Resident birds in temperate zones respond to seasonally fluctuating temperatures by adjusting their physiology, such as changes in basal metabolic rate or peak metabolic rate during cold exposure, or altering their organ sizes, so as to match the thermogenic requirements of their current environment. Climate change is predicted to cause increases in the frequency of heat and cold wave events, which could increase the likelihood that birds will face an environmental mismatch. Here, we examined seasonality and the effects of acute and chronic heat shock to 33°C and subsequent recovery from heat shock on the ultrastructure of the superficial pectoralis muscle fiber diameter, myonuclear domain (MND) and capillary density in two temperate bird species of differing body mass, the black-capped chickadee (Poecile atricapillus) and the rock pigeon (Columba livia). We found that muscle fiber ultrastructure did not change with heat treatment. However, in black-capped chickadees, there was a significant increase in fiber diameter in spring phenotype birds compared with summer phenotype birds. In rock pigeons, we saw no differences in fiber diameter across seasons. Capillary density did not change as a function of fiber diameter in black-capped chickadees, but did change seasonally, as did MND. Across seasons, as fiber diameter decreased, capillary density increased in the pectoralis muscle of rock pigeons. For both species in this study, we found that as fiber diameter increased, so did MND. Our findings imply that these two temperate birds employ different muscular growth strategies that may be metabolically beneficial to each.
Many long‐lived animals do not appear to show classic signs of aging, perhaps because they show negligible senescence until dying from “catastrophic” mortality. Muscle senescence is seldom examined in wild animals, yet decline in muscle function is one of the first signs of aging in many lab animals and humans. Seabirds are an excellent study system for physiological implications of aging because they are long‐lived animals that actively forage and reproduce in the wild. Here, we examined linkages between pectoralis muscle fiber structure and age in black‐legged kittiwakes (Rissa tridactyla). Pectoralis muscle is the largest organ complex in birds, and responsible for flight and shivering. We obtained and fixed biopsies from wild black‐legged kittiwakes of known age. We then measured muscle fiber diameter, myonuclear domain and capillaries per fiber area among birds of differing ages. All muscle parameters were independent of age. Number of nuclei per mm of fiber showed a positive correlation with muscle fiber cross‐sectional area, and myonuclear domain increased with muscle fiber diameter. Thus, as muscle fibers increased in size, they may not have recruited satellite cells, increasing the protein turnover load per nuclei. We conclude that senescence in a long‐lived bird with an active lifestyle, does not entail mammalian‐like changes in muscle structure.
Muscle ultrastructure is closely linked with athletic performance in humans and lab animals, and presumably plays an important role in the movement ecology of wild animals. Movement is critical for wild animals to forage, escape predators, and reproduce. However, little evidence directly links muscle condition to locomotion in the wild. We used GPS-accelerometers to examine flight behaviour and muscle biopsies in breeding black-legged kittiwakes (Rissa tridactyla) to assess muscle ultrastructure. Biopsied kittiwakes showed similar reproductive success and subsequent over-winter survival to non-biopsied kittiwakes, suggesting that our study method did not greatly impact foraging ability. Muscle fibre diameter was negatively associated with wing beat frequency, suggesting that larger muscle fibres facilitate powered flight. Number of nuclei per fibre was positively associated with average airspeed, likely because higher power output needed by faster-flying birds required plasticity for muscle fibre recruitment. These results suggest the potential for flight behaviour to predict muscle ultrastructure.
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