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Racing the wind. Water economy and energy expenditure in avian endurance flight

(2005) Engel, Sophia Barbara

Ever since Ikarus, bird flight has been a fascinating miracle to man. Fragile birds cross deserts and overcome mountain ranges. They endure fasting, adverse climates, span the globe on the wing. What are the traits that make such a performance possible, what are the trade-offs, what the limitations?
This thesis is meant as a contribution to an integrated understanding of the challenges associated with avian flight, and the ways in which animals cope with them both physiologically and behaviourally. The experiments presented here deal with the different sometimes opposing demands on a bird’s energy and water budget during sustained flight periods under controlled ambient conditions in a wind tunnel.

The challenges of avian long distance migration
Powered flight as a means of locomotion is a salient characteristic of birds, and migratory endurance flight is outstanding in its high sustained metabolic demands compared to other activities in a bird’s life. The physiological mechanisms and adaptations that enable some species to cross the globe on their way from wintering to breeding grounds and back again, traversing vast inhospitable areas like deserts or oceans without eating or drinking, are part of the mystery that still waits to be solved. Three factors have been suggested as shaping the physiology and behaviour of migrants: time, energy and safety. For the flight period itself, energy is generally considered to be the most important factor of the three, due to the very high sustained metabolic rates. A fourth factor that has not received much attention but might be equally important is water. Long migratory flights may sometimes be limited by dehydration rather than by energy depletion. Energy and water management are closely interlinked and to assess the physiological challenges of long distance flights neither factor can be studied in isolation.
During their natural migratory flights, birds change their position in a three dimensional world, thereby choosing from a continuum of ambient conditions, temperature, air pressure, humidity, wind direction or speed, to name only a few. All of these have an effect on flight performance, sometimes in conflicting directions for energy metabolism or water flux: Ambient temperature is dependent on geographic location, season, time of day and flight altitude. Through its effect on thermoregulation, temperature is one of the main factors affecting evaporative water loss. While birds can in principle choose a preferred temperature during their flights by adjusting flight altitude, air pressure changes concurrently. This has effects on flight costs (negatively related with air density), but also on respiration (via decreasing oxygen partial pressure) and evaporation (via decreasing ambient humidity, which increases the driving force for evaporation). To complicate a bird’s decision even further, wind direction and wind speed are also dependent on geographic location, season and altitude. In principle, tail or head winds do not affect flight costs per se, as a bird is moving with its surrounding air, like a balloon carried by a breeze. Active flight leads to movement of the bird relative to the air, irrespective of the air’s movement. Wind conditions affect the bird’ s movement with respect to the ground. This is what matters for a migrating bird, especially if it is under time pressure to arrive at the breeding grounds in time. Therefore, a bird may choose its flight speed according to wind conditions (increase its flight speed to offset a head wind, for instance). Flight speed is a factor assumed to determine energy requirements during flight. Flight costs, migration speed, flight route and flight altitude might therefore be affected by prevalent wind conditions.

