.. Of relevance to this difference,
nis, represented by colonies and populations
seawater sampled for this study was collected against
n Mean Standard Range
the breakwater where metal-bearing sediment was
deviation
suspended by tidal backwash, and continually circu-
Pioneer Bay
lated over corals.
Cu
Population 19 1.57 0.79 2.36 This study is suggestive that concentrations of
Colony 3 5 1.73 0.31 0.63 lead and copper were slightly, but not significantly,
Colony 4 5 1.73 0.79 2.36 higher in unfiltered seawater because suspended,
Ni metal-bearing fine sediment was present. These ob-
Population 19 31.2 20.8 65.4
servations correspond with earlier works that associ-
Colony 1 5 8.18 5.79 11.1
Colony 2 5 16.4 20.6 47.4 ate copper and zinc with suspended matter, to which
Cr the presence of Trichodesmium algae is an important
Population 19 44.2 69.6 213 cofactor ŽJones, 1992.. Suspended sediment is a
Colony 3 5 11.0 14.8 34.2 small fraction of bulk seawater, but represents a
Nelly Bay concentrated source of biologically available metals
Cu that adheres to mucosal coral surfaces. Hence, sus-
Population 19 5.51 3.30 11.2 pended sediment is an important transport medium
Colony 1 5 2.04 0.79 1.89 for transferring heavy metals to corals in Townsville
Colony 3 4 4.72 4.72 10.5
Harbour, and has been shown to transfer metals to
Zn
Population 19 37.8 15.0 52.9 coral surfaces elsewhere in Halifax Bay as discussed
Colony 1 5 10.7 0.76 1.84 below.
Colony 3 4 23.7 9.02 20.3
Ni 5.2. HeaÕy metals in sediment
Population 19 10.4 12.4 34.9
Colony 3 4 36.3 10.9 26.2
Colony 4 5 9.54 8.35 18.2 The mineral compositions of Nelly Bay and Pio-
neer Bay sediments were sufficiently similar for
Caption as for Table 8. quantitative comparison, although coarse-grained
carbonate–quartz mineral surfaces are poor accumu-
lators of heavy metals other than lead ŽTalbot and
workers ŽBurdon-Jones et al., 1982; Jones 1992.. Chegwidden, 1983.. In contrast, fine-grained, fre-
Burdon-Jones et al. Ž1982. measured significantly quently resuspended clays in the harbour accumulate
higher zinc concentrations in filtered seawater from heavy metals efficiently, and will naturally concen-
Townsville Harbour relative to their control site ¨
trate heavy metals ŽForstner and Salomons, 1980..
ŽTicklebelly Bay., but concentrations of cadmium, Therefore comparisons of metal loads in the different
lead, copper, and nickel were similar at both sites. neritic and harbour sediments are qualitative.
Concentrations of copper and zinc reported by Jones Concentrations of reactive heavy metals in sedi-
Ž1992. appeared higher in filtered and unfiltered ments show that lead, copper, and zinc were signifi-
waters of Townsville Harbour relative to Cleveland cantly more available to biota in Townsville Harbour
Bay, as did particle-bound nickel, but statistical com- than in Nelly Bay or Pioneer Bay, with no significant
parisons were not done in that study. differences between the latter two sites. Furthermore,
Concentrations of dissolved lead and copper in Townsville Harbour sediment featured high concen-
Townsville Harbour were similar or slightly higher trations of nickel and chromium in stable, relatively
than concentrations measured by earlier workers, and nonreactive phases, which may have been small
were within the ANZECC Ž1992. guidelines. How- amounts of amorphous oxides as naturally occurring
ever, concentrations of lead and copper in unfiltered laterite, or nickel laterite ore spilt into the harbour.
seawater exceeded recommended limits, and copper Lead was also concentrated in relatively non reactive
concentrations measured in this study were higher sediment phases of Nelly Bay than Pioneer Bay.
