Temporal profiles of cortisol accumulation and clearance support scale cortisol content as an indicator of chronic stress in fish

Abstract

The development of chronic stress indicators for fish is of great interest, but appropriate non-invasive methods are lagging those used in terrestrial vertebrates. Here, we explore the possibility that levels of the stress hormone cortisol in scales could be used as a chronic stress indicator. Three experiments were conducted to assess the temporal profiles of cortisol rise and fall in plasma and scales of goldfish (Carassius auratus) in response to stressors of varying intensity and duration. Results show that a single acute air emersion stressor does not influence scale cortisol content. In contrast, relative to plasma levels, the fall in scale cortisol content following a high-dose cortisol implant is delayed by at least 8 days, and the rise and fall in scale cortisol content in response to unpredictable chronic stress are delayed by at least 7 days. Also, scale cortisol content is spatially heterogeneous across the body surface of goldfish. Overall, since high and sustained circulating cortisol levels are needed to influence scale cortisol content and the rates of cortisol accumulation and clearance are much slower in scales than in plasma, our results show that scales can provide an integrated measure of cortisol production and serve as a chronic stress indicator.

Measuring cortisol in fish scales to study stress in wild tropical tuna

“…According to the sampling size of this study, neither the size:species interactions nor the size:location interactions were found to be significant (p = 0.5 & 0.6, respectively). Cortisol in scales has been proven to be an effective marker of chronic stress in various fish species (Aerts et al 2015;Carbajal et al 2019;Laberge et al 2019;Hanke et al 2020). Yet, the mechanisms of cortisol clearance in scales are not well described, and to our knowledge, only one recent study on goldfish (Carassius auratus) has provided insights regarding its rate (Laberge et al 2019).…”

“…Recently, new matrices have emerged to measure cortisol; these are being used as relatively non-invasive markers of stress (Sadoul and Geffroy 2019). Among these markers, fish scales are the most promising matrix as they provide a record of the integrated stress response over time (i.e., from weeks to months, Aerts et al 2015) and a grid to highlight behavioral ecology regarding exposure to stress factors such as temperature (Goikoetxea et al 2020), since the metabolic clearance rate in scales is much slower than in plasma (Laberge et al 2019). Previous studies have shown that intra-specific differences in basal cortisol are genetically driven (Øverli et al 2002a) and are generally aligned with differences in behavior or coping style, in which reactive individuals display higher basal cortisol levels compared to proactive individuals (Koolhaas et al 1999).…”

What are you actually measuring? A review of techniques that integrate the stress response on distinct time‐scales

“…These scales are calcified external structures that grow as the fish grows, and when they are removed, they regrow within days (Metz, de Vrieze, Lock, Schulten, & Flik, 2012). Cort is detectable in these scales and is sensitive to seasonal variation, habitat quality, and repeated stressors (Aerts et al., 2015; Carbajal et al., 2019; Laberge, Yin‐liao, & Bernier, 2019; Table S1). In sum, the growth rate of scales suggests a response latency of days with scale Cort sensitive to stressors lasting days‐to‐months (Figure 1).…”

Analysis of stress responses in Astyanax larvae reveals heterogeneity among different populations

“…The zebrafish, Danio rerio, and a number of other teleost species, have emerged as powerful models for addressing neuronal and genetic principles underlying the regulation of stress (Cachat et al, 2010;Laberge, Yin-Liao, & Bernier, 2019;Maximino et al, 2010Maximino et al, , 2014Sakamoto, Yoshiki, & Sakamoto, 2017;Schreck, Tort, Farrell, & Brauner, 2016). Studying stress in fish not only has implications in aquaculture and farming (Sneddon, Wolfenden, & Thomson, 2016), but the principles, neuronal circuitry, and neuroendocrine systems that modulate these behaviors are largely analogous with mammalian systems (Biran, Tahor, Wircer, & Levkowitz, 2015;Mueller, Dong, Berberoglu, & Guo, 2011).…”