Diving into old age: muscular senescence in a large-bodied, long-lived mammal, the Weddell seal (Leptonychotes weddellii)

Abstract

SUMMARYClassic aging theory postulates the absence of pronounced organismal senescence in wild animals since mortality probably occurs first. Large-bodied, long-lived mammals are a recognized exception to this tenet, yet organismal senescence has not been investigated to date in such mammals in the wild. Furthermore, oxidative stress theory of aging supports the suggestion that exercise hypoxia, as regularly incurred during apneustic foraging in diving mammals might lead to cellular dysfunction and accelerated aging. To determine if an aspect of organismal senescence occurs in wild marine mammals, we examined the pattern of skeletal muscle aging (contractile and connective tissue components of longissimus dorsi and pectoralis muscles) in freeranging adult Weddell seals (9-26 years). The average myocyte cross-sectional area was 22% greater with age in the longissiums dorsi, but no significant increase occurred in the pectoralis. Cross-sectional area was not related to body mass. Changes in myocyte number per area were consistent with the 35-40% age-increase in extracellular space in both muscle groups. Also consistent with extracellular space remodeling, total and relative collagen contents were significantly elevated in older seals (115% in longissimus dorsi; 65% in pectoralis). The ratio of muscle myocyte to collagen declined with age (50-63%) at both sites. Additionally, a shift towards a higher ratio of type I to type III collagen occurred with advancing age in both muscle groups (79% increase in pectoralis; 49% in longissimus dorsi). We reject the classic tenet and null-hypothesis that Weddell seals do not survive to an age where muscular senescence becomes detectable.

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

“…As muscle Mb loads often correlate with dive durations (Noren and Williams 2000;Lestyk et al 2009), higher Mb concentrations in deep-diving Weddell seals make their O 2 -storage capacities more similar to those previously reported in other phocid species capable of extended breath hold diving Lestyk et al 2009;Hassrick et al 2010). That Weddell seals expend energy to continue producing equivalent RBCs and iron-containing O 2 -carrying proteins during all times of the year (i.e., reduced and intense foraging periods, and the energetically expensive molt period), and also through senescence (Hindle et al 2009 demonstrates the importance of maintaining aerobic diving capacities. One possibility is that any summer diving activity and exercise would be sufficient to maintain protein production in Weddell seals.…”

King penguins adjust their diving behaviour with age

“…Penguins primarily use the pectoral muscles for propulsion (see Bannasch, 1995;Alexander, 1992); thus, theoretically muscle development could influence swimming capacity (Hindle et al, 2009). Muscle efficiency is obviously a difficult parameter to estimate in free-ranging animals, and this hypothesis cannot be verified.…”

Effects of early-stage aging on locomotor dynamics and hindlimb muscle force production in the rat

“…Previous studies have found that in both longand short-lived wild mammal species, muscular deficits and a reduction in fitness can precede reproductive senescence (e.g. Abrams, 1991;Hindle et al, 2009a;Hindle et al, 2009b). This decrease in fitness may be due in part to early age-related changes, which likely negatively impact individual survivorship in the wild, as the risk of predation increases and foraging capabilities are reduced.…”