ABSTRACT Diving animals must sustain high muscle activity with finite oxygen (O2) to forage underwater. Studies have shown that some diving mammals exhibit changes in the metabolic phenotype of locomotory muscles compared with non-divers, but the pervasiveness of such changes across diving animals is unclear, particularly among diving birds. Here, we examined whether changes in muscle phenotype and mitochondrial abundance are associated with dive capacity across 17 species of ducks from three distinct evolutionary clades (tribes) in the subfamily Anatinae: the longest diving sea ducks, the mid-tier diving pochards and the non-diving dabblers. In the gastrocnemius (the primary swimming and diving muscle), mitochondrial volume density in both oxidative and glycolytic fiber types was 70% and 30% higher in sea ducks compared with dabblers, respectively. These differences were associated with preferential proliferation of the subsarcolemmal subfraction, the mitochondria adjacent to the cell membrane and nearest to capillaries, relative to the intermyofibrillar subfraction. Capillary density and capillary-to-fiber ratio were positively correlated with mitochondrial volume density, with no variation in the density of oxidative fiber types across tribes. In the pectoralis, sea ducks had greater abundance of oxidative fiber types than dabblers, whereas pochards were intermediate between the two. These data suggest that skeletal muscles of sea ducks have a heightened capacity for aerobic metabolism and an enhanced ability to utilize O2 stores in the blood and muscle while diving.
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Comparative mechanisms for O2 storage and metabolism in two Florida diving birds: the anhinga (Anhinga anhinga) and the double-crested cormorant (Nannopterum auritum)
Abstract Air-breathing vertebrates face many physiological challenges while breath-hold diving. In particular, they must endure intermittent periods of declining oxygen (O2) stores, as well as the need to rapidly replenish depleted O2at the surface prior to their next dive. While many species show adaptive increases in the O2storage capacity of the blood or muscles, others increase the oxidative capacity of the muscles through changes in mitochondrial arrangement, abundance, or remodeling of key metabolic pathways. Here, we assess the diving phenotypes of two sympatric diving birds: the anhinga (Anhinga anhinga) and the double-crested cormorant (Nannopterum auritum). In each, we measured blood- and muscle-O2storage capacity, as well as phenotypic characteristics such as muscle fiber composition, capillarity, and mitochondrial arrangement and abundance in the primary flight (pectoralis) and swimming (gastrocnemius) muscles. Finally, we compared the maximal activities of 10 key enzymes in the pectoralis, gastrocnemius, and left ventricle of the heart to assess tissue level oxidative capacity and fuel use. Our results indicate that both species utilize enhanced muscle-O2stores over blood-O2. This is most apparent in the large difference in available myoglobin in the gastrocnemius between the two species. Oxidative capacity varied significantly between the flight and swimming muscles and between the two species. However, both species showed lower oxidative capacity than expected compared to other diving birds. In particular, the anhinga exhibits a unique diving phenotype with a slightly higher reliance on glycolysis and lower aerobic ATP generation than double-crested cormorants.
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- Award ID(s):
- 2419773
- PAR ID:
- 10621582
- Publisher / Repository:
- Springer
- Date Published:
- Journal Name:
- Journal of Comparative Physiology B
- Volume:
- 195
- Issue:
- 2
- ISSN:
- 0174-1578
- Page Range / eLocation ID:
- 191 to 208
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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