Seasonal Adaptations in the Breathing Mechanics of High Arctic Ptarmigan.

Lead Research Organisation: University of Manchester
Department Name: Life Sciences

Abstract

Rock Ptarmigan (Lagopus mutus) inhabit the alpine regions of the northern hemisphere. A sub species of these birds found only on the high arctic islands of Svalbard, Norway seasonally deposit very large amounts of body fat. This fat serves as emergency stores of energy for the arctic winter when these birds repeatedly face potentially lethal periods of total starvation, due to extreme weather in combination with permanent darkness. In summer these birds normally weigh less then 0.5kg but during autumn their mass doubles to around 1kg, with body fat making up more than 30% of their body weight. This adaptation to life in high arctic conditions represents a significant physiological challenge for these animals, not only in providing the resources to deposit such a large amount of fat but also functioning with the relatively large extra body mass. The Codd lab has recently demonstrated that accessory breathing structures found on the ribs (uncinate processes) act as levers for the forward and downward movement of the ribs and sternum, respectively, when the bird is breathing in and also as a mechanical strut for muscles to pull the sternum up when the bird breathe out. Interestingly these structures vary in length depending if the bird is adapted to running, flying or diving. The rock ptarmigan have unique uncinate processes which suggest there may be fundamental differences in their mechanics of ventilation. Moreover, because during winter the additional mass is primarily deposited around the breast musculature and abdomen, respiratory movements may also be severely affected. We believe that L. m. hyperboreus will demonstrate respiratory adaptations that may the recruitment of novel accessory breathing muscles and pelvic aspiration to ventilate their lungs when their body mass is high. We will use electromyography to determine whether target muscles are active during ventilation or locomotion. Interclavicular and abdominal air sacs pressure will be recorded and locomotion will be monitored using video footage. For metabolic power we will use respirometry. The Department of Arctic Biology (University of Tromso) where experiments will take place is well set up for the maintenance of ptarmigan colonies under natural conditions; expertise and facilities which are not available in the UK. Examination of the breathing mechanics of ptarmigan will be fascinating and shed new light on the complexities of avian respiration. Our study will be the first to determine the effect of seasonal fluctuations in body mass to the mechanics of breathing in birds.

Technical Summary

Unlike mammals, birds breathe not by contraction and relaxation of a muscular diaphragm but by the rhythmic pumping up and down of the sternum, which in turn facilitates the bellows-like movement of air through the air sac system to the lung, where gas exchange occurs. The avian lung is highly efficient and complex, with each breath taking an average of two cycles of inspiration and expiration to move through the respiratory system. In birds both inspiration and expiration are active processes driven by the hypaxial musculature; in conjunction with rib movements, the sternum is actively moved downwards during inspiration and pulled upwards during expiration. Recent work has demonstrated that acessory breathing structures, the uncinate processes, play a crucial role in both inspiration and expiration in birds. A sub species of Rock Ptarmigan, found only on the high arctic island of Svalbard, Norway, seasonally deposit large amounts of fat around the breast and abdominal regions which helps them to survive overwinter. These seasonal changes in weight represent a significant challenge for these birds as this increased mass must continually be moved up and down with each breath. Therefore, this project will examine adaptations in the respiratory mechanics of summer (low body mass) and winter (high body mass) Svalbard Rock Ptarmigan. I will use electromyography to determine whether target muscles are active during ventilation or locomotion. Interclavicular and abdominal air sacs will be cannulated with polyethylene tubing connected to miniaturised differential pressure transducers which will record changes in pressure. Locomotion will be monitored using video footage and accelerometry. Matching kinematic data with ventilation will enable the quantification of the degree of coupling. Metabolic power will be calculated using respirometry.

Publications

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Brocklehurst RJ (2020) Respiratory evolution in archosaurs. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Brocklehurst RJ (2019) XROMM kinematics of ventilation in wild turkeys (Meleagris gallopavo). in The Journal of experimental biology

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Codd JR (2010) Uncinate processes in birds: morphology, physiology and function. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Lees JJ (2012) Understanding sex differences in the cost of terrestrial locomotion. in Proceedings. Biological sciences

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Mármol-Guijarro A (2021) The Influence of Snow Properties on Speed and Gait Choice in the Svalbard Rock Ptarmigan (Lagopus muta hyperborea). in Integrative organismal biology (Oxford, England)

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Nudds RL (2010) Energetics and kinematics of walking in the barnacle goose (Branta leucopsis). in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Perry SF (2010) The evolutionary origin of the mammalian diaphragm. in Respiratory physiology & neurobiology

 
Description This project has shed new and important light on the energetics and biomechanics of locomotion in an animal that shows marked seasonal changes in body mass - namely the more than doubling of body weight during winter including the acquisition of more than 30% body fat reserves. The key findings are summarised below:



