Avian Forelimb Muscles and Nonsteady Flight: Can Birds Fly Without Using the Muscles in Their Wings?

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10-1992

Avian Forelimb Muscles and Nonsteady Flight: Can Birds Fly Without Using the Muscles in their Wings?

Kenneth P. Dial University of Montana - Missoula, [email protected]

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Recommended Citation Dial, Kenneth P., "Avian Forelimb Muscles and Nonsteady Flight: Can Birds Fly Without Using the Muscles in their Wings?" (1992). Biological Sciences Faculty Publications. 215. https://scholarworks.umt.edu/biosci_pubs/215

This Article is brought to you for free and open access by the Biological Sciences at ScholarWorks at University of Montana. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. The Auk 109(4):874-885, 1992

AVIAN FORELIMB MUSCLES AND NONSTEADY FLIGHT: CAN BIRDS FLY WITHOUT USING THE MUSCLES IN THEIR WINGS?

KENNETH P. DIAL Divisionof BiologicalSciences, University of Montana,Missoula, Montana 59812, USA

Al•sTRACT.--Intensitypatterns of electromyographic(EMG) signalsfrom selectedmuscles of the wing were studied during different modesof flight in trained Rock doves(Columba livia). Shoulder musclesexhibited a stereotypicpattern producing maximal EMG intensity during the decelerationphases of the upstrokeand the downstroke,whereas the musclesof the brachium and antebrachiumacted primarily as joint stabilizersduring level flapping flight. During nonsteadyflight (e.g. takeoff, landing, vertical ascendingflight), the distal forelimb musclesexhibited maximal EMG intensity; their primary function appearsto be associatedwith changing the camberand planform of the wing during rapid oscillation. During steady flight, an automaticlinkage systemconsisting of forelimb skeletal elements and ligamentousattachments is thoughtto permit properexcursion of the wing as a result of forcesgenerated solely by proximal musclesof the wing. To test this hypothesis,the medianoulnarisand radialisnerves were cut in five animals,thus eliminating the contribution of the forearm muscles,and flight testswere performed. Even though forearm muscleswere incapableof contracting,the birdswere capableof sustainedlevel flappingflight. They were unable to take off independently or perform controlled landings. Received3 October1991, accepted29 March 1992.

DESPITETHE large number of bird species,the and antebrachialmuscles within the avian wing wide range of wing shapes(Savile 1957), and retained?Are these musclesnecessary to extend variation in flight stylesor wing-beat gaits(Ray- and flex the wing during each and every wing- net 1988), natural selection has acted to retain beat and/or do they make subtle changesto the the basic musculoskeletaldesign of the avian shape of the wing during different modesof forelimb. Few data exist on the functional re- flight? In someavian speciesthe forearmmus- lationshipbetween a species'flying capabilities culature is proportionally reduced (e.g. alba- and its forelimb musculoskeletal architecture. trosses)and in othersit is relatively robust(e.g. Previousstudies of the musculoskeletalsystem pigeons, gallinaceous birds, and humming- document structural variation, but few studies birds). In order to understand the contribution (seeBrown 1948,Fisher 1946,Sy 1936)address of forelimb musclesto wing kinematics,it would the functional aspectsof forelimb components. be helpful to determine when they are active Comparedwith terrestriallocomotion, flying during normal locomotion. is metabolicallyefficient per unit distancetrav- Bock(1974) and Raikow (1985) noted the pau- elled, but energeticallyexpensive per unit time city of studiesin avian functionalanatomy that (Tucker 1968, Schmidt-Nielsen 1984); this is due incorporate the latest techniques to measure to the muscular demands associatedwith gen- neuromuscular physiology and musculoskele- erating lift using a rapidly oscillatingappend- tal biomechanics.Over the past several decades age. Consequently,the musculoskeletalappa- electromyography, coupled with high-speed ratus of the avian forelimb should be subjectto photography, has proven to be an important considerable selective pressures. One way to tool for assessingin vivo muscle function (e.g. minimize the moment of inertia of a rapidly Gorniak and Gans 1980, Jenkins and Goslow moving appendage is to distribute the mass 1983, Shaffer and Lauder 1985, Dial et al. 1987, closerto the pivot (Hildebrand 1988).This phe- 1988, 1991, Dial 1992). In this study, I focuson nomenonis evident amongbirds asthe bulk of changesin the intensity of electromyographic the wing's mass is positioned proximally. In signals(EMGs) during phaseswithin the wing- manycases, the distalone-half of the wing con- beat cycle and among modesof flight from se- sistsalmost entirely of feathers. lectedwing musclesin trained Rock Doves(Co- If natural selection acts to reduce energeti- lumbalivia). Then, by eliminating the neural cally costly distal mass,then why are brachial control (i.e. denervation) of certain muscle

