skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Gas exchange, oxygen transport and metabolism in high-altitude waterfowl
High-altitude life poses physiological challenges to all animals due to decreased environmental oxygen (O2) availability (hypoxia) and cold. Supporting high metabolic rates and body temperatures with limited O2is challenging. Many birds, however, thrive at high altitudes. The O2-transport cascade describes the pathway involved in moving O2from the environment to the tissues encompassing: (i) ventilation, (ii) pulmonary O2diffusion, (iii) circulation, (iv) tissue O2diffusion, and (v) mitochondrial O2use for ATP production. Shared avian traits such as rigid lungs with cross-current gas exchange and unidirectional airflow aid in O2acquisition and transport in all birds. Many high-altitude birds, however, have evolved enhancements to some or all steps in the cascade. In this review, we summarize the current literature on gas exchange and O2transport in high-altitude birds, providing an overview of the O2-transport cascade that principally draws on the literature from high-altitude waterfowl, the most well-studied group of high-altitude birds. We close by discussing two important avenues for future research: distinguishing between the influences of plasticity and evolution and investigating whether the morphological and physiological differences discussed contribute to enhanced locomotor or thermogenic performance, a potential critical link to fitness. This article is part of the theme issue ‘The biology of the avian respiratory system’.  more » « less
Award ID(s):
2419773
PAR ID:
10621583
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Publisher / Repository:
The Royal Society
Date Published:
Journal Name:
Philosophical Transactions of the Royal Society B: Biological Sciences
Volume:
380
Issue:
1920
ISSN:
0962-8436
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Abstract Background Complex organismal traits are often the result of multiple interacting genes and sub-organismal phenotypes, but how these interactions shape the evolutionary trajectories of adaptive traits is poorly understood. We examined how functional interactions between cardiorespiratory traits contribute to adaptive increases in the capacity for aerobic thermogenesis (maximal O 2 consumption, V̇ O 2 max, during acute cold exposure) in high-altitude deer mice ( Peromyscus maniculatus ). We crossed highland and lowland deer mice to produce F 2 inter-population hybrids, which expressed genetically based variation in hemoglobin (Hb) O 2 affinity on a mixed genetic background. We then combined physiological experiments and mathematical modeling of the O 2 transport pathway to examine the links between cardiorespiratory traits and V̇ O 2 max. Results Physiological experiments revealed that increases in Hb-O 2 affinity of red blood cells improved blood oxygenation in hypoxia but were not associated with an enhancement in V̇ O 2 max. Sensitivity analyses performed using mathematical modeling showed that the influence of Hb-O 2 affinity on V̇ O 2 max in hypoxia was contingent on the capacity for O 2 diffusion in active tissues. Conclusions These results suggest that increases in Hb-O 2 affinity would only have adaptive value in hypoxic conditions if concurrent with or preceded by increases in tissue O 2 diffusing capacity. In high-altitude deer mice, the adaptive benefit of increasing Hb-O 2 affinity is contingent on the capacity to extract O 2 from the blood, which helps resolve controversies about the general role of hemoglobin function in hypoxia tolerance. 
    more » « less
  2. Justin Boyles (Ed.)
    Abstract Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines.In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water‐gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μLVO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance.We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss.These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species‐ or lineage‐wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance. Read the freePlain Language Summaryfor this article on the Journal blog. 
    more » « less
  3. Abstract Desert communities are threatened with species loss due to climate change, and their resistance to such losses is unknown. We constructed a food web of the Mojave Desert terrestrial community (300 nodes, 4080 edges) to empirically examine the potential cascading effects of bird extinctions on this desert network, compared to losses of mammals and lizards. We focused on birds because they are already disappearing from the Mojave, and their relative thermal vulnerabilities are known. We quantified bottom‐up secondary extinctions and evaluated the relative resistance of the community to losses of each vertebrate group. The impact of random bird species loss was relatively low compared to the consequences of mammal (causing the greatest number of cascading losses) or reptile loss, and birds were relatively less likely to be in trophic positions that could drive top‐down effects in apparent competition and tri‐tropic cascade motifs. An avian extinction cascade with year‐long resident birds caused more secondary extinctions than the cascade involving all bird species for randomized ordered extinctions. Notably, we also found that relatively high interconnectivity among avian species has formed a subweb, enhancing network resistance to bird losses. 
    more » « less
  4. To cope with the reduced availability of O 2 at high altitude, air-breathing vertebrates have evolved myriad adjustments in the cardiorespiratory system to match tissue O 2 delivery with metabolic O 2 demand. We explain how changes at interacting steps of the O 2 transport pathway contribute to plastic and evolved changes in whole-animal aerobic performance under hypoxia. In vertebrates native to high altitude, enhancements of aerobic performance under hypoxia are attributable to a combination of environmentally induced and evolved changes in multiple steps of the pathway. Additionally, evidence suggests that many high-altitude natives have evolved mechanisms for attenuating maladaptive acclimatization responses to hypoxia, resulting in counter-gradient patterns of altitudinal variation for key physiological phenotypes. For traits that exhibit counteracting environmental and genetic effects, evolved changes in phenotype may be cryptic under field conditions and can only be revealed by rearing representatives of high- and low-altitude populations under standardized environmental conditions to control for plasticity. 
    more » « less
  5. 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. 
    more » « less