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State of the Marine Environment Report for Australia: The Marine Environment - Technical Annex: 1

Compiled by Leon P. Zann
Great Barrier Reef Marine Park Authority, Townsville Queensland

Ocean Rescue 2000 Program
Department of the Environment, Sport and Territories, Canberra, 1995

ISBN 0 642 17399 0

Marine phytoplankton communities in the Australian region: current status and the future threats

Gustaaf M. Hallegraeff

Department of Plant Science
University of Tasmania
GPO Box 252C, Hobart, Tas, 7001

Introduction - value and usage

The phytoplankton algae that make up the floating pastures of Australia's marine environment are the food base that supports, either directly or indirectly, the entire production of the open sea. These microscopic plants range in size from 0.2 m to 200 m (a m is 1/1000 mm), with the exceptional few reaching 4 mm in length. The diversity of organisms involved is immense and encompasses representatives of 13 algal divisions. These classes include the well-known diatoms (5000 species), dinoflagellates (2000 species), golden-brown flagellates and green flagellates (several hundred species) and the coccoid picoplanktonic forms (cyanobacteria, prochlorophytes). Just like land plants, phytoplankton algae require carbon dioxide, water, sunlight and nutrients for growth and photosynthesis. Their depth distribution is limited by the extent to which photosynthetically available sunlight can penetrate, and this ranges from 200 m in the clearest oceanic water to several metres in turbid estuaries. For their nutritional requirements (nitrates, phosphates, silicates, trace elements) the phytoplankton are strongly dependent upon physical dynamic processes which move nutrient-rich deeper water into the upper lighted zone. 'Nutrient upwelling' can occur by many mechanisms, mostly driven by winds interacting with currents and continental shelf topography. While Australian waters have no major upwelling systems comparable to those off Peru, California or north-west Africa, enrichments of a lesser kind do occur regularly and provide the nutrients for the rich diatom blooms which support Australia's most productive fisheries grounds. Anthropogenic nutrient discharges via domestic and industrial wastes can also increase the algal biomass of coastal waters but, more seriously, this has the potential to dramatically alter the original phytoplankton species composition with far-reaching implications for the structure of entire marine food chains.

This review summarises the status of our knowledge on marine phytoplankton communities in the Australian region (excluding the Antarctic) and identifies the impact of human disturbances upon them.

Description and status

Phytoplankton species composition

Recognition of three distinct phytoplankton assemblages in Australian tropical and oceanic waters has come from light microscope and electron microscope studies of the extensive phytoplankton collections made by CSIRO scientists on the research vessels RV Sprightly and FRV Soela (1980-1985). A tropical oceanic community occurs in the offshore waters of both the Coral Sea and Indian Ocean, a tropical shelf community is confined to the Gulf of Carpentaria and the North West Shelf and a temperate neritic (inshore) community is found in coastal waters of New South Wales, Victoria and Tasmania (Figures 1, 2). The larger (30-200 m) diatom and dinoflagellate species in the assemblages are different, but the smaller nanoplankton (2-20 m) are remarkably similar in all environments studied. Sometimes typical warm-water species are found in subtropical or temperate waters. This phenomenon results from tropical waters penetrating southwards in the current or eddy formations and carrying their entrained plants and animals within them. Conversely, a fourth assemblage of subantarctic phytoplankton species has been observed episodically off southern Tasmania.

The phytoplankton flora of the Australian region has strong similarities with the warm- and cold-water phytoplankton floras of the northern hemisphere. In contrast to the macroalgal flora, there is virtually no endemism in the phytoplankton. The concept of threatened species is difficult to apply to phytoplankton communities, although there is growing evidence for immigrant species being introduced into local waters of many countries via ships' ballast water (Hallegreaff & Bolch 1992). Well-documented examples are the diatom Coscinodiscus wailesii in the North Sea (which can clog fishermen's nets) and the dinoflagellate Gymnodinium catenatum in Tasmanian waters (which can contaminate shellfish with toxins harmful to the human consumer). Such introduced species or other human-made disturbances of the marine environment can only be identified from a thorough baseline knowledge of the 'normal' phytoplankton taxa and their seasonal changes in abundance and diversity in a region. In Australian coastal waters, phytoplankton checklists exist for the North West Shelf (Hallegreaff & Jeffrey 1984), the East Australian Current (Jeffrey & Hallegreaff 1987), the waters of the Great Barrier Reef (Revelante & Gilmartin 1982) and Port Hacking, New South Wales (Hallegreaff & Reid 1986). A diatom flora for the Swan River estuary in Western Australia has been prepared by John (1983) and a comprehensive phytoplankton flora for Bass Strait is also in preparation (D. Hill and co-workers). Such information is still lacking for many other parts of the Australian coastline.

