Organochlorine, Heavy Metal and Polyaromatic Hydrocarbon Pollutant Concentrations in the Great Barrier Reef (Australia) Environment: a Review

Organochlorine, Heavy Metal andPolyaromatic Hydrocarbon PollutantConcentrations in the Great BarrierReef (Australia) Environment: a ReviewDAVID HAYNES* and JOHANNA E. JOHNSONGreat Barrier Reef Marine Park Authority, P.O. Box 1379, Townsville, Qld 4810, Australia

Past monitoring of heavy metals, organochlorine com-pounds and polyaromatic hydrocarbons (PAHs) has foundthat pollutant concentrations are generally low within theGreat Barrier Reef Marine Park and World HeritageArea and are indicative of a relatively unpolluted envi-ronment. The exceptions are sites that are adjacent tohuman activity such as ports and harbours, urban centresand areas adjacent to intensive agricultural activity. Thesesites have elevated concentrations of a range of pollutants.Concentrations of dioxins have also been found to be el-evated in marine park sediments. Elevated pollutant con-centrations are generally the consequence of e�uentdischarge, urban stormwater, and agricultural and indus-trial runo�. However, a majority of Great Barrier Reefpollutant data are now dated, and contemporary infor-mation is required concerning the distribution and impactof pollutants in the Queensland marine environment. Theutility of specialized monitoring tools such as biomarkersfor tropical marine environments urgently needs to beexamined. With this information, appropriate risk as-sessment and monitoring can be implemented and e�ectivemanagement strategies developed to protect tropical ma-rine ecosystems including the Great BarrierReef. Ó 2000 Elsevier Science Ltd. All rights reserved.

Keywords: chemical pollution; Great Barrier Reef; heavymetals; pesticides; petroleum hydrocarbons.

Introduction

Agriculture, urban settlement and industrial activitiesaround the world have contributed to the widespreadcontamination of global marine ecosystems with orga-nochlorine compounds, petroleum products and heavymetals (Fowler, 1990; Tatsukawa et al., 1990). All of

these types of pollutants are conservative and many areessentially permanent additions to the environment(Clark, 1992). They are also often highly toxic to biota(Richardson, 1995).

Chlorinated organic compounds (or organochlorines)are organic (carbon based) chemicals that containbound chlorine. A majority of these compounds arearti®cial and enter the environment through humanactivities, although it is now recognized that marine al-gae and invertebrates and natural processes such asforest ®res also contribute variable quantities of orga-nochlorines (and other halogenated organics) to theenvironment (Leach et al., 1985; Enell and Wennberg,1991; Gribble, 1994). Chlorinated organic compoundshave a wide range of industrial and agricultural ap-plications. They include pesticides such as DDT (dichlo-ro-diphenyl-trichloroethane) and lindane (c-HCH orgamma-hexachlorocyclohexane) and polychlorinatedbiphenyls (PCBs) which are used in a range of industrialapplications including dielectrics in electrical trans-formers. Organochlorines have been implicated in re-productive and immunological abnormalities observedin birds and marine mammals (Livingston, 1976). Thefew studies of the impacts of organochlorine compoundscarried out in Australian freshwater and marine envi-ronments indicate that environmental contamination byorganochlorine substances has occurred at relatively lowconcentrations in Australia and that highest concentra-tions have been associated with centres of urbanization(Connell, 1993; Richardson, 1995). This contaminationpattern is similar to the ®ndings of studies elsewherewhich have identi®ed chlorinated organic compounds inestuarine and marine sediments near major metropoli-tan areas along the eastern coast of the United States(NRC, 1989) and at a wide range of locations in Europeand Asia associated with human settlement (AlvarezPi~neiro et al., 1995; Mohapatra et al., 1995; Agnihotriet al., 1996; Thompson et al., 1996).

Polycyclic aromatic hydrocarbons (PAHs) are naturalconstituents of crude oil and are a mixture of organic

Marine Pollution Bulletin Vol. 41, Nos. 7±12, pp. 267±278, 2000

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*Corresponding author. Tel.: +61-747-500-700.E-mail address: [email protected] (D. Haynes).

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compounds of fossil and biogenic origin (Ne�, 1990).PAHs account for ca 20% of total hydrocarbons incrude oil and are the most biologically toxic of all thepetroleum compounds (Ne�, 1990). Generally, a mixedpetroleum product containing a broad spectrum of hy-drocarbon classes is released to the marine environmentwhere it may a�ect a variety of biological processes andbe a potent cell mutagen and carcinogen (Capone andBauer, 1992).

Heavy metals are natural constituents of rocks andsoils and enter the environment as a consequence ofweathering and erosion (F�orstner, 1989). Many metalsare biologically essential, but all have the potential to betoxic to biota above certain threshold concentrations.Following industrialization, unnatural quantities ofmetals such as arsenic (As), cadmium (Cd), copper (Cu),mercury (Hg), lead (Pb), nickel (Ni) and zinc (Zn) havebeen released, and continue to be released into theaquatic environment through stormwater and waste-water discharges. As, Cd, Cu, Hg and Zn are the ®vemetals with most potential impact that enter the envi-ronment in elevated concentrations as a consequence ofagricultural activity. Zn and Cu are used in smallamounts as fertilizers in some soils de®cient in theseelements, and As, Cd and Hg are constituents of somefungicides (Hunter, 1992). Cu is also used as an algae-cide, and Cd and Zn occur as contaminants of phos-phatic fertilisers (Rayment et al., 1989). Organotincompounds have no natural counterparts and are gen-erally introduced into the marine environment throughbiocide applications, principally as constituents ofantifouling paints (Whitney, 1990).

