The authors state that they flowed nitrogen directly into the mask at a rate that brought O2 levels approximately to FiO2 of 0.105 and 0.07. Flight Club is the home of Social Darts. Bioclusive transparent film dressing (Henry Schein, Melville, NY, USA) was placed over the insertion site of the electrodes and Elastinet stocking placed over the neck to protect the insertion site, secured by Bioclusive at each end. If so, I think it helps clarify your explanation in the last paragraph of the subsection “Effects of Hypoxia” – about how the birds cope with the metabolic challenge – they "become more efficient" because they are restricted to fly in only the most efficient manner; one they occasionally used in normoxic conditions during the experiment and probably the way they'd fly during an actual migration. The birds also wore a breathing mask that could simulate the limited oxygen availability at altitudes of roughly 5,500 and 9,000 meters, and measure the oxygen consumed and the carbon dioxide produced by the geese. Heart rate and metabolic rate of bar-headed geese at rest in normoxia in this study were remarkably similar to those obtained by Ward et al. We misunderstood the Data Dryad system and neglected to provide the temporary DOI link rather than the DOI itself (the data were available in Dryad at the time of submission). As blood travels away from the lung toward the exercising tissue, it would be expected to warm, enhancing O2 unloading. 040’, Henry Schein, Canada), which was softened with a heating gun and stretched over the cast to create a light-weight, form-fitted mask that could be secured with a thin elastic strap below the base of the skull. Arterial values in the range measured in 0.07 FiO2 are strikingly low (Supplementary files 1 and 3), particularly given the need to support the metabolically costly activity of flight. Apologies for the lack in availability of the data. There was no significant effect of oxygen level on venous blood temperature (F2, 72.225=1.7253, p=0.1854; Figure 3B) nor the interaction of O2 level*timepoint (F8, 71.045=0.3347, p=0.9497). 9. Don’t be fooled by it’s simplicity, this tower is easy to install and performs like any other at a fraction of the cost. One concern of mine that appeared repeatedly is a sort of survivor bias in the presentation of the results, where summary data from the moderate and severe hypoxia treatments are shown together. Bar-headed geese trained to run on a treadmill did not show a significant change in metabolic rate between normoxia and severe hypoxia, however the increase in metabolic rate from rest to running was only ~2.5 fold (Hawkes et al., 2014). But, they did not derived VO2 data from hypoxic flights (and do not present such data for the recovery period). However, wingbeat frequencies measured during flight in normoxia in the previous study were lower, as was V˙CO2 (by approximately 29%). As near complete utilization of the available O2 store (venous PO2 values near zero at the end of dives) certainly contributes to the success of elite divers like elephant seals and emperor penguins (Ponganis et al., 2007; Meir et al., 2009), the capacity to effectively maximize O2 resources in the O2-limited environment of high altitude flight would also afford a distinct advantage. Descriptive statistics are reported in Table 1 and supplementary files, mean ± SEM is reported here unless estimated marginal mean (EMM ± SEM) or median is indicated. As heart rate in the current study was unaffected by hypoxia (Table 1), this suggests that the increases in heart rate measured in wild bar headed geese migrating at altitudes above 2,300 meters may be a consequence of flight dynamics in hypobaria, rather than hypoxia. Birds that fly at high altitudes must support vigorous exercise in oxygen-thin environments. Important conclusions are based on the data obtained from only a small few (e.g. Figures and tables where presentation appears to be affected by a survivor bias: Figure 2, Figure 3A, Figure 4, Table 1, Supplementary file 2. We conclude that flight in hypoxia is largely achieved via the reduction in metabolic rate compared to normoxia. The birds took their first flights either in a 30-meter wind tunnel at an engineering department in the University of British Columbia or, if the wind tunnel was unavailable, alongside a bicycle or a motor scooter. Makalu (8,485 m; Swan, 1961). Example PO2 recordings during normoxic and hypoxic flights are shown in Figure 4. Google has many special features to help you find exactly what you're looking for. Despite a constant wing beat frequency, flight biomechanics of the geese in our study were altered in response to hypoxia, with increased upstroke duration (T) and decreased upstroke wingtip speed (Utip), upstroke plane amplitude (FSP), and mid-upstroke angle of inclination (a) (Supplementary file 4; Whale, 2012) As the downstroke produces the majority of lift and all forward thrust, by increasing the ratio of the duration of upstroke to downstroke, the duration of activation of the pectoralis major muscle group is decreased (responsible for the majority of downstroke power). High in the sky fly Bar-headed Geese. Our understanding of the adaptations that support high-altitude flight in birds is growing, particularly in the bar-headed goose, Anser indicus (Storz et al., 2010; Scott et al., 2015). CO2 pulse in moderate hypoxic flight was significantly higher (t = −3.666, p=0.0008) than in severe hypoxia (EMM = 0.514 ± 0.034 mL CO2 beat−1 kg−1). (2002) also concluded that their wind tunnel data could not be used directly to calculate the metabolic rate of wild migratory geese from measurements of heart rate alone. Whale (2012) is cited several times but as far as I can tell is not publicly available. Filmed at 125 frames per second, shown here at 7.5 frames per second playback. There was a significant effect of activity on RER (F2, 301.95=54.37, p<0.0001, ICC=0.254). Only one bird (bird 45) flew in severe hypoxia consistently, with a median duration of 100 s. This was significantly shorter (one-way ANOVA on ranks; H(2)=14.911, p<0.001; post-hoc Dunn’s method Q = 3.815, p<0.05) than this bird would fly in normoxia (median = 232.5 s) but not moderate hypoxia (median = 158 s, Q = 2.113, p>0.05; Supplementary file 1). This was also the case for the relationship between heart rate and wing-beat frequency in wild birds, although mean values were well correlated (Bishop et al., 2015). Search the world's information, including webpages, images, videos and more. Masks were custom-made on a Plaster of Paris cast of the head of a deceased bar-headed goose using heat-moldable dental mouth-guard compound (Thermo-Forming Material, Clear-Mouthguard,. (2002) experienced the same difficulty (Pers. Wing-beat frequencies of bar-headed geese in this study were similar in both normoxia and hypoxia. moderate hypoxia) or one (severe hypoxia) individuals that consistently performed. Consent has been obtained by all subjects in the photo and videos used in this manuscript. This is supported by our data as RER falls to 0.921 ± 0.02 for flights longer than six minutes. The tubes sampling air and delivering nitrogen to the mask exited the tunnel to the respirometry set-up at an access point (Figure 5). Ward et al. Interestingly, these values are equivalent to the mean minimum arterial PO2 values obtained near the end of dives in elephant seals, and are similar to the range exhibited by diving emperor penguins (Ponganis et al., 2007; Fedak et al., 1981). Flow turbulence in the tunnel, the presence of the experimenters and the presence of the mask and tubing all will have increased flight costs and may have contributed to this (Hedenström and Lindström, 2017). The foster parent stood against the wall at the front of the flight section of the wind tunnel to encourage the bird to sustain flight. In post-hoc testing, no comparisons among preflight arterial PO2 were significant (p>0.05). These High-Flying Geese Are ‘the Astronauts of the Bird World’ Bar-headed geese migrate above 26,000 feet. This is troubling because we know that 3 of the birds in the moderate hypoxia group were unwilling/unable to fly in severe hypoxia and are therefore not directly comparable to the birds that were willing and able. Because the RER averaged 0.988 ± 0.01 during flight in normoxia and flight durations between normoxia and moderate hypoxia were not significantly different, we have made the assumption that V˙CO2 and V˙O2 can be used interchangeably under this condition. This discussion was included in the original manuscript, but has been further edited to clarify (subsection “Effects of Hypoxia”, last paragraph). We found that the primary contribution to increased gas transport between rest and flight in both normoxia and hypoxia was from increases in the estimated O2 pulse (between 6 and 8-fold; inferred from the calculated CO2 pulse). This work would not have been possible without the tireless efforts of the numerous UBC undergraduate volunteers that assisted with animal husbandry, training, and data collection (in particular, Erin Erskine, Michelle Reichert, Anthony Pang, Alice Kuan, Judy Cha, Deanna White, Christine Yeung, Winnie Cheung and Nici Darychuk). (2015) (B). It appears from your results (Figure 2) that the minimum cost of flight is similar for all three oxygen levels. found that bar-headed geese could indeed fly at these simulated extreme altitudes in the wind tunnel, and that the birds largely achieved this by reducing their