ADAPTIVEMECHANISMS

OF THERAPTORPELVICLIMB

G•o•o• E. GosLow,JR.
THxs study presentssome adaptations in the pelvic limb of six North

American raptorial species. Bock and von Wahleft (1965) point out
the term "adaptation" needsto be defined when used. I studied evolutionary adaptations as I am interested in those structural features thatenableraptors to sustaina predatory role within a given environment.
I am not concernedwith evolutionary pathways. In this regard, I
studiedcloselyrelated and diversespecieshaving similar habits. I investigated the raptorial speciesfrom both orders and four of the five
familiesin North America (the nonpredaceous
New World vultures,theCathartidae, were omitted). The speciesstudied were the Cooper's
Hawk ( Accipitercooperii), Red-tailedHawk ( Buteo jamaicensis) , Prairie
Falcon (Falco mexicanus),SparrowHawk (Falco sparverius),Screech
Owl (Otus asio), Burrowing Owl (Speotyto canicularia), and the Barn
Owl (Tyto alba). I comparedthe raptors to one another, as well as toa generalizednonraptorialspecies.A "generalized"speciesis difficult
to define,but one that doesnot use its legsand feet for any particular
activity other than walkingor standingseemsappropriate.I selectedthe
domesticpigeon(Columbalivia).
The functionalaspectsof the anatomyof the birds of prey have been
little studied. Gatrod (1875) describedthe vinculumconnectingthe
tendonsof the flexor digitorumlongusand flexor hallicuslongusfor
severalgeneraof Falconiformes.Subsequent
workers (Shufeldt, 1887;
Hudson, 1937; Ruggeberg,1960) further discussedthe fusion of thesetendons. Shufeldt (1909) presenteda very general account of theosteology
of severalspecies
includingA. cooperii,B. jamaicensis,
and F.
mexicanus. Peczely (1964) compared the thoracic vertebrae of several
generaof raptorsincludingButeo,Accipiter,and Falco. Wherepossible,
he related anatomical differences to the habits of the birds. Studies ofthe pelvicregionof variousgeneraof Falconiformes
and Strigiformeswere
made by Hudson (1937, 1948) and Berlin (1963).

Accuratedeterminationof muscleforceshas long presenteda problem
to morphologists.
Presentknowledgeof musclestructureand physiology
limit severelythe traditionaltechniquesof comparingmusclevolumes
and weights (for a review, see Gans and Bock, 1965). Eccles andSherrington(1930) demonstrated
the dangersof usingthe weight (andthus volume)of musclesas an indicationof tension.They showedthat
though the medial õastrocnemiusof the cat weighs2• to 3 times asmuch as the soleus,it developsabout 6 times as much tetanic tension
47

The Auk, 89: 47-64. January 1972

48GEORÙEE. Gos•ow, JR.
TABLE[Auk, Vol. 89

1

SPECIES•NUI•I-BER•
WEIGIIT ANDANESTIIESIALEVELUSEDFORLENGTII-TENSIONANALYSES

SpeciesNumber and sex

Body weight(g)•

Total pentobarbital
(rag)

10.5

A. cooperil

19

393

B. jamaicensis

19

1546

15

C. livia

29--

40 mg/kg •'30 mg/kg•'

F. sparverius

8 • ; 2 i•--O. asio

13

124

4

F. mexicanus

13

503

12

S. canicularia

13

101

4

T. alba

13

35

7.5

Body weight recordedafter removal of the reproductiveorgansand digestive tract.
Average number of mg given per kg of body weight.

when stimulated. I have similar data (MS) for a large seriesof pelvic
limb musclesof F. sparverius. In accordance,I stimulatedeach muscle
under study and recordedthe tensionproduced. It is hoped further useof this techniquefor certain kinds of functional morphologicalproblems
will proverewarding.
METHODSAs muscle can develop different active tensions at different lengths (Evans andHill, 1914), it must be stimulated over a range of lengths to determine its tension
parameters. To this end I anesthesizedthe bird, ventilated its lungs, and surgicallyisolated and stimulated select leg muscles. The birds were anesthesizedintravenouslywith pentobarbital sodium as a 1% solution. I injected dosesof •z• to 1 mg/$rain until plucking of the breast feathers produced no overt movements. I administered further amounts as required throughout the experiment (Table 1).
After anesthetizationI surgically isolated the trachea and prepared it for cannulation. To assure adequate lung ventilation I opened the abdominal cavity,punctured the ventral and posterior thoradc air sacs, and passed a mixture of

60%, O_•,39% N2, and 1% CO• through the lungs via the tracheal cannula. Gas
flow was adjusted to a level that prevented the bird from breathing actively. Before
enteringthe bird, the gasmixture was humidified to 100% and brought to a temperature of 38øC by passing it through a Plexiglas cylinder into which water at 38ø
was sprayed continually.

