Diseases of pearl oysters and other molluscs: a Western Australian perspective.

ABSTRACT Mollusc culture, particularly the cultivation of pearl oysters, is an important component of the aquaculture industry in Western Australia. As a result, there has been a long-term investment in surveys of commercial mollusc species for potential diseases of concern. A number of pathogens, particularly haplosporidans, identified within wild-stock shellfish have the potential to adversely affect mollusc populations. Others pose risks for translocations associated with aquaculture. The microsporidan Steinhausia mytilovum (Field), found in ova of the blue mussel Mytilus galloprovincialis (Lamarck), poses intriguing questions about the origin and dispersal of its host.

KEY WORDS: abalone, ciliates, parasites, Perkinsus, Thraustochytridea, scallops

INTRODUCTION

The most valuable of the marine mollusc culture industries in Western Australia is pearling. The main species cultured is the golden-lipped pearl oyster Pinctada maxima (Jameson), but other pearl shells grown commercially include P. margaratifera (L), P. albina (Lamarck) and Pteria penguin (Roding). The pearling industry is supported by four operational hatcheries capable of supplying all of the spat requirements of industry. Western Australia also has a small mussel industry based on culture of Mytilus galloprovincialis; an abalone culture industry based on hatchery produced Haliotis spp. (greenlip abalone, H. laevigata (Donovan), brownlip abalone, H. conicopora Peron and Roe's abalone, 14. roei Gray); a rock oyster farm hatching and growing Saccostrea sp.; a hatchery producing scallops (Amusium balloti Bernardi) for reseeding and there is also some experimental reseeding of tropical reefs with hatchery produced trochus (Tectus niloticus [L]).

Because of this aquaculture activity, the disease status of these Western Australian molluscs is relatively well known. To date there have been few diseases of concern. The health status of the aquaculture industry in a State such as Western Australia is based on two factors. The first is the presence of a disease reporting procedure and a diagnostic capacity to identify causative agents. The second is the existence of passive and targeted surveillance programs aiming to identify endemic diseases not associated with morbidity or mortality. In Western Australia a dedicated fish disease diagnostic unit of the Department of Fisheries has worked with industry since 1988 to identify and solve disease problems. There have also been 3 major mollusc disease surveys in the State; one involved a wide range of molluscs around the coast (Hine & Thorne 2000), one on P. maxima (Humphrey et al. 1998) and an ongoing national survey of abalone diseases. Some additional information is available in isolated publications on individual parasites and further unpublished information is available from laboratory records. Parasites that are known from shellfish in Western Australia are listed in Table 1.

Pearl Oysters

The disease that has caused most economic loss to the P. maxima industry is vibriosis (Pass et al. 1987). In the 1980s Vibrio spp. bacteria caused significant losses to the pearling industry that have now been overcome by improved management practices. The presence of a very rare haplosporidan in the digestive tubules is cause for concern (Hine & Thorne 1998) because very little is known about the biology of this parasite. The haplosporidan has been identified only three times and each time the oysters on the infected farm site have been destroyed. During the second occurrence, in late December 1995, 4.6% of a sample of 150 farmed juvenile pearl oysters was found infected within 6 weeks of being set at a remote site in Western Australia. By the time the oysters were destroyed 15 days later the infection prevalence had increased to 10% (n = 238). The notifiable disease Perkinsus olseni/ atlanticus has been reported from P. maxima in the Torres Strait (Norton et al. 1993a) but not from Western Australia, though the disease agent does occur here in bivalve molluscs other than P. maxima (Table 1).

Another parasite of concern in pearl oysters has only been detected in spat from the Exmouth Gulf and outlying islands since 2001, despite comprehensive monitoring of oysters in the State and the industry practice of harvesting and translocating shell to all other oyster growing areas for over 50 y. It is an intracellular ciliate similar in appearance to ciliates reported as nonpathogenic commensals in Spanish Mytilus galloprovincialis (Villalba et al. 1997) and in Mytilus edulis (L) on the east and west coasts of North America (Figueras et al. 1991a). The teardrop shaped basophilic ciliate (10.15 [micro]m x 5 [micro]m) has a dense polymorphic macronucleus and normally occupies an intraluminal or intraepithelial location within the digestive gland in P. maxima spat (Fig. 1). The ciliate is often associated with an inflammatory response in oysters smaller than 70 mm with 20-50 mm shell being most affected. A feature in smaller (20-40 mm) spat is the ciliate's capacity to penetrate the mucosal basal lamina and reside within hemolymph spaces or free within interstitial connective tissue. Translocation of infected pearl oysters beyond the Exmouth zone is not permitted.