Potential impacts from heavy metals are generallyrestricted to locations adjacent to major cities or in-dustrialized areas on the coastal fringe (Batley, 1995)and to site draining areas of intensive agriculture. Onceintroduced into the marine environment, heavy metalshave the potential to a�ect sediment nutrient cycling,cell growth and regeneration, as well as reproductivecycles and photosynthetic potential of marine organisms(Peters et al., 1997). Results of Australian studies ofmarine environmental metal contamination indicatethat sur®cial sediments adjacent to most urbanized andindustrialized estuaries are contaminated with metals,particularly Pb and Zn (Connell, 1993; Batley, 1995).

Sources and Movement of Pollutants

Organochlorine pesticides enter the environment via anumber of routes following their release or application.They may enter the atmosphere directly during spraying,and later following volatilization of deposited sprayfrom both foliage and surface soil (Nash and Hill, 1990).Volatilization rates are related to the vapour pressure ofthe compound as well as to other environmental factorssuch as temperature and soil moisture content (Nashand Hill, 1990). Pesticides may also enter the atmo-sphere adsorbed to wind-blown dust particles (Clark,

1992). Airborne pesticides are ultimately re-deposited onland or water. Applied and deposited pesticides aretransported from application and depositional sites tothe aquatic environment in overland ¯ows and groundleachate following rainfalls (Clendening et al., 1990).Organochlorine compounds can also enter the environ-ment as contaminants contained in e�uent dischargesand in urban stormwater runo�. Organochlorine com-pounds are highly hydrophobic and once in the watercolumn, tend to adsorb to ®ne particulates or be bio-accumulated into lipids in aquatic biota (Olsen et al.,1982). The ®nal distribution of organochlorine com-pounds between the di�erent phases in the aquatic en-vironment is complex and is dependent on partitioningco-e�cients which are de®ned by the properties of theorganochlorine compound (Connell, 1995). The conse-quences of organochlorine tissue accumulation are alsocomplex (Clark, 1992) and organochlorine pesticidesand PCBs have been implicated in reproductive andimmunological abnormalities observed in terrestrial birdpopulations and in marine mammal populations (Boonet al., 1992).

It is estimated that approximately 6.1 million metrictons of petroleum products are released to global oceansannually, the majority of which is derived from an-thropogenic sources and which pass through the coastalzone before being carried out to sea (Capone and Bauer,1992). Worldwide, major inputs of petroleum into themarine environment occur via industrial discharge andurban runo� (37%), vessel operations (33%), tankeraccidents (12%), atmospheric deposition (9%), naturalresources (8%) and exploration production (2%)(Queensland Transport, 1997). The fate of petroleumhydrocarbons once they enter the marine environment issimilar to that of many organic pollutants. The bulk ofthe petroleum initially introduced into the water columnrapidly becomes associated with hydrophobic organicmatter and suspended particulates, the volatile com-pounds then evaporate and the non-volatiles are de-posited into the sediment (Capone and Bauer, 1992).The component of petroleum left, the emulsion or`mousse', is not likely to dissolve, adsorb, evaporate orbe rapidly biologically degraded and will eventually sinkto the bottom and settle in the sediment. While thelighter fractions are suspended in the water column, themost damaging impacts are on larvae and low motilityorganisms that cannot escape the oil. The e�ects aremost notable in changes in feeding or reproductive cy-cles that ultimately a�ect population size and fecundity.Once the PAHs have settled in the sediment, ®lterfeeders and benthic organisms are a�ected with thebioaccumulation of toxic compounds in their tissues,genetic mutations and cell atrophy often occurring(Peters et al., 1997).

Metals are also strongly associated with particulatesand enter the marine environment in a similar fashion toorganochlorine compounds. The major routes of envi-ronmental entry include atmospheric transport of dust

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Marine Pollution Bulletin

and through sediment movement in overland ¯ows andin waterways (Bryan, 1971). Additional quantities ofmetals are also added to the environment via the dis-charge of e�uent and urban stormwater. Particulatemetals in suspension and in bottom sediments are notgenerally directly available to aquatic organisms. (Theexception to this are sediment bound metals which canbe accumulated following solubilization in the acidicjuices of a sediment-feederÕs gut (Waldichuk, 1985).) Therates at which metals are solubilized from particulates isdependent on environmental factors including dissolvedoxygen concentrations, pH, salinity and temperature(Waldichuk, 1985). Once dissolved in the water column,metals may be accumulated by marine invertebratesfrom solution via passive uptake across permeable sur-faces such as gills and the digestive tract (Rainbow,1990). Cellular metal toxicity is primarily due to thechemical inactivation of cellular enzymes responsible fornormal organism survival and function (F�orstner, 1989),and organism growth, reproduction and behaviour arepotentially e�ected by elevated environmental metalconcentrations (Langston, 1990).