I surgically isolated select tibiotarsal musclesbut left the origins intact. Damage
to blood supply was minimal and I took care not to cut the fibers of dosely
adjoining muscles. I maintained the temperature of the exposed leg relatively
constantwith the aid of a heat lamp and intermittantly bathed the preparation withwarm (38øC) saline. I measuredintermusculartemperatureswith a thermocouple
at 5-10 minute intervals.

I stimulated each muscle directly with a grid of silver electrodesleading froma Grass Model SD5 stimulator. Supramaximalstimuli every 15-20 secondsproduced
brief tetani. I delivered impulses of 0.5 msec duration at frequendes of 60-180

January 1972]

Raptor Pelvic Limb Mechanics

49

pulses/secondand voltages of 10-80 V depending on the muscle investigated. For
each muscle, I took care to insure a combination of voltage and frequency thatwould result in maximummuscleresponse(Joyce et al., 1969). I noted the actionof each muscleby observinglimb movementsfollowing stimulation.
In preparing to measure muscle force, I first measured the length of the muscle
before cutting the tendon of insertion. I clamped a solderlessterminal onto thetendonand thenconnected

itto a Grass FTIZ

tensiontransducer

thatrecordedon a Beckman RB Dynograph. I maintained the sensitivity of the dynograph atindex 10. I fixed the transducer on an adjustable jack that could be raised andlowered in 1-mm intervals. The head of the femur was firmly fixed to the tableto facilitate near isometric recording. Each muscle tested was first shortened to alength at which it developed little tension xvhen stimulated. I then stretched it
1 mm and stimulated, stretched it a secondmm and stimulated again until I reacheda length at which no further active tensioncould be produced. During the original
measurementof musclelength, I maintained the digits in an extended position, andheld the coxofemoral, femorotibial, and intertarsal joints at 90ø.
In addition to the birds used for tension measurements,I made fresh dissectionsof the following birds (numbers studied in parentheses): A. cooperil (2), B.
jamaicensis(2), C. livia (2), F. mexicanus(1), F. peregrinus(1), F. sparverius(5),O. asio (1), S. canicularia (1), and T. alba (2). I described the muscles andmeasured their appropriate moment arms and tendon excursions.
For many muscles the effective moment arm changes as the angle of the jointchanges. In these instances I measured the moment arm at increments from fulljoint flexion to full extension. I laid the specimenon a plastic sheet upon which
was drawn a circle divided into 360ø. Placing the pivot of the joint over thecenter of the circle, I moved the distal limb segment and measured the moment
arm at 10 ø intervals. I made the measurements twice for each muscle and used
the average.
I determined the passive excursion of a tendon that occurs with change in theangleof the joint by moving the joint through 30ø and noted the distancemoved.
I did this three times for each muscle and used the average. I made all measurements to the nearest 0.1 mm using dividers and vernier calipers.
MYOLOGY

I selected for analysis 16 major flexor and extensor muscles of the tibiotarsus
and digits; space limits this report to only 3 of these muscles,the tibialis anterior,
flexor hallucis longus, and flexor digitorum longus (see Goslow• 1967, for a similar
treatment of the remaining 13 muscles).
The following muscle descriptionsare based on two specimensof the Red-tailed
Hawk (Buteo jamaicensis). The patterns found in the other speciesare discussed
in relation to B. jamaicensis as a standard.
M. tibialis anterior (tib. ant.).---This muscle is located on the anterior border of
the tibiotarsus (Figure 1). It originates by two heads, the larger arising from theanteriorside of the tibial

crest and also froma line down the medialsurface of the

shaft of the tibia. The other head arises by a tendon from the distal apex of theexternal condyle and passesdistally between the head of the fibula and the lateralapex of the tibial crest. The heads fuse and passdistally becominga strong tendon
that passesunder a fibrous loop near the distal end of the tibiotarsus. The tendon
passes between the condyles of the tibiotarsus and inserts on a tubercle located on
the anterior surface of the tarsometatarsus.

50

GEORGE
E. GOSLOW,Ja.

--[Auk, Vol. 89

Flex. hal. I.

Tib.

dig.
I.••ib'ant'
Medial

view

Tib.

--

Flex. dig. I.
hal. I.

