J. exp. Biot. 160, 233-262 (1991) 2 3 3Printed in Great Britain © The Company of Biologists Limited 1991

EXERCISE IN BIRDS

BY P. J. BUTLER

School of Biological Sciences, University of Birmingham, Birmingham,B15 2TT, United Kingdom

Summary

Birds have two independent locomotor systems: the forelimbs (wings) are usedpredominantly for aerial flight, but may be used for underwater propulsion, e.g. inpenguins; the hindlimbs (legs) are used for running, surface swimming and diving.In birds of similar mass, energy consumption during flight is approximately 2.5times greater than that when running or swimming at maximum speed. Thisdifference is the result not only of the larger mass of the flight muscles comparedwith that of the leg muscles, but also of their greater oxidative capacity.Interestingly, the relationship of energy consumption to body mass in cursorialbirds when running is similar to that of volant birds when flying. Energyconsumption during diving may be as high in some birds (e.g. tufted duck) as whenthey are swimming at maximum sustainable speed, and this is not influenced bywater temperature.

The composition of the flight and leg muscles is different. The muscles of the legconsist of deeply situated slow oxidative (SO) fibres, which are active during quietstanding and walking, fast oxidative glycolytic (FOG) fibres, which are recruitedduring walking and sustained running or swimming, and peripherally located fastglycolytic (FG) fibres, which are recruited at the highest running or swimmingspeeds. In most volant birds, the pectoralis muscle consists predominantly of FOGfibres with a smaller percentage of FG fibres. There is some controversy over theoccurrence of SO fibres in some species, although they are most probably presentin those that glide. The FOG fibres are highly oxidative, with a high capillarydensity.

The respiratory and cardiovascular adjustments that occur during flying,running and diving are described, and the ability of some species of birds to fly atextremely high altitudes, where the partial pressure is one-third of the sea levelvalue, is discussed.

Introduction

An important feature of exercise in birds is the fact that most of them have twoindependent locomotor systems. The forelimbs (wings) are used predominantlyfor aerial flight, but in some species, most notably the penguins, they are used forunderwater propulsion. The hindlimbs (legs) are used for running, surface

words: birds, flying, running/swimming, diving.

234 P. J. BUTLER

swimming and diving. This review will therefore look at oxygen uptake duringvarious forms of locomotion performed by a range of species of birds, the musclesof the legs and breast that generate the extra demand for oxygen duringlocomotion, and the role of the respiratory and cardiovascular systems combinedin presenting the necessary oxygen to the working muscles.

Exercise in air

Oxygen uptake

It has been noted previously (Butler, 1981, 1982a; Butler and Woakes, 1985)that maximum oxygen uptake (VO2max) in volant birds when running or swimmingis similar to that in mammals of similar body mass (Pasquis etal. 1970), and lessthan half of the minimum oxygen uptake (VO2mw) in birds during level flappingflight. What is more, birds that are exclusively cursorial, such as the domesticcockerel, rhea and emu, have a V^max when running that is similar to V'o min ofbirds during forward flapping flight.

When comparing maximum oxygen consumption during exercise in differentspecies of bird and mammal, values are often given as a multiple of the restingvalue. This is only really of any use if the resting values are obtained understandard conditions, which is not always the case. Making direct comparisonsbetween values of VOl during exercise is complicated by the fact that the animals tobe compared are of different body mass and VOl is not linearly related to mass(Fig. 1). Using data from seven species of birds during forward flapping flight inwind tunnels (Tucker, 1968, 1972; Bernstein etal. 1973; Butler etal. 1977; TorreBueno and Larochelle, 1978; Gessaman, 1980; Hudson and Bernstein, 1983),^o2min (mlrnin"1

STPD) was found to be 149M072 (where M is body mass in kg).Using data for six species of volant birds (Prange and Schmidt-Nielsen, 1970;

Fedak etal. 1974; Bamford and Maloiy, 1980; Grubb, 1982; Woakes and Butler,1983; Warncke et al. 1988)and two species of penguins (Pinshow et al. 1976, 1977)while walking, running or swimming, Vo2max was found to be 60.5M081 and forthree species of cursorial birds (Taylor et al. 1971; Brackenbury and Avery, 1980;Grubb etal. 1983) Vo2max was found to be 145M074. Thus, although the massexponents are not exactly the same for the three groups, these equations (seeFig. 1) illustrate the large (2.4 times for a 1 kg animal) difference in aerobicmetabolism in different species of birds engaged in the same type of exercise(running) and, it is assumed, between different types of exercise (running vsflying) in the same species. The only species, in fact, for which data have beenobtained during forward flapping flight and while running is the pigeon (Butleretal. 1977; Grubb, 1982), in which VOl while flying at 10ms"1 was 77.8mlmin"1

and Vo max while running was 27.4mlmin~1, a ratio of 2.8. During gliding flight,metabolic rate is twice the resting value in herring gulls, Larus argentatus, andapproximately three times the predicted basal metabolic rate in grey-headedalbatrosses, Diomedia chrysostoma (Baudinette and Schmidt-Nielsen, 1974; Costaand Prince, 1987).

Exercise in birds 235

10000

S 1000

I I0.001 0.01 0.1 1.0

Body mass (kg)10 50

Fig. 1. Double logarithmic plots of oxygen consumption (ml min ' STPD) against bodymass (kg) for hovering hummingbirds (A A), birds during forward flapping flight( • • ) , cursorial birds running (A A), volant birds and penguins running orswimming (x x) and bats during forward flapping flight (O O) . For furtherdetails, see text.

Hovering flight is, at least theoretically (Rayner, 1979), energetically very costlyand data from eight studies on six species of hummingbirds (Lasiewski, 1963;Berger and Hart, 1972; Berger, 1974, 1985; Epting, 1980; Bartholomew andLighton, 1986) tend to support this; VOl during hovering is 371M087. However, ifthe data from these six species of hummingbirds are added to those from the sevenspecies of birds during forward flapping flight, the relationship is VOl=\A5M°i69,i.e. no different from that obtained solely from the birds during forward flappingflight. These equations indicate that a 1 kg hovering hummingbird would have anoxygen consumption some 2.5 times that of a lkg bird during forward flappingflight. They also indicate, more realistically, that hummingbirds, when hovering,are using oxygen at a rate that is similar to what would be predicted from dataobtained from larger birds during forward flapping flight. In other words, the highmass-specific values for oxygen uptake during hovering and, perhaps, the activityof aerobic enzymes (see later) in hummingbirds are merely manifestations of the

ometric relationship, with a mass exponent of approximately 0.7. In someof hummingbirds, at least, it appears that ambient temperature has a large

236 P. J. BUTLER

60 i—

50

g 40

I 30exBCO -v,o 2U

10

0 1 - I I I I JF, off F, on 0.25 0.35 0.45 0.55

Water velocity (ms" 1 )

0.65 0.75 0.85

Fig. 2. The relationship between mean (±S.E., N=6) oxygen consumption andswimming speed in trained (•) and untrained (D) tufted ducks. F, off, F, on, flumemotor turned off or on. (From Butler and Turner, 1988.)

influence on VOl during hovering (Schuchman, 1979), whereas in other speciesthere is only a slight effect (Berger and Hart, 1972).

