An assessment of the environmental impact of wild harvest pearl aquaculture (Pinctada maxima) in western Australia.

ABSTRACT Typical operating procedures used in the wild harvest pearl aquaculture (Pinctada maxima) industry in Western Australia are described as a basis for examining the potential environmental impact of the industry. A risk analysis workshop was held, which included industry representatives, marine scientists, regulatory agencies and conservation interests. The goal of the workshop was to document the main potential environmental and ecological risks that arise from the various activities carried out by the P. maxima industry. Thirteen environmental and ecological issues were identified across the P. maxima fishery. None were considered to be high risks; all were ranked as either moderate (23%) or low (77%). Moderate risk rankings included: introduction of disease from seeding; attraction of other fauna and introduction of exotic organisms. Low risks were: spread of disease; introduction of disease from hatchery; introduction of disease from translocation; impact to protected and endangered species resulting from entanglement; impact of habitat; impact to protected and endangered species resulting from farm lighting; nutrient impacts in sediment; perceived change in water quality; potential for litter and reduction of primary productivity. The low ratings given to disease risks took into account current strict regulatory controls for minimizing disease risks. The industry is considered to be environmentally benign. However, recommendations are made on how to further minimize risk.

KEY WORDS: pearling, aquaculture, environment, Pinctada maxima

INTRODUCTION

The Western Australian pearling industry is a world leader, with a current average annual value of about $125 million Australian. The Australian South Sea pearls produced are well regarded in the industry worldwide, and Western Australian companies have an enviable record for producing a high quality product. The pearling industry is unique in being a mix of wild capture and growout. It is the second largest successful aquaculture industry in Australia. In terms of dollar value, the fishery is second in Western Australia only to the western rock lobster, Panulirus cygnus. The industry is based on the pearl oyster Pinctada maxima (Jameson 1901), a bivalve mollusk species that has a widespread distribution in the Indo-Pacific and is not limited to Western Australia. Several other species of pearl oysters are cultured on a small scale in Western Australia, but are not covered in this article.

Pearl production has a long history in Western Australia, with the first recorded operations being in Shark Bay in 1850. In the early years, natural pearls were harvested from Pinctada albina (Lamarck 1819) collected intertidally or dredged from shallow water. Later shells became more valuable than the pearls and the industry was based on mother of pearl. No regulations were in place to sustainably manage the industry. As a result, pearl oysters were over collected, stocks became depleted and the fishery collapsed. The industry moved to the north coast of Western Australia where it centered on Broome and used the larger P. maxima. Shells were still the dominant product. By 1910 there were nearly 400 luggers and 3,500 people in the industry. However, when plastic buttons were introduced the industry crashed, and Western Australian pearling almost disappeared entirely during World War II. The industry made a comeback after the war with the beginning of the cultured pearl industry. The settlement of Kuri Bay started in 1956 and is still in operation (Shepherd 1975, Taylor 1985, Anderson 1996). In the early decades the fishery went through cycles of boom and bust, with the loss of men and boats through cyclones and other storms, loss of life and permanent injuries through diving mishaps and the bends, labor problems, racial tensions and fluctuating prices. Whereas there are still variations in the economic cycles, the industry is now highly organized and is geared to maintain sustainable production on an economically and environmentally sound basis. In this study we describe operations of the industry and assess its environmental impact.

INFORMATION SOURCES

This study combines information gathered in two studies. For the first study (Enzer Marine Environmental Consulting 1998), an extensive literature search was undertaken to obtain information on the industry and the possible environmental effects of it. Copies of regulatory requirements were obtained from appropriate agencies. Discussions about the perceived environmental effects of the industry were held with governmental officers and other people within and outside of the industry. An 8-day field trip to the North West was undertaken to obtain first hand knowledge of the industry and its practices. The trip included an examination of a pearl oyster hatchery in Broome, 3 days observing fishing operations off Eighty Mile Beach, including several dives on various bottom types during the collection of pearl oysters and on shell holding areas to examine for any effects of the bottom longlines. One day was spent in Roebuck Bay at Broome on a bottom culture farm to observe the effects of shell culture and structures close to the bottom in various bottom types in the area. Three days were spent in King Sound to examine how surface longline farms operate, the cleaning process, methods of handling various wastes and rubbish, etc. Two types of farms were visited, a shore-based farm and two that are sea based.

For the second study (Jernakoff 2002), a site visit was conducted to evaluate current pearl industry practices and procedures. The objectives of the site visit were to: visit three pearl farms (Bynoe Harbour, Northern Territory; Kuri Bay, Western Australia and Talbot Bay, Western Australia), fishing vessels and interview staff to assess how the fishery operates and how closely its procedures and practices are in line with those required of an internationally recognized environmental management system; assess the degree to which existing practices and procedures are implemented; and report on the site visit and evaluate physical conditions, existing practices and procedures of a pearl industry in operation in the Broome, Darwin and Kimberley region, the area of Western Australia that is northeast of Broome. During the visit the observed farming activities included growout, seeding and harvesting. The physical conditions were observed in which the activities operated and the extent to which management systems were implemented.

An environmental and ecological risk assessment workshop was then conducted in September 2001 based on existing knowledge, considering all aspects of the fishery, identifying and prioritizing gaps in knowledge and producing a set of prioritized risks. The workshop included eight representatives of industry, five fishery scientists and managers, four staff from regulatory agencies and two community environmental representatives. The goal of the workshop was to document and risk rank the main potential environmental and ecological risks that arise from the various activities carried out by the P. maxima industry. This risk register is used to identify the underlying issues so that these may be addressed through the development of an appropriate management strategy to reduce the risk of deleteriously affecting the ecosystem in which the industry occurs. The aim was also to integrate the workshop with a broader ecological sustainable development (ESD) research program by providing a session of the workshop for the Department of Fisheries Western Australia (DFWA) to address environmental and ecological risks for the wild harvest component of the P. maxima fishery. The identification of key environmental issues assisted in determining if adequate information on those issues exists or if information is required after a review of national and international literature.