874 October1992] WingMuscles and Nonsteady Flight 875 groups,I examinewhether forelimb musclesare California Fine Wire, Chatsworth, California) and was required for sustainedflapping flight. sutured to the intervertebral ligaments between the scapulae.Electrodes were threaded subcutaneously MATERIALS AND METHODS from the back plug to the site of implantationby guiding them through a temporarily inserted poly- Animalsand training procedures.--I used 23 adult Rock ethylene canula.Each electrode pair was implanted Dovesin the electromyographicexperiments, five of into a muscleusing a 25-gaugehypodermic needle. which were usedspecifically for denervationexper- To preventelectrodes from slippingout of the muscle, iments. All birds (body mass,œ = 326 + SD of 19 g) eachelectrode pair wassutured to surroundingfascia were capturedfrom wild populationsin Missoula or, if necessary,to the muscletissue at the electrode County, Montana, housedin stainless-steelcages (! exit point. Following surgerythe bird was fitted with m wide x 1 m deep x 1.5 m high), and maintained a protective, cone-shapedcollar and placed in a re- with commercialpigeon feed, vitamins, and water ad coverycage supplied with food, water, and a heated libitum. pad.All electromyographicrecordings were madethe Birds were trained to fly down a hallway (50 m day following surgery. long x 3.1 m wide x 2.7 m high) and to land on a Simultaneoussignals from up to six muscleswere platform (1.3 m high). Takeoff was analyzed as the amplified (gain = 500x to 2,000x using GrassP511J first five wing beats following an unassistedliftoff preamplifiers;filter settings= 100 high passand 300 from the ground. Level flight wasmeasured from five low pass)and recordedon a Keithley DAS analog-to- random wing beatsduring a 30-m flight, where the digital 12-bitcomputer (sampling rates = 2,040-3,000 animal flew level along the flyway. Landing wasan- Hz per channel) and signalsstored on a Zenith 386SX alyzed from the final five wing beats as the animal personalcomputer. Electromyographic data were an- approachedthe landing platform. Vertical ascending alyzed by converting the digital data back into their flight was recordedas the bird flew to a perch posi- analogform (usingsoftware developed by GeorgeV. tioned 2.5 m directly above the bird. To simulate ex- Lauder[University of California at Irvine] and by Garr perimental recording conditions,each bird was con- Updegraff [DataCrunch, San Clemente, California]) ditioned to fly carrying one end of a recording cable and displayedon a Tektronix 4109 graphicsterminal. (enclosing12 insulatedand electricallyshielded re- The intensity of eachEMG was measuredby dividing cording wires approximately 25 m long) securedto the rectified burst of activity for each wing beat into the animal'sback and directedalong the flank of the 5-millisecond(ms)-wide bins and calculating the bird, permitting normal movementof the wings and productof the meanspike amplitude times the num- tail. ber of spikesfor eachbin; the resultswere displayed Cinematography.--EachEMG recordingsequence was asintensity profiles under eachraw EMG signal.On- filmed usinga 16-ram,high-speed movie camera(Lo- set, offset, and total duration (0.3-ms accuracy)also Cam, Red LakesLaboratory) at 200 to 400 framess •. were measuredfor eachEMG signal with the pector- An electricalpulse synchronizedwith each frame of alis EMG onset as the reference for all muscles. EMGs film (Kodak 7250 Ektachrome) was used to reference and intensity profiles were plotted using a Hewlett- wing position during flights of denervatedand non- Packard7470A plotter (100-points-per-inchresolu- denervatedbirds. Lighting for the high-speedcamera tion). required 12 1,000-wattquartz lights (Tota-Light, T1- Electrodetip placementwas verified by: (1) visual 10, Lowel Company) positioned along the flyway. observationduring surgicalimplantation; (2) electri- Films were analyzed usingan L-W (model 224-S)film cal"back stimulation" (providing observation of mus- projector, and kinematic measurementswere made cle contraction);and (3) postmortemdissection. Data using a ruler and protractorset againsta projection from electrodesthat moved during recording were screen.Flight velocity,body angle, and flight trajec- eliminatedfrom analyses. tory were determinedfrom films taken in lateralview. Denervationexperiments.--Selected muscle groups of Measurementsof wing excursionand observationsof the wing (e.g. flexorsof wrist) were incapacitatedby deviations in wing movement between normal and sequentiallycutting the medianoulnarisnerve (along denervated wings were made from films taken in an- proximal, dorsalbrachlure) and then the radialis nerve terior view. (near proximal, midventral brachlure; Fig. 1). Birds Electromyography.--Electromyogramswere ob- were flown and electrodesignals monitored prior to tained usingprocedures presented in Dial et al. (1988) and following each denervation (45 rain after pro- and Dial (1992). Pigeons were anesthetized with in- cedure and once each day for seven days following tramuscularinjections of ketamine (25 mg/kg) and denervation). The bird was administered a local an- xylazine(2 mg/kg). Severalincisions (10-15 ram) were esthetic (Lidocaine), and the medianoulnaris nerve made on the skin located over the muscle(s) to be and radialisnerve were approachedthrough skin in- implanted and also where a back plug was secured. cisionsprepared the previousday (i.e. sameday elec- This connectorplug (Microtech, FG-6) containedsix trodeswere implanted).Nerves were severed(using fine-wire bipolar silver electrodes(100 •m diameter, microscissors)unilaterally (left side) in three birds 876 KENNETHP. DIAL [Auk, Vol. 109