It is interesting to note, in passing, that for five species of bats flying on the levelin wind tunnels, V^mm was found to be 151A/0'71 (Thomas, 1975; Carpenter, 1985,1986) and that this is similar to that for birds during forward flapping flight (Fig. 1).

It is clear from studies on the tufted duck, Ay thy a fuligula, that the level offitness of an animal can have a large influence on VO2max (Butler and Turner,1988). Training resulted in a 27% increase in VOimax in swimming ducks (Fig. 2)or, looking at it the other way round, VO2max

w a s approximately 22 % lower ininactive birds compared with that in active ones. It would be of great interest toknow to what extent flight performance can be influenced by training (see below).

Exercise under water (diving)

Aerobic metabolism

Mean oxygen uptake at mean dive duration has been estimated for freely divingtufted ducks (Woakes and Butler, 1983). Oxygen consumption was measuredbetween dives by way of an open-circuit respirometer and a fast-responding massspectrometer. A linear multiple regression analysis was performed between diveduration, the succeeding duration at the surface and oxygen uptake during thesurface period. The regression coefficients represent the mean oxygen u p t a k e ^mean dive duration and at mean duration at the surface. At a mean dive duratJH

Exercise in birds 237

14.4s (water temperature 13.5°C), mean oxygen uptake (VOl, STPD) was34.0mlmin~1 (57mlmin~1kg~1) and not significantly different from the value(SS^mlmin"1, 63mlmin~1kg~1) obtained from the same ducks swimming atmaximum sustainable speed on the surface. These values are some 3.5-3.8 timesresting oxygen consumption, respectively, and indicate that feeding under wateris, in energetic terms, a very costly business for these animals.

On the basis of the usable oxygen stores in the tufted duck (Keijer and Butler,1982), this species should be able to remain submerged and metabolise aerobicallyat the level given above for approximately 50 s. This is some 2.5 times longer thanthe preferred dive duration of these animals on a 1.9-2.8 m deep pond (Stephen-son et al. 1986), and would suggest that they metabolise completely aerobicallyduring most voluntary dives, using the oxygen stored in the body and replacing itupon surfacing. It could be, however, that oxygen consumption actually decreasesas dive duration progresses beyond 15 s (Bevan et al. 1991). Certainly, obser-vations on individual ducks indicate that mean oxygen consumption at mean diveduration is lower in those that perform longer dives (Fig. 3). This could result fromreduced buoyancy as the dive progresses [in those birds that perform longer divesit could be the result of the reduced volume of the respiratory system (Stephensonet al. 1989a,fr)] and/or it could indicate that aerobic metabolism declines as a diveproceeds with, perhaps, increasing anaerobiosis. This latter suggestion wouldimply associated cardiovascular adjustments (see below).

As the energetic cost of feeding under water is so high for aquatic birds such as

0.8 r-

0.6

o •«

1.9 0.4

H -5

0.2

0.0 L

I I10 15 20 25

Mean dive duration (s)

30 35

Fig. 3. The relationship between mean oxygen consumption at mean dive durationand mean dive duration from individual tufted ducks. O, data from six ducks divingfreely in a tank 1.7 m deep (Woakes and Butler, 1983). # , data from seven duckstrained to dive for different durations in a shallow (0.6 m) tank (Bevan et al. 1991). Theregression line through all of these data points is described by the equation>-=0.838-0.019JC, r2=0.87.

238 P. J. BUTLER

tufted ducks, an important question is what happens in winter when they arecold water? When at rest on water under winter conditions (air temperature 6°C,water temperature 7.5 °C), oxygen consumption in tufted ducks is twice that undersummer conditions (26°C and 23°C, respectively), and deep body temperaturesare similar (Fig. 4). However, mean oxygen consumptions at mean dive durationsare not significantly different under the two conditions (Bevan and Butler, 1989),whereas mean oxygen consumption at mean duration at the surface is some 50 %higher under winter conditions. Deep body temperature is a full 1°C lower after about of diving in winter conditions compared with that at summer temperatures(Fig. 4B). It would appear that while actually feeding under water the heat fromlocomotor activity is insufficient to maintain core temperature in winter, but thatthe ducks do not enhance metabolic heat production during this period. Incontrast, while at the surface between dives, aerobic metabolism is higher duringwinter but is still insufficient to prevent a reduction in body temperature over acomplete bout of diving. The outcome is that, overall, feeding in winter ismetabolically more expensive (approximately 40 % in the present study) for tuftedducks than it is in summer, but not as great as might be expected from theelevation of oxygen uptake seen in ducks resting on water in winter conditions.

Penguins, which are much better adapted than tufted ducks to an aquaticexistence, may be able to feed much more efficiently. From direct measurementsof oxygen uptake in Humboldt penguins, Spheniscus humboldti, diving for food ina pool and in little penguins, Eudyptula minor, swimming at 0.7 ms" 1 in a waterchannel, it appears that aerobic energy expenditure during underwater swimmingin penguins is approximately 30% greater than, but not significantly different

o.&

0.6

0.4

0.2

0.0Rest At mean dive At mean interdive

duration duration

U

03

42

41

40

r B

Rest At the end ofa diving bout

Fig. 4. (A) Histogram showing mean oxygen uptake (+S.E., ^=6) in tufted ducks atrest, at mean dive duration and at mean interdive duration. The birds were acclimatedto summer (air temperature 26°C, water temperature 23°C; filled columns) or winter(air temperature 6°C, water temperature 7.5°C; hatched columns) conditions.(B) Histogram showing mean deep body temperature (+S.E., N=6) in tufted ducks atrest and at the end of a bout of dives. The birds were acclimated to summer (filledcolumns) or winter (hatched columns) conditions (see above). (From R. M. Bevan andP. J. Butler, in preparation.)

Exercise in birds 239

Pbm, that in resting birds (Butler and Woakes, 1984; Baudinette and Gill, 1985).Clearly, these experimental conditions are somewhat different from those thatexist at the feeding grounds. However, from the measurements of oxygenconsumption that have been made for Humboldt penguins swimming under waterand from the usable oxygen stores of a similar-sized penguin, calculated from thedata of Kooyman (1975), these birds should be able to remain submerged andcompletely aerobic for approximately 2.3 min. Data from chinstrap penguins,Pygoscelis antarctica (which are of a similar size to Humboldt penguins), divingfreely off Signy Island, South Orkneys, indicate that at night these birds dive for anaverage of approximately 1.6 min (Lishman and Croxall, 1983). It would appear,therefore, that these medium-sized penguins, like diving ducks, remain com-pletely aerobic during normal feeding dives.