Figure 1. Lateral view of the left pelvic limb bones of B. jamalcensis,showing
principal areasof muscleorigin and insertion.
Action: Flexon of the tarsometatarsus.

M. flexor digitorum longus (flex. dig. 1.).--This deep muscleis large and rises
from an extensivearea of the posterolateral,posteromesial,and posteriorsurfacesof the tibiotarsus(Figure 1). Its tendon passesthrough the tibial cartilage andcoursesdistally along the posterior sulcusof the tarsometatarsus.Just above thebasesof the digits the tendon dividesinto three branches,one of which passesto
eachof the foretoes.Thesecourseventral to the phalanges0
perforatingthe superficial
flexors of the digits, to insert on the base of the unguinal phalanges. Distally
along the tarsometatarsus, this muscle tendon fuses with the tendon of the flexor

hallucislongusby way of a strong tendinousvincu!um. Thus independentmovement of the two tendons is lost.

Action: The flexor digitorum longus is a flexor of the unguinal phalanges(talons)of the foretoes, but its fusion with the tendon of the flexor hallucis

longuslets it contribute to the flexon of the talon of digit I. Some flexon of theentire digit resultsfrom tension applied to the tendon of the flexor digitorium
longus.

January 1972]

Raptor Pelvic Limb Mechanics

51

Figure 2. Representationof the method followed in the analysisof inforces andoutforcesof bone-musclesystemsused in this study. F, initial force; Fo, outforce;lo, out lever; m, moment arm.

M. ]lexor hallucislongus (flex. hal. 1.).•This large musclerisesby two heads, asmall anterior head and a larger posterior one. The anterior head rises from theposterolateralside of the fernoral shaft just proximal to the external condyle. The
posterior head rises from the intercondyloid region of the femur, and the two heads
fuse almost immediately. The muscle'sbelly extends the length of the tibiotarsus
before forming a strong tendon that passesthrough the tibial cartilage and continues distally along the sulcus of the tarsometatarsus.At the distal end of thetarsometatarsus the tendon passes between the first and second metatarsals. Aftersending a stout branch to the tendon of the flexor digitorum longus leading todigit II, it coursesdistally to insert on the base of the unguinal phalanx of thehallux. As noted above, the tendons of the flexor hallucis longus and the flexor
digitorum longus are closely fused at the level of the tarsometatarsus.
Action: The flexor hallucis longus is a strong flexor of the unguinal phalanges(talons) of digits I and II, but its fusion with the main tendon of the flexor
digitorum longus permits it to flex the talons of the digits III and IV as well.
Some flexion of the entire digit results from tension applied to the tendon of theflexor hallucis longus.
MECHANICS

I determined the tetanic tensionsof the three muscles,and thesetensions,coupled with osteologicalmeasurements,provided the basis
for analysis. Using the method of torque analysisI calculatedthe approximate forces produced by certain bone-musclesystems. I ignored
the forcesof friction (probablynegligible)and the restrictiveforcesimposed upon joints by ligamentsand musclemasses(assumedrelatively
small). Forcesof gravitation and inertia (not negligible,but less thanfor heavieranimals)werealsoignoredand loading,whereapplicable,wasconsideredsymmetrical.

52

GEORGEE. GOSLOW,JR.

[Auk, Vol. 89mdig.
Figure 3.

Points of measurement for the inforce and outforce calculations of

the flexor hallucis longus and flexor digitorum longus. F, initial force; Fo, outforce;lo, out lever; ms moment arm.

Torque is the effect of a force on an object with respect to a centerof rotation.

For skeletal elements the center of rotation

is an anatomical

joint. The magnitudeof a torque is equal to the product of the magnitude of the force and its moment arm. The length of the moment arm
is the perpendiculardrawn from the center of rotation to the vector lineof the force. Torques are expressedin units of force and length. In
this study the unit used is the gramweight-centimeter.The vector lineof the force producedby the muscleis the inforce, while the vector lineof the force producedat the end of the bone affected is the outforce.
ConsiderFigure 2. The outforce (Fo) may be determinedby solving
for Fo in the equation (Fo) (lo) ---- (F) (m), where F is the original
inforce; m is the moment arm; 1 is the lever arm of the. outforce; andFo is the outforce at right angles to the direction of movement. The

outforce (Fo) was computedwith knowledgeof the physiologicalforce
producedby the muscle (F), coupledwith measurementsof the momentarm (m) and outlever (1o).