carpiulnads

Biceps brachii

dohumeralis caudalis

Pectoralis

Pectoralis - TB'

B cut cut i

I ,,',,' Radialis nerve Medianoulnaris nerve Fig.1. (A)Musculature of flight apparatus of the Rock Dove. Supracoracoideus liesdeep to pectoralis. (B) Nervesof wing(dorsal view on right, ventral view on leftside) illustrating regions where nerve branches were cut (modified from Breazile and Yasuda 1979:fig.5). and bilaterallyin two birds.Unilateral denervations downstroke)of each wing-beat cycle are peri- permittedsimultaneous comparison of kinematicsof ods of peak muscleactivity (Fig. 2). In other denervated and normal wings. words, during level flapping flight, the major downstrokemuscle (pectoralis thoracicus) nor- RESULTS mally exhibitedits greatestEMG intensitydur- ing the final one-thirdof the upstrokephase. Muscleintensity.--The EMG intensityprofiles The primary upstroke muscle (supracoracoi- from the three majorshoulder muscles reveal deus) always exhibited its greatestactivity at that the neuromuscularinput during the de- the end of the downstrokephase (Fig. 2). The celerationphases (end of both upstrokeand scapulohumeraliscaudalis, considered to be a PECTORALIS- SB

INTENSITY

tO0 t20 ]40 t6Q

SUPRACORACOIDEUS

INTENSITY

201 40 60 80 f,00 ]20

,, , ,, ,I [ • • HUMERUS

DEPRESSION

SCAPULOHUMERALIS CAUDALIS

INTENSITY

t40 •60 ]8OI 200

, ,, , ,, HUMERUS • 7o

RETRACTION 10

Fig. 2. Raw EMG activity (mV) and intensity profiles (mV multiplied by milliseconds,calculated for each 5-ms bin within a wing beat; time in ms on x-axis) during two wing-beat cyclesfor three shoulder muscles of Rock Dove. Approximateangles (degrees)of excursionof humerus determined from movie film and manipulationof wing in hand. Estimatedflight velocity was 7 to 8 ms-1. 878 KENNETHP. DIAL [Auk, Vol. 109

HUMEROTRICEPS

INTENSITY

0 20 40 80 I II 200 220

I I I I I I

INTENSITY50 ' 150

BICEPS BRACHII

40 60 80 •.00 160 2OO 220 •40 INTENSITY.!!. I I • ELBOW EXTENSION

FLEXLON

Fig. 3. Raw EMG activity(mV) and intensityprofiles (mV multipliedby milliseconds,calculated for each 5-msbin within a wing beat;time in ms on x-axis)during two wing-beatcycles for three brachialmuscles of Rock Dove. Approximate angles (degrees)of excursionof humerus determined from movie film and manipulation of wing in hand. Estimatedflight velocity was 7 to 8 ms •. October1992] WingMuscles and Nonsteady Flight 879

EXTENSOR METACARPI RADIALIS

INTENSITY

FLEXORCARPI - -'• ULNARIS

INTENSITY 4 • • I,

, • •,

.• ,• WRIST • •

Fig. 4. Raw EMG activity (mV) and intensity profiles (mV x ms calculatedfor each 5-ms bin within a wing beat; time in ms on x-axis) during two wing-beat cyclesfor two major antebrachialmuscles of Rock Dove. Approximateangles (degrees) of excursionof humerusdetermined from movie film and manipulation of wing in hand. Estimatedflight velocity was 7 to 8 ms •.