Jones and Furilla (1987) point out that the average daily metabolic rate(ADMR) measured with labelled water in a number of species of penguins whenforaging is between 40 and 60% greater than the fasting rate. Unfortunately, insome of the field studies it was not possible to estimate metabolic rate when thebirds were actually diving, so the value for ADMR probably includes periods ofrest (Kooyman et al. 1982; Davis et al. 1983). By incorporating information ontime budgets, Nagy et al. (1984) estimated that, when swimming under water atsea at an average velocity of 1.75 ms"1 , energy expenditure in jackass penguins,Spheniscus demersus, is six times the resting value. This can be compared with themetabolic rate of 4.3 times the lowest resting value in Humboldt penguinsswimming at 1.25ms"1 (Hui, 1988). Also, estimated metabolic rate for gentoopenguins, Pygoselis papua, foraging at sea is some 6-7 times the calculatedstandard metabolic rate (Davis et al. 1989). It would appear, therefore, thataerobic metabolism during diving in penguins can be substantially elevated abovethe resting value, as it is in ducks; the difference is that penguins can swim faster.

Locomotory muscles

It is the muscles, of course, that produce the demand for the extra oxygen duringexercise. The muscles of the hindlimbs of birds consist of a mixture of slowoxidative (SO), fast oxidative glycolytic (FOG) and fast glycolytic (FG) fibres(Kiessling, 1977; Talesara and Goldspink, 1978; Turner and Butler, 1988). Thedistribution of these fibres has been studied in the thigh muscles of chickens(Suzuki et al. 1985). Postural muscles, such as the pubo-ischio-femoralis-parsmedialis, possess a high percentage (>50%) of SO fibres. Other muscles containless, and the flexor cruris lateralis pars pelvica has none. FOG and FG fibres varyin proportion in different muscles and in different regions of the same muscles. SOand FOG fibres are generally concentrated in the deeper regions, close to thefemur, and in the medial regions, whereas the FG fibres are placed moresuperficially and laterally. This is very similar to the situation that exists in the

s of mammals (Armstrong and Laughlin, 1985). It is interesting to note thatfibres are scarce in the hindlimbs of tufted ducks (Turner and Butler, 1988),

240 P. J. BUTLER

which is probably related to the fact that they spend much of their time floatingwater.

Studies on mammals also indicate that the deep extensor muscles (mainly SOfibres) are active during quiet standing as well as during locomotion. Duringwalking, deep SO and FOG fibres are recruited in extensor muscle groups, andwith increasing speed there is progressive recruitment of the more peripheral FGfibres (Armstrong et al. 1977; Walmsley et al. 1978). Suzuki etal. (1985) proposethat a similar recruitment pattern exists in the leg muscles of birds. Laughlin andArmstrong (1982) have demonstrated for the rat that blood flow distributionwithin and among different muscles is related to their recruitment patterns duringquiet standing and exercise. Again, a similar situation is assumed to exist in thelegs of birds.

The major flight muscles in birds are the pectoralis and supracoracoideus andtogether they constitute, on average, 17 % of body mass for a range of birds, withthe pectoralis being approximately 10 times the mass of the supracoracoideus(Greenewalt, 1962). This reflects the more important role of the former in causingdepression of the wing and therefore in generating lift and thrust. The upstroke,which is effected by the supracoracoideus, is merely a recovery stroke. Inhummingbirds and penguins, in contrast, the ratio of the masses of the two musclesis approximately 2 and in the former their combined mass accounts for 20-30 % oftotal body mass (Greenewalt, 1962; Baldwin et al. 1984). Lift is generated duringboth phases of the wingbeat during hovering in hummingbirds and duringswimming in penguins.

In volant birds, the pectoralis muscle consists predominantly of FOG fibrestogether with a smaller (usually) percentage of FG fibres. In a few species of birdsthere are also some SO fibres, which are normally involved in postural support.Their presence was thought to be associated with the gliding or soaring behaviourof some birds, e.g. herring gull (Talesara and Goldspink, 1978). This appears to bethe case for the turkey vulture, Cathartes aura (Rosser and George, 1986a),although Rosser and George (19866) found SO fibres in the pectoralis muscle ofonly two out of 42 volant species, and this did not include the herring or ring-billedgulls. The reported presence of a large percentage (12 %) of SO fibres in the dorsalareas of the pectoralis of the grey catbird, Dumetella carolinensls (Marsh, 1984),which is a migrating species, is perplexing in view of the fact that Rosser andGeorge (19866) found no indication of such fibres in the pectoralis muscles of 17other species of passerines. Thus, the functional significance of SO fibres in thepectoralis of volant birds, when they are present, is not clear in all cases.

The FG fibres are relatively large and make up anything from 0 % toapproximately 50 % of the fibres in the pectoralis of the volant species (Rosser andGeorge, 19866). They metabolize glycogen anaerobically and are used predomi-nantly during take-off and landing and when the birds undergo sudden changes indirection (Parker and George, 1975; Dial etal. 1987).

The FOG fibres have smaller diameters than FG fibres and, despite the fact ththey possess some glycolytic enzymes and can, presumably, produce

Exercise in birds 241

Piaerobically, are nonetheless highly oxidative. In free-living tufted ducks, themass-specific activity of citrate synthase (CS), an indicator of the capacity foroxidation of acetyl Co A in the citric acid cycle, is approximately 20 % higher in thepectoralis muscle than in the heart (Butler and Turner, 1988). CS activity in the legmuscles of volant birds may be less than half of that in the pectoralis muscles(Marsh and Dawson, 1982; Butler and Turner, 1988). Marsh (1981) reported avery high activity of CS (200 /imolmin^g"1 fresh mass) in the pectoralis of thegrey catbird just prior to migration and claimed that it was 'the highest reported forany vertebrate skeletal muscle' (it is approximately twice that for the supracora-coideus muscles of the same species). An even higher activity of CS (343jumolm i n ^ g " 1 wet mass) has been reported in the flight muscle of the hummingbird,Selasphorus rufus (Suarez et al. 1986). It must be remembered, however, that CSactivity most likely scales with body mass in a similar fashion to oxygen uptake (seeabove, and Somero and Childress, 1980). Nonetheless, the FOG fibres in thepectoralis muscle are so oxidative that Talesara and Goldspink (1978) havesuggested that they should be designated FO fibres.

The proportion of FO(G) fibres varies throughout the pectoralis muscle of anyone species, being greater in the deeper regions, and also between volant species,from 100% in starlings, owls, hawks and kingfishers (and, it is assumed,hummingbirds) to approximately 50% in the ruffed grouse (Rosser and George,1986£>). Thus, the pectoralis muscle normally consists of a preponderance of fastcontracting but highly oxidative fibres, which are required to beat the wings at highfrequencies, sometimes for many hours.

Related to the greater potential oxygen demand in the pectoralis of flying birdsis a greater capillary/fibre ratio than that in the leg muscles of birds and mammals(Pietschmann et al. 1982; Turner and Butler, 1988). Along with the smaller cross-sectional area of the FO(G) fibres in the pectoralis, there are, therefore, shorterdiffusion distances from capillaries to fibres. In fact, the smallest fibres and thegreatest capillary densities are found in birds that migrate the longest distances(Lundgren and Kiessling, 1988). Also, in the tufted duck, the volume density ofmitochondria is greater in the pectoralis muscle than in the muscles of the leg(Turner and Butler, 1988). In fact, it is evident from this last study that thedifference in Vo2max during running in volant birds and V^mm during forwardflapping flight is not merely the result of the different muscle masses, as suggestedby Prange and Schmidt-Nielsen (1970), but also of the different oxidativecapacities of the muscles.