226 G. Esslemontr Marine Chemistry 71 (2000) 215–231
Within Townsville Harbour, total lead, copper, zinc,
and nickel, and reactive lead, copper, and zinc were
concentrated in the fine sediment fraction. This frac-
tion is most relevant to metal transport, because it is
frequently mobilised by tidal, shipping, and dredging
activities.
Heavy metal behaviour in the marine sediments of
Halifax Bay can be interpreted by linking this study
to the work of Reichelt and Jones Ž1994.. Direct
comparisons of data reported by both studies are
precluded by the different extraction procedures used,
but observations of metal concentrations and
bioavailability were generally similar. Relative to
Cleveland Bay sites, Reichelt and Jones Ž1994. re-
ported high total zinc, lead, and nickel concentra-
tions in harbour sediments, and high total zinc in
Platypus Channel sediments. Dredging along Platy-
pus Channel during 1991 generated sediment plumes
that impinged on fringing reefs along the southeast-
ern side of Magnetic Island, with disturbances due to
dredging waning northward. Metal-bearing fine sedi-
ments were deposited onto coral surfaces, and conse-
quently reefs near Nelly Bay experienced elevated
concentrations of labile copper and zinc for between
1 and 3 months, before tidal action diluted sediments
to pre-dredging concentrations. Nickel showed little
variation during the whole dredging program.
Collectively, this study with Reichelt and Jones
Ž1994. indicates that reactive, biologically available
lead, copper, and zinc phases are concentrated in fine
sediments of Townsville Harbour, which are resus-
pended during dredging of the harbour and Platypus
Channel. Reefs adjacent to Magnetic Island are thus
subject to intermittent turbidity, when fine sediments
rich in labile copper and zinc are periodically de-
posited on corals. Fine sediments do not usually
persist in coral reef environments Žthey constitute
less than 3% of Nelly Bay or Pioneer Bay sediments.,
so periods of intermittent heavy metal influx are not
recorded. These observations correspond with an-
other work that shows calcareous, inner-neritic sedi-
ment of this nature to be poor recorders of heavy
metals ŽTalbot and Chegwidden, 1983..
5.3. HeaÕy metals in corals
Higher concentrations of heavy metals partitioned
into coral tissues relative to skeletons, as was ob-
served by McConchie and Harriott Ž1992.. Levels of
partitioning varied with species, indicating differ-
ences that may result from: Ža. varied efficiencies of
metal transfer from tissue to skeleton by different
species, Žb. varied tolerances of certain metals by
different species Žwhere tissue concentrations may be
regulated, as discussed later., or Žc. simply that
different species had different amounts of zooxan-
thellae at the time of sampling, where zooxanthellae
are known to assimilate certain metals ŽHarland and
Nganro, 1990; Harland et al., 1990.. These interspe-
cific differences may not be consistent if zooxanthel-
lar activities and metal uptake patterns change over
space and time. Although coral eggs are rich in trace
metals ŽReichelt-Brushett, 1998., it is unlikely in this
case that interspecific variation is influenced by dif-
ferent reproductive states of corals. Mass spawning
in the Townsville region is synchronous across coral
species ŽHarrison et al., 1984., therefore reproduc-
tive states will be similar regardless of species.
Heavy metal concentrations bound by tissues and
skeletons varied substantially within some colonies
of P. damicornis at Pioneer Bay and Nelly Bay, but
only slightly within other colonies. Possible reasons
for heterogeneity may include: Ž1. metal concentra-
tions may have been skewed within a colony to the
side experiencing highest growth, Ž2. metal-rich par-
ticles may have adhered to mucus on the side facing
upcurrent, or may settle on horizontal surfaces as
was observed by Reichelt and Jones Ž1994., and Ž3.
there may have been irregular distributions of
metal-bearing phases within coral colonies Že.g. more
zooxanthellae on surfaces facing light.. With respect
to the first possible reason, it has been demonstrated
that corals transport calcium and soluble organic
compounds within a colony to areas of highest growth
such as branch tips ŽTaylor, 1977.. It is likely that
essential trace metals, such as zinc which is com-
monly used for protein synthesis and repair ŽBeyers-
mann, 1994., would also be transported to portions
experiencing high growth.