major humeral retractor (Raikow 1985), exhib- of the upstrokeand continuedinto the first one- ited its strongestactivity during the secondone- third of the downstroke (Fig. 3). The bicepsbra- half of the downstroke (Dial 1992). These data chii was active during the upstroke-downstroke suggestthat the greatestEMG intensity gen- transition. Both muscles exhibited relatively erated by the major shoulder musclesis asso- uniform intensity when active during level ciated with the period of active lengthening flapping flight. The scapulotricepswas active (i.e. when muscleis stretching)in preparation throughout the upstroke-downstroketransition for the subsequentshortening phase in order (wing turnaround) and exhibited its greatest to generate greater forces of contraction (for activity during the final one-third of the down- discussionof this neuromuscularphenomenon, stroke. During level flapping flight, the scapu- see Cavagna et al. 1965). lotriceps and the biceps brachii were consis- Moving distally along the wing, the humero- tently coactive(Fig. 3). triceps was active during the final two-thirds Antebrachial (forearm) musclesexhibited low- 880 KENNETHP. DIAL [Auk,Vol. 109

LEVEL FLAPPING FLIGHT and variable-amplitude signals during level I • DOWNSTROKE flight (Fig. 4). Two of the major antebrachial muscles,the extensormetacarpi radialis and the flexorcarpi ulnaris, exhibited their greatestEMG activity during nonsteadyflight when the wing dramaticallychanges its surfacearea from that of level flappingflight. As eachbird established straightand level flight following takeoff,EMG activity from all antebrachial musclesgreatly diminished.A survey of the EMG activity patterns for most of the antebrachial muscles is presentedelsewhere (Dial 1992). The durationsof the upstrokephase and the downstrokephase within a wing-beatcycle dif- fered between vertical and all other modes of flight. Downstrokeand upstroke phaseswere of equalduration (i.e. eachrepresenting 50% of the wing-beatcycle) during level flappingflight, takeoff, and landing (wing-beat duration, œ= 121 + SD of 12 ms, 110 + 13 ms, and 119 + 11 UPSTROKE• I ms, respectively;n = 50 wing beatsper flight ASCENDING FLIGHT mode). During vertical ascending flight, the downstrokeaccounted for 43%and the upstroke 57%of the wing-beatcycle (wing-beat duration, œ= 104 _+7 ms, n = 50 wing beats;Fig. 5). The relative timing of the EMG signals(e.g. onset and offset times) changed little during different modesof flight (Fig. 5), whereasthe EMG intensity changedsignificantly. This was most obvious for muscles distal to the shoulder. For example, the duration and relative offset times of the extensormetacarpi radialis exhibited minor changesamong the different modes of flight, whereastheir EMG intensitychanged 3.5-foldfrom level flappingflight to takeoff.