Concentrations of Pollutants in the GreatBarrier Reef Marine Park

The Great Barrier Reef Region contains the largestsystem of coral reefs and associated life forms anywherein the world (Craik, 1992). It extends approximately2000 km parallel to the Queensland coast between 9 and24°S latitude and covers approximately 350 000 km2

(Fig. 1). It contains many important Queensland marineecosystems such as seagrass meadows, and mangroveforests, as well as coral reefs including the Great BarrierReef (Fig. 1). It is a largely unspoiled environment withmuch of the adjacent coastline relatively una�ected bycoastal development (Brady et al., 1994). However, theregion is a focus of tourism and population centrespresenting a risk from inputs from recreational, indus-trial and urban activities. Shipping and agricultural ac-tivities also input contaminants into the marineenvironment via river runo�, vessel operations and ac-cidental spillage. Principal coastal population centreswhich result in port developments are located at Cairns,Mourilyan (near Innisfail), Lucinda (near Ingham),Townsville, Abbot Point (near Bowen), Mackay, HayPoint, Rockhampton, Gladstone and Bundaberg. Littleis known about contaminant concentrations in thelargely remote Great Barrier Reef Region and publisheddata are summarized below.

Air and seawaterAs is the case for most areas of the world (Phillips and

Spies, 1988), little information is available on the con-centrations of chlorinated hydrocarbons in air and sea-water in the Great Barrier Reef region. Published datafor the Great Barrier Reef are presented in Tables 1±3.

Relatively low concentrations of hexachlorocyclo-hexanes (HCHs) and DDT and its breakdown productswere reported in air and water samples collected fromthe Coral Sea in 1981 (Tanabe et al., 1982), particularlycompared with concentrations in eastern Americanwaters. Concentrations of c-HCH exceeded a-HCH,implying locally sourced contamination from agricul-tural lindane application rather than from southern-moving airborne contaminants from Asia. This was incontrast to a later study where a-HCH was detected inrelatively high concentrations in the Coral Sea waters(Kurtz and Atlas, 1990). Due to the limited samplingundertaken at this time, it was unclear whether the highconcentrations detected in 1987 were a short-term in-crease caused by improper local pesticide disposal orwere indicative of long-term regional contamination.Very low concentrations (4±140 ng lÿ1) of polycyclicaromatic hydrocarbons (PAHs) were detected in 1983 inseawaters around Green Island, (near Cairns) (Smithet al., 1987). The compounds detected were two ringedaromatics (which were probably re®ned oil products)and were present in samples collected adjacent toboating activity or e�uent discharge.

Concentrations of metals in Great Barrier Reef sea-waters are also relatively unstudied. Seawater metalconcentrations in samples collected in nearshore waters

Fig. 1 Great Barrier Reef Marine Park and World Heritage Area.

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Volume 41/Numbers 7±12/July±December 2000

between 1976 and 1977 adjacent to Townsville and be-tween Townsville and Cardwell in 1979 were found to besimilar and were within the range of mean world datareported at that time (Burdon-Jones et al., 1982;Klumpp and Burdon-Jones, 1982). The exception wasZn, which was elevated in seawaters collected nearTownsville compared with a control site in BowlingGreen Bay. Seawater metal concentrations aroundLizard, Orpheus and Heron Islands in 1982±1983 werealso similar to concentrations reported for unpollutedsites (Denton and Burdon-Jones, 1986a). Concentra-tions of Cd, Cu, Ni and Zn varied both temporally andspatially at island collection sites. Concentrations of Cuand Zn were highest at Orpheus Island, and the authorsattributed this to the islandÕs relative proximity to urbanand industrial activity. Highest Cd concentrations werepresent at the end of the wet season for all sites. Asurvey of tributyltin (TBT) levels in Queensland marinewaters was carried out by the Queensland Departmentof Primary Industry in 1989 (Whitney, 1990). In generalthe environmental levels of TBT in the Rockhamptonregion were consistently low, with only water samplesfrom one site, exceeding United Kingdom Environ-mental Quality Targets (UK EQT is 0.8 lg/l as Sn). TBTlevels in the Townsville region were marginally higherthan those of the Rockhampton region, however fewsamples exceeded the UK EQT.