Data from studies on intracellular glycogen and lipid content (Parker andGeorge, 1975, 1976) and on gas exchange (Butler et al. 1977; Rothe et al. 1987)indicate that the substrate for aerobic metabolism switches from a mixture ofcarbohydrate and fat to almost exclusively fat as forward flapping flight progresses(Fig. 5). Indeed, it seems likely that the preferred fuel for hovering in hum-mingbirds is carbohydrate, with fat being used during extended forward flappingjght (migration) (Suarez et al. 1986). The use of fat as a metabolic substrate forng flights is energetically beneficial as each gram, when fully oxidised, produces

242 P. J. BUTLER

o 09

2 0.8

0.7

I10 20 30

Flying time (min)

40 50 60

Fig. 5. Mean values (±S.D. , N=5) of the respiratory exchange ratio of pigeons at restand when flying for up to 60 min in a wind tunnel. (After Rothe et al. 1987.)

approximately 40kJ of energy, whereas for carbohydrate the value is 17.5 kJg \Also, it can be stored in adequate abundance for long-term or migratory flight(Blem, 1976). However, the maximum theoretical rate of catabolism of aparticular fuel for muscle contraction is determined by the activities of the relevantenzymes, but factors such as transport of substrates, particularly free fatty acids(FFA), and availability of cofactors will also limit its rate of utilization (Hultmanand Harris, 1988). These authors quote calculated values, based on data fromhumans, which indicate that the maximum rate of ATP synthesis from thecomplete oxidation of carbohydrate is 0.51-0.68 mmol s"1 kg"1, whereas the valuefor the oxidation of FFA is 0.24 mmol s"1 kg"1. This relatively low rate indicates arate-limiting step before the formation of acetyl CoA, as succeeding steps are alsoinvolved in oxidation of carbohydrates. If birds do metabolize at the ratesindicated in Fig. 1 during long-distance flight, while oxidizing fats, it must beassumed that they do not possess the constraints associated with oxidation of FFAthat are present in humans.

Associated with pre-migratory fattening is an increase in the mass of thepectoralis muscle (Marsh, 1984). In the grey catbird, there is no associated changein the specific activity of CS, although there is an increase in activity of3-hydroxyacyl-CoA dehydrogenase (HAD), which is a key enzyme in the/S-oxidation of fatty acids (Marsh, 1981). There is, however, an increase in CS andcytochrome oxidase (COX) activities in a number of other species prior tomigration (Lundgren and Kiessling, 1985, 1986). ^

It is not clear to what extent endocrine changes themselves and increased

Exercise in birds 243

^comotor activity (training) just prior to migration effect the adaptations seen inthe pectoralis muscle. It would seem that hypertrophy of the pectoralis is a directresult of the increase in body mass associated with pre-migratory fattening (Marsh,1984). Endurance training can increase muscle capillarity and mass-specificactivity of CS and cause a transformation of muscle fibres from FG to FOG in theleg muscles of ducks (Butler and Turner, 1988). It has been proposed that theincreased oxidative capacity in migratory reed warblers Acrocephalus scirpaceus isa training effect (Lundgren and Kiessling, 1986). These authors do point out,however, that both increased locomotor activity and hyperphagia are initiated bythe hormones corticosterone and prolactin (Meier and Martin, 1971). Nonethe-less, studies on the levels of thyroid hormones (T3 and T4) and growth hormone inmigratory Canada geese have suggested that they are directly involved in thehypertrophy of the pectoral muscles prior to migration (John and George, 1978;John et al. 1983). Also, high levels of T4 and T3 can cause increases in activities ofCS and cytochrome c in the soleus muscle of rats (Winder, 1979).

'Conditioning' of the pectoral muscles before migration takes on even greatersignificance when it is realised that periods of relative inactivity, such as thoseoccurring during moulting and incubation, cause significant reductions in musclemass and myoglobin concentration and in CS and HAD activities (Pages andPlanas, 1983; George et al. 1987; Butler and Turner, 1988; Piersma, 1988). Incontrast, the relative mass of the leg muscles may increase during the moultingperiod, which could be an undesirable burden during migration.

With the possible exception of the larger and deeper-diving penguins (emperor,king, AdeTie), the anaerobic capabilities of the locomotory muscles of diving birds(pectoralis in penguins and alcids) are relatively low (Baldwin et al. 1984; Davisand Guderley, 1990). In fact, the latter authors conclude that there are no specialbiochemical adaptations in the locomotory muscles of diving birds, although thereis a tendency, particularly among the penguins, for them to have a higherconcentration of myoglobin (Butler, 1990).

Respiratory and cardiovascular adjustments during exercise in air

It is the combined functions of the respiratory and cardiovascular systems tosupply the required oxygen and metabolic substrates to the locomotor muscles andto remove the waste products of metabolism (e.g. CO2 and heat). It is clear fromthe earlier discussion that the respiratory and central cardiovascular systems donot impose any limit on oxygen consumption during running or swimming involant birds. Thus, this part of the review will concentrate mainly on those studiesperformed on flight and on running in cursorial species.

It is perhaps worth mentioning that the lungs of birds have a completelydifferent structure from those of mammals and that they are more effective gas-£xchange organs (Scheid, 1979). Nonetheless, these differences do not appear toPbnfer any particular advantages on birds with respect to oxygen uptake during

244 P. J. BUTLER

flight (cf. VQ2 of birds and bats during flight) or with respect to theirtolerance of high altitude (see below).

Ventilation

Respiratory data are given for six species of birds in Table 1. Two of these arehovering hummingbirds and four are birds during forward flapping flight. It can beseen that, for the flying birds at relatively low ambient temperatures (<23°C),ventilation volume (Vi) increases by a similar proportion as oxygen uptake (Vo2)and that the proportion of oxygen extracted from the inspired gas (O2ext) issimilar to that in resting birds. Oxygen extraction during hovering for one of thehummingbirds, Colibri coruscans, is similar to that for the flying birds, whereas forthe other, Amazilia fimbriata, it is somewhat lower. The respiratory frequencies(/resp) a r e verY high m the hovering hummingbirds. The relative contributions ofrespiratory frequency and tidal volume (Vt) to the increase in Vi during forwardflapping flight vary among species. In white-necked ravens, VT does not change atall, in fish crows it almost doubles and in starlings there is a fourfold increase.Thus, in the first two species, frequency makes the greater contribution, whereasin the third, volume predominates.

Despite the apparent matching between ventilation volume and oxygen uptakein the four species of flying birds listed in Table 1, there does appear to be anincrease in effective lung ventilation above that required by metabolic rate(hyperventilation) during flight in starlings, as partial pressure of oxygen (-PoJ inthe air sacs increases and Pco2 decreases (Torre-Bueno, 1978a). Such hyperventi-lation is even more apparent in ducks when running or swimming (Kiley et al.1979; Woakes and Butler, 1986) and in running chickens (Brackenbury et al. 1982).An explanation could be that hyperventilation results from the increase in bodytemperature that occurs in all exercising birds, even during flight at low (0°C)environmental temperatures (see, for example, Torre-Bueno, 1976; Hudson andBernstein, 1981; Hirth et al. 1987). However, when the usual elevation in bodytemperature during running is prevented in ducks and domestic fowl, there are stillsigns of hyperventilation (Kiley et al. 1982; Gleeson and Brackenbury, 1984). Inboth cases there was a slight acidosis which could have stimulated ventilation.Thus, it does appear as if factors other than hyperthermia contribute to the overallhyperventilation in exercising birds.

