Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout

Abstract

Stable isotopes can illuminate resource usage by organisms, but effective interpretation is predicated on laboratory validation. Here we develop stable isotope clocks to track resource shifts in anadromous rainbow trout (Oncorhynchus mykiss). We used a diet-switch experiment and model fitting to quantify N stable isotope (δ(15)N) turnover rates and discrimination factors for seven tissues: plasma, liver, fin, mucus, red blood cells, muscle, and scales. Among tissues, diet-tissue δ(15)N discrimination factors ranged from 1.3 to 3.4 ‰. Model-supported tissue turnover half-lives ranged from 9.0 (fin) to 27.7 (scale) days. We evaluated six tissue turnover models using Akaike's information criterion corrected for small sample sizes. The use of equilibrium tissue values was supported in all tissues and two-compartment models were supported in plasma, liver, and mucus. Using parameter estimates and their uncertainty we developed stable isotope clocks to estimate the time since resource shifts. Longer turnover tissues provided accurate estimates of time since resource switch for durations approximately twice their half-life. Faster turnover tissues provided even higher precision estimates, but only within their half-life post-switch. Averaging estimates of time since resource shift from multiple tissues provided the highest precision estimates of time since resource shift for the longest duration (up to 64 days). This study therefore provides insight into physiological processes that underpin stable isotope patterns, explicitly tests alternative models, and quantifies key parameters that are the foundation of field-based stable isotope analysis.

Tissue-specific turnover rates of the nitrogen stable isotope as functions of time and growth in a cyprinid fish

“…This strong influence of growth on isotopic turnover has also been reported for ectothermic animals more generally (e.g. MacAvoy et al, 2001;Perga & Gerdeaux, 2005;Heady & Moore, 2013) and is attributed to them having lower metabolic activities than endotherms (Bosley et al, 2002;Tominaga et al, 2003). Indeed, Perga and Gerdeaux (2005) suggested that as fish, and other ectotherms, have a discontinuous pattern of growth over the year, the stable isotope values of their muscle might only reflect their food consumed during periods of growth.…”

“…Where experimental studies have been completed on larger or older fishes, and those with lower specific growth rates, the results suggest that metabolic replacement contributes a major proportion of total turnover, in some cases accounting for 80% of isotopic change in dorsal muscle (Suzuki et al, 2005;Logan et al, 2006;Tarboush et al, 2006). Heady and Moore (2013) revealed that catabolism contributed more to 15 N turnover in tissues with faster turnover rates, contributing 68% for fin compared to 0.7% for scales. Experimental design, especially the temperature used, can also significantly impact turnover rates, with higher water temperatures reducing the half-lives of the carbon stable isotope of muscle in similar sized fish (Bosley et al, 2002;Witting et al, 2004).…”

“…Thus, tissue turnover differentiation, as well as the relative ordering of turnover rates among tissues, appears to be speciesspecific. For example, Heady and Moore (2013) calculated half-lives for muscle, fin and scales in rainbow trout Oncorhynchus mykiss (Walbaum, 1792) and found fin had the fastest isotopic half-life (13 days), followed by muscle (39 days) and scales (40 days). Whilst these O. mykiss turnover estimates are shorter than those produced here, the authors recognised that their turnover rates were fast, approximately 71% faster for muscle than previous estimates for O. mykiss from an isotope diet-switch study (Church et al, 2009).…”

“…McIntyre & Flecker, 2006;Church et al, 2009;Carleton & Del Rio, 2010). Rather than relying on data collected in the wild, an alternative approach is the use of experimental diet-switch studies completed in controlled conditions (Heady & Moore, 2013;Xia et al, 2013a, b;Busst & Britton, 2016). In these studies, diet tends to be fixed so that the food items have relatively consistent stable isotope values that should provide more reliable turnover estimates in the tissues (Logan et al, 2006).…”

“…In these studies, diet tends to be fixed so that the food items have relatively consistent stable isotope values that should provide more reliable turnover estimates in the tissues (Logan et al, 2006). These approaches should also provide enhanced understandings of the mechanisms involved in isotopic replacement (Buchheister & Latour, 2010;Heady & Moore, 2013). The data generated also favour the testing of different models to determine the best-fitting model that provides the best estimate of the turnover rate, and enable the relative contributions of growth and metabolism to turnover to be estimated (Fry & Arnold, 1982;Hobson & Clark, 1992;Hesslein et al, 1993).…”