Figure 1: Map of the Australian region showing the major current systems (after Jeffrey & Hallegraaf 1990).

Figure 1

Phytoplankton biomass and nutrients

Open ocean and coastal waters

The open ocean waters surrounding the Australian continent (Figure 1) are generally poor in nutrients (Jeffrey, Rochford & Cresswell 1990). The major factors responsible for this low nutrient status include: general nutrient impoverishment (particularly in phosphates) of coastal-drained soils; lack of a nutrient-rich eastern boundary current in the Indian Ocean originating in high latitudes; isolation by the Subtropical Convergence of Great Australian Bight waters from rich subantarctic waters to the south; and dominance of large areas by subtropical waters with limited nutrient reserves down to 100-200 m. Natural enrichment mechanisms in the Australian region include limited upwelling along the outer margin of the Great Barrier Reef, along the New South Wales coast between the Queensland border and Port Stephens, off the Gippsland coast of Victoria and off Port Macdonnell in South Australia; seabed coastal enrichments off New South Wales; deep convective overturn within warm-core eddies in the Tasman Sea providing nutrient enrichment to the surface; and some nutrient enrichment in the eastern Arafura Sea and northern Gulf of Carpentaria, possibly originating in the Aroe Island upwelling system. Table 1 summarises typical phytoplankton chlorophyll biomass values in various oceanic, coastal and estuarine Australian waters. Significant increases in chlorophyll biomass, exceeding these average values, are one of many signs of cultural eutrophication (see below). Well-studied phytoplankton communities in the Australian region are those of the North West Shelf and the Great Barrier Reef region, the New South Wales coast, and eddy systems of the East Australian Current.

Table 1. Summary of the seasonal range of phytoplankton chlorophyll a biomass in Australian waters

 
mg L-1
mg m-2
(water column total)
Reference
Oceanic  
Indian Ocean
0.1-1.1
10-80
Humphrey 1966
Coral Sea
0.1-0.8
15-70
Furnas & Mitchell 1986
East Australian Current
0.05-0.9
20-80
Jeffrey & Hallegraeff 1987
Coastal
 
Gulf of Carpentaria,
0.8-2.3
26-49
Hallegraeff & Jeffrey 1984
Arafura Sea
0.7-1.3
34-41
Hallegraeff & Jeffrey 1984
North West Shelf
0.2-1.1
20-55
Hallegraeff & Jeffrey 1984
Sydney coastal waters
0.1-15.0
20-280
Hallegraeff 1981
Bass Strait
0.1-1.6
-
Gibbs et al. 1986
Great Australian Bight
0.1-0.4
12
Motoda et al. 1978
Tasmanian coastal waters
0.1-6.0
-
Harris et al. 1991
Inshore  
Sydney Harbour
1.8-19.0
-
Revelante & Gilmartin 1978
Port Hacking estuary
0.1- 8.0
-
Scott 1978
Cleveland Bay,Townsville
0.1-10.0
-
Walker 1981
Port Phillip Bay, Melbourne
0.1-30.0
-
Axelrad et al. 1981.

Figure 2: The distribution of three distinct marine phytoplankton assemblages in Australian waters: (a) tropical oceanic species; (b) tropical neritic species; and (c) temperate neritis species (after Jeffrey & Hallegreaff 1990). These assemblages support differnt marine food chains and are likely to have different sensitivities towards nutrient and pollutant stress.