Coastal sedimentsOrganochlorine compounds, PAHs and heavy metals

tend to partition to sediments, and as a consequence,

marine sediments are usually regarded as the ultimatesink for persistent pollutants discharged into the envi-ronment (Gibbs, 1973). A majority of studies carried outto determine pollutant concentrations in Great BarrierReef sediments have been initiated in response to portand harbour developments or dredging of shippingchannels. Published data for the Great Barrier Reef aresummarized in Tables 4 and 5. Low levels of a range ofmetals have been detected in sur®cial sediments inCairns Harbour, Port of Mourilyan, Port of Townsville,Hay Point and Gladstone Port (Reichelt and Jones,1993; Gladstone Port Authority, 1994; Anon, 1996;Cairns Port Authority, 1998). Elevated concentrationsof Cu, which were attributed to past use of copper-basedmarine anti-fouling paints have been found in CairnsHarbour (Brady et al., 1994). Elevated concentrations ofNi, Cr, Fe and Zn which were associated with nickel oreloading berths have also been detected in the Port ofTownsville (Reichelt and Jones, 1993). Nearshore ma-rine sediments collected in the vicinity of the KeppelIsland Group (near Rockhampton) have been analysedfor metal concentrations using techniques to report bothbiologically available and total metal concentrations(Ahlers and Szymczak, 1993). All metal concentrationswere in the range typically found in undisturbed sys-tems. Marine sediments collected from the Torres Straitsduring 1992 and 1993 have been analysed for heavymetal concentrations (Dight and Gladstone, 1993;Gladstone, 1996). This studies concluded that sedimentmetal levels were low and comparable with concentra-tions found elsewhere in unpolluted tropical marine

TABLE 3

Heavy metal concentrations, Great Barrier Reef seawater.a

Location Date Matrix n Cd Cu Pb Ni Zn References

Townsville Harbour 1976/1977 Seawater 15 0.32 0.38 0.72 0.28 2.19 Burdon-Jones et al. (1982)Bowling Green Bay 1976/1977 Seawater 15 0.22 0.16 0.77 0.23 0.82 Burdon-Jones et al. (1982)Lizard Island 1982/1983 Seawater 8 <0.03 0.13 <0.06 0.09 0.08 Denton and Burdon-Jones (1986a,b)Orpheus Island 1982/1983 Seawater 8 <0.06 0.18 <0.06 0.12 0.14 Denton and Burdon-Jones (1986a,b)Heron Island 1982/1983 Seawater 8 <0.02 0.14 <0.06 0.08 0.17 Denton and Burdon-Jones (1986a,b)

aAll concentrations lg lÿ1.

TABLE 1

Organochlorine concentrations in air and surface seawater, Coral Sea, 1981 and 1987.a

Location Date Matrix n a-HCH c-HCH b-HCH d-HCH p,p0-DDE p,p0-DDT o,p0-DDT References

Coral Sea 1981 Atmosphere 1 91 200 37 45 200 100 Tanabe et al. (1982)Coral Sea 1987 Atmosphere 1 17 4 Kurtz and Atlas (1990)Coral Sea 1981 Seawater 1 160 720 220 2 13 5 Tanabe et al. (1982)Coral Sea 1987 Seawater 3 1480±5100 153±330 63±111 9±13 Kurtz and Atlas (1990)

aAll concentrations pg mÿ3 or pg lÿ1.

TABLE 2

Polyaromatic hydrocarbon concentrations, Great Barrier Reef seawater.a

Location Date n Phe Anth Pyr Chry B(a)P B(ghi)P Reference

Green Island 1983 7 <1±3 <1±25 <1±53 <3±140 <0.2±6 <0.3±16 Smith et al. (1987)

aAll concentrations ng lÿ1.

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sediments. O�shore sediments in the vicinity of RaineIsland predominantly comprise calcium carbonate andcontained very low concentrations of heavy metals(Barry and Rayment, 1992).

A limited number of Great Barrier Reef sedimentshave also been analysed for organochlorine contami-nation. Lindane (c-HCH) was detected in sedimentsfrom the mouth of the Burdekin River (near Ayr) in1984 and 1985 (Dyall and Johns, 1985), however, or-ganochlorine pesticides were not detected in sedimentsamples collected in Bowling Green Bay or at LizardIsland during this survey. The authors concluded thatfrom the limited sampling carried out, sedimentary ac-cumulation of organochlorines was con®ned to withinclose proximity of coastal sugarcane growing areas(Dyall and Johns, 1985). Organochlorine compoundswere not detected in surface sediment samples or insediment cores collected in the vicinity of HinchinbrookIsland and from Bowling Green Bay in 1997 (Cavanaghet al., 1999). Unexpectedly high concentrations ofpolychlorinated dibenzodioxins were detected in marinesediments collected along the northern Queenslandcoast adjacent to the Great Barrier Reef in 1998, sug-gesting that an unknown source for higher chlorinated

dioxins exists along the Queensland coast (M�uller et al.,1998a,b, 1999).

PAHs have also been detected in GBR sediments.Highest concentrations were present in sediments col-lected from Townsville Harbour and were a conse-quence of fuel discharges and motor exhaust emissionsto the water (Smith et al., 1985). PAH concentrations inGladstone Harbour sediments were also comparablewith concentrations present in polluted marine sedi-ments elsewhere. In contrast, petroleum hydrocarbonswere not detected in sediments collected in the vicinity ofHay Point in 1996 (Anon, 1996). Low levels of PAHswere also found in sediments adjacent to boat landingand mooring areas around Green and Heron Islands(Smith et al., 1985, 1987). In contrast, sediments col-lected from the mid-shelf John Brewer Reef were un-contaminated with PAHs (Smith et al., 1985), as weresamples collected in 1980 and 1981 from other remotesites in northern waters (Lizard Island) and in the TorresStrait (Coates et al., 1986). Molecular markers (triterp-enoid hydrocarbons), indicative of petrogenic pollutionwere recovered in 1986 from Cairns Harbour and werebelieved to have originated from harbour boat tra�c(Johns et al., 1988).

