A case report and statewide surveillance of "weak meat" condition of Alaska weathervane scallops, Patinopecten caurinus, linked to a recently identified pathogenic parasite, Merocystis kathae (Apicomplexa: Aggregatidae).

Weathervane scallop, Patinopecten caurinus, the largest scallop species in the world, is distributed from northern California, U.S.A., to the Bering Sea, and is only commercially harvested in Alaska. The fishery is considered well managed by the State of Alaska (U.S.A) Department of Fish and Game (ADF&G) and federal government, with many precautionary measures in place to avoid overharvest. There have been episodic declines in some management areas due to unknown causes. Fishermen also encounter scallops with abnormal adductor muscles, a condition colloquially termed "weak meat", characterized by the retention of muscle when shucked, an obvious darkened discoloration, and/or an abnormal texture making the product unacceptable for marketing. A similar syndrome in Atlantic sea scallops, Placopecten magellanicus, described as "gray meat", occurs in the eastern U.S. and Canada, and proposed causes include senescence, loss of bioenergetics due to chronic infestations, or a synergism of these factors. Recently a severe apicomplexan infection was found to cause a gray meat condition in Iceland scallops, Chlamys islandica, and the collapse of that stock. This parasite was subsequently detected in Atlantic sea scallops with the gray meat condition off the U.S. East Coast. Studies that followed identified the parasite as Merocystis kathae, previously described from the common whelk, Buccinum undatum, more than 100 years ago. In 2015 Bering Sea fishermen reported weak meat in their catch, so samples were submitted to ADF&G for diagnosis. Adductor muscles from all affected scallops had many large foci of an apicomplexan associated with necrosis, fibrosis, and muscular atrophy. Given the reduced quality, marketability, and possibly fitness of affected scallops, we performed a survey to estimate prevalence, intensity, and geographic distribution of this apicomplexan in Alaskan weathervane scallops. We sampled 180 scallops, from individual beds within each of the three major geographically broad scallop areas in Alaska. Overall prevalence was about 82%, ranging from 69 to 100% by district. Overall mean infection intensity, based on the number of parasite foci/section, was about 9 (range of 5-29, by location), with scallops from the Bering Sea and Southwest Kodiak being most severely infected. Molecular analyses confirmed that the Alaskan parasite is M. kathae, i.e., the same apicomplexan that caused the collapse of Icelandic scallops and a suspected cause for gray meat and mass mortality of Atlantic sea scallops in northeast North America.

The presence of Apicomplexan parasites in king scallops (Pecten maximus) in Scottish waters.

The king scallop (Pecten maximus) is a commercially important species found around the United Kingdom coast. The association of an Apicomplexan-like parasite with mass mortality of Icelandic scallop (Chlamys islandica) in Iceland and the presence of identical parasites in king scallop (Pecten maximus) and queen scallop (Aequipecten opercularis) in Scotland raised serious concerns regarding the health of Scottish king scallops. Marine Scotland Science (MSS) conducted a survey in 2016 to assess the prevalence and the intensity of parasite infection in king scallops. King scallops were collected and sampled during the annual scallop dredge surveys in the Shetland Isles and the east and west coast of Scotland. The king scallop adductor muscle was macroscopically examined and tissue imprints taken to grade the intensity of infection. The parasite was present in the majority of the king scallops sampled in all surveyed areas: Shetland Isles 87.1%, east coast 76.0% and west coast of Scotland 64.1%. However, the parasitic infestations were light in intensity with the majority of the king scallops graded as 1 (≤20 zoites per microscopic field). No macroscopic changes in the adductor muscle were observed and histopathology examination revealed minor localized fiber degeneration of adjacent fibers to parasite clusters. The results suggested the parasite to be widespread around the Scottish coast and it appears to be able to live within the king scallop at low intensity of infection without causing significant downgrade of the adductor muscle (in terms of colour or texture) or mortality. The partial genome sequence of the parasite in king scallops from Scottish waters was identical to the one reported by Kristmundsson and Freeman (2018) in the Icelandic scallop in Icelandic waters.

Perkinsus mediterraneus infection induces oxidative stress in the mollusc Mimachlamys varia.