Figure 2

North West Shelf and Gulf of Carpentaria: The phytoplankton chlorophyll biomass (10-55 mg m2) of the warm continental shelf waters of north-west Australia, the Timor Sea, the Gulf of Carpentaria and Arafura Sea is significantly higher than that of other parts of the Eastern Indian Ocean. This is reflected in the fisheries resources of the region. The North West Shelf is the site of a productive demersal trawl fishery and the Gulf of Carpentaria supports a productive prawn fishery. In summer the North West Shelf region is invaded by nutrient-rich tropical waters, and a variety of processes such as tidal currents, internal waves and cyclone mixing carry these nutrients into the bottom waters of the shelf. Nutrient enrichment in the eastern Arafura Sea and northern Gulf of Carpentaria possibly originates in the Aroe Island upwelling system. The phytoplankton community of these waters is basically a diatom flora (Bacteriastrum, Chaetoceros, Rhizosolenia, Thalassionema ), except on occasion of episodic cyanobacterial blooms of Trichodesmium (Hallegreaff & Jeffrey 1984). Symbioses of algae within algae, or algae within animals are a feature of this tropical assemblage.

Figure 3: Annually recurrent phytoplankton blooms (as water column chlorophyll a) in Sydney coastal waters in the years 1958,1959, 1960 and 1978 (after Hallegreaff & Jeffrey 1993). It would be of considerable interest to reexamine the phytoplankton species successionsand nutrient status of these waters following the commissioning of the three new sewage outfalls in the area in 1990-91.

Figure 3

Great Barrier Reef region: The warm oligotrophic waters of the Coral Sea are characterised by low phytoplankton concentrations (15-20 mg m2), with a dominant contribution (more than 50%) of picoplanktonic cyanobacteria and coccoid eukaryotes (Furnas & Mitchell 1986). Limited upwelling occurs along the outer margin of the Great Barrier Reef and the strong tides of the region periodically pulse deep nutrient-rich waters into the coral reef lagoons during the flood tide (Andrews & Gentien 1982). This results in diatom blooms (Nitzschia, Pseudonitzschia) close to the outer reef barrier (30-70 mg m2). The Great Barrier Reef, the largest assemblage in the world of living coral-symbiotic dinoflagellate (zooxanthellae) communities, therefore represents an ecological response to tropical upwelling. Any change in the nutrient status or turbidity of these coral reef waters is likely to have significant impact on the diverse tropical benthic communities it supports. Episodic cyanobacterial blooms of Trichodesmium are also a prominent feature of the waters of the Great Barrier Reef ( Revelante & Gilmartin 1982; see below).

New South Wales coastal waters: Coastal waters off Sydney are characterised by a series of sharp chlorophyll peaks (more than 10 times normal algal biomass) due to short-lived diatom blooms (Lauderia, Pseudonitzschia, Rhizosolenia, Thalassiosira) which usually occur in spring, early summer and autumn. This phenomenon, first recognised in the 1930s (Dakin & Colefax 1933), was documented in more detail in 1958-60 (Humphrey 1963) and 1978-79 (Hallegreaff 1981) (Figure 3). Surveys in 1981 and 1984 (Hallegreaff & Jeffrey 1993) demonstrated that these diatom blooms are a feature of the entire New South Wales coastline, from Cape Hawke in the north (32oS) where the East Australian Current separates from the coast, to Maria Island off Tasmania in the south (43oS). These blooms result from nutrients brought into surface waters by the shoreward transport of deep continental slope waters, induced by the action of the East Australian Current and its associated eddies. These phytoplankton peaks (100-280 mg chlorophyll m2) must have profound significance for New South Wales coastal fisheries and coincide, for example, with the spring time spawning migrations of gemfish. It would be of considerable interest to re-examine the nutrient and phytoplankton status of Sydney coastal waters following the commissioning of three new submarine sewage outfalls in 1990-91. Extensive red tides by the dinoflagellate Noctiluca scintillans in Sydney coastal waters in early 1993 could well be an early sign of eutrophication.

East Australian Current eddies: Warm-core eddies of the East Australian Current are parcels of Coral Sea water which pinch off from meanders of the East Australian Current and drift southwards into the cooler Tasman Sea. As the surface waters cool and sink, the thermocline becomes eroded and convective overturn leads to a progressively deeper surface mixed layer of up to 300 m depth. Nutrients brought up by these deep mixing processes recirculate into the photic zone causing enrichments and diatom blooms (Pseudonitzschia, Rhizosolenia), especially at the eddy centre and sometimes also at the western boundaries where the eddies interact with the continental shelf (Jeffrey & Hallegreaff 1980, 1987). Valuable pelagic fish such as tuna tend to congregate at temperature discontinuities associated with eddy systems.