At the environmental risk assessment workshop, participants were asked to list all of the sources of environmental problems that could potentially be caused by the industry. The potential sources were then entered into a risk matrix of likelihood and consequence. Each of these was assessed against a score varying from 1-6. A likelihood of 1 was considered to be remote, whereas 6 was considered to be very likely. If the event did occur, the consequence was judged against a scale where 1 was negligible and 6 was catastrophic. Multiplying the two scores together provided their position on the matrix. Scores of 20 and above were assessed as being of high concern, 7-19 were moderate, and 6 and below were low.

BIOLOGY OF PINCTADA MAXIMA

The pearl oyster, P. maxima is widespread in the Indo-West Pacific. In Western Australia it has been recorded as far south as Shark Bay, but it is not commercially fished south of North West Cape. The species is a protandrous hermaphrodite, maturing first as males at an age of 3 to 4 years and a size of 110-120 mm. As they age, the animals undergo a sex change and become female. By 170 mm half of the animals are males and half are females. By 190 mm the population is entirely female. Because the animals can spawn every year, each individual functions as both a male and then a female for several spawning seasons. Very few animals are simultaneous hermaphrodites. The breeding season is long, from September to October to April to May; most spawning occurs from the middle of October to December, with a smaller secondary spawning in February and March (Rose et al. 1990, Rose & Baker 1994, Knuckey 1995).

Gametes are spawned into the water column and fertilization is external. Females release from 2-12 million ova each, with a diameter of 60 [micro]m. Veliger shells form after 1 day, at an average size of 79 [micro]m. The planktonic veliger stage is a distributional phase that allows the young pearl oysters to colonize new areas if suitable bottom can be found. The pediveliger stage is reached by day 22 to 24. The majority of veligers start metamorphosing into juveniles on day 24. Settlement occurs over days 28 to 35. In nature, when veligers are ready to metamorphose they settle to the bottom and search for a suitable habitat. If an appropriate area is found, they settle on it and metamorphose into the juvenile stage. If no suitable settlement site is located within a short period the animals metamorphose and die (Rose & Baker 1994).

After settling to the bottom, P. maxima is byssate and attached to the bottom during its juvenile and adult phases of the life cycle. It requires a hard surface for the initial attachment, and once it is attached to the bottom the connection is permanent. P. maxima lives on shallow rocky pavements on the continental shelf where there are small crevices into which the young animals can settle and develop. Like most bivalves, pearl oysters are filter feeders. Growth rates are initially fast. Field measurements at Eighty Mile Beach have shown that the animals reach the minimum legal size of 120 mm shell height in their third year of life. They are fished for 3 to 4 years before growing to a size of 160 mm, beyond which they are no longer suitable for round pearl culture. Large oysters of 200 mm are 15-20 y old (Joll 1996). The animals can reach a maximum of 270 mm (Rose & Baker 1994).

MANAGEMENT OF THE INDUSTRY

Pearling and pearl farms for P. maxima, are managed by the Department of Fisheries Western Australian (DFWA) under the provisions of the Pearling Act 1990. The definition of P. maxima in the act includes any hybrids of P. maxima produced through laboratory technology. The Act is currently being rewritten. Other pearl oysters, such as P. margaritifera (Lamarck 1819), are regulated under the Fish Resources Management Act 1994. The industry is also regulated by a number of acts that deal with items such as marine safety, employment conditions, etc, which are not considered in this study. Under the Australian Commonwealth government's Environmental Protection and Biodiversity Conservation Act 1999, a fishery must be certified as environmentally sustainable by the Commonwealth Department of Environment and Heritage. This has been done for the maxima pearling industry. A copy of the assessment application and determination are available at http://deh.gov.au/coasts/fisheries/wa/pearl/index.html. Whereas culture and management methods are similar, the other species are not discussed in this study. The major fisheries regulations for P. maxima are described later.

Pearl oysters caught in the wild are seeded with a nucleus at sea in laboratory type conditions on board specially built vessels, then grown out in controlled sea lease areas for 2 years to produce cultured pearls. The wild stock of pearl oysters has thus been the basis of the industry. Several standard fisheries management procedures protect the stocks and ensure continuity of supply. Taking of pearl oysters for seeding is currently controlled by a quota system (total allowable catch is 572,000, but can be varied as necessary) and additional measures, including size limits. Each operator has an annual quota of live pearl shell. In addition, the animals must be collected from specified zones within the fishery (Fig. 1). The minimum size limit for collection of pearl oysters is 120 mm, when the animals are 3 to 4 years old. There is no regulated maximum size, but in practice individuals are not taken over 160 mm because they are too slow growing to produce high quality pearls. This has a beneficial effect in helping to maintain the breeding stocks because the larger animals are females. Maximum sizes may be specified for particular areas of the fishery (e.g., Exmouth Gulf). Catch and effort data must be provided to DFWA on each dive made during the collecting season. Details are logged using square blocks of 10 nautical miles divided into subblocks of squares with sides of 2.5 nautical miles.

