Abalone Viral Mortality

On this page

• Category
• Common, generally accepted names of the organism or disease agent
• Scientific name or taxonomic affiliation
• Geographic distribution
• Host species
• Impact on the host
• Diagnostic techniques
• Methods of control
• References
• Citation information

Category

Category 3 (Host Not in Canada)

Common, generally accepted names of the organism or disease agent

Information on 2, apparently different diseases are included on this page. The common name indicated by the letter code a) in the following text is crack-shell disease of Haliotis discus hannai, while that for b) had the initial common name of Sphereovirus of “liver cells” in Haliotis diversicolor and was subsequently named abalone shriveling syndrome (AbSS), shriveling syndrome-associated virus (AbSV) or low-temperature viral disease.

Scientific name or taxonomic affiliation

Since the late 1990s, several reports of viral diseases in various species of abalone along the Pacific coast of Asia have been published. In all reports, the etiological agent was not fully understood (Zhengli and Handlinger 2004, OIE 2008). Following is a list of these reports (and more recent information) clustered according to similarity of disease etiology. Available information pertaining to each cluster of reports has the same letter code in subsequent subject headings presented below.

1. A kind of spherical virus found mainly in haemocytes and possibly in connective tissue cells and is referred to as “cracked shell disease” (Wang et al. 1997, 2000; Li et al. 1998, 2000). OIE ad hoc Group (2008) suggested that this virus as well as the viral infections of glioma which causes Amyotrophia of Abalone  in Japan may constitute a subacute to chronic syndrome within the abalone viral mortality complex.
2. Sphereovirus of “liver cells” (Wang et al. 1999, Song et al. 2000, Zhang et al. 2001, Huang et al. 2002, Fang et al. 2002) was subsequently named abalone shriveling syndrome-associated virus (AbSV) and abalone low-temperature viral disease (Zhuang et al. 2010, Jiang et al. 2012, Yang 2013, Chen et al. 2016, Gu et al. 2019). A similar virus was reported by Wang et al. (2004) in the cytoplasm of connective tissue cells and occasionally in haemocytes. The AbSV genome is a 34.952-kilobase circular double-stranded DNA (Zhuang et al. 2010, Jiang et al. 2014). Zhuang et al. (2010) indicated that AbSV contained putative genes with similarity to bacteriophages, eukaryotic viruses, bacteria and some endosymbionts and speculated that AbSV may represent a transitional form of microbial evolution from viruses to bacteria. OIE ad hoc Group (2008) suggested these viruses described generally as spherical virus may constitute an acute syndrome of abalone viral mortality.

Note that the virus(es) associated with “Abalone Viral Mortality” is/are apparently not the same as abalone herpesvirus (original acronym of AbHV and now known as HaHV-1) that causes ganglioneuritis (AVG) in abalone from Australia, Taiwan (Chinese Taipei) and south eastern China. For example, Wei et al. (2018) used metagenomics technology to detect both AbHV and AbSV in moribund Haliotis diversicolor collected between 1999 and 2003 from the south coast of China (Dongshan district, Fujian province and Nanao district, Guangdong province). However, McGladdery (2011) and Chen et al. (2012) grouped some of the reports from various hosts and locations indicated above (e.g., Wang et al. 1997, 2000, 2004; Song et al. 2000; and Zhang et al. 2001) as describing herpes-like viral pathogens. Corbeil et al. (2010) also referred to the spherical virus described by Wang et al. (2004) as a herpes-like virus. However, the OIE ad hoc Group (2008) and Bai et al. (2019) indicated that the relationship between the disease in China and AVG is still not defined due to the lack of further characterization of the virus and histopathology of diseased abalone from China. Nevertheless, Gu et al. (2019) suggested that abalone herpesvirus (AbHV) is the most probable cause of low-temperature viral disease.