Ranges of heavy metal concentrations between P.
damicornis colonies exceeded ranges measured
within colonies, though not always by much. Inter-
colony ranges of metal concentrations were one to
five times the sample means accumulated by these
populations, and population distributions were often
skewed.
 G. Esslemontr Marine Chemistry 71 (2000) 215–231
This investigation supports earlier studies that
show corals record environmental heavy metal loads
ŽDelaney et al., 1993; Shen and Boyle, 1987, 1988;
Shen and Sanford, 1990; Linn et al., 1990., but there
were cases where metal concentrations in coral
skeletons and tissues did not correspond with envi-
ronmental loads, as discussed later. Sediments and
waters of Townsville Harbour showed elevated con-
centrations of bioavailable lead, copper, and zinc,
which were represented in skeletons of G. aspera.
Sediments also showed that reactive nickel concen-
trations in Townsville Harbour and Pioneer Bay
were similar, and correspondingly nickel in G. as-
pera skeletons was similar at both locations.
Cadmium and chromium concentrations in skele-
tons of G. aspera were higher in Townsville Har-
bour than in Pioneer Bay. However, effective mea-
surement of these metals was hampered by naturally
low cadmium concentrations, and poor analytical
detection limits for chromium. Hence it is unclear
whether increased uptake resulted from higher envi-
ronmental metal concentrations, metal speciation as-
sociated with the river mouth location, or environ-
mental stresses caused by harbour conditions. It is
likely that turbid harbour conditions increase cad-
mium and chromium loads, through increased net
quantities of metal-bearing fine sediment. Interest-
ingly, higher concentrations of cadmium, nickel and
chromium were recorded in coral skeletons sampled
furthest into the harbour.
Data from seawater, and extracts of reactive sedi-
ment phases, showed similar concentrations of bio-
logically available heavy metals in Nelly Bay and
Pioneer Bay. Despite this, copper and zinc concen-
trations in coral skeletons from Nelly Bay were
higher, and nickel concentrations lower, than in
skeletons from Pioneer Bay. A potential explanation
is that corals in Nelly Bay record intermittent copper
and zinc anomalies caused by dredging, whereas
coarse-grained, calcareous sediments associated with
the hard-ground reef habitat do not. However at this
stage, there is no obvious reason for greater inclusion
of nickel into coral skeletons at Pioneer Bay than at
Nelly Bay. Previously high nickel availability due to
natural fluxes, or more subtle environmental factors
that influence the biological availability of nickel
Že.g. metal speciation, turbidity and diet., may be
relevant.
227
Heavy metal concentrations in coral tissues did
not always correspond with concentrations observed
in skeletons, or with environmental metal loads. G.
aspera tissues recorded high copper and zinc concen-
trations in Townsville Harbour relative to Pioneer
Bay and Nelly Bay, but high lead concentrations in
harbour sediment were not recorded by tissues de-
spite being clearly recorded by skeletons. Further-
more, cadmium and chromium in G. aspera tissues
from Townsville Harbour were less concentrated than
in tissues from Pioneer Bay, contrasting directly with
results measured in skeletons. Nickel was also no-
table because patterns of bioaccumulation by G.
aspera tissues Žprocedure A. contrasted with skele-
tons and evident environmental loads. Nickel con-
centrations in tissues were lower in the harbour than
in Pioneer Bay, contrasting with uniform concentra-
tions in skeletons and reactive sediment phases from
both locations.
Heavy metal concentrations in tissues of P. dami-
cornis corals from Pioneer Bay and Nelly Bay corre-
sponded with sediment and water data, suggesting
similar contemporary metal concentrations at both
locations, except that chromium was more concen-
trated in tissues from Pioneer Bay Žprocedure B..