[FIGURE 1 OMITTED]

The origin of the ciliate is unknown, and its relationship to similar organisms seen in northern hemisphere mussels is unknown. Either the ciliate has become much more prevalent in recent years or it has been introduced into the region. Its infectivity to other bivalves is also unknown.

During surveys to determine the distribution of the ciliate, a single infected oyster was found with an enigmatic unidentified proctistan parasite (Fig. 2). The putative sporoblasts develop within the epithelial cells of the digestive tubules and fill the lumen of the tubules, with an associated basophilic hemocyte inflamma inflammatory response. With a prevalence of less than 0.005% it is not feasible to attempt follow-up sampling, but it does indicate that parasitic organisms can be present at extremely low prevalence in a population.

[FIGURE 2 OMITTED]

Another proctistan was detected at a low prevalence in P. maxima from the Exmouth Gulf during investigations into the ciliate parasite. The parasite was elongated (30 [micro]m x 20 [micro]m) and intimately associated with the digestive gland epithelial cells to which it appeared to have a sessile attachment (Fig. 3). The tubule epithelial cells beneath the site of attachment were multinucleated and ultrastructural examination indicated the multiple nuclei were of molluscan origin, suggesting the proctistan had induced this change within the host.

[FIGURE 3 OMITTED]

A proctistan tentatively attributed to the Thraustochytridea was identified in moribund, gaping P. maxima from a farm that had experienced losses after a cyanobacterial (Trichodesmium sp.) bloom. The affected oysters showed extensive necrosis of external epithelial surfaces of the palps and mantle with invasion of the underlying leydig tissues by brown pigmented and eosinophilic, segmented unicellular organisms 10-15 [micro]m in diameter, and smaller dense basophilic 5-[micro]m diameter cells that appeared to be embedded in a mucinous matrix (Fig. 4).

[FIGURE 4 OMITTED]

Rock Oysters

One of 411 Saccostrea glomerata (Gould) collected between Carnarvon to the Dampier Archipelago during 1995 was infected with a parasite histologically identical to Marteilia sydneyi Perkins and Wolf, the cause of QX disease in Saccastera commercialis (Iredale and Roughley) in Queensland and New South Wales. The same pathogen was also found in S. glomerata by Hine and Thorne (2000). On the eastern seaboard where QX occurs, it has caused losses of over 90% (Witney et al. 1988) and has resulted in a decline in New South Wales rock oyster production since the 1970s.

S. cucullata (Born) from Airlie Island, Rosily Island, Varanus Island, Hermite Island, King Bay and East Lewis Island in the north of Western Australia are infected by a second species of pathogenic haplosporidan protozoan, Haplosporidium sp. The parasite was identified as the cause of a significant mortality (up to 80%) of rock oysters at Airlie Island (Hine & Thorne 2000). The presence of this haplosporidan will threaten the viability of any rock oyster farm sited north of Exmouth.

Mussels

The ova of mussels in Cockburn Sound, Western Australia are infected with the microsporidan Steinhausia mytilovum but the parasite has not been found in mussels from other growing areas. Heavily infected mussels are readily identified by the gross appearance of the mantle of cooked females. Infected mantle tissue has an uneven surface with depressed cream white patches and swollen tubercles forming spots against the orange-pink background color of healthy female gonad. Mussel samples in August and October 1995 from sites around the Sound showed a prevalence of Steinhausia sp. ranging from 22% to 57%, or 44.4% overall. Histology revealed that the patches and tubercles were associated with a marked infiltration of circulating granulocytes and large basophilic hemocytes into affected follicles with resorption of the germinal epithelium and ova (Fig. 5). Small basophilic hemocytes were not prominent in the response. Also present in 2% to 4% of the ova were parasitophorous vacuoles closely associated with the nucleus. These vacuoles measured 13.27 [+ or -] 2.37 [micro]m (n = 20) and contained over 30 small spores 2.5-[micro]m diameter. There was usually only one vacuole in an ovum, but occasionally up to three parasitophorous vacuoles could be seen. In histological sections the presence of resorbing follicles and focal accumulation of granulocytes among the developed ova was evidence of infection, but infected oocytes were also observed in apparently healthy follicles. Ova (normal, infected and degenerating), granulocytes, large basophilic granular hemocytes and cell debris occurred in the ciliated gonad ducts. Parasitophorous cysts containing spores also occurred free in the lumen of the ducts. The spore walls and contents stained negative to Feulgen, Ziehl-Neelsen and Grocotts, were Gram positive and Periodic-Acid-Schiffs negative.