I measuredthe outforceat a point along the bone or segmentwhere
I thought it to be the most important. For exampleI measuredthe out-

force for the tibialisanterior (Figure 2) at the tarsal region,but I could
have measuredit at the end of the talons. This would have lengthened
the outlever (lo) and thus reducedthe magnitudeof the outforce. I consideredthe probable functional relationshipsbefore I determinedthe outforce used. This methodis somewhatarbitrary, but using the sameloca-

January 1972]

Raptor Pelvic Limb Mechanics

53

9OO

700
•. Elø
•m•m
m

,.-

500

•

SO0

Length in mm
Figure 4. Length-tension relationships of the tlblalis anterior of F. sparverius.
A, active tension; B, passive tension; C, total tension.

tion of the outforcefor all speciesin analyzim a given bone-musclesystem introducedno errors. Figure 3 illustrates,5.•epositionof the inforce,
moment arm, and outforce for the flexor (i•gitorum longus and flexor
hallucislongus.
Mechanicaltreatmentof the flexorsof the digits is difficult. Dempster(1961) discusses
the problemwith respectto analysisof the human digit.
Tension of the tendon of the talon flexor for example, results in theapplicationof forcesto the intermediatephalangesof the digit as wellas to the talon. Thus intradigital forcesresult from a flexion force applied to the distal phalanxor phalanges,as well as from contactsbetween
phalanges.To simplify analysisthe segmentsof the digit proximal tothe insertionof thesetendonsweretreatedas if they were rigid structures.
RESULTS

The active force producedby a musclewhen stimulatedreachesa
maximumat someparticular musclelength (Evans and Hill, 1914). This
length, at which active isometric tension is greatest, has been termedthe "reference length" of the muscle. When the muscle is either
shortenedor lengthenedbeyond its referencelength, the active tensionthat it candevelopdiminishes.
Figure 4 showsthe length-tensionrelationshipfor the tibialis anterior
muscleof a SparrowHawk. The numeral "0" along the abscissaof thegraph representsthe length of the musclein the leg of the bird when thefemorotibialand intertarsal joints are at a 90ø angle. Muscle lengths
longer and shorter than the "0" length are shownby positiveand nega-

54G•o•c• E. GOSLOW,J•.

,[Auk, Vol. 89

11
/

I

I

I

!

I

I

I

I

0

qD

(•OLX)UUO-1MI5
U!enbJo.
L

II T
I[. I. I

I

I. I

I

I
C)

I

I
(.0

I

I
½xJ

(cOL
X)LUO-I•fi
u!enbJo/

January 1972]

Raptor Pelvic Limb Mechanics

55

tive numerals. The figure illustrates the amount of active tension themuscledevelopsat differentlengths(A) as well as the amountof passive
tension (B) and the total tension (C) developed.The active tension
is a result of the isometrictensiondevelopedat stimulation. The stretchof inert elasticmaterial (connectivetissue) in the muscleproducesthepassivetension(Banusand Zetlin, 1938). The total tensionis a combination of both these componentsand is the tension consideredmost important to this study.

After I determinedlength-tensioncurves for the three pelvic limb
muscles,I measuredthe length changeof each muscleas the affectedjoint was moved. The lengthof the muscle(and thus its tension),coupledwith its moment arm (measuredfrom dissectiondata) determine theamountof torquepossiblearounda joint at any given time.
A factor contributingto torque,which has been more or lessignored
up to this point, is the number of motor units within the muscle thatare activated at the time of contraction. In the living organism avariable numberof motor units are activatedwithin a muscleto produce

a smoothmovement(Mollet, 1966). The torque data presentedin thisinvestigationare basedupon muscleforcesderived at maximal stimulation,and the forcesderived by this method are probably higher than thosethe living bird actually developsduring normal movements.In otherwords, the forcesmeasuredwere actual forcesof the musclesbut only
potential forces for the organism. A basic assumptionof this study isthat a direct relationship exists between maximal "potential" force
measuredand the actual forcedevelopedin the organism.
Figures 5 through 7 present muscle force data. The upper graphs ofeach figure show maximum muscle forces and resultant outforces of thebone-muscle
system; the lower graphspresenttorque or turning forces.
The uppergraphswill be discussed
first.
The upper left-hand graphs express the maximum muscle force developedby a muscleas a percentageof the bird's body weight (intestinal
tract and reproductiveorgansremoved). The right-hand graphsexpress
the maximumoutforceproducedas a percentageof the bird's bodyweight. The two graphs show the relative developmentof a particular
muscleand the relative muscleforce and (or) skeletal componentsin
determiningthe effectivenessof a particularlever system.
I determinedlength-tension
curvesfor eachof the three pelvicmusclesof 10 Sparrow Hawks. It cannot be assumedthat the amount o.f variation

found in these 10 musclesis. equal to that found in the musclesof theother species. Intraspecific differencesare probably not great, particularly as the coefficientof variation for the musclesof the Sparrow
Hawk were relatively high--they ranged from 9 to 18. Gans (1963)

56

Gso•c• E. Goszow, J•.