times for each muscle do not change dramatically between flight modes, and that downstroke repre- sents7% lessof total cyclein ascendingthan in level []SHOULDERupMUSCLES • flapping flight. Abbreviations:Pec-SB and Pec-TB= pectoralis major pars thoracicussternobrachialis and [] BRACHIALMUSCLES thoracobrachialis,respectively; T.P. Biceps= tensor I ANTEBRACHIALMUSCLES propatagialis pars biceps;Biceps = bicepsbrachii; H. Tri. = humerotriceps; E.M.R. = extensor metacarpi Fig. 5. Cycleof electromyographicactivity in wing radialis;F.C.U. = flexor carpi ulnaris;Pro. = pronator musclesof Rock Dove during level flapping flight superficialis;Supn. = supinator; F.C.U. = flexor carpi (upper) and verticalascending flight (lower). Dashed ulnaris;E.D.C. = extensordigitorum carpi;E.M.U. = line at top of two circulardiagrams (at 0ø) identifies extensormetacarpi ulnaris; S. Tri. = scapulotriceps; the point within wing-beat cycle when humerus is T.P. Brev.= tensorpropatagialis pars brevis; T.P. Long. fully elevated(i.e. beginning of downstroke),and = tensor propatagialispars 1onga;S.H.C. = scapulo- dashed line at bottom of each circular diagram (at humeralispars caudalis; Delt. maj. = deltoideusmajor; 180ø ) identifies when humerus is fully depressed(i.e. and Supra. = supracoracoideus.Adapted from Dial beginningof upstroke).Note that onsetand offset (1992). October1992] WingMuscles and Nonsteady Flight 881