Perkinsus mediterraneus is a protozoan parasite that can cause marine mollusc diseases known as perkinsosis being a serious threat for clam cultures worldwide. The aim of the present study was first to determine the Perkinsus species infecting the variegated scallop Mimachlamys varia and then to evaluate the existence of oxidative stress in gills of M. varia according to different degrees of infection. DNA sequencing confirmed that P. mediterraneus was the species infecting M. varia. ROS production was progressively increasing with the degree of infection although the differences were only significant in the high-infected group. Low degree of infection significantly increased superoxide dismutase (SOD) and glutathione S-transferase (GST) activities and nitrite levels with respect to the control group. In the high-infected group, a significant increase was evidenced in all analysed enzymes, catalase, SOD, glutathione reductase and GST. Non-significant differences in MDA levels were observed between the control and low-infected groups; however, a significant increase in MDA levels was observed in the high-infected group. In conclusion, the infection by Perkinsus mediterraneus in M. varia induces oxidative stress and an antioxidant response directly related to the infection degree that can contribute to the pathogenicity of the infection.

First report of the metacestode Caulobothrium sp. in the Peruvian scallop Argopecten purpuratus from Sechura Bay, Piura, Peru.

In recent parasitological surveys performed on the Peruvian scallop, Argopecten purpuratus, from bottom cultures of Sechura Bay, Piura, Peru, free and encysted metacestodes were frequently found in their gonads. The objective of this study was to identify this metacestode, determine their prevalence and intensity and briefly assess the histopathological impact in the affected tissues. A parasitological study of 890 scallops over a 3-year period was performed in order to determine the parasite prevalence and intensity. Microscopical observation of details of the scolex and histopathological study of the affected host tissues were performed as well as molecular characterization of the parasite based on 18S and 28S rDNA sequences. The prevalence of the metacestode was 82.2% in August of 2013, 90.4% in November of 2014, and 83.1% and 85.6% in April and September of 2015, respectively. The highest average intensity (218.4) was found in spring of 2014. The histopathological study showed that plerocercoids reduced the gonadal space where the ovules develop. The molecular characterization and phylogenetic analysis revealed that the metacestodes belong to the genus Caulobothrium having high sequence similarity to Caulobothrium opisthorchis. This study constitutes the first report of Caulobothrium metacestodes in the scallop A. purpuratus.

Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation.

The Japanese scallop (Mizuhopecten yessoensis) is one of the most important aquaculture species in Asian countries; however, it has suffered severe infection by Polydora in northern China in recent years, causing great economic losses. The Polydora parasitizes the shell of scallops, badly destroying the shell's structure. To investigate the molecular response mechanism of M. yessoensis to Polydora infestion, a comprehensive and niche-targeted cDNA sequence database for diseased scallops was constructed. Additionally, the transcriptional changes in the edge mantle, central mantle and hemocytes, tissues directly related to the disease, were first described in this study. The results showed that genes involved in shell formation and immunomodulation were significantly differentially expressed due to the infestation. Different transcriptional changes existed between the two mantle regions, indicating the different molecular functions likely responsible for the formation of different shell layers. The differential expression of genes for immune recognition, signal transduction and pathogen elimination presented an integrated immune response process in scallops. Moreover, neuromodulation and glycometabolism involved in the regulation process with relevant function significantly enriched. The study provides valuable information for mechanism study of shell formation and immunomodulation in scallops.

Harmless sea snail parasite causes mass mortalities in numerous commercial scallop populations in the northern hemisphere.

Apicomplexans comprise a group of unicellular, often highly pathogenic, obligate parasites exploiting either one or two hosts to complete a full reproductive cycle. For decades, various scallop populations have suffered cyclical mass mortality events, several of which shown to be caused by apicomplexan infections. We report the first dual mollusc life cycle for an apicomplexan: a species highly pathogenic in various pectinid bivalve species, but apathogenic when infecting the common whelk as Merocystis kathae. The sympatric distribution of the common whelk and scallops in the North Atlantic makes transmission extremely effective, occurring via the gastrointestinal tract, by scavenging and predation in whelks and unselective filter feeding in scallops. Infective sporozoites from whelks utilize scallops´ haemocytes to reach muscular tissue, where asexual reproduction occurs. Phylogenetically, this apicomplexan is robustly placed within the Aggregatidae and its inclusion in analyses supports a common ancestry with other basal invertebrate apicomplexans. Scallops seem able to regulate low-level infections of M. kathae as they exist in normal populations while epizootics occur during high levels of exposure from locally infected whelks. A targeted removal of whelks from valuable scallop grounds would be advantageous to minimize the occurrence of M. kathae epizootics and prevent damaging economic losses.