[FIGURE 1 OMITTED]

Pearl oysters are seeded after collection and held on the pearling grounds for a period of about 3 months before they are transferred to the farm leases. This allows the animals to recuperate after the stress of being collected, transported to the holding areas and having the nucleus inserted. After the nucleus is inserted, the shells are held in areas separated from those of other operators and areas being fished. Farms are also separated from each other, usually by 5 nautical miles as a counter disease method. However, if the licensee of an existing farm agrees, a new farm can be established as near as 2 nautical miles (FDWA 1997a). Additional reasons for having a clear separation between operators include providing each farm with opportunities for expansion and security of their equipment and pearl oysters.

In recent years hatchery-grown spat have been increasingly used to supplement wild stock. This provides a mechanism for enlarging the industry in a controlled manner, ensuring a steady supply of stock and in the future potentially reducing costs of obtaining pearl oysters for seeding. Several hatcheries are now in operation. They are all subject to a stringent translocation protocol developed by DFWA in liaison with industry (FDWA 1997b). The hatchery technology provides increased potential for mixing genetically distinct populations during culturing. Johnson and Joll (1993) examined the genetic structure of P. maxima collected from 5 widely separated areas: Exmouth Gulf and Cape Bossut, Western Australia; Flat Top Bank and Oxley Island, Northern Territory and Thursday Island, Queensland. Most of the variation found was clinal between western and eastern populations, but comparisons between adjacent pairs of samples usually showed significant genetic differences. This includes the two locations in the Northern Territory that were only 320 km apart. Western Australian samples showed little subdivision over the 800 km from Exmouth Gulf to Cape Bossut. Johnson and Joll (1993) suggested that stocks are in general highly divided in northern Australia but that there are also substantial connections that occur in Western Australia over long distances. The 80,000 to 100,000 P. maxima transported annually from Western Australia to farms in the Northern Territory do not seem to have affected adjacent natural populations.

The Western Australian Department of Conservation and Land Management administers several types of marine reserves, and a formal assessment process is undertaken for any application for a pearling lease in a marine reserve. The decision on whether to grant lease approval in a marine reserve rests with the Minister for the Environment, not the Minister for Fisheries. The management areas are:

* Marine nature reserves are set aside for the protection of flora and fauna. Pearling activities are not permitted.

* Marine parks. A series of management zones is established in each marine park to determine the activities that can be undertaken in each zone. Pearling activities may be undertaken in general use zones and some special purpose zones but not in sanctuary and recreation zones.

* Marine management areas allow a broader management approach in the marine environment. Pearling activities are permitted.

* Land reserves include nature reserves, conservation parks and national parks. Land-based pearling activities are not considered to be compatible with the purposes and objectives of the land reserves and are not allowed.

METHODS USED BY THE FISHERY

Background

In 2004 there were 16 operators in the pearl industry in Western Australia, with locations from Exmouth Gulf to the Kimberley. Pearl oysters collected in Western Australia are also used to produce pearls at growout areas in the Northern Territory. Because of differing geography and size of the individual operations, there are differences in the approaches used to produce pearls, but all share common features. The techniques outlined later are generic for the industry, and may be modified by individual operators to adapt to local conditions.

During the late 1970s and early 1980s serious mortality of pearl oysters occurred in the transportation phase of the industry. The mortality was attributed to the bacterium Vibrio harveyi, which occurs naturally in the marine environment, including the water column, in sediments and in the guts of marine animals. The mortality occurred after transportation of the pearl oysters from collection areas to the lease sites. Instead of the usual 10% to 20% mortality, losses on lease sites were up to 80%. Surviving pearl oysters developed deformed nacre and were useless for half pearl or mother of pearl production. Poor water circulation and accumulations of mollusk feces on the bottoms of the tanks in which the oysters were transported were found to allow the number of bacteria to increase exponentially during transport. The possibility was also raised that circulation was not as effective on culture rafts as on long lines, and bacterial densities were higher. Whereas other infectious agents or causative factors could have been involved, it was concluded that pearl oysters were weakened during the low temperatures of winter, and they became infected when they came into contact with high bacterial concentrations (Wolf & Sprague 1978, Pass & Perkins 1985, Dybdahl & Pass 1985, Pass et al. 1987, 1988).

The mortality experience has made the pearling industry operators acutely aware that they are dealing with live animals that must be treated properly if high quality pearl production is to be achieved. A number of changes were made to improve treatment of the animals. The various processes are now staged to allow the animals to recover from each procedure (collection, transportation, seed implantation, etc.) before the next stage is attempted. Water circulation during transportation has been improved considerably, and the water in tanks is now exchanged about every 10 min. High-density raft culture has ceased and been replaced with long line techniques that use a lower stocking density.

The pearl industry makes use of a natural phenomenon that occurs in shelled mollusks. Shells produced by mollusks are a mixture of an organic matrix that provides the shape and structure and calcium carbonate that is the actual hard shell material. As a protective mechanism, many species secrete calcium carbonate around a foreign object that becomes lodged in their tissues. This seals the object off from the tissues, rendering it inert to the moilusk. The animal continues to secrete additional material onto the foreign object over time as it secretes additional shell. Many species of bivalves in a variety of groups, and indeed even some gastropods, produce pearls naturally. Because of their high quality, marine bivalves of the family Pteriidae produce most commercial pearls; some are also produced by freshwater species.

Because foreign objects, which lodge in tissues, vary considerably in shape and size; natural (keshi or seedless) pearls tend to be irregular in shape and lustre. Cultured pearls are produced by placing an inert foreign object into a pearl oyster so that it is completely surrounded by mantle tissue inserted in the gonad. The pearl oyster secretes shell material that seals the nucleus completely from the remainder of the body. Over time the animal continues to add layers to the pearl, continually enlarging it. The most common type of nucleus in use at present is made from the shells of freshwater bivalves from the Mississippi River of the United States, but there is an active search by the industry for an alternative source of nuclei.

