Mass mortality of pearl oyster ( Pinctada fucata (Gould)) in Japan in 2019 and 2020 is caused by an unidentified infectious agent
Tomomasa Matsuyama 1 ,
Satoshi Miwa 1 ,
Tohru Mekata 1 ,
Yuta Matsuura 1 ,
Tomokazu Takano 1 ,
Chihaya Nakayasu 1
Affiliations
Free PMC article
Abstract
Mass mortality of 0-year-old pearl oysters,
Pinctada fucata (Gould), and anomalies in adults were observed in Japan's major pearl farming areas in the summer of 2019 and 2020. Although adult oyster mortality was low, both adult and juvenile oysters underwent atrophy of the soft body, detachment of the mantle from nacre (the shiny inner surface of the valves), deposition of brownish material on the nacre, and loss of nacre luster. Infection trials were conducted to verify the involvement of pathogens in this phenomenon. Healthy adult pearl oysters were obtained from areas where this disease had not occurred to use as the recipients. The sources of infection were either affected adult oysters with atrophied soft bodies or batches of juveniles in which mortality had reached conspicuous levels. Transmission of the disease to the healthy oysters were tested either by cohabitation with affected oysters or by injections of the hemolymph of affected animals. The injection infection test examined the effects of filtration and chloroform exposure on the pathogen. Occurrence of the disease was confirmed by the appearance of brown deposits on the nacre and loss of nacre luster. The abnormalities of nacre were clearly reproduced in recipient shells in three out of four cohabitation trials with affected oysters. The disease was also reproduced in six out of six injection trails either with hemolymph filtered through 100 nm filter or with hemolymph treated with chloroform. In a serial passage with hemolymph injections, the disease was successfully transmitted through eight passages. These results suggest that the etiology of the disease is a non-enveloped virus with a diameter ≤100 nm.
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Other mass mortalities of pearl oysters.
From 1969–1970 a mass mortality of pearl oysters occurred in pearl farms from Port Moresby (Papua New Guinea) to Kuri Bay and Smith’s Harbour (Australia). It was observed that death rate on many occasions reached 100 per cent and many times, out of one cage containing ten oysters, only one had survived (George 1992). Mortality of pearl oyster, Pinctada maxima was about 80 per cent, although 30 to 60 per cent was
more common in the Australian pearl culture industry since 1974. It continued for more than one decade, and a three-year investigation (1980–1983) into the causes of mortality was conducted. The investigation found that mortality was related to transporting oysters from fishing grounds to lease sites, which took a ship about 37 hours. During the longer fishing periods, collected oysters were held on board for a maximum of four or five days. The oysters were kept and transported in high densities on fishing vessels with inadequate water circulation, which caused a build-up of bacteria in oyster carrier tanks. A bacterium, Vibrio harveyi, was found to be responsible for high mortality rates in the tanks (Dybdahl and Pass 1985)
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While the latter describes bacterial infection in history, the former suggests viral infection in Pinctada fucata. That can be worrisome. While bacteria can wreck havoc on a biomass, it's often short lived whether seasonally active or running it's course naturally.
In recent years, the west coast of N. America was infected by a syndrome known as "Sea Star Wasting Disease". This virus was first isolated and identified in 1948, but overall concentrations remained low. However, this has proliferated in the last decade, likely due to changes in marine pH (ocean acidification) and rising water temperatures though climate change.
Densoviruses are small (18–25 nanometers in diameter) and non enveloped. Densoviruses are known to infect members of insect orders while some viruses infect and multiply in crustaceans such as crabs and shrimp, or sea stars from phylum Echinodermata. Densovirinae are a subfamily of Parvoridae, aka Canine/Porcine Parvovirus. I suspect freshwater mussels are highly resistant to this (especially China, where pig manure fertilizes those ponds) whereas marine mollusks are greatly more susceptible.
Over the years, farmers reduced densities especially during relaying and transportation and final grow out. Running a clean operation, allowing fallow 33% of the time and greater sterility during grafting procedures will greatly reduce mass infection bacteria (namely vibrio sp.).
Viruses on the other hand are not so concerned with environmental stresses whilst infecting oysters. The infection rate among populations are very high, where mortalities follow. 80% is an insidious rate. Like fish, once a rate of 50% is surpassed, the better proactive solution is 100% destruction, lest surviving brood stock become infected. "Whirling Disease" in salmonids and trout is caused by a protozoan parasite carried by snails in fresh water streams, thus the entire biomass must be anhilated and otherwise reintroduced. That's not practical for marine mollusks though, because the virus is still present in the water column.
For years, relaying shellfish was commonplace. Once harvested, fishermen tended to relay to temporary locations pending sale. Producers very often relayed contaminated stocks to clean areas to flush toxins then sell them later. During my time contracting samples for red tide testing, we were required to relay mussels from clean areas to contaminated areas for 30 days then send them to the lab. Thus uptake is controlled as far a human biotoxins are concerned, but may give rise to spreading viruses to susceptible biomasses.
Although DFO approved (even insisted) relaying in my operation, I saw it as problematic. In 2011, oyster farms near Lagoon Island were infected with Norovirus (Macrocytosis mykena). I voluntarily suspended relaying from the farm for fear of infecting other areas. Instead, worked "in situ" with wild stocks. At the end of the day it was a lot less work, but not without other issues. While norovirus is not particularily harmful to shellfish, it poses a serious health risk to those who consume it.
Relaying invariably leads to monoculture, a dirty word to mother nature. Healthy populations come from genetic diverisity, not inbreeding or overcrowding. In our history as a society, monoculture provides sustainance for a massive population, where scarcely a farm exists where innoculation/sacrifices due to viruses are not standard operating practices.
Fishermen and farmers are generally marginal interests economically. Simply put, there are not enough resources to undertake even the simplest scientific research, no less something complicated as virology. Wholesalers, manufacturers and retailers generate millions, probably billions over the years, do woefully little for science and research. Japan and Australia to some degree, but mostly taxpayer funded because their respective countries depend on it. A grant here or a bursary there is all well and good locally for job creation, training or community support, but in the big picture, pearl farmers are left to their own devices for survival.