TABLE 5

PAH concentrations in GBR sediments.a

Location Date n Phe Anth Flu Pyr B(a)A Chry B(e)P B(k)F B(a)P B(ghi)P References

Green Island 1983 21 <0.06±4.2<0.06±1 <0.1±7.2 <0.1±15 <0.01±6 <0.04±0.8 <0.1±0.6 <0.001±2.5 <0.004±4.3 <0.01±2.6 Smith et al.(1987)

TownsvilleHarbour

1982 5 6.5±1400 10±4500 4.4±1700 7.3±1500 1±200 10±2600 3±1500 Smith et al.(1985)

Heron Island 1982 4 <0.6±1.3 <0.1±8 <0.3±2 <0.01±0.5 <0.1±2.6 <0.3±6.7 Smith et al.(1985)

Hinchin-brook Island

1982 5 7.3±15 7±15 <0.4±2.2 <2.2 0.3±0.7 2.9±4.4 0.5±2.6 Smith et al.(1985)

GladstoneHarbour

1982 1 270 180 11 16 820 200 Smith et al.(1985)

John BrewerReef

1982 2 <0.05 <0.1 <0.04 <0.2 <0.01 <0.01 <0.02 Smith et al.(1985)

aAll concentrations lg kgÿ1 dry wt.

TABLE 4

Average total sediment metal concentrations, GBR region.a

Location Date n As Cd Cr Cu Fe Hg Mn Ni Pb Zn References

Raine Island 1991 0.6 0.01 2 2 <0.05 7 <0.2 4 Barry and Rayment (1992)Trinity Inlet (Cairns) 1990 2 8.5 0.76 <0.3 0.27 0.72 Anon (1991)Trinity Inlet (Cairns) 1991 2 17 16000 40 Brady et al. (1994)Cape Cleveland (Townsville) 1991 1 27 60 41 Reichelt and Jones (1994)Cleveland Bay (Townsville) 1991 32 53 <13 40 Reichelt and Jones (1994)Cleveland Bay (Townsville) 1991 10 5.3 4871 139 1.5 8.6 14 Reichelt and Jones (1993)Bowling Green Bay (Townsville) 1991 6 2.5 7.5 11 Reichelt and Jones (1993)Hay Point 1996 1 10 <1 8 8 8020 <0.1 244 1 19 Anon (1996)

aAll concentrations lg gÿ1.

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InvertebratesBioaccumulation of organochlorines and metals by

invertebrates is variable, with some groups such asbivalve molluscs accumulating many pollutants in veryhigh concentrations. Other groups such as crustaceanshave the ability to regulate certain pollutant body bur-dens (Phillips and Rainbow, 1993). Pollutant concen-trations present in Great Barrier Reef invertebrateshave only been investigated in a limited number ofspecies. Low concentrations of p,p0-DDT and dieldrinwere determined in gonad tissue from crown of thornsstar®sh (Acanthaster planci) collected from SlasherÕsReef and the Bunker Group in the southern section ofthe Marine Park in 1970 and 1971 (McCloskey andDuebert, 1972), and low concentrations of c-lindane,heptachlor and DDT were reported being present inhard corals (Fungia sp. and Acropora sp.) and a bivalvemollusc (Tridacna crocea) collected from inner shelfreefs between Heron and Lizard Islands in 1976 and1977 (Olafson, 1978).

Concentrations of PAHs have been found to be belowor close to the limit of detection in clams (Tridacnamaxima) collected from a wide range of sites in theGreat Barrier Reef in 1982 and 1983 (Smith et al., 1984,1987). The only exceptions were clams collected fromLizard Island and Heron Island, which had measurableconcentrations of hydrocarbons. Both these islands haveresorts and scienti®c ®eld stations, and the pollutantswere probably sourced from small boats (Smith et al.,1984). Low concentrations of petroleum-like hydro-carbons were also isolated from tissue samples from theholothurian Holothuria sp. and the coral Acropora sp.collected from the southern section of the Marine Parkin 1981 (Coates et al., 1986). These contaminants werebelieved to originate from industrial operations atGladstone or from petroleum bearing shale deposits inthe region.

Metal (Cd, Cu, Pb, Ni, Zn) concentration in variousspecies of soft (octocorallian) and hard (scleractinian)corals from Heron, Orpheus and Lizard Islands wereexamined between 1980 and 1983 (Denton and Burdon-Jones, 1986b). Of the two groups, the octocoralsaccumulated signi®cantly higher concentrations of alldetectable metals. The soft coral Sarcophyton sp. con-tained highest concentrations of Cd at the southernHeron Island site. Three species of hard corals, Go-niastrea aspera, Favites chinensis and Platygyra ryuky-uensis were studied for the impacts of Cu and Zn onfertilization success (Heyward, 1988). Reproductivesuccess of all three species was reduced deleteriouslywhen exposed to elevated (compared with ambient)concentrations of 0.01±0.1 mg lÿ1 of the heavy metals(Heyward, 1988). Ecotoxicological studies investigatingthe impact of metals on coral ecology have been few innumber, although exposure to metals may be an addedstress connected with zooxanthellae loss and coralbleaching (Harland and Brown, 1989). This responsehas been observed under laboratory conditions for

Galaxea fascicularis at Heron Island (Ballestrin, 1993).More recently the utility of a number of scleractiniancorals (Pocillopora sp., Acropora sp., Goniastrea sp. andMontastrea sp.) resident in Townsville harbour andaround Heron Island to act as biomonitors of ambientmetal concentrations were assessed (Esslemont, 1997). Itwas concluded that G. aspera and P. damicornis weresuitable sentinel organisms for monitoring metal loadsin Great Barrier Reef waters.

