Comparative mechanisms for O2 storage and metabolism in two Florida diving birds: the anhinga (Anhinga anhinga) and the double-crested cormorant (Nannopterum auritum)

J Comp Physiol B. 2024 Dec 20. doi: 10.1007/s00360-024-01593-x. Online ahead of print.

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 O2 at the surface prior to their next dive. While many species show adaptive increases in the O2 storage 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-O2 storage 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-O2 stores 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.

Keywords: Breath-hold diving; Hemoglobin; Muscle metabolism; Myoglobin; Oxygen storage.