Geographic distribution

1. Coast of People's Republic of China including abalone farms (Li et al. 1998, 2000). Specifically, the north and northeast coasts of China including Dalian, Liaoning Province and along the Bohai coast line (Zhengli and Handlinger 2004).
2. Abalone farms and wild stocks of abalone from the south coast of People's Republic of China (Zhengli and Handlinger 2004, Zhuang et al. 2010), specifically, in Fujian Province (Wang et al. 1999, Song et al. 2000, Zhang et al. 2001, Huang et al. 2002, Fang et al. 2002, Zhuang et al. 2010, Yang 2013, Wei et al. 2018) and Guangdong Province (Wang et al. 2004, Wei et al. 2018), where abalone herpesvirus (AbHV) is known to occur (Gu et al. 2019). Huang et al. (1999) indicated that the disease first appeared in Dongshan County of Fujian Province in 1999 and spread to Guangdong (Nie and Wang 2004). Jiang et al. (2012) indicated that the disease also spread to Taiwan.

Host species

1. Haliotis discus hannai (Wang et al. 1997, Li et al. 1998). Similar viral infection was reported from mussels (Mytilus edulis) within the known distribution of diseased abalone and artificial infections were achieved in the turban shell (Turbo sp.) and tegula (Tegula (=Chlorostoma) rusticum) (Li et al. 2000, Zhengli and Handlinger 2004).
2. Haliotis diversicolor, including Haliotis diversicolor supertexta and Haliotis diversicolor aquatilis (Wang et al. 1999, 2004; Song et al. 2000; Zhang et al. 2001; Huang et al. 2002; Zhuang et al. 2010; Jiang et al. 2012). Yang (2013) described the disease in farmed juvenile hybrids of Haliotis discus hannai and Haliotis discus discus in Fuzhou, Fujian Province.

Impact on the host

1. Infection caused a phenomenon called “crack shell disease” in early life stages of farmed Haliotis discus hannai (Li et al. 1998) and resulted in 50% mortality among experimentally exposed abalone (Wang et al. 1997). Apparently the effects of the disease decreased at temperatures above 20°C (Li et al. 2000).
2. The viral infection was associated with epidemics of mass mortalities in farmed Haliotis diversicolor (Wang et al. 1999, 2004; Song et al. 2000; Zhang et al. 2001). Nie and Wang (2004) claimed that it caused 100% mortality at 22 farms within 43 days in the spring of 1999 in Dongshan County. All sizes (life stages) of abalone were vulnerable (Wang et al. 2004, Zhuang et al. 2010). Temperatures less than 20°C seem to be required for expression of the disease (Wang et al. 2004) and thus the common name of abalone low-temperature viral disease (Gu et al. 2019). The disease was experimentally transferred between abalone in which the greatest pathology associated with mortality was observed in the digestive gland (liver, digestive diverticulum) (Song et al. 2000, Wang et al. 2004). In addition, this malady produced histological necrosis and abnormally modified macromolecules of hemocyanin and ferritin (Zhuang et al. 2010). Vibrio alginolyticus and Vibrio parahaemolyticus may co-infect abalone infected with the virus and could be co-factors for disease in H. diversicolor (Wang et al. 1999, Zhang et al. 2001, Zhengli and Handlinger 2004). During investigations into abalone herpes virus (AbHV)  in Taiwan, Chen et al. (2016) also analysed their samples by PCR for AbSV but found no positive signals for AbSV. They suggested that coinfections of AbHV and AbSV may have occurred in abalone chronic mortality events but did not consider AbSV to be the main pathogen and speculated that genome mutation in AbSV may have led to a decrease in virulence and lower mortalities in the field (Chen et al. 2016).

Diagnostic techniques

Gross observations

1. Infection was associated with shell deformities including a thin shell with turned-down front edge (turned inside out) and linked respiratory holes in early life stages of H. discus hannai (Li et al. 1998, Wang et al. 2000). Activity decreased, the soft body became slim and the abalone gradually died (Wang et al. 2000).
2. Diseased abalone became less active and increased mucus production (Zhang et al. 2001). Also, tanks containing diseased abalone had turbid water and filled with foam (Nie and Wang 2004, Wang et al. 2004). The foot (pleopod) of diseased abalone became stiff with a black surface and the mantle and foot shrank, and dead abalone were attached to the culture tank or cage (Nie and Wang 2004, Wang et al. 2004, Zhuang et al. 2010).