The physiological significance of the hyperthermia during flapping flight, even atlow ambient temperatures, is uncertain, although Torre-Bueno (1976) concludedthat birds adjust their insulation to allow a certain increase in body temperatureduring flight in order to improve muscle efficiency and increase maximal workoutput. Whatever the significance of the increase in core temperature, braintemperature is maintained at a lower level. In fact, even in birds under restingthermoneutral conditions, there is approximately a 1°C difference between brainand body temperatures (Bernstein et al. 1979), and this difference is at leastmaintained as the birds become hyperthermic during flight, and may even increasj(Fig. 6). The important structure in this phenomenon is the rete mirabii

Tab

le 1

. V

alue

s of

res

pira

tory

freq

uenc

y,

f,,, (m

in-'

); t

idal

vol

ume,

VT

(ml)

; ven

tila

tion

vol

ume,

VI

(1 m

in-'

BT

PS,

exc

ept

for

fish

cro

w w

here

it is

1 m

in-'

ST

PD

), o

xyge

n ex

trac

tion

, 0

2ex

t, a

nd o

xyge

n up

take

, vO

, (ml O

2 m

in-'

STD

P)

duri

ng r

est a

nd

whi

le h

o~

win

g in t

wo

spec

ies

of h

umm

ingb

irds

and

whi

le fl

ying

in

a w

ind

tunn

el fo

r fo

ur o

ther

spe

cies

of

bird

s

Res

t Fl

ight

M

ass

(kg)

fr

ebp

VT

VI

Oze

xt

vOz

fres

p V

T ~1

O

zext

ib

2m

in

Hum

min

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43 I -

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Flying time (min)

5 + Post-flight

Fig. 6. Mean values (±2s.E., N=5) of brain (O) and colonic (•) temperatures inkestrels before, during and after flapping flight at 10 ms"1 at an ambient temperatureof 23°C. Data at 5+ min were obtained between 5 and 15 min after the onset of flightand represent steady-state values. (After Bernstein et al. 1979.)

opthalmicum (RMO). It is closely associated with the circulatory system of theeye, and warm arterial blood from the body is thought to be cooled by the counter-current exchange with venous blood returning from the relatively cool beak,evaporative surfaces of the upper respiratory tract and the eye (Mitgard, 1983).

The hyperventilation during flight no doubt serves a thermoregulatory functionand as ambient temperature increases, a greater proportion of total heat lossduring flight is by respiratory evaporation. However, even at an ambienttemperature of 30°C this is only approximately 20% for the budgerigar (Tucker,1968) and 30 % for the fish crow, white-necked raven and pigeon (Hudson andBernstein, 1981; Biesel and Nachtigall, 1987). So, the majority of metabolic heatmust be dissipated by means other than respiratory evaporation. Indeed, herringgulls can lose up to 80 % of total heat production through their feet during flight(Baudinette et al. 1976). In pigeons, the value is probably slightly less, at 50-65 %(Martineau and Larochelle, 1988).

At moderate to high ambient temperatures, water is lost at a greater rate than itis produced metabolically, i.e. the birds are dehydrating (Tucker, 1968; Biesel andNachtigall, 1987). In the case of the starling, water balance while flying is onlymaintained at temperatures below 7°C (Torre-Bueno, 1978£>). This authorsuggested that, during migrations, birds ascend to altitudes where the air is cool

Exercise in birds 247

Biough to enable a greater proportion of heat to be dissipated by non-evaporativemeans, thus keeping them in water balance.

Studies on ventilatory control in running Pekin ducks have indicated thatneither the carotid bodies nor the pulmonary CO2 receptors are of any importanceand that input from muscle afferents may play a major role (Kiley and Fedde,I983a,b; Faraci et al. 1984).

Circulation

The role of the various components of the circulatory system in presentingoxygen to (and removing CO2 from) the exercising muscles can best be describedby Fick's formula: F O 2 = / H X Vs(CaO2-CvO2), where VOz is the rate of oxygenconsumption, /H is heart rate, Vs is cardiac stroke volume, CaO2 is the oxygencontent of arterial blood and CvO2 is the oxygen content of mixed venous blood.

There are two studies on flying or cursorial birds in which data have beencollected on all but one of these variables (thus allowing the absent one to becalculated), Butler et al. (1977) working with pigeons and Grubb et al. (1983)working with emus. When flying in a wind tunnel at 10 m s"1, oxygen uptake in thepigeons was 10 times the resting value (Table 2). The respiratory systemmaintained CaO2 at slightly below the resting value but CvO2 was halved, giving a1.8-fold increase in (CaO2—CvO2). There was no significant change in Vs, so themajor factor in transporting the extra oxygen to the muscles was the sixfoldincrease in heart rate. When running on a treadmill at a 6° incline and a speed of1.33 m s"1, emus had an oxygen uptake that was 11.4 times the resting value and,although an increase in heart rate to 3.9 times the resting value was the majorfactor, a 1.8-fold increase in cardiac stroke volume and a similar increase in(CaO2—Cvch) both made significant contributions to the enhanced delivery ofoxygen to the exercising muscles. As mean arterial blood pressure did not changein either species during exercise, total peripheral vascular resistance fell by thesame proportion as cardiac output (faxVs) increased. It is interesting to note that

Table 2. Mean values of oxygen uptake and cardiovascular variables measured inpigeons (Butler et al. 1977) and emu (Grubb et al. 1983) at rest and after 6min ofsteady level flight in a wind tunnel at a speed of 10ms~' for the former and after20min running on a treadmill at a 6° incline and a speed of 1.33 ms'1 for the latter

Pigeon (0.442 kg) Emu (37.5 kg)

Oxygen uptake (ml min i STPD)Heart rate (beats min"1)Cardiac stroke volume (ml)Oxygen content of arterial blood

Oxygen content of mixed venousblood (vol%)

Rest

9.0115

1.4415.1

10.5

Flying

88.4670

1.5813.7

5.4

Rest

156.745.85715.2

9.0

Running

1807180102.715.2

4.6

248 P. J. BUTLER

heart rate in hovering hummingbirds may exceed 1200 beats min 1 (Berger et afl1979).

During swimming in both tufted ducks and barnacle geese, an approximatelytwofold increase in oxygen consumption above the resting value is accompanied bya threefold increase in blood flow to the muscles of the legs (Butler et al. 1988;R. M. Bevan and P. J. Butler, in preparation). In the ducks, there is also asignificant reduction in blood flow to the flight muscles, whereas this is not the casefor the barnacle geese (Fig. 7). As the cardiovascular system is able to cope withthe greater demand for oxygen during flapping flight, redistribution of blood awayfrom the inactive pectoral muscles during swimming may not be important tovolant birds. It is possible that the difference in response between the tufted duckand barnacle goose is related to the diving behaviour of the duck, when reducedblood flow to the flight muscles is a likely mechanism for conserving oxygen for thecentral nervous system (CNS), heart and leg muscles (Butler, 1988). It should benoted, however, that 'resting' blood flow to the flight muscles is higher in thetufted duck than in the barnacle goose. Whether this is an artefact remains to beseen, but it could be an explanation for the different responses in the two species.Nonetheless, it would certainly be interesting to see what happens to blood flow tothe leg muscles during forward flapping flight.