Gray meat in the Atlantic sea scallop, Placopecten magellanicus, and the identification of a known pathogenic scallop apicomplexan.

Atlantic sea scallop (Placopecten magellanicus) meats are normally firm and creamy white. However, scallops with small, darkened and stringy adductor muscle (gray meat) episodically occur along the Eastern Seaboard, most recently in the rotational management areas of Georges Bank after extended fishing closures. These gray meat scallops are associated with reduced harvestable biomass and mass mortality events. We tested age, nutritional stress and disease as causative agents for this condition. Adult scallops of different shell heights (SH) ranging from (90-145mm) were collected from Georges Bank and analyzed for meat quality and the presence of pathogens using biochemical, histopathological and molecular methods. Gray meat occurrence was weakly correlated with shell height only explaining 8.49% of the variance in a generalized additive model (GAMS). Gray meat weights were lower than white meat (p<0.001) and there was a dramatic reduction in protein content (p<0.05) in gray meat scallops associated with extensive myodegeneration. Amino acid profiles confirmed the breakdown of muscle tissue with an increase in free hydroxyproline in gray meat scallops. Infection by an apicomplexan parasite was detected in the muscle tissue of all gray meat scallops tested. An intermediate pathology stage (brown meat) was also identified. As the parasitic infection increased, meat quality decreased. Numerous developmental stages of the parasite were present in various organs of the scallops. This apicomplexan has an identical SSU rDNA sequence to a novel parasite occurring in the Iceland scallop during a recent mass mortality event. The range of this parasite in Atlantic sea scallops and the effect of abiotic/biotic stressors on pathogenicity are currently unknown. Results from this study link an apicomplexan species, known to be highly pathogenic in scallops, to gray meat occurrence with a potentially high impact on the fishery.

Is an Apicomplexan Parasite Responsible for the Collapse of the Iceland Scallop (Chlamys islandica) Stock?

Due to the total and unexpected collapse of the Iceland scallop, Chlamys islandica, stocks around Iceland during the 2000s, a commercial fishing ban has been imposed on this valuable resource since 2003. Following the initial identification of an apicomplexan parasite in the scallops, a long-term surveillance program was established to evaluate the effect of the parasite on the population. The infections were highly prevalent in all shell sizes throughout the study. However, the parasite only impacts mature scallops where they cause severe macroscopic changes, characterized by an extensively diminished and abnormally coloured adductor muscle. A highly significant relationship was observed between infection intensity and gonad and adductor muscle indices. The first four years of the study, were characterized by high infection intensity and very poor condition of the adductor muscle and gonads, whilst during subsequent years, infections gradually decreased and the condition of the scallops improved. Histopathological changes were restricted to the presence of apicomplexan zoites which were widely distributed, causing varying degrees of pathology in all organs. In heavy infections, muscular and connective tissues were totally necrotized, destroying significant parts of numerous organs, especially the adductor muscle, digestive gland and gonads. The progression of the disease was in good synchrony with the mortality rates and the subsequent decline observed in the scallop stock and recruitment indices. Our findings strongly suggest that the apicomplexan parasite played a major role in the collapse of the Iceland scallop stock in Breidafjordur. In addition to causing mortality, the infections significantly impact gonad development which contributes further to the collapse of the stock in the form of lower larval recruitment. Furthermore, compelling evidence exists that this apicomplexan pathogen is causing serious disease outbreaks in other scallop populations. Similar abnormal adductor muscles and the parasite itself have been identified or observed in association with other mass mortality events in several different scallop species and commercial stocks in the northern hemisphere.

