Physiological mechanisms underlying individual variation in tolerance of food deprivation in juvenile European sea bass, Dicentrarchus labrax

Abstract

Although food deprivation is a major ecological pressure in fishes, there is wide individual variation in tolerance of fasting, whose mechanistic bases are poorly understood. Two thousand individually tagged juvenile European sea bass were submitted to two 'fasting/feeding' cycles each comprising 3 weeks of food deprivation followed by 3 weeks of ad libitum feeding at 25°C. Rates of mass loss during the two fasting periods were averaged for each individual to calculate a population mean. Extreme fasting tolerant (FT) and sensitive (FS) phenotypes were identified that were at least one and a half standard deviations, on opposing sides, from this mean. Respirometry was used to investigate two main hypotheses: (1) tolerance of food deprivation reflects lower mass-corrected routine metabolic rate (RMR) in FT phenotypes when fasting, and (2) tolerance reflects differences in substrate utilisation; FT phenotypes use relatively less proteins as metabolic fuels during fasting, measured as their ammonia quotient (AQ), the simultaneous ratio of ammonia excretion to RMR. There was no difference in mean RMR between FT and FS over 7 days fasting, being 6.70±0.24 mmol h −1 fish −1 (mean ± s.e.m., N=18) versus 6.76±0.22 mmol h −1 fish −1 (N=17), respectively, when corrected to a body mass of 130 g. For any given RMR, however, the FT lost mass at a significantly lower rate than FS, overall 7-day average being 0.72±0.05 versus 0.90±0.05 g day −1 fish −1 , respectively (P<0.01, ttest). At 20 h after receiving a ration equivalent to 2% body mass as food pellets, ammonia excretion and simultaneous RMR were elevated and similar in FT and FS, with AQs of 0.105±0.009 and 0.089±0.007, respectively. At the end of the period of fasting, ammonia excretion and RMR had fallen in both phenotypes, but AQ was significantly lower in FT than FS, being 0.038±0.004 versus 0.061±0.005, respectively (P<0.001, t-test). There was a direct linear relationship between individual fasted AQ and rate of mass loss, with FT and FS individuals distributed at opposing lower and upper extremities, respectively. Thus the difference between the phenotypes in their tolerance of food deprivation did not depend upon their routine energy use when fasting. Rather, it depended RESEARCH ARTICLE 1 UMR5119, Ecologie des systèmes marins côtiers (ECOSYM), Place Eugène Bataillon, Université Montpellier 2, 34095 Montpellier Cedex 5, France. upon their relative use of tissue proteins as metabolic fuels when fasting, which was significantly lower in FT phenotypes.

An early-life hypoxia event has a long-term impact on protein digestion and growth in European sea bass juvenile

“…More recently, McKenzie et al (2014), working on fish exhibiting the same phenotype as those of Dupont-Prinet et al (2010), revealed that the difference in fasting tolerance did not depend on the routine energy expenditure during fasting; rather, it relied on a lower use of proteins as metabolic fuel, particularly during fasting. Vanderplancke et al (2015b) showed that in sea bass juveniles that experienced the same moderate hypoxia at the larval stage as in the present experiment, the growth reduction was not due to a lower feed ingestion, and was associated with a metabolic depression.…”

Corrigendum to “Unpredictability in food supply during early life influences growth and boldness in European seabass, Dicentrarchus labrax” [Appl. Anim. Behav. Sci. 180 (July) (2016) 147–156]

“…In the present study, inter-strain differences only appeared during the second session, when the fish were older, with FD+ fish first passing into the normoxic tank at a higher oxygen level during the second session than during the first session, in contrast with FD-fish, which behaved similarly during both sessions. Because FD+ fish are less tolerant to feed deprivation, they may be more affected by the unpredictability of food supply, leading to an energetic trade off, herein a faster escape of low oxygen conditions (leading to an higher risk taking behavior), although the RMR of these strains are similar (McKenzie et al, 2014).…”

Plasma osmolality and oxygen consumption of perch Perca fluviatilis in response to different salinities and temperatures

“…The fasting period allowed the fish, particularly at 5° C, to be post‐prandial. Three weeks of fasting at the higher temperatures should not cause physiological impairment (Killen et al ., ; McKenzie et al ., ) and while routine metabolic rate can be affected by fasting period, SMR remains constant after digestion has ended, regardless of temperature (Beamish, ). O 2 was measured in trials lasting c .…”