Denervationexperiments.--An example of the ing of the featherscould be achieved(for fur- EMG activity from a pre-denervated pigeon ther discussion,see Sy 1936,Hildebrand 1988). during level flapping flight from three muscles Fisher (1957) found that, when the tendons of (the major wing depressor[pectoralis], a wrist the wrist flexors and extensors were cut in a extensor [extensor metacarpi radialis], and a pigeon,the bird wascapable of flight. However, wrist flexor [flexor carpi ulnaris]) is provided in Fisherdid not specifyanything aboutthe type Figure 6A. Subsequentto the denervation of of flight the birds achieved (i.e. takeoff, ascend- the medianoulnaris, the animal was unable to ing, descending,landing) but only that two birds activate its wrist flexors or pronators(Fig. 6B). could fly after recoveryfrom operation. This is evident by the flat-line signal for the It appears that the skeletal linkage system EMG electrode residing in the flexor carpi ul~ within the avian forearm (comprising a col- naris. The animal struggled to take off, but was lapsible parallelogram) is particularly impor- able to sustain level flapping flight. In this tant during level flapping flight becauseit per- condition, the bird struggled to alight on the mits a coordinatedextension and alignment of 0.3-m2 landing platform. When both the me- the wing. I propose that the evolutionary re- dianoulnaris and radialis nerves were severed tention of the forearm musclesis a consequence (Fig. 6C), incapacitatingall of the wing muscles of the fact that those muscles are needed for distal to the shoulder (except the biceps and modification of the shape of the wing during brachialis [innervated by musculocutaneous periodsof nonsteadyflight. I proposefurther nerve] and triceps[two heads of which are in- that forelimb muscles in most birds are not es- nervatedby more proximalbranches of radial sential for normal extension and flexion of the nerve]), the animal was unable to take off. How- wing during each and every wing beat. Even ever, after being launched(by hand) into the thoughall forelimb musclesgenerated low-lev- air, the bird was able to fly the entire length of el electromyographicsignals during short-range the 50-m flyway. With both the medianoulnaris flights (30-50 m) when the birds were carrying and radialis nerves cut, all birds were incapable a sectionof the recordingcable, these muscles of performing a controlled landing. The bird are primarily involved in controlling the wing either gradually descendedfrom level flight during nonsteadyflight (e.g. takeoff and land- prior to reaching the platform, whereupon it ing). The forcesrequired to modify the shape landed on its belly and slid along the floor for of a rapidly moving wing during nonsteady a distance of 3 to 5 m, or the bird descended flight are expected to be substantial,and the vertically, in an uncontrolled manner, to the degreeof forearmmuscle development may be floor. correlatedwith the amount of nonsteadyflight Inspectionof movie films of unilaterally de- eachspecies routinely performs. nervatedbirds showedthat the denervatedwing The significanceof the changeof wing span was unable to fully extend during nonsteady during each wing beat in steadyflight has been flight. However, during level flapping flight, discussedby Spedding(1987). He suggeststhat the normal and denervatedwings moved sym- the observed forelimb kinematics enables the metrically, with no discernabledifference in bird to maintain a bound vortex of constant wing kinematicsobserved from the films. An- circulation on its wing, thus minimizing the imals that were denervated bilaterally exhib- amount of energy wastedin sheddingvortices ited the same flight capabilitiesas the unilat- into the wake. Spedding(! 987) and Pennycuick erally denervatedanimals. (1988) maintainedthat cyclicchanges of wing spanare a key adaptationfor economicalcruis- DISCUSSION ing flight in birds, but this phenomenon ap- parently is absentin bats. A biomechanicallinkage system within the My resultssuggest that significantmetabolic forelimb, identified over 100 years ago, appar- savingsmay be enjoyedby birds that undertake ently provides the necessarycontrol to auto- frequent and prolonged periods of level flap- matically extend and flex the wing using input ping flight. If the muscleactivity is reducedor solelyfrom the shouldermusculature. Headley completelyshut down, then the metaboliccosts (1895) demonstrated,using a dead bird, that required to operate the avian locomotor appa- when the elbow joint is passivelyextended, an ratus would be reduced. Perhaps birds use a automaticextension of the wrist and the spread- physiologicalstrategy similar to that employed 882 KENNETHP. DIAL [Auk,Vol. 109

A NORMAL PIGEON DURING LEVEL FLAPPING FLIGHT

PECTORALIS

EXT. METACARPI RADIALIS

FLEX. CARP1 ULNARIS

B DENERVATION OF MEDIANOULNARIS PECTORALIS

EXT.METACARPI RADIALIS

FLEX. CARPI ULNARI$

c DENERVATION OF RADIALIS AND MEDIANOULNARIS

PECTORALIS

EXT. METACARPI RADIALIS

FLEX. CARPI ULNARIS

Fig.6. Electromyographicsignals of theprimary downstroke muscle (pectoralis), a wrist extensor (extensor metacarpiradialis), and a wrist flexor(flexor carpi ulnaris) during four wing-beatcycles. (A) EMG signals recordedfrom normalRock Dove prior to denervation.(B) EMG signalsrecorded following denervationof medianoulnarisnerve. Note that flexorsand pronatorsof wing are incapacitated(indicated by flat-linesignal from flexorcarpi ulnaris). (C) EMG signalsrecorded from RockDove during level flappingflight after both radialisand medianoulnarisnerves cut. Note that pectoralisis active,but extensorsand flexorsof wrist exhibit no EMG activity.Bird is capableof level flappingflight, but cannottake off or land in coordinatedfashion. October1992] WingMuscles and Nonsteady Flight 883 (Cs•II.i,aOPcae•Ho•ingblrd r•• Z''•