The factors affecting energy costs of flight
During flight, birds can sustain metabolic rates of more than ten times basal metabolism for several hours or even days. This is about twice the maximum sustained metabolic rate of similarly-sized running mammals. What are the physiological adaptations of birds to these high sustained metabolic demands, and which factors determine flight costs in birds? Body mass is an important factor determining energy costs of flight: Interspecific comparisons have generated allometric equations that allow an estimate of flight costs for any species based on body mass.
Intraspecifically or intraindividually, the scaling of flight costs and body mass is less clear. It appears, though, that flight costs increase less dramatically than predicted by interspecific allometry. Aerodynamic theory has led to mathematical models designed to predict mechanical costs of flight for any bird and under different ambient conditions. Following the elementary physical principles that the power to generate lift is inversely proportional to flight speed, and the power needed to generate thrust increases with the speed cubed, flight costs as the sum of both are predicted to depend on flight velocity in a U-shaped curve. This mechanical power output is only a fraction of the total metabolic power expended during flight. The major part of the metabolic energy ends up as heat and has to be dissipated. Further energy is required for respiration and circulation to supply the tissues with metabolites and oxygen, and for some basic physiological processes that are not directly involved in the generation of flight muscle work. The whole-body efficiency at which metabolic power is transformed into mechanical work remains poorly understood. We also do not know whether muscle efficiency is a fixed factor irrespective of body mass or flight velocity.
Calculations of metabolic power requirements on the basis of aerodynamic modelling can be only tentative for these reasons. The application of aerodynamic theory for fixed wing aircraft, which is the basis of all available models, gets complicated further by the fact that most birds usually use flapping flight instead of gliding, thereby changing the shape of the wings continuously by stretching or flexing them. They can vary the angle of attack, wing beat frequency, and wing beat amplitude, as well as using intermittent flight and changing many other parameters that might affect flight costs. Although the predicted U-shaped power curve applies well to aircraft, experimental evidence for birds is weak and controversial. Most studies report flight costs and power-to-speed relationships only for short flights. Migratory flights differ substantially from short flights both in energetic costs and in physiological processes underlying these costs. For example, short flights are powered mainly by muscular and hepathic carbohydrate stores. Endurance flight is fuelled by the combustion of extramuscular fat reserves, accompanied by a small but important fraction of protein catabolism. Therefore, to understand the physiology of bird migration we need more studies on long duration flight under controlled environmental conditions.
The factors affecting water fluxes during flight
Water gain through metabolic water production is the only positive part in the water balance equation of a flying bird, standing against water loss through excretion and evaporation. High metabolic rates as they occur during bird flight are associated with a high production of metabolic water. The exact amount of water formed in the chemical process of fuel oxidation depends not only on the metabolic rate but also on the fuel type (carbohydrates, fat or protein) and the end product of protein metabolism: urea or, in the case of birds, uric acid. Apart from other possible physiological functions of protein catabolism, it could help to counteract dehydration during flight because it releases more water per unit energy than lipid combustion.
Water loss via excretion and evaporation is inevitable, and both processes are affected by physiological requirements other than the need to conserve water. The primary function of excretion is the elimination of metabolic waste products, which must be accompanied by water. This obligatory water loss – albeit limited by the excretion of non-soluble uric acid - and the high metabolic rate during flight could conceivably constrain the bird’s ability to reduce excretory water loss. Evaporation is a basic physical process following the water vapour pressure gradient between the bird’s body (skin and respiratory surfaces) and the environment. Still, resting birds can regulate their evaporation rates within certain limits by changing the lipid composition in the skin, thereby regulating cutaneous evaporation or by cooling the respired air below body temperature upon exhalation, thereby reducing respiratory evaporation.
During flight and its associated high levels of heat, evaporation plays an important role in thermoregulation, especially at high ambient temperatures. Although a powerful means of heat dissipation, cooling by evaporation implies the risk of dehydration. Heat balance and water fluxes during flight, both in and out, are still poorly quantified.

Experimental approaches to assess energy costs and water fluxes during flight
To assess the energetics and water economy of bird migration, studies on free flying birds under natural conditions would be desirable. There are major technical difficulties in obtaining such measurements. Furthermore the ambient conditions during natural migratory flights are hardly constant nor comparable between different locations. This limits the feasibility and value of such measurements.
To control and manipulate effects of ambient conditions on bird flight performance, we conducted experiments in a large wind tunnel.
Research questions and outline of the thesis
We chose a few key aspects of flight physiology to study in the wind tunnel, which define the scope of this thesis. We focused on the water economy of birds flying at a range of ambient temperatures, on energy metabolism - since metabolic water production is the only source of water influx during flight – and on the two main factors that determine the amount of water lost with the ventilated air: exhaled air temperature and respiratory air flow.

In chapter 2 we present energy requirements and evaporation rates of resting Rose Coloured Starlings (Sturnus roseus) as determined in a temperature-controlled metabolic chamber at temperatures between 7 °C and 30 °C. The relationship between total evaporation (TEWLr ) and ambient temperature (Tamb ) was best described by two linear regressions. At temperatures below 21.9 °C, TEWLr was on average 6.73 ± 1.07 g d-1 and increased only slightly with Tamb, following the equation TEWLr = 0.09 · Tamb + 5.28 [g d-1]. At higher temperatures (Tamb > 21.9 °C), the relationship was much steeper, following TEWLr = 0.37 · Tamb – 0.68 [g d-1].
Resting metabolic rate (RMR) was positively correlated with body mass and was therefore expressed as mass-specific metabolic rate. The relationship between RMR and Tamb was best described by two linear regressions. At temperatures above 12.9 °C mass specific RMR was constant at 0.021 ± 0.001 W g-1. At lower temperatures, RMR was negatively correlated with Tamb following RMR = 0.0011 · Tamb + 0.0366 [W g-1]. These data allow a comparison of resting energy expenditure and total evaporative water loss with flight measurements, as determined in the following chapters.

In chapter 3 the metabolic costs of flight at a natural range of speeds were investigated in Rose Coloured Starlings (Sturnus roseus) using doubly labelled water. Eight birds flew repeatedly and unrestrained for bouts of six hours at speeds from 9 to 14 m s-1 in a low-turbulence wind tunnel, corresponding to travel distances between 200 and 300 km, respectively. This represents the widest speed range where we could obtain voluntarily sustained flights. From a subset of these flights data on the wing beat frequency and intermittent flight behaviour were obtained. Over the range of speeds that were tested, flight costs did not change with velocity and were on average 8.17 ± 0.64 W. Body mass was the only parameter with a significant (positive) effect on flight costs, which can be described as EEf=0.741· M 0.554. Wing beat frequency changed slightly with speed, but correlated better with body mass. Birds showed both types of intermittent flight, undulating and bounding, but their frequencies did not systematically change with flight speed.

