Antifoulant (butyltin and copper) concentrations in sediments from

the Great Barrier Reef World Heritage Area, Australia

David Haynes*, Dominica Loong1

Great Barrier Reef Marine Park Authority, PO Box 1379, Townsville 4810, Australia

Received 31 May 2001; accepted 31 December 2001

‘‘Capsule’’: Antifoulant concentrations are generally low in the Great Barrier Reef, although ship grounding sites present

a previously unidentified significant source of antifoulant pollutants in the Great Barrier Reef.

Abstract

Antifoulant concentrations were determined in marine sediments collected from commercial harbours, marinas, mooring locations on mid-shelf continental islands, and outer reef sites in four regions within the Great Barrier Reef World Heritage Area in

1999. Highest copper concentrations were present in sediments collected from commercial harbour sampling sites (28–233 mg Cu

g1 dry wt.). In contrast, copper concentrations in sediments collected from boat mooring sites on mid-shelf continental islands and

outer reef sites were at background concentrations (i.e. <20 mg Cu g1 dry wt.). Butyltin was only detectable in four of the 42

sediments sampled for analysis, and was only present in sediments collected from commercial harbours (18–1275 ng Sn g1 dry wt.)

and from marinas (4–5 ng Sn g1 dry wt.). The detection of tributyltin at marina sites implies that this antifoulant may continue to

be used illegally on the hulls of smaller recreational vessels. Sediment samples were also collected opportunistically from the site of a

22,000 t cargo ship grounding in May 1999 at Heath Reef, in the far northern Great Barrier Reef. Butyltin concentrations were

grossly elevated (660–340,000 ng Sn g1 dry wt.) at the grounding site. The impact of residual antifoulants at large ship grounding

sites should be recognised as a significant, long-term environmental problem unless antfoulant clean-up strategies are undertaken.

# 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Copper; Great Barrier Reef; Harbours; Ship grounding; TBT

1. Introduction

Organotin compounds are potent toxins, and this

property has lead to their use in a range of biocides

including ship antifouling paints (Stewart and Thompson, 1994). Their use on ocean going ships is extensive,

with most of the world’s ocean-going fleet reliant on

their use to inhibit fouling growth (Bosselmann, 1996;

Hallers-Tjabbes, 1997; Michel and Averty, 1999a). Tributyltin (TBT) based antifoulant paints have been used

in Australia since the early 1970s, although use on vessels smaller than 25m was banned in Eastern Australian

States in 1989 in response to growing evidence of environmental impacts in semi-enclosed waters subject to

intensive shipping or ship-related activity (Batley and

Scammell, 1989a,b; Batley et al., 1992; Batley, 1995,

1996; Evans, 1999). Monitoring of various locations

around the world (e.g. Dowson et al., 1993; Evans et

al.,1995; Chau et al., 1997; Michel and Averty, 1999b;

Shim et al., 1999; Tselentis et al., 1999) has indicated

that reductions in TBT concentrations have occurred in

some areas frequented by smaller vessels such as marinas, whereas concentrations of TBT present in areas

used by larger vessels still exceed those that will result in

environmental impacts.

Copper is also a widely used antifoulant. It is used as

both an additive in TBT-based paints (usually as copper

oxide or copper thiocyanate) to increase the spectrum of

biocidal activity in these paints, as well as the main

biocide in copper based paints applied to smaller craft

(Batley et al., 1992). As a consequence, concentrations

of copper in marine sediments in enclosed waters such

as marinas and harbours have also increased to levels of

concern (Hall and Anderson, 1999; Olsgard, 1999).

0269-7491/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.

PII: S0269-7491(02)00113-6

Environmental Pollution 120 (2002) 391–396

www.elsevier.com/locate/envpol

* Corresponding author. Tel.: +61-747500700; fax: +61-

747726093.

E-mail address: d.haynes@gbrmpa.gov.au (D. Haynes). 1 Present address: Australian Centre for Tropical Freshwater

Research, James Cook University, Townsville 4811, Australia.
Surveys of antifoulant concentrations in Australian

waters are limited (Batley et al., 1989a, 1989b; Batley

and Scammell, 1991; Kilby and Batley, 1993), with the

most comprehensive survey of Queensland waters being

carried out in 1989 (Witney, 1991). This current work

presents the first data on concentrations of TBT present

in the Great Barrier Reef World Heritage Area, Australia, as well as presenting contemporary data on concentrations of copper associated with shipping and ship

related activity in the region.