Histology

1. Histopathology in the epidermis and connective tissue cells of the mantle, foot, gill, digestive gland and crop (Li et al. 1998). The usual pathological changes include:
   • necrosis and disorder of connective tissues of all organs;
   • necrosis of haemocytes and epithelial cells;
   • disorder and detachment of epithelial cells of the foot, mantle, digestive gland and gills (Zhengli and Handlinger 2004).
2. Pathology was observed in the digestive gland and intestinal tract (Zhang et al. 2001). Zhengli and Handlinger (2004) described the pathology as disorder and hypertrophy of epithelial cells of the digestive gland including detachment and vacuolization of the epithelium and connective tissues. Yang (2013) described broken digestive gland lobule basal lamina muscle fibers, autolysis and pyknosis of microvillus and ciliated columnar epithelial cells in digestive gland tubules.

Electron microscopy

1. A spherical virion between 90 – 140 nm in diameter in membranous structures in the haemocyte cytoplasm and was associated with expansion of the mitochondria (Wang et al. 1997; Li et al. 1998, 2000). Wang et al. (2000) reported a size between 150-200 nm and indicated that the virus was not observed in the host cell nucleus and mainly infected cells in the foot muscle, mantle, gonad, digestive gland (liver), and gills.
2. The virus has been described as 'a globular virus of dimensions 5-8 x 120-150 nm' (Huang et al. 1999, Nie and Wang 2004). Wang et al. (1999) and Zhang et al. (2001) reported 3 forms of spheroid viruses (each about 50 nm, 110 nm and 150 nm in diameter), whereas Song et al. (2000) and Wang et al. (2004) indicate that the virus was either hexagonal and about 100 nm in diameter or spheroid and about 100 to 130 nm in diameter, respectively. These descriptions incorporate virus types 2, 3 and 4 of Zhengli and Handlinger (2004). Wang et al. (2004) indicated that the viral particles were contained in an electron dense nucleocapsid and a thick outer envelope with an electron lucent layer about 10-15 nm between them. Associated with infection of the virus in the cytoplasm of the host cell was: deformation and membrane damage of the nucleus, dilation and fragmentation of the mitochondria and proliferation of endoplasmic reticulum (Zhang et al. 2001, Wang et al. 2004). In addition, Zhengli and Handlinger (2004) and Zhuang et al. (2010) noted swollen membranes, denatured nucleoplasm with marginalization of the chromatin and vacuolisation of the cells. Yang (2013) suggested that the digestive gland basophilic cells may be the target cell of the virus where it developed in the nucleus of the basophilic cell leading to nuclear heteromorphosis, chromatin condensation, endoplasmic reticulum expansion, and mitochondria cristae breakage.

DNA probes

2. Zhuang et al. (2010) analysed the genome of AbSV. Jiang et al. (2012a) described a primer pair with good specificity and high efficiency of amplification when used in a quantitative real-time polymerase chain reaction (qPCR) assay. This test was used by Jiang et al. (2012a) to detect AbSV in apparently healthy mature hybrid (unclear genetic background) and juvenile H. diversicolor and by Gu et al. (2015) to confirm the presence of AbSV in an isolate produced by anion exchange chromatography technology. Jiang et al. (2012b) subsequently developed 2 nested PCR detection methods. For a more convenient and faster method for use in the field, Jiang et al. (2014) modified the loop-mediated isothermal amplification (LAMP, a nucleic acid amplification approach which uses a single incubation temperature) procedure and demonstrated that the assay had high specificity and sensitivity at a level similar to other reported PCR methods for viral detection in molluscs. Wei et al. (2018) used metagenomics technology on tissues from 3 groups of moribund Haliotis diversicolor collected between 1999 and 2003 from 2 districts on the south coast of China (Dongshan district, Fujian province and Nanao district, Guangdong province) and detected high levels of AbSV in one group and lower levels in the other two.

Methods of control

Infected abalone should not be transported into areas known to be free of the disease. Mortalities may be avoided if the farmed abalone are held at temperatures optimal for the abalone species being cultured (e.g., about 25°C for Haliotis diversicolor) (Wang et al. 2004). Huang et al. (2002) claimed that AbSS was cured in 5 abalone farms by using isolation methods, breeding in healthy water, and bathing and feeding abalone with some drugs.