1) svalbard ptarmigan are exceptional athletes capable or three distinct locomotor gaits - walking, grounded running and aerial running. Through our work we were able to demonstrate that for the first time in a small bipedal runner a drop in the metabolic cost of locomotion upon the switch to an aerial gait. These data were published in Proceedings: Nudds RL, Folkow LP, Lees JJ, Tickle PG, Stokkan K-A & Codd JR (2011) Evidence for energy savings from aerial running in the Svalbard rock ptarmigan (Lagopus muta hyperborea) Proc. Roy. Soc. B. 278: 2646-2653 (doi:10.1098/rspb.2010.2742)



2) We compared the metabolic cost of locomotion in summer (when the birds and thin) and winter (when the birds are fat) remarkably we found that during winter despite these birds being more than double their summer body weight they are able to move around more efficiently than in the summer - however the birds are unable to aerial run. These data were published in PLoS ONE: Lees JJ, Nudds RL, Stokkan K-A, Folkow LP & Codd JR (2010) Reduced metabolic cost of locomotion in Svalbard rock ptarmigan (Lagopus muta hyperborea) during winter. PLoS ONE. 5(11): e15490 (doi:10.1371/journal.pone.0015490)



3) we also compared the metabolic cost of locomotion in male and female birds. These data indicated that there were differences between the sexes - with male birds being able to run faster and at a reduction in energetic cost thought to be a result of sexual selection on male performance to ensure successful maintenance of breeding grounds and harem access. These data are important as many studies do not take sex of the animal into account which potentially cloud the results from this work. These date were published in Proceedings: Lees JJ, Nudds RL, Folkow LP, Stokkan K-A & Codd JR (2012) Understanding sex differences in the cost of terrestrial locomotion. Proc. Roy. Soc. B. 279: 826-832 (doi:10.1098/rspb.2011.1334)



4) we also looked at the development of locomotor performance in juvenile male ptarmigan. Generally many studies focus on adults however it is the juvenile birds that typically suffer the greatest predation - this is especially pertinent for birds in the Arctic who must survive their first winter. We were able to show that in the Svalbard ptarmigan the young rapidly develop adult levels of performance and that this is a key adaptation to enable them to survive the harsh Arctic winter in good condition for breeding the following spring. These data were published in Polar Biology: Lees JJ, Stokkan K-A, Folkow LP & Codd JR (2012) Locomotor development in the Svalbard rock ptarmigan (Lagopus muta hyperborea) Polar Biol. 35:869-874 (doi:10.1007/s00300-011-1131-x)



5) Much of the research on animal locomotion is carried out on treadmill with animals running on the level - however in the wild the environment is varied and moving up or down inclines must be achieved. We examined the influence of running up different incline grades on the energetics and biomechanics of locomotion and found that the animals experience different costs depending on how steep the slope is that they must move up. These data are published in JEB: Lees JJ, Folkow LP, Stokkan K-A & Codd JR (2013) The metabolic cost of incline locomotion in the Svalbard rock ptarmigan (Lagopus muta hyperborea): the effects of incline grade and seasonal fluctuations in body weight. J. Exp. Biol. in press
Exploitation Route These data have provided new information that can be used to understand and to ultimately protect this Arctic species. the Svalbard ptarmigan are listed as a bioindicator species for biodiversity in the Arctic and the information we have obtained can lead to the development of better strategies for managing this species. This is particularly pertinent given the potential impact of climate change on the Arctic regions. These data have looked at how these birds are able to adapt to carrying large amounts of body fat and have some spin offs for research into obesity and understanding its influence on how animals, including humans, move around.
Sectors Environment

 
Description data we collected are being used in conjunction with population survey data collected by the norwegian polar institute towards developing a new species management plan for the Svalbard ptarmigan
First Year Of Impact 2010
Sector Environment
Impact Types Policy & public services

 
Description University of Tromso 
Organisation University of Tromso
Country Norway 
Sector Academic/University 
PI Contribution The research was based at the University of Tromso we contributed manpower as myself and the PDRA stayed in Tromso during the course of data collected - this facilities knowledge transfer between the 2 universities
Collaborator Contribution The research was based at the University of Tromso and made use of their animals holding facilities and laboratory space during the course of all data collection in the project
Impact all publications are in collaboration with Professors Lars Folkow and Karl-Arne Stokkan at the University of Tromso
Start Year 2009
 
Description High arctic avian athlete gives lessons about animal welfare 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Press release via BBSRC News and Events pages that was picked up and run in national and international media outlets web site link video of research being undertaken

no actual impacts realised to date
Year(s) Of Engagement Activity 2010,2011,2012,2013