Inserting a hollow plastic shape between the tissues of the animal and the shell of a pearl oyster in its final year of production makes half round or mabe pearls. The animal secretes shell over the foreign material, resulting in a half globe shape that is continuous with the remainder of the interior of the shell. Mabe pearls are large, with a thin covering of calcium carbonate over the base that had been inserted into the animal. All parts of the animal are used after an individual oyster produces its final pearl: pearls are harvested, the shell is sold for mother of pearl, and the adductor muscle for edible meat.

Obtaining Wild Caught Pearls

Harvesting of wild pearl oysters occurs from Cape Leveque to Exmouth Gulf, with most collected off Eighty Mile Beach (Bowen 1991). Stocks of commercial quantities of animals at fishable depths (i.e., safe diving depths of <20 m) were surveyed between Broome and the Lacepede Islands in the 1980s (Penn & Dybdahl 1988). Other industry-based surveys have been made in other areas and are available to the industry but have not been formally published (Bowen 1991).

Sea bottoms on which pearl oysters are common are areas where there are crevices that allow the young animals to settle into a protected environment and a hard substratum for them to attach. The industry recognizes a variety of bottom types and has developed names for each. There are transitional zones between the bottom types. If a boat is traveling at a speed of 1 knot during a 1-hour dive, the total distance traversed will be about 1,800 m and there can be several minor changes in bottom type during the dive.

The bottom is typically a fiat basement rock with very little relief. Fine sediment accumulates on it to a depth of a few millimeters, obscuring the underlying rock surface. A variety of organisms attach to the rock and provide the vertical relief up to 1 m off the bottom. There can be a substantial overlap in the fauna on the various bottom types; the type is determined by the dominant species present.

A low, round densely packed ascidian species, which lives attached on the bottom is the dominant species on potato bottom. In areas of heavy potato bottom the ascidians are almost completely dominant. Sponges are the next most dominant group, with a large variety of vase shaped, basket sponges and massive sponges up to 0.5 m high interspersed with smaller sponges of only a few centimeters. A variety of other attached fauna is also present, including sea fans, soft corals and sea whips. Despite the diversity of taxa present, total density is low. A very few corals (Turbinaria) are present. Faunal density rapidly decreases in areas where the rock is covered with sediment 2-3 cm deep. Bare sand patches can be interspersed between areas of potato bottom.

Garden bottom has a diverse faunal assemblage dominated by alcyonarian sea whips. Distance between the sea whips is variable, but on average they grow about 1 meter apart. The animals grow rapidly to up to 1 meter in height and quickly become encrusted with a variety of organisms, some very colorful, so the bottom does in fact resemble a garden. Sponges and other small encrusting organisms grow on the sea whips. Other than sea whips, a variety of sponges is present on the bottom. Ascidians are present, but are a larger species than that found on potato bottom. Other fauna present includes soft corals, sea pens and crinoids. No hard corals are present.

Whereas potato and garden bottoms dominate in the fishing area, several other bottom types are recognized by the industry, including collar, asparagus, etc. All share the common features of being located on a bottom with underlying rock that are inhabited by a wide variety of invertebrates. None of the habitats are in ecologically sensitive areas such as seagrasses, coral reefs or mangroves, which lack commercial quantities of pearl oysters.

The pearling vessel is a boat up to about 35 m long. Some of the modern vessels are custom made for the pearling industry, others are modifications of existing boats. To save costs there has been a recent trend for the modern vessels owned by one company to be contracted to also collect pearl oysters for the smaller companies and all gain from economies of scale. The boat crew is usually from 10-12 people, including the skipper, engineer, deckhands, cook(s) and six divers. Booms are extended outward from each side of the vessel during the fishing for pearl oysters. On an average boat, three weighted ropes are hung vertically from each boom to a height of about 1 m off the bottom. There are thus six divers working at a time on the boat. A Morse code type of signal system is used by the chief diver to communicate with the crew on the boat, and control the boat speed, direction, height of the weights and divers, etc. On the rare occasion the weight strikes the bottom, the boat is signaled and the weight is raised. Not only does this practice prevent damage to the bottom, but if the weight is not raised it clouds the water, preventing the diver from fishing efficiently. A large bag near the weight is used to store pearls after they are collected. A good diver collects an average of 250 pearl oysters per day. The areas where pearls are collected are subject to extreme tidal ranges ([less than or equal to] 9 m), and consequently have very strong tidal currents. Diving is too difficult and dangerous during the spring tidal periods, and is only undertaken on the neap cycle when currents are substantially reduced and visibility is good. Fishing for live pearl oysters begins in January and continues for up to 5 months. The locations of patches have been logged and are revisited on a regular basis. The boat starts at one side of a patch and moves slowly with the tide across the patch at a rate of about 1 knot. Divers operate on hookah, or air supplied from a surface compressor; oxygen may be used at the end of the dive recompression to increase the rate at which nitrogen is purged from the body tissues of the diver. Each diver wears a smaller neck bag during the dive. As pearl oysters are collected they are kept in the neck bag until it is full. The pearl oysters are then transferred to the larger holding bag at the end of each weighted rope. The divers swim about 1.5 m off the bottom to obtain the maximum field of view. In murky water they swim closer to the bottom but are still off it.