I

I

I

o

o

•

,•-

[Auk, Vol. 89

I

m0- lta15 u! anb]olo(•01-X)CUO-•-•6
u! anbJol

January1972]

RaptorPelvicLimbMechanics

57

T

I

I

!

I

I

I

I

I

I

I

0

bu•-•,•i3

ul @nbJo/00/ / !f//// • / \/

V "

i

I

I

I

I

f

I

I

I

i

I

I

I

(gO[X)wo-l/•fi ul anbJol

GEORGEE. GOSLOW,JR.

[Auk, Vol. 89

pointed out the shortcomingsof using a detailed analysis where variability is great; in accordancewith this, rangesof variability are noted
and usedin comparisons.
I could make only one or two measurementsfor each muscle of theother speciesunder consideration.Statistical techniquesemployedfor
comparing these data follow the single specimenmethods often usedby paleontologists
as describedby Simpsonet al. (1960). I determined
the standard deviation (s) and coefficient of variation (V) for eachmuscle of the Sparrow Hawk and two standard deviations above andbelow the true mean for this specieswere plotted. I treated the single
measurementmade for an individual of another speciesas though it
coincidedwith the populationmean (m). Assumingthe value of V inthis speciesto be the sameas that for the SparrowHawk, I calculateda
probable standard deviation (V = 100 s/m). The single measurement
could representeither the low end of the population distribution or thehigh end. Since95 percentof the measurements
within a normal population fall within two standard deviations above and two standard devia-

tions below the mean for that measurement,I comparedthese data as
follows:

Four calculated standard deviations were established above andbelow the single point measurementfor each species. These are shownas the rangelinesaboveand belowthe points (Figure 5, upper graphs).
If the measuredpoint for a secondspeciesdoesnot fall within the range
establishedfor the first, I assumethe muscleforce percentagesare
significantlydifferent. For example,in the upper left-hand graph of
Figure 5, a comparisonof the measuredmuscleforce of the tibialis anterior of the pigeon with the ranges of the other speciesindicates asignificantdifferencebetweenthese forcesin the pigeon and those in
all the raptors studied. The horizontalaxis of each graph is drawn
on a log scale. This was done to maintain the appropriaterelationshipbetweenthe coefficientof variation and the standard deviation, as theabsolutesize of the meansvaried from thosedeterminedfor the Sparrow
Hawk.

The lower graphsof each figure show data derivedby plotting thetorque (moment arm x force) of a muscleagainst the angle throughwhich the joint involved rotates. Unless otherwise stated, these data
incorporateboth the change in moment arm length and the change
in the musclelength (thus its force) as the angle of the joint rotates(see METHOVS). The left-hand graph plots data for the larger species
and the right-hand graph data for the smaller ones. The initialsof eachgenusand species
accompanythe respectivecurves.The important
thing to note in thesefiguresis the angle(s) of the intertarsaljoint at
which torqueis maximum.

January 1972]

Raptor Pelvic Limb Mechanics

59

Figure 5 presentsdata for the major flexor of the tarsometatarsus.The
tibialis anterior appearsto be significantlymore developedin the raptors
as a group, with F. sparverius,A. cooperii, and the three owl species
representingthe most developedcondition. The torque curves for these
species illustrate that the tibialis anterior is capable of maintaining
maximum effectivenessthrough a relatively wide range of intertarsal
angles.
Figures 6 and 7 illustrate data for the two major flexor musclesof
the talons. These muscles affect all of the talons simultaneously but
each to a different degree. The effect is dependenton the length of the
moment arm involved. To gain an outforce value resemblingthe actual
value producedby the bird, I divided the muscle'sforce by four before
making the outforcecalculations. Data are presentedfor talon II only.
Figure 6 illustrates relatively greater developmentof the flexor digitorum longus in the three owl species. This muscle appears least welldevelopedin B. jamaicensisand C. livia. Combining the outforce datafor both these flexors showsa significantly least amount of developmentof thesemusclesin C. livia as comparedto the raptors. A relatively highdegree of developmentis shown in the small raptors O. asio and S.
canicularia.