metabolism to match low oxygen conditions. RER in flight (EMM of 1.00 ± 0.034) was significantly higher than pre-flight (EMM of 0.87 ± 0.035; t=7.026, p<0.0001) and rest (EMM of 0.80 ± 0.035; t=10.073, p<0.0001). Birds were familiarized with dummy respirometry masks and backpack systems soon after hatching. Asterisks indicate significant difference from normoxia (* indicates p<0.05; ** indicates p<0.01; *** indicates p<0.001, § indicates difference from pre-flight value, # indicates difference from recovery value, and $ indicates difference from start value). FLY Racing is committed to developing the highest quality apparel, accessories, and hard parts for whatever sport you love. Despite possible instrumentation effects or the short flight durations, flights were repeatable, of similar length under all conditions, and most importantly, produced stable levels of the measured variables, allowing us to make robust comparisons between flight in normoxia vs. hypoxia, thus examining the effects of hypoxia on flight physiology under similar conditions. Interestingly, blood temperature dynamics may also play a critical role in enhancing O2 loading in this species during its exceptional migration. Another investigator initially lifted the bird into the air stream from behind, then supported the tubing running from the mask to the data acquisition system, holding them 2–3 feet above and behind the bird to allow free movement of the flying bird (Figure 5 and Video 2). Bar-headed geese lower their flight metabolic rates to fly in low-oxygen conditions. We have reworded this point throughout the manuscript as “maintaining the increase in O2 pulse also measured in normoxia”, which more accurately reflects the data. Normoxia and moderate hypoxia data from this study shown in (A), inset shows expansion of data at rest. We used the afex package in RStudio (R version 3.5.1) for generating the models, the emmeans package for post-hoc comparisons with Bonferroni adjustment where appropriate, and calculated the adjusted intraclass correlation coefficient (ICC) by dividing the variance of the random intercept by the sum of the random effect variances (a value closer to 1 indicates a greater effect of the individual bird). The bar-headed goose is famed for migratory flight at extreme altitude. Flapping flight in birds is the most metabolically costly form of locomotion in vertebrates (Butler and Bishop, 2000). We do expect that RER would fall in longer flights (see the aforementioned paragraph). The bird is not usually seen at its full altitude but it’s still uncertain as to why the vulture flies this high. We have added discussion of this issue to the Results, as well as to the figure legends for the figures indicated. In (B) oxygen consumption versus heart rate for bar-headed geese from three studies, Hawkes et al. A subsample of the outflow was pulled into the field metabolic system (FMS). For birds flying in FiO2 = 0.105, V˙CO2 was 16% lower than in birds flying in normoxia. The geese appear to have ample cardiac reserves, as heart rate during hypoxic flights was not higher than in normoxic flights. You may still download the video for offline viewing. Note that only one bird flew consistently in severe hypoxia (red trace in panel A). Here I discuss the characteristics that help high fliers sustain the high rates of metabolism needed for flight at elevation. Only the overall average metabolic rate differs, indicating that birds may employ more or less efficient flight strategies in normoxia, but shift towards using only the most efficient strategies when oxygen limited. We obtained the first measurements of arterial and venous PO2 and temperature records in this species, and that of any equivalently sized bird, during flight. Geese (twelve bar-headed geese in 2010, seven in 2011) were imprinted on a human foster parent (J.U.M. The authors dismiss the potential criticism that I allude to below regarding the possibility of tapping into anaerobic metabolism to support flight under hypoxia (or of an induced metabolic acidosis) concluding that there was no apparent oxygen debt to be repaid after the flights had ended. Based on your description in the subsection “Calculations and statistical analysis”, your statistical tests may avoid this problem, but also might not because the birds that did not fly in severe hypoxia are not just "missing data", they were unable/unwilling to fly and that information may not be effectively incorporated in the tests. But this parameter actually decreases in hypoxic flight relative to normoxic flight (Table 1, bottom line). The bar-tailed godwit (Limosa lapponica) breeds in the tundra and Arctic coasts of Eurasia and winters in the tropical and temperate habitat of Europe, Africa, Asia