At the end of each of the dives the pearl oysters that have been collected are recovered and measured. Under- and oversize oysters are returned immediately to the sea. As divers are paid only for correctly sized animals, novice divers rapidly learn to select sized animals. Shells are cleaned by simply scraping encrusting organisms off the pearl shell with a knife. A high-pressure hose is then used to wash the shells; no chemicals are used. The pearl oysters are placed in wire frame panels holding six animals each, and every panel is individually tagged to indicate which company has collected the shell and placed in a recirculating tank on board. When sufficient animals have been collected, they are taken to a holding area where they are carefully placed on the sea bottom in a marked area for later usage. The panels are attached at 900 mm intervals to lines, which may be several hundred meters long. Divers inspect the line on the bottom to ensure the pearl oysters are in the proper orientation. The bottom selected in this region is very similar to the fishing ground. Sponges are dominant, but there are also soft corals, sea fans and other fauna present, including some Turbinaria corals. The period of up to 2 months that the pearl oysters remain in the holding area minimizes the physiological effect of having been collected and allows the animals to recover before the nucleus is inserted. Additional holding areas are used because the boat works different areas.

Seeding the Pearl Oyster

When they are to be seeded, the pearl oysters are recovered, and a piece of mantle tissue from another animal is inserted into the host oyster gonad along with the nucleus for the pearl. The operation is simple, but delicate. The inserted mantle tissue becomes part of the host oyster's tissues, creating a sac around the nucleus. If the oyster is subsequently used to produce a second pearl, the same sac of tissue is used (Joll 1996). After the operation the animals are returned to the ocean in panels at the holding area, again to minimize stress to the pearl oyster. After an initial recovery period of 7 to 8 days the pearl oyster panels are turned by divers over every 2 to 5 days. The turning helps to develop the sac around the nucleus and prevents the nucleus from breaking out of the tissue. The pearl oysters are x-rayed after 4 to 6 months to determine whether nucleus has been retained and the pearl has started to grow. If the nucleus has been rejected from the animal, the pearl oyster is operated on again in the following year or replaced with a hatchery shell (Scoones 1991, Joll 1996).

Transportation to the Farm

Pearl oysters must be cleared from the holding areas by December 31 of every year. They are transported by boat to the pearl farm usually in the waters north of Broome. During transportation, the animals are maintained in seawater in holding tanks on the vessel with running seawater to keep the animals in as natural water conditions as possible. The water may be coarsely filtered to remove large particles. The rate of flow into the tanks changes the water about every 10 min. No feeding or chemicals are used in the transportation process. Each boat is capable of transporting 20,000 to 25,000 animals on a single trip.

Farming Methods

The pearl oysters in the panels are removed from the holding tanks on the boat at the farm. The tanks are emptied and cleaned using a disinfectant before the boat returns to the holding area to obtain a second load of pearl oysters. After the animals have been transported to the pearl farm they are placed in panels on surface long lines into the ocean for a period of 2 years to allow the pearls to grow. When the pearls have been harvested, as many pearl oysters as possible are reseeded. Approximately 40% to 50% of the animals can be used a second time. Forty to fifty percent of these can be reused for a third time; some individual pearl oysters can be used for up to 8 years.

Two anchoring systems are used to keep pearl oysters in the water at the farm, based on the amount of exposure at the site. Most farms use surface longlines. This has the advantages of avoiding the use of divers, minimizing interactions with large saltwater crocodiles and allowing the use of less skilled workers for routine work. In the longline method, steel pegs are anchored up to 2 m deep in the mud of the sea floor. Longlines with surface buoys are used to provide flotation. Vertical lines with panels containing pearl oysters are hung from the buoys and are maintained well off the bottom to avoid fouling. The lines are at least 100 m offshore and are 20-30 m apart to avoid entangling adjacent lines if one breaks. An average line is 100 m long with panels every meter for a total of 600 pearl oysters on the line. This gives a density of only 0.2-0.3 pearl oysters per square meter. A less common method, the bottom farm, is used in areas of harder bottom in more exposed areas such as Roebuck Bay (Scoones 1991). On these farms galvanized steel bars ("star pickets") are used to hold the panels. Surface floats are used only to mark the locations of the farm.

At the farm, the pearl oysters are removed from the water for several minutes only and mechanically cleaned every 4 to 5 weeks, and more frequently in the wet season when growth of fouling organisms is faster. Cleaning machines that use high-pressure water to remove as much growth as possible have been developed; calcareous encrustaceans may be mechanically scraped off; no chemicals are used in cleaning. Dead shells are removed during the cleaning operations.

Harvest of the Pearls

The temperature of the surrounding seawater has an important effect on the lustre and color of the pearl. These are best in winter, so the pearls are harvested during July and August (Scoones 1991). During harvest, suitable pearl oysters are reseeded with a new nucleus to begin the 2-year process of producing a new pearl.

ASSESSMENT OF ENVIRONMENTAL EFFECTS OF PEARLING

In total, 13 environmental and ecological issues were identified across the P. maxima fishery. No high risks were identified during the workshop; risks were ranked as either moderate (23%) or low (77%). Moderate risk rankings included: introduction of disease from seeding; attraction of other fauna and introduction of exotic organisms (Fig. 2). The low risks were: spread of disease; introduction of disease from hatchery; introduction of disease from translocation; impact to protected and endangered species resulting from entanglement; impact of habitat; impact to protected and endangered species attracted to farm lighting; nutrient impacts in sediment; perceived change in water quality; potential for litter (e.g., plastic zip tie tags, plastic bags, buoys) to enter water and reduction of primary productivity.

