Effects of incubation temperature on survival, growth, morphology, and gene expression of artificially reared cisco (Coregonus artedi): implications for best practices for captive propagation and restoration

Andrew Honsey (USGS, ahonsey@usgs.gov), Travor Krabbenhoft (University at Buffalo), Amanda Ackiss (USGS), Roger Gordan (USFWS), Jose Bonilla-Gomez (USFWS), Kevin McDonnell (USFWS), Marc Chalupnicki (USGS), Gregg Mackey (USGWS), Brian O'Malley (USGS), Alex Gatch (USGS), Christopher Osborne (USFWS)

A key tool for Great Lakes coregonine restoration is reintroduction via fish stocking. Stocking programs are currently underway, including efforts to restore cisco Coregonus artedi in Saginaw Bay, Lake Huron (Lake Huron Technical Committee 2007; Riley and Ebener 2020) and bloater C. hoyi in Lake Ontario (Weidel et al. 2022). One critical challenge for coregonine reintroduction efforts is producing hatchery fish that are phenotypically and ecologically suitable for the environments into which they are stocked, and/or for meeting restoration objectives. Unfortunately, captive rearing often results in hatchery fish that are notably different from wild fish. For example, hatchery-reared individuals often differ in morphology compared to wild fish (Honsey et al. in review), and, in at least one case, gill raker morphologies can vary dramatically between wild and artificially reared fish (Fig. 1). Developmental abnormalities in ciscoes and other coregonines raised in captivity are likely to have negative impacts on survival and fitness in the wild, especially when they are severe. For example, deformities in gill rakers or mouth parts likely impact feeding efficiency, and pugheadedness (a deformity commonly seen in artificially reared coregonines) can reduce fitness (Näslund and Jawad 2022). Minimizing the differences between wild and hatchery fish may help to achieve fishery management goals. Gene expression data can inform the specific types of stress driving these phenotypic abnormalities, such as physical trauma, temperature effects, light, dietary issues, etc., by showing the specific types of genes that respond to different incubation and/or rearing conditions. A pilot gene expression study by Krabbenhoft and Stott showed that ciscoes reared at different temperatures at Great Lakes Science Center had dramatically different amounts of gene expression of cold-inducible binding protein, a gene that controls the physiological response to temperature-driven problems with protein folding in vertebrates. This result indicates that ciscoes reared at relatively high temperatures have difficulties controlling the three-dimensional structure of proteins, which likely leads to phenotypic abnormalities that may impact survival and fitness. When misfolded proteins form in fish cells, they build up in special cellular compartments called ‘stress granules’, and the formation of these granules can be visualized with specialized microscopy. Thus, gene expression and microscopy can provide quantitative data in early ontogenetic stages on phenotypic abnormalities that occur later in development. Understanding the physiological mechanisms that drive these developmental problems provides a clear path to mitigating them through optimizing hatchery conditions. We propose to augment our understanding of the impacts of environmental factors in early life on artificially reared cisco. Specifically, we will investigate the impacts of varying egg incubation temperatures on cisco survival, growth, morphology, and gene expression. This work will complement previous research on early life temperature effects on coregonines (e.g., Price 1940; Colby and Brooke 1970; Brooke 1975; Luczynski and Kirklewska 1984; Malzahn et al. 2003; Cingi et al. 2010; Eme et al. 2015; Mueller et al. 2015; Mitz et al. 2019; Stewart et al. 2021) and will provide a more thorough and mechanistic understanding of the impacts of temperature on coregonine development and resultant fitness. Results from this work can inform hatchery rearing protocols, stocking regimes, and reintroduction planning basin-wide. The decision to vary temperature during egg incubation was made in close consultation with Roger Gordon, an expert in coregonine rearing with FWS.