Parasites of blood cockle (Anadara granosa Linnaeus, 1758) from the Straits of Malacca.
Article Type: Report
Subject: Parasitic diseases (Distribution)
Shellfish (Diseases)
Shellfish (Growth)
Aquaculture industry (Forecasts and trends)
Authors: Uddin, M. Jasim
Yasin, Zulfigar
Khalil, Munawar
Shau-Hwai, Aileen Tan
Pub Date: 12/01/2011
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2011 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: Dec, 2011 Source Volume: 30 Source Issue: 3
Topic: Event Code: 690 Goods & services distribution; 010 Forecasts, trends, outlooks Advertising Code: 59 Channels of Distribution Computer Subject: Company distribution practices; Company growth; Market trend/market analysis
Product: Product Code: 0913000 Shellfish NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish; 0273 Animal aquaculture
Geographic: Geographic Scope: Malaysia Geographic Code: 9MALA Malaysia
Accession Number: 278595630
Full Text: ABSTRACT This is the first report on the parasites of blood cockle Anadara granosa from the Straits of Malacca. For a histopathological survey, samples were collected for 13 mo from 3 natural habitats: the west coast of Pulau Aman, Malaysia; the east coast of Banda Acheh: and the east coast of Lhokseumawe, Indonesia. After reviewing histological preparations, Nematopsis sp. was found in the connective tissue, gills, gonad, mantle, digestive glands, and foot: trematode sporocysts were identified in the gonads, stomach epithelium, mantle, digestive glands, and foot: and a turbellarian was observed in the stomach epithelium, gonads, digestive glands, mantle, and gills. Remarkable spatial differences were found in the parasitic communities of A. granosa of the Straits of Malacca; however, no apparent temporal variation in the prevalence of any parasite was evident. Nematopsis sp. infection was very common in A. granosa collected from Pulau Aman, with no clear host tissue damage. Trematode sporocysts were observed at all sites, and the gonads were completely lacking in some individuals as a result of infection. A turbellarian was detected without any evidence of pathological damage to the host. From the survey, only a trematode was detected as a potential threat to the natural stocks of A. granosa along the coasts of the Straits of Malacca. Further study should be carried out to identify the specific taxonomic affiliation of the parasites.

KEY WORDS: blood cockle, Anadara granosa, parasites, pathology, Straits of Malacca, spatial variation, temporal variation

INTRODUCTION

Shellfish aquaculture is one of the most rapidly expanding food production sectors in the world and it contributes a quarter of the global aquaculture production by volume. Most important, more than 80% of the world shellfish production in 2007 originated from Asia and bivalves--including oysters, clams, cockles, scallops, and mussels--covered more than 90% of the world shellfish aquaculture production (FAO 2009). Although Asia is the main contributor to mollusc aquaculture production in the world, the study of mollusc diseases at the farm level and in natural habitats remained a neglected field in most parts of Asia. There are many examples of the severe impact of disease outbreaks and mass mortality that are increasingly recognized as a significant constraint to aquaculture production and trade. Therefore, it is time to focus on this field for the protection of the increasingly active mollusc aquaculture sector in this region.

Mollusc aquaculture and exploitation from natural stocks have long been practiced along the coasts of the Straits of Malacca. The blood cockle, Anadara granosa, is the most important commercial species in this region, and is extensively harvested from the natural habitats in Malaysian and Indonesian waters. In addition to natural harvest, A. granosa is commercially cultivated in the tidal mudflats along the western coast of Peninsular Malaysia. A. granosa is the key contributor in the brackish water aquaculture sector in this country, accounting for 20.3% (64,938 MT) by volume in 2009 (Department of Fisheries, Malaysia 2011). Diseases and parasites affecting bivalves in Malaysian and Indonesian waters have not been systematically investigated. However, a number of parasites have been reported to cause diseases in farmed and natural bivalve stocks from neighboring countries. In Thailand, sporozoites of Nematopsis spp. were found in the cultivated and locally harvested bivalves (Tuntiwaranuruk et al. 2004). Marteilia sp., Perkinsus sp., and trematodes were also detected in oyster samples from the Gulf of Thailand (Taveekijakarn et al. 2008). Nematopsis sp., Tylocephalum sp., digenetic trematodes, and ciliates were detected from Crassostrea iredalei from the coast of the Philippines (Erazo-Pagador 2010). Therefore, it is necessary to investigate the presence of pathogenic and symbiotic parasites of A. granosa in Malaysian and Indonesian waters from their economic and epidemiological point of view. The objective of the current study was to report the occurrence of diseases and parasites in natural stocks of A. granosa from the Straits of Malacca.