Population Dynamics and Parasite Load of a Foraminifer on Its Antarctic Scallop Host with Their Carbonate Biomass Contributions.

We studied the population dynamics and parasite load of the foraminifer Cibicides antarcticus on its host the Antarctic scallop Adamussium colbecki from three localities differing by sea ice cover within western McMurdo Sound, Ross Sea, Antarctica: Explorers Cove, Bay of Sails and Herbertson Glacier. We also estimated CaCO3 biomass and annual production for both species. Cibicides populations varied by locality, valve type, and depth. Explorers Cove with multiannual sea ice had larger populations than the two annual sea ice localities, likely related to differences in nutrients. Populations were higher on Adamussium top valves, a surface that is elevated above the sediment. Depth did not affect Cibicides distributions except at Bay of Sails. Cibicides parasite load (the number of complete boreholes in Adamussium valves) varied by locality between 2% and 50%. For most localities the parasite load was < 20%, contrary to a previous report that ~50% of Cibicides were parasitic. The highest and lowest parasite load occurred at annual sea ice localities, suggesting that sea ice condition is not important. Rather, the number of adults that are parasitic could account for these differences. Cibicides bioerosion traces were categorized into four ontogenetic stages, ranging from newly attached recruits to parasitic adults. These traces provide an excellent proxy for population structure, revealing that Explorers Cove had a younger population than Bay of Sails. Both species are important producers of CaCO3. Cibicides CaCO3 biomass averaged 47-73 kg ha(-1) and Adamussium averaged 4987-6806 kg ha(-1) by locality. Annual production rates were much higher. Moreover, Cibicides represents 1.0-2.3% of the total host-parasite CaCO3 biomass. Despite living in the coldest waters on Earth, these species can contribute a substantial amount of CaCO3 to the Ross Sea and need to be incorporated into food webs, ecosystem models, and carbonate budgets for Antarctica.

Identification and characterisation of pathogenic Vibrio splendidus from Yesso scallop (Patinopecten yessoensis) cultured in a low temperature environment.

A fatal disease with apparent lesions on the adductor muscles of Yesso scallop Patinopecten yessoensis has occurred for three consecutive years from 2009 to 2011 in the northeastern China. This disease has been suspected to be closely associated with bacterial infections. In the present study, 96 bacteria were isolated from the lesions of moribund scallops. They were grouped into Vibrio (88 strains), Moritella (5 strains), Pseudomonas (2 strains) and Shewanella (1 strain) by 16S rDNA sequencing. In the Vibrio group, Vibrio splendidus was the predominant species, consisting of 43 strains. A strain of V. splendidus, named JZ6, was identified as a potential pathogen because it possessed two important virulence factors, Vsm and OmpU. Stain JZ6 was cold-adapted, and could surviveand exhibit haemolytic activity from 4°C to 32°C, with the highest activity observed at 10°C. The pathogenicity of JZ6 was further confirmed by injection and immersion challenges to scallops at 10°C. The cumulative mortality rates in the two experiments were 80% and 45%, respectively, which were significantly higher (P<0.05) than those of control and blank groups. The disorganisation of muscle fibres in challenged scallops was observed to be histopathologically identical to that in moribund Yesso scallop collected from the same farm. The results indicate that V. splendidus is the predominantly culturable bacteria from the lesions of diseased Yesso scallop, and JZ6 probably is the pathogenic agent to Yesso scallop in this low temperature environment.

Haplosporidium nelsoni (MSX) in Japanese scallops Patinopecten yessoensis (Jay, 1857) from Dalian along the northern coast of the Yellow Sea, China.

The protozoan parasite Haplosporidium nelsoni (MSX) was identified in Japanese scallops Patinopecten yessoensis (Jay, 1857) from Dalian along the northern coast of the Yellow Sea, China by histopathologic examination, polymerase chain reaction (PCR) amplification, and in situ hybridization (ISH) assay. H. nelsoni plasmodia-like structures were identified in the digestive glands of scallops by histologic examination, but no parasite spores were observed. PCR using the Hap-F2, R2 primer pair produced a sequence with 100% homology with the corresponding small subunit rDNA region of H. nelsoni. An ISH assay using the oligonucleotide probe MSX1347 produced a positive reaction with the Japanese scallop parasite. This is the first report of H. nelsoni in P. yessoensis in China.