Birds have larger hearts and lower resting heart rates than mammals of similarbody mass (Lasiewski and Calder, 1971; Grubb, 1983). They also have a greatercardiac output for a given oxygen consumption than similar-sized mammals(Grubb, 1983). In other words, (Cao^-Cvo,) is lower in birds than in similar-sizedmammals, because CvOl is not normally reduced to such a low level. Thus, the

200

7 150c

100

5 5°

Heart Gastro- Kidneys Total Totalintestinal flight hindhmb

tract muscles muscles

Heart Gastro- Kidneys Total Totalintestinal flight hindhmb

tract muscles muscles

Fig. 7. Histograms showing mean (+S.E. , N=6) values of blood flow to some majorvascular beds in (A) tufted ducks and (B) barnacle geese before (hatched columns) andduring swimming at close to their maximum sustainable speed (filled columns).* indicates a significant difference between pre-exercise and swimming values(P<0.05). (A is taken from Butler et al. 1988 and B from R. M. Bevan and P. J. Butler,in preparation.)

Exercise in birds 249

cardiac output in birds may be an important factor in their attaining ahigher maximum oxygen uptake (V^max) during flight than similar-sized mammalswhen running. It is certainly interesting to note that bats have larger hearts and ahigher blood oxygen-carrying capacity than other mammals of similar size(Jiirgens etal. 1981) and that, as mentioned earlier, their VOl during flight issimilar to that of birds of similar mass.

High altitude

Most passerines migrating at night fly below 2000 m, although some birds havebeen observed at extremely high altitudes. A flock of 30 swans (probably whooper:Cygnus cygnus) was located by radar off the west coast of Scotland at an altitude of8000-8500 m (Stewart, 1978). Bar-headed geese Anser indicus have been observedflying at altitudes of approximately 9000 m (where the PO2 is, at 6.9 kPa,approximately one-third of the sea-level value) during their migration across theHimalayas (Swan, 1961). Unfortunately, there have been no physiological studieson birds flying at high altitude (real or simulated), but work on inactive animalshas indicated the adaptations that may be of great importance in the altitudeperformance of birds.

It is the cardiovascular system that shows most adaptations to the conditions ofhigh altitude. Unlike Pekin ducks, bar-headed geese do not increase theirhaematocrit (packed cell volume of the blood) and haemoglobin (Hb) concen-tration when exposed to simulated high altitude (Black and Tenney, 1980). Thismeans that there is no increase in blood viscosity, thus preventing a possiblereduction in circulation of the blood. It also means that there is no increase in theoxygen-carrying capacity of the blood. This is more than counterbalanced by thehigher affinity for oxygen (low P^) of the Hb of the goose (P50 for goose blood isapproximately 5kPa at pH7.5 compared with 7.5kPa in the duck), which allowsthe maintenance of a higher CaO2 (and hence CaO2-CvO2) at high altitudes than inthe duck. A comparison between the Hb of greylag and bar-headed geeseindicated that the difference in oxygen affinity is the result of a very small intrinsicdifference that is magnified by the presence of inositol pentaphosphate (Rollemaand Bauer, 1979).

It is also clear from the data of Black and Tenney (1980) that the respiratorysystem of the bar-headed goose is able to maintain a very small difference betweenthe Po2 >

n inspired air (PioJ a n ^ t n a t in arterial blood (Pao2) when at high altitude.At sea level, P\O2—Pa.O2 is 7 kPa, whereas at a simulated altitude of 10 668 m it is amere 0.5 kPa. The large increase in ventilation that is required to maintain such asmall difference between PiO2 and Pao, also causes a decline in PaCOz and anincrease in arterial pH (pHa); the bird becomes hypocapnic and alkalotic.

In a number of mammals (dog, monkey, rat, man) hypocapnia causes areduction in cerebral blood flow. This is not so in ducks and bar-headed geese(Grubb etal. 1977; Faraci and Fedde, 1986). Also, hypoxia causes a greater

iicrease in cerebral blood flow in ducks than in dogs, rats and man (Grubb et al.P . At high altitude, of course, both of these factors occur together (hypocapnic

250 P. J. BUTLER

hypoxia) and hypocapnia attenuates the increase in cerebral blood flow induced rj^hypoxia (Grubb etal. 1979). However, these authors found that blood flow issimilar at a given O2 content in both normocapic and hypocapnic ducks. This isbecause during hypocapnia (and alkalosis) there is a leftward shift of the oxygenequilibrium curve so that a given oxygen content is achieved at a lower POl. In fact,in bar-headed geese, the alkalosis during severe hypoxia is greater than that inPekin ducks which, together with the higher affinity of their Hb for oxygen, meansthat at a given (low) PaOl, Ca^ is much (two times) greater in the geese (Faracietal. 1984). Thus, similar (or even greater) oxygen deliveries to the brain andheart can be achieved in hypoxic bar-headed geese at lower cerebral and coronaryblood flows than in hypoxic ducks. This may be a very important feature when thegeese are flying over the Himalayas.

It has been suggested that the more effective lungs of birds, compared withthose of mammals, may contribute significantly to the ability of birds better totolerate high altitude (Scheid, 1985). A more recent analysis, however, hasdismissed this notion (Shams and Scheid, 1989). The difference between birds andmammals appears to be the ability of the former to tolerate lower Paco2> thusenabling the respiratory system to maintain PaO:, at as high a level as possible.

Despite all of these apparent adaptations to life at high altitude, experiments onbar-headed geese running on a treadmill under hypoxic conditions, similar tothose at the top of Mount Everest, indicate severe limitations to oxygen uptake(Fedde et al. 1989). Under normoxic conditions, running at 0.6ms"1 at a 2° inclinecaused a doubling in VOl and cardiac output from approximately 20 ml min"1 kg"1

and 0.241 min"1 kg"1, respectively (Fig. 8). Cardiac stroke volume was constant atapproximately 2.5 ml. Under hypoxic conditions, resting oxygen uptake fell toapproximately 15 ml min"1 kg"1 and was not significantly different after 6 min ofexercise. Cardiac output also remained unchanged during exercise at approxi-mately 0.251 min"1 kg"1, whereas cardiac stroke volume declined significantlyfrom 1.9ml at rest to 1.4ml during exercise. The authors argue that diffusion ofoxygen from the muscle capillaries to the mitochondria may limit the aerobiccapacity of the exercising leg muscles during hypoxia. If this is the case, thesituation could be different in the pectoral muscles during flight at high altitude.The question is, how does the heart manage to cope with the extra demands offlight at high altitude when it appears to be at its limit during running underhypoxic conditions similar to those at the top of Mount Everest? The resting heartrate was rather high in the birds used in this study, which probably means that theywere stressed (see Woakes and Butler, 1986). Whether this could explain theresults remains to be seen. It is also possible that birds of this species routinelymigrate across the Himalayas at altitudes substantially below that at the top ofMount Everest.