[FIGURE 5 OMITTED]

The relationship between this Steinhausia sp. and the one previously described by Anderson et al. (1995) from cysts within ova of the rock oyster S. commercialis in Queensland, Australia is unknown. The biology of Steinhausia sp. is not well understood. Field (1923) reported that infected eggs were shed along with normal eggs. Sparks (1985) suggested that infected eggs do not seem to become necrotic or degenerate though Rybakov and Kholodkovskaya (1987) noted that Steinhausia sp. clearly distorts the nucleus of the ovum and can also cause the destruction of the egg, as has been seen in Western Australian mussels. It is likely that the loose spores are released along with intact eggs or through phagocytosis and subsequent diapediasis. Figueras (1991) reported that the presence of the parasite is always accompanied by a strong hemocyte response and the impact on the host has been described as severe (Rybakov & Kholodkovskaya 1987) to negligible (Maurand & Loubbs 1979). In the case of the S. mytilovum infection seen here, there is an absence of the typical bivalve inflammatory response, which involves invasion of the site of trauma primarily by small agranular hyalinocytes (90%), granular basophils (8%) and granular acidophils (2%) (Bayne et al. 1979, Brereton & Alderman 1979). Instead the major components are the phagocytic hemocyte and the granular acidophil and the process closely resembles gonad resorption. Prevalence of Steinhausia mytilovum does not increase with the size of the mussel, suggesting that infection is annual (Table 2).

The proctistan observed in the ova of Western Australian blue mussel has the same measurements and appearance under the light microscope as S. mytilovum from both European and American M. galloprovincialis. The taxonomy of the blue mussel in Western Australia is disputed. Still referred to as M. edulis planulatus (L), electrophoretic studies have shown that the species is M. galloprovincialis and that M. galloprovincialis from Australasia, eastern Asia, Western Europe, the Mediterranean and California, and M. edulis from eastern North America and Western Europe are electrophoretically distinct species with an overlapping distribution (Koehn 1991, McDonald et al. 1991, Geller et al. 1993). There is a fossil record of mussels in Australian waters and Koehn (1991) hypothesized that M. galloprovincialis may have been an early introduction into the Northern Hemisphere as a hull-fouling organism. Distribution of parasites often reflects the distribution of their primary hosts so S. mytilovum may also be an introduction from the Southern Hemisphere. Steinhausia mytilovum is reported to infect the ova of M. edulis along the Atlantic coast of the USA (Field 1923, Figueras et al. 1991a). Sparks (1985) reported that, based on examination of thousands of mussels, the parasite was absent from California, Oregon and Washington and it was unreported from Europe. It now occurs in M. galloprovincialis from Spain (Figueras et al. 1991b), Italy (De Vincentiis & Renzoni 1963), Greece (Rayyan et al. 2004), the Black Sea (Rybakov & Kholodkovskaya 1987, Gayevskaya & Machkevskiy 1991), northern France (Comtet et al. 2004) and the west coast of the USA (Hillman 1990, 1991). Hillman (1990) noted that M. galloprovincialis had been accidentally introduced into southern California and suggested that S. mytilovum had been introduced with the mussels.

Scallops

There are two nematode larvae found in scallops (Amusium balloti) in the Shark Bay area of Western Australia. The "common" nematode in scallops is Sulcascaris sulcata. This was reported by Lester et al. (1980) to infect up to 64% of the landed catch in Shark Bay and occurs in a brownish capsule 3-7 mm dia. The adult nematodes of S. sulcata live in the loggerhead turtle Caretta caretta (L) and have a wide geographic distribution and range of molluscan hosts. The second species, Echinocephalus sp., forms small yellow-brown cysts 2-3 mm dia. Lester et al. (1980) reported that only 2 of 10 scallops he examined were infected, but in recent years the nematode has been much more common and in 2001 was the dominant nematode in A. balloti. The genus Echinocephalus occurs widely in molluscs in warm waters, and probably matures in marine skates or rays.

