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

Kevin G. McCracken, Department of Biology, Department of Marine Biology and Ecology at the Rosenstiel School of Marine, Atmospheric, and Earth Science, and Human Genetics and Genomics at the Miller School of Medicine, University of Miami; University of Alaska Museum, University of Alaska Fairbanks; Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks
Graham R. Scott, Department of Biology, McMaster University
Luis Alza, Department of Biology, Casper College, Casper, Wyoming; 6 Centro de Ornitología y Biodiversidad (CORBIDI), Lima, Perú
Andrea Astie, Instituto Argentino de Investigaciones de las Zonas Áridas (IADIZA-CONICET), Mendoza, Argentina
Ciska Bakkeren, Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
Emil Bautista, Department of Biology, Casper College, Casper, Wyoming, USA
Mariana Bulgarella, University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, USA; Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA; School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Rebecca Cheek G. Cheek, University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska; Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA; Department of Biology, Colorado State University, Fort Collins, Colorado, USA
Beverly A. Chua, Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
Neal J. Dawson, Department of Biology, Department of Marine Biology and Ecology at the Rosenstiel School of Marine, Atmospheric, and Earth Science, and Human Genetics and Genomics at the Miller School of Medicine, University of Miami, Coral Gables, Florida, USA; Department of Biology, McMaster University, Hamilton, Ontario, Canada; Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
Alexis Diaz, Department of Biology, Department of Marine Biology and Ecology at the Rosenstiel School of Marine, Atmospheric, and Earth Science, and Human Genetics and Genomics at the Miller School of Medicine, University of Miami, Coral Gables, Florida, USA; Centro de Ornitología y Biodiversidad (CORBIDI), Lima, Perú
Catherine M. Ivy, Department of Biology, McMaster University, Hamilton, Ontario, Canada;Department of Biology, Western University, London, Ontario, Canada
Peter B. Frappell, 3Institute for Marine and Antarctic Studies, University of Tasmania, Tasmania, Australia
Cecilia Kopuchian, Centro de Ecología Aplicada del Litoral (CECOAL-CONICET), Corrientes, Argentina
Sabine L. Laguë, Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
John N. Maina, Department of Zoology, University of Johannesburg, Johannesburg, South Africa
Violeta Muñoz-Fuentes, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom
Elizabeth R. Schell, Department of Biology, Department of Marine Biology and Ecology at the Rosenstiel School of Marine, Atmospheric, and Earth Science, and Human Genetics and Genomics at the Miller School of Medicine, University of Miami, Coral Gables, Florida, USA
Matthew M. Smith, 3 Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA
Ryan J. Sprenger, Comparative Biosciences, University of Wisconsin-Madison, Madison, Wisconsin, USA
Pablo L. Tubaro, División Ornitología, Museo Argentino de Ciencias Naturales (MACN-CONICET), Buenos Aires, Argentina
Elizabeth R. Schell, Department of Biology, Department of Marine Biology and Ecology at the Rosenstiel School of Marine, Atmospheric, and Earth Science, and Human Genetics and Genomics at the Miller School of Medicine, University of Miami, Coral Gables, Florida, USA
Matthew M. Smith, Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA
Ryan J. Sprenger, Comparative Biosciences, University of Wisconsin-Madison, Madison, Wisconsin, USA
Pablo L. Tubaro, División Ornitología, Museo Argentino de Ciencias Naturales (MACN-CONICET), Buenos Aires, Argentina
Thomas Valqui, Centro de Ornitología y Biodiversidad (CORBIDI), Lima, Perú; 9Facultad de Ciencias Forestales, Universidad Nacional Agraria, La Molina, Perú
Roy E. Weber, 0Section for Zoophysiology, Department of Biology, Aarhus University, Aarhus, Denmark
Daniela Wilner, Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA
Robert E. Wilson, University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, USA; Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, Alaska, USA; 1School of Natural Resources and Nebraska State Museum, University of Nebraska-Lincoln, Lincoln, Nebraska, USA
Julia M. York, Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada; School of Integrative Biology, University of Illinois Urbana-Champaign, Illinois, USA
William K. Milsom, Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

Abstract

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.

DOI

10.31390/opmns.093

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