The effects of dietary linoleic acid and hydrophilic antioxidants on basal, peak, and sustained metabolism in flight‐trained European starlings

Abstract

Dietary micronutrients have the ability to strongly influence animal physiology and ecology. For songbirds, dietary polyunsaturated fatty acids (PUFAs) and antioxidants are hypothesized to be particularly important micronutrients because of their influence on an individual's capacity for aerobic metabolism and recovery from extended bouts of exercise. However, the influence of specific fatty acids and hydrophilic antioxidants on whole‐animal performance remains largely untested. We used diet manipulations to directly test the effects of dietary PUFA, specifically linoleic acid (18:2n6), and anthocyanins, a hydrophilic antioxidant, on basal metabolic rate (BMR), peak metabolic rate (PMR), and rates of fat catabolism, lean catabolism, and energy expenditure during sustained flight in a wind tunnel in European starlings (Sturnus vulgaris). BMR, PMR, energy expenditure, and fat metabolism decreased and lean catabolism increased over the course of the experiment in birds fed a high (32%) 18:2n6 diet, while birds fed a low (13%) 18:2n6 diet exhibited the reverse pattern. Additionally, energy expenditure, fat catabolism, and flight duration were all subject to diet‐specific effects of whole‐body fat content. Dietary antioxidants and diet‐related differences in tissue fatty acid composition were not directly related to any measure of whole‐animal performance. Together, these results suggest that the effect of dietary 18:2n6 on performance was most likely the result of the signaling properties of 18:2n6. This implies that dietary PUFA influence the energetic capabilities of songbirds and could strongly influence songbird ecology, given their availability in terrestrial systems.

The energy savings-oxidative cost trade-off for migratory birds during endurance flight

“…less energy used per km) during endurance flights (6 hr, ca. 260 km) compared to birds composed of more MUFA, and a recent companion study ( Carter et al, 2020 ) suggests that this is because of the signaling properties of omega-6 PUFA.…”

“…Migratory distances for this population vary from many hundreds of kilometers to several thousand kilometers, with some individuals overwintering in the Euro-Mediterranean region and others in northwest Africa ( Bairlein, 2014 ). European starlings are also quite social and curious, and quickly learn to successfully fly together in a given windtunnel as demonstrated by several recent studies ( Carter et al, 2020 ; Casagrande et al, 2020 ). We conducted two complimentary experiments that involved feeding starlings over many months two diets that differed only in the relative amounts of mono- and polyunsaturated fats ( Table 1 ), specifically the amounts of omega-9 18:1 and omega-6 (18:2) and omega-3 (18:3) (no.…”

“…Fatty acid composition of the two semi-synthetic diets ( Table 2 ) was measured by gas chromatography in lipids extracted using a modified Folch method ( Carter et al, 2020 ) from composited subsamples of each diet taken over the course of the experiments. We collected adipose tissue from the visible fat stores in the furcular area of starlings used in Experiment I ( n = 29) 5–7 days after their longest flight in the windtunnel.…”

“…Dietary fat and furcular fat samples were stored at −80°C until fatty acid composition was measured by gas chromatography. We thawed samples, extracted total lipids using a modified Folch method ( Carter et al, 2020 ), and then the extracted lipids were esterified into fatty acid methyl esters (FAMEs) by heating at 70°C for 2 hr in 1M acetyl chloride in methanol. Duplicate 1 µL aliquots of sample FAMEs (I mg/mL in dichloromethane) were injected into a Shmadzu Scientific Instruments QP2010S GC-MS linked to a 2010 FID (Shmadzu Scientific Instruments, Kyoto, Japan) at Sacred Heart University (Fairfield, CT).…”

Migrant blackbirds, Turdus merula, have higher plasma levels of polyunsaturated fatty acids compared to residents, but not enhanced fatty acid unsaturation index

“…For example, red‐eyed vireos ( V. olivaceus ) and white‐throated sparrows ( Zonotrichia albicollis ) that were fed ω‐6 PUFAs had higher peak metabolic rates compared to birds fed MUFAs or ω‐3 PUFAs, respectively (Pierce et al., 2005; Price & Guglielmo, 2009). However in starlings ( Sturnus vulgaris ), birds provided a diet rich in ω‐6 PUFA (linoleic acid) decreased energy expenditure, fat metabolism, as well as basal and peak metabolism compared to birds that were fed a low ω‐6 PUFA diet (Carter, DeMoranville, Pierce, & McWilliams, 2020). It was suggested that the signaling property of linoleic acid is the mechanism behind this metabolic change (Carter et al., 2020).…”