MATERIALS AND METHODS

For the histopathological survey, samples of the blood cockle, Anadara granosa, were collected from three distant locations along the coasts of the Straits of Malacca. The sampling sites were the west coast of Pulau Aman, Penang, Malaysia (Pulau Aman); the east coast of Banda Acheh, Sumatra, Indonesia (Banda Acheh); and the east coast of Lhokseumawe. Sumatra, Indonesia (Lhokseumawe; Fig. 1). Samples were collected monthly from natural populations from September 2009 to September 2010. For histopathological investigations, 10 cockles were randomly selected from the monthly samples for each site. After recording the shell length and tissue wet weight, the soft body was processed for histology. Surface water temperature and salinity at three sampling sites were monitored monthly during the course of study.

For histopathology, the soft tissue of each cockle was fixed in Bouin's fixative. After fixation, a transverse section was taken from the middle of the body to incorporate the gonads, digestive gland, mantle, gills, and muscular foot tissue. The tissues were then dehydrated and embedded in paraffin. The paraffin blocks were sectioned at a thickness of 6 [micro]m and stained with Harris' hematoxylin and counterstained with eosin Y. The presence of parasites in different tissues was investigated in the histological preparations under a light microscope. Parasite prevalence (i.e., [number of animals infected / number of animals examined] x 100) and distribution in each host were evaluated for each site. All data were analyzed statistically using the SPSS statistical package v. 11.0 to calculate the mean and SD.

[FIGURE 1 OMITTED]

RESULTS

Water Temperature and Salinity

The water temperature varied from 26.0 29.7[degrees]C in Pulau Aman, from 26.5-29.8[degrees]C in Banda Acheh, and from 28.7-29.9[degrees]C in Lhokseumawe during the 13-too study period (Fig. 2). There was no remarkable seasonal fluctuation in water temperature at each site throughout the course of the study. Small fluctuations were noted in the salinity of water in all sampling sites throughout the study. Salinity ranged from 25.2-31.1 psu, 26.5-31.5 psu, and 29.1-31.8 psu at Pulau Aman, Banda Acheh, and Lhokseumawe, respectively (Fig. 3).

Histopathology

This is the first report of a histopathology survey on bivalves from the Straits of Malacca. In the current study, the presence of Nematopsis sp., a digenetic trematode, and a turbellarian were confirmed in the histological preparations of the blood cockle, A. granosa, collected from three natural habitats of the Straits of Malacca. Table 1 shows the prevalence of different parasites in cockle samples collected from three sites for each sampling date during the study. Remarkable spatial differences were found in the parasitic communities of A. granosa of the Straits of Malacca. However, no apparent temporal variation in the prevalence of any parasite was found.

[FIGURE 2 OMITTED]

The apicomplexan protozoan parasite Nematopsis sp. was detected in A. granosa from all sites. The prevalence of infection was much higher in A. granosa collected from Pulau Aman compared with the infection prevalence reported from the other two sites. Mean prevalence was 60.0% in Pulau Aman, 1.5% in Banda Acheh, and 3.1% in Lhokseumawe (Table 1). There was no clear seasonality in the prevalence of infection during the investigated period. However, the values were considerably lower during February and June to August. The most frequent tissue location was the connective tissue adjacent to the epithelium of the intestinal tract, followed by gills, gonads, mantle, digestive glands, and muscular foot tissue (Table 2). The maximum number of hemocytes containing Nematopsis sp. per histological section was 12. The number of oocysts per Nematopsis sp. containing phagocytes varied from 1-5, with 2-3 oocysts being the most frequent condition, with a single uninucleate sporozoite in each oocyst. Oocysts were ellipsoidal, and the infection was light without any clear host tissue damage (Fig. 4). Oocyst length varied from 10-15 [micro]m (mean [+ or -] SD, 12.6 [+ or -] 1.4 [micro]m; n = 32), and the width ranged from 6.4-12.7 [micro]m (mean [+ or -] SD, 10.4 [+ or -] 1.7 [+ or -]m; n = 32).