Abalone

The Western Australian component of a national health survey of abalone has recently been completed. In this survey, up to 25% of wild-caught green-lipped abalone (Haliotis laevigata) were infected with trematode metacercariae. Low prevalences of proctistans in the lumen of the stomach and digestive gland, apicomplexans and putative viral inclusions in the intestinal tract were observed. Abalone in Western Australia are free of the disease perkinsosis, found in South Australia and New South Wales, but the organism does exist on the south coast of Western Australia. Perkinsus is a primitive fungus-like organism of uncertain taxonomic status, probably in the phylum Labrinthulomycota. A worldwide effort to understand the taxonomy of this organism (or group of organisms) is underway. In South Australia and New South Wales Perkinsus olseni/atlanticus affects abalone with yellow-green pus filled blisters (0.5-8 mm dia.) containing a creamy brown deposit. Once processed the lesions appear as pale brown circles. Perkinsosis occurs in a variety of shellfish in the north of the State (Hine & Thorne 2000), however, a survey of 300 abalone from six sites along the south and west coasts of Western Australia in 1995 were negative for Perkinsus sp. by the thioglycolate media method. Subsequently, in 2003 Perkinsus sp. was cultured from the gill tissue of one clinically normal abalone (14. laevigata) from the south coast.

FUTURE TRENDS

Whereas, overall, disease has not been a problem for the molluscs industry in Western Australia, it is certain that many more pathogenic organisms remain to be discovered, particularly as molluscs become subject to aquaculture or are subject to environmental stresses associated with economic activity. Because of the age of the Australian continent and the relative isolation of the coastal fauna it is likely that many of these will prove to be unique to Western Australia. Strict controls are therefore imposed to limit translocation of parasites by aquaculture. Whereas these pathogens may represent an economic threat, it is probable that they will also provide new insights on the zoogeography and derivation of the Western Australian mollusc fauna.

ACKNOWLEDGMENTS

The authors thank the shellfish industries in Western Australia for their assistance in providing specimens and Paul Hillier and Tina Thorne for help in collecting mussels. Melanie Crockford, Greg Maguire and Fran Stephens provided editorial comment.

LITERATURE CITED

Anderson, T. J., P. M. Hine & R. J. G. Lester. 1995. A Steinhausia-like infection in the ovocytes of Sydney rock oysters Saccostrea commercialis. Dis. Aquat. Org. 22:143-146.

Bayne, C. J., M. N. Moore, T. H. Carefoot & R. J. Thompson. 1979. Hemolymph functions in Mytilus californianus: the cytochemistry of hemocytes and their responses to foreign implants and hemolymph factors in phagocytosis. J. Invert. Pathol. 34:1-20.

Brereton, J. D. & D. J. Alderman. 1979. Wound healing in the European oyster, Ostrea edulis L. Aquaculture 16:147-151.

Comtet, T., C. Garcia, Y. Le Coguic & J.-P. Joly. 2004. First record of the microsporidian parasite Steinhausia mytilovum in Mytilus sp. (Bivalvia: Mytilidae) from France. Dis. Aquat. Org. 58:261-264.

De Vincentiis, M. & A. Renzoni. 1963. Sulla presenza di uno sporozoo in ovociti di Mytilus galloprovincialis Lam. Archo. Zool. Ital. 47:21-26.

Field, I. A. 1923. Biology and economic value of the sea mussel Mytilus edulis. Bull. U.S. Bur. Fish. Wash. 38:127-259.

Figueras, A. J. 1991. Mortalities, parasites and diseases of mussels (Mytlus edulis and Mytilus galloprovincialis) from natural and cultured populations. Bull. Aquacult. Assn. Can. 91-2:54-62.

Figueras, A. J., C. F. Jardon & J. R. Caldas. 1991a. Diseases and parasites of mussels (Mytilus edulis Linnaeus, 1758) from two sites on the east coast of the United States. J. Shellfish Res. 10:89-94.

Figueras, A. J., C. F. Jardon & J. R. Caldas. 1991b. Diseases and parasites of rafted mussel (Mytilus galloprovincialis Lmk.): preliminary results. Aquaculture 99:17-33.

Gayevskaya, A. V. & V. M. Machkevskiy. 1991. Parasitologic aspects of mariculture in the Black Sea. Gidrobiologicheskiy Zhurnal 27(2):76-79.