and even as far as Australia and New Zealand.The bar-tailed godwit is unique in that its migration is the longest non-stop migration of avian species in the world. R script and data files (including source data for figures, although figures were not generated in R) were deposited in Dryad (doi:10.5061/dryad.fg80hp6). In moderate hypoxia, venous temperature in steady state (steady state EMM = 39.998 ± 0.509°C) was significantly lower than both preflight (preflight EMM = 41.473 ± 0.509°C; t = 3.139, p=0.0247) and the start of the flight (start EMM = 41.373 ± 0.509°C; t=−2.926, p=0.0460). Flight Clubs, also runs AceBounce, a game venue; Puttshack, a high-tech mini golf experience; and Wonderball, a ping-pong bar. Electrodes were inserted to lie close to the heart to sample mixed venous blood (ranging from 9 to 13.5 cm from insertion site to cannula tip, depending on the bird and insertion site). We apologize that this point was not clear in the original submission. Authors Jessica U Meir 1 , William K Milsom. Based on these observations, we aimed to determine (1) how the metabolic challenge of flight differs between normoxia and normobaric hypoxia, and (2) whether bar-headed geese are capable of wind tunnel flight in severe normobaric hypoxia equivalent to altitudes of roughly 9,000 m (0.07 FiO2), the maximum altitude at which they have been anecdotally reported to fly (Swan, 1961). Seven bar-headed geese (2.21 ± 0.26 kg) managed steady, stationary, and prolonged flight in the wind tunnel while fully instrumented. In hypoxia both at rest and preflight in the wind tunnel, V˙CO2 fell by 22 and 26% for FiO2=0.105 and by 10 and 29% for FiO2=0.07. The reduction in metabolism in hypoxia observed in the current study could represent O2 limitation, selective suppression of metabolism to specific tissues or increased efficiency of flight pattern and thus O2 utilization. Electric atmosphere. We have significantly modified the Abstract as suggested, and also modified the title. We generated individual models for each dependent variable (duration, RER, V˙CO2, heart rate, CO2 pulse, blood PO2, venous temperature) and compared main effects of oxygen level (partial pressure of oxygen) and activity or time point, as well as the interaction (oxygen level*activity) and compared estimated marginal means post-hoc assuming significance at p<0.05. It is unclear if individual birds had both venous and arterial PO2 sensors implanted. Another weakness is that the sample sizes were quite low, especially in hypoxia, where it was difficult to get the birds to fly. We have clarified the language here, but it was clearly stated in the Materials and methods that “only one site, either arterial or venous, was targeted per surgery”. The discrepancy in heart rates may also be due to methodological differences, as we found it necessary to visually verify each heart rate peak while Ward et al. Mixed venous PO2 decreased during the initial portion of flights in hypoxia, indicative of increased tissue O2 extraction. Tubes ran from mask out of the tunnel, one introducing a calibrated amount of dry nitrogen into the mask, and the other pulling from the mask by way of an air pump. During testing to calibrate the hypoxic levels (using a Plaster of Paris goose head mold in the mask), we obtained stable O2 levels for both levels of hypoxia using this method, so we believed it would be adequate and result in a stable baseline under all conditions. Flying requires ten to … We have reworded the Discussion in regard to oxygen pulse in normoxia vs. hypoxia in order to clarify (see Essential revisions point 1). A two-part list of links to download the article, or parts of the article, in various formats. Metabolic rate during flight increased 16-fold from rest, supported by an increase in the estimated amount of O2 transported per heartbeat and a modest increase in heart rate. For venous deployments, Po2 electrodes and thermistors were inserted percutaneously via the right jugular vein using a peel-away catheter over needle (Arrow 15 Ga, Teleflex Medical, Markham, Ontario, Canada; similar to methods described in Meir et al., 2008; Ponganis et al., 2007; Meir et al., 2009; Ponganis et al., 2009). At these heights, the air is so thin that it contains only about 30–50% of the oxygen available at sea-level. How do bar-headed geese cope with low oxygen levels when flying over the Himalayas? Heart rates during flight, however, were lower in the current study suggesting that our birds were working harder but were employing larger increases in cardiac output and/or pulmonary exchange (Figure 1B). N=7 birds for all data, n=89 sessions for rest in normoxia, n=113 flights in normoxia, n=54 sessions for rest in moderate hypoxia, n=74 flights in