Recall that the tendonsof the flexor digitorum longusand the flexor
hallucis longus are fused in the speciesstudied. The muscleshave undoubtedly lost their independentaction. Figure 6 shows the flexor
digitorum longus to be most effective for most specieswhen the intertarsal joint is maximally extended. The curvesin Figure 7 for the flexor
hallucislongus,however,indicatejust the oppositepattern of effectivenessfor the largerspecies
and C. livia. For the other smallerspeciesmaximum
effectivenessappearsto be at intermediateanglesof extension.A divisionof labor betweenthese two musclesis probable, the flexor digitorum
longusfunctioningwith maximumeffectivenesswhen the legs are wellextended,and the flexor hallucis longusbecomingmost effective as theintertarsal angle is closed. Recall that the segmentsof the digit wereextendedwhen the data were recorded. As the digits are flexed, bothcurves will be shifted to the left thus changingtheir effectivenesswith
respectto the intertarsal angle.
DISCUSSION

This study contributesto the interpretationsof various adaptationsof raptorial birds by determining the relative magnitudesof the outforcesof selectpelvic limb muscles.Despite the limited number of specimens subjectedto muscleanalysisin this study, certain morphologicaltrends are evident, and the techniquesdescribedhere should be useful

60

GEORGEE. GOSLOW,JR.

Figure 8.

[Auk, Vol. 89

Action of the deep flexor muscles on the hallux and on digit III

at thefoot of the raptor. The distal phalangesare flexed around the proximal ones as
prey size is reduced. This mechanismof conformity to different shapes maximizes
contact surface between the digits and a variety of prey. F, force of flexors.

for other similar investigations.Techniquesemployingelectromyography
or implants of minute tensiometersin the tendonsof musclesmight also
aid in determiningthe exact form-functioncomplexespresent.
As a group, the raptors have marked developmentof the tibialis
anterior muscle,the flexor of the tarsometatarsus.This muscle'sdevelopment is undoubtedlycorrelatedwith the action of holdingstrugglingprey
close to the body at the time of the kill (all raptors consideredexcept'T. alba). The upperright-handgraphof Figure5 illustrates
relatively
low developmentof the outforce system of the tibialis anterior in C.
livia

and T. alba.

The loss in outforce in T. alba is a result of therelatively long tarsometatarsusin this speciesas seen in osteologicalcomparisons(Goslow, 1967). This increase in the length of thetarsometatarsusmight be correlatedwith increasedvelocity of the foot at
the time of leg extensionor with the amountof vegetationpresentin the
habitat of the raptor and its common prey. An analysis of the attackand strike of T. alba (Payne, 1962; Goslow, 1967) revealed the owl
thrusts the feet markedly downwardjust before contact with the prey.
An increasedvelocity of the foot during such a strike would be advantageous.

On the other hand F. mexicanushas a relatively short tarsometatarsus

January 1972]

Raptor Pelvic Limb Mechanics

61(Goslow,1967) and markeddevelopmentof the outforcesystemof thetibialisanterior(upper right-handgraph,Figure 5). This falcon'sshortand stout tarsometatarsus
may be the resultof selectivepressuretoward
strengtheningthe bone to withstandthe stressesencounteredat impact
with the prey.

Also the raptorsshowmarkeddevelopmentof the two talon flexors.
In the owlsthe morehighly developedof the two is the flexor digitorum
longus,whilein the falconsit is the flexorhallucislongus.In A. cooperii
and B. jamaicensisthe two musclesare equivalent. As the talon closes
its momentarm increases,
thus increasingthe outforceat the end of thetalon. The presenceof ligamentousslingsmakesthesemuscleseffective
for closingthe entire digit as well as for closing the talon. Figure
8 showsthe basic mechanism.If resistenceis met at any point along
the ventral surfaceof the digit, the segmentsof the digit distal to thepoint of resistancecontinueto rotate. This arrangementfacilitatesmaximum contactbetweenprey and digit (reptorial birds) or perchand digit(perchingbirds). In some speciesof raptors the talons and digits are
relativelylong. This is particularlytrue of accipiters,someof the large
falcons,and T. alba. If the digits are unusuallylong and there is notcompensatorydevelopmentof the musclesresponsiblefor flexion, thenthe relative outforceat the end of the segmentsis reduced. If, however,thesesegments
are relativelyshort,the ability to secureprey is probably
impaired. Undoubtedly there is some relationship between the size ofthe digits and the characteristicsof the prey involving its weight, its
agility, and the relative ease or difficulty of killing it. The relative
lengthsof the digits vary markedly within someof the speciesof raptors
studied. Within the large falcons, for example,the female's digits areoften relatively longerthan the male's. In Peale'sFalcon (F. peregrinus
pealei) I have measuredindividualsin which digit III is as long as thetarsometatarsus.This is not the averagecondition for PeregrineFalcons,
yet it does exist. Whether these marked variations are random or
adaptive within particular populationsis difficult to ascertain.