However, if some species of birds do routinely fly at altitudes similar to, or evengreater than, that at the top of Mount Everest, there is no doubt that the next greatchallenge in the study of exercise physiology of birds is to determine just how ipossible for these species to fly at altitudes where mammals can barely survive.

Exercise in birds 251

5O

40Q

I 6D.I

Ofe

20

10

I I

i1 1Rest

CO J 2U CO

X «

500r

400

300

200

100

Jft

6 12Exercise RecoveryTime (min)

0.5

0.4

f-f" 0.3

•2'g 0.2CO

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I

12Rest Exercise

Time (min)Recovery

0 6Rest Exercise

Time (min)

Fig. 8. Mean values (+S.E.) of oxygen uptake, heart rate and cardiac output in bar-headed geese at rest and while running at 0.6 ms"1 on a 2° incline (exercise) duringnormoxia (D) and hypoxia simulating that at the top of Mount Everest (0). (Modifiedfrom Fedde et al. 1989.)

Cardiovascular adjustments during divingEqually intriguing is how some species of aquatic birds can spend what amount

to substantial periods of time foraging under water while holding their breath. Formany birds that feed on benthic organisms, dive duration is related to the depth ofthe water (Dewar, 1924), at least to a depth of 4 m (Draulans, 1982). At a depth of2m, tufted ducks, pochards, Aythya ferina, and the white-headed duck, Oxyuraieucocephala, dive, on average, for 20-25 s (Butler and Stephenson, 1987) with amaximum duration of 45 s (Stephenson et al. 1986). A number of birds, such as

252 P. J. BUTLER

grebes, divers, cormorants and a range of auks, are, to a greater or lesser exten™active predators of fish and remain submerged for an average of 20-70 s, with theguillemot, Uria aalge, having a reported maximum dive duration of 202 s (Wanlesset al. 1988) and the imperial cormorant (blue-eyed shag), P. atriceps, of 312s(Naito et al. 1991). The latter species has been monitored diving to a maximumdepth of 116 m, whereas other birds have been trapped in nets at 180 m(guillemots), 120m (razorbills Alca torda) and 60m (great northern diver, Gaviaimmer) (Schorger, 1947; Piatt and Nettleship, 1985). These dive durations anddepths compare very favourably with those of the smaller penguins. Wheninshore, the little penguin, Eudyptula minor, remains submerged for very shortperiods of 10-15 s and the greatest recorded depth is 60m (Mill and Baldwin,1983), whereas the larger chinstrap and gentoo penguins have mean dive durationsof 91 and 128 s and maxima of 130 and 190 s, respectively (Trivelpiece et al. 1986).The greatest recorded depths for these birds are 70 and 100 m, respectively(Lishman and Croxall, 1983; Conroy and Twelves, 1972).

It is the larger penguins, the kings and emperors, Aptenodytes patagonica andA. forsteri, that are the most impressive avian divers. When diving naturally andpresumably feeding, the emperors remain submerged for 2.5-9min with amaximum recorded depth of 265 m (Kooyman et al. 1971). King penguins can diveto between 240 and 290 m, although 50% of the dives are probably to less than50 m (Kooyman et al. 1982).

With oxygen consumption of tufted ducks during dives of approximately 15 sduration being similar to that at maximum sustained swimming speed, similarcardiovascular adjustments might also be expected. However, Woakes and Butler(1983) discovered that mean heart rate just before surfacing from dives ofapproximately 15 s duration is significantly lower than that recorded from the sameanimals w ien they are swimming at the surface and consuming oxygen at the samerate (Fig. 9). Assuming that heart rate is an indicator of the degree of peripheralvasoconstriction (and thus, of anaerobic metabolism), it has been suggested(Butler, 19826) that, during most dives, perfusion (and hence aerobic metabolism)of the active muscles (heart, legs) and of the central nervous system is similar tothat during exercise in air, whereas the viscera and inactive muscles (which, ofcourse, includes the large pectorals in these birds) may be perfused less thanduring exercise in air in order to conserve oxygen for the active muscles, heart andCNS. This hypothesis has gained some support from qualitative studies usingmicro-aggregated albumin labelled with " m T c (Jones et al. 1988), and from directmeasurements of blood flow through major arteries (R. M. Bevan and P. J. Butler,in preparation).

Blood flow through the right pulmonary, left brachiocephalic, left carotid andright ischiadic arteries has been continuously monitored in resting, diving andswimming tufted ducks. Cardiac output was assumed to be twice the flow throughthe right pulmonary artery and brachial flow (to the breast muscles) was estimatedby subtracting flow through the carotid from that through the brachiocephalia|Resting cardiac output was 342 ml min"1 kg"1. It increased by 74% when thl

Exercise in birds

300r

253

Fig. 9. Mean heart rate (±S.E. , N=6) for tufted ducks at rest, during voluntary divesof 14.4 s mean duration and while swimming. Oxygen consumptions (VOi) at meandive duration and while swimming were the same: 34mlmin~'. (From Woakes andButler, 1983.)

ducks were swimming at 0.75 m s"1 and by 33 % during the last 5 s (excluding dataover the final second) of dives with a mean duration of 15.5s. Under similarconditions, blood flow through both ischiadic arteries was SOmlmin"1 at rest,increasing 4.8 times during swimming and 5.1 times during diving. Thus, theproportion of cardiac output flowing through the ischiadic arteries was greaterduring diving than during swimming and this inevitably means that the rest of thebody was perfused by less blood during diving than during swimming. This is,unfortunately, not clearly reflected in the estimated blood flow through thebrachial artery. Although flow through the brachial arteries, at 26 ml min"1, wassignificantly lower during diving than that in the resting birds (66 ml min"1), it wasnot, however, significantly lower than that during swimming (42ml min"1). Aregion of the body that could well receive less blood during diving than duringswimming is, of course, the respiratory muscles.

It would appear, therefore, from the evidence presented so far, that Butler's(1982b) hypothesis is correct, i.e. during diving in ducks the cardiovascular systemexhibits a modified exercise response, with the legs, as well as the heart and CNS,being perfused adequately to maintain overall aerobic metabolism. Other,inactive, parts of the body are less well perfused than during surface swimming.Under certain circumstances, however, the balance may tip towards more of an^xygen-conserving response.

Stephenson et al. (1986) found that, when tufted ducks swim long horizontal

254 P. J. BUTLER

distances under water for their food (e.g. under ice in winter), heart rai lprogressively declines after approximately 10 s, so that by approximately 30 s it issignificantly below the resting value (Fig. 10A). During these dives the birdsactively swim to and from the food. However, during normal vertical dives ofsimilar duration and when the birds surface passively, heart rate remains elevatedabove the resting level. If, as indicated by the sub-resting heart rate, blood lactatedoes accumulate during a long horizontal dive, it does not have a large inhibitoryeffect on exercise, because the birds are still able to perform a number of dives insuccession. There may, however, be a cumulative effect since the number of divesin a bout is lower than normal. If a duck is temporarily unable to surface from avoluntary dive, e.g. if it is disoriented under ice, there is an immediate reduction inheart rate as soon as the bird becomes aware of the situation. Heart rate followsthe same time course and reaches a similar level to that seen during involuntarysubmersion (Fig. 10B), when selective vasoconstriction, a reduction in aerobicmetabolism and increased lactate production are known to occur (Butler andJones, 1982). This intense bradycardia occurs in 'trapped' ducks, despite the factthat they are still active under water.

