Reduced salinity tolerance in the Arctic grayling (Thymallus arcticus) is associated with rapid development of a gill interlamellar cell mass: implications of high-saline spills on native freshwater salmonids

Arctic grayling (Thymallus arcticus) are salmonids that have a strict freshwater existence in post-glacial North America. Oil and gas development is associated with production of high volumes of hypersaline water. With planned industrial expansion into northern areas of Canada and the USA that directly overlap grayling habitat, the threat of accidental saline water release poses a significant risk. Despite this, we understand little about the responses of grayling to hypersaline waters. We compared the physiological responses and survivability of Arctic grayling and rainbow trout (Oncorhynchus mykiss) to tolerate an acute transfer to higher saline waters. Arctic grayling and rainbow trout were placed directly into 17 ppt salinity and sampled at 24 and 96 h along with control animals in freshwater at 24 h. Serum sodium, chloride and osmolality levels increased significantly in grayling at both 24 and 96 h time points, whereas trout were able to compensate for the osmoregulatory disturbance by 96 h. Sodium-potassium ATPase mRNA expression responses to salinity were also compared, demonstrating the inability of the grayling to up-regulate the seawater isoform nkaα1b. Our results demonstrated a substantially lower salinity tolerance in grayling. We also found a significant salinity-induced morphological gill remodelling by Arctic grayling, as demonstrated by the rapid growth of an interlamellar cell mass by 24 h that persisted at 96 h. We visualized and quantified the appearance of the interlamellar cell mass as a response to high salinity, although the functional significance remains to be understood fully. Compared with rainbow trout, which are used as an environmental regulatory species, Arctic grayling are unable to compensate for the osmotic stressors that would result from a highly saline produced water spill. Given these new data, collaboration between fisheries and the oil and gas industry will be vital in the long-term conservation strategies with regard to the Arctic grayling in their native habitat.