moderate hypoxia, n=13 flights in severe hypoxia (note that only one bird flew consistently in severe hypoxia), n=29 sessions for rest in severe hypoxia. Social Entertainment Ventures, the company running the U.S. Asia is the highest populated continent, and it has also suffered the greatest economic losses with night club entertainment businesses being greatly affected due to the closing down. Although we cannot reject this possibility as lactate was not measured in this study, we consider it unlikely as there was no sign of an oxygen limitation, because: 1) the birds could still increase V˙CO2 by 14 to 23-fold during flight, 2) reductions in metabolic rate also occurred under rest and preflight conditions, and 3) the birds sustained flights of similar durations at constant levels of arterial PO2. For example, they have larger lungs than most other birds their size, and their red blood cells contain a version of hemoglobin that binds oxygen much more tightly. Dashed line shown to indicate 300 beats per minute in each plot (for aid in visual comparison only). Direct and integrated physiological measures of oxygen transport during flight, on the other hand, are extremely limited (Butler and Bishop, 2000; Ward et al., 2002), and none have been made under hypoxic conditions. We thank the reviewers of this manuscript for their valuable comments and suggestions. For example, the associated hyperventilation (decreased CO2) and decrease in temperature (below) in the flying goose correspond to a much higher arterial O2 content for the same low levels of PO2 experienced between these species (Meir and Milsom, 2013). Briefly, bar-headed goose (Anser indicus) eggs were obtained from the Sylvan Heights Bird Park (Scotland Neck, North Carolina). Data were plotted using Origin2016 software (OriginLab, Northampton, MA, USA). Hopefully, further gains made in the field of bio-logging systems directly measuring PO2 or SO2 will elucidate these variables in wild, migrating birds in the future. The thermistor could not be deployed simultaneously with the arterial Po2 electrode due to aortic size. of Mechanical Engineering for use of the wind tunnel; Marty Loughry and Tom Wright of UFI for design and construction of the recorders; Bob Shadwick for use of his rad scooter and transport van; Yvonne Dzal for her mad chauffeur skills; James Whale for flight kinematic data and video; Graham Scott for manuscript review; and Erika Hale for assistance with statistics. This bird did have a higher heart rate (333.6 ± 11 beats min−1) despite the lower V˙CO2 (157.4 ± 8.4 ml CO2 kg−1 min−1) in normoxia than the other birds, likely also contributing to its exceptional performance. There was a significant main effect of timepoint (F4, 71.036=11.4269, p<0.0001), which held within each oxygen level (normoxia: F4, 71.17=6.333, p=0.0002; moderate hypoxia: F4, 71.01=3.547, p=0.0107; severe hypoxia: F4, 71.01=3.497, p=0.0115). Thank you for submitting your article "Reduced metabolism and increased O2 pulse support hypoxic flight in the bar-headed goose (Anser indicus)" for consideration by eLife. Flight is very metabolically costly at high-altitudes because birds need to flap harder in thin air to generate lift. We suggest that this would largely be possible via a reduction in metabolism in hypoxia, while maintaining the heart rate and relative-increase in O2 pulse also measured in flight in normoxia. If it is publicly available, please include a URL in the reference. Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus. The work is made available under the Creative Commons CC0 public domain dedication. The gas analyzer was calibrated to account for sensor drift using: 1) two point calibration for CO2, 0% and 1.0% CO2 balance air (Praxair Canada, Scarborough, ON, Canada); 2) a single point calibration for O2 at a baseline of 20.95% for dried room air at experimental flow rates since zero is extremely stable (Fedak et al., 1981). We intended Supplementary file 1 to show directly comparable data, as is Figure 2—figure supplement 1 where data are plotted by individual bird for direct comparison. Discover releases, reviews, credits, songs, and more about Bar-Kays - Flying High On Your Love at Discogs. Experimental flights took place primarily during times that corresponded to spring and fall migration of wild bar-headed geese (Jan. 2011-Nov. 2012). Flight duration of (A) 3.3 minutes, (B) 4.2 minutes, (C) 5.7 minutes, and (D) 5.5 minutes. raised bar-headed geese from eggs, with experimenters acting as the birds’ foster parents. They have been documented flying at altitudes as high as 7,290 m (Bishop et al., 2015; Hawkes et al., 2013). Bar-headed geese are native to Central Asia. There was a significant effect of oxygen level on venous