Reduced farming density of New Zealand flat oyster Ostrea chilensis is associated with decreased infection by Bonamia ostreae and other parasites

The haplosporidian parasites Bonamia ostreae and Bonamia exitiosa are notifiable to the World Organisation for Animal Health. The first detection of B. ostreae in the southern hemisphere in 2015 was associated with high mortality in some stocks of farmed flat oysters, Ostrea chilensis, in the Marlborough Sounds, Aotearoa New Zealand (NZ), whereas B. exitiosa is considered endemic and commonplace. Subsequently, national restrictions were placed on flat oyster movements, and ultimately, in 2017, all flat oyster farms in NZ were de-populated and farming stopped. The farm where B. ostreae was first detected, adapted their practices following the detection and held oysters at both normal stocking densities and lowered stocking densities for 2+ years (2015 to 2017). Although this study was opportunistic and could not determine causality, and other factors may also have influenced parasite prevalence and intensity, flat oysters cultured at reduced densities had significantly lower prevalence and intensity of B. ostreae infections compared with those cultured at a higher (normal pre-2015) density on the same farm (22 % vs 95 % prevalence, and 0.18 vs 1.31 mean intensity grade on a scale of 1–3). There was also significantly lower prevalence of infection of other common parasites including apicomplexan X (APX; 3 % vs 45 %) and the trematode Alcicornis longicornutus (3 % vs 23 %) at lower density. We also hypothesise that some degree of resistance to B. ostreae , and tolerance to bonamiosis existed in this population of NZ flat oysters, as in the high-density group that experienced very high levels of mortality, around a quarter of the 5 % of survivors were healthy and lacked any detectable Bonamia infection, with some PCR negative for Bonamia . Regardless of density, there was a marked reduction in prevalence of B. exitiosa in 2017 (just 1/98 oysters) compared to a previous study of the same farm in 2015. Finally, we also provide novel insights into the progression of B. ostreae infection in NZ flat oysters. Infections were initially detected in the mid-gut, followed by the digestive gland, mantle, gill and finally gonad, and although APX prevalence was not correlated with Bonamia, both APX-infected animals and those infected with A. longicornutus had reduced gonad size and density compared to uninfected animals. These data suggest that reducing stocking density may significantly reduce parasite infection in this species. Changes in husbandry, along with production of disease-free juveniles and potential selective breeding, may enable re-establishment of this important aquaculture industry, with potential benefits for the long-term protection of fisheries and biodiversity in NZ. • Lower oyster farming density was associated with lower Bonamia ostreae infection. • Variation likely exists for tolerance or resistance to Bonamia in O. chilensis. • Bonamia infection progressed from digestive tissues to the mantle, gill and gonad. • Lowered stocking density may substantially improve oyster health and production. • Husbandry and selective breeding may enable farming in parasite-infected areas.