Effects of flight on blood parameters in homing pigeons

SUMMARYOne cellular mechanism thought to be particularly important as a constraint on lifespan and life-history strategies is oxidative stress. Susceptibility to oxidative stress is influenced by a number of antioxidant defences, whose effectiveness depends on the synergistic and competitive interactions among them (biochemical integration). It is generally assumed that exposure to oxidative stress is detrimental, but it is also possible that low level oxidative stress has a positive effect on integration, and therefore carries some benefits. Using three experimental groups of zebra finches (control, mild and high flight activity), we tested whether exercise-induced oxidative stress altered the integration of the pro-oxidant/antioxidant system by manipulating levels of flight activity, known to generate oxidative stress in birds. We show for the first time that a short-term high level of physical activity leads to a reduction in integration among components of the blood antioxidant defences, associated with a reduced resistance to oxidative stress. We found no evidence of improved integration in the antioxidant defences at low levels of oxidative stress exposure, suggesting that improved integration is not the route whereby any benefits of low level stress exposure occur. These findings point to a reduction in biochemical integration as a potential mechanism explaining a reduced resistance to oxidative stress induced by short-term stressors. Supplementary material available online at

Section: Discussionmentioning

confidence: 99%

Loss of integration is associated with reduced resistance to oxidative stress

Costantini

Monaghan

Metcalfe

2013

“…Triacylglycerol tended to decrease and phospholipids decreased significantly in American robins (Turdus migratorius) flying for 18-55 min in a wind tunnel (Gerson and Guglielmo, 2013). Plasma triacylglycerol concentration either does not change or decreases in flying homing pigeons (Columba livia; Bordel and Haase, 1993;Schwilch et al, 1996). In red knots (Calidris canutus), plasma triacylglycerol decreased during the first hour and then remained stable for up to ten hours of wind tunnel flight, but was lower than time-matched fasting controls (JenniEiermann et al, 2002).…”

Section: Meeting the Challenge Of Fat-fueled Flightmentioning

confidence: 98%

“…The potential for lipoproteins to transport large amounts of lipids to muscles with a lesser osmotic challenge seems attractive and would make lipid transport of birds during exercise more similar to that of flying insects and some fish than mammals (Weber, 2009). However, although plasma NEFA generally increases during flight in birds (Bordel and Haase, 1993;Gerson and Guglielmo, 2013;Jenni-Eiermann et al, 2002;Schwilch et al, 1996), the lipoprotein pathway of fatty acid delivery has not been empirically replicated in birds flying under controlled conditions. Plasma triacylglycerol and phospholipids remained the same or decreased during flight wheel exercise lasting 30-45 min in redeyed vireos and yellow-rumped warblers (Guglielmo et al, 2017).…”

Section: Meeting the Challenge Of Fat-fueled Flightmentioning

confidence: 99%

Obese super athletes: fat-fueled migration in birds and bats

Guglielmo

2018

123

111

Migratory birds are physiologically specialized to accumulate massive fat stores (up to 50-60% of body mass), and to transport and oxidize fatty acids at very high rates to sustain flight for many hours or days. Target gene, protein and enzyme analyses and recent -omic studies of bird flight muscles confirm that high capacities for fatty acid uptake, cytosolic transport, and oxidation are consistent features that make fat-fueled migration possible. Augmented circulatory transport by lipoproteins is suggested by field data but has not been experimentally verified. Migratory bats have high aerobic capacity and fatty acid oxidation potential; however, endurance flight fueled by adipose-stored fat has not been demonstrated. Patterns of fattening and expression of muscle fatty acid transporters are inconsistent, and bats may partially fuel migratory flight with ingested nutrients. Changes in energy intake, digestive capacity, liver lipid metabolism and body temperature regulation may contribute to migratory fattening. Although control of appetite is similar in birds and mammals, neuroendocrine mechanisms regulating seasonal changes in fuel store set-points in migrants remain poorly understood. Triacylglycerol of birds and bats contains mostly 16 and 18 carbon fatty acids with variable amounts of 18:2n-6 and 18:3n-3 depending on diet. Unsaturation of fat converges near 70% during migration, and unsaturated fatty acids are preferentially mobilized and oxidized, making them good fuel. Twenty and 22 carbon n-3 and n-6 polyunsaturated fatty acids (PUFA) may affect membrane function and peroxisome proliferator-activated receptor signaling. However, evidence for dietary PUFA as doping agents in migratory birds is equivocal and requires further study.