Fig. 7. Skeletalelements of forelimb in five speciesof birds scaledso that carpometacarpiof equal length. In birds that display large amount of nonsteadyflight (e.g. Black-chinnedHummingbird, Rock Dove, and Wild Turkey), all possessrobust skeletal elements, and ulna and radius bow away from each other. This indicatesa significantamount of musclemass associated with antebrachium.Species with no bowing of ulna and radius, such as the albatross,possess little forelimb musculatureand are not coordinated in nonsteady flight. Most spedes, such as passetines,possess an intermediate condition with a modest massof forelimb musculature. by various marine mammals, which metaboli- are not necessaryto actively extendand flex the cally shut down the peripheral body parts dur- wrist within each wing beat during level flap- ing extended underwater dives (Irving et al. ping (i.e. steady)flight. 1942, Scholander 1964). An interesting study Our present understanding of the relation- would be to determine if birds restrict both the shipbetween musculoskeletal design and flight circulationand degreeof muscleactivity within styles among birds is in its infancy. Biome- the wing during steadyflight and, thus, rely on chanical linkage systemsand neuromuscular their forelimb linkage systemto controlthe wing control of the avian wing have only recently movementsat a fraction of the energetic cost. been investigated under experimental condi- The activity patternsof the scapulotricepsand tions.Can anything be deducedabout the flight bicepsbrachii suggestthat theseantagonists are style of a bird solely from inspection of the actingas elbow-joint stabilizersduring the final wing skeletal elements?Consider the forelimb one-half of the downstroke and, therefore, do skeletalelements of five different speciesof birds not appear to be responsiblefor actively ex- (Fig. 7). The degreeof stoutnessof the ulna and tending or flexing the wrist during level flap- radius, and the amount of lateral bowing of ping flight. Consistentwith the brachial mus- these two bones provide an indicator of the cles, the activity of the antebrachial muscles relative muscle mass attached to these struc- suggeststhey alsoact to stabilizetheir common tures.Inspection of these elementsalone may limb joint (i.e. the wrist). Clearly, thesemuscles be sufficientto interpret somethingmeaningful 884 KENNETHP. DIAL [Auk, Vol. 109