[FIGURE 3 OMITTED]

Sporocysts of a digenetic trematode, enclosing germ balls and developing cercariae, were observed having the same apparent morphology in A. granosa collected from all three locations. Mean prevalence of infection was the highest in Pulau Aman (14.6%), followed by Banda Acheh (10.8%) and Lhokseumawe (3.9%: Table 1). No clear seasonality was evident in the prevalence of infection of trematodes in A. granosa obtained from all the sampling sites. The most frequent parasite location was the gonad followed by stomach epithelium, mantle, digestive glands, and foot muscle. In some animals, the gonad was completely lacking as a result of heavy infection (Fig. 5).

A turbellarian parasite was detected in A. granosa collected from all sites; however, the prevalence of infection was very low (Table 1). In some cases, a hemocytic response was associated with the metazoan. In the photomicrograph (Fig. 6), cilia are visible lining the outer margin of the parasite. The structural organization was typical of many turbellarians. The parasite was detected in stomach epithelium, gonad, digestive glands, mantle, and muscular foot tissue without evidence of any clear host tissue damage (Table 2).

DISCUSSION

This article describes the first histological screening of the blood cockle, A. granosa, for the presence of parasites in the Straits of Malacca. Histopathological investigation confirmed the presence of protozoan and metazoan parasites in the natural stocks of A. granosa collected from three distinct locations in Malaysian and Indonesian waters. Remarkable differences were found in the parasitic community in A. granosa collected from the three natural habitats of the Straits of Malacca, but no clear seasonality was noted. The gregarine parasite Nematopsis sp. was very common in cockles obtained from Pulau Aman. A digenetic trematode was detected in the samples obtained from all habitats, but different prevalence of infection was evident among the sites. A turbellarian was also detected in A. granosa from all sites.

Intrahemocytic oocysts of gregarines of the genus Nematopsis were detected from A. granosa collected from all three sites of the Straits of Malacca. The apicomplexan protozoan parasite, Nematopsis spp., has been reported to infect several bivalve species from many locations in tropical to temperate waters. The genus Nematopsis was reported to infect Arcuatula arcuatula (Tuntiwaranuruk et al. 2004), A. granosa (Tuntiwaranuruk et al. 2004), and Perna viridis (Tuntiwaranuruk et al. 2004, Tuntiwaranuruk et al. 2008) from the tipper Gulf of Thailand. Nematopsis sp. was the most prevalent parasite of the farmed silver-cupped oyster Crassostrea iredalei from the Philippines (Erazo-Pagador 2010). Such infection was also reported to occur along the Brazilian coast in Crassostrea rhizophorae (Nascimento et al. 1986, Sabry et al. 2007), Mytella guyanensis (Azevedo & Mates 1999, Boehs et al. 2010), and Anomalocardia brasiliana (Boehs et al. 2010). The parasite was also reported to infect bivalves in European, North American, and Australian waters (Lauckner 1983. Goggin & Cannon 1989, Carballal et al. 2001, Bower 2004, Francisco et al. 2010). Our preliminary data added new information on their distribution in natural stocks of blood cockles from the Straits of Malacca.

[FIGURE 4 OMITTED]