Garrod (1875) notedthat the vinculumconnectingthe flexor digitorum
longus and the flexor hallicus longus is oriented downward from thetendon of the latter to the former. Thus he speculatedwhen the flexor
digitorum longus contractsonly the foretoesare closed but when the
flexor hallicuslonguscontractsall of the toes close. The flexor hallicus
longusis the morehighly developedtalon flexorin the falcons,whereasin
the other raptors studied, and most perching species(Hudson, 1937;

Ruggeberg,1960), the flexor digitorumlongusis the more highly developed.In the latter species,this pattern of development
would correlate well with perchinghabits.

62

GEORGEE. GOSLOW,JR.

[Auk, Vol. 89

Length-tension data indicate a division of labor between the two
flexors; the flexor digitorum longus being more effective at the timeof full extensionof the leg, and the flexor hallucis longus being more
effective at the time of flexion. Films revealed that most raptors close
the toes around the prey at contact when the legs are extended (Goslow,1971). In this situation the flexor of the foredigits (flexor digitorum
longus) seems to be the most important flexor of the talons. The
large falconsoften strike with their legs flexed and feet maximally extended (Goslow,1971). In many instances,the falconsdeliver a glancing
strike to the prey. At contact the falcons immediately close their toes,
but becauseof their high speed,contact time with the prey is brief.
This appearsto limit the degree of piercing and tearing possiblewith
the foretalons,but the speedand directionof movementappear optimum
for effectivenessof the hind talon (hallux). These two factors, then,the degreeof flexon of the legs and the positionof the hallux at impact,
appear to be adaptive factors coincidingwith maximal developmentof
the flexor hallucislongusof the falcons. Why this muscleis so highly
developedin the small falcon (F. sparverius)is not clear. Its mostcommonlyemployedpattern of attack and strike is quite different fromthat of the larger falcons. Quite possiblythis smaller falcon descended
from a larger ancestoradapted for striking in a manner similar to F.
mexicanus.If this is the case,marked developmentof the flexor hallucis
longusover the flexor digitorumlongusin F. sparveriuswould be ancestraland not directly adaptive. Fossilevidenceon this subjectwould
be of interest.

Analysisof outforcedata for the small superficialflexorsof the digits
show no major trends or patterns that separate the pigeon from theraptors (Goslow, 1967). Isolated variations are seen but no adaptive
significancecanbe givento them.
The owls as a group normally demonstratethe zygodactylouscondition of the digits when perchingor standing. This digit orientationis

maintainedduring the strike by O. asio, S. canicularia,and T. alba
(Goslow, 1967). Payne (1962) noted this posture in T. alba anddemonstratedvia a seriesof experimentsthe symmetricalplacementof
the eight talons to maximizethe area coveredby the feet at impact.
The adaptive value of such talon positioningby a nocturnal raptor
intent upon pinningits prey to the groundis great.
ACKNOWLEDG!VlENTS

I would like to thank Jim Boda and Ray Berger of the University of California,
Davis, for their assistancewith the physiologicalaspectsof this study. Thanks also
goesto Walter Bock, Columbia University, for his critical review of portions of themanuscript. Above all, it gives me great pleasure to acknowledgeMilton Hilde-

January 1972]

Raptor Pelvic Limb Mechanics

63

brand, University of California, Davis, whoseinspiration,support, and ready advice
made this study possible. This work was supported by a National Institute ofGeneral Medical SciencesPre-Doctoral Fellowship (3-F1-GM-33, 006-0151).
SU•a•aAR¾

A method for the mechanicalanalysis of bone-musclesystemsis presented. Select systemsof the pelvic limb of sevenspeciesof raptors arecomparedwith a nonraptorialbird, the domesticpigeon (C. livia).