Estuaries

There is a growing public concern about the environmental quality of most major rivers, estuaries and coastal waters near Australia's large population centres where discharges of industrial, domestic and agricultural wastes are raising the nutrient levels in the water. Phytoplankton species that have always been present in low concentrations can respond to this increase by growing to bloom proportions (millions of cells per litre). Bloom-forming algae can become so densely concentrated that they generate anoxic conditions resulting in indiscriminate kills of both fish and invertebrates, especially in sheltered bays. The dinoflagellate Scrippsiella trochoidea has caused red-brown seawater discolourations and fish kills; for example, in the Hawkesbury River (New South Wales) and West Lakes (South Australia) (Hallegreaff 1991). This species (under the name Glenodinium rubrum) has also been implicated in causing fish kills in Sydney Harbour as early as 1890 (Whitelegge 1891). Other estuaries with annually recurrent algal bloom problems are Port Phillip Bay (Victoria), Huon and Derwent rivers (Tasmania), the Port River (South Australia) and the Peel-Harvey estuary and Cockburn Sound (Western Australia). As in many other parts of the world (Anderson 1989, Smayda 1990, Hallegreaff 1993), in the past two decades there has been a recognition of an apparent increase in the frequency, intensity and geographic distribution of such harmful algal blooms in the Australian region (Hallegreaff 1992).

Figure 4: Long-term nutrient data for the River Rhine in europe, showing evidence for a 7.5-fold increase in phosphate loading, a 3-fold increase in nitrate levels , but more seriously a significant decrease in Si:P and N:P nutrient ratios. Such altered nutrient ratios favour blooms of nuisance flagellate species ( Phaeocystis pouchetii, Chrysochromulina polylepis) replacing the normal 'wholesome' spring and autumn blooms of siliceous diatoms (after Hallegreaff 1993).

Figure 4

Issues

Cultural eutrophication

Overseas experience from areas such as Hong Kong harbour, the Seto Inland Sea in Japan and northern European coastal waters indicates that 'cultural eutrophication' from domestic, industrial and agricultural wastes can stimulate harmful algal blooms. Figure 4 illustrates the pattern of long-term increase in nutrient loading of coastal waters of the North Sea. Since 1955 the phosphate loading of the River Rhine has increased 7.5-fold, while nitrate levels have increased 3-fold. This increase has resulted in a significant 6-fold decline in the silicate:phosphorus ratio, because long-term reactive silicate concentrations (a nutrient derived from natural land weathering) have remained constant. More recently, improved wastewater treatment has also been causing increases in the ammonia:nitrate ratio of River Rhine discharge (see review by Hallegreaff 1993). It is important to realise that the nutrient composition of treated wastewater is never the same as that of the waters in which it is being discharged, and indiscriminate reductions in nutrient discharges are therefore not addressing the problem of changing nutrient ratios of coastal waters. There is considerable concern (Smayda 1990) that such altered nutrient ratios may favour blooms of nuisance flagellate species which replace the normal spring and autumn blooms of 'wholesome' siliceous diatoms. Changed patterns of land use, such as deforestation, can also cause shifts in phytoplankton species composition by increasing the concentrations of humic substances in land run-off (Figure 5). Only three comparable long-term phytoplankton and nutrient data are available for Australian waters, viz. the CSIRO hydrological stations at Port Hacking (New South Wales), Maria Island (Tasmania) and Rottnest Island (Western Australia).

Figure 5: Changed patterns of land use, such as deforestation, increase the concentration of humic substances and trace metals in land runoff and can cause shifts in phytoplankton species composition (from Graneli el al. 1989).