References

Bai, C.-M., Y.-N. Li, P.-H. Chang, J.-Z. Jiang, L.-S. Xin, C. Li, J.-Y. Wang and C.-M. Wang. 2019a. Susceptibility of two abalone species, Haliotis diversicolor supertexta and Haliotis discus hannai, to Haliotid herpesvirus 1 infection. Journal of Invertebrate Pathology 160: 26-32.

Chen, M.H., S.T. Kuo, T. Renault, C.S. Friedman and P.H. Chang. 2012. Development of a polymerase chain reaction for the detection of abalone herpesvirus infection based on the DNA polymerase gene. Journal of Virological Methods 185: 1-6.

Chen, I.-W., P.-H. Chang, M.-S. Chen, T. Renault, M.-M. Chen, S.-T. Kuo and C.-H. Cheng. 2016. Exploring the chronic mortality affecting abalones in Taiwan: differentiation of abalone herpesvirus-associated acute infection from chronic mortality by PCR and in situ hybridization and histopathology.  Taiwan Veterinary Journal 42: 1-9.

Corbeil, S., A. Colling, L.M. Williams, F.Y.K. Wong, K. Savin, S. Warner, B. Murdoch, N.O.I. Cogan, T.I. Sawbridge, M. Fegan, I. Mohammad, A. Sunarto, J. Handlinger, S. Pyecroft, M. Douglas, P.H. Chang and M.St.J. Crane. 2010. Development and validation of a TaqMan® PCR assay for the Australian abalone herpes-like virus. Diseases of Aquatic Organisms 92: 1-10.

Fang, Y., Y.-y. Huang, J.-h. Yan, Q. Yan, W.-z. Wu and Z-m. Ni. 2002. Isolation and observation of “virus disease” virus of abalone in Dongshan, Fujian. Journal of Oceanography in Taiwan Strait 21: 199-203. (In Chinese with English abstract).

Gu, L., J.-Z. Jiang and J.-Y. Wang. 2015. Isolation of abalone shriveling syndrome-associated virus by anion exchanger chromatography. Journal of Southern Agriculture (Guangxi Agricultural Sciences) 46(12): 2223-2228. (In Chinese with English abstract).

Gu, L., R.-J. Qi, R. Yang, T. Han, J.-Z. Jiang and J.-Y. Wang. 2019. The prevalence of abalone herpesvirus in two Haliotis species in South China during 2002–2013. Aquaculture 505: 18-26.

Huang, Y., W. Wu, J. Yan, W. Zhou, X. Chen, Z. Ni and X. Chen. 1999. Investigation on an exterminate disease of Haliotis diversicolor aquatilis. Fujian Journal of Animal Husbandry and Veterinary 21: 4-5. (In Chinese with English abstract).

Huang, Y., W. Wu, Fangying, X. Chen, J. Yan and Z. Ni. 2002. Study on the spherical virus disease in cultured abalone Haliotis divericolor. Fujian Journal of Animal Husbandry and Veterinary 24(3): 1-3. (In Chinese with English abstract).

Jiang, J.-Z., Z.-N. Zhu, H. Zhang, Y.-Y. Liang, Z.-X. Guo, G.-F. Liu, Y.-L. Su and J.-Y. Wang. 2012a. Quantitative PCR detection for abalone shriveling syndrome-associated virus. Journal of Virological Methods 184: 15-20.

Jiang, J.-Z., Y.-Y. Liang, L.-J. Luo, Z.-X. Guo, J. Zhuang, G.-F. Liu, Y.-L. Su and J.-Y. Wang. 2012b. Nested PCR detection of abalone shriveling syndrome-associated virus in China. Journal of Virological Methods 184: 21-26.

Jiang, J.-Z., R. Yang, H. Zhang, G.-F. Liu, Z.-N. Zhu, Y.-L. Su, E.-Y. Wu and J.-Y. Wang. 2014. Detection of abalone shrivelling syndrome-associated virus using loop-mediated isothermal amplification. Journal of Fish Diseases 37: 63-67.

