An unusually high upper thermal acclimation potential for rainbow trout

Abstract

Thermal acclimation, a compensatory physiological response, is central to species survival especially during the current era of global warming. By providing the most comprehensive assessment to date for the cardiorespiratory phenotype of rainbow trout (Oncorhynchus mykiss) at six acclimation temperatures from 15°C to 25°C, we tested the hypothesis that, compared with other strains of rainbow trout, an Australian H-strain of rainbow trout has been selectively inbred to have an unusually high and broad thermal acclimation potential. Using a field setting at the breeding hatchery in Western Australia, thermal performance curves were generated for a warm-adapted H-strain by measuring growth, feed conversion efficiency, specific dynamic action, whole-animal oxygen uptake (ṀO₂) during normoxia and hypoxia, the critical maximum temperature and the electrocardiographic response to acute warming. Appreciable growth and aerobic capacity were possible up to 23°C. However, growth fell off drastically at 25°C in concert with increases in the time required to digest a meal, its total oxygen cost and its peak ṀO₂. The upper thermal tipping points for appetite and food conversion efficiency corresponded with a decrease in the ability to increase heart rate during warming and an increase in the cost to digest a meal. Also, comparison of upper thermal tipping points provides compelling evidence that limitations to increasing heart rate during acute warming occurred well below the critical thermal maximum (CT_max) and that the faltering ability of the heart to deliver oxygen at different acclimation temperatures is not reliably predicted by CT_max for the H-strain of rainbow trout. We, therefore, reasoned the remarkably high thermal acclimation potential revealed here for the Australian H-strain of rainbow trout reflected the existing genetic variation within the founder Californian population, which was then subjected to selective inbreeding in association with severe heat challenges. This is an encouraging discovery for those with conservation concerns for rainbow trout and other fish species. Indeed, those trying to predict the impact of global warming should more fully consider the possibility that the standing intra-specific genetic variation within a fish species could provide a high thermal acclimation potential, similar to that shown here for rainbow trout.

Keywords: aerobic capacity; digestion; growth; heart rate; hypoxia; standing variation.

Figure 1

Mass, length, average daily feed, food conversion ratio (FCR), specific dynamic action (SDA) duration and peak SDA, standard metabolic rate (SMR) and net peak SDA values for PFRC H-strain rainbow trout (O. mykiss). (A) Body mass (g), (B) fish length (mm) and (C) average daily feed ration (total per tank and averaged to number of rainbow trout in tank and per day) for each temperature acclimation group held in triplicate tanks (n = 3) and measured at weeks 0, 2 and 4. (D) FCR of rainbow trout as function of acclimation temperature (n = 3). (E) Peak SDA, measured as the highest oxygen uptake rate (ṀO2) value following feeding, SMR, measured as ṀO2 and net peak SDA measured as the difference between peak SDA and SMR, all presented as a function of acclimation temperature (n = 12–16). (F) SDA duration measured as a function of acclimation temperature (n = 12–16). Data points not sharing letters indicate significant differences between acclimation groups for that week. Asterisk indicates significant differences of all acclimation groups between two consecutive sampling time points. All values are presented as means ± sem. Mass, length and feed were assessed using a linear mixed effects model while FCR, SDA duration, peak SDA, SMR and net peak SDA were assessed using a one-way ANOVA with Tukey’s post-hoc tests.