It is clear that the cardiovascular response to diving in ducks is highly labile. Onthe basis of the cardiac response, it does appear that, under certain circumstances,the cardiovascular and metabolic responses during voluntary dives can shiftprogressively or more immediately to an oxygen-conserving response, i.e.relatively more intense peripheral vasoconstriction and increased lactate pro-duction in some tissues and organs, maybe even in the legs themselves in 'trapped'ducks.

Although physiologically expedient, in as much as oxygen is conserved, itappears that such a shift affects the feeding behaviour of the birds. At oneextreme, it is usual for a bird to remain at the surface for an hour or more beforemaking another dive after temporarily being unable to surface from a voluntarydive. Also, the time spent feeding during each dive decreases as horizontaldistance to the food increases (Stephenson etal. 1986). This is contrary to thepredictions of optimal foraging theory, which suggest that if more energy isexpended in reaching a source of food, more time would be spent in obtaining(more) food (Charnov, 1976). This apparent contradiction in aquatic birds mayresult from the opposing time constraint imposed by physiological factorsassociated with the maintenance of aerobic metabolism, at least in the activemuscles, CNS and heart. It appears that, under such conditions, the physiologicaladjustments allow optimization of feeding behaviour, but that these adjustmentsimpose their own constraints upon that behaviour.

The lability of the cardiovascular response to voluntary diving indicates that thecontrol processes must be complex, involving higher regions of the brain as well asperipheral sense organs and simple reflexes. However, studies so far have beenrestricted to investigating the role of the latter. Arterial baroreceptors appear notto be involved in the cardiac response to voluntary diving (Furilla and Jones^1987). The carotid body chemoreceptors do contribute to, but are not solelj

Exercise in birds 255

500

400

300

200

100

o

r- A

I I I I I I I t I I I I I I I I I

-20-15-10 -5 0 5 10 15 20 25 30 35 40 45 50 55 60 65

500

400

300

200

100

0

r B

Af_ iRest

1 A

-10-5 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70

Time (s)

Fig. 10. (A) Mean heart rate (±S.E., /V=6) of tufted ducks before, during and afternormal vertical dives (•) and extended, 'horizontal' dives (A). Downward-pointingarrowhead (time zero) represents point of immersion and upward-pointing arrowheadsrepresent mean points of emersion for 'normal' dives (22.4 s) and 'horizontal' dives(41.4s). • , resting heart rate. (B) Mean heart rate (±S.E. , JV=6) of tufted ducksbefore, during and after normal, vertical dives (•) , normal dives from which the duckswere temporarily unable to surface, 'trapped' (•) and involuntary submersion(A; data from Butler and Woakes, 1982ft). Downward-pointing arrowhead representsthe point of immersion in normal feeding dives and 'trapped' dives (but not involuntarysubmersions). Upward-pointing arrowheads represent points of emersion for all dives.The vertical dashed line represents the point at which the ducks apparently becameaware that they were temporarily unable to surface during 'trapped' dives (after 13.8 smean duration of submersion) and it also represents the point of head immersion in thecase of involuntary submersion. • , resting heart rate. (After Stephenson et al. 1986.)

256 P. J. BUTLER

responsible for, the bradycardia seen during extended horizontal dives and whentufted ducks are temporarily unable to surface from a voluntary dive (Fig. 10,Butler and Stephenson, 1988). They also have a slight inhibitory effect on heartrate towards the end of 'normal' vertical dives of approximately 20 s duration(Butler and Woakes, 19826). In the latter study, there was also a significantincrease in dive duration following bilateral denervation of the carotid bodies.Thus, these sense organs do not appear to play a dominant role in cardiac controlduring voluntary diving in ducks and are not involved in the immediate reductionin heart rate seen when 'trapped' ducks become aware of their predicament(Fig. 10B). Inactivation of receptors in the nasal passages with local anaesthesiaprevented voluntary diving in some redhead ducks and heart rate was 10-30 %higher than in untreated ducks during the first 12-5 s of submersion when theanimals dived in response to being chased (Furilla and Jones, 1986).

Thus, it seems that receptors in the nasal passages have an inhibitory effectduring the first few seconds of voluntary submersion and that the carotid bodychemoreceptors have a similar influence after 10-15 s of submersion. However, itis clear that the dramatic reduction in heart rate, from the elevated pre-dive level,occurs before the nasal areas contact the water (Butler and Woakes, 1982a) and isprobably centrally mediated. The motor side of the cardiac response residesentirely in the vagal branches to the heart (Butler and Woakes, 1982a; Furilla andJones, 1987). It is clear from this brief discussion that the neural control of thecardiac response in freely diving birds is very complex and well worthy of furtherstudy.

ReferencesARMSTRONG, R. B., MARUM, P., SAUBERT, C. W., SEEHERMAN, H. J. AND TAYLOR, C. R. (1977).

Muscle fiber activity as a function of speed and gait. J. appl. Physiol. 43, 672-677'.ARMSTRONG, R. B. AND LAUGHLIN, M. H. (1985). Metabolic indicators of fibre recruitment in

mammalian muscles during locomotion. J. exp. Biol. 115, 201-213.BALDWIN, J., JARDEL, J.-P., MONTAGUE, T. AND TOMKIN, R. (1984). Energy metabolism in

penguin swimming muscles. Molec. Physiol. 6, 33-42.BAMFORD, O. S. AND MALOIY, G. M. O. (1980). Energy metabolism and heart rate during

treadmill exercise in the Marabou stork. J. appl. Physiol. 49, 491-4%.BARTHOLOMEW, G. A. AND LIGHTON, J. R. B. (1986). Oxygen consumption during hover-feeding

in free-ranging anna hummingbirds. J. exp. Biol. 123, 191-199.BAUDINETTE, R. V. AND GILL, P. (1985). The energetics of 'flying' and 'paddling' in water:

locomotion in penguins and ducks. J. comp. Physiol. 155, 373-380.BAUDINETTE, R. V., LOVERIDGE, J. P., WILSON, K. J., MILLS, C. D. AND SCHMIDT-NIELSEN, K.

(1976). Heat loss from feet of herring gulls at rest and during flight. Am. J. Physiol. 230,920-924.

BAUDINETTE, R. V. AND SCHMIDT-NIELSEN, K. (1974). Energy cost of gliding flight in herringgulls. Nature 248, 83-84.

BERGER, M. (1974). Energiewechsel von Kolibris beim Schwirrflug unter Hohenbedingungen./. Orn. 115, 273-288.

BERGER, M. (1978). Ventilation in the humming birds Colibri coruscans during altitudehovering. In Respiratory Function in Birds, Adult and Embryonic (ed. J. Piiper), pp. 85-89.Berlin: Springer-Verlag.

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