[FIGURE 2 OMITTED]

Introduction of disease from seeding was considered to be of moderate risk. Three related risks, introduction of disease from hatchery or from translocation and spread of disease, were considered to be low. The low ratings given to disease risks took into account current strict regulatory controls for minimizing disease risks. As discussed earlier, during the late 1970s and early 1980s serious losses occurred because of V. harveyi killing the oysters. The bacterium occurs naturally in the oysters, water and sediments. Crowded conditions and poor handling techniques used at the time placed the oysters under considerable stress, which allowed the bacteria to multiply and cause disease outbreaks. Once the causes were known, handling techniques were improved considerably and the pearl oysters were more widely spread in the growout areas. There is now emphasis in the industry on caring for the pearl oysters and the problem has not recurred. It should be noted that V. harveyi was not introduced by the pearling industry, rather the crowded conditions allowed it to spread. There are clear DFWA guidelines for procedures to minimize the possibility of introducing diseases through hatcheries. Also, equipment used in inserting the nucleus into the pearl oysters is sterilized before it is used in a different area.

Attraction of Other Fauna

Saltwater crocodiles might be attracted to the farms because of the lights and food wastes. However, these animals are dangerous, and activities that might attract them to the farms are minimized because of safety concerns. Small fish are attracted to the boats when pearl shells are being cleaned, and feed on portions of the material being removed from the shells. This is an intermittent activity, which occurs in a given spot only once every 3 to 5 wk, and then only in the daytime. The effect is transitory, and there is no longer-term buildup of fish populations.

Introduction of Exotic Organisms is a Major Concern in Australia

Once species become established in a new area they may be free of natural predators and other natural constraints on their populations. In these conditions a number of species have developed into plague proportions, which have caused severe environ mental problems. Once a species becomes established, it is virtually impossibly to be eradicated. The only reported successful eradication of a marine introduction worldwide occurred recently in Darwin Harbour. The mussel Mytilopsis sallei (Recluz 1849) was successfully removed from three small artificial boat marinas. The eradication was successful because the marinas use locks to allow vessels to enter and leave. They could be sealed off and chemicals introduced to kill the mussels (and virtually everything else) in the marinas (Willan et al. 2000). The issue of possible introduction of exotic organisms has two components, introductions by the pearling industry and introductions from other sources. The north coast of Western Australia is part of the tropical Indo-West Pacific biogeographical zone, which extends from the east coast of Africa across the tropical areas of the Indian and Pacific Oceans to Hawaii. Many species are widely distributed in the region, and some have ranges that extend over the full range. The north coast of Australia, including the full range of the P. maxima pearling industry, is part of the Indo-West Pacific (Wilson & Allen 1987). There are no major distributional barriers on the north coast of Western Australia; species tend to be distributed over the entire area if the proper habitat is available. Because the boats in the pearling industry operate within this zone, there is little likelihood of them introducing a species from overseas or eastern Australia.

The Remaining Potential Effects of Pearling Were all Considered to be Low Risk

Impact to protected and endangered species resulting from entanglement would arise if a protected or endangered species became trapped in one or more of the pearl lines. There are no known instances of this happening in the P. maxima industry, but there was a recent case in the black lip pearl (P. margaritifera) industry in the Houtman Abrolhos Islands on the west coast of Western Australia where a dead whale was washed ashore entangled in pearl lines. It could not be established whether the whale became entangled before or after death. Such occurrences do occasionally happen in the crayfish industry on the west coast, but there are tens of thousands of pot lines in the water during the 7.5 mo season. Entanglements in the pearl industry are at most very rare. Impact to protected and endangered species resulting from farm lighting is a related potential effect of the pearling industry. Oil rigs off the north coast of Western Australia are known to attract sea birds and turtles at night when their lights are on. However, the rigs have considerable lighting for safety and are worked 24 h a day. The small vessels and shore base farms of the pearling industry use only the lighting necessary for their activities, and are largely darkened for much of the night.

Impact of Habitat

Clearly establishing facilities for the pearling industry has some effect on the habitat. However the farms are small when compared with the vast distances on the north coast of Western Australia. They are also predominantly situated over mud bottom for maximum pearl growth. The major impact is the visual presence of the longlines, which are floating in the water, except for an anchor on each end, which is placed in the mud bottom

Nutrient impacts in sediment, perceived change in water quality and reduction of primary productivity are three interrelated possible effects of pearl oysters being maintained on the farms for 2 years. To some extent they are contradictory. Possibly nutrient impacts on sediment and perceived changes in water quality were considered to be a possible result of feces from the pearl oysters and residue from the cleaning process. Pearl oysters are sedentary animals with a low metabolic rate. At a density of 0.24).3 pearl oysters per square, there is unlikely to be much feces settling to the bottom. There is material cleaned off the shells every 3-5 wk. Again, the low stocking density of the pearl oysters suggests only a small amount of material is put into the system during cleaning. Portions are actively consumed by fish and the remainder is dispersed as it settles to the bottom. In any event, there is no net increase in nutrients, because the biological material was produced from nutrients already present in the water column. Reduction in primary productivity would occur because of the pearl oysters removing material from the water. Again, the effects would be negligible given the low stocking density of the pearl oysters and the dynamic environment of the north coast, where spring tidal ranges vary from 3-10 m, creating strong currents and considerable water flow.

Potential for Litter (e.g., Plastic Zip Tie Tags, Plastic Bags, Buoys) to Enter Water

The litter issue has 2 components: littering and loss of lines during storms. The industry has been very much aware of basic littering issues and has taken steps to minimize this through a code of practice. The northwestern coast of Australia is cyclone prone, with several storms occurring in an average year. If the storm passes near a pearl farm, lines and their attached buoys and panels are occasionally torn free. In such cases every possible effort is made to recover the panels because of their high value.