“…Additionally, calculated estimates of the migratory energy requirements of red knots, which are shorebirds, indicate that fat provides 95% of the fuel supply during flight (Jenni and Jennie-Eiermann, 1998). Although pigeons exhibit minimal changes in blood glucose concentrations during flights lasting 2-10h (Bordel and Haase, 1993;Schwilch et al, 1996), mammalian dependence on carbohydrates at a similar relative intensity depletes body carbohydrate stores and precipitates fatigue, which coincides with low muscle glycogen and blood glucose (Ahlborg et al, 1974; Baldwin et al, 1973;Coyle, 1995;Fitts et al, 1975;Holloszy and Coyle, 1984;Wahren et al, 1971).Both training and diet have been shown to modulate fuel selection; however, these effects are modest compared with the apparent differences that exist between avians and mammals. At a given absolute workload, trained individuals exhibit lower respiratory exchange ratio (RER) values compared with untrained individuals; however, when matched for % V O2,max , the RER does not appear to be different during moderate and moderate-high intensity exercise (Bergman and Brooks, 1999;Hurley et al, 1986).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

Mitochondrial function in sparrow pectoralis muscle

Kuzmiak

Sweazea

Willis

2012

SUMMARYFlying birds couple a high daily energy turnover with double-digit millimolar blood glucose concentrations and insulin resistance. Unlike mammalian muscle, flight muscle predominantly relies on lipid oxidation during locomotion at high fractions of aerobic capacity, and birds outlive mammals of similar body mass by a factor of three or more. Despite these intriguing functional differences, few data are available comparing fuel oxidation and free radical production in avian and mammalian skeletal muscle mitochondria. Thus we isolated mitochondria from English sparrow pectoralis and rat mixed hindlimb muscles. Maximal O 2 consumption and net H 2 O 2 release were measured in the presence of several oxidative substrate combinations. Additionally, NADand FAD-linked electron transport chain (ETC) capacity was examined in sonicated mitochondria. Sparrow mitochondria oxidized palmitoyl-L-carnitine 1.9-fold faster than rat mitochondria and could not oxidize glycerol-3-phosphate, while both species oxidized pyruvate, glutamate and malate-aspartate shuttle substrates at similar rates. Net H 2 O 2 release was not significantly different between species and was highest when glycolytic substrates were oxidized. Sonicated sparrow mitochondria oxidized NADH and succinate over 1.8 times faster than rat mitochondria. The high ETC catalytic potential relative to matrix substrate dehydrogenases in sparrow mitochondria suggests a lower matrix redox potential is necessary to drive a given O 2 consumption rate. This may contribute to preferential reliance on lipid oxidation, which may result in lower in vivo reactive oxygen species production in birds compared with mammals.Key words: skeletal muscle mitochondria, substrate oxidation, aging, reactive oxygen species, bird. THE JOURNAL OF EXPERIMENTAL BIOLOGY 2040to complete substrate oxidation pathways would be coupled with lower superoxide production (measured as net H 2 O 2 release) in mitochondria from English sparrow (Passer domesticus) pectoralis compared with rat (Rattus norvegicus) mixed hindlimb muscle. Thus, one purpose of the present study was to measure the maximum (state 3) mitochondrial O 2 consumption rate (J . O2 ), ETC flux capacity in sonicated mitochondria from three sites of electron entry, and ROS production by intact 'resting' (oligomycin-inhibited) mitochondria. To our knowledge, no investigation into ROS production from avian muscle mitochondria currently exists.Fuel selection by contracting muscles during locomotion differs markedly between birds and mammals. Humans and rats run at 75% of their maximum rate of O 2 uptake (V O2,max ) with a respiratory quotient (RQ) at or above 0.90 (Brooks and Donovan, 1983;Brooks and Gaesser, 1980; O'Brien et al., 1993), which reflects a general pattern of carbohydrate dependence in mammals exercising at or above moderate intensity (Roberts et al., 1996). In contrast, pigeons fly at this intensity with an RQ of 0.73 (Rothe, 1987), indicating that pigeon flight muscle supports locomotion with the almost exclusive oxidatio...