Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla)

Abstract

In late summer, semipalmated sandpipers (Calidris pusilla) migrate nonstop from eastern Canada to wintering sites on the northwest coast of South America. Before their transoceanic flight, the birds feed intensively for about 15 days during which time lipids are stored. The fat-free dry mass of the pectoralis muscle increases during the fattening period, probably increasing the maximal power output of the muscle. Plasma free fatty acids and triglycerides, pectoralis muscle lipid content, and the activity of carnitine oleoyl coenzyme A transferase are higher in heavy (fat) than in light (lean) birds. These alterations imply an enhanced capacity to utilize fatty acids as a metabolic fuel during migration. Total pectoralis muscle glycogen levels and the activity of pyruvate kinase increase, suggesting a higher capacity for glycogenolysis, which may be important during intense levels of energy demand. Heart size and protein content per gram of tissue increase in association with an increase in body mass. However, total levels of key mitochondrial enzymes, citrate synthase and carnitine oleoyl coenzyme A transferase, do not change, suggesting that in the heart an increase in total protein content occurs without an increase in mitochondrial proteins.

Body condition and physiological changes in male green turtles during breeding

“…Given that testosterone is a key anabolic steroid capable of causing hypertrophy of skeletal muscle, this hormone could be involved in pre-migratory body changes that lead to increased pectoral and shoulder muscle mass that facilitates swimming activities during 286 Jessop et al: Breeding in male green turtles migration and reproduction. Before migration, several bird species enlarge their pectoral muscles to increase flight performance (Fry et al 1972, Driedzic et al 1993, Dietz et al 1999. The decreased body condition and elevated plasma protein levels found during the later phases of the breeding period, associated with declining levels of plasma testosterone, may indicate that reduced testosterone levels facilitate catabolism of muscle to provide energy at the later stage of the migratory breeding period.…”

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

“…Thus, if a flying bird exercises at nearly 80% VȮ 2,max , then the mammal crossover model would predict that only 5-10% of its energy would come from the oxidation of fatty acids delivered from adipose tissue to muscles through the circulation; however, the value is closer to 90% (Guglielmo, 2010). Flight muscles of migratory birds have very high activities of mitochondrial enzymes involved in fatty acid oxidation, such as hydroxyacyl-CoAdehydrogenase (HOAD) and carnitine palmitoyltransferase (CPT), that are greater in more migratory species (Lundgren and Kiessling, 1985), increase during migration seasons (Banerjee and Chaturvedi, 2016;Guglielmo et al, 2002a;Kiessling, 1985, 1986;Marsh, 1981;McFarlan et al, 2009;Zajac et al, 2011), and may increase at stopovers as birds refuel and prepare to depart (Driedzic et al, 1993;Maillet and Weber, 2007). However, increasing the mitochondrial fatty acid oxidation potential alone does not solve the problem with using adipose-derived fatty acids as fuel because the limitation in mammals appears to be due to constraints on transport through the circulation and uptake and transport of fatty acids by myocytes (Guglielmo, 2010;Vock et al, 1996).…”

“…2), the aerobic capacity of muscles and supporting systems must increase. This can be achieved in migratory birds by increasing flight muscle mass (Bauchinger et al, 2005;Guglielmo and Williams, 2003;Marsh, 1984;Piersma and van Gils, 2011), capillarity (Lundgren and Kiessling, 1988), mitochondrial volume (Evans et al, 1992), heart size (Bauchinger et al, 2005;Guglielmo and Williams, 2003;Piersma and van Gils, 2011), hematocrit (Piersma and Everaarts, 1996;Wingfield et al, 1990) and activities of the citric acid cycle and electron transport chain enzymes, such as citrate synthase (CS), malate dehydrogenase (MDH) or cytochrome oxidase (COX; Banerjee and Chaturvedi, 2016;DeMoranville, 2015;Dick, 2017;Driedzic et al, 1993;Guglielmo et al, 2002a;Kiessling, 1985, 1986;Maillet and Weber, 2007;Marsh, 1981;McFarlan et al, 2009;Zajac et al, 2011), and by decreasing anaerobic potential as indicated by muscle lactate dehydrogenase (LDH) activity (Banerjee and Chaturvedi, 2016;Dick, 2017;McFarlan et al, 2009;Zajac et al, 2011). Similarly, hoary bats were found to increase pectoralis muscle CS activity, shift lean body composition toward exerciserelated organs and have significantly larger lungs during migration (McGuire et al, 2013a,b).…”

“…Fat is the preferred fuel for migration because the highly reduced nature and hydrophobicity of fatty acids result in fat providing approximately eight times more energy per unit wet mass (∼37 kJ g −1 ) than carbohydrates or protein (∼4-5 kJ g −1 ; Blem, 1990;Jenni and Jenni-Eiermann, 1998). Although glucose from muscle and liver glycogen is important for burst flight to escape predators and may be important early in migratory flight while fatty acid mobilization is being induced (Gerson and Guglielmo, 2013), glycogen stores of migrant birds (ranging from ∼3-20 mg g −1 wet depending on the time of day) are too small to meaningfully contribute to multi-hour or multi-day flights (Banerjee and Chaturvedi, 2016;Blem, 1990;Driedzic et al, 1993;Marsh, 1983). For example, using a total pectoralis glycogen content of 34 mg (∼600 J) of departure-ready semipalmated sandpipers (Calidris pusilla; Driedzic et al, 1993) and a measured flight cost of ∼2.6 W for similarly sized western sandpipers (Calidris mauri; Maggini et al, 2017b) we can calculate that muscle glycogen would power flight for less than five minutes.…”

“…Although glucose from muscle and liver glycogen is important for burst flight to escape predators and may be important early in migratory flight while fatty acid mobilization is being induced (Gerson and Guglielmo, 2013), glycogen stores of migrant birds (ranging from ∼3-20 mg g −1 wet depending on the time of day) are too small to meaningfully contribute to multi-hour or multi-day flights (Banerjee and Chaturvedi, 2016;Blem, 1990;Driedzic et al, 1993;Marsh, 1983). For example, using a total pectoralis glycogen content of 34 mg (∼600 J) of departure-ready semipalmated sandpipers (Calidris pusilla; Driedzic et al, 1993) and a measured flight cost of ∼2.6 W for similarly sized western sandpipers (Calidris mauri; Maggini et al, 2017b) we can calculate that muscle glycogen would power flight for less than five minutes. Marsh (1983) reported up to threefold greater pectoralis glycogen concentrations in gray catbird (Dumetella carolinensis) than in sandpipers, and high liver glycogen levels, yet these stores would still only meet flight energy demands for a short period.…”