DISCUSSION

The studies of Enzer Marine Environmental Consulting (1998) and Jernakoff (2002) examined the potential environmental effects of the pearling (P. maxima) industry in Western Australia but used very different techniques. However, both came to the same conclusion, that the environmental impacts of the P. maxima industry in Western Australia are small. This is accentuated when one compares the industry to the other two major aquaculture industries in Australia, sea cage farming of Atlantic salmon in Tasmania and southern bluefin tuna ranching in South Australia. Both of these industries involve feeding considerable amounts of food to active fish, creating potential problems with uneaten food and fish feces falling through the nets to the bottom in low tidal areas, where it is broken down by physical and biological processes. These problems do not occur in the P. maxima industry, where the pearl oysters filter feed naturally and are stocked at much lower densities in high tidal areas where there is considerable natural water flushing.

The Australian Commonwealth government passed the Environmental Protection and Biodiversity Conservation Act in 1999; the act was gazetted in 2000. Under this act the Commonwealth Minister for the environment must certify that a fishery is operated in an environmentally sustainable manner if the fishery is to export its product from Australia. There was a 4-year period during which the initial applications could be submitted and assessed. DFWA (2002) submitted an application based on Enzer Marine Environmental Consulting (1998) and Jernakoff (2002). The Commonwealth Minister assessed the fishery as environmentally sustain able on November 5, 2003. Certification is for a 5-year period, after which a fishery must be assessed again.

In Japan, Yokoyama (2002) provided a clear demonstration of the differential effects of fish and pearl aquaculture. Monthly samples of macrobenthos were collected from a fish farm and a pearl farm in Gokasho Bay from June 1995 to July 1996. The results demonstrated that the community structure of the two sites showed distinct differences with seasonal fluctuations. At the fish farm, azoic conditions were found from July to November. After December, diversity increased markedly through successive recruitments of small-sized species such as the polychaetes Capitella sp. and Pseudopolydora paucibranchiata, and the amphipods Aoroides spp. Macrofaunal density, biomass and species richness peaked from March to April. In contrast, at the pearl farm site, a higher diversity, including larger-sized species, and no clear seasonal fluctuations in abundance were found, and community structure was similar to that at the control site. These results show that there was a large impact on the macrofauna at the fish farm, but little effect on the benthic fauna as a result of pearl farming. Yokoyama (2002) suggested that the difference in the level of organic input between the two sites results in the differences in the dissolved oxygen content of the bottom water, sulfide content of the sediments and, subsequently, the macrobenthic assemblages. It should be noted that environmental effects of fish farming depend on site and management. Felsing and Glencross (2004) showed that macrofauna minimized organic accumulation on the seabed at one site in Western Australia.

There have been few other assessments of the environmental impacts of pearl aquaculture, possibly because of the lack of perceived impacts. The studies that have been undertaken are in agreement with the results of the present evaluation of the environmental effects of pearling in Western Australia. Cheney et al. (1995) examined farming of the Black-lip pearl oyster (Pinctada margaritifera) in the Tongareva Lagoon, Cook Islands, where commercial farming began in mid 1993 but found little effect. Abo and Toda (2001) examined the relationship between stocking density of the Japanese pearl oyster, P. fucata martensii (Dunker, 1850), and planktonic food density measured as the chlorophyll a concentration at Gokasho Bay, central Japan. Food density (as chlorophyll a) is determined by the balance among the phytoplankton growth, filtration of pearl oysters and outflow by water exchange. A model was developed, which simulated food density and growth of pearl oysters associated with change in the farming density. The calculated food density and growth rate of pearl oyster were higher when the farming density was lower, whereas the food density and the growth rate were lower when the farming density was higher. During the summer peak of chlorophyll a, the concentration was about 7 [micro]g/L in areas of normal stocking density of pearl oysters, compared with about 8 [micro]g/L where the stocking density was reduced by half. Increasing the density of pearl oysters to 7 times the in situ farming density decreased the phytoplankton density by three-quarters to about 2 [micro]g/L. The authors concluded that filtration intensified by overcrowded pearl oysters decreases food availability, which then retards the growth rate of the pearl oysters. Their model also suggested that the present farming density of the pearl oysters is appropriate under the food condition of their habitat in Gokasho Bay.

Whereas there have been no reports of environmental damage caused by pearl farms, the opposite may be true: the presence of pearl farms may improve water quality. There have been a number of studies suggesting the use of edible oysters to remediate marine water conditions. For example, Jones (1999) found that the Australian oyster Saccostrea glomerata (Gould 1850) acted as a biological filter in reducing phytoplankton, bacteria, total nitrogen, total phosphorus and total suspended solids by amounts ranging from 5% to 67%. Oyster excretion increased concentrations of dissolved ammonium, nitrate/nitrite and phosphate. However, these concentrations were in turn reduced by absorption by the macroalga Gracilaria edulis. Whereas the same benefits could theoretically accrue from the use of pearl oysters, in practice stocking densities used in northwestern Australia would be too low to have much effect. Qian et al. (1996) demonstrated that the growth rates of both Pinctada martensi and the red alga Kappaphycus alvareji were higher in a coculture system than when the species were cultured independently. When temperatures were above 20[degrees]C the alga used nitrogenous wastes from the pearl oysters. Below that temperature algal growth was inhibited and there was no measurable effect. The authors speculated that the reason for improved growth rates of the pearl oysters was improved water quality.

