Xenohaliotis californiensis infection

International Common Names

• English: abalone rickettsiosis; abalone wasting disease; foot withering syndrome; infection with Xenohaliotis californiensis; withering disease; withering syndrome; withering syndrome of abalone

English acronym

• WS

Xenohaliotis californiensis (also called WS-RLO) is a bacterium that causes a fatal disease of marine gastropod molluscs of the genus Haliotis (abalones), called withering syndrome (WS).  Disease occurs in abalones along the eastern Pacific margin of North America in California, USA and Baja California, Mexico; it was first reported in California in 1985 and has been spreading both northwards and southwards.  As infected abalones have been transported to many countries around the world, the geographic range is likely to be broader than originally suspected.  WS is characterized by degeneration of the digestive gland of the host and depletion of glycogen reserves.  Animals cease feeding and catabolize foot muscle protein as an energy source, resulting in atrophy of the pedal muscle, and ultimately death. Some abalone species are endangered or of concern regarding their status, and some are important for fisheries or aquaculture, so the disease can have a significant impact on biodiversity and a significant economic impact. It is on the list of diseases notifiable to the World Organisation for Animal Health (OIE).

See Disease Course section.

WS-RLO infects the gastrointestinal epithelial cells of the posterior oesophagus, digestive gland and intestine (Friedman et al., 2000).  The incubation period is prolonged and can range from 3 to 7 months (Balseiro et al., 2006; Braid et al., 2005; Friedman et al., 2002; Moore et al., 2000).  It has been shown that infections may persist for long periods without the development of clinical disease when the host is maintained at a low water temperature (e.g. 15°C), and that exposure to elevated seawater temperatures (e.g. >17°C) results in clinical disease (Friedman and Finley, 2003; Moore et al., 2011; Moore et al., 2000).  Clinical disease is characterized by morphological changes in the digestive gland, which can vary depending on the species and may include degeneration and/or metaplasia (i.e., the replacement of one mature cell type by another) of the digestive tubules.  Metaplastic changes in the digestive gland include the transformation of the terminal secretory acini into absorptive/transport epithelia.  Morphological changes are accompanied by anorexia and depletion of glycogen reserves followed by catabolism of the foot muscle and use of this protein as an energy source, resulting in atrophy of the pedal muscle, and ultimately death (Balseiro et al., 2006; Braid et al., 2005; Kismohandaka et al., 1993; Moore et al., 2000).  Histologically, the foot of affected abalones contains fewer and less organized muscle bundles, abundant connective tissue, and in some cases more cerous cells than in unaffected individuals (Crosson et al., 2014; Friedman et al., 2007; Moore et al., 2000).  Microscopically, basophilic, oval intracytoplasmic bacterial inclusions can be observed in digestive epithelia (OIE, 2012).  Abalones that survive the disease can remain infected, even at low water temperature (Friedman and Finley, 2003).

Temperature appears to have a significant influence on the ecology, epidemiology and transmission of withering syndrome (WS).  The initial observation of WS occurred after the strong 1982-1983 El Niño event, which warmed the waters of the equatorial Eastern and Central Pacific Ocean by more than 3.5°C (an El Niño event is declared if the sea surface temperatures exceed 0.5°C above average for three months continuously).  Since then, WS has been repeatedly associated with seasonal or decadal thermal events and has also been observed in areas of thermal discharge from power plants, where water temperature can be more than 10°C above ambient (Crosson et al., 2014).  Likewise, during the severe El Niño of 1997-1998, when markedly elevated seawater temperature occurred throughout the southern and central Californian coast, up to 70% of black abalone (Haliotis cracherodii) examined showed clinical signs of WS (Raimondi et al., 2002). In the laboratory, a similar effect of temperature is observed; temperatures below 13°C have been demonstrated to limit transmission of the bacterium (only 1% transmission and no clinical signs of disease), while up to 94% transmission and extreme clinical signs were observed at 18.7°C (Braid et al., 2005).

Transmission of WS-RLO is postulated to be via a faecal-oral route.  Exposure of abalones to seawater containing infectious material is sufficient for transmission of the bacterium, and no direct animal contact is required (Balseiro et al., 2006; Braid et al., 2005; Friedman et al., 2002).

While no definitive vector or intermediate host for WS-RLO has been identified, it has been suggested that some colonial ascidians (commonly called “sea squirts”) may concentrate the bacterium (based on polymerase chain reaction evidence).  Thus, the possibility exists of such species acting as vectors for the bacterium, but further investigation of possible vectors is warranted (OIE, 2012).

Economic Impact

The meat (foot muscle) of abalone is used for food, and the shells are used as decorative items and as a source of ‘mother of pearl’ for jewelry, buttons, buckles, and inlay.  Abalone is one of the most highly prized seafood delicacies in many parts of the world, particularly in some parts of Latin America and Asia.  In 2013, the total global production of abalone from legal fisheries and farms was 110,950 metric tonnes (Cook, 2014).  Given that certain species of abalone can sell for about US$30/Kg or more (Cook, 2014), the economic impact from losses due to diseases such as WS can be significant.

Environmental Impact

Impact on habitats

Abalones of the genus Haliotis inhabit the nearshore intertidal and shallow subtidal zones.  They are ecologically important in engineering habitat by grazing on micro- and macroalgae, thereby maintaining open areas for the recruitment of conspecifics and other benthic organisms (Crosson et al., 2014). A reduction in their population caused by withering syndrome could therefore have significant ecological effects.

Impact on biodiversity

Withering syndrome is an important reason for the Critically Endangered status of Haliotis cracherodii (IUCN, 2014), and one of a number of causes of the decline in the populations of H. fulgens and H. corrugata which have led to their being classed as a species of concern in the USA (National Marine Fisheries Service, 2009). It is considered to be a potential threat to the Endangered H. sorenseni, but not so far to have been a major factor in the decline of this species in the wild (National Marine Fisheries Service, 2008).

There is no evidence that WS-RLO can infect humans; thus there is no concern regarding zoonotic disease or food safety.

Oxytetracycline (OTC) is approved for use in aquaculture and has been demonstrated to be effective against rickettsiae.  Oral administration of OTC in a medicated diet for 10 or 20 days provides protection against bacterial re-infection for several months.  Data suggest that a single-day oral administration of OTC can reduce bacterial infections from 80% to 10% prevalence and also reduce mean infection intensities (Friedman et al., 2007; Rosenblum et al., 2008).  The use of OTC water bath treatment (400 mg/l for one hour daily over 7 days) has also shown promising results (García- Esquivel et al., 2011). As the appearance of a bacteriophage virus infecting WS-RLO appears to attenuate WS disease, the prospects for phage therapy are intriguing (Friedman et al., 2014a).  No vaccines or other chemotherapeutic treatments are currently available for this disease (OIE, 2012).