High prevalence of vaterite in sagittal otoliths causes hearing impairment in farmed fish

Abstract

The rapid growth of aquaculture raises questions about the welfare status of mass-produced species. Sagittal otoliths are primary hearing structures in the inner ear of all teleost (bony) fishes and are normally composed of aragonite, though abnormal vaterite replacement is sometimes seen in the wild. We provide the first widespread evaluation of the prevalence of vaterite in otoliths, showing that farmed fish have levels of vaterite replacement over 10 times higher than wild fish, regardless of species. We confirm this observation with extensive sampling of wild and farmed Atlantic salmon in Norway, the world’s largest producer, and verify that vateritic otoliths are common in farmed salmon worldwide. Using a mechanistic model of otolith oscillation in response to sound, we demonstrate that average levels of vaterite replacement result in a 28–50% loss of otolith functionality across most of a salmonid’s known hearing range and throughout its life cycle. The underlying cause(s) of vaterite formation remain unknown, but the prevalence of hearing impairment in farmed fish has important implications for animal welfare, the survival of escapees and their effects on wild populations, and the efficacy of restocking programs based on captive-bred fish.

Rapid growth causes abnormal vaterite formation in farmed fish otoliths

“…Both otoliths were removed from Atlantic salmon from each experiment, cleaned, dried, and photographed under a dissecting microscope at 10× magnification. As vateritic otoliths from Atlantic salmon are easy to distinguish visually from aragonitic ones (Sweeting et al, 2004;Oxman et al, 2007;Reimer et al, 2016), they were visually scored as 'vaterite' if any vaterite crystals were visible (indicating that the switch to vaterite formation had been made), or 'aragonite' if they were not. Vaterite prevalence was defined as the proportion of vaterite otoliths in each replicate tank.…”

“…A deformity in which the aragonite is replaced by vaterite crystals is abnormal in the wild, occurring in 1-24% of otoliths. However, it is extremely common in farmed fish, with on average a 3.7 times higher prevalence than in their wild counterparts and, in the most recent study, affecting 100% of harvest-size farmed Norwegian salmon (Reimer et al, 2016). Vaterite formation is irreversible once begun, and vaterite replacement results in otoliths which are larger, lighter, more brittle and less regularly shaped than their aragonite counterparts.…”

“…Previous attempts to induce vaterite formation by temporarily exposing juvenile fish to different temperatures for short periods of time were unsuccessful (Gauldie, 1996), and there is no correlation between vaterite prevalence and fish sex or early maturation rates (Sweeting et al, 2004), or the prevalence of other skeletal deformities (Tomás and Geffen, 2003). The recent discovery of marked differences in prevalence between wild and farm-reared fish suggests that the cause(s) of vaterite formation is a consistent difference between these two groups or the environments they experience (Reimer et al, 2016).…”

“…As >50% of farmed fish have ∼50% loss in hearing sensitivity due to vaterite (Reimer et al, 2016), pinpointing the cause of this deformity could drive measures to improve the welfare of billions of farmed fish worldwide. Furthermore, over 100 countries release hatchery-raised fish for restocking wild fisheries (sea ranching or supportive breeding).…”

“…Vaterite formation is irreversible once begun, and vaterite replacement results in otoliths which are larger, lighter, more brittle and less regularly shaped than their aragonite counterparts. Because of these differences, replacement of aragonite by vaterite probably causes severe hearing loss by reducing otolith function, potentially impacting fish welfare and restocking efficiency (Reimer et al, 2016).…”