Preparing Muscles for Diving: Age-Related Changes in Muscle Metabolic Profiles in Harp (Pagophilus groenlandicus) and Hooded (Cystophora cristata) Seals

Abstract

In adult marine mammals, muscles can sustain aerobic metabolism during dives in part because they contain large oxygen (O2) stores and metabolic rates are low. However, young pups have significantly lower tissue O2 stores and much higher mass-specific metabolic rates. To investigate how these differences may influence muscle function during dives, we measured the activities of enzymes involved in aerobic and anaerobic metabolic pathways (citrate synthase [CS], β-hydroxyacyl-coenzyme A dehydrogenase [HOAD], lactate dehydrogenase [LDH]) and the LDH isoform profile in six muscles from 41 harp (Pagophilus groenlandicus) and 30 hooded (Cystophora cristata) seals ranging in age from fetal to adult. All neonatal muscles had significantly higher absolute but lower metabolically scaled CS and HOAD activities than adults (∼ 70% and ∼ 85% lower, respectively). Developmental increases in LDH activity lagged that of aerobic enzymes and were not accompanied by changes in isozyme profile, suggesting that changes in enzyme concentration rather than structure determine activity levels. Biochemical maturation proceeded faster in the major locomotory muscles. In combination, findings suggest that pup muscles are unable to support strenuous aerobic exercise or rely heavily on anaerobic metabolism during early diving activities and that pups' high mass-specific metabolic rates may play a key role in limiting the ability of their muscles to support underwater foraging.

Hooded seal Cystophora cristata foraging areas in the Northeast Atlantic Ocean—Investigated using three complementary methods

“…In contrast to some other seal species, such as northern ( Mirounga angustirostris) and southern elephant seals ( Mirounga leonina) , that develop diving skills prior to dispersal from natal areas, while they are still being fed by their mothers [ 82 – 83 ], hooded seal pups are weaned when they are only a few days old and must learn to swim and dive on their own [ 42 , 84 ]. Although hooded seals are born with fully developed hemoglobin stores, their myoglobin levels are only 25–30% of adults’ levels [ 85 – 86 ], which means that pups rely heavily on anaerobic metabolism during early diving activities [ 87 ]. Their myoglobin levels increase concomitantly with increased swimming activity [ 85 – 86 ], which is consistent with the previously reported rapid development of diving capacity in wild [ 42 ] and with the results of this study that showed progression in their diving and swimming skills from the post-breeding period to the post-molting period.…”

Fatty Acid Composition in Blubber, Liver, and Muscle of Marine Mammals in the Southern Baltic Sea

“…The blubber was isolated before conduction of the lipid extraction and fatty acid ester preparation. The skeletal muscle samples were taken from the longissimus dorsi and psoas muscle to ensure standardization of the sampling process and also to ensure that for pinnipeds and cetaceans the same muscles with similar functionality (aquatic locomotion) were used following [35]. Directly after, sampling tissues were stored again at −20 • C until further analysis.…”

Iron mobilization during lactation reduces oxygen stores in a diving mammal

“…Diving metabolic rates (DMR) are suppressed through bradycardia, selective vasoconstriction prioritizing O 2 delivery to anoxia-intolerant tissues, and lowering body temperature 13,14 . Locomotor activities are further supported by elevated muscle catabolic enzyme activities and high mitochondrial and lipid droplet densities [15][16][17][18][19] . Large O 2 stores paired with slow O 2 consumption allows marine mammals to extend dive durations while relying on aerobic metabolism (i.e., staying below the aerobic dive limit, ADL, prior to a rise in lactate production).…”