The forelimb musculature of passetinestypi- cally falls between the characteristicsof hummingbird and albatrossforelimbs. Future studies should investigate the functional relationship between muscle architecture,skeletal forelimb characteristics,and flight styles. Comparing closely related taxa that exhibit different flight habitsmay provide insight into the relationshipbetween form and function of the musculoskeletalsystem within the wing. Fig. 8. Skeletal elementsof forelimb in Archae- Hummingbirds are capable of sophisticated opteryxlithographica. Note simplearticular surfaces of nonsteadyflight. Their ability to change body ulna-radiuscomplex with carpometacarpus,and also positionin a fixed location,such as at a flower the absenceof bowing between ulna and radius. Il- during feeding, and their maneuverability in lustrationdrawn from photographtaken of Berlin dense vegetation is unparalleled among birds. specimenhoused in Humbolt Museum fur Natur- kunde. On the other hand, swifts perform an appreciable amount of steady flight while foraging in primarily open habitats.The high degree of about the flight stylesand capabilitiesof the radio-ulnar bowing in the hummingbird ap- speciesin question.For example,birds that per- pears associatedwith the pronounced devel- form a substantialamount of nonsteadyflight opment of the pronatorsand supinatorswithin (e.g. hummingbirds,pigeons, and gallinaceous the antebrachium(unpubl. data). In swifts, the birds) possessstout skeletal forearm elements radiusand ulna are essentiallyparallel and ex- and,additionally, the ulna and radiusbow away hibit a modestamount of bowing. While swifts from one another. These conditions are indic- possessa robust extensor metacarpi radialis, their ative of specieswith substantialforearm mus- pronators and supinators are modest in size, culature.Hummingbirds hover while foraging, and their radii and ulnae are not robust nor do while pigeonsexhibit nearvertical takeoffs and they bow away from each other as in hum- descents from cliffiike structures. Galliforms are mingbirds (unpubl. data). primarily terrestrialand employ short-distance The flight capabilityof Archaeopteryxhas been, maneuverableflights when disturbed.In con- and continuesto be, hotly debated (e.g. Hecht trast,species that perform predominatelysteady et al. 1984). Therefore, it is of considerable in- flight, suchas long-distance shorebird migrants terest that the forearm elements of Archaeopter- and pelagicspecies (e.g. large procellariiforms), yx do not suggestthat theseanimals possessed have forearm skeletal elements that are slender a sophisticatedlinkage system (Fig. 8). Their and lack pronouncedbowing or separationbe- ulnae and radii did not bow to any appreciable tween the ulna and radius (this condition is degree, indicating that they probably did not particularly obviousin albatrosses;Fig. 7). Al- routinely perform nonsteady flight nor pro- batrossesare sometimesreferred to as "gooney longed level flapping flight. However, Archae- birds" becauseof the lack of finessethey display opteryxmay have beena capableglider. Further duringtakeoffs and landings(in additionto their work on the skeletal reconstruction of the fore- comical courtship behavior). These birds are limb will be necessaryin order to advanceour unableto changesignificantly the shapeof their understandingof the flight behavior of Archae- wings during nonsteadyflight and, therefore, opteryx.In addition, continued work in the area look uncoordinatedduring takeoffsand land- of experimental functional morphology using ings. Albatrossesperform dynamic soaring at extant specieswill provide novel information moderate to high velocities. They change the for a better understanding of the evolution of shape of their outstretched wings primarily avian flight. during gliding and, therefore,possess minimal musculature within their forelimbs. ACKNOWLEDGMENTS Most bird speciespossess forelimbs with a moderate degree of ulna-radial bowing, and L. Becker,C. Bocker,D. Conway,J. Felix, N. Olson, these skeletal elements are of conservative girth W. Peters,and R. Trenary helped train the birds, as- (e.g. EuropeanStarling, Sturnus vulgaris; Fig. 7). sistedin the experimental recordings,and were in- October1992] WingMuscles and Nonsteady Flight 885 volved in various aspectsof data analysis.R. Petty domesticcats (Feliscatus). J. Morphol. 163:253- assistedin the preparation of Figures 1, 7 and 8. I 281. thankW. Bock,S. Gatesy, R. Hutto,J. Marks, G. Schnell, HEADLE¾, F. W. 1895. Structure and life of birds. B. Tobalskeand two anonymousreaders for critically Macmillan, London. reviewing the paper. The experimental procedures HECHT, M. K., J. H. OSTROM, G. VIOHL, AND P. followed the guidelines establishedby the IACUC WELLNHO•ER,EDS. 1984. Thebeginningsofbirds: for animal care at the Animal Facilities at the Uni- Proceedingsof the InternationalArchaeopteryx versity of Montana.This projectwas supported by the Conference Eichstatt. Bronner and Daentler, National Science Foundation Grant BNS-89-08243. Eichstatt. HILDEBRAND, M. 1988. Form and function in verte- LITERATURE CITED bratefeeding and locomotion.Am. Zool. 28:727- 738. BOCK,W.J. 1974. The avianskeletomuscular system. IRVING, L., P. F. SCHOLANDER,AND S. W. GRINNELL. Pages120-257 in Avian biology, vol. IV (D. S. 1942. The regulation of arterial blood pressure Farner, J. R. King, and K. Parkes,Eds.). Academic in the seal during diving. Am. J. Physiol. 135: Press, New York. 557-566. BREAZILE,J.E., ANDM. YASUDA.1979. SystemaNer- JENKINS,F. 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