Geller, J. B., J. T. Carlton & D. A. Powers. 1993. Interspecific and interpopulation variation in mitochondrial ribosomal DNA sequences of Mytilus spp. (Bivalvia: Mollusca). Mol. Mar. Biol. Biotechnol. 2:44-50.

Hillman, R. E. 1990. The implications to the taxonomy of Mytilus of histopathological observations of Mytilus edulis collected for the mussel watch program. National Shellfish Program Abstracts. J. Shellfish Res. 8:452.

Hillman, R. E. 1991. Steinhausia mytilovum (Minisporida: Chitridiopsidae) in Mytilus sp. in California: a new geographic record. J. Invert. Pathol. 57:144-145.

Hine, P. M. & T. Thorne. 1998. Haplosporidium sp. (Haplosporidia) in hatchery reared pearl oysters Pinctada maxima (Jameson, 1901) in Western Australia. J. Invert. Pathol. 71:48-52.

Hine, P. M. & T. Thorne. 2000. A survey of some parasites and diseases of several species of bivalve mollusc in northern Western Australia. Dis. Aquat. Org. 40:67-78.

Humphrey, J. D., J. H. Norton, J. B. Jones, M. A. Barton, M. T. Connell, C. C. Shelley & J. H. Creeper. 1998. Pearl oyster (Pinctada maxima) aquaculture: health survey of Northern Territory, Western Australia and Queensland pearl oyster beds and farms. FRDC project number 94/079 final report. 108 pp.

Koehn, R. K. 1991. The genetics and taxonomy of species in the genus Mytilus. Aquaculture 94:125-145.

Lester, R. J. G., D. Blair & D. Heald. 1980. Nematodes from scallops and turtles from Shark Bay, Western Australia. Aust. Z Mar. Freshwater Res. 31:713-717.

Maurand, J. & C. Loubes. 1979. Les microsporides parasites de mollusques. Haliotis 8:39-48.

McDonald, J. H., R. Seed & R. K. Koehn. 1991. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar. Biol. 111:323-333.

Norton, J. H., M. A. Shepherd, F. P. Perkins & H. C. Prior. 1993a. Perkinsus-like infection in farmed golden-lipped Pearl oyster, Pinctada maxima, from the Torres Strait, Australia. J. Invert. Pathol. 62:105-106.

Norton, J. H., M. A. Shepherd & H. C. Prior. 1993b. Papovavirus-like infection of the golden-lipped Pearl oyster, Pinctada maxima, from the Torres Strait, Australia. J. Invert. Pathol. 62:198-200.

Pass, D. A., R. Dybdahl & M. M. Mannion. 1987. Investigations into the causes of mortality of the pearl oyster, Pinctada maxima (Jameson) in Western Australia. Aquaculture 65:149-169.

Pass, D. A., F. P. Perkins & R. Dybdahl. 1988. Virus-like particles in the digestive gland of the pearl oyster (Pinctada maxima). Z Invert. Pathol. 51:166-167.

Rayyan, A., G. Phots & C. C. Chintiroglou. 2004. Metazoan parasite species in cultured mussel Mytilus galloprovincialis in the Thermaikos Gulf (north Aegean Sea, Greece). Dis. Aquat. Org. 58:55-62.

Rybakov, A. V. & E. V. Kholodkovskaya. 1987. Parasites and commensals of the mussel Mytilus galloprovincialis in the Northwest Black Sea. Biol. Mor. 2:22-29.

Sparks, A. K. 1985. Synopsis of invertebrate pathology exclusive of insects. Netherlands: Elsevier. 423 pp.

Villalba, A., S. Mourelle, M. J. Carballal & C. Lopez. 1997. Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rias of Galicia (NW Spain). Dis. Aquat. Org. 31:127-139.

Witney, E., J. Beumer & G. Smith. 1988. Oyster culture in Queensland. Department of Primary Industries, Queensland Government. 27 pp.

J. B. JONES * AND J. CREEPER

Department of Fisheries, Government of Western Australia, P.O. Box 20, North Beach, WA 6920, Australia

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

TABLE 1. Molluscan disease-causing agents (other than bacteria)
reported from Western Australia.

                                                      Associated
       Agent                   Host                with Epizootic?