2. Materials and methods

2.1. Sediment collection

Marine sediment samples were collected from four

regions [Port Douglas, Cairns, Townsville and Airlie

Beach (the Whitsundays)] within the Great Barrier Reef

World Heritage Area which have a variety of commercial, tourist and recreational maritime activity (Fig. 1).

Within each region, three or four locations representing

commercial harbours (Cairns and Townsville regions

only), marinas, boat mooring locations on mid-shelf

continental islands, and outer reef sites were sampled

for sediment antifoulant concentrations in April and

May 1999 (Table 1). A commercial harbour is not present in the Port Douglas or Whitsunday regions.

Collection of surficial (top 10 cm) sediment was carried out using a van-Veen grab lowered over the side of

a boat or jetty at inshore and mid-shelf continental

island sites; or by divers at outer reef sites. Three replicate sediment samples were collected randomly at each

site. Each replicate sample was composited from three

‘‘grabs’’ or successive container scoops of sediment and

contained approximately 500 g of sediment. Samples

were stored frozen in acid-washed plastic containers.

Sediment samples were also collected opportunistically from the site of a ship grounding in May 1999 at

Heath Reef (13280

S, 143400E), far-north Queensland

(Fig. 1). The 22,000 tonne cargo ship New Reach was

grounded on the outer reef for 6 h before being freed

from the reef under its own power. Two replicate sediment samples were collected in acid-washed plastic

containers by scuba divers from three sites at increasing

distances from the grounding location, 9 days after the

ship was refloated.

2.2. Laboratory analyses

Sediment samples were thawed, sub-sampled and

analysed for antifoulant concentrations. Butyltin determinations were performed at the CSIRO Centre for

Analytical Chemistry, Sydney. Sediment subsamples

were thoroughly homogenised by grinding in a porcelain mortar and pestle. One gram of sediment was

separated from the homogenised sample for analysis.

Butyltins were extracted from each sediment sample

matrix using 50% v/v methanol in 10 M HCl in an

ultrasonic bath. The supernatant was then extracted

with dichloromethane in the presence of tropolone and

finally back-extracted into dilute nitric acid. Volatile tin

hydrides were formed by the addition of sodium borohydride to the nitric acid solutions and these were trapped onto a packed column at 190 C and thermally

desorbed into the light path of an electrically heated

quartz furnace atomic absorption spectrometer (AAS).

Sediment copper analyses were carried out at the

Advanced Analytical Centre, James Cook University,

Cairns. Sediment samples were dried in a Gallenkamp

oven at 60 C overnight and then ground to a fine

powder in a Rocklabs benchmill and prepared as compressed pellets. The pellets were analysed for copper

using X-ray fluorescence spectrometry (Siemens

SRS3000). Compton scatter techniques were used for

correction of absorption effects in copper determination

(Potts, 1996).

2.3. Quality sssurance and satistical analysis

External calibration standards and blank reagents

were measured at the same time as antifoulant analyses.

Table 1

Sediment antifoulant sampling locations and port and harbour capacities, central and northern Great Barrier Reef World Heritage Area

Region Harbour type and capacity

Commercial harbours Mainland marinas Mooring sites, mid-shelf island Mooring sites, outer reef

Port Douglas npa Port Douglas Marina Low Isles Agincourt Reef

(120 berths)

Cairns Cairns Port Yorkey’s Knob Fitzroy Island Michaelmas Reef

(1.1 million tonnes per annum) (197 berths)

Townsville Townsville Port Breakwater Marina Magnetic Island Kelso Reef

(8.9 million tonnes per annum) (243 berths)

Whitsundays np Abel Point Marina South Molle Island Bait Reef

(235 berths)

a Not present.

392 D. Haynes, D. Loong / Environmental Pollution 120 (2002) 391–396
Fig. 1. Antifoulant sampling sites, 1999, Great Barrier Reef World Heritage Area, Australia.

