Abstract
ABSTRACTBottlenose dolphins (Tursiops truncatus) typically feed on prey that are high in lipid and protein content and nearly devoid of carbohydrate, a dietary feature shared with other marine mammals. However, unlike fasted-adapted marine mammals that predictably incorporate fasting into their life history, dolphins feed intermittently throughout the day and are not believed to be fasting-adapted. To assess whether the physiological response to fasting in the dolphin shares features with or distinguishes them from those of fasting-adapted marine mammals, the plasma metabolomes of eight bottlenose dolphins were compared between post-absorptive and 24-h fasted states. Increases in most identified free fatty acids and lipid metabolites and reductions in most amino acids and their metabolites were consistent with the upregulation of lipolysis and lipid oxidation and the downregulation of protein catabolism and synthesis. Consistent with a previously hypothesized diabetic-like fasting state, fasting was associated with elevated glucose and patterns of certain metabolites (e.g. citrate, cis-aconitate, myristoleic acid) indicative of lipid synthesis and glucose cycling to protect endogenous glucose from oxidative disposal. Pathway analysis predicted an upregulation of cytokines, decreased cell growth and increased apoptosis including apoptosis of insulin-secreting β-cells. Metabolomic conditional mutual information networks were estimated for the post-absorptive and fasted states and ‘topological modules’ were estimated for each using the eigenvector approach to modularity network division. A dynamic network marker indicative of a physiological shift toward a negative energy state was subsequently identified that has the potential conservation application of assessing energy state balance in at-risk wild dolphins.
Highlights
The physiological response to food deprivation in mammals is characterized by changing substrate utilization to maintain energy demands and is commonly divided into three phases (Castellini and Rea, 1992; McCue, 2010; Wang et al, 2006)
The two principal components of the discriminant function, which explained respectively 52% and 10% of the variance in metabolite intensity (Fig. 1A), were primarily associated with metabolites involved in amino acid and lipid metabolism (Fig. 2)
Metabolites associated with lipid metabolism increased in expression with the fasted profile while metabolites associated with amino acid metabolism decreased
Summary
The physiological response to food deprivation in mammals is characterized by changing substrate utilization to maintain energy demands and is commonly divided into three phases (Castellini and Rea, 1992; McCue, 2010; Wang et al, 2006). Received 6 October 2020; Accepted 18 March 2021 fasting varies by species but starts immediately after the animal is post-absorptive from its last meal and lasts typically no longer than several days This phase is characterized by a depletion of available glucose reserves (e.g. glycogen stores), a gradual reduction in the resting metabolic rate, and transition to lipid as the prime fuel substrate. It has been hypothesized that phocid seals are pre-adapted to a fasting state because their prey are high in fat and protein and lack significant carbohydrate, i.e. the gross utilization of fuel substrates is similar between feeding and fasting states (Houser et al, 2007; Houser and Costa, 2001; Kirby and Ortiz, 1994). We conclude with insight on how techniques utilized in this study might be applied to conservation purposes in wild dolphins through identification of whether individuals are sampled (e.g. remote biopsy) while in a negative energy state
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