Virus
  Virus-like
    inclusions         Pinctada maxima                    No
                       Haliotis laevigata                 No
                       Isognomon isognomum                No
                       Pinna bicolor                      No
                       Saccostrea cucullata               No
                       Haliotis laevigata                 No
  Papova-like virus    Pinctada maxima                    No
Rickettsia-like
  organisms            Barbatia helblingii                No
                       Haliotis laevigata                 No
                       Isognomon isognomum                No
                       Pinctada maxima                    No
                       Pinna bicolor                      No
                       Pinna deltoides                    No
                       Pteria penguin                     No
                       Saccostrea glomerata               No
                       Saccostrea cucullata               No
                       Stavilia horrida                   No
Haplosporidia
  Bonamia sp.          Ostrea sp.                         Yes
  Haplosporidium sp.   Saccostrea cucullata               Yes
  Haplosporidium sp.   Pinctada maxima                    No
  Marteilia sydneyi    Saccostrea cucullata               No
                       Saccostrea glomerata               No
  Mikvocytos
    roughleyi          Saccostrea sp.                     No
Microspora
  Steinhausia
    mytilovum          Mytilus galloprovin-               No
                         cialis
  Marteilioides sp.    Saccostrea echinata                No
Apicomplexa
  Heart apicomplexan   Pinctada maxima                    No
  Perkinsus olseni     Barbatia helblingii                No
                       Isognomon isognomum                No
                       Malleus meridianus                 No
                       Pinctada albina                    No
                       Pinna deltoides                    No
                       Saccostrea cucullata               No
                       Saccostrea glomerata               No
                       Septifer bilocularis               No
                       Spondylus sp.                      No
                       Haliotis laevigata                 No
Ciliates
  Ciliates on gills    Pinctada spp.                      No
                       Saccostrea sp.                     No
  Ciliates in gut      Pinctada maxima                    No
                       Haliotis laevigata                 No
  Ancistrocomids       Pinctada albino                    No
                       Pinna bicolor                      No
                       Saccostrea cucullata               No
                       Saccostrea echinata                No
                       Saccostrea glomerata               No
                       Haliotis laevigata                 No
  Sphenophyra-like
    ciliates           Saccostrea glomerata               No
Trematoda
  Proctoeces sp.       Malleus meridianus                 No
  Sporocysts           Haliotis laevigata                 No
                       Isognomon isognomum                No
                       Pinctada albina                    No
                       Pinctada maxima                    No
                       Malleus malleus                    No
                       Saccostrea echinata                No
                       Saccostrea glomerata               No
Cestoda
  Tylocephalum sp.     Dendostrea folium                  No
                       Isognomon isognomum                No
                       Malleus malleus                    No
                       Malleus meridianus                 No
                       Pinctada spp.                      No
                       Pinna bicolor                      No
                       Pinna deltoides                    No
                       Pteria penguin                     No
                       Saccostrea cucullata               No
                       Saccostrea glomerata               No
                       Saccostrea echinata                No
                       Stavilia horrida                   No
  Tetrabothriate
    cestodes           Pteria penguin                     No
Nematoda
  Nematode larvae      Saccostrea cucullata               No
  Sulcascaris
    sulcata            Amusium balloti                    No
  Echinocephalus sp.   Amusium balloti                    No
Gregarines
  Nematopsis sp.       Saccostrea cucullata               No
  Unidentified
    gregarine          Pinctada maxima                    No
Copepoda
  Anthessius
    pinctadae          Pinctada maxima                    No

