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Interindividual plasticity in metabolic and thermal tolerance traits from populations subjected to recent anthropogenic heating

Citation

Drown, Melissa et al. (2021), Interindividual plasticity in metabolic and thermal tolerance traits from populations subjected to recent anthropogenic heating, Dryad, Dataset, https://doi.org/10.5061/dryad.0gb5mkm0w

Abstract

To better understand temperature’s role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus populations from different thermal environments. F. heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographic cline. In this study, we focus on three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12°C or 28°C, we quantified whole animal metabolic rate (WAM), critical thermal maximum (CTMax) and substrate specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous [i.e., no added substrates]) in ~160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within each population and variation in acclimation response within any single trait. In general, for WAM and CTMax the interindividual variation in acclimation response (log2 ratio 28°C/12°C) was a function of performance at 12°C with greater acclimation response for individuals that had lower 12°C performance. In contrast, for CaM the rates when acclimated and assayed at 12°C or 28°C were nearly identical. The small differences in CaM between 12°C and 28°C temperature were partially explained by cardiac remodeling where individuals acclimated to 12°C had larger hearts than individuals acclimated to 28°C, resulting in a higher CaM rate per unit heart mass at 28°C than 12°C. Correlation among physiological traits were dependent on acclimation temperature. For example, WAM was negatively correlated with CTMax at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher cardiac metabolism than fatty acid, and fatty acid supported higher cardiac metabolism than LKA or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These data suggest a complex relationship between specific, temperature-dependent physiological traits. 

Methods

Whole animal metabolism, substrate specific cardiac metabolic rate and critical thermal maximum were measured in individuals from three wild caught Fundulus heteroclitus populations. All traits were measured after individuals were common gardened at 20°C and 15ppt salinity for 6 weeks then overwintered at 10°C and 15ppt salinity for 4 weeks. Individuals were then acclimated to 12°C or 28°C and 15ppt salinity for 4 weeks and whole animal metabolism was measured followed by critical thermal maximum one week later. Individuals were then acclimated to the opposite temperature (12°C to 28°C or 28°C to 12°C) for 4 weeks before repeating trait measures in the following order: whole animal metabolism, critical thermal maximum, substrate specific cardiac metabolic rate. All traits were measured at the acclimation temperature. Whole animal metabolic rate was measured using intermittent flow respirometry. Critical thermal maximum was measured by placing fish in a 10 gallon aquarium with fully oxygenated 15ppt seawater at the acclimation temperature. Water was slowly heated (0.3°C per minute) using a submersible heating coil. Critical thermal maximum was defined as the temperature at which the individual exhibited no coordinated movement for 5 consequtive seconds. Cardiac metabolic rate was measured with four substrates: glucose, fatty acids, lactate with ketones and ethanol, and endogenous (i.e., no added substrate). To measure cardiac metabolic rate, heart ventricles were dissected, splayed in ringer's media with hepes, and placed in 1mL chambers with the desired substrate to measure oxygen consumption over time. Processed data (multiple replicate measures of oxygen consumption over time averaged for a single individual) for whole animal metabolic rate and substrate specific cardiac metabolic rate are provided here. Raw critical thermal maximum data in °C are also provided. Metadata includes population, acclimation temperature, acclimation order (12°C first or 28°C first acclimation), habitat temperature, body mass (at time of whole animal and cardiac metabolic rate), heart mass, date of data collection, and sex for all individuals. Mass corrected metabolic rates (log10 regression with body mass for whole animal and regression with body mass for cardiac metabolic rate) are also included in the data set.

Usage Notes

Please reference the "Notes" tab of the data file for descriptions of abbreviations used, units for trait measures, and important information about metadata columns and missing data.

Funding

National Science Foundation, Award: 1556396

National Science Foundation, Award: 1754437