A remarkable difference in the spatial distribution of Nematopsis sp. was observed, with a higher prevalence of infection (60%) in A. granosa from Pulau Aman compared with Banda Acheh (1.5%) and Lhokseumawe (3.1%). Because temperature and salinity were more or less similar at all sampling sites during the study, some other factors are responsible for yielding such differences in the presence of this parasite in the same host among the sampling locations. Nematopsis spp. commonly infects molluscs as an intermediate host, and decapod crustaceans as a final host (Bower et al. 1994). There are a number of shrimp farms around Pulau Aman. The presence of crustaceans might facilitate the completion of the life cycle and the provision of stages capable of infecting the cockles, as also outlined by Tuntiwaranuruk et al. (2008) and Boehs et al. (2010). In tropical waters, the prevalence of Nematopsis spp. infection reported was 65-71% in C. iredalei from the Philippines (Erazo-Pagador 2010), 92% in A. arcuatula, 59%, in A. granosa, 60%, in P. viridis, 70% in Paphia undulata from the Gulf of Thailand (Tuntiwaranuruk et al. 2004), 73% in M. guyanensis, and 1% in A. brasiliana from the coast of South Bahia. Brazil (Boehs et al. 2010). The prevalence of infection obtained for A. granosa from Pulau Aman is comparable with the prevalence of such parasitic infections in bivalves from tropical waters noted earlier. Lower prevalence of infection in other sites in relation to these reports might be a spatial variation, often related to distance between infected and uninfected animals (density), presence of alternate host, and so on.

[FIGURE 5 OMITTED]

No clear seasonality in the prevalence of Nematopsis sp. in A. granosa was evident at the sampling sites. This might be a result, in part, of the tropical environment having slight fluctuations in temperature and salinity at all sampling stations during the study period, as also noted by Boehs et al. (2010). In contrast, temporal variations in the infection prevalence of this parasite were reported as a result of seasonal changes in water temperature, salinity, and rainfall (Tuntiwaranuruk et al. 2008). The prevalence of infection in 4 bivalve species from the Gulf of Thailand was generally high during the northeast monsoon season (November to February), which is characterized by low water temperature, high salinity, and low rainfall amounts (Tuntiwaranuruk et al. 2004, Tuntiwaranuruk et al. 2008).

[FIGURE 6 OMITTED]

In the current study, the high prevalence of infection of Nematopsis sp. was noted at one site, but there was no obvious host tissue damage from infection. It was reported that gregarines of the genus Nematopsis cause focal hemocytic infiltration at most, without obvious pathogenic effects (Bower et al. 1994). However, Tuntiwaranuruk et al. (2004) reported decreased filtering efficiency and food intake of the infected animal resulting from the presence of a large number of Nematopsis sp. containing phagocytes in the gill lumen, which resulted in the obstruction of the water flow between the inhalant and exhalent currents. Although gills and mantle tissue were reported as the most frequent locations for Nematopsis spp. (Carballal et al. 2001, Winstead et al. 2004, Sabry et al. 2007), in the current investigation, this parasite was most frequently observed in the connective tissue adjacent to epithelium of the intestinal tract, followed by the gills of the host.

Digenetic trematodes have complex life cycles in which bivalves are intermediate hosts that harbor larval stages, and carnivorous fish are the definitive hosts. In the current study, spatial variations in trematode infection were noted, with relatively higher prevalence of infection in Pulau Aman than that the other two sites, but with no apparent seasonality. The infection prevalence of digenetic trematodes in bivalves is generally low; however, their damage to the host is often noticeable. Digenean trematode infection was reported in up to 19.6% in Crassostrea forskali from the coast of Thailand (Taveekijakarn el al. 2008), 12% in Ruditapes philippinarum from Korean waters (Ngo & Choi 2004), 62% in Perna perna from the south and east coasts of South Africa (Calvo-Ugarteburu & McQuaid 1998), and 4% in Pinetada radiata from the coast of Bahrain (Khamdan 1998). Calvo-Ugarteburu and McQuaid (1998), and Ngo and Choi (2004) reported spatial variations of trematode infection in bivalves with no seasonality, as was observed in our study.

In the current study, trematode infection mostly occurred in the female gonad, and some animals were castrated as a result of heavy infection of trematode sporocysts. The sporocysts reduce the glycogen content (energy reserves) of the tissues and the efficiency of the circulatory system, resulting in a disturbance to gametogenesis, and castration (Bower et al. 1994). In the infected condition, the gonad appears well developed externally, and mature, but internally it is devoid of eggs or sperm: the only contents are the cercariae and tissue fluids. In castrated R. philippinarum, the gonad was completely occupied by sporocysts and cercaria of Cercaria tapidis instead of eggs (Lee et al. 2001, Ngo & Choi 2004). Khamdan (1998) reported that Bucephalus sp. destroyed female gonads of the pearl oyster P. radiata, resulting in reproductive failure. Degenerated gonads with smaller ova were observed in oysters that were heavily infected with a trematode parasite.