Notably, the different concentrations of copper, zinc,
and nickel in skeletons from Pioneer Bay and Nelly
Bay already discussed, were not observed in tissues.
Patterns of metal uptake by coral tissues and
skeletons differed by metal, in response to environ-
mental loads. G. aspera in Townsville Harbour as-
similated high concentrations of lead and zinc in
their skeletons in response to high environmental
availability of these metals. However, lead and zinc
were concentrated proportionally less in tissues rela-
tive to skeletons. Copper was proportionally similar
in coral tissues and skeletons at both locations, and
both tissues and skeletons recorded high copper con-
centrations in Townsville Harbour. Partitioning of
lead contrasted markedly with copper: lead parti-
tioned differently between tissues and skeletons at
the two locations, whereas copper partitioning be-
tween tissues and skeletons was unaffected by envi-
ronmental loads.
Metal assimilation by coral skeletons show a re-
sponse to increased availability of absorbed lead and
zinc. Tissue–metal concentrations appear to be regu-
lated, possibly by preferential transport of metals
 228
G. Esslemontr Marine Chemistry 71 (2000) 215–231
Table 10
Means Žparentheses. and ranges of heavy metal concentrations ŽnMrg., in brown algae and oysters from the Townsville Harbour precincts
Site Organism Cd Pb Cu Zn Ni Cr References
Townsville Harbour Brown algae: 1.8–5.3 9.7–48 629–173 1025–2539 12–95 – Burdon-Jones
P. tenuis et al. Ž1982.
Halifax Bay P. tenuis 1.8–12 0.5–26 22–69 57–459 15–143 –

Townsville Harbour Rock oyster: 0.9–7.1 Ž3.6. 1.5–8.7 Ž3.9. 189–1196 Ž456. 7648–23,402 Ž15,999. 10–22 Ž17. 1.9–21.2 Ž9.6. Esslemont
Saccostrea sp. Žunpublished.
Magnetic Island Saccostrea sp. F 0.9 0.5–1.9 Ž1.5. 47–142 Ž110. 4894–13,613 Ž9361. 12–49 Ž27. 3.8–19.2 Ž9.6.
Townsville Harbour S. amassa 8.9–107 Ž38. – 7868–50,357 Ž25,729. 10,249–321,199 Ž126,185. 6.8–307 Ž61. – Jones Ž1992.

Metal concentrations in Padina tenuis ŽBurdon-Jones et al., 1982. and Saccostrea amassa ŽJones, 1992. are reported on a dry-weight basis. Saccostrea sp. ŽEsslemont,
unpublished. is reported on a wet-weight basis.
 G. Esslemontr Marine Chemistry 71 (2000) 215–231
into skeletons, or by elimination of metals from
tissues. The disparate concentrations of cadmium and
chromium in tissues and skeletons of G. aspera
coral from Townsville Harbour and Pioneer Bay may
also have resulted from regulation. Interestingly, G.
aspera did not respond to increased copper availabil-
ity by reducing tissue concentrations of this metal
relative to skeleton as was observed for lead and
zinc, suggesting that tolerance limits of tissues to
copper were not reached. The bioavailable copper
concentrations in fine harbour sediment were sub-
stantially lower than concentrations of lead and zinc.
A potential regulatory mechanism used by corals
may include zooxanthellar expulsion ŽHarland and
Brown, 1989., as demonstrated for cadmium, copper,
and zinc in the coelenterate Anemonia Õiridis ŽHar-
land and Nganro, 1990; Harland et al., 1990.. This
process was not investigated here, but the response
of G. aspera to high availabilities of lead and zinc is
interesting. Lead is considered toxic ŽBeyersmann,
1994., whereas zinc is an essential micronutrient
ŽBrown and Howard, 1985.. G. aspera appears to
tolerate zinc better than lead because zinc is not as
strongly eliminated from tissues, notwithstanding the
higher availability of zinc in the reactive phases of
fine harbour sediment.