Figure 2

Standard metabolic rate (SMR), maximum oxygen uptake (ṀO_2max), absolute aerobic scope (AAS) and factorial aerobic scope (FAS) of PFRC H-strain rainbow trout (O. mykiss) as a function of acclimation temperature. (A) SMR, ṀO_2max and AAS (difference between ṀO_2max and SMR) as a function of acclimation temperature (n = 12–16). SMR (blue square) was fitted with a polynomial quadratic function and one-way ANOVA (Y = 135.0 + 10.5^*X + 1.35^*X², R² = 0.67, F = 31.14, P < 0.0001), ṀO_2max (red circle) and AAS (green triangle) were fit with a Gaussian distribution curve and one-way ANOVA (Y = 760.2^*exp(−0.5^*((X-19.6)/9.89)2), R² = 0.22, F = 4.91, P = 0.0006; Y = 634.7^*exp(−0.5^*((X-18.6)/7.37)2), R² = 0.42, F = 15.40, P < 0.0001). ṀO_2max and SMR values were corrected to mean body mass of acclimation group, presented per unit kg. (B) Factorial of ṀO_2max/SMR (FAS) and peak SDA/SMR (n = 12–16). FAS (green circle) was fitted with a Gaussian distribution curve and one-way ANOVA (Y = 1.9^*exp(−0.5^*((X-2.0)/1.7)2), R² = 0.73, F = 43.41, P < 0.0001). (C) Critical oxygen level to maintain SMR (P_crit or C_crit) and oxygen level when fish is loss of whole animal equilibrium (ILOP or ILOC), as a function of acclimation temperature. P_crit (or C_crit) and ILOP (or ILOC) are presented as both water PO₂ (mm Hg; left y-axis) and dissolved oxygen concentration (mg O₂ l^-1; right y-axis). Curve was fit with polynomial quadratic function and one-way ANOVA (Pcrit: Y = 26.3 + 1.60^*X + 0.19^*X²), R² = 0.57, F = 22.19, P < 0.0001; Ccrit: Y = 1.54 + 0.062^*X + 0.0095^*X²), R² = 0.40, F = 11.58, P < 0.0001; ILOP: Y = 23.3 + 0.80^*X + 0.061^*X²), R² = 0.28, F = 6.41, P < 0.0001; ILOC: Y = 1.37+ 0.021^*X + 0.0031^*X²), R² = 0.57, F = 1.91, P = 0.10, (n = 12–16). Data points not sharing letters indicate significant differences between acclimation groups for that variable. All values are presented as mean ± sem and were assessed using a one-way ANOVA with Tukey’s post-hoc (α = 0.05).

Figure 3

Maximum heart rate (f_Hmax) and critical thermal maximum (CT_max) in response to acute warming of PFRC H-strain rainbow trout (O. mykiss) as a function of acclimation temperature. (A) Mean f_Hmax for each acclimation temperature group during acute warming (n = 12). Acclimation temperatures were 15°C (), 17°C (), 19°C (), 21°C (), 23°C () and 25°C (). Data points are connected by a solid line provided all fish in an acclimation group retained a rhythmic heartbeat at that temperature. If not a broken line connects the average f_Hmax for the fish the still retained a rhythmic heartbeat, with the percentage count remaining indicated in the inset. All individual fish had developed an arrhythmic heartbeat by 31°C and by 28°C for those at the two coldest acclimation temperatures. (B) Temperature at which each acclimation group reached its CT_max (n = 10), cardiac arrhythmia temperature (T_arr) and maximum f_Hmax (T_peak). Amber area labels the difference between whole-organism and tissue thermal tolerance and the differences between CT_max and T_arr at 15°C, 23°C and 25°C acclimation temperature are denoted. Two-way ANOVA performed indicates T_arr is significantly different from CT_max (F = 213.2, P < 0.0001). (C) Peak f_Hmax reached at each acclimation temperature (n = 12). All values are presented as means ± sem, except right y-axis in (A) presented as count in %. (sem may be hidden by the symbol). Dissimilar letters represent statistically significant differences among mean values for that variable.

Figure 4

Maximum oxygen uptake (ṀO_2max), absolute aerobic scope (AAS) and factorial aerobic scope (FAS) as a function of acclimation temperature. The data are synthesized from literature for geographically distant rainbow trout (O. mykiss) strains. ṀO_2max; (A), AAS (B) and FAS (C) over a range of testing temperatures in various studies on rainbow trout (O. mykiss) strains. The data are presented in either Gaussian or linear regressions models as mean ± 95% C.I. Figure legends state the acclimation temperature, body mass, location, strains, original studies and whether standard metabolic rate (SMR) or resting metabolic rate (RMR) are measured. The studies had different mass, testing protocols and analytical techniques, as well as acclimation temperatures (indicated), but not all of the differences in the curves can be attributed to these. A red vertical dash line marks 18°C as the 7-day average of the daily maxima criterion for the management of rainbow trout habitat in the Pacific Northwest (U.S. Environmental Protection Agency, 2003). Rainbow trout (O. mykiss) and redband trout (O. mykiss gairdneri) are in blue and green, respectively, where the aerobic capacity thermal performance curves are measured by acute exposure. The performance curves measured by the previous acclimation study are in orange, and the data of the present acclimation study are in red. Patterns of lines differentiate the strains. The range of the curve is constrained by testing temperature ranges. This is modified from McKenzie et al. (2021) by adding data from Dickson and Kramer (1971; a 95% CI for FAS was unavailable) and excluding data from Poletto et al. (2017).