Diving at High Altitude: O2 Transport and Utilization in the Ruddy Duck and Torrent Duck in the Andes

MCCRACKEN, KEVIN G.; SCOTT, GRAHAM; ALZA, LUIS; ASTIE, ANDREA; BAKKEREN, CISKA; BAUTISTA, EMIL; BULGARELLA, MARIANA; CHEEK, REBECCA CHEEK; CHUA, BEVERLY; DAWSON, NEAL; DIAZ, ALEXIS; IVY, CATHERINE; FRAPPELL, PETER; KOPUCHIAN, CECILIA; LAGUË, SABINE; MAINA, JOHN; MUÑOZ-FUENTES, VIOLETA; SCHELL, ELIZABETH; SMITH, MATTHEW; SPRENGER, RYAN; TUBARO, PABLO; VALQUI, THOMAS; WEBER, ROY; WILNER, DANIELA; WILSON, ROBERT; YORK, JULIA; MILSOM, WILLIAM

Occasional Papers of the Museum of Natural Science, Louisiana State University

Louisiana State University

Lugar: Baton Rouge; Año: 2024 vol. 1

Hypoxia and cold temperatures create unique physiological challenges for high-altitude organisms that can vary depending on lifestyle. While nearly all studies of air-breathing animals at high altitude are from terrestrial species, species that breath-hold dive underwater at high altitude encounter a very different set of selective pressures influencing their phenotype. The goal of this publication is to highlight the changes in O2 transport and utilization in high-altitude diving birds relative to divers at sea level, and the extent to which these changes are qualitatively distinct from phenotypic changes in non-diving species at high altitude. For example, while high capacities for sustained O2 transport may be required for sustained flight and thermogenesis (particularly in small endotherms), high-altitude breath-hold diving is a form of intense exercise uniquely defined by transient and sometimes severe O2 depletion (hypoxemia) and CO2 accumulation (hypercapnia), interspersed by recovery between dives when O2 stores must be rapidly replenished despite the hypoxic environment at high altitude. Given this, diving behavior may preclude or constrain the physiology of divers, such that high-altitude divers are predicted to exhibit qualitatively distinct phenotypic changes compared to non-divers, as each likely experience unique signals for phenotypic plasticity and selective pressures driving their evolution. Here, we reanalyze and synthesize new and recent findings describing O2 transport for two high-altitude breath-hold divers in the Andes of South America, the ruddy duck (Oxyura jamaicensis) and the torrent duck (Merganetta armata). Analysis across the O2-transport cascade including (1) ventilation, (2) pulmonary O2 diffusion, (3) circulatory O2 delivery, (4) tissue O2 diffusion, and (5) tissue O2 utilization reveals that different routes to functional adaptation have emerged between diving and non-diving birds in the high Andes. While ruddy ducks and torrent ducks differed in numerous ways, we found that these two high-altitude divers had generally much higher blood-O2 carrying capacity relative to non-divers. Furthermore, unlike non-diving high-altitude waterfowl, these highaltitude divers did not increase Hb-O2 affinity at high altitude, because Hb-O2 affinity was already high in the low-altitude diving ancestor. Due to these factors, these divers always had higher arterial O2 content (CaO2) than non-divers, but unlike the non-divers, there was never any difference in CaO2 between high- and low-altitude populations among the divers. Finally, high-altitude divers exhibited greater magnitudes of body temperature (Tb) suppression during hypoxia than their corresponding low-altitude populations, whereas hypoxic Tb suppression was similar between high- and lowaltitude taxa among non-divers. In fact, the ruddy duck had the lowest Tb of all species under extreme hypoxia. Such changes may be beneficial by reducing the metabolic cost of thermogenesis during dives in cold alpine waters. Further insight into the unique physiology of high-altitude divers would benefit from future study of cardiorespiratory control and pulmonary function during the recovery phase between dives, as well as mitochondrial bioenergetics, reactive oxygen species (ROS) production, and antioxidant defense.