Muscle fiber structure in an aging long‐lived seabird, the black‐legged kittiwake (Rissa tridactyla)

Abstract

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 myonuclear domain, but not oxidative stress, decreases with age in a long-lived seabird with high activity costs

“…In humans, normal muscle aging patterns show a decrease in muscle fiber diameters with age through sarcopenia (Young et al, 1985;Lexell et al, 1988;Frontera et al, 2000), though it is unclear whether age-related decreases in muscle fiber diameter are a general trend in most animals or just the pattern observed in humans and mammals (Young et al, 1985;Lexell et al, 1988;Frontera et al, 2000). Similar non-significant changes in fiber diameter were observed in another long-lived seabird, the black-legged kittiwake (Brown et al, 2019). Additionally, we did not find a correlation between CFA and age.…”

“…Birds are able to phenotypically adjust their muscle mass during increases in workloads, such as migration (e.g. Swanson, 1991;O'Connor, 1995;Cooper, 2002), or for increased thermogenic requirements (Milbergue et al, 2018); however, how muscle fiber ultrastructure changes during aging in long-lived seabirds has only been documented in a single species, the black-legged kittiwake (Brown et al, 2019). In humans and laboratory rodents, normal muscle aging patterns show a decrease in muscle fiber diameters with age through sarcopenia (Young et al, 1985;Lexell et al, 1988;Frontera et al, 2000), an age-related impairment of muscle function that includes deterioration of quantity and quality of muscle, decreases in myofibrillar protein expression, mismatch in rates of protein synthesis and degradation, and a decrease in force generating capacity (Cristea et al, 2010).…”

Effects of age, sex, and ENSO phase on foraging and flight performance in Nazca boobies

“…While muscle function does degrade in old age in several wild mammals (Hämäläinen et al, 2015;, equivalent studies in two seabirds gave mixed results. The myonuclear domain, but not muscle diameter, of the pectoralis muscle shrinks with increasing age in thick-billed murres (Elliott et al, 2015;Jimenez et al, 2019), but black-legged kittiwakes (Rissa tridactyla) showed no change in musculature with age (Brown et al, 2019). Instead of a deficit in power production, stamina deficits of appendicular muscles that control the position and movement of flight surfaces during flapping (Pennycuick et al, 1988) remain as a possible physiological cause of the Airspeed decline in old age.…”

Extraordinarily rapid proliferation of cultured muscle satellite cells from migratory birds

“…However, there is no strong evidence for performancebased declines in long-lived birds, but instead these birds may suffer from catastrophic senescence as a result of the rapid failure of physiological systems resulting in death [43]. Long-lived seabirds (thick-billed murres, Uria lomvia and black-legged kittiwakes, Rissa tridactyla) do not exhibit age-related declines in muscle fibre cross-sectional area [44,45] that occurs in humans and other mammals [46][47][48]. Decreasing myonuclear domain (MND; i.e.…”