       Agent                   Host                   Reference

Virus
  Virus-like
    inclusions         Pinctada maxima         Pass et al. (1988);
                                                 Humphrey et al. (1998)
                       Haliotis laevigata      Laboratory records
                       Isognomon isognomum     Hine & Thorne (2000)
                       Pinna bicolor           Hine & Thorne (2000)
                       Saccostrea cucullata    Hine & Thorne (2000)
                       Haliotis laevigata      Laboratory records
  Papova-like virus    Pinctada maxima         Norton et al. (1993b);
                                                 Humphrey et al. (1998)
Rickettsia-like
  organisms            Barbatia helblingii     Hine & Thorne (2000)
                       Haliotis laevigata      Laboratory records
                       Isognomon isognomum     Hine & Thorne (2000)
                       Pinctada maxima         Humphrey et al. (1998)
                       Pinna bicolor           Hine & Thorne (2000)
                       Pinna deltoides         Hine & Thorne (2000)
                       Pteria penguin          Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
                       Saccostrea cucullata    Hine & Thorne (2000)
                       Stavilia horrida        Hine & Thorne (2000)
Haplosporidia
  Bonamia sp.          Ostrea sp.              Laboratory records
  Haplosporidium sp.   Saccostrea cucullata    Hine & Thorne (2000)
  Haplosporidium sp.   Pinctada maxima         Hine & Thorne (1998)
  Marteilia sydneyi    Saccostrea cucullata    Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
  Mikvocytos
    roughleyi          Saccostrea sp.          Laboratory records
Microspora
  Steinhausia
    mytilovum          Mytilus galloprovin-    Laboratory records
                         cialis
  Marteilioides sp.    Saccostrea echinata     Hine & Thorne (2000)
Apicomplexa
  Heart apicomplexan   Pinctada maxima         Humphrey et al. (1998)
  Perkinsus olseni     Barbatia helblingii     Hine & Thorne (2000)
                       Isognomon isognomum     Hine & Thorne (2000)
                       Malleus meridianus      Hine & Thorne (2000)
                       Pinctada albina         Hine & Thorne (2000)
                       Pinna deltoides         Hine & Thorne (2000)
                       Saccostrea cucullata    Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
                       Septifer bilocularis    Hine & Thorne (2000)
                       Spondylus sp.           Hine & Thorne (2000)
                       Haliotis laevigata      Laboratory records
Ciliates
  Ciliates on gills    Pinctada spp.           Humphrey et al. (1998)
                       Saccostrea sp.          Laboratory records
  Ciliates in gut      Pinctada maxima         Laboratory records
                       Haliotis laevigata      Laboratory records
  Ancistrocomids       Pinctada albino         Hine & Thorne (2000)
                       Pinna bicolor           Hine & Thorne (2000)
                       Saccostrea cucullata    Hine & Thorne (2000)
                       Saccostrea echinata     Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
                       Haliotis laevigata      Laboratory records
  Sphenophyra-like
    ciliates           Saccostrea glomerata    Hine & Thorne (2000)
Trematoda
  Proctoeces sp.       Malleus meridianus      Hine & Thorne (2000)
  Sporocysts           Haliotis laevigata      Laboratory records
                       Isognomon isognomum     Hine & Thorne (2000)
                       Pinctada albina         Hine & Thorne (2000)
                       Pinctada maxima         Humphrey et al. (1998);
                                                 Pass (1987); Hine &
                                                 Thorne (2000)
                       Malleus malleus         Hine & Thorne (2000)
                       Saccostrea echinata     Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
Cestoda
  Tylocephalum sp.     Dendostrea folium       Hine & Thorne (2000)
                       Isognomon isognomum     Hine & Thorne (2000)
                       Malleus malleus         Hine & Thorne (2000)
                       Malleus meridianus      Hine & Thorne (2000)
                       Pinctada spp.           Hine & Thorne (2000);
                                                 Humphrey et al. (1998)
                       Pinna bicolor           Hine & Thorne (2000)
                       Pinna deltoides         Hine & Thorne (2000)
                       Pteria penguin          Hine & Thorne (2000)
                       Saccostrea cucullata    Hine & Thorne (2000)
                       Saccostrea glomerata    Hine & Thorne (2000)
                       Saccostrea echinata     Hine & Thorne (2000)
                       Stavilia horrida        Hine & Thorne (2000)
  Tetrabothriate
    cestodes           Pteria penguin          Hine & Thorne (2000)
Nematoda
  Nematode larvae      Saccostrea cucullata    Hine & Thorne (2000)
  Sulcascaris
    sulcata            Amusium balloti         Lester et al. (1980)
  Echinocephalus sp.   Amusium balloti         Lester et al. (1980)
Gregarines
  Nematopsis sp.       Saccostrea cucullata    Hine & Thorne (2000)
  Unidentified
    gregarine          Pinctada maxima         Humphrey et al. (1998)
Copepoda
  Anthessius
    pinctadae          Pinctada maxima         Humphrey et al. (1998)

TABLE 2.

Prevalence of Steinhausia sp. in female Mytilus galloprovincialis
from Cockburn Sound, Western Australia.

                     Number     Total number
Size of host (mm)   infected      examined     % infected

 <50                   16            34           47.0
50-59                  33            65           50.7
60-69                  23            80           28.7
70-79                  93           189           49.2
80-89                  51           114           44.7
 >90                    7            10           70.0
Overall               223           492           45.3

There is no increase in prevalence of infection with mussel size.