Development of endothermy and concomitant increases in cardiac and skeletal muscle mitochondrial respiration in the precocial Pekin duck (Anas platyrhynchos domestica)

Abstract

Attaining endothermic homeothermy occurs at different times posthatching in birds and is associated with maturation of metabolic and aerobic capacity. Simultaneous measurements at the organism, organ and cellular levels during the transition to endothermy reveal means by which this change in phenotype occurs. We examined development of endothermy in precocial Pekin ducks (Anas platyrhynchos domestica) by measuring whole-animal O 2 consumption (V O2 ) as animals cooled from 35 to 15°C. We measured heart ventricle mass, an indicator of O 2 delivery capacity, and mitochondrial respiration in permeabilized skeletal and cardiac muscle to elucidate associated changes in mitochondrial capacities at the cellular level. We examined animals on day 24 of incubation through 7 days post-hatching. V O2 of embryos decreased when cooling from 35 to 15°C; V O2 of hatchlings, beginning on day 0 posthatching, increased during cooling with a lower critical temperature of 32°C. Yolk-free body mass did not change between internal pipping and hatching, but the heart and thigh skeletal muscle grew at faster rates than the rest of the body as the animals transitioned from an externally pipped paranate to a hatchling. Large changes in oxidative phosphorylation capacity occurred during ontogeny in both thigh muscles, the primary site of shivering, and cardiac ventricles. Thus, increased metabolic capacity necessary to attain endothermy was associated with augmented metabolic capacity of the tissue and augmented increasing O 2 delivery capacity, both of which were attained rapidly at hatching.

The 12-day thermoregulatory metamorphosis of Red-winged Blackbirds (Agelaius phoeniceus)

“…Both breast and thigh of Red-winged Blackbird exhibited a OXPHOS CI flux capacity (Fig. 4b) above the corresponding tissues in Pekin duck (Sirsat et al 2016a). Breast and thigh OXPHOS CI flux capacity of Red-winged Blackbird increased similarly through early development, then diverged after 7 dph, with thigh OXPHOS CI flux plateauing at a lower rate than breast.…”

“…As the pump of the cardiovascular system, the heart plays an important role in delivery of oxygen required for sufficient thermogenesis. Precocial Pekin duck hatchlings have a low fractional heart mass as embryos but then experience a rapid increase in fractional heart mass upon hatching and attainment of endothermic capacity (Sirsat et al 2016a), while ectothermic species maintain a low fractional heart mass as embryos and juveniles (Sirsat et al 2016b). In contrast, Red-winged Blackbird heart mass relative to body mass remained moderately constant throughout the nestling period suggesting this system grows in concert with others, contributing to provision of sufficient fuel delivery for the rapid growth rates of this altricial species.…”

“…The continuum of metamorphosis that defines the transition from an ectothermic state to one of endothermic capacity in birds is generally parsed into a series of three to four stages based on the limitations of each stage Sirsat et al 2016a;Tazawa et al 1988). All avian species share an initial Arrhenius-limited stage which corresponds to most of the incubation period and is characterized by a declining metabolic rate in the face of cooling temperature; altricial birds hatch during this period, resulting in ectothermic nestlings (Tazawa et al 1988).…”

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

“…For example, bird embryos have been instrumental in our understanding of the evolution of endothermy (Walter and Seebacher, 2009;Tzschentke and Rumpf, 2011;Sirsat et al, 2016). Hypothermic bird embryos have also led to an understanding of how cardiac function is altered during hypothermic surgery in humans (Sarre et al, 2006;Shao et al, 2007).…”

Biological and environmental factors related to communal roosting behavior of breeding Bank Swallow (Riparia riparia)

“…We predicted that several factors could relate to the likelihood of communal roosting by the Bank Swallow, including the thermoregulatory needs of the offspring and adults, the risk of collapsing burrows and predation, ectoparasite avoidance, and prospecting opportunities. If communal roosting is limited by the thermoregulatory needs of the offspring, we hypothesized that females, who are the primary incubators and brooders (Petersen 1955), will roost communally less often and for shorter periods than males, and that both sexes will limit this behavior when nests are active, at ages when young are most sensitive to temperature (in late incubation and in the first week after hatching; Dunn 1975, Marsh 1979, Marsh and Wickler 1982, Cooper and Voss 2013, Sirsat et al 2016, in poor weather conditions (low temperatures and high humidity; Coe et al 2015), and in nests with small broods that are less able to thermoregulate (Dunn 1975). We also hypothesized that if communal roosting is limited by the thermoregulatory needs of the adults, Bank Swallow individuals will refrain from roosting communally and reduce their time away from the nests while roosting in poor weather conditions (low temperatures, high humidity, high wind).…”