The outforcesystemsof the tibialis anterior (flexor of the tarsometatarsus), flexor digitorumlongus,and flexor hallucislongus(deep flexorsof the digits) are significantlydevelopedin raptors. Of the two flexorsof the digits, the flexor digitorum longus is more highly developedin
owls, while in falconsthe flexor hallucislongusis stronger. In the Redtailed Hawk and the Cooper'sHawk they are equal.
Torque data reveal a divisionof labor betweenthe two flexorsof thedigits. The flexor digitorum longusis more effective when the leg
is fully extendedwhile the flexor hallucis longus is more effective at
the time of flexion. Most raptors close their toes around the prey atcontactwhenthe leg is extendedthus placingthe flexor digitorumlongus
at its most optimum length for tension. But the Prairie Falcon and
PeregrineFalconoften strikewith the leg in a flexedpositionthusplacing
the flexorhallucislongusat its optimumlengthfor tension.
LITERATURE

CITEDBA•IJS• M. G.• .a.I•DA.M.
ZETLI•. 1938. The relation of isometric tension tolength in skeletal muscle. J. Cell. Comp. Physiol., 12: 403-420.

BERLIlV,O. G. W.

1963. A comparativestudy of the hind limb musculatureand

the toes of four local representativeof falconiforrnes. J. Anita. Morphol. Physiol.•
9:

1-17.

BOCK,W. J., A•D G. vo• WAltLERT. 1965. Adaptation and the form-function complex. Evolution, 19: 279-299.

DE•PSTER, W.T.
1961. Free-body diagrams as an approach to the mechanicsof
human postureand motion. Pp. 81-135 in Biomechanicalstudiesof the musculoskeletalsystem (F. G. Evans, Ed.). Springfield,Illinois, Charles C. Thomas.
ECCtES, J. C., ^•) C. S. SHERRI>mTO>•.
1930. Numbers and contraction valuesof individual motor units examined in some musclesof the limb. Proc. Royal Soc.
London, Set. B, 106: 326-357.
EVA>•S,C. L., A>mA. V. HItt.
1914. The relation of length to tension development
and heat production on contraction in muscle. J. Physiol., London, 49: 10-22.
GA>•S,C. 1963. Functional analysis in a single adaptive radiation. Proc. 16th
Intern. Congr. Zool., 3: 278-282.
GA>•S,C., Am) W. J. Boca. 1965. The functional significance of muscle archi-

tecture; A theoreticalanalysis.Ergeb. Anat. Entwickl.-Gesch.,38: 115-142.
GARRO•),A. H. 1875. On the disposition of the deep plantar tendons in different
birds. Proc. Zool. Soc. London, Part 2: 339-348.

64GEo}•c,E
E. GosLow, J}•.

[Auk, Vol. 89

GosLow, G. E., J}•. 1967. The functional analysisof the pelvic limbs of raptorial
birds. Unpublished Ph.D. dissertation, Davis, Univ. California.
Gos•ow, G. E., J}•. 1971. The attack and strike of some North American raptors.
Auk, 88: 815-827.
Hul)SO•, G. E. 1937. Studies on the muscles of the pelvic appendage in birds.

Amer. Mid[ Naturalist, 18: 1-108.
Hul)SO•, G. E. 1948. Studies on the muscles of the pelvic appendage of birds.
2: The heterogeneousorder Falconiformes. Amer. Midl. Naturalist, 39: 102-127.
JoYcE, G. C., P.M.
H. Rac•:, ^•i) D. R. W•STmYR¾. 1969. The mechanicalproperties of cat soleus muscle during controlled lengthening and shortening
movements. J. Physiol., 204: 461-474.

MOLEST,E.

1966. The chewing apparatus (An electromyographicstudy of theaction of the musclesof mastigation and its correlation to facial morphology).
Acta Physiol. Scand., 69, Suppl. 280.
P^¾N•, R. S. 1962. How the Barn Owl locates prey by hearing. Living Bird, 1:
151-159.

P•cz•¾, P. 1964. Functional-anatomicalexamination of the interconnectionbetween
the morphological features of the thoradc vertebrae in birds of prey and theiracquisition of food. Acta Morphol., 13: 101-118.
RuC,cEB•}•C,,T. 1960. Aur funktionellen anatomieder der hinter Extremitat einiger
mitteleuropaischerSingvogelarten.Z. Wiss. Zool., 164: 1-106.

SxMvso•, G. G., A. ROE,^•I) R. C. LEwo•zx•.

1960. Quantitative zoology. New

York, Harcourt, Brace and World Inc.
SI•uV•z•)r, R.W.
1887. A review of the musclesused in the classificationof birds.
J. Comp. Med. Surg., 8: 321-344.
SI•uV•Ll)r, R. W. 1909. Osteology of birds. Education Dept. Bull., New YorkState Mus., 446: 5-365.

Department of Zoology, University of California, Davis, California
95616. Present address: Department of Biological Sciences,Northern
Arizona University, Flagstaff, Arizona 86001. Accepted 15 November
1970.