Po2 at rest (F2, 17.33=27.775, p<0.0001). This product has not been reviewed yet. There was a significant effect of oxygen level on flight duration (F2, 363.35=6.55, p=0.0016). It would benefit the lay reader to have this, and the reason for this study, explained in the Abstract. Why did the authors not mix nitrogen with ambient air upstream of delivery to the mask? Stable data were obtained under all conditions for V˙CO2, however it was not possible to gather reliable V˙O2 data in hypoxia (as in other studies: Hawkes et al., 2014). (links to download the citations from this article in formats compatible with various reference manager tools), (links to open the citations from this article in various online reference manager services),, Exercise-induced hypercapnia in the horse,, Energiewechsel von kolibris beim schwirrflug unter höhenbedingungen, The roller coaster flight strategy of bar-headed geese conserves energy during himalayan migrations,, The aerodynamics of hovering insect flight. Again, heart rates were not significantly different when flying in hypoxia. Increases in heart rate contributed less (between 2 and 3-fold), with large variations in heart rate at any level of CO2 production and vice versa. It is quite possible that while flying under the more metabolically challenging conditions of hypoxia, the birds are minimizing energy supply to less essential processes (e.g. We are indebted to Gordon Gray and the staff of the UBC Centre for Comparative Medicine for their tireless support and expertise in animal care. 3) There should be discussion of the issue of the minimum cost of flight and the possibility that hypoxic birds "cheated" to remain aloft, since the major finding was that metabolic rate decreased during forward flight in hypoxia. V˙o2 and V˙CO2 were measured using mask respirometry. The arterial PO2 of geese flying at 0.105 FiO2 was similar to that of geese running on a treadmill in a previous study at 0.07 FiO2 (Figure 4; Hawkes et al., 2014). This video cannot be played in place because your browser does support HTML5 video. We have added some discussion of the possibility that the birds are simply employing the most efficient (minimal cost) flight pattern as suggested by the reviewers (subsection “Effects of Hypoxia”, last paragraph). Thirty-eight-year-old executive chef Jon Cropf has only been living in the Maggie Valley area for a few weeks, but he already feels at home. Only one site, either arterial or venous, was targeted per surgery and subsequent flights (n=5 birds). To better understand how the bar-headed goose accomplishes its remarkable, high altitude migration, Meir et al. At the end of the experiments the cannulae were removed and the animals inspected by veterinary surgeons and recovered in outdoor aviaries. Such adaptations are distributed throughout the oxygen transport cascade, the steps involved in oxygen transfer from atmosphere to mitochondria (ventilation, lung oxygen diffusion, circulation and tissue oxygen extraction) (Scott et al., 2015). So, for the November release of their second Mercury LP, Flying High on Your Love, the inner sleeve featured the band's photos -- complete with star signs. Alternatively, they may increase efficiency by "cheating" and taking advantage of turbulence or lower-speed regions created by the operator and experimental apparatus, a possibility you should also note. We thank Charles Bishop, Sally Ward, and Pat Butler for helpful suggestions and correspondence during the experimental design and training phases and for critical feedback through numerous discussions. The bar-headed goose is famed for migratory flight at extreme altitude. Cultural depiction Human subjects: Although the subjects in this study were not human, the investigators do appear in supplementary files (photographs). Comm. Three bar-headed geese also flew in severely hypoxic conditions [equivalent to an altitude of roughly 9,000 m (0.07 FiO2)], at least for the short duration of flights in this study. Although wing-beat frequencies of our birds were higher than those of bar-headed geese in the wild (Bishop et al., 2015), values were similar between normoxic vs. hypoxic and instrumented vs. uninstrumented flights (Supplementary file 4; Whale, 2012). A second important finding was that heart rate showed little change during hypoxia. relied on periodic averages. All Po2 values were temperature corrected for construction of Po2 profiles as previously described (Ponganis et al., 2007). The bar-headed goose is famous for reaching extreme altitudes during its twice-yearly migrations across the Himalayas. To date, however, there has been no work that has comprehensively measured how the bar-headed goose adapts its physiology to fly under low oxygen conditions.