Figure 5

Cyanobacterial blooms

Trichodesmium blooms in tropical waters

The filamentous cyanobacterium Trichodesmium erythraeum is the most common 'red tide' organism in tropical Australian coastal and oceanic waters. At the start of the bloom, the filaments usually appear throughout the water column, but during late-bloom stages the development of strong gas vacuoles causes a massive rise of the alga to the surface layers. This species produces seasonal (February-April) water blooms in the Java, Banda, Arafura and Coral seas, and from there the East Australian Current and Leeuwin Current transport the algal masses (covering up to 40 000 km2) as far south as Sydney (Jervis Bay) and Perth (Albany) respectively. The alga is perceived as a nuisance to swimmers on Australian beaches and has significant impacts on recreation, but harmful effects on humans or marine life have seldom been reported. It is not yet known whether Australian strains of Trichodesmium produce neurotoxic compounds similar to those reported from populations from the Virgin Islands (Hawser et al. 1991). Trichodesmium red tides ('sea sawdust') were observed as early as 1770 during Captain Cook's voyage through the Coral Sea, and in a strict sense, they should be regarded as completely natural events. Differentiated cells in the centre of each minute Trichodesmium colony are capable of fixing atmospheric nitrogen, which allows the alga to thrive under nutrient-impoverished oceanic conditions. It is possible, however, that coastal nutrients (especially phosphates) can stimulate or prolong the blooms once they are washed inshore. It is a contentious issue, at present, whether or not the apparent increase in Trichodesmium blooms in the Great Barrier Reef region is caused by coastal eutrophication (Kinsey 1991).

Figure 6: Long-term pattern of toxic Nodularia spumigena cyanobacterial blooms in the Peel-Harvey estuary, Western Australia, related to phosphate discharge from agricultural fertilisers in the previous winter period (after Hillman, Lukatelich & and McComb 1990).

Figure 6

Figure 7: The production by plankton dinoflagellates of potent neurological toxins which accumulate in shellfish and thereby can poison human consumers. Until 1980, this phenomenon of paralytic shellfish poisoning (PSP) was unknown fron the Australian region and there exist, for example, no historic Aboriginal reports of poisoning after shellfish consumption. There is strong circumstantial evidence the PSP dinoflagellate Gymnodinium catenatum was introduced into Tasmanian waters via ships' ballast water originating from either Japan or Korea.

Figure 7

Toxic cyanobacterial blooms in freshwaters and estuaries

Toxic blooms of the brackish water cyanobacterium Nodularia spumigena were first recorded in Australia from Lake Alexandrina as early as 1878 (Francis 1878). However, their increasing frequency and distribution in the Gippsland Lakes system in eastern Victoria, in Orielton Lagoon in Tasmania, in the Darling and Murray rivers of South Australia and in the Peel-Harvey, Cockburn Sound and Vasse- Wonnerup estuaries of Western Australia, appears to be related to phosphorus from agricultural fertilisers and sewage being washed into the river systems (Hillman, Lukatelich & McComb 1990; Figure 6). This brackish water organism produces the hepatotoxic peptide, nodularin, which has killed domestic and wild animals that drink from the shores of eutrophic ponds, lakes and reservoirs (Main et al. 1977). The species Anabaena circinalis (producer of the neurotoxic alkaloid, saxitoxin and derivatives) and Microcystis aeruginosa (producer of the hepatotoxic polypeptide, microcystin) cause similar problems, but tend to be confined to truly freshwater environments. In November- December 1991, a massive bloom of Anabaena circinalis throughout 1200 km of the Darling River system contaminated essential drinking water supplies for country towns, killing sheep, cattle and wildlife. This bloom has been attributed to a combination of sluggish river flow, high water temperatures and the build-up in sediments of nutrients from agricultural fertilisers, feedlot wastes and especially sewage from townships.

Impact of algal blooms on aquaculture

The considerable expansion of marine and freshwater aquaculture production in Australia (O'Sullivan, 1990) is focusing attention on phytoplankton species that can contaminate shellfish with human neurotoxins or damage the sensitive gill tissues of finfish, especially when held in intensive cage culture systems.

Algal blooms affecting shellfish aquaculture

Until the late 1980s, the phenomenon of paralytic shellfish poisoning (PSP; Figure 7) was unknown from the Australian region. Tasmania was the first State in Australia to suffer major problems with toxic dinoflagellates contaminating farmed shellfish. Blooms of the dinoflagellate Gymnodinium catenatum in 1986, 1987, 1991 and 1993 caused the temporary closure of up to 48 shellfish farms for periods of up to six months Hallegreaff et al. 1989). The localised distribution of G. catenatum around the port of Hobart and the absence of plankton and benthic cyst records of this species prior to 1980 led to speculation that this organism had been introduced. Cyst stages of this species have been detected in ships' ballast water entering Australian ports from Japan and Korea (Hallegreaff & Bolch, 1992).