The turbellarian Urastoma cyprinae has been reported to parasitize the gills of various bivalves (Villalba et al. 1997, Bataller et al. 2003, Rayyan et al. 2004). From histological preparations, turbellarians can be observed adjacent to the gills or mantle, or within the lumen of gut and kidney (Bower 2004). In the current study, a turbellarian was found in the stomach epithelium, gonad, digestive glands, mantle, and gills of A. granosa. No pathological damage to the host was detected, which is inconsistent with the findings reported by Bower (2004). Although the prevalence of infection was very low, the presence of this parasite in this habitat can be used as a baseline for future investigations.

In conclusion, we conducted a 13-month histopathological survey to report the presence of parasites of the blood cockle, A. granosa, from three natural habitats in the Straits of Malacca. Our preliminary data revealed that the natural Stocks of blood cockle are infected by a number of parasites that have distinct spatial differences with no apparent tempo,al patterns. This preliminary survey will bc useful for planning a health monitoring program for the natural and cultivated blood cockle and other bivalves of commercial importance in Malaysian and Indonesian waters of the Straits of Malacca.

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M. JASIM UDDIN,* ZULFIGAR YASIN, MUNAWAR KHALIL AND AILEEN TAN SHAU-HWAI Marine Sciences Laboratory School of Biological Sciences, Universiti Sains Malaysia, 11800 Penang, Malaysia

* Corresponding author. E-mail: jasimfm11@yahoo.co.in

DOI: 10.2983/035.030.0328
TABLE 1.
Parasite prevalence (%) in Anadara granola collected from 3 different
sites in the Straits of Malacca.

                                     Sites
                  Pulau Aman (n = 130;    Banda Acheh (n = 130;
                  shell length, 38.2 [+   shell length, 46.8 [+
                  or -] 3.1 mm)           or -] 3.1 mm)

Months              N       T      Tur    N       T       Tur

September 2009    90       0      10       0       0       0
October 2009      50      40      10       0      10      10
November 2009     80      30       0       0      20       0
December 2009     90      50      10       0      20       0
January 2010      70      10       0      10      20       0
February 2010     20       0       0       0      30       0
March 2010        80      20       0       0      30       0
April 2010        90      10      10       0       0       0
May 2010          50      20       0       0       0       0
June 2010         40       0       0       0       0       0
July 2010         20       0       0       0       0       0
August 2010       40      10       0       0       0       0
September 2010    60       0      20      10      10       0
Mean prevalence   60.0    14.6     4.6     1.5    10.8     0.8

                         Sites
                  Lhokseumawe (n = 130;
                  shell length, 52.2 [+
                  or -] 6.4 mm)

Months            N       T       Tur

September 2009     0       0       0
October 2009       0       0       0
November 2009      0       0       0
December 2009      0      10       0
January 2010      20       0       0
February 2010     20      10      10
March 2010         0       0       0
April 2010         0       0       0
May 2010           0      10       0
June 2010          0       0       0
July 2010          0      20       0
August 2010        0       0       0
September 2010     0       0       0
Mean prevalence    3.1     3.9     0.8

N, Nematopsis sp.; T, Trematode sporocysts; Tur, Turbellarian.

TABLE 2.
Presence of parasites in different tissues of infected Anadara granosa
collected from the Straits of Malacca.

                 Parasites in Different Tissues among Infected
                                     Cockles (%)

Parasites        Gonads   Mantle   Gills   Digestive    Stomach
                                             Gland     Epithelium

Nematopsis sp.    35.0     28.8    51.3      25.0         0.0
Trematode         83.8     27.0     0.0      10.8         40.5
  Turbellarian    25.0     12.5    12.5      25.0         75.0

                 Parasites in Different Tissues
                   among Infected Cockles (%)

Parasites        Connective   Foot

Nematopsis sp.      60.0      3.8
Trematode           0.0       8.1
  Turbellarian      0.0       0.0
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