Extremely high concentrations of arsenic have beenobserved in the tissues of various bivalves collected fromGreat Barrier Reef waters (Benson and Summons,1981). This accumulation is a consequence of the me-tabolism of arsenate by algae under low nutrient con-ditions. Although arsenic accumulation in algae is notexcessive, it is bioaccumulated to high concentrations inthe tissues (particularly in the kidney) of ®lter feedingbivalves such as Tridacna sp., which use the algae as afood source. Background tissue concentrations of Ag,Cd, Cu, Co, Pb, Ni and Zn have also been assessed innine species of tropical bivalves (Arca ventricosa, Chamaisotoma, Lithophaga teres, P. margiritfera, Pycnodontehyotis, Spondylus ducalis, Modiolus auriculatus, Trich-omya hirsuta and Ustularca renuta) collected from thegreater Townsville region in 1979 (Klumpp and Burdon-Jones, 1982). This study concluded that most of thebivalve species studied were strong accumulators ofmetals, although accumulation was variable betweensampling locations. The relationship between bivalvetissue metal concentration, location and environmentalimpact was not assessed. More recently, trace metallevels in six species of bivalves (Tridacna crocea, T.maxima, Pinctata margaritifera, Hyotissa hyotis, Chamaplinthota, Trochus niloticus and Strombus luhuanus), thegastropod Polmesoda erosa and the sea cucumberStichopus chloronotus were assessed in animals collectedfrom Torres Strait (Dight and Gladstone, 1993; Glad-stone, 1996). P. erosa and T. crocea were identi®ed assuitable heavy metal bioindicators for Torres Strait. Thecontamination of marine sites by tributyltin (TBT), acommonly used anti-fouling paint, has been shown tohave deleterious e�ects on many marine species, par-ticularly commercial shell®sh and wild populations ofgastropods (Waldock and Thain, 1983; Foale, 1993).Aberrations that have been attributed to organotin ex-posure include abnormal shell calci®cation, inhibition ofegg development, imposex, inhibition of reproduction,inhibition of enzymatic pathways and ultimately death(Whitney, 1990). A study carried out in the Townsvilleregion investigated the phenomenon of imposex in ma-rine snails and noted there was a high incidence of im-posex, re¯ecting high localized levels of TBT (Whitney,1990).

Algae and seagrassMarine and estuarine macroalgae and angiosperms

are able to concentrate metals from surrounding waters(Ward et al., 1986; Phillips, 1994). Accumulation is

272


thought to occur through both active and passive pro-cesses, and many metals are believed to be accumulatedin proportion to environmental concentrations (Bryan,1971). Most metals are not signi®cantly toxic to algae orseagrasses at concentrations likely to be present incoastal seawaters (Ward, 1989; Phillips, 1994). Tracemetal concentrations (Zn, Cu, Cd, Ni, Pb and Hg) in 48species of reef algae collected in Great Barrier Reefwaters between Lizard and Heron Islands in 1980 werelow and indicative of an unpolluted environment(Denton and Burdon-Jones, 1986b). Metal concentra-tions have also been assessed in a number of seagrassspecies collected from Shoalwater Bay and Townsville,Cape York and Torres Strait in 1975 and 1991 (Dentonet al., 1980; Dight and Gladstone, 1993). Data aresummarized in Table 6. Concentrations of Mn and Znwere relatively high in samples collected from theTownsville sites and all Northern Australian samplescontained high concentrations of Fe. Torres Straitsamples were lower in Fe and Zn. Metal concentrationsin the seagrasses Halophila ovalis, H. uninervis and Cy-modocea serrulata collected from the Townsville regionhave also recently been assessed (Mauger, 1997). Thisstudy concluded that there was no direct relationshipbetween seagrass and their associated sediments.

The major response in marine plants to organochlo-rine pollutants is often decreased photosynthesis andeither respiration inhibition or enhancement and growthreduction (Butler, 1977). Di�erent species of algae andseagrasses vary in their sensitivity to exposure to orga-nochlorine compounds (Ramachandran et al., 1984).The site and mechanism of pollutant action has not beenclearly demonstrated, although inhibition of cyclicphosphorylation and suppression of electron transportand ATP turnover have been documented (Ramachan-dran et al., 1984). Macroalgae and seagrasses haverarely been used to monitor trace organic contaminants(Phillips and Rainbow, 1993). There is no publisheddata on organochlorine concentrations in algae or sea-grass in Great Barrier Reef waters, and the potentialrole of these chemical stressors on seagrass decline hasnot been fully investigated in Queensland waters(Haynes et al., 1998a).