Previously unknown apicomplexan species infecting Iceland scallop, Chlamys islandica (Müller, 1776), queen scallop, Aequipecten opercularis L., and king scallop, Pecten maximus L.

Examination of three scallop species from three separate locations: Iceland scallop from Icelandic waters, king scallop from Scottish waters and queen scallop from Faroese and Scottish waters, revealed infections of a previously unknown apicomplexan parasite in all three scallop species. Developmental forms observed in the shells appeared to include both sexual and asexual stages of the parasite, i.e. merogony, gametogony and sporogony, which suggests a monoxenous life cycle. Meronts, gamonts, zygotes and mature oocysts were solely found in the muscular tissue. Zoites, which could be sporozoites and/or merozoites, were observed in great numbers, most frequently in muscles, both intracellular and free in the extracellular space. Zoites were also common inside haemocytes. Examination of the ultrastructure showed that the zoites contained all the major structures characterizing apicomplexans. This apicomplexan parasite is morphologically different from other apicomplexan species previously described from bivalves. Presently, its systematic position within the phylum Apicomplexa cannot be ascertained.

Margolisiella islandica sp. nov. (Apicomplexa: Eimeridae) infecting Iceland scallop Chlamys islandica (Müller, 1776) in Icelandic waters.

Wild Iceland scallops Chlamys islandica from an Icelandic bay were examined for parasites. Queen scallops Aequipecten opercularis from the Faroe Islands and king scallops Pecten maximus and queen scallops from Scottish waters were also examined. Observations revealed heavy infections of eimeriorine parasites in 95-100% of C. islandica but not the other scallop species. All life stages in the apicomplexan reproduction phases, i.e. merogony, gametogony and sporogony, were present. Trophozoites and meronts were common within endothelial cells of the heart's auricle and two generations of free merozoites were frequently seen in great numbers in the haemolymph. Gamonts at various developmental stages were also abundant, most frequently free in the haemolymph. Macrogamonts were much more numerous than microgamonts. Oocysts were exclusively in the haemolymph; live mature oocysts contained numerous (>500) densely packed pairs of sporozoites forming sporocysts. Analysis of the 18S ribosomal DNA revealed that the parasite from C. islandica is most similar (97.7% identity) to an unidentified apicomplexan isolated from the haemolymph of the giant clam, Tridacna crocea, from Japan. Phylogenetic analyses showed that the novel sequence consistently grouped with the Tridacna sequence which formed a robust sister clade to the rhytidocystid group. We propose the name Margolisiella islandica sp. nov., referring to both type host and type locality.

Superoxide dismutase activity in juvenile Litopenaeus vannamei and Nodipecten subnodosus exposed to the toxic dinoflagellate Prorocentrum lima.

The toxic effect of the dinoflagellate Prorocentrum lima on juvenile American whiteleg shrimp Litopenaeus vannamei and giant lion-paw scallop Nodipecten subnodosus was evaluated. Organisms were exposed to three densities (500, 2000, or 5000 cells mL(-1)), superoxide dismutase activity and soluble protein in the hepatopancreas and muscle were determined at 1, 6, 24 and 48 h after challenge. Shrimp exposed at 5000 cells mL(-1) significantly increased SOD activity in the hepatopancreas at 1 h post-challenge, whereas enzymatic activity in muscle significantly increased at 24 h at all densities. Scallops exposed to 500 and 2000 cells mL(-1) showed significant SOD activity increase in hepatopancreas at 24 and 12 h, respectively. Mortality at 48 h was 100% in scallops exposed to 5000 cells mL(-1). Shrimp showed higher levels of SOD activity than scallops. Soluble protein content in the shrimp hepatopancreas was significantly higher at densities of 500 and 2000 cells mL(-1) at 6 and 1 h, respectively. Soluble protein content in the scallop hepatopancreas was higher than control values at 1 h after challenge. In this study, 500 cells mL(-1) was enough to trigger SOD activity in two benthic species exposed to the toxic dinoflagellate P. lima.