Li, X., B. Wang, S. Liu, M. Liu and Q. Wang. 1998. Studies on pathogeny and histopathology of “Crack Shell Disease” of Haliotis discus hannai. Journal of Fisheries of China 22(1): 61-66. (In Chinese with English abstract).

Li, X., B. Wang, S. Liu and J. Xu. 2000. The infection to a few kinds of shellfish inshore by a kind of virus. Journal of Dalian Fisheries University 15(2): 86-91. (In Chinese with English abstract).

McGladdery, S.E. 2011. Shellfish diseases (viral, bacterial and fungal), In: Woo, P.T.K., D.W. Bruno (eds.) Fish diseases and disorders. Volume 3: viral bacterial and fungal infections. CABI, pp. 748-854.

Nie, Z. and S. Wang. 2004. The status of abalone culture in China. Journal of Shellfish Research 23: 941-945.

OIE ad hoc Group. 2008. Report of the Meeting of the OIE ad hoc Group on the OIE List of Aquatic Animal Diseases - Mollusc Team - for the OIE Aquatic Animal Health Code. Paris, 25-27 January 2008., pp. 135-162. Available in the Report of the Meeting of the OIE Aquatic Animal Health Standards Commission . Paris, 3–7 March 2008.

Song, Z., R. Ji, S. Yan, C. Chen, Y. Zhong, Y. Jiang and Z. Ni. 2000. A sphereovirus resulted in mass mortality of Haliotis diversicolor aquatilis. Journal of Fisheries of China 24(5): 463-466. (In Chinese with English abstract).

Wang, B., X. Li and C. Gou. 1997. Infection of spherical virus from Haliotis discus hannai Ino. Virologica Sinica 12(4): 360-363. (In Chinese with English abstract).

Wang, J., Y. Su, J. Zhang, Y. Huang, Z. Zhang, Q. Yan and D. Wang. 1999. Spring explosive epidemic disease of abalone in Dongshan District. Journal of Xiamen University (Natural Science) 38(5): 641-644. (In Chinese with English abstract).

Wang, J., B. Chen, J. Feng, M. Yu and X. Wu. 2000. Primary observation on spherical virus in diversicolor abalone (Haliotis diversicolor) with crack shell disease. Tropic Oceanology 19(4): 82-85. (In Chinese with English abstract).

Wang, J., Z. Guo, J. Feng, G. Liu, L. Xu, B. Chen and J. Pan. 2004. Virus infection in cultured abalone, Haliotis diversicolor Reeve in Guangdong Province, China. Journal of Shellfish Research 23: 1163-1168.

Wei, H.-Y., S. Huang, T. Yao, F. Gao, J.-Z. Jiang and J.-Y. Wang. 2018. Detection of viruses in abalone tissue using metagenomics technology. Aquaculture Research 49: 2704-2713.

Yang, X.-Q. 2013. Studies on pathology of “Shriveling Syndrome Associated Virus (AbSV)” in juvenile hybrid abalone. Fujian Journal of Agricultural Sciences 28(5): 432-437. (In Chinese with English abstract).

Zhang, Z., J. Wang, Y. Su, Q. Yan, X. Chi, H. Zhou and Y. Zhou. 2001. Pathogeny and histopathology of the epidemic disease in Haliotis diversicolor supertexta. Journal of Xiamen University (Natural Science) 40(4): 949-956. (In Chinese with English abstract).

Zhengli, S. and J. Handlinger. 2004. Abalone Viral Mortality - Disease card. Developed to support the NACA/FAO/OIE regional quarterly aquatic animal disease (QAAD) reporting system in the Asia-Pacific. NACA, Bangkok, Thailand. 5 pp.

Zhuang, J., G. Cai, Q. Lin, Z. Wu and L. Xie. 2010. A bacteriophage-related chimeric marine virus infecting abalone. PLoS ONE 5(11): e13850.

Citation information

Bower, S.M. (2022): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Abalone viral mortality.

Date last revised: January 2022
Comments to Susan Bower