MangrovesMangrove forests occur along the entire Queensland

coast and are important bu�er zones for Great BarrierReef ecosystems as they act as traps for sediment, nu-trients and anthropogenic chemical contaminants beforethey enter adjacent waters (Peters et al., 1997). Man-grove trees however, are e�ective at sequestering toxicheavy metals and immobilising them as sulphides in thesediments as well as taking up the metals and accumu-lating them within their leaves, which are then exportedas detritus (Peters et al., 1997). Investigations of metalsexported within detritus have found that Cu, Zn, Cd,Pb, Mg and Mn are all exported from the forests viadetritus and used as a food source, and are subsequentlydetectable in tissues of mangrove oysters and various®sh (Boto and Bunt, 1981). No studies of Queenslandmangrove metal concentrations are available. PAHs arehighly toxic to mangrove forests. All types of oil areeasily trapped in mangrove forests due to the low waveaction and small tidal amplitude and readily adhere tothe mangrove roots, clogging their pneumatophores anddepriving the trees of oxygen (Peters et al., 1997).Mangroves also translocate PAHs into their tissues re-sulting in reduced productivity, lower rates of litterproduction and lower seedling survival (Saenger et al.,1983). Organochlorines vary in their impacts on man-grove forests. Some species are more susceptible to or-ganochlorines while di�ering pesticides elicit di�erentbiological responses. Species of Rhizophora spp. areparticularly sensitive to 2,4-D and will take up thecompound and transport it to their tissues. 2,4-D in-duces the breakdown of cell walls in roots and leavesand this loss of meristematic tissue results in death of thetree (Walsh et al., 1974). To date investigations of theimpacts of organochlorines and PAHs on mangroveforests have been conducted outside Australia and nocomprehensive review of the impacts of contaminantson mangroves in the GBR has been undertaken.

FishWith the exception of mercury, ®sh are generally able

to regulate accumulation of most metals (Phillips andRainbow, 1993). In contrast, organochlorines are not

TABLE 6

Metal concentrations in Great Barrier Reef seagrasses.a

Species Date Location As Ag Cd Cr Co Cu Fe Hg Mn Ni Pb Zn References

Halophila ovalis 1975 Cape York <0.2 0.5 1.0 <0.4 9.0 4418 68 1.7 1.0 67 Denton et al. (1980)Halodule pinifolia 1975 Cape York 0.1 1.1 2.3 <0.4 7.7 2010 46 4.9 3.6 26 Denton et al. (1980)Cymodocea serrulata 1975 Townsville <0.3 0.6 0.3 <0.9 3.5 563 91 3.0 0.5 50 Denton et al. (1980)Halodule uninervis 1975 Townsville <0.3 0.5 1.6 <0.6 2.7 1995 96 0.7 7.0 11 Denton et al. (1980)H. ovalis 1975 Townsville <0.3 0.2 1.2 <0.6 2.4 1985 110 0.7 6.0 12 Denton et al. (1980)Zostera capricornia 1975 Upstart Bay <0.2 0.2 0.9 <0.5 3.0 5250 70 0.6 0.4 18 Denton et al. (1980)Z. capricornia 1975 Shoalwater Bay <0.2 0.2 1.9 <0.4 2.8 3500 44 1.8 0.4 14 Denton et al. (1980)Thalassia hemprichii 1992 Torres Strait 1.83 1.02 0.89 0.171 5.94 134 27 2.74 0.37 4.91 Dight and Gladstone

(1993)Thalassodendronciliatum

1992 Torres Strait 0.84 0.93 1.01 0.26 7.6 180 <0.05 38 2.32 0.81 6.1 Dight and Gladstone(1993)

aAll concentrations lg gÿ1 dry wt.

273


regulated, and may bioaccumulate in ®sh (Phillips andRainbow, 1993; Vassilopoulou and Georgakopoulos-Gregoriades, 1993; Pastor et al., 1996), although con-centrations are related to tissue lipid levels as well asenvironmental factors such as salinity (Phillips andRainbow, 1993). Liver and muscle tissue from coraltrout (Plectropoma maculatum) and surf parrot ®sh(Scarus fasciatus) collected between Heron and LizardIslands in 1976 and 1977 were analysed for organochl-orine compounds (Olafson, 1978). Lindane (c-HCH)and DDT and its metabolites were detected in thesesamples, although concentrations were an order ofmagnitude lower than those reported for the BrisbaneRiver (Thomson and Davie, 1974). Runo� from thesugar cane industry was proposed as the source ofcontamination (Olafson, 1978). Reef sharks were foundto contain an average of 36 ng PCB gÿ1 wet wt of muscletissue which was considered to be in the range of con-centrations in biota sampled from more contaminatedwaters (Smillie and Waid, 1985). Average muscle tissueconcentrations of chlorinated organics (PCBs, DDTs,HCHs, aldrin, dieldrin and chlordanes) in coastal ma-rine ®sh species collected in the vicinity of Townsvillebetween 1989 and 1993 were low compared to samplesfrom the Brisbane region and other urbanized centres(Kannan et al., 1995). Further sampling was carried outin 1992 and 1993 of ®sh livers from 142 individual ®sh ofa wide range of species collected in the central section ofthe Great Barrier Reef Marine Park (Von Westernhagenand Klumpp, 1995). Low levels of DDE and dieldrinwere detected in 8% of samples. Fifteen species of ®sh

collected from Torres Strait were also assessed for metalconcentrations in 1992 and 1993 were found to containvery low concentrations of heavy metals (Gladstone,1996).