In chapter 4 we combine data on total body water and water fluxes (derived from DLW measurements) during flight in Rose Coloured Starlings, with mass balance calculations of net water loss. These data allow the estimation of total evaporative water loss and the modelling of heat balance during flight. During all flights, the birds experienced a net water loss. Water influx was on average 0.98 g h-1 and water efflux 1.29 g h-1, irrespective of flight speed. Evaporation was related to temperature in a biphasic pattern. At temperatures below 18.2 °C net evaporation was constant at 0.36 g h-1, rising at higher temperatures with a slope of 0.11 per degree to about 1.5 g h-1 at 27 °C. We calculated the relative proportion of dry and evaporative heat loss during flight. Our data suggest that for prolonged flights Rose Coloured Starlings should adopt behavioural water saving strategies and that they can not complete their annual migration without stopover to replenish their water reserves.

In chapter 5 we present data on exhaled air temperature of flying and resting ducks. Exhaled air temperature was measured with a microbead thermistor at the nostril of the birds which was connected to a recording system via thin copper leads. A thermistor changes electrical resistance with temperature and can therefore be used as thermometer. Exhaled air temperature (Texh) has a paramount effect on respiratory water loss during flight. For migratory birds, low Texh potentially reduces water loss and increases flight range. The aim of this study was to record Texh of birds during rest and flight at a range of controlled ambient temperatures (Tamb). One wigeon and two teal flew a total of 20 times in a wind tunnel at Tamb ranging from 1 to 24 °C. Texh during flight did not differ between the two species and was strongly correlated with Tamb (Texh = 1.036 Tamb + 13.426; R2 = 0.58). In addition, body temperature had a weak positive effect on Texh. At a given Tamb, Texh was about 5 °C higher during flight than at rest. The steep slope of the relationship between Texh and Tamb during flight indicates that Texh is actively regulated and not simply the result of passive heat exchange.

In chapter 6 we assessed respiratory water loss in European Starlings (Sturnus vulgaris) both at rest and during steady flight in a wind tunnel over a range of ambient temperatures using respiratory air flow and exhaled air temperature data. In resting Starlings, breathing frequency (f) was constant at 1.4 ± 0.3 Hz at ambient temperatures (Tamb) between 6 °C and 25 °C. Also tidal volume (Vt, ml) was independent of Tamb with an average value of 1.9 ± SD = 0.4 ml. There was a negative correlation between Vt and f (Vt = -1.01 × f + 3.30; n = 17; p < 0.01; R2 = 0.45). Mean ventilation rate (Vmin, ml min-1), the product of f and Vt, was 156 ± 28 ml min –1 (n = 17) at all Tamb. Exhaled air temperature (Texh) during rest was strongly dependent on Tamb (Texh = 0.92 × Tamb + 12.45; n = 23; p < 0.001; R2 = 0.89). Respiratory water loss at rest (REWL) averaged 0.18 ± 0.09 ml h-1 (n = 10) and was independent of Tamb, but showed a slight positive dependence on f and Texh. In flying Starlings, f was on average 4.0 ± 0.4 Hz (n = 44) and unchanging over the range of Tamb measured. Vt during flight averaged 3.6 ± 0.4 ml (n = 25) and increased with Tamb (Vt = 0.06 × Tamb + 2.83; n = 25; p < 0.01; R2 = 0.29), as a consequence, the volume of ventilated air during flight (average Vmin = 789.9 ± 210.0 ml min-1), increased with Tamb as well. Texh during flight was 4.6 °C higher than at rest and strongly dependent on Tamb (Texh = 0.85 × Tamb + 17.29; n = 36; p < 0.001; R2 = 0.74). All factors together result in respiratory water loss during flight (average REWLf = 0.74 ± 0.22 ml h-1) significantly higher than at rest and increasing with Tamb. REWLf correlated best with the water vapour pressure deficit (VPD, hPa) in ambient air. From our measurements and data from the literature, we conclude that respiratory evaporation accounts for most water loss in flying European Starlings and increases to a higher degree than cutaneous evaporation with rising ambient temperature.

Chapter 7 synthesizes the experimental results presented in this thesis. Our data are integrated into available literature data on short and long flights. We discuss these results also in the context of field studies to draw a picture as complete as possible of the energy and water requirements during long distance flight.

file:Title and contents
file:Chapter 1
file:Chapter 2
file:Chapter 3
file:Chapter 4
file:Chapter 5
file:Chapter 6
file:Chapter 7
file:Addresses of Co-authors
file:Complete thesis

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