Gifford et al. (2004) suggested that pearl farms could be used as biological filters in coastal areas with anthropogenic nutrient enrichment and pollution. Pearl oysters are capable of filtering water at rates of up to 25 1 [h.sup.-1] [g.sup.-1] of dry weight tissue. They extrapolated published information to suggest that a pearl farm of 100 tons of pearl oysters could remove 300 kg of heavy metals and 24 kg of organic contaminants through deposition into the pearl oyster tissue and shell, and that up to 19 kg of nitrogen would be removed per ton of pearl oyster harvested. There would also be substantial removal of bacteria. Gifford et al. (2004) suggested the concentration of heavy metals and other pollutants in the tissues and shells would not be a problem because the material would be disposed of at land sites and would not be used for human consumption. Gifford et al. (in press) tested this hypothesis at a small Pinctada imbricata farm in Port Stephens, New South Wales, which produced 9.8 tonnes.[yr.sup.-1]. The farm removed 703 g of metals, 7452 g nitrogen, and 545 g phosphorus. The authors concluded that if production was scaled up to 499 tonnes.[y.sup.-1], extraction of nitrogen would equal that being produced by a small sewage treatment plant. Changing the harvest dates of the pearls to coincide with the period of peak condition of oyster tissues would substantially increase material removed from the water column. The suggestion is that pearls produced could be sold to provide funding for the remedial activities and a profit. However, there is no information available on the quality of the pearls that would be produced. The P. maxima industry in Western Australia is based on producing high quality pearls in natural conditions. It is doubtful that the high quality could be maintained in polluted areas. Further, the north coast of Western Australia, where the industry is located, has few towns and sources of anthropogenic pollution, so there is no possibility of using pearl oysters for environmental remediation in this area.

As indicated earlier, the possible introduction of marine pest species into Australia was assessed as having a moderate risk. Reasons are provided earlier in the study as to why this risk is considered to be low as a result of pearling activities. On the other hand, species that have been introduced by vessels not associated with the pearl industry may potentially affect the industry, and such introductions could have significant impacts. Whereas not all of the ports on the north coast of Western Australia have been surveyed, there are known to be a number of species that have been introduced. NIMPIS (2005) lists 43 introduced or cryptogenic marine species in Western Australia. Seven of these species are on the north coast of the state, but the list is incomplete. For example, Jones (2004) records six barnacles as introduced to the Dampier Archipelago. Matsuyama (2003) presented an outstanding example damage, which can be caused by an introduced species. The dinoflagellate Heterocapsa circularisquama is a causative agent of red tide. It appeared in Japanese waters for the first time in 1988, then spread rapidly in the costal waters of western Japan. By 2000 there had been 43 red tides caused by H. circularisquama, including 18 that damaged fisheries, including the manila clam Ruditapes philippinarum (Adams & Reeve 1850) Pacific oyster Crassostrea gigas (Thunberg 1793), pearl oyster Pinctadafucata, and the blue mussel Mytilus galloprovincialis Lamarck, 1819. Economic losses in shellfish aquaculture by direct killing of marketable products were estimated to be at least 10 billion-yen in the last decade; at current exchange rates this is approximately one hundred million US dollars. Heterocapsa circularisquama red tides primarily affect bivalve aquaculture. No harmful effects on wild or cultured fish, other marine vertebrates or any public health hazard have been recorded. This is a tropical species, which could potentially cause substantial effects to the pearl industry if introduced into Western Australia.

ACKNOWLEDGMENTS

The authors thank the following people and organizations that have generously provided time and information during the two studies: Mark Alexander, skipper, and crew of the Paspaley Pearls vessel Clare; Dr Dave Mills, Paspaley Pearls; Peter Bergsma and Serena Sanders, Arrow Pearls Pty Ltd; Mick Buckley, John Kelly and Brett McCallum, Pearl Producers Association; Mel Carrington, Shina Gugeri, and Neil Marston Maxima Pearls; John Carroll, Fremantle Paint Suppliers; Nick Duyst, Broome Pearl Hatchery; Jennie Carey and Dr Chris Simpson, WA Department of Conservation and Land Management; Dr Jim Penn, Andrew Bartleet, Heather Brayford Robin Clarke, Colin Chalmers, Dr Rick Fletcher, Ross Gould, Vicki Gouteff, Jo Bunting, Dr Kim Freidman, Greg Finlay. and WA Department of Fisheries; Ben Hollyock and Craig Manning, WA Department of Environmental Protection; Brian Martin, Harbour master, Broome; Rick Scoones, Rick Scoones & Associates; Astrida Mednis, Environment Australia; Harriet Paterson, Sustainable Fisheries Office, Conservation Council and Owen Bunter, MG Kailis. The following PPA member companies responded to the EMS gap analysis questionnaire: Australian Sea Pearls Pry. Ltd; Broome Pearls Pry. Ltd; Cygnet Bay Pearls; Exmouth Pearls; Hamaguchi Pearls; Paspaley Pearling Co; Pearls Pty Ltd; Morgan & Co; and Roebuck Pearl Producers. This project work was funded in part by financial or support-in-kind contributions from the following bodies: Fisheries Research and Development Corporation; WA Industry Development Unit; Pearl Producers Association and International Risk Consultants.

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FRED E. WELLS (1,2) * AND PETER JERNAKOFF (3)

(1) Enzer Marine Environmental Consulting, PO Box 4176, Wembley, Western Australia 6014; (2) Western Australian Department of Fisheries, Locked Bag 39, Cloisters Square, Western Australia 6850 (Present address)," (3) IRC Environment, 26 Colin Street West Perth, Western Australia 6005

* Corresponding author. E-mail: [e-mail]