Red tides by the toxic dinoflagellate Alexandrium minutum were first recognised in the Port River area near metropolitan Adelaide in October 1986 (Hallegreaff, Steffensen & Wetherbee 1988). This species now produces annually recurrent red water blooms (up to 10 8 cells per l) in the period September-November (Cannon, 1990) and has also been detected in low concentrations in Western Australia and New South Wales. Wild mussels from the Port River area can be highly toxic to humans (Oshima et al. 1989), but fortunately no commercial shellfish farms are located in the affected area. Plankton and cyst surveys in Port River in 1983 failed to detect A. minutum in an area which now has recurrent blooms. This result has led to speculation that A. minutum could also be an introduced species, and genetic studies using ribosomal DNA sequencing have confirmed a close affinity between Australian and Spanish isolates of this species complex (Scholin, Hallegreaff & Anderson 1994). Finally, the toxic dinoflagellate Alexandrium catenella was first recognised in 1986 in Port Phillip Bay where it caused significant toxicity in wild mussels. Fortunately only minor effects on commercial shellfish farms have been reported ( Hallegreaff et al. 1991). This species is also known from New South Wales (Port Jackson, Port Botany, Batemans Bay). Once an area has been infested with cyst-producing toxic dinoflagellates, there is little hope to eradicate the problem. The only solution is an avoidance strategy of regularly monitoring shellfish products for toxins and, on the basis of the results, imposing temporary closures of farms. Every attempt should be made not to spread the problem - for example, by resuspending cysts by dredging operations or by relaying shellfish stocks to non-infected areas.

Algal blooms affecting finfish aquaculture

A wide range of prymnesiophyte, diatom and dinoflagellate species can damage fishes' gills, either by purely physical mechanisms such as increased seawater viscosity due to secretion of algal mucilages, by chemical mechanisms such as the production of substances which affect cell permeability and/or cause a necrosis and sloughing of epithelial tissues of the gills and digestive system. While wild fish stocks have the freedom to swim away from problem areas, caged fish are extremely vulnerable to noxious algal blooms. In January 1989, a bloom of the raphidophyte flagellate Heterosigma akashiwo in Big Glory Bay, Stuart Island, New Zealand, killed NZ$ 12 million worth of cage-reared chinook salmon (Chang, Anderson & Boustead 1990). Within the Australian region, blooms of this species are known from Port Stephens (New South Wales), West Lakes (South Australia) and Cockburn Sound (Western Australia), but no major marine mortalities have been reported. The dinoflagellate Gymnodinium mikimotoi (related to the Norwegian fish-killer Gyrodinium aureolum Tangen 1977) has caused some mortality in fish farms in south-eastern Tasmania (Hallegreaff 1991) and a diatom bloom of Chaetoceros criophilum has been associated with irritation among caged fish in south-eastern Tasmanian waters. The diatom's spines (setae) can break off and penetrate the gill membranes of fish .

Sensitivity of phytoplankton to chemical pollutants

Chemical pollutants, including both organic and inorganic compounds, can cause selective inhibition of phytoplankton species, with wide ranging effects at higher trophic levels. Chlorinated organics, including DDT, dieldrin, chlordane, polychlorinated biphenyls (PCBs) and chlorophenols, are of particular concern because they readily absorb to particulates and sediments, are resistant to degradation and have the potential to bioaccumulate. PCB levels (1-10 mg per l) have been reported in Botany Bay and Port Phillip Bay, and may depress the growth of sensitive diatoms (Fisher & Wurster 1973). Pesticides in agricultural land run-off may inhibit zooplankton grazing, thereby stimulating algal blooms. The effects on phytoplankton of effluents from chlorine-bleaching pulp and paper mills, including chlorate, chlorophenols, resin acids and chlorinated lignin derivatives, are also receiving attention (J. Stauber, pers. comm.). Some of the chlorophenolic compounds, such as the more substituted chlorocatechols, are toxic to freshwater algae and marine diatoms (Kuivasniemi, Eloranta & Knuutinen 1985), with chlorate being particularly toxic to phytoplankton. Petroleum hydrocarbon contamination (1-23 mg per l) has also been documented in Australian waters - for example in Port Phillip Bay (Smith & Burns 1978). While occasional oil spills may lead to acute toxic effects (ie plankton mortality) chronic effects are less likely to occur because of degradation and removal processes.

The Australian coastline has a number of locations with high heavy metal concentration

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