Patterns of metal uptake by corals in response to
high environmental loads within Townsville Harbour
are supported by studies using other indicator organ-
isms ŽBurdon-Jones et al., 1982; Jones, 1992., shown
in Table 10. Rock oysters collected from the
Townsville Harbour seaward breakwater and Mag-
netic Island during a preliminary survey in March
1993, showed increased uptake of cadmium, copper,
zinc Žtwo tailed Student’s t-test assuming unequal
variance, p - 0.05., and lead Ž p - 0.1. at Townsville
Harbour. Uptake of nickel and chromium was similar
at both sites.
This study supports the use of coral skeletons
over tissues for measuring environmental loads of
copper, lead, and zinc, because skeletons appear to
represent environmental metal loads more faithfully.
Furthermore, skeletons are easier to collect, smaller
samples are required, and analysis is cheaper. Multi-
ple small Že.g. 1–2 g. samples can be removed from
a colony, leaving most of it intact. Coral tissues are
suitable for bioassays of a limited range of metals
Žcopper and zinc..
229
6. Conclusions
Ž1. Partitioning of heavy metals between coral
tissues and skeletons varied with species. In Pioneer
Bay, G. aspera partitioned more cadmium and
chromium, and less copper, into tissues relative to
skeletons than P. damicornis. In Nelly Bay A. for-
mosa partitioned more cadmium, lead, and zinc into
tissues relative to skeletons than P. damicornis.
Ž2. Heavy metal concentrations in tissues and
skeletons of coral colonies varied substantially within
some colonies, but were uniform within other
colonies of the same population. Reasons for incon-
sistent levels of variation were unclear, but may have
included growth factors, and irregular distributions
of particles or metal-bearing phases in coral colonies.
Heavy metal concentrations varied more in popula-
tions than in colonies, though not always by much,
and population distributions were often non-normal.
Ž3. G. aspera responded to high concentrations of
biologically available lead, copper, and zinc at
Townsville Harbour by including more of these met-
als in their skeletons. Cadmium and chromium were
similarly included, but whether this response related
to increased environmental concentrations or harsher
environmental conditions is uncertain, and turbid
conditions may have been influential. Regulation of
cadmium, lead, zinc, and chromium by tissues was
implied by lower concentrations of these metals in
tissues versus skeletons, in G. aspera from the har-
bour relative to the control site. Copper ratios be-
tween G. aspera tissues and skeletons were similar
at Townsville Harbour and the control site, showing
that regulation did not occur, but threshold concen-
trations of copper tolerated by tissues may not have
been reached.
P. damicornis skeletons recorded high copper and
zinc loads at Nelly Bay, possibly caused by periodic
dredging activities. Notably, these episodes were not
recorded in surface sediments or coral tissues, which
indicated uniform metal availability in Nelly Bay
and Pioneer Bay at the time of sampling. Nickel
concentrations were elevated in skeletons at Orpheus
Island without obvious reason, and factors other than
total nickel concentrations may be relevant.
Ž4. Skeletons are recommended over tissues for
monitoring purposes because they represent environ-
mental metal loads more faithfully, are easier to
230 G. Esslemontr Marine Chemistry 71 (2000) 215–231
collect, involve smaller samples, and are cheaper to
analyse. Multiple, small skeleton samples can be
removed from a colony and homogenised for better
representation, leaving most of the colony intact.
Coral tissues can be used for bioassays of copper and
zinc, which are accumulated by tissues in relation to
availability possibly because they provide useful bio-
chemical functions.
Acknowledgements
Site selection benefited from advice given by Ray
Berkelmans and Jamie Oliver. Assistance in the field
was given by Karen McGoogan, and in the labora-
tory by Richard Bush and Geoff Kerr. Dr. Graham
Jones allowed use of laboratory facilities, and Dr.
Vicki Harriott confirmed coral identification. Colleen
Hanahan and Geoff Kerr reviewed the manuscript.
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