D. Haynes, D. Loong / Environmental Pollution 120 (2002) 391–396 393
TBT and its breakdown products dibutyltin (DBT) and

monobutyltin (MBT), were undetectable in all laboratory reagent blanks and mean recoveries of spiked TBT

and DBT samples ranged from 86–104%, and 80–113%

respectively. Recoveries of copper certified reference

materials (MAG-1 and GSD-3) were 960.5 and

872% respectively.

Differences in sediment copper concentrations were

investigated using a two-factor analysis of variance

(ANOVA) with sampling locations (marinas, boat

mooring locations on mid-shelf continental islands and

outer reef sites) nested in sampling regions (Port Douglas, Cairns, Townsville and the Whitsundays). Commercial harbour sites were excluded from this analysis

as they are only present in the Townsville and Cairns

regions. All statistical analyses were carried using

SYSTAT V7 software (Wilkinson, 1996).

3. Results and discussion

3.1. Butyltin

Butyltin was only detectable in four of the 42 sediments sampled for analysis, and only occurred in

sediments collected from commercial harbours and

from inshore marinas (Table 2). Highest tributyltin

concentrations (1275 ng Sn g1

) were detected in the

Cairns Port Authority harbour adjacent to a large

shipyard and slipway, and in the Townsville Port

Authority swing-basin adjacent to a large shipping

berth (Berth 2, 18 ng Sn g1

). Low concentrations of

TBT were detected in samples collected from both the

Townsville and Cairns marinas (4 ng Sn g1 and 5 ng Sn

g1 respectively). TBT was undetectable (<1 ng Sn g1

)

at all other sites including mid-shelf mooring sites and

outer reef sites. This is in agreement with studies of

concentrations of TBT in open waters around the

world, which have indicated that these types of environments are generally free of butyltin contamination

(Evans, 1999). Low concentations (<1–161 ng Sn g1

)

of DBT and/or MBT were usually detectable whenever

TBT was present in collected sediments (Table 3), implying that TBT deposition had also occurred historically.

The presence of TBT in commercial harbour sediments

is typical of mooring locations used by ocean-going

vessels greater than 25 m in length, which legally rely on

TBT as an antifoulant. Levels of TBT contamination

only exceeded ANZECC (2000) effect range low (ERL)

guideline (5 ng S g1

) at one sampling site in Cairns and

Townsville harbours, and were low in comparison to

levels detected in sediments from harbours elsewhere

(Chau et al., 1997; Shim et al., 1999; Tselentis et al.,

1999). Concentrations of TBT detected in the Cairns

and Townsville marinas were two to three orders of

magnitude lower than concentrations detected in sediments adjacent to European and Canadian marinas (e.g.

Dowson et al., 1993; Chau et al., 1997; Tselentis et al.,

1999), and can be regarded as lightly contaminated

(Dowson et al., 1993). However, the detection of TBT

and its breakdown products at marina sites, not visited

by large vessels, raises the possibility that this antifoulant is currently being used illegally on the hulls of

smaller recreational vessels, or that TBT is being dispersed away from harbours through wind and wave

action.

3.2. Copper

The highest sediment copper concentrations were

associated with the intensive shipping and industrial

activity in Cairns and Townsville commercial harbours,

(28–140 mg g1 and 37–233 mg g1

, respectively; Table 4).

These concentrations of copper are consistent with contamination arising from hull cleaning and painting practices, and stormwater runoff from large urban centres.

Significant differences in sediment copper concentrations were present between sampling regions (F3, 29.05,

P<0.001), and sampling locations (F8, 58.30, P<0.001),

with sediments collected from all marinas except Port

Douglas having the highest average concentrations of

copper (32–112 mg g1

; Table 4). Copper concentrations

Table 2

Sediment TBT concentrations, central and northern Great Barrier Reef Region (all concentrations ng Sn g1 dry w.t., n=3)

Commercial harbours Mainland marinas Mooring sites, mid-shelf island Mooring sites, outer reefs

Port Douglas npa <1 <1 <1

Cairns <1–1275 <1–5.5 <1 <1

Townsville <1–18 <1–4.2 <1 <1

Whitsundays np <1 <1 <1

a Not present.