Marine mammalsVery few studies describing body burdens of con-

taminants in tropical Australian marine mammals havebeen carried out. Collected data are summarized inTable 7. Denton and co-workers reported metal con-centrations in muscle, liver, kidney, lung and brain tis-sue and in the blood of 48 dugongs (Dugong dugon)collected from Torres Strait and Townsville between1974 and 1978 (Denton et al., 1980; Denton, 1981).These studies detected unusually high concentrations ofFe and Zn in liver tissue and high concentrations of Cdin kidney tissue. Concentrations of Cu, Cd, Co and Agwere also elevated in the liver compared with concen-trations in other species of marine mammals. Levels ofFe, Zn, Cd and Co in the liver and Cd in the kidney werepositively correlated with age of the animal. It wasconsidered unlikely that the high metal concentrationsaccumulated by dugongs were a re¯ection of anthrop-ogenic impacts, given the remoteness of the samplingsites (Denton et al., 1980).

Similar metal concentrations were reported in muscle,kidney and liver of three dugongs stranded following acyclone in northern Australia in 1984 (Marsh, 1989).More recently, metal concentrations in muscle, liver,kidney and intestine tissue sampled from three dugongscollected from Mabuiag Island, Boigu Island and Daru

TABLE 7

Dugong metal concentrations.a

Date Location Tissue n As Ag Cd Cr Co Cu Fe Hg Mn Ni Pb Zn References

1974±1978

N Qld Liver 48 0.2±38.8 <0.1±58.8 <0.5 0.5±72 9.1±608 778±82363 1.3±9.2 <0.3 <0.3 219±4183 Dentonet al. (1980)

1974±1978

N Qld Kidney 48 <0.1±8 0.2±309 <0.3 0.1±6.5 2.7±16.6 222±3059 1.3±8.9 <0.3 <0.3 74.4±278 Dentonet al. (1980)

1974±1978

N Qld Muscle 48 <0.2 <0.2 <0.5 <0.5 0.4±2.9 28±337 0.1±3.6 <0.5 <0.5 32±113 Dentonet al. (1980)

1984 Gulf ofCarpentaria

Liver 3 26 64 47600 1653 Marsh (1989)


Kidney 3 57 10.3 844 164 Marsh (1989)


Muscle 3 <0.16 0.95 76 0.39 Marsh (1989)


Liver 1 0.37 <1.4 12.6 10.5 <0.03 4.2 0.36 1234 Parry andMunksgaard

(1992)1992 Gulf of

CarpentariaKidney 1 0.32 <1.4 116 8.2 <0.03 2.1 0.18 160 Parry and

Munksgaard(1992)


Muscle 1 <0.12 <1.4 <0.6 <1.1 <0.2 <0.2 0.13 82 Parry andMunksgaard

(1992)1993 Gulf of

CarpentariaLiver 2 0.5 <2.4 <0.6 28 8.3 0.2 1295 3


Kidney 2 0.4 <1.3 14 6.9 2.5 <0.06 115 Parry andMunksgaard

(1992)

aAll concentrations lg gÿ1 dry wt.

274


(Torres Strait) between October and December 1992were assessed (Gladstone, 1996). Three dugongs caughtin the Gulf of Carpentaria in 1992 and 1993 (Parry andMunksgaard, 1992; Parry and Munksgaard, 1993) werealso analysed for a range of heavy metals (As, Cd, Cu,Hg, Pb, Se and Zn). As found in previous Queenslandstudies, kidney and liver tissues contained the highestconcentrations of metals in the analysed tissues. Metallevels in some tissues were high enough to have healthimplications for human consumers (Gladstone, 1996).Liver tissue collected from dugong stranded at threesites along the northern Great Barrier Reef in 1996 wasfound to have elevated concentrations of As, Cr, Mnand Ni (Haynes et al., 1998b).

Very low levels of lindane and dieldrin concentrationsin the liver of four dugongs collected from Townsville in1977 were reported (Heinsohn and Marsh, 1978). PCBconcentrations in the muscle, liver and blubber of asingle dugong caught at Magnetic Island (Townsville) inthe early 1980s have also been reported (Smillie andWaid, 1985). Fat tissue collected from dugong strandedat three sites along the northern Great Barrier Reef in1996 was found to have relatively high concentrations ofpolychlorinated dibenzodioxins. In particular, octa-chlorinated species were found at levels higher than re-ported for other marine mammals (Haynes et al., 1998b,1999).

Conclusion

A range of chemical contaminants can be introducedto the Great Barrier Reef region via e�uent discharge,urban stormwater, and agricultural and industrial run-

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Documents

Organochlorine, Heavy Metal and Polyaromatic Hydrocarbon Pollutant Concentrations in the Great Barrier Reef (Australia) Environment: a Review