Bird Flight Energetics - from tissues to free-flight

Birds are amongst the most diverse, successful and ecologically important groups on earth and flight is key to their success. However, flight is one of the most energetically expensive modes of locomotion and there are few aspects of a bird's ecology, behaviour and physiology that are not affected by its energetic demands. In all modes of locomotion, energetics and locomotor performance are linked via an energy transduction cascade in which muscles convert chemical energy (derived from food) into mechanical work that is transferred to the environment to produce movement. Free-flight energy expenditure is difficult to measure directly, but proxies (components of the energy transduction chain such as heart rate and body acceleration) have been shown to be generally related to metabolic rate. However, underlying assumptions and simplifications inherent in these indirect approaches have not been rigorously assessed and validated for animals during flight. Ideally, the transfer of energy between all levels of organization should be determined: a full understanding of the system is required to improve the predictive power of using proxies as indicators of metabolic rate. This is achievable in bird flight by combining research expertise in muscle physiology and flight energetics at Leeds with expertise in studying free-flight using physiological and biomechanical sensors and modelling flight energetics at Bangor.

The overall aim of this project is to use a multidisciplinary approach to determine the relationship between the mechanical performance and energy utilisation of birds during flight across a range of speeds, its partitioning at the level of individual muscles and non-muscular systems, and the functional linkage to the indirect measures of heart rate and dynamic body acceleration. To achieve this goal, we will track the transduction of energy by quantifying the following. First, we will determine the whole organism metabolic rate of species with a U-shaped power curve, by measuring the rates of oxygen consumption and carbon dioxide production during flight in a wind tunnel, while simultaneously recording heart rate, dynamic body acceleration and kinematics. This has not yet been undertaken for any flying animal. Second we will use regional blood flow as a measure of tissue-level energy expenditure, enabling us to separate out the factors contributing to overall flight energy expenditure by quantifying the energy used by all of the muscles and by other, non-muscular physiological systems (e.g. respiratory, circulatory and homeostatic) in relation to flight speed. Third, the mechanical performance of the major flight muscles will be determined by measuring their length change and activity patterns during flight and simulating these conditions in vitro to measure force and power generation. By recording the 3D kinematics of the wings and body we will be able to characterize the instantaneous accelerations and, by extension, the instantaneous aerodynamic forces. By integrating energetics and mechanical measurements we will obtain the most comprehensive understanding of the energy transduction chain for any flying animal.

Ultimately, we will establish the detailed relationship between whole organismal and tissue-level metabolic energy expenditure with that of proxies of energy turnover that can be measured in the field and that lie at opposite ends of the energy transduction chain: heart rate and 3-axis accelerometry and 3-axis gyroscope. These integrated measurements will allow us to refine and improve the predictive power of using such proxies as indicators of metabolic rate. The wind tunnel based studies will provide a firm footing understanding animal flight behaviour in the field. These results may also inform decisions in conservation, land use planning and public health issues; to mitigate the combined effects of habitat fragmentation and climate change, or when birds are implicated in the spread of disease.

In all modes of locomotion, energetics and locomotor performance are linked via an energy transduction cascade in which muscles convert chemical energy into mechanical work that is ultimately transferred to the environment to produce movement. A full understanding of this system is required in order to refine the use of proxies as indicators of metabolic rate in the field. Flight is one of the most energetically expensive modes of locomotion and understanding free-flight energetics is key to understanding the behavioural ecology of birds. The ultimate aim of our proposal is to provide validated and robust approaches to measuring energy use in the field, based on comprehensive physiological and biomechanical datasets from birds flying in a wind tunnel. Specifically we will: (1) measure organismal and tissue-level energy expenditure, of species with a U-shaped power curve; (2) determine the mechanical function of the flight muscles; and (3) quantify 3D body and wing kinematics. By integrating energetics and mechanical measurements we will obtain the most comprehensive understanding of the energy transduction chain for any mode of locomotion. Simultaneously, we will also measure proxies of energy expenditure that can be measured in the field and that lie at opposite ends of the energy transduction chain: ECG (post-processed to heart rate) and 3-axis accelerometry and 3-axis gyroscope. We will establish and quantify the link between both heart rate, dynamic body acceleration and organismal metabolic rate throughout the velocity range. Having validated models of locomotory performance that can be used in the field is important as they can provide insight into many areas of biology. Not only for the scientific value of understanding animal flight behavior and energetics, but to inform decisions in conservation, land use planning and public health issues; thus helping to mitigate the combined effects of habitat fragmentation and climate change, or disease transmission.

Obtaining an integrative understanding of locomotor energetics and its interaction with the environment is of broad scientific relevance and will have impact on the aeronautic industry, the general public, ecological and conservation NGO's and on the researchers employed on the grant, in addition to the benefits to the academic community (see Academic Beneficiaries).

APPLIED LINKS WITH THE POTENTIAL TO IMPROVE HEALTH & DEVELOP THE 3Rs
The knowledge gained in this project will help in the development and refinement of computational models of muscle contraction. Our work is focused on healthy muscle tissue works, which is central to developing an understanding of malfunctions that occur during ageing and disease. In all modes of locomotion, energetics and locomotor performance are linked via an energy transduction chain. Therefore, whilst our work is on flying birds the models developed should be generally applicable to other modes of locomotion and the development of an understanding of locomotor energetics in the field. Developing accurate computational models of muscle contraction may allow some animal experiments to be replaced and in other cases refined or reduced as model simulations may allow research efforts involving animal research to be better designed.

There has recently been a notable increase of interest in the local, national and international changes in the distribution of organisms in response to climate change. Some organisms have considerably modified their ranges while others have not. Flight energetics is an important factor that could influence the migratory paths, distribution and survival of birds. An improved ability to study energetics in the field will enhance our understanding of how flight energetics can vary between different species or individuals or between different years. This provides a useful tool, alongside ecological and developmental factors, to help explain current changes in population and species distribution and in predicting which species are likely to be adversely or favourably affected by future changes in climate. For example, differential survival in populations taking different migratory routes and flyways could have implications for population and species level conservation management of stop-over sites and/or the spread of avian-borne diseases. The rapid increase in the number of migratory species being studied has revealed the importance of higher resolution data at the individual and population level and the need to understand the ecological and energetic drivers that underpin lifetime reproductive success.

IMPACT ON THE GENERAL PUBLIC
Animal locomotion is a topic that consistently arouses public interest. We are committed to using our research to inspire young audiences to take an interest in science. Our work will have a positive impact by informing the general public about technological advances in animal science and the applications of biological research. We will engage with the public through open lectures, school visits and exhibitions (e.g. Great Yorkshire Show, Leeds City Museum, Bangor Science Festival). There will also be opportunities to publicise our work through Institutional webpages, twitter, and writing articles for "The conversation" and other related science blogs, while also conducting interviews with radio, print and internet-based journalists (such as the "The Naked Scientists").

OTHER SPECIFIC IMPACTS
Specific beneficiaries include the PDRA who will develop their scientific career with BBSRC funding. They will be involved in a multi-disciplinary research project that integrates physiology, biomechanics and modelling approaches. They will benefit from working closely with laboratories in different leading institutions (as verified by the 2014 REF). The research will also impact on the training of undergraduates who will benefit from carrying out final year research projects and postgraduates completing MSc or PhD's within our laboratories.