Table 3

Tributyltin degradation species concentrations (all concentrations ng

Sn g1 dry w.t., n=1)

Sampling location TBT DBT MBT

Cairns harbour 1275 71 161

Cairns marina 5.5 <1 33

Townsville harbour 18 <1 47

Townsville marina 4.2 <1 <1

394 D. Haynes, D. Loong / Environmental Pollution 120 (2002) 391–396
in sediments collected from boat mooring sites on midshelf continental islands, outer reef sites and from the

Port Douglas marina were at background concentrations (i.e. <20 mg g1 dry w.t.; Doherty et al., 2000).

Concentrations of copper detected in sediments collected from commercial harbours and a majority of the

recreational marina sites in this study were similar, and

are likely to reflect its extensive use in antifouling paints

where it is legally used on boats and ships for antifouling purposes (Brady et al., 1994). Average copper concentrations at both commercial harbour locations and

at two of the marina locations exceeded the ANZECC,

(2000) effect range low (ERL) guideline (65 mg g1

),

implying that the heavy metal has some potential for

environmental impact at these sites.

3.3. Ship grounding antifoulant concentrations

Butyltin concentrations detected in sediments collected from the Heath Reef grounding site, far northern

Great Barrier Reef, were grossly elevated (Table 5).

Heath Reef was extensively damaged at the time of the

ship grounding and elevated concentrations of butyltin

were a consequence of antifoulant paint being abraded

from the ships hull at the time of grounding and during

subsequent refloating. Butyltins are highly toxic to a

range of marine reef biota including scleractinian corals

(Morse et al., 1988; Allemand et al., 1998; Heyward and

Negri, 1999; Negri and Heyward, 2001), octocorals

(Sebens, 1983), other cnidarians (Mercier et al., 1996;

Leitz, 1997) and molluscs (Labare et al., 1997), bryozoans (Kitamura and Hirayama, 1987) and echinoderms

(Johnson and Sutton, 1994). Its mode of action is primarily through disruption of the functioning of cell

membranes (Viarengo, 1989; Fent, 1996), and microcosm

experiments have demonstrated its effectiveness against

organisms that recruit to hard substrata (Henderson,

1988). This present study identifies, for the first time,

that the potential long-term impacts of residual antifoulants at such grounding sites need to be recognised

as a significant environmental problem. Where possible,

clean-up strategies to remove antifoulant contaminants

from the sites of large ship groundings should be completed to ensure long-term viability of the affected marine

environment.

Acknowledgements

Graham Batley and Chris Brockbank (CSIRO Centre

for Analytical Chemistry, Sydney) supervised butyltin

analyses, and Rob Cirroco, Advanced Analytical Centre, James Cook University, analysed copper samples.

Ken Anthony, Barney Bebendorf and Britta Schafelke

(Great Barrier Reef Marine Park Authority) and

Andrew Griffith, Rob Buck and Mike Short (Queensland Parks and Wildlife Service) are thanked for assistance with sediment collection. Jane Waterhouse (Great

Barrier Reef Marine Park Authority) is thanked for

assistance with Fig. 1. Andrew Negri (Australian Institute of Marine Science) and John Lewis (DSTO Aeronautics and Maritime Research Laboratory) are

thanked for comments on a draft of the manuscript.

References

Allemand, D., Tambutte ́, E ́ ., Girard, J., Jaubert, J., 1998. Organic

matrix synthesis in the scelactinian coral Stylophora pistillata: role in

biomineralisation and potential target of the organotin tributyltin.

The Journal of Experimental Biology 201, 2001–2009.

ANZECC, 2000. Australian and New Zealand guidelines for fresh and

marine water quality. Australian and New Zealand Environment

and Conservation Council and Agriculture and Resource Management Council of Australia and New Zealand.

Batley, G.E., 1995. Heavy metals and tributyltin in Australian coastal

and estuarine waters. In: Zann, L.P., Sutton, D. (Eds.), State of the

Marine Environment Report for Australia, Technical Annex: Pollution. Great Barrier Reef Marine Park Authority, Townsville, pp.

63–72.

Batley, G.E., 1996. The distribution and fate of tributyltin in the

marine environment. In: deMora, S.J. (Ed.), Tributyltins: Case

Study of an Environmental Contaminant. Cambridge University

Press, Cambridge, pp. 139–166.

Table 4

Mean (SD) sediment copper concentrations, northern and central Great Barrier Reef region (all concentrations mg g1 dry wt., n=3)

Commercial harbour Mainland marina Mooring sites, mid-shelf islands Mooring sites, outer reef

Port Douglas npa 9 (5) 20 (1) 20 (2)

Cairns 70(61) 33 (1) 20 (2) 20 (1)

Townsville 113 (105) 72 (7) 11 (8) 22 (1)

Whitsundays np 95 (18) 12 (8) 21 (0)

a Not present.

Table 5

Summary of butyltin concentrations detected at the Heath Reef shipgrounding site, far northern Great Barrier Reef, May 1999 (all concentrations ng Sn g1 dry wt., n=6)

TBT DBT MBT

Minimum 7500 660 660

Maximum 340,000 32,000 61,000

Average 81,300 8600 18,300

Standard deviation 13,200 12,400 25,300

D. Haynes, D. Loong / Environmental Pollution 120 (2002) 391–396 395
Batley, G.E., Scammell, M.S., 1991. Research on tributyltin in Australian estuaries. Applied Organometallic Chemistry 5, 99–105.

Batley, G.E., Mann, K.J., Brockbank, C.I., Maltz, A., 1989a. Tributyltin in Sydney Harbour and Georges River waters. Australian

Journal of Marine and Freshwater Research 40, 39–48.

Batley, G.E., Fuhua, C., Brockbank, C.I., Flegg, K.J., 1989b. Accumulation of tributyltin by the Sydney rock oyster Saccostrea commercialis. Australian Journal of Marine and Freshwater Research

40, 39–48.

Batley, G.E., Scammell, M.S., Brockbank, C.I., 1992. The impact of

the banning of tributyltin-based antifouling paints on the Sydney

rock oyster, Saccostrea commercialis. The Science of the Total

Environment 122, 301–314.

Bosselman, K., 1996. Environmetal law and tributyltin in the environment. In: deMora, S. (Ed.), Tributyltin: Case Study of an

Environmental Contaminant. Cambridge University Press, Great

Britian, pp. 237–263.

Brady, B.A., Johns, R.B., Smith, J.D., 1994. Trace metal geochemical

association in sediments from the Cairns region of the Great Barrier

Reef, Australia. Marine Pollution Bulletin 28, 230–234.

Chau, Y.K., Maguire, R.J., Brown, M., Yang, F., Batchelor, S.P.,

1997. Occurrence of organotin compounds in the Canadian aquatic

environment five years after the regulation of antifouling uses of

tributyltin. Water Quality Research Journal of Canada 32, 453–521.

Doherty, G.B., Brunskill, G.J., Ridd, M.J., 2000. Natural and

enhanced concentrations of trace metals in sediments of Cleveland

Bay, Great Barrier Reef Lagoon, Australia. Marine Pollution Bulletin 41, 337–344.

Dowson, P.H., Bubb, J.M., Lester, J.N., 1993. Temporal distribution

of organotins in the aquatic environment: five years after the 1987

UK retail ban on TBT based antifouling paints. Marine Pollution

Bulletin 26, 487–494.

Evans, S.M., 1999. Tributyltin pollution: the catastrophe that never

happened. Marine Pollution Bulletin 38, 629–636.

Evans, S.M., Leksons, T., McKinnell, P.D., 1995. Tributyltin pollution: a diminishing problem following legislation limiting the use of

TBT-based antifoulant paints. Marine Pollution Bulletin 30, 14–21.

Fent, K., 1996. Ecotoxicology of organotin compounds. Critical

Reviews in Toxicology 26, 1–117.

Hall, L.W., Anderson, R.D., 1999. A deterministic ecological risk

assessment for copper in European saltwater environments. Marine

Pollution Bulletin 38, 207–218.

Hellers-Tjabbes, C.C.T., 1997. Tributyltin and policies for antifouling.

Environmental Technology 18, 1265–1268.

Henderson, R.S., 1988. Marine Microcosm Experiments on Effects of

Copper and Tributyltin-Based Antifoulant Paint Leachates (Technical Report No. 1060). Naval Ocean Systems Centre, San Diego, CA.

Heyward, A.J., Negri, A.P., 1999. Natural inducers for coral larval

metamorphosis. Coral Reefs 18, 273–279.

Johnson, C.R., Sutton, D.C., 1994. Bacteria on the surface of crustose

coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Marine Biology 120, 305–310.

Kitamura, H., Hirayama, K., 1987. Effect of cultured diatom films on

the settlement of larvae of a bryozoan Bugula neritina. Nippon Suisan Gakkaishi 52, 1383–1385.

Kilby, G.W., Batley, G.E., 1993. Chemical indicators of sediment

chronology. Australian Journal of Marine and Freshwater Research

44, 635–647.

Labare, M.L., Coon, S.L., Mathias, C., Weiner, R.M., 1997. Magnification of tributyltin toxicity to oyster larvae by bioconcentration

in biofilms of Shewanella colwelliana. Applied and Environmental

Microbiology 63, 4107–4110.

Leitz, T., 1997. Induction of settlement and metamorphosis of cnidarian larvae: signals and signal transduction. Invertebrate Reproduction and Development 31, 109–122.

Mercier, A., Pelletier, E., Hamel, J., 1996. Toxicological response of

the symbiotic anemone Aiptasia pallida to butyltin contamination.

Marine Ecology Progress Series 144, 133–146.

Michel, P., Averty, B., 1999a. Distribution and fate of tributyltin in

surface and deep waters of the northwestern Mediterranean. Environmental Science and Technology 33, 2524–2528.

Michel, P., Averty, B., 1999b. Contamination of French coastal waters

by organotin compounds: 1997 update. Marine Pollution Bulletin

38, 268–275.

Morse, D.E., Hooker, N., Morse, A.N.C., Jensen, R.A., 1988. Control

of larval metamorphosis and recruitment in sympatric agariciid

corals. Journal of Experimental Marine Biology and Ecology 116,

193–217.

Negri, A.P., Heyward, A.J., 2001. Inhibition of coral fertilisation and

larval metamorphosis by tributyltin and copper. Marine Environmental Research 51, 17–27.

Olsgard, F., 1999. Effects of copper contamination on recolonisation

of subtidal marine soft sediments—an experimental field study.

Marine Pollution Bulletin 38, 448–462.

Potts, P.J., 1996. X-ray fluorescence analysis: principles and practices

of wavelength dispersive spectrometry. In: Potts, P.J. (Ed.), A

Handbook of Silicate Rock Analysis. Chapman and Hall, London,

pp. 226–285.

Sebens, K.P., 1983. Settlement and metamorphosis of a temperate

soft-coral larvae (Alcyonium siderium Verril): induction by crustose

algae. Biological Bulletin 165, 286–304.

Shim, W.J., Oh, J.R., Kahng, S.H., Shim, J.H., Lee, S.H., 1999.

Horizontal distribution of butyltins in surface sediments from

an enclosed bay system, Korea. Environmental Pollution 106,

351–357.

Stewart, C., Thompson, J.A.J., 1994. Extensive butyltin contamination in southwestern coastal British Columbia, Canada. Marine

Pollution Bulletin 28, 601–606.

Tselentis, B.S., Maroulakou, M., Lascourreges, J.F., Szpunar, J.,

Smith, V., Donard, O.F.X., 1999. Organotins in sediments and biological tissues from Greek coastal areas: preliminary results. Marine

Pollution Bulletin 38, 146–153.

Viarengo, A., 1989. Heavy metals in marine invertebrates: mechanisms

of regulation and toxicity at the cellular level. Reviews in Aquatic

Sciences 1, 295–317.

Wilkinson, L., 1996. Systat 7.0 for Windows: Statistics. Microsoft,

Chicago.

Witney, E. (1991). TBT in antifouling paints—a Queensland perspective. Information Series Q191930, Department of Primary Industries, Brisbane.

396 D. Haynes